Contents
VOLUME 135 (2)
2005 135 (2)
105
Introduction. Ninth International Congress on the Zoogeography and Ecology of Greece and Adjacent Regions (9ICZEGAR)
(Thessaloniki, Greece). Assessing Biodiversity in the Eastern Mediterranean Region: Approaches and Applications
109
Haralambos ALIVIZATOS, Vassilis GOUTNER and Stamatis ZOGARIS
Contribution to the study of the diet of four owl species (Aves, Strigiformes) from mainland and island areas of Greece
Belgian Journal of Zoology
119
Chryssanthi ANTONIADOU, Drossos KOUTSOUBAS and Chariton C. CHINTIROGLOU
Mollusca fauna from infralittoral hard substrate assemblages in the North Aegean Sea
127
Maria D. ARGYROPOULOU, George KARRIS, Efi M. PAPATHEODOROU and George P. STAMOU
Epiedaphic Coleoptera in the Dadia Forest Reserve (Thrace, Greece) : The Effect of Human Activities on Community
Organization Patterns
135
Tsenka CHASSOVNIKAROVA, Roumiana METCHEVA and Krastio DIMITROV
Microtus guentheri (Danford & Alston) (Rodentia, Mammalia) : A Bioindicator Species for Estimation of the Influence of
Polymetal Dust Emissions
139
Rainer FROESE, Stefan GARTHE, Uwe PIATKOWSKI and Daniel PAULY
Trophic signatures of marine organisms in the Mediterranean as compared with other ecosystems
A N
I N T E R N A T I O N A L
J O U R N A L
P U B L I S H E D
B Y
145
Giorgos GIANNATOS, Yiannis MARINOS, Panagiota MARAGOU and Giorgos CATSADORAKIS
The status of the Golden Jackal (Canis aureus L.) in Greece
THE ROYAL BELGIAN SOCIETY FOR ZOOLOGY
151
Marianna GIANNOULAKI, Athanasios MACHIAS, Stylianos SOMARAKIS and Nikolaos TSIMENIDES
The spatial distribution of anchovy and sardine in the northern Aegean Sea in relation to hydrographic regimes
157
Vassilis GOUTNER, Triantafyllos ALBANIS and Ioannis KONSTANTINOU
PCBs and organochlorine pesticide residues in eggs of threatened colonial charadriiform species (Aves, Charadriiformes)
from wetlands of international importance in northeastern Greece
Volume 135 (2) July 2005
165
Savas KAZANTZIDIS and Vassilis GOUTNER
The diet of nestlings of three Ardeidae species (Aves, Ciconiiformes) in the Axios Delta, Greece
171
Theodoros KEVREKIDIS, Theodora BOUBONARI and Vasilios GOUTNER
Seasonal variation in abundance of Corophium orientale (Crustacea : Amphipoda) in Monolimni lagoon (Evros Delta,
North Aegean Sea)
PROCEEDINGS OF THE 9th INTERNATIONAL CONGRESS ON THE ZOOGEOGRAPHY
175
Panagiotis KORNILIOS, Basil CHONDROPOULOS & Stella FRAGUEDAKIS-TSOLIS
Allozyme variation in populations of the karyotypically polymorphic vole Microtus (Terricola) thomasi (Mammalia,
AND ECOLOGY OF GREECE AND ADJACENT REGIONS
Rodentia) from Greece
181
George D. KOUFOS, Dimitris S. KOSTOPOULOS and Theodora D. VLACHOU
THESSALONIKI, GREECE, 22-25 MAY 2002
Neogene/Quaternary mammalian migrations in Eastern Mediterranean
191
Mary LABROPOULOU and Costas PAPACONSTANTINOU
Effect of fishing on community structure of demersal fish assemblages
199
Eugenia LEFKADITOU and Panagiotis KASPIRIS
Distribution and abundance of sepiolids (Mollusca : Cephalopoda) off the north-eastern Greek coasts
205
Mirjana LENHARDT, Roderick Nigel FINN, Predrag CAKIC, Jelena KOLAREVIC, Jasmina KRPO-
CETKOVIC, Ivica RADOVIC and Hans Jørgen FYHN
Analysis of the post-vitellogenic oocytes of three species of Danubian Acipenseridae
209
Georgios MANOUDIS, Chryssanthi ANTONIADOU, Konstantinos DOUNAS and Chariton Ch. CHINTIROGLOU
Successional stages of experimental artificial reefs deployed in Vistonikos gulf (N. Aegean Sea, Greece) : Preliminary
results
217
Yorgos MERTZANIS, Isaak IOANNIS, Avraam MAVRIDIS, Olga NIKOLAOU, Suzanne RIEGLER, Armin
RIEGLER and Athanasios TRAGOS
Movements, activity patterns and home range of a female brown bear (Ursus arctos, L.) in the Rodopi Mountain Range,
Greece
223
Evangelia MICHALOUDI
Dry Weights of the Zooplankton of Lake Mikri Prespa (Macedonia, Greece)
229
Chryssi MYTILINEOU, Chrissi-Yianna POLITOU, Costas PAPACONSTANTINOU, Stefanos KAVADAS,
Gianfranco D'ONGHIA and Leticia SION
Deep-water fish fauna in the Eastern Ionian Sea
235
Chrissi-Yianna POLITOU, Porzia MAIORANO, Gianfranco D'ONGHIA and Chryssi MYTILINEOU
Deep-water decapod crustacean fauna of the Eastern Ionian Sea
243
George SKOUFAS
Nesting and hatching success of the sea turtle Caretta caretta on Marathonissi island (Zakynthos, Ionian Sea, Greece)
247
Stylianos SOMARAKIS
Marked interannual differences in reproductive parameters and daily egg production of anchovy in the northern Aegean
ZOOLOGY
Sea
253
George P. STAMOU, Efi M. PAPATHEODOROU, Anastasios HOVARDAS and Maria D. ARGYROPOULOU
OF
Some structural and functional characteristics of a soil nematode community from a Mediterranean grassland
261
Stavros XIROUCHAKIS
The avifauna of the western Rodopi forests (N. Greece)
271
Lily VENIZELOS, Kalliopi PAPAPAVLOU, Marc-Antoine DUNAIS and Calliope LAGONIKA
Belgian Journal of Zoology A review and reappraisal of research in some previously unsurveyed Mediterranean marine turtle nesting sites, 1990-2001
JOURNAL
279
A. ZENETOS, D. KOUTSOUBAS and E. VARDALA-THEODOROU
Origin and Vectors of Introduction of Exotic Molluscs in Greek Waters
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Volume 135 (2)
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Belg. J. Zool., 135 (2) : 105-107
July 2005
INTRODUCTION
Ninth International Congress
on the Zoogeography and Ecology of Greece and Adjacent Regions (9ICZEGAR)
(22-25 May 2002, Thessaloniki, Greece)
Assessing Biodiversity in the Eastern Mediterranean
Region: Approaches and Applications
Biodiversity, as a concept and research objective, has
Despite the significance of all those contributions, the
been the focus of the international scientific community
Organizing Committee was forced to select a limited
ever since the last Tasmanian wolf (Trylacinus cynoceph-
number of papers in order to have them published in a
alus) disappeared in the mid-30s. Several decades later, in
special issue of the Belgian Journal of Zoology. The
1992, the Convention of Rio came as a result of the urgent
selection was done according to the standards of the host-
need to record and conserve biodiversity. Despite its inev-
ing journal following peer reviews from an international
itable deficiencies, the Convention remains the most
committee of referees. The list of referees is found at the
important tool for the conservation of biological diversity
end of this introduction. Fifty papers were submitted for
(GASTON & SPICER, 1998). Following this line of thought,
review and 25 of them met the international standards
the Hellenic Zoological Society organised the 9th Interna-
imposed by the journal and are included in these proceed-
tional Congress on the Zoogeography and Ecology of
ings.
Greece and Adjacent Regions (9ICZEGAR) focusing on
The papers on aquatic ecosystems refer mostly to the
the main topic of "Assessing Biodiversity in the Eastern
marine environment and only few deal with freshwater
Mediterranean Region: Approaches and Applications".
biology. Summarizing the contents of those papers, there
The congress was held in Thessaloniki (Greece) from 22
is an apparent increasing interest in certain groups of the
to 25 May 2002.
eastern Mediterranean Sea, such as mollusks and deca-
The scope of that endeavor was (a) to assess the gen-
pods. For instance, new data are presented on the struc-
eral inquiries on biodiversity and its three major
ture of the mollusk fauna on the hard substrate of the
components : taxonomy, genetics, and ecology, (b) to
lower sublittoral zone (15-45 m depth). There are also
unfold the range of investigations that take place in the
first records of species at various locations in the eastern
eastern Mediterranean and (c) to establish biodiversity as
Mediterranean, which show a high level of spatial homo-
a mean for developing management models with viable
geneity in the abundance of species. A review of the
predictions. Prior to this congress, several other important
fauna of exotic mollusk species in the Greek seas con-
scientific conferences and papers have tackled the general
firms the continuous species migrations from one geo-
concept of biodiversity (e.g. MARBENA e-conference,
graphic region (e.g. Red Sea, Indian Ocean) to another
GRAY, 1997 ; BIANCHI & MORRI, 2000 ; JACKSON et al.,
(e.g. Mediterranean). Similar information is also recorded
2001 ; ORME et al., 2002 ; PRICE, 2002 ; PAULY &
for cephalopods, where preliminary results and an analy-
WATSON, 2003 ; among others). The present effort, with-
sis of their abundance in space and time contribute signif-
out losing any of the innate meaning, aimed to contribute
icantly to our knowledge of this group in the broader
significantly to the propagation of scientific research in
region of .. Mediterranean. Another study of great
the eastern Mediterranean as well as to the understanding
interest focusing on deep-sea decapods of the Ionian Sea
of the priorities set by the scientific community for this
records 39 species and describes their bathymetrical dis-
region.
tribution.
A total of 304 scientists, representing 60 research cent-
The research of deployment of artificial reefs in the
ers (Universities or Institutes) from 16 different countries,
Eastern Mediterranean has not started until recently.
participated in the 9th ICZEGAR. During this congress,
Despite the delay, the results of these efforts have so far
156 papers were presented comprising 8 invited lectures,
shown the significant contribution of the artificial reefs to
106 oral presentations, and 42 posters that were divided
the reservation and upgrade of the marine environment in
into a terrestrial fauna session and an aquatic fauna ses-
the N.E. Mediterranean. The region of the North Aegean
sion. A closer view of the abstracts of these contributions
Sea, though richer in nutrients than the Southern Aegean
revealed a diverse array of research subjects. More specif-
or even the Levantine Sea, is still not as rich as the West-
ically, 25 presentations dealt with issues of marine Biol-
ern Mediterranean. These data can induce further discus-
ogy, 23 of ichthyology, 21 of mammalian biology, 19 of
sion on the value of such deployments and also on the
freshwater ecology, 15 of soil biology, 14 of ornithology,
introduction of new temporal-spatial strategies for the
7 of insects, 6 of wetlands, 5 of amphibians and reptiles,
exploitation of similar developmental practices.
and 5 of terrestrial gastropods. Moreover, there were 16
The on-growing interest of the scientific community on
contributions dealing with molecular biology and genet-
the subject of fishery resources and management is
ics, whereas 10 presentations referred to threatened spe-
present in three of the papers. Two of them examine the
cies, such as cetaceans, monk seals or loggerhead turtles.
influence of climatic changes on the reproduction of fish
106
Introduction
and substantiate the concern for the future of fish stocks
agreed in (a) the need for collaboration between research
in the Mediterranean. Lastly, a significant study of the
institutions and NGOs on an international level for long-
functional importance of marine ecosystems, one of the
term continuous basic and applied research on threatened
three levels of biodiversity, contributes extensively to the
species, and (b) the formation of national policies for
assessment of the physical or physiological condition of
environmental protection incorporating large mammals
the Mediterranean, a sea with particular environmental
within the frames of European action plans.
and socio-economic problems, as indicated in many
F.A.O. reports.
ACKNOWLEDGEMENTS
As far as the terrestrial fauna is concerned, the selected
The Organizing Committee of the 9th ICZEGAR is grateful to
contributions deal with soil invertebrates, birds, and
all major and minor sponsors : the Ministry of Culture, the
mammals. In terms of soil invertebrates, changes in the
Egnatia Odos S.A., and the Aristotle University of Thessaloniki.
community organization patterns of epiedaphic coleopter-
We also like to express our gratitude to all the invited speakers
ans was used to assess human impact in a protected forest
who honoured the congress with their presence : Bailly N.
reserve, while another contribution explores the effects of
(Paris, France), Boero F. (Lecce, Italy) Bouchet P. (Paris,
global climate change on the structural and functional
France), Froese R. (Kiel, Germany), Goujet D. (Paris, France),
features of a soil nematode community. The subjects of
Koufos G. (Thessaloniki, Greece), Lazaridou-Dimitriadou M.
the contributions on birds range from detailed investiga-
(Thessaloniki, Greece), Scouras Z. (Thessaloniki, Greece),
tions of the feeding patterns and diets of owls, herons, and
Sgardelis S. (Thessaloniki, Greece), Schockaert E. (Diepenbeek,
Belgium). Special thanks go to Damianidis P. and Christidis J.
egrets, to the composition and species richness of bird
for their tireless work during all the stages of the organization of
species in protected mountain forests. Another contribu-
this congress. Lastly, we wish to thank all the referees for their
tion uses eggs of gulls, avocets, and terns as bioindicators
valuable and instructive remarks during the selection process of
for the evaluation and impact of agrochemical pollutants
the papers of this special issue of Belgian Journal of Zoology.
in Greek wetlands of international importance. Lastly,
one contribution on mammals explores the major Neo-
Chariton C. Chintiroglou
gene/Quaternary mammalian migrations and faunal
Maria D. Argyropoulou
changes in the southern Balkans that contributed to mod-
Dionisios Youlatos
ern mammalian diversity in the eastern Mediterranean
Kostas Stergiou
region. Two other contributions focus on voles, one
Aristotle University of Thessaloniki,
investigating patterns of interpopulation variability based
School of Biology, Department of Zoology,
on allozyme variation, the other one focuses on their use
54124 Thessaloniki, Greece
as efficient bioindicators of polymetal dust emissions.
Two contributions deal with carnivores in Greece, one
exploring the activity patterns, movements, and home
REFERENCES
ranges of female brown bears, and one assess the popula-
tion status of golden jackals.
BIANCHI, C.N. & C. MORRI (2000). Marine Biodiversity of the
Mediterranean Sea : Situation, problems and prospects for
future research. Mar. Poll. Bull., 40 : 367-376.
In addition to the paper presentations, a round table
GRAY, J.S. (1997). Marine biodiversity : patterns, threats and
was organized concerning the Protection and Manage-
conservation needs. Biodiv. Conserv., 6 : 153-175.
ment of Wild Populations of Large Mammals in Southern
ORME, C.D.L., QUICKE, D.L.J., COOK, J.M. & A. PURVIS (2002).
Balkans. Many authorities from Hellenic Universities, as
Body size does not predict species richness among the meta-
well as Hellenic and international NGOs participated and
zoan phyla. J. Evol. Biol., 15 : 235-247.
exchanged basic and applied knowledge on this issue. All
PRICE, A.R.G. (2002). Simultaneous "hotspots" and "coldspots"
parties concluded that recent evaluation on the population
of marine biodiversity and implications for global conserva-
estimates of large terrestrial mammals in Southern Bal-
tion. Mar. Ecol. Prog. Ser., 241 : 23-27.
kans shows an alarming reduction. The main causes
PAULY, D. & R. WATSON (2003). The last fish. Sci. Amer., July :
assessed were (a) human-induced habitat fragmentation
43-47.
and degradation resulting in small, genetically isolated
JACKSON, J.B.C., KIRBY, M.X., BERGER, W.H., BJORNDAL, K.A.,
populations, (b) poaching and intense hunting pressure
BOTSFORD, L.W., BOURQUE, B.J., BRADBURY, R.H., COOKE,
without legal regulations, and (c) absence of a policy
R., ERLANDSON, J., ESTES, J.A., HUGHES, T.P., KIDWELL, S.,
L
incorporating mammals within the larger frame of biodi-
ANGE, C.B., LENIHAN, H.S., PANDOLFI, J.M., PETERSON,
C.H., STENECK, R.S., TEGNER, M.J. & R.R. WARNER (2001).
versity conservation. The situation is considered critical,
Historical overfishing and the recent collapse of coastal eco-
demanding state and public awareness through the propa-
systems. Science, 293 : 629-637.
gation of information coming from current and ongoing
GASTON, K.J. & J.I. SPICER (1998). Biodiversity : An Introduc-
research. All parties acknowledged these problems and
tion. Blackwell Science, Oxford.
Introduction
107
LIST OF REFEREES
Kevrekidis T. (Alexandroupolis, Greece)
Korfiatis K. (Nicosia, Cyprus)
Abatzopoulos T. (Thessaloniki, Greece)
Koutsoubas D. (Mytilini, Greece)
Akriotis T. (Mytilini, Greece)
Lanszki J. (Kaposvar, Hungary)
Argyropoulou M.D. (Thessaloniki, Greece)
Lazaridou M. (Thessaloniki, Greece)
Bellan-Santini D. (Marseille, France)
Lescure J. (Paris, France)
Bitar G. (Hadath, Lebanon)
Loumbourdis N. (Thessaloniki, Greece)
Boitani L. (Roma, Italy)
Magura T. (Debrecen, Hungary)
Bose M. (Milano, Italy)
Michaloudi E. (Thessaloniki, Greece)
Bustness J.O. (Tromso, Norway)
Nagy P. (Godollo, Hungary)
Catsadorakis G. (Dadia, Greece)
Paillison J.M. (Rennes, France)
Chintiroglou C.C. (Thessaloniki, Greece)
Perez-Mellado V. (Salamanca, Spain)
Cooper W. (Fort Wayne, U.S.A.)
Rook L. (Firenze, Italy)
Copplestone D. (Liverpool, U.K.)
Searle J.B. (York, U.K.)
Dahle B. (As, Norway)
Sergio F. (Trento, Italy)
Denys C. (Paris, France)
Sgardelis S. (Thessaloniki, Greece)
Eleutheriou E.(Heraklion, Greece)
Sinis A. (Thessaloniki, Greece)
Fasola M. (Pavia, Italy)
Skoufas G. (N. Moudania, Greece)
Ferris H. (Davis, U.S.A.)
Somarakis S. (Patra, Greece)
Froese R. (Kiel, Gremany)
Stergiou K. (Thessaloniki, Greece)
Galil B. (Haifa, Israel)
Swenson J. (As, Norway)
Gasc J.-P. (Paris, France)
Thessalou-Legaki M. (Athens, Greece)
Gautier M. (Lyon, France)
Triantafyllidis A. (Thessaloniki, Greece)
Goutner V. (Thessaloniki, Greece)
Triantafyllidis C. (Thessaloniki, Greece)
Hafner H. (Arles, France)
Verriopoulos G. (Athens, Greece)
Hays G.C. (Swansea, U.K.)
Voultsiadou E. (Thessaloniki, Greece)
Hudec I. (Kosice, Slovakia)
Xirouchakis S. (Heraklion, Greece)
Karamanlidis A. (Thessaloniki, Greece)
Youlatos D. (Thessaloniki, Greece)
Kazantzidis S. (Thessaloniki, Greece)
Zenetos A. (Athens, Greece)
Belg. J. Zool., 135 (2) : 109-118
July 2005
Contribution to the study of the diet of four owl species
(Aves, Strigiformes) from mainland and island areas of
Greece
Haralambos Alivizatos1, Vassilis Goutner2 and Stamatis Zogaris3
1 4 Zaliki Street, GR-11524 Athens, Greece
2 Department of Zoology, School of Biology, Aristotelian University of Thessaloniki, GR-54124, Thessaloniki, Greece
3 40 Perrikou Street, GR-11524 Athens, Greece
Corresponding author : Vassilis Goutner, e-mail : vgoutner@bio.auth.gr
ABSTRACT. The diets of the Barn Owl (Tyto alba), Little Owl (Athene noctua), Long-eared Owl (Asio otus) and
Eagle Owl (Bubo bubo) were studied through analysis of pellets collected at 13 different continental areas and
islands of Greece. The most important prey of the Barn Owl was mammals (mainly Microtus, Mus, Apodemus, Rat-
tus and Crocidura), although birds and amphibians were of some importance on Antikythera island and Potidea
(Central Macedonia), respectively. Average prey biomass ranged from 12.5 g to 42.8 g. The median prey biomass
differed significantly between areas (p<0.001). The diet of the Little Owl was more diverse, consisting mainly of
mammals (mostly Microtus, Mus, Apodemus, Micromys and Crocidura) in the Evros and Axios Deltas, mainly of
insects (mostly Orthoptera and Coleoptera) in the Kitros Lagoon, Psara and Tilos islands, while birds and reptiles
were common supplementary prey. Average prey biomass ranged from 0.7 g to 11.9 g. The median prey biomass
differed significantly between the areas studied (p<0.001). The diet of the Long-eared Owl in both Nestos Delta
and Porto Lagos consisted mainly of mammals (mostly Microtus, Mus and Apodemus), with some reptiles in the
former area and birds in the latter. Average prey biomass was 18.5 g and 19.5 g respectively. The median prey bio-
mass did not differ significantly between the two areas. The diet of the Eagle Owl in the Amvrakikos wetland con-
sisted mostly of birds (62 % by biomass) and mammals (36 %, mainly Rattus norvegicus). Insects were the most
important prey by numbers - 47 % (1% by biomass). The prey diversity of the Eagle Owl was the highest while that
of the Barn Owl was the lowest. Prey use by owls tended to clump by geographic area. We conclude that the owl
species studied make use of prey according to the local availability and in accordance to the hunting abilities of
each species.
KEY WORDS : Barn Owl Tyto alba, Little Owl Athene noctua, Long-eared Owl Asio otus, Eagle Owl Bubo bubo,
diet, feeding ecology, Greece.
INTRODUCTION
MATERIAL AND METHODS
The study areas (Fig. 1) encompass different habitats.
Studies carried out on the diet of owls (Strigiformes) in
The Evros, Nestos and Axios Deltas, as well as Porto
Europe have revealed considerable geographical variation
Lagos, Kitros Lagoon and Amvrakikos area are major
in the diet of each species (BUNN et al., 1982; MIKKOLA,
wetlands, with a high diversity of habitats, such as salt-
1983; CRAMP, 1985; TAYLOR, 1994). Generally, prey
marshes, lagoons, reedbeds, tamarisk and riparian forest,
composition and diversity in the Mediterranean area are
marshes and cultivations (MEHPW, 1985; 1986a;
different to those in central and northern Europe (HER-
1986b). Potidea and Parthenio areas, both in central Mac-
edonia, include mainly agricultural land. The study sites
RERA & HIRALDO, 1976).
in Mt. Hymettus and Avlona (both near Athens) include
In Greece, nine owl species are known to occur and
open scrublands (phrygana) habitat and farmland. The
islands of Psara (NE Aegean), Tilos (SE Aegean) and
some of them are common in both continent and island
Antikythera (between Peloponese and Crete) include
habitats (HANDRINOS & AKRIOTIS, 1997) but dietary stud-
mainly phrygana and (to a lesser extent) farmland.
ies are scarce. The aims of this study were : a) to describe
Pellets were collected opportunistically from roosts
and compare the diet and feeding ecology of the Barn
between December 1997 and August 2001 (Table 1). The
Owl (Tyto alba (Scopoli, 1769)), Little Owl (Athene noc-
material was collected out of the breeding season, mostly
tua (Scopoli, 1769)), Long-eared Owl (Asio otus (Lin-
in winter, excepting that of the Eagle Owl collected at
naeus, 1758)) and Eagle Owl (Bubo bubo (Linnaeus,
nests. Pellets were analyzed using reference books
1758)) studied in various parts of Greece and, b) to com-
(Mammals : LAWRENCE & BROWN, 1973; CHALINE, 1974.
pare our results with those of studies carried out in Greece
Birds : BROWN et al. (1987). Reptiles : ARNOLD & BUR-
and other European countries.
TON (1980). Insects : CHINERY (1981)). The average
110
Haralambos Alivizatos, Vassilis Goutner and Stamatis Zagoris
weight of each prey taxon was taken from the literature
M. rossiaemeridionalis was by far the most important
(Mammals : MACDONALD & BARRET (1993). Birds : PER-
prey species (84%). The relative contributions of other
RINS (1987). Reptiles : HELMER & SCHOLTE (1985).
mammal species were below 5%. Birds formed only a
Insects : ZERUNIAN et al. (1982)). Because of the diffi-
minor part of the diet in this area (2%).
culty of distinguishing mice Mus spp. and Apodemus spp.
from skulls (VOHRALIK & SOFIANIDOU, 1992), these were
TABLE 1
often not separated by species. Average prey weight for
Number of samples collected in each study area
each sample was estimated by multiplying the numbers of
each prey by its average weight, adding the weights pro-
Athene
Asio
Bubo
duced and dividing the sum by the total numbers of prey
Area
Tyto alba
noctua
otus
bubo
in each sample. The trophic diversity (NB) was estimated
by using the antilog of the Shannon-Weiner index, while
Evros Delta
4
6
-
-
in order to standardize the trophic diversity for compari-
Porto Lagos
1
-
1
-
Potidea
1
-
-
-
son within and between the areas we calculated evenness
Parthenio
1
-
-
-
index. Both were calculated on a class prey level. The
Hymettus
2
-
-
-
Mann-Whitney U-test or Kruskall-Wallis test (where
Avlona
1
-
-
-
appropriate) compared the median prey weights of the
Antikythera
1
-
-
-
same species. Cluster analysis was also performed (using
Axios Delta
-
3
-
-
Euclidean distances as distance measure and single link-
Kitros Lagoon
-
1
-
-
age as a linkage rule) on biomass proportions of prey in
Tilos
-
1
-
-
order to determine geographical relationships in the owls'
Psara
-
1
-
-
diet. The author names of prey identified in pellets of the
Nestos Delta
-
-
1
-
owls studied are indicated in Appendix 5.
Amvrakikos
-
-
-
2
In Potidea, mammalian prey dominated (at least seven
species, 92% by biomass). The main prey species was
M. macedonicus (74 %). Of moderate importance were
Apodemus spp. (7%), C. suaveolens (6%), birds (7%) and
frogs (Rana spp.) (6%).
In Parthenio, various species of mammals composed
the greater part of the diet, although birds, amphibians
and insects were also present. The most important species
by biomass were M. rossiaemeridionalis (35%), M. mac-
edonicus (21%), Rattus spp. (15%), and Apodemus syl-
vaticus (12%), while birds formed 7% of the diet. Inver-
tebrates were unimportant in the diet.
In Mt. Hymettus, at least eight mammalian species
made up 92% of the diet by biomass. The most important
prey species by biomass were A. sylvaticus (35%),
A. mystacinus (33%) and Microtus thomasi (8%). Other
species' participation did not exceed 5%. Birds formed
8% of the diet.
In Avlona, mammals again were the most important
Fig. 1. Map showing the areas where pellets of owls were col-
prey of the Barn Owl (eight species, 96% by biomass)
lected for this study.
and birds were also represented (4%). The most impor-
tant species by biomass was M. thomasi (49%), followed
by Mus domesticus (25%), M. macedonicus (8%) and
RESULTS
A. sylvaticus (6%).
In Antikythera Island, the main prey consisted of three
Barn Owl
species of mammals (83% by biomass). By far the most
important prey was Rattus rattus (73%) followed by birds
In the Evros Delta, small mammals (including at least
(16%) and M. domesticus (6%). Reptiles were repre-
10 species) composed 90% of the Diet of the Barn Owl
sented by geckoes (Gekkonidae) and formed 10% of the
(Appendix 1). The most important prey species by bio-
diet by number but only 1% by biomass.
mass was Microtus rossiaemeridionalis (37%) followed
by Mus spp. (20%), Crocidura suaveolens (12%) and
The median prey biomass was significantly different
Arvicola terrestris (7%). Birds were moderately impor-
between the seven areas (Kruskall-Wallis test, x2 =
tant by biomass (9%). Amphibians and arthropods
304.04, df = 6, p<0.001). Average prey biomass ranged
formed only a minor part of this species' diet.
from 12.5 g in Potidea to 42.8 g in Antikythera. The prey
diversity ranged from 1.12 in Porto Lagos to 2.14 in
In Porto Lagos small mammals were also the most
Antikythera, while the evenness ranged from 0.11 in
important prey (of at least five species, 97% by biomass).
Evros Delta to 0.69 in Antikythera (Table 2).
Owl diet in Greece
111
TABLE 2
diet by biomass, represented by only two species, namely
M. domesticus (15%) and C. suaveolens (7%).
Prey size and prey diversity indices of the four owl species in
Greece
The median prey biomass was significantly different
between the five areas (Kruskall-Wallis test, x2 = 367.88,
Aver-
Me-
Diver-
Eve-
N
Min
Max
df = 4, p<0.001). Average prey biomass ranged from 0.7
age
dian
sity
ness
g on Tilos Island to 11.9 g in the Axios Delta. Prey diver-
Tyto alba
sity ranged from 1.15 on Tilos Island to 2.45 in Evros
Delta, while the evenness ranged from 0.12 on Tilos to
Evros
487
14.5
12.0
1.0
100
1.17
0.11
0.58 in the Axios Delta (Table 2).
P. Lagos
116
17.2
20.0
2.0
20
1.12
0.17
Parthenio
463
18.8
20.0
1.0
150
1.31
0.20
Potidea
296
12.5
12.0
2.0
60
1.20
0.17
Long-eared Owl
Avlona
94
14.8
12.0
2.0
20
1.15
0.20
Hymettus
152
22.2
20.0
6.0
80
1.20
0.27
In the Nestos Delta, the Long-eared Owl preyed mainly
Antikythera
106
42.8
60.0
5.0
200
2.14
0.69
on mammals (at least five species, 87% by biomass) and
Athene noctua
secondarily on reptiles and birds (Appendix 3). The most
important mammalian prey was M. rossiaemeridionalis
Evros
996
10.7
12.0
0.1
70
2.45
0.46
Axios
273
11.9
12.0
0.2
60
2.24
0.58
(44% by biomass), followed by M. macedonicus (11%),
Kitros
99
1.1
0.5
0.2
25
1.45
0.26
Talpa europaea (7%), C. suaveolens (7%) and Apodemus
Lagoon
spp. (6%). Reptiles (indeterminate snakes) formed 10%
Tilos
154
0.7
0.5
0.1
12
1.15
0.12
of the prey by biomass. However, because of the small
Psara
74
1.1
1.0
0.1
12
1.45
0.26
sample, these results should be treated with caution.
Asio otus
In Porto Lagos the diet of this species consisted mainly
Nestos
52
18.5
20.0
6.0
60
1.29
0.23
of mammals (at least four species, 79% by biomass), but
P. Lagos
83
19.5
20.0
0.5
100
1.58
0.41
also included birds and insects. The most important mam-
Bubo bubo
mals were M. rossiaemeridionalis (52%), M. macedoni-
Amvrakikos
66
108.1
3.0
1.0
800
2.88
0.77
cus (17%) and Apodemus spp. (10%). Birds contributed
21% by biomass including small passerines and medium-
sized species.
Little Owl
The median prey biomass did not differ significantly
The most numerous prey types of the Little Owl in
between the two areas (Mann-Whitney U test, Z = -1.20,
Evros Delta were mammals and insects (54% and 41%
n. s.). Average prey biomass was 18.5 g. and 19.5 g. in the
by numbers respectively), although other arthropods, rep-
Nestos Delta and Porto Lagos respectively. Both prey
tiles, birds and molluscs were also represented (Appendix
diversity and evenness were higher in the Nestos Delta
2). The most important prey were mammals (at least six
(1.29 and 0.23 respectively vs. 1.58 and 0.41) (Table 2).
species, 90% by biomass), mainly M. rossiaemeridionalis
(54%), Mus spp. (13%), Apodemus spp. (10%) and Cro-
Eagle Owl
cidura spp. (6%). Birds contributed 6% by biomass,
insects only 2%.
The Eagle Owl in Amvrakikos wetland preyed on
In the Axios Delta, the most important prey were small
mammals, birds, amphibians and insects (Appendix 4).
mammals (at least eight species, 93% by biomass). The
While insects (mainly Orthoptera) formed 47% of the diet
most important species were M. rossiaemeridionalis
by number, they contributed only to 1% by biomass.
(39%), Mus spp. (12%), Micromys minutus (11%), Apo-
Birds (of at least eight large-sized species) and mammals
demus spp. (6%) and Rattus spp. (6%). Reptiles contrib-
(at least seven species) formed 62% and 36% of the bio-
uted 5% to the diet and insects only 1%.
mass of prey respectively. The most important prey spe-
In the Kitros Lagoon insects (mainly Coleoptera) were
cies were Rattus norvegicus (40%), Gallinula chloropus
the most important prey by both number (92%) and bio-
(25%), Buteo buteo (11%), Fulica atra (10%) and Eri-
mass (43%), other prey consisting of mammals, Diplop-
naceus concolor (7%). Because of the small size of the
oda and birds. Mammals formed 35% of the diet by bio-
sample (though it included prey from two different, dis-
mass, represented by Mus spp. (23%) and Crocidura
tant roosts), these results should not be considered repre-
suaveolens (12%), while birds formed 19%.
sentative of the diet of the species in our region. The prey
diversity and evenness were 2.88 and 0.77 respectively.
On Tilos Island insects were again the most important
Average prey biomass was 108.1 g. (Table 2).
prey (97% by numbers, 69% by biomass). Orthoptera
(51%) and Coleoptera (14%) were the most important
Dietary comparison between owls
insect groups. Other prey consisted of mammals and rep-
tiles. Mammals formed 27% of the diet by biomass repre-
The cluster analysis closely grouped the diets of Barn
sented by M. domesticus (21%) and C. suaveolens (5%),
Owl, Little Owl and Long-eared Owl in the wetlands of
while reptiles contributed to 5%.
northeastern Greece (group on the upper part of the clus-
On Psara Island, insects (mainly Orthoptera and Cole-
ter) (Fig. 2). The three Little Owl samples where insects
optera) were also the most important prey (92% by
predominated (Kitros Lagoon, Psara and Tilos islands)
number, 71% by biomass). Prey also included other
were also grouped together in the middle area of the clus-
arthropods and mammals. Mammals formed 24% of the
ter. The lower part of the cluster grouped the diets of the
112
Haralambos Alivizatos, Vassilis Goutner and Stamatis Zagoris
Barn Owl and Eagle Owl mainly from the western part of
al., 1982; MIKKOLA, 1983; CAPIZZI & LUISELLI, 1995) but
the study area (Athens region and Amvrakikos).
in some Mediterranean areas small mammals are domi-
nant in the diet (LO VERDE & MASSA, 1988; GOODMAN,
1988; this study) The much larger Eagle Owl can take
TaEV
much larger prey, mainly mammals and birds (frequently
TaPR
AnEV
including raptors and other owls) (MIKKOLA, 1983 :
AoPL
CRAMP, 1985; PAPAGEORGIOU et al., 1993, MARCHESI et
AnAX
al., 2002, SERGIO et al., 2003).
AoNS
TaAV
TaPL
Geographical variation in owl diet
AnAL
AnTL
In mid-European countries, voles (Microtinae) and
AnPS
TaPD
shrews are the main prey of the Barn Owl, while in the
TaHM
Mediterranean countries mice (Muridae) are more impor-
TaAN
tant (BOHR, 1962; CHEYLAN, 1976; TAYLOR, 1994). Even
BbAM
on a smaller geographical scale, as in this study, there
0
10
20
30
40
50
60
70
80
were considerable differences in the diet of the Barn Owl
Linkage distance
between the areas studied. Although mammals always
Fig. 2. Cluster analysis of the prey of the four owl species. Ta :
made up the bulk of the diet, different species predomi-
Tyto alba; An : Athene noctua; Ao : Asio otus; Bb : Bubo bubo.
nated in different areas. Microtus, Mus and to a lesser
EV : Evros Delta; PR : Parthenio; PL : Porto Lagos; AX : Axios
extent, Crocidura species were important prey in most
Delta; NS : Nestos Delta; AV : Avlona; AL : Kitros Lagoon;
areas, but other taxa were important locally (notably Apo-
TL : Tilos; PS : Psara; PD : Potidea; HM : Hymettus; AN :
demus spp. in Mt. Hymettus and R. rattus on Antikythera
Antikythera; AM : Amvrakikos.
Island). These differences may be partly seasonal (CAM-
BELL et al., 1987; TAYLOR, 1994) due to different dates the
DISCUSSION
pellets were collected, but they must also be due to zoog-
eographical reasons related to the distribution of prey spe-
Interspecific variation in owl diet
cies and also to the type, availability and extent of forag-
There were considerable differences in prey use
ing habitats of the Barn Owl in each area (DOR, 1947;
between the four owl species. The Barn Owl preyed
YOM-TOV & WOOL, 1997; MARTI, 1988). Inevitably, habi-
mainly on small mammals, while birds and amphibians
tat differences accounted for dietary differences in this
were only of local importance, and, accordingly, diet
study, as two of the areas sampled (Evros Delta and Porto
showed low diversity. Although the Long-eared Owl
Lagos) constitute wetlands, three (Parthenio, Potidea and
preyed mainly on small mammals, also took other prey
Avlona) included mainly agricultural areas, while the rest
(particularly birds and reptiles), having a more diverse
(Mt. Hymettus and Antikythera Island) included mainly
diet. The diet of the Little Owl was more variable : in two
phryganic habitats. Of Barn Owl prey, Microtus spp., as
of the study areas the main prey were mammals but other
well as Mus macedonicus, normally occur in grassland
prey involved resulted in relatively high diversity. In the
habitats, including agricultural land (VOHRALIK & SOFI-
other three areas the species took mainly insects, thus
ANIDOU, 1992), which explains their predominance as
showing a more restricted diet based on small-sized prey.
prey in areas with this habitat type. The habitat effect in
The Eagle Owl had the most diverse diet of all, taking
prey selection is also indicated in a previous study in Mt.
many species of birds, mammals and insects, and, on
Hymettus where the diet of the Barn Owl comprised M.
average, its prey was much larger than that of the other
domesticus (39%), birds (24%) (primarily Passer domes-
species.
ticus (15%) and Turdus merula (5%)), A. mystacinus
(19%) and A. sylvaticus (17%) (TSOUNIS & DIMITROPOU-
The differences in prey type and size between owl spe-
LOS, 1992). It is likely that this study encompassed a dif-
cies are due to a variety of factors such as interspecific
ferent area, probably closer to urban environment, as sug-
differences in morphology and hunting techniques, as
gested by the high numbers of M. domesticus and P.
well as different prey availability in different parts of the
domesticus.
species' range (BUNN et al., 1982). The geographical dis-
tribution and consequently availability of prey species,
The preponderance of M. rossiaemeridionalis in Porto
seemed to be important in our study as revealed by the
Lagos and of M. macedonicus in Potidea may be due to
cluster analysis where diets were clumped by geographi-
temporarily high population peaks of these species, as
cal area rather than by owl species. Despite these, there is
reported in many studies, particularly regarding Microtus
evidence that some prey types may be selected by the spe-
spp. (BUNN et al., 1982; MIKKOLA, 1983; TAYLOR, 1994).
cies studied. Thus, the Barn Owl frequently selects
It is probable that this phenomenon resulted in the consid-
shrews (Soricidae) as prey (B
erable differences in the composition of mammalian prey
UNN et al, 1982; CRAMP,
1985; T
of the Barn Owl in Porto Lagos found in a previous study
AYLOR, 1994). The Long-eared Owl, preying
mainly upon small mammals, takes shrews relatively
(Mus spp., 32% by biomass, M. rossiaemeridionalis
infrequently, while, on the other hand, it often takes birds,
28%, Apodemus spp. 10% and C. suaveolens 8%, ALIVI-
particularly in Europe (MARTI, 1976; MIKKOLA, 1983;
ZATOS & GOUTNER, 1999).
CRAMP, 1985; ALIVIZATOS & GOUTNER, 1999). In most
The low diversity of mammals in the diet of the Barn
relative studies, the Little Owl has been found to prey
Owl on Antikythera Island reflected the poor mammalian
mainly on arthropods, particularly insects, (ZERUNIAN et
fauna on the island. On the other hand, the high diversity
Owl diet in Greece
113
of birds is explained mainly by the fact that the island is
Birds are often important prey in Europe but not in North
an important migration crossroad (MESSINEO et al., 2001).
America (MARTI, 1976).
Generally, the average prey biomass is within the range
known for the Mediterranean countries. In our study areas
ACKNOWLEDGEMENTS
the differences in average biomass of the Barn Owl prey
were due to the different proportions of prey types
We are grateful to Stavros Kalpakis (Hellenic Wildlife Hospi-
tal), Stratis Bourdakis (Hellenic Ornithological Society), Theod-
involved in the areas studied. Low values were found
oros Kominos, Periklis Menounos, Maria Panayotopoulou and
where shrews and small mice were the main prey, and
Danae Portolou for collecting pellets from various areas. Also
high where rats and birds were commonest. The highest
thanks to Dr. Vladimir Vohralik for information on small mam-
value at Antikythera is more similar to that found in Israel
mals in northern Greece.
and Egypt where large-sized prey such as gerbils and rats
are consumed (GOODMAN, 1986; YOM-TOV & WOOL,
REFERENCES
1997). Thus, Barn Owls, being mainly predators of small
mammals, seem to exploit the most abundant or locally
ALIVIZATOS, H & V. GOUTNER (1999). Winter diet of the barn
available prey, according to the local conditions.
owl (Tyto alba) and long eared owl (Asio otus) in northeast-
ern Greece : a comparison. J. Raptor Res., 33 : 160-163.
The diet of the Little Owl also differed considerably in
ANGELICI, F. M., L. LATELLA, L. LUISELLI & F. RIGA (1997). The
the areas studied. In the deltas the most important prey
summer diet of the little owl (Athene noctua) on the island of
were mammals (mainly Microtus, followed by Mus and
Astipalaia (Dodecanese, Greece), J. Raptor Re.,. 31 : 280-
Apodemus spp.). In the three other areas, insects formed
182.
most of the diet. These differences could only in part be
ARNOLD, E. N. & J. A. BURTON (1980). A Field Guide to the
attributable to seasonal prey variability (CRAMP, 1985;
Reptiles and Amphibians of Britain and Europe. Collins,
ZERUNIAN et al., 1982) as the pellets from all areas were
London.
collected in winter, except on Rsara Island where they
BOHR, H. J. (1962). Zur kenthis der Vogerwelt von Korfu. Bonn.
were collected in the summer. The diet of Athene owls
Zool. Beitr., 13 : 50-114.
B
varies greatly according to habitat, location and season, as
ROWN, R., J. FERGUSON, M. LAWRENCE & D. LEES (1987).
Tracks and signs of the birds of Britain and Europe. Helm.
found in Italy, Spain, North and South America, and dif-
London.
ferences in diet most likely reflect availability rather than
BUNN, D. S., A. B. WARBURTON & R. D. S. WILSON (1982). The
prey selection (ZERUNIAN et al., 1982; JAKSIC & MARTI,
barn owl. T & D Poyser, Calton.
1988). The predominance of Microtus spp. among mam-
CAMBELL, R. W., D. A. MANUWAL & A. S. HARESTAD (1987).
malian prey was probably due to the ease of capture (lack
Food habits of the common barn owl in British Columbia.
of cover after crop harvest).
Can. J. Zool., 65 : 578-586.
CAPIZZI, D. & L. LUISELLI (1995). Comparison of the trophic
The Eagle Owl is known to take a great variety of prey,
niche of four sympatric owls (Asio otus, Athene noctua, Strix
much larger on average than those of other owls. Mam-
aluco and Tyto alba) in Mediterranean central Italy. Ecol.
mals and birds are the main prey but the participation of
Medit., 21 : 13-20.
mammals found in our study (36.2% by biomass) is the
CAPIZZI, D. & L. LUISELLI (1996). Feeding relationships and
lowest reported in Europe ranging from 62% to 94%
competitive interactions between phylogenetically unrelated
predators (owls and snakes). Acta Oecol., 17 : 265-284.
(MARTINEZ et al., 1992). In addition, the main prey of the
CHALINE. J. (1974). Les prois des rapaces. Doin, Paris.
Eagle Owl in other Mediterranean areas is Oryctolagus
CHEYLAN, G. (1976). Le regime alimentaire de la chouette
cuniculus (MARTINEZ et al., 1992), lacking from the diet
effraie Tyto alba en Europe Mediterraneene. Rev. Ecol.
in Greece. Insects, which usually constitute a prey taken
(Terre Vie), 4 : 565-579.
in small numbers (MIKKOLA, 1983; CRAMP, 1985; PAPA-
CHINERY, M. (1981). Collins Guide to the Insects of Britain and
GEORGIOU et al., 1993), in this study are exceptionally
Western Europe. Collins, London.
high in their numerical representation. The differences
CRAMP, S. (ed.). (1985). The birds of the western Palearctic.
may be due to a higher availability of other prey types in
Vol. 4, Oxford Univ. Press, Oxford.
Greece and suggest a rather opportunistic foraging behav-
GOODMAN, S. M. (1986). The prey of Barn Owls (Tyto alba)
iour in this part of the region.The mammalian prey of the
inhabiting he ancient temple complex of Karnak, Egypt.
Ostrich, 57 : 109-112.
Long-eared Owl was rather similar in the two study areas,
GOODMAN, S. M. (1988). The food habits of the little owl inhab-
made up mainly by Microtus, Mus and Apodemus species.
iting Wadi el Natrun, Egypt. Sandgrouse, 10 : 102-104.
No conclusion can be drawn on the relative importance of
HELMER, W. & P. SCHOLTE (1985). Herpetological research in
birds in Porto Lagos and reptiles in the Nestos Delta in
Evros, Greece : proposals for a biogenetic reserve. Res. Inst.
this study due to small sample sizes. In a previous study
Nature Manage., Arnhem & Dept. Animal Ecol., Nijmegen.
in Porto Lagos the Long-eared Owl was found to prey
HERRERA, C. M. & F. HIRALDO (1976). Food-niche and Trophic
mainly on Mus spp. (35%), Apodemus spp. (28%), birds
relationships among European owls. Ornis Scand., 7 : 29-41.
(16%), and only 15% on M. rossiaemeridionalis (ALIV-
JAKSIC, F. M. & C. D. MARTI (1981). Trophic ecology of Athene
owls in Mediterranean-type ecosystems : a comparative
IZATOS & GOUTNER, 1999). The predominance of the lat-
ter species in the present study can, as in the case of the
analysis. Can. J. Zool., 59 : 2331-2340.
Barn Owl, be attributed either to a temporary high popu-
LAWRENCE, M. J. & R. W. BROWN (1973). Brown mammals of
Britain. Their tracks, trails and signs. Blandford Press, Dor-
lation increase or recent habitat changes. In Greece, mice
set.
have been recorded as the most important prey (ALIVIZA-
LO VERDE, G & B. MASSA (1998). Abitudini alimentari della
TOS & GOUTNER, 1999 ; AKRIOTIS unpubl. data) but in
civetta (Athene noctua) in Sicilia. Naturalista sicil., 12
mid-Europe voles are more important (MIKKOLA, 1983).
(suppl.) : 145-149.
114
Haralambos Alivizatos, Vassilis Goutner and Stamatis Zagoris
MACDONALD, D. & P. BARRET (1993). Mammals of Britain and
MINISTRY OF ENVIRONMENT, HOUSING AND PUBLIC WORKS
Europe. Harper Collins, London.
(MEHPW) (1986b). Project for delineation of Ramsar Con-
MARCHESI, L., F. SERGIO & P. PEDRINI (2002). Costs and benefits
vention wetlands. Wetland : Amvrakikos Gulf. MEHPW,
of breeding in human-altered landscapes for the Eagle Owl
Athens (in Greek).
Bubo bubo. Ibis, 144 : E164-E 177.
PAPAGEORGIOU, N. K., C. G. VLACHOS & D. E. BAKALOUDIS
MARTI, C. D. (1976). A review of prey selection by the long-
(1993). Diet and nest site characteristics of eagle owl (Bubo
eared owl. Condor, 78 : 331-336.
bubo) breeding in two difefrent habitats in north-eastern
MARTINEZ, J. E., M. A. SANCHEZ, D. CARMONA, J. A. SANCHEZ,
Greece. Avocetta, 17 : 49-54.
A. ORTUNO & R. MARTINEZ (1992). The ecology and conser-
PERRINS, C. (1987). Collins New Generation Guide, Birds of
vation of the Eagle Owl Bubo bubo in Murcia, south-east
Britain and Europe. Collins, London.
Spain. In : GALBRAITH, TAYLOR & PERCIVAL (eds), The ecol-
SERGIO, F., L. MARCHESI & P. PEDRINI (2003). Spatial refugia
ogy and conservation of European owls, Joint Nature Con-
and the coexistence of a diurnal raptor with its intraguild owl
servation Committee (UK Nat. Cons. No 5), Peterborough :
predator. J. Anim. Ecol., (in press).
84-88.
TAYLOR, D. (1994). Barn owls. Predator-prey relationships and
MESSINEO, A., F. SPINA, & R. MANTOVANI (2001). Mediterra-
conservation. University Press, Cambridge.
nean Island Project : results 1998-1999. Biologia e con-
TSOUNIS, G. & A. DIMITROPOULOS (1992). Seasonal variation of
servazione della fauna. Istituto Nationale per la fauna selvat-
the feeding of barn owl, Tyto alba (Scopoli 1769) in Mount
ica «Alessandro Ghigi».
Hymettus, Attica, Greece. Biol. Gallo-hellenica, 19 : 29-36.
MIKKOLA, H. (1983). Owls of Europe. T & D Poyser, Calton.
VOHRALIK, V. & T. S. SOFIANIDOU (1992). Small mammals
MINISTRY OF ENVIRONMENT, HOUSING AND PUBLIC WORKS
(Insectivora, Rodentia) of Thrace, Greece. Acta Univ. Caro-
(MEHPW) (1985). Project for delineation of Ramsar Con-
linae, 36 : 341-369.
vention wetlands. Wetland : Evros Delta. MEHPW, Athens
YOM-TOV, Y. & D. WOOL (1997). Do the contents of barn owl
(in Greek).
pellets accurately represent the proportion of prey species in
MINISTRY OF ENVIRONMENT, HOUSING AND PUBLIC WORKS
the field ? Condor, 99 : 972-976.
(MEHPW) (1986a). Project for delineation of Ramsar Con-
ZERUNIAN, S., G. FRANZINI & L. SCISCIONE (1982). Little owls an
vention wetlands. Wetland : Lake Vistonis - Porto Lagos.
their prey in a Mediterranean habitat. Boll. Zool., 49 : 195-
MEHPW, Athens (in Greek).
206.
Owl diet in Greece
115
APPENDIX 1
Prey of the Barn Owl in the areas studied. N: numbers; B: biomass
EVROS
ANTI-
P. LAGOS
POTIDEA
PARTHENIO HYMETTUS
AVLONA
DELTA
KYTHERA
Prey
N % N % B
N % N % B
N % N % B
N % N % B
N % N % B
N % N % B
N % N % B
CHILOPODA
2 0.4 <0.1
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
Scolopend ra spp.
2 0.5 <0.1
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
INSECTA
3 0.7 <0.1
-
-
-
-
-
-
3 0.6 0.1
-
-
-
-
-
-
-
-
-
Tettigoniidae
2 0.6 <0.1
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
Carabidae
1 0.2 <0.1
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
Gryllotalpa gryllotalpa
-
-
-
-
-
-
-
-
-
2 0.4 <0.1
-
-
-
-
-
-
-
-
-
Scarabaeidae
-
-
-
-
-
-
-
-
-
1 0.2 <0.1
-
-
-
-
-
-
-
-
-
AMPHIBIA
1 0.2 0.4
-
-
-
7 2.4 5.7
6 1.3 2.1
-
-
-
-
-
-
-
-
-
Rana spp.
-
-
-
-
7 2.4 5.7
6 1.3 2.1
-
-
-
-
-
-
-
-
-
An
ura indet.
1 0.2 0.4
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
REPTILIA
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
11 10.4 1.2
Gekkoni
dae indet.
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
11 10.4 1.2
AVES
12 2.5 9.3
3 2.6 3.2
4 1.3 2.1
19 4.1 7.4
7 4.6 8.4
3 3.2 3.5
17 16.0 15.6
Gallinago gallinago
1 0.2 1.1
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
Erithacus rubecula
1 0.2 0.3
1 0.9 1.1
-
-
-
-
-
-
-
-
-
1 1.1 1.0
-
-
-
Sturnus vulgaris
4 0.8 4.0
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
Fringilla coelebs
-
-
-
2 1.7 2.1
-
-
-
3 0.7 0.7
4 2.6 4.6
2 2.1 2.7
-
-
-
Streptopelia sp.
-
-
-
-
-
-
-
-
-
1 0.2 1.7
-
-
-
-
-
-
-
-
-
Alcedo atthis
1 0.2 0.6
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
Turdus merula
1 0.2 1.4
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
Emberiza sp.
1 0.2 0.4
-
-
-
-
-
-
1 0.2 0.3
-
-
-
-
-
-
-
-
-
Parus major
-
-
-
-
-
-
1 0.3 0.4
-
-
-
-
-
-
-
-
-
-
-
-
Tur
dus sp.
-
-
-
-
-
-
-
-
-
-
-
-
1 0.7 2.3
-
-
-
-
-
-
Passer spp.
-
-
-
-
-
-
-
-
-
2 0.4 0.6
2 1.3 1.4
-
-
-
-
-
-
Alectoris chukar (pull.)
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
1 0.9 2.2
Porza na spp.
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
2 1.9 2.2
Otus scops
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
1 0.9 1.8
Hirundo rustica
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
2 1.9 0.9
Ficedula spp.
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
2 1.9 0.5
Lanius spp.
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
2 1.9 1.3
Miliaria calandra
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
1 0.9 0.9
Passeriformes indet.
3 0.6 1.3
-
-
-
3 1.0 1.6
12 2.6 4.1
-
-
-
-
-
-
2 1.9 1.3
A
ves indet.
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
4 3.8 4.4
MAMMALIA
468 96.1 90.2 113 97.4 96.8 285 96.3 92.2 435 94.0 90.4 145 95.4 91.6
91 96.8 96.5
78 73.6 83.2
Neomys anomalus
10 2.1 1.4
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
Crocidura leucodon
26 5.3 3.0
-
-
-
2 0.7 0.4
2 0.4 0.2
2 1.3 0.5
-
-
-
-
Crocidura suaveolens
144 29.6 12.3 13 11.2 4.2
39 13.2 6.4
42 9.2 2.9
14 9.2 2.4
9 9.6 3.7
-
-
-
Crocidura spp.
-
-
-
-
-
-
-
-
-
-
-
-
3 2.0 0.6
-
-
-
-
Suncus etruscus
2 0.4 0.1
1 0.9 0.1
2 0.7 0.1
-
-
-
-
-
-
3 3.2 0.4
-
-
-
Micromys minutus
-
-
-
-
-
-
-
-
-
7 1.5 0.6
-
-
-
-
-
-
-
-
-
Microtus rossiaemeridionalis 136 27.9 38.6 78 67.2 83.7
1 0.3 0.5 150 32.9 34.6
-
-
-
-
-
-
-
-
-
Microtus guentheri
1 0.2 0.4
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
Apodemus spp.
18 3.7 5.1
4 3.4 4.3
13 4.4 7.1
-
-
-
5 3.3 4.3
-
-
-
-
-
-
Apodemus sylvaticus
-
-
-
-
-
-
-
-
-
54 11.8 12.4
60 39.5 34.6
4 4.2 5.5
-
-
-
Apodemus mystacinus
-
-
-
-
-
-
-
-
-
-
-
-
29 19.1 33.4
-
-
-
-
-
-
Cricetulus migratorius
-
-
-
-
-
-
-
-
-
-
-
-
2 1.3 1.2
1 1.1 1.4
-
-
-
Microtus thomasi
-
-
-
-
-
-
-
-
-
-
-
-
13 8.6 7.5
35 37.2 48.5
-
-
-
Mus domesticus
-
-
-
-
-
-
-
-
-
2 0.4 0.3
-
-
-
30 31.9 24.9
22 20.8 5.8
Mus macedonicus
-
-
- 17 14.7 4.5 224 75.7 73.5 151 33.1 20.9
15 9.9 5.2
9 9.6 7.5
-
-
-
Mus spp.
117 24.0 20.0
-
-
-
-
-
-
-
-
-
1 0.7 0.3
-
-
-
-
-
-
Mustela nivalis
1 0.2 1.4
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
Rattus rattus
-
-
-
-
-
-
2 0.7 3.3
9 2.0 6.2
1 0.7 1.7
1 1.1 4.2
55 51.9 73.0
Rattus norvegicus
-
-
-
-
-
-
-
-
-
3 0.7 2.1
-
-
-
-
-
-
-
-
-
Rattus spp.
-
-
-
-
-
-
-
-
-
9 2.0 6.2
-
-
-
-
-
-
-
-
-
Arvicola terrestris
8 1.6 6.8
-
-
-
-
-
-
3 0.7 2.1
-
-
-
-
-
-
-
-
-
Talpa europaea
-
-
-
-
-
-
-
-
-
3 0.7 2.1
-
-
-
-
-
-
-
-
-
Oryctolagus cunicu
lus (juv.)
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
1 0.9 4.4
Muri
dae indet.
3 0.6 0.6
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
-
Rodentia indet.
2 0.4 0.6
-
-
-
2 0.7 1.4
-
-
-
-
-
-
-
-
-
-
-
-
Total No of prey
486
-
- 116
-
- 296
-
- 463
-
- 152
-
-
94
-
- 106
-
-
116
Haralambos Alivizatos, Vassilis Goutner and Stamatis Zagoris
APPENDIX 2
Prey of the Little Owl in the areas studied N: numbers; B: biomass
EVROS DELTA
AXIOS DELTA
KITROS LAGOON
TILOS
PSARA
Prey
N
% N
% B
N % N
% B
N
% N
% B
N
% N
% B
N
% N % B
DIPLOPODA
-
-
-
-
-
-
3
3.0
2.9
-
-
-
-
1.4
0.6
Julidae
-
-
-
-
-
-
3
3.0
2.9
-
-
-
-
1.4
0.6
MOLLUSCA
1
0.1
<0.
1
-
-
-
-
-
-
-
-
-
-
-
-
Stylommatophora indet.
1
0.1
<0.1
-
-
-
-
-
-
-
-
-
-
-
-
CHILOPODA
1
0.1
<0.
1
-
-
-
-
-
-
-
-
-
-
-
-
Scolopendra sp.
1
0.1
<0.
1
-
-
-
-
-
-
-
-
-
-
-
-
ARACHNIDA
2
0.2
<0.
1
-
-
-
-
-
-
-
-
-
3
4.1
3.7
A
ranae indet.
2
0.2
<0.
1
-
-
-
-
-
-
-
-
-
-
-
-
Solifugae indet.
-
-
-
-
-
-
-
-
-
-
-
-
3
4.1
3.7
INSECTA
408
41.1
2.4
50 17.9
1.3
91
91.9
43.2
150
97.4
68.8
68
91.9 71.1
Dermaptera
56
5.6
0.2
4
1.5
0.1
2
2.0
0.4
-
-
-
1
1.4
0.2
Labiduridae
37
1.9
0.1
3
1.1
<0.1
-
-
-
-
-
-
-
-
-
Forficulidae
19
3.7
0.1
1
0.4
<0.1
2
2.0
0.4
-
-
-
1
1.4
0.2
Odonata
55
5.5
0.
5
-
-
-
-
-
-
-
-
-
-
-
-
Anisoptera indet.
55
5.5
0.5
-
-
-
-
-
-
-
-
-
-
-
-
Orthoptera
154
15.4
1.2
34 12.5
1.2
-
-
-
114
74.0
50.9
60
81.1 65.8
Gryllotalpa gryllotalpa
24
2.4
0.4
21
7.7
0.7
-
-
-
-
-
-
-
-
-
Tettigoniidae
50
5.0
0.4
6
2.6
0.4
-
-
-
-
-
-
48
64.9 58.5
Acrididae
77
7.7
0.4
7
2.2
0.1
-
-
-
114
74.0
50.9
12
16.2
7.3
Hemiptera
6
0.6
<0.
1
-
-
-
-
-
-
-
-
-
-
-
-
Heteroptera indet.
6
0.6
<0.1
-
-
-
-
-
-
-
-
-
-
-
-
Coleoptera
68
6.8
0.3
6
2.6
0.1
89
89.9
42.0
18
11.7
13.8
5
6.8
4.9
Staphylinidae
3
0.3
<0.1
-
-
-
4
4.0
1.9
-
-
-
-
-
-
Scarabaeidae
3
0.3
<0.1
2
0.7
<0.1
-
-
-
1
0.6
0.9
3
4.1
3.7
Curculionidae
1
0.1
<0.1
1
0.4
<0.1
-
-
-
-
-
-
-
-
-
Carabidae
49
4.9
<0.1
1
1.5
<0.1
85
85.9
40.1
3
1.9
1.3
2
2.7
1.2
Dytiscus marginalis
4
0.4
<0.
1
-
-
-
-
-
-
-
-
-
-
-
-
Hydrophilus sp.
1
0.1
<0.
1
-
-
-
-
-
-
-
-
-
-
-
-
Coleoptera indet.
2
0.2
<0.1
1
0.4
<0.1
-
-
-
-
-
-
-
-
-
Tenebrionidae
-
-
-
-
-
-
-
-
-
2
1.3
0.9
-
-
-
Geotrupidae
-
-
-
-
-
-
-
-
-
12
7.8
10.7
-
-
-
Dytiscidae
5
0.5
<0.
1
-
-
-
-
-
-
-
-
-
-
-
-
Coccinellidae
1
0.1
<0.1
1
0.7
<0.1
-
-
-
-
-
-
-
-
-
Hymenoptera
59
5.9
0.1
-
-
-
-
-
-
15
9.7
1.3
2
2.7
0.2
Formicidae
59
5.9
0.1
-
-
-
-
-
-
15
9.7
1.3
2
2.7
0.2
Mantodea
14
1.4
0.1
1
0.4
<0.1
-
-
-
3
1.9
2.7
-
-
-
Mantidae
14
1.4
0.1
1
0.4
<0.1
-
-
-
3
1.9
2.7
-
-
-
REPTILIA
15
1.5
1.5
25
9.2
4.6
-
-
-
1
0.6
4.5
-
-
-
Podarcis taurica
13
1.3
0.5
24
8.8
3.1
-
-
-
-
-
-
-
-
-
Natrix sp.
1
0.1
0.
5
-
-
-
-
-
-
-
-
-
-
-
-
Colubridae indet.
1
0.1
0.5
1
0.4
1.6
-
-
-
-
-
-
-
-
-
Lacertilia indet.
-
-
-
-
-
-
-
-
-
1
0.6
4.5
-
-
-
AVES
22
2.8
6.1
2
0.7
1.3
1
1.0
19.2
-
-
-
-
-
-
Passeriformes indet.
16
3.6
3.6
2
0.7
1.3
1
1.0
19.2
-
-
-
-
-
-
Galerida cristata
2
0.2
0.
7
-
-
-
-
-
-
-
-
-
-
-
-
Sturnus vulgaris
1
0.1
0.
6
-
-
-
-
-
-
-
-
-
-
-
-
Erithacus rubecula
2
0.2
0.
4
-
-
-
-
-
-
-
-
-
-
-
-
Passer spp.
3
0.3
0.
7
-
-
-
-
-
-
-
-
-
-
-
-
MAMMALIA
520
54.2
90.2
69 72.2
92.8
4
4.0
34.6
3
1.9
26.8
2
2.7 24.4
Crocidura suaveolens
25
2.5
5.7
8
2.9
1.5
2
2.0
11.5
1
0.6
5.4
1
1.4
7.3
Crocidura leucodon
2
0.2
0.
1
-
-
-
-
-
-
-
-
-
-
-
-
Microtus rossiaemeridionalis 296
29.7
54.0
51 18.7
38.5
-
-
-
-
-
-
-
-
-
Apodemus spp.
56
5.6
10.2
10
3.7
6.3
-
-
-
-
-
-
-
-
-
Mus spp.
118
11.8
12.9
31 11.4
11.7
2
2.0
23.1
-
-
-
-
-
-
Mus domesticus
-
-
-
-
-
-
-
-
-
1
1.3
21.4
1
1.4 14.6
Rattus spp.
-
-
-
3
1.1
5.7
-
-
-
-
-
-
-
-
-
Micromys minutus
-
-
-
49 17.9
10.8
-
-
-
-
-
-
-
-
-
Suncus etruscus
-
-
-
1
0.4
0.1
-
-
-
-
-
-
-
-
-
Pipistrellus sp.
-
-
-
1
0.4
0.2
-
-
-
-
-
-
-
-
-
Muridae indet.
14
1.4
1.9
18
6.6
8.5
-
-
-
-
-
-
-
-
-
Rodentia indet.
28
2.8
5.1
25
9.2
15.8
-
-
-
-
-
-
-
-
-
Mammalia indet.
1
0.1
0.1
-
-
-
-
-
-
-
-
-
-
-
-
Total No of prey
996
-
-
273
-
-
99
-
-
154
-
-
74
Owl diet in Greece
117
APPENDIX 3
APPENDIX 4
Prey of the Long-eared Owl in the areas studied.
Prey of the Eagle Owl in Amvrakikos.
N: numbers; B: biomass
N: numbers; B: biomass
NESTOS DELTA
P. LAGOS
Prey
N
% N
% B
Prey
N
% N
% B
N % N
% B
INSECTA
35
53.0
1.4
INSECTA
-
-
-
2
2.4
0.1
Orthoptera
31
47.0
1.3
Tettigoniidae
31
47.0
1.3
Acrididae
-
-
-
1
1.2
0.1
Coleoptera
4
6.1
0.1
Tenebrionidae
-
-
-
1
1.2
0.1
Carabus sp.
1
1.5
<0.1
REPTILIA
2
3.8
10.4
-
-
-
Oryctes spp.
2
3.0
0.1
Colubridae indet.
2
3.8
10.4
-
-
-
Cerambyx cerdo
1
1.5
0.7
AVES
1
1.9
2.1
9
10.8
21.1
AMPHIBIA
1
1.5
0.7
Alauda arvensis
-
-
-
1
1.2
2.5
Rana sp.
1
1.5
0.7
Turdus sp.
-
-
-
1
1.2
5.0
AVES
13
20.0
61.7
Fringilla coelebs
-
-
-
1
1.2
1.3
Buteo buteo
1
1.5
11.2
Carduelis sp.
-
-
-
1
1.2
0.9
Gallinula chloropus
6
9.1
25.2
Passeriformes indet.
1
1.9
2.1
4
4.8
5.0
Fulica atra
1
1.5
9.8
Aves indet.
-
-
-
1
1.2
6.3
Charadriiformes indet.
1
1.5
1.4
MAMMALIA
49
94.2
87.5
72
86.7
78.8
Columba livia
1
1.5
3.5
Crocidura suaveolens
11
21.1
6.9
1
1.2
0.4
Streptopelia decaocto
1
1.5
2.8
Talpa europaea
2
3.8
14.6
-
-
-
Tyto alba
1
1.5
4.2
Microtus rossiaemer-
21
40.4
43.8
41
49.4
51.7
Asio otus
1
1.5
3.5
idionalis
MAMMALIA
17
25.8
36.2
Apodemus spp.
3
5.8
6.3
8
9.6
10.1
Erinaceus concolor
1
1.5
7.0
Mus macedonicus
9
17.3
11.3
22
26.5
16.6
Sciurus vulgaris
1
1.5
2.8
Rodentia indet.
3
5.8
4.7
-
-
-
Glis glis
1
1.5
1.4
Total No of prey
52
-
-
83
-
Microtus thomasi
1
1.5
0.3
Rattus rattus
1
1.5
1.4
Rattus norvegicus
11
16.7
39.9
Mus sp.
1
1.5
0.2
Total No of prey
66
-
-
118
Haralambos Alivizatos, Vassilis Goutner and Stamatis Zagoris
APPENDIX 5
Full names of prey identified in owls' pellets in this study
ARTHROPODA
Parus major Linnaeus 1758
Scolopendra Linnaeus 1758
Emberiza calandra Linnaeus 1758
Gryllotalpa gryllotalpa Linnaeus 1758
Emberiza Linnaeus 1758
Dytiscus marginalis (Linnaeus 1758)
Fringilla coelebs Linnaeus 1758
Hydrophilus Geoffroy 1762
Carduelis Brisson 1760
Carabus Linnaeus 1758
Passer Brisson 1760
Oryctes Illiger 1798
Sturnus vulgaris Linnaeus 1758
Cerambyx cerdo Linnaeus 1758
MAMMALIA
AMPHIBIA
Erinaceus concolor Martin 1838
Rana Linnaeus 1758
Neomys anomalus Cabrera 1907
REPTILIA
Talpa europaea Linnaeus 1758
Podarcis taurica Pallas 1814
Suncus etruscus (Savi 1822)
Natrix Laurenti 1765
Crocidura suaveolens (Pallas 1811)
Crocidura leucodon (Hermann 1780)
AVES
Crocidura Wagler 1832
Buteo buteo (Linnaeus 1758)
Pipistrellus Kaup 1829
Alectoris chukar (J. E. Gray 1830)
Oryctolagus cuniculus (Linnaeus 1758)
Porzana Vieillot 1816
Sciurus vulgaris (Linnaeus 1758)
Gallinula chloropus (Linnaeus 1758)
Glis glis (Linnaeus 1766)
Fulica atra Linnaeus 1758
Cricetulus migratorius (Pallas 1773)
Gallinago gallinago (Linnaeus 1758)
Microtus rossiaemeridionalis Ognev 1924
Columba livia Gmelin 1789
Microtus guentheri (Danford & Alston 1880)
Streptopelia decaocto (Frivaldsky 1838)
Microtus thomasi (Berrett-Hamilton 1903)
Streptopelia Bonaparte 1855
Arvicola terrestris (Linnaeus 1758)
Tyto alba (Scolopi 1769)
Asio otus (Linnaeus 1758)
Rattus norvegicus (Berkenhout 1769)
Otus scops (Linnaeus 1758)
Rattus rattus (Linnaeus 1758)
Alcedo atthis (Linnaeus 1758)
Rattus Fischer 1803
Alauda arvensis Linnaeus 1758
Apodemus sylvaticus (Linnaeus 1758)
Galerida cristata (Linnaeus 1758)
Apodemus Kaup 1829
Hirundo rustica Linnaeus 1758
Apodemus mystacinus (Danford & Alston 1877)
Lanius Linnaeus 1758
Micromys minutus (Pallas 1771)
Ficedula Brisson 1760
Mus domesticus Swarz & Swarz 1943
Erithacus rubecula (Linnaeus 1758)
Mus Linnaeus 1766
Turdus merula Linnaeus 1758
Mus macedonicus Petrov & Ruzic 1983
Turdus Linnaeus 1758
Mustela nivalis Linnaeus 1766
Belg. J. Zool., 135 (2) : 119-126
July 2005
Mollusca fauna from infralittoral hard substrate assem-
blages in the North Aegean Sea
Chryssanthi Antoniadou1, Drossos Koutsoubas2 and Chariton C. Chintiroglou1
1 Aristotle University, School of Biology, Department of Zoology, P.O. Box 134 Gr-540 06 Thessaloniki, Greece
2 Department of Marine Science, University of the Aegean, 81100, Mytilene, Greece.
Corresponding author : C. Chintiroglou, e-mail : chintigl@bio.auth.gr
ABSTRACT. The spatial distribution of the molluscan fauna from infralittoral hard substrate assemblages in the
North Aegean Sea was studied during summer 1997 and 1998. Material was collected from six stations located in
Chalkidiki peninsula, plus one in Kavala Gulf. Samples were collected by means of SCUBA diving (5 replicates
with a quadrate sampler covering the surface of 400cm2). Examination of the 10917 living molluscs collected
revealed 111 species, belonging to three different classes (five Polyplacophora, 85 Gastropoda and 21 Bivalvia).
Skeneopsis planorbis, Trapania maculata and Limapontia capitata are reported for the first time as elements of the
molluscan fauna in the Eastern Mediterranean or the Aegean Sea, and Callistochiton pachylasmae, Raphitoma leu-
froyi, Polycera quadrilineata, Phyllaplysia lafonti and Petalifera petalifera as elements in the North Aegean Sea.
Multivariate analyses (Cluster and MDS), discriminate the sampling stations into four main groups, indicating, that
apart from the rough dispersion of the molluscs, a more homogenous pattern is detectable at the middle part of the
lower infralittoral zone.
KEY WORDS : Keywords : Molluscs, infralittoral, Aegean Sea, hard substrate, biodiversity
INTRODUCTION
When considering hard substrate within the infralittoral
zone, three different ecological sub-zones can be
The term `biodiversity' is recently defined as the col-
recognized : a high one, which extends from 0 to 2m and
lection of genomes, species and ecosystems occurring in a
is characterized by the assemblage of photophilic algae,
geographically defined region (CBDMS, 1995). Its value
an intermediate one extending from 2 to approximately
as an indicator of environmental health is now largely rec-
12m and dominated by several hydrozoans species, and a
ognized (GASTON & SPICER, 1998 ; BIANCHI & MORRI,
low one extending to almost 40m, where the sciaphilic
2000) and species diversity, i.e. composition, recognised
algal assemblage occurs (MARINOPOULOS, 1988). Biodi-
as an important indicator of diversity across spatial scales
versity aspects in these three sub-zones are rather well
and habitats. A considerable amount of information con-
studied in the Western and Central Mediterranean (BIGGS
cerning the biodiversity of Mediterranean ecosystems has
& WILKINSON, 1966 ; BELLAN-SANTINI, 1969 ; HONG,
been organised and presented with reference to the classi-
1983 ; RICHARDS, 1983 ; POULICEK, 1985 ; GIANGRADE,
fication of benthic biocenoses (PÉRÈS, 1967) or organis-
1988) and the neighbouring Atlantic Ocean (e.g. the
mic assemblages (PÉRÈS, 1982), since this scheme has
North Sea - KLUIJVER, 1997), but less so for the Eastern
been considered as appropriate for that basin (AUGIER
Mediterranean (PÉRÈS & PICARD, 1964 ; AUGIER, 1982 ;
1982).
DAUVIN, 1993 ; BELLAN-SANTINI et al., 1994).
Considering molluscs, available information during the
The present study discusses in detail the molluscan
earlier parts of the 20th century came mainly from general
diversity, and qualitatively illustrates its spatial dispersion
ecological and faunal surveys in the Eastern Mediterra-
in the lower infralittoral hard substrate assemblages in the
nean (e.g. PÉRÈS & PICARD, 1958 ; LEDOYER, 1969 ;
North Aegean Sea.
STRACK, 1988). Throughout the last ten years, records of
molluscs were included in almost all research surveys
carried out in Greek waters, mainly in the Aegean and the
Ionian Seas, and information is summarized in KOUTSOU-
BAS (1992), DELAMOTTE & VARDALA-THEODOROU (1994),
ZENETOS (1997), KOUTSOUBAS et al. (2000a). However, a
biotope approach, based on the molluscan fauna distrib-
uted along the continental shelf of the Greek Seas and
using numerical taxonomic methods, has been attempted
in very few cases and even those cover only the soft sub-
strate assemblages (e.g. ZENETOS et al., 1991, 1997 ;
Fig. 1. Map of the study area, showing the location of sam-
KOUTSOUBAS et al. 2000b).
pling sites.
Figure 1. Map of the study area, showing the location of sampling sites.
120
Chryssanthi Antoniadou, Drossos Koutsoubas and Chariton C. Chintiroglou
MATERIAL AND METHODS
strate extension and inclination (ranging from 45 to 90°).
According to the maximum depth of hard substrate at each
Sampling sites
station, one to three substations were set (a-15 meters, b-30
Seven stations were set at different locations in the North
meters and c-40 meters) in order to cover bathymetrically
Aegean Sea (Fig. 1). They were chosen for their dispersion
the entire range of the lower infralittoral zone. Basic char-
in this specific biogeographical zone and their hard sub-
acteristics of all stations are given in Table 1.
TABLE 1
Physical and biotic characteristics of sampling stations.
Station
Slope (o)
Maximum Depth (m)
Prevailing Winds
Substations
Biotic Characteristics
1 Kakia Skala
90
65
N, NE, SE
a - 15m
Womersleyella setacea
b - 30m
Womersleyella setacea
c - 40m
Lithophylum sp., Peysonellia sp.
2 Kelyfos
70
35
S, SW, SE, NW
a - 15m
Padina pavonica, Codium bursa
b - 30m
Womersleyella setacea
3 Porto Koufo
90
50
SW
a - 15m
Womersleyella setacea
b - 30m
Womersleyella setacea
c - 40m
Lithophylum sp., Peysonellia sp.
4 Armenistis
50-60
35
NE
a - 15m
Womersleyella setacea, Padina pavonica
b - 30m
Womersleyella setacea
5 Vourvourou
55
18
N, SE
a - 15m
Pseudolithophylum expansum, Gelidium pecti-
natum, Cladocora caespitosa
6 Eleftheronissos
70
30
NE, SE, N, S
b - 30m
Lithothamnion sp., Polysiphonia sp.
7 N.Iraklitsa
65
35
NE, NW, SE
a - 15m
Cutleria multifida, Gelidium pectinatum
b - 30m
Cutleria multifida, Gelidium pectinatum
Sampling techniques
ethyl alcohol (70%). All living molluscs, after sorting,
were identified to species level and counted.
Physico-chemical factors
At each station measurements of the main abiotic
Data analysis
parameters of the water column, i.e. temperature, salinity,
Common biocoenotic methods were employed to ana-
conductivity, dissolved O and pH, were carried out along
2
lyze the data (G
the column of the water using the WTW salinity-conduc-
UILLE 1970 ; HONG 1983, BAKUS, 1990
and others). Thus, the molluscan community structure
tivity-O meter and Lovibond Checkit (pH meter) micro-
2
was analysed by means of total number of species (S),
electronic equipment. Water clarity was also detected
average density (D - mean number of individuals/m2),
using the Secchi disc.
Shannon-Weaver diversity (H', log basis), Margalef's
2
Data collection
species richness (d) and Pielou's evenness (J') indices.
Sampling was carried out by means of scuba diving
Molluscs were classified according to their distribution
using a modified quadrate sampler, covering a surface of
to organismic assemblages (summarized in Table 2) based
400cm2, which is the minimum necessary for a statisti-
on information derived from PÉRÈS & PICARD, 1958;
cally sound investigation on hard substrate benthic com-
FRETTER & GRAHAM, 1962; LEDOYER, 1969; SMECKEL
munities (W
& PORTMANN, 1982; ROS & GILI, 1985; ZENETOS, 1993,
EINBERG 1978 ; STIRN 1981). Five replicate
samples (B
1997; STRACK, 1988; CATTANEO-VIETTI et al., 1990;
ELLAN-SANTINI, 1969 ; MARINOPOULOS, 1988),
were taken at each substation. All samples (75 overall)
KOUTSOUBAS, 1992; DELAMOTTE & VARDALA-THEOD-
were collected by the same divers (authors), during sum-
OROU, 1994).
mer months (July, August). At St.3 one more sampling
The multivariate analysis was based on presence/
attempt was performed at the depth of 30m, after one
absence data per sampling substation, in order to equalize
year, in order to identify annual changes in the structure
the contribution of each species. Thus, cluster analysis
of the fauna. During sampling the physiognomic aspects
(group average) and non-metric multidimensional scal-
of the biotopes were registered by means of an underwa-
ing, based on the Bray-Curtis similarity, were performed,
ter camera. All the samples were sieved through a 0.5mm
using PRIMER package (CLARKE & GREEN 1988;
mesh, fixed in 10% neutralized formalin and preserved in
CLARKE & WARWICK 1994; DIGBY & KEMPTON 1994).
Molluscan fauna from infralittoral hard substrate assemblages in the North Aegean Sea
121
The significance of the multivariate results was assessed
and 8.2 at the rest of the stations). Dissolved oxygen val-
with ANOSIM test (CLARKE, 1993).
ues were generally high (from 6.5-10 mg/l) with an aver-
age value of 7.5 mg/l. Water clarity exceeded 20m in all
RESULTS
sampling sites apart from st.5 (Vourvourou), where it was
reduced to 12m, probably due to the increased presence of
Abiotic factors
suspended particulate organic matter in the area.
The pattern of the main abiotic parameters showed
slight variation in relation to bathymetry or the location of
Faunal composition and zoogeographical Remarks
the sampling sites. Temperature values fluctuated with
depth, ranging from a minimum of 16.1°C at 40m to
Examination of the collected living material (10917
27.5°C at water surface. The seasonal thermocline, due to
individuals), revealed 111 mollusc species. Gastropoda
summer (sampling was performed at the end of July-
dominate in species number (85 species) followed by
beginning of August), was detected at all stations at the
Bivalvia (21 species) and Polyplacophora (five species).
average depth of 25m (end of July- first days of August),
Within Gastropoda the taxonomic groups with the highest
with the exception of St.5 (Vourvourou), possibly due to
number of species and individuals were the prosobranch
its shallow depth (18m). Salinity and conductivity
families Trochidae, Rissoidae, Cerithiidae, Muricidae and
showed similar variations. Their values ranged from 29.1
Turridae and the heterobranch family Pyramidellidae. A
to 37.8 psu and 41.1 to 51.6 µS/cm respectively, with no
complete list of the species in phylogenetic order within
really significant change in relation to depth, except from
major taxa is presented in Table 2. The total number of
St.7 (N. Iraklitsa), where a notable decrease was observed
species ranged from 64 at St.1 to 17 at St.5. Stations 1, 2,
(29.1 psu). The pH values were almost constant in rela-
3 and 4 were the most species rich, with stations 5, 6 and
tion to depth in all stations (8.5 at St.1 and St.7; 7.5 at St.4
7 the most poor.
TABLE 2
Molluscs reported from the hard substrata infralittoral assemblages. The numerical abundance is estimated from the total number of
replicates per each substation (number of individuals per 0.2m2). The ecological status of each species (EC), is given by HS for hard
substrate, C for coralligenous, PA for photophilic algae, HP for Posidonia oceanica meadows, DC for detritic costs, G for caves, SS
for soft sediments, VTC for coastal terrigenous mud and U for unknown demands.
St.1
St.1 St.1
St.2
St.2
St.3
St.3
St.3
St.3
St.4
St.4
St.5
St.6
St.7
St.7
taxa
EC
15m
30m 40m 15m 30m 15m 30m 40m 30'm 15m
30m 18m 30m 15m 30m
Polyplacophora
Callistochiton pachylasmae (Monterosato, 1878)
C
1
Callochiton septemvalvis (Montagu, 1803)
HS
1
1
1
Lepidochiton monterosatoi Kaas & Van Belle, 1981
HS
1
1
1
1
Chiton olivaceus Spengler, 1797
HS
1
1
Acanthochitona fascicularis (Linnaeus, 1767)
HS
1
1
1
1
1
Bivalvia
Arca tetragona Poli, 1795
HS
2
2
2
2
10
6
2
4
1
8
2
6
2
6
Barbatia pulchella (Reeve, 1844)
HS
1
Barbatia scabra (Poli, 1795)
C
1
Striarca lactea (Linnaeus, 1758)
HS
1
1
Musculus costulatus (Risso, 1826)
2
3
1
3
3
3
1
1
Lithophaga lithophaga (Linnaeus, 1758)
HS
1
4
2
Modiolus barbatus (Linnaeus, 1758)
HS,HP
1
27
13
9
42
3
12
16
7
4
11
4
Modiolus adriaticus (Lamarck, 1819)
DC,SS
23
19
1
165
49
85
28
29
97
38
6
15
6
3
Chlamys varia (Linnaeus, 1758)
HS,SS
1
3
1
3
Lima lima (Linnaeus, 1758)
HS,C
1
Limatulla subovata (Jeffreys, 1876)
HS,DC,C
4
3
1
3
3
6
Anomia ephippium Linnaeus, 1758
HS
1
1
2
1
Lucinella divaricata (Linnaeus,1758)
SS
17
4
1
2
8
12
Myrtea spinifera (Montagu, 1803)
SS
1
1
2
24
1
Chama (Psilopus) gryphoides Linnaeus, 1758
HS
1
1
1
4
2
Acanthocardia aculeata (Linnaeus, 1758)
SS
1
2
8
4
1
2
20
21
1
4
Acanthocardia tuberculata (Linnaeus, 1758)
SS
2
2
1
2
Dosinia exoleta (Linnaeus, 1758)
SS
1
16
2
4
4
37
Irus irus (Linnaeus, 1758)
C
1
1
1
3
1
4
1
2
3
21
Lentidium mediterraneum (CostaO.G.,1839)
SS
1
7
2
2
5
11
3
3
66
Hiatella arctica (Linnaeus, 1767)
HS,C
17
10
6
78
49
38
31
10
20
38
24
34
59
28
11
Gastropoda
Acmaea virginea (Mueller O.F., 1776)
HS,PA
1
2
Emarginula adriatica CostaO.G., 1829
HS,M
1
Emarginula octaviana Coen, 1939
HS
1
1
2
1
1
1
Emarginula huzardii (Payraudeau, 1826)
HS
2
Anatoma crispata Fleming, 1828
DC
7
3
2
1
13
5
13
1
1
Clanculus corallinus (Gmelin, 1791)
PA
1
1
1
1
Clanculus jussieui (Payraudeau, 1826)
PA
1
Gibbula magus (Linnaeus, 1758)
DC
15
34
2
5
2
18
14
1
15
2
3
3
Gibbula adansonii (Payraudeau, 1826)
SS,HP
1
Jujubinus exasperatus (Pennant, 1777)
C
1
10
1
3
8
6
13
1
4
6
1
2
Homalopoma sanguineum (Linnaeus, 1758)
HP,C
2
5
3
5
2
1
Tricolia pullus pullus (Linnaeus, 1758)
PA,HP
1
6
122
Chryssanthi Antoniadou, Drossos Koutsoubas and Chariton C. Chintiroglou
TABLE 2 (cont.)
Molluscs reported from the hard substrata infralittoral assemblages. The numerical abundance is estimated from the total number of
replicates per each substation (number of individuals per 0.2m2). The ecological status of each species (EC), is given by HS for hard
substrate, C for coralligenous, PA for photophilic algae, HP for Posidonia oceanica meadows, DC for detritic costs, G for caves, SS
for soft sediments, VTC for coastal terrigenous mud and U for unknown demands.
St.1
St.1 St.1
St.2
St.2
St.3
St.3
St.3
St.3
St.4
St.4
St.5
St.6
St.7
St.7
taxa
EC
15m
30m 40m 15m 30m 15m 30m 40m 30'm 15m
30m 18m 30m 15m 30m
Truncatella subcylindrica (Linnaeus, 1767)
SS
1
Benthonella tenalla (Jeffreys, 1856)
VP
3
Bolma rugosa (Linnaeus, 1767)
PA,C
2
Cerithium vulgatum (Bruguiere, 1792)
PA
2
1
1
2
3
8
10
1
Bittium latreillii (Payraudeau, 1826)
PA,C
1131
1880 121
340
400
414
547
90
629
254
1510
2
138
80
26
Pirenella conica (Blainville, 1826)
SS
1
1
1
Alvania aspera (Philippi, 1844)
PA
1
Alvania cimex (Linnaeus, 1758)
PA
8
31
2
2
1
9
23
6
5
11
3
2
5
3
Alvania discors (Allan, 1818)
SS,HP
5
4
Alvania mamillata Risso, 1826
PA
18
88
10
3
7
12
34
16
17
23
3
3
Alvania semistriata (Montagu, 1808)
PA
2
1
2
Manzonia crassa (Kanmacher, 1798)
HP
2
7
1
3
1
2
1
2
Pusillina radiata (Philippi, 1836)
PA
16
56
8
4
17
48
74
7
32
6
14
1
3
1
2
Setia turriculata Monterosato, 1884
PA
7
2
10
3
Setia sp. juveniles
PA
8
3
Skeneopsis planorbis (Fabricus, 1780)
U
1
Rissoina bruguieri (Payraudeau, 1826)
HP
9
38
4
4
2
14
18
7
1
1
1
1
3
Caecum trachea (Montagu, 1803)
DC
38
33
2
4
44
20
27
45
88
5
7
Luria lurida (Linnaeus, 1758)
PA
1
Pseudosimnia carnea (Poiret, 1789)
C,G
1
1
Erato voluta (Montagu, 1803)
DC
1
Euspira macilenta (Philippi, 1884)
SS
2
1
1
Payraudeautia intricata (Donovan, 1804)
HP
2
1
Monophorus perversus (Linnaeus, 1758)
PA,HP
2
5
1
Metaxia metaxae (Delle Chiaje, 1828)
HP
1
3
Cerithiopsis tubercularis (Montagu, 1803)
DC
2
4
1
1
3
1
1
1
1
4
1
Epitonium commune (Lamarck, 1822)
PA
1
Melanella polita (Linnaeus, 1758)
SS,HP
1
1
1
1
1
Hadriana oretea (De Gregorio, 1885)
SS,DC
1
Muricopsis cristata (Poiret, 1883)
PA
3
Ocinebrina aciculata (Lamarck, 1822)
PA
1
Buccinulum corneum (Linnaeus, 1758)
PA,DC
1
Engina leucozona (Philippi, 1843)
PA
1
Fasciolaria lignaria (Linnaeus, 1758)
PA
1
Fusinus pulchellus (Philipi, 1884)
C,G
1
1
Nassarius incrassatus (Stroem, 1768)
PA,SS
1
1
1
3
5
Nassarius limata (Chemnitz, 1795)
PA,SS
1
Stramonita haemastoma (Linnaeus, 1758)
PA
1
1
1
Vexillum tricolor (Gmelin, 1791)
PA
1
3
1
2
1
2
Vexillum littorale (Philippi, 1843)
PA
1
Mitra cornicula (Linnaeus, 1758)
PA,SS,HP
1
Conus mediterraneus Hwass in Bruguiere, 1792
PA
1
Mangelia attenuata (Montagu, 1803)
SS
1
Mangelia vauquelini (Payraudeau, 1826)
HP
2
1
1
1
Clavus maravignai (Bivona, 1838)
SS
1
Haedropleura septangularis (Montagu, 1803)
SS
1
Mitrolumna olivoidea (Cantraine, 1835)
PA
1
1
1
1
1
Raphitoma echinata (Brocchi, 1814)
C
4
22
3
3
5
10
8
1
4
2
Raphitoma concinna (Scacchi, 1836)
PA,C
1
Raphitoma leufroyi (Michaud, 1828)
C
2
2
2
2
1
1
1
Philbertia densa (Monterosato, 1884)
PA
1
Pseudotorinia architae (Costa O.G., 1841)
DC
1
Omalogyra atomus (Philippi, 1841)
SS
1
1
1
1
Chrysallida doliolum (Philippi, 1844)
SS
4
5
1
1
2
Folinella excavata (Philippi, 1836)
SS
2
11
1
1
1
5
12
2
2
2
2
Odostomia conoidea (Brocchi, 1814)
SS,HP
3
1
1
Turbonilla lactea (Linnaeus, 1758)
SS
2
1
1
Cylichnina umbilicata (Montagu, 1803)
VTC
2
1
1
1
1
Haminaea navicula (Da Costa, 1778)
SS
3
9
2
1
4
5
2
Philine catena (Montagu, 1803)
SS,HP,DC
1
Ascobulla fragilis (Jeffreys, 1856)
HP
1
Limapontia capitata (Mueller, 1774)
U
1
Umbraculum umbraculum (Roeding, 1798)
C,DC
1
Pleurobranchus membranaceus (Montagu, 1815)
DC
1
Phyllaplysia lafonti (Fischer P., 1798)
2
Petalifera petallifera (Rang, 1828)
U
1
Trapania maculata Haefelfinger, 1960
1
Hypselodoris webbi (D'Orbignyi, 1839)
PA
1
Discodoris atromaculata Bergh, 1880
PA,C,G
1
Paradoris indecora Bergh, 1881
PA
1
Polycera quadrilineata (Mueller, 1876)
1
Dendrodoris sp.
PA
1
Molluscan fauna from infralittoral hard substrate assemblages in the North Aegean Sea
123
The dominant species in terms of average density was
Trapania maculata, CERVERA & GARCIA-GOMEZ 1988 :
the prosobranch gastropod Bittium latreillii (2520 indi-
166, Figs 1-5.
viduals/m2), followed by the bivalves Modiolus adriati-
CATTANEO-VIETTI et al. 1990 : 45, Fig. 11, Pl.1 Fig. 7.
cus (215 individuals/m2) and Hiatella arctica (175 indi-
viduals/m2), the prosobranch gastropods Caecum trachea
Material : Station 5 (Vourvourou), 1 specimen, 15m,
(120 individuals/m2), Pusillina radiata (110 individuals/
bottom covered with the Rhodophycea Pseudolithophy-
m2) and Alvania mammilata (90 individuals/m2), the
lum expansum, Gelidium pectinatum
bivalve Modiolus barbatus (60 individuals/m2) and
Distribution : Mediterranean : various areas of the
finally the prosobranch gastropods Gibbula magus (45
Western Mediterranean (CATTANEO-VIETTI et al., 1990) ;
individuals/m2) and Alvania cimex (40 individuals/m2).
Eastern Atlantic : European coasts (BROWN & PICTON,
Molluscs were among the dominant taxa, accounting
1976 ; CERVERA & GARCIA-GOMEZ, 1989).
for 60% of the mean density of the macrofauna in the
sampling sites (polychaetes accounted for 20% and crus-
Structural analysis
taceans 15%) and were also the richest group in terms of
Diversity indices showed a variation in different sam-
species composition (ANTONIADOU & CHINTIROGLOU,
pling sites, with species richness (d) values ranging from
unpublished data).
3.79 to 5.73, community diversity (H') values ranging
Three of these species namely : Skeneopsis planorbis,
from 1.28 to 3.62, and evenness (J') values from 0.24 to
Limapontia capitata and Trapania maculata are reported
0.79 (Fig. 2). The diversity values were quite low as a
for the first time as elements of the molluscan fauna in the
consequence of the great density values of the species Bit-
Eastern Mediterranean or the Aegean Sea. Five other spe-
tium latreillii recorded in most of the sampling stations.
cies, namely : Callistochiton pachylasmae, Raphitoma
Furthermore, the high density of very few species (e.g.
leufroyi, Phyllaplysia lafonti, Petalifera petalifera and
Modiolus adriaticus, Hiatella arctica, Caecum trachea,
Polycera quadrilineata, are reported for the first time in
Pusillina radiata, Alvania cimex, Modiolus barbatus,
the North Aegean Sea. For the species that are new
Gibbula magus, Alvania mammilata) strongly influenced
records for the Eastern Mediterranean or the Aegean Sea
diversity indices values and in particular Shannon-
some taxonomic, ecological and zoogeographical infor-
Weaver's diversity and Pielou's evenness. However, the
mation is given below.
above calculations after the elimination of the species Bit-
New Records for the Eastern Mediterranean or the
tium latreillii showed high values (Fig.2 red points-dash
Aegean Sea
symbols), with d' ranging from 4.2 to 7.49, H' from 2.44
to 4.34 and J' from 0.5 to 0.86.
GASTROPODA
PROSOBRANCHIA
50
N'
2500
Family : Skeneopsidae
45
N
40
S'
2000
Skeneopsis planorbis (Fabricius O., 1780)
35
S
30
1500
Skeneopsis planorbis, F
25
RETTER & GRAHAM 1962 : 550,
20
1000
Fig. 290.
15
10
500
Material : Station 3 (Porto-Koufo), 1 specimen, 30m,
5
0
0
bottom covered with the Rhodophycea Womersleyella
St.1 St.1 St.1 St.2 St.2 St.3 St.3 St.3 St.3 St.4 St.4 St.5 St.6 St.7 St.7
setacea
15m 30m 40m 15m 30m 15m 30m 30'm 40m 15m 30m 18m 30m 15m 30m
Distribution : Mediterranean : various areas of the
Western and Central Mediterranean (SABELLI et al.,
8
d'
1990) ; Eastern Atlantic : Boreal region (FRETTER & GRA-
7
d
HAM 1962).
6
J'
5
J
OPISTHOBRANCHIA
4
H'
Family : Stiligeridae
3
H
2
Limapontia capitata (O.F. Mueller, 1773)
1
Limapontia nigra, P
0
RUVOT-FOL 1954 : 205, Fig. 79a-e.
St.1
St.1
St.1
St.2
St.2
St.3
St.3
St.3
St.3
St.4
St.4
St.5
St.6
St.7
St.7
Limapontia capitata, S
15m 30m 40m 15m 30m 15m 30m 30'm 40m 15m 30m 18m 30m 15m 30m
CMECKEL & PORTMAN 1982 :
311, Abb. 3.1.
Fig. 2. Biocoenotic parameters (up) and diversity indices
Figure 2. Biocoenotic parameters (up) and diversity indices (down) per substation of
(down) per substation of spatially-dispersed stations, where d is
Material : Station 5 (Vourvourou), 1 specimen, 15m,
spatially dispersed stations, where d is Margalef's richness, H is Shannon-Weaver
index, J Pielou's evenness, S number of species/0.2m2 and N number of
Margalef's richness, H is Shannon-Weaver index, J Pielou's
bottom covered with the Rhodophycea Pseudolithophy-
individuals/0.2m2. The dash (') indicates the above calculations after the elimination
evenness, S number of species/0.2m2 and N number of individu-
lum expansum, Gelidium pectinatum
of the species Bittium latreillii.
als/0.2m2. The dash (`) indicates the above calculations after the
Distribution : Mediterranean : various areas of the
elimination of the species Bittium latreillii.
Western and Central Mediterranean (PRUVOT-FOL, 1954 ;
S
Both multivariate analyses of the sampling sites, based
MECKEL & PORTMAN, 1982) and the coasts off Turkey
(S
on presence/absence data, indicate the separation of the
WENNEN, 1961) ; Eastern Atlantic : European coast
south to Marocco (S
samples in four main groups (Fig. 3). At about 40% simi-
CMECKEL & PORTMAN, 1982).
larity level, the samples from station 3 (c-40m) and the
Family : Goniodorididae
samples from station 5 form the first two single site
Trapania maculata Haefelfinger, 1960
groups. The third group includes the samples from sta-
124
Chryssanthi Antoniadou, Drossos Koutsoubas and Chariton C. Chintiroglou
tions 6 and 7 (a-15m & b-30m), while the fourth group
other areas of the Western and Central Mediterranean
matches the leftover stations at a 65% similarity level.
where quantitative sampling has been performed in hard
The stress value for the two-dimensional MDS configura-
substrate infralittoral assemblages [e.g. Banyuls Sur Mer
tion is 0.13, so a useful picture is gained. However, a
(72 species) : MARINOPOULOS, 1988 ; Corsica (109
cross check of any conclusion by the superimposition of a
species) : POULICEK, 1985 ; Malta (44 species) : RICH-
cluster is suggested (CLARKE & WARWICK, 1994). The
ARDS, 1983]. The higher species richness (total number of
performance of a one-way ANOSIM test gave global R :
species) found in the Aegean and Corsica, indicates that
0.955 at a significance level of p<0.1%, indicating an ele-
the survival ability of these assemblage is extremely high.
vated degree of discrimination between the groups, con-
According to WALKER (1992), who expressed the hypoth-
firming both Cluster and MDS. The discrimination of sta-
esis of `over-species', the function of an ecosystem is lit-
tion 7 should probably be attributed to its slightly
tle affected by the loss of species when there are always
different abiotic characteristics (low salinity values). Its
some representatives of all the basic functional groups in
relatively moderate inclination places this station (St.7)
an assemblage (e.g. GASTON & SPICER, 1998). Secondly,
near station 6, while the sharpest slope of stations 1, 2, 3
the same also applies to density values, where 1200 indi-
and 4 clusters them together. The substrate at St.5 is
viduals/m2 had been reported from the photophilic algae
unique, formed by the coral Cladocora caespitosa. Fur-
assemblages off the coasts of Corsica (POULICEK, 1985).
thermore a significant lowering in water clarity values
To a certain degree species with the maximum density in
discriminates this station from all others. At both stations
both aforementioned study areas i.e. North Aegean and
6 and 7 the sciaphilic algal assemblage is characterized by
Corsica, were either the same or congeneric (Alvania
the occurrence of the Rhodophyceae Gelidium pectina-
mammilata, Pusillina radiata, Bittium latreillii, Hiatella
tum and Cutleria multifida, while at all the other stations
arctica North Aegean Sea ; Alvania cimex, Pusillina
the dominant algae were the Rhodophyceae Womers-
lineolata, Bittium reticulatum, Hiatella arctica Cor-
leyella setacea and the Phaeophyceae Padina pavonica
sica). Thirdly a strong difference exists concerning the
and Codium bursa. Furthermore at the third substation set
density of the species Bittium latreillii. This species was
at the depth of 40m, the dominant algae were the encrust-
reported as one of the most abundant species from 20
ing Rhodophyceae Lithothamnion sp., Lithophyllum sp.
meters downwards (BELLAN-SANTINI 1969 ; MARINOPOU-
and Peyssonnelia sp.
LOS 1988), but as far as the western Mediterranean is con-
cerned, it's normalized abundance (number of individuals
per 5 replicates of 400cm2) never exceeds 90, while at our
Bra
y
7a 7b
stations it reached 1880. This is the case for the two upper
-Curtis
20
6b
substations (15 and 30 meters depth), while at the third
40
Similarit
3c
substation (40 meters) and at stations 5, 6 and 7 the
60
2a
3a
1c
4b
5a
numerical abundance ranged from 2 to 138 individuals.
1b
80
3b'
3b
y
1a 2b
The high values of Bittium latreillii abundance are proba-
100 5a 3c 6b 7a 7b 4a 2a 3a 1a 3b 1b 3b' 4b 1c 2b
4a
bly related to the branching form of the dominant algae,
Figure 3. Spatial results of a cluster (left) and multidimensional scaling (right) based
which serves as an excellent ecological niche for this
on Bray-Curtis similarity index on presence/absence data.
Fig. 3. Spatial results of a cluster (left) and multidimensional scal-
mollusc. This particular shape offers the opportunity for
ing (right) based on Bray-Curtis similarity index on presence/absence
quantities of organic material to be trapped in the algae,
data.
thus offering suitable conditions for the species' trophic
demands (herbivore-deposit feeder according to GAMBI et
DISCUSSION
al., 1992).
The majority of the molluscs collected during this
Generally speaking, Mollusca appear to be one of the
study, including most of the dominant species, were eco-
most intensively studied taxa in marine habitats. How-
logically classified as members of the photophilic algal
ever, as our revision shows, the knowledge concerning
assemblage in various areas of the Mediterranean and the
the abundance and the spatial dispersion of this taxon is
Eastern Atlantic (e.g. Table 2). However, quite few of
very restricted. The study of hard substrate infralittoral
them have been recorded in soft sediments, submarine
assemblages in the North Aegean has revealed the pres-
caves and sea-grass meadows. It seems that this specific
ence of a rich molluscan community in this type of
habitat (rocky infralittoral) may be suitable for soft sub-
marine coastal ecosystem, while eight new records were
strate and detritic species. The branching algae, which
set up for the N. Aegean molluscan fauna. These findings
dominate the higher and middle layers of the infralittoral,
support previous authors' claims (e.g. KOUTSOUBAS et al.,
offer suitable substrate for the settlement of most pho-
1997; ZENETOS, 1997) that the marine biodiversity in
tophilic algal species. In-between the thallus of the algae
Greek waters will be revealed to be even more rich when
and the hard substrate, an amount of soft sediment is
extended studies cover neglected geographical locations
trapped, leading to an increased occurrence of species
or habitats and contribute to the overthrow of the "impov-
demanding soft sediments. Our multivariate results
erished Eastern Mediterranean theory" expressed earlier
revealed that the composition of the flora had a signifi-
in this century (e.g. PÉRÈS, 1967).
cant effect on the faunistic discrimination of the stations.
Comparing our results with the relevant reports from
They also indicate that molluscs are qualitatively distrib-
other investigators, we could focus to some major differ-
uted more evenly in terms of similarity at the middle part
ences between the eastern and the western part of that
(20 to 30 meters) of the lower infralittoral zone. At that
semi-closed sea. Firstly the number of mollusc species
depth a high similarity in terms of the dominant species of
found in this study (111) is higher than that reported from
flora is detectable. This demonstrates that hard substrate
Molluscan fauna from infralittoral hard substrate assemblages in the North Aegean Sea
125
with either photophilic or sciaphilic algae may be a tem-
ClARKE, K.R. & WARWICK, R.M. (1994). Change in marine
porary, preferential site for various reasons, such as food
communities : an approach to statistical analysis and inter-
demands, protection from predators, spawning, settlement
pretation. Natural Environment Research Council, UK.
and early development for individuals of many infralitto-
144 pp.
ral or even circalittoral molluscs belonging to other
CERVERA, J.L. & J.C. GARCIA-GOMEZ (1988). Redescripción de
assemblages. A similar statement has been made by
Trapania maculata Haefelfinger, 1960 (Gastropoda, Nudi-
branchia). Boll. Malacol., 24 : 161-172.
POULICEK (1985) who noticed an increased presence of
COSTELLO, M.J. (1998). To know, research, manage and con-
juveniles of mollusc species belonging to other assem-
serve marine biodiversity. Oceanis., 24 : 25-49.
blages in the photophilic algal communities of the coasts
DAUVIN J.C. (1993). Typologie des ZNIEFF- mer. Liste des par-
of Corsica over the reproduction period.
amètres et des biocénoses des côtes francaises métropoli-
Therefore, we can imply that the complexity of the
taines. Col. Patrimoines Nat., 12 : 1-44.
biotopes included in the hard substrate infralittoral zone,
DELLAMOTTE M., & E. VARDALA-THEODOROU (1994) : Shells
is not only insufficiently studied but also its importance is
from the Greek Seas (In Greek).The Goulandris Natural His-
not well defined. The ecological approach of biodiversity,
tory Museum, Athens. 313 pp.
as G
DIGBY, P.G.N. & Kempton, R.A. (1994). Multivariate analysis of
ASTON & SPICER (1998) points out, is a firm compo-
ecological communities. Chapman and Hall, London.
nent to its total definition. Consequently, the fact that
206 pp.
these assemblages hold a very rich fauna (Mollusca in
FRETTER, V. & GRAHAM, A. (1962). Brittish Prosobranch Mol-
this specific case) of typical hard but also of soft sub-
luscs. Their functional anatomy and ecology. Ray Society,
strate, reveals that they can play a key role for the mainte-
London. 748 pp.
nance of biodiversity of the broader geographical area.
GAMBI, M.C., LORENTI, M., RUSSO, G.F., SCIPPIONE, B. & V.
Lack of knowledge on a quantitative basis makes it dif-
ZUPPO (1992). Depth and Seasonal Distribution of Some
ficult to formulate general testimonials concerning the
Groups of the Vagile Fauna of the Posidonia oceanica Leaf
biogeography, although these would be valuable for
Stratum : Structural and Trophic Analyses. Pubbl. Stat. Zool.
Napoli, Mar. Ecol., 13 : 17-39.
building a broad picture of the biodiversity of the Medi-
GASTON, K. & SPICER, J.I. (1998). Biodiversity. An introduction.
terranean. These gaps were recently pointed out by STER-
Blackwell Science. 175 pp.
GIOU et al. (1997), verifying that the problem of insuffi-
GIANGRADE, A. (1988). Polychaete zonation and its relation to
cient and piecemeal information applies not only for the
algal distribution down a vertical cliff in the Western Medi-
phylum Mollusca, but also for the majority of the fauna in
terranean (Italy) : structural analysis. J. Exp. Mar. Biol.
the Mediterranean.
Ecol., 120 : 263-276.
GUILLE, A. 1970. Bionomie benthique du plateau continental de
la cote catalane francaise. II Les communautés de la macro-
REFERENCES
faune. Vie Milieu., 21 : 149-280.
HONG J. S.,1983. Impact of the pollution on the benthic commu-
AUGIER, H. (1982). Inventory and classification of marine ben-
nity. Bull. Korean Fish. Soc., 16 : 279 290.
thic biocoenoses of the Mediterranean. Strasburg Council of
KLUIJVER, M.J., 1997. Sublittoral communities of North Sea
Europe, Publication Section. Nat. Environ. 25 :1-57.
hard-substrata. Print Partners Ipskamp, Enschede, S.B.N.O.,
BAKUS, J.G. (1990). Quantitative ecology and marine biology.
Amsterdam, AquaSense, Amsterdam 330p.
G.A.Balkenna, Rotterdam. 157 pp.
KOUTSOUBAS D. (1992). Contribution in the study of the Gastro-
BELLAN-SANTINI D., 1969. Contribution a l'étude des peuple-
pod Molluscs of the continental shelf of the North Aegean
ments infralittoraux sur substrat rocheux. Etude quantitative
Sea. Ph D. Thesis. Biology Department, Aristotle University
et qualitative de la frange superieure. Thèse Univ. Aix-Mar-
of Thessaloniki (in Greek with English summary). 585 pp.
seille. 294 pp.
KOUTSOUBAS, D., KOUKOURAS, A. & VOULTSIADOU-KOUKOURA,
BELLAN-SANTINI D., LACAZE J.C., POIZAT C. (1994). Les
E. (1997). Prosobranch Mollusc Fauna of the Aegean Sea :
biocénoses marines et littorales de Méditerranée, synthèse,
New information, checklist, distribution. Isr. J. Zool., 43 :
menaces et perspectives. Muséum National d'Histoire
19-54.
Naturelle Paris. 246 pp.
KOUTSOUBAS D., TSELEPIDES, A. & A. ELEFTHERIOU (2000a).
BIANCHI, C.N. and MORRI, C. (2000). Marine Biodiversity of the
Deep Sea Molluscan Fauna of the Cretan Sea (Eastern
Mediterranean Sea : Situation, Problems and Prospects for
Mediterranean) : Faunal, Ecological and Zoogeographical
Future Research. Mar. Pollut. Bull., 40(5) : 367-376.
Remarks. Senkenbergiana marit., 30 : 85-98.
BIGGS, H.E.J. & C. WILKINSON (1966). Marine Mollusca from
KOUTSOUBAS D., ARVANITIDIS, C., DOUNAS, C. & L. DRUMMOND
Malta. J. Conch. Lond., 26 : 52-65.
(2000b). Community and dynamics of the molluscan fauna
BROWN, G.H. & B.E. PICTON (1976). Trapania maculata
in a Mediterranean lagoon (Gialova lagoon, SW Greece).
HAEFELFINGER, a doridacean nudibranch new to the British
Belg. J. Zool., 130 (Supplement) : 135-142.
fauna. J. Conch., 29 : 63-65.
LEDOYER, M. (1969). Aperçu sur la faune vagile de quelques
CATTANEO-VIETTI, R., CHEMELLO, R. & R. GIANNUZZI-SAVELLI
biotopes de substrat dur de Méditerranée Orientale com-
(1990). Atlas of Mediterranean Nudibranchs. La Conchiglia,
paraison avec les mêmes biotopes en Méditerranée Occiden-
Roma. 264 pp.
tale. Tethys., 1 : 281-290.
CBDMS (1995). Understanding Marine Biodiversity. A
MARINOPOULOS 1988. Etude des peuplements infralittoraux de
Research Agenda for the Nation. National Academy Press.
substrat rocheux de la région de Marseille et des facteurs
Washington, D.C. 114 pp.
abiotiques (lumière, hydrodynamique) les influençant. Thèse
CLARKE, K.R. & GREEN, R.H. (1988). Statistical design and
doctorat d'Etat, Sciences naturelles. Univ. Aix-Marseille II.
analysis for a `biological effects' study. Mar. Ecol. Prog.
317 pp.
Ser., 46 : 213-226.
PÉRÈS, J.M. (1967). The Mediterranean Benthos. Oceanogr.
ClARKE, K.R. (1993). Non-parametric multivariate analyses of
Mar. Biol., An. Rev., 5 : 449-533.
changes in community structure. Austr. J. Ecol., 18 : 117-
PÉRÈS, J.M. (1982). General features of organismic assemblages
143.
in pelagial and benthal. Structure and dynamics of assem-
126
Chryssanthi Antoniadou, Drossos Koutsoubas and Chariton C. Chintiroglou
blages. Major benthic assemblages. Specific benthic assem-
STIRN, J. (1981). Manual of methods in Aquatic environment
blages. In : KINNE, O. (ed.), Marine Ecology. Vol. V, Part 1.
research. Part 8. Ecological assessment of pollution effects.
John Wiley, Chichester., 9-66, 119-186, 373-581.
(Guidelines for the F.A.O. (GFCM) / UNEP Joint Coordi-
PÉRÈS, J.M. & J. PICARD (1958). Recherches sur les peuplements
nated Project on Pollution in Mediterranean). F.A.O. Fisher-
benthiques de la Méditerranée nord-orientale. Ann. Inst.
ies Technical Paper., 209 : 1-190.
Océanogr., Monaco., 34 : 213-291.
STRACK, H.L. (1988). The distribution of Chitons (Polyplacoph-
PÉRÈS, J.M. & PICARD, J. (1964). Nouveau manuel de la bion-
ora) in Greece. Apex., 3 : 67-80.
omie benthique de la mer Méditerranée. Rec. Trav. Stat. Mar.
SWENNEN, C. (1961). On a collection of Opisthobranchia from
Endoume., 31 (47) : 1-137.
Turkey. Zool. Meded., 38 : 41-75.
POULICEK, M. (1985). Les mollusques des biocenoses a algues
WALKER, B.H. (1992). Biodiversity and ecological redundancy.
photophiles en Mediterranee : II. - Analyse du peuplement.
Cons Biol., 6 : 18-23.
Cah. Biol. Mar., 26 : 127-136.
WEINBERG, S. (1978). The minimal area problem in invertebrate
PRUVOT-FOL, A. (1954). Faune de France. 58. Mollusques
communities of Mediterranean rocky substrate. Mar. Biol.,
Opisthobranches. Paul Lechevalier, Paris, 460 pp
49 : 33-40.
RICHARDS, G.W. (1983). Molluscan Zonation on Rocky Shores
ZENETOS, A., PAPATHANASSIOU, E. & AARTSEN, J.J. van (1991).
in Malta. J. Conch. Lond., 31 : 207-224.
Analysis of benthic communities in the Cyclades Plateau
ROS, J.D. & J.M. GILLI (1985). Opisthobranches des Grottes
(Aegean Sea) using ecological and paleoecological data sets.
sous-marines de l' île de Majorque (Baleares). Rapp. Comm.
Pubbl. Stat. Zool. Napoli, Mar. Ecol., 12 : 123-137.
Int. Mer. Médit., 29 : 141-145.
ZENETOS, A. (1993). Infralittoral Macrobenthos of the Patras
SABELLI, B., GIANNUZZI-SAVELLI, R & BEDULLI, D. (1990). Cat-
Gulf and Ionian Sea. Bivalvia, Mollusca. Malac. Rev., 26 :
alogo annotato dei Molluschi Marini del Mediterranea.
51-62.
Vol.1 Libreria Naturalistica Bolognese, Bologna, 348 pp.
ZENETOS, A. (1997). Diversity of Marine Bivalvia in Greek
SCHMEKEL, L. & A. PORTMANN (1982). Opisthobranchia des
waters : Effects of Geography and Environment. J. Mar.
Mittelmeeres. Nudibranchia and Saccoglossa. Springer Ver-
Biol. Ass., U.K., 77 : 463-472.
lag, Berlin, 410 pp.
ZENETOS, A., CHRISTIANIDIS, S., PANCUCCI, M.A., SIMBOURA, N.
STERGIOU, K.I., CHRISTOU E.D., GEORGOPOULOS, D., ZENETOS,
& C. TZIAVOS (1997). Oceanological Study of an open
A. & SOUVERMEZOGLOU, C. (1997). The Hellenic Seas :
coastal area in the Ionian Sea with emphasis on its benthic
physics, chemistry, biology and fisheries. Ocean. Mar. Biol.
fauna and some zoogeographical remarks. Ocean. Acta, 20 :
Ann. Rev., 35 : 415-538.
437-451.
Belg. J. Zool., 135 (2) : 127-133
July 2005
Epiedaphic Coleoptera in the Dadia forest reserve
(Thrace, Greece) : the effect of human activities on com-
munity organization patterns
Maria D. Argyropoulou1, George Karris1, Efi M. Papatheodorou2 and George P. Stamou2
1 Dept. of Zoology, School of Biology, UPB 134, Aristotle University, GR-54124 Thessaloniki, Greece
2 Dept. of Ecology, School of Biology, UPB 119, Aristotle University, GR-54124 Thessaloniki, Greece
Corresponding author : M. D. Argyropoulou, e-mail : margyrop@bio.auth.gr
ABSTRACT. In this work we described and compared the community organization patterns of Coleoptera in vari-
ous sites of the Dadia forest reserve, including different types of vegetation and management practices (grazing,
cultivation, afforestation). Sampling was carried out every two months for a year, by means of pitfall traps. For
studying diversity and community structure, we used Renyi's parametric index of diversity and fitted the geometric
series model on rank/abundance data. In order to study the changes of species composition, we used the Indicator
Value method (IndVal), after a tree clustering of our sampling sites.
According to our results, although the three management practices increased the diversity of epiedaphic Coleoptera,
their effects on the community organization patterns were different. Grazing did not affect the species composition of
the communities but altered the community structure. The communities in the ungrazed forests were over-dominated
by one species, while those of the grazed sites were hierarchically structured. On the other hand, the main effect of cul-
tivation on the coleopteran communities was a profound change in species composition. The cultivated site was domi-
nated by characteristic species that were almost absent from all other sites. Afforestation caused intermediate changes
in both community structure and composition.
Finally, although certain species of Coleoptera seemed to be good indices for assessing human impacts on natural envi-
ronment, the study of changes in the community organization patterns is even more appropriate.
KEY WORDS : Diversity, community structure, indicator species, grazing, cultivation, afforestation.
INTRODUCTION
reserve, which differ regarding vegetation and human
activities. The Dadia forest is near the Greek-Turkish bor-
Different land use and management practices affect the
der. It is famous for the endangered and/or vulnerable
variability of ecological factors in space and consequently
populations of birds of prey, and it is under protection
the habitat heterogeneity, which is reflected in the com-
since 1980. Our work was part of a wider monitoring
munities of soil arthropods. Due to high turnover and
project of the protected area, which was funded by WWF-
growth rates of most species, these animals serve as
Hellas, and where several research teams worked on dif-
probes that quickly respond to environmental change
ferent animal groups as well as on vegetation. Our interest
(MATTONI et al., 2000). Thus, the use of soil arthropods in
was focused on identifying the importance of three man-
monitoring for purposes of conservation biology,
agement practices, namely grazing, cultivation and affor-
although limited until the beginning of the last decade, is
estation, in shaping the coleopteran species assemblages.
continuously increasing.
More specifically, we compared the effects of these prac-
tices on diversity, community structure and species com-
Many bioindication studies aiming at habitat evalua-
position of surface dwelling beetles.
tion and monitoring have been based on the coleopteran
fauna, focusing either on certain species or families or
even on the whole order (e.g. BOHAC, 1999 ; HUMPHREY
MATERIAL AND METHODS
et al., 1999 ; MOLINA et al., 1999 ; MAGURA et al., 2000a ;
BAUR et al., 2002). In many of these studies, the research-
Study sites and sampling
ers have tried to assess the effect of human practices, such
Ten sites were sampled, including different types of
as grazing (GARDNER et al., 1997 ; PETIT & USHER, 1998),
vegetation and management practices (Table 1). Some of
farming activities (KROOSS & SCHAEFER, 1998 ; KROMP,
these sites were adjacent to each other, forming distinct
1999 ; VARCHOLA & DUNN, 1999) and forestry practices
gradients according to the management practice to which
(INGS & HARTLEY, 1999 ; MAGURA et al., 2001, 2002) on
they are subject. For example, the natural pine forest, the
the coleopteran communities.
grazed pine forest and the overgrazed meadow constituted
In the work we present here, we have tried to describe
a gradient of grazing pressure (PINEgPINEMEAD).
and compare the community organization patterns of
The same holds for the ungrazed and the adjacent grazed
epiedaphic Coleoptera at various sites of the Dadia forest
area of the mixed oak forest (MOAKgMOAK).
128
Maria D. Argyropoulou, George Karris, Efi Papatheodorou and George P. Stamou
Another grazed site was a typical mediterranean maquis
PHEDGCULT). And lastly, we compared a pine
(MAQ) with a variety of shrub species, which is used as
afforestation (AFF) with the natural pine forest, in order
pastureland. Another case was a natural oak-pine forest,
to explore the effect of this management practice on the
an adjacent cultivated field, and a natural hedgerow that is
coleopteran community.
connected to the forest and borders the field (OAK-
TABLE 1
Characteristics of the ten sampling sites within the Dadia protected area.
Site
Code
Habitat characteristics
Management practice
1 Pine forest
PINE
Ungrazed dense mature forest of Pinus brutia
2 Grazed pine forest
gPINE
Sparse P. brutia trees and grass-covered areas.
grazing
3 Overgrazed meadow
MEAD
Overgrazed grass-covered meadow with microhabitats of bare soil
4 Mixed oak forest
MOAK
Ungrazed mature forest of Quercus sp.and Carpinus orientalis.
5 Grazed mixed oak forest
gMOAK
Sparse trees of Quercus sp., Carpinus orientalis, Fraxinus ornus,
grazing
Cornus mas, Acer sp. and open grass-covered areas
6 Mediterranean shrubland
MAQ
Typical mediterrannean maquis with Phillyrea latifolia, Juniperus
grazing
oxycedrus, Erica arborea, Cistus sp. and grass-covered areas
7 Mixed oak-pine forest
OAKP
Ungrazed mature forest of Pinus brutia and Quercus frainetto
8 Natural hedgerow
HEDG
The species composition includes Ulmus sp., Clematis sp., Rubus
cultivation
spp., Rosa sp. and Prunus spinosa.
9 Cultivated field
CULT
Non-irrigated organic wheat cultivation
10 Afforestation
AFF
P. brutia afforestation.
afforestation
Sampling was carried out by means of unbaited pitfall
(1932). In a geometric series, the abundance of species
traps (diameter 5.4 cm, height 15 cm), every two months
ranked from most to least abundant is :
for one year. The traps contained 10% ethylene glycol as
n = N k (1-k)i-1 [1-(1-k)s]-1
a killing-preserving solution. We used five traps per site
i
where n = number of individuals of the ith species, N=
(5x10=50 traps in total), which remained in the field for
i
total number of individuals, s= total number of species
seven days on each sampling occasion. Samples from the
and k= environmental constant.
whole experimental year were used for data analysis. All
specimens were identified to morphospecies, while for
In order to study the changes of species composition at
further identification of Carabidae, Staphylinidae and
the different sites, we used the IndVal (Indicator Value)
Cerambycidae, expert assistance was offered by the
method of DUFRENE & LEGENDRE (1997). This method
National Museum of Natural History of Bulgaria.
assigns indicator (characteristic) species to a site or a
group of sites, on the basis of species relative abundance
Data Analysis
and relative frequency of occurrence in the various
groups of samples. The approach requires a former classi-
For assessing the diversity of coleopteran communities
fication of sample units. We obtained a typology based on
in the different sites, we used the method of diversity
a tree clustering of our sampling sites (linkage rule :
ordering proposed by RENYI (1961). Renyi's parametric
unweighted pair-group centroid, distance measure : 1-
index of order a shows varying sensitivity to the rare and
Pearson r). The statistical significance of the species indi-
abundant species of a community, as the scale parameter
cator values was also evaluated by the IndVal program by
a changes (RICOTTA, 2000). It provides a profile of the
means of a randomization procedure.
most widely used diversity indices. For a=0, the index
equals log species number, for a=1, it equals Shannon's
index, for a=2, it equals Simpson's index. For a tending
RESULTS
to infinite, the index is most sensitive to the abundant spe-
cies. Thus, when two diversity profiles differ in the range
Diversity
of low a values, this is due to the number of species. In
In Fig. 1a, we present the diversity profiles of the sites
the range of high a values, differences are due to the pres-
that differ due to grazing. In the case of the natural mixed
ence of abundant species. When two diversity profiles
oak forest and the grazed one, we can see that the diver-
intersect, the two communities may be ordered differently
sity of the coleopteran community is much higher in the
by different diversity indices. For calculations we used
grazed forest than in the natural one. The difference of the
DivOrd (TOTHMERESZ, 1995).
two curves falls mainly in the range of high values of the
For further insight into the community structure, we
scale parameter. This means that the difference is mostly
estimated the environmental constant from the rank/abun-
due to the presence of abundant species in the grazed site,
dance plots, as proposed by MAY (1975) and MOTOMURA
rather than to the higher number of species. The same
Human impact on Community Organization Patterns of Coleoptera
129
holds in the case of the natural and the grazed pine forest.
number of species was higher. As regards the mediterra-
In comparison with these two sites, the overgrazed
nean pasture land, it exhibited the highest diversity of all
meadow exhibited intermediate diversity, although the
sites.
3.5
3.5
PINE
PINE
gPINE
C U L T
M E A D
H E D G
3.0
g M O A K
3.0
O A K P
M O A K
AFF
M A Q
2.5
2.5
2.0
2.0
1.5
1.5
5HQ\L
VGLYHUVLW\LQGH[
5HQ\L
VGLYHUVLW\LQGH[
1.0
1.0
0.5
0.5
-0.5
0.5
1.5
2.5
3.5
4.5
5.5
-0.5
0.5
1.5
2.5
3.5
4.5
5.5
a
VFDOHSDUDPHWHU.
b
VFDOHSDUDPHWHU.
Fig. 1. Diversity profiles of coleopteran communities (a) in PINE, gPINE, MEAD, MOAK, gMOAK, MAQ and (b) in OAKP,
HEDG, CULT, AFF, PINE. PINE was also included in (b) for comparative purposes. For site codes see Table 1.
In Fig. 1b, we present the diversity profiles of the sites
est, we can see that in the natural forest one species over-
that differ due to the two other management practices, i.e.
dominated the community and almost all the others were
cultivation and afforestation. The diversity profiles of the
represented by very low numbers. This is the reason for
coleopteran communities in the natural forest, the hedge-
the high value of the environmental constant. At the
row and the cultivated field intersect, which means that
grazed site, dominance was shared by several species, and
the communities may be ordered differently by different
the value of the constant was very low. The same changes
diversity indices. What is obvious here is that the natural
in community structure may also be observed in the case
forest had the lowest diversity, and more specifically the
of the natural and the grazed pine forest, i.e. an over-dom-
lowest number of species, since the difference of the
ination of a single species at the natural site and a more
curves falls in the range of low values of the scale param-
hierarchical community structure at the grazed site. The
eter. Moreover, the differences in diversity due to cultiva-
hierarchical community structure was most obvious in the
tion were not as pronounced as the ones that were caused
mediterranean pastureland, which exhibited the lower
by grazing.
value of the environmental constant.
As regards afforestation, the third management prac-
These changes of community structure cannot be
tice, its effect on diversity was intermediate, compared to
observed in the case of the sites that differ due to cultiva-
the effects of grazing and cultivation. The afforested site
tion. The values of the environmental constant were
was more diverse than the natural pine forest, both
almost the same for the three sites, which means that this
regarding the species number and the equitability, since
management practice does not induce pronounced
the two diversity curves differ equally through the whole
changes in community structure as is the case with graz-
range of the scale parameter.
ing.
Community structure
As regards afforestation, it is obvious from the rank/
abundance plots and the values of the environmental con-
In Fig. 2, we present the rank/abundance plots for all
stant, that the changes in community structure were once
sites together with the values of the environmental con-
again intermediate, compared with those induced by graz-
stant (k). Comparing the natural with the grazed oak for-
ing and cultivation.
130
Maria D. Argyropoulou, George Karris, Efi Papatheodorou and George P. Stamou
estation altered the species composition of the commu-
nity, while this is not the case with grazing.
10
O.integer
C.montiv
L.c.weirath
Tenebr.1
9
C.cinctus
T.quadr*
C.g.morio
Oxytelus*
Dorc.ped.
Anthic*
8
C.f.latus*
Chrysom
Scar.2
Silph
C.c.ceris
7
P.mus
Curcul.1 *
Dorc.sp
Colpt.4
Scar.3
6
Scar.4
Scar.1 *
P.cupr
Colpt.2
5
4
Curcul.2
Colpt.1
M.melol
N.bigut
Colpt.3
3
Tenebr.2
Elater
2
Curcul.3
1
Staphyl*
Ocalea
0
CULT
AFF
gPINE gMOAK MEAD
MAQ
OAKP
HEDG
MOAK
PINE
Fig. 3. Dendrogram presenting the indicator species of each
sampling site, identified by IndVal. Significant indicator species
are noted by * (p<0.05). Names in bold indicate species that
dominate the corresponding site. For site codes see Table 1. Spe-
cies names are listed in Table 2.
TABLE 2
Species indicator values for the corresponding clustering level,
i.e. the site or group of sites where the species exhibits maxi-
mum indicator value. Statistical significance is also indicated
(p<0.05)
Species list
IndVal
sites
Carabidae
Trechus (Trechus) quadristriatus
58.45
CULT
*
(Schrank, 1781)
Fig. 2. The geometric series model fitted on rank/abundance data
from all sampling sites. Species are ordered from the most to the least
Calathus (Calathus) fuscipes
44.47
AFF
*
abundant. The environmental constant (k) and the goodness of fit (R)
latus Audinet-Serville, 1821
are also noted. For site codes see Table 1.
Carabus (Procrustes) coriaceus
31.13
AFF
ns
cerisyi Dejean, 1826
Species composition
Laemostenus (Pristonychus) cim-
22.03
all sites
ns
merius weiratheri G. Mller, 1931
In order to explore changes in species composition due
Notiophilus (Latviaphilus) bigut-
18.62
MEAD
ns
to the three management practices, we used the IndVal
tatus (Fabricius, 1779)
method after a tree clustering of our sites. Species
recorded only on one sampling occasion were not taken
Calathus (Neocalathus) cinctus
18.52
all unculti-
ns
into account in this analysis and thus the whole number of
(Motschulsky, 1850)
vated sites
species recorded in this study was reduced to 34. The
Carabus (Pachystus) graecus
16.67
all unculti-
ns
results are presented in Fig. 3 and Table 2. In the dendro-
morio Mannerheim, 1830
vated sites
gram of Fig. 3, we can see that the natural sites are
grouped together ; the same happens with most of the
Carabus (Archicarabus) montiva-
37.04
all unculti-
ns
gus Palliardi, 1825
vated sites
grazed sites, while the cultivated field and secondly the
pine afforestation are separated from all the others. These
Staphylinidae
two sites have the greatest number of characteristic spe-
Oxytelus sp.
47.85
CULT
*
cies. We must note here that the characteristic species of
the cultivated field were also the dominant ones at this
Staphylinidae unid.
29.22
MOAK
*
site. As regards the pine afforestation, three out of the
Ocypus integer Abeille, 1900
28.81
all sites
ns
eight characteristic species were among the five most
dominant species of this site, while the other five species
Pseudocypus (s. str.) mus Brulle,
26.49
AFF
ns
simply contributed to habitat specificity. The dominant
1832
species of most other sites were eurytopic species. These
Ocalea sp.
23.22
MOAK
ns
results imply that cultivation and, to a lesser degree, affor-
Human impact on Community Organization Patterns of Coleoptera
131
TABLE 2 (cont.)
DISCUSSION
Species indicator values for the corresponding clustering level,
Grazing
i.e. the site or group of sites where the species exhibits maxi-
mum indicator value. Statistical significance is also indicated
Our results showed that the diversity of the coleopteran
(p<0.05)
community was much higher in the grazed than in the
undisturbed part of both the deciduous and the pine forest,
Species list
IndVal
sites
a result also reported by INGS & HARTLEY (1999) for cara-
Pseudocypus (s. str.) cupreus
13.01
AFF
ns
bid assemblages of forest environments. This increase of
Rossi, 1790
diversity may be attributed to several factors that affect
the coleopteran communities, such as the light (FAHY &
Scarabaeidae
GORMALLY, 1998) that penetrates the overstorey, the
species unid.1
33.57
MAQ
*
development of ground vegetation (INGS & HARTLEY,
1999), and most importantly the high degree of structural
species unid.2
32.54
AFF
ns
heterogeneity induced by grazing (GARDNER et al., 1997)
species unid.3
15.96
AFF
ns
and the consequent changes of microclimatic conditions
(RODRIGUEZ et al., 1998). Moreover, the grazed pine for-
species unid.4
14.86
AFF
ns
est is actually a forest edge, while the overgrazed meadow
Melolontha melolontha (Lin-
12.29
gMOAK
ns
is the other extreme of the forest-grass spectrum.
naeus, 1758)
Increased diversity of the coleopteran fauna in forest
edges has been well established (MAGURA et al., 2000b ;
Curculionidae
HORVATH et al., 2002). In the overgrazed grass covered
species unid.1
33.33
gPINE,
*
meadow, diversity was higher than that recorded at the
gMOAK,
undisturbed site but lower than that recorded at the mod-
MEAD
erately grazed site. Indeed, too much grazing reduces
species unid.2
21.76
gMOAK
ns
structural variation of vegetation and thus diversity of
coleoptera (GARDNER et al., 1997), and as CONNELL
species unid.3
11.49
HEDG
ns
(1978) pointed out, medium disturbance may indeed
Cerambycidae
enhance diversity.
Diversity increase due to grazing was accompanied by
Dorcadion sp.
23.24
AFF
ns
changes in the hierarchical structure of the community. In
Dorcadion cf. pedestre (Poda,
12.96
all unculti-
ns
the natural forest, one species over-dominated the com-
1761)
vated sites
munity and almost all the others were represented by very
low numbers, while in the grazed site dominance was
Anthicidae
shared by several species. As far as we know, up to now,
species unid.
39.1
CULT
*
only MOLINA et al. (1999) have reported the dominance of
a single species within the forest catches as a reason
Silphidae
accounting for the low diversity of the forest ground-
species unid.
10.56
CULT
ns
dwelling community. In line with their work, we believe
that the mosaic structure of vegetation at the grazed sites
Elateridae
offers a variety of microhabitats where soil arthropods
species unid.
16.85
HEDG
ns
may establish and increase their local population size.
Indeed, in the mediterranean pastureland, which is the
Chrysomelidae
most heterogeneous of all our sampling sites due to the
species unid.
19.4
CULT
ns
variety of shrub species, we recorded the most diverse
and hierarchically-structured community.
Tenebrionidae
Regarding the species composition of the coleopteran
species unid.1
25.93
all unculti-
ns
community, according to our results, it does not seem to
vated sites
alter due to grazing. ELEK et al. (2001) state that the
species unid.2
16.67
forested
ns
movement of forest species is prevented in more grassy
sites and
sites, while RODRIGUEZ et al. (1998) claim that the habitat
HEDG
breadth of species correlates with the degree of distur-
bance at a site. However, the IndVal analysis did not
Families unidentified
reveal any characteristic forest species that disappeared in
species unid.1
20.86
MEAD
ns
the grazed sites or vice versa, since the dominant species
of both natural and grazed forests were eurytopic.
species unid.2
9.09
MAQ
ns
species unid.3
15.9
MEAD
ns
Cultivation
species unid.4
13.56
gPINE,
ns
Apart from grazing, cultivation also had a positive
gMOAK,
result on the diversity of the coleopteran community.
MEAD
However, the only component of diversity that increased
from the natural forest to the adjacent cultivated field was
the number of species, while no pronounced changes in
132
Maria D. Argyropoulou, George Karris, Efi Papatheodorou and George P. Stamou
the community structure were recorded, as was the case
reported also by KOIVULA et al. (2002) and MAGURA et al.
with grazing. BOHAC (1999) and KROMP (1999) have also
(2002).
reported high species numbers of Coleopterans in arable
habitats. We should also note that in the wheat cultivation
CONCLUSIONS
that we studied there was no insecticide application,
which is known to have detrimental effects for several
families of beetles (W
To sum up, although the three management practices
ILSON et al., 1999). Moreover, the
existence of the natural hedgerow at the edge of the field
increased the diversity of epiedaphic Coleoptera, their
is very important for maintaining biodiversity, since it
effects on the community organization patterns differed.
acts as a refuge for overwintering field species (K
Grazing did not affect the species composition of commu-
ROMP,
1999), or relict woodland species (A
nities but altered the community structure. The communi-
STERAKI et al., 1995),
from where beetles may reinvade the adjacent field in
ties of the ungrazed forests were over-dominated by one
response to changing field conditions (V
species, while those of the grazed sites were hierarchi-
ARCHOLA &
D
cally structured. On the other hand, the main effect of cul-
UNN, 1999).
tivation on the coleopteran communities was the pro-
The most important effect of cultivation recorded in
found change in species composition. The cultivated site
this study was the changes in species composition. Such
was dominated by characteristic species that were almost
changes are also reported by KROOSS & SCHAEFER (1998).
absent from all other sites. Afforestation caused interme-
SIEREN & FISCHER (2002) state that arable land is a suita-
diate changes in both community structure and composi-
ble habitat for eurytopic species without special ecologi-
tion.
cal preferences. However, the field of our study was dom-
The use of a community measure to track habitat
inated by stenotopic indicator species, the number of
changes is an important alternative to assessments
which was the highest one recorded at all sampling sites.
focused on single species (MATTONI et al., 2000). Our
This is again a completely different effect from the one
results show that although certain species of Coleoptera
induced by the previous human intervention, i.e. grazing.
had significant indicator value and seemed to be good
indices for assessing human impacts on natural environ-
Afforestation
ments, the study of changes in the community organiza-
As regards the effect of afforestation on the community
tion patterns is even more appropriate.
patterns of Coleoptera, this was intermediate compared
with the effects of grazing and cultivation. The afforested
ACKNOWLEDGEMENTS
site was more diverse than the natural pine forest, regard-
ing both the species number and the equitability. Thus,
We are indebted to Dr. Borislav Gueorguiev and Mr. Ognyan
high diversity was accompanied by changes in commu-
Mikov from the National Museum of Natural History (Sofia,
nity structure, although the latter were not as striking as
Bulgaria) for identifying our Coleoptera specimens. We also
the ones recorded at grazed sites. Furthermore, apart from
wish to thank WWF-Hellas for financing this work.
the cultivated field, which had a completely different spe-
cies composition from all other sampling sites, the cole-
REFERENCES
opteran community of the afforested site was clearly dis-
cernible as well.
ASTERAKI, E.J., C.B. HANKS & R.O. CLEMENTS (1995). The
Our results are quite different from those of ELEK et al.
influence of different types of grassland field margin on
(2001), who found a more abundant and species rich cara-
carabid beetle (Coleoptera, Carabidae) communities. Agr.
bid assemblage in a native forest than in a conifer planta-
Ecosyst. Environ., 54 : 195-202.
tion. However, the fact that the native forest that they
BAUR, B., S. ZSCHOKKE, A. CORAY, M. SCHLAPFER & A.
studied was a deciduous one, might be a possible explana-
ERHARDT (2002). Habitat characteristics of the endangered
flightless beetle Dorcadion fuliginator (Coleoptera : Ceram-
tion. Besides, there is both a geographical and a habitat
bycidae) : implications for conservation. Biol. Conserv.,
associated variation in the effects of afforestation on cole-
105 : 133 142.
opteran communities (BUTTERFIELD et al., 1995). For
BOHAC, J. (1999). Staphylinid beetles as bioindicators. Agr. Eco-
example, FAHY & GORMALLY (1998) imply that the low
syst. Environ., 74 : 357-372.
carabid diversity that they found in a conifer plantation is
BUTTERFIELD, J., M.L. LUFF, M. BAINES & M.D. EYRE (1995).
related to low plant species richness and consequently to
Carabid beetle communities as indicators of coservation
low food availability, but they state that the inclusion of
potential in upland forests. Forest Ecol. Manag., 79 : 63-77.
open areas within plantations will increase available
CONNELL, J.H. (1978). Diversity in tropical rainforests and coral
microhabitats and thus coleopteran diversity. Indeed, in
reefs. Science, 199 : 1302-1310.
the pine plantation of our study there is no dense oversto-
DUFRENE, M. & P. LEGENDRE (1997). Species assemblages and
rey, because the trees are about 7 years old and of low
indicator species : the need for a flexible asymmetrical
height, and thus there are still grass covered areas
approach. Ecol. Monogr., 67 : 345-366.
between them. Based on findings of I
ELEK, Z., T. MAGURA & B. TOTHMERESZ (2001). Impacts of non-
NGS & HARTLEY
(1999), who believe that in mature forests or even planta-
native Norway spruce plantation on abundance and species
richness of ground beetles (Coleoptera : Carabidae). Web
tions, it is the shady and humid microclimate that species
Ecol., 2 : 32-37.
are responding to, we speculate that the alteration of
FAHY, O. & M. GORMALLY (1998). A comparison of plant and
shade and soil moisture due to the eventual growth of
carabid beetle communities in an Irish oak woodland with a
trees will lead to an homogeneous microclimate and to an
nearby conifer plantation and clearfelled site. Forest Ecol.
adverse effect on coleopteran diversity. Such an effect is
Manag., 110 : 263-273.
Human impact on Community Organization Patterns of Coleoptera
133
GARDNER, S.M., S.E. HARTLEY, A. DAVIES & S.C.F. PALMER
MAY, R.M. (1975). Patterns of species abundance and diversity.
(1997). Carabid communities on heather moorlands in north-
In : CODY M.L. & J.M. DIAMOND (eds), Ecology and Evolu-
east Scotland : The consequences of grazing pressure for
tion of Communities. Harvard University Press, Cambridge,
community diversity. Biol. Conserv., 81 : 275-286.
MA : 81-120.
HORVATH, R., T. MAGURA, G. PETER & B. TOTHMERESZ (2002).
MOLINA, S.I., G.R. VALLADARES, S. GARDNER & M.R. CABIDO
Edge effect on weevils and spiders. Web. Ecol., 3 : 43-47.
(1999). The effects of logging and grazing on the insect
HUMPHREY, J.W., C. HAWES, A.J. PEACE, R. FERRIS-KAAN &
community associated with a semi-arid chaco forest in cen-
M.R. JUKES (1999). Relationships between insect diversity
tral Argentina. J. Arid Environ., 42 : 2942.
and habitat characteristics in plantation forests. Forest Ecol.
MOTOMURA, I. (1932). A statistical treatment of associations (in
Manag., 113 :11-21.
Japanise and cited in MAY 1975). Jpn. J. Zool., 44 : 379-383.
INGS, T.C. & S.E. HARTLEY (1999). The effect of habitat struc-
PETIT, S. & M.B. USHER (1998). Biodiversity in agricultural
ture on carabid communities during the regeneration of a
landscapes : The ground beetle communities of woody
native Scottish forest. Forest Ecol. Manag., 119 : 123-136.
uncultivated habitats. Biodivers. Conserv., 7(12) : 1549-
KOIVULA, M., J. KUKKONEN & J. NIEMELA (2002). Boreal cara-
1561
bid-beetle (Coleoptera, Carabidae) assemblages along the
RENYI, A. (1961). On measures of entropy and information. In :
clear-cut originated succession gradient. Biodiversity and
NEYMAN, J. (ed.), Proceedings of the 4th Berkeley Sympo-
Conservation, 11 : 1269-1288.
sium on Mathematical Statistics and Probability, Vol 1. Uni-
KROMP, B. (1999). Carabid beetles in sustainable agriculture : a
versity of California Press : 547-561.
review on pest control efficacy, cultivation impacts and
RICOTTA, C. (2000). From theoretical ecology to statistical phys-
enhancement. Agr. Ecosyst. Environ., 74 : 187228.
ics and back : self-similar landscape metrics as a synthesis of
KROOSS, S. & M. SCHAEFER (1998). The effect of different farm-
ecological diversity and geometrical complexity. Ecol.
ing systems on epigeic arthropods : a five-year study on the
Model., 125 : 245-253.
rove beetle fauna (Coleoptera : Staphylinidae) of winter
RODRIGUEZ, J.P., D.L. PEARSON & R. BARRERA (1998). A Test
wheat. Agr. Ecosyst. Environ., 69 : 121-133.
for the adequacy of bioindicator taxa : are tiger beetles
MAGURA, T., V. KODOBOCZ & ZS BOKOR (2001). Effects of for-
(Coleoptera : Cicindelidae) appropriate indicators for moni-
estry practices on carabids (Coleoptera : Carabidae)-implica-
toring the degradation of tropical forests in Venezuela ? Biol.
tions for nature management. Acta Phytopathologica et
Conserv., 83(1) : 69-76.
Entomologica Hungarica, 36(1-2) : 179-188.
SIEREN, E. & F.P. FISCHER (2002). Evaluation of measures for
MAGURA, T., B. TOTHMERESZ & ZS. BORDAN (2000a). Effects of
enlargement, renaturation and development of a dry grass-
nature management practice on carabid assemblages
land biotope by analysing differences in the carabid fauna
(Coleoptera : Carabidae) in a non-native plantation. Biol.
(Coleoptera). Acta Oecologica, 23 : 112.
Conserv., 93 : 95-102.
TOTHMERESZ, B. (1995). Comparison of different methods for
MAGURA, T., B. TOTHMERESZ & T. MOLNAR (2000b). Edge effect
diversity ordering. J. Veg. Sci., 6 : 283-290.
on carabid assemblages along forest-grass transects. Web
VARCHOLA, J.M. & J.P. DUNN (1999). Changes in ground beetle
Ecol., 2 : 7-13.
(Coleoptera : Carabidae) assemblages in farming systems
MAGURA, T., B. TOTHMERESZ & Z. ELEK (2002). Impacts of non-
bordered by complex or simple roadside vegetation. Agr.
native spruce reforestation on ground beetles. Eur. J. Soil
Ecosyst. Environ., 73 : 41-49.
Biol., 38 : 291-295.
WILSON, J.D., A.J. MORRIS, B.E. ARROYO, S.C. CLARK & R.B.
MATTONI, R., T. LONGCORE & V. NOVOTNY (2000) Arthropod
BRADBURY (1999). A review of the abundance and diversity
Monitoring for Fine-Scale Habitat Analysis : A Case Study
of invertebrate and plant foods of granivorous birds in north-
of the El Segundo Sand Dunes. Environ. Manag., 25(4) :
ern Europe in relation to agricultural change. Agr. Ecosyst.
445452.
Environ., 75 : 13-30.
Belg. J. Zool., 135 (2) : 135-137
July 2005
Microtus guentheri (Danford & Alston) (Rodentia,
Mammalia) : a bioindicator species for estimation of the
influence of polymetal dust emissions
Tsenka Chassovnikarova, Roumiana Metcheva and Krastio Dimitrov
Institute of Zoology, BAS, 1 Tsar Osvoboditel Blvd., Sofia 1000, Bulgaria
Corresponding author : K. Dimitrov, e-mail : biokd@biology.au.dk
ABSTRACT. Chemical pollution of ecosystems resulting from human activity is an ecological factor in the living
world, affecting individuals, populations, communities and ecosystems as a whole. This laboratory investigation
studied the toxic effects of polymetal ferosilicic dust on Microtus guentheri (Rodentia, Mammalia), measuring path-
ological changes in blood components (haemoglobin, erythrocyte, leucocyte and platelets number, erythrocyte sedi-
mentation rate (ESR) and white cell count). Biochemical indices were established for levels of the following blood
components : blood sugar, albumin, uric acid, triglycerides, cholesterol, total protein, creatinine, calcium and inor-
ganic phosphorus. The results obtained indicate that Microtus guentheri can be used as a species for evaluation of
the influence of polymetal dust emission.
KEY WORDS : Microtus guentheri, industrial polymetal dust, bioindication, biochemical and haematological indices
INTRODUCTION
basic haematological and biochemical indices in the
peripheral blood of the Guenther's vole, Microtus guenth-
Chemical pollution of ecosystems resulting from
eri (Danford & Alston) (Rodentia, Mammalia) and to
human activity and having an influence on individuals,
determine indices important for biological monitoring.
populations, communities and the ecosystem as a whole is
an ecological factor for wildlife. Detailed analysis of the
MATERIAL AND METHODS
entry of various such pollutants into the environment,
their concentration in selected organs and their role in
Polymetal microsilicic dust emission is a waste product
development and vitality of organisms is necessary for
from iron-bearing alloy production of metallurgical
revealing the effects of chemical pollution.
works. The present laboratory eco-toxicological experi-
Recently, dust pollution has increased, reaching its
ment assessed its effect on Microtus guentheri (Danford
highest values in the Northern hemisphere. During the
& Alston), which is a convenient subject for such investi-
past 20 years the atmosphere has been polluted with
gations because of its high reproductive potential. Being
240,000 t of ferosilicic dust. In the atmosphere of Sofia,
herbivorous, it is also an important link in the trophic
Bulgaria, the current amount of polymetal microsilicic
chain, and its stationary way of life determines the perma-
dust emissions is 0.75 1.0 mg/ m3 (FeSi-45%, Fe-
nent influence of different pollutants on its food base.
3,11%, Pb2, 03%, Mn-0,25%, Cd-0,57%, MgO-1,07%,
The toxic effect of the polymetal dust was studied
SiO-7,65%, AlO-1,76%, KO-2,60%, NaO-0,85%)
under experimental subchronic conditions. Eighty-five
(EEABG, 2002). Iron, magnesium and manganese are
individuals were divided into one control (15 individuals)
microelements that are absolutely necessary for hemo-
and two test groups (Group I and Group II with 35 indi-
globin synthesis and enzyme activity, while cadmium,
viduals each). In order to best approximate natural condi-
lead and aluminum are not nutritionally essential ele-
tions, the microsilicic dust was given through food in two
ments for animals. Exposure to acutely high, or chroni-
concentrations : Group I at 5% and Group II at 10% of
cally low levels may induce intracellular production of
food quantity. Samples for analysis were taken at 30, 60
metallothionein, which has an important function as a
and 90 days for all groups.
store in zinc metabolism (CHAKRABORTY et al., 1987,
The bioaccumulation and distribution of Cu, Pb, Zn,
FERNANDO et al., 1989). The high accumulation of cad-
Cd, Mn and Fe in different organs and tissues were exam-
mium can lead to food chain amplification (increases in
ined using an atomic absorption spectrometer (Perkin
concentration in animals at each step in the food chain),
Elmer). The pathological changes caused by the toxicant
because metallothionein bound cadmium has a long bio-
to the haemoglobin content, erythrocyte, leucocyte and
logical half-life in animals and because concentrations
platelet numbers, erythrocyte sedimentation rate (ESR)
tend to increase with age (VERMEER & CASTILA, 1991).
and white cell count were measured using an automatic
The main aim of this study was to investigate the heavy
hematological counter (HC-333). The following bio-
metal accumulation and distribution in different organs,
chemical indices were studied : blood sugar, albumin, uric
and the influence of polymetal microsilicic dust on some
acid, triglycerides, cholesterol, total protein, creatinine,
136
Tsenka Chassovnikarova, Roumiana Metcheva and Krastio Dimitrov
calcium and inorganic phosphorus levels using the bio-
possible detoxification mechanisms. The animal's organs
chemical analyzer Technicon RA-1000.
differed from one another in respect to heavy metal con-
centration. The most sensitive organs were the kidneys,
RESULTS AND DISCUSSION
where the accumulated levels of lead and cadmium were
the highest (29 mg/kg Pb and 32 mg/kg Cd for Group I on
The concentrations of the most toxic heavy metals are
the 90th day and 40 mg/kg Pb and 125 mg/kg Cd for
presented in Table 1. The elements considered were very
Group II on the 90th day), and the differences in cadmium
unevenly distributed. It seems important to recognize the
and lead concentrations between experimental and con-
pattern of distribution because this may allow an estimate
trol groups are statistically significant (t=4.36 ; p <
of the impact on organisms, as well as give an insight into
0,0001).
TABLE 1
Heavy metals concentrations in the whole body and in different organs of M. guentheri in mg/kg dry weight
Control
30th Day
60th Day
90th Day
N
Fe
Mn
Pb
Cd
Fe
Mn
Pb
Cd
Fe
Mn
Pb
Cd
Fe
Mn
Pb
Cd
Whole body
X±
10
203.4
2.6
1.7
1.4
Sd
48.1
0.5
0.5
0.4
Group I
X±
10
217.2
2.4
1.9
3.8 257.8
1.5
4.0
2.8
281.3
1.4
3.2
2.1
Sd
40.6
1.6
0.6
1.8
76.1
0.6
1.5
1.9
24.8
1.1
1.3
0.5
Group II
X±
8
240.0
3.5
7.4
3.9 265.3
3.0
8.3
3.1
320.8
4.0
5.8
4.6
Sd
63.8
0.4
4.3
4.3
118.0
0.5
3.0
0.5
21.0
1.4
3.2
1.6
Kidneys
X±
10
479.7
3.9
7.5
7.6
Sd
46.4
0.2
7.9
3.0
Group I
X±
10
507.6
12.1
19.2
86.6 470.6
5.4
22.4
53.9
659.6
14.7
28.1
31.6
Sd
144.8
4.9
7.8
72.4 162.9
3.9
7.9
27.3
170.8
6.1
21.0
10.5
Group II
X±
10
439.6
10.1
28.7 107.2 389.7
12.1
44.2 152.9
683.1
12.3
40.3 125.1
Sd
97.5
2.9
15.6
45.0
43.1
2.5
18.1
54.4
213.7
5.7
16.1
20.8
Liver
X±
10
784.4
8.7
3.8
7.6
Sd
31.9
2.4
1.0
2.6
Group I
X±
10
1064.8
8.8
3.2
20.9 901.3
6.1
5.7
71.0
1103.2
7.2
2.8
20.1
Sd
70.9
2.3
1.9
19.6
49.8
2.7
1.9
19.3
343.2
5.6
1.6
9.7
Group II
X±
10
868.9
9.0
5.4
37.3 645.3
8.6
10.4
48.5
800.6
8.1
10.0 114.8
Sd
237.3
2.8
3.0
23.9 155.1
2.2
3.2
12.7
407.7
2.2
5.4
8.6
Cadmium and lead cause kidney toxicity in M. guen-
The changes in the average values of basic blood indi-
thery. The results concerning the accumulation of cad-
ces (Table 2) have an analogous character to that of the
mium are very interesting. In the first variant of the expe-
metal data. In both test groups there was a statistically
riment the bioaccumulation of this element was three
significant reduction of the average values on the 30th day
times higher on the 30th day than on the 90th day, confirm-
(with the exception of the average number of leucocytes),
ing data obtained by MILLS & DELGRANO (1972) and
followed by a significant increase on the 60th day. At the
TOPASHKA-ANCHEVA et al. (1998). The high cadmium
end of the experimental period a tendency towards com-
concentration on the 30th day may induce intracellular
pensation of the changes occurred but, once more, it was
production of matallothionein, a low-molecular-weight
not entirely effective.
protein rich in sulfur amino acids to which cadmium can
The average values of albumin, creatinine, cholesterol
be bound and, hence, rendered less toxic (SCHREIBER &
and total protein varied similarly : at the beginning of the
BURGER, 2002). At the end of the experimental period a
experiment there was an initial reduction followed by evi-
tendency towards compensation of the toxic effect
dence of a compensatory mechanism. Group II exhibited
occurred but it was not entirely effective.
a constant increase in blood sugar and uric acid, while
From an ecological point of view, the data obtained for
triglycerides showed a decrease over the experimental
the total bioaccumulation of these heavy metals in the
time period to nearly that of the control value.
body of the Guenter's vole are very important because
The results obtained show anemic effects during the
they show an average assessment of the organism's intox-
experiment, which were surmounted. On the 60th day, a
ication a fact that could be used for prognoses in biologi-
dissociation of erythrocyte number and hemoglobin con-
cal monitoring.
centration occurred as an expression of hypochromic ane-
A bioindicator species for estimation of the influence of polymetal dus emissions
137
TABLE 2
Hematological and biochemical values in exposed and control time
Referent
30th day
60th day
90th day
Indices
values
n = 15
n = 15
n = 15
n = 90
Group I
Group II
Group I
Group II
Group I
Group II
Hemoglobin (g/l)
161.0±9.0
123.1±5.3
136.2±4.9
160.8±2.6
149.0±8.3
169.0±9.2
178.2±6.9
Erythrocytes (10 12/l)
4.9±0.3
3.7±0.9
4.3±1.1
9.5±0.3
9.0±0.2
5.1±0.6
5.3±0.4
Leukocytes (109/l)
4.1±0.3
3.9±0.8
6.4±0.7
9.6±1.4
14.4±1.3
3.8±0.9
8.6±0.6
ESR (mm/h)
1.2±0.3
-
-
0.8±1.9
1.5±2.2
0.8±0.9
0.8±1.3
Thrombocytes (109/l)
268.5±9.2
198.0±7.4
212.3±8.8
430.5±9.8
456.0±8.3
268.5±9.3
316.5±9.1
Blood sugar (mmol/l)
2.6±0.1
3.6±0.4
3.2±0.2
3.7±0.4
4.0±0.2
4.6±0.2
4.2±0.3
Albumin (g/l)
43.0±0.8
-
-
40.0±0.8
33.4±0.4
42.6±0.7
44.3±0.6
Uric acide (µmol/l)
86.1±0.3
-
-
80.1±0.4
108.2±0.3
105.8±0.4
194.2±0.6
Creatinine (µmol/l)
165.2±2.5
21.2±3.5
41.3±3.3
43.0±2.9
40.3±3.1
161.2±3.9
148.4±4.1
Cholesterol (mmol/l)
2.1±0.2
1.7±0.6
1.4±0.3
2.1±0.2
2.0±0.2
2.3±0.3
2.1±0.4
Triglycerides (mmol/l)
1.2±0.3
2.7±0.3
2.9±0.2
-
-
1.7±0.4
0.9±0.5
Total protein (g/l)
82.0±1.4
71.3±1.9
72.6±1.8
80.3±1.7
74.2±1.9
86.3±2.1
93.4±2.0
Calcium (mmol/l)
1.9±0.2
2.4±0.6
2.3±0.5
2.7±0.3
2.7±0.6
-
-
Inorganic Phosphorus (mmol/l)
2.5±0.3
2.3±0.7
2.2±0.9
1.7±0.8
2.1±0.6
-
-
mia. The acceleration of blood sedimentation rate on the
The pathological changes observed in the tested blood
60th day supported this. Evidently toxic polymetal dust
indices, as a result of synergetic action of the metal cap-
irritates marrow and stimulates erythropoiesis. Many
tions or ferosilicic dust show that M. guentheri is a good
young erythrocytes with reduced hemoglobin were
bioindicator species for the evaluation of dust emissions.
pushed out to the periphery. On the 30th day the average
number of leukocytes in Group II was twice as high as the
control value. Consequently, this index is a very good
REFERENCES
marker for the toxic action of polymetal dust.
CHAKRABORTY T., I. B. MAITI & B. B. BISWAS (1987). A single
The changes of biochemical indices show that a hyper-
form of metallothionein is present in both heavy metal
glycemic effect occurred during the whole experiment,
induced and neonatal chicken liver. L. Biosci. (Bangalore)
and its expression depended to a certain extent on dose
11 : 379-390.
and time. The hyperuricaemic effect in Group II was the
EEABG (2002). Air pollution bulletin. Executive Environmen-
reason for reduced elimination of uric acid because of
tal Agency. Sofia, Bulgaria, 01.2002.
kidney damage resulting from exposure.
FERNANDO, L. P., D. WEI & G. K. ANDREWS (1989). Structure
and expression of metallothionein. J. Nutr., 119 : 309-318.
Physiological triglyceridemia in M. guentheri was
MILLS, C. F. & A.C. DELGRANO (1972). Copper and status of
reduced during the course of the experiment. Anabolic
ewes and lambs receiving increased dietary concentration of
processes were affected leading to a reduction and stunt-
cadmium. Nature, 239 : 171-173.
ing of growth. This is also confirmed by the suppressed
NYHOLM, N.E. & A.A. RUELING (2001). Effects of Decreased
synthesis of triglycerides. The increased amount of cho-
Atmospheric Heavy Metal Deposition in South Sweden on
lesterol shows an acute hepatotoxic effect on the 30th day.
Terrestrial Birds and Small Mammals in Natural Popula-
The opposite tendency in the changes of triglycerides and
tions. Water, Air and Soil Pollution : Focus; vol. 1, no. 3/4,
cholesterol is connected with lipoprotein exchange. Evi-
pp. 439-448.
dently the synthesis of lipoproteins in the liver is reduced.
SCHREIBER, E., A. & J. BURGER (2002). Biology of Marine Birds,
CRC Press, Boca Raton.
The increased level of urea shows that a nephrotoxic
TOPASHKA-ANCHEVA, M., R. METCHEVA, N. ATANASSOV (1998).
effect is probably occurring with an impact at the tubular
Bioaccumulation and clastogenic effects of industrial dust on
level. This is why, at the beginning of the experiment,
M. guentheri (Microtinae, Rodentia) in eco-toxicological
urea concentrations increase but creatinine levels do not.
experiment. Act. Zool. Bulg., 12 : 45-67.
The polyurea observed is due to hypoglycemia. Although
VERMEER, K. & J.C. CASTILA (1991). High cadmium residues
Cd, Fe, Mn and Mg cause damage to the liver at very high
observed during a pilot study in shorebirds and their prey
concentrations, the critical organ is generally considered
downstream from the El Salvador copper mine, Chile. Bull.
to be the kidney (NYHOLM & RUELING, 2001). Nephropa-
Environ. Contam. Toxicol., 56 : 242-248.
thy is indicated by proximal tubule cell necrosis, proteiu-
WHITE, D.H., M.T. FINLEY & J.F. FERRELL (1978). Histopatho-
ria, glucosuria, increased urinary cadmium and decreased
logical effects of dietary cadmium on kidneys and testes of
cadmium content in kidneys (WHITE at al., 1978).
mallard ducks. J. Toxicol. Environ. Health, 4 : 551-558.
Belg. J. Zool., 135 (2) : 139-143
July 2005
Trophic signatures of marine organisms in the
Mediterranean as compared with other ecosystems
Rainer Froese1, Stefan Garthe2, Uwe Piatkowski1 and Daniel Pauly3
1 Leibniz Institute of Marine Sciences, Düsternbrooker Weg 20, D-24105 Kiel, Germany
2 Research and Technology Centre (FTZ), University of Kiel, Hafentörn, D-25761 Büsum, Germany
3 Fisheries Centre, 2204 Main Mall, University of British Columbia, Vancouver, B.C., Canada V6T 1Z4
Corresponding author : Rainer Froese, rfroese@cifm-geomar.de
ABSTRACT. We compared several large marine ecosystems in terms of species numbers of fishes, sea birds,
marine mammals, and cephalopods. We examined how these numbers were distributed by trophic level, from her-
bivores to top predators. We created group-specific trophic signatures as plots of number of species by trophic level,
and used these to identify similarities and discrepancies between taxonomic groups and ecosystems. Preliminary
results suggested that trophic signatures are similar for ecosystems previously known to share major features, and
different for dissimilar ecosystems. In the Mediterranean, as well as in the other large marine ecosystems, fish
clearly dominate the predatory trophic levels above 3.0. Preliminary signatures for cephalopods, marine mammals,
and sea birds in the Mediterranean and in the North Sea indicate that these groups are restricted to trophic levels
above 3.0, and are represented by many fewer species than are predatory fish. Notably, cephalopods are the only
invertebrates present at higher trophic levels (>= 4). Invertebrates other than cephalopods are restricted to trophic
levels below 3, with very few exceptions. Trophic signatures appear to be useful tools for better understanding of
the roles that different groups of organisms play in different ecosystems. We also applied free-scale network theory
to analyse the food web created by trophic links of fishes. Our preliminary results indicated that Mediterranean
fishes are, on average, only two trophic links away from each other.
KEY WORDS : trophic level ; food web ; Mediterranean ; North Sea ; Baltic ; Black Sea ; Caribbean ; South China
Sea
INTRODUCTION
Another type of trophic signature is generated by a plot
of species frequency in relation to their number of trophic
links (WILLIAMS et al., 2000). Such plots can be inter-
There is wide agreement that modern fisheries manage-
preted by applying `small world' or `free-scale network'
ment has to take into account not only prey and predators
theories (JEONG et al., 2000 ; ALBERT & BARABASI, 2002).
of a target species, but also their role in an overall ecosys-
Within such framework species are nodes that are inter-
tem context (CHRISTENSEN, 1996). There also are increas-
connected through trophic relationships (links). The dis-
ing calls for ecosystem-based management as an alterna-
tance or path length between two species is the number of
tive, or at least a complement, to the single-species
links (k) between them. For example, a species A is one
approaches so far used exclusively, and with little suc-
link away from species B if A is prey or predator of B ; it
cess, to manage commercial fisheries (NRC, 1999). Large
is two links away if A and B do not interact directly but A
Marine Ecosystems (LMEs) have been identified as suita-
shares with B at least one prey or predator, etc. Analysis
ble units for management (see SHERMAN & DUDA, 1999
of non-biological free-scale networks suggested that path
and http ://www.edc.uri.edu/lme/), yet our understanding
length will increase considerably if a certain quantity of
of LMEs is still limited. In this study we compared the
the most connected nodes is removed, compared with a
Mediterranean with five other LMEs based on the respec-
random removal of nodes, which will have little effect on
tive trophic structures of important species groups. We
path length. Here we test this prediction for the Mediter-
used signatures created by plots of number and average
ranean.
size of species by trophic level as conservative, long-term
characteristics of LMEs. We compared these signatures
MATERIAL AND METHODS
between groups of organisms and between LMEs. Our
first hypothesis was that a given group of organisms will
For the purpose of this study, we used fish, cephalo-
show similar signatures in similar LMEs, and vice-versa.
pods, marine mammals and sea birds as groups of organ-
Our second hypothesis stated that different groups of
isms. We followed the LME definitions of SHERMAN &
organisms will have typical and different signatures. We
DUDA (1999). We used the Baltic and the Black Sea as
expected that the subtropical Mediterranean would show
analogue brackish, temperate, and species-poor ecosys-
an intermediate position between temperate LMEs (North
tems. We used the North Sea as a marine, temperate eco-
Sea, Baltic and Black Sea) and tropical LMEs (Caribbean
system, and we used the Caribbean and the South China
and South China Sea).
Sea as examples of tropical, species-rich ecosystems.
140
Rainer Froese, Stefan Garthe, Uwe Piatkowski and Daniel Pauly
For fishes, we used the trophic levels, maximum
RESULTS AND DISCUSSION
lengths, and LME assignments given in FishBase (FROESE
& PAULY, 2000 ; www.fishbase.org). For cephalopods, we
used data on distribution and food in NORMAN (2000) and
Fig. 1 shows the trophic signatures of 567 species of
in CephBase (www.cephbase.org). For marine mammals,
fish in the Mediterranean, plotted as number of species
we used trophic levels from PAULY et al. (1998). For
per 0.5 trophic level. The standard errors increase with
marine birds, we used information on food and distribu-
trophic levels because second and third-level predators
tion from DEL HOYO et al. (1992 ; 1996), BEZZEL (1985),
typically exploit a wide range of prey, from herbivores to
MELTOFTE et al. (1994), and SKOV et al. (1995). Trophic
other second or third-level predators.
levels (trophs) were calculated from diet composition
data as Troph = 1 + weighted mean troph of the food
Fig. 2 shows the trophic signatures of fishes in the Bal-
items (see CHRISTENSEN & PAULY (1992) for details,
tic, the Black Sea, the North Sea, the Mediterranean, the
including estimation of standard errors). If no diet compo-
Caribbean and the South China Sea, with total number of
sition, but individual food items were known, trophic lev-
species increasing in the same sequence. Despite the con-
els and their standard errors were estimated using a
siderable differences between these ecosystems in terms
Monte Carlo routine described in PAULY & SA-A (2000).
of salinity, size, temperature, and species numbers, the
Both routines are implemented in the TrophLab software,
signatures are strikingly similar : in all ecosystems fishes
which can be downloaded at www.fishbase.org/down-
cover the whole range of trophic levels, from herbivores
load/. If no food information was available for a given
near 2.0 to top predators at above 4.5. Both herbivores
species, it was assigned the mean troph of congeners or of
and top predators contribute about or less than 5% of total
the respective family. For invertebrates, we relied on an
species numbers. Highest species numbers always occur
estimate of Mediterranean `macroscopic fauna' (8500
around troph 3.2, i.e., with first-level predators feeding
species) by the European Environment Agency (www/
eea/ei/int.). We subtracted from this estimate the 691
mainly on herbivorous organisms. The signatures of the
Mediterranean species of fish, birds, cephalopods and
brackish, species-poor Baltic and Black Seas are more
marine mammals, and assumed that, for the purpose of
similar to each other than to the marine, more speciose
this study, the remainder could be assigned to trophic lev-
North Sea, which has more top-predators and fewer
els between 2 and 3.49 (see below).
lower-level species, resulting in a signature that cuts
across that of the brackish systems. As expected, the sub-
For the free-scale network analysis we used data on
tropical Mediterranean takes an intermediate position
prey items as recorded in FishBase (FROESE & PAULY,
between the temperate and the tropical systems. The Car-
2000). In FishBase food items of fishes are classified into
ibbean signature is the only one where the lower leg is
59 categories such as diatoms, polychaetes, euphausiids,
bent to the right, indicating a relatively higher number of
or squids/cuttlefish (SA-A et al., 2000). These categories
herbivorous fishes than in the other systems.
are similar to the `trophic species', which have been used
5
in other food web studies and which are defined as "func-
Baltic
tional groups of taxa that share the same consumers and
Black Sea
resources within a food web" (W
4.5
ILLIAMS et al., 2000). For
South China Sea
the purpose of this study we considered 385 Mediterra-
Caribbean
nean fish species as nodes and their reported food catego-
4
North Sea
Mediterranean
ries as links.
evel
L
c 3.5
ophi
trophic level
Tr
3.2
3
5
2.5
4.5
2
l
e
4
1
10
100
1000
10000
v
Fig. 2. A comparison of trophic signatures of fishes in six
Le
Num ber of Fish Species
c
large marine ecosystems.
3.5
ophi
trophic level
Tr
3.2
Fig. 3 shows the geometric mean maximum lengths of
3
Mediterranean fishes per half trophic level class. Most
first-level predators at trophs of about 3.0 are small fishes
2.5
of about 20 cm maximum length, generally feeding on
zooplankton and/or small benthic invertebrates. As
2
expected the mean maximum length increases with
1
10
100
1000
10000
Fig. 1.
Num ber
Number of fish sp o
ec f F
ie ish
s Specie
of thes Mediterranean by
trophic level to 1.5 m for top-predators, but it also
trophic level. Error bars show the mean standard error of indi-
increases to about 27 cm for herbivores. Variation in 95%
g. 1. Number of fish species of the Mediterranean by trophic level.
vidual trophic level estimates.
confidence limits follows the same pattern.
Trophic signatures of marine organisms in the Mediterranean
141
of just a few species may alter the signature. Neverthe-
5.0
less, the maximum at 4.2 for marine mammals shows
their position as top predators in the Mediterranean, also
4.5
confirmed by a plot (not shown here) of all marine mam-
mals in the world showing a similar signature and the
4.0
same maximum. Fig. 6 shows a similar graph for the
North Sea, with similar signatures for the respective
evel
i
c l
groups. Species numbers for fish and cephalopods in the
3.5
h
p
North Sea are only about 1/3 of that in the Mediterranean,
r
o
T
whereas numbers for sea birds and marine mammals are
3.0
increased by 50% and 20%, respectively. This reflects the
greater role of homoeothermic groups (i.e., marine mam-
2.5
mals and sea birds) in colder waters.
5.0
2.0
0
50
100
150
Geometric mean maximum length (cm TL)
4.5
Fig. 3. Geometric mean maximum length of Mediterranean
Birds (48)
g. 3. Geometric mean maximum length of Mediterranean fishes at differe
fishes at different trophic levels, with error bars showing 95%
4.0
confidence limits.
th error bars showing 95% confidence limits
evel
l
Mammals (17)
Fig. 4 shows the length signatures of all six LMEs, all
c 3.5
Cephalopods (59)
with a signature roughly similar to that of the Mediterra-
ophi
Fish (567)
Tr
nean, with minimum mean size around trophic level 3 and
3.0
an increase towards higher and lower trophic levels.
Tropical systems are typically dominated by smaller spe-
2.5
cies, which is shown here by the signatures of the South
China Sea and the Caribbean being mostly left of the tem-
2.0
perate systems. The subtropical Mediterranean shows
1
10
100
1000
again an intermediate position between temperate and
Fig. 5.
Number
Number of species per tr of spec
ophic ies
level for four groups of
tropical systems, except for the lower trophic levels
organisms in the Mediterranean.
where it overlaps with the tropical systems.
5
5
Marine
Mammals (22)
4.5
4.5
Cephalo-
pods (20)
4
4
l
e
v
evel
e
l
l
Birds (69)
c 3.5
3.5
ophic
ophi
Fish (186)
Tr
Tr
Baltic
3
3
Black Sea
South China Sea
Caribbean
2.5
2.5
North Sea
Mediterranean
2
2
1
10
100
1000
0
50
100
150
Number of species
Geom etric m ean m axim um length (cm TL)
Fig. 6. Number of species per trophic level for four groups of
Fig. 4. Comparison of geometric mean maximum lengths at
g. 6. Number of species per trophic level for four groups of organisms in the
organisms in the North Sea.
g. 4. Geometric mean maximum lengths of fishes at different trophic levels
different trophic levers for fishes in six large marine ecosys-
tems.
arine ecosystems.
Fig. 7 shows the sum of species per trophic level across
the considered groups, resulting in the pyramid structure
Fig. 5 shows the trophic signatures of fish, cephalo-
that is commonly encountered when plotting individual
pods, sea birds, and marine mammals in the Mediterra-
numbers (LINDEMAN, 1942), or biological production
nean. Total species numbers of fish are an order of magni-
(CHRISTENSEN & PAULY, 1992) by trophic level. Looking
tude higher than those of the other groups. Only fish
at Fig. 7 from a phylogenetic perspective, it appears that
species occupy all trophic levels, whereas birds, cephalo-
the four groups jointly dominating the upper trophic lev-
pods and mammals are restricted to levels above 3.0.
els of marine ecosystems (i.e., fish, marine mammals, sea
Most cephalopods feed at about trophic level 3.7 (0.5
birds and cephalopods) tend to be highly derived, preda-
above fish), and most birds and mammals feed above 4.0,
tory representatives of their class or phylum, while the
one level above fish. Because of the low number of
organisms abundant at the lower trophic levels (<3), tend
marine mammals (17), their signature must be viewed
to belong to stem groups, and to feed mainly on phyto-
with some caution, as improved understanding of the diet
plankton, benthic algae and detritus (though other inverte-
142
Rainer Froese, Stefan Garthe, Uwe Piatkowski and Daniel Pauly
brates are also consumed, and cnidarians, chaetognaths
of species (380.9, SE +/-0.10) within 3 links, and all spe-
and other groups of carnivorous zooplankton are actually
cies (384) within 4 links distance from themselves. The
restricted to trophic levels above 3).
weighted mean path length in the food web was 2.38 (SE
+/-0.033) links. This agrees well with other food-web
4.5-5
Mammals
analyses, where path lengths between 1.4 and 2.7 have
Birds
been found (WILLIAMS et al., 2000). Knowledge about
4-4.5
mean path length is important as it quantifies the average
Cephalopods
number of links necessary for an effect to propagate from
Fish
3.5-4
one species to other species. Significant effects have been
Benthic invertebrates
shown to propagate often two and sometimes three links
3-3.5
Planktonic
away from manipulated species, whereas species more
invertebrates
than three links away from each other are functionally
2.5-3
disconnected (BRETT & GOLDMAN, 1997; PACE et al.,
1999).
2-2.5
It has been suggested that the removal of 5% of the
0
1000
2000
3000
4000
5000
6000
nodes starting with those with highest numbers of links
can double path length (COHEN, 2002). In our data set
Fig. 7. Numbers of Mediterranean species per trophic level.
Fig. 7. Numbers of Mediterranean species per trophic level.
such removal of species with highest numbers of trophic
Note that about 7800 invertebrates are assumed, with most
links increased mean path length to 2.43 (SE +/-0.066),
invertebrates are assumed, with most being herbivores, fewer being
being herbivores, fewer being omnivores, and very few being
which is not significantly (t-test, n=740, P<0.05) differ-
first-order predators.
ent from 2.38. To choose a more realistic scenario we
b i
fi t
d
d t
removed 38 Mediterranean fishes that were marked in
This suggests that overfishing, which tends to remove
FishBase as `highly commercial,' many of them upper-
upper-trophic level animals (PAULY et al., 1998) will tend
trophic level species with many (median=5) trophic links.
to reverse the implied evolutionary sequence, as noted in
This removal increased mean path length to 2.45 (SE +/-
PAULY (1979), and further developed in PARSONS (1996).
0.033), which is also not significantly (t-test, n=712,
Feeding studies exist only for a fraction of the inverte-
P<0.05) different from 2.38. Thus, it appears that food
brates in the Mediterranean or other LMEs, and thus the
webs are relatively robust towards removal of 5-10% of
distribution to trophic levels shown in Fig. 7 is hypotheti-
highly connected species. This might explain the observa-
cal. Detailed trophic studies on invertebrate species, as
tion that many ecosystems have apparently withstood
well as generalizations by higher taxa such as families
very strong fishing pressure for a very long time. We want
and orders, are urgently needed for a better understanding
to stress that our application of scale-free network theory
of the foundation of LME food webs.
to food-web data of Mediterranean fishes is preliminary
and a more thorough study of trophic relationships
120
including non-fish species is needed to confirm or reject
y = ~k^ -2.2
our results.
100
s
k
i
n
l
c
80
ACKNOWLEDGMENTS
r
ophi
t
60
k
We thank the FishBase team for accumulating much of the
i
t
h
data on which this study was based, and Cornelia Nauen for
w
s
40
pointing us towards free-scale network analysis. We thank
i
e
c
e
Ulrich Sommer for comments on the manuscript.
p
S
20
REFERENCES
0
0
5
10
15
20
25
ALBERT, R. & A.-L. BARABASI (2002). Statistical mechanics of
Number of trophic links (k)
complex networks. Rev. Mod. Phys., 74(1) : 47-97
Fig. 8. Frequency distribution of species with k trophic links,
Fig. 8. Frequency distribution of species with k trophic links, with eye-fitte
BEZZEL, E. (1985). Kompendium der Vögel Mitteleuropas. Non-
with eye-fitted curve. Note that number of species with one
passeriformes - Nichtsingvögel. Aula Verlag, Wiesbaden.
link is probably too high and number with two links probably
number of species with one link is probably too high and number with two
too low because of a bias caused by `understudied' species.
BRETT, M.T. & C.R. GOLDMAN (1997). Consumer versus
resource control in freshwater pelagic food webs. Science,
275 : 384-386
Fig. 8 shows a frequency plot of the number of trophic
C
link categories per Mediterranean fish species. The plot
HRISTENSEN, V. (1996). Managing fisheries involving predator
and prey species. Rev. Fish Biol. Fish., 6 : 1-26.
shows the typical shape of a scale-free network which is
C
roughly described by a power-law function of the form k-
HRISTENSEN, V. & D. PAULY (1992). The ECOPATH II - a soft-
ware for balancing steady-state ecosystem models and calcu-
y, and where y typically takes values between 2 and 3
lating network characteristics. Ecol. Model., 61 : 169-185.
(here y = 2.2). Thirty-two fishes (8%) preyed directly on
COHEN, D. (2002). All the world's a net. New Scientist, 2338 :
other Mediterranean fishes and the shortest distance
24-29
between them was thus one link. Analysis of ten ran-
DEL HOYO, J., A. ELLIOTT & J. SARGATAL (1992). Handbook of
domly selected species showed that they had, on average,
the birds of the world. Vol. 1 : Ostrich to ducks. Lynx Edi-
54% of species (208.1, SE +/-16.7) within 2 links, 99%
cions, Barcelona
Trophic signatures of marine organisms in the Mediterranean
143
DEL HOYO, J., A. ELLIOTT & J. SARGATAL (1996). Handbook of
PAULY, D. (1979). Biological overfishing of tropical stocks.
the birds of the world. Vol. 3 : Hoatzin to auks. Lynx Edi-
ICLARM Newsletter 2 (3) : 3-4.
cions, Barcelona
PAULY, D. & P. SA-A (2000). Estimating trophic levels from
FROESE, R. & D. PAULY (2000). FishBase 2000 : concepts,
individual food items. In : FROESE & PAULY (eds.), FishBase
design and data sources. ICLARM [Distributed with 4 CD-
2000 : concepts, design and data sources. ICLARM : 185.
ROMs].
J
PAULY, D., V. CHRISTENSEN, J. DALSGAARD, R. FROESE & F.C.
EONG, H., B. TOMBOR, R. ALBERT, Z.N. OLTVAI & A.-L. BARA-
TORRES JR. (1998). Fishing down marine food webs. Science,
BASI. (2000). The large-scale organization of metabolic net-
works. Nature, 407 :651-654.
279 : 860-863.
LINDEMAN, R.L. (1942). The trophic dynamic concept in ecol-
PAULY, D., A.W. TRITES, E. CAPULI & V. CHRISTENSEN (1998).
ogy. Ecology, 23 (4) : 399-418.
Diet composition and trophic levels of marine mammals.
MELTOFTE, H., J. BLEW, J. FRIKKE, H.-U. RÖSNER & C. J. SMIT
ICES J. Mar. Sci., 55 : 467-481.
(1994). Numbers and distribution of waterbirds in the Wad-
SA-A, P., M.L.D. PALOMARES & D. PAULY (2000). The Food
den Sea. Results and evaluation of 36 simultaneous counts in
Items Table. In : FROESE & PAULY (eds.), FishBase 2000 :
the Dutch-German-Danish Wadden Sea 1980-1991. IWRB
concepts, design and data sources. ICLARM : 182-188.
Publ. 34 & Wader Study Group Bull. 74, Spec. Issue : 1-192.
S
N
HERMAN, K. & A.M. DUDA. (1999). An ecosystem approach to
ORMAN, M. (2000). Cephalopods, a world guide. CochBooks,
global assessment and management of coastal waters. Mar.
Hackenheim.
Ecol. Progr. Ser., 190 : 271-287.
NRC (1999). Sustaining marine fisheries. National Research
Council. National Academy Press, Washington D.C.
SKOV, H., J. DURINCK, M. F. LEOPOLD & M. L. TASKER (1995).
PARSONS, T.R. (1996). The impact of industrial fisheries on the
Important bird areas for seabirds in the North Sea including
trophic structure of marine ecosystems. In : POLIS & WINNE-
the Channel and the Kattegat. BirdLife International, Cam-
MILLER (eds.), Food webs : integration of patterns and
bridge.
dynamics. Chapman & Hall, New York : 352-357.
WILLIAMS, J.R., N.D. MARTINEZ, E.L. BERLOW, J.A. DUNNE &
PACE, M.L., J.J. COLE, S.R. CARPENTER & J.F. KITCHELL. (1999).
A-L. BARABASI. (2000). Two degrees of separation in com-
Trophic cascades revealed in diverse ecosystems. Trends
plex food webs. Santa Fe Institute Working Paper 01-07-
Ecol. Evol., 14 : 483-488.
036.
Belg. J. Zool., 135 (2) : 145-149
July 2005
The status of the Golden Jackal (Canis aureus L.) in
Greece
Giorgos Giannatos, Yiannis Marinos, Panagiota Maragou and Giorgos Catsadorakis
WWF Greece, 26 Filellinon St., Gr-10558 Athens, Greece
Corresponding author : Giorgos Giannatos, e-mail : giannatos@bid.uoa.gr
ABSTRACT. Broadcasted jackal howls were used to survey the status of the golden jackal in Greece. All sites with
recent indication of jackal presence were surveyed at selected calling stations, and minimum population estimates
were recorded. The results of the survey show that both populations and distribution area of the golden jackal in
Greece have been declining steadily during the last three decades. The golden jackal has disappeared from Central
and Western Greece and is currently confined in discontinuous, isolated population clusters in Peloponnese, Fokida,
Samos isl., Halkidiki and North-eastern Greece. The reduction was more distinct in Southern Greece, which used to
be the jackal's main area 20 years ago. The current minimum size of the jackal population in Greece was estimated
at 152-162 different territorial groups. The largest population cluster was found in Nestos Vistonida area, NE
Greece. In Southern Greece, the jackal is found in the Mediterranean maquis zone at altitudes below 600m asl.
Some individuals were observed up to 1000m asl, but were considered exceptional. In Northern Greece the species
was found in areas below 250m asl, while the highest population densities were found in thickets around wetlands
up to 10m asl.
KEY WORDS : Canis aureus, Greece, status, acoustics, vocalization, howling response
INTRODUCTION
MATERIAL AND METHODS
The jackal in Europe is distributed in small and scat-
Survey area
tered populations, mainly along the Mediterranean and
The survey was carried out between May 2000 and
Black Sea coast of the Balkan Peninsula (DEMETER &
June 2001. The survey area included all localities in
SPASSOV, 1993 ; KRYSTUFEK et al., 1997). In this area
Greece with recent sightings, confirmed damage, or at
occurs only in Mediterranean-type scrubland and lowland
least some (even doubtful) evidence of jackal presence.
wetlands (DEMETER & SPASSOV, 1993), and being on the
Selection of these areas was based on relevant informa-
top of the food chain it is an important indicator of these
tion collected through questionnaires addressed to Forest
ecosystems.
Services, Hunting Associations, WWF Greece members,
The golden jackal has become by far the most rare
and personal interviews with local people, especially
canid species in Greece (G
shepherds. After gathering and verifying all collected
IANNATOS & IOANNIDIS, 1989;
1991; K
answers, a total of 264 possible areas of presence were
ARANDINOS & PARASCHI, 1992) as its population
has been declining during the last three decades. The
identified. In each of these areas selected survey routes
jackal is the only medium-sized carnivore in Greece that
were drawn based on existing road networks, vegetation,
has suffered a rapid decline in its distribution and popula-
and morphology. Calling stations were set along these
tion numbers, and the exact causes for the species' reduc-
routes in such a way as to cover completely each area of
tion in Greece are generally unknown. No systematic sur-
presence. Each station was located in a site with good vis-
vey has been carried out so far.
ibility and acoustics, and usually but depending on the
terrain at a high vantage point. Linear distance between
The legal status of the species is still obscure and unde-
successive trial calling stations was between 2-4 km,
termined. It is listed as "vulnerable" in the Red Data Book
depending on the topography of the sampling area. Each
for Greek Vertebrates (KARANDINOS, 1992) but otherwise
station's co-ordinates were recorded by GPS.
it is neither officially declared as a game species nor as a
protected one. In general very little information is availa-
Acoustic method
ble on jackal ecology and conservation status in Europe.
The current population status of the jackal in Greece
In order to elaborate conservation measures for the spe-
was assessed by a calling survey method that combined
cies and develop an action plan for its conservation,
acoustic and visual observations of jackals after stimula-
WWF Greece completed a country-wide survey and map-
tion with playback howls. Similar methods have been
ping of the species' population status, distribution, and
extensively used to survey social and vocal carnivores
status changes during the last 25 years. This study sum-
(MC CARLEY, 1975 ; HARRINGTON & MECH, 1982 ; CREEL
marises the first results of this project.
& CREEL, 1996 ; JAEGER et al., 1996 ; MILLS et al., 2001).
146
Giorgos Giannatos, Yiannis Marinos, Panagiota Maragou and Giorgos Catsadorakis
A broadcasted group-yip howl by three to four jackals
and 12.5 km2, depending on the different landscape
was used at each calling station. The howl was recorded
topography of the surveyed area.
on a mini disc and broadcasted using an Aiwa AMF 65
At each site the following parameters were also
recorder wired to a 20-Watt caller with 15-Watt chip
recorded to assess major features of the habitat and
amplifier. The howls were played from the roof of a vehi-
jackal-human interactions. 1) Altitude and the most domi-
cle at night at the selected calling stations, always one
nant plant species within a 1km radius from the approxi-
hour after sunset on calm and dry nights. Windy or rainy
mate location of the jackals during the point count survey.
nights, which could seriously disturb the observers' hear-
The radius was selected under the assumption that these
ing capacity or animal responsiveness, were strongly
locations were within the jackals' home range. 2) The dis-
avoided (MC CARLEY, 1975 ; JAEGER et al., 1996). Each
tance from the nearest human settlement.
howl broadcast lasted for 30-sec and was followed by a 5-
minute pause. This set of broadcast and pause was
repeated six times, for an overall session time of ca. 30
RESULTS
minutes. The direction of the caller was changed every
two to three howls, depending on the landscape structure
Population status
and the direction of the wind. During and after each howl
During the survey 264 possible areas of presence were
broadcast, two to three members of the field team
visited and a positive jackal response was recorded in 131
recorded the direction and the possible number of the
(50%). The easternmost peninsula of Halkidiki (Mt.
responding jackhals. It was assumed that each response-
Athos) was not surveyed because a research permit was
direction coincided with a territorial group.
not issued in time. However, from personal observations
In the event of an immediate response from close-quar-
we can verify that the species was present in almost all
ters, high intensity spotlights (500,000-1,000,000 candle
areas of the peninsula.
power) were used to survey the area for 3600 around the
At the majority of calling stations (67%) the jackals
calling station to locate approaching animals. When the
responded within the first five minutes. In 45 cases it was
response was heard from a great distance, or if no
possible to attract animals from the responding jackal
response at all was recorded, the area was surveyed after
group. The majority of sightings (85%) involved one to
the 2nd or 3rd howl broadcast (i.e. 5-10 minutes from the
two animals. The largest group observed consisted of five
beginning of a session), in order not to scare away possi-
individuals, but such a number was observed only once
ble approaching animals. Observation was facilitated by
(Fig. 1). The minimum total number of groups found was
7x50 binoculars. In locations with good visibility,
152-162 (Tab. 1).
approaching animals could be identified from more than
250m by their characteristic gait and shining eyes. In
30
cases of approaching animals we counted all the animals
in view.
25
It was assumed that only territorial groups of jackals
20
were responding to the broadcast playbacks. Identifica-
tion of different individuals howling in chorus within
15
each group was not possible by hearing alone, especially
in cases of groups of more than two animals.
10
Frequency of sightings
Maximum human hearing distance on windless nights
5
from a vantage point in open terrain with no background
noise was determined at 1.8-2 km, whereas the maximum
0
1
2
3
4
5
distance for attracting jackals was determined at 1.5 km.
Fig. 1. Freq
Number of individuals observ
uency and number of ap ed in each case
proaching jackal individ-
In order to experimentally test the maximum distance that
uals
the jackals could be heard with accuracy in a relatively
open terrain, after the detection of a jackal group one of
According to records of the Ministry of Agriculture
the observers stayed close to the animals, while the rest of
(Min of Agriculture, unpublished data), the decline of the
the team drove to distances of 1.5 and 2 km. The jackal
jackal population started in the 70s and was even more
howls were broadcasted in both distances. After the jack-
intense in the early eighties. Even by 1980, the harvest
als responded the two groups communicated to verify
was much reduced compared with those of the years 1974
audibility. At both distances both the playbacks and the
to 1979 (Tab.1).
jackal howls were audible to all observers, but at the 2 km
Information from local observers, verified by the
distance the broadcast was faint. Maximum audibility was
present survey, showed that no jackal groups existed
achieved during the night, when it was silent and the ani-
between Fokida and the southernmost jackal population
mals forage in the open.
in Northern Greece in Halkidiki. There was only one, but
The attracting distance was tested in an open area
unconfirmed, report of the presence of one jackal group in
where jackals had been previously located. After the stim-
Central Macedonian Province (Fig. 2).
ulation howling, jackals were observed approaching from
distances of 1.5 km down to 50 m from the calling station.
Habitat types
At each calling station the effective area for an audible
Because of distinctive differences and similarities in
response from the jackals was estimated to be between 7
the habitat types, the jackal distribution in Greece was
Population status of the Golden Jackal
147
divided in two sub-regions : Southern Greece (Pelopon-
divided into two main categories : wetlands, mainly in
nese, Fokida, Samos) and Northern Greece (Halkidiki,
Northern Greece (Fig. 3a), and other habitat types, mostly
Serres, Nestos-Vistonida, Evros) (Fig.2). Based on the
Mediterranean maquis (Fig. 3b).
predominant habitat types, the jackal presence areas were
Fig. 2. The golden jackal distribution in Greece in the 1970s and today. 1) Evros, 2) Vistonida-Nestos, 3) Serres,
4) Halkidiki, 5) Fokida, 6) Peloponnisos, 7) Samos
In Southern Greece, jackals were found in more moun-
tainous habitats than in the North (Fig.4). The highest
observed group in Northern Greece was in Halkidiki at
Arbutus unedo
250m asl, while in the south (Peloponnese) jackals were
Gramminae sp.
1%
Tamarix sp.
17%
observed even at 1050m asl. The largest population clus-
16%
ter in Greece (located in Nestos Vistonida area) as well
as other coastal wetland populations were found in areas
Salix sp.
15%
Phragmites sp.
at less than 10 m altitude.
16%
Salikornia sp.
Pinus sp.
4%
1%
Platanus
TABLE 1
Rubus sp.
orientalis
Querqus
Populus sp.
14%
1%
Estimated minimum number of jackal territories in each area in
coccifera
14%
1%
Greece
AREA
Number of
Number
Minimum
3a
jackals killed
of jackals number of
annually in
killed
jackal group
the 1974
in1980
territories
Vitis vinifera
1979 period
(2000 -2001
5%
Arbutus unedo
(min-max)
survey data)
Querqus
14%
coccifera
Peloponnese
517-1049
192
43 45
16%
Fokida
1-8
5
9 11
Platanus
Erika sp.
Samos
13 96
0
12
orientalis
14%
3%
Serres
14 63
52
1-2
Pistacea
Halkidiki
33-90
20
26
lentiscus
Vistonida- Nestos
53-122
16
53
Gramminae sp.
8%
12%
Evros
27-74
1
8 12
Pinus sp.
Rest Of Greece
34 - 254
83
1?
Olea europea
7%
17%
TOTAL
903 1332
369
152 162
Phragmites sp.
4%
The highest jackal population densities were found in
3b
the wetlands of Northeastern Greece. If we set the effec-
Fig. 3. The most frequent plant species in the jackal habitats
tive area in each survey trial at 7 to 12.5 km2 the jackal
of Northern Greece (3a) and in Southern Greece (3b).
territory densities range from 0.08 to 0.5 groups/km2. The
highest densities were detected in wetland and riparian
148
Giorgos Giannatos, Yiannis Marinos, Panagiota Maragou and Giorgos Catsadorakis
areas, namely in Vistonida Nestos and in Mornos delta
- In three cases during the survey, wolves approached
in Fokida, while the lowest were in Mediterranean maquis
the jackal-calling stations at a quick trotting pace, pre-
vegetation areas in Peloponnese.
sumably to chase off the jackals from the location.
- Dogs barked aggressively whenever jackal howling
was heard, and at close quarters some became strongly
45
agitated. In many cases dog groups (three to seven indi-
s
40
viduals) approached the calling station in a running man-
35
ner, barking in a hostile way after hearing broadcast
30
jackal howls. The reaction of unleashed dogs was to chase
25
away the jackals instantly.
20
- Although no actual observations of close fox - jackal
15
interactions were made during the survey, in our current
study area in Fokida, foxes occurred permanently only on
10
Number of positive jackal response
the fringes of the jackal territories. However, in the winter
5
we have seen a few individual foxes within jackal territo-
0
ries, and in one case a fox approached about 250 m of a
0-50
50
51-100
-10
jackal group of four (GIANNATOS pers. obs.).
101-150151-200201-250251-300301-350351-400401-450451-500501-550551-600601-650651-700701-750751-800801-850851-900901-950
951-1000
1001
Altitude classes
Southern Greece
Northern Greece
DISCUSSION
Fig. 4. Observed jackal groups per altitude intervals
The results show a very sharp decline of the golden
jackal population in South Peloponnese, where, according
Jackals and humans
to the records of the Ministry of Agriculture and the
results of our questionnaires and interviews, the jackal
According to local shepherds, very little damage to
population was thriving in the 70s and 80s. The process of
livestock is recorded in marginal mountainous areas in
disappearance in Peloponnese is ongoing since local
Peloponnese, and what does occur is caused mostly by
extinctions of jackals are still reported. The jackal popula-
isolated roaming individuals. In Peloponnese, stray dogs
tion in Peloponnese is now estimated at close to 10% of
and jackals are the only animals that could prey on small,
the population level 20-25 years ago.
hoofed livestock, since there are no wolves. The shep-
herds usually know which of the two canids is responsible
According to the survey data the jackal population in
for the losses. In areas with relatively large jackal popula-
Samos Isl. has also declined during the last decade, and
tions no complaints about livestock damage were
the species has become rare in parts of the island. How-
recorded.
ever a rapid population recovery was observed in the
island recently.
The mean distance of the observed jackal groups from
With the exception of Fokida prefecture, jackals have
the nearest human settlement was found to be 2.61 km
disappeared from all central and western Greece. The spe-
(Range : 0.1-4.5 km). (Fig.5).
cies still survives in isolated and mostly fragmented pop-
ulation clusters in a few locations in North-eastern
35
Greece. In Halkidiki, the distribution of the jackal has
also been reduced but not as sharply as in Peloponnese. In
30
s
Evros prefecture the jackals remain only in a few isolated
locations. There may be a source population in eastern
25
Evros delta, near the borders with Turkey, but its status is
unclear. The only area where the jackal population seems
20
stable or even locally increasing is Nestos-Vistonida and
the surrounding lagoons, which host the largest continu-
15
b
ous jackal sub-population in Greece. A major threat to the
10
jackal population in this area is the destruction of the
coastal marshes due to the building of summerhouses.
Number of possitive jackal response
5
The decline of the jackal can be partly attributed to the
fact that all wild canid species (namely the jackal, the fox
0
0,1
0,2
0,5
1
1,5
2
2,5
3
3,5
4
4+
and the wolf) were considered pests during the '70 and
Distance from settlements (km)
'80s, and consequently legally persecuted by every possi-
ble means, including poisoning. This poisoning campaign
Fig. 5. Jackal group sighting distances from nearest settle-
had generally a short-term effect on most of the other
ments
canids involved : both foxes and wolves quickly recov-
ered and reoccupied their areas soon after the ban of poi-
Jackals and other canids
soning in 1980 (Min. of Agriculture). However, this was
not the case for the golden jackal whose populations con-
Some observations :
tinued to decline alarmingly.
Population status of the Golden Jackal
149
Preliminary data from the field indicate that the rela-
known isolated group consisting of two sub-adults
tionship of the jackal to other canid species was that of a
responded every time that the playbacks were played.
competitor. Wolves usually dominated jackals, and jack-
More research is needed to establish the effective time
als dominated foxes. The ranges of jackals and wolves in
and conditions for repeatability.
Central and Northern Greece were almost exclusive.
According to GENOV & WASSILIEV (1989) and KRYSTUFEK
ACKNOWLEDGEMENTS
& TVRTKOVIC (1990) the wolf presence is a limiting fac-
tor for jackal distribution in the Balkan Peninsula. It
seems that jackal population density is a factor that could
We would like to thank MAVA Foundation for their generous
funding and support. We also thank the Ministry of Agriculture,
greatly influence the presence of foxes. In our current
the local Forestry Services and the personnel of the local Game
study area in Fokida, foxes were very scarce in the main
Departments for the provision of information and data. The help
jackal territory. This is a high-density jackal area with few
of the local Hunting Associations was invaluable. We are
hiding places, very different from many other areas that
indebted to the Federal Gamekeepers, the numerous anonymous
have been surveyed in Greece. In Israel where jackals and
hunters, shepherds and local people all over the study area for
foxes co-exist, the jackals may kill or displace foxes
their valuable information and guidance.
(MACDONALD, 1987). In southern Peloponnese an
increase of the fox population was observed in areas
REFERENCES
where the jackals have been decimated. No foxes existed
in Samos island (DIMITROPOULOS et al., 1998).
CREEL S. & N. M. CREEL (1996). Limitation of African Wild
Dogs by Competition with Larger Carnivores. Conserv. Biol.
Although jackal-induced damage and general distur-
10, 2 :526-538.
bance to humans was minimal, the public attitude to the
DEMETER & SPASSOV (1993). Canis aureus Linnaeus, 1758
animal seemed to be from negative to indifferent. This is
Schakal, Goldschakal. In : STUBBE M. & F. KRAPP (eds),
probably related to the official designation of the species
Handbuch der Säugetiere Europas, AULA Verlag,
as harmful in Greece until 1990. The jackals in Greece
Wiesbaden : 107-138
were found only in Mediterranean-type habitats and low-
DIMITROPOULOS A. DIMAKI M. IOANNIDIS I. (1998). The animals
land wetlands, close to human settlements. This indicates
of Samos. Contribution to island fauna. pp 180. Cultural
possible dependance on human produced food. Jackals as
Society of Samos.
opportunistic foragers have been known to subsists
GENOV & WASSILIEV (1989). Der Schakal Canis aureus Lin-
almost entirely on garbage and human waste (M
naeus, 1758 in Bulgarien. Ein Beitrag zu seiner Verbreitung
ACDON-
und Biologie. Zeit. Jagdwiss. 35 :145-150
ALD, 1979). In conclusion, the existing jackal populations
G
in Greece are discontinuous and clustered. The survival of
IANNATOS G., IOANNIDIS I. (1989) Project of fauna inventory of
Greece. The jackal (Canis aureus) in southern Greece. Uni-
these populations is dependent on the size of each cluster
versity of Athens-Biological Dept 27 pp.
and the connectivity between them.
GIANNATOS G. & I. IOANNIDIS (1991). Preliminary survey on the
distribution and status of jackal (Canis aureus L. 1758) in
The applied survey method proved to be quick, easy
southern Greece. Biol. Gallo-Hellenica 18(1) : 67-74
and inexpensive. Jackal groups were detected even in
JAEGER M, PANDIT-RANDAT K. & HAGUE-EMDADUL (1996). Sea-
areas with very thin presence, in marginal habitats, or
sonal differences in territorial behaviour by Golden Jackal in
even close to fierce competitors such as stray dogs.
Bangladesh : Howling versus confrontation. J. Mammal.
Absence of response to the acoustic stimuli cannot be
77(3) 768-775.
translated to absence of jackals. However, the 30 min
HARRINGTON H. F. & L. D. MECH (1982). An analysis of howl-
duration of the trial at each calling station seemed be
ing response parameters useful for wolf pack censuring. J.
Wildl. Mgt. 46(3) : 686-693.
enough to stimulate even the shyest animals. In two areas
KARANDINOS M. & L. PARASCH (1992). The Red Data Book of
where the jackal group territories were known, there was
Threatened Vertebrates of Greece, Hellenic Zoological Soci-
an absolute accordance between the actual number of
ety, 356 pp.
groups and the number recorded during the 2000 2001
KRYSTUFEK B., D. MURARIU & C. KURTONUR (1997). Present
acoustic survey (GIANNATOS, pers.obs.). The possibility
distribution of the Golden Jackal Canis aureus in the Bal-
for a lone animal, probably a free-ranging young, to
kans and adjacent regions. Mammal Rev. 27(2) : 109-114
respond is usually lower than that of one belonging to a
KRYSTUFEK & TVRTKOVIC (1990). Range expansion by Dalma-
family group. In known groups we noticed that sub-adults
tian jackal population in the 20th Century (Canis aureus Lin-
do not always vocalize (GIANNATOS, pers. obs.). It is also
naeus, 1758). Folia Zool. 39(4) : 291-296
ossible that responsiveness of the animals could be une-
MC CARLEY H. (1975). Long-distance vocalization of coyotes. J.
ven, since the large groups in high-density areas tend to
Mammal., 56 : 847-856.
respond more readily than small groups in low-density
MILLS M.G.L., J. M. JURITZ & W. ZUCCHINI (2001). Estimating
areas (J
the size of spotted hyena (Crocuta crocuta) populations
AEGER et al., 1996 ; MOEHLMAN, 1981). The repe-
through playback recordings allowing for non-response. Ani-
tition of trials at certain periods of time will help us to
mal Conservation 4, 335-343.
understand the situation of the existing groups in different
MACDONALD D.W. (1979). The flexible social system of the
locations (M. JAEGER, pers. comm.). Jackals could
golden jackal, Canis aureus. Behavioural Ecology and
become habituated to the sounds and thus not respond to
Sociobiology, 5 : 17-38.
the playbacks. We don't know how often the howls could
MACDONALD D.W. (1987). Running with the fox. Unwin-
be repeated while maintaining good results. In known
Hyman. London, United Kingdom.
locations in Samos the jackals did not respond when the
MOEHLMAN, P.D. (1981). Why do jackals help their parents?
playbacks were played two nights in a row. However, one
Nature. 289 : 824-825.
Belg. J. Zool., 135 (2) : 151-156
July 2005
The spatial distribution of anchovy and sardine in the
northern Aegean Sea in relation to hydrographic
regimes
Marianna Giannoulaki1,2, Athanasios Machias1, Stylianos Somarakis1,3 and Nikolaos Tsimenides2
1 Hellenic Centre for Marine Research, P.O. Box 2214, GR 710 03 Iraklion, Crete, Greece
2 University of Crete, Department of Biology, P.O. Box 2208, GR 71409 Iraklion, Crete, Greece
3 University of Patras, Department of Biology, GR 26500 Patra, Greece
Corresponding author : marianna@imbc.gr
ABSTRACT. Acoustic survey data were combined with hydrological parameters with the aim of understanding the
relationships between the spatial distribution of anchovy and sardine and environmental regimes. Acoustic and con-
current hydrological sampling was carried out in the Northern Aegean Sea (eastern Mediterranean) during June
1995 and June 1996. In order to examine hydrological parameter selection by anchovy (Engraulis encrasicolus) and
sardine (Sardina pilchardus), cumulative distribution functions were estimated. Both species were significantly
associated with areas of deeper surface and upper mixed layers, which implied an association of anchovy and sar-
dine with anticyclones. Within the range of available temperatures and bottom depths, sardine further showed a sig-
nificant affinity to warm as well as to shallow waters. These results are discussed in relation to species' life histories
and existing knowledge of oceanographic features in the surveyed area.
KEY WORDS : anchovy, sardine, Northern Aegean Sea, spatial distribution, environmental variable selection.
INTRODUCTION
and hydrographic surveys carried out in June 1995 and
June 1996 over the continental shelf.
Small pelagic species comprise a very important part of
the total world fisheries catch. About 25% of the total
MATERIAL AND METHODS
catch of the European pilchard (Sardina pilchardus (Wal-
baum, 1792)) and almost 90% of the total catch of the
Acoustic data were collected during two surveys car-
European anchovy (Engraulis encrasicolus (Linnaeus,
ried out on board the "R/V PHILIA" in June 1995 and
1758)) is taken in the Mediterranean Sea (FREON & MIS-
June 1996. The study area covered the continental shelf
UND, 1999). To improve the understanding of the mecha-
and slope waters of the Thracian Sea, Strymonikos Gulf
nisms that are responsible for the availability of these
and Thermaikos Gulf (Fig. 1). The sampling scheme was
resources, there is a need to integrate environmental
based on 30 predetermined transects and the surveyed
information with biological and fishery knowledge. Habi-
area was stratified into : Thracian Sea (Stratum I), Stry-
tat selection affects the spatial distribution of the species
monikos Gulf (Stratum II) and Thermaikos Gulf (Stratum
and is often the outcome of trade-offs between different
III). Stratum I covered 29%, stratum II 27% and stratum
agents such as heredity, predation and availability of food
III 44% of the study area. (for details see TSIMENIDES et
(FREON & MISUND, 1999).
al., 1992).
The acoustic equipment used was a Biosonic Dual
Although the Northern Aegean Sea is the most impor-
Beam 120 kHz V-Fin Echosounder (Model 120, 3o + 3o).
tant fishing ground for anchovy and sardine in the Eastern
The system was regularly calibrated using the standard
Mediterranean (STERGIOU et al., 1997), published studies
sphere method (FOOTE, 1987). The echoes were processed
on their spatial distribution in the area are generally lack-
using the software ESP v3 of Biosonics Inc. The speed of
ing and the linkage to hydrological regimes has never
the vessel was 8 nautical miles (nm) per hour. Acoustic
been studied. Previous investigations in the Northern
echoes were registered continuously along transects and
Aegean Sea mainly focused on the ichthyoplankton distri-
were integrated over one nm, which served as the Ele-
bution and abundance in relation to oceanographic condi-
mentary Distance Sampling Unit (EDSU). The sardine
tions (SOMARAKIS et al., 2002), the estimation of the size
and anchovy echoes were discriminated from those of
of the stocks using fisheries independent techniques
other fishes by the characteristic echogram shape and
(MACHIAS & SOMARAKIS 1997), and the analysis of fisher-
back-scattered energy of the schools (GIANNOULAKI et al.,
ies landings data (STERGIOU et al., 1997 and references
1999). Information on fish schools was obtained by
therein). The present study attempts to relate the spatial
means of identification hauls made with a pelagic trawl
distribution of anchovy and sardine to environmental con-
(vertical opening : 10 m, codend : 10 mm) (GIANNOULAKI
ditions, combining data from concurrent hydroacoustic
et al., 1999).
152
Mariama Giannoulaki, Athanasios Machias, Stylianos Somarakis and Nikolaos Tsimenides
Greece
Thracian Sea
Strymonikos Gulf
Samothraki
Island
Thermaikos Gulf
200 m
Fig. 1. Map of the study area (Northern Aegean Sea) showing transects (lines) and toponyms mentioned in the text.
Hydrographic sampling was performed over a grid of
tion of latitude and longitude, all the above-mentioned
144 and 147 stations in 1995 and 1996, respectively. At
variables onto the anchovy and sardine locations (multi-
each station vertical profiles of temperature and salinity
ple R-squared >0.94). A neighbourhood of 40% of the
were obtained with a SBE-19 Seacat internally recording
data (span =0.4) was used here. The number of nearest-
CTD unit (Sea Bird Electronics). To study the association
neighbours (i.e. size of the neighbourhood) usually
of fish with environmental factors, we calculated the
expressed as percentage or span of the data points, is a
depth and mean values for temperature and salinity of the
smoothing parameter. LOESS models provide much flex-
following water column layers : (a) the surface mixed
ibility because the model is fitted as a single smooth func-
layer (SML) ; (b) the upper mixed layer (UML) and (c)
tion of all the predictors.
the bottom layer (BL) (LAPRISE & PEPIN 1995). In addi-
The habitat selection of the two species was simplified
tion, (d) the mean temperature stratification (oC m-1) and
by analysis of cumulative distribution functions (CDFs)
(e) mean salinity stratification (psu m-1) for the UML
following PERRY & SMITH (1994). We examined relation-
were calculated. The SML was defined as the homogene-
ships between each species density (integrated echo per
ous layer immediately below the sea surface where tem-
nautical mile) and each one of the hydrological variables,
perature was 1oC less than that of surface waters (LAPRISE
as well as bottom depth. The CDF (in %) for all variables
& PEPIN 1995). The UML was the layer from the surface
f(t), were calculated as follows :
down to the depth where temperature was 1 oC higher
than that of bottom waters. The BL was the layer from the
L
nh A
end of the upper mixed layer down to the bottom or until
h I
200m, wherever bottom depth was greater than 200 m.
1
1 n
h= i=
h
,
1
if x < t
The breakdown of the water column into SML, UML and
f(t)=1000
where I=
hi
L
nh
BL described better the well-stratified conditions at sea
A
0
h
otherwise
and provided a rough indication of the water circulation
1
1 n
h= i=
(e.g. UML depth was deeper in anticyclonic than in
h
cyclonic areas).
and t is a level of each variable ; A is the area of stra-
h
We used the local regression model, LOESS (CLEVE-
tum h ; n is the number of EDSU in stratum h ; x is the
h
hi
LAND 1979), in a predictive mode, to interpolate as a func-
value of the variable at the EDSU i in stratum h ; L is the
The spatial distribution of anchovy and sardine
153
t
number of strata. The CDF for anchovy or sardine inte-
S= [f t() - g t()]
grated echo per mile, g(t), was calculated similarly :
t =1
for each variable. S compares average available varia-
L
nh Ah
ble to the average variable selected by anchovy or sar-
y Ihi
dine. Positive values of S indicated that anchovy or sar-
1
1 n
h= i=
h
,
1
if x < t
g(t)= 100
hi
n
where I=
dine select high values within the ranges studied (SWAIN
L
h
A
& KRAMER, 1995). We used a Kolmogorov-Smirnov type
h
0
y
otherwise
hi
of statistic to test the significance of variable selection.
1
1 n
h= i=
h
The test statistic D was defined
and y is anchovy or sardine integrated echo in EDSU i
D=max f (t) - g(t)
hi
in stratum h.
(maximum absolute vertical distance) when f(t) and
To examine variation in the parameters selection by
g(t) were the two functions compared. Significance was
anchovy or sardine, we compared CDFs of each variable,
assessed using randomisation tests (PERRY & SMITH,
f(t), and anchovy or sardine echo in relation to the corre-
1994). All statistical inferences were based on a 0.05 sig-
sponding variable g(t). We calculated parameter
nificance level.
TABLE 1
Northern Aegean Sea. The hydrological characteristics of the water column in June 1995 and June 1996. Avg.: Average values, s.d.:
standard deviation, Max: maximum value, Min: minimum value, SML: surface mixed layer, UML: upper mixed layer, BL: bottom
layer (see text for layer definition).
June 1995
June 1996
Layer
Avg.
s.d.
Max
Min
Avg
s.d.
Max
Min
Depth (m)
SML
9.15
1.86
12.51
5.08
8.23
2.05
11.63
4.61
Uml
35.51
7.45
48.17
16.93
25.55
4.70
35.83
19.59
Mean Temperature (0C)
Sml
24.30
0.58
25.06
23.01
21.93
0.86
24.47
20.00
Uml
19.57
0.64
21.38
18.13
19.04
0.44
19.89
18.04
Bl
14.38
0.41
15.47
13.74
12.86
0.24
13.58
12.31
Mean Salinity (psu)
Sml
34.66
1.11
36.07
32.46
33.89
1.19
35.33
31.05
Uml
36.55
0.88
37.97
34.65
35.43
0.93
37.07
33.86
Bl
38.52
0.22
39.01
37.75
38.24
0.22
38.64
37.67
Temperature stratification (oCm-1)
Uml
-0.31
0.07
-0.20
-0.62
-0.35
0.09
-0.22
-0.58
Salinity stratification (psu m-1)
UML
0.13
0.06
0.38
0.07
0.18
0.06
0.33
0.08
RESULTS
distributed more inshore in Strymonikos Gulf during June
1996 when compared to June 1995 (Fig. 2d). In the Ther-
maikos Gulf, anchovy distribution consisted of two major
The water column in the North Aegean Sea presented
groups, one in the inner and another one in the outer part
typical spring-to-early summer conditions. It was gener-
of the Gulf, whereas the distribution of sardine comprised
ally well stratified during both surveys (SOMARAKIS et al.,
many small clusters (Fig. 2).
2002). The upper water column as well as the bottom
layer was generally warmer and more saline in 1995 than
Analysis of the CDFs revealed positive associations of
in 1996 (Table 1). Acoustic data were used to estimate the
anchovy with SML depth, UML depth and BL tempera-
anchovy and sardine biomass in the area, which was simi-
ture at a significant level (Table 2, Fig. 3). These results
lar for the two years (EPET, 19961 ; MACHIAS & SOMAR-
were indicative of a higher probability of occurrence for
AKIS, 1997).
anchovy in water columns characterized by deeper sur-
Distribution and abundance maps of anchovy and sar-
face and upper mixed layers. Anchovy affinity to warmer
dine (Fig. 2) showed that, in the Thracian Sea, the main
waters below the thermocline (BL) was marginally signif-
concentrations of both species generally occurred
icant (p=0.049, Table 2). Sardine showed a strong posi-
between the islands of Thasos and Samothraki. High
tive relationship (p << 0.01) with SML depth, UML
numbers for both species were also recorded between the
depth, SML temperature, UML temperature and BL tem-
island of Thasos and the Athos peninsula (Strymonikos
perature (Table 2, Fig. 3). Hence, in contrast to anchovy,
Gulf), however anchovy abundance was lower and fish
sardine was clearly associated with warmer waters. More-
over sardine showed a negative relationship with bottom
depth (Table 2, Fig. 3) indicating a selection for shallow
1 EPET (1996). Development of Greek Fisheries. EPET 125, II/94, Final
waters. Salinity and stratification parameters did not
Report.
exhibit statistically significant effects (Table 2).
154
Mariama Giannoulaki, Athanasios Machias, Stylianos Somarakis and Nikolaos Tsimenides
TABLE 2
Indices of parameter selection by species. S: index of parameter selection; D: test statistic; p-value: probability of statistical signifi-
cance of parameter selection based on the randomization test described in the text. SML: surface mixed layer; UML: upper mixed
layer; BL: bottom layer.
Anchovy
Sardine
Parameters
Layer
S
D
p-value
S
D
p-value
Bottom Depth (m)
-68.63
11.26
0.629
-123.33
8.75
0.018
Depth of SML (m)
117.23
20.06
0.016
69.52
12.10
0.004
Depth of UML (m)
103.48
18.78
0.035
93.88
11.58
0.006
Temperature (oC)
Sml
169.63
16.82
0.121
211.47
20.13
0.000
Uml
43.91
8.92
0.853
74.23
12.87
0.000
Bl
131.81
17.62
0.049
193.93
23.87
0.000
Salinity (psu)
Sml
-2.75
6.70
0.992
-20.37
7.90
0.058
Uml
6.91
16.84
0.117
6.44
4.75
0.445
Bl
-11.33
13.21
0.463
15.73
8.13
0.053
Temperature stratification (oC m-1)
Uml
-77.65
11.43
0.605
-54.24
6.41
0.170
Salinity stratification (psu m-1)
Uml
-80.20
12.69
0.550
-35.59
7.32
0.105
41o
41o
A
C
39o
39o
22o
26o
22o
26o
41o
41o
B
D
39o
39o
22o
26o
22o
26o
0.0
0.2
0.4
0.6
0.8
1.0
0.0
0.1
0.3
0.4
0.6
Fig. 2. Contour maps of fish acoustic cross section (in md) in the Northern Aegean Sea. (A) Sardine distribution in June 1995, (B)
Sardine distribution in June 1996, (C) Anchovy distribution in June 1995, and (D) Anchovy distribution in June 1996.
DISCUSSION
origin onto the Samothraki plateau (SOMARAKIS et al.,
2002). Deeper surface and upper mixed layers character-
The present study showed a high concentration for both
ize the anticyclonic gyres due to the tendency of isopyc-
anchovy and sardine in the waters between the islands of
nals to move downward in down-welling areas in contrast
Thasos and Samothraki, as well as the island of Thasos
to cyclonic (up-welling) areas where the isopycnals tend
and the Athos peninsula. These areas were characterized
to move upwards (POND & PICKARD, 1983). The associa-
by the presence of two anticyclonic systems : one in the
tion of anchovy and sardine with anticyclones was shown
Samothraki plateau (the Samothraki gyre) and another
by the significant relationships with deeper SMLs and
one in the Strymonikos Gulf (SOMARAKIS et al. 2002).
UMLs (Table 2). These anticyclonic gyres are plankton
These gyres are an almost permanent feature in the area
retention areas and characterized by high concentrations
during early summer and are coupled with a cyclonic sys-
of mesozooplankton (SOMARAKIS, 1999), i.e. high food
tem located south of the island of Thasos, the overall cir-
availability for small pelagic fish. Such structures are also
culation being mainly determined by the presence of the
known to entrain fish eggs and larvae and restrict their
Limnos-Imvros stream, which carries waters of Black Sea
dispersal (HEATH, 1992). Early summer is the spawning
The spatial distribution of anchovy and sardine
155
period of anchovy in Greek waters (SOMARAKIS, 1999),
for their spawn, because of retention and the reduced off-
thus, selection by spawning adults of areas of favourable
shore dispersal (BLAXTER & HUNTER, 1982).
feeding conditions within gyres, would also be favourable
100
SML Temperature
90
Bottom Depth
80
70
60
50
% 40
30
20
10
0
10
60
110
160
210
260
310
360
410
460
510
560
610
660
20.0
20.4
20.8
21.2
21.6
22.0
22.4
22.8
23.2
23.6
24.0
24.4
24.8
Depth (m)
Temperature ( oC)
100
SML Depth
UML Temperature
90
80
70
60
50
% 40
30
20
10
0
6
6
6
6
6
6
6
6
6
0
2
4
6
8
0
2
4
6
8
0
2
4
6
8
0
2
4.
5.
6.
7.
8.
9.
10.
11.
12.
18.
18.
18.
18.
18.
19.
19.
19.
19.
19.
20.
20.
20.
20.
20.
21.
21.
Depth (m)
Temperature (oC)
100
UML Depth
BL Temperature
90
80
70
60
50
%
40
30
20
10
0
3
5
7
9
1
3
5
7
9
1
3
5
7
9
1
3
5
17
21
25
29
33
37
41
45
49
Depth (m)
12.
12.
12.
12.
13.
13.
13.
13.
13.
14.
14.
14.
14.
14.
15.
15.
15.
Temperature (oC)
Parameter
anchovy
sardine
Fig. 3. Cumulative distribution functions of bottom depth, significant hydrological parameters and anchovy/ sardine backscattering
cross-section in relation to the available values of the parameters. SML : surface mixed layer ; UML : upper mixed layer ; BL : bottom
layer.
In the Thermaikos Gulf, which is a semi-enclosed gulf,
by the species in its habitat (URSIN, 1979). Hence sar-
fish were generally distributed in many small clusters
dine`s selection for warm waters is probably related to
covering most parts of the gulf. The degree of enclosure
growth optimisation.
of an area is significantly related to higher spatial patchi-
Another significant relationship for sardine was its
ness for pelagic resources in the Greek seas, as has been
affinity to shallow waters. Inshore waters are the pre-
shown by a recent study using geostatistical techniques
ferred habitat for age-0 fish, which dominate the sardine
(GIANNOULAKI et al., 2002).
population during early summer (SARDINE, 2001).
Within the range of available temperatures, sardine was
Close association of sardine to shallow waters has also
further selective for warm waters, which was not the case
been reported for Sardinops sagax in the Southern Ben-
for anchovy. Sardine spawns during winter, whereas dur-
ing summer it is characterised by fast somatic growth and
fat deposition (SARDINE, 20012). Temperature acceler-
2 SARDINE 2001: Evaluation of the Southern Greek Sardine Stocks, No
ates growth, within the natural thermal range experienced
98/039. Final Report.
156
Mariama Giannoulaki, Athanasios Machias, Stylianos Somarakis and Nikolaos Tsimenides
guela up-welling region (BARANGE & HAMPTON, 1997)
LAPRISE, R. & P. PEPIN (1995). Factors influencing the spatio-
and Sardina pilchardus pilchardus in the Bay of Biscay
temporal occurrence of fish eggs and larvae in a northern,
(SCALABRIN & MASSE, 1993).
physically dynamic coastal environment. Mar. Ecol. Prog.
Ser., 122 : 73-92.
The present study is the first attempt to relate the spa-
MACHIAS, A. & S. SOMARAKIS (1997). The state of anchovy
tial distribution of anchovy and sardine to hydrology in
stocks. Fishing News, 190 : 40-45.
the Northern Aegean Sea. It highlights the significance of
MASSE, J., C. KOUTSIKOPOULOS & W. PATTY (1996). The struc-
environmental regimes in determining population pat-
ture and spatial distribution of pelagic fish schools in multi-
terns in space. Further investigations on the spatial pat-
species clusters : an acoustic study. ICES J. Mar. Sci., 53(2) :
terns of these planktivorous fish should address the effect
155-160.
of food availability, which controls both their growth and
PERRY, R.I. & S.J. SMITH (1994). Identifying habitat associations
reproduction (F
of marine fishes using survey data : An application to the
REON & MISUND, 1999).
Northwest Atlantic. Can. J. Fish. Aquat. Sci., 51 : 589-602.
POND, S. & G.L. PICKARD (1983). Introductory Dynamical Oce-
REFERENCES
anography. 2nd Ed., Pergamon Press, Oxford.
SCALABRIN, C. & J. MASSE (1993). Acoustic detection of the
B
spatial and temporal distribution of fish shoals in the Bay of
ARANGE, M. & I. HAMPTON (1997). Spatial structure of co-
occurring anchovy and sardine populations from acoustic
Biscay. Aquat. Living Resour., 6 :269-283.
data : implications for survey design. Fish. Oceanogr., 6(2) :
SOMARAKIS, S. (1999). Ichthyoplankton of the Northeastern
94-108.
Aegean Sea with emphasis on anchovy, Engraulis encrasico-
B
lus (Linnaeus, 1758) (June 1993, 1994, 1995, 1996). Ph.D.
LAXTER, J.H.S. & J. HUNTER (1982). The biology of the Clupe-
oid fishes. Adv. Mar. Biol., 20 : 1-223.
Thesis, University of Crete.
S
C
OMARAKIS, S., P. DRAKOPOULOS & V. FILIPPOU (2002). Distribu-
LEVELAND, W.S. (1979). Robust locally weighted regression
tion and abundance of larval fishes in the northern Aegean
and smoothing scatterplots. J. Amer. Statistical Assoc.,
Sea-eastern Mediterranean- in relation to early summer oce-
74(368) : 829-836.
anographic conditions. J. Plankton Res., 24(4) : 339-357.
FOOTE, K.G. (1987). Fish target strengths for use in echo integra-
STERGIOU, K.I., E.D. CHRISTOU, D. GEORGOPOULOS, A.ZENETOS
tor surveys. J. Acoust. Soc. Am., 82(3) : 981-987.
& C. SOUVERMEZOGLOU (1997). The Hellenic Seas : Physics,
FREON, P. & O.A. MISUND (1999). Dynamics of Pelagic Fish
chemistry, biology and fisheries. Oceanogr. Mar. Biol., Ann.
Distribution and Behaviour : Effects on Fisheries and Stock
Rev., 35 : 415-538.
Assessment. Fishing New Books, Oxford.
SWAIN, D.P. & D.L. KRAMER (1995). Annual variation in tem-
GIANNOULAKI, M., A. MACHIAS & N. TSIMENIDES (1999). Ambi-
perature selection by Atlantic cod Gadus morhua in the
ent luminance and vertical migration of the sardine Sardina
southern Gulf of St. Lawrence, Canada, and its relation to
pilchardus. Mar. Ecol. Prog. Ser., 178 : 29-38.
population size. Mar. Ecol. Prog. Ser., 116 : 11-23.
GIANNOULAKI, M., A. MACHIAS, C. KOUTSIKOPOULOS, S. SOMAR-
TSIMENIDES, N., G. BAZIGOS, S. GEORGAKARAKOS & A. KAPAN-
AKIS, J. HARALAMBOUS & N. TSIMENIDES (2002). Spatial
TAGAKIS (1992). Distribution of acoustic pelagic fish popula-
structure of pelagic fish in Greek waters determined by
tions in the Northern Aegean Sea. Proc World Fish Cong, 5 :
acoustics. Book of Abstracts of the 6th ICES Symp.
33-42.
Montpellier :120-121.
URSIN, E. (1979). Principles of Growth in Fishes. In MILLER P.J.
HEATH, M.R. (1992). Field investigations of the early life stages
(ed) "Fish Phenology : anabolic adaptiveness in teleosts".
of marine fish. Adv. Mar. Biol., 28 :1-174.
Symp. Zool. Soc. Lond., 44 : 63-87.
Belg. J. Zool., 135 (2) : 157-163
July 2005
PCBs and organochlorine pesticide residues in eggs of
threatened colonial charadriiform species (Aves,
Charadriiformes) from wetlands of international impor-
tance in northeastern Greece
Vassilis Goutner1, Triantafyllos Albanis2 and Ioannis Konstantinou2
1 Department of Zoology, Aristotelian University of Thessaloniki, GR-54124, Thessaloniki, Macedonia, Greece
2 Department of Chemistry, University of Ioannina, GR-45110, Epirus, Greece
Corresponding author : Vassilis Goutner, e-mail : vgoutner@bio.auth.gr
ABSTRACT. The levels of eight PCB congeners (IUPAC 8, 20, 28, 52, 101, 118, 138 and 180) and 13 organochlo-
rine pesticides (a-HCH, b-HCH, Lindane, Heptachlor, Heptachlor epoxide, Aldrin, Dieldrin, Endrin, 2,4'-DDT,
2,4'-DDD, 4,4'-DDT 4,4'-DDD and 4,4'-DDE) were measured in eggs of Mediterranean gulls (Larus melanocepha-
lus) (Lm), avocets (Recurvirostra avosetta) (Ra) and common terns (Sterna hirundo) (Sh) collected at the Evros
Delta (Lm, Ra), Porto Lagos (Lm) and Axios Delta (Lm, Sh), north-eastern Greece in 1997. All pollutants were
detected in all areas and species, with the exception of Dieldrin in the Mediterranean gull. Percent levels of higher
chlorinated PCB congeners (IUPAC 118, 138 and 180) were greater than other compounds in all species and areas,
probably due to their bioaccumulative properties. Only the median concentrations of PCB 28 differed significantly
among areas in Mediterranean gull eggs. Significant differences between Mediterranean gulls and avocets (Evros)
were found with regard to PCB 138 and PCB 180, whereas differences between Mediterranean gulls and common
terns (Axios) were found in all PCBs except PCB 8 and PCB 20. These differences were due to the different diets of
the species studied. Maximum pesticide concentrations in all samples were below 50 ppb, except for ß-HCH and
2,4'-DDD, both of which predominated among all compounds in all areas and species. The same trend has been
found in other waterbird species in Greece, suggesting a particular pollution pattern in the region. Significant differ-
ences in the median concentrations of most pesticides were found among areas in the Mediterranean gull. Such dif-
ferences were also found between Mediterranean gulls and avocets and between Mediterranean gulls and common
terns, again due to different feeding habits. Our results suggest that, in the wetlands of northeastern Greece, agro-
chemical sources dominate over industrial pollution. Pollutants still persist in Greek wetlands, but their levels are
too low to have any adverse biological effect on the species studied.
KEY WORDS : Polychlorinated biphenyls, organochlorine pesticides, Larus melanocephalus, Recurvirostra avosetta,
Sterna hirundo, Greek wetlands.
INTRODUCTION
in higher-level consumers (TANABE et al., 1987 ; HARDING
et al., 1997).
In Greece, pesticides and PCBs were banned before the
Polychlorinated biphenyls (PCBs) and organochlorine
mid-seventies, but studies have indicated that both groups
pesticides (hereafter pesticides) are two groups of sub-
persist in the Greek environment (ALBANIS et al., 1994 ;
stances that have different chemical structure and applica-
KONSTANTINOU et al., 2000 ; GOUTNER et al., 2001). Mon-
tions. PCBs were extensively used as plasticizers, as addi-
itoring and comparative studies in multiple areas using
tives in hydraulic and dielectric fluids in industry and as
higher trophic level receptors are scarce. However, Greek
fire retardants. Numerous organochlorine compounds
wetlands are of particular interest for such studies, as they
have been used as pesticides. Nevertheless, both groups
a) support in their vicinity considerable human popula-
of chemicals have high toxicity and persistence in the
tions, who consume local resources such as water and fish
environment. Studies have shown that some compounds
and b) they also provide refuge to internationally impor-
of both groups can negatively affect wildlife reproduction
tant populations of wildlife, especially birds.
and population levels and/or (particularly PCBs) cause
The levels of organochlorines in seabird eggs reflect
various embryonic deformities and mortality (GILBERT-
the diet of the female and pollutant levels in body
SON et al., 1991 ; YAMASHITA et al., 1993 ; CUSTER et al.,
reserves, thus constituting a useful indicator of environ-
1999). Some of these substances can also pose threats to
mental contamination (PEARCE et al., 1989). Waterbirds
humans, especially at high levels, but also due to back-
are top predators in aquatic environments, and, especially
ground exposure (LONGNECKER et al., 1997). Due to their
fish-eating species, are suitable bioindicators (SCHAREN-
lipophilic structure, both groups tend to bioaccumulate
BERG, 1991). Nevertheless, due to the complexity of the
along food chains, and thus reach greater concentrations
food chains and particularities in the response of each
158
Vassilis Goutner, Triantafyllos Albanis and Ioannis Konstantinou
species to these chemicals, pollution studies must con-
Delta) and common tern (Sterna hirundo L. 1758) (Axios
tinue.
Delta) (Fig. 1). These species represent different links in
The aims of this study were : a) to investigate the
the food chains of wetlands, as they have different diets.
occurrence of PCBs and pesticides in the eggs of some
Eggs collected were either laid outside nests or from nests
threatened waterbirds that represent different links in the
that were destroyed and abandoned by breeding birds due
food chain of Greek wetlands ; b) to find out whether
to flooding. Flooding may happen to these species' nests
these chemicals occur in levels threatening the survival of
because they are made at close proximity to water. Eggs
these species ; c) to obtain indirect information about the
were opened in the laboratory on the day of collection and
pollution of these birds' habitats, especially as all wet-
their contents were placed in chemically cleaned jars and
lands where we collected data are of international impor-
deep frozen until analysis.
tance and protected by the Ramsar Convention.
The following eight PCB congeners were analysed :
PCB 8, 20, 28, 52, 101, 118, 138, 180. Of these conge-
MATERIAL AND METHODS
ners, five (PCB 28, 52, 101, 138, 180) belong to the group
known as "target" or "indicator" PCBs (BACHOUR et al.,
This study was carried out in wetlands of northeastern
1998). The organochlorine pesticides analysed in this
Greece (Fig. 1). The Evros Delta, at the Greek-Turkish
study were -HCH, ß-HCH, Lindane, Heptachlor, Hep-
border, is the easternmost Greek wetland (40o47'N,
tachlor epoxide, Aldrin, Dieldrin, Endrin, 2,4'-DDT, 2,4'-
26o05'E), extending over 11,000 ha, and with a great a
DDD, 4,4'-DDT 4,4'-DDD 4,4'-DDE.
variety of habitats (BABALONAS, 1980). The river Evros,
PCB-standards were obtained from Dr. Ehrensdorfer
originating in Bulgaria, is the border between Greece and
GmbH laboratory in concentrations of 10 mg/ml. Supelco
Turkey for about 200 km and receives considerable
No. 4-9151 organochlorine pesticides mixture standard in
amounts of transboundary pollution. Porto Lagos (40o01'
isooctane was used in concentrations of mg/ml for the
N, 25o08' E), is an area in a wide wetland complex
chromatographic analysis. All solvents used (hexane, ace-
including the shallow, polluted, brackish Lake Vistonis
tone, petroleum ether), were pesticide residue analysis
and multifarious coastal lagoons. The Axios Delta
grade, purchased from Pestiscan (Labscan Ltd, Dublin,
(40o30'N, 22o53'E) is part of an extensive wetland com-
Ireland). Florisil (50-100 mesh) and sodium sulfate (pro-
plex, situated at the west coast of Thermaikos Gulf
analysis) were from Merck (Darmstadt, Germany).
(KAZANTZIDIS et. al., 1997). This river originates in the
The analytical procedures and chromatographic condi-
former Yugoslavia and suffers considerable pollution,
tions used have been described in detail in other recent
probably being the most highly polluted water body of
papers of the authors (KONSTANTINOU et al., 2000 ; GOUT-
northeastern Greece (FYTIANOS et al., 1986). All three
NER et al., 2001). Here we provide a brief outline of the
wetlands are of international importance and protected by
respective methods. An aliquot of 5-10 g of homogenized
the Ramsar convention.
egg contents was extracted using sodium sulphate and
petroleum ether (1 :1) mixture.The centrifuged superna-
tant was evaporated in a rotary evaporator to 10 ml and
lipids were then removed using sulfuric acid. The clean-
up was completed by adsorption chromatography, eluting
the colorless layer through a chromatography glass col-
umn. All solvents used for packing the column were
degassed in sonication bath. The purified sample was
evaporated in a rotary evaporator to ca. 5 ml and in gentle
N stream at 35°C to ca. 0.5 ml. Then samples were
2
stored in silanized vials in a refrigerator (-20°C). Mean
recoveries and method detection limits for each congener
and compound are given in KONSTANTINOU et al. (2000).
A Shimadzu 14B gas chromatograph equipped with a
Ni 63 electron capture detector (ECD) was used for the
organochlorine residue analysis. Helium was used as the
carrier and nitrogen as the make-up gas. Pure reference
standard solutions were used for instrument calibration,
recovery, quantification and confirmation. The confirma-
tion of organochlorine residues was performed by using a
GC-MSD, QP 5000 Shimadzu equipped with DB-5 capil-
lary column.
Fig. 1. Map indicating the areas and species studied within the
Concentrations of pollutants were not normally distrib-
context of Greece.
uted, thus the median of each pollutant, and the median
total concentrations of PCBs (hereafter PCBs) and pesti-
Colonies were visited during the egg-laying period in
cides (pesticides) were compared. We used the Mann-
April and May 1997. Under licence, we collected eggs of
Whitney U test to compare concentrations between spe-
the Mediterranean gull (Larus melanocephalus Tem-
cies in the Evros and Axios Deltas and Kruskal-Wallis 2
minck 1820) (from the Evros and Axios Deltas and Porto
test to compare concentrations in Mediterranean gull eggs
Lagos), avocet (Recusvirostra avosetta L. 1758) (Evros
from the three areas. We calculated the ratio pesticides/
Organochlorine residues in Greek wetlands
159
S
P
n.s.
n.s.
0.037
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
0.009
-
0.020
n.s.
< 0.001
0.009
0.029
0.009
n.s.
n.s.
0.003
2 x
a
nocephalus
a
llis
ALL WETLAND
L. mel
K-W
1.34
2.87
6.59
0.72
1.34
2.57
4.54
8.97
4.99
0.19
2.94
4.21
9.40
-
7.79
3.64
14.14
9.34
7.08
9.55
1.57
2.18
1
1.68
)
Max
3
3
6
3
17
41
42
16
7
8
1
1
15
1
1
< d. l.
9
1
0
8
7
3
4
3
7
3
(N = 13)
d. l.
d. l.
d. l.
d. l.
d. l.
d. l.
Min
< d. l.
<
<
<
<
< d. l.
< d. l.
<
3
< d. l.
2
2
< d. l.
< d. l.
< d. l.
< d. l.
< d. l.
<
3
< d. l.
< d. l.
< d. l.
t significant
l.
: no
O LAGOS (PL
T
o
cephalus
d. l.
d. l.
d. l.
d. l.
d. l.
d. l.
d. l.
d.
d. l.
d. l.
d. l.
R
Median
<
1
2
2
6
<
21
4
43
<
8
4
<
<
<
<
<
1
24
<
<
<
PO
l.
s); n.s.
L. melan
d. l.
d. l.
d. l.
d.
d. l.
Mean
1
1
2
2
6
7
21
5
45
<
7
6
<
<
<
1
<
5421
2
26
1
1
2
6314
mit
ion li
P
n.s.
n.s.
0.002
0.005
< 0.001
< 0.001
< 0.001
0.002
< 0.001
< 0.001
n.s.
< 0.001
n.s.
0.023
0.002
n.s.
< 0.001
0.020
0.016
n.s.
n.s.
0.001
n.s.
ct
a
t
i
s
t
i
c
s
St
Z
-2.50
-
1.33
-3.16
-2.83
-
4.08
-
3.30
-3.52
-
3.06
-3.66
-
3.49
-1.40
-
3.52
-
0.23
-
2.27
-
3.09
-
0.70
-
3.34
-
2.33
-2.42
-
0.02
-
0.86
-
3.27
1.73
below dete
Max
< d. l.
2
22
10
1
2
6
9
68
2
7
173
3
243
4
1
1
4
1
1
9
7
700
2
8
7
l.:
(N = 13)
d. l.
d. l.
d. l.
d. l.
d. l.
d. l.
Min
< d. l.
<
< d. l.
<
4
2
14
7
52
< d. l.
24
< d. l.
< d. l.
< d. l.
<
< d. l.
6
<
105
<
< d. l.
<
s
(< d.
A (AD)
rundo
T
d. l.
d. l.
S. hi
Median
< d. l.
1
9
5
6
26
25
1
2
85
1
127
<
< d. l.
< d. l.
2
< d. l.
1
2
3
350
1
<
5
549-
d. l.
d. l.
Mean
<
1
1
0
4
7
30
30
1
3
95
1
122
1
< d. l.
< d. l.
2
<
1
2
3
342
1
1
4
5
Greek wetland
AXIOS DEL
Max
3
2
4
3
9
66
36
1
132
47
149
< d. l.
< d. l.
< d. l.
6
2
9
7
7
1
1
3
< d. l.
9
5
7
1
E
gs from
(N = 15)
L
d. l.
d. l.
d. l.
d. l.
d. l.
B
eg
Min
< d. l.
< d. l.
<
<
<
< d. l.
< d. l.
4
< d. l.
< d. l.
< d. l.
< d. l.
< d. l.
<
< d. l.
<
9
< d. l.
< d. l.
< d. l.
1
TA
cephalus
d. l.
d. l.
Median
< d. l.
< d. l.
1
1
1
4
1
1
32
<
85
< d. l.
< d. l.
< d. l.
1
< d. l.
1
76
< d. l.
< d. l.
<
10
aradriiform
L. melano
d. l.
d. l.
d. l.
Mean
1
<
2
1
2
1
1
12
7313
35
3
85
< d. l.
<
< d. l.
1
<
7314
1
186
1
< d. l.
1
16
1
P
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
< 0.001
< 0.001
< 0.001
0.055
0.008
0.034
n.s.
0.012
0.051
n.s.
0.01
0.014
0.005
n.s.
< 0.001
0.008
0.023
a
t
i
s
t
i
c
s
St
Z
-
0.22
-
0.03
-0.83
-
1.00
1.20
-0.90
-
4.60
-
4.52
-3.60
-
1.92
-2.63
-
2.13
-
0.18
-2.51
-
1.95
-
1.13
-
2.53
-
2.47
-2.83
-
0.50
-
5.06
-2.64
-2.27
5
4
6
1
s
(ppb wet weight) in ch
Max
4
3
1
1
1
1
3
54
1
277
2
1
20
8
1
5
694
6
44
44
d. l.
d. l.
d. l.
d. l.
d. l.
d. l.
d. l.
d. l.
Min
< d. l.
<
<
<
<
1
1
< d. l.
16
< d. l.
< d. l.
< d. l.
<
< d. l.
<
1
<
<
1
A (EV)
n
c
entration
T
L
d. l.
co
E
Median
< d. l.
1
4
6
1
25
< d. l.
61
< d. l.
< d. l.
<
1
< d. l.
1
266
1
3
1
3
R. avosetta (N = 20)
d. l.
d. l.
d. l.
EVROS D
Mean
1
1
4
5214
2213-
6
6531
1
26
<
76
1
<
1
2
<
7511
1
252
1
3211
5
1
6
pesticide
Max
8
3
36
6
5
28
1
5
33
152
7
774
9
2
< d. l.
7
3
3
3
7
735
4
1
1
1
3
3
s
(N = 15)
u
.
l
.
.
l
.
.
l
.
d. l.
d. l.
d
d
d. l.
d
Min
< d. l.
<
<
<
<
<
71
1
19
< d. l.
3
< d. l.
< d. l.
< d. l.
< d. l.
< d. l.
<
< d. l.
1
1
< d. l.
< d. l.
< d. l.
1
r
ganochlorine
d. l.
d. l.
d. l.
d. l.
d. l.
Median
<
1
3
2
1
7
2
0
8
54
<
1
1
3
<
< d. l.
< d. l.
<
< d. l.
1
1
2
2
5
1
< d. l.
<
4
L. melanocephal
B and o
d. l.
Mean
1
1
6
2
1
10
2
6
10
57
1
203
1
< d. l.
< d. l.
1
<
1
2
2
1
1
2
1
< d. l.
2
8
PC
p
o
x
.
CBs
es
0
8
P
5
2
1
0
1
18
1
3
8
80
B
B
B
C
C
C
e
p
t
a
c
h
l
o
r
e
PCBs
PCB8
PCB2
PCB2
P
P
PCB1
P
PCB1
PCBs
Pesticid
-BHC
-BHC
Lindane
Aldrin
Dieldrin
Endrin
Heptachlor
H
4,4'-DDE
2,4'-DDD
2,4'-DDT
4,4'-DDD
4,4'-DDT
OCs/
160
Vassilis Goutner, Triantafyllos Albanis and Ioannis Konstantinou
/PCBs in samples as a measure of agrochemical vs.
were found in the Evros Delta. The maximum levels of
industrial pollution (FOSSI et al., 1984 ; PASTOR et al.,
PCB 118 were found in the Axios Delta, whereas of con-
1995b) and then we compared the median values as previ-
geners 20 and 101 at Porto Lagos.
ously specified. Separate cluster analyses for PCB and
The proportions of congeners with a higher substitution
pesticide percentage levels were used to evaluate differ-
pattern (118 and above) predominated in all species and
ences in pollution patterns among the areas studied. As
areas, but some of the "lower" congeners occurred in rela-
linkage rule we used the "single linkage", where the dis-
tively high concentrations, mostly in avocet eggs less so
tance between two clusters is determined by the distance
in common tern and Mediterranean gull eggs, resulting in
of the two closest objects (nearest neighbors) in the differ-
characteristic fingerprints (Fig. 2).
ent clusters. This rule will string objects together to form
clusters, and the resulting clusters tend to represent long
Cluster analysis separated the pollution pattern of
chains. As distance measure we used the "Euclidean dis-
avocet eggs from all other samples. Another group
tance" that is the geometric distance in the multidimen-
included both species sampled in the Axios Delta, while a
sional space. Euclidean distances are computed from raw
third joined the pollution patterns of Mediterranean gulls
data, and this has certain advantages, as the distance
from the Evros Delta and Porto Lagos (Fig. 3).
between any two objects is not affected by the addition of
new objects, which may be outliers, to the analysis (STA-
TISTICA, 1999).
L. melan., EV
L. melan., PL
L. melan., AX
50
S. hirundo, AX
45
40
R. avosetta, EV
35
PCB 138
30
PCB 118
6
8
10
12
14
16
18
20
22
25
PCB 180
Linkage distance
20
PCB 101
% PCBs
15
Fig. 3. Cluster indicating the PCB pollution patterns of the
PCB 52
10
species studied in the three wetlands. Euclidean distance meas-
PCB 28
5
ures and single linkage rule were used.
PCB 20
0
PCB 8
Organochlorine pesticides
Of the 13 compounds analysed in bird eggs, Dieldrin
L. mel., EVROS
L. mel., AXIOS
was below detection limits in Mediterranean gulls in all
L. mel., P. LAGOS
wetlands, but was detectable in the other two species.
R. avosetta EVROS
S. hirundo, AXIOS
Median concentrations of most compounds (except
Fig. 2. Fingerprint of PCB congeners (% of total concentra-
Aldrin, Heptachlor and 2,4'-DDT) differed significantly
tion in each egg sample) detected in the charadriiform species
between Mediterranean gulls and avocets in the Evros
studied in three Greek wetlands.
Delta (Table 1). Notably, of all samples, the maximum
concentrations of Dieldrin, 2,4'-DDT, 4,4'-DDD and 4,4'-
DDT were found in avocets. In the Axios Delta, the
RESULTS
median concentrations of most compounds (except ß-
HCH, Aldrin, Heptachlor 2,4'-DDT and 4,4'-DDD) were
Polychlorinated biphenyls
significantly different between Mediterranean gulls and
With the exception of PCB 8, which was not detected
common terns. The median concentrations of Aldrin,
in common tern eggs in the Axios Delta, all other conge-
Endrin, Heptachlor epoxide, 4,4'-DDE, 2,4'-DDD and
ners analysed were detected in all species' eggs. In the
2,4'-DDT differed significantly among Mediterranean
Evros Delta significant differences were found only in the
gull eggs from the three different wetlands (Table 1). The
median concentrations of PCB congeners 138 and 180
maximum concentrations of six organochlorines, namely
between Mediterranean gull and avocet egg samples, due
ß-HCH, Lindane, Aldrin, Heptachlor, 2,4'-DDD and 4,4'-
to higher concentrations in the gull eggs (Table 1). In con-
DDT, were found in the Evros Delta, whereas maximum
trast, in the Axios Delta, the median concentrations of all
concentrations of -HCH and Heptachlor epoxide were
congeners, except 8 and 20, were significantly different
found in the Axios Delta, and maximum concentrations of
between Mediterranean gull and common tern egg sam-
Endrin, 4,4'-DDE, 2,4'-DDT and 4,4'-DDD were meas-
ples. In this case, the concentrations of all congeners were
ured at Porto Lagos.
higher in the common tern. The only congener with con-
Of all compounds, the proportions of ß-HCH and 2,4'-
centrations differing significantly among Mediterranean
DDD clearly predominated in all areas and in all three
gull eggs from the three wetlands was PCB 28, showing
species studied, resulting in a characteristic fingerprint. In
highest levels in the Evros Delta. Of eight congeners ana-
addition, levels of Heptachlor epoxide were higher than
lysed, the maximum levels of PCB 8, 28, 52, 138 and 180
Heptachlor (Fig. 4).
Organochlorine residues in Greek wetlands
161
tution pattern (METCALFE & METCALFE, 1997). Congeners
118, 138, 180 have also been found in high concentrations
80
in larids' eggs in other areas of the Mediterranean
70
(FOCARDI et al., 1988 ; PASTOR et al., 1995b).
60
The differences in median congener concentrations
ines
50
detected between Mediterranean gulls and avocets in the
40
Evros Delta, and especially between Mediterranean gulls
r
ganochlor
30
and common terns in the Axios Delta, were probably due
% O
20
to the different feeding habits of the species involved.
S. hirundo, AXIOS
Avocets are lower in the food chain than larids feeding
10
R. avosetta EVROS
mainly on invertebrates (GOUTNER, 1985 ; FOCARDI et al.,
0
L. mel., P. LAGOS
C
C
L. mel., AXIOS
1988 ; DENKER et al., 1994). The common tern is mainly
H
H
-B
n
-B
L. mel., EVROS
ndane
d
r
i
n
o
r
de
piscivorous, whereas the Mediterranean gull's diet varies
Li
Al
e
l
d
r
i
n
Di
Endri
achl
-
DDE
e
pt
-
DDT
greatly among years and areas. It is mainly composed of
4
H
.
epoxi
-
DDT
4,
4
-
DDD
-
DDD
e
pt
2,
4
4
4
4,
4,
insects and fish (GOUTNER, 1986), but may also include
H
2,
Fig. 4. Fingerprint of organochlorine pesticides (% of total
considerable amounts of plant material (GOUTNER, 1994).
concentration in each egg sample) detected in the charadriiform
The similarity in PCB pollution of Mediterranean gull
species studied in three Greek wetlands.
eggs from all study areas suggests dietary similarities dur-
ing the study.
Cluster analysis distinguished two groups : one joined
The pattern of pollution found by the cluster analysis,
the pollution patterns of Mediterranean gulls from the
that is the grouping of the Axios Delta samples as a dis-
Evros Delta and Porto Lagos, while the other connected
tinct cluster from that of the Mediterranean gull samples
common terns and avocets, which were separate from the
from the eastern part of the study area, together, may sug-
Mediterranean gulls of the Axios Delta (Fig. 5).
gest different historical patterns of management regime of
PCBs in the areas studied. The sources of PCB pollution
at the Axios Delta have been transboundary and of
municipal origin (LARSEN & FYTIANOS, 1989), while the
L. melan., EV
other areas' pollutant sources are unknown at present.
To compare the PCB levels found in this study with
L. melan., PL
results of other studies, we multiplied by two the sum of
PCB concentrations in the eggs of the three species sam-
L. melan., AX
pled (DIRKSEN et al., 1995). In the avocet, the mean
(median) concentration multiplied by two was 51 (50)
R. avosetta, EV
ppb, in the common tern 189 (170) ppb, and in the Medi-
terranean gull 114 (109) ppb. In the Great Lakes' Herring
S. hirundo, AX
Gulls (Larus argentatus Pontoppidan 1763), concentra-
tions that have been associated with reduced hatching
0
5
10
15
20
25
30
35
40
45
success are generally higher than 70 ppm (GILMAN et al.,
Linkage distance
1977 ; WESELOH et al., 1979). In the Great Lakes' Double-
crested Cormorants, Phalacrocorax auritus (Lesson
Fig. 5. Cluster indicating the organochlorine pollution patterns
1831), total PCB means of c. 4 to 7 ppm were associated
of the species studied in the three wetlands. Eucledian distance
with live-deformities (hard tissue malformations, YAMAS-
measures and single linkage rule were used.
HITA et al., 1993), whereas in Massachusets, USA, total
PCB means of 1.4-6.0 ppm were not associated with
The medians of the ratio Spesticides/SPCBs varied
adverse biological effects in the common tern (NISBET &
from 2.62 (Mediterranean gull, P. Lagos) to 13.49
REYNOLDS, 1984). Consequently, the contaminant levels
(avocet, Evros Delta). The difference of the medians of
found in this study seem to pose no threat to the popula-
this ratio was significant between Mediterranean gulls
tions of the waterbirds studied.
and avocets and also among Mediterranean gulls from all
areas (Table 1). Spearman Rank Correlations between
Although pesticides (with the exception of Lindane)
pesticides and PCBs for Mediterranean gulls (pairs
were banned in Greece in 1972 (ALBANIS et al., 1994),
between areas), for Mediterranean gull and avocet, and
most of them were detected in egg samples in our areas,
Mediterranean gull and common tern were all statistically
though in low levels. The occurrence of pesticides in bird
insignificant.
eggs seems also to be dependent on their feeding habits
(FASOLA et al., 1987). Nevertheless, the differences in
median concentrations we detected between species in the
DISCUSSION
same area or in the same species among areas, can only in
part be attributed to different feeding habits. We suppose
Of PCBs detected in our samples, some mono- and di-
that Dieldrin and probably the other drins found in avocet
ortho coplanar congeners such as 28, 118, 138, 180 were
and common tern eggs are accumulated during wintering
the most elevated in all species and areas. These conge-
or migration, as these species follow the eastern flyway to
ners exhibit considerable bioaccumulation patterns and
African wintering quarters. In the Axios Delta, drins were
are persistent in the environment because of their substi-
also found in eggs of other distant migrants, such as the
162
Vassilis Goutner, Triantafyllos Albanis and Ioannis Konstantinou
little tern (Sterna albifrons Pallas 1764) and the Squacco
species. Predominance of ß-HCH and 2,4-DDD' in all
heron (Ardeola ralloides Scopoli 1769) (ALBANIS et al.,
species' eggs and also in others studied in Greece (P.
1996 ; GOUTNER et al., 1997).
carbo, L. audouinii), suggests a particular pattern of agro-
The elevated amounts of 2,4'-DDD in comparison to
chemical pollution in this region.
4,4'-DDE are probably due to its presence in zooplankton
and in the water column. Zooplankton possibly acquires
ACKNOWLEDGEMENTS
DDTs from sediments or from the water column, where
the DDD form constitutes the major fraction of DDTs
We are grateful to K. Poirazidis and S. Kazantzidis for aid in
(STRANBERG et al., 1998). Elevated 2,4'-DDD levels may
the field. Dr. G. Papakostas checked the English of the manu-
indicate that this compound was a major constituent in a
script.
technical mixture used in the region. An important find-
ing is that the characteristic similarity of pesticide finger-
REFERENCES
prints in all areas and species was also found in previous
studies in Greece involving the cormorant, (Phalacroc-
ALBANIS, T. A., T. G. DANIS & M. K. KOURGIA (1994). Transpor-
orax carbo (L. 1758) and Audouin's gull (Larus audoui-
tation of pesticides in estuaries of the Axios, Loudias and
nii Payraudeau 1826) (KONSTANTINOU et al., 2000 ;
Aliakmon rivers (Thermaikos Gulf), Greece. Sci. Total Envi-
GOUTNER et al., 2001). These suggest a particular pattern
ron., 156 : 11-22.
of organochlorine pesticide pollution in Greece.
ALBANIS, T. A., D. HELA, G. PAPAKOSTAS & V. GOUTNER (1996).
Concentration and bioaccumulation of organochlorine pesti-
The higher levels of ß-HCH in all egg samples were
cide residues in herons and their prey, in wetlands of Ther-
probably due to the relatively high stability of this
maikos Gulf, Macedonia, Greece. Sci. Total Environ., 182 :
compound against metabolism (OXYNOS et al., 1993).
11-19.
Lindane is still used as seed and soil insecticide in various
BABALONAS, D. (1980). Vegetationseinheiten und Vegetation-
cultivations. Lindane levels were lower than those
skartierung in fem Mundungsgebiet des Flusses Ewros. Fed-
reported in waterbids in other studies, but ß-HCH levels
des Rep., 91 : 615-627.
(where analysed) were generally higher (FOSSI et al.,
BACHOUR, G., K. FAILING, S. GEORGII, I. ELMADFA & H. BRUNN
1984 ; F
(1998). Species and organ dependence of PCB contamina-
ASOLA et al., 1998). Lindane is not harmful to
birds, in contrast to Heptachlor and especially its
tion in fish, foxes, roe deed and humans. Arch. Environ.
Contam. Toxicol., 35 : 666-673.
metabolite Heptachlor epoxide, which are lethal for birds
BLUS, L. J. (1984). DDE in bird eggs : comparison of two meth-
in concentrations 9 ppm (BLUS et al., 1985).
ods for estimating critical levels. Wilson Bull., 96 : 268-276.
Concentrations found in our egg samples did not seem to
BLUS, L. J., C. J HENNY & A. J KRYNITSKY (1985). The effects
pose any threat to the birds studied. DDE is a compound
of heptachlor and lindane on birds, Columbia Basin, Oregon
that can lower the breeding productivity of waterbird pop-
and Washington, 1976-1981. Sci. Total Environ., 46 : 73-81.
ulations by reducing eggshell thickness (BLUS, 1984 ;
CUSTER, T. W., C. M. CUSTER, R. K. HINES, S.GUTREUTER, K. L.
CUSTER et al., 1999). Levels of DDE that can affect egg-
STROMBORG, P. D. ALLEN & M. J. MELANCON (1999). Orga-
shell thickness in the common tern are beyond 4 ppm
nochlorine contaminants and reproductive success of Dou-
(W
ble-crested Cormorants from Green Bay, Wisconsin, USA.
ESELOH et al., 1989). For the American avocet (R.
americana J. F. Gmelin 1789), the presumptive adverse
Environ. Toxicol. Chem., 18 : 1209-1217.
D
threshold of DDE in eggs is 3-8 ppm (R
ENKER, E., P. H. BECKER, M. BEYERBACH, A. BÜTHE, W. A.
OBINSON et al.,
HEIDMANN & G. STAATS DE YANÉS (1994). Concentrations
1997). Thus, it seems that the DDE levels we found in our
and metabolism of PCBs in eggs of waterbirds on the Ger-
study are too low to be harmful for the birds involved.
man North Sea Coast. Bull. Environ. Contam. Toxicol., 52 :
The median ratio of pesticides/PCBs was > 1 in the
220-225.
samples from all areas, denoting a dominance of agro-
DIRKSEN, S., T. BOUDEWIJN, L. K. SLAGER, R. G. MES, M. J. VAN
chemical over industrial pollution in northeastern Greece.
SCHAICK,. & P. DE VOOGT (1995). Reduce breeding success
Similar results have been found in other studies in Greece
of Cormorants (Phalacrocorax carbo sinensis) in relation to
persistent organochlorine pollution of aquatic habitats in the
and in the eastern Mediterranean and Black Sea regions
Netherlands. Environ. Pollut., 88 : 119-132.
(FOSSI et al., 1984 ; PASTOR et al., 1995a ; GOUTNER et al.,
FASOLA, M., I. VECCHIO, G. CACCIALANZA, C. GANDINI & M.
2001).
KITSOS (1987). Trends of organochlorine residues in eggs of
birds from Italy, 1977 to 1985. Environ. Pollut., 48 : 25-36.
CONCLUSIONS
FASOLA, M., P. A. MOVALLI, & C. GANDINI (1998). Heavy metal,
organochlorine pesticide, and PCB residues in eggs and
feathers of herons breeding in northern Italy. Arch. Environ.
The most heavily polluted wetland area studied was the
Contam. Toxicol., 34 : 87-93.
Evros Delta, where maximum concentrations of most pol-
FOCARDI, S., C. LEONZIO & C. FOSSI (1988). Variations in poly-
lutants were found in birds' eggs. Pollution patterns
chlorinated biphenyl congener composition in eggs of Medi-
reflected the birds' different positions in the food chain.
terranean water birds in relation to their position in the food
Levels of both pollutant groups were of the lowest
chain. Environ. Pollut., 52 : 243-255.
reported, being rather a normal follow up of the ban of
FOSSI, C., S. FOCARDI, C. LEONZIO & A. RENZONI (1984). Trace
these substances in the mid-seventies, and were too low to
metals and chlorinated hydrocarbons in birds' eggs from the
have adverse effects on birds. The higher agrochemical
Delta of the Danube. Environ. Conserv., 11 : 345-350.
FYTIANOS, K., V. SAMANIDOU & T. AGELIDIS (1986). Compara-
pollution reflects the underdevelopment of industry in the
tive study of heavy metals pollution in various rivers and
region. The occurrence of compounds such as drins may
lakes of Northern Greece. Ambio, 15 : 42-44.
reflect differences in bioaccumulation patterns due to dif-
GILBERTSON, M., T. KUBIAK, J. LUDWIG & G. A. FOX (1991).
ferent migration routes and/or wintering grounds of some
Great Lakes embryo mortality, edema, and deformities syn-
Organochlorine residues in Greek wetlands
163
drome (GLEMEDS) in colonial fish-eating birds : similarity
METCALFE, T. L. & C. D. METCALFE (1997). The trophodynam-
to chick edema disease. J. Toxicol. Environ. Health., 33 :
ics of PCBs, including mono- and non-ortho congeners, in
455-520.
the food web of north-central Lake Ontario. Sci. Total. Envi-
G
ron., 201 : 245-272.
ILMAN, A. P., G. A. FOX, D. B. PEAKALL, S. M. TEEPLE, T. R.
CARROLL & G. T. HAYMES (1977). Reproductive parameters
NISBET, I. C. & L. M. REYNOLDS (1984). Organochlorine resi-
and egg contaminant levels of Great Lakes Herring Gulls. J.
dues in Common Terns and associated estuarine organisms,
Wildl. Manage., 41 : 458-468.
Massachusetts, USA, 1971-81. Marine Environ. Res., 11 :
G
33-66.
OUTNER, V. (1985). Breeding ecology of the Avocet (Recurvi-
rostra avosetta L.) in the Evros Delta (Greece). Bonn. Zool.
OXYNOS, K., J. SCHMITZER & A. KETTRUP (1993). Herring gull
Beitr., 36(1/2) : 37-50.
eggs as bioindicators for chlorinated hydrocarbons (contri-
bution to the German Federal Environmental Specimen
GOUTNER, V. (1986). Distribution, status and conservation of the
Bank). Sci. Total Environ., 139/140 : 387-398.
Mediterranean Gull (Larus melanocephalus) in Greece. In :
MONBAILLIU, X. (ed), Mediterranean Marine Avifauna-
PASTOR, D., L. JOVER, X. RUIZ & J. ALBAIGÉS (1995a). Monitor-
Population Studies and Conservation. Springer-Verlag, pp.
ing organochlorine pollution in Audouin's Gull eggs : the
431-447.
relevance of sampling procedures. Sci. Total Environ., 162 :
215-223.
GOUTNER, V. (1994). The diet of Mediterranean Gull (Larus
P
melanocephalus) chicks at fledging. J. Ornithol., 135 : 193-
ASTOR, D., X. RUIZ, D. BARCELO & J. ALBAIGÉS (1995b). Diox-
201.
ins, furans, and AHH-active PCB congeners in eggs of two
gull species from the western Mediterranean. Chemosphere,
GOUTNER V., I. CHARALAMBIDOU & T. A. ALBANIS (1997). Orga-
31 : 3397-3411.
nochlorine insecticide residues in eggs of the Little Tern
PEARCE, P. A., J. E. ELLIOTT, D. B. PEAKALL & R. J. NORSTROM
(Sterna albifrons) in the Axios Delta, Greece. Bull. Environ.
(1989). Organochlorine contaminants in eggs of seabirds in
Contam. Toxicol., 58 : 61-66.
the northwest Atlantic, 1968-1984. Environ. Pollut., 56 :
GOUTNER V., T. A. ALBANIS & I. K. KONSTANTINOU (2001).
217-235.
PCBs and organochlorine pesticide residues in eggs of
ROBINSON, J. A., L. W. ORING, J. P. SKORUPA & R. BOETTCHER
Audouin's Gull (Larus audouinii) in the north-eatstern Med-
(1997). American Avocet (Recurvirostra americana). Birds
iterranean. Marine Pollut. Bull., 42 : 377-388.
N. America, 275 : 1-32.
Harding, C. G., R. J. LEBLANC, W. P. VASS, R. F. ADDISON, B.T.
SCHARENBERG, W. (1991). Cormorants (Phalacrocorax carbo
HARGRAVE, S. PEARRE, S. DUPUIS & P. F. BRODIE (1997).
sinensis) as bioindicators for chlorinated biphenyls. Arch.
Bioaccumulation of polychlorinated biphenyls (PCBs) in the
Environ. Contam. Toxicol., 21 : 536-540.
marine pelagic food web, based on a seasonal study in the
STATISTICA (1999). Kernel release 5.5. StatSoft Inc., Tulsa.
southern Gulf of St. Lawrence, 1976-1977. Marine Chem.,
S
56 : 145-179.
TRANBERG, B., C. BANDH, B. VAN BAVEL, P.-A. BERGQVIST, D.
BROMAN, C. NAF, H. PETTERSEN & C. RAPPE (1998). Con-
KAZANTZIDIS, S., V. GOUTNER, M. PYROVETSI & A. SINIS (1997).
centrations, biomagnification and spatial variation of orga-
Comparative nest site selection and breeding success in 2
nochlorine compounds in a pelagic food web in the northern
sympatric ardeids, Black-crowned Night Heron (Nycticorax
part of the Baltic Sea. Sci. Total Environ., 217 : 143-154.
nycticorax) and Little Egret (Egretta garzetta) in the Axios
TANABE, S., N. KANNAN, A. SUBRAMANIAN, S. WATANABE & R.
Delta, Macedonia, Greece. Colonial Waterbirds, 20 : 505-
TATSUKAWA (1987). Highly toxic coplanar PCBs : occur-
517.
rence, source, persistency and toxic implications to wildlife
KONSTANTINOU, I. K., V. GOUTNER & T. A. ALBANIS (2000). The
and humans. Environ. Pollut., 47 : 147-163.
incidence of polychlorinated biphenyl and organochlorine
WESELOH, D. V., P. MINEAU & D. J. HALLETT (1979). Orga-
pesticide residues in the eggs of the Cormorant (Phalacroco-
nochlorine contaminants and trends in reproduction in Great
rax carbo sinensis) : an evaluation of the situation in four
Lakes Herring Gulls, 1974-1978. 44th N. American Wildl.
Greek wetlands of international importance. Sci. Total Envi-
Conf., pp. 543-557.
ron., 257 : 61-79.
WESELOH, D., V., T. W. CUSTER & B. M. BRAUNE (1989). Orga-
LARSEN, B. & K. FYTIANOS (1989). Organochlorine compounds
nochlorine contaminants in eggs of Common Terns from the
and PCB congeners in contaminated sediments. Sci. Total
Canadian Great Lakes, 1981. Environ. Pollut., 59 : 141-160.
Environ., 86 : 273-279.
YAMASHITA, N., S. Tanabe, J. P. LUDWIG, H. KURITA, M. E. Lud-
LONGNECKER, P., W. J. ROGAN & G. LUCIER (1997).The human
wig & R. TATSUKAWA (1993). Embryonic abnormalities and
health effects of DDT (Dichlorodiphenyl-trichloroethane)
organochlorine contamination in double-crested Cormorants
and PCBs (Polychlorinated Biphenyls) and an overview of
(Phalacrocorax auritus) and Caspian Terns (Hydroprogne
organochlorines in public health. Ann. Rev. Publ. Health.,
caspia) from the upper Great Lakes in 1988. Environ. Pol-
18 : 211-244.
lut., 79 : 163-173.
Belg. J. Zool., 135 (2) : 165-170
July 2005
The diet of nestlings of three Ardeidae species (Aves,
Ciconiiformes) in the Axios Delta, Greece
Savas Kazantzidis1 and Vassilis Goutner2
1 Forest Research Institute, National Agricultural Research Foundation, GR-57006 Vassilika, Thessaloniki, Greece
2 Aristotelian University of Thessaloniki, School of Biology, Dept. of Zoology, GR-54006 Thessaloniki, Greece
Corresponding author : Savas Kazantzidis, e-mail : savkaz@fri.gr
ABSTRACT. The diets of the little egret (Egretta garzetta), the night heron (Nycticorax nycticorax) and the
squacco heron (Ardeola ralloides) were studied by analyzing nestling regurgitations collected during five breeding
seasons (1988-1990 and 1994-1995) at a heronry in the Axios Delta (Northern Greece). In total, 267 regurgitations
from little egrets, 247 from night herons and 19 from squacco herons (only in 1995) were collected and analyzed.
Each prey item was identified to the lowest possible taxon. The dry mass of each prey taxon was also estimated
from oven-dried prey specimens collected in the field.
At least 58 different prey taxa were identified among 5,108 items found in little egret regurgitations, at least 45 taxa
among 2,373 items regurgitated by night herons and 12 taxa among 277 items from squacco herons regurgitations. Dif-
ferences were detected between the three ardeid species in the proportion of each prey category. Little egret nestlings
were mainly fed fish (39.6% by number) and insects (32.0%), but amphibians and fish were the most important groups
by biomass (44.9% and 32.9% respectively). The proportions of prey categories varied significantly between years
(x2 = 922.91, p < 0.001). The night heron nestlings were mainly fed insects and the crustacean Triops cancriformis,
12
although the dry mass of the latter contributed little to the consumed biomass (4.0% compared to the 37.9% of insects).
Small mammals and reptiles were included in the diet of the young night herons, while the fish they ate were much
bigger than those consumed by little egret nestlings. The proportions of the night herons' main prey categories varied
significantly between years (x2 = 598.67, p < 0.001). Squacco heron chicks were fed mainly insects (50.9%) and
24
amphibians (31.8%), the latter being more important by biomass (73.6%). In a cluster analysis, diet of young little
egrets and night herons showed greater similarity from 1988 to 1990 than between 1994 and 1995, suggesting tempo-
ral changes in prey use. Study years tended to group separately for each species, but those of the little egret were more
scattered in the cluster than the night heron's, thus reflecting greater prey use variability. The diet of the squacco heron
was similar to that of the little egret when prey type frequencies were considered, but closer to the night heron's by dry
mass. The dry mass differed significantly between the species (x2 = 87.39, p < 0.001, Kruskal-Wallis test). This dietary
segregation may be a mechanism that reduces competition among these ardeid species, especially when prey is lim-
ited.
KEY WORDS : Ardeidae, diet, Axios, little egret, night heron, squacco heron
INTRODUCTION
Greece. The diet of the three ardeid species has been studied
in more detail in other Mediterranean countries : France
The little egret (Egretta garzetta Linnaeus, 1766), the
(VALVERDE, 1956 ; HAFNER, 1977 ; VOISIN, 1991), Italy
night heron (Nycticorax nycticorax Linnaeus, 1758) and
(MOLTONI, 1936 ; FASOLA et al., 1981, FASOLA et al., 1993 ;
the squacco heron (Ardeola ralloides Scopoli, 1769)
FASOLA, 1994), Spain (GONZALES-MARTIN & GONZALES-
breed in a multi-species colony in the Axios Delta. These
SOLIS, 1990 ; PEREZ et. al., 1991 ; MARTINEZ et. al., 1992)
ardeid species share certain foraging habitats, such as
and Israel (ASHKENAZI and YOM-TOV, 1996). Although, the
freshwater marshes and rice fields, but exploit them in
diet of various herons has often been studied in the western
different proportions (FASOLA, 1994). The little egret
Palearctic multiyear studies comparing the diet of sympatric
exploits all aquatic habitats in the Axios Delta, including
species are generally scarce. The objectives of this study
salt marshes and the seashore, whereas the other two her-
were to describe the diets of these three ardeid species, and
ons forage only in freshwater habitats. Thus, although the
to compare them between species and years. For the
three sympatric species may be considered generalists,
squacco heron we have data from 1995 only, and are there-
they seem to be separated ecologically by their selection
fore unable to present a comparison between years.
of different prey type or size.
The diet of the three study species is poorly known in
Greece. Studies concerning the diet of the little egret are
MATERIAL AND METHODS
available from Kerkini Lake (TSACHALIDIS, 1990) and the
Axios Delta (FASOLA 1994 ; KAZANTZIDIS et al., 1996 ;
The study was carried out in the Axios Delta, northern
KAZANTZIDIS, 1998). The diet of the night heron has been
Greece (40° 30' N, 22° 53' E), part of a large wetland
studied at the Kerkini Lake (BIRTSAS, 2002), while the
complex situated in the western part of Thermaikos Gulf
squacco heron data presented here are the first published for
(N. Aegean Sea). It extends over 68.7 km2 and comprises
166
Savas Kazantzidis and Vassilis Goutner
estuarine and deltaic areas, with a variety of
dry mass of 3,207 g belonging to 74 different taxa
natural and man-made habitats such as salt
(Appendix 1).
and fresh water marshes, ricefields, vege-
tated islets, river banks, tamarisk shrubland,
and sandy shores (ATHANASSIOU, unpub-
Arachnida
lished data). This wetland complex is of
Annelida
0.5%
Annelida
Crustacea
1.5%
Crustacea
0.5%
0.3%
Insecta larvae
international importance according to the
Amphibia tadpoles
Amphibia tadpoles
1.4%
17.3%
7.0%
21.2%
Ramsar convention, and a Special Protected
Insecta larvae
Insecta imagoes
17.1%
14.3%
Area.
Amphibia adults
The heron colony where the regurgita-
3.7%
tions were collected is located in a riverine
Insecta imagoes
15.0%
Amphibia adults
forest of Tamarisks (Tamarix spp.), Willows
28.3%
(Salix spp.) and Alders (Alnus glutinosa),
Pisces
on an island near the mouth of the River
32.3%
Pisces
39.6%
Axios. This colony is the second biggest in
Greece in terms of both number of breeding
pairs and number of species (KAZANTZIDIS,
Amphibia tadpoles
Mammalia
3.2%
Mammalia
4.8%
Annelida
1998). Other breeding species were great
0.5%
Reptilia
Reptilia
1.4%
Crustacea
Amphibia adults
0.3%
Annelida
4.6%
4.3%
cormorants (Phalacrocorax carbo Lin-
6.3%
10.5%
Amphibia tadpoles
1.2%
naeus, 1758), pygmy cormorants (Phalac-
Pisces
Insecta larvae
6.6%
2.0%
rocorax pygmaeus Pallas, 1773), spoonbills
Amphibia adults
21.7%
Crustacea
(Platalea leucorodia Linnaeus, 1758) and
23.0%
Insecta imagoes
glossy ibises (Plegadis falcinellus Lin-
35.9%
naeus, 1766). The total breeding population
of the colony ranged, in recent years from
1,100 to 2,000 pairs (K
Insecta imagoes
AZANTZIDIS, 1998).
Insecta larvae
40.3%
9.3%
Pisces
24.1%
Heron diet was studied by analyzing
nestling regurgitations collected during the
breeding seasons of 1988-1990 and 1994-
Insecta larvae
1995 (squacco heron data were collected
Amphibia tadpoles
Amphibia tadpoles
6.5%
12.6%
4.9%
only in 1995). Regurgitations were col-
Insecta imagoes
Insecta larvae
15.9%
lected throughout each nestling period, on
31.1%
a weekly basis, from April until early July.
Amphibia adults
After collection, the regurgitations were
19.1%
Pisces
4.0%
refrigerated until analysis. In order to esti-
mate the quantitative contribution of each
prey type, the dry mass of each prey taxon
Amphibia adults
was measured. Samples from each prey
Pisces
Insecta imagoes
68.7%
17.3%
19.9%
type were collected during the nestling
period from the main feeding habitats
(ricefields, irrigation canals, salt- and
Fig. 1. The diets of nestlings of the little egret (top), night heron (middle) and
freshwater marshes). Dry mass was meas-
squacco heron (bottom) by number (left) and by dry mass (right) of the main
ured by weighing each prey taxon dried in
prey categories.
an electric oven for 48 hours at approxi-
mately 70°C. Intact items found in the regurgitations
were also used for the estimation of their dry mass.
Little egret
In order to compare the frequencies of items from the
different prey categories between years, we used Chi-
At least 58 different taxa were identified among 5,108
square tests. We used Mann-Whitney U-tests and Kruskal-
prey items (1,499 g dry mass). By number, fish were the
Wallis x2 tests to compare median prey dry mass between
most important prey category (39.6%), followed by
the study species. In order to identify the diet similarities or
insects (32.1%) and amphibians (24.9%) (Fig.1). From a
differences between the three study species and the years of
total of 22 fish species identified, Aphanius fasciatus,
the study, a cluster analysis was applied to the proportions
Gambusia affinis and Gasterosteus aculeatus represented
of main prey categories in each study species X year com-
85.5% of all items. Of at least 27 species of insects, the
bination.
majority were larvae of Odonata, Dytiscidae and
Hydrophilidae (94.3% of all insect larvae). Among ima-
goes, Gryllotalpa gryllotalpa and Zygoptera spp. (Odo-
RESULTS
nata) prevailed, making up 72.2% of all items. Tadpoles
predominated among amphibians (85.0%), while the
We collected 533 regurgitations in total (267 from little
adults were mainly Rana ridibunda and Hyla arborea.
egrets, 247 from night herons and 19 from squacco her-
annelids (Lumbricus terrestris), arachnids (mainly Argy-
ons). In these we identified 7,758 prey items with a total
roneta aquatica) and crustaceans (Gammaridae and the
The diet of three Ardeidae in Greece
167
phyllopod Triops cancriformis) contributed less to the
and 50.9% of all prey items) were the most important
diet and were not present in all study years (Figs 1-2).
prey category, followed by amphibians (31.8%) and fish
By dry mass, amphibians and fish were the most impor-
(17.3%) (Fig. 1). The majority of insects (61.0%) were
tant food resources (45.6% and 32.3%, respectively, of the
larvae (mainly Odonata, Dytiscidae and Hydrophilidae),
total dry mass) (Fig. 1). Each of the other prey categories
while imagoes were mainly G. gryllotalpa (65.5% of all
contributed less than 1% (Fig. 1). The average dry mass of
imagoes). Amphibians were mainly adults of R. rid-
all prey items was 0.29g ± 0.72 (Table 1).
ibunda (60.2% of all amphibians). Of the three fish spe-
cies found, G. affinis was the most numerous (81.3%).
TABLE 1
By dry mass, R. ridibunda was the most important prey
taxon (68.7% of the total dry mass), followed by G. gryl-
The average dry mass (± SD) of the main prey categories con-
lotalpa (15.9%), whereas fish represented only 4.0% of
sumed by the three ardeid species
the total (Fig. 1). The average dry mass of all prey items
Night
Squacco
Kruskal-
was 0.62g ± 0.81 (Table 1).
Prey type Little Egret
Heron
Heron
Wallis x2 1
Insects
0.20 ± 0.26 0.50 ± 0.31
0.27 ± 0.29
379.4
100%
Fish
0.24 ± 0.96 2.37 ± 5.43 0.14 ± 0.13
221.5
80%
Amphibians 0.53 ± 0.69 1.56 ± 0.93
1.43 ± 0.97
337.2
Others
0.03 ± 0.04 0.11 ± 0.01
0
-17.382
60%
Total
0.29 ± 0.72
0.65 ± 1.7
0.62 ± 0.81
87.39
%
1. p < 0.0001 in all cases.
40%
2. Mann-Whitney U-test was applied. Annelids, crustaceans and arach-
nids only are included.
20%
0%
Diet composition differed between years (x2
=
12
1988
1989
1990
1994
1995
922.91, p<0.001). Within the main prey categories, the
Years
differences were also significant (fish : x2 = 598.72,
Annelida
Arachnida
Crustacea
Insecta
Pisces
Amphibia
4
p<0.001 ; insects : x2 = 369.65, p < 0.001 ; amphibians :
4
x2 = 159.6, p<0.001) (Fig. 2).
4
100%
Night heron
80%
At least 45 different taxa were found among 2,373 prey
items (1,537 g dry mass). Insects (at least 22 taxa) were by
60%
far the most numerous prey (49.6%), followed by crusta-
%
40%
ceans (exclusively T. cancriformis) (23.1%), amphibians
(9.5%) and fish (6.6%). Annelids (Lumbricidae) also con-
20%
tributed in relatively high proportion (10.5% by number),
although they appeared only in three out of five study years
0%
(Figs 1-2). Reptiles (Natrix natrix and Emys orbicularis)
1988
1989
1990
1994
1995
Years
and mammals (Arvicola terrestis, Microtus arvalis, Rattus
Annelida
Crustacea
Insecta
Pisces
Amphibia
Mammalia & Reptilia
spp.) were also found in low proportions (Figs 1-2). The
majority of insects were imagoes (81.3% of all insect
Fig. 2. The yearly composition of the diet (by number of the
items), predominantly G. gryllotalpa (77.8% of all imagoes
main prey categories) of the little egrets (top) and night herons
(bottom).
and 31.3% of all prey items). Amphibians were mainly
adult R. ridibunda (66.7%). Of 13 fish species found in the
regurgitations, Leuciscus cephalus, Carassius auratus and
Interspecific comparison
Lepomis gibbosus were the most numerous (58.3% of all
The little egret had a more diverse diet than the other
fish items). By dry mass, insects were the most important
two species, and preyed mainly upon small-sized prey.
category (37.9%), followed by fish (24.1%) and adult
Both fish and amphibians (mainly tadpoles) eaten by little
amphibians (21.7%) (Fig. 1). The average dry mass of all
egrets were small-sized (average dry masses of 0.24g ±
prey items was 0.65 g ± 1.7 (Table 1).
0.96, and 0.21g ± 0.69 respectively).
Diet composition differed between years, both consid-
The median prey dry mass differed significantly
ering all prey types (x2 = 598.67, p<0.001), and within
24
between the three ardeid species as a result of the smaller
each of the main prey categories (fish : x2 = 41.45,
4
average dry mass of prey of the little egret (Table 1).
p<0.05 ; insects : x2 = 184.36, p<0.001 ; amphibians :
4
x2 = 102.48, p<0.001). The number of mammals and
The night herons took insects, fish and amphibians of
4
reptiles did not differ between years (x2 = 8.07, p = 0.089
larger size than those taken by the other two species
4
and x2 = 2.56, p = 0.633, respectively) (Fig. 2).
(Table 1). In addition, night herons fed on large prey such
4
as reptiles and mammals, which were absent from the diet
Squacco heron
of the little egret and the squacco heron (Fig. 1, Appendix
1). Crustaceans (T. cancriformis) were also absent from
The 277 prey items found (171 g dry mass) belonged to
the diet of these two species while they were common in
at least 12 different taxa. By number insects (eight species
the night heron's diet. This difference may be due to the
168
Savas Kazantzidis and Vassilis Goutner
absence of T. cancriformis from the foraging areas during
same area, fish seems to be the most important prey for
the nestling period of the little egret and the squacco
the little egret (VOISIN, 1991).
heron, but its availability to night herons, which start
breeding at least two weeks earlier than the other two spe-
Night herons fed heavily on insects (especially G. gryl-
cies (F
lotalpa), which were the most important prey category by
ASOLA et al., 1981, KAZANTZIDIS et al., 1997).
both number and dry mass. T. cancriformis and annelids
Of 74 different taxa identified in the nestlings' regurgi-
were present in only some years of the study. Fish and
tations, 37 were common to the three ardeid species while
amphibians were not common (both less than 10% of all
only four (namely R. ridibunda, Dytiscidae and
prey items). These findings differ from those of all other
Hydrophilidae larvae, and G. gryllotalpa) participated in
studies of this species' diet conducted in Greece and in
proportions of more than 10% of all prey items in the
other Mediterranean countries. BIRTSAS (2002) reported
diets of all three ardeid species.
that in Kerkini Lake the nestlings' diet consisted mainly
The diets of the squacco heron and the little egret
of fish (86.5%) and amphibians (12.1%), while insects
shared 11 species in common (Fig. 3, Appendix 1), while
represented only 1.5% of all prey items. Similarly, fish
a higher resemblance was found between the diets of the
was the night heron's major food type (93.7%) in Extrem-
little egret and the night heron (31 common species or
adura, Spain, (PEREZ et al., 1991), in Israel (ASHKENAZI &
taxa). Only nine species or taxa were common to the
YOM-TOV, 1996) and in Serbia (LASZLO 1986). Further-
squacco and the night herons' diets.
more, FASOLA et al. (1981, 1993) and FASOLA (1994)
reported that in various Italian colonies, fish (Cyprinidae)
Inter-year comparison
or amphibians dominated the diet, while insects were
found in very low proportions. In the Camargue, night
Differences between years were detected, and the diets
herons feed mostly on fish and coleopteran larvae (VAL-
of both the little egret and the night heron showed greater
VERDE, 1956 ; HAFNER, 1977). The great geographical
similarity from 1988 to 1990 than between 1994 and
variability in the night heron's diet probably reflects dif-
1995, suggesting temporal changes in prey use (Figs 2-3).
ferences in prey availability in each breeding area and a
Study years tended to group separately for each species,
great flexibility in prey use by this species.
but those of the little egret were more scattered in the
The diet of the squacco heron at the Axios Delta is sim-
cluster, indicating a greater prey use variability (Fig. 3).
ilar to that reported by MOLTONI (1936), CRAMP & SIM-
MONS (1977), HAFNER (1977), HANCOCK & KUSHLAN
(1984), LASZLO (1986) and VOISIN (1991). In all of the
NN88
above studies, insects or amphibians predominated by
NN90
number, although amphibians or fish had greater dry
NN89
mass. Differences between colonies were found in Italy
EG88
(FASOLA et al., 1993 ; FASOLA 1994), where fish (Cyprini-
EG90
dae) was the most frequent prey type in two out of three
NN94
heronries, whereas insects participated in small propor-
NN95
tions in all three colonies.
EG94
EG95
Dietary differences between the years of our study also
AR95
indicate that these ardeid species are opportunistic forag-
EG89
ers, changing their diet from one year to the next accord-
ing to prey abundance and availability. For example, crus-
5
10
15
20
25
30
35
40
taceans, which were taken by both the little egret and the
Linkage distance (Single Linkage)
night heron, were completely absent in 1994 from both
Fig. 3. Comparison of the diet (by prey categories) between
species' diet, suggesting a decrease of crustacean popula-
the three ardeid species and study years (EG : little egret, NN :
tion in that year. Where studies of more than one year are
night heron, AR : squacco heron).
available, they report temporal differences. In 1970, little
egrets in the Camargue preyed mainly on insects, while in
DISCUSSION
1971 fish and crustaceans were more frequent (more than
50%) (HAFNER 1977). In the same study, no differences
were detected in the proportions of prey types in the night
The three ardeid species considered in this study had
and squacco herons.
distinctive diets. Little egrets took a wide variety of prey
types and fed mainly on small-sized fish, insects and tad-
The differences in prey taken by the three study species
poles. Similar findings have also been reported from Ker-
reflect mainly differences in their foraging habitats and
kini Lake (TSACHALIDIS, 1990) although the size of fish
distribution of prey. Little egrets were foraging in all
there was larger (up to 9.3 cm) and T. cancriformis con-
available feeding habitats (KAZANTZIDIS & GOUTNER,
tributed to the diet in a higher proportion (up to 8.1%). In
1996), which may account for the high prey variation
the Camargue, S. France, freshwater fish also predomi-
reported in this study. Night and squacco herons avoid
nated in the diet of little egrets' nestlings (HAFNER, 1977 ;
open habitats and forage mainly in fresh water marshes
KAZANTZIDIS et al., 1996). In Italy the contribution of fish
and occasionally in ricefields, thus limiting the range of
to the diet was smaller, but still significant (28.07%)
prey types they can capture. The differences in prey dry
(FASOLA et al., 1981). Generally, although differences
mass also indicate a dietary segregation between the
have been detected even among different colonies of the
ardeid species.
The diet of three Ardeidae in Greece
169
In conclusion, there is a dietary segregation between
HAFNER, H. (1977). Contribution à l'étude écologique de quatre
the three ardeid species with regard to both relative fre-
espèces des hérons (Egretta g. garzetta L., Ardeola r. ral-
quencies and dry mass of prey types. There is a partition-
loides Scop., Ardeola i. ibis L., Nycticorax n. nycticorax L.)
ing of food resources by foraging habitats and/or choice
pendant leur nidification en Camargue. Thèse à l' Université
of prey. This resource partitioning may be a mechanism
de Toulouse, (183 pp).
that reduces competition among the species, especially
HANCOCK, J. and J. KUSHLAN (1984). The Herons handbook.
when prey is limited.
Croom Helm Ltd. London.
KAZANTZIDIS, S. (1998). The breeding ecology of the little egret
(Egretta g. garzetta) in the Axios Delta, Macedonia, Greece.
ACKNOWLEDGEMENTS
Doctorate Thesis. Aristotelian University of Thessaloniki
(208 pp).
We would like to thank the Greek General Secretariat of
KAZANTZIDIS, S. and V. GOUTNER (1996). Foraging ecology and
Research and Technology for the financial support of a part of
conservation of feeding habitats of little egrets (Egretta
this study. We are grateful to Professor Apostolos Sinis (Aristo-
garzetta) in the Axios river delta, Macedonia, Greece.
telian University of Thessaloniki, Greece) for the assistance in
Colon. Waterbirds, 19 (Special publication 1) : 115-121.
the identification of fish species, Iris Charalambidou, Stavroula
Papoulia and Chryssoula Athanassiou (biologists) for their
KAZANTZIDIS, S., H. HAFNER & V. GOUTNER (1996). Compara-
assistance in the field and Dr Grigorios Papakostas (Michigan
tive breeding ecology of the little egret (Egretta g. garzetta)
State University, USA) for commenting on linguistic matters.
in the Axios Delta (Greece) and the Camargue (France). Rev.
We are also grateful to Dr. Mauro Fasola for providing many
Ecol. (Terre Vie), 51 : 313-327.
helpful comments on an earlier draft of this article.
KAZANTZIDIS, S., V. GOUTNER, M. PYROVETSI & A. SINIS (1997).
Comparative nest site selection and breeding success in 2
sympatric ardeids, Black-crowned Night-Heron (Nycticorax
REFERENCES
nycticorax) and little egret (Egretta garzetta) in the Axios
Delta, Macedonia, Greece. Colon. Waterbirds, 20 (3) : 505-
ASHKENAZI, S. & Y. YOM-TOV (1996). Herons and fish farming
517.
in the Huleh Valley, Israel : Conflict or mutual benefit ?
L
Colon. Waterbirds, 19 (Special Publication 1) : 143-151.
ASZLO, S. (1986). Data on the food of the Purple (Ardea purpu-
rea), Night (Nycticorax nycticorax), and Squacco (Ardeola
BIRTSAS, P. (2002). Ecology and conservation of the Black-
ralloides), herons on Lake Ludas. Larus, 36-37 : 175-182.
crowned night heron (Nycticorax n. nycticorax L. 1758) at
the Kerkini reservoir, Macedonia, Greece. Doctorate Thesis.
MARTINEZ, C., X. RUIZ & L. JOVER (1992). Allimentacion de los
Aristotelian University of Thessaloniki, (151 pp).
pollos de Martinete (Nycticorax nycticorax) en el delta del
CRAMP, S. & K. E. L. SIMMONS, (eds), (1977). The birds of the
Ebro. Ardeola, 39 :25-34.
Western Palearctic. Oxford University Press, Oxford.
MOLTONI, E. (1936). Le Garzaie in Italia. Rivista Italiana di
FASOLA, M. (1994). Opportunistic use of foraging resources by
Ornithologia, 6 : 109-148, 210-269.
heron communities in southern Europe. Ecography, 17 :
PEREZ, J.J., F. DE LOPE, B. TUREGANO & C. DE LA CRUZ (1991).
113-123.
The food of Black-crowned night heron nestlings in Extrem-
FASOLA, M., P. ROSA & L. CANOVA (1993). The diets of squacco
adura (W. Spain). Ardeola, 38 (2) : 277-287.
herons, little egrets, Night, Purple and Grey Herons in their
T
Italian breeding ranges. Rev. Ecol. (Terre Vie), 48 : 35-47.
SACHALIDIS, E. (1990). Biology and behavioral ecology of little
egret (Egretta garzetta) in the artificial Lake Kerkini, Serres,
FASOLA, M., P. GALEOTI, G. BOGLIANI & P. NARDI (1981). Food
Greece. Doctorate Thesis. Aristotelian University of Thessa-
of Night heron (Nycticorax nycticorax) and little egret
loniki, (146 pp).
(Egretta garzetta) feeding in rice fields. Riv. Ital. Orn., Mil-
ano, 51 (1-2) : 97-112.
VALVERDE, J. A. (1956). Essai sur l' Aigrette Garzette en France
GONZALES-MARTIN, M. & J. GONZALES-SOLIS (1990). Datos
(Egretta garzetta). Alauda, 24 : 1-36.
sobre la alimentacion de ardeidos en el delta del Ebro. Mis-
VOISIN, C. (1991). The Herons of Europe. T. and A. D. Poyser
cellania Zoologica, 14 : 240-244.
Ltd. London.
170
Savas Kazantzidis and Vassilis Goutner
APPENDIX 1
Egretta
Nycticorax Ardeola
Species
garzetta
nycticorax
ralloides
The prey species (number of items) identified in the nestling
Coccinellidae
-
16
-
regurgitations of the three ardeid species
Coccinella 7-punctata
2
14
-
Propylea 14-punctata
-
1
-
Chrysomelidae
1
2
-
Egretta
Nycticorax Ardeola
Species
Leptinotarsa decemlineata
-
1
-
garzetta
nycticorax
ralloides
Dytiscidae imagoes
22
37
-
Prey type
Dytiscidae larvae
275
82
31
INVERTEBRATES
Lybius spp.
-
2
-
ANNELIDA
Hydrophilidae imagoes
2
15
-
Oligochaeta
Laccobius spp.
2
-
-
Lumbricidae
-
68
-
Laccobius sinuatus
-
1
-
Lumbricus terrestris
79
149
Hydrophilus piceus
-
1
-
Allolopophora spp.
-
3
-
Hydrophilidae larvae
218
75
-
Eisenia foetida
-
30
-
Hydrophilus piceus
25
2
19
ARTHROPODA
Heteroceridae
Chelicerata
Heterocerus flexuosus
-
1
-
Argyroneta aquatica
9
-
-
Unidentified Coleoptera
16
32
-
Pholcus phalangioides
1
-
-
VERTEBRATES
Unidentified Arachnida
14
-
-
Pisces
Crustacea
Cyprinidae
2
2
-
Phillopoda
Leuciscus cephalus
5
17
-
Triops cancriformis
36
547
-
Cyprinus carpio
4
-
-
Amphipoda
Pseudorasbora parva
1
2
-
Gammaridae
32
-
-
Rutilus rutilus
8
8
1
Talitridae
2
-
-
Carassius auratus
7
15
-
Decapoda
Phoxinus phoxinus
4
1
-
Palaemonidae
3
-
-
Rhodeus sericeus
18
-
1
Insecta
Alburnus alburnus
2
2
-
Odonata
Cobitidae
Larvae
328
31
35
Cobitis spp.
3
-
-
Imagoes
Cobitis taenia
2
-
-
Zygoptera
276
22
5
Gasterosteidae
Platycnemis spp.
2
-
-
Gasterosteus aculeatus
150
-
-
Anisoptera
9
18
-
Poeciliidae
Aeshnidae
46
-
7
Gambusia affinis
567
-
39
Libellulidae
30
-
-
Centrarchidae
Unidentified Odonata
Lepomis gibbosus
2
12
-
Orthoptera
Gobiidae
Acrididae
3
8
2
Gobius spp.
21
-
-
Tetrigidae
1
-
-
Knipowitschia caucasica
2
-
-
Tettigoniidae
3
-
-
Pomatoschistus spp.
3
1
-
Gryllotalpidae
Clupeidae
Gryllotalpa gryllotalpa
276
744
36
Sardina pilchardus
1
-
-
Unidentified Orthoptera
-
1
-
Atherinidae
Dictyoptera - Mantodea
1
-
-
Atherina spp.
68
6
-
Hemiptera - Heteroptera
Atherina boyeri
24
1
-
Naucoridae
2
1
-
Cyprinodontidae
Llyocoris cimicoides
8
-
-
Aphanius fasciatus
1013
6
-
Notonectidae
Mugilidae
5
-
-
Notonecta glauca
5
-
-
Liza saliens
2
-
-
Gerridae
Blenniidae
Gerris lacustris
9
-
-
Blennius pavo
8
-
-
Aquarius najas
1
-
-
Pleuronectidae
Scutelleridae
Platichthys flesus
1
-
-
Eurygaster maura
1
-
-
Soleidae
Lygaeidae
-
2
-
Solea solea
4
-
-
Unidentified Hemiptera
7
5
2
Exocoetidae
-
2
-
Diptera
Unidentified fish
95
81
7
Cyclorrhapha
Amphibia
Tachinidae
1
-
-
Rana ridibunda
158
95
52
Calliphoridae
1
-
-
Hyla arborea
9
1
-
Syrphidae
18
2
-
Rana spp. adults
24
54
1
Brachycera
Rana spp. tadpoles
1084
75
35
Stratiomyidae imagoes
7
1
3
Reptilia
Stratiomyidae larvae
25
26
-
Natrix natrix
-
6
-
Tabanidae larvae
-
-
1
Emys orbicularis
-
1
-
Unidentified Diptera
5
2
-
Mammalia
Hymenoptera
3
3
-
Arvicola terrestris
-
1
-
Apocrita
2
1
-
Microtus arvalis
-
2
-
Formicidae
-
1
-
Rattus spp.
-
2
-
Coleoptera
Unidentified mammals
-
7
-
Carabidae
-
15
-
TOTAL
5108
2373
277
Amara aenea
-
2
-
Scarabaeidae
1
5
-
Elateridae imagoes
1
2
-
Elateridae larvae
-
2
-
Belg. J. Zool., 135 (2) : 171-173
July 2005
SHORT NOTE
Seasonal variation in abundance of Corophium orientale
(Crustacea : Amphipoda) in Monolimni lagoon (Evros
Delta, North Aegean Sea)
Theodoros Kevrekidis1, Theodora Boubonari1 and Vasilios Goutner2
1 Democritus University of Thrace, Laboratory of Environmental Research and Education, GR-68100, Alexandroupolis, Hel-
las.
2 Department of Zoology, School of Biology, Aristotelian University of Thessaloniki, GR-54006, Thessaloniki, Hellas
Corresponding author : T. Kevrekidis, e-mail : tkebreki@eled.duth.gr
increased from April onwards and peaked in June (Fig.
KEY WORDS. Amphipods, Corophium orientale, abundance,
1). It decreased in July August. Density increased again
seasonal variation, Aegean sea
in September, while after September it varied at relatively
lower levels (Fig. 1). Density of C. orientale showed a
significant seasonal variation in both stations (Kruskal
Amphipods of the genus Corophium are frequently
Wallis one way analysis of variance : H=22.398, DF=3,
important components of inshore ecosystems. Corophium
P<0.001 in station I ; H=9.152, DF=3, P<0.05 in station
1
orientale Schellenberg, 1928 is a common and frequently
B ) being lowest in spring in both stations and highest in
2
abundant inhabitant of Mediterranean lagoons and coastal
summer in station I and in autumn in station B . During
1
2
brackish environments; nevertheless, its population
spring density of the two populations did not differ signif-
dynamics have not yet been studied. The present study
icantly (Mann Whitney U test) ; however, density in
describes the monthly variation in population density of
station I was significantly higher than that in station B
1
2
the amphipod C. orientale in the two parts of Monolimni
mainly in summer (P<0.001), but also in autumn and win-
lagoon, Evros Delta, N. Aegean Sea. This variation is dis-
ter (P<0.01).
cussed in relation to the life cycle of the species and to
some abiotic and biotic factors.
Monolimni (or Paloukia) lagoon, occupying an area of
about 115 ha, communicates with the sea mainly through
an opening 15m wide. Between February 1998 and Feb-
ruary 1999 macroalgae were occasionally observed in
both parts of the lagoon (the southern and northern ones),
while a meadow of Ruppia maritima occurred in the
innermost northern one. During the aforementioned
period monthly samples of benthic macrofauna were col-
lected at the stations I and B located in the southern and
1
2
northern part of Monolimni lagoon, respectively (1). For
this study all Corophium orientale specimens were sepa-
Fig. 1. Monthly variation in population density (mean ±
rated from the remaining macrofauna and counted.
standard error) of Corophium orientale in station I and sta-
1
Further examination of C. orientale specimens was
tion B in Monolimni lagoon, Evros Delta.
2
used for the description of the life cycle of this species
(2). The structure of the macrobenthic assemblages in
We tested for significant correlations (Spearman's
these stations throughout the period February 1998 to
Rank correlation coefficient ) between the monthly vari-
February 1999, as well as the monthly variation in several
ation in population density of C. orientale and that in (a)
water and sediment parameters were also described (1).
several physicochemical parameters of the water and sed-
Table I shows the fluctuations of all these environmental
iment, and (b) the abundance of the constant co-occurring
parameters over the sampling period.
macrofaunal taxa [Ventrosia maritima (Milaschewitch,
In station I , population density of Corophium orien-
1916), Streblospio shrubsolii (Buchanan, 1890), Hediste
1
tale was low in February April, increased in May July
diversicolor (Muller, 1776), Gammarus aequicauda
and peaked in August (Fig. 1). It decreased in September
(Martynov, 1931), Abra ovata (Philippi, 1836) in both
October ; after October, density gradually decreased
stations, as well as Cumacea in station I and Cerasto-
1
until the last sampling (Fig. 1). In station B , the abun-
derma glaucum (Poiret, 1789), Chironomidae larvae and
2
dance of C. orientale was low in February March 1998,
Tubificidae in station B ]. In station I , there was a signif-
2
1
172
Theodoros Kevrekidis, Theodora Boubonari and Vasilios Goutner
icant positive correlation between density of C. orientale
with those of the constant macrobenthic taxa were not
and salinity (Table 1) ; salinity had a value of about 0.3
significant. In station B , no significant correlation was
psu in spring, 1.2 5.6 psu in summer, 3 4 psu in
2
found between C. orientale abundance and any one of the
autumn and 0.5 1.5 psu in winter. A significant negative
abiotic parameters (Table 1) ; there was a positive correla-
correlation was found between C. orientale abundance
and dissolved O and also O saturation (Table 1), since
tion with the abundance of the bivalve A. ovata (=0.736,
2
2
these parameters had higher values during the colder
P<0.01) and the amphipod G. aequicauda (=0.648,
period of the year, when the amphipod abundance was
P<0.05), which showed similar trends in seasonal varia-
more or less low. The correlations of C. orientale density
tion.
TABLE 1
The range of several physicochemical parameters of water and sediment and Spearman's rank correlation coefficient (r) values
between density of Corophium orientale and these physicochemical parameters throughout the sampling period in stations I and B in
1
2
Monolimni Lagoon, Evros Delta (*: P<0.05; **: P<0.01; ns: not significant; n=13; a: n=12; b: n=11).
Station I
Station B
1
2
Variable
Variable
Variable
Range
Range
Water
Depth (cm)
50 - 85
-0.048 ns
30 55
0.599 ns b
Salinity (psu)
0.3 5.6
0.810 **
0.3 5.7
0.377 ns
Dissolved O (mg l-1)
6.05 14.7
-0.706 * b
9.78 18.0
-0.400 ns b
2
O saturation (%)
74 122
-0.645 * b
101 220
-0.064 ns b
2
pH
7.4 9.1
-0.349 ns
7.45 9.32
0.069 ns
Transparency (cm)
35 65
0.019 ns
15 55
0.046 ns a
Temperature (oC)
1.8 26.7
0.516 ns
4.2 28.5
0.126 ns
Sediment
Temperature 1cm (oC)
2.1 26.6
0.512 ns
3.7 27.0
0.190 ns
Temperature 5cm (oC)
1.9 26.5
0.512 ns
3.5 28.6
0.176 ns
Median diameter (µm)
143 176
-0.108 ns
94 129
-0.033 ns
Organic matter (%)
0.15 1.73
0.525 ns
0.48 2.20
0.538 ns
Salinity was the only examined parameter that essen-
nus, Calidris spp.), which gather especially in that part of
tially showed an association with the density of C. orien-
the lagoon during summer. As a consequence, recruitment
tale. Extremely low salinities coincided with decreases in
occurred only during late spring and early autumn, two
abundance in winter and with low abundances in spring.
discrete generations, a spring and an overwintering one,
Nevertheless, the increase in population density during
were produced (2) and population density decreased in
late spring at salinities of 0.3 0.4 psu indicates that this
July. Predation by migratory shorebirds (Callidris pusilla)
amphipod is highly tolerant to extremely low salinities ;
has been considered itself responsible for a similar
particularly, it appears to be more tolerant than other
decline in densities of Corophium volutator during sum-
brackish water Corophium species, such as C. volutator
mer in intertidal mudflats of the Bay of Fundy, Canada (9,
and C. insidiosum (3, 4).
10). In addition, the major part of the C. orientale popula-
In station I breeding of C. orientale peaked in March,
tion may have temporarily emigrated from station B dur-
1
2
June and September, and a spring, a summer and an over-
ing August, when dense vegetation of Ruppia maritima
wintering cohort were produced showing a life span of
and high temperatures occurred, in order to avoid some
about 4, 5 and 8 9 months, respectively (2). Therefore,
unfavorable conditions such as low oxygen concentra-
population density increased during late spring and sum-
tions at night. Under experimental conditions an emigra-
mer following the recruitment of the spring and summer
tion of Corophium volutator from sediments associated
cohorts, while it decreased after summer mainly or partly
with low oxygen saturation has been observed (11).
due to the die off initially of the spring cohort and after-
wards of the summer one. A similar increase in density
REFERENCES
during the main reproductive period has been also
reported for other Corophium populations (e.g. 5, 6).
1. KEVREKIDIS, T., (2004). Seasonal variation of the macrozoo-
Breeding of various Corophium species occurs mainly
benthic community structure at low salinities in a Mediterra-
from mid or late spring to autumn in northern brackish
nean lagoon (Monolimni lagoon, Northern Aegean Sea).
habitats, while in more southerly ones the breeding period
Intern. Rev. Hydrobiol, 89: 407-425.
is usually wider (e.g. 7, 8). Comparison of the monthly
2. KEVREKIDIS, T. Life history, aspects of reproductive biology
variation in abundance of C. orientale in the two parts of
and productivity of Corophium orientale (Crustacea :
Monolimni lagoon revealed a striking difference during
Amphipoda) in Monolimni lagoon (Northern Aegean Sea).
Hydrobiologica (in press).
summer. In station B breeding of C. orientale peaked in
2
3. MCLUSKY, D.S., (1967). Some effects of salinity on the sur-
April and then, in September ; a lack of large individuals
vival, moulting and growth of Corophium volutator
observed in summer possibly contributed to that hiatus in
(Amphipoda). J. mar. biol. Ass. UK., 47 : 607-617.
reproduction (2). That lack should be attributed to a size
4. CASABIANCA, M.L., (1972/73). Influence des apports d' eau
selective predation probably by shorebirds (Tringa tota-
douce sur la dynamique des populations de crustacés con-
Seasonal variation in abundance of Corophium orientale
173
structeurs de l' étang de Biguglia, Corse (Corophium insidi-
Aveiro (NW Portugal). I. Life history and aspects of repro-
osum C., Tanais cavolinii M.E., Erichthonius brasiliensis
ductive biology. Mar. Biol., 137 : 637-650.
D.). Vie Milieu, 23C : 45-63.
5. S
9. P
HEADER, M., (1978). Distribution and reproductive biology
EER, D.L., L.E. LINKLETTER & P.W. HICKLIN, (1986). Life
of Corophium insidiosum (Amphipoda) on the north east
history and reproductive biology of Corophium volutator
coast of England. J. mar. biol. Ass. UK., 58 : 585-596.
(Crustacea : Amphipoda) and the influence of shorebird pre-
6. F
dation on population structure in Chignecto Bay, Bay of
LACH, E.C., (1992). The influence of four macrozoobenthic
species on the abundance of the amphipod Corophium volu-
Fundy, Canada. Neth. J. Sea Res., 20 : 359-373.
tator on tidal flats of the Wadden Sea. Neth. J. Sea Res., 29 :
10. MATTHIEWS, S.L., J.S. BOATES & S.J. WALDE, (1992). Shore-
379-394.
bird predation may cause discrete generations in an amphi-
7. FISH, J.D. & A. MILLS, (1979). The reproductive biology of
pod prey. Ecography, 15 : 393-400.
Corophium volutator and Corophium arenarium (Crustacea,
Amphipoda). J. mar. biol. Ass. UK., 59 : 355-368.
11. OSTERLING, M. & L. PIHL, (2001). Effects of filamentous
8. CUNHA, M.R., J.C. SORBE & M.H. MOREIRA, (2000). The
green algal mats on benthic macrofaunal functional feeding
amphipod Corophium multisetosum (Corophiidae) in Ria de
groups. J. exp. mar. Biol. Ecol., 263 : 159-183.
Belg. J. Zool., 135 (2) : 175-179
July 2005
Allozyme variation in populations of the karyotypically
polymorphic vole Microtus (Terricola) thomasi (Mamma-
lia, Rodentia) from Greece
Panagiotis Kornilios, Basil Chondropoulos and Stella Fraguedakis-Tsolis
Section of Animal Biology, Department of Biology, University of Patra, 260 01 Patra, Greece, e-mail : fraqued@upatras/gr
ABSTRACT. Five distinct karyotypic forms of the vole Microtus (Terricola) thomasi are known in Greece so far :
the earlier described forms "thomasi" (2n=44, FN=44) and "atticus" (2n=44, FN=46), and the more recently discov-
ered ones with a)2n=41,42, FN=42,43,44, b)2n=40, FN=42, and c)2n=38, FN=40. The present study gives informa-
tion on genetic relationships between vole populations belonging to the different karyotypic forms, based on alloz-
yme variation. Eighteen loci were typed on cellulose acetate plates in 102 voles collected from six localities of
mainland Greece, and the allelic data obtained were analysed using the biostatistical program BIOSYS-1. Popula-
tions studied show high intra- and interpopulation electrophoretic variability. A UPGMA dendrogram revealed clear
separation of the "atticus" karyotype population from all others. Among the latter, two main groups exist : one
including the population with the typical "thomasi" karyotype and another comprising all populations with poly-
morphic karyotypes. The clustering of the six populations studied is in agreement with karyological data given in
recent literature.
KEY WORDS : Allozymes, voles, Microtus (Terricola) thomasi, Greece, karyotype variation
INTRODUCTION
ditions (GIAGIA-ATHANASOPOULOU & STAMATOPOULOS
unpublished data).
Voles of the genus Microtus (subgenus Terricola) of the
The present study aims to clarify the genetic relation-
Arvicolidae family are represented in Greece by three
ships between some of the Greek M.(T.) thomasi popula-
species; Microtus (Terricola) subterraneus, M. (T.)
tions representing all known karyotypic forms.
felteni, and M.(T.) thomasi (MITCELL-JONES et al., 1999).
Microtus (Terricola) thomasi Barrett-Hamilton, 1903, is
endemic to the SW Balkan peninsula; in Greece it is dis-
tributed in the mainland (except Thrace and Eastern and
Central Macedonia) and on the Evvoia island. It can be
found from sea level up to an altitude of 1700 m.
Extensive karyological investigations (GIAGIA &
ONDRIAS 1973; GIAGIA 1985; GIAGIA-ATHANASOPOULOU
et al., 1995; GIAGIA-ATHANASOPOULOU & STAMATOPOU-
LOS, 1997) have shown that M. (T.) thomasi occurs as sev-
eral different karyotypic forms in Greece. Table 1 shows
these forms, their geographical distribution and the way
each has evolved from another. Discovery of this karyo-
typic polymorphism triggered interest in the study of its
possible role in the speciation process (KING 1993;
SEARLE 1993; FRAGUEDAKIS-TSOLIS et al. 1997).
Fig. 1. Map of Greece showing sampling localities of the
Some morphological and ethological studies indicate
present study and numbers of individuals collected from each
that the "thomasi" and "atticus" karyotypic forms can be
locality.
regarded as two different species (MILLER 1910; MILLER
1912; KRATOCHVIL 1971; PETROV & ZIVCOVI ´C 1972;
MATERIAL AND METHODS
STAMATOPOULOS & ONDRIAS 1986), whereas other mor-
phological, behavioural, immunological and biochemical
102 individuals of M.(T.) thomasi were collected from
studies suggest these two forms are conspecifics
six localities of mainland Greece taking care that each of
(NIETHAMMER 1974; CORBET 1978; PETROV & ZIVCOVI ´C
the populations belonged to one of the six known karyo-
1979; NIETHAMMER & KRAPP 1982; NIKOLETOPOULOS et
typic forms (Table 1, Fig. 1). All individuals were live-
al. 1992; PETROV 1992; TSEKOURA et. al. 2002). In sup-
trapped between September 1995 and May 2001, and
port of the latter opinion, no reproductive isolation was
each was karyotypically analysed by GIAGIA-ATHANASO-
observed between these two forms under laboratory con-
POULOU (personal communication).
176
Panagiotis Kornilios, Basil Chondropoulos and Stella Fraguedakis-Tsolis
TABLE 1
The six known karyotypic forms of Microtus (Terricola) thomasi, their distribution in Greece and the populations that represent these
forms in the present study (2n=diploid chromosome number, FN=fundamental number, n=number of individuals) (karyotypic data
were obtained from GIAGIA & ONDRIAS 1973; GIAGIA 1985; GIAGIA-ATHANASOPOULOU et al. 1995; GIAGIA-ATHANASOPOULOU & STAM-
ATOPOULOS 1997)
Karyotypic form
Karyotype
Distribution
Populations
"thomasi"
2n=44, FN=44
Parts of Central Greece and the central part of
Itea (Fokida pref., Sterea
South Peloponnese
Ellada) (n=27)
Pericentric inversion of the X chromosome
"atticus"
2n=44, FN=46
Parts of Central Greece and the largest part of
Ag. Stefanos (Attiki pref.,
Peloponnese
Sterea Ellada) (n=22)
Tandem fusion between the X chromosome and a small acrocentric autosome
"subalpine"
2n=42, FN=42
Parts of Pindos mountain range, as well as areas Mikrokastro (Kozani pref.,
of eastern Epirus and Western Macedonia
Macedonia) (n=18)
Robertsonian centric fusion of an autosome
"Rb-subalpine"
2n=40, FN=42
Epirus and mountainous Central Greece
Oiti Mt. (Fthiotida pref., Ste-
rea Ellada) (n=12)
Unnamed
2n=41,42,
A small area around Baldouma village, pref. of
Baldouma (Ioannina pref.,
FN=42,43,44
Ioannina (Epirus)
Epirus) (n=15)
Unnamed
2n=38, FN=40
A zone along the Greek-FYROM borders (Cen-
Edessa (Pella pref., Mace-
tral-West Macedonia)
donia) (n=8)
TABLE 2
The allelic data obtained were analysed using BIO-
SYS-1 (SWOFFORD & SELANDER 1981).
The enzymes and loci analyzed, their code numbers, the tissues
they were extracted from and the buffers used (Buffers : A =
25mM Tris - 190mM glycine - pH 8.5, B = 40mM Tris - 10mM
RESULTS
citrate - pH 7.6, C = 40mM phosphate - pH 6.3).
Of the 18 loci examined, 13 (72.2%) were found poly-
E.C.
Enzyme
Tissue
Locus
Buffer
morphic. Three of these 13 loci (Gpi-1, Mpi-1, Idh-1)
number
were polymorphic in only one of the six populations (Ag.
Aconitase
Heart
Aco-1
4.2.1.3.
B
Stefanos) while another locus (Np-1) was polymorphic in
Adenosine deaminase
Spleen
Ada-1
3.5.4.4.
A
all six populations. Each monomorphic locus was fixed
Adenylate kinase
Heart
Ak-1
2.7.4.3.
B
for the same allele in all populations (Table 3).
Creatine kinase
Heart
Ck-1
2.7.3.2.
B
The mean values of the expected (He) and observed
Glutamate oxaloacetate
Kidney
Got-1,2
2.6.1.1.
C
(Ho) heterozygosity, the percentages of polymorphic loci
transaminase
(P%), and the mean number of alleles per locus (A) for
Glucose dehydrogenase
Kidney
Gpd-1
1.1.1.47.
A
each of the examined populations are also shown in Table
Glucose phosphate
Kidney
Gpi-1
5.3.1.9.
A
3. Itea is the population with the most polymorphic loci
isomerase
(50.00%) and also shows the highest mean number of
Isocitrate dehydrogenase
Kidney
Idh-1,2
1.1.1.42.
B
alleles per locus (1.56), whereas Edessa and Baldouma
Lactate dehydrogenase
Kidney
Ldh-1,2
1.1.1.27.
A
are the least polymorphic populations both with 22.22%
Malic enzyme
Liver
Mod-1
1.1.1.40.
B
of loci polymorphic and 1.22 alleles per locus. Low val-
Malate dehydrogenase
Kidney
Mor-1,2
1.1.1.37.
B
ues of heterozygosity characterize all six poplulations.
Mannose phosphate
Kidney Mpi-1
5.3.1.8.
A
This excess of homozygotes is also revealed by the val-
isomerase
ues of the F , F and F indices (W
IS
IT
ST
RIGHT 1951 ; NEI
Nucleoside phosphorylase Kidney
Np-1
2.4.2.1.
A
1977) (Table 4). Indeed, although the genetic loci Gpi-1,
Phosphoglucomutase
Kidney
Pgm-1
2.7.5.1.
A
Idh-1 and Ldh-1 present negative values of the fixation
index F and the locus Idh-1 also presents a negative
After the animals were humanely killed, their heart,
IS
value of F , these values are very small in contrast with
liver, spleen and kidneys were removed and placed in a
IT
the high positive values obtained for all the other cases ;
deep-freezer (-75° C). Skulls and skins of the specimens
this strong general tendency of the F-statistics for positive
are deposited in the collections of the Zoological Museum
values is theoretically known to indicate a deficiency of
of Patra University.
heterozygotes. The mean value of the fixation index FST
of all polymorphic loci reveals that the genetic differenti-
The tissues were homogenized and used for the electro-
ation among the six populations is responsible for 51.6%
phoretic analysis of 14 enzymes coded by 18 loci
of the total genetic variability, whereas intrapopulation
(Table 2) on prepared cellulose acetate plates (Helena
polymorphism is the cause of the remaining 48.4% of this
Laboratories). The electrophoretic procedure was carried
variability (WRIGHT 1951).
out according to TSEKOURA et al. (2002), following meth-
The values of Rogers' genetic similarity varied from
ods developed for other small mammals (SEARLE 1985;
0.614 (Ag. Stefanos and Edessa) to 0.964 (Oiti Mt. and
FRAGUEDAKIS-TSOLIS et al. 1997; HAUFFE et al. 2002).
Edessa), while those of Nei's genetic distance varied from
Intraspecific variation in M. (T.) thomasi
177
TABLE 3
The allelic frequencies for all polymorphic loci, the mean values
of expected (He) and observed (Ho) heterozygosity, the percent-
age of polymorphic genetic loci (P%) and the mean number of
alleles per locus (A) of each studied population (n = number of
individuals collected) (Populations: 1.Itea, 2.Ag. Stefanos,
3.Mikrokastro, 4.Oiti Mt., 5.Edessa, 6.Baldouma).
Fig. 2. UPGMA dendrogram of genetic relationships among
Genetic loci
Populations
the six populations, based on Nei's unbiased genetic distances.
1
2
3
4
5
6
Ada-1
a
0.685
0.000
0.806
0.708
1.000
1.000
TABLE 4
b
0.315
1.000
0.194
0.292
0.000
0.000
Got-1
a
0.889
0.500
0.000
0.000
0.000
0.000
The values of F ,F and F fixation indices of all polymorphic
IS
IT
ST
b
0.111
0.500
1.000
1.000
1.000
1.000
loci
Got-2
a
0.648
0.500
0.000
0.000
0.000
0.000
Locus
F
F
F
b
0.352
0.500
1.000
1.000
1.000
1.000
IS
IT
ST
Gpd-1
a
0.333
0.568
1.000
1.000
1.000
1.000
Ada-1
0.576
0.805
0.541
b
0.667
0.432
0.000
0.000
0.000
0.000
Got-1
1.000
1.000
0.673
Gpi-1
b
0.000
0.886
0.000
0.000
0.000
0.000
Got-2
0.961
0.980
0.485
c
1.000
0.114
1.000
1.000
1.000
1.000
Idh-1
a
1.000
0.909
1.000
1.000
1.000
1.000
Gpd-1
0.775
0.883
0.479
b
0.000
0.000
0.000
0.000
0.000
0.000
Gpi-1
-0.128
0.850
0.867
c
0.000
0.091
0.000
0.000
0.000
0.000
Ldh-1
a
1.000
1.000
0.472
0.083
0.125
0.933
Idh-1
-0.100
-0.015
0.077
b
0.000
0.000
0.528
0.917
0.875
0.067
Ldh-1
-0.056
0.635
0.654
Ldh-2
a
0.241
1.000
0.722
0.167
0.250
0.967
Ldh-2
0.830
0.915
0.499
b
0.759
0.000
0.278
0.833
0.750
0.033
Mod-1
a
0.500
0.000
0.194
0.375
0.571
1.000
Mod-1
0.321
0.593
0.401
b
0.500
1.000
0.806
0.625
0.429
0.000
Mor-1
0.689
0.744
0.175
Mor-1
a
0.926
0.955
1.000
1.000
1.000
0.700
b
0.076
0.045
0.000
0.000
0.000
0.300
Mor-2
0.328
0.381
0.079
Mor-2
a
0.130
0.000
0.056
0.000
0.000
0.000
Mpi-1
1.000
1.000
0.366
b
0.870
1.000
0.944
1.000
1.000
1.000
Np-1
0.286
0.605
0.447
Mpi-1
a
0.000
0.409
0.000
0.000
0.000
0.000
b
1.000
0.591
1.000
1.000
1.000
1.000
Mean
0.545
0.780
0.516
Np-1
a
0.481
0.955
0.222
0.042
0.063
0.133
b
0.481
0.045
0.750
0.917
0.938
0.867
DISCUSSION
c
0.037
0.000
0.028
0.000
0.000
0.000
d
0.000
0.000
0.000
0.042
0.000
0.000
The percentage of polymorphic loci (72.2%) of the
n
27
22
18
12
8
15
populations studied is quite high compared to those calcu-
He
0.187
0.143
0.115
0.085
0.071
0.048
lated by GRAF (1982), which varied from 27.3% to
Ho
0.053
0.035
0.080
0.051
0.071
0.048
42.1%, for a number of arvicolid species not including M.
P%
50.00
44.44
33.33
27.78
22.22
22.22
(T.) thomasi. That author also calculated a mean value of
A
1.56
1.44
1.39
1.33
1.22
1.22
the percentage of heterozygosity per locus for the Arvi-
colidae family (4.3% ± 2.5%), which he considered rela-
tively high compared to other mammals. Our values vary
from 3.0% (Baldouma) to 8.0% (Mikrokastro) and are
0.004 (Oiti Mt. and Edessa) to 0.374 (Ag. Stefanos and
similar to those of Graf. Therefore, we could conclude
Edessa) (Table 5).
that the populations examined in the present study are
characterized by a pronounced genetic variability.
The UPGMA dendrogram of the genetic relationships
between the six populations, resulting from the Nei's dis-
The F-statistics reveal a general excess of homozy-
tance values, is shown in Fig. 2. It demonstrates a clear
gotes in the populations examined (F ,F >0), evincing
IS
IT
separation of the Ag. Stefanos population, with the rest of
the tendency of most polymorphic loci to stabilize some
the examined populations being divided into two groups:
of the alleles, perhaps resulting from a population subdi-
one including the Itea population and another one com-
vision into smaller units (tribes, families), a fact that has
prising all the others. The population of Baldouma
also been confirmed for other species of this genus
branches next, while the other populations form two
(NYGREN & RASMUSON 1980). The presence of loci that
branches : one of them involves the Mikrokastro popula-
exhibit negative values of F and F (Gpi-1, Idh-1, Ldh-
IS
IT
tion, and the other the populations of Oiti Mt. and Edessa.
1), could be due to positive selection of heterozygotes.
178
Panagiotis Kornilios, Basil Chondropoulos and Stella Fraguedakis-Tsolis
TABLE 5
Values of ROGERS' genetic similarity (below diagonal) and NEI'S unbiased genetic distance (above diagonal)
between the six populations studied.
Itea
Ag. Stefanos
Mikrokastro
Oiti Mt.
Edessa
Baldouma
Population
(2n=44, FN=44)
(2n=44, FN=46)
(2n=42, FN=42)
(2n=40, FN=42)
(2n=38, FN=40)
(2n=41,42, FN=42,43)
Itea
-
0.193
0.162
0.186
0.184
0.182
(2n=44, FN=44)
Ag. Stefanos
0.738
-
0.225
0.337
0.374
0.309
(2n=44, FN=46)
Mikrokastro
0.775
0.698
-
0.030
0.030
0.063
(2n=42, FN=42)
Oiti Mt.
0.779
0.634
0.919
-
0.004
0.119
(2n=40, FN=42)
Edessa
0.771
0.614
0.910
0.964
-
0.086
(2n=38, FN=40)
Baldouma
0.748
0.667
0.880
0.836
0.871
-
(2n=41,42, FN=42,43)
The mean value of the fixation index F (0.516)
FN=40). The Edessa population karyotype, as already
ST
reveals that the populations studied present about equal
mentioned, is closely related to the "Rb-subalpine" one
inter- and intrapopulation genetic variability.
(GIAGIA-ATHANASOPOULOU & STAMATOPOULOS 1997),
Moreover, GRAF (1982) calculated mean Nei's genetic
which, in turn, has emerged from the "subalpine" type
distances for different taxonomic levels within the family
(GIAGIA-ATHANASOPOULOU et al. 1995). The Baldouma
Arvicolidae. However, a recent study on Greek popula-
population can be regarded as a hybrid one, because it
tions of M.(T.) thomasi showed that their genetic dis-
consists of individuals with the "subalpine" karyotype
tances do not agree with those given by Graf for the popu-
(2n=42, FN=42) and hybrids with 2n=41, FN=43, result-
lation level, and appear to be much greater (TSEKOURA et
ing from crosses of "Rb-subalpine" (2n=40, FN=42)
al. 2002). This conclusion is also verified by our results,
individuals with 2n=42, FN=44 ones, the latter not being
suggesting that M.(T.) thomasi exhibits an intraspecific
included in our sample (Table 1) (GIAGIA-ATHANASOPOU-
variability much higher compared to other European
LOU & STAMATOPOULOS 1997). Therefore, this population
Microtus species. Therefore, it appears that GRAF's con-
is expected to have intermediate karyotypic characteris-
clusions should be revised to include the case of M. (T.)
tics between the populations of Mikrokastro and Oiti Mt..
thomasi, which does not seem to follow GRAF's pattern.
Our results confirm this point, since the population of
Nonetheless, it is worth mentioning that, as has also been
Baldouma exhibits similar values of genetic distance
indicated in TSEKOURA et al. (2002), our results show that
from both these two populations (Table 5, Fig. 2).
the population of Ag. Stefanos presents the highest
The results of the electrophoretic analysis and the clus-
genetic distances from all the other populations.
tering of the populations examined agree to a large extent
The UPGMA dendrogram (Fig. 2) indicates a clear
with the karyological data. This correspondence encour-
separation of the "atticus" karyotype population (Ag.
ages us to make further attempts to clarify genetic rela-
Stefanos) from all others. Among the latter ones, consist-
tionships among the Greek populations of this species.
ing of two main groups, the population with the original
Our main approach will concern more electrophoretic and
"thomasi" karyotype (Itea) separates from all populations
other molecular studies of populations belonging to the
with polymorphic karyotypes. With the exception of the
already known karyotypic forms and any as yet undiscov-
Ag. Stefanos population, this clustering is in agreement
ered ones.
with the pattern of karyotype evolution within Microtus
thomasi in the area of Greece, as indicated in Table 1. The
ACKNOWLEDGEMENTS
genetic differentiation of the population of Ag. Stefanos
which has a derived karyotype ("atticus", 2n=44,
FN=46), is possibly due to particular environmental con-
We thank Dr. C. Stamatopoulos and Dr. G. Tryfonopoulos,
University of Patras, who collected part of the animal material
ditions that prevailed in this sampling area alone (inten-
studied in this work. We are also grateful to reviewers for their
sive urbanization and other human activities). This area
critical comments and suggestions, which provided considerable
was selected because it is the closest available to the terra
improvements to our manuscript.
typica of the originally described vole taxon Pitymys atti-
cus Miller, 1910, from which later the "atticus" karyo-
type was firstly described (G
REFERENCES
IAGIA & ONDRIAS 1973 ;
GIAGIA 1985).
C
Within the cluster of the polymorphic karyotypes, the
ORBET, G. B. (1978). The mammals of the Palearctic region : a
taxonomic review. British Museum (Natural History), Cor-
population of Baldouma (2n=41,42, FN=42,43) separates
nell University Press, New York.
from the others, which form two groups : one composed
FRAGUEDAKIS-TSOLIS, S.E., H.C. HAUFFE & J.B. SEARLE (1997).
of the population of Mikrokastro (2n=42, FN=42-"subal-
Genetic distinctiveness of a village population of house
pine") and another composed of the populations of Oiti
mice : relevance to speciation and chromosomal evolution.
Mt. (2n=40, FN=42-"Rb-subalpine") and Edessa (2n=38,
Proc. R. Soc. Lond. B, 264 : 355-360.
Intraspecific variation in M. (T.) thomasi
179
GIAGIA, E.B. (1985). Karyotypes of "44-chromosomes" Pitymus
genetic relationships among Greek rodents of the families
species (Rodentia, Mammalia) and their distribution in
Arvicolidae and Muridae. J. Zool. Lond., 228 : 445-453.
Southern Greece. Säugetierk. Mitt., 32 : 169-173.
NEI, M. (1977). F-statistics and analysis of gene diversity in
GIAGIA, E.B. & J.C. ONDRIAS (1973). Karyological analysis of
subdivided populations. Ann. Hum. Genet., 41 : 225-233.
the vole Pitymus atticus (Rodentia, Mammalia) from
NYGREN, J. & M. RASMUSON (1980). Allozyme variation in nat-
Greece. Biol. gallo-hellen., 4 : 205-212.
ural populations of field vole (Microtus agrestis L.) : I. Sur-
GIAGIA-ATHANASOPOULOU, E.B. & C. STAMATOPOULOS (1997).
vey of the "semi-stable" population in southern Sweden.
Geographical distribution and interpopulation variation in
Hereditas, 92 : 65-72.
the karyotypes of Microtus (Terricola) thomasi (Rodentia,
PETROV, B.M. (1992). Mammals of Yugoslavia : Insectivores
Arvicolidae) in Greece. Caryologia, 50 : 303-315.
and rodents. Natural History Museum of Belgrade, Bel-
GIAGIA-ATHANASOPOULOU, E.B., B.P. CHONDROPOULOS & S.E.
grade.
FRAGUEDAKIS-TSOLIS (1995). Robertsonian chromosomal
PETROV, B. & S. ZIVCOVI ´C (1972). Zur Kenntnis der Thomas-
variation in subalpine voles Microtus (Terricola), (Rodentia,
Kleinwuhlmaus, Pitymus thomasi (Barrett-Hamilton, 1903)
Arvicolidae) from Greece. Acta theriol., 40 : 139-143.
eines der wenig bekannten Säugetiere Jugoslawien. Säuge-
GRAF, J.D. (1982). Génétique biochimique, zoogeographie et
tierk. Mitt., 20 : 249-258.
taxonomie des Arvicolidae (Mammalia, Rodentia). Rev.
P
suisse Zool., 89 : 749-787.
ETROV, B.M. & S. ZIVKOVI ´C (1979). Present knowledge on the
systematics and distribution of Pitymys (Rodentia, Mamma-
HAUFFE, H.C., S. FRAGUEDAKIS-TSOLIS, P.M. MIROL & J.B.
lia) in Yugoslavia. Biosistematika, 5 : 113-125.
SEARLE (2002). Studies of mitochondrial DNA, allozyme
and morphometric variation in a house mouse hybrid zone.
SEARLE, J.B. (1985). Isoenzyme variation in the common shrew
Genet. Res. Camb., 80 : 117-129.
(Sorex araneus) in Britain in relation to karyotype. Heredity,
K
55 : 175-180.
ING, M. (1993). Species Evolution : The role of chromosome
change. Cambridge University Press, Cambridge.
SEARLE, J.B. (1993). Chromosomal hybrid zones in Eutherian
K
mammals. In : H
RATOCHVÍL, J. (1971). Der Status der Populationen der Gattung
ARRISON R.G. (ed.), Hybrid zones and the
Pitymus aus Attika (Rodentia, Mammalia). Zool. Listy, 20 :
evolutionary process, Oxford University Press, New York :
197-206.
309-351.
MILLER, G.S., (1910). Description of six new European mam-
STAMATOPOULOS, C. & J.C. ONDRIAS (1986). Observations on
mals. Ann. Mag. Nat. Hist. London, (8)6 : 458-461.
the underground activity and behavior of the vole Pitymys
MILLER, G.S. (1912). Catalogue of the mammals of Western
atticus (Mammalia, Rodentia). Säugetierk. Mitt., 33 : 253-
Europe (Europe exclusive of Russia) in the collection of the
259.
British Museum. British Museum (Natural History), London.
SWOFFORD, D.L. & R.B. SELLANDER (1981). BIOSYS-1 : a
MITCHELL-JONES, A.J., G. AMORI, W. BOGDANOWICZ, B.
FORTRAN program for the comprehensive analysis of elec-
KRYSTUFEK, P.J.H. REIJNDERS, F. SPITZENBERGER, M.
trophoretic data in population genetics and systematics. J.
STUBBE, J.B.M. THISSEN, V. VOHRALÍK & J. ZIMA (1999). The
Hered., 72 : 281-283.
Atlas of European Mammals, Academic Press, London.
TSEKOURA, N., S. FRAGUEDAKIS-TSOLIS, B. CHONDROPOULOS &
NIETHAMMER, J. (1974). Zur Verbeitung und Taxonomie griech-
G. MARKAKIS (2002). Morphometric and allozyme variation
scher Saügetiere. Bonn. Zool. Beitr., 25 : 28-55.
in central and southern Greek populations of the vole Micro-
NIETHAMMER, J. & F. KRAPP (1982). Handbuch der Säugetiere
tus (Terricola) thomasi (Rodentia, Arvicolidae). Acta the-
Europas. Akademische Verlagsgesellschaft, Wiesbaden.
riol., 47 : 137-149.
NIKOLETOPOULOS, N.P., B.P. CHONDROPOULOS & S.E.
WRIGHT, S. (1951). The genetical structure of populations. Ann.
FRAGUEDAKIS-TSOLIS (1992). Albumin evolution and phylo-
Eugen., 15 : 323-354.
Belg. J. Zool., 135 (2) : 181-190
July 2005
Neogene/Quaternary mammalian migrations in Eastern
Mediterranean
George D. Koufos*, Dimitris S. Kostopoulos* and Theodora D. Vlachou*
* Aristotle University of Thessaloniki, Department of Geology. Laboratory of Geology and Palaeontology. 54124 Thessaloniki,
Greece. e-mail :koufos@geo.auth.gr
ABSTRACT. Palaeogeographic and climatic changes in the Eastern Mediterranean during the Neogene/Quaternary
led to extended mammalian migrations and faunal exchanges between Eurasia and Africa. At the same time, the
Beringian landbridge was activated several times, and American faunal elements entered Eurasia. It appears that the
main factor affecting migration potential and faunal changes/exchanges during the Neogene was palaeogeography,
while after the early Pliocene migrations were mainly controlled by climatic changes. Several mammalian migra-
tions can be distinguished, but the most important was that of the middle Orleanian at about 17.0-18.0 Ma when
Africa and Eurasia were connected after a long separation and a great number of African faunal elements entered
Eurasia and vice versa. Some more important faunal changes also occurred : 1. at ~5.5 Ma, marking the beginning
of the Pliocene, 2. at ~ 2.0-1.8 Ma, marking the beginning of the Pleistocene, and 3. at ~1.0 Ma, defining the early/
middle Pleistocene boundary and the establishment of modern mammal fauna. During the Pleistocene, oscillation of
glacial and inter-glacial periods caused an alternation of cold-steppic faunas with temperate ones in the Eastern
Mediterranean. Endemic late Pleistocene mammalian faunas developed in the Mediterranean islands after their
isolation ; "dwarf" elephants, cervids and hippos occurred, as well as giant rodents.
KEY WORDS : Eastern Mediterranean, Neogene/Quaternary, Mammalia, migration, faunal changes, paleobiogeogra-
phy.
INTRODUCTION
MIGRATION FACTORS
The migration of a mammal depends upon various fac-
The Eastern Mediterranean is regarded as an impor-
tors. The most important are topographic/physicogeo-
tant domain for mammal exchanges between Asia,
graphic and climatic parameters. Geographic barriers,
Europe and Africa during the Neogene/Quaternary. The
such as high mountain chains and/or sea channels are
enlarged area of the Eastern Mediterranean includes the
restrictive for the migration of mammals. Knowledge of
Balkan Peninsula, the Aegean Sea, Asia Minor and the
the palaeogeography (global or regional) during the vari-
Middle East. In this geographic region migration path-
ous geological periods is essential to extrapolation of
ways between the three continents crossed. The number
migration waves and faunal turnovers. Climatic condi-
of localities for mammal fossils found in the Eastern
tions and the palaeoenvironment of the origin and arrival
Mediterranean is quite significant, providing a good
areas also control migration potential. Animals adapted to
base for further comparisons and discussion. The geo-
warm climatic conditions cannot occupy cool areas and
logical age of the faunas and the palaeogeography of the
vice versa.
area are already well known from previous and essential
The size of an animal and the migration distance are
works. However, the scarcity of the fossil record and the
positively related. A large-sized animal can cover a long
limited dating of several sites is a great disadvantage to
migration distance during its life-span, while a micro-
reconstruct the palaeobiogeography.
mammal (e.g. a rodent) usually needs more generations in
order to cover the same distance or to pass a significant
topographical barrier. In this case evolution and migration
The main Neogene/Quaternary mammalian migration
can be simultaneous.
waves between Eurasia and Africa are associated with
important mammal turnovers, climatic and tectonic
The study of past migrations presupposes a good
knowledge of taxonomy and age of the fossils. The taxo-
changes and in some cases also include mammalian forms
nomic determination of the mammalian fossils is an
arrived from America via the Beringian landbridge. The
important factor for establishing mammal migration and
present article combines available data from the men-
distribution. Differences in the definition of a "biologi-
tioned region and neighbouring ones, in order to extract
cal" and "palaeontological" taxon make the taxonomic
the main migrations, the time spans during which they
determination of fossils more delicate. Geologic timing is
occurred and the palaeogeographic conditions under
another important factor. The age of mammalian faunas is
which they took place. Our work also focuses on the
determined either biochronologically (based on the faunal
arrival of some important taxa into Greece and their sig-
composition and its evolutionary stage) or radiometrically
nificance in establishing the evolution of Greek faunas.
if possible. Magnetostratigraphy also provides good age
182
George D. Koufos, Dimitris S. Kostopoulos and Theodora D. Vlachou
resolution, but the method has not been extensively used
During that time the Northern Aegean was a continental
in continental mammal-bearing deposits. During the last
domain with low relief (DERMITZAKIS & PAPANIKOLAOU,
30 years new methods were developped allowing quite
1981).
precise age determination for the fossil mammalian fau-
nas providing a good base for comparisons.
GEOTECTONIC BACKGROUND
It is generally accepted that during the entire Neogene/
Quaternary there was a continuous connection between
Europe and Asia, in the north Caspian region. The South
European area and especially its eastern part was defi-
nitely formed during this period, by alpine orogenesis,
extending the terrestrial communication between Asia
and Europe. The following Quaternary tectonism and eus-
tatic movements did not change dramatically the geogra-
phy of the area, but were mainly of local significance.
Neogene was also a time of important geotectonic events
that allowed successive connections between Eurasia and
Africa, creating great opportunities for faunal exchanges
between these continents. The most important Neogene/
Quaternary palaeogeographic changes are schematically
given in the palaeomaps of STEININGER & RÖGL (1985)
and RÖGL (1999), used as background for our work. Geo-
logical time is mainly expressed by the system of Mam-
mal Biozones of MEIN (1990, 1999), which permits defi-
nition and recognition of small time-units and correlation
between neighboring areas (Fig. 1).
AGENIAN-EARLY ORLEANIAN MIGRATION
(23.8-18.0 MA)
During the Oligocene/Miocene boundary a deep trough
between Arabian and Iranian plates, known as Tethyan
Seaway (Fig. 2A), allowed communication of the Medi-
terranean with the Atlantic and the Indo-Pacific Oceans.
The closure of the Tethyan Seaway was gradual, starting
at ~19.0 Ma, and continuing until the end of MN 3 at
~18.0 Ma (RÖGL, 1999). At the same time, Asia commu-
nicated with America through the Beringian landbridge
and an important immigrant, the equid Anchitherium,
invaded Asia. It rapidly dispersed to Europe as it is
known from MN 3 of the Iberian Peninsula (MEIN, 1990).
Anchitherium is unknown in the Balkan Peninsula, while
it appeared in MN 6 of Asia Minor (FORSTEN, 1990 ; NOW
2002). Its absence from the Balkans could suggest that the
area was not connected with Asia Minor, or more likely,
that it has not yet been found there. Some inner-Eurasian
faunal exchanges have also been recognized. In W.
Europe the suids Hyotherium appeared in MN 1 and
Xenohyus in MN 2 (M
Fig. 1. Chronologoical table for Neogene/Quaternary with
ADE, 1990), and the anthracothere
the European land mammal stages and MN-Zones. According
Brachyodus in MN 3 (MEIN, 1990). The MN 1-3 faunas
to MEIN (1990), STEININGER et al. (1990) and STEININGER
are very rare in the Eastern Mediterranean. However, the
(1999).
presence of Brachyodus is recorded in the locality of
Kalimeriani, Greece (MELENTIS, 1966). The sole speci-
men of Brachyodus cannot give a precise age for the
MIDDLE ORLEANIAN MIGRATION
locality, but an MN 3-4 age was suggested (BONIS &
(18.0-17.0 MA)
KOUFOS, 1999). The first spalacid Debruijnia is known
from MN 3 of Asia Minor, while it was also found in
The Arabian and Anatolian plates collided at the end of
Aliveri, Greece, dated at the base of MN 4 (DE BRUIJN et
MN 3 (middle Orleanian) re-establishing communication
al., 1992). These data suggest an early connection of Asia
between Africa and Eurasia (Fig. 2B). The landbridge
Minor with the Balkan Peninsula at the end of MN 3.
connecting the two continents is known as "Gomphoth-
Neogene/Quaternary mammalian migrations in Eastern Mediterranean
183
erium-landbridge" (RÖGL, 1999 ; AGUSTI et al., 2001).
with Europe allowed its migration to the Balkans and
The closure of the Tethyan Seaway probably provided an
Central Europe during MN 4 (SCHMIDT-KITTLER, 1999).
earlier connection with Asia as Pliohyrax, originating
from Africa, was found in India at the end of MN 3 (PICK-
FORD, 1986). Its presence in the Eastern Mediterranean is
reported later in the locality of Pasalar, Turkey, dated to
MN 6 (NOW, 2002). This earlier connection is also con-
firmed by the recent trace of a primitive deinothere Pro-
deinotherium in Lesvos island, Greece. Its dental mor-
phology and the absolute age of the sediments including
it, suggest an age of >18.4 Ma (KOUFOS et al., 2003). This
means that before the final closure of the Tethyan Sea-
way, there were some early short or temporary land-
bridges connecting Africa and Eurasia (before 18.0 Ma),
allowing the entrance of some mammals. The Indopacific
Seaway to the Eastern Paratethys was closed too. The
western part of Paratethys was also closed and thus it
became an isolated basin with endemic fauna and reduced
salinity (RÖGL, 1999). The Balkan Peninsula was com-
pletely connected with Asia Minor (Fig. 2C) except for
some lakes or lagoons in the northern Aegean area (DER-
MITZAKIS & PAPANIKOLAOU, 1981).
A great number of African taxa migrated to Eurasia
through the "Gomphotherium-landbridge", while a simul-
taneous migration is also traced from Eurasia to Africa.
The fauna of Negev in Israel, dated to MN 3, corresponds
to the first exchange between them as it includes a mixed
fauna with African (Prodeinotherium, Gomphotherium,
Anasipora, Dorcatherium, Kenyalagomys, Megapedetes)
and Asian (Eotragus, Listriodon, Rhinocerotidae) ele-
ments (TCHERNOV et al., 1987 ; AGUSTI et al. 2001 ; PICK-
FORD 2001). Recent radiometric data suggest an age of
~20.7 Ma for this event (RÖGL, 1999). The first African
immigrants were the proboscideans ; the gomphotheres
and the deinotheres, arriving in India (Bugti Fauna) at
~18.3 Ma (BARRY et al., 1985 ; TASSY, 1990) and in East-
ern Mediterranean at ~18.4 Ma (KOUFOS et al., in press).
The proboscideans rapidly dispersed in W. Europe as they
Fig. 2. Palaeogeographic map of Mediterranean region with
the main mammalian migration pathways and arrivals in East-
were found in the Iberian Peninsula at the beginning of
ern Mediterranean.
MN 4, ~ 18.0 Ma (TASSY, 1990).
a) Agenian-early Orleanian (MN 1-3)
b) Middle Orleanian (MN 4)
Several Asian taxa, such as the bovid Eotragus, the
c) Late Orleanian-Early Astaracian (MN 5-6)
suid Bunolistriodon, the nimravid Prosansanosmilus and
Palaeogeographic maps from RÖGL (1999).
the rodents Megacricetodon, Democricetodon, Criceto-
don, Eumyarion e.t.c. migrated also to Europe and/or to
Africa (AGUSTI et al., 2001 and literature listed). The sub-
family Democricetodontinae appeared in Asia Minor dur-
LATE ORLEANIAN-ASTARACIAN
ing the early Miocene (MN 1-2) and then migrated to
MIGRATIONS (17.0-10.7 MA)
Africa and Asia (MN 3), as well as to America through
the Beringian landbridge (MN 3-4). During MN 4 the
subfamily appeared in the Balkans and Western Europe
A succession of short-term sea level oscillations during
(THEOCHAROPOULOS, 1999).
this time interval caused several changes to the palaeoge-
ography of the Eastern Mediterranean. There is evidence
Many Asian and African immigrants arrived in Greece
of a late Orleanian transgression, re-opening the Tethyan
too. The genera Megacricetodon, Democricetodon and
Seaway (RÖGL, 1999). Thus, the landbridge between
Karydomys are recognized in Aliveri (early MN 4), Kary-
Africa and Eurasia was active for short periods allowing
dia and near Komotini (upper MN 4) (THEOCHAROPOU-
faunal migrations between the two continents (Figs 2C,
LOS, 1999). The first carnivores (Palaeogale, Euboictis)
3A). However, such short-term connections between the
appeared in Aliveri, Evia dated at the base of MN 4 (DE
continents are not confirmed by mammal evidence. In any
BRUIJN et al., 1992). The genus Euboictis has possibly a
case three migration waves can be recognized at this
southern Asian origin and the connection of Asia Minor
time :
184
George D. Koufos, Dimitris S. Kostopoulos and Theodora D. Vlachou
fid Georgiomeryx, the tragulid Dorcatherium, and the
ctenodactylid Sayimys indicate African origin confirming
the above-mentioned connection. The proboscidean
Choerolophodon, appeared firstly in Chios island coming
probably from Asia since it was already present in the
Bugti fauna, India, dated to MN 3, or ~18.3 Ma (TASSY,
1990). However, the most important arrival was that of
the primates, originating from Africa and invading Eura-
sia during MN 5. The first primates with the genus Pliop-
ithecus are known from the localities of Elgg (Switzer-
land) and Pontlevoy-Thenay (France) dated to MN 5, and
they existed until the end of Vallesian (ANDREWS et al.,
1996).
b. A second migration wave from Africa during early
Astaracian, MN 6 (15.0-13.5 Ma) brought several immi-
grants into Eurasia and the Eastern Mediterranean (Fig.
2C). The most important new element was the hominoid
Griphopithecus of African affinities. It was recognized in
the Turkish localities of Pasalar and Candir, as well as in
Neudorf-Sandberg, Slovakia, all dated to MN 6. The Eur-
Asian Griphopithecus is related to the African Kenyap-
ithecus known from Maboko, East Africa dated to MN 4
(ANDREWS et al., 1996). The arrival of the aardwark
Orycteropus in the Eastern Mediterranean is also referred
to this wave. The genus has African origin and its oldest
remains out of Africa are those from Pasalar, Turkey
dated to MN 6 (FORTELIUS, 1990). During MN 6 some
asian elements also entered into Europe, such as the hyra-
coid Pliohyrax, the cervid Dicroceros and the suid Listri-
odon (THENIUS, 1952 ; MADE, 1990). The hyracoids origi-
nated from Africa and entered into the indian
subcontinent at the end of MN 3. Pliohyrax dispersed
eastwards in MN 6, appeared in the Eastern Mediterra-
nean locality of Pasalar Turkey, dated to MN 6
(FORTELIUS, 1990). Several asian bovids (Protragocerus,
Tethytragus and Hypsodontus) known from MN 5 of Asia
Minor and Chios island migrated to Africa.
Fig. 3. Palaeogeographic map of Mediterranean region with
c. A third migration wave from Africa seems to have
the main mammalian migration pathways and arrivals in East-
taken place, mainly in MN 8, but the poorly known late
ern Mediterranean.
a) Late Astaracian (MN 7+8)
Astaracian, MN 7+8 (13.5-10.7 Ma), faunas of the East-
b) Late Miocene (MN 9-12)
ern Mediterranean do not allow detailed conclusions. The
c) Latest Miocene (MN 13)
most important appearance was that of the hominoid Dry-
Palaeogeographic maps from RÖGL (1999) and STEINIGER &
opithecus in Europe at about 12.5 Ma ago (Fig. 3A). The
RÖGL (1985).
Asian suid Propotamochoerus entered Europe at that time
(MADE, 1999). The genus Cricetulodon arrived in the area
a. During the late Orleanian, MN 5 (17.0-15.0 Ma) a
at the end of MN 7+8 and it is known from Turkey and
migration wave from Africa arrived in the Eastern Medi-
Greece (KOUFOS, 2003). The genus is known from MN 3
terranean. The Greek fauna of Antonios, Chalkidiki dated
of W-C Europe where it persisted until MN 7+8 (AGUSTI
to MN 4/5 at ~17.0 Ma (KOUFOS & SYRIDES, 1997) fits
et al. 2001 ; NOW, 2002). According to RÖGL (1999) dur-
quite well with it. The Antonios fauna includes a small-
ing the late Astaracian there was a seaway between Para-
sized Dorcatherium very close to the small-sized African
tethys and Mediterranean, prohibiting the migrations.
form described by PICKFORD (2001). The giraffid Palae-
These data suggest that at the end of MN 7+8 the connec-
omeryx is another African element present in Antonios
tion between Europe and Asia was fully established.
fauna. The sanitheres known from MN 3 of Africa
migrated to Asia (PICKFORD, 1984) at the end of MN 3. In
the Eastern Mediterranean they appeared firstly in Anto-
LATE MIOCENE MIGRATION
nios fauna. These data indicate a short-term mammal
(10.7-6.7 MA)
invasion, may be before the re-opening of the Tethyan
Seaway. The locality of Thymiana, Chios Island, Greece
The arrival of Hipparion in Eurasia from America,
includes strong evidences of a migration from Africa dur-
known as Hipparion-datum is a major event used exten-
ing this time span. The locality is dated to MN 5 or to
sively in biostratigraphy and biochronology as a marker
15.5 Ma according to magnetostratigraphic data (KON-
of the beginning of the late Miocene (MN 9). A strong sea
DOPOULOU et al., 1993 ; DE BONIS et al., 1998). The giraf-
level drop around 11.0 Ma re-opened the Beringian land-
Neogene/Quaternary mammalian migrations in Eastern Mediterranean
185
bridge (HAQ et al., 1988) and some North-American
During this time-span a significant number of homi-
mammals entered Eurasia. However, there are different
noids appeared, representing a local European evolution.
opinions about the age of Hipparion-datum in Europe.
BEGUN (2001) proposed that Dryopithecus, after its
The available faunal and magnetostratigraphic data from
appearance to Europe, evolved and then, during the late
Spain suggest an age of 11.1 Ma (GARCES et al., 1997). In
Miocene dispersed to the whole of Eurasia, giving rise to
the Eastern Mediterranean recent magnetostratigraphic
various forms, while at the end of the Miocene it re-
data from Turkey suggest an age of 10.7 Ma (KAPPELMAN
entered Africa. The genera, Dryopithecus in W-C.
et al., 2003). Similar dating is also proposed for the Hip-
Europe, Oreopithecus in Italy, Ankarapithecus in Turkey,
parion-datum in Pakistan 10.7 Ma (PILBEAM et al., 1996).
Sivapithecus in India and Lufengpithecus in China are
Thus, the beginning of late Miocene (arrival of Hippa-
representatives of the late Miocene group of hominoids.
rion) must be considered at 10.7 in the Eastern Mediterra-
In Greece the hominoid primate Ouranopithecus macedo-
nean, at the moment. The hipparionine horses immedi-
niensis with an age from 9.0-9.6 Ma was found in the
ately entered Africa and dispersed rapidly to the whole
localities Ravin de la Pluie and Xirochori of Axios valley
continent, remaining until the beginning of the Pleis-
and Nikiti 1, in Chalkidiki (DE BONIS & KOUFOS, 1999 ;
tocene.
KOUFOS, 1993, 1995). Ouranopithecus is of special inter-
est as it has strong relationships with the Plio-Pleistocene
During the late Miocene there was a short landbridge
hominines (DE BONIS & KOUFOS, 2001).
between Africa and Eurasia (Fig. 3B), while the Red-Sea
was more or less formed (RÖGL, 1999). This landbridge
allowed faunal exchanges with the most important arrival
LATEST MIOCENE MIGRATION
being that of the cercopithecid Mesopithecus. The genus
(6.7-5.3 MA)
is very well known in Greece (Pikerni, Axios valley, Mar-
amena), but it is also known in Bulgaria, Former Yugosla-
Although basin re-organization around the Mediterra-
vian Republic of Macedonia (FYROM), Afghanistan, and
nean provoked several regional phenomena of isolation
Iran. Its first appearance in the Eastern Mediterranean
already during the middle Late Miocene (late Tortonian,
was recorded in Axios valley, Greece at ~8.2 Ma (KOU-
MN 12 ; KRIJGSMAN et al., 2000), accumulated data from
FOS, in press.). The giraffids are well represented by sev-
Spain, Italy, Sicily, Gavdos, Crete and Cyprus suggest
eral genera, such as Palaeotragus, Bohlinia, Samoth-
that a major isochronous palaeoenvironmental change at
erium, Helladotherium (Fig. 3B). The different climatic
6.8-6.7 Ma affected the entire Mediterranean (KRIJGSMAN
and environmental conditions between South-Eastern and
et al., 2002). This age marks the beginning of MN 13
Central-Western Europe did not allow to these large-sized
zone, characterized by an important mammal turnover
mammals to pass into the occidental part. Only the small-
(AGUSTI et al., 2001). It seems that at 6.1 Ma an ephem-
sized Palaeotragus migrated to W.-C. Europe.
eral landbridge between Africa and Europe already
However, the most important arrivals during the late
existed in the Gibraltar area, caused by the emergence of
Miocene were those from Asia. The invasion of Hippa-
the Betics intamontane basins, allowed the first terrestrial
rion into Eastern Mediterranean was accompanied by the
faunal exchange between these two lands across the Ibe-
arrival of several Asian mammal immigrants such as the
rian peninsula (GARCES et al., 1998). At 5.9 Ma a climatic
large hyaena Dinocrocuta, the ictitheres and the exten-
trend towards increased aridity and continentality com-
sively known hyaena Adcrocuta. The suid Microstonyx
bined with the continuous tectonic convergence between
appeared in the Eastern Mediterranean at the end of MN
Africa and Europe and the uplift of the Spanish and NW
10 or more precisely at ~9.0 Ma (K
African mountain chains, caused the closure of the Ibe-
OSTOPOULOS, 1994 ;
K
rian and Rifian Seaways and the definitive isolation of the
OUFOS, 2000). The carnivores Plesiogulo and Chas-
maporthetes entered Eastern Mediterranean from Asia
Mediterranean basin from the Atlantic ocean (STEININGER
and were found in the Greek localities of Vathylakkos and
& RÖGL, 1985 ; PARTRIDGE, 1997 ; DINARES-TURELL et
Ravin des Zouaves-5, dated at ~7.5 Ma and 8.2 Ma
al., 1999). Conditions of high evaporation in the Mediter-
respectively (S
ranean led to a significant sea level drop (more than 200m
EN et al., 2000). The Asian bovid associa-
tion, arriving at the same time, included many genera,
according to deltaic deposits) and the deposition of thick
such as Tragoportax, Gazella, Prostrepsiceros, Nisidor-
evaporitic beds, starting at 5.96 Ma (KRIJGSMAN et al.,
cas, Protoryx, Palaeoryx, but most of them did not pass to
2002). More or less at the same time the Beringian land-
the west of Europe. Among the small mammals invading
bridge was re-activated as a result of a global regression,
the area the genus Progonomys, of Asian origin, arrived
allowing several mammalian taxa to invade Eurasia from
in the Eastern Mediterranean at ~ 10.1 Ma (K
N. America (Alilepus, ancestor of Leporidae). The Cen-
APPELMAN et
al., 2003). There is a clear diachrony in its distribution as
tral Paratethys was divided in two intermountain basins :
it is known from Pakistan at 12.3 Ma and from Spain at
the Dacian Basin in Romania and the Pannonian Basin in
9.64-9.74 Ma (P
Hungary. Sea temperatures in the Mediterranean for that
ILBEAM et al., 1996 ; AGUSTI et al., 1997).
The rodent Parapodemus is known from MN 12 of the
period apparently showed strong fluctuations, with short
Eastern Mediterranean, and arrived in the area from the
warm and cold seasons. The relative fall of humidity and
north. Other rodents are the genera Byzantinia, Occitano-
temperature in the continent allowed expansion around
mys, and Apodemus, all of Asian origin (A
the Mediterranean of hard-leaved evergreen forests, but
GUSTI et al.,
2001; K
the peri-Mediterranean flora was not dramatically
OUFOS, 2003). Thus, an extended bioprovince of
savannah character was established from the Balkans to
changed (SUC, 1986 ; SUC et al., 1995)
Iran-Afganistan, named Creco-Iranian Province (BONIS et
These important physiogeographic transformations
al., 1993).
provided new migration pathways for mammals, and
186
George D. Koufos, Dimitris S. Kostopoulos and Theodora D. Vlachou
allowed more rapid and easy faunal exchanges between
(Fig. 4A). The uplift of the Alpine chain separated North-
Africa and Europe. The main way between Africa and
ern-Central from Southern Europe distinguishing their
Eurasia in the Middle East remained open, as the Saharo-
biotopes. The Black Sea was restricted more or less at its
Arabic channel was not a significant obstacle for large
present limits, while the Caspian Sea formed a larger
mammals. However, the supposed connection between
marine/submarine system ; communication between these
Africa and Europe across Tunis-Sicily or Sardinia-Cor-
two basins was possible, but not certain. The continuous
sica-Tuscuny was no longer sustainable, since the faunal
northward drift of the Arabian plate allowed definitive
data from this area indicate a high endemism, plausibly
opening of the Red Sea, but the African-Middle East
suggesting an insular palaeoprovince (BERNOR et al.,
migration pathway remained active. Climatic conditions
2001). The exchange of mammals between the Iberian
changed to more warm and wet. This is clear from the
Peninsula and Africa is fully substantiated by the study of
extended Pliocene lignitic deposits in Greece, Turkey,
micromammals (THOMAS et al., 1982, AGUSTI et al.,
FYROM and Bulgaria. The great percentage of Desmani-
2001). The communication of the Mediterranean with the
nae in the Greek mammalian faunas of this period
Atlantic Ocean by the Gibraltar Seaway became re-estab-
(Spilia 1, Kardia) confirms this opinion (VAN DER MEU-
lished at the end of the Miocene, at about 5.3 Ma. An
LEN &VAN KOLFSCHOTTEN, 1986).
extensive transgression raised the sea level, and the Medi-
terranea filled again. Climatic conditions were also
changed, being less dry. The presence of tragulids and
cervids in the Greek fauna of Dytiko, Macedonia, dated to
latest Miocene, is strong evidence for an increase of
humidity in the Eastern Mediterranean (DE BONIS et al.,
1992). The end of the Miocene is characterized by the dis-
appearance of several mammalian taxa including masto-
donts (Choerolophodon), carnivores (Adcrocuta, Thalas-
sictis), suids (Microstonyx), giraffids (Bohlinia,
Samotherium, Helladotherium), bovids (Tragoportax,
Prostrepsiceros, Protoryx, Palaeoryx), cervids (Procapre-
olus), micromammals (Parapodemus). This extinction
probably resulted from the change in palaeoecological
conditions. Few taxa adapted to the newly established
environment and entered to Pliocene, e.g. Gazella.
The extinction, however, left free ecological space, and
new steppic immigrants, mainly from Asia, arrived and
dispersed in the Eastern Mediterranean : Pliospalax, Pro-
mimomys, Rhagapodemus, Mesocricetus, Parabos,
Korynochoerus, Nyctereutes, belong to these immigrants
and characterize the beginning of the Pliocene. The ear-
lier camelid Paracamelus was previously considered as
belonging to this migration wave, but new data confirm
an even earlier invasion. Moreover, forest dwellers, possi-
bly of African origin, also arrived. Tapirus arvernensis
appeared firstly in Italy in MN 13-14 (NOW 2002). The
mastodont Anancus, an African immigrant already men-
tioned from MN 12 of the Iberian Peninsula, dispersed
eastwards and occurred in the Balkans and the Black Sea
in MN 14 (Greece, Hungary, Romania, Ukraine). Two
Greek faunas (Maramena and Silata) correspond to this
transitional period. Their mammal association includes
young elements such as the suid Korynochoerus and the
rodents Rhagapodemus, Mesocricetus, Apodemus and
Fig. 4. Palaeogeographic map of Mediterranean region with
Micromys together with Miocene genera such as Choerol-
the main mammalian migration pathways and arrivals in East-
ophodon, Tragoportax, Samotherium and Pliocervus.
ern Mediterranean.
Both faunas have been dated to the Miocene/Pliocene
a) Early-Middle Pliocene (MN 14-16a)
boundary (S
b) Middle-Late Villafranchian (MN 17)
CHMIDT-KITTLER et al., 1995, VASSILIADOU et
c) Pliocene-Pleistocene
al., 2003).
Palaeogeographic maps from STEINIGER & RÖGL (1985).
EARLY-MIDDLE PLIOCENE MIGRATION
Pliocene fossil mammal records in the Eastern Medi-
(5.3-2.5 MA)
terranean are, however, scarce. Between 5.3 Ma and ~3.5
Ma ago several new forms arrived in Europe. The cercop-
The main palaeogeography of the Mediterranean
ithecid Dolichopithecus and the rodent Pelomys arrived
region changed slightly after the beginning of the
from Africa via the Middle East. The former appeared in
Pliocene, being more or less similar to the recent one
the Eastern Mediterranean in the Greek locality of Meg-
Neogene/Quaternary mammalian migrations in Eastern Mediterranean
187
alo Emvolon, dated to the base of MN 15 (KOUFOS &
Europe, as it is traced in Spain at the same time. Elephas
KOSTOPOULOS, 1997). The rodent Pelomys arrived earlier
arrived from Africa following the Middle East pathway.
at the beginning of the Pliocene, found in the Greek local-
Leptobos is an immigrant from Southern Asia and firstly
ity of Maritses, Rhodes (DE BRUIJN et al., 1992). Several
appeared in the Eastern Mediterranean in the locality of
carnivores, cervids, bovids and rodents migrated to
Damatria. At the same time the second dispersal event of
Europe, mainly from Asia. The cervids differentiated rap-
arvicolids appeared (STEININGER & RÖGL, 1985). During
idly and gave rise to several genera, occupying a signifi-
MN 16 several cervids of Asian origin adapted to local
cant number of mainly forest ecological niches. The suid
conditions providing new species or even genera. From
Sus, most possibly of southern Asian origin, made its first
the beginning of MN 17 three cervids Croizetoceros,
appearance in the Greek locality of Kessani dated to the
Eucladoceros and "Cervus" / "Pseudodama" appeared in
base of MN 14 (KOUFOS & KOSTOPOULOS, 1997). It rap-
the Eastern Mediterranean. The mountain bovid Gall-
idly dispersed to the whole of Europe as it is known from
ogoral and the slender antelope Gazellospira, both possi-
MN 14 of Italy, France and Spain (NOW, 2002). Later, it
bly of Asian origin, migrated to the Eastern Mediterra-
was found in the localities of Apolakkia, Rhodes and
nean and they were noted at several Greek localities
Megalo Emvolon dated to MN 15 (KOUFOS & KOSTOPOU-
(KOUFOS & KOSTOPOULOS, 1997). Early ovibovines also
LOS, 1997). These types of mammalian faunas were partly
appeared during this time (SPASSOV, 2000 ; ATHANASSIOU,
changed at ~3.2 Ma because of a worldwide climatic
2002). In the Eastern Mediterranean and the Black Sea a
cooling, causing a renewal of the mammal communities.
possible descendant of the late Miocene Palaeotraginae,
Early Villafranchian (3.2 2.6 Ma) faunas are, however,
the giraffid Mitilanotherium, is also present (KOUFOS &
poorly known in the Eastern Mediterranean.
KOSTOPOULOS, 1997 ; KOSTOPOULOS & ATHANASSIOU, in
press). Incidentally, the presence of giraffids in W. Europe
seems to be underestimated. New data from Spain justify
THE MIDDLE-LATE VILLAFRANCHIAN
the occurrence of late Pliocene giraffids in this area too
FAUNAL TURNOVER (2.6-2.0 MA)
(ARRIBAS et al., 2001 and pers. obs.).
Since the main morphotectonic structures of the peri-
EARLY PLEISTOCENE MIGRATION
Mediterranean region were completely developed, the
(2.0-1.0 MA)
palaeogeography of the area did not change. Migration
and dispersion of the mammals were mainly affected by
The climatic alternations and their effects on the sea
climatic fluctuations. At ~2.6 Ma (Middle Villafranchian,
level are the crucial factors of faunal changes during this
MN16) a climatic deterioration allowed a more arid
period, which is characterized by a rapid renewal of the
phase, which characterized the rest of this period until 1.8
mammalian fauna at ~2.0-1.8 Ma (K
Ma ago. This time-span correlates to the development in
OSTOPOULOS & KOU-
the Mediterranean region of the steppic floras character-
FOS, 2000). The palaeogeography of the Eastern Mediter-
ranean is similar to the recent one (Fig. 4C). During a
ized by Artemisia and Ephedra (SUC, 1986 ; SUC et al.,
short time span from 2.0-1.8 Ma several taxa enter
1995), and probably to the first major cool event of the
Europe via the Balkan Peninsula and the Middle East
northern hemisphere (TURNER, 1995 ; BLUM, 1997). The
(S
character of the mammalian faunas became more steppic,
PASSOV, 2000 ; KOSTOPOULOS et al., 2002). Between
them the canid Canis, the rodent Lagurodon, the bovids
especially in Southeastern Europe. Nevertheless, the pal-
Bison, Hemitragus and Ovis are Asian immigrants arrived
aeoecological conditions changed gradually westwards
in the Eastern Mediterranean at the beginning of the
delaying their presence in the Western Mediterranean.
Pleistocene. The carnivores Pachycrocuta brevirostris
Therefore, during this time interval the palaeoecological
and Panthera gombaszoegensis, as well as Hippopota-
conditions appeared to be more arid in the Eastern than in
mus, all of African origin, arrived in the area through the
the Western Mediterranean. The middle Villafranchian
Middle East. All these immigrants replaced the typical
faunas from Greece, Turkey and neighboring areas
Villafranchian faunas of the Eastern Mediterranean and
already had a more open/dry character than the iso-
Europe. Several old taxa (Nyctereutes, Pliohyaena, Gall-
chronous faunas from Southwestern Europe as confirmed
ogoral, Procamptoceras, Leptobos, Gazellospira,
by the persistence of Gazella, giraffids e.t.c. (KOSTOPOU-
Gazella, Sus strozzii, Mitilanotherium, Croizetoceros
LOS & SEN, 1999 ; KOSTOPOULOS & KOUFOS, 2000).
e.t.c) disappeared and were replaced by new ones. This
The most important arrivals in the Eastern Mediterra-
faunal change is well recorded in the Greek locality of
nean and the whole of Europe are referred to the genera
Gerakarou and the Bulgarian locality of Slivnitsa, both
Elephas, Leptobos and Equus, known as E-L-E event. The
dated at the end of the Pliocene (KOUFOS & KOSTOPOU-
genus Equus migrated earlier to Asia from N. America
LOS, 1997 ; SPASSOV, 1997). From the beginning of the
via the Beringian landbridge, but it arrived in the Eastern
Pleistocene (~1.8 Ma) new immigrants, especially from
Mediterranean at the beginning of middle Villafranchian,
Asia, penetrated further : the characteristic steppic rodent
c.a ~2.6 Ma (AZZAROLI, 1990 ; KOUFOS, 2001). Its possi-
Allophaiomys pliocaenicus dispersed in the whole peri-
ble first appearance in the Eastern Mediterranean has
Mediterranean area. The bovids Pontoceros, Praeovibos,
been traced in Damatria, Rhodes Island, Greece. The
Soergelia and the cervid Praemegaceros arrived in the
fauna of Damatria is poor, but a dating to the upper part of
Eastern Mediterranean and then dispersed to Europe
early Villafranchian (MN 16b) is possible for it (KOUFOS,
(AZZAROLI, 1983 ; KOSTOPOULOS et al., 2002). These
2001). This age corresponds to ~2.6 Ma and fits quite
migration waves are closely related to the expansion of
well with the abovementioned first appearance of Equus
the steppe towards the southwest, including some north-
in Europe. The genus dispersed rapidly throughout
ern and possibly cooler inhabitants.
188
George D. Koufos, Dimitris S. Kostopoulos and Theodora D. Vlachou
MIDDLE-LATE PLEISTOCENE MIGRATION
of the Pliocene, and b) the latest Pliocene change, mark-
(<1.0 MA)
ing the beginning of the Pleistocene. Known but less sig-
nificant faunal changes are important for the division of
During the early Pleistocene a large steppic belt was
the various stages into smaller time-spans. The migrations
established along Eurasia and N. America. At the begin-
and faunal changes of the Neogene are mainly due to pal-
ning of the middle Pleistocene wet climatic conditions
aeogeographic re-organization of the Mediterranean area
allowed an increase of humidity and rehabilitation of the
during the Pliocene and Pleistocene. When the Mediterra-
forestrial cover. For the next one million years the cli-
nean acquired its final palaeogeography and structure, cli-
matic conditions are characterized by a cyclicity with
matic changes became the main factor controlling mam-
alternation of cold and temperate periods, establishing the
malian migrations. Since the study of Neogene/
oscillations of the Pleistocene glaciations (AZZAROLI,
Quaternary faunas of the peri- Mediterranean region con-
1983 ; SUC, 1986 ; TURNER, 1995). During this period no
tinues new data become available to confirm or modify
important arrivals are mentioned. Steppic and cold step-
our ideas.
pic forms of North Asian and American origin such as the
bovids Praeovibos, Ovibos, Soergelia and the cervid
REFERENCES
Rangifer, as well as temperate dwellers such as the ele-
phant Palaeoloxodon, the rhino Dicerorhinus and the
AGUSTI J., L. CABRERA, M. GARCES & M. J. PARES (1997). The
large bovid Bubalus arrived in the Eastern Mediterranean
Vallesian mammal succession in the Valles Penedes basin
and then dispersed almost throughout Europe. The expan-
(northeast Spain). Pal. Pal. Pal., 133 :149-180.
sion of their biomes depended on the alternation of the
AGUSTI J., L. CABRERA, M. GARCES, W. KRIJGSMAN, O.OMS &
glacial/interglacial periods. In Southern Europe the so-
J.M. PARES (2001). A calibrated mammal scale for the Neo-
called "Mediterranean biosystem" was established. The
gene of Western Europe. State of the art. Earth Sc. Rev.. 52 :
most important migrations followed a N-S and vice versa
247-260.
direction, caused by expansion of the glacial cover. How-
ANDREWS P., T. HARISSON, E. DELSON, R-L. BERNOR. & L. MAR-
ever, the uplifted Alpine chain is a significant barrier for
TIN (1996). Distribution and biochronology of European and
most of the mammalian taxa. The Southern European
southwest Asian Miocene Catarrhines. In : BERNOR, FAHL-
fauna is only affected by the paroxysmal phases of the
BUSCH & MITTMANN (eds), The evolution of Western Eura-
central European N-S migrations. Cold steppic faunal ele-
sian Neogene mammal faunas, Columbia Univ. Press, New
ments such as Mammuthus and the wooly rhino Coelo-
York : 168-207.
donta are occasionally present there, while temperate
ARRIBAS A., L.A. RIQUELME, P. PALMQVIST, G. GARRIDO, R.
H
dwellers predominated. Both cold and temperate taxa are
ERNANDEZ, C. LAPLANA, J.M. SORIA, C. VISERAS, J.J.
DURAN, P. GUMIEL, F. ROBLES, J. LOPEZ-MARTINEZ & J. CAR-
known from the middle-late Pleistocene of Greece
RION (2001). Un Nuevo yacimiento de grandes mamiferos
(MELENTIS, 1961 ; MARINOS, 1965).
villafranquienses en la Cuenca de Guadix-Baza (Granada) :
On the contrary, the Mediterranean islands show a
Fonelas P-1, primer registro de la fauna proxima al limite
completely different faunal pattern from middle-late
Plio-Pleistoceno en la peninsula Iberica. Bol. geol. y min.,
Pleistocene. The isolation of the islands due to tectonic
112 (4) : 3-34.
movements or/and sea level fluctuations, allowed the
ATHANASSIOU A. (2002). Euthyceros thessalicus, a new bovid
from the Late Pliocene of Sesklo (Thessaly, Greece).
development of special endemic faunas. The absence of
N.Jb.Geol. Palaeont. Mh., 2 : 113-128.
predators and the dramatic reduction of the living space
AZZAROLI A. (1983). Quaternary mammals and the "end-Villa-
gave rise to an evolutionary process known as insular
franchian"dispersal event a turning point in the history of
endemism. The body mass of the island mammals,
Eurasia. Pal. Pal. Pal., 44 : 117-139.
adapted progressively to the new conditions, reduced or
AZZAROLI A. (1990). The genus Equus in Europe. In : LINDSAY,
increased accordingly to their initial size (insular "nan-
FAHLBUSCH & MEIN (eds), European Neogene Mammal
ism" in elephants, hippos or "gigantism" in rodents). Sev-
Chronology, Plenum Press, New York and London : 339-
eral islands in the Eastern Mediterranean (Rhodes, Carpa-
356.
thos, Tilos, Crete, Cyprus e.t.c.) include poor mammalian
BARRY J. C., N. M. JOHNSON, S. M. RAZA, & L. L. JACOBS
communities of endemic character with small-sized ele-
(1985). Neogene mammalian faunal change in southeern
phants, hippos and cervids (DERMITZAKIS & SONDAAR,
Asia : Correlations with climatic, tectonic, and eustatic
1978 ; KOTSAKIS et al., 1979 ;).
events. Geology, 13 : 637-640.
BEGUN R. D. (2001). African and Eurasian Miocene hominoids
and the origins of the Hominidae. In : DE BONIS, KOUFOS &
CONCLUSION
ANDREWS (eds), Hominoid Evolution and climatic change in
Europe, vol. 2, Phylogeny of the Neogene Hominoid Pri-
During the Neogene/Quaternary several mammalian
mates of Eurasia, Cambridge Univ. Press, London : 231-
migrations and faunal changes have been recognized in
253.
the Eastern Mediterranean. The recognized main migra-
BERNOR R.L., M. FORTELIUS & L. ROOK (2001). Evolutionary
tions of this period are : a) the middle Orleanian (18.0-
biogeography and paleoecology of the Oreopithecus bam-
bolii "Faunal Zone" (late Miocene, Tusco-Sardinian prov-
17.0 Ma), b) the late Miocene (10.7-6.7 Ma), and c) the
ince). Boll. Soc. Paleont. It., 40 (2) : 139-148.
middle Viffafranchian (~2.6 Ma) one. At the same time
BLUM J.D. (1997). The effect of late Cenozoic glaciation and
smaller migration waves from Africa and Asia allowed
tectonic uplift on Silicate weathering rates and the marine
the entrance of various mammalian taxa into Europe. Two
87Sr-86Sr record. In : RUDDIMAN (ed.), Tectonic uplift and
important faunal changes have been recognized : a) the
Climate change, Plenum Press, New York & London : 259-
latest Miocene faunal change, which marks the beginning
288.
Neogene/Quaternary mammalian migrations in Eastern Mediterranean
189
DE BONIS L. & G. D. KOUFOS (1999). The Miocene large mam-
nia, Greece. Some rematks about the species. Bull. Geol.
mal succession in Greece. In : AGUSTI, ROOK & ANDREWS
Soc. Greece, 30 : 341-355.
(eds), Hominoid Evolution and climatic change in Europe,
KOSTOPOULOS D. S. (1997). The Plio-Pleistocene artiodactyls
vol. I, The evolution of the Neogene terrestrial ecosystems in
(Vertebrata, Mammalia) of Macedonia 1. The fossiliferous
Europe, Cambridge Univ. Press, London : 205-237.
site "Appolonia-1", Mygdonia basin of Greece. Geodiversi-
DE BONIS L. & G. D. KOUFOS (2001). Phylogenetic relationships
tas, 19 : 845-875.
of Ouranopithecus macedoniensis (Mammalia, Primates,
KOSTOPOULOS D. S. & S. SEN (1999). Late Pliocene (Villa-
Hominoidea, Hominidae) of the late Miocene deposits of
franchian) mammals from Sarikol Tepe, Ankara, Turkey.
Central Macedonia, Greece. In : DE BONIS, KOUFOS &
Mitt. Bayer. Staatslg. Palaeont. Hist. Geol., 39 : 165-202.
ANDREWS (eds), Hominoid Evolution and climatic change in
KOSTOPOULOS D. S. & G. D. KOUFOS (2000). Palaeoecological
Europe, vol. II, Phylogeny of the Neogene Hominoid Pri-
remarks on Plio-Pleistocene mammalian faunas. Compara-
mates of Eurasia, Cambridge Univ. Press, London : 254-
tive analysis of several Greek and European assemblages.
268.
In : KOUFOS & IOAKIM (eds), Mediterranean Neogene
DE BONIS L., G. BOUVRAIN, D. GERAADS & G. D. KOUFOS
cyclostratigraphy in marine-continental deposits, Bull. Geol.
(1992). Diversity and palaeoecology of Greek late Miocene
Soc. Greece, Athens, sp. publ., no 9 : 139-150.
mammalian faunas. Pal.,Pal.,Pal., 91 : 99-121.
KOSTOPOULOS D. S. & A. ATHANASSIOU (in press). In the
DE BONIS L., G. D. KOUFOS & S. SEN (1998). Ruminants
shadow of Plio-Pleistocene Bovidae : Suids, cervids and
(Bovidae and Tragulidae) from the middle Miocene (MN 5)
giraffids from the Greek territory. Quaternaire, in press.
of the island of Chios, Aegean sea (Greece). N. Jb. f. Geol.
KOSTOPOULOS, D. S., K. VASSILIADOU & G. D. KOUFOS (2002).
Palaont. Abh., 210 : 399-420.
The beginning of Pleistocene in the Balkan area, according
DE BONIS L., M. BRUNET, E. HEINTZ & S. SEN (1993). La prov-
to the mammal record ; palaeogeographic approach. Ann.
ince Greco-irano-afgane et la repartition des faunes mam-
géol. pays Hell., 39(A) : 253-278.
maliennes au Miocene superieur. Paleont. i Evol., 24-25 :
KOTSAKIS T., C. PETRONIO & G. SIRNA (1979). The Quaternary
96-106.
vertebrates of the Aegean islands : Paleogeographical impli-
DE BRUIJN H., R. DAAMS, G. DAXNER-HACK, V. FAHLBUSCH, L.
cations. Ann. géol. pays Hell., 30 : 31-64.
GINSBURG, P. MEIN & J. MORALES (1992). Report of the
KOUFOS G. D. (1993). A mandible of Ouranopithecus macedo-
RCMNS working group on fossil mammals, Reisensburg
niensis from a new late Miocene locality of Macedonia
1990. Newslet. Strat., 26(2/3) : 65-117.
(Greece). American Jour. Phys. Anthropology, 91 : 225-234.
DERMITZAKIS D. M. & J. D. PAPANIKOLAOU (1981). Palaeogeog-
KOUFOS G. D. (1995). The first female maxilla of the hominoid
raphy and Geodynamics of the Aegean region during the
Ouranopithecus macedoniensis from the late Miocene of
Neogene. Ann. géol. Pays hell., hors ser., IV : 245-266.
Macedonia, Greece. Journ. Hum. Evol., 29 : 385-399.
DERMITZAKIS M. D. & P.Y. SONDAAR (1978). The importance of
KOUFOS G. D. (2000). The hipparions of the late Miocene local-
fossil mammals in reconstructing palaeogeography with spe-
ity "Nikiti 1", Chalkidiki, Macedonia, Greece. Revue Palae-
cial reference to the Pleistocene of Aegean Archipelago.
obiologique, 19(1) : 47-77.
Ann. géol. Pays hell., 29 : 808-840.
KOUFOS G. D. (2001). The Villafranchian mammalian faunas
DINARES-TURELL J., F. ORTI, E. PLAYA & L. ROSELL (1999). Pal-
and biochronology of Greece. Boll. Soc. Paleont. Italiana,
aeomagnetic chronology of the evaporitic sedimentation in
40(2) : 217-223.
the Neogene Fortuna Basin (SE Spain) : early restriction pre-
KOUFOS G. D. (2003). Late Miocene mammal events and bios-
ceding the "Messinian Salinity Crisis". Pal., Pal., Pal., 154 :
tratigraphy in Eastern Mediterranean. Deinsea, 10 : 343-371.
161-178.
KOUFOS G. D. & G. E. SYRIDES (1997). A new mammalian local-
FORSTEN A. (1990). Anchitherium from Pasalar, Turkey. J. Hum.
ity from the early-middle Miocene of Macedonia, Greece. C.
Evol., 19 : 471-478.
R. Acad. Sc. Paris, 325 : 511-516.
FORTELIUS M. (1990). Less common ungulate species from
KOUFOS G. D. & D. S. KOSTOPOULOS (1997). Biochronology and
Pasalar, middle Miocene of Anatolia (Turkey). Jour. Hum.
succession of the Plio-Pleistocene macromammalian locali-
Evol., 19 : 479-487.
ties of Greece. In : AGUILAR, LEGENDRE & MICHAUX (eds),
GARCES M., L. CABRERA, J. AGUSTI & M. J. PARES (1997). Old
Actes Congres BIOCHROM'97, Mem. Trav. E.P.H.E., Inst.
World appearance datum of Hipparion horses : Late
Montpellier, 21 : 619-634.
Miocene large mammal dispersal and global events. Geol-
KOUFOS G. D., N. ZOUROS & O. MOUROUZIDOU (2003). Prodei-
ogy, 25 : 19-22.
notherium bavaricum (Mammalia, Proboscidea) from early
GARCES M., W. KRIJGSMAN & J. AGUSTI (1998). Chronology of
Miocene of Lesvos island, Greece ; the appearance of dei-
the late Turolian deposits of the Fortuna basin (SE Spain) :
notheres in Eastern Mediterranean. Geobios, 36 : 305-315.
implications for the Messinian evolution of the eastern Bet-
KRIJGSMAN W., M. GARCES, J. AGUSTI, I. RAFFI, C. TABERNER &
ics. Earth & Plan. Sc. Let., 163 : 69-81.
W.J. ZACHARIASSE (2000) The "Tortonian salinity crisis" of
HAQ, B. U., J. HARDENBOL & P. R. VAIL (1988). Mesozoic and
the eastern Betics (Spain). Earth & Plan. Sc. Let., 181 : 497-
Cenozoic chronostratigraphy and cycles of sea-level
511.
changes. In : WILGUS et al. (eds), Sea-level changes- an inte-
KRIJGSMAN W., M.-M. BLANC-VALLERON, R. FLECKER, F.J.
grated approach., SEMP spec. publ., 42 : 71-108.
HILGEN, T.J. KOUWENHOVEN, D. MERLE, F. ORSZAG-SPERBER
KAPPELMAN J., A. DUNCAM, M. FESHEA, J-P. LUNKKA, D. EKART,
& J.-M. ROUCHY (2002). The onset of the Messinian salinity
F. MCDOWELL, T. RYAN, & C.C. SWISHER III. Chronology of
crisis in the Eastern Mediterranean (Pissouri basin, Cyprus).
the Sinap Formation. In : FORTELIUS, KAPPELMAN, SENGBER-
Earth & Plan. Sc. Let., 194 : 299-310.
NOR (eds), Geology and Paleontology of the Miocene Sinap
MADE J. VAN DER (1990). A range chart for European Suidae
Formation, Turkey, Columbia Univ. Press, New York : 41-
and Tayassuidae. Palaeont. i Evol., 23 : 99-104.
66.
MADE J. VAN DER (1999). Intercontinental relatioship Europe-
KONDOPOULOU D., L. DE BONIS, G. D. KOUFOS, & S. SEN (1993).
Africa and the Indian Subcontinent. In : RÖSSNER & HEISSIG
Palaeomagnetic and biostratigraphic data from the middle
(eds), The Miocene Land Mammals of Europe, Verlag Dr
Miocene vertebrate locality of Thymiana (Chios island,
Friedrich Pfeil., Munchen : 457-473.
Greece). Proc. 2nd Congr. Geophys. Soc. Greec : 626-635.
MARINOS G. (1965). Beitrage zur Kenntnis der Verbreitung des
KOSTOPOULOS D. S. (1994). Microstonyx major (Suidae, Artio-
Pleistozäns in Mazedonien. Scient.. Annals, Fac. Phys. &
dactyla) from the late Miocene locality of Nikiti-1, Macedo-
Math. Univ. Thessaloniki, 9 : 95-111.
190
George D. Koufos, Dimitris S. Kostopoulos and Theodora D. Vlachou
MEIN P. (1990). Updating of MN zones. In : LINDSAY, FAHL-
SPASSOV N. (2000). Biochronology and zoogeographic affinities
BUSCH & MEIN (eds), European Neogene Mammal Chronol-
of the Villafranchian faunas of Bulgaria and South Europe.
ogy, Plenum press, New York and London : 73-90.
Historia naturalis bulgarica, 12 : 89-128.
MEIN P. (1999). European Miocene Mammal Biochronology.
STEININGER F. F. (1999). Chronostratigraphy, Geochronology
In : RÖSSNER & HEISSIG (eds), The Miocene Land Mammals
and Biochronology of the Miocene "European Land Mam-
of Europe, Verlag Dr Friedrich Pfeil., Munchen : 25-38.
mals Mega-Zones" (ELMMZ) and the Miocene " Mammal-
MELENTIS J. (1961). Die dentition der Pleistozanen Proboscidier
Zones (MN-zones)". In : RÖSSNER & HEISSIG (eds), The
des Beckens von Megalopolis im Peloponnes (Griechen-
Miocene Land Mammals of Europe, Verlag Dr Friedrich
land). Ann. géol. Pays hell., 12 :153-262.
Pfeil., Munchen : 9-24.
MELENTIS J. (1966). Der erste nachweis von Brachyodus onoi-
STEININGER F. F. & F. RÖGL (1985). Paleogeography and palins-
deus (Mammalia, Anthracotheriidae) aus Griechenland und
pastic reconstruction of the Neogene of the Mediterranean
die datierung der fundschichten. Ann. géol. Pays hell., 17 :
and Paratethys. In : DIXON (ed.), The Geological Evolution
221-235.
of the Eastern Mediterranean, Geological Society, sp. publ.,
N
17 : 659-668
OW (2002). Database with the Neogene localities and their fau-
nal lists. www.helsinki.fi/science/now/database.htm
STEININGER F. F., R. L. BERNOR & V. FAHLBUSCH (1990). Euro-
P
pean Neogene Marine/continental chronologic correlations.
ARTRIDGE T. (1997). Late Neogene uplift in Eastern and South-
ern Africa and its paleoclimatic implications. In : RUDDI-
In : RÖSSNER & HEISSIG (eds), The Miocene Land Mammals
MAN (ed.), Tectonic uplift and Climate change, Plenum
of Europe, Verlag Dr Friedrich Pfeil., Munchen : 15-26.
Press, New York & London : 63-86
SUC J-P. (1986). Floras neogenes de Mediterranee occidentale,
PICKFORD M. (1984). A revision of the Sanitheriidae, a new fam-
climat et paleogeographie. Bull. Centres Research. Expl.
ily of Suiformes (mammalia). Geobios, 17(2) : 133-154.
Prod. Elf-Aquitaine, 10(2) : 477-488.
PICKFORD M. (1986). Premiere decouverte d' un Hyracoide pale-
SUC J-P., A BERTINI, N. COMBOURIEU-NEBOUT, F. DINIZ, S.
ogene en Eurasie. C. R. Acad. Sc. Paris, 303(13) :1251-
LEROY, E. RUSSO-ERMOLLI, Z. ZHENG., E.BESSAIS & J. FER-
1254.
IER (1995). Structure of West Mediterranean vegetation and
P
climate since 5.3 Ma. Acta zool. Cracov., 38(1) : 3-16.
ICKFORD M. (2001). Africa's smallest ruminant : A tragulid
from the Miocene of Kenya and the biostartigraphy of east
TASSY P. (1990). The "Proboscidean datum event" : How many
African Tragulidae. Geobios, 34(4) : 437-447.
proboscideans and how many events. In : LINDSAY, FAHL-
P
BUSCH & MEIN (eds), European Neogene Mammal Chronol-
ILBEAM J., M. MORGAN, J. C. BARRY, & L. FLYNN (1996). Euro-
pean MN Units and the Siwalik Faunal Sequence of Paki-
ogy, Plenum press, New York and London : 237-252.
stan. In : BERNOR, FAHLBUSCH & MITTMANN (eds), The evo-
TCHERNOV E., L. GINSBURG, P. TASSY & N. F. GOLDSMITH
lution of Western Eurasian Neogene mammal faunas,
(1987). Miocene mammals of the Negev (Israel). Journ.
Columbia Univ. Press, New York : 96-105.
Vert. Palaeont., 7 : 284-310.
RÖGL F. (1999). Circum-Mediterranean Miocene Paleogeogra-
THENIUS E. (1952). Die Saugetierfauna aus dem Torton von
phy. In : RÖSSNER & HEISSIG (eds), The Miocene Land Mam-
Neudorf an de March (CSR). N. Jb. f. Geol. Palaont. Abh.,
mals of Europe, Verlag Dr Friedrich Pfeil., Munchen : 39-48.
96 : 27-136.
SCHMIDT-KITTLER N. (1999). Subfamily Lophocyoninae. In :
THEOCHAROPOULOS K. (1999). Late Oligocene-Middle Miocene
RÖSSNER & HEISSIG (eds), The Miocene Land Mammals of
Democricetodon and Spanocricetodon from the eastern
Europe, Verlag Dr Friedrich Pfeil, Munchen : 149-153.
Mediterranean area. Ph.D thesis Univ. of Athens, pp. 1-91
SCHMIDT-KITTLER N., H. DE BRUIJN & C. DOUKAS (1995). The
THOMAS H., R-L. BERNOR & J-J. JAEGER (1982). Origines du
Vertebrate locality Maramena (Macedonia, Greece) at the
peuplement mammalien en Afrique du nord durant le
Turolian/Ruscinian boundary (Neogene). 1. General Intro-
Miocene terminal. Geobios, 15 : 283-297.
duction. Munch. Geowiss. Abh., 28 : 9-18.
TURNER A. (1995). Plio-Pleistocene correlations between cli-
SEN S., G. D. KOUFOS, D. KONDOPOULOU & L. DE BONIS (2000).
matic change and evolution in terrestrial mammals : the 2.5
Magnetostratigraphy of the late Miocene continental depos-
Ma event in Africa and Europe. Acta Zool. Cracov., 38(1) :
its of the lower Axios valley, Macedonia, Greece. In : KOU-
45-58.
FOS & IOAKIM (eds), Mediterranean Neogene cyclos-
VAN DER MEULEN A. & T. VAN KOLFSCHOTEN (1986). Review of
tratigraphy in marine--continental deposits, Bull. Geol. Soc.
the Late Turolian to Early Biharian mammal faunas from
Greece, Athens, sp. publ., no 9 : 197-206.
Greece and Turkey. Mem. Soc. Geol. Ital. 31 : 201-211.
SPASSOV N. (1997). Varshets and Slivnitsa new localities of
VASSILIADOU E., G. D. KOUFOS, & G. E. SYRIDES (2003). A new
Villafranchian vertebrate fauna from Bulgaria (taxonomic
micromammalian locality from the Miocene/Pliocene
composition, biostratigraphy and climatology). Geol. Bal-
boundary of Chalkidiki peninsula, Macedonia, Greece.
canica, 27 (1-2) : 83-90
Deinsea, 10 : 549-562.
Belg. J. Zool., 135 (2) : 191-197
July 2005
Effect of fishing on community structure of demersal
fish assemblages
Mary Labropoulou and Costas Papaconstantinou
National Center for Marine Research, Agios Kosmas, 166 04 Hellinikon, Greece
Corresponding author : Mary Labropoulou, e-mail : mlabro@ncmr.gr
ABSTRACT. Seasonal experimental trawl surveys (fall 1991-winter 1993) carried out in the Thracian Sea and
Thermaikos Gulf (N. E. Mediterranean, Greece). In this area, fishing pressure is very high, since approximately
50% of the Greek otter trawl fleet operates here, producing more than 57% of the total demersal landings. From a
total of 285 bottom trawls sampled at depths between 16-420 m, 157 fish species were caught. Indices of diversity,
richness, evenness, dominance and ABC plots were used to assess spatial structure, seasonal changes and diversity
of the demersal fish assemblages. In general, species diversity, richness and evenness decreased with water depth,
with the highest values at depths <100 m. Dominance increased with depth, getting its maximum at depths >200 m.
The effect of depth on the diversity patterns observed was always significant, while no seasonal trends were
detected. Commercially important species were dominant in the shallowest zone, while non-commercial species
predominated at depths below 200 m. At intermediate depths (30-200 m) almost 50% of the total catches comprised
of non-commercially important fish species. The abundance/biomass comparison method proved a useful tool for
assessing the impact of stresses on fish populations since it revealed moderate disturbance on fish communities at
those depths where fishing pressure is the highest.
KEY WORDS : Community structure, diversity, ABC method, fishing effects, North Eastern Mediterranean
INTRODUCTION
nental shelf and the upper slope of the Thracian sea were
analysed to investigate the structure of the demersal fish
The reductions of catch rates and mean size of individ-
community. The main objective was to identify aspects of
uals is well documented in world fisheries (PITCHER,
community structure that are most likely to reveal evi-
1996, PAULY et al. 1998). Consequently, new approaches
dence of anthropogenic impact due to exploitation.
to the study of exploited populations have been sug-
gested, including the study of the fish assemblage struc-
ture in relation to environmental variables, and the char-
MATERIALS AND METHODS
acterization of seasonal changes to improve management
practices (i.e. GISLASON et al. 2000). As pointed out by
Sampling procedure
CADDY & SHARP (1988) this type of study is a necessary
step towards understanding the dynamics of multispecies
A total of 285 hauls were taken during 8 experimental
stocks. Such work can then be extended to find general
bottom trawl survey cruises on a seasonal basis (fall
patterns, which may be associated with particular envi-
1991-winter 1993) in the Thracian Sea and Thermaikos
ronmental conditions and fishing effort.
Gulf from standard depth stations between 16-420 m.
Sampling stations were selected on a depth-stratified ran-
Information on soft-bottom fish assemblages is particu-
dom decision and the otter trawl used (foot-rope length :
larly scarce in the Eastern Mediterranean region where
65.7 m, headline height : 1.5 m) was equipped with a cod-
demersal fish are heavily exploited as principal targets or
end bag liner of 16 mm stretched mesh size. Samples
as by-catch. In Greek waters, demersal fishes of the conti-
were collected during daylight between 08:00 and 17:00
nental shelf and slope are subjected to an intensive fishery
hours. The duration of each trawl (bottom time) was 30-
carried out by trawl, gillnet and longline fleets. Gillnets
60 min and the trawling speed fluctuated from 2.5 to 3.0
and longlines catch a small number of species, whereas
knots depending on the depth and the nature of the sub-
the trawl fleet exploits a multi-species fishery targeting
strate. The catch from each haul was sorted and identified
several demersal and benthic species. The results of
to species level, and each species was enumerated and
experimental trawl fishing in the Greek seas indicate that
weighed separately on board. Since all hauls were carried
commercially important demersal and inshore stocks suf-
out using the commercial trawl vessel (`Ioannis Rossos')
fer from growth over-fishing. As a result, commercial
and the same fishing gear, it was assumed that gear selec-
catches consist mainly of young immature individuals
tivity was constant. Those species regarded as pelagic or
and a variety of non-commercial species that are dis-
semi-pelagic in behaviour were excluded from the analy-
carded (STERGIOU et al., 1997).
ses since they had not been quantitatively sampled (i.e.
In the present study, trawl catch data obtained season-
Scomber sp., Trachurus sp., Sardina pilchardus, Engrau-
ally, between fall 1991 and winter 1993, from the conti-
lis encrasicolus).
192
Mary Labropoulou and Costas Papaconstantinou
Data analysis
number of species (S), species diversity (Shannon-Wiener
index, H
Species abundance and biomass were calculated for
URLBERT, 1978), richness (MARGALEF, 1968),
dominance (Simpson's index, K
each haul after standardization of the data to a 1 hour tow.
REBS, 1989) and evenness
(P
Cluster analysis (group average) employing the Bray-
IELOU, 1966) were calculated for each of the station-
groups defined by cluster analysis.
Curtis similarity index (FIELD et al., 1982) was performed
to the standardized abundance values of the species using
the PRIMER algorithms, Plymouth Marine Laboratory
RESULTS
(CLARKE, 1993). In order to normalize the data and avoid
skew a square root transformation was applied to the
A total of 157 species belonging to 60 families were
abundance data prior to cluster analysis (FIELD et al.,
collected from 285 trawl stations at depths ranging from
1982). Multidimensional scaling (MDS) ordination analy-
16 to 420 m. On the basis of classification and ordination
sis was also performed with the same configuration as in
of the 285 hauls, in terms of species abundance, 4 major
cluster analysis with respect to similarity index and trans-
station-groups (I to IV) were distinguished, reflecting
formation. The typifying and discriminating species of
depth-related differences in demersal fish assemblages
each group of stations were determined using the SIM-
associated with the continental shelf and the upper slope
PER procedure (CLARKE, 1993). This procedure indicates
(Fig. 1). Group I included stations from intermediate
the average contribution of each species to the similarity
depth (30-90 m), while group II comprised all the deepest
(typifying species) and dissimilarity (discriminating spe-
stations from the continental shelf (100-190 m). Group III
cies) between groups of samples. Variation in species rel-
consisted entirely of the shallow stations (16-28 m). All
ative abundance and biomass was also examined by using
stations from the upper slope (200-420 m) were classified
the graphical representations of species cumulative fre-
in group IV. Species dominated in each group are pre-
quency distributions (k-dominance curves, LAMBSHEAD et
sented in Table 1. However, a relatively small number of
al., 1983). Relative abundance and biomass of demersal
species contributed most to the similarity of each group,
species were superimposed using the ABC method of
but their relative abundances varied between adjacent
WARWICK (1986) to provide information on the size of the
groups (i.e. Groups I-III) (Table 1).
most dominant species. The ecological parameters
Table 1. Dominant fish species in the Thracian Sea and Thermaikos Gulf, based on abundance rank for each
station group identified by cluster analysis. Densities (%N) are averaged over all samples in each group.
% Cum: average contribution to the similarity in each group. C indicates commercially important species. SD :
Standard Deviation
Group III (16-28 m)
Group I (30-90 m)
% N
% Cum.
% N
% Cum.
average similarity: 67.8 SD: 4.9
average similarity: 73.8 SD: 7.1
Arnoglossus laterna
13.55
12.37
C
Serranus hepatus
17.36
7.85
Serranus hepatus
8.75
23.29
Trisopterus minutus capelanus
17.59
15.12
C
Diplodus annularis
4.24
32.27
Mullus barbatus
7.44
21.29
C
Gobius niger
6.74
40.72
Arnoglossus laterna
10.12
27.00
C
Mullus barbatus
30.75
48.11
C
Merluccius merluccius
3.21
32.08
C
Trisopterus minutus capelanus
1.21
53.63
C
Spicara flexuosa
6.92
37.10
Spicara flexuosa
5.43
59.14
Lepidotrigla cavillone
2.75
41.71
Trigla lucerna
1.61
64.48
C
Cepola rubescens
2.34
46.23
Merlangius merlangus euxinus
3.54
69.45
C
Deltentosteus quadrimaculatus
5.35
50.73
Scorpaena notata
0.45
74.15
C
Callionymus maculatus
3.40
55.06
Merluccius merluccius
0.76
78.50
C
Scyliorhinus canicula
2.45
58.74
Gobius paganellus
4.45
82.18
Citharus linguatula
1.67
62.33
C
Solea vulgaris
4.45
85.36
C
Lophius budegassa
0.90
65.76
C
Cepola rubescens
0.65
88.03
Serranus cabrilla
0.84
68.74
Symphurus ligulatus
0.58
71.51
Gaidropsarus sp.
0.42
74.05
Raja clavata
0.15
76.18
C
Arnoglossus thori
0.75
78.27
C
Group II (100-190 m)
Group IV (200-420 m)
% N
% Cum.
% N
% Cum.
average similarity: 73.6 SD=4.4
average similarity: 72.3 SD: 7.8
Trisopterus minutus capelanus
27.74
10.17
C
Hymenocephalus italicus
14.71
11.03
Merluccius merluccius
10.16
18.29
C
Gadiculus argenteus argenteus
24.52
21.95
Argentina sphyraena
2.04
23.95
Lepidorhombus boscii
5.30
31.81
C
Lophius budegassa
2.26
29.31
C
Micromesistius poutassou
26.42
40.85
C
Lepidorhombus boscii
1.38
34.50
C
Coelorhynchus coelorhynchus
2.41
47.97
Arnoglossus laterna
2.46
39.37
C
Phycis blennoides
1.06
54.59
C
Scyliorhinus canicula
2.18
44.11
Lophius budegassa
1.14
61.12
C
Lepidotrigla cavillone
4.05
48.77
Argentina sphyraena
14.07
67.63
Callionymus maculatus
2.54
53.41
Merluccius merluccius
6.88
74.03
C
Cepola rubescens
1.59
57.88
Galeus melastomus
0.50
78.95
Serranus hepatus
6.99
62.10
Trigla lyra
0.37
82.62
C
Capros aper
0.88
66.07
Capros aper
0.16
86.12
Phycis blennoides
0.31
69.75
C
Aspitrigla cuculus
1.68
73.02
C
Trigla lyra
0.33
76.27
C
Mullus barbatus
4.53
79.52
C
Effect on fishing on community structure of demersal fish assemblages
193
mean commercial/noncommercial ratio in terms of both
number and weight of the species consisting each group
revealed that commercially important species were domi-
nant in the shallow zone (16-28 m). At intermediate
depths (30-200 m) almost 50% of the total catches com-
prised of non-commercially important species, while non-
commercially species predominated at depths below 200
m (Table 2).
a
b
Fig. 1. Classification (a) and ordination (b) of the sampling
stations based on species abundance from the Thracian Sea and
Thermaikos Gulf.
Differentiation between groups of station was evident
in the k-dominance curves, in terms of both number and
weight. Stations corresponded to groups I and II revealed
more diversified and less dominated communities than
those from the upper slope (group IV), with shallow sta-
tions (group III) having an intermediate position (Fig. 2).
The curves got steeper and more elevated for group IV,
suggesting that depths below 200 m were dominated by
fewer species. Combined k-dominance curves for number
and biomass (Fig. 3) showed that the dominant species
occupied a larger proportion of the total when expressed
as biomass rather than as numerical abundance in groups
III and IV. At high species rank, both curves were steeper
in gradient, indicating that fish assemblages in groups III
and IV were dominated by few species. On the contrary,
the k-dominance plots for group I exhibited an inverted
pattern with the abundance curve more elevated than the
biomass curve, indicating that several of the numerically
most abundant species are small in size. A combination of
large and small species, each with different rank in terms
of abundance and biomass, produced k-dominance
curves, which crossed for those hauls taken from depths
Fig. 2. Cumulative species richness curves in the four groups
between 100-190 m depth (group II). Estimations of the
identified by cluster analysis
Table 2. Estimates of commercial / non commercial ratio by number and weight for species in each group iden-
tified by cluster analysis
Group III
Group I
Group II
Group IV
Commercial / non-commercial ratio
(16-28 m)
(30-90 m)
(100-190 m)
(200-420 m)
Number
1.30
0.79
1.03
0.70
Weight
1.53
0.96
1.10
0.74
194
Mary Labropoulou and Costas Papaconstantinou
Fig. 3. Comparison of k-dominance curves (abundance and biomass) for the demersal fish communities between the four station-
groups from the Thracian Sea and Thermaikos Gulf
Significant differences in mean species abundance,
sampled (Group IV), as well as for the shallowest stations
biomass and diversity indices existed between the four
(<30 m, group I). However, ecological parameters
station-groups (Fig. 4). The highest values of these
appeared to be more or less uniform at depths between
parameters were found in samples from the continental
30-190 m (P>0.05, Tukey HSD test). A steady decrease
shelf (Groups II and III, 30-190 m depth). A converse
was observed for the stations of the upper slope together
trend was noted from 200 m down to the maximum depth
with the shallow-water coastal stations.
Effect on fishing on community structure of demersal fish assemblages
195
DISCUSSION
Four distinct demersal fish assemblages were clearly
associated with the topography of the study area. A shal-
low assemblage reached to about 30 m and represents
coastal shallow bottom fauna of the continental shelf.
Two assemblages corresponded to the middle (30-90 m)
and deeper (100-190 m) parts of the continental shelf, and
a deep assemblage extended beyond that depth which rep-
resents the upper slope. The continental shelf assem-
blages exhibited greater abundance and contained species
of commercial interest such as : Merluccius merluccius,
Mullus barbatus, Mullus surmuletus, Pagellus erythrinus,
and Trisopterus minutus capelanus. The upper slope
assemblage is characterized by the predominance of spe-
cies like Micromesistius poutassou, Gadiculus argenteus
argenteus, Argentina sphyraena and Hymenocephalus
italicus, which are small and not commercially important.
The main determining feature associated with the struc-
ture of the demersal fish assemblages is depth, as it
reflects the changes from the continental shelf to the con-
tinental slope. However, other bottom and oceanographic
characteristics must also play a role, at least for structur-
ing assemblages on the continental shelf. These include
the gradient in eutrophy, fresh/brackish water runoff, tem-
perature and salinity differences along a NNW to SSE
axis, and differences in the extent and the bottom type of
the continental shelf (STERGIOU et al., 1997). Neverthe-
less, the most important quantitative boundary for all
areas was located around 200 m, a depth separating the
species of the continental shelf from those of the upper
slope extending down to 500 m.
High species richness and diversity characterized the
continental shelf, but both variables decreased markedly
at the deepest waters, while the reverse was true for spe-
cies dominance. On the other hand, evenness also
decreased with depth, but remained rather constant at
depths between 30-190 m, indicating little variability in
the numerical codominance of species over the continen-
tal shelf. The disparities in these general trends for the
shallowest depths (group III) may be attributed to the
more variable environmental characteristics (temperature
and salinity) in shallow coastal waters. The k-dominance
analysis suggested that the spatial trend in diversity and
dominance was a strong feature of the species assem-
blages under study, with dominance being the highest in
group IV. Consequently it appears that the highest values
of species diversity at depths between 30-190 m, coin-
cided with those depths where fishing pressure has been
the greatest.
Increasing levels of disturbance have generally been
considered to decrease diversity, species richness and
evenness. These observations have also been made in
many studies as response of demersal fish communities to
intense fishing effort (GREENSTREET & HALL, 1996 ;
RIJNSDORP et al., 1996 ; HALL, 1999 ; JENNINGS et al.,
1999). However, recent theories on the influence of dis-
Fig. 4. Ecological parameters (a : number of species, b :
turbance or stress on diversity suggest that at intermediate
evenness, c : dominance, d : richness, e : Shannon-Wiener
levels of disturbance, diversity could be the highest
diversity) by depth zone (I : 16-28 m, II : 30-90 m, III : 100-
(MURAWSKI, 2000). Fishing might cause major species
190 m, IV : 200-420 m) for the demersal fish communities in
the Thracian Sea and Thermaikos Gulf
replacement but the actual changes in their reletive abun-
dance are rather subtle. Other changes in assemblage's
species composition generally involve relatively rare spe-
196
Mary Labropoulou and Costas Papaconstantinou
cies and thus indices based on multispecies information
ZWANENBURG, 2000). In the present study, the fish assem-
do not always reflect major species replacement events
blages under consideration have suffered a long history of
(MURAWSKI, 2000). Therefore, depending on the starting
fishery exploitation. Therefore overfishing has affected
point of the community in relation to existing stress lev-
the population structure and densities of the demersal fish
els, increasing levels of stress may either result in an
communities, at least at depths up to 200 m, where most
increase or decrease in diversity. BIANCHI et al. (2000),
of the fishing activity is focused. It is possible that the
who investigated whether changes in diversity and domi-
organization of the demersal fish assemblages analysed is
nance of demersal fish communities could be related to
determined to a great extent by unidirectional trend
fishing, concluded that the largest changes in diversity
induced by fishing, bottom topography and oceano-
appeare to be due to changes in evenness or species rich-
graphic features of the study area.
ness, or both, often leading to an increase in diversity in
response to heavy exploitation. Since diversity measures
REFERENCES
have a specific sensitivity to changes in weight or num-
bers, dominant or rare species occurrrences, evenness
B
among species and other attributes (M
IANCHI, G., H. GISLASON, K. GRAHAM, L. HILL, X. JIN,
AURAWSKI, 2000),
K. KORANTENG, S. MANICKCHAND-HEILEMAN, I. PAYÁ,
no consensus has developed yet on the utility of tradi-
K. SAINSBURY, F. SANCHEZ & K. ZWANENBURG (2000).
tional diversity indices as a measure of ecosystem over-
Impact of fishing on size composition and diversity of
fishing (JENNINGS & REYNOLS, 2000 ; RICE, 2000).
demersal fish communities. ICES J. Mar. Sci., 57 : 558-571.
Some spatial effects of fishing in the study area were
CADDY, J.F. & G.D. SHARP (1988). An ecological framework for
adequately well illustrated by abundance/biomass com-
marine fishery investigations. FAO Fish. Tech. Pap. 283.
parison (ABC) method. The logic behind using ABC
CLARKE, K.L. (1993). Non-parametric multivariate analyses of
curves to evaluate effects of perturbations is that in undis-
change in community structure. Aust. J. Ecol., 18 : 117-143.
turbed communities the presence of large organisms
FIELD, J.G, K.R. CLARKE & R.M. WARWICK (1982). A practical
strategy for analysis of multispecies distribution patterns.
results in the biomass curve lying entirely above the
Mar. Ecol. Prog. Ser., 8 : 37-52.
abundance curve, due to the dominance of few large spe-
GISLASON H., M. SINCLAIR, K. SAINSBURY, R. O' BOYLE (2000).
cies each represented by few individuals (WARWICK &
Symposium overview : incorporating ecosystem objectives
CLARKE, 1994). Under environmental stress the commu-
within fisheries management. ICES J Mar Sci 57 : 468-475.
nities become increasingly dominated by large numbers
GREENSTREET, S.P.R. & S.J. HALL (1996). Fishing and the
of small individuals and the abundance curve lies entirely
ground-fish assemblage structure in the Nort-western North
above the biomass curve. In moderate disturbed commu-
Sea : an analysis of long-term and spatial trends. J. Anim.
nities these curves closely coincident and may cross over
Ecol., 65 : 577-598.
one or more times (WARWICK, 1986). This method has
HALL, S. (1999). The effects of fishing on marine ecosystems
successfully been used for assessing the degree to which
and communities. Blackwell Science, London.
macrobenthic communities respond to increasing levels
HURLBERT, S.H. (1978). The measurement of niche overlap and
of pollution-induced disturbance (W
some relatives. Ecology 59 : 67-77.
ARWICK, 1986 ; WAR-
JENNINGS S., S.P.R. GREENSTREET & J.D. REYNOLDS (1999).
WICK et al., 1987 ; WARWICK & RUSWAHYUNI, 1987 ;
Structural changes in an exploited fish community : a conse-
MEIRE & DEREU, 1990 ; WARWICK & CLARKE, 1994).
quence of differential fishing effects on species with con-
Recently, PENCZAK & KRUK (1999) who employed the
trasting life histories. J. Anim. Ecol., 68 : 617-627.
ABC comparison method for detecting human impacts on
JENNINGS, S. & J.D. REYNOLDS (2000). Impacts of fishing on
freshwater fish populations reported that it proves a use-
diversity : from pattern to process. In : KAISER M.J. & S.J. de
ful tool for indicating disturbance in fish communities.
GROOT (eds), Effects of fishing on non-target species and
Although ABC curves have not been widely used for eval-
habitats, Biological, conservation and socio-economic
uating fishery impacts on fish community structure, it
issues, Blackwell Scientific, Oxford : 235 -250.
appears, in the present study, that they can be a useful tool
KREBS, C.J. (1989). Ecological methodology. Harper and Row,
as an indicator of overfishing. The biomass and abun-
New York.
dance curves are close together, crossing each other at
LAMBSHEAD, P.J.D., H.M. PLATT & K.M. SHAW (1983). The
depths between 30 and 190 m, where fishing pressure is
detection of differences among assemblages of marine ben-
the highest. Together with the negative values of W statis-
thic species based on an assessment of dominance and diver-
sity. J. Nat. Hist., 17 : 859-874.
tics obtained, these results indicate moderate disturbance
MARGALEF, R. (1968). Perspectives in ecological theory. Uni-
of demersal fish communities. Also present in these com-
versity of Chicago Press, Chicago, Illinois.
munities are small, non-commercially important fish spe-
MEIRE, P.M. & J. DEREU (1990). Use of the abundance/biomass
cies, as confirmed by SIMPER analysis. These species
comparison method for detecting environmental stress :
are numerically dominant but do not represent a large pro-
some considerations based on intertidal macrozoobenthos
portion of the community biomass.
and bird communities. J. Appl. Ecol., 27 : 210-223.
Studies in other areas, based on extended time series
MURAWSKI, S.A. (2000). Definitions of overfishing from an eco-
during which major increases in fishing effort took place,
system perspective. ICES J. Mar. Sci., 57 : 649-658.
indicate that fishing leads to a decrease in catches and to
OVERHOLTZ, W.J. & A.V. TYLER (1985). Long-term changes of
the demersal fish assemblages of Georges Bank. Fish. Bull.,
increases in non-commercial species (OVERHOLTZ &
83 : 507-520.
TYLER, 1985 ; ROTHSCHILD, 1992). Furthermore, there is
PAULY D., V. CHRISTENSEN, J. DALSGAARD, R. FROESE & F.C. Jr
evidence that the size structure of demersal fish commu-
TORRES (1998). Fishing down marine food webs. Science,
nities is affected by fishing (PAULY et al., 1998). The
279 : 850-863.
overall trend is one of a reduction in large fish and a rela-
PENCZAK, T. & A. KRUK (1999). Applicability of the abundance/
tive increase in small fish (BIANCHI et al., 2000 ;
biomass comparison method for detecting human impacts on
Effect on fishing on community structure of demersal fish assemblages
197
fish populations in the Pilica River, Poland. Fish. Res., 39 :
chemistry, biology and fisheries. Oceanogr. Mar. Biol. Ann.
229-240.
Rev., 35 : 415-538.
PIELOU, E.C. (1966). The measurement of diversity in differ-
WARWICK, R.M. & RUSWAHYUNI (1987). Comparative study of
ences types of biological collections. J. Theor. Biol., 13 :
the structure of some tropical and temperate marine soft-bot-
131-144.
tom macrobenthic communities. Mar. Biol. 95 : 641-649.
P
W
ITCHER, A. (1996). Reinventing fisheries management. NAGA
ARWICK, R.M. (1986). A new method for detecting pollution
ICLARM, 19(3) : 15-17.
effects on marine benthic communities. Mar. Biol., 92 : 557-
R
562.
ICE, J.C. (2000). Evaluating fishery impacts using metrics of
W
community structure. ICES J Mar. Sci., 57 : 682 -688.
ARWICK, R.M. & K.R. CLARKE (1994). Relearning the ABC :
taxonomic changes and abundance/biomass relationships in
RIJNSDORP, K.J., P.I. van LEEUWEN, N. DAAN & H.J.L. HEESEN
disturbed benthic communities. Mar. Biol., 118 : 739-744.
(1996). Changes in abundance of demersal fish species in the
WARWICK, R.M., T.H. PEARSON & RUSWAHYUNI (1987). Detec-
North Sea between 1906-1909 and 1990-1995. ICES J. Mar.
tion of pollution effects on marine macrobenthos : further
Sci., 53 : 1054-1062.
evaluation of the species abundance/biomass method. Mar.
ROTHSCHILD, B.J. (1992). Multispecies interactions on George
Biol., 95 : 193-200.
Bank. ICES Mar. Sci. Symp., 195 : 418-423.
ZWANENBURG, K.C.T. (2000). The effects of fishing on demersal
STERGIOU, K.I., E.D. CHRISTOU, D. GEORGOPOULOS, A. ZENETOS
fish communities of the Scotian Shelf. ICES J. Mar. Sci., 57 :
& C. SOUVERMEZOGLOU (1997). The Hellenic Seas : physics,
503-509.
Belg. J. Zool., 135 (2) : 199-204
July 2005
Distribution and abundance of sepiolids (Mollusca :
Cephalopoda) off the north-eastern Greek coasts
Eugenia Lefkaditou1 and Panagiotis Kaspiris2
1 National Centre for Marine Research, Aghios Kosmas, Helliniko, 16604 Athens, Greece. E-mail : teuthis@ncmr.gr
2 University of Patras, Department of Biology, 26110 Patras, Greece.
Corresponding author : E. Lefkaditou, e-mail : teuthis@ncmr.gr
ABSTRACT. Sepiolids are a lesser known group of cephalopods. This paper aims to increase knowledge of their
distribution and abundance in the NE Mediterranean.
A total of 3404 sepiolids were collected off the north-eastern coasts of Greece, between 17 and 400 m of depth, during
four seasonal trawl surveys carried out from November 1992 to August-September 1993. Nine species were
identified : Neorossia caroli, Rondeletiola minor, Rossia macrosoma, Sepietta neglecta, Sepietta oweniana, Sepiola
affinis, Sepiola intermedia, Sepiola ligulata and Sepiola rondeleti.
S. oweniana was the most abundant species among them, followed by R. minor, R. macrosoma and S. rondeleti. The
results of multivariate analysis, based on Bray-Curtis similarity indices, showed the presence of three main groups :
one related to the shallower hauls near the coast (<60m) where S. rondeleti and S. intermedia were more frequently
caught, a second one consisting of hauls carried out at depths 55-105 m, in which S. oweniana was the dominant spe-
cies, and a third one with deeper hauls characterised by the highest abundance of S. oweniana, R.. minor and R. macro-
soma.
Length frequencies and maturity stages are presented by season and sex for the four most abundant species. Seasonal
changes in the bathymetric distribution of these species are also discussed in relation to their life cycle.
KEY WORDS : cephalopoda, sepiolidae, Aegean, Mediterranean.
INTRODUCTION
Rossia macrosoma and Sepiola rondeleti, was examined
in relation to their size and maturity.
Sepiolids are among the least known groups of cepha-
lopods in the Mediterranean Sea at least with regard to
their distribution and life history at sea. Although they
present little interest for fisheries they seem to play an
important role in the marine food webs since members of
this family have been frequently found in the stomach
contents of various marine organisms such as dolphins,
sharks, demersal and pelagic fishes (BELLO, 1991, 1996,
1999; WÜRTZ et al., 1992; BLANCO et al., 1995; ORSI-
RELINI et al., 1994, 1995).
Cephalopod species of the Sepiolidae family have been
Fig. 1. Illustration of the area investigated and the sampling
recorded in the Aegean Sea quite recently (KATAGAN &
stations of trawl surveys carried out from November 1992 to
KOCATAS, 1990; D'ONGHIA et al., 1991,1996; SALMAN et
September 1993.
al., 1997, 2002; LEFKADITOU & KASPIRIS, 1998; LEFKADI-
TOU et al., 1999; KOUTSOUBAS et al., 2000). Within the
last decade, biogeographic knowledge of sepiolids has
MATERIAL AND METHODS
greatly increased also in other areas of the western and
central Mediterranean Sea (TURSI & D'ONGHIA, 1992;
Samples were collected from four bottom trawl surveys
VILLANUEVA, 1992; BOLETZKY, 1995, JEREB et al., 1997;
carried out seasonally from November-December 1992 to
CASALI et al., 1998; QUETGLAS et al., 2000; SÁNCHEZ &
August-September 1993. The geographical area investi-
DEMESTRE, 2001; GONZÁLEZ & SÁNCHEZ, 2002), as well
gated extends off the coasts of north-eastern Greece, con-
as, in the Levantine basin (SALMAN et al, 1998; 2002) and
sisting of Thracian Sea, Strymonikos, Sygitikos, Toro-
the Marmara Sea (KATAGAN et al, 1993; ÜNSAL et al.,
neos and Thermaikos gulfs (Fig. 1). Four depth strata, 1-
1999).
50, 51-100, 101-200 and 201-400 m, were considered and
This work concerns the distribution and abundance of
sampling was based on random-stratified design. A com-
the sepiolid species found at the northernmost part of the
mercial trawler (115 tons gross tonnage, 250 Hp twin
Aegean Sea. In addition seasonal distribution of the most
engines) and the typical nylon commercial bottom trawl
abundant species, Sepietta oweniana, Rondeletiola minor,
net (16 mm cod-end mesh size from knot to knot) were
200
Eugenia Lefkaditou and Panagiotis Kaspiris
used. Hauls were performed during daytime and ranged
Rossia macrosoma and Sepiola rondeleti, the mean catch
from 30 to 60 min in duration.
per unit of effort (CPUE) in number of individuals per
fishing hour was calculated by species per depth stratum
and survey, as well as the seasonal length-frequency dis-
tributions and percentages of maturity stages by species
and sex.
Fig. 3. Dendrogram of the hauls carried out by bottom trawl
in September 1993 off the north-eastern Greek coasts, using
group-average linking of Bray-Curtis similarities calculated on
log(x+1) transformed numbers of individuals of sepiolid spe-
cies per fishing hour. 1 : cluster of shallower hauls (30-60m),
2 : hauls at intermediate depths (50-100m), 3 : deeper hauls
cluster (over 100 m).
RESULTS
Taxonomic composition and species assemblages
A total of 3404 specimens comprising nine species
belonging to two sepiolid subfamilies were collected
between 17 and 400 m of depth (Table I). S. oweniana
was the most abundant species followed by R. minor, R.
macrosoma and S. rondeleti.
Dominant species were widely distributed over the
whole study area, whereas the less frequently caught S.
affinis was not found in Strymonikos gulf, S. ligulata was
absent from catches in the Thracian Sea and the bathy-
benthic N. caroli did not appear in the deep hauls at Toro-
neos and Thermaikos gulfs (Fig. 2).
The results of the multivariate analysis, based on Bray-
Curtis similarity indices, showed the presence of three
Fig. 2. Distribution of sepiolid species in the studied area.
main clusters (Fig. 3) : one consisting of hauls carried out
Sepiolids were present in 126 out of the 148 hauls per-
at depths 30-60 m, another related with the depth stratum
formed in total. The specimens caught at each station
50-100 m and a third one with deeper hauls (over 100 m).
were preserved in 5% formalin in sea water, and identi-
Although most of the species were present in several clus-
fied at the laboratory following the key for sepiolids in
ters, the species composition and catch rates distinguish
G
them from each other. S. rondeleti and S. intermedia were
UERRA (1992). Dorsal mantle length (in mm), weight (in
g), sex and maturity stage were reported for each speci-
the species more frequently caught in the shallower hauls
men together with the haul data (date, location, duration,
(Table I), S. oweniana was the dominant species at depths
depth). A three stage scale : immature, maturing, mature,
between 50 and 100 m, whereas the deep-haul group
(J
(100-400 m) was characterised by the highest abundance
UANICO, 1979) was used for sexual maturity.
of S. oweniana, R. minor and R. macrosoma..
To detect zonation patterns, the data of the survey car-
ried out in August-September 1993 were considered
Seasonal distribution of the most abundant sepiolids.
because of the greater number of hauls performed during
this survey. The data matrices comprising the numbers of
individuals per hour of trawling of each species and sta-
S. oweniana
tion were log (x+1) transformed, and the haul-similarity
Over all, 2411 specimens were caught during the four
percentage was calculated using the Bray-Curtis coeffi-
surveys, at depths ranging between 40 and 400 m. Higher
cient (BRAY & CURTIS, 1957) by the PRIMER-v5 soft-
CPUE indices were estimated for waters deeper than
ware (CLARKE & GORLEY, 2001).
100 m (Fig. 4), where smaller individuals (ML<22 mm)
To investigate seasonal variation in the abundance and
generally constituted the greatest part of the catches (Fig.
distribution of Sepietta oweniana, Rondeletiola minor,
5). Differences in the bathymetric distribution by size
Sepiolids along the north-eastern Greek coasts
201
TABLE 1
Number of individuals, depth range and catch rates in each bathymetric stratum (f%, percentage frequency of appearance in hauls,
CPUE in number of individuals per fishing hour) for sepiolids caught by bottom trawl off the north-eastern Greek coasts from Novem-
ber 1992 to September 1993.
Depth stratum
Number
Depth
<50
50-100
100-200
200-400
Species
of
range
individuals
(m)
f%
CPUE
f%
CPUE
f%
CPUE
f%
CPUE
Sepiolinae
Sepiola afinis
5
40-89
2.6
0.1
4.1
0.1
Sepiola rondeleti
155
24-195
35.9
1.5
63.3
3.0
25.0
1.0
Sepiola intermedia
34
17-113
17.9
1.2
2.0
0.1
3.6
0.3
Sepietta oweniana
2411
40-400
7.7
0.3
87.8
16.6
100.0
29.0
90.3
43.9
Sepietta neglecta
64
24-262
2.6
0.4
8.2
0.6
17.9
0.9
6.5
0.6
Rondeletiola minor
360
66-338
8.2
0.2
64.3
5.4
38.7
8.9
Sepiola ligulata
14
80-328
4.1
0.1
14.3
0.3
9.7
0.2
Rossinae
Rossia macrosoma
239
78-400
2.0
0.0
35.7
4.3
90.3
5.5
Neorossia caroli
124
237-400
32.1
4.0
TABLE 2
Maturity stages seasonal percentages and mantle length ranges of sepiolids collected off the north-eastern Greek coasts from Novem-
ber 1992 to September 1993
Species
Sex
Maturity
Cruises
ML (mm)
I
II
III
IV
range
mean
S. oweniana
females
immature
19
20
26
54
11-26
18
maturing 26
21
25
15
14-29
21
mature
55
59
49
31
18-35
25
males
immature
1
0
3
7
12-20
16
maturing 4
7
15
7
13-24
18
mature
95
93
82
86
14-30
22
R. macrosoma
females
immature
62
61
30
35
15-50
31
maturing 15
28
39
26
30-51
40
mature
23
11
31
39
38-84
55
males
immature
53
22
3
28
14-33
22
maturing 12
6
3
17-28
24
mature
35
72
97
70
26-51
39
R. minor
Females
immature
2
12
maturing 20
3
5
11
12-14
13
Males
mature
80
95
95
89
13-21
16
maturing 5
1
10-11
11
mature
95
100
100
99
11-20
16
S. rondeleti
females
immature
20
8
8
14-22
18
maturing 40
8
8
16-20
18
mature
40
100
84
84
13-27
20
males
mature
100
100
100
100
12-30
18
N. caroli
females
immature
75
90
20
60
15-34
26
maturing 25
5
20
23-32
29
mature
5
60
40
31-43
39
males
immature
100
7
67
17-27
21
maturing 23
12
22-29
24
mature
70
88
33
22-40
31
S. neglecta
females
maturing
10
13
mature
100
90
100
100
12-23
17
males
immature
20
50
25
15
maturing 50
19
mature
100
80
75
13-23
18
S.affinis
females
immature
100
16
mature
100
15
males
mature
100
16
S. intermedia
females
mature
100
100
100
14-18
16
males
mature
100
100
100
13-21
16
S.ligulata
females
mature
100
100
100
13-17
16
males
22-40
31
202
Eugenia Lefkaditou and Panagiotis Kaspiris
were mainly observed in summer and autumn, when
Sepietta ow eniana
Rossia m acrosom a
larger individuals (ML>22 mm) concentrated in shallow
waters. Most males caught were mature, their percentage
extending to 90% in November and March. Mature
100
10
females represented 44.5% of the examined specimens,
)
)
/
hd
/
h
with a maximum percentage in March and a minimum in
50
(in
5
(ind
UEP
UEP
<50
0
C
C
September (Table II). An analysis of the occurrence of
<50
0
Sep-93
Sep-93
50-100
50-100
Jun-93
mature individuals in relation to depth, showed higher
Jun-93
Dep
100-200
D
t
Mar-93
100-200
h
e
Mar-93
(
pt
percentages of mature females at depths less than 100 m
m
h
)
200-400
Nov-92
(m
200-400
Nov-92
)
all year round, whereas, no trend was identifiable in the
distribution of mature males.
Rondeletiola m inor
Sepiola rondeleti
R. minor
20
10
)/h
)
d
/
h
10
d
(inE
5
(in
This species is one of the smallest sepiolids (Table II).
U
E
P
U
0
C
P
<50
C
Sep-93
<50
0
Mature individuals comprised over 95 % of the total of
Sep-93
50-100
Jun-93
50-100
Jun-93
360 individuals caught (Table II). The greatest part of the
D
D
e
100-200
Mar-93
e
p
100-200
p
t
Mar-93
h
th
(
(m
population was distributed deeper than 200 m from
m
200-400
Nov-92
)
)
200-400
Nov-92
March to September. In November `92 the species was
less abundant (Fig. 4) with a lower percentage of mature
Fig. 4. Seasonal abundance of Sepietta oweniana, Rondeleti-
males and females (Table II), and only some smaller indi-
ola minor, Rossia macrosoma and Sepiola rondeleti, by bathy-
viduals (ML<16 mm) was fished at depths 200-400
metric stratum in the study area, from November `92 to August-
(Fig. 5)
September `93.
Sepietta oweniana
Rondeletiola minor
Rossia macrosoma
Sepiola rondeleti
15
50
40
40
November '92
November '92
12
November '92
40
November '92
30
30
9
30
%
%
%
%
20
20
6
20
3
10
10
10
0
0
0
0
20
40
40
40
March '93
March '93
March '93
March '93
15
30
30
30
%
%
%
%
10
20
20
20
5
10
10
10
0
0
0
0
15
50
40
30
June '93
June '93
June '93
June '93
12
40
30
9
20
30
%
%
%
20
%
6
20
10
3
10
10
0
0
0
0
15
40
25
40
September '93
September '93
12
September '93
September '93
30
20
30
9
%
15
%
%
20
%
20
6
10
10
10
3
5
0
0
0
0
10 14 18 22 26 30 34 38
8
12
16
20
24
10 20 30 40 50 60 70 80 90
10
14
18
22
26
30
34
ML (mm)
ML (mm)
ML (mm)
ML (mm)
<100
100-200
>200
<200
>200
<200
>200
<50
>50
Fig. 5. Length frequency distribution of Sepietta oweniana, Rondeletiola minor, Rossia macrosoma and Sepiola rondeletti by season
and depth zone.
Sepiolids along the north-eastern Greek coasts
203
R. macrosoma
whereas there was no evidence of such migration in areas
with more abrupt waters such as the North Aegean Sea
A total of 239 specimens were fished between 78 and
(D'ONGHIA et al., 1996) and the Strait of Sicily (JEREB et
400 m. However findings at depths lower than 148 m
al., 1997).
were reported only in the Thracian Sea. As shown in
Figs 4 and 5, in November and March the species was
R. minor and R. macrosoma seem to concentrate in
more abundant at depths 100-200 m, in June the popula-
deeper waters during summer and early autumn, whereas
tion consisted mostly of larger individuals (ML>30 mm)
recruitment is mainly observed in November at depths
distributed deeper than 200 m, whereas in September the
shallower than 200 m. Similar concentration on the slope
strong recruitment in shallower waters resulted in almost
has been noted during summer in the Ligurian Sea for R.
equal abundance of the species in the two bathymetric
minor (ORSI-RELINI & BERTULETTI, 1989) and in the
strata, 100-200 and 200-400 m. Mature individuals of
lower Tyrrhenian Sea during autumn for R. macrosoma
both sexes were mainly found deeper than 200 m all year,
(BOLETZKY, 1995). However, in the northern Catalan Sea,
where as spawns of this species were always collected
MANGOLD-WIRTZ (1963) observed a greater abundance of
deeper than 250 m. The maximum percentage of mature
mature specimens on detritic bottoms shallower than 130
females was observed in September and that of males in
m during summer, supposing a population movement
June.
towards shallower waters for reproduction. The collection
of R. macrosoma eggs, as well as the higher percentages
S. rondeleti
of mature males and females on the slope of our study
area, are not in agreement with the above consideration.
This species was the most abundant of the genus Sepi-
The occurrence of mature individuals of these species all
ola (Table I), with 153 individuals collected between
year-round indicates an extended spawning period, thus
depths 24 and 195 m. Large individuals (ML>20 mm)
suggesting that the species' seasonal migrations should be
during all cruises were found deeper than 50 m (Fig. 5).
rather attributed to other reasons than reproduction.
Smaller ones were mostly recruited during early summer
Dense waters, rich in nutrients, formed over the shallow
in shallow waters but during the rest of the year they were
waters of the shelf areas of the North Aegean Sea during
found deeper than 50 m. In March all males and females
winter, slide towards the deep cavities (G
caught were mature.
EORGOPOULOS et
al., 1988). This may result in higher biological productiv-
ity in deeper waters and could probably be related to the
DISCUSSION
seasonal movement of these species.
The nine species found off north-eastern Greek coasts
R. minor was the second most abundant sepiolid spe-
cover 2/3 of the 12 sepiolids recorded from the Aegean
cies, caught mostly together with S. oweniana and R.
Sea (LEFKADITOU, unppublished data). Among the sepi-
macrosoma. These three species show an aggregation-
olid species missing from our collection, Sepiola robusta
forming behaviour as also reported for other areas
and Sepietta obscura have been rarely caught in the
(BOLETZKY, 1995), although the number of caught speci-
southern and eastern part of the Aegean Sea (SALMAN et
mens per haul very rarely exceeded 100 in the area inves-
al., 1997, 2002), whereas the pelagic Heteroteuthis dispar
tigated. On the contrary, species of the genus Sepiola pre-
was the most common cephalopod collected by frame
sented a low frequency of occurrence in the catches,
mid-water trawl over the trench south of Chalkidiki
never exceeding ten individuals per haul. Among them S.
peninsula (LEFKADITOU et al., 1999). In the Mediterranean
rondeleti was most frequently caught, extending its maxi-
Sea, up to now, there are records for 15 sepiolid species
mum depth distribution previously recorded (GUERRA,
(BELLO, 1995), including three more species: the infralit-
1982). This species has been generally poorly represented
toral Sepiola aurantiaca, and the bathyal Sepiola steen-
in samples from the Mediterranean Sea, most probably
strupiana and Stoloteuthis leucoptera, which generally
due to its preference for shallow waters (JEREB et al.,
have been very rarely caught.
1997).
The bathymetric distribution of the identified species
Mature specimens of both sexes of the species caught
and their numerical consistence in the catches is generally
during this study were generally present all over the year
in accordance with what has been reported for other Med-
(Table II), indicating an extended reproductive period of
iterranean areas (ORSI-RELINI & BERTULETTI, 1989;
sepiolids. For the species of the Rossinae subfamily, a
BOLETZKY, 1995; JEREB et al., 1997, 1998; SÁNCHEZ &
seasonal peak of spawning activity, as well as earlier mat-
DEMESTRE, 2001).
uration of males could be detected, as has also been men-
S. oweniana was the most abundant and eurybathic
tioned for other areas (D' ONGHIA et al., 1993, 1994;
sepiolid species, as has been observed in other areas of
JEREB et al., 1998). For the species of Sepiolinae sub-
the Mediterranean Sea (BOLETZKY, 1995). Seasonal
family, as mentioned also by other authors (JEREB et al.,
changes in the species abundance by depth are related to
1997), mature specimens represent higher percentages
recruitment variation in deeper grounds, as well as to
with no substantial differences related to seasons. How-
migration of larger individuals in shallower waters from
ever it has to be noted that the low percentages of imma-
early summer to autumn most probably for spawning
ture individuals of the species of the Sepiolinae subfamily
since highest percentages of mature females were found
and especially those of smaller sizes (Table II), may be
in these depths. Similar migration has been reported by
due to the low efficiency of the commercial trawl net used
MANGOLD-WIRTZ (1963) in the northern Catalan Sea,
in capturing smaller individuals.
204
Eugenia Lefkaditou and Panagiotis Kaspiris
REFERENCES
Ripo de Janeiro e Mar de Plata. D.Sc. Thesis, Instituto Oce-
anografico de São Paolo, 102 p.
BELLO, G. (1991). Role of cephalopods in the diet of swordfish,
KATAGAN, T. & A. KOCATAS (1990). Note préliminaire sur les
Xiphias Gladius, from the eastern Mediterranean Sea. Bulle-
Céphalopodes des Eaux Turques. Rapports Commision
tin of Marine Science, 49 : 312-324.
International Mer Méditerranée, 32 : 242.
BELLO, G. (1995). A key for the identification of the Mediterra-
KATAGAN, T., A. SALMAN & H.A. BENLI (1993). The cephalopod
nean sepiolids (Mollusca : Cephalopoda). Bulletin de l'Insti-
fauna of the Sea of Marmara. Israel Journal of Zoology, 39 :
tut Océanographique Monaco, no spécial 16 : 41-55.
255-262.
BELLO, G. (1996). Teuthophagous predators as collectors of oce-
KOUTSOUBAS, D., A. TSELEPIDES & A. ELEFTHERIOU (2000).
anic cephalopods : The case of the Adriatic Sea. Bolletino
Deep-sea Molluscan Fauna Of The Cretan Sea (Eastern
Malacologico, 32(1-4) : 71-78.
Mediterranean) : Faunal, Ecological & Zoogeographical
B
Remarks. Senk. Maritima, 30(2) : 85-98.
ELLO, G., (1999). Cephalopods in the diet of albacore, Thunnus
alalunga, from the Adriatic Sea. Journal of Molluscan Stud-
LEFKADITOU, E. & P. KASPIRIS (1998). Distribution an reproduc-
ies, 65 : 233-240.
tive biology of Sepietta neglecta (Naef, 1916)
BLANCO, C., J. AZNAR & J.A. RAGA (1995).Cephalopods in the
(Cephalopoda : Sepioidea) in the North Aegean Sea (Eastern
diet of the striped Dolphin Stenella coeruleoalba from the
Mediterranean). The Veliger, 41 : 239-242.
estern Mediterranean during an epizotic in 1990. Journal of
LEFKADITOU, E., C. PAPACONSTANTINOU & K. ANASTASOPOULOU
Zoology, London, 237 : 151-158.
(1999). Juvenile cephalopods collected in the midwater
BOLETZKY, S.V. (ed.) (1995). Mediterranean Sepiolidae. Bulletin
macroplankton over a trench, in the Aegean Sea (north east-
de l'Institut Océanographique Monaco, no spécial 16.
ern Mediterranean). Israel Journal of Zoology, 45 : 395-405.
BRAY, J.R., & J.T. CURTIS (1957). An ordination of the upland
MANGOLD-WIRTZ, K. (1963). Biologie des Cephalopodes ben-
forest communities of Southern Wisconsin. Ecol. Monogr.
thiques et nectoniques de la Mer Catalane. Vie Millieu, Supl.
27 : 325-349.
13 : 285p.
CASALI, P., G. MANFRIN-PICCINETTI & S. SORO (1998). Cephalo-
ORSI RELINI, L. & M. BERTULETTI (1989). Sepiolinae (Mollusca,
pods distribution in the North and Central Adriatic Sea. Bio-
Cephalopoda) from the Ligurian Sea. Vie Milieu, 39 (3/4) :
logia Marina Mediterranea, 5(2) : 307-317.
183-190.
CLARKE, K.R., & R.N. GORLEY (2001). PRIMER v5 : User Man-
ORSI-RELINI, L., F. GARIBALDI, G. PALANDRI, & C. CIMA (1994).
ual/Tutorial. Plymouth : PRIMER-E Ltd, 91p.
La comunita mesopelagica e i predatori "di superficie". Bio-
D'O
logia Marina Mediterranea, 1 : 105-112.
NGHIA, G., A. TURSI, C. PAPACONSTANTINOU & A. MATARRESE
(1991). Teuthofauna of the North Aegean Sea : Preliminary
ORSI-RELINI, L., F. GARIBALDI, C. CIMA & G. PALANDRI (1995).
results on catch, composition and distribution. FAO Fisheries
Feeding of the swordfish, the bluefin and other pelagic nek-
Report No 477 : 69-84.
ton in the western Ligurian Sea. ICCAT Collective Volume
D'O
of Scientific Papers, 44(1) : 283-286.
NGHIA, G., A.TURSI, P. PANETTA & A. MATARRESE (1993).
Occurrence of Neorossia caroli (Joubin, 1902) (Mollusca :
QUETGLAS, A., A. CARBONELL & P. SÁNCHEZ (2000). Demersal
Cephalopoda) in the Middle-Eastern Mediterranean Sea. In
continental shelf and upper slope cephalopod assemblages
T. OKUTANI, R. K. O' DOR & T. KUBODERA (eds). Recent
from the Balearic Sea (north-western Mediterranean). Bio-
Advances in Fisheries Biology, pp 93-96.
logical aspects of some deep-sea species. Estuarine, Coastal
D'ONGHIA, G., A.TURSI, P. PANETTA & P. MAIORANO (1994).
and Shelf Science, 50 : 739-749.
Nota sula biologia di Rossia macrosoma (Mollusca, Cepha-
SALMAN, A., T. KATAGAN, & H. A. BENLI (1997). Bottom trawl
lopoda) nel Mar Egeo Settentrionale. Biologia Marina Medi-
teuthofauna of the Aegean Sea. Archive of Fishery and
terranea, 1(1) : 329-330.
Marine Research, 45(2) : 183-196.
D'ONGHIA, G., A. MATARRESE, A.TURSI & P. MAIORANO (1996).
SALMAN, A., T. KATAGAN, & H. A BENLI (1998). On the cepha-
Cephalopods collected by bottom trawling in the North
lopod fauna of northern Cyprus. Israel Journal of Zoology,
Aegean Sea (Eastern Mediterranean). Oebalia, 22 : 33-46.
44 : 47-51.
GEORGOPOULOS, D., A. THEOCHARIS, G. ZODIATIS & S. CHRISTIANI-
SALMAN, A., T. KATAGAN, & H. A BENLI (2002). Cephalopod
DIS (1988). On the formation of dense water over the shelf
Fauna of the Eastern Mediterranean. Turkish Journal of
areas of the northern Aegean Sea. Rapports Commision Inter-
Zoology, 26 : 47-52.
national Mer Méditerranée, 31 : 201.
SÁNCHEZ, P. & M. DEMESTRE (2001). Sepiolidae (Mollusca,
GONZÁLEZ, M. & P. SÁNCHEZ (2002). Cephalopod assemblages
Cephalopoda) from the Catalan Sea, northwestern Mediter-
caught by trawling along the Iberian Peninsula Mediterra-
ranean. Rapports Commision International Mer Méditer-
nean coast. Scientia Marina, 66 (Suppl. 2) : 199-208.
ranée, 36 : 320.
GUERRA, A. (1982). Cefalópodos capturados en la campaña
TURSI, A. & G. D'ONGHIA (1992). Cephalopods of the Ionian Sea
"Golfo de Cádiz-81". Resultados de Expediciones Científi-
(Mediterranean Sea) Oebalia, 18 N.S. : 25-43.
cas del B/O Cornide, 10 : 17-49.
ÜNSAL, Ï., N. ÜNSAL, M. H. ERK & H. KABASAKAL (1999).
GUERRA, A. (1992). Mollusca, Cephalopoda. In : RAMOS, M. A. et
Demersal cephalopods from the Sea of Marmara with
al., eds. Fauna Ibérica, Vol. 1. Museo Nacional de Ciencias
remarks on some ecological characteristics. Acta Adriatica,
Naturales. CSIC, Madrid, 327p.
40(1) : 105-110.
JEREB, P., A. MAZZOLA & M. DI STEFANO (1997). Sepiolinae
VILLANUEVA, R. (1992). Deep-sea cephalopods of the north-
(Mollusca : Cephalopoda) from the strait of Sicily. Scientia
western Mediterranean : indications of up-slope ontogenetic
Marina, 61(4) : 459-470.
migration in two bathybenthic species. Journal of Zoology,
JEREB, P., A. MAZZOLA & M. DI STEFANO (1998). Rossiinae (Mol-
London, 227 : 267-276.
lusca, Cephalopoda) from the Strait of Sicily. Bolletino
WÜRTZ, M., R. POGGI & M. R. CLARKE (1992). Cephalopods
Malacologico, 33 (9-12) : 157-160.
from the stomachs of a Risso's Dolphin (Grampus griseus)
JUANICO, M. (1979). Contribuçao ao estudo da biologia dos
from the Mediterranean. Journal of the Marine Biological
Cephalopoda Loliginidae do Atlantico sul ocidental, entre
Association of the United Kingdom, 72 : 861-867.
Belg. J. Zool., 135 (2) : 205-207
July 2005
Analysis of the post-vitellogenic oocytes of three species
of Danubian Acipenseridae
Mirjana Lenhardt1, Roderick Nigel Finn2, Predrag Cakic1, Jelena Kolarevic3, Jasmina Krpo-
Cetkovic3, Ivica Radovic3 and Hans Jørgen Fyhn2
1 Institute for Biological Research "Sinisa Stankovic", 29 novembra 142, 11000 Belgrade, Serbia and Montenegro
2 Department of BiOlogy, University of Bergen, Allegt 41, N-5020 Bergen, Norway
3 Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia and Montenegro
Corresponding author : Mirjana Lenhardt, e-mail : lenhardt@ibiss.bg.ac.yu
ABSTRACT. Post-vitellogenic oocytes of beluga (Huso huso Linnaeus, 1758), Russian sturgeon (Acipenser
gueldenstaedtii Brandt, 1883) and sterlet (Acipenser ruthenus Linnaeus, 1758), sampled downstream of the "Iron
Gate II" dam on the Danube River, were characterised according to diameter, dry mass, water and protein contents.
All oocytes examined were ovoid in shape with the major diameter being measured in the animal-vegetal axis. The
beluga oocytes were the largest, with major and minor diameters of 4.18 ± 0.13 and 3.61 ± 0.14 mm, respectively.
The oocytes of the Russian sturgeon were the next largest, with major and minor diameters of 3.69 ± 0.16 and 3.36
± 0.15 mm, respectively, while those of the sterlet were the smallest, with major and minor diameters of 2.40 ± 0.10
and 2.14 ± 0.07 mm, respectively. Values for oocyte wet and dry mass (mg/ind) ranged from 25.9-32.1 for wet mass
and 12.2-15.5 for dry mass of the beluga oocytes, 18.9 ± 1.4, and 9.01 ± 0.12 for wet and dry mass of the Russian
sturgeon oocytes, to 6.5 ± 0.3 and 3.07 ± 0.14 of the sterlet oocytes. The water content of the oocytes of all three
sturgeons was very similar (51-53% of wet mass). The protein content (% of dry mass) was highly conservative
among the species at 53.0 ± 2.0, 55.9 ± 3.8 and 50.0 ± 1.2 for the oocytes of beluga, Russian sturgeon and sterlet,
respectively.
KEY WORDS : Russian sturgeon, beluga, sterlet, oocytes, Acipenseridae, yolk proteins
INTRODUCTION
The most significant research on the biology and culti-
vation of sturgeons was conducted in the former Soviet
The Acipenseriformes live almost exclusively in the
Union (DETTLAFF et al., 1993). Since the collapse of the
Northern Hemisphere with half of the extant number of
Soviet Union, however, virtually all research effort has
species occurring in Europe, mostly in the Ponto-Caspian
ceased through lack of funding.
region (Billard & Lecointre, 2001). Recently several asso-
The situation is very much the same in the countries
ciations have recommended that the status of beluga (Huso
bordering the lower region of the Danube (Serbia and
huso) be upgraded to Appendix I under current CITES list-
Montenegro, Romania, Bulgaria and Ukraine). Despite
ings since it has almost been extirpated from the Black Sea
the research effort of DETTLAFF et al. (1993), some
(Vecsei et al., 2002). Indeed many of the stocks of stur-
problems regarding normal growth and success of fer-
geons have dramatically decreased, primarily as a result of
tilization of the oocytes and eggs still exist. According
over fishing and habitat deterioration. Habitat loss is pre-
to AMIRKHANOV (1974) earlier studies suggested that
dominantly caused by pollution and damming of rivers,
protein concentration in oocytes can be a valid indica-
which blocks migration and access to proper spawning
tor of the staging, quality and successful fertilization
grounds (STEVENSON & SECOR, 1999 ; Vecsei et al., 2002).
and normal growth of the fertilized eggs (BRASHE,
In Yugoslavia there was a significant drop in catch of
1964 ; FEDOROVA & GRUDANOV, 1968). More recently,
all sturgeon species after 1970 and 1984, when the lower
CHEBANOV (2001) conducted similar research on Rus-
stretch of the Danube was dammed by, respectively, Djer-
sian sturgeon (Acipenser gueldenstaedtii) in which he
dap I and II hydropower stations (JANKOVIC, 1993 ; VEC-
followed protein and water contents in the oocytes over
SEI et al., 2002). Today, species of Acipenseridae, except
a ten year period. Together with other physiological
sterlet, occur in Serbia and Montenegro only in a 17.8 km
parameters, these findings helped him to evaluate
stretch of the Danube River, from the Djerdap II dam to
reproductive quality of the natural and artificially
the border with Bulgaria, close to the Timok River mouth.
reared populations.
Presently sturgeon farming, outside of Serbia and Mon-
Consequently, the goal of this investigation was to
tenegro, yields more than 2,000 tons of fish per year and
make a preliminary comparative study of the biometry,
about 15 tons of caviar. Such efforts could contribute to a
gravimetry and protein contents of the oocytes of three
reduction of fishing pressure on wild stocks (BILLARD &
species of Danube sturgeons : beluga, Russian sturgeon
LECOINTRE, 2001).
and sterlet (Acipenser ruthenus).
206
M. Lenhardt, R.N. Finn, P. Cakic, J. Kolarevic, J. Krpo-Cetkovic, I. Radovic and H.J. Fyhn
MATERIAL AND METHODS
All females were sampled during the spring and fall of
2001 in the Danube, downstream of "Iron Gate II" dam
(863 km from the Danube delta). Oocytes were sampled
from three beluga females (BeB, BeC, BeD) caught in
April and May, total length (TL) = 282, 287, 304 cm and
wet mass (W) = 161, 194.5, 159.6 kg respectively, one
Russian sturgeon (GuA) caught in October, TL = 180 cm,
W = 25 kg and two sterlets (RuA, RuB) caught in April,
total length (TL) = 64, 68 cm and wet mass (W) = 1.3, 1.5
kg. The second sterlet (RuB) had undergone final oocyte
maturation and provided ovulated eggs.
Major (D ) and minor (D ) diameters were measured in
1
2
0.9% NaCl. Wet masses were determined after removal
of excess ovarian fluid, and the samples were frozen and
stored at 20°C until lyophilisation, dry mass and protein
content analyses.
Oocyte volume (V) was calculated using the formula :
2
4
v = - ·
D
·
1
D
·
2
3
---
---
2
2
where D and D represent the major and minor diame-
1
2
ters respectively.
Oocyte wet and dry masses were measured to the near-
est 0.1 mg. Lyophilisation was performed for 48 hours.
Oocyte proteins were precipitated with 1 mL 6%
trichloro-acetic acid TCA to remove free amino acids,
then centrifuged (10,000 x g, 5 min, 4° C). The precipitate
was washed once in 6% (TCA), then solubilised in 1M
NaOH. Solubilisation was accomplished with sonification
(3 x 15 sec at 400 Hz). Prior to analyses, 1 mL double-
distilled water was added to give a final concentration of
0.5M NaOH. Following the addition of the Lowry rea-
gents (LOWRY et al., 1951), triplicate samples were read at
650 nm with a Pye Unicam spectrophotometer. Bovine
Fig. 1. Major (D ) and minor (D ) diameter, volume, wet
1
2
serum albumin was used as standard.
(WM) and dry (DM) mass, water and protein content of beluga
(Be) oocytes, sterlet (RuA) oocytes, sterlet (RuB) eggs and
Russian sturgeon (GuA) oocytes.
RESULTS
The largest oocytes were obtained from beluga, and
smallest from sterlet, while Russian sturgeon had inter-
DISCUSSION
mediate sized oocytes (Fig. 1). The size classification was
also evident for wet mass and dry mass, and reflected the
The data concerning oocyte biometry and gravimetry
size of the female caught. However, despite the differ-
for three Danube sturgeon species were correlated with
ences in size, all oocytes had similar water content with
parental size. Beluga oocyte diameter, volume, wet and
values of 51-53% of wet mass. Similarly, the oocyte rela-
dry mass were the largest followed by Russian sturgeon,
tive protein content (% of dry mass) was also conserved
then sterlet.
between the species and ranged from 50-56%.
Average diameters of three beluga oocytes were
Overall the data show that irrespective of size, the pro-
4.18 mm for major and 3.61 mm for minor diameter. Data
tein content and cell water are closely regulated compo-
given by HOLCIK (1989) for this parameter were around
nents of the post-vitellogenic oocytes of the Danube stur-
3.8 mm for major and 3.4 mm for minor diameter, which
geons.
corresponded better to the data obtained for Russian stur-
From one species only, the sterlet, we had the opportu-
geon (3.7 and 3.4 mm). Between these two results are
nity to sample oocytes (RuA) and ovulated eggs (RuB).
those (4.0 and 3.6 mm) obtained by Dettlaff & Ginsburg
From Fig. 1 it is possible to see that ovulated eggs of ster-
(1954). According to BERG (1949) 3.5 mm and 3.0 mm
let had bigger values for diameter, volume and protein
are average values for major and minor diameters respec-
content compared to the oocytes of the RuA female.
tively.
Danube sturgeons' oocytes
207
There are several data given for sterlet oocyte diame-
DETTLAFF, T.A. & A.S. GINSBURG (1954). The embryonic devel-
ters by different authors. According to HOLCIK (1989)
opment of sturgeons (stellate sturgeon, Russian sturgeon,
oocyte diameter is around 2.5 mm. JANKOVIC (1958)
beluga) in connection with questions of their reproduction.
noted that oocyte diameters ranged from 2.0-2.9 mm for
Acad. Sci. Press, Moscow.
major axis and 1.8-2.8 mm for minor axis. Values
DETTLAFF, T.A., A.S. GINSBURG & O.I. SCHMALHAUSEN (1993).
obtained in the present study were 2.7 and 2.4 mm for the
Sturgeon fishes development biology and aquaculture. Hei-
delberg, Berlin, Springer-Verlag, New-York.
major and minor diameters of the ovulated eggs found in
FEDOROVA, L.S. & S.D. GRUDANOV (1968). Some aspects of the
the abdomen of RuB, and 2.4 mm and 2.1 mm for the
protein metabolism in beluga females from the spring
major and minor diameters of the post-vitellogenic
migration during gonad maturation. In : Elaboration of the
oocytes of RuA.
biological bases and biotechnics of rearing in sturgeon
Average wet mass of beluga oocytes was 29.3 mg, and
fisheries in bodies of water of the USSR, Astrakhan.
14.0 for its dry mass. Wet and dry mass for oocytes of
FINN, R.N., H.J. FYHN, B. NORBERG, J. MUNHOLLAND, & M.
REITH (2000). Oocyte hydration as a key feature in the adap-
Russian sturgeon were 18.9 mg and 9.0 mg, and 6.5 mg
tive evolution of teleost fishes to seawater. In : NORBERG,
and 3.1 mg for sterlet oocytes. CHEBANOV (2001) found a
KJESBU, TARANGER, ANDERSON & STEFANSSON (eds), Proc 6th
difference in Russian sturgeon oocytes wet mass in the
Int. Symp. Reprod. Physiol. Fish, Inst Mar Res & Univ Ber-
years 1991 - 2000. In that period, values ranged from 17.9
gen, ISBN : 82-7461-048-2 : 289-291.
to 20.4 mg, which is very similar to results presented
FINN, R. N., M. LENHARDT, A. FERRARA, P. CAKIC, J.J. ISELY, J.
here.
DEAN, M.S. EVJEN & H.J. FYHN (2001). Yolk proteins and
free amino acids in Acipenseriformes. Abstract : Tenth Euro-
Oocyte water and relative protein content of all three
pean Ichthyological Congress in Prague 3-7th September
sturgeons were very similar. The water content results are
2001.
at the lower range of 50-70 % reviewed by KAMLER
FINN, R.N., G.C., ØSTBY, B. NORBERG, & H.J FYHN. (2002a). In
(1992) for freshwater fishes, and the protein content was
vivo oocyte hydration in Atlantic halibut (Hippoglossus hip-
similar to the lower range reviewed by KAMLER (1992).
poglossus). Proteolytic liberation of free amino acids, and
Indeed the values found here for beluga are considerably
ion transport are driving forces for osmotic water influx. J.
lower than the recomputed 63% reported by KAMLER
Exp. Biol., 205 : 211-224.
(1992). Unlike the pelagic eggs of marine fishes (F
F
INN et
INN, R.N., M. WAMBOLDT, & H.J. FYHN (2002b). Differential
al., 2000 ; 2002a ; 2002b), sturgeon oocytes do not
processing of yolk proteins during oocyte hydration in fishes
(Labridae) that spawn benthic and pelagic eggs. Mar. Ecol.
undergo proteolysis and hydration during final oocyte
Prog. Ser. 237 : 217-226.
maturation (FINN et al., 2001 ; 2002c). Our findings sug-
FINN, R.N., M., LENHARDT, A., FERRARA, J.J., ISELY, J. DEAN, &
gest that, despite the difference in size of both female and
H.J. FYHN (2002c). Yolk proteins and free amino acids in
oocyte, water content and protein levels are conservative
Acipenseriformes. Proc. 26th Larval Fish Conference of the
aspects of the reproductive biology of sturgeons.
American Fisheries Society. Bergen, Norway, 22-26 July.
HOLCIK, J. (1989). Freshwater fishes of Europe. General intro-
duction to fishes and Acipenseriformes. Aula Verlag, Wies-
REFERENCES
baden.
JANKOVIC, D. (1958). Ecology of Danubian sterlet (Acipenser
AMIRKHANOV, G.A. (1974). The dynamics of free amino acid
ruthenus). Institute for Biological Research, Belgrade.
content during the embryonic development of the sturgeon,
JANKOVIC, D. (1993). Populations of Acipenseridae prior and
Acipenser gueldenstaedtii. Vopr Ihtiol., 19 : 127-131.
after the construction of the HEPS Djerdap I and II. Ichthyo-
B
logia, 25 : 29-34.
ERG, L.S. (1949). The freshwater fishes of the USSR and adja-
cent countries. Akademia nauk USSR, Moscow & Lenin-
KAMLER, E. (1992). Early life history of fish. An energetic
grad.
approach. Chapman and Hall, Fish and Fisheries Series 4.
London
BILLARD, R. & G. LECOINTRE (2001). Biology and conservation
L
of the sturgeon and paddlefish. Rev Fish Biol Fish, 10 : 355-
OWRY O.H., N.J. ROSEBROUGH, A.L. FARR & R.J. RANDALL
(1951). Protein measurement with the folin phenol reagent. J
392.
Biol Chem, 193 : 265-275.
BRASHE, Z. (1964). Biochemical embryology. Inostr. Lit-ra,
STEVENSON, J.T. & D.H. SECOR (1999). Age determination and
Moscow.
growth of Hudson River Atlantic sturgeon, Acipenser
CHEBANOV, M.S. (2001). Ecological-technological principles of
oxyrinchus. Fish. Bull., U.S., 98 : 153-166.
stock enchancement and living gene bank formation for con-
VECSEI, P., R. SUCUI & D. PETERSON (2002) Threatened fishes of
servation of Caspian and Azov Sea sturgeon diversity.
the world : Huso huso (Linnaeus, 1758) (Acipenseridae).
Report of Krasnodar Research Institute of Fisheries.
Environ Biol Fish 65 : 363-365.
Belg. J. Zool., 135 (2) : 209-215
July 2005
Successional stages of experimental artificial reefs
deployed in Vistonikos gulf (N. Aegean Sea, Greece) :
Preliminary results
Georgios Manoudis1, Chryssanthi Antoniadou1, Konstantinos Dounas2 and Chariton Ch.
Chintiroglou1
1 Department of Zoology, School of Biology, Aristotle University of Thessaloniki, PO Box 134, Gr-540 06, Thessaloniki, Greece
2 Institute of Marine Biology of Crete, PO Box 2214, Gr-71003, Heraklion, Greece
Corresponding author : Chariton Ch. Chintiroglou, e-mail : chintigl@bio.auth.gr
ABSTRACT. In 1999 an artificial reef system, consisting of a protective zone (240 cubic modules) and a nucleus (9
Italian type and 9 French type artificial reefs), was constructed and deployed at cape Fanari (Vistonikos Gulf, North
Aegean Sea) occupying an area of 6 Km2 (25m depth). Samples, (8 cement plates, 35cmx35cm) were collected sea-
sonally with SCUBA-diving from March 2000 till May 2001. Overall 46986 individuals were counted belonging to
13 classes, while 88 species were recorded. Common biocoenotic parameters (numerical abundance, frequency,
mean dominance) were calculated. Shannon-Weaver index ranged from 2.509 to 3.741 and evenness from 0.388 to
0.579, both exhibiting a maximum in summertime. The analysis revealed a clear dominance of Serpulids during the
first three periods and of Peracarida for the last two. Filter-feeder organisms including Pomatoceros triqueter,
Spirobranchus polytrema and Corophium sextonae dominated the samples. Two-way ANOVA indicated significant
differences in numerical abundance of each taxon with time. However, no differences were recorded among taxon
from the top and the base of the pyramids except for Gastropods,which showed a significant increase in numerical
abundance at the top blocks. Cluster analysis provided a dendrogram with 6 groups at a 73% similarity level, 5 of
which group together the replicates of each period, except one replicate, from the last period, that forms the 6th
cluster. Filter-feeders appeared to be the prevailing organisms in artificial reefs communities.
KEY WORDS : artificial reefs, benthic communities, filter- feeder organisms, Aegean Sea.
INTRODUCTION
Posidonia oceanica meadows. The aim of this study was
to provide preliminary information on the successional
The establishment of artificial reefs is a measure of
stages of benthic invertebrates during the first year of the
global importance for the management of coastal marine
reef's deployment at cape Fanari (Vistonikos gulf).
ecosystems (FITZHARDINGE & BAILEY-BROCK, 1989 ;
RELINI et al., 1990). During the last ten years, artificial
MATERIAL AND METHODS
reefs have proved to be a very effective means for fishery
enhancement (PICKERING et al., 1998). However, they can
Description of the deployment area
play an important role for the coastal zone marine bio-
coenoses, including protection from the mechanical
The deployment area, located between Vistonikos Gulf
impact of trawling, habitat restoration, increase of the
and cape Corosmilou (N Aegean Sea) (Fig.1), included
spatial heterogeneity and variety of substrata on soft sea-
the nucleus of the artificial reefs (3.500 m2) and the pro-
beds, aquaculture and, recently, tourism (B
tective zone (6 km2). The bottom of the study area slopes
OMBACE et al.,
1994 ; P
slightly offshore, forming a flat field at a depth of 20 m,
ICKERING et al., 1998). Consequently, the majority
of the studies concern the potential and capability of these
which is covered by a dense, well-developed Posidonia
structures to act as fish attracting and aggregating
oceanica meadow. However, during the last years,
devices. However, an aspect of artificial reef studies that
repeated mechanical damaging caused mainly by otter-
is often overlooked is their colonization by sessile and
and beam-trawling, resulted to serious regression of these
other invertebrate organisms, which provide food and
meadows and their associated biota. Thus, the main part
shelter for fish and crustaceans (C
of the seabed consists of a completely degraded meadow,
ARTER et al., 1985).
which is often replaced by muddy sheets containing
Although artificial reefs have been deployed in Europe
organic detritus and characterized by the presence of Tur-
since 1960s, their use has increased in the last two dec-
itella communis (BELLAN-SANTINI et al., 1994). Only 25%
ades (SANTOS & MONTEIRO, 1998). In Greece, the first
of the area is covered by a well-developed and continuous
experimental reefs were deployed in July 1998 (SINIS et
Posidonia oceanica meadow. Seawater samples, at the
al., 2000) and the first extensive protective zone with arti-
broader coastal region, were carried out at approximately
ficial reefs was established in October 1999, primarily in
bimonthly intervals from October 1997 to April 1998,
order to increase fish production and protect the existing
using NISKIN (5L) sampler. Nutrients (phosphate,
210
Georgios Manoudis, Chryssanthi Antoniadou, Konstantinos Dounas and Chariton Ch. Chintiroglou
nitrate, nitrite, silica, and ammonia), organic carbon,
productivity that, often, favours phytoplankton blooms
chlorophyll-a and phaeopigments concentrations for the
(DOUNAS, unpubl. data). Moreover, prevailing currents
critical periods (October and February) are shown in
are easterly and their velocity ranges from 1cm/sec to
Table 1. The coastal area of Rodopi could be character-
24.4 cm/sec, with a mean value of 6.8 cm/sec (DOUNAS,
ized as typically eutrophic, with relatively high primary
1998).
Fig. 1. Location of the deployment area. Site A represents the protective zone and
the nucleus.
TABLE 1
Nutrients, organic carbon (POC), chlorophyll-a and phaeopigments concentrations in Vistonikos Gulf during October 1997 and Febru-
ary 1998 (Mean value, Standard deviation and range).
October 1997
February 1998
Parameter
Mean value (SD)
Range
Mean value (SD)
Range
Chlorophyll (m/L)
0.292 (0.387)
0.096-1.897
0.663 (0.29)
0.213-1.381
Phaeopigments (m/L)
0.236 (0.386)
0.044-1.828
0.601 (0.252)
0.046-1.113
POC (m/L)
499.8 (197.69)
308-1053
661 (208.4)
276-1029
Nitrate NO (mM)
2.8 (0.989)
1.41-4.40
1.12 (0.53)
0.38-2.52
3
Nitrite NO (mM)
0.46 (0.306)
0.14-1.38
0.42 (0.211)
0.11-0.97
2
Phosphorus PO (mM)
0.056 (0.026)
0.035-0.160
0.115 (0.041)
0.065-0.2
4
Silica SiO (mM)
2.68 (0.995)
1.12-4.78
3.04 (1.867)
1.26-9.65
2
Ammonium NH (mM)
0.496 (0.149)
0.256-0.768
0.454 (0.304)
0.16-1.17
4
Description of the reef
meadow. Moreover, they provided additional hard sub-
strata for benthic fauna thus increasing environmental
Two groups of artificial reefs, located 25 m apart from
carrying capacity of the reef.
each other, formed the nucleus zone of the deployment
area. The first group was formed of 9 pyramids (Italian
type), which are placed in a three-series arrangement.
Data collection
Each pyramid was made of 5 cubic concrete blocks
The survey of the colonization process was restricted to
(2x2x2 m), four at the base and one at the top, placed at
the Italian type units. For this purpose, square concrete
about 15 m from each other. At the sides of the blocks
plates (35x 35 cm) were placed at the 2 upper corners at
holes of different diameter were created, increasing shel-
each side of each block. A total of 5 samplings were car-
ter availability (BOMBACE et al., 1994 ; ARDIZZONE &
ried out from March 2000 till May 2001. The initial sam-
BOMBACE, 1983 ; BOMBACE, 1977 ; BOMBACE, ; RELINI &
pling took place 5 months after immersion of the reef. At
RELINI, 1989). The second group was consisted of nine
each sampling, 8 plates (3 from the top and 5 from the
more units, each one made of bulky cement-bricks on a
base block) were collected by divers, while visual moni-
cement base.
toring of the reef was carried out using an underwater
At the broader protective zone, 240 smaller units of
camera. The plates were transferred to the laboratory
artificial reefs (1,2x1,2x1, 2m), were placed on the seabed
where the surface of each plate was scraped, washed
at distances ranging from 80 to 250 m. The aim of these
through sieve with 0.5 mm mesh size and preserved in a
units was, mainly, the prevention of the illegal trawling at
10% formalin solution. After sorting, all faunal elements
the nucleus zone, in order to protect fish stocks and the
were counted and identified to species level.
Successional stages of experimental artificial reefs deployed in Vistonikos gulf
211
Data analysis
RESULTS AND DISCUSSION
Common biocoenotic parameters, including numerical
abundance (number of individuals/m2), mean dominance
Overall 46,986 individuals were counted belonging to
(number of ind. of each species/ total number of ind.), fre-
13 classes, while 88 species were recorded (Table 2). Dur-
quency and total species richness were calculated for each
period. Species diversity was estimated by using Shan-
ing the first three sampling periods (March/2000, May/
non-Wiener (H') and Pielou's Evenness (J') indices based
2000, July/2000) the dominant taxon was Polychaetes,
on log (B
mainly Serpulids, followed by Bivalves. During March/
2
AKUS, 1990 ; HONG, 1983). Two-way analysis
of variance was applied in order to check for significant
2000 and May/2000 the species are dominated by Spiro-
differences in each taxon's mean numerical abundance
branchus polytrema (27.1% and 54.6% for the first and
with time and, also, to compare between replicates of
second period respectively), while in July/2000 this spe-
each sample from different sites. Fisher's Least Signifi-
cies was replaced by Pomatoceros triqueter (18.4%).
cant Difference (LSD) test was used to compare across all
Concerning Bivalves, Anomia ephippium showed the
pairs of group means when corresponding ANOVA tests
highest mean dominance during March/2000, May/2000
were significant (p<0.05). Prior to performing these sta-
and July/2000, followed by Hiatella arctica. During
tistical tests, data were transformed (log ), when neces-
10
December/2000 Polychaetes and Peracarida exhibited
sary, to meet the assumptions of ANOVA. Numerical
equal values of mean dominance (34.0% and 32.0%
abundance data were analyzed using multivariate tech-
respectively) with Pomatoceros triqueter constituting on
niques (i.e., cluster analysis and multidimensional scal-
ing), based on the Bray-Curtis similarity, as adopted in
its own 28.7% of the mean dominance followed by
the PRIMER package (C
Corophium sextonae (26.4%). Bivalves were the third
LARKE & WARWICK, 1994 ;
C
dominant taxon (16.0%) represented mainly by Hiatella
LARKE & GREEN, 1988). All data were transformed (log
(x+1)) in order to weight the contribution of common and
arctica (6.8%). During May 2001, settlement was charac-
rare species (KLUIJVER, 1997 ; CLARKE & WARWICK,
terized by the clear dominance of Peracarida (56.0%)
1994). The significance of the multivariate results was
with Corophium sextonae (56.1%) being the most impor-
assessed by ANOSIM test.
tant species.
TABLE 2
Species found at each sampling period (from March 2000 until May 2001) on the cement blocks immersed in Vistonikos Gulf (F: Fre-
quency, mD: mean Dominance).
Sampling period
Species
March 2000
May 2000
July 2000
December 2000
May 2001
F
mD
F
mD
F
mD
F
mD
F
mD
Foraminifera
0
0
100
8,01
100
9,84
100
3,70
25
0,02
Calcarea
Sycon sp.
0
0
0
0
0
0
0
0
87,5
0,22
Polychaeta
Harmothoe spinifera (Ehlers, 1864)
37,5
0,23
25
0,05
37,5
0,04
87,5
0,24
100
0,25
Chrysopetalum debile
(Grube, 1855)
0
0
0
0
0
0
0
0
12,5
0,004
Phyllodoce madeirensis(Langerhans,1880)
12,5
0,03
0
0
0
0
12,5
0,01
87,5
0,10
Kefersteinia cirrata (Kef
erstein, 1862)
0
0
0
0
0
0
0
0
12,5
0,004
Odontosyllis ctenostoma (Claperede, 1868)
12,5
0,03
0
0
0
0
0
0
0
0
Syllis hyaline
(Grube, 1863)
0
0
0
0
0
0
12,5
0,01
100
0,37
Trypanosyllis zebra
(Grube, 1860)
0
0
0
0
0
0
0
0
12,5
0,004
Autolytus edwardsii (Saint-Joseph, 1887)
12,5
0,09
0
0
0
0
0
0
0
0
Nereis rava (Ehlers, 1868)
0
0
12,5
0,01
12,5
0,01
62,5
0,35
100
1,13
Platynereis dumerilii (Fauvel, 1916)
12,5
0,03
25
0,03
37,5
0,10
75
0,24
37,5
0,03
Glycera tesselata (Ehlers, 1868)
0
0
0
0
0
0
0
0
25
0,01
Eunice vittata (delle Chiaje, 1929)
0
0
12,5
0,01
0
0
50
0,05
87,5
0,11
Lysidice ninetta (A
udiuin & E
dwards, 1834)
0
0
0
0
0
0
25
0,02
12,5
0,004
Marphysa fallax (
Marion & Bob
retzky, 1857)
0
0
0
0
0
0
0
0
12,5
0,01
Scoletoma funchalensis (K
inberg, 1865)
0
0
0
0
0
0
0
0
75
0,06
Terebella lapidaria (Linnaeus, 1767)
0
0
0
0
0
0
0
0
37,5
0,01
Polyophthalmus pictus (Cla
parede, 1864)
0
0
0
0
0
0
0
0
100
0,29
Nematonereis unicornis
(Grube, 1840)
0
0
0
0
0
0
0
0
100
0,50
Branchiomma bombyx (D
alyell, 1853)
0
0
0
0
0
0
0
0
37,5
0,03
Hydroides pseudouncinata (Zibrowius, 1971)
100
2,90
100
1,62
100
1,40
100
0,82
100
0,80
Pomatoceros triquete (Linnaeus, 1865)
100
12,49
100
18,09
100
18,39
100
28,73
100
14,93
Placostegus tridentatus (Fabricius, 1779)
100
0,82
0
0
0
0
0
0
0
0
Serpula vermicularis (Linnaeus, 1767)
100
3,29
100
2,59
100
1,97
100
2,89
100
4,72
Spirobranchus polytrema (Philippi, 1844)
100
54,58
100
27,10
100
14,66
100
1,87
100
1,06
Vermilliopsis infundibulum (Gmelin, 1788)
12,5
0,03
0
0
0
0
0
0
87,5
0,16
Protula sp.
(Risso, 1826)
0
0
0
0
0
0
0
0
25
0,01
Bivalvia
Chlamys varia (Linnaeus, 1758)
0
0
50
0,15
100
0,32
62,5
0,14
50
0,05
Acanthocardia tubercolata (Linnaeus, 1758)
0
0
100
0,56
37,5
0,07
100
0,35
37,5
0,01
Mytilus galloprovincialis (Lamarck, 1819)
12,5
0,06
37,5
0,31
75
0,38
62,5
0,26
87,5
0,13
Musculus subpictus (Cantraine, 1835)
100
2,43
100
1,25
100
3,79
100
1,41
0
0
Modiolus adriaticus (Lamarck, 1819)
100
1,84
100
0,68
100
1,19
100
2,28
87,5
0,85
212
Georgios Manoudis, Chryssanthi Antoniadou, Konstantinos Dounas and Chariton Ch. Chintiroglou
TABLE 2 (CONT.)
Species found at each sampling period (from March 2000 until May 2001) on the cement blocks immersed in Vistonikos Gulf (F: Fre-
quency, mD: mean Dominance).
Sampling period
Species
March 2000
May 2000
July 2000
December 2000
May 2001
F
mD
F
mD
F
mD
F
mD
F
mD
Hiatella arctica (Linnaeus, 1767)
100
2,10
100
6,11
100
6,79
100
6,80
87,5
6,19
Anomia ephippium (Linnaeus, 1758)
100
6,32
100
15,50
100
16,16
100
4,31
87,5
4,64
Ostrea edulis (Linnaeus, 1758)
0
0
12,5
0,05
0
0
0
0
62,5
0,03
Chamelea gallina (Li
nnaeus, 1758)
0
0
0
0
0
0
0
0
12,5
0,01
Arca tetragona
(Poli, 1795)
0
0
0
0
0
0
0
0
37,5
0,01
Polyplacophora
Acanthochitona fascicularis
(Risso, 1826)
0
0
0
0
0
0
0
0
12,5
0,004
Gastropoda
Jujubinus exasperatus (Pennant, 1777)
0
0
0
0
100
0,17
75
0,19
62,5
0,02
Bittium latreillei (Payraudeau, 1826)
0
0
0
0
100
1,44
100
7,14
87,5
2,32
Pusillina radiate (Philippi, 1836)
37,5
0,23
87,5
0,81
100
2,24
100
1,38
87,5
0,05
Odostomia conoidea (Brocchi, 1814)
12,5
0,03
12,5
0,05
0
0
0
0
50
0,05
Raphitoma echinata (Brocchi, 1814)
12,5
0,03
0
0
37,5
0,04
0
0
0
0
Anatoma crispate (F
leming, 1828)
0
0
0
0
0
0
0
0
87,5
0,27
Cerithium vulgatum (Bru
guiere, 1792)
0
0
0
0
0
0
0
0
37,5
0,03
Acmaea virginea (M
ueller O.F., 1776)
0
0
0
0
0
0
0
0
25
0,01
Nassarius incrassatus (
Stroem, 1768)
0
0
0
0
0
0
100
0,33
100
0,13
Turritella communis
(Risso, 1826)
0
0
0
0
0
0
0
0
12,5
0,004
Copepoda
100
0,92
100
3,53
100
1,31
75
0,24
12,5
0,01
Cirripedia
Balanus trigonus (Darwin, 1854)
100
1,51
100
1,82
87,5
0,85
75
0,44
100
0,32
Balanus perforatus (Brug
uiere, 1789)
50
1,61
75
1,41
50
0,52
62,5
1,33
37,5
0,87
Verruca stroemia (M
ueller O.F., 1776)
0
0
0
0
0
0
0
0
37,5
0,01
Malacostraca
Microdeutopus anomalus (Rathke, 1843)
100
3,85
100
3,94
100
5,48
100
0,31
75
0,03
Caprella acanthifera (Mayer, 1890)
37,5
0,36
50
0,22
100
0,68
100
0,51
62,5
0,03
Corophium sextonae (Crawford, 1937)
100
2,01
100
2,26
100
6,80
100
26,41
100
56,13
Dexamine spinosa (Montagu, 1813)
25
0,06
75
0,15
100
1,45
37,5
0,05
62,5
0,06
Stenothoe antennulariae (Della Valle, 1893)
75
0,56
25
0,05
50
0,36
0
0
0
0
Stenothoe bosphorana (Sowi
nsky, 1898)
0
0
87,5
1,07
25
0,12
0
0
75
0,07
Stenothoe monoculoides (Montagu, 1815)
37,5
0,16
87,5
1,98
75
1,79
87,5
0,21
100
0,30
Stenothoen gallensis (Walker, 1904)
0
0
0
0
12,5
0,05
0
0
0
0
Metaphoxus sp. (Bonier, 1890)
0
0
0
0
25
0,02
0
0
0
0
Metaphoxus simplex (B
ate, 1857)
0
0
25
0,07
12,5
0,01
12,5
0,01
0
0
Lysianassa caesarea (Ruffo, 1987)
37,5
0,09
37,5
0,07
75
0,14
100
0,91
100
0,11
Phtisica marina (Slabber, 1796)
12,5
0,06
0
0
25
0,02
0
0
0
0
Leucothoe spinicarpa (Abil
dgaard, 1789)
0
0
0
0
0
0
75
0,32
25
0,01
Liljeborgia dellavallei (St
ebbing, 1906)
0
0
0
0
0
0
87,5
0,53
37,5
0,02
Synchelidium longidigitatum
(Ruffo, 1947)
0
0
0
0
0
0
25
0,02
0
0
Iphimedia minuta (G.O. Sars, 1882)
0
0
12,5
0,01
0
0
62,5
0,11
25
0,01
Elasmopus rapax (A. Costa, 1853)
12,5
0,13
0
0
0
0
0
0
12,5
0,01
Gnathia vorax (Lu
cas, 1849)
0
0
12,5
0,01
12,5
0,01
50
0,09
62,5
0,03
Gnathia sp praniza (Leach, 1814)
0
0
37,5
0,05
25
0,03
37,5
0,04
37,5
0,03
Idotea baltic a (A
udouin, 1827)
0
0
0
0
0
0
0
0
37,5
0,01
Leptochelia savignyi (Kroyer, 1842)
50
0,16
12,5
0,01
100
0,35
87,5
2,21
87,5
0,08
Thorulus cranchii (Leach, 1817)
37,5
0,39
37,5
0,07
75
0,21
100
0,90
87,5
0,15
Athanas nitescens (Leach, 1814)
50
0,26
12,5
0,01
75
0,11
100
0,21
87,5
0,08
Alpheus dentipes (
Guérin, 1832)
0
0
0
0
0
0
75
0,17
50
0,03
Galathea intermedia (Lilljeborg, 1851)
0
0
0
0
0
0
0
0
25
0,05
Pisidia longicornis (Linnaeus, 1767)
0
0
0
0
25
0,10
100
0,42
75
0,05
Pilumnus spinifer (Edwards, 1834)
0
0
0
0
50
0,05
100
0,39
100
0,17
Pilumnus hirtellus (Linnaeus, 1761)
0
0
0
0
25
0,02
0
0
0
0
Pycnogonida
Achelia longipes (
Hodge, 1864)
0
0
0
0
0
0
0
0
37,5
0,02
Echinoidea (juveniles)
0
0
0
0
75
0,26
50
0,08204
25
0,01
Ophiur
oidea (juveniles)
0
0
0
0
0
0
12,5
0,01
12,5
0,004
Ascidiacae
Did
emnum sp.
0
0
0
0
0
0
12,5
0,01
50
0,01
Styela partita (Stimpson, 1852)
0
0
0
0
12,5
0,02
62,5
0,12
87,5
0,19
Styela plicata (Lesueur, 1823)
12,5
0,06
37,5
0,07
12,5
0,03
75
0,09
0
0
Phallusia mammillata (Cu
vier, 1815)
12,5
0,09
12,5
0,01
25
0,02
62,5
0,08
87,5
0,07
Number of individuals
3034
5655
9461
8532
20304
Number of species
36
39
46
50
74
Shannon index (H')
2,6594
3,3801
3,741
3,45028
2,5076
Evenness index (J')
0,4117
0,5233
0,5792
0,53415
0,3882
Successional stages of experimental artificial reefs deployed in Vistonikos gulf
213
The performance of two-way ANOVA indicated signif-
ences were recorded between samples from March/2000
icant differences among samples for every taxa : Peracar-
and May/2001, May/2000 and May/2001, March/2000
ida (F=36.05, p<0.05), Polychaetes (F=30.14, p<0.05),
and December/2000. Polychaetes showed higher signifi-
Eucarida (F =12.74, p<0.05), Bivalves (F=63.06, p<0.05)
cant differences between samples from March/2000 and
and Gastropods (F=16.82, p<0.05). The results of
May/2001, May/2000 and May/2001, December/2000
Fisher's Least Significant Difference (LSD) test are
and May/2001.
shown in Table 3. As regards Peracarida, higher differ-
TABLE 3
Results of two-way ANOVA (Fisher's LSD) among samples for each taxon. (* denotes a statistically signifi-
cant difference).
Polychaeta
Peracarida
Eucarida
Bivalves
Gastropods
March/00-May/00 -67,5
*-0,444
0,446
*-0,567
*-0,901
March/00-July/00
*150,0
*-0,928
-0,039
*-0,851
*-1,03
March/00-December/00
*93,5
*-1,15
*-0,709
*-0,553
*-0,665
March/00-May/01
*344,0
*-1,695
*-0,493
*-0,902
-0,296
May/00-July/00
*82,5
*-0,484
*-0,485
*-0,283
-0,131
May/00-December/00
-26
*-0,706
*-1,154
0,014
0,235
May/00-May/01
*276,5
*-1,251
*-0,939
*-0,334
*0,605
July/00-December/00
56,5
-0,222
*-0,669
*0,297
*0,366
July/00-May/01
*194,0
*-0,767
*-0,454
-0,051
*0,736
December/00-May/01
*250,5
*-0,544
0,215
*-0,349
*0,369
algal mean wet biomass at the top blocks was 169.8 g m-2
(a)
and at the base ones was 9.79 g m-2. Consequently, Gas-
Shannon Index (H')
4
Evenness Index (J')
tropods, which are mainly grazers, showed higher num-
3.74
3.5
bers at the top of the pyramids.
3.45
3.38
3
Serpulids, which was the main taxon in the present
2.5
2.659
2.507
study, have been reported among the first fouling organ-
2
isms that settle after the development of the bacterial film
1.5
(BOUGIS, 1976). Moreover, in our case the dense coloni-
1
zation of Serpulids may be attributed to the eutrophic
0.579
0.411
0.523
0.534
0.5
0.388
character of the deployment area of the reefs. Conse-
0
quently a high occurrence of filter-feeder organisms is
3/00
5/00
7/00
12/00
5/01
expected. Amphipods with the prevailing species
Month/ Year
Corophium sextonae which is also a filter-feeder organ-
ism and builds its tubes among Serpulids, using them as a
shelter from predators (BARNARD, 1958). The clear domi-
nance of the latter species in May/2001 could be attrib-
uted to its rapid maturation and long reproductive periods,
(b)
lasting, sometimes, for the whole year. Additionally, tur-
N.of Individuals
25000
80
bid waters bear organic and mineral particles, which are
74
N.of Species
70
20304
useful to fouling organisms for tube construction and food
s 20000
60
s
(BARNARD, 1958). BOMBACE et al. (1994), studying settle-
i
e
50
i
dual
v
46
ec
15000
50
p
ment on artificial substrata of sessile organisms, report
di
n
39
S
I
36
40
that the dominant organisms are always filter-feeders,
of
of
10000
9461
er
8532
30
b
including serpulids (Pomatoceros triqueter and Serpula
ber
m
m
5655
u
u
20
vermicularis) ascidians and some bivalve species
N
N
5000
3034
10
(Hiatella arctica and Anomia ephippium), that they were
0
0
present in this study too.
3/00
5/00
7/00
12/00
5/01
Month/ Year
Shannon-Wiener index (H') values ranged from 2.509
Fig. 2. (a) Shannon (H') and evenness (J') indices, based on
to 3.741 and Evenness (J') from 0.388 to 0.579, both
log transformation, and (b) number of individuals and number
2
showing a maximum in summertime (July 2000) (figure 2
of species for each sampling period (from March 2000 until
(a)). For both indices, the lowest value was recorded dur-
May 2001) in Vistonikos Gulf.
ing May/2001 due to the clear dominance of Corophium
sextonae.The low evenness values revealed that the com-
Finally, comparing replicates from the top and the base
munity has not reached the final climax stage yet (FIT-
of the pyramids, there were no significant differences for
ZHARDINGE, & BAILEY-BROCK, 1989 ; RELINI et al., 1990 ;
the four taxa except for Gastropods, which showed a sig-
RELINI, ; ODUM, 1993). The pattern of total species rich-
nificant increase in numerical abundance at the top blocks
ness and number of individuals (figure 2(b)) differed from
(F=37.33, p<0.05). At the top blocks algae exhibited
that of species diversity (H') with the highest values
faster growth due to better light conditions which
recorded during the last period (May/2001), when it rose
favoured higher productivity. For instance, in July/2000,
from 50 to 74 species. Such an increase was mainly attrib-
214
Georgios Manoudis, Chryssanthi Antoniadou, Konstantinos Dounas and Chariton Ch. Chintiroglou
uted to Errantia (Polychaeta) and Gastropods, which were
composition of the substrate, the season the material was
represented more frequently at this period.
deposit and on environmental variables including water
The results of cluster analysis and MDS are shown in
temperature, chemistry and current patterns (BOHNSACK
figure 3. Cluster analysis indicated two main groups at the
& SUTHERLAND, 1985). This study reveals that sufficient
49.5% similarity level. The first one consisted of all repli-
amount of nutrients is very important for the development
cates of the last sampling period (May/2001), due to high
of the colonization, as they favour the faster completion
total species richness, while the other one comprised the
of the colonization process. The high abundance of the
remaining ones. The second group included four main
individuals recorded in this study (about 20.000 ind. / m2
subgroups of clusters at about 60% similarity level, each
in the last period), are not consistent with the results
corresponding to all replicates of the four periods. The
reported by ANTONIADOU et al. (2001, and, also, from
results of ANOSIM (R=0.948, p<0.01) indicate discrimi-
unpublished data), in a similar study that was conducted
nation between the groups of samples, so the cluster is
in the oligotrophic system of Chalkidiki (N. Aegean Sea).
confirmed. The results of MDS agreed with those of clus-
While the dominant taxon in Chalkidiki was Mollusca
ter analysis. The stress value for the two dimensional
(herbivore grazers), it is the filter-feeders that prevail in
MDS configuration was 0.09 indicating very good group
Cape Fanari (Peracarida, Serpulidae). These facts imply
separation (C
that the feeding types of the colonizing fauna depend
LARKE & WARWICK, 1994).
mainly on the available food supply in the area where the
(a)
reefs are deployed. Apparently, as Carter et al. (1985)
noted, the best areas for reef deployment, in order to
40
achieve the optimum growth of the fishing stock, are
rity
those that favour a fast qualitative and quantitative colo-
60
nization growth.
-
Curtis Simila
80
y
REFERENCES
Bra
100 E2 E6 E4 E5 E7 E8 E1 E3 A2 A3 A1 A6 A5 A7 A4 A8 D1 D2 D6 D4 D8 D3 D5 D7 B7 B5 B8 B3 B2 B1 B4 B6 C5 C8 C3 C1 C2 C6 C4 C7
ANTONIADOU, C & C. CHINTIROGLOU, (2001). Colonization pat-
tern of the infralittoral hard substrate community in the
North Aegean Sea (Chalkidiki, Greece). Preliminary results.
(b)
Rapp. Comm.int. Mer Médit., 36 : 351
ARDIZZONE, G.D. & G. BOMBACE, (1983). Artificial experiments
along Tyrrenian coasts. Journee Etud. Recif Artif. et Mari-
culture, Cannes, CIESM : 49-51.
BAKUS, G.J. (1990). Quantitative ecology and marine biology.
A.A. Balkema, Rotterdam.
BARNARD, L. (1958). Amphipod crustaceans as fouling organ-
isms in Los Angeles-long beach harbors, with reference to
the influence of seawater turbidity. California Fish and
Game, Conservation of wildlife through education, 44 (2) :
161-169.
BELLAN-SANTINI, D., J.C. LACAZE & C. POIZAT (1994). Les
biocénoses marines et littorales de Méditerranée, synthèse,
menaces et prespectives. In : Secretariat de la faune et de la
flore. Collection Partimoines Naturels n.19. Serie Partimoine
ecologique. Paris : 246.
BOMBACE, G. (1977). Aspetti teorici e sperimentali concernenti
le barrire artificiali. Atti IX Congresso SIMB, Lacco Ameno :
29-41.
BOMBACE, G.(1980). Experiments on artificial reefs in Italy.
Fig. 3. Results of (a) cluster and (b) multidimensional scaling
GFCM/XV/80/21 : 11.
(stress value=0.09) based on Bray-Curtis similarity index, of the
BOMBACE, G., G. FABI, L. FIORENTINI & S. SPERANZA (1994).
cement blocks immersed in autumn 1999 (A1-A8 : March 2000,
Analysis of the efficacy of the artificials reefs located in five
B1-B8 : May 2000, C1-C8 : July 2000, D1-D8 : December
different areas of the Adriatic Sea. Bull. Mar. Science, 55 (2-
2000, E1-E8 : May 2001).
3) : 559-580.
BOHNSACK J. & D. SUTHERLAND (1985). Artificial reef research :
As mentioned in the introduction, the studies that refer
A review with recommendations for future priorities. Bull.
to the colonization of artificial reefs are very few in
Mar. Sci., 37(1) : 11- 39.
number. However, Fager (1971) noted that algae and
BOUGIS, P. (1976). Océanographie biologique appliquée,
invertebrates usually colonize new reef materials rapidly,
l'exploitation de la vie marine. MASSON : 320.
although attaining an equilibrium community structure
CARTER, J.W., A.L. CARPENTER, M.S. FOSTER & W.N. JESSEE
(1985). Benthic succession on an artificial reef designed to
can take several years. A review of the relevant bibliogra-
support a Kelp-reef community. Bull. Mar. Sci., 37 : 86-113.
phy revealed that filter-feeders appeared to be the prevail-
CLARKE, K.R. & R.H. GREEN (1988). Statistical design and anal-
ing organisms in artificial reefs communities (BOMBACE
ysis for a `biological effects' study. Mar. Eco. Prog. Ser., 46 :
et al., 1994 ; RELINI et al., 1990). However, initial coloni-
213-226.
zation, successional patterns and the final composition
CLARKE, K.R. & R.M. WARWICK (1994). Change in marine
and abundance of benthic organisms can depend on the
communities : an approach to statistical analysis and inter-
Successional stages of experimental artificial reefs deployed in Vistonikos gulf
215
pretation. In : Natural Environment Research Council, UK :
Investigating the potential. Mar. Pol. Bul., 37 (8-12) : 505-
144.
514.
FAGER E.W. (1971). Pattern in the development of a marine com-
RELINI, G. (1974). Collonizzazione del substrati duri in mare.
munity. Linol. Oceanogr. 16 : 241- 253.
Mem. Biol. Mar. Oceanogr., 6 : 201-261.
FITZHARDINGE, R.C. & J.H. BAILEY-BROCK (1989). Colonization
RELINI, G. & L. RELINI(1989). Artificial reefs in the Ligurian
of artificial reef materials by corals and other sessile organ-
Sea. FAO Fisheries Report 428 : 114-119.
isms. Bulletin of Marine Science, 44 (2) : 567-579.
H
RELINI, G., N. ZAMPONI & F. SOMMEZER(1990). Development of
ONG, J.S. (1983). Impact of the pollution on the benthic com-
munity. Bulletin of the Korean Fisheries Society, vol.16,
sessile macrobenthos community in the Loano artificial reef.
No 3.
Rapp. Com. Int. Mer. Medit., 32 (1) : 24-27.
KLUIJVER, M.J.(1997). Sublittoral communities of North Sea
SANTOS, M. & C. MONTEIRO (1998). Comparison of the catch
hard-substrata. Print Partners Ipskamp, Enschede, S.B.N.O.,
and fishing yield from an artificial reef system and neigh-
AquaSence, Amsterdam : 330.
bouring areas off Faro (Algarve, S. Portugal). Fish.
ODUM, P.E. (1993). Ecology and our endangered life-support
Research, 39 : 55-65.
systems. Sinaur Associates, Inc., North Main Street Sunder-
SINIS, A., CH. CHINTIROGLOU & K STERGIOU (2000). Preliminary
land, Massachusetts 1375, USA : 301.
results from the establishment of experimental artificial reefs
PICKERING, H., D. WHITMARSH & A. JENSEN (1998). Artificial
in the North Aegean Sea (Chalkidiki, Greece). Belg. J. Zool.,
reefs as a tool to aid rehabilitation of coastal ecosystems :
130 (1) : 143-147.
Belg. J. Zool., 135 (2) : 217-221
July 2005
Movements, activity patterns and home range of a
female brown bear (Ursus arctos, L.) in the Rodopi
Mountain Range, Greece
Yorgos Mertzanis1, Isaak Ioannis1, Avraam Mavridis2, Olga Nikolaou3, Suzanne Riegler1,
Armin Riegler1 and Athanasios Tragos1
1 "CALLISTO" NGO, 5, Nik Foka street, GR54625 Thessaloniki, Greece
2 Aristotle University of Thessaloniki, School of Engineering, Laborantory of Geodesy, GR54625 Thessaloniki, Greece
3 The University of Reading, School of Animal and Microbial Sciences, Whiteknights, PO Box 228, Reading, RG6 6AJ, UK.
Corresponding author : Y. Mertzanis, e-mail : ymertz@otenet.gr
ABSTRACT. Movements and activity patterns of an adult radio-tagged female brown bear accompanied by her
cubs were documented for the first time in Rodopi area (NE Greece) from August 2000 to July 2002. Average daily
movements were 2.45 ±2.26 SD km, (range 0.15-8.5 km). The longest daily range could be related to human distur-
bance (hunting activity).The longest seasonal distance (211 km), during summer 2001 coincided with the dissolu-
tion of the family. With cubs, the female was more active during daytime (73% of all radio-readings) than when sol-
itary (28%). The female switched to a more crepuscular behaviour, after separation from the yearling (July 2001).
According to pooled data from 924 activity - recording sessions, during the whole monitoring period, the female
was almost twice as active during day time while rearing cubs (51% active) than when solitary (23%). The autumn
and early winter home range size of the family was larger (280 km2) than after the separation from the cubs
(59 km2). During the family group phase, home range size varied from 258 km2 in autumn to 40 km2 in winter
(average denning period lasted 107 days : December 2000-March 2001). The bear hibernated in the Bulgarian part
of the Rodopi Range during winters of 2001 and 2002.
KEY WORDS : Ursus arctos, brown bear, movements, activity patterns, home range, Rodopi, Greece.
INTRODUCTION
ging of an adult female bear with her cubs occurred in
summer (August) 2000.
The brown bear (Ursus arctos, L.) distributional range
This study was carried out from August 2000 to July
in Greece comprises two distinct nuclei located in the
2002 within the framework of a "LIFE-Nature" project
Pindos Mountain Range (NW Greece) and the Rodopi
for the Conservation of the brown bear in Greece. The
Mountain Complex (NE Greece). The total area of con-
fragile status of brown bears in Europe and especially in
tinuous bear range comprises 8,600 sq.km, while re-col-
the southern parts of the continent, as well as the lack of
onization of former range appears in southern Pindos
data on the ecology and behaviour of the animals in
Mountains (Fig. 1). The minimum population has been
Greece, incited us to undertake this study. The present
estimated at 130-160 individuals (MERTZANIS, 1999).
paper aims to document for the first time movements and
The minimum brown bear sub-population in Rodopi
activity patterns of a radio-tagged adult female brown
area is estimated up to 25-30 individuals (MERTZANIS,
bear accompanied by her cubs in the Rodopi area. This
1999), which is 19% of the total bear population in
and similar results will contribute to the adjustment and
Greece. This sub-population is connected only with the
orientation of conservation measures for the species.
southern Bulgarian bear sub-population (Bulgarian
Rodopi).
MATERIAL AND METHODS
The brown bear is a fully protected species in Greece
under national and EU legislation. Since 1994 and until
Study Area
2003 systematic monitoring programs for brown bear
conservation purposes in Greece are conducted on a con-
The study area is located in NE Greece and comprises
tinuous basis by the NGO "Arcturos" in cooperation with
the medium and higher altitudes of the western and cen-
the national competent authorities. Telemetry techniques
tral Rodopi Mountain Complex (Fig. 1). The Mountain
to study bear behaviour and ecology were implemented
Complex is located between 41° 12' and 41° 36' N and
for the first time in 1997. Until then monitoring data came
24° and 25° 06' E. The total surface is about 1,731 sq km.
from observation and compilation of bear activity signs.
It is a vast granitic complex covered with large forests
In Rodopi area, the first successful capture and radio-tag-
and located in the drainage of the Nestos River valley.
-118_1.jpg)
218
Yorgos Mertzanis et al.
Fig. 1. Location of the study area and brown bear range in Greece.
Continuous forest covers about 68% of the study area.
two cubs of the year was captured with an `Aldrich Foot
Main forest types and percentage of coverage are : oak
Snare' trap on 4 August 2000 (at 20:30) after 64 trapping
(Quercus sp.) (60%) at lower altitudes, beech (Fagus sp.)
nights. The bait used was an active beehive. The bear was
(20%), Spruce (Picea excelsa) (15%), Scots pine (Pinus
sedated with KHCl/xylazine (Rompun) (initial volume
sylvestris) (17.5%) and black pine (Pinus nigra) (3%).
750mg/3ml injected with blowpipe) and a booster volume
The terrain is generally rugged and is characterized by
of 750mg/3ml (with intra-muscular injection). Time to
perennial, cold water streams and rivers. Elevations range
anaesthesia was less than 5 minutes. Total immobilization
from 500-2,232 m above sea level. Mean annual tempera-
time was approx. 30min. The bear was fitted with a radio-
tures range from 27.1° C in summer to -4.7° C in winter.
collar (`Telonics MOD-500 NH') with bi-modal "activity-
Mean annual precipitation is 980 mm. Nearly all native
inactivity" signal. The antagonist used was "Yohimbine"
European mammal species are present in the area, includ-
(25 mg /ml). Radiolocations were taken on a daily basis
ing the wolf (Canis lupus), roe deer (Capreolus capreo-
using a TR-4 "Telonics" receiver, with a minimum of
lus), chamois (Rupicapra rupicapra), wild cat (Felis syl-
three bearings using the "raised antenna - null signal"
vestris) and otter (Lutra lutra). The study area is remote,
(RA NS) technique.
characterized by low human density and scattered human
settlements. Abandoned villages have increased the diver-
Data Processing and plotting was achieved using
sity of bear food because of abundant orchards. A high
`LOCATE' and GIS (ArcInfo, ArcView) software. Daily
density of forest road network related to timber activities
movements were calculated from consecutive day to day
reaches almost 15m/ha, and gives access to a relatively
radiolocations, using ArcView program extension "Ani-
high level of hunting pressure. Hunting is allowed from
mal Movement Analysis" (Kenward, 2001). Geographic
August to January. Game reserves cover 6.16% of the
coordinates of the bearing points were obtained by GPS
core part of the study area.
and were processed through LOCATE software for trian-
gulation. Subsequently, the exported co-ordinates were
Study Animals and Methods
used in several functions (as well as by the standard
An adult female brown bear, aged 8-10 years [age esti-
ArcView functions). The line coverage that was used was
mated in situ from dentition characteristics (JONKEL,
optimised with the "point to polyline" tool in the pro-
1993)], weighing approx. 120 kg and accompanied by
gram.
Brown Bears in Rodopi, Greece
219
Two approaches were used to evaluate activity levels.
Whitney U-Test, p<0.05,). This pattern was confirmed by
The first approach consisted of recording the activity sta-
comparing the overall activity frequencies (924 bearings)
tus at each daily bearing and radio-location. In this case
between day (from 07:00 to 19:00) and night (from 19:00
activity levels were examined over the whole dataset,
to 07:00) hours (Fig. 3). The activity of the female during
which was separated into two different groups : the day-
daylight fell from 52.1% while with her cubs, to 23.1%
light hours, that is from 07:00-19:00, and the night hours,
after having separated from her cubs in July 2001. On
19:00-07:00. The second approach was achieved through
12 July 2001 a short visual contact with the bear family
24h monitoring sessions operated once every month. The
confirmed the presence of one cub.
bear's activity was recorded every half hour for 3-5 min
of continuous listening. Activity status was deduced by
measuring the time of the active and inactive signal
Frequency of daily activity pattern of adult female brown bear with cub
within the Rodopi study area between 4/8/00-30/06/01 in
modes. Mann-Whitney U Tests were used for statistical
relation to the photoperiod(n=589, total bearings)
comparisons of results. Home Range estimation was
80,0
75,0
based on the `Minimum Convex Polygon' (MCP) method
70,0
Active %
(MOHR 1947, HAYNE 1949).
60,0
52,1
49,2
50,0
equency
Inactive %
RESULTS
40,0
Activity fr
30,0
25,0
Between August 2000 and December 2001, daily
20,0
movements of the bear family were defined with
10,0
924 bearings, which yielded 365 radiolocations that were
0,0
plotted, averaging one location /1.3 days. Average
07:00-18:59 day
19:00-06:59 night
straight-line distance between successive daily radioloca-
tions of the bear averaged 2.45 km (± 2.26 SD). Of all
daily movements 65% were less than 2.45 km. The short-
Frequency of daily activity pattern of adult female brown bear without
cub within the Rodopi study area between 01/07/01-05/12/01 in relation
est distance was 0.15 km whereas the longest daily dis-
to the photoperiod(n=335 total bearings).
tance was 8.5 km and occurred in early autumn (Septem-
100
87,5
ber) 2000. In both autumn 2000 and 2001 (mid September
90
to end of November) daily distances travelled in week-
80
76,9
Active
ends were significantly higher than those travelled during
70
%
weekdays (Mann-Whitney U-Test : autumn 2000 :
60
p<0.05 ; autumn 2001 : p<0.05,).
50
Inactive
%
40
30
23,1
Total distance (km) travelled seasonally by an adult female brown bear
20
%
12,5
in Rodopi Mountains, Greece
10
(Aug 2000-Dec 2001) (n=365 radiolocations).
0
07:00-18:59
19:00-06:59
family
dissolution
Fig. 3. Female brown bear activity patterns with and without
cubs in the Rodopi Mountains, Greece, as shown by daily loca-
tions (n=924).
Diel activity of the female during the two periods with
and without cub(s), was also recorded. While with her
cub(s) the female showed more continuous periods of
activity throughout the day, and especially during day-
time. In this case the 24h cycle was interrupted by rela-
tively short intervals of inactivity (Fig. 4). After separa-
Fig. 2. Seasonal mouvements of the brown bear family inthe
tion from her cub(s) the 24h activity pattern became much
Rodopi Mountains, from August 2000 to December 2001.
longer with clearly continuous intervals of inactivity dur-
For the same monitoring period and at a seasonal scale,
ing the day, from 10:00 to 17:00, and clear bouts of activ-
total seasonal movements of the bear family and the lone
ity during the night, between 19:00 and 03:00 (Fig. 4).
female showed also characteristic variations (Fig. 2). The
Winter inactivity of the female bear during two den-
highest values were obtained in three periods : mid June to
ning periods averaged 107 days and concerned the same
mid September 2001, time of the family dissolution,
denning site that was used repeatedly for two consecutive
autumn 2000, bear with cubs, and mid September to end of
winters (2000 and 2001). The site was located on Bulgar-
November 2001, when the bear was solitary without year-
ian territory in the Rodopi Mountain Range, in a small
ling with 211, 178.8 and 130.2 km travelled respectively.
and steep canyon covered by spruce (Picea excelsa) for-
Another shift in the female bear's activity pattern
est. This small valley had a northern exposure and was
occurred after separation from her cub(s). The female
characterized by harsh winter conditions. The den was
bear was significantly more active during the daylight
dug under a rock, and the entrance was camouflaged with
hours when the family group was still together (Mann-
spruce branches.
-120_1.jpg)
220
Yorgos Mertzanis et al.
.
her cub(s). The most marked difference occurred from
mid September to end of November declining from
349 sq. km in 2000 (female with cubs) to 107.5 sq. km in
2001 (solitary female). This can be associated with the
overall decrease of the home range area, which was
280 sq km in mid September to mid December 2000
when the family was intact, to 59 sq km at the same
period in 2001 when the female was solitary (Fig. 5). In
addition the smallest home range area was recorded dur-
ing the winter, from mid December to early March and
measured 40 sq km, at the pre-denning period. In contrast,
the largest home range area was recorded during the
period from mid September to end of November, and
measured 280 sq km, when the family group was
together. In general, seasonal variations of home range
area appeared to follow and correspond to the seasonal
variations of movements.
Fig. 5. Female brown bear home range areas in autumn 2000
(with cubs) and autumn 2001 (without cubs).
DISCUSSION
In terms of daily movements, the female bear covered
distances more or less similar to bears in other European
countries, such as those for male and female bears in
Croatia (HUBER & ROTH, 1986 ; 1993) and for a male bear
in Spain (CLEVENGER et al., 1990). On the other hand, the
significant differences of the bear family's daily move-
ments in autumn 2000 and notably during weekends
could be related to the high hunting pressure occurring in
the study area in weekends. Many hunters were present
during the weekends, they were organized into groups,
used base camps within the forest as headquarters and
conducted drive-hunts as the main hunting practice for
wild boars (Sus scrofa). This was a major factor of distur-
bance probably causing the bear family to move continu-
ously to avoid humans. Drive-hunts have been also identi-
fied as a serious human caused mortality factor for bears
in the study area (MERTZANIS, 1994).
Field observations, corroborating telemetry data, con-
Fig. 4. Female brown bear diel activity patterns with and
firmed that displacement of the bear family from undis-
without cubs as shown by 24h monitoring sessions in autumn
turbed sectors (with continuous presence and activity dur-
2000 and summer 2001.
ing the week), coincided with hunting activity occurring
Data on home range area also showed notable variation
in the same sectors during the weekends. Similar avoid-
most likely related to the separation of the female from
ance movements in response to human activities, such as
Brown Bears in Rodopi, Greece
221
recreation, have also been recorded for a bear family in
ACKNOWLEDGMENTS
the Cantabrian Mountains in Spain (NAVES et al., 2001).
On the other hand, the long distances travelled by the
This work was accomplished in the frame of the LIFE-Nature
Project (LIFE99NAT/GR/6498) co-financed by the E.U., the
family (176.8 km) as well as the high home range values
Hellenic competent authorities (Ministry of Agriculture-Game
(255.08 sq km) in autumn 2000 might further be related to
Division and Ministry of Environment, Planning & Public
educational processes of the female towards the cub(s).
Works) and ARCTUROS NGO. We thank the field-team for its
This process includes learning of locations with available
tenacious and efficient work as well as the Forest Services of the
and suitable food resources, safe shelter as well as avoid-
Prefecture of Drama for their help and support.
ance of human disturbance. In contrast, the relatively long
distances (130.2 km) travelled by the solitary female in
REFERENCES
autumn 2001, within a comparatively smaller home range
(57.6 sq km), could be related to avoidance behaviour of
CLEVENGER, A., F. PURROY, M. PELTON (1990). Movement and
the mother towards her yearling(s). This happened after
activity patterns of a European brown bear in the Cantabrian
the dissolution of the family, which is assumed to have
mountains, Spain. Proceedings Int. Conf. Bear Res. & Mgmt.
occurred in late July 2001.
8 : 205-211.
As far as dial activity is concerned, the patterns found
HAYNE, D.W. (1949). Calculation of home range. J. Mammal.
30(1) : 1-18.
in Rodopi are very similar to the ones observed for five
HUBER D. & H.V. ROTH (1986). Home ranges and movements of
males and one female adult bear in Pindos Mountain
brown bears in Plitvice National Park, Yugoslavia. Proceed-
Range, Greece (MERTZANIS et al., 2003), as well as for
ings Int. Conf. Bear Res. & Mgmt. 6 : 93-98.
solitary bears in Italy (ROTH, 1983), Croatia (ROTH &
HUBER, D. & H.V. ROTH (1993). Movements of European brown
HUBER, 1986) and Spain (CLEVENGER et al., 1990). On the
bears in Croatia. Acta Theriol. 38(2) :151-159.
other hand, the differences in diel patterns observed
JONKEL J. (1993). A manual for handling bears for managers and
between the solitary and family phases of the same
researchers. T.J.Thier ed.175 pp.
female bear and more particularly, the increased level of
KENWARD, R. (2001). A Manual for Wildlife Radio Tagging.
activity during daylight hours for the bear accompanied
Academic Press, New York, USA. 307 pp.
by the yearling(s) could be associated with an increased
MERTZANIS, G. (1994). Brown bear in Greece : distribution,
present status, ecology of a northern Pindus sub-population.
nutritional need due to lactation, the education of the
Proceedings Int. Conf. Bear Res. & Mgmt. 9 : 187-197.
yearling and its familiarisation with the surrounding habi-
MERTZANIS, G. (1999). Supporting monitoring of key indices
tat, as well as with the avoidance of infanticidal males
related to bear populations status and feedback : Monitoring
that kill cubs (SWENSON et al., 2001).
of bear population levels and trends. in : Project
Lastly, results concerning the home range areas of soli-
LIFE96NAT/GR/003222, Final Report.& Final Report
tary females are very similar to those recorded for solitary
Annex 7, NGO Arcturos ed., Thessaloniki 1999, Pp. 47-48
& 85-87 (unpublished report.).
animals in Croatia (HUBER & ROTH, 1993). Larger home
MERTZANIS, G. et al. (2003). Monitoring of brown bear using
ranges for the family could be related to greater nutri-
telemetry in Gramos and Rodopi Mountains, Greece. Project
tional needs not only of the female but also for the cubs in
LIFE99NAT/GR/006498, Final Report Annex.NGO Arc-
search for suitable and patchy food sources.
turos ed., Thessaloniki 2003, 54 pp + Annexes & maps.
The combination of the results of the present study
(unpublished report, in Greek).
M
with previous systematic surveys enhances considerably
OHR, C.O. (1947). Table of equivalent populations of North
American small mammals. Am. Midl. Nat. 37 : 223-249.
the proposed delineation of important bear habitat units in
NAVES, J., A. FERNADEZ-GIL, M. DELIBES (2001). Effects of rec-
the study area. These results have been incorporated in
reation activities on a brown bear family group in
the final zoning proposals for the creation of a National
Spain.Ursus.12 : 135-140.
Park in the Rodopi area, as processed by "Arcturos" NGO
ROTH, H.V. (1983). Home ranges and movement patterns of
and in cooperation with national competent authorities,
European brown bears as revealed by radiotracking. Acta
under the National Environment Law 1650/86. In addi-
Zool. Fenica 174 :143-144.
tion, the above results confirmed the ecological impor-
ROTH, H.V. (1983). Diel activity of a remnant population of
tance of the "NATURA" 2000 (pSCI) site "Elatia"
European brown bears. Proceedings Int. Conf. Bear Res. &
(GR1140003) located in the study area. Moreover, we
Mgmt. 5 : 223-229.
hope that similar results will also contribute in the reor-
ROTH, H.U. & D. HUBER (1986). Diel activity of brown bears in
Plitvice Lakes National Park, Yugoslavia. Proceedings Int.
ganisation of warden patrols during the hunting season in
Conf. Bear Res. & Mgmt. 6 : 177-181.
order to minimize disturbance related to hunting pressure,
SWENSON, J., F. SANDEGREN, S. BRUNBERG, & P. SEGERSTROM
and a co-ordination of management actions engaged on a
(2001). Factors associated with loss of brown bear cubs in
trans-border scale.
Sweden. Ursus 12 : 69-80.
Belg. J. Zool., 135 (2) : 223-227
July 2005
Dry Weights of the Zooplankton of Lake Mikri Prespa
(Macedonia, Greece)
Evangelia Michaloudi
Aristotle University, School of Biology, Laboratory of Ichthyology, Box 134, Gr-54124 Thessaloniki, Greece
Corresponding author : E. Michaloudi, e-mail : tholi@bio.auth.gr
ABSTRACT. Length-weight regressions and dry weight estimates of the main crustaceans of Lake Mikri Prespa are
presented. The calanoid copepod and most of the cladocerans were heavier during summer than in other seasons,
while the rest of the crustaceans were heavier during spring. The mean calculated dry weights were : (a) 0.005 µg
(Keratella cochlearis), 2.268 µg (Asplanchna priodonta), 0.033 µg (Trichocerca capucina), 0.024 µg (Filinia long-
iseta) for the predominant rotifer species ; and (b) 0.420 µg for the planktonic larvae of the molluscan Dreissena
polymorpha.
KEY WORDS : Dry weights, length-weight regressions, zooplankton, Greece
INTRODUCTION
for the copepodites of the calanoid Arctodiaptomus stein-
dachneri. The above procedure was done for each season
Dry weight data exist for several areas mainly in
separately except for the groups of very low density (e.g.
Europe and America (e.g. NAUWERK 1963 ; DUMONT et
Daphnia cucullata of IV size class), for which individuals
al., 1975; SCHINDLER & NOVEN 1971, LAWRENCE et al.,
were sorted out from all the samples throughout the year.
1987; MALLEY et al., 1989), while the length-weight rela-
Length-weight regressions were performed using the lin-
tionships of freshwater zooplankton species from the
ear form ln(W)=lna+bln(L), where L is body length in
same areas are reviewed by BOTTRELL et al. (1976) and
mm and W is body weight in µg dry weight.
McCAULEY (1984). Nevertheless, no data are available for
For rotifers, the wet weight was calculated using the
the Balkan lakes, including for the calanoid copepod Arc-
geometric formulae of RUTTNER-KOLISKO (1977), applied
todiaptomus steindachneri, an endemic species of the
on live individuals. Wet weight was consequently trans-
Western Balkan. On the other hand, many factors have
formed to dry weight assuming that dry weight is 10% of
been found to control the individual weight underlining
wet weight except for Asplanchna for which it was
the necessity to develop length-weight relationships spe-
assumed to be 4% (DUMONT et al., 1975). The same
cific to an area (RAHKOLA et al., 1998). Thus, the data pre-
method was applied for the dry weight calculation of the
sented herein will allow the estimation of the zooplank-
planktonic larvae of Dreissena polymorpha using the
tonic biomass and production of the lakes in the
10% factor to convert wet to dry weight (M. VRANOVSKY,
surrounding area.
pers. comm.). The biovolume estimates for Dreissena
were based on the formula of the ellipsoid of revolution
MATERIAL AND METHODS
(RUTTNER-KOLISKO, 1977).
Samples were collected monthly from June 1990 to
RESULTS
October 1992 from Lake Mikri Prespa. A detailed
description of the lake, the phytoplankton and zooplank-
Weight data for the crustacean populations of Lake
ton communities as well as the sampling procedure has
Mikri Prespa are shown in Table 1. The main filter feed-
been presented by TRYPHON et al. (1994) and MICHALOUDI
ers Daphnia cucullata, Diaphanosoma cf. mongolianum,
et al. (1997).
Ceriodaphnia pulchella and Arctodiaptomus stein-
Crustacean samples were preserved immediately in 4%
dachneri were heavier during summer than in other sea-
formalin. Individuals were sorted from the samples and
sons. Bosmina longirostris, Mesocyclops leuckarti and
grouped according to species, sex, developmental stage
the calanoid copepodites were heavier during spring,
(copepodites, nauplii), and size class (see Table 1) in the
while nauplii were heavier in the winter.
laboratory. Each group comprised 30-100 individuals.
The length-weight regressions are shown in Table 2.
The individual length was measured (to the nearest 0.01
The slopes of the length-weight regressions were all sig-
mm) and the animals were rinsed with distilled water,
nificantly (p<0.01) different from zero and ranged from
placed on pre-weighed and pre-dried (60° C for 48 h) alu-
1.9 to 3.5.
minium boats, dried at 60° C for 48 h, cooled in a desicca-
tor and weighed on a microbalance (10 µg precision).
For rotifers and the molluscan larvae of Dreissena pol-
Ovigerous females were not selected. The developmental
ymorpha the dimensions (mean values) and calculated
stages of copepods were not separated by species except
dry weights for each species are shown in Table 3.
224
Evangelia Michaloudi
TABLE 1
(MICHALOUDI et al., 1997) when their main food source is
probably bacteria (GLIWICZ, 1969 ; SOMMER et al., 1986).
Dry weights (in µg) of the crustacean species of Lake Mikri Pre-
At the same period they were also heavier (Table 1). This
spa. W=winter, Sp=spring, SU=summer, A=autumn. *Data
could be the result of the increased food availability as
refer to groups for which the number of individuals was not
well as the increase of temperature that has a positive
enough for seasonal weight determination, and which were
effect on their filtering rate (BURNS, 1969 ; MOURELATOS
sorted out from all samples throughout the year.
& LACROIX, 1990). Such a coincidence of maximum
Species
weight and abundance is also reported by VUILLE & MAU-
W
SP
SU
A
all*
size class (µm)
RER (1991). On the other hand, Bosmina longirostris was
Daphnia cucullata Sars, 1862
heavier during spring although it reaches maximum abun-
300-500
0.47
0.4
0.4
0.408
dance during autumn (MICHALOUDI et al., 1997). At this
501-700
0.606
0.909
2.75
1.886
time the phytoplankton community is dominated by
701-900
2.5
2.258
3.125
2.058
Cyanobacteria while during spring nanoplankton biomass
901-1100
4.8
is at its peak (TRYPHON et al., 1994). Moreover, it has
Diaphanosoma cf. mongolianum Ueno, 1938
been found that although temperature has no considerable
300-500
0.5
0.425
501-700
0.82
0.43
effect on its filtration rates (BOGDAN & GILBERT, 1982 ;
701-900
2
1.38
MOURELATOS & LACROIX, 1990), high concentration of
901-1100
2.727
inedible particles has a distinct negative effect (BOGDAN
males
0.57
& GILBERT, 1982).
Bosmina longirostris (O.F. Müller, 1758)
200-300
0.29
0.48
0.224
TABLE 2
301-400
0.78
1
0.886
401-500
1.14
1.54
Length-dry weight relationships of the planktonic crustaceans
Ceriodaphnia pulchella Sars, 1862
(all size classes included) in Lake Mikri Prespa
200-300
0.309
0.156
ln(W)=lna+bln(L), R2=coefficient of determination, p=probabil-
301-400
0.64
0.454
ity of b being different from zero, S.E.=standard error of b. L in
401-500
0.816
0.816
13.33
mm and W in µg.
Leptodora kindtii (Focke, 1844)
Arctodiaptomus steindachneri (Richard, 1897)
Species
N
R2
p
S.E.
females
5
6
6.845
3.47
D. cucullata 13
Ln(W)=1.586+2.963Ln(L)
0.797
0.0001
0.451
males
3
4
3.66
2.325
copepodites
B. longirostris 8
Ln(W)=3.203+3.466Ln(L)
0.909
0.0002
0.448
300-500
0.45
0.92
0.8
0.416
501-700
1.304
1
1.13
0.8
C. pulchella 6
Ln(W)=1.807+2.517Ln(L)
0.836
0.0107
0.557
701-900
1.67
3.45
2
1
901-1100
3.6
5.2
2.67
1.79
D. cf. mongo-
7
Ln(W)=1.046+2.501Ln(L)
0.857
0.0028
0.458
lianum
Mesocyclops leuckarti (Claus, 1857)
females
4.117
1.38
2
A. steindachneri (1) 24
Ln(W)=1.111+2.121Ln(L)
0.796
0.0001
0.229
males
1.034
1.33
1
copepodites
11
Ln(W)=1.535+3.532Ln(L)
0.908
0.0001
0.376
Cyclops vicinus Ulianine, 1875
cyclopoida
females
21.67
25.315
Cyclopoida (1)
25
Ln(W)=1.205+2.685Ln(L)
0.902
0.0001
0.185
males
10
9
Macrocyclops albidus (Jurine, 1820)
nauplii
9
Ln(W)=1.777+1.914Ln(L)
0.715
0.0041
0.457
females
20
1.Pooled data for adults and copepodites
males
5
Eucyclops serrulatus (Fischer, 1851)
females
7.5
The weights of Bosmina longirostris, Mesocyclops
males
6.25
leuckarti, Cyclops vicinus and Diaphanosoma cf. mongo-
cyclopoid copepodites
lianum (Table 1) are in good agreement with those
300-500
0.4
0.2
0.196
reported by BURGIS (1974) ; DUMONT et al. (1975) ;
501-700
1.76
0.87
0.46
0.884
701-900
1.272
2.33
2.72
GOPHEN (1976) ; LAWRENCE et al. (1987) and VUILLE &
901-1100
4.29
MAURER (1991) for individuals of the same length. On the
nauplii
other hand Ceriodaphnia pulchella is much lighter than
200-300
0.303
0.202
0.235
0.119
C. quandrangula (DUMONT et al., 1975) probably because
301-400
0.58
0.5
0.303
0.303
the first one is a pelagic and the second one a littoral spe-
401-500
1.35
cies (VUILLE & MAURER, 1991). As for the non pelagic
Eucyclops serrulatus and Macrocyclops albidus, they
DISCUSSION
were found to be lighter though bigger than the individu-
als reported by DUMONT et al. (1975). Considering the
altitude of Mikri Prespa (850 m asl) it is evident that the
The filter feeders Daphnia cucullata, Diaphanosoma
assumption of DUMONT et al. (1975), that non-pelagic
cf. mongolianum, Ceriodaphnia pulchella and Arctodiap-
species tend to be lighter at high altitudes, is true for the
tomus steindachneri are the main components of the
above species.
spring and summer crustacean community (MICHALOUDI
et al., 1997). They increase in numbers after the nano-
From the above it can be concluded that crustacean
plankton peak and dominate throughout summer
weight is controlled by geographical distribution, differ-
Zooplankton of Lake Mikri Prespa
225
TABLE 3
Mean dimensions (in µm) and calculated dry weight (in µg) of the rotifers and D. polymorpha in Lake Mikri
Prespa, n=number of individuals, S.E.=standard error.
a=lenght
b=height
c=width
w=weight
Species
n
Mean
S.E.
Mean
S.E.
Mean
S.E.
Mean
S.E.
Asplanchna priodonta Gosse, 1850
145
653.55
16.06
397.50
13.12
2.268
0.1000
Brachionus angularis Gosse, 1850 (1)
30
102.08
0.81
92.29
1.11
52.29
1.18
0.026
0.0010
B. diversicornis (Daday, 1883)
99
262.50
6.18
157.19
5.39
85.13
5.01
0.188
0.0210
B. forficula Wierzejski, 1891
30
87.50
1.09
78.00
1.71
49.50
1.06
0.018
0.0010
Conochilus hippocrepis (Schrank, 1830)
30
301.50
9.08
72.50
1.74
0.043
0.0030
Filinia longiseta (Ehrenberg, 1834)
46
39.75
25.25
54.58
6.83
0.024
0.0100
Keratella cochlearis (Gosse, 1851)
359
118.46
3.53
55.02
1.07
0.005
0.0003
Polyarthra sp.
60
142.75
0.25
95.00
5.00
65.63
1.13
0.090
0.0300
Synchaeta pectinata Ehrenberg, 1832
60
294.75
6.25
205.50
1.50
0.343
0.0200
Trichocerca capucina Wierzejski & Zacharias, 1893
4
202.50
4.33
56.25
2.17
0.033
0.0020
T. cylindrica (Imhof, 1891)
33
284.88
5.13
64.38
4.38
0.012
0.0020
T. similis (Wierzejski, 1893)
142
148.39
3.71
46.55
1.74
0.017
0.0020
Dreissena polymorpha (Pallas, 1771)
240
185.88
6.47
206.88
8.28
0.420
0.0400
1. Measures on preserved specimens
ent habitat types, temperature and food availability and
REFERENCES
composition. Moreover, the trophic status of a lake may
have an impact on the seasonal variations of the weights.
ANDREW, T.E. & A.G. FITZISIMONS (1992). Seasonality, popula-
This could be seen when comparing the results of the
tion dynamics and production of planktonic rotifers in
present study, where most crustaceans were heavier dur-
Lough Neagh, Northern Ireland. Hydrobiologia, 246 : 147-
ing summer, with the results from HAWKINS & EVANS
164.
(1979) at the oligotrophic Lake Michigan, where most
BOGDAN, K.G.. & J.J. GILBERT (1982). Seasonal patterns of feed-
crustaceans were heavier during winter and spring.
ing by natural populations of Keratella, Polyarthra and
Bosmina : Clearance rates, selectivities and contributions to
The slopes of the length-weight regressions were all
community grazing. Limnol. Oceanogr., 27(5) : 918-934.
significantly (p<0.01) different from zero and ranged
BOTTRELL, H.H., A. DUNCAN, Z.M. GLIWICZ, E. GRYGIEREK, A.
from 1.9 to 3.5 (Table 2). The smallest b value was found
HERZIG, A. HILLBRICHT-ILKOWSKA, H. KURASAWA, P. LARS-
for nauplii, which could be attributed to the fact that they
SON & T. WEGLENSKA (1976). A review of some problems in
tend to elongate faster than they grow in the other two
zooplankton production studies. Norw. J. Zool., 24 : 419-
dimensions (M
456.
ALLEY et al., 1989). The values of lna and
b found for the crustacean species in Lake Mikri Prespa
BURGI, H.R., P. WEBER & H. BACHMANN (1985). Seasonal varia-
(Table 2) generally fall within the range of values for
tions in the trophic structure of phytoplankton and zooplank-
other species of the world (D
ton communities in lakes in different trophic states. Schweiz.
UMONT et al., 1975 ; McCAU-
Z. Hydrol., 47 : 197-224.
LEY, 1984 ; LAWRENCE et al., 1987 ; MALLEY et al., 1989 ;
V
BURGIS, M.J. (1974). Revised estimates for the biomass and pro-
UILLE & MAURER, 1991).
duction of zooplankton in Lake George, Uganda. Freshwat.
As for rotifers, comparing the results from the present
Biol., 4 : 535-541.
study with those from other lakes worldwide (Table 4) it
BURNS, C.W. (1969). Relation between filtering rate, tempera-
is evident that rotifer volumes cover quite a wide range of
ture and body size in four species of Daphnia. Limnol. Ocea-
values. Thus, it seems that rotifer biomass estimates must
nogr., 14 : 693-700.
be calculated for each lake separately.
DUMONT, H.J., I. VAN DE VELDE & S. DUMONT (1975). The dry
weight estimate of biomass in a selection of Cladocera,
Copepoda and Rotifera from the plankton, periphyton and
benthos of continental waters. Oecologia, 19 : 75-97.
ACKNOWLEDGEMENTS
GLIWICZ, Z.M. (1969). Studies on the feeding of pelagic zoo-
plankton in lakes with varying trophy. Ekol. Pol.-Seria A,
This research was financed by grant from the Greek Ministry
XVII (36) : 663-708.
of Agriculture. The author would also like to thank Dr. K. Ster-
GOPHEN, M. (1973). Zooplankton in Lake Kinneret. - In : BER-
giou and Dr. I. Hudec for their valuable comments on the manu-
MAN (ed.), Lake Kinneret data record, Israel Scientific
script.
Research Conference : 61-67.
226
Evangelia Michaloudi
GOPHEN, M. (1976). Temperature effect on lifespan, metabo-
RAHKOLA, M., J. KAPJLAINEN & V.A. AVINSKY (1998). Individ-
lism, and development time of Mesocyclops leuckarti
ual weight estimates of zooplankton based on length-weight
(Claus). Oecologia, 25 : 271-277.
regressions in Lake Ladoga and Saimaa Lake System. Nor-
HAWKINS, B.E. & M.S. EVANS (1979). Seasonal cycles of zoo-
dic J. Freshw. Res., 74 : 110-120.
plankton biomass in southeastern Lake Michigan. Internat.
RUTTNER-KOLISKO, A. (1977). Suggestions for biomass calcula-
Assoc. Great Lakes Res., 5 : 256-263.
tion of planktonic rotifers. Arch. Hydrobiol. Beih. Ergebn.
LAWRENCE, S.G., D.F. MALLEY, W.J. FINDLAY, M.A. MACIVER &
Limnol., 8 : 71-76.
I.L. DELBAERE (1987). Method for estimating dry weight of
SAUNDERS, J.F. & W.M. LEWIS (1988). Composition and season-
freshwater planktonic crustaceans from measures of length
ality of the zooplankton community of Lake Valencia, Vene-
and shape. Can. J. Fish. Aquat. Sci., 44 : 267-274.
zuela. J. Plank. Res., 10 : 957-985.
LEWIS, W.M. (1979). Zooplankton community analysis : studies
SCHINDLER, D.W. & B. NOVEN (1971). Vertical distribution and
on a tropical system. Springer-Verlag, New York, 163 pp.
seasonal abundance of zooplankton in two shallow lakes of
MALLEY, D.F., S.G. LAWRENCE, M.A. MACIVER & W.J. FINDLAY
the Experimental Lakes Area, northwestern Ontario. J. Fish.
(1989). Range of variation in estimates of dry weight for
Res. Board Can., 28, 245-256.
planktonic crustacea and rotifera from temperate North
American Lakes. Can. Techn. Rep. Fish. Aquat. Sci., 1666 :
SOMMER, U., Z.M. GLIWICZ, W. LAMPERT & A. DUNCAN (1986).
The PEG-model of seasonal succession of planktonic events
iv + 49 p.
McC
in fresh waters. Arch. Hydrobiol., 106(4) : 433-471.
AULEY, E. (1984). The estimation of the abundance and bio-
mass of zooplankton in samples. In : D
TRYPHON, E., M. MOUSTAKA-GOUNI, G. NIKOLAIDIS & I. TSEKOS
OWNING & RIGLER
(eds), A manual on methods for the assessment of secondary
(1994). Phytoplankton and physical-chemical features of the
productivity in fresh waters, IBP 17, Blackwell Scientific
shallow Lake Mikri Prespa, Macedonia, Greece. Arch. Hyd-
Publications : 228-265.
robiol., 131 : 477-494.
MICHALOUDI, E., M. ZARFDJIAN & P.S. ECONOMIDIS (1997). The
URABE, J. (1992). Midsummer succession of rotifer plankton in
zooplankton of Lake Mikri Prespa. Hydrobiologia, 351 : 77-
a shallow eutrophic pond. J. Plank. Res., 14 : 851-866.
94.
VUILLE, T. & V. MAURER (1991). Bodymass of crustacean plank-
MOURELATOS, S. & G. LACROIX (1990). In situ filtering rates of
ton in Lake Biel : A comparison between pelagic and littoral
Cladocera : Effect of body length, temperature and food con-
communities. Verh. Int. Verein. Limnol., 24 : 938-942.
centration. Limnol. Oceanogr., 35(5) : 1101-1111.
ZARFDJIAN, M. (1989). Seasonal variations and spatial distribu-
NAUWERK, A. (1963). Die Beziehungen zwischen Zooplankton
tion of planktic invertebrates in Lake Volvi (Macedonia,
und Phytoplankton im See Erken. Symbolae Botanicae
Greece). Doctoral Dissertation, Univ. of Thessaloniki,
Upsalienses, 17 : 1-163.
Greece, 249 pp. (In Greek).
TABLE 4
Volumes (µm3 10-6) of rotifer species from Lake Mikri Prespa and other lakes.
Species
Volume
Site
Country
Trophic Status
Source
Asplanchna
57.16
Lake Mikri Prespa
Greece
eutrophic
present study
priodonta
33.6
Lake Volvi
Greece
eutrophic
ZARFDJIAN 1989
30-300
Lake Erken
Sweden
eutrophic
NAUWERK 1963
200
Lake Windermere
England
eutrophic
RUTTNER-KOLISKO 1977
44
Lake Suwa
Japan
eutrophic
BOTTRELL et al. 1976
37.5
Lake Kinneret
Israel
eutrophic
GOPHEN 1973
22.5
Lake Lucerne
Switzerland mesotrophic
BURGI et al. 1985
20
Danube river+ sidearms
Slovakia
mesotrophic
VRANOVSKY (pers.comm.)
16
Lake Lunz
Austria
mesotrophic
RUTTNER-KOLISKO 1977
13.12
ELA lakes
Canada
oligotrophic
MALLEY et al. 1989
Brachionus
0.26
Lake Mikri Prespa
Greece
eutrophic
present study
angularis
0.4
Lake Volvi
Greece
eutrophic
ZARFDJIAN 1989
0.5
Lake Suwa
Japan
eutrophic
BOTTRELL et al. 1976
0.1
Lake Kinneret
Israel
eutrophic
GOPHEN 1973
0.28
Funada-ike pond
Japan
eutrophic
URABE 1992
0.45-0.63
Lake Lough Neagh
Ireland
eutrophic
ANDREW & FITZISIMONS 1992
0.4
Danube river+ sidearms
Slovakia
mesotrophic
VRANOVSKY (pers.comm.)
Brachionus
1.88
Lake Mikri Prespa
Greece
eutrophic
present study
diversicornis
2.9
Lake Volvi
Greece
eutrophic
ZARFDJIAN 1989
1.5
Lake Suwa
Japan
eutrophic
BOTTRELL et al. 1976
3
Danube river+ sidearms
Slovakia
mesotrophic
VRANOVSKY (pers.comm.)
Brachionus
0.18
Lake Mikri Prespa
Greece
eutrophic
present study
forficula
0.22
Funada-ike pond
Japan
eutrophic
URABE 1992
Conochilus
0.43
Lake Mikri Prespa
Greece
eutrophic
present study
hippocrepis
0.6
Lake Erken
Sweden
eutrophic
NAUWERK 1963
0.15
Lake Suwa
Japan
eutrophic
BOTTRELL et al. 1976
Filinia
0.24
Lake Mikri Prepsa
Greece
eutrophic
present study
longiseta
1.5
Lake Suwa
Japan
eutrophic
BOTTRELL et al. 1976
0.41
Funada-ike pond
Japan
eutrophic
URABE 1992
0.17-0.24
Lake Lough Neagh
Ireland
eutrophic
ANDREW & FITZISIMONS 1992
0.32
Lake Lucerne
Switzerland mesotrophic
BURGI et al. 1985
0.3
Danube river+ sidearms
Slovakia
mesotrophic
VRANOVSKY (pers.comm.)
0.52
ELA lakes
Canada
oligotrophic
MALLEY et al. 1989
Zooplankton of Lake Mikri Prespa
227
TABLE 4 (CONT.)
Volumes (µm3 10-6) of rotifer species from Lake Mikri Prespa and other lakes.
Species
Volume
Site
Country
Trophic Status
Source
Keratella
0.05
Lake Mikri Prespa
Greece
eutrophic
present study
cochlearis
0.05
Lake Volvi
Greece
eutrophic
ZARFDJIAN 1989
0.05
Lake Erken
Sweden
eutrophic
NAUWERK 1963
0.15
Lake Windermere
England
eutrophic
RUTTNER-KOLISKO 1977
0.1
Lake Kinneret
Israel
eutrophic
GOPHEN 1973
0.09
Funada-ike pond
Japan
eutrophic
URABE 1992
0.046
Lake Lough Neagh
Ireland
eutrophic
ANDREW & FITZISIMONS 1992
0.07
Lake Lanao
Philippine
eutrophic
LEWIS 1979
0.11
Lake Lunz
Austria
mesotrophic
RUTTNER-KOLISKO 1977
0.04
Lake Lucerne
Switzerland mesotrophic
BURGI et al. 1985
0.25
Danube river+ sidearms
Slovakia
mesotrophic
VRANOVSKY (pers.comm.)
0.15
Lake Balaton
Hungary
RUTTNER-KOLISKO 1977
0.15
ELA lakes
Canada
oligotrophic
MALLEY et al. 1989
0.7
ELA lakes
Canada
oligotrophic
SCHINDLER & NOVEN 1971
Polyarthra
0.9
Lake Mikri Prespa
Greece
eutrophic
present study
spp.
1.1
Lake Volvi
Greece
eutrophic
ZARFDJIAN 1989
0.55
Lake Erken
Sweden
eutrophic
NAUWERK 1963
0.65
Lake Winderermere
England
eutrophic
RUTTNER-KOLISKO 1977
2
Lake Suwa
Japan
eutrophic
BOTTRELL et al. 1976
0.3
Lake Kinneret
Israel
eutrophic
GOPHEN 1973
0.23
Funada-ike pond
Japan
eutrophic
URABE 1992
0.3-0.54
Lake Lough Neagh
Ireland
eutrophic
ANDREW & FITZISIMONS 1992
0.29
Lake Lanao
Philippine
eutrophic
LEWIS 1979
0.3
Lake Valencia
Venezuela
eutrophic
SAUNDERS & LEWIS 1988
0.4
Lake Lunz
Austria
mesotrophic
RUTTNER-KOLISKO 1977
0.14
Lake Lucerne
Switzerland mesotrophic
BURGI et al. 1985
0.1-1
Danube river+ sidearms
Slovakia
mesotrophic
VRANOVSKY (pers.comm.)
0.38
Lake Balaton
Hungary
RUTTNER-KOLISKO 1977
0.5
ELA lakes
Canada
oligotrophic
MALLEY et al. 1989
1.4
ELA lakes
Canada
oligotrophic
SCHINDLER & NOVEN 1971
Synchaeta
3.43
Lake Mikri Prespa
Greece
eutrophic
present study
pectinata
1.5
Lake Volvi
Greece
eutrophic
ZARFDJIAN 1989
2
Lake Erken
Sweden
eutrophic
NAUWERK 1963
4.5
Lake Kinneret
Israel
eutrophic
GOPHEN 1973
0.65
Lake Lucerne
Switzerland mesotrophic
BURGI et al. 1985
1
Danube river+ sidearms
Slovakia
mesotrophic
VRANOVSKY (pers.comm.)
Trichocerca
0.33
Lake Mikri Prespa
Greece
eutrophic
present study
capucina
0.7
Lake Volvi
Greece
eutrophic
ZARFDJIAN 1989
0.15
Lake Erken
Sweden
eutrophic
NAUWERK 1963
1
Lake Kinneret
Israel
eutrophic
GOPHEN 1973
0.11
Lake Lucerne
Switzerland mesotrophic
BURGI et al. 1985
0.2
Danube river+ sidearms
Slovakia
mesotrophic
VRANOVSKY (pers.comm.)
Trichocerca
0.12
Lake Mikri Prespa
Greece
eutrophic
present study
cylindrica
0.2
Danube river+ sidearms
Slovakia
mesotrophic
VRANOVSKY (pers.comm.)
1
ELA lakes
Canada
oligotrophic
MALLEY et al. 1989
0.1
ELA lakes
Canada
oligotrophic
SCHINDLER & NOVEN 1971
Trichocerca
0.17
Lake Mikri Prespa
Greece
eutrophic
present study
similis
0.3
Lake Volvi
Greece
eutrophic
ZARFDJIAN 1989
0.15
Lake Erken
Sweden
eutrophic
NAUWERK 1963
1
Lake Kinneret
Israel
eutrophic
GOPHEN 1973
0.08
Lake Lucerne
Switzerland mesotrophic
BURGI et al. 1985
0.2
Danube river+ sidearms
Slovakia
mesotrophic
VRANOVSKY (pers.comm.)
Belg. J. Zool., 135 (2) : 229-233
July 2005
Deep-water fish fauna in the Eastern Ionian Sea
Chryssi Mytilineou1, Chrissi-Yianna Politou1, Costas Papaconstantinou1, Stefanos Kavadas1,
Gianfranco D'Onghia2 and Leticia Sion2
1 Hellenic Centre for Marine Research, Ag. Kosmas, 16604 Helliniko, Athens, Greece
2 University of Bari, Department of Zoology, Via Orabona 4, 70125 Bari, Italy
Corresponding author : e-mail address : chryssi@ncmr.gr
ABSTRACT. Existing information on the ichthyofauna of the Eastern Ionian Sea (Greece) was enriched by a recent
research project carried out in its northern part at depths ranging from 300 to 1200 m. The frequency of occurrence
of the identified fish species and their abundance were examined. In total, 101 fish species were identified. Their
number and abundance decreased significantly with depth. Argentina sphyraena presented the highest frequency of
occurrence and Chlorophthalmus agassizi the highest abundance at depths ranging between 300 and 500 m. In the
depth zone 500-700 m, Chlorophthalmus agassizi predominated in abundance and Phycis blennoides in frequency
of occurrence. In the zone 700-900 m, Galeus melastomus and Nezumia sclerorhynchus showed both the highest
abundance and frequency of occurrence. These two species were also the most abundant at depths 900-1200 m,
whereas Lampanyctus crocodilus was the most frequently encountered. Four species (Benthocometes robustus, Mic-
roichthys coccoi, Nemichthys scolopaceus and Epigonus constanciae) are reported for the first time in Greek
waters, and twenty species are reported for the first time in the Greek Ionian Sea. Moreover, one specimen of
Caelorinchus mediterraneus IWAMOTO & UNGARO, 2002, a species that has only recently been described for the
Mediterranean Sea, was also identified.
KEY WORDS : deep sea, fish fauna, Eastern Ionian Sea, Greece
INTRODUCTION
face of each stratum (COCHRAN, 1977). However, for
experimental purposes, sampling was also extended to
The ichthyofauna of the Eastern Ionian Sea (Greece)
depths 900-1200 m with some additional stations. In total,
consists of Atlantic-Mediterranean and cosmopolitan spe-
148 hauls were carried out during the four surveys
cies. Few studies exist, most of which concern the fish
(Fig. 1), three hauls of which were not considered valid.
fauna of the continental shelf and the upper slope
The duration of the hauls was 30 min for depths <500 m
(KASPIRIS, 1973; PAPACONSTANTINOU, 1986; PAPACON-
and one hour for depths >500 m. Catches were identified
STANTINOU et al., 1987). The previously available data on
to species level and the abundance of each species was
the fish fauna of the deep waters of the Eastern Ionian Sea
recorded on board.
were derived from the research expeditions "Dana" and
The number of species and their total abundance per
"Thor" (TÅNING, 1918; 1923; EGE, 1930; 1934; 1948;
fishing hour in each haul were examined and the relation
1953). No recent published data appear in the literature,
of their logarithms to depth was tested using linear regres-
although unpublished data for depths down to 800 m of
sion. Moreover, the frequency of occurrence (F) and the
the central and southern part of the Greek Ionian Sea exist
mean abundance (A) in terms of number per fishing hour
from research projects carried out in recent years.
per species for each depth stratum were estimated as
The present work provides information on the qualita-
follows :
tive and quantitative fish species composition of the East-
F = hn * 100 / h,
ern Ionian Sea for depths ranging between 300 and
where hn = sum of the number of the n hauls where a
1200 m.
species was present in a depth stratum, and h = sum of
the number of all the hauls carried out in that depth stra-
tum, and
MATERIALS AND METHODS
A = Nn / tn,
Sampling was carried out in the deep waters of the
where Nn = sum of the numbers of a species in the n
northern part of the Eastern Ionian Sea (Fig. 1) during
hauls carried out in a depth stratum and tn = sum of the
four experimental surveys (September 1999, April 2000,
fishing time of the n hauls in that depth stratum.
July 2000 and September 2000). Two hired commercial
trawlers equipped with trawls of 40 mm (stretched) mesh
RESULTS
size in the cod-end were used for sampling. The study
area included between the 300 and 900 m isobaths, and
In total, 101 fish species were caught in the study area,
was divided into three depth strata (300-500, 500-700,
of which 81 were osteichthyes and 20 were chondrich-
700-900 m). A random stratified design was applied for
thyes (Table 1). The relationships of the number of spe-
the sampling, taking into account the depth and the sur-
cies and their total abundance with depth were statisti-
230
C. Mytilineou, C.-Y. Politou, C. Papaconstantinou, S. Kavadas, G. D'Onghia and L. Sion
cally significant with decreasing trend (b = -0.001,
their total abundance (b = -0.0069, DF = 144, P<0.05)
r = 0.65, DF = 144, P<0.05 and b = -0.006, r = 0.79,
with depth as well as for the number of chondrichthyes
DF = 144, P<0.05, respectively) (Figs. 2, 3). Similar
(b = -0.002, DF = 141, r = 0.61, P<0.05) and their total
results were obtained from the analysis of the number of
abundance with depth (b = -0.002, DF = 141, r = 0.40,
osteichthyes (b = -0.009, r = 0.57, DF = 144, P<0.05) and
P<0.05).
19°0'0"E
20°0'0"E
21°0'0"E
22°0'0"E
!
!
!
!
! !
!
!
!
!
!
!
!
!
! !
!
!
!
! !!! ! !
! !
!!
!
!
!
!
!
!
!
!!
!
!
!
GREECE
!
!
!
!
!
! !!!
!
IO
! !
!
!
!
N
!
!
39°0'0"N
!
!
!
39°0'0"N
!
! !
!
!
I
!
!
A
!
! !
!
!
! !!
N
! ! !
!
S
!
!
!! !
E
!
A
!
!
!
!
!
!
!
!
!
!
!
!
!!
!
38°0'0"N
!
!
38°0'0"N
!
!
!
!
!
!!
® ! 300-500 m
!
501-700 m
!!
!
!
701-900 m
!
> 900 m
!
19°0'0"E
20°0'0"E
21°0'0"E
22°0'0"E
Fig. 1. Map of the study area showing sampling stations.
TABLE 1
List of fish species collected in the E. Ionian Sea with species depth range, frequency of occurrence (%) and abundance (N/h) per
depth stratum. Species names are given according to FishBase. (* species for the first time in the Greek ionian Sea)
Depth
Depth strata (m)
range (m)
300-500
500-700
700-900
900-1200
No. of hauls
44
52
36
13
Species
%
N/h
%
N/h
%
N/h
%
N/h
CHONDRICHTHYES
Centrophorus granulosus (Bloch & Schneider, 1801)
512-823
7.7
0.2
10.5
0.1
Chimaera monstrosa Linnaeus, 1758 *
514-1171
7.7
0.1
7.9
0.1
15.4
0.2
Dalatias licha (Bonnaterre, 1788)
655-764
3.8
0.1
15.8
0.2
Dipturus batis (Linnaeus, 1758) *
700
2.6
0.1
Galeus melastomus Rafinesque, 1810
305-1171
55.6
60.8
98.1
54.6
94.7
36.1
92.3
18.4
Heptranchias perlo (Bonnaterre, 1788) *
388-501
4.4
0.2
1.9
0.1
Hexanchus griseus (Bonnaterre, 1788) *
700
2.6
0.1
Leucoraja circularis (Couch, 1838)
463-676
2.2
0.1
7.7
0.1
Mustelus mustelus (Linnaeus, 1758) *
624
1.9
0.1
Oxynotus centrina (Linnaeus, 1758) *
549-777
3.8
0.1
7.9
0.1
Raja asterias Delaroche,1809
333-343
6.7
0.3
Raja clavata Linnaeus, 1758
300-577
44.4
3.1
3.8
0.1
Raja miraletus Linnaeus, 1758
462
2.2
0.1
Raja montagui Fowler 1910 *
318-345
11.1
0.3
Raja oxyrinchus Linnaeus, 1758
288-640
77.8
3.9
15.4
0.2
Raja polystigma Regan,1923
328
2.2
0.1
Raja sp.
462-473
4.4
0.3
Scyliorhinus canicula (Linnaeus, 1758)
288-780
88.9
25.1
7.7
0.1
2.6
0.1
Squalus blainville (Risso, 1827)
300-780
77.8
20.1
17.3
0.5
15.8
0.2
Torpedo marmorata Risso, 1810
317-368
6.7
0.2
Torpedo nobiliana Bonaparte, 1835 *
300-388
4.4
0.1
OSTEICHTHYES
Acantholabrus palloni (Risso,1810)
351
2.2
0.1
Argentina sphyraena Linnaeus, 1758
288-700
95.6
760.6
28.8
2.9
Argyropelecus hemigymnus Cocco,1829
460-1082
4.4
0.2
32.7
0.7
15.8
0.2
23.1
0.3
Arnoglossus rueppelli (Cocco, 1844) *
288-897
73.3
26.0
5.8
0.1
5.3
0.1
Bathypterois dubius Vaillant, 1888 *
700-1171
34.2
1.1
84.6
4.6
Bellottia apoda Giglioli, 1883
460-569
2.2
0.1
3.8
0.1
Benthocometes robustus (Goode & Bean, 1886)
503
1.9
0.1
Benthosema glaciale (Reinhardt, 1837)
541-1085
9.6
0.4
2.6
0.1
7.7
0.1
Deep fish fauna in the Eastern Ionian
231
TABLE 1
List of fish species collected in the E. Ionian Sea with species depth range, frequency of occurrence (%) and abundance (N/h) per
depth stratum. Species names are given according to FishBase. (* species for the first time in the Greek ionian Sea)
Depth
Depth strata (m)
range (m)
300-500
500-700
700-900
900-1200
No. of hauls
44
52
36
13
Species
%
N/h
%
N/h
%
N/h
%
N/h
Caelorinchus caelorinchus (Risso, 1810)
305-710
51.1
175.7
65.4
22.5
7.9
0.2
Caelorinchus mediterraneus Iwamoto & Ungaro, 2002
1032
7.7
0.1
Capros aper (Linnaeus, 1758)
288-700
68.9
283.1
3.8
0.1
Centracanthus cirrus Rafinesque, 1810
327-464
13.3
1.6
Centrolophus niger (Gmelin 1789) *
624-770
1.9
0.1
2.6
0.1
Ceratoscopelus maderensis (Lowe, 1839)
460-1082
2.2
0.1
1.9
0.1
2.6
0.1
7.7
0.2
Chauliodus sloani Bloch & Schneider, 1801
473-1192
2.2
0.3
32.7
0.9
39.5
0.6
30.8
0.9
Chelidonichthys cuculus (Linnaeus, 1758)
288-356
22.2
3.8
Chelidonichthys gurnardus (Linnaeus, 1758)
340
2.2
0.1
Chelidonichthys lucerna (Linnaeus, 1758)
318
2.2
0.1
Chlorophthalmus agassizi Bonaparte, 1840
300-897
88.9 3958.2
78.8
165.7
5.3
1.0
Conger conger (Linnaeus, 1758)
305-1171
24.4
1.1
23.1
0.9
26.3
0.5
23.1
0.4
Deltentosteus quadrimaculatus (Valenciennes, 1837)
333
2.2
0.8
Diaphus holti Tåning, 1918
300-777
4.4
0.1
3.8
0.1
5.3
0.1
Diaphus metopoclampus (Cocco, 1829)
518-1085
5.8
0.2
7.9
0.1
7.7
0.1
Diaphus rafinesquii (Cocco, 1838)
616-660
3.8
0.1
Electrona risso (Cocco, 1829)
614
1.9
0.1
Epigonus constanciae (Giglioli, 1880)
351-742
2.2
1.1
15.4
0.3
2.6
0.1
Epigonus denticulatus Dieuzeidei, 1950 *
351-660
2.2
0.1
5.8
0.1
Epigonus spp
620
1.9
0.1
Epigonus telescopus (Risso, 1810)
351-780
4.4
0.1
1.9
0.1
5.3
0.1
Etmopterus spinax (Linnaeus, 1758)
327-1171
4.4
0.1
40.4
3.2
65.8
2.0
69.2
1.4
Gadella maraldi (Risso, 1810)
368-748
2.2
0.1
7.7
0.1
2.6
0.1
Gadiculus argenteus argenteus Guichenot, 1850
300-518
66.7
647.0
1.9
0.4
Gaidropsarus biscayensis (Collette, 1890) *
549
1.9
0.1
Gnathophis mystax (Delaroche, 1809)
700
2.6
0.1
Gonostoma denudatum Rafinesque, 1810
531
1.9
0.1
Helicolenus dactylopterus (Delaroche, 1809)
288-852
91.1
35.0
94.2
53.6
78.9
8.8
Hoplostethus mediterraneus Cuvier, 1829
388-897
6.7
1.1
94.2
47.6
73.7
10.5
Hymenocephalus italicus Giglioli, 1884
305-897
53.3
321.5
96.2
70.1
47.4
2.1
Ichthyococcus ovatus (Cocco, 1838)
614
1.9
0.1
Lampanyctus crocodilus (Risso, 1810)
318-1192
4.4
0.1
71.2
11.2
92.1
14.4
100.1
6.4
Lepidopus caudatus (Euphrasen, 1788)
333-620
8.9
0.2
9.6
0.1
Lepidorhombus boscii (Risso, 1810) *
300-700
51.1
18.0
80.8
10.1
2.6
0.1
Lepidorhombus whiffiagonis (Walbaum, 1792) *
288-700
55.6
3.7
40.4
1.2
2.6
0.1
Lepidotrigla dieuzeidei Blanc & Hureau, 1973
288-596
55.6
73.0
1.9
0.1
Lestidiops sphyrenoides (Risso, 1820)
518
1.9
0.1
Lesueurigobius suerii (Risso, 1810) *
322-337
6.7
0.3
Lobianchia dofleini (Zugmayer, 1911)
318
2.2
0.2
Lophius budegassa Spinola, 1807
300-1013
42.2
2.8
32.7
0.5
10.5
0.1
7.7
0.1
Lophius piscatorius Linnaeus, 1758
370-770
2.2
0.1
5.8
0.1
7.9
0.1
Macroramphosus scolopax (Linnaeus, 1758)
322-342
4.4
0.2
Maurolicus muelleri (Gmelin,1789) *
318-351
6.7
4.8
Merluccius merluccius (Linnaeus, 1758)
288-764
86.7
35.3
50.1
2.8
13.2
0.1
Microichthys coccoi Rüppell, 1852
549
1.9
0.1
Micromesistius poutassou (Risso, 1827)
305-676
26.7
14.1
44.2
1.1
Molva macrophthalma (Rafinesque, 1810)
388-754
4.4
0.3
26.9
0.4
7.9
0.1
Mora moro (Risso, 1810)
512-1171
28.8
3.5
92.1
9.3
92.3
13.3
Mullus barbatus Linnaeus, 1758
328
2.2
0.2
Mullus surmuletus Linnaeus, 1758
305-409
22.2
2.8
Myctophidae
754-1082
5.3
0.1
7.7
0.2
Myctophum punctatum Rafinesque, 1810 *
549
1.9
0.2
Nemichthys scolopaceus Richardson, 1848
390-1079
2.2
0.1
1.9
0.1
7.7
0.1
Nettastoma melanurum Rafinesque, 1810
305-1171
11.1
0.3
84.6
3.5
89.5
9.1
76.9
4.8
Nezumia sclerorhynchus (Valenciennes, 1838)
388-1171
2.2
0.2
98.1
46.5
94.7
35.1
92.3
18.5
Notacanthus bonaparte Risso, 1840
487-1034
1.9
0.1
13.2
0.2
15.4
0.2
Pagellus acarne (Risso, 1827)
302-318
6.7
3.0
Pagellus bogaraveo (Brünnich, 1768)
305-700
37.8
8.6
50.1
2.1
Paralepis coregonoides Risso, 1820
1032
7.7
0.1
Paralepis speciosa Bellotti, 1878
660
1.9
0.1
Peristedion cataphractum (Linnaeus, 1758)
288-848
91.1
141.9
42.3
2.1
2.6
0.1
Phycis blennoides (Brünnich, 1768)
300-1047
75.6
10.6
100.1
29.0
92.1
7.3
61.5
0.8
Polyprion americanus (Bloch & Schneider, 1801)
503-577
3.8
0.1
Scorpaena elongata Cadenat, 1943
300-710
31.1
0.9
1.9
0.1
2.6
0.1
Spicara smaris (Linnaeus, 1758)
328
2.2
0.1
Stomias boa (Risso, 1810)
473-1032
2.2
0.2
28.8
1.5
26.3
0.8
7.7
0.1
Symphurus ligulatus (Cocco, 1844) *
531-761
15.4
0.4
7.9
0.1
Symphurus nigrescens Rafinesque, 1810
533-601
7.7
0.2
Synchiropus phaeton (Günther, 1861)
302-848
31.1
3.3
17.3
0.5
2.6
0.1
Trachurus picturatus (Bowdich, 1825)
305-368
8.9
0.3
Trachurus trachurus (Linnaeus, 1758)
300-318
6.7
0.3
Trachyrincus scabrus (Rafinesque, 1810) *
480-1171
2.2
0.1
15.8
0.9
46.2
0.7
Trigla lyra Linnaeus, 1758
288-620
57.8
5.4
9.6
0.1
Trisopterus minutus (Linnaeus, 1758)
333
2.2
0.4
Zeus faber Linnaeus, 1758
328
2.2
0.1
232
C. Mytilineou, C.-Y. Politou, C. Papaconstantinou, S. Kavadas, G. D'Onghia and L. Sion
DISCUSSION
1.4
1.2
From the 101 species identified in the present work,
one fish was identified as the new Mediterranean macru-
1
rid species, Caelorinchus mediterraneus IWAMOTO &
0.8
UNGARO, 2002 (Table 1). It was caught at a depth of 1032
0.6
m, which is within the depth range reported in the litera-
log(Number of Species)
ture for the species (IWAMOTO & UNGARO, 2002). This
0.4
species has been recently described from specimens col-
0.2
lected in the Catalan, Ligurian and Adriatic Seas
200
400
600
800
1000
1200
(IWAMOTO & UNGARO, 2002) but it has not been reported
Depth (m)
so far from the Ionian Sea.
Fig. 2. Relationship of the number of species with depth.
Four species are recorded for the first time in Greek
waters : Benthocometes robustus, Microichthys coccoi,
Nemichthys scolopaceus and Epigonus constanciae. The
4.3
first two were found only in one station at depths 500-700
3.8
m. The third one was encountered in three depth zones
(300-500, 500-700 and 900-1200 m) in very low frequen-
3.3
cies and abundances (Table 1). Finally, Epigonus constan-
2.8
ciae was caught at depths between 351 and 742 m, with
log(N/h) 2.3
higher occurrence at depths 500-700 m (Table 1). Accord-
1.8
ing to the literature, Benthocometes robustus has been
rarely found in the Mediterranean Sea and Microichthys
1.3
coccoi is reported only from the Strait of Messina (Italy)
0.8
200
400
600
800
1000
1200
(WHITEHEAD et al., 1989). Nemichthys scolopaceus is
Depth (m)
recorded for the first time for all the Ionian Sea, although
Fig. 3. Relationship of the total abundance (N/h) with depth.
it is known in the western Mediterranean and the Atlantic
(WHITEHEAD et al., 1989). Epigonus constanciae has also
In the depth zone 300-500 m, 72 species were found
been found in the western Mediterranean and eastern
(59 osteichthyes and 13 chondrichthyes). Argentina sphy-
Atlantic off West Africa with a maximum of occurrence
raena, Peristedion cataphractum, Helicolenus dactylop-
between 200 and 400 m (WHITEHEAD et al., 1989).
terus, Chlorophthalmus agassizi, Scyliorhinus canicula
Twenty species (indicated in Table 1 by asterisk) are
and Merluccius merluccius presented high frequency of
reported for the first time for the fish fauna of the Greek
occurrence (Table 1). Chlorophthalmus agassizi was
Ionian Sea. Most of them are species encountered mainly
dominant in terms of abundance (Table 1). Most of the
at depths >500 m, which have only recently been investi-
chondrichthyes caught in this zone belonged to species of
gated.
the genus Raja.
The results of this study showed a general decrease in
the number of fish species and of their abundance with
In the zone 500-700 m, 70 fish species were identified
depth. More specifically, the number of fish species
(58 osteichthyes and 12 chondrichthyes) (Table 1). Chlo-
decreased considerably in waters deeper than 700 m,
rophthalmus agassizi still predominated in terms of abun-
whereas the species abundance declined sharply in waters
dance (Table 1). Phycis blennoides was present at all sta-
deeper than 500 m. The decline in both number of species
tions (100% frequency of occurrence). Galeus
and abundance is also true for other Mediterranean areas
melastomus, Nezumia sclerorhynchus, Hymenocephalus
as well as for other taxonomic groups (ABELLO et al.,
italicus, Helicolenus dactylopterus and Hoplostethus
1988; BIAGI et al., 1989; CARTES et al., 1994; STEFA-
mediterraneus were also found in high frequency of
NESCU et al., 1994; ABELLA & SERENA, 1995; D'ONGHIA
occurrence (Table 1).
et al., 1998; 2002 KALLIANIOTIS et al., 2000).
The ichthyofauna in the Eastern Ionian Sea (Greece) is
From the 47 species (38 osteichthyes and 9 chondrich-
quite similar to that of the North-western Ionian Sea
thyes) caught in the depth zone 700-900 m and from the
(Italy) (D'ONGHIA et al., 1998), a fact also mentioned by
22 species (20 osteichthyes and 2 chondrichthyes) caught
D'ONGHIA et al., (2002). However, important differences
in the zone 900-1200 m, Galeus melastomus and Nezumia
were detected concerning the abundance of various spe-
sclerorhynchus were the most abundant in both zones
cies. Gadiculus argenteus argenteus and Hymenocepha-
(Table 1). Galeus melastomus, Nezumia sclerorhynchus,
lus italicus are the most abundant fish in the upper slope
Lampanyctus crocodilus and Mora moro were the most
of the Italian Ionian (D'ONGHIA et al., 2002), whereas
frequent in the zone 700-900 m (Table 1). Their order of
Chloropthalmus agassizi was found to be the dominant
importance in terms of frequency of occurrence changed
species in the Greek Ionian with considerably higher
in the deeper zone as follows : Lampanyctus crocodilus,
abundance values. Moreover, abundance values were
Galeus melastomus, Nezumia sclerorhynchus and Mora
generally much higher in Greek than Italian Ionian Sea.
moro. Furthermore, Phycis blennoides was also fre-
Another remarkable discrepancy between the two neigh-
quently present in the depth zone 700-900 m, but less so
bouring areas is the higher number of species and abun-
in deeper waters (Table 1).
dance of chondrichthyes in the upper slope of the Greek
Deep fish fauna in the Eastern Ionian
233
Ionian than the Italian one. The higher abundance for
EGE, V. (1930). Sudidae (Paralepis). Rep. Danish Oceanogr.
many species, the dominance of few species and the
Exped. Med., 1908-1910, 2(10), A13 : 193p.
greater number of species and specimens of chondrich-
EGE, V. (1934). The genus Stomias Cuv., taxonomy and bioge-
thyes, characteristics found for the Eastern Ionian
ography. Dana Rep., 5 : 58p.
E
(Greece), could be explained by the environmental and
GE, V. (1948). Chauliodus Schn., Bathypelagic genus of fishes.
A systematic, phylogenetic and geographical study. Dana
fisheries conditions prevailing in each area. It must be
Rep., 31 : 148p.
underlined that fishing pressure is low at the Greek Ionian
EGE, V. (1953). Paralepididae I. (Paralepis and Lestidium). Tax-
upper-slope bottoms, and fisheries activities are scarcely
onomy, ontogeny, phylogeny and distribution. Dana Rep.,
exercised at depths greater than 500 m in Greek waters,
40 : 184p.
whereas the Italian waters are fished intensively down to
IWAMOTO, T. & N. UNGARO (2002). A new grenadier
(Gadiformes, Macrouridae) from the Mediteranean. Cybium,
700 m by commercial trawlers. Fisheries exploitation
26 (1) : 27-32.
affects species abundance and especially long-lived,
KALLIANIOTIS, A., K. SOPHRONIDIS, P. VIDORIS & A. TSELEPIDES
large-sized species, and species generally positioned high
(2000). Demersal fish and megafaunal assemblages on the
in the food web (PAULY et al., 1998) such as chondrich-
Cretan continental shelf and slope (NE Mediterranean) : sea-
thyes (S
sonal variation in species density, biomass and diversity.
TEVENS et al., 2000). However, some Chondrich-
Prog. in Oceanogr., 46 : 429-455.
thyes species such as S. blanville and R. clavata not found
KASPIRIS, P. (1973). Contribution on the study of Osteichthyes of
in the north-western Ionian (Italy) (MATARRESE et al.,
the Korinthiakos and Patraikos Gulfs and Ionian Sea. PhD.
1996; D'ONGHIA et al., 2002) are frequently found in the
Thesis, University of Patras. (in Greek)
neighbouring Sicilian channel (RELINI et al., 2000). This
MATARRESE A., G. D'ONGHIA, A. TURSI & M. BASANISI (1996).
indicates that the environmental conditions should also be
New information on the Ichthyofauna of the south-eastern
considered in order to explain the differences in the fish
Italian coasts (Ionian Sea). Cybium, 20(2) : 197-211.
P
fauna between the Greek and Italian Ionian Sea.
APACONSTANTINOU, C. (1986). The ichthyofauna of Korinthia-
kos, Patraikos Gulfs and Ionian Sea. Biologia Gallo-Hellen-
ika, 12 : 229-236.
REFERENCES
PAPACONSTANTINOU, C., E. KARAGITSOU, K. STERGIOU, V. VASSI-
LOPOULOU, G., PETRAKIS, CH. MYTILINEOU & TH. PANOS
(1987). Dynamics of the demersal fish populations in the
ABELLO, P., F.J. VALLADARES & A. CASTELLON (1988). Analysis
Korinthiakos, Patraikos Gulfs and Ionian Sea. N.C.M.R.
of the structure of decapod crustacean assemblages off the
Spec. Publ. No 13 : 208p.
Catalan coast (North-West Mediterranean). Mar. Biol., 98 :
PAULY, D., V. CHRISTENSEN, J. DALSGAARD, R. FROESE & F. C.
39-49.
TORRES JR (1998). Fishing down marine food webs. Science,
ABELLA, A., & F. SERENA (1995). Definizione di assemblaggi
297 : 860-863.
demersali nell' alto Tirreno. Biol. Mar. Medit., 2 : 451-453.
R
B
ELINI G., F. BIAGI, F. SERENA, A. BELLUSCIO, M. T. SPEDICATO,
IAGI, F., S. DE RANIERI, M. MORI, P. SARTOR & M. SBRANA
P. R
(1989). Preliminary analysis of demersal fish assemblages in
INELLI, M. C. FOLLESA, C. PICCINETTI, N. UNGARO, L.
S
the Northern Tyrrenian Sea. Nova Thalassia, 10 (Suppl. 1) :
ION & D. LEVI (2000). I Selaci pescati con lo strascico nei
mari italiani. Biol. Mar. Medit., (7)1 : 347-384.
391-398.
C
STEFANESCU, C., B. MORALES-NIN & F. PERRI (1994). Fish
ARTES, J. E., J. B. COMPANY & F. MAYNOU (1994). Deep-water
decapod crustacean communities in the Northwesten
assemblages on the slope in the Catalan Sea (Western
Mediterranean : influence of submarine canyons and season.
Mediterranean) : influence of a submarine canyon. J. Mar.
Mar. Biol., 120 : 221-229.
Biol. Ass. U.K., 74 : 499-512.
C
S
OCHRAN, W. G. (1977). Sampling techniques. Third edition.
TEVENS, J. D., R. BONFIL, N. K. DULVY & P. A. WALKER
John Wiley and Sons, New York, New York, USA.
(2000). The effects of fishing on sharks, rays, and chimaeras
D'O
(chondrichthyans), and the implications for marine ecosys-
NGHIA, G., A. TURSI, P. MAIORANO, A. MATARRESE & M.
Panza (1998). Demersal fish assemblages from the bathyal
tem. ICES J. Mar. Sci., 57 : 476-494.
grounds of the Ionian Sea (middle-eastern Mediterranean).
TÅNING, A.V. (1918). Mediterranean Scopelidae. Rep. Danish
Ital. J. Zool., 65 (Suppl.) : 287-292.
Oceanogr. Exped. Med., 1908-1910, 2(5), A(7) : 154p.
D'ONGHIA, G., C.-Y. POLITOU, F. MASTROTOTARO, CH. MYTILIN-
TÅNING, A.V. (1923). Lophius. Rep. Danish Oceanogr. Exped.
EOU, & A. MATARRESE (2002). Biodiversity from the upper
Med., 1908-1910, 2(7), A10 : 30p.
slope demersal community of the eastern Mediterranean :
WHITEHEAD, P.J. P., M.-L. BAUCHOT, J.-C. HUREAU & J. NIELSEN
preliminary comparison between two areas with and without
(1989). Fishes of the North-eastern Atlantic and the Mediter-
fishing impact. J. Northw. Atl. Fish. Sci., Vol. 31 : 1-11.
ranean. UNESCO. Vols I to III.
Belg. J. Zool., 135 (2) : 235-241
July 2005
Deep-water decapod crustacean fauna of the Eastern
Ionian Sea
Chrissi-Yianna Politou1, Porzia Maiorano2, Gianfranco D'Onghia2 and Chryssi Mytilineou1
1 Hellenic Centre for Marine Research, Aghios Kosmas, 16604 Helliniko, Greece
2 Department of Zoology, University of Bari, Via Orabona 4, 70125 Bari, Italy
Corresponding author : C.-Y. Politou, e-mail : c-y@ncmr.gr
ABSTRACT. Knowledge on the decapod crustacean fauna of the E. Ionian Sea was enriched by a recent research
program, carried out in deep waters (300-1200 m) of its northern part. The data were collected from a total of 148
hauls towed during four experimental trawl surveys from September 1999 to September 2000.
Thirty nine decapod species were identified, of which eight were Dendrobranchiata and 31 Pleocyemata (17 Caridea,
9 Brachyura, 3 Anomura, 1 Astacideum and 1 Palinurum). Concerning their depth distribution, 30 species were found
in the depth zone 300-500 m, with Parapenaeus longirostris being the most abundant species. Plesionika heterocarpus
and P. antigai followed in terms of abundance. Of the 27 species caught in the zone 500-700 m, Aristaeomorpha folia-
cea and Plesionika martia were the most abundant. In the zone 700-900 m, 19 species were found and Aristaeomorpha
foliacea with Aristeus antennatus were the most numerous. Finally, the 18 decapod species encountered in the zone
900-1200 m showed low abundance, and Sergia robusta with Polycheles typhlops predominated in numbers.
From the identified decapods, Acanthephyra eximia, Philoceras echinulatus and Pontophilus norvegicus were men-
tioned for the first time in the E. Ionian Sea. Some other species, such as Acanthephyra pelagica, Geryon longipes,
Munida tenuimana, Paromola cuvieri, Parthenope macrochelos, Pasiphaea multidentata, Plesionika narval, Polyche-
les typhlops, Sergestes arachnipodus and Sergestes arcticus have been reported for the area only in the gray literature.
Additionally, new depth distribution records for the Mediterranean were obtained for some species.
KEY WORDS : Decapoda, deep-water, Ionian See, Mediterranean.
INTRODUCTION
(Fig. 1) using two chartered commercial trawlers. The
gear used was a commercial bottom trawl with a cod end
The literature on the decapod crustacean fauna of the
mesh size of 20 mm (side). The vertical and horizontal
Eastern Ionian Sea (Greece) is limited comparing to that
opening of the trawl were estimated, using a remote
referring to other Greek seas and more specifically to the
acoustic sensing system attached to the gear, as 1.5 m and
Aegean Sea (e.g. THESSALOU-LEGAKIS & ZENETOS, 1985 ;
17 m respectively at a towing speed of 2.4 knots. The ran-
THESSALOU-LEGAKIS, 1986 ; D'UDEKEM D'ACOZ, 1995).
dom stratified sampling design was applied using depth
The systematic investigation of the decapod fauna of the
for the stratification of the study area. Three depth zones
Greek waters in the Ionian Sea has started quite recently
were defined, 300-500 m, 500-700 m and 700-900 m.
in the framework of larger projects (MEDITS projects
Some additional experimental hauls were carried out in
1994-2001) or in restricted areas of the Ionian Sea,
the depth zone 900-1200 m. A total of 148 hauls were car-
always at depths not exceeding 800 m ("Deep Water Fish-
ried out. The tow duration was 30 minutes for depths
eries" and RESHIO projects). Some information,
<500 m and one hour for depths >500 m. After each haul,
obtained during the MEDITS project, is given by POLITOU
catches were identified to species level. Species abun-
et al. (1998, 2000).
dance was recorded on board. The mean abundance in
The aim of the present work is to enrich the knowledge
number of individuals per fishing hour (CPUE) was esti-
on the decapod crustacean fauna of the Eastern Ionian Sea
mated for each depth zone as :
with information obtained in the framework of the project
CPUE=SNn/Stn
INTERREG Italy-Greece, which was carried out in deep
waters (300-1200 m) of its northern part. This informa-
where SNn=sum of individuals of a species in the n
tion concerns the decapod faunistic composition, the spe-
hauls carried out in the depth zone and Stn=sum of fish-
cies depth distribution, their frequency of occurrence and
ing time of the n hauls in the depth zone.
abundance.
RESULTS
MATERIALS AND METHODS
Thirty nine decapod species were identified in total in
Sampling took place in depths from 300 to 1200 m of
the study area. Of them eight were Dendrobranchiata and
the Greek Ionian Sea during four experimental trawl sur-
31 Pleocyemata (17 Caridea, 9 Brachyura, 3 Anomura,
veys carried out from September 1999 to September 2000
1 Astacideum and 1 Palinurum) (Table 1).
236
Chrissi-Yianna Politou, Porzia Maiorano, Gianfranco D'Onghia and Chryssi Mytilineou
Fig. 1. Map of the study area showing the sampling stations.
Thirty species were found in the depth zone 300-500 m
DISCUSSION
(6 Dendrobranchiata and 24 Pleocyemata : 14 Caridea,
6 Brachyura, 2 Anomura, 1 Astacideum and 1 Palinurum).
Parapenaeus longirostris was the most important species,
Including results from the present study, the number of
since it presented a remarkably high frequency of occur-
known decapods from the Ionian Sea has now reached 82
rence and abundance (Fig. 2). Although different species,
species. Of the identified decapods, Acanthephyra eximia,
such as Plesionika antigai, P. gigliolii, P. heterocarpus,
Philoceras echinulatus and Pontophilus norvegicus are
Nephrops norvegicus, Munida rutllanti, P. edwardsii and
reported for the first time in the E. Ionian Sea. Acanthep-
Chlorotocus crassicornis, were also found frequently, only
hyra eximia was found in waters deeper than 800 m,
which were not investigated earlier. Only one specimen of
P. heterocarpus, P. antigai and P. edwardsii were worth a
Philoceras echinulatus was caught in a single station.
mention in terms of their abundance.
Finally, only one specimen of Pontophilus norvegicus
was found in a deep station (965 m). Some other species,
Of the 27 species caught in the zone 500-700 m, six
such as Acanthephyra pelagica, Geryon longipes, Munida
were Dendrobranchiata and 21 Pleocyemata : 9 Caridea,
tenuimana, Paromola cuvieri, Parthenope macrochelos,
7 Brachyura, 3 Anomura, 1 Astacideum and 1 Palinurum.
Pasiphaea multidentata, Plesionika narval, Polycheles
P. martia was present in all stations, whereas other highly
typhlops, Sergestes arachnipodus and Sergestes arcticus,
occurring species were, in order of importance, Polyche-
have been reported for the area only in the gray literature
les typhlops, Aristaeomorpha foliacea, P. acanthonotus,
(Deep Water Fisheries technical report, unpublished data ;
P. gigliolii, P. longirostris, N. norvegicus and P. antigai.
D'ONGHIA et al., 2001 ; POLITOU et al., 2001). Most of
Aristaeomorpha foliacea and Plesionika martia were
them are also uncommon species or mainly found in the
dominant in terms of abundance.
two deepest strata. The two commercial deep-water
shrimps Aristaeomorpha foliacea and Aristeus antenna-
In the zone 700-900 m, 19 species were found (7 Dend-
tus that were absent from the list of POLITOU et al. (1998)
robranchiata and 12 Pleocyemata : 7 Caridea, 3 Brachy-
were found during the surveys of the Deep Water Fisher-
ura, 1 Astacideum and 1 Palinurum). Many species, such
ies project and later in the framework of the MEDITS
as A. foliacea, Polycheles typhlops, Aristeus antennatus,
project (KAPIRIS et al., 1999 ; KAPIRIS & THESSALOU-
P. martia, Sergia robusta and P. acanthonotus, showed
LEGAKI, 2001 ; PAPAKONSTANTINOU & KAPIRIS, 2001 ;
high frequency of occurrence. However, their abundance
CAU et al., 2002). Most of the decapod species found in
was generally low with A. foliacea followed by Aristeus
the present study, with the exception of Acanthephyra
eximia, Aegaeon lacazei, Munida rutllanti, Paromola
antennatus being the most numerous.
cuvieri, Philoceras echinulatus, Plesionika edwardsii,
Plesionika narval and Pontophilus norvegicus, were also
Finally, of the 18 decapod species encountered in the
found in the SE Adriatic Sea, which is adjacent to the E.
zone 900-1200 m, six were Dendrobranchiata and 12
Ionian (VASO & GJIKNURI, 1993 ; UNGARO et al., 1999 ;
Pleocyemata : 7 Caridea, 4 Brachyura and 1 Palinurum. S.
MARSAN et al., 2000). Comparing data from the rest of the
robusta was the most frequently occurring species fol-
Greek waters (Aegean and Cretan Sea) reveals that all the
lowed by A. antennatus, P. typhlops, Acanthephyra pelag-
species found in the present study, with the exception of
ica, Pasiphaea multidentata, Sergestes arachnipodus,
Pontophilus norvegicus and Sergestes arachnipodus,
Acanthephyra eximia and P. acanthonotus. Although,
have been reported in the existing literature for these
Sergia robusta and Polycheles typhlops predominated in
areas (KOUKOURAS et al., 1992, 1997, 1998, 2000 ; KALLI-
numbers, their abundance was remarkably low.
ANIOTIS et al., 2000).
Deep-water decapod crustacean fauna of the Eastern Ionian Sea
237
TABLE 1
List of decapod species collected in the E. Ionian Sea with species depth range and frequency of occurrence (%) per depth stratum.
Depth strata (m)
Depth range (m)
300-500
500-700
700-900
900-1200
No. of hauls
45
52
38
13
Dendrobranchiata
Aristaeomorpha foliacea (Risso, 1827)
388-1047
2.2
88.5
94.7
15.4
Aristeus antennatus (Risso, 1816)
480-1171
2.2
53.8
89.5
76.9
Gennadas elegans (Smith,1882)
1082-1192
15.4
Parapenaeus longirostris (Lucas, 1846)
288-840
93.3
57.7
10.5
Sergestes arcticus Kröyer, 1855
700-1192
2.6
23.1
Sergestes arachnipodus (Cocco, 1832)
318-1171
2.2
5.8
10.5
46.2
Sergia robusta (S.I. Smith, 1882)
480-1192
2.2
23.1
63.2
84.6
Solenocera membranacea (Risso, 1816)
322-823
6.7
1.9
2.6
Pleocyemata
Anomura
Munida intermedia A. Milne Edwards & Bou-
328-503
11.1
1.9
vier, 1899
Munida rutllanti Zariquiey Alvarez, 1952
300-533
37.8
3.8
Munida tenuimana G.O. Sars, 1872
518-518
1.9
Astacidea
Nephrops norvegicus (Linnaeus, 1758)
317-700
42.2
57.7
2.6
Brachyura
Bathynectes longipes (Risso, 1816)
620
1.9
Bathynectes maravigna (Prestandrea, 1839)
322-1003
6.7
23.1
13.2
15.4
Calappa granulata (Linnaeus, 1758)
302-553
8.9
1.9
Geryon longipes A. Milne Edwards, 1881
644-965
1.9
7.9
7.7
Macropipus tuberculatus (Roux, 1830)
343-462
11.1
Macropodia longipes A. Milne Edwards &
340-1003
2.2
7.7
Bouvier, 1899
Monodaeus couchii (Couch, 1851)
460-965
2.2
1.9
7.7
Paromola cuvieri (Risso, 1816)
597-742
7.7
2.6
Parthenope macrochelos (Herbst, 1790)
302-582
11.1
1.9
Caridea
Acanthephyra eximia S.I. Smith, 1886
897-1047
2.6
38.5
Acanthephyra pelagica (Risso, 1816)
480-1192
2.2
15.8
61.5
Aegaeon lacazei (Gourret, 1887)
340-464
17.8
Alpheus glaber (Olivi, 1792)
373
2.2
Chlorotocus crassicornis (Costa, 1871)
300-614
35.6
3.8
Pasiphaea multidentata Esmark, 1866
518-1171
9.6
28.9
53.8
Pasiphaea sivado (Risso, 1816)
377-1082
6.7
23.1
10.5
7.7
Philoceras echinulatus (M. Sars, 1861)
407
2.2
Plesionika acanthonotus (Smith, 1882)
317-1047
13.3
86.5
44.7
30.8
Plesionika antigai Zariquiey Alvarez, 1955
288-700
77.8
34.6
Plesionika edwardsii (Brandt, 1851)
305-700
35.6
23.1
2.6
Plesionika gigliolii (Senna, 1903)
300-700
75.6
61.5
Plesionika heterocarpus (Costa, 1871)
300-676
64.4
23.1
Plesionika martia (A. Milne Edwards, 1883)
317-1085
15.6
100
65.8
15.4
Plesionika narval (Fabricius, 1787)
356
2.2
Pontophilus norvegicus (M. Sars, 1861)
965
7.7
Pontophilus spinosus (Leach, 1815)
322-460
8.9
Palinura
Polycheles typhlops Heller, 1862
328-1171
17.8
98.1
92.1
76.9
238
Chrissi-Yianna Politou, Porzia Maiorano, Gianfranco D'Onghia and Chryssi Mytilineou
Others (14)
300-500 m
500-700 m
Plesionika martia
Others (17)
(11)
Polycheles
typhlops (12)
Plesionika
heterocarpus (270)
Parapenaeus
Aristaeomorpha
longirostris (432)
foliacea (357)
Plesionika
martia (344)
Plesionika gigliolii
(31)
Munida rutllanti (19)
Plesionika edwardsii
Plesionika
Pasiphaea
(60)
acanthonotus
sivado (42) Aristeus
(17)
antennatus (19)
Plesionika antigai
Plesionika
Parapenaeus
(133)
edwardsii (29)
longirostris (17)
700-900 m
900-1200 m
Others (14)
Polycheles
r2
typhlops (9)
Polycheles typhlops
Others (9)
(10)
Aristaeomorpha
foliacea (70)
Aristeus antennatus
(28)
Sergia robusta
(15)
Fig. 2. Relative abundance of decapod species per depth stratum in the E. Ionian Sea. In parenthesis the mean number of
specimens caught per hour (CPUE) is given.
Although comparison of abundance with other studies
reported for the Mediteranean. Concerning Bathynectes
is difficult, because of the different types of gear and
longipes, it is considered a scarce species (ABELLO et al.,
methods used, the general fauna distribution is quite simi-
2001) and no depth distribution ranges are given for it.
lar to that found in other Mediterranean areas (ABELLO et
A remarkable difference between the Greek Ionian Sea
al., 1988 ; CARTES & SARDA, 1992, 1993 ; CARTES et al.,
1994 ; U
and the westernmost areas of the Mediterranean is the
NGARO et al., 1999 ; ABELLO et al., 2002). A
high abundance of A. foliacea in the former area and its
dominance of shrimps in all depth strata observed in the
absence or scarcity in the latter ones. This difference may
present study was mentioned also by POLITOU et al.
(1998) for the slope of the region. In relation to the west-
be explained by the vulnerability of this species to over-
fishing (O
ern Mediterranean, our results are more comparable with
RSI RELINI & RELINI, 1985 ; MATARRESE et al.,
1997) in combination with the fishing pressure exercised
those of ABELLO et al. (1988), whose samples were col-
lected with a commercial trawl. A high presence of small
in the deep waters of the westernmost areas. Such pres-
sure is negligible in the Greek Seas. Furthermore, differ-
species, such as Calocaris macandreae Bell, 1864 and
ent hydrological conditions (i.e. salinity and temperature)
Processa nouveli Al-Adhub & Williamson, 1975, was
mentioned by some authors (C
between areas are reported as factors affecting the distri-
ARTES & SARDA, 1992 ;
bution of the species along the Mediterranean (R
C
ELINI &
ARTES et al., 1994) for these depths in the Catalan Sea.
O
These species were not found in the present study. This
RSI RELINI, 1987 ; MURENU et al., 1994). A. foliacea is
discrepancy can be explained by the smaller cod-end
considered to prefer waters of relatively high salinity and
temperature such as those of the E. Ionian Sea in compar-
mesh size of the experimental trawl used in the former
ison to the westernmost Mediterranean areas (T
studies. Furthermore, although the species depth distribu-
HEO-
tion observed in the present study was generally within
CHARIS et al., 1993 ; HOPKINS, 1985).
the ranges given in the literature for the Mediterranean, in
A decline in the number of decapod species and of their
some cases new depth records were obtained (Table 2).
abundance with depth was evident in the Ionian Sea. This
More specifically, the distribution of the species Aristaeo-
pattern was observed also in the western Mediterranean
morpha foliacea, Bathynectes maravigna, Monodaeus
(CARTES & SARDA, 1992, 1993 ; CARTES, 1993). The
couchii, Parapenaeus longirostris, Pasiphaea sivado,
upper part of the slope (300-700 m) was characterized by
Plesionika antigai, Plesionika edwardsii and Plesionika
a relatively high number of species found in abundance.
martia was extended into waters deeper than those
Parapenaeus longirostris, Aristaeomorpha foliacea, Ple-
Deep-water decapod crustacean fauna of the Eastern Ionian Sea
239
sionika martia, P. heterocarpus, P. antigai and P. edward-
tus) were found in non negligible quantities in the zone
sii were the species that displayed the highest abundance
700-900 m. Given the relatively constant environmental
values, and most of them are of important commercial
conditions in these depths and the high oligotrophy of the
value. Below 700 m of depth, the number of species and
area (STERGIOU et al., 1997), the main factor determining
mainly their abundance decreased sharply, although red
this reduction with depth seems to be the low trophic
shrimps (mainly A. foliacea and secondarily A. antenna-
resource availability.
TABLE 2
Depth range of occurrence for decapod species in the Mediterranean updated with the results of the present study.
Species
Depth range (m)
Min
Max
Acanthephyra eximia
421 (ABELLO et al., 2002)
2261 (CARTES, 1993)
Acanthephyra pelagica
176 (ABELLO et al., 1988)
2261 (CARTES, 1993)
Aegaeon lacazei
13 (ABELLO et al., 1988)
1041 (CARTES, 1993)
Alpheus glaber
3 (ABELLO et al., 1988)
871 (ABELLO et al., 1988)
Aristaeomorpha foliacea
150 (MATARRESE et al., 1995)
1047 (present study)
Aristeus antennatus
150 (MATARRESE et al., 1995)
2200 (SARDÀ et al., 1994)
Bathynectes longipes
620 (present study)
Bathynectes maravigna
245 (ABELLO et al., 2001)
1003 (present study)
Calappa granulata
25 (ABELLO et al., 2002)
712 (ABELLO et al., 2002)
Chlorotocus crassicornis
55 (ABELLO et al., 1988)
742 (PIPITONE & TUMBIOLO, 1993)
Gennadas elegans
250 (KOUKOURAS et al., 1997)
2261 (CARTES, 1993)
Geryon longipes
439 (ABELLO et al., 1988)
1895 (CARTES, 1993)
Macropipus tuberculatus
48 (ABELLO et al., 1988)
748 (ABELLO et al., 1988)
Macropodia longipes
18 (ABELLO et al., 1988)
748 (ABELLO et al., 1988)
Monodaeus couchii
44 (ABELLO et al., 2002)
965 (present study)
Munida intermedia
35 (ABELLO et al., 1988)
871 (ABELLO et al., 1988)
Munida rutllanti
40 (ABELLO et al., 2002)
587 (ABELLO et al., 2002)
Munida tenuimana
286 (ABELLO et al., 2002)
1899 (CARTES, 1993)
Nephrops norvegicus
58 (ABELLO et al., 2002)
871 (ABELLO et al., 1988)
Parapenaeus longirostris
26 (PIPITONE & TUMBIOLO, 1993)
840 (present study)
Paromola cuvieri
267 (PIPITONE & TUMBIOLO, 1993)
795 (PIPITONE & TUMBIOLO, 1993)
Parthenope macrochelos
20 (ABELLO et al., 1988)
655 (PIPITONE & TUMBIOLO, 1993)
Pasiphaea multidentata
128 (ABELLO et al., 1988)
2261 (CARTES, 1993)
Pasiphaea sivado
33 (ABELLO et al., 1988)
1082 (present study)
Philoceras echinulatus
55 (ABELLO et al., 1988)
871 (ABELLO et al., 1988)
Plesionika acanthonotus
141 (PIPITONE & TUMBIOLO, 1993)
1680 (CARTES, 1993)
Plesionika antigai
98 (ABELLO et al., 2002)
700 (present study)
Plesionika edwardsii
250 (GARCIA-RODRIGUEZ et al, 2000)
700 (present study)
Plesionika gigliolii
101 (ABELLO et al., 1988)
748 (ABELLO et al., 1988)
Plesionika heterocarpus
45 (ABELLO et al., 2002)
699 (ABELLO et al., 1988)
Plesionika martia
165 (ABELLO et al., 1998)
1085 (present study)
Plesionika narval
5 (THESSALOU-LEGAKI et al., 1989)
510 (POLITOU et al., 2000)
Polycheles typhlops
241 (ABELLO et al., 2002)
1927 (CARTES, 1993)
Pontophilus norvegicus
366 (ABELLO et al., 1998)
2261 (CARTES, 1993)
Pontophilus spinosus
69 (ABELLO et al., 2002)
871 (ABELLO et al., 1998)
Sergestes arachnipodus
279 (ABELLO et al., 2002)
1224 (CARTES, 1993)
Sergestes arcticus
160 (ABELLO et al., 2002)
2188 (CARTES, 1993)
Sergia robusta
220 (ABELLO et al., 1998)
2261 (CARTES, 1993)
Solenocera membranacea
3 (ABELLO et al., 1998)
871 (ABELLO et al., 1998)
ACKNOWLEDGEMENTS
The project "INTERREG II Greece-Italy" was financially
supported by the Greek Ministry of Economy and the EC.
The authors are grateful to their colleagues who participated
REFERENCES
in the sampling cruises and in the laboratory work. Special
thanks to Stefanos Kavadas and John Dokos for their help in the
ABELLO, P., A. CARBONELL & P. TORRES (2002). Biogeography
data base management and the map drawing.
of epibenthic crustaceans on the shelf and upper slope off the
240
Chrissi-Yianna Politou, Porzia Maiorano, Gianfranco D'Onghia and Chryssi Mytilineou
Iberian Peninsula Mediterranean coasts : implications for the
Aegean Sea. In : POLITOU, C.-Y., M. STOUMBOUDI & D.
establishment of natural management areas. Sci. Mar., 66
SAKELLARIOU (eds), Proc. 5th Hel. Symp. Oceanogr. & Fish.,
(Suppl. 2) : 183-198.
NCMR, Athens, vol. II : 91-94.
ABELLO, P., N. UNGARO, C.-Y. POLITOU, P. TORRES, E. ROMAN, P.
KOUKOURAS, A., C. DOUNAS, M. TÜRKAY & E. VOULTSIADOU-
RINELLI, P. MAIORANO & G. NORRITO (2001). Notes on the
KOUKOURA (1992). Decapod crustacean fauna of the Aegean
distribution and biology of the deep-sea crab Bathynectes
Sea : new information, check list, affinities. Senckenber-
maravigna (Brachyura : Portunidae) in the Mediterranean
giana marit., 22(3/6) : 217-244.
Sea. Hydrobiologia, 449 : 187-192.
KOUKOURAS, A., A. KALLIANIOTIS & D. VAFIDIS (1998). The
ABELLO, P., F.J. VALLADARES & A. CASTELLON (1988). Analysis
decapod crustacean genera Plesionika Bate (Natantia) and
of the structure of decapod crustacean assemblages off the
Munida Leach (Anomura) in the Aegean Sea. Crustaceana,
Catalan coast (North-West Mediterranean). Mar. Biol., 98 :
71(6) : 714-720.
39-49.
MARSAN, R., N. UNGARO, C.A. MARANO & M.C. MARZANO
CARTES, J.E. (1993). Deep-sea decapod fauna of the Western
(2000). Remarks on distribution and fishery biology of some
Mediterranean : bathymetric distribution and biogeographic
Plesionika species (Decapoda, Pandalidae) in the southern
aspects. Crustaceana, 65(1) : 29-40.
Adriatic basin (Mediterranean Sea). In : VON VAUPEL KLEIN,
CARTES, J.E., J.B. COMPANY & F. MAYNOU (1994). Deep-water
J.C. & F.R. SCHRAM (eds), The biodiversity crisis and
decapod crustacean communities in the Northwestern
Crustacea : Proceedings of the fourth international crusta-
Mediterranean : influence of submarine canyons and season.
cean congress, Amsterdam, July 20-24, 1998, volume 2,
Mar. Biol., 120 : 221-229.
A.A. Balkema, Rotterdam : 763-769.
CARTES, J.E. & F. SARDA (1992). Abundance and diversity of
MATARRESE, A., G. D'ONGHIA, M. DEFLORIO, M. PANZA & G.
decapod crustaceans in the deep-Catalan Sea (Western Med-
COSTANTINO (1995). Recenti acquisizioni sulla distributione
iterranean). J. nat. Hist., 26 : 1305-1323.
batimetrica di Aristaeomorpha foliacea e Aristeus antenna-
CARTES, J.E. & F. SARDA (1993). Zonation of deep-sea decapod
tus (Crustacea, Decapoda) nel Mar Ionio. Biol. Mar. Medit.,
fauna in the Catalan Sea (Western Mediterranean). Mar.
2(2) : 299-300.
Ecol. Prog. Ser., 94 : 27-34.
MATARRESE, A., G. D'ONGHIA, A. TURSI & P. MAIORANO (1997).
CAU A., A. CARBONELL, M.C. FOLLESA, A. MANNINI, G.
Vulnerabilità e resilienza in Aristaeomorpha foliacea (Risso,
NORRITO, L. ORSI-RELINI, C.-Y. POLITOU, S. RAGONESE & P.
1827) e Aristeus antennatus (Risso, 1816) (Crostacei, Deca-
RINELLI (2002). MEDITS-based information on the deep-
podi) nel Mar Ionio. S.It.E. Atti, 18 : 535-538.
water red shrimps Aristaeomorpha foliacea and Aristeus
MURENU, A., D. CUCCU, C. FOLLESA, A. SABATINI & A. CAU
antennatus (Crustacea : Decapoda : Aristeidae). Sci. Mar.,
(1994). The occurrence of Aristaeomorpha foliacea in Sar-
66 (Suppl.2) : 103-124.
dinia waters. In : BIANCHINI, M. & S. RAGONESE (eds), Life
D'ONGHIA, G., C.-Y. POLITOU, F. MASTROTOTARO, CH. MYTILIN-
cycles and fisheries of the deep-water red shrimps Aristaeo-
EOU & A. MATARRESE (2001). Biodiversity from the upper
morpha foliacea and Aristeus antennatus. N.T.R.-I.T.P.P.
slope demersal community of eastern Mediterranean : pre-
Special publication, 3 : 49.
liminary comparison between two areas with and without
ORSI RELINI, L. & G. RELINI (1985). The red shrimps fishery in
fishing impact. NAFO Scientific Council Meeting-September
the Ligurian Sea : Mismanagement or not ? FAO Fish. Rep.,
2001, SCR Doc. 01/135 : 11p.
336 : 99-106.
GARCIA-RODRIGUEZ, M., A. ESTEBAN & J.L. PEREZ GIL (2000).
PAPACONSTANTINOU, C. & K. KAPIRIS (2001). Distribution and
Considerations on the biology of Plesionika edwardsi
population structure of the red shrimp (Aristeus antennatus)
(Brandt, 1851) (Decapoda, Caridea, Pandalidae) from exper-
on an unexploited fishing ground in the Greek Ionian Sea.
imental trap catches in the Spanish western Mediterranean
Aquat. Living Resour., 14 : 303-312.
Sea. Sci. Mar., 64(4) : 369-379.
PIPITONE, C. & M.L. TUMBIOLO (1993). Decapod and stomato-
HOPKINS, T.S. (1985). Physics of the Sea. In : MARGALEF, R.
pod crustaceans from the trawlable bottoms of the Sicilian
(ed.), Key environments : Western Mediterranean, Pergamon
Channel (Central Mediterranean Sea). Crustaceana, 65(3) :
Press, New York : 100-125.
358-364.
KALLIANIOTIS, A., K. SOPHRONIDIS, P. VIDORIS, A. TSELEPIDES
POLITOU, C.-Y., M. KARKANI & J. DOKOS (1998). Distribution of
(2000). Demersal fish and megafaunal assemblages on the
decapods caught during MEDITS surveys in Greek waters.
Cretan continental shelf and slope (NE Mediterranean) : sea-
In : BERTRAND, J.A. & G. RELINI (eds), Demersal resources
sonal variation in species density, biomass and diversity.
in the Mediterranean, Ifremer-Actes de Colloques, 26 : 196-
Progress in Oceanography, 46 : 429-455.
207.
KAPIRIS, K.& M. THESSALOU-LEGAKI (2001). Sex-related varia-
POLITOU, C.-Y., M. KARKANI & J. DOKOS (2000). Distribution of
bility of rostrum morphometry of Aristeus antennatus
pandalid shrimps in Greek waters (Ionian Sea and Argosa-
(Decapoda : Aristeidae) from the Ionian Sea (Eastern Medi-
ronikos). In : LABROPOULOU, M. (ed.), Proc. 6th Hel. Symp.
terranean, Greece). Hydrobiologia, 449 : 123-130.
Oceanogr. & Fish., NCMR, Athens, vol. II : 61-66.
KAPIRIS, K., M. THESSALOU-LEGAKI, M. MORAITOU-APOSTOLO-
POLITOU, C.-Y., S. KAVADAS, CH. MYTILINEOU, A. TURSI, G.
POULOU, G. PETRAKIS & C. PAPACONSTANTINOU (1999). Pop-
LEMBO & R. CARLUCCI (2001). Fisheries resources in the
ulation characteristics and feeding parameters of Aristaeo-
deep waters of eastern Mediterranean (Greek Ionian Sea).
morpha foliacea and Aristeus antennatus (Decapoda :
NAFO Scientific Council Meeting-September 2001, SCR
Aristeidae) from the Ionian Sea (Eastern Mediterranean).
Doc. 01/104, 12p.
In : VON VAUPEL KLEIN, J.C. & F.R. SCHRAM (eds), The bio-
RELINI, G. & L. ORSI RELINI (1987). The decline of red shrimps
diversity crisis and Crustacea : Proceedings of the fourth
stocks in the Gulf of Genoa. Inv. Pesq., 51(suppl. 1) : 245-
international crustacean congress, Amsterdam, July 20-24,
360.
1998, A.A. Balkema, Rotterdam : 177-191.
SARDA, F., J.E. CARTES & W. NORBIS (1994). Spatio-temporal
KOUKOURAS, A., S. DOULGERAKI & M.-S. KITSOS (2000). Notes
structure of the deep-water shrimp Aristeus antennatus pop-
on the vertical distribution of pelagic shrimps (Decapoda,
ulation in the Western Mediterranean. Fish. Bull., 92 :599-
Natantia) in the Aegean Sea. Crustaceana, 73(8) : 979-993.
607.
KOUKOURAS, A., S. DOULGERAKI, M.-S. KITSOS & C. PAPACONS-
STERGIOU, K.I., E.D. CHRISTOU, D. GEORGOPOULOS, A. ZENETOS
TANTINOU (1997). The vertical distribution of the pelagic
& C. SOUVERMEZOGLOU (1997). The Hellenic Seas : Physics,
shrimps (Crustacea, Decapoda, Natantia) of the North
Chemistry, Biology and Fisheries. In : ANSELL, A.D., R.N.
Deep-water decapod crustacean fauna of the Eastern Ionian Sea
241
GIBSON & M. BARNES (eds), Oceanography and Marine
THESSALOU-LEGAKIS, M. & A. ZENETOS (1985). Autoecological
Biology : an Annual Review, UCL Press, 35, 415-538.
studies on the Thalassinidea (Crustacea, Decapoda) of the
THEOCHARIS, A., D. GEORGOPOULOS, A. LASKARATOS & K. NIT-
Patras Gulf and Ionian Sea (Greece). Rapp. Comm. int. Mer
TIS (1993). Water masses and circulation in the central region
Médit., 29(5) : 309-312.
of the Eastern Mediterranean : Eastern Ionian, South Aegean
UDEKEM D' ACOZ, C. D' (1995). Contibution à la connaissance
and Northwest Levantine, 1986-1987. In : ROBINSON, A.R.
des crustacés décapodes helléniques II : Penaeidea,
& P. MALANOTTE-RIZZOLI (eds), Topical studies in Oceanog-
Stenopodidea, Palinuridea, Homaridea, Thalassinidea,
raphy, Part. II. Deep-Sea Res., 40(6) : 1121-1142.
Anomura, et note sur les stomatopodes. Bios (Macedonia,
THESSALOU-LEGAKIS, M. (1986). Preliminary data on the occur-
Greece), 3 : 51-77.
rence of Thalassinidea (Crustacea, Decapoda) in the Greek
UNGARO, N., C.A. MARANO, R. MARSAN, M. MARTINO, M.C.
seas. Biologia Gallo-hellenika, 12 : 181-187.
MARZANO, G. STRIPPOLI & A. VLORA (1999). Analysis of
THESSALOU-LEGAKI, M., A. FRANTZIS, K. NASSIOKAS & S. HATZ-
demersal species assemblages from trawl surveys in the
INIKOLAOU (1989). Depth zonation in a Parapandalus narval
South Adriatic Sea. Aquat. Living Resour., 12(3) : 177-185.
(Crustacea, Decapoda, Pandalidae) population from Rhodos
VASO, A. & L. GJIKNURI (1993). Decapod crustaceans of the
Island, Greece. Estuar. coast. shelf Sci., 29 : 273-284.
Albanian coast. Crustaceana, 65(3) : 390-407.
Belg. J. Zool., 135 (2) : 243-246
July 2005
Nesting and hatching success of the sea turtle Caretta
caretta on Marathonissi island (Zakynthos, Ionian Sea,
Greece)
George Skoufas
Technological Educational Institute, Department of Fisheries Technology and Aquacultures, N. Miltiadi 1, GR- 63200, N. Mou-
dania, Greece
Corresponding author : Georges Skoufas, e-mail : gskoufas@hotmail.com
ABSTRACT. Nesting behaviour and hatching success of the sea turtle Caretta caretta (loggerhead) were studied on
Marathonissi island in Zakynthos (Ionian Sea, Greece) during the summer of 1995. On this island there exist two
discrete nesting areas : the North sector and the West sector. Nesting activity was greatest in both sectors during
July. The number of nests was significantly higher in the North sector, whereas remarkably more attempts were
observed in the West sector. Hatching success was also greater in the North sector where there were significantly
more empty eggshells, mark of successful hatching, than in the West sector. Moreover, the number of dead embryos
was significant in the West sector. The current study demonstrates a correlation between the choice of nesting area
and hatching success.
KEY WORDS : Caretta caretta, loggerhead, hatching success, nesting behaviour, sea turtle.
INTRODUCTION
exists between the females' choice of nesting site and the
hatching success.
Caretta caretta (loggerhead or caouanne in French) is
MATERIAL AND METHODS
one of the two common sea turtle species in the East
Mediterranean Sea. The other one is the green turtle, Che-
Laganas bay in Zakynthos is one of the most important
lonia mydas. The reproductive behaviour of loggerhead is
nesting places of the loggerhead C. caretta. The sites of
not so clear while most of the existing data concern its
the present study are located on the beaches of Maratho-
nesting behaviour. C. caretta displays a wide geographi-
nissi island. Seven discrete nesting beaches occur in
cal distribution, encompassing Mexico, Australia and the
Laganas bay : Laganas, Kalamaki, Theiafi, Sekania,
Mediterranean Sea. A typical characteristic of the logger-
Daphni, Gerakas and Marathonissi. Marathonissi is a
head's nesting behaviour is migration (MEYLAN et al.,
small, uninhabited island in Laganas Bay, allowing all
1983; HUGHES, 1989; LIMPUS et al., 1992). Scientific data
field observations to be carried without interference from
obtained via tagging of the females during nidification
anthropogenic activities (i.e. tourism). The nesting area of
(MARGARITOULIS, 1988a) as well as by examination of the
Marathonissi is dense and for the needs of this study was
mitochondrial DNA (BOWEN et al., 1994; LAURENT et al.,
subdivided into two sectors : West sector and North sector
1993) enhance the hypothesis of the existence of different
(Fig. 1).
populations of C. caretta. The age of reproductive matu-
One nesting area, that of the North sector, was 200 m
rity is 22-26 years for the West Atlantic population (KLIN-
long and closer to the sea, comprising rocks and stones.
GER & MUSIK, 1995) and more than 30 years for the Aus-
Halophytic vegetation began at a distance of 150 m from
tralian loggerhead population (BOWEN et al., 1994;
the beach. The slope of the infralittoral zone was steep. A
LAURENT et al., 1993). Regarding the present study, the
dense meadow of the phanerogam Posidonia oceanica
population nesting on the Greek beaches passes the win-
was located close to the beach. The other area, that of the
ter months in Tunisia (LAURENT & LESCURE 1994). Only
West sector, was 150 m long and narrower than that of the
the adult females leave the sea so as to nest and their cor-
North sector. A dense meadow of the phanerogam Cymo-
responding behavioural patterns have been described
docea nodosa at 0-2 m, as well as a deeper meadow of P.
(HAILMAN & ELOWSON, 1992). During the same reproduc-
oceanica characterized the infralittoral zone. All field
tive period the females nest more than once (HUGHES et
observations and consequent data collections were con-
al., 1967; WORTH & SMITH, 1976). Several studies have
ducted between 28 May and 25 September 1995.
examined the factors implicated in juvenile mortality
The first part of the study involved observation of the
(PRITCHARD 1980; YNTEMA & MROSOVSKY, 1980;
adult females, coming out to the beach so as to nest. The
BLANCK & SAWYER, 1981; YNTEMA & MROSOVSKY, 1982;
term "nest" was utilized to characterize the successful
WYNKEN et al., 1988; HAYS & SPEAKMAN, 1993). The aim
oviposition along with all the distinctive behavioural pat-
of the current study is to investigate whether a correlation
terns. Occasionally, exit of the females from the sea was
244
George Skoufas
followed by unsuccessful oviposition, attributed to vari-
The second phase of the current study focused on
ous reasons. In this case, the term "attempt" was used to
hatching. The data demonstrated in Table 1 were col-
characterize such a behaviour. Observations were direct
lected via excavation of the nests five days after the last
during the night watch, when animals were tagged, and
hatchlings' tracks. The time of the incubation period was
indirect every morning via examination of tracks on the
practically the same in both sectors (t-impaired : t=1.1,
beach.
d.f.=16, p>0.05). The mean incubation period was
72.0±8.4 days (n: 8) in the North sector and 66.0±13.4
days (n: 10) in the West sector. Another parameter not
significantly different in the two sectors was the depth of
the nest (t-impaired : t=-0.293, d.f. =37, p>0.05). The
mean depth of the nest was 48.2±7.2 cm in the North sec-
tor and 48.8±5.3 cm in the West sector. As observed, all
the hatchlings did not leave the nest at the same time. The
period between the first and the last tracks was similar in
the two sectors (t-impaired : t=-0.251, d.f.=37, p>0.05).
Mean time of the hatchlings' exit from the nest was
5.2±1.8 days in the North sector and 5.4±3.8 days in the
West sector.
sector NORTH
70
63
sector WEST
60
53
47
50
40
28
30
21
number of nests
16
20
10
Fig. 1. Map of the nesting areas on Marathonissi island in
Zakynthos (A), Laganas bay with the potential nesting beaches
0
(B) and Marathonissi nesting beaches (C).
JUNE
JULY
AUGUST
Fig. 2. Number of nests in the North and West sectors on Mar-
Similar methods were applied during the second part of
athonissi island (Zakynthos, Greece) during the summer of
the study to estimate the hatching success, including indi-
1995.
rect observations of the tracks of hatchlings and direct
observations after excavation of the nests. Each nest exca-
vation was carried out five days after the last tracks.
200
sector NORTH
175
Empty eggshells were characterized as successful hatch-
sector WEST
180
ing.
160
140
116
RESULTS
120
100
Nests and attempts were observed in both sectors. One
80
48
51
of the factors influencing the hatching success was the
number of attempts
60
37
36
distance of the nest from the sea. This distance was signif-
40
icantly greater in the North sector (24.6±7.6 m; n : 131)
20
than in the West sector (20.9±7.5m; n : 97) (t-impaired :
0
t=3.582, d.f. =226, p<0.001). As shown in Fig. 2, more
JUNE
JULY
AUGUST
nests were present in both sectors during July. However,
Fig. 3. Number of attempts in the North and West sectors on
the number of nests was significantly higher in the North
Marathonissi island (Zakynthos, Greece) during the summer of
sector than in the West sector during July (t-impaired :
1995.
t=1.935, d.f. =73, p<0.05). Based on Fig. 3, the number
of attempts was also greater in both sectors during July. In
After nest excavation it was found that the number of
contrast to nests, significantly more attempts were
eggs per nest was also not significantly different (t-
observed in the West sector than in the North sector dur-
impaired : t=-0.541, d.f. =37, p>0.05) in the two sectors.
ing July (t-impaired: t=3.426, d.f. =, p<0.05). As a gen-
The mean number of eggs per nest was 127.4±19.8 in the
eral remark the percentage of nests was higher in the
North sector and 122.6±33.7 in the West sector. Never-
North sector (39% nests/61% attempts) than in the West
theless the number of empty eggshells, mark of successful
sector (27% nests/73% attempts) during the nesting
hatching, was greater in the North sector than in the West
phase.
sector (t-impaired : t=-2.498, d.f. =37, p<0.05). Moreover
Nesting and hatching success of Caretta caretta
245
there were more dead embryos in the West sector than in
Sand temperature is one of the factors that influence
the North sector (t-impaired : t=-2.828, d.f. =37, p<0.05).
the sex ratio and probably the hatchlings' mortality
Finally, the numbers of unfertilized eggs (t-impaired : t=-
(MROSOVSKY & YNTEMA, 1980). Temperature is also the
1.532, d.f. =37, p>0.05), of live embryos (only one,
major factor that affects the incubation period. The two
found in the West sector), of live hatchlings (t-impaired :
nesting sectors in Marathonissi did not exhibit remarkable
t=0.082, d.f. =37, p>0.05) and of dead hatchlings (t-
differences in the incubation time (HAYS et al., 1992).
impaired : t=-1.544, d.f. =37, p>0.05) did not show sig-
Hatchling emergence, as has been observed in Cephalo-
nificant differences between the two sectors.
nia, is an asynchronous phenomenon (HOUGHTON &
HAYS, 2001). In other nesting areas shorter incubation
TABLE 1
periods than that in Marathonissi have been observed,
such as 55 days in Kiparissia (Greece) (MARGARITOULIS,
Hatching parameters in the North and West sectors on Maratho-
1988), 47.9 days in Cyprus (BRODERICK & GODLEY, 1994;
nissi island (Zakynthos, Greece) during the summer of 1995.
GODLEY et al., 2001), 54 days in Israel (SILBERSETEIN &
Sector NORTH
Sector WEST
DMI'EL, 1991) and 55.0 in Turkey (BARAN & TURKOZAN,
(n :19)
(n :20)
1996).
min-
min-
mean±SD
mean±SD
max
max
Other studies on the neighboring island of Cephalonia
Number of eggs per nest
127.4±19.8
88-172
122.6±33.7
76-238
demonstrate a positive linear relationship between the
Empty eggshells
97.7±33.6
13-143
70.9±33.3
14-120
number of clutches into which eggs could be divided and
Unfertilised eggs
24.3±24.0
0-86
39.3±36.0
0-125
the total time spent by nesting turtles on the beach, and
Dead embryos
2.3±2.9
0-10
6.5±7.6
0-28
hence a negative relationship between the time invested
Dead hatchlings
1.6±2.1
0-7
4.3±7.2
0-26
on the beach per egg and clutch size (HAYS & SPEAKMAN,
Live hatchlings
1.5±2.7
0-11
1.4±2.9
0-11
1991). Body size of females was also positively related to
the number of eggs laid and clutch volume (HAYS &
SPEAKMAN, 1992).
DISCUSSION
The current study showed that in both nesting areas in
Marathonissi a correlation existed between the number of
Marathonissi island is one of the most important nest-
nests, the number of hatchlings and their mortality. Most
ing beaches of Zakynthos, where, during the summer of
likely factors, such as sand granulometry, humidity, pres-
1995, 228 nests on 350 meters of beach length were
ence of rocks and stones e.t.c. influence both nesting
observed. During this study the curve length of the adult
choice and successful incubation. Nevertheless, further
females C. caretta was measured. Such results confirm
investigation is required to establish the significance of
the hypothesis of the presence of different loggerhead
this correlation, as well as to demonstrate the factors
populations in the East Mediterranean Sea. The females
affecting nesting choice and hatching success.
of the loggerhead's Cyprus population are larger in size
than the Greek ones (BRODERICK & GODLEY, 1996). In
ACKNOWLEDGEMENTS
support of the morphological parameters the same
hypothesis was confirmed by the examination of mito-
chondrial DNA (B
I would like to thank S.T.P.S, G. Pologiorgis, Ch. Irvine and
OWEN et al., 1994; LAURENT et al.,
D. Dimopoulos for applied help.
1993).
The observations of the present study have shown that
REFERENCES
the period with the greatest nesting activity was July.
Similar data were collected in Cyprus (DEMETROPOULOS
BARAN, I., & O. TYRKOZAN (1996). Nesting activity of the Log-
& HADJICHRISTOPHOROU, 1989). However, respective
gerhead turtle Caretta caretta on Fetihye beach, Turkey in
observations on Turkish beaches in Mugla (ERK'AKAN,
1994. Chelon Conserv. Biol., 2(1) : 93-96.
1993) and in Fetihye (BARAN & TÜRKOZAN, 1996) have
BLANK, C., E., & R. H. SANWER (1981). Hatcheries practices in
demonstrated that the month with the highest nesting
relation to early embryology of the loggerhead sea turtle
activity is June.
Caretta caretta (Linné). J. Exp. Biol. Ecol., 49 : 163-177.
BOWEN, B., W., N. KAMEZAKI, C. J. LIMPUS, G. R. HUGHES, A.
The mean number of eggs per nest observed in Mara-
B. MEYLAN & J. C. AVISE (1994). Global phylogeography of
thonissi was 127.4 in the North sector and 122.6 in the
the loggerhead turtle (Caretta caretta) as indicated by mito-
West sector. These values were higher than those meas-
chondrial DNA haplotypes. Evolution, 48(6) : 1820-1828.
ured in Kyparisisa (Greece) 117.7 eggs/nest, (MARGARI-
BRODERICK, A., C., & B. GODLEY (1994). Marine turtles in
TOULIS, 1988b), in Israel 82 eggs/nest (SILBERSETEIN &
northern Cyprus : results from Glasgow University Turtle
DMI'EL, 1991), in Turkey 82.9 eggs/nest (BARAN &
Conservation Expeditions, 1992-1993. Mar. Turtle Newsl.,
TÜRKOZAN, 1996) and in Cyprus 61.0 eggs /nest (Broder-
67 : 8-11.
ick & Godley, 1994). Based on bibliographic data, hatch-
BRODERICK, A., C., & B. J. GODLEY (1996). Population and nest-
lings show high mortality and it is estimated only 1/1,000
ing ecology of the green turtle Chelonia mydas and the log-
survives to adulthood (F
gerhead turtle, Caretta caretta, in northern Cyprus. Zoology
RAZER, 1986). It can be assumed
in the Midle East, 12 : 1-48.
that the increased number of eggs/nest in Marathonissi
DEMETROPOULOS, A., & M. HADJICHRISTOPHOROU (1989). Sea
demonstrates a reproductive strategy. Such a hypothesis is
turtle conservation in Cyprus. Mar. Turtle Newsl., 44 : 4-6.
enhanced by the percentage of successful hatching in both
ERK'AKAN, F., (1993). Nesting biology of the loggerhead turtles
sectors of Marathonissi (empty eggshells/total of number
Caretta caretta L. on Dalyan beach, Mugla-Turkey, Biol.
eggs), being only 65.1%.
Conserv., 66 : 1-4.
246
George Skoufas
FRAZER, N., B., (1986). Survival from egg to adulthood in
populations méditerranéenne et atlantique d'une tortue
declining population Caretta caretta. Herpetologica, 42 :
marine (Caretta caretta) à l'aide d'un marqueur mitochon-
47-55.
drial. C. R. Acad. Sci. Paris, Science de la vie / Life sciences,
GODLEY, B., J., A. C. BRODERICK, J. R. DOWNIE, F. GLEN,
316 : 1233-1239.
J. D. HOUGHTO, I. KIRKWOOD, S. REECE & G. C. HAYS
LAURENT, L., & J. LESCURE (1994). L'hivernage des tortues
(2001). Thermal conditions in nests of loggerhead turtles
Caouannes Caretta caretta (L) de Méditerranée occidentale.
evidence suggesting female skewed sex ratios of hatchling
Rapp. Comm. Int. Mer Medit., 32(1) : 240.
production in Mediterranean. Journ. Exp. Mar. Biol. And
LIMPUS, C., J., J. D. MILLER, C.J. PARMENTER, D. REIMER,
Ecol., 263(1) : 45-63.
N. MCLACHALND & R. WEB (1992). Migration of green
HAILMAN, J., P., & A. M. ELOWSON (1992). Ethogramm of the
(Chelonia mydas) and loggerhead (Caretta caretta) turtles to
nesting female loggerhead (Caretta caretta). Herpetologica,
and from eastern Australian roockeries. Wildilife Research,
48(1) : 1-30.
19 : 347-358.
HAYS, G., C., & J. R. SPEAKMAN (1991). Reproductive invest-
MARGARITOULIS, D. (1988a). Post-nesting movement of logger-
ment and optimum clutch size of loggerhead sea-turtles
head sea turtles tagged in Greece. Rapp. Com. Int. Mer
(Caretta caretta). Journ. Animal. Ecol., 60(2) : 455-462.
Medit., 31(2) : 284.
HAYS, G., C., & J. R. SPEAKMAN (1992). Clutch size for Mediter-
MARGARITOULIS, D., (1988b). Nesting of the loggerhead sea tur-
ranean loggerhead turtles (Caretta caretta). Journ. Zool.,
tle Caretta caretta on the shore of Kypasrisia Bay, Greece in
226 :321-327.
1987. Mésogeé, 48 : 59-65.
HAYS, G., C., & J. R. SPEAKMAN (1992). The pattern of emer-
M
gence by loggerhead turtle (Caretta caretta) hatchlings on
EYLAN, A., B., K. A. BJORNDAL & B. J. TURNER (1983). Sea
Turtle nesting at Melbourne Beach, Florida. II. Post nesting
Cephalonia, Greece. Herpetologica, 48(4) : 396-401.
movements of Caretta caretta. Biol. Conserv., 26 : 79-90.
HAYS, G., C., & J. R. SPEAKMAN (1993). Nest placement by log-
gerhead turtles Caretta caretta. Animal Behaviour, 45 : 47-
MROSOVSKY, N., & C. L. YNTEMA (1980). Temperature depend-
53.
ence of sexual differenciation in sea turtles : implications for
H
conservation practices. Biolog. Conserv., 18 : 271-280.
OUGHTON, J., D., R., & G. C. HAYS (2001). Asynchronous
emergence by loggerhead (Caretta caretta) hatchlings.
PRITCHARD, P., C., H., (1980). The conservation of sea turtles :
Naturwssenscaften, 88(3) :133-136.
Practices problems. Am. Zool., 20 : 609-617.
HUGHES, G., R., (1989). Sea Turtles. In: A. I. L. PAYN and
SILBERSETEIN A. & L. DMI'EL (1991). Loggerhead sea turtle
J. M. GRAWFORD eds. Oceans of Life of South Africa. Vlae-
nesting in Israel. Mar. Turtle Newsl., 53 : 17-18.
berg, Cape Town : 230-243.
YNTEMA, C., L., & N. MROSOVSKY (1982). Critical periods and
HUGHES, G., R., A. J. BASS, & M. T. MENTIS (1967). Further
pivotal temperatures for sexual differentiation in loggerhead
studies on marine turtles in Togaland. Lammergeyer, 7 :1-55.
sea turtles. Canad. Journ. Zool., 60 : 1012-1016.
KLINGER, R., C., & J. A. MUSIK (1995). Age and growth of log-
WORTH, D., W., & J. B. SMITH (1976). Marine turtle nesting on
gerhead turtles which inhabit Chesapeak Bay. Copeia
Hutchimson Island Florida, in 1973. Fla. Mar. Res. Publ. 18.
LAURENT, L., J. LESCURE, L. EXCOFFIER, B. BOWEN, M.
WYNKEN, J., T., J. BURKE, M. SALMON & D. K. PEDERSEN
DOMINGO, M. HADJICHRISTOPHOROU, L. KORNARAKI & G.
(1988). Egg failure in natural and relocated sea turtle nests.
TRABUCHET (1993). Etude génétique des relations entre les
J. Herpetol., 22 : 88-96.
Belg. J. Zool., 135 (2) : 247-252
July 2005
Marked interannual differences in reproductive para-
meters and daily egg production of anchovy in the
northern Aegean Sea
Stylianos Somarakis
University of Patras, Department of Biology, GR-26500 Patra, Greece
Corresponding author : S. Somarakis, e-mail : somarak@upatras.gr
ABSTRACT. In the present paper, an overview of the application of the Daily Egg Production Method (DEPM) to
the northern Aegean Sea anchovy stock is presented, and reproductive parameters are compared in the framework
of ambient oceanographic regimes. The DEPM was applied twice : in June 1993 and June 1995. Data collection was
based on bongo-net ichthyoplankton surveys and concurrent adult surveys onboard the commercial fishing fleet.
Revised, more precise estimates of the daily egg production are presented based on the inclusion of both eggs and
yolksac stages in the estimation procedure (fit of single embryonic mortality curves). Remarkable between-years
differences in the daily egg production, batch fecundity and spawning frequency were found. These parameters
were significantly higher in June 1993 than in June 1995. In June 1993, waters were colder, less saline and richer in
zooplankton compared to 1995. Adult somatic condition and egg size were also higher in June 1993 than in 1995.
These findings emphasize the importance of adult prey availability in determining anchovy egg production.
KEY WORDS : Engraulis encrasicolus, Aegean Sea, DEPM, Reproduction
INTRODUCTION
MATERIAL AND METHODS
The Daily Egg Production Method (DEPM) is an ich-
The biomass model
thyoplankton-based method for estimating biomass of
The spawning stock biomass was estimated according
fish stocks and monitoring trends in fish abundance
to the model (LASKER, 1985) :
(HUNTER & LO, 1997). It has been developed for fishes
B = (k . P . A . W)/(R . F . S)
that have indeterminate annual fecundity, like most clupe-
oids (LASKER, 1985), and has been applied to a variety of
where, B = spawning stock biomass in metric tons, k =
anchovy and sardine species and stocks (ALHEIT, 1993 ;
conversion factor from grams to metric tons, P = daily
HUNTER & LO, 1997). Besides biomass estimation, the
egg production (number of eggs per sampling unit, m2), A
application of DEPM provides regional time series on
= total survey area (in sampling units, m2), W = average
important biological variables of fish stocks, which can
weight of mature females (grams), R = sex ratio (fraction
lead to new insights into the reproductive biology of mul-
of mature females by weight), F = batch fecundity (mean
tiple spawning fishes, particularly when such variables
number of eggs per mature females per spawning), and S
can be compared and subsequently related to environ-
= fraction of mature females spawning per day (spawning
mental regimes.
frequency).
Based on the delta method, the approximate variance of
This paper presents an overview of the application of
the biomass estimate is a function of sample variances
DEPM to the anchovy [Engraulis encrasicolus (Linnaeus,
and covariances (LASKER, 1985) :
1758)] stock of the northern Aegean Sea (Greece, Eastern
Mediterranean). The DEPM has been applied to anchovy
2
2
2
2
2
stocks in the Western Mediterranean (G
VarB B (CV ( P) + CV W
( ) + CV (F) + CV (S) + 2COVS)
ARCIA & PALOM-
ERA, 1996), the northern Aegean Sea (SOMARAKIS & TSI-
where CV denotes coefficient of variation, and COVS is
MENIDES, 1997 ; SOMARAKIS et al., 1997 ; SOMARAKIS,
the sum of terms involving covariances.
1999), the central Aegean and Ionian Seas (SOMARAKIS et
al., 2002) and the Sicilian channel (QUINTANILLA & GAR-
Survey description
CIA, 2001). The applications in the northern Aegean Sea
were carried out in June 1993 and June 1995 and were
Two oceanographic surveys were carried out during
largely experimental, based on bongo-net larval surveys
June 1993 and June 1995 in the northern Aegean Sea
coupled with concurrent adult surveys onboard the com-
(eastern Mediterranean). The sampling scheme was based
mercial purse seine fleet. Reproductive parameter esti-
on transects spaced approximately ten nautical miles
mates are compared in an effort to understand the repro-
apart and stations located at five nautical-mile intervals
ductive strategy of the species.
on each transect (Fig. 1). The same stations (n=111) were
248
Stylianos Somarakis
sampled in both years. The total survey area was
profiles of temperature and salinity) were performed at
17396 km2. Plankton and hydrographic sampling (vertical
each station.
Fig. 1. Northern Aegean Sea. Map of the surveyed area showing the location of sampling stations. : plank-
ton and hydrographic samples. : 1993, purse seine samples. : 1995, purse seine samples.
: 1993, pelagic
trawl samples.
: 1995, pelagic trawl samples.
A 60-cm bongo-net sampler was used on both cruises.
(YSI) and larvae with traces of brown pigment or brown-
Mesh sizes on the sampler were 335 and 250 microns.
ish eyes (YSII). Eggs and yolk-sac larvae at each devel-
The 0.250-mm mesh net is considered to completely
opmental stage were counted and their abundance stand-
retain anchovy eggs and larvae (SOMARAKIS et al., 1998 ;
ardized to number per m2. Zooplankton displacement
SOMARAKIS, 1999). Tows were double oblique and the
volume (ZDV) was measured for each sampling site from
volume filtered was determined by a calibrated flowmeter
the catch of the 0.250-mm mesh bongo net (SMITH &
(Hydrobios) in the mouth of each of the nets. The depth of
RICHARDSON, 1977). ZDV values were standardized to
the sampler could be monitored onboard at any time dur-
ml/m2. At each station, the major and minor diameters of
ing the tow by means of a recording depthmeter attached
ten anchovy eggs were measured to the nearest 0.02 mm
to the sampler. Maximum tow depth and volume of water
using an ocular micrometer. Egg volumes were calculated
filtered were subsequently used to standardize catches to
using the formula for a prolate spheroid.
numbers per m2. More details are provided in SOMARAKIS
Processing of an adult sample in the laboratory con-
et al. (1998).
sisted of measuring length and weight (both total and
Adult samples were collected on board the commercial
gonad free weight), and sexing of all or at least 50 fish per
purse seine fleet of Kavala and Moudania and were repre-
sample. Correction factors were applied to convert forma-
sentative of the fishing grounds (Fig. 1). Additional sam-
lin-weight to wet weight and the total weight of hydrated
ples of hydrated females were obtained by means of a
females was corrected for the increase in weight due to
pelagic trawl operated from the research vessel
hydration of the ovaries (SOMARAKIS et al., 2002). Rela-
"PHILIA", during the daily spawning interval (21:00-
tive condition factor of females (BOLGER & CONNOLLY,
2:00). Fish were fixed onboard immediately after collec-
1989) was calculated. The gonads of ten females per sam-
tion, using 15 l jars filled with 10% neutral-buffered for-
ple were randomly selected and subjected to histological
malin. Each sample consisted of random collection of
analysis. All macroscopically detected hydrated or run-
1.5-2 kg of anchovies.
ning females were measured and their gonads weighed
and preserved in formalin for subsequent histological and
Laboratory procedures
batch fecundity analysis. The hydrated oocyte method
Anchovy eggs and larvae were sorted from the plank-
was used for batch fecundity measurements (HUNTER et
ton samples. The eggs were staged using the eleven -
al., 1985).
stages system of MOSER & AHLSTROM (1985). Yolk-sac
Spawning frequency (S), i.e., the fraction of mature
larvae were staged into larvae with un-pigmented eyes
females spawning per night, was assessed by the postovu-
Anchovy egg production
249
latory follicles (POFs) method. The three types of POFs
for eggs and yolk-sac larvae, and we included both in sin-
described by HUNTER & MACEWICZ (1985) (Day-0, Day-
gle embryonic mortality curves (LO et al., 1996 ; SOMAR-
1, and Day-2+ POFs) were also observed in our histologi-
AKIS et al., 2002). The estimate of daily production of
cal preparations and were used in classifying ovaries as to
eggs was derived by regressing the counts of embryos
the date of spawning (SOMARAKIS et al., 2002). Actively
(eggs and yolk sac larvae) on their age using the exponen-
spawning anchovy (hydrated and Day-0 females) are
tial mortality model :
oversampled during the hours of spawning (SOMARAKIS,
P = Pe- Zt
1999 ; SOMARAKIS et al., 2002 and references therein). To
t
overcome this problem, we used samples collected out-
where P = number of embryos at age t produced per
t
side the daily spawning interval, i.e. after 4 :00 a.m., and
day per m2, t = age in days, P = daily egg production per
calculated spawning frequency based on the composite
m2, Z= daily rate of instantaneous embryonic mortality.
fraction of Day-0 and Day-1 spawners, to increase preci-
We used both yolk-sac larvae stages (YSI and YSII)
sion of the spawning frequency estimates (QUINTANILLA
and calculated their duration and age from fertilization
& PEREZ, 2000). Fractions of Day-0 and Day-1 spawners
following methods described in SOMARAKIS et al. (2002).
had the same statistical distributions after 4:00 a.m. (Wil-
The technique to estimate P and Z was weighted non-lin-
coxon paired sample tests, p>0.05).
ear least squares regression. Station weighting factors
were proportional to the station representative area.
Parameter estimation
We used the ratio estimator (PICQUELLE & STAUFFER,
Age of eggs was calculated based on a temperature
1985) for adult parameters W, R, F, and S. Data on the
dependent model of European anchovy developmental
number of eggs per batch (F ) and the ovary free weight
ij
rate (REGNER, 1985), the station surface temperature (5
(W*) recorded for the hydrated females were used to fit a
ij
m), peak spawning time (midnight ; SOMARAKIS, 1999),
linear model :
and time of tow (LO, 1985). Procedures of ageing
F = a + bW*
anchovy eggs are described in S
ij
ij
OMARAKIS et al. (2002).
The regressions were forced through zero because a
The estimation of the daily egg production generally
was not significantly different from zero at the 0.05 level.
involves the fit of an exponential mortality model to the
abundance-at-age egg data set (PICQUELLE & STAUFFER,
1985). A preliminary estimate of the daily egg production
RESULTS
for the 1993 survey, based on the egg data set (SOMARAKIS
& TSIMENIDES, 1997) was problematic and highly uncer-
The distribution and abundance of eggs and yolk-sac
tain because of inadequate numbers of positive egg data.
larvae are presented in Fig. 2. Higher egg concentrations
This was mainly due to the effect of high incubation tem-
were found in the Thracian Sea and Thermaikos Gulf.
peratures and corresponding occurrence of only single or
The surveys did not cover the entire anchovy egg and
two daily cohorts of eggs in the samples. To increase the
yolksac distribution. Particularly in the Thracian Sea, a
number of age categories for constructing the mortality
significant fraction of egg and larval production seemed
curves, we assumed that the mortality rate was the same
to extend offshore as well as in Turkish territorial waters.
1993
1995
Eggs
Eggs
Yolksac larvae
Yolksac larvae
0
10
50
100
500
Fig. 2. Contour maps of anchovy eggs and yolksac larvae abundance (numbers/m2) in June 1993 and June 1995.
250
Stylianos Somarakis
On the basis of the egg distribution pattern and regional
allocation of adult samples (Fig. 1) the surveyed area was
stratified into two sub-regions : the Eastern region (Thra-
cian Sea and Kavala - Stratum I) and the Western region
(Thermaikos and Chalkidiki Gulfs - Stratum II). The
DEPM was applied separately for the two strata. Statum I
covered 9354 km2 and stratum II 8042 km2. Parameter
and biomass estimates are given in Table 1.
TABLE 1
Biomass and parameter estimates of the DEPM applied to the
northern Aegean anchovy stock in June 1993 and June 1995.
Stratum I comprised the Thracian Sea and Kavala Gulf. Stratum
II comprised the Thermaikos and Chalkidiki Gulfs (see Fig. 1).
Coefficients of variation are given in parentheses.
Stratum I
Strarum II
(East)
(West)
Fig. 3. Batch fecundity (number of eggs)-on-gonad free
weight relationsships. : 1993, Stratum I. : 1995, Stratum I.
Parameter
1993
1995
1993
1995
: 1995, Stratum II. : 1995, Stratum II. Zero-forces regres-
Daily egg Production (P,
109.22
25.71
87.19
19.75
sion lines for 1993 (solid line) and 1995 (broken line) are also
eggs/m2)
drawn.
(0.27)
(0.24)
(0.33)
(0.26)
Instantaneous embryonic
0.17
0.52
1.26
0.54
mortality rate (Z)
Mean egg size and somatic condition of adult females
(0.36)
(0.40)
(0.39)
(0.48)
were also significantly higher (t-tests, p<0.05) in June
Average weight of mature
24.89
25.65
20.88
22.72
1993 than in 1995 (Fig. 4). Concurrently, waters were
females (W, g)
colder, less saline and richer in zooplankton during 1993
(0.03)
(0.03)
(0.03)
(0.03)
than in 1995 (p<0.05, Fig. 4).
Weight specific sex ratio (R)
0.51
0.51
0.60
0.61
(0.05)
(0.08)
(0.05)
(0.03)
DISCUSSION
Average batch fecundity (F,
12451
7781
10474
5128
number of eggs)
(0.05)
(0.06)
(0.04)
(0.10)
The applications of the DEPM to the northern Aegean
Sea anchovy stock were largely experimental, based on
Fraction of mature females
0.29
0.15
0.26
0.13
data from bongo-net larval fish surveys and opportunistic
(S)
(0.21)
(0.11)
(0.20)
(0.23)
adult sampling on board the commercial fleet (SOMAR-
AKIS & TSIMENIDES, 1997). A concurrent total biomass
Spawning biomass (B, met-
14002
10282
9030
8948
survey carried out by acoustic methods during June 1995
ric tons)
(0.34)
(0.22)
(0.38)
(0.36)
(MACHIAS et al., 1997), gave the estimates of 26671
(CV=0.19) and 17929 metric tons (CV=0.15) for the east-
ern and the western stratum respectively. The surveyed
Estimates of the daily egg production (P) and adult
area during the DEPM applications did not cover the
reproductive parameters (F, S) indicated a higher spawn-
entire spawning area of the anchovy stock, thus, the cal-
ing intensity in 1993 than in 1995. Batch fecundity (F )-
culated biomass values are underestimates of the total
ij
on-gonad free weight (W *) relationships were :
spawning biomass of this stock. However, sampling pro-
ij
cedures and subsequent laboratory and analytical meth-
Stratum I : 1993 : F = 563 W*, r2 = 0.63, n=25
ij
ij
ods were identical between 1993 and 1995 and allowed
the between-year comparison of the estimated parame-
1995 : F = 325 W*, r2 = 0.22, n=70
ij
ij
ters. The robustness of the DEPM to opportunistic adult
Stratum II :1993 : F = 558 W*, r2 = 0.81, n=43
sampling is discussed elsewhere (SOMARAKIS & TSIME-
ij
ij
NIDES, 1997).
1995 : F = 242 W*, r2 = 0.27, n=15.
ij
ij
In comparing the DEPM parameters between 1993 and
Analysis of covariance showed that, for each year sepa-
1995 in relation to various environmental and fish param-
rately, the between-strata difference in batch fecundity
eters, we observed that adult food availability (mesozoo-
was not significant (P>0.05). However, the slope of the
plankton) was higher in the cooler and fresher waters of
regression line (relative batch fecundity, eggs/g) was sig-
1993 (Fig. 4). Concurrently, female anchovies were in
nificantly higher in 1993 than in 1995 (P<0.05, Fig. 3).
better condition, producing numerous large-sized eggs at
Spawning frequency estimates (Table 1) indicated a mean
a higher spawning frequency (short interspawning inter-
inter-spawning interval (=1/S) of 3.5 days and 3.9 days,
val). These observations are consistent with a ration-
for Stratum I and II respectively, during June 1993, and
related reproductive tactic in anchovy (SOMARAKIS et al.,
6.7 days and 7.7 days for the same areas in June 1995.
2000).
Anchovy egg production
251
ALMATAR, 1989 ; TSURUTA & HIROSE, 1989). In south-
African pilchard, females spawn an increased number of
4.3
eggs in response to better fish condition, irrespective of
temperature (LE CLUS, 1992). Energy allocated to multi-
2.63
)
4.2
ple spawnings is derived primarily from feeding rather
(
K
n
than from energy reserves in many small pelagic fishes
io
it 2.6
(e.g. WRIGHT, 1990 ; WANG & HOUDE, 1994). In other
4.1
nd
cases, spawning is related to both dietary intake and nutri-
o
C
tional status of the fish (e.g. MILTON et al. 1994). A link
2.57
4
between adult forage and spawning is reasonable because
of the high energetic cost of frequent spawnings and the
0.21
0.21
fact that areas suitable for planktivorous adults are also
)
3
suitable for the planktivorus larvae (BLAXTER & HUNTER,
1982). Recently, PEEBLES et al. (1996) showed that bay
(
mm
e
anchovy's egg and subsequent larval production is related
0.2
i
z
0.19
s
to adult as well as larval prey availability. They suggested
g
that hatching larvae are likely to be associated with ele-
Eg
vated nauplius densities because of the inherent interde-
0.19
0.17
pendence between copepod life stages.
Applying the terminology of life history evolution
27
34
(STEARNS, 1992), SOMARAKIS et al. (2000) labeled plank-
)2
tivorous short-lived small pelagic species, such ancho-
l
/
m
vies, as `income breeder', spawning soon after energy for
(
m
23
n
egg production becomes available. These species are
t
o
24
k
characterized by substantial, ration-related variations in
n
a
19
batch fecundity, spawning frequency, and, probably, in
oopl
egg size. In multiple-spawning fish, batch fecundity does
Z
15
14
not necessarily increase to compensate for smaller egg
sizes (LE CLUS, 1992).
24
25
The DEPM applications to the northern Aegean Sea
anchovy stock are the first to be made in the eastern Med-
C)
o (
iterranean. The comparison of parameter estimates in
r
e
u
relation to environmental regimes highlights the impor-
22
at
24
tance of inter-annual variations in the oceanographic hab-
er
p
m
itat in controlling anchovy egg production.
e
T
20
23
REFERENCES
34
ALHEIT, J. (1993). Use of the daily egg production method for
estimating biomass of clupeoid fishes : a review and evalua-
)
u
s
tion. Bull. Mar. Sci., 53(2) : 750-767.
35.5
(
p
BAGENAL, T.B. (1973). Fish fecundity and its relation with stock
33
i
ty
and recruitment. Rapp. P.-v. Reun. Cons. int. Explor. Mer.,
l
i
n
164 : 186-198.
Sa
BAILEY, R.S. & S.M. ALMATAR (1989). Variation in the fecun-
32
34.5
dity and egg weight of herring (Clupea harengus L.). Part II.
1993
1995
1993
1995
Implications for hypotheses on the stability of marine fish
populations. J. Cons. int. Explor. Mer., 45 : 125-130.
Year
BLAXTER, J.H.S. & J.R. HUNTER (1982). The biology of clupeoid
fishes. Adv. Mar. Biol., 29 : 1-223.
Fig. 4. Averages and 95% confidence intervals
BOLGER, T. & P.L. CONNOLLY (1989). The selection of suitable
per area (East: Stratum I West: Stratum II) and
indices for the measurement and analysis of fish condition.
year (1993-1995) for relative condition factor
J. Fish. Biol., 34 : 171-182
(K), mean egg size, zooplankton displacement
GARCIA, A. & I. PALOMERA (1996). Anchovy early life history
volume, surface temperature (5 m) and surface
and its relation to the surrounding environment in the West-
salinity (5 m).
ern Mediterranean basin. Sci. Mar., 60 (Suppl. 2) : 155-166.
HUNTER, J.R. & B. MACEWITZ (1985). Measurement of spawn-
In short-living multiple spawning fishes, adults may
ing frequency in multiple spawning fishes. In : LASKER, R.
spawn in direct response to temperature and photoperiod,
(eds), An Egg Production Method for Estimating Spawning
however, there are examples that minimum forage be
Biomass of Pelagic Fish : Application to the Northern
Anchovy, Engraulis mordax. NOAA Tech. Rep. NMFS, 36 :
required for the onset of spawning, despite ample fat
79-93.
stores (BLAXTER & HUNTER, 1982). Several studies indi-
HUNTER, J.R. & N.C.H. LO (1997). The daily egg production
cate a ration-related variation in size-specific fecundity or
method of biomass estimation : some problems and potential
interspawning interval (e.g. BAGENAL, 1973 ; BAILEY &
improvements. In : MOTOS, L. (ed), Improvements of Daily
252
Stylianos Somarakis
Egg Production Method techniques. Ozeanografika, 2 : 41-
QUINTANILLA L. & N. PEREZ (2000). Spawning frequency of sar-
69.
dine Sardina pilchardus (Walb.) off the Spanish North
HUNTER, J.R., N.C.H. LO & R.J.H. LEONG (1985). Batch fecun-
Atlantic coast in 1997. Fish. Res., 45 : 73-79.
dity in Multiple Spawning Fishes. In : LASKER, R. (ed), An
QUINTANILLA L., & A. GARCIA (2001). Daily egg production
Egg Production Method for Estimating Spawning Biomass
method for estimating Sicilian channel anchovy spawning
of Pelagic Fish : Application to the Northern Anchovy,
biomass in 1998 and 1999. Rapp. Comm. Int. Mer Medit.,
Engraulis mordax. NOAA Tech. Rep. NMFS, 36 : 67-77.
36 : 312.
LASKER, R. (ed) (1985). An Egg Production Method for Estimat-
REGNER, S. (1985). Ecology of planktonic stages of the anchovy
ing Spawning Biomass of Pelagic Fish : Application to the
Engraulis encrasicolus (L. 1758), in the cental Adriatic.
Northern Anchovy, Engraulis mordax. NOAA Tech. Rep.
Acta Adriat., 26(1) : 1-113.
NMFS, 36.
SMITH, P.E. & S.L. RICHARDSON (1977). Standard techniques for
L
pelagic fish eggs and larval surveys. FAO Fish. Tech. Pap.,
E CLUS, F. (1992). Seasonal trends in sea surface temperature,
dry mass per oocyte and batch fecundity of pilchard Sardi-
175 : 1-107.
nops ocellatus in the northern Benguela system. S. Afr. J.
SOMARAKIS, S. & N. TSIMENIDES (1997). A Daily Egg Produc-
mar. Sci., 12 : 123-134.
tion Biomass Estimate of the Northern Aegean anchovy
L
stock. In : MOTOS, L. (ed), Improvements of Daily Egg Pro-
O, N.C.H. (1985). A Model for Temperature-Dependent North-
ern Anchovy Egg Development and an Automated Proce-
duction Method techniques. Ozeanografika, 2 : 133-148.
dure for the Assignment of Age to Staged Eggs. In : L
SOMARAKIS, S. (1999). Ichthyoplankton of the N.E. Aegean Sea
ASKER,
R. (ed), An Egg Production Method for Estimating Spawning
with emphasis on anchovy, Engraulis encrasicolus (L., 1758)
Biomass of Pelagic Fish : Application to the Northern
(June 1993, 1994, 1995, 1996). PhD thesis. University of
Anchovy, Engraulis mordax. NOAA Tech. Rep. NMFS, 36,
Crete.
43-50.
SOMARAKIS, S., B. CATALANO & N. TSIMENIDES (1998). Catcha-
L
bility and retention of larval European anchovy, Engraulis
O, N.C.H., Y.A. GREEN RUIZ, M.J. CERVANTES, H.G. MOSER &
encrasicolus, with bongo nets. Fish. Bull., 96 : 917-925.
R.J. LYNN (1996). Egg production and spawning biomass of
Pacific sardine (Sardinops sagax) in 1994, determined by the
SOMARAKIS, S., C. KOUTSIKOPOULOS, A. MACHIAS & N. TSIME-
daily egg production method. Cal.C.O.F.I. Rep., 37 : 160-
NIDES (2002). Applying the Daily Egg Production Method to
small stocks in highly heterogeneous seas. Fish. Res., 55 :
174.
193-204.
MACHIAS, A., S. SOMARAKIS, M. GIANNOULAKI, L. MANOUSAKIS,
SOMARAKIS, S., A. MACHIAS, A. KAPANTAGAKIS & N. TSIME-
A. KAPANTAGAKIS & N. TSIMENIDES (1997) Estimation of the
NIDES (1997) Application of the Daily Egg Production
northern Aegean anchovy stock in June 1995 by means of
Method (DEPM) for the estimation of the northern Aegean
hydroacoustics. Proceedings of the 5th Panhellenic Sympo-
Sea anchovy stock in June 1995. Proceedings of the 5th Pan-
sium on Oceanography and Fisheries, Vol. 2 : 47-50.
hellenic Symposium on Oceanography and Fisheries, Vol.
MILTON, D.A., S.J.M. BLABER & N.J.F. RAWLINSON (1994).
2 : 43-46.
Reproductive biology and egg production of three species of
SOMARAKIS, S., E. MARAVEYA & N. TSIMENIDES (2000). Multi-
Clupeidae from Kiribati, tropical central Pacific. Fish. Bull.,
species ichthyoplankton associations in epipelagic species :
92 : 102-121.
Is there any intrinsic adaptive function ? Belg. J. Zool., 130
MOSER, H.G. & E.H. AHLSTROM (1985). Staging Anchovy Eggs.
(Suppl. 1) : 125-129.
In : LASKER, R. (ed), An Egg Production Method for Estimat-
STEARNS, S.C. (1992). The evolution of life histories. Oxford
ing Spawning Biomass of Pelagic Fish : Application to the
Univiversity Press, New York.
Northern Anchovy, Engraulis mordax. NOAA Tech. Rep.
TSURUTA, Y. & K. HIROSE (1989). Internal regulation and repro-
NMFS, 36 : 37-41.
duction in Japanese anchovy (Engraulis japonica) as related
PICQUELLE, S.J. & G. STAUFFER (1985). Parameter Estimation for
to population fluctuation. Can. Spec. Pub. Fish. Aquat. Sci.,
an Egg Production Method of Anchovy Biomass Assess-
108 : 111-119.
ment. In : LASKER, R. (ed), An Egg Production Method for
WANG, S.B. & E.D. HOUDE (1994). Energy storage and dynam-
Estimating Spawning Biomass of Pelagic Fish : Application
ics in bay anchovy Anchoa mitchilli. Mar. Biol., 121 : 219-
to the Northern Anchovy, Engraulis mordax. NOAA Tech.
227.
Rep. NMFS, 36 : 7-16.
WRIGHT, S.P. (1990). The reproductive strategy of Stolephorus
PEEBLES, E.B., J.R. HALL & S.G. TOLLEY (1996). Egg production
heterolobus in the south Java Sea. In : BLABER, S.J.M. &
by the bay anchovy Anchoa mitchilli in relation to adult and
J.W. Copland (eds), Tuna baitfish in the Indo-Pacific region,
larval prey fields. Mar. Ecol. Prog. Ser., 131 : 61-73.
Aust. Coun. Int. Agr. Res. Proc., 30 : 83-88.
Belg. J. Zool., 135 (2) : 253-259
July 2005
Some structural and functional characteristics of a soil
nematode community from a Mediterranean grassland
George P. Stamou1, Efi M. Papatheodorou1, Anastasios Hovardas1 and Maria D.
Argyropoulou2
1 Dept. of Ecology, School of Biology, UPB 119, Aristotle University, GR-54124 Thessaloniki, Greece
2 Dept. of Zoology, School of Biology, UPB 134, Aristotle University, GR-54124 Thessaloniki, Greece
Corresponding author : G. P. Stamou, e-mail : gpstamou@bio.auth.gr
ABSTRACT. This paper refers to the effects of large-scale seasonal fluctuations as well as experimentally induced
small-scale variations of soil temperature and moisture on the structural and functional characteristics of a soil nem-
atode community from a Greek Mediterranean grassland. Two levels of soil temperature, with a mean difference of
1.4° C, and two levels of moisture (2.3% difference in water content) were created. The experiment lasted for a six-
month period (from July to December).
All nematode community parameters vary significantly with season, with the exception of the environmental constant
(C ), which reflects the intensity of competition. The Maturity Index (MI) is affected only by seasonally fluctuating
env
soil conditions, while the Plant Parasite Index (PPI) is affected only by the small-scale differences in soil temperature
and moisture. The high value (1.48) of bacterivorous to fungivorous ratio (B/F) indicates mainly bacterial mediated
decomposition, resulting in good soil fertility. The B/F ratio is affected both by large and small-scale changes in soil
conditions. Diversity and richness show dependence on seasonal variations as well as on small changes in temperature,
while no effect of moisture is recorded. The correlations between nematode community parameters, microflora param-
eters and soil nitrogen pools show independence of nematode parameters from soil N-pools (N
and N
) and
organic
inorganic
parameters relating to microflora, as well as strong dependence on microbially-bounded nitrogen.
KEY WORDS : climatic change, Mediterranean-type ecosystems, functional groups, community structure
INTRODUCTION
data regarding the effects of the foreseen global climatic
changes on soil ecosystem components, especially at a
Organic matter transformation and nutrient turnover in
local scale, are missing (BAKONYI & NAGY, 2000). Our
terrestrial ecosystems involve a large array of soil organ-
work was carried out in a Mediterranean grassland and
isms (SWIFT et al., 1979). Among them, nematodes play a
constitutes a part of our contribution to an EU-project,
quite important role in determining soil functioning
entitled «Diversity Effects in Grassland Ecosystems of
(EKSCHMITT et al., 2001), since the major part of nutrient
Europe (DEGREE)» focusing on climatic change effects
interchange in soils is due to the activity of microbial-
on soil nematodes, microbial processes and nutrient trans-
feeding nematodes (GRIFFITHS et al., 1995). Nematofauna
formation patterns. The soil microclimate at each Euro-
has been the target group of different studies aiming to
pean grassland included in this project was experimen-
seek effects associated with changes in organic matter
tally manipulated, according to a common design for all
input (ARMENDARIZ & ARPIN, 1996 ; ARMENDARIZ et al.,
partner countries. The microclimatic changes obtained by
1996 ; FU et al., 2000 ; AKHTAR, 2000), modified micro-
temperature and moisture manipulations in our field site,
bial productivity (SOHLENIUS, 1990 ; GRIFFITHS et al.,
were of a small-scale and could be considered similar to
1994), soil pollution (RUESS et al., 1993 ; KORTHALS et al.,
those predicted by some climate change scenarios for the
1996) etc. Moreover, community diversity indices
Mediterranean region (OSBORNE & WOODWARD, 2001).
together with indices such as the ratio of bacterivorous to
The effects of those small-scale microclimatic changes on
fungivorous nematodes (B/F), the plant parasite (PPI) and
the structural and functional characteristics of the nema-
the maturity (MI) indices, accounting for both quantita-
tode community were explored and compared to the
tive and qualitative ecological aspects of nematode com-
effects of the seasonal changes of temperature and humid-
munities (BONGERS, 1990, PORAZINSKA et al., 1999), have
ity. These latter climatic changes were considered of a
been extensively used for bioindication purposes, relating
large-scale, since the mediterranean climate exhibits a
to the degree of human intervention in agricultural sys-
clear-cut seasonality, characterised by hot-dry summers
tems (FRECKMAN & ETTEMA, 1993), the soil quality
and mild-wet winters. Furthermore, though a full list of
(YEATES & VAN DER MEULEN, 1996) and the recovery
the nematode taxa recorded in our filed site has already
after perturbation (URZELAI et al., 2000).
been given in NAGY & STAMOU (1998), information asso-
In the present work, we used the above mentioned
ciating the nematode community characteristics with soil
parameters of a nematode community in order to assess
biochemical parameters is missing. Thus, in this paper we
the impact of climatic changes on soil dynamics. Indeed,
also tried to correlate the nematode community parame-
254
George P. Stamou, Efi M. Papatheodorou, Anastasios Hovardas and Maria D. Argyropoulou
ters with parameters relating to soil microflora and nitro-
ence (1.4° C on average) was statistically significant
gen pools.
(p<0.05). Regarding moisture levels, the average differ-
ence between dry and wet plots was 2.3% d.w., and this
MATERIAL AND METHODS
difference was highly significant (p<0.01). Thus,
although the experimental modifications of moisture and
Site description
temperature were of small scale, they were not masked by
the seasonal variations of those variables, which were of a
The research site lies at an altitude of 210-215m, 55km
larger scale.
south-east of Thessaloniki (40° 20' N latitude, 23° 12' E
Soil sampling was conducted on a monthly basis for
longitude), and has a south-easterly orientation. It lies on
the 6-month experimental period. On each sampling occa-
a limestone block of Kimmeridgian-Portlandian age, sur-
sion, three random soil cores were taken from the top
rounded by Miocene-Pliocene deposits. The soil is shal-
8 cm of soil of each field plot with a steel cylinder (7 cm
low, discontinuous and generally not more than 10 cm
diameter). The three cores from each plot were unified in
deep. The profiles are classified as lithic leptosols (FAO)
one composite sample, packed in polythene bags, trans-
with a gravely and stony clay-loam texture. Soil particles
ported to the laboratory and stored at 4° C for further
bigger than 2 mm represent 69.46% of fresh weight of
analyses. The composite samples taken from plots of each
soil. Soil organic carbon varies from 4.01 to 5.32% and
treatment were grouped as replicates. In total, 12 compos-
total amount of organic matter from 6.89 to 9.18% dry
ite samples (3 replicate plots x 4 treatments) were taken
matter of soil. The pH (H O) and pH (KCL) is 7.7 and 6.6
2
each month.
respectively.
According to previous data (DIAMANTOPOULOS et al.,
Nematode analyses
1996), the climate of the region is characterized as Medi-
A portion of 100g fresh weight was separated from the
terranean with small amounts of rainfall during the hot
composite soil sample from each plot for the purposes of
summer months. The dry period lasts from mid June to
nematode extraction. Nematodes were isolated using
mid October. Mean annual air temperature and precipita-
Cobb's sieving and decanting method (
tion is 16.03° C and 435.53 mm, respectively.
S'JACOB & VAN
BEZOOIJEN 1984). Nematode extraction through a double
Experimental design and sampling
layer of cotton wool filters lasted for two days. After total
numbers of specimens were counted, nematodes were
The experiment lasted for a six-month period, from
fixed in 4% formalin. Expert assistance was offered by
July to December, during which soil microclimate was
the Hungarian partners of DEGREE for the identification
manipulated in 12 adjacent field plots (1x1m), covered by
of nematodes to genus level and their classification to
the grasses Stipa bromoides (L) Dorf., Aegilops genicu-
feeding types following YEATES et al. (1993). The group
lata (Roth.), Aegilops triuncialis (L.), Avena sterilis (L.),
of plant-feeders was separated into epidermal and rooth-
Brachypodium distachyum (L.) Beauv., Bromus tectorum
air feeding nematodes and plant parasites.
(L.) and Dactylis glomerata (L.) among others (DALAKA
Maturity Index (MI) and Plant Parasite Index (PPI)
2001). In order to modify soil temperature conditions, we
were calculated according to BONGERS (1990), while
used vertical windshields and horizontal transparent
diversity (Shannon-Weaver index) together with evenness
greenhouse roofs (cutting off also precipitation). Soil
and richness were calculated according to PIELOU (1975).
water content was manipulated by weekly irrigation. The
The assessment of genera biomass was based on average
experimental set-up of the whole DEGREE project, com-
body dimensions and was calculated via the formula of
mon for all partner countries, aimed at obtaining different
ANDRASSY (1984). For the assessment of nematode activ-
combinations of soil temperature and water content in the
ity, a model developed by EKSCHMITT et al. (1999) was
field plots, and superimposing them on the local seasonal
used. For the construction of the model, data concerning
variations of these climatic variables. A detailed descrip-
abundance of nematode genera and body dimensions
tion of DEGREE's experimental design is given in
were used. Activity was expressed as released carbon
EKSCHMITT et al. (1999) as well as in BAKONYI & NAGY
mass per hour and g dry mass soil.
(2000).
The environmental constant (C ), which reflects the
The within plots microclimatic conditions were quanti-
env
intensity of competition, was estimated from the rank/
fied by measuring soil temperature and soil water content
abundance plots, as proposed by MAY (1975) and
on a monthly basis for the 6-month experimental period.
MOTOMURA (1932). In a geometric series, the abundance
Temperature was measured by min-max thermometers
of genera ranked from most to least abundant is :
placed 5 cm below surface and left in the field plots for
n = N C (1- C )i-1 [1-(1- C )s]-1
the whole month, while soil water content at each plot
i
env
env
env
was determined by drying 5g of soil at 104° C for 24h and
where n = nb. of individuals in the ith genus, N= total
i
estimating evaporation loss.
nb. of individuals, s= total nb. of genera and C = envi-
env
ronmental constant.
Finally, the experimental manipulations of microcli-
mate resulted in a full factorial scheme of two tempera-
Biochemical analyses
ture (warm, cold) x two moisture (wet, dry) levels. Each
treatment, i.e. each temperature x moisture combination
Ergosterol was used as an index of active fungal bio-
comprised three plots. Average temperature for the whole
mass. It was estimated from 5 g fresh mass soil by means
sampling period was 23.6° C and 25° C in cold and warm
of quantitative HPLC analysis after ethanol extraction
plots respectively. A t-paired test showed that this differ-
(DJAJAKIRANA et al., 1996). For the determination of soil
Characteristics of a soil nematode community
255
microbial-C the fumigation-incubation method of JENKIN-
iation (from 55 to 69%), whereas the opposite held for
SON & POWLSON (1976), with the modifications recom-
parameters related to diversity.
mended by ROSS (1990) for grassland soils, was used. N-
microbial was measured by the method of BROOKES et al.
TABLE 1
(1985). Soil respiration was measured by absorption in
alkali (1 N KOH) followed by titration with 0.1 N HCL
Overall mean values of some structural and functional charac-
after incubation for three days at 10° C (I
teristics of the nematode community as well as some indices
SEMEYER 1952).
Bacterial substrate utilization, which reflects the func-
relating to life history strategies. Values for 95% confidence
tional diversity of the bacterial community, was estimated
limits, minimum, maximum and estimates for the coefficient of
in Gram-negative plates by a modified BIOLOG method
variation are also given
(VAHJEN et al., 1995). Inorganic-N (NO - and NH +) was
3
4
Variable
Mean
Min.
Max. CV%
determined by distillation, while organic-N was assessed
by the Kjeldahl method (ALLEN, 1974).
Abundance (ind./g d.w.)
16.00±2.08
3.01
53.50 55.23
Richness (nb. genera)
21.26±0.70
16.00
27.00 14.11
Diversity
2.56±0.04
2.21
2.97
7.03
RESULTS
Evenness
83.93±0.92
75.41
92.93
4.64
C
0.21±0.01
0.09
0.59 33.00
env
In total 39 nematode genera with an overall mean den-
Biomass (µg f. w./ g d.w.)
12.18±1.83
2.77
41.49 63.79
sity of about 16 ind.g-1 were sampled during the six-
Activity (ng CO -C/g d.w.* h) 4.57±0.74
0.75
17.09 68.92
2
month period. In Table 1 mean values of different nema-
B/F
1.48±0.18
0.18
3.69 53.89
tode community parameters are presented. Parameters
MI
2.33±0.05
2.00
2.92
7.72
related to phenology and activity exhibited the higher var-
PPI
2.47±0.04
2.11
2.94
6.88
TABLE 2
Percentage contribution of the different nematode functional groups to abundance, richness, biomass, activity, MI and PPI.
Variables
Bacterivorous
Fungivorous
Root feeders
Plant Parasites
Predators
Omnivorous
Abundance (ind./g d.w.)
31.36
27.37
17.35
16.52
0.56
6.87
Richness (nb. genera)
32.07
21.67
9.39
20.44
2.55
13.87
Biomass (µg f.w/gd.w.)
18.95
12.06
2.22
5.82
1.10
59.82
Activity (ngCO -C/g d.w. * h)
27.00
17.69
4.73
9.20
1.05
40.32
2
MI
41.40
37.75
1.25
19.55
PPI
41.63
58.19
TABLE 3
Statistically significant effects of seasonal large-scale fluctuation and experimentally created
small-scale variation in soil temperature and moisture conditions on nematode community param-
eters.
Variables
Season
Moisture Temperature
Interactive effect
Abundance (ind./g d.w.)
0.01
0.00
Biomass (µg f.w./g d.w.)
0.05
0.01
0.01
0.01
Diversity
0.05
0.00
Richness (nb. genera)
0.01
0.05
Activity (ngCO -C/g d.w. * h)
0.01
0.05
2
C
0.05
0.00
0.05
env
MI
0.00
PPI
0.00
0.00
B/F
0.05
0.00
In Table 2, the percentage contribution of the different
small-scale effect of our experimental manipulations on
feeding groups to nematode biomass, activity, richness,
the nematode community, we analysed data from the
density, MI and PPI is displayed. Omnivorous nematodes
whole sampling period by a Two-way ANOVA. The
contributed most to biomass and activity, whereas their
experimental temperature and moisture levels were the
contribution to MI value was quite important. Among the
grouping variables, while the month of sampling, which
remaining groups, bacterivorous and fungivorous nema-
accounts for the effect of seasonality, was the blocking
todes contributed more to total density and richness fol-
one. The seasonal effect was significant for all parameters
lowed by plant-parasite and root-hair feeders. Finally,
except C and PPI (Table 3). Higher values for nema-
env
predacious nematodes had the lowest contribution to all
tode abundance, biomass and activity occurred in Sep-
community parameters.
tember in dry-cold samples (Fig. 1). The ratio B/F dis-
played a significant temporal pattern and was
In order to explore the effect of the large-scale seasonal
significantly affected by small-scale differences in soil
changes of soil temperature and moisture as well as the
temperature and moisture (Table 3, Fig. 2). Bacterivorous
256
George P. Stamou, Efi M. Papatheodorou, Anastasios Hovardas and Maria D. Argyropoulou
50
0.45
40
0.40
30
20
0.35
10
Abundance (ind./g)
0.30
0
Jul
Jul
env
Aug
Sep
Oct
Nov
Dec
Aug
Sep
Oct
Nov
Dec
C
0.25
Dry
Wet
0.20
40
0.15
30
0.10
Jul
Jul
Aug
Sep
Oct
Nov
Dec
Aug
Sep
Oct
Nov
Dec
20
Dry
Wet
10
Biomass (mg*10-3/g)
Fig. 3. Estimates of the environmental constant in dry and wet
0
samples plotted against time. Circles and squares correspond to
Jul
Jul
Aug
Sep
Oct
Nov
Dec
Aug
Sep
Oct
Nov
Dec
cold and warm samples respectively.
Dry
Wet
2.8
2.7
12
2.6
2.5
8
PPI
2.4
4
2.3
2.2
Activity (ng CO2-C/g*h)
Jul
Jul
0
Aug
Sep
Oct
Nov
Dec
Aug
Sep
Oct
Nov
Dec
Dry
Wet
Jul
Jul
Aug
Sep
Oct
Nov
Dec
Aug
Sep
Oct
Nov
Dec
2.8
Dry
Wet
2.7
Fig. 1. Abundance, biomass and activity of nematodes in rela-
2.6
tion to time and moisture conditions. Circles and squares corre-
2.5
2.4
spond to cold and warm samples respectively.
MI
2.3
2.2
2.1
3.0
2.0
Jul
Jul
Aug
Sep
Oct
Nov
Dec
Aug
Sep
Oct
Nov
Dec
Dry
Wet
2.5
Fig. 4. PPI and MI values in dry and wet samples plotted
against time. Circles and squares correspond to cold and warm
2.0
samples respectively.
1.5
ited only seasonal fluctuations with higher values in
B/F ratio
August and November (Table 3, Fig. 4). For richness and
1.0
diversity, beyond the seasonal effect, the independent
effect of small-scale differences in temperature was also
0.5
significant. Higher values occurred in the middle of the
sampling period in warm samples (Table 3, Fig. 5).
0.0
Jul
Jul
Aug
Sep
Oct
Nov
Dec
Aug
Sep
Oct
Nov
Dec
Dry
Wet
2.7
25
Fig. 2. Ratio bacterivorous to fungivorous nematodes in dry
and wet samples plotted against time. Circles and squares corre-
spond to cold and warm samples respectively.
2.6
23
nematodes dominated over fungivorous during almost the
2.5
21
whole sampling period especially in dry-warm and in
Diversity
Richness
wet-cold samples. Values of C were controlled by
env
2.4
19
small-scale changes in temperature and moisture. Higher
C values were recorded in wet than in dry and in warm
env
than in cold samples (Table 3, Fig. 3). For PPI, the inde-
2.3
17
pendent effect of small-scale changes in moisture as well
Jul
Jul
Aug
Sep
Oct
Nov
Dec
Aug
Sep
Oct
Nov
Dec
as the interactive effect of temperature x moisture were
Time (months)
Time (months)
highly significant (Table 3, Fig. 4). Higher PPI values
Fig. 5. Shannon diversity and Richness plotted against time.
were recorded in wet than in dry and in dry-warm than in
Circles and squares correspond to cold and warm samples
dry-cold samples. MI was the only parameter that exhib-
respectively.
Characteristics of a soil nematode community
257
No correlation between nematode community parame-
parameters, only N-microbial was correlated positively
ters and parameters associated with soil nitrogen pools
with nematode abundance, richness, biomass and activity.
was revealed (Table 4). Among microbial community
TABLE 4
Correlation of nematode community parameters with parameters relating to soil microflora and nitrogen pools. Only significant values
are figured.
CO
Biolog
C-mic
N-mic
Ergoster.
N-NO
N-NH
N-org
Variables
2
3
4
(mgC/g d.w. *h)
(Ext.650/g d.w.)
(mgC/g d.w.)
(mgN/g d.w.)
(µg/g d.w.)
(mgN/g d.w.)
(mgN/g d.w)
(mgN/g d.w.)
Abundance (ind./g d.w.)
0.34
0.50
Richness (nb. genera)
-0.24
0.31
Diversity
MI
-0.26
PPI
Biomass (µg f.w./g d.w.)
0.45
Activity (ngCO -C/g d.w. * h)
0.37
0.33
2
Cenv
DISCUSSION
activity and consequently no changes either in dominance
or in the ratio persisters/opportunists occur.
The number of nematode genera recorded in the medi-
The effect of the experimentally created small-scale
terranean grassland of our study is comparable with that
changes in soil temperature and moisture was variable.
of other European grasslands (COOK et al., 1992 ; FRECK-
Moisture manipulations proved inadequate to induce sig-
MAN & ETTEMA, 1993 ; HANEL, 1996 ; BONGERS, 1998 ;
nificant changes in MI. This is opposite to suggestions of
BONGERS et al., 1998 ; NAGY, 1998), while nematode den-
PORAZINSKA et al. (1998) for positive correlation between
sity is much lower than that recorded in Hungarian and
nematode MI and irrigation levels. By contrast, C was
env
Germany grasslands subject to similar experimental treat-
significantly affected by such differences. Thus, this
ments (NAGY 1998, BONGERS et al., 1998). MI is lower
parameter proved efficient for indicating effects of small-
and PPI is similar to those recorded in a Spanish Mediter-
scale microclimatic changes, analogous to those of cli-
ranean grassland (URZELAI et al., 2000), while they are
mate change scenarios. Microclimatic manipulations sig-
lower than those recorded in Australian and New Zealand
nificantly affected most other parameters. The tempera-
soils (YEATES, 1996 ; YEATES & VAN DER MEULEN, 1996).
ture effect on nematode community appeared much more
Concerning diversity, its value is comparable to data
pronounced in dry than in wet plots. In dry-cold samples
reported by FRECKMAN & ETTEMA (1993) ; YEATES (1996)
higher values of nematode abundance, biomass and respi-
and URZELAI et al. (2000).
ration were recorded accompanied by low C values.
env
Interpreted in terms of competition, these latter values
The composition of nematode community is typical of
indicate non-effective exploitation of resources. Taking
a dry mediterranean soil. As in Spanish mediterranean
into account that under these conditions PPI values are
grasslands (URZELAI et al., 2000), predators represented a
lower, it is inferred that increased phenological and activ-
small proportion of the community. Bacterivorus and fun-
ity parameters in dry-cold samples result from increased
givorus nematodes had a good contribution to overall
abundance of all nematode groups except persister plant
density, a feature commonly shared by nematode commu-
feeding nematodes. Finally, concerning diversity, it is
nities from dry soils (GRIFFITHS et al., 1995). Contrary to
remarkable that beside temporal variation, diversity com-
coniferous forests where this ratio is much lower than unit
ponents are sensitive also to small-scale changes in tem-
(DE GOEDE et al., 1993), the mean value of the B/F ratio
perature, a fact that was also reported by BAKONYI &
in our site showed bacterial predominance, probably
NAGY (2000) for Hungarian soil nematodes. PATE et al.
reflecting good soil fertility (POPOVICI & CIOBANU, 2000).
(2000) argued that changes in diversity parameters might
Omnivorous feeders made a good contribution to bio-
reflect changes in ecological resilience related to the qual-
mass, activity and MI. Obviously, it is due to weighty per-
ity of soil conditions. Thus, we may infer that in our study
sisters with high metabolic rate.
site most favorable temperature conditions for resilience
Concerning the effects of seasonality, most nematode
occurred in the middle of the sampling period in warm
indices exhibited temporal fluctuations. This is in agree-
plots.
ment with data referring to Netherlands grasslands (VER-
Small-scale changes in temperature and moisture also
SCHOOR et al., 2001). However, as with data from a semi-
influenced the ratio B/F and consequently the outcome of
arid zone in West-Africa (PATE et al., 2000), crucial
the decomposition processes (WASILEWSKA, 1979 ; HEN-
parameters regarding the structure of the nematode com-
DRIX et al., 1986). Bacterial feeders dominated over fun-
munity remained rather invariable in time. Indeed, our
gal feeders in samples from dry-warm and wet-cold plots.
results showed temporal constancy of C and slight tem-
Following P
env
ORAZINSKA et al. (1999) the dominance of
poral variations of MI (in the range 2.20-2.47). Following
bacterial feeders might be related to the quick turnover of
PORAZINSKA et al. (1999) and BONGERS & FERRIS (1999)
the available organic matter in these samples. Moreover,
we can infer that presumably, large seasonal variations of
changing soil conditions result in a switch to a fungal
soil temperature and moisture do not stimulate microbial
pathway probably accompanied by slow rate of decompo-
258
George P. Stamou, Efi M. Papatheodorou, Anastasios Hovardas and Maria D. Argyropoulou
sition. In dry-warm samples higher PPI values were also
forests of Navarra Spain. Fundam. Appl. Nematol., 19 : 561-
recorded. Changes in PPI relate to changes in the soil
577.
nutritional status following modifications in the dynamics
BAKONYI, B. & P. NAGY (2000). Temperature- and moisture-
of vegetation (BONGERS et al., 1997). The higher PPI val-
induced changes in the structure of the nematode fauna of a
ues in dry-warm samples compared to dry-cold ones
semiarid grassland - patterns and mechanisms. Glob.
could be probably attributed to the development of more
Change Biol., 6 : 697-707.
diverse or more favorable, in terms of nutrients, ground
BONGERS, T. (1990). The maturity index, an ecological measure
vegetation (V
of environmental disturbance based on nematode species
ERSCHOOR et al., 2001).
composition. Oecologia, 83 : 14-19.
Analysing DEGREE's data from a geographical-cli-
BONGERS, M. (1998). Nematode fauna of an extensively man-
matic cross-gradient (from Greece to Sweden), EKSCH-
aged wet grassland in the Netherlands. In : DE GOEDE &
MITT et al. (2001) reported significant correlation between
BONGERS (eds), Nematode communities of northern temper-
nematode abundance, biomass, activity and soil nitrogen
ate grassland ecosystems, Giessen, Focus-Verlag, 1-6.
pools. This is not the case with data from the Mediterra-
BONGERS, T. & H. FERRIS (1999). Nematode community struc-
nean grassland of our study. Furthermore, EKSCHMITT et
ture as a bioindicator in environmental monitoring. TREE,
al. (2001) reported richness as the only nematode parame-
14(6) : 224-228.
ter that was correlated with soil microflora parameters.
BONGERS, T., H. VAN DER MEULEN & G. KORTHALS (1997).
Again, this fact is not supported by our results. By con-
Inverse relationship between the nematode maturity index
trast, this paper shows a remarkable correlation between
and plant parasite index under enriched nutrient conditions.
N-microbial and the majority of the nematofauna parame-
Appl. Soil. Ecol., 6 : 195-199.
ters such as biomass, density, activity and richness. More-
BONGERS, M., H. DOGAN, K. EKSCHMITT & R.G.M. DE GOEDE
over, it shows no effect of the microflora characteristics
(1998). Nematode fauna of semi-natural temperate grassland
(biolog, ergosterol) on nematode community. Non corre-
in central Germany. In : DE GOEDE & BONGERS (eds), Nema-
lation between microbivorous nematodes and microflora
tode communities of northern temperate grassland ecosys-
tems, Giessen, Focus-Verlag, 7-14
is often recorded (WARDLE et al. 1995) and it is generally
attributed to non-linear trophic interactions (E
BROOKES, P.C., A. LANDMAN, G. PRUDEN & D.S. JENKINSON
TTEMA et al.
(1985). Chloroform fumigation and the release of soil
1999). According to ANDERSSON (1995), linear trophic
nitrogen : a rapid direct extraction method to measure micro-
synchronization follows environmental disturbances. If
bial biomass nitrogen in soil. Soil Biol. Biochem., 17 : 837-
this holds true, we may infer that the experimentally
842.
induced changes in soil temperature and moisture condi-
COOK, R., K.A. MIZEN, R.A. PLOWRIGHT & P.A. YORK (1992).
tions cannot be considered serious disturbance for the
Observations on the incidence of plant parasitic nematodes
Mediterranean grassland. Besides, previous studies (STA-
in grassland in England and Wales. Grass and For. Sci., 47 :
MOU 1998) showed limited significance of much more
274-279.
pronounced disturbances, such as fire and overgrazing on
DALAKA, A. (2001). Grasses in evergreen sclerophyllous forma-
the structure and functioning of soil biota in Mediterra-
tions. Growth, reproduction and resource allocation of Stipa
nean areas.
bromoides (L.) Dorf. Ph.D. Thesis, Aristotle University of
Thessaloniki.
DE GOEDE, R.G.M., S.S. GEORGIEVA, B.C. VERSCHOOR & J.W.
ACKNOWLEDGEMENTS
KAMERMAN (1993). Changes in nematode community struc-
ture in a primary succession of blown-out areas in a drift
We wish to thank P. Nagy for the indentification of nema-
sand landscape. Fundam. Appl. Nematol., 16 : 501-513.
todes and K. Ekschmitt for ergosterol and BIOLOG determina-
DIAMANTOPOULOS, J., J. PANTIS, S. SGARDELIS, G. IATROU, S.
tion. We also thank B. Sohlenius, S. Boström, A.G. O'Donell
PIRINTSOS, E. PAPATHEODOROU, A. DALAKA, G.P. STAMOU,
and A.M.T. Bongers for valuable discussions. This work was
L.H. CAMMERAAT & S. KOSMAS (1996). The Petralona and
conducted within the DEGREE project funded by the European
Hortiatis Field Sites (Thessaloniki, Greece). In : BRANDT &
Commision (DG XII, contract no. ENV4-CT95-0029).
THORNES (eds), Mediterranean Desertification and Land
Use, John Wiley and Sons ltd, Chichester, 229-245.
REFERENCES
DJAJAKIRANA, G., R.G. JOERGENSEN & B. MEYER (1996). Ergos-
terol and microbial biomass relationship in soil. Biol. Fertil.
Soils, 22 : 299-304.
AKHTAR, M. (2000). Effect of organic and urea amendments in
E
soil on nematode communities and plant growth. Soil Biol.
KSCHMITT, K., G. BAKONYI, M. BONGERS, T. BONGERS, S. BOS-
Biochem., 32 : 573-575.
TRÖM, H. DOGAN, A. HARRISON, A. KALLIMANIS, P. NAGY,
A.G. O'DONNELL, B. SOHLENIUS, G.P. STAMOU & V. WOLTERS
ALLEN, S.E. (1974). Chemical analysis of ecological materials.
(1999). Effects of the nematofauna on microbial energy and
Blackwell Scientific Publications.
matter transformation rates in European grassland soils.
ANDERSON, J.M. (1995). Soil organisms as engineers : microsite
Plant and Soil, 212 : 45-61.
modulation of macroscale processes. In : JONES & LAWTON
EKSCHMITT, K., G. BAKONYI, M. BONGERS, T. BONGERS, S. BOS-
(eds), Linking species and ecosystems, Chapman and Hall,
TRÖM, H. DOGAN, A. HARRISON, P. NAGY, A.G. O'DONNELL,
New York, 94-106.
E.M. PAPATHEODOROU, B. SOHLENIUS, G.P. STAMOU & V.
ANDRASSY, I. (1984). Klasse Nematoda. Akademie-Verlag, Ber-
WOLTERS (2001). Nematode community structure as indica-
lin.
tor of soil functioning in European grassland soils. Eur. J.
ARMENDARIZ, I. & P. ARPIN (1996). Nematodes and their rela-
Soil. Biol., 37 : 263-268.
tionship to forest dynamics : I. Species and trophic groups.
ETTEMA, C.H., R. LOWRANCE & D.C. COLEMAN (1999). Riparian
Biol. Fertil. Soils, 23 : 405-413.
soil response to surface nitrogen input : the indicator poten-
ARMENDARIZ, I., M.A. HERNANDEZ & R. JORDANA (1996). Tem-
tial of free-living soil nematode populations. Soil Biol. Bio-
poral evolution of soil nematode communities in Pinus nigra
chem., 31 : 1625-1638.
Characteristics of a soil nematode community
259
FRECKMAN, D.W. & C.H. ETTEMA (1993). Assessing nematode
tion to vegetation and soil characteristics. Appl. Soil Ecol.,
communities in agroecosystems of varying human interven-
14 : 27-36.
tion. Agric. Ecosyst. Environ., 45 : 239-261.
PORAZINSKA, D.L., R. MCSORLEY, L.W. DUNCAN & J.H. GRA-
FU, S., D.C. COLEMAN, P.F. HENDRIX & D.A.JR. CROSSLEY
HAM (1998). Relationship between soil chemical status, soil
(2000). Responses of trophic groups of soil nematodes to
nematode community and sustainability indices. Nematrop-
residue application under conventional tillage and no-till
ica, 28 : 249-262.
regimes. Soil Biol. Biochem., 32 : 1731- 1741.
PORAZINSKA, D.L., L.W. DUNCAN, R. MCSORLEY & J.H. GRA-
GRIFFITHS, B.S., K. RITZ & R.E. WHEATLEY (1994). Nematodes
HAM (1999). Nematode communities as indicators of status
as indicators of enhanced microbiological activity in a Scot-
and processes of a soil ecosystem influenced by agricultural
tish organic farming system. Soil Use and Manage., 10 : 20-
management practices. Appl. Soil Ecol., 13 : 69-86.
24.
ROSS, D.J. (1990). Measurements of microbial biomass C and N
GRIFFITHS, B.S., I.M. YOUNG & S. CAUL (1995). Nematode and
in grassland soils by fumigation-incubation procedures :
protozoan population dynamics on decomposing barley
Influence of inoculum size and the control. Soil Biol. Bio-
leaves incubated at different soil matric potentials. Pedobio-
chem., 3 : 289-294.
logia, 39 : 454-461.
RUESS, L., W. FUNKE & A. BREUNIG (1993). Influence of experi-
HANEL, L. (1996). Composition and seasonal changes of soil
mental acidification of nematodes, bacteria and fungi : soil
nematode community in a South Bohemian meadow. Acta
microcosms and field experiments. Zool. Jb. Syst., 120 :
Soc. Zool. Bohem., 60 : 103-114.
189-199.
HENDRIX, P.F., R.W. PARMELEE, D.A.JR. CROSSLEY, D.C. COLE-
S'JACOB, J.J. & J. VAN BEZOOIJEN (1984). A manual for practical
MAN, E.P. ODUM & P.M. GROFFMAN (1986). Detritus food
work in nematology. Wageningen Agricultural University,
webs in conventional and no-tillage agroecosystems. Bio-
Dept. Nematology, Wageningen.
Science, 36 : 374-380.
SOHLENIUS, B. (1990). Influence of cropping system and nitro-
ISEMEYER, H. (1952). Eine einfache Methode zur Bestimmung
gen input on soil fauna and microorganisms in a Swedish
der Bodenatmung und der Karbonate im Boden. Z. Pflanzen-
arable soil. Biol. Fertil. Soils, 9 : 168-173.
ernaehr. Bodenk., 56 : 26-38.
S
J
TAMOU, G.P. (1998). Arthropods of Mediterranean-Type Eco-
ENKINSON, D.S.& D.S. POWLSON (1976). The effects of biocidal
systems. Springer-Verlag, Berlin, Heidelberg.
treatments on metabolism in soil-V. Soil Biol. Biochem., 8 :
209-213.
SWIFT, M.J., O.W. HEAL & J.M. ANDERSON (1979). Decomposi-
tion in Terrestrial Ecosystems. Blackwell Scientific, Oxford,
KORTHALS, G.W., R.G.M. DE GOEDE, J.E. KAMMENGA & T.
B
UK.
ONGERS (1996). The maturity index as an instrument for
risk assessment of soil pollution. In :
URZELAI, A., A.J. HERNANDEZ & J. PASTOR (2000). Biotic indi-
VAN STRAALEN &
K
ces based on soil nematode communities for assessing soil
RIVOLUTSKY (eds), Bioindicator systems for soil pollution,
ASI, 85-93.
quality in terrestrial ecosystems. The Science of the Total
M
Environ., 247 : 253-261.
AY, R. M. (1975). Patterns of species abundance and diversity.
In : C
V
ODY & DIAMOND (eds), Ecology and Evolution of Com-
AHJEN, W., J.C. MUNCH & C.C. TEBBE (1995). Carbon source
munities, Harvard Univ. Press, Cambridge, MA, 81-120.
utilization of soil extracted microorganisms as a tool to
M
detect the effect of soil supplemented with genetically engi-
OTOMURA, I. (1932). A statistical treatment of associations (in
Japanise). Jpn. J. Zool., 44 : 379-383.
neered and non engineered Corynebacterium glutamicum
N
and a recombinant peptid at the community level. FEMS
AGY, P.I. (1998). The nematode fauna of a dry continental
steppe grassland at Lake Donger, Hungary. In :
Microb. Ecol., 18 : 317-328.
DE GOEDE &
B
V
ONGERS (eds), Nematode communities of northern temper-
ERSCHOOR, B.C., R.G.M. DE GOEDE, F.W. DE VRIES & L. BRUS-
ate grassland ecosystems, Giessen, Focus-Verlag, 181-186.
SAARD (2001). Changes in the composition of the plant-feed-
N
ing nematode community in grasslands after cessation of fer-
AGY, P.I. & G.P. STAMOU (1998). Nematode fauna of a Meddi-
terranean grassland (garrigue) at Mt. Vermion, Greece.. In :
tiliser application. Appl. Soil Ecol., 17 : 1-17.
DE GOEDE & BONGERS (eds), Nematode communities of
WASILEWSKA, L. (1979). The structure and function of soil nem-
northern temperate grassland ecosystems, Giessen, Focus-
atode communities in natural ecosystems and agrocenoses.
Verlag, 187-188.
Pol. Ecol. Stud., 5 : 97-145.
OSBORNE, C.P. & F.I. WOODWARD (2002). Potential effects of
WARDLE, D.A., G.W. YEATES, R.N. WATSON & K.S. NICHOLSON
rising CO and climatic change on Mediterranean vegeta-
(1995). The detritus foodweb and the diversity of soil fauna
2
tion. In : GEESON, N.A., BRANDT, C.J., THORNES, J.B. (Eds),
as indicators of disturbance regimes in agroecosystems.
Mediterranean Desertification : A Mosaic of Processes and
Plant and Soil, 170 : 35-43.
Responses. John Wiley & Sons, Ltd, 33-54.
YEATES, G.W. (1996). Diversity of nematode fauna under three
PATE, E., N. NDIAYE-FAYE, J. THIOULOUSE, C. VILLENAVE, T.
vegetation types on a pallic soil in Otago, New Zealand. NZ.
BONGERS, P. CADET & D. DEBOUZIE (2000). Successional
J. Zool., 23 : 401-407.
trends in the characteristics of soil nematode communities in
YEATES, G.W. & H. VAN DER MEULEN (1996). Recolonization of
cropped and fallow lands in Senegal (Sonkorong). Appl.
methyl-bromide sterilized soils by plant and soil nematodes
Soil. Ecol., 14 : 5-15.
over 52 months. Biol. Fertil. Soils, 21 : 1-6.
PIELOU, E.C. (1975). Ecological diversity. New York, John
YEATES, G.W., T. BONGERS, R.G.M. DE GOEDE, D.W. FRECKMAN
Wiley.
& S.S. GEORGIEVA (1993). Feeding habits in soil nematode
POPOVICI, I. & M. CIOBANU (2000). Diversity and distribution of
families and genera-An outline for soil ecologists. J. Nema-
nematode communities in grasslands from Romania in rela-
tol., 25 : 315-331.
Belg. J. Zool., 135 (2) : 261-269
July 2005
The avifauna of the western Rodopi forests (N. Greece)
Stavros Xirouchakis
Natural History Museum of Crete, University of Crete, P.O. Box 2208, Heraklion GR-71409, Crete, Greece
e-mail : sxirouch@nhmc.uoc.gr
ABSTRACT. The composition of the avifauna in the upland forests of western Rodopi (North Greece) was investi-
gated during spring and summer of 1997 and 1998. A total of 109 species were detected in the area, while 93 of
them (85.3%) are regarded as breeders. Ten-minute counts in 260 points in plots of the most representative forest
stands produced 3 418 bird sightings of 42 species (13.14 individuals/ point, x = 6.2 species/ point). Bird density in
different forest habitats ranged from six to 34 birds/ 10 ha (x= 19 birds/ 10 ha). The greatest figure was recorded in
oak woods and conifer forests dominated by mature Norway spruce (Picea abies) and the lowest in pinewoods. Spe-
cies diversity was also greater in Norway spruce and broadleaf forests. Species richness should be attributed to the
geographical position of the area, and the differences in bird density to the vegetation structure in the various forest
habitats.
KEY WORDS : Forest birds, species richness, bird density, Rodopi.
INTRODUCTION
encompasses the southern slopes of the Rodopi mountain
chain whose highest peaks are located in Bulgaria. Its alti-
In Greece very few studies have looked at forest bird
tude ranges from 300 to 1 600 m a.s.l and covers approxi-
communities (CATSADORAKIS, 1991, 1997 ; SFOUGARIS et
mately 1 400 km2. The climate is transitional from the
al., 1998), and for species inhabiting commercially
sub-Mediterranean type to central European with a strong
exploited forests relevant published accounts are even
continental character. Mean annual temperature is 11.4° C
scarcer. In the Rodopi region (North Greece) special cli-
while the mean annual precipitation is about 1 200 mm
matic and geomorphologic conditions as well as sociopo-
distributed through out the year in 100-130 days (M
litical events have produced widespread woodlands with
AVRO-
low human pressure and very few settlements (0.01%).
MATIS, 1980 ; Sidironero-Drama & Leivaditis-Xanthi
Forested areas cover about 1 180 km2, which represents
Meteorological Stations : 1978-1989). Forests cover 83%
68% of the region. The forests of the area are the most
of the study area with 65% of them containing dense for-
productive in the country and one the most intensively
est stands (i.e. 50-75% coverage). In the southern part
commercialized. Logging usually extracts 187 000 m3 of
100,339 ha (61%) of oak woodland cover the hilly coun-
wood per year, a figure that represents 30% of the annual
try, adjacent to the valley of the Nestos river and comprise
timber production in Greece and gives the highest annual
the sub-Mediterranean zone (300-600 m a.s.l). Moving up
forestry revenue at the national level (DAFIS & SMIRIS,
to the north the beech-spruce zone spreads over 34 500 ha
1981; GATZOGIANNIS, 1999). The ecological value of the
(21%) dominated by beech (Faqus sylvatica), Mace-
area lies in its homogenous forests, some of them at the
donian fir (Abies borisii-regis), black pines (Pinus nigra),
edge of their European distribution, and a great variety of
and silver birch (Betula pendula). Between the two previ-
habitats that result in a high degree of biodiversity
ous zones black pine forests occupy 6700 ha (4%) only in
(SMIRIS, 1987 ; BAUER, 1986).
6.5% of pure stands, but mainly in mixtures with beech,
The aim of this study was to increase the knowledge on
Scots pine and oaks (e.g. Quercus frainetto, Quercus
the distribution of certain bird groups (i.e. birds of prey,
pubescens and Quercus dalechampii). Further north the
grouses) in the vegetation zones of the region and to pro-
conifer-broadleaf zone extends up to the Greek-Bulgarian
vide preliminary information on their breeding status. An
border (1600 m a.s.l) and covers 23 400 ha (14%) of
attempt was also made to evaluate the significance of the
dense woodland dominated by Scots pine (Pinus sylves-
different forest habitats for the avifauna by estimating
tris) (78%), Norway spruce (Picea abies) and silver birch
bird species richness and density.
(ATHANASIADIS et al., 1993 ; TSIAOUSSI, 1996 ; GATZO-
GIANNIS, 1999). Basic human activities include apiculture,
MATERIAL AND METHODS
cattle raising, lumbering and agriculture. Grassland and
farmland cover 8.9% and 5.8% respectively of the total
Study area
area. The greater region is almost void of habitations and
The study area is located in the western Rodopi region
human density is about three people per square kilometer
in the Drama prefecture, North Greece (Fig. 1) and
(GATZOGIANNIS, 1999).
262
Stavros Xirouchakis
detection strip was estimated as the one where the number
of birds (regardless of species) dropped below 20% of the
average number of the five meters strips closest to the
observer (EMLEN 1977). Twenty sample points per plot
were established by making stops at 150-m intervals
along a straight line by using a prismatic compass. The
centre of the sample point was checked by a densiometer
for the right percentage of canopy closure. All sample
points were situated within the forest away from openings
in order to minimize the edge effect. The duration of each
count was ten minutes starting about five minutes after
arrival, allowing the birds to recover from any distur-
bance. At each sample point the highest count for each
bird species was taken at ranges 0-r m and 0 m to infinity.
The pre-selected radius r was equal to the length of the
full-detection strip produced by the transect lines' count.
Densities were estimated by assuming that the probability
of detecting a bird declines with distance from the
observer. The general shape of this decline follows a half
normal function, exp [-(x/a)2] where x is the distance
from the observer and a is a constant equivalent to the
effective radius of the census depending on the circum-
stances (JARVINEN & VAISANEN 1975). Given that the
Fig. 1. Location of the study area in Northern Greece.
detectability function has this shape and certain assump-
tions are met (BUCKLAND 1984), the constant a and the
Field techniques and statistics
bird density D can be calculated directly by the formula :
Bird surveys were carried out in May-July 1997 and
D= log (n/n ) x n/m(pr2) where n = total number of birds
e
2
1998. In 1997 most of the fieldwork was spent collecting
detected, n = number outside the fixed radius (r) and m=
2
quantitative data on the species distribution and breeding
the number of points. Standard errors of bird density esti-
status. During 11:00 am-15:00 pm observations were
mates were calculated by using the jackknife method
made from vantage points and by road surveys with a
(MILLER 1974, KREBS 1989). Differences in bird abun-
mean speed of travel of 35 km/h, investigating for birds of
dance between sample plots were evaluated using one-
prey. All raptors sighted with the unaided eye were identi-
way ANOVA (F statistic). The Shannon index of diver-
fied by the use of binoculars (8x50) and plotted on
sity (H') and a heterogeneity index (H'/ H' max) were cal-
1 :50.000 scale maps in an effort to delineate their territo-
culated (MAGURRAN 1988) per sample plot based on the
ries (WOFFINDEN & MURFHY 1977, BILSTEIN 1978, FULLER
mean number of individuals counted within the fixed
& MOSHER 1987). The distribution of owl species was
detection radius in the point counts. Statistical compari-
surveyed by the playback method by eliciting calls from
sons were made using the student's t-test with a= 0.01
20:30h till 23:30h (FALLS 1981). Voice imitations started
(ZAR, 1984).
with the smallest species gradually proceeding to the
larger ones (CALL 1978). A search for the abundance of
RESULTS
the Capercaillies (Tetrao urogallus) was also undertaken
by following 35 transects of 42 km total length, all above
the 1000-m contour line. As the species is quite cryptic
Signs of breeding activity and suitable nesting habitat
and very reluctant to fly counts were made within a 10m
accounted for 93 (85.3%) species out of a total of 109 that
belt walking in a zigzag manner or throwing stones in
belong to 29 families (Appendix 1).
order to flush any close-sitting individuals.
Diurnal raptors were poorly represented with only ten
In 1998 the relative abundance and density of passe-
species. The buzzard (Buteo buteo) was the commonest
rines was censused by point counts (BIBBY et al., 1992).
raptor distributed equally in all forest habitats and vegeta-
Thirteen sample plots were selected from maps of a land-
tion zones. Twenty eight territories were located over an
scape analysis by the use of a geographic information sys-
area of about 300 km2 producing a density of one pair per
tem in such a manner as to comprise of homogeneous for-
10.7 km2. Honey buzzards (Pernis apivorus) were
est stands in terms of age (DBH>30 cm), tree condition
recorded in oak forests and mixed stands of conifers with
and canopy closure (50-75%). Forest stands were
deciduous trees up to the conifer-broadleaf zone where no
selected to be large enough (>60 ha) and dominated by
more than five territories were detected. In addition four
the main tree species of the area. Transient areas among
territories of short-toed eagle (Gircaetus gallicus) were
the four vegetation zones were avoided apart from those
delineated at middle and low altitude (<600 m), all in oak
encompassing oaks with black pines and Scots pines with
forests and marginally in the transient zone between the
beech as these tree species intermix a lot in the area. Line
oaks and the birch-fir forests. The golden eagle (Aquila
transects were firstly followed in order to determine the
chrysaetos) was located in the Greek-Bulgarian border
width of the full-detection strip. Ten transects of about
with one active territory. The breeding distributions of the
one km each were followed and every bird cue was tallied
Levant sparrowhawk (Accipiter brevipes), the spar-
in five meters strips on either side of the route. The full-
rowhawk (Accipiter nisus) and the goshawk (Accipiter
The avifauna of the western Rodopi forests (N. Greece)
263
gentilis) were sparse and restricted to the upper zone of
ests or mixed forests of Norway spruce/ Scots pine with
the conifer-deciduous forests. The hobby (Falco subbu-
beech as well as forests dominated by silver birch.
teo) occurred in the lowlands (<400 m) in open oak for-
A full detection strip in point counts was determined as
ests and grasslands with scattered shrubs. Two kestrel
equal to 30 m, and this figure was appointed as the fixed
pairs (Falco tinnunculus) were spotted in rocky outcrops
radius in each sample point, thus bird counts were made
within oak stands well below the 800 m contour line.
at ranges 0-30 m and 0 m to infinity. Excluding raptors
Moreover a flock of Eleonorae's falcon (Falco eleonorae)
and grouses, a total of 3,418 birds belonging to 42 species
comprising 20-30 individuals was present in the area,
were detected in 260 point counts (x= 6.2 species and
roosting in oaks in the sub-mediterranean zone and hunt-
13.14 individuals/ point). Twelve species (29%) were
ing flying insects in forest openings or along riverside
recorded within the 30m radius in more than 50% of the
vegetation just before dusk. In the day time the falcons
plots, and 15 species (36%) at a distance of more than
dispersed further north in the Bulgarian part.
30 m (Table 1). Thirteen species, robin (Erithacus rube-
As far as nocturnal raptors are concerned five species
cola), coal tit (Parus ater), chaffinch (Fringla coelebs),
were detected. The tawny owl (Stix aluco), was found in
marsh tit (Parus pallustris), blue tit (Parus caeruleus),
all forest habitats and constituted the commonest owl spe-
wren (Troglodytes troglodytes), nuthatch (Sitta euro-
cies. It showed strong preference for open stands in mixed
paea), goldcrest (Regulus regulus), great tit (Parus
beech-spruce forests and exhibited the highest density in
major), bullfinch (Phyrrula phyrrula), hawfinch (Cocco-
mature forests (e.g. five different responses in a single
thraustes coccothraustes), chiffchaff (Phylloscopus colly-
voice imitation). The Tengmalm's owl (Aegolius
bita) and blackbird (Turdus merula) constituted 85% of
funereus), was restricted in the upper conifer zone
the bird community in terms of numbers, while the first
(>1400 m a.s.l) showing high densities in mature mixed
three species accounted for almost half of the bird num-
stands of Norway spruce and fir (e.g. four different
bers (48%) in point counts (Table 1).
responses in a single voice imitation). The long-eared owl
By comparing the most common species (those
(Asio otus), exhibited an irregular distribution up to the
recorded in more than 50% of the sample points) to the
beech-spruce zone, always heard near small openings
most numerous ones (species with densities over 5 indi-
within the forests. The little owl (Athene noctua) and the
viduals/ 10 ha) 11 species were equally distributed in high
scops owl (Otus scops) were heard near settlements and
densities, e.g. chaffinch, robin, great tit, blue tit, marsh tit,
cultivation in middle altitude areas (<700 m) or in open
coal tit, wren, nuthatch, blackbird, chiffchaff and gold-
shrub land and degraded oak forests that are used as
crest. Four species, cuckoo (Cunculus canorus) great
rangelands. The highest altitude at which the little owl
spotted woodpecker (Dendrocopos major), jay (Garrulus
was heard was 900 m.
glandarius) and blackcap (Sylvia atricapilla), were wide-
The Rodopi forests constitute the only place in Greece
spread but in low densities, and two species (bullfinch
where all tetraonids can be found, namely the Capercaillie
and hawfinch) exhibited dense but localized populations.
(Tetrao urogallus) the hazel grouse (Bonasia bonasia)
Species richness ranged from eight to 18 species
and the black grouse (Tetrao tetrix) although the breeding
(x=14 species) in different forest habitats, and bird den-
status of the latter remains unclear (HANDRINOS & AKRIO-
sity from six to 34 birds/ 10 ha (x = 19 birds/ 10 ha) and
TIS 1997). In the present study four individuals of
differed significantly (F =8.35, P<0.01). Greatest bird
12
Capercaillie were recorded in the 0.42 km2 belt giving an
density was detected in oak woods and mixed conifers
estimate of 9.5 individuals/km2. Moreover, in random
dominated by mature Norway spruce (Table 2). Black
walks around the forests the species was recorded
pine stands had the lowest bird densities and the least
11 times in small groups or individual birds (mostly
number of species. Beech forests showed an intermediate
females). All Capercaillie observations were made in for-
situation, having relatively low bird densities and species
est stands dominated by Norway spruce and Scots pine or
richness (average). Pure conifers and silver birch forests
in mixed forests of beech and conifers along the Greek-
accommodated many bird species but in rather low densi-
Bulgarian border. The group size was one male and one
ties. Species diversity was greater in Norway spruce and
female or one male with two females although this figure
broadleaved forests than in pine forests, although these
should be regarded as minimum since the survey did not
differences were not all statistically significant (Table 2).
cover displaying males in leks. The species' population
Considering heterogeneity (H'/max H'), bird species
density has been estimated at 10-16 individuals/ km2
were represented more equally in broad-leaf than in coni-
(POIRAZIDIS, 1990). The hazel grouse was common in the
fer forests especially those encompassing Scots pines
area. Most of the sightings took place in pure conifer for-
(Table 2).
264
Stavros Xirouchakis
TABLE 1
Frequency of observations, numbers counted and estimated bird species densities (mean number of individuals/ 10 ha) from 260 sam-
ple points in western Rodopi forests
Frequency
No. of individuals
Species
Density
S.E.
0-30
All
0-30
All
Coal Tit (Parus ater)
237
77
238
477
44.86
11.33
Chaffinch (Fringila coelebs)
253
139
216
694
35.22
7.76
Robin (Erithacus rubecula)
169
148
184
474
31.70
2.73
Marsh Tit (Parus palustris)
47
27
87
123
20.57
7.55
Blue Tit (Parus caeruleus)
66
54
81
124
17.87
8.83
Wren (Troglodytes troglodytes)
66
46
79
194
13.81
2.26
Nuthatch (Sitta europaea)
56
29
72
156
13.14
4.24
Goldcrest (Regulus regulus)
53
60
57
106
11.13
5.80
Great Tit (Parus major)
39
91
53
111
9.81
4.42
Bullfinch (Pyrrhula pyrrhula)
10
16
34
44
8.87
6.26
Hawfinch (Coccothraustes coccothraustes)
7
8
32
43
7.89
6.26
Chiffchaff (Phylloscopus collybita)
31
50
44
259
6.56
2.01
Blackbird (Turdus merula)
31
43
33
110
5.34
1.29
Long-tailed Tit (Aegithalos caudatus)
5
30
20
30
4.49
1.89
Great Spotted Woodpecker (Dendrocopos major)
23
50
24
80
3.88
1.42
Crossbill (Loxia curvirostra)
35
7
20
57
3.35
2.45
Blackcap (Sylvia atricapilla)
14
37
15
40
2.56
1.02
Mistle Thrush (Turdus viscivorus)
8
13
9
19
1.66
0.71
Jay (Garrulus glandarius)
8
25
10
31
1.64
0.45
Crested Tit (Parus cristatus)
7
6
7
16
1.25
1.35
Water Pipit (Anthus spinoletta)
4
4
4
5
1.10
1.21
Rock Bunting (Emberiza cia)
2
3
5
8
1.07
0.83
Cuckoo (Cuculus canorus)
7
81
7
113
0.98
0.55
Cirl Bunting (Emberiza cirlus)
3
7
5
11
0.91
0.57
Red-backed Shrike (Lanius collurio)
3
7
3
7
0.53
0.34
Syrian Woodpecker (Dendrocopos syriacus)
2
1
2
3
0.45
0.40
Nutcracker (Nucifraga caryocatactes)
3
13
3
34
0.43
0.38
Black Woodpecker (Dryocopus martius)
2
4
2
7
0.32
0.29
Short-toed Treecreeper (Certhia brachydactyla)
1
2
1
2
0.19
0.17
Woodpigeon (Columba palumbus)
1
4
1
4
0.16
0.14
Hooded Crow (Corvus corone cornix)
1
4
1
4
0.16
0.14
Song Thrush (Turdus philomelos)
1
1
1
7
0.15
0.13
Black Redstart (Phoenicurus ochruros)
1
8
1
11
0.14
0.13
Green Woodpecker (Picus viridis)
0
1
0
1
0
Middle Spotted Woodpecker (Dendrocopos medius)
0
1
0
1
0
Tree Pipit (Anthus trivialis)
0
2
0
2
0
Black-headed Wagtail (Motacilla flava)
0
17
0
2
0
Firecrest (Regulus ignicapillus)
0
1
0
1
0
Sombre Tit (Parus lugubris)
0
1
0
2
0
Lesser Spotted Woodpecker (Dendrocopos minor)
2
2
2
2
0
Ring Ouzel (Turdus torquatus)
0
6
1
1
0
Wood Warbler (Phylloscopus sibilatrix)
0
61
2
2
0
Total
1 356
3 418
The avifauna of the western Rodopi forests (N. Greece)
265
TABLE 2
Bird density, number of species, bird species diversity and homogeneity indices in the forest stands of western Rodopi.
Sample plots/ dominant tree species
Ind./ 10 ha
S*
S
H'
H'/ max H'
1. Picea abies- Picea abies (2,5,8,9,12,13)*
20.29
17
24
2.26
0.531
2. Pinus sylvestris- Picea abies (1)
14.52
9
16
1.68
0.598
3. Picea abies - Pinus sylvestris (1,2)
34.40
11
17
4.97
0.624
4. Fagus sylvatica Picea abies (2,3)
13.44
15
19
2.27
0.595
5. Fagus sylvatica Pinups sylvestris (1,3,4)
13.13
10
17
1.68
0.622
6. Pinus sylvestris - Fagus sylvatica (2,3,5)
11.58
12
14
2.08
0.657
7. Quercus frainetto - Pinus nigra (2,3,5,6)
32.17
16
18
2.35
0.453
8. Pinus nigra - Pinus nigra (1,3,4,6,7)
6.37
8
15
1.75
0.679
9. Betula pendula - Pinups sylvestris (1,2,3,5,6,7,8)
17.90
16
26
2.48
0.612
10. Fagus sylvatica - Fagus sylvatica (2,3,5,8)
18.88
17
28
2.37
0.495
11. Quercus frainetto - Quercus frainetto (2,3,5,8)
32.33
18
24
2.28
0.453
12. Pinus sylvestris - Pinus sylvestris (1,3,4,7,9,10,11)
13.28
11
22
1.79
0.559
13. Betula pendula - Betula pendula (1,2,3,5,6,8,11,12)
14.04
18
20
2.52
0.470
Average
18.64
20
S* : Number of species detected within the 30m-fixed radius from the observer
S : Total number of species detected
H' : Shannon-Wiener diversity index
Max H' : maximum diversity
H'/ max H' : Heterogeneity index
()* Forest stands with statistical differences in species diversity
DISCUSSION
exhibit a higher ecological value in terms of bird species
richness and abundance (MACARTHUR & MACARTHUR,
Overall the Rodopi forests seem to host both central
1961; MOSS, 1978, SMART & ANDREWS, 1985; ANDREWS,
European and Mediterranean species and could be classi-
1986; AVERY & LESLIE, 1990).
fied as a transitional zone between the lowest part of tem-
Regarding tree species composition, it is generally
perate forest and the highest part of the Mediterranean
accepted that spruce carries more bird species than pine
one. The composition and structure of the vegetation in
(NEWTON 1986), as spruce woodland provides birds with
the area is typical of montane forests, dominated by broa-
greater amounts of food (e.g. insects) and better shelter
dleaved species at lower elevations and conifers at higher
for nests. Birch forests support greater densities of birds
altitudes (TUCKER & EVANS, 1997). However in the sub
than pines (NEWTON & MOSS 1977) while oak woods
alpine coniferous zone, which is dominated by Norway
maintain greater densities than both (FRENCH et al., 1986).
spruce and Scots pine some of the species recorded are
Pure conifer forests in the study area are rather dark with
typical of boreal forests such as the willow tit, the nut-
closed canopy and for this reason field layers are mostly
cracker (Nucifraga caryocatactes), the ring ouzel (Turdus
absent or poorly developed. As a result their avifauna is
torquatus), the bullfinch, and the Capercaillie which are
less diverse but the species are quite characteristic. These
considered to be rare in Greece. Meanwhile in the temper-
forests are heavily exploited for timber production and
ate forests, dominated by beeches and oaks, the bird com-
subsequently the bird communities often follow the man-
munity included typical species of broadleaved forests,
induced succession of the forest. On the contrary mixed
some of them rather common in many parts of the country
forests dominated by oaks exhibit greater development of
(e.g. honey buzzard, short-toed eagle, goshawk, spar-
understory growth and a higher diversity of vascular
rowhawk, tawny owl and a variety of chats, tits and war-
plants thus supporting a much richer avifauna. In addi-
blers). This pattern is expected in woodland habitats dom-
tion, broadleaves often experience an outbreak of foliage-
inated by central European species at the edge of their
feeding caterpillars, which leads to the defoliation of the
distribution due to the fact that some of the mountain
canopy branches. This feature was most pronounced in
parts in intermediate zones of the Balkans have been
the pure oak woods of the Sub-Mediterranean zone where
moderately affected by the glacial and interglacial peri-
the young oak trees, although they had a very low foliage
ods. It has also been suggested that mountain regions fac-
profile, attracted insectivorous passerines from adjacent
ing south, east and southeast (such as the mountains of the
forest habitats.
study area) act as "refugia" for the mediterranean fauna
Beech and silver birch forests are multi-layered but
(MATVEJEV, 1976).
they are dominated by more homogeneous stands with
Species diversity and density in point counts coincide
less horizontal heterogeneity and exhibited an intermedi-
with and confirm general conclusions in the existing liter-
ate situation regarding bird abundance and density. Above
ature. Considering woodland structure it has been shown
all, the mixed stands of Norway spruce with Scots pine
in many studies that forests with mature trees, standing
proved of exceptionally high ornithological value. These
dead timber, small open areas and many layers of foliage
forests supported a great structural and floristic diversity
266
Stavros Xirouchakis
and offer ample feeding and nesting opportunities to a rel-
ATHANASIADIS, N., A. GERASIMIDIS, E. ELEFTHERIADOU & K.
atively high number of birds. Similarly pure Norway
THEODOROPOULOS (1993). Zur postglazialen Vegetation-
spruce forests where large amounts of dead wood and
sentwicklung des Rhopdopi-Gebirges (Elatia Dramas-
small openings were present supported forest birds with
Grichenland). Diss. Bot., 196 : 427-537
many different types of food and nesting sites. Breeding
AVERY, M. & R LESLIE (1990). Birds and Forestry. A & A.D.
and foraging habitat are mostly suitable for these species
Poyser, London.
B
that are insectivorous and hole nesting. Woodpeckers
AUER, W. & H.J. BOHR (1987). Zut Kenntnis der sudlichen
Arealgrenzen einiger Vogellarten in den griechischen
largely acquired their food in open conifer stands with
Rhodopen. Vogelwelt, 108 : 1-13
many snags, and in areas where intense logging takes
BIBBY, C.J., N.D BURGESS & D. HILL (1992). Bird Census Tech-
place they preyed upon insects thriving in the stools. On
niques. Academic Press, London.
the contrary, in beech stands they foraged in mature trees
BILSTEIN, K.L. (1978). Behavioural ecology of Red-Tailed
with DBH of 30-50 cm. The diverse avifauna detected in
Hawks, Rough-legged Hawks, Northern Harriers, American
silver birch forests should be attributed to the variety of
Kestrels and other raptorial birds wintering in South central
habitats and microhabitats occurring within certain sam-
Ohio. Ph.D. Dissertation, Ohio State University, Columbus.
pling plots (e.g. mature trees, rocky outcrops, freshwater
BUCKLAND, S. (1984). Models for the variable circular plot
streams and an understory vegetation rich in shrubs).
method of estimating animal density. Dept. of Stat. Techni-
cal. Report No. 6. University of Aberdeen.
On the other hand the low density of diurnal birds of
CALL, M.W. (1978). Nesting Habitats and Surveying techniques
prey is the most striking case of low human intervention
for the common Western Raptors. Technical Note, TN-316.
on the upland forests. The area seems to sustain atypical
U.S. Department of the Interior-Bureau of Land Manage-
habitat for many raptors. The lack of suitable breeding
ment.
sites for cliff nesters and the scarcity of foraging areas
CATSADORAKIS, G. (1991). On the avifauna of Samaria gorge
must have had a critical impact on many Greek-Mediter-
(Crete, Greece). Kartieung mediterraner Brutvoegel, 6 : 3-
ranean species. The extensive area was inhabited by an
12
C
ancient Greek race (Sarakatsani) that practiced traditional
ATSADORAKIS, G. (1997). Breeding birds from reedbeds to
alpine meadows (Lake Prespa, northwestern Greece : a uni-
stock raising till late `50s (PSYHOGIOS & PAPAPETROU,
quie Balkan wetland). Hydrobiologia, 351 : 143-155
1995). However nomadic flocks were eliminated almost
DAFIS, S. & P. SMIRIS (1981). Forest and stage research in Fir
completely during the first two decades after World War
forests of Greece. Scientific Yearbook. Dept. of Forestry,
II. The reduction of extensive grazing has resulted in
Vol. 104. No. 5 : 145-191. (In Greek).
regeneration of the forest, which was also enhanced by
EMLEN, J.T. (1977). Estimating breeding season bird densities
depopulation of the area and abandonment of agricultural
from transect counts. Auk, 94 : 455-468.
land for political and social reasons (e.g. Greek civil war,
FALLS, J.B. (1981). Mapping territories with playback : an accu-
GIANNATOS, 1997). As a result forest openings became
rate census method for songbirds. In : RALPH & SCOTT (eds),
scarce and foraging habitat for hunting raptors has been
Estimating numbers of terrestrial birds. Studies in Avian
substantially reduced.Nevertheless forest management
Biology 6, Cooper Ornith. Society : 86-91.
may counterbalance some of the differences detected in
FRENCH, D.D., D. JENKINS & J.W.H. CONROY (1986). Guidelines
for managing woods in Aberdeenshire for song birds. In :
bird species richness and abundance. Conifer stands are
JENKINS, D. (ed) : Trees and Wildlife in the Scottish Uplands,
quite intact as they are managed by group felling or selec-
ITE Symposium No. 17, pp. 121-128. Huntingdon, Institute
tive thinning and are restocked by natural regeneration
of Terrestrial Ecology.
from shelter wood. On the contrary oak woods are nor-
FULLER, M.R. & J.A. MOSHER (1987). Raptor survey techniques.
mally under severe forestry operation such as clear cut-
In : PENDLETON, MISSLAP, CLINE & BIRD (eds), Raptor Man-
ting or coppicing on a 10-year rotation cycle, and natural
agement techniques Manual. Institute for Wildlife Research
regrowth comes mostly from the stumps. The impact has
National Wildlife Federation. Sc. Tech. Series No. 10.
been most severe in the lowlands close to villages where
GATZOGIANNIS, S. (1999) : Special Environmental Study of
oak woods are used as pastureland and fuelwood produc-
the Rodopi region. Project LIFE- NATURE, ARCTOS (Phase
tion.
II), Vol. A & B, pp. 439. Thessaloniki.
GIANNATOS, G (1997). Human-related factors affecting Brown
bear conservation in the Rodopi mountains of Northeastern
ACKNOWLEDGEMENTS
Greece. M.Sc. Thesis, Missoula, Un. of Montana.
HANDRINOS, G. & T. AKRIOTIS (1997). The Birds of Greece.
Helm-A&C Black, London.
I would like to thank the Forestry Department of Drama pre-
JARVINEN, O. & R.A. VAISANEN (1975). Estimating relative den-
fecture for offering me accommodation at the village of Elatia. I
sities of breeding birds by the line transect method. Oikos,
am especially thankful to the Forester G. Isaak for assistance in
26 : 316-322.
the fieldwork, S. Roberts for improvement of the English text,
KREBS, C. (1989). Ecological Methodology. Harper Collins,
the Society for the protection of the Brown Bear "Arctouros" for
New York.
technical support and the Hellenic Ornithological Society for
MACARTHUR, R.H. & J.W. MACARTHUR (1961). On bird species
allowing me access to its archives.
diversity. Ecology, 42 : 594-598
MAGURRAN, A. (1988). Ecological Diversity and Its Measure-
ments. Croom Helm, London.
REFERENCES
MATVEJEV, S.D. (1976). Survey of the avifauna of the Balkan
peninsula. The Serbian Academy of Sciences and Arts
ANDREWS, J.H. (1986). The implications for birds of farm wood-
Monog., Vol. CDX-CI, pp. 321. Beograd.
land expansion. Farming and Forestry. In : HATFIELD, G.R.
MAVROMATIS, G. (1980). The bioclimatic zones of Greece. Rela-
(ed.), Proceedings of Conference,Loughborough University.
tion of the climate and vegetation. Bioclimatic zones of
Forestry Commission, Occasional Paper 17.
Greece. Forest Research, Athens, 63 pp. (In Greek).
The avifauna of the western Rodopi forests (N. Greece)
267
MILLER, R.G. (1974). The Jackknife-a review. Biometrika 61 : 1-
European less favoured areas, Proceedings of EU EQULFA
15.
Project : 57-62
MOSS, D. (1978). Diversity of woodland song-bird populations.
SMART, N. & J. ANDREWS (1985). Birds and broadleaves hand-
Journal of Animal Ecology, 47 : 521-527.
book. RSPB.
NEWTON, I. (1986). Principles underlying bird numbers in Scot-
SMIRIS, P. (1987). The dynamic evolution of vegetation stucture
tish woodlands. In : JENKINS, D. (ed) : Trees and Wildlife in
of the "Virgin Forest" in Paranesti. Sci. Ann. Fac. Forest.,
the Scottish Uplands, ITE Symposium No. 17, pp. 121-128.
Vol. A, No. 13. Aristotle University of Thessaloniki, Thessa-
Huntingdon, Institute of Terrestrial Ecology.
loniki.
NEWTON, I. & D. MOSS (1977). Breeding birds of the Scottish
pinewoods. In : B
TSIAOUSSI, V. (1996). Specific Management Plan for the site
UNCE & JEFFERS. (eds), Native Pinewoods
Periochi Elatia (GR1140003). The Goulandris Natural His-
of Scotland, pp. 26-34. Institute of Terrestrial Ecology, Cam-
bridge.
tory Museum-Greek Biotope/ Wetland Centre, pp. 197.
P
Thermi, Salonika.
OIRAZIDIS, C. (1990). The Capercaillie (Tetrao urogallus, L.) in
the Greek forests. Physis, 48 : 3-7 (In Greek).
TUCKER, G.M. & M.I., EVANS (1997). Habitats for birds in
P
Europe : a conservation strategy for the wider environment,
SYHOGIOS, D. & G. PAPAPETROU (1995). The movements of
pastoralism in Sarakaqtsani : A Hellenic pastoralist popula-
BirdLife Conservation Series no. 6, pp. 464. BirdLife Inter-
tion. Proceedings of Congress in Serres, pp. 27-46. Athens
national, Cambridge.
(In Greek).
WOFFINDEN N. & J. MURFHY (1977). A roadside reptor census in
SFOUGARIS, A., P. BIRTSAS & A. NASTIS (1998). Bird diversity
the eastern Great Basin 1973-1974. Raptor Research, 11 :
and density in relation to different habitats and land uses in
62-66.
Portaicos-Pertouli area, Greece. In : WATERHOUSE &.
ZAR, J. (1984). Biostatistical analysis. Prentice Hall, New Jer-
MCEWAN (eds) Landscape, Livestock and Livelihoods in
sey.
268
Stavros Xirouchakis
APPENDIX 1
Breeding
Species
status
Breeding status of bird species detected
Picoides tridactylus (Linnaeus)
1
in the western Rodopi forests
FAMILY : Alaudidae
1 : Suitable nesting habitat
Melanocorypha calandra (Linnaeus)
1
2 : Territorial defense/ Aerial display/ Courtship behaviour
Caladrella brachydactyla (Leisler)
1
3 : Nest with chicks found
Galerida cristata (Linnaeus)
1
4 : Adult feeding chicks/ carrying food to the nest
FAMILY : Hirundidae
5 : Fledglings observed
Pryonopogne rupestris (Scopoli)
6
6 : Data insufficient
Hirundo rustica (Linnaeus)
6
Delichon urbica (Linnaeus)
6
Breeding
Species
status
FAMILY : Motacillidae
FAMILY : Accipitridae
Anthus trivialis (Linnaeus)
1
Pernis apivorus (Linnaeus)
2, 4
Anthus spinoletta(Linnaeus)
1, 2
Circaetus gallicus (Gmelin)
3, 4
Motacilla flava (Linnaeus)
6
Accipiter brevipes (Severtzov)
1, 2
Motacilla cinerea (Tunstall)
6
Accipiter nisus (Linnaeus)
1, 2
Motacilla alba (Linnaeus)
6
Accipiter gentiles (Linnaeus)
1, 2
FAMILY : Cinclidae
Buteo buteo (Linnaeus)
2, 4
Cinclus cinclus (Linnaeus)
1
Aquila chrysaetos (Linnaeus)
1, 2
FAMILY : Troglodytidae
FAMILY : Falconidae
Troglodytes troglodytes (Linnaeus)
5
Falco tinnunculus (Linnaeus)
2, 2
FAMILY : Turdidae
Falco subbuteo (Linnaeus)
1, 2, 4
Erithacus rubecola (Linnaeus)
1, 5
Falco eleonorae (Cene)
6
Luscinia megarhynchos (Brehm)
1, 2
FAMILY : Tetraonidae
Phoenicurus ochruros (Gmelin)
5
Bonasia bonasia (Linnaeus)
1, 5
Phoenicurus phoenicurus (Linnaeus)
1
Tetrao urogallus (Linnaeus)
1, 5
Saxicola rubetra (Linnaeus)
5
FAMILY : Columbidae
Saxicola torquata (Linnaeus)
6
Columba palumbus (Linnaeus)
1, 4
Oenanthe isabellina (Temminck)
6
Streptopelia turtur (Linnaeus)
1, 2, 5
Oenanthe oenanthe (Linnaeus)
1
FAMILY : Cuculidae
Turdus torquatus (Temminck)
3, 5
Cunculus canorus (Linnaeus)
1, 2
Turdus merula (Linnaeus)
5
FAMILY : Strigidae
Turdus philomelos (Brehm)
5
Otus scops (Linnaeus)
1
Turdus viscivorus (Linnaeus)
5
Athene noctua (Scopoli)
1
FAMILY : Sylvidae
Asio otus (Linnaeus)
1, 2
Hippolais pallida (Hemprich-Ehrenberg)
1
Stix aluco (Linnaeus)
1, 2
Sylvia cantillans (Pallas)
1
Aegolius funereus (Linnaeus)
1, 2
Sylvia melanocephala (Gmelin)
2
FAMILY : Caprimulgidae
Sylvia communis (Latham)
1,1
Captimulgus europeus (Linnaeus)
1
Sylvia atricapilla (Linnaeus)
3, 5, 4
FAMILY : Apodidae
Phylloscopus bonelli (Vieillot)
1, 2
Apus apus (Linnaeus)
6
Phylloscopus sibilatrix (Bechstein)
1, 2
Apus melba (Linnaeus)
6
Phylloscopus collybita (Veillot)
1, 2
FAMILY : Meropidae
Regulus regulus (Linnaeus)
1, 2
Merops apiaster (Linnaeus)
1
Regulus ignicapillus (Temminck)
1
FAMILY : Coracidae
FAMILY : Muscicapidae
Coracias garrulous (Linnaeus)
1
Muscicapa striata (Pallaas)
1
FAMILY : Upupidae
Ficedula parva (Bechstein)
1
Upupa epops (Linnaeus)
1, 4
FAMILY : Aegithalidae
FAMILY : Picidae
Aegithalos caudatus (Linnaeus)
5
Picus canus (Gmelin)
1, 2
FAMILY : Paridae
Picus viridis (Linnaeus)
1, 2
Parus lugubris (Temminck)
2
Dryocopus martius (Linnaeus)
1, 5
Parus palustris (Linnaeus)
1, 5
Dendrocopos major (Linnaeus)
1, 3
Parus montanus (Conrad)
1
Dendrocopos syriacus (Hemprich-Ehrenberg)
1, 2
Parus cristatus (Linnaeus)
5
Dendrocopos medius (Linnaeus)
1, 3
Parus ater (Linnaeus)
5, 4
Dendrocopos leucotos (Bechstein)
1
Parus caeruleus (Linnaeus)
5
Dendrocopos minor (Linnaeus)
1, 3
Parus major (Linnaeus)
5
The avifauna of the western Rodopi forests (N. Greece)
269
Breeding
Breeding
Species
Species
status
status
FAMILY : Sittidae
Passer montanus (Linnaeus)
1
Sitta europaea (Linnaeus)
5
FAMILY : Fringilidae
Sitta neumayer (Michahelles)
1
Fringila coelebs (Linnaeus)
5
FAMILY : Certhiidae
Serinus serinus (Linnaeus)
5
Certhia familiaris (Linnaeus)
1
Carduelis chloris (Linnaeus)
5
Certhia brachydactyla (Brehm)
1
Carduelis carduelis (Linnaeus)
5
FAMILY : Oriolidae
Carduelis spinus (Linnaeus)
1
Oriolus oriolus (Linnaeus)
1
Carduelis cannabina (Linnaeus)
5
FAMILY : Laniidae
Loxia curvirostra (Linnaeus)
5, 4
Lanius collurio (Linnaeus)
5
Pyrrhula pyrrhula (Linnaeus)
5, 4
Lanius minor (Gmelin)
1
Coccothraustes coccothraustes (Linnaeus)
5
Lanius senator (Linnaeus)
2
FAMILY : Emberizidae
FAMILY : Corvidae
Emberiza citrinella (Linnaeus)
6
Garrulus glandarius (Linnaeus)
1, 2, 5
Emberiza cirlus (Linnaeus)
1, 2
Nucifraga caryocatactes (Linnaeus)
1, 5
Emberiza cia (Linnaeus)
5
Corvus corone (Linnaeus)
1
Emberiza hortulana (Linnaeus)
6
Corvus corax (Linnaeus)
6
Emberiza melanocephala (Linnaeus)
6
FAMILY : Passeridae
Milaria calandra (Linnaeus)
6
Passer domesticus (Linnaeus)
4
Belg. J. Zool., 135 (2) : 271-277
July 2005
A review and reappraisal of research in some previously
unsurveyed Mediterranean marine turtle nesting sites,
1990-2001
Lily Venizelos, Kalliopi Papapavlou, Marc-Antoine Dunais and Calliope Lagonika
MEDASSET (The Mediterranean Association to Save the Sea Turtles), Licavitou 1(c), 106 72, Athens, Greece
Corresponding author : L. Venizelos, e-mail : medasset@hol.gr
ABSTRACT. One of MEDASSET's main objectives has been the assessment of coastal areas on a pan-Mediterra-
nean scale in a search for potential nesting sites of Caretta caretta (loggerhead turtle) and Chelonia mydas (green
turtle), the only two marine turtle species known to reproduce in the Mediterranean. The specific characteristics of
each coastal region were logged, as turtles cannot be successfully protected unless all their reproductive habitats are
known. If any important turtle nesting sites were found, recommendations for implementation of protective meas-
ures were made to the States involved, followed by efforts towards the implementation of protective legislation and
conservation measures. These surveys took place in Sardinia, Italy (1990 & 1991), the North Aegean (mainland and
islands), Greece (1991), the western part of the Egyptian Mediterranean coast (1993), Syria (1991), Libya (1995 &
1998) and Lebanon (2001). This review sums up data resulting from these pioneering studies and re-evaluates it in
the light of more recent information regarding marine turtle nesting and conservation in the Mediterranean.
KEY WORDS : marine turtles, Mediterranean, coastal assessment, conservation, nesting beach
INTRODUCTION
beaches or to assess the status of known ones, with
respect to conservation priorities for marine turtles.
The Mediterranean region hosts breeding populations
The purpose of this paper is to provide a summary of
of two of the seven marine turtle species that occur in the
all research surveys funded or co-funded by MEDASSET
world : Caretta caretta (L., 1758) (Reptilia : Cheloniidae)
in the past 12 years that aimed to locate new nesting
nests widely within the eastern basin and North Africa,
beaches. The majority of these projects were also co-
whereas the green turtle Chelonia mydas (L., 1758)
funded by the European Community, UNEP-MAP
(Reptilia : Cheloniidae) nests in a more restricted range,
(United Nations Environment Program Mediterranean
mainly comprising Turkey and Cyprus. In the early `90s
Action Plan) and/or others. In the light of more recent
both species were reported as declining (GROOMBRIDGE,
information, the importance of past data can now be eval-
1990) with the Mediterranean green turtle population
uated more objectively. Knowledge of marine turtle popu-
being reported recently as "critically endangered"
lations in several less-researched Mediterranean areas
(HILTON-TAYLOR, 2000).
may thus become more clearly appraised, focusing atten-
Today, comprehensive long-term field data on nesting
tion for future research and conservation efforts.
numbers for C. caretta in several Mediterranean areas are
not available, although there are some reviews that con-
MATERIAL AND METHODS
centrate on the conservation aspect (MARGARITOULIS et
al., 2003 ; LAURENT, 1998). An overall estimation of the
population status of C. mydas and C. caretta in the Medi-
Data from past surveys funded or co-funded by
terranean was recently presented in B
MEDASSET have been provided from the organisation's
RODERICK et al.
(2002) and K
archives after reviewing published and, in some cases,
ASPAREK et al. (2001) ; for C. mydas, high
variation between annual nesting numbers does not seem
unpublished information (Table 1). In order to reappraise
to indicate any particular trend regarding changes in the
this information we next considered accessible published
nesting population size.
scientific literature originating from more recent surveys
conducted within the same geographical area. It became
Since its formation in 1988, MEDASSET has been
obvious that the fieldwork protocol differed greatly
committed to safeguarding the Mediterranean marine tur-
between surveys and/or years, in each case varying
tle populations through scientific research and conserva-
according to the particular constraints that researchers
tion activities. Following the principle that "....there is no
faced : however, in all cases "nesting evidence" was
other basis for sound political decisions than the best
standardized to include either direct observations of ovi-
available scientific evidence..." (BRUNDTLAND 1997),
position and/or indirect signs such as nesting tracks, false
surveys in various Mediterranean countries have been
tracks, nests, eggs/egg shells and/or hatchlings. It should
conducted either in order to search for new nesting
be emphasised that most of these pioneering projects
272
Lily Venizelos, Kalliopi Papapavlou, Marc-Antoine Dunais and Calliope Lagonika
,
es
:
y
P/
of
n
se
e
2 km
ach
ay
th
r
i
,
r
. I
d
re
s
nest-
d
b
et al
T
,
UNE
th
30.
g
sum-
M
ks in
E
,
Adloun
an
rte
AK
S
e
b
a
ne
ent
y be
d
in detail)
3
days
ies.
A(
rin
(
ly - 5
e
n
.
S
001
2 days
,
1
iye, Mah-
a
s
we
ec
po
AY
t
r
y
of
banon, 2001
nd
ys
st)
a
n
sou
ansouri both
A
)
, L
onm
2
R
e
),
Ju
rd
s
m
a
r
e
tta
s re
D
P
vir
Le
0 km (
uly)
3
fp
-
M
l
-M
h
e
r
m
EMI
03
i
nis
20
o
f
sa
surveye
late sp
mer
1
7
da
Jun
(J
(2
Augu
b,
nests/trac
El
Qa
moudiye
and Damou
E
C.c
C.myd
identified a
ing sp
additional nesting
site
fis
D
20
ME
RAC/SP
MA
M
En
8
m
th
ch
6
.
EP/
e
199
1
rin
a
),
T
,
(NW
0
5
.
7
k
st
EP
et al
r
n
a
-
A(UN
C
iby
Ma
line),
(1
98
(
1
a
r
e
tta
y Resear
(L
SSE
nte
ENT
, T
A
FI
Libya
ast
km
y
a
),
7
C.c
99
C/SP
co
sandy beaches
l
y
)
i
o
l
og
e
n
t
re
40
of
s
u
rveyed in detail)
J
uly 19
1
6
days
Ju
c
,
fp
15
tracks
L
AUR
19
RA
MAP)
(Lib
B
C
MED
WW
tional
m
e
s
tail)
te -
996
3 k
6
a
s
.
,
1
86.
b
each
e
tta
et al
a
(Sir
ah)
(1
199
C. myd
y
ed in de
NT
.
car
E
R
Liby
9 km
mmer
C
c
ks
99
Misrat
sandy
-2001
20
of
surve
su
66
tra
2 dead
hatchlings
L
AU
19
95
.
65
l
-
.
-
S
e
1991
a,
19
95
e
tta
Oum-
al
141
th
ly)
nests)
em
s
t
Sirte
DA
P
a
rin
Ju
th
ng
Ras-e
et
A(UNEP/
a
j
ur
WWF
tline),
sandy
s
(
1
6
th
Bengazi
y Research
(T
C. car
alo
is,
ENT
)
ME
a
)
,
M
Libya (NE
e
-
J
u
l
y
,
19
7
ost of
eija, Ea
5
P
T
,
TCE
t
re
y
a),
rnational
coas
und
-Fra
w
iby
1
1
9
5
km (
km of
beaches surveyed
in detail)
Jun
21 day
J
u
ne
c
,
fp
>300
tracks (176
(m
fo
el
A
and N.
beaches)
L
AUR
199
RAC/SP
MA
SE
(L
Biolog
Cen
Lib
Inte
e
98
dy
.
ir
acks
e
tta
UK)
e Mediterranean,
san
al
st,
tr
s
t
f
e
r-
th
)
, 19
e
of
)
car
et
e (
t (ent
gu
s
y -
th
p
m
s
em.
C.
ELL
mm
s
tline
5 k
Au
day
Ma
a
r
e
tta
C. mydas
on
B
a
n
d re
in Initiative
ra
Egy
th
e
ral
coa
ache
a
y-
0
Sept
C. c
sts
AMP
og
6
16.
be
M
1
998
1
03
(2 st 1
3
on the northwest
coastline
sev
and
ne
N.Sinai coa
C
2
001
ences therein
Darw
pr
een
93
e
s
,
k
m
93
,
phy
plored areas of
Kas-
), 19
rently
i
b-
Kas-
P)
,
1
etw
A
b
255
e
tta
the sur-
C.
s &
6,
3
SET
ria
E
ex
m
b
e
ach
d
in detail)
l
y
,
19
ea
hatchling
A
e
r
ies
L
alu
appa
ar
e
ad
a
nd
t
)
B
a
ys
ceanogra
less
exandria and
DAS
l
-
S
2 km (
e
Ju
i
onal Institute
sandy
d
C. car
e
tta
e
k 199
e
k 199
acks,
e d
e
n
i
z
e
lo
E
NEP/M
lex
yp
TA
Egypt (
Al
E
60
of
surveye
Jun
29
f
p
10
tr
evenly distr
uted over
veyed
on
car
V
par
par
M
RAC/SP
(U
Nat
of O
and Fish
(A
Eg
along
e
1
)
er
93
,
eys
rd
95;
94;
ntir
199
5 km
8
an-
9,
th
een
5 km
beaches
d
(1
5.
a
r
t
ous
acks
T
auna
line),
(7
91
s
(
2
0
e
t
w
SSET
vation
une)
c
ks
e
s
e
bo
A
5 km)
arek 19
arek 19
er
)
Syria (e
k
m
J
a
lse tr
D
p
etof
e
rnational
CI
coast
th
8.
e
nizelos 19
E
193
of sandy
surveyed in detail)
June 19
10 day
30
fp
2
5
tra
nests) b
Latakia an
Jablah (1
2 f
between
a
n
d the Syri
Leban
(2
Kasp
Kasp
V
M
Her
Cons
Int
(H
il)
o
s
an
e
s
1
3;
64 km
i
mn
T
.
turtle nesting surv
e
ge
ust,
.
C.
313
199
(6
, L
E
4
t
h A
y beach
t
r
ack close
i
na
0)
an
ct No
Sea,
k
m
DASSE
t
ra
(9
Nor
neAug
a
lse
Mir
e
nizelos 199
2
078
o
f
sand
surveyed in deta
Ju
1
991
2
8
days
f
p
1 f
to
V
Kasparek 1991
ME
u
nder
Con
6
610
of marine
3;
.
ccord-
90
13
199
et al
C.
o
.
S
E
R
SSET
) 43
Summary
(
b
e
aches
991
O
act N
90
1
M
DA
Sardinia, 1991
d
a
y
s
HIT
91
E
der an E.
10(
70 km
prioritised a
ing to the 19
results)
July
10
fp
none
V
ENIZELO
W
19
M
un
Contr
66
a
e
;
.
990
th
3
ith
th
t
7
993
.
. Ann
T
w
osei)
1
et al
.
C
E
431
(
S
gus
Or
u
g
u
s
t 1
(
J
uly
R
O
SSE
n
E
A
A
act No.
ZELOS
M
r a
phasis on
lf of
Au
,
f
p
T
Sardinia, 1990
0 km
th
HI
91
de
ontr
75
to Murtas
em
Gu
J
u
ly
1
3
days
24
b
,
c
none
V
ENI
W
19
MED
un
C
6
6
1
0
(
90)
ols
ot patr
ce
r
v
eyed
,
f
p
: fo
o
n
a
ed by:
s
u
car
e
as
v
iden
e
of
fund
c:
h
e
y s
ect
at,
oj
Lengt
coastline
Surv
Survey duration
Survey type
Nesting e
Literatur
Pr
b: bo
a.
Marine turtle research in some previously unsurveyed marine turtle nesting sites of the Mediterranean
273
intended to survey Mediterranean areas where little or no
TABLE 2
marine turtle nesting data were available. As a result,
Spearman rank correlation coefficients r for nesting density
researchers were interested in providing primary evidence
s
comparisons between adjacent coastal zones along the northern
of nesting if any rather than monitoring nesting num-
shore of Cyprus shown in Fig.2. Significant values (n=6,
bers or producing other quantitative information. Field
p<0.05) are shaded in grey.
data on nesting population size or other reproduction
parameters are therefore lacking herein.
zone 1
zone 2
zone 3
zone 4
zone 5
zone 1
0.8286
0.715
0.886
-0.6
The non-parametric Spearman rank correlation coeffi-
zone 2
0.99
0.715
-0.714
cient was used to assess correlation in temporal variation
zone 3
0.543
-0.77
zone 4
-0.2
of C. caretta nesting densities along different coastal sec-
tions in the Mediterranean (Fig.1, Fig.2 ; Table 2). Data
for Kyparissia Greece were adapted after M
Application of rank correlation on marine turtle nesting
ARGARI-
data may raise the point of temporal pseudo-replication,
TOULIS & REES (2001). Data in Cyprus were adapted after
G
as the compared "replicates" (in this case, nesting densi-
ODLEY et al. (1998) ; BRODERICK et al. (1997) ; GODLEY
& K
ties as estimated in different zones for each year) are not
ELLY (1996) ; BRODERICK & GODLEY (1995) ; GOD-
truly independent (KREBS, 1989) ; the fact that individual
LEY & BRODERICK (1994) and BRODERICK & GODLEY
1993. According to G
marine turtles return to nest every 2-3 years to the same
ODLEY et al. (1998), the methodol-
ogy of nest number assessment has changed little through
geographical zone (MILLER, 1997) gives rise to dependent
this time period so primary data on nesting numbers is
data along the entire time series. Yet, it is assumed that, as
considered as being already standardised. Coastal zone
this is a general phenomenon in marine turtle populations,
lengths were taken after G
the same bias will be reflected along any time series of
ODLEY & BRODERICK (1992) ;
these zones include virtually the same beaches from one
marine turtle nesting density data, so the correlation anal-
year to the other (B
ysis may proceed by ignoring it.
RODERICK & GODLEY, 1993).
RESULTS
70
60
Sardinia - Italy, 1990 and 1991
50
This short term EC project was undertaken in the
40
Beach section
absence of any previous comprehensive survey for nest-
A-C
30
ing in Sardinia and in the light of increasing pressures
Beach section
from tourism along the coastline. Past reports had indi-
20
D-K
cated scarce nesting of C. caretta in the western part of
10
Nesting density (nests/km)
Sardinia, and in the east within the Gulf of Orosei
0
(GROOMBRIDGE, 1990 and references therein). The survey
1984 1985 1986 1987 1988 1989
was repeated in July 1991. No evidence of nesting activ-
Years
ity was recorded in either survey despite evaluation of a
few beaches (especially in East Sardinia) as potential
Figure 1
Fig. 1. Nesting density comparison between adjacent beach
sections in Kyparissia, Peloponnisos-Greece (data after MARGA-
nesting sites (Table 1). Fishermen confirmed a continuing
RITOULIS & REES 2001).
presence of adult and sub-adult C. caretta offshore.
There has been no recent information to confirm C.
caretta nesting in Sardinia and it is now considered
16
improbable. As individual C. caretta recorded in the Gulf
14
of Naples showed movements that extended well over
)
2000 km, (BENTIVEGNA, 2002), it is possible that turtles
12
observed along the Sardinian coast could be from popula-
10
zone 1
tions nesting in other parts of the basin. Although turtle
zone 2
nesting in the Western Mediterranean is almost non-exist-
8
zone 3
ent nowadays, a recent report has indicated nesting activ-
zone 4
6
ity of C. caretta on the Spanish Mediterranean coast
zone 5
(TOMÁS et al., 2003).
4
Nesting density (nests/km
2
Northern Aegean Sea (mainland and islands) 1991
0
During the summer of 1991, 2078 km of the North
1993
1994
1995
1996
1997
1998
Aegean coast were surveyed for C. caretta nesting,
Years
including the islands of Thassos, Limnos, Lesvos and
Samothraki (Table 1). Further surveys were carried out in
Fig. 2. Nesting density comparisons between adjacent coastal
July and August on beaches considered most suitable for
zones along the northern shore of Cyprus (data after references
nesting ; dune systems and coastal pollution were also
mentioned in text)
recorded. Despite the presence of potentially suitable
sites, the only nesting evidence found was a false track
recorded on the island of Limnos: the authors speculated
274
Lily Venizelos, Kalliopi Papapavlou, Marc-Antoine Dunais and Calliope Lagonika
that despite the presence of apparently suitable beaches,
in July 1998 (Table 1). This report also included primary
unfavourable climatic conditions may deter turtles from
data that had originated from an independent survey
nesting. Five young loggerheads (carapace length 20-25
undertaken in 1996 between Sirte and Misratah (in LAU-
cm) found dead in the area indicated, however, that a
RENT et al., 1999) (Table 1).
nearby shallow water area could be a foraging site for
The extrapolation method applied in 1995 to deduce
juveniles.
marine turtle nesting numbers along the whole Libyan
A later survey also reports no indication of C. caretta
coast (LAURENT et al., 1995) has since been criticised (see
nesting in the Northern Aegean mainland and islands
"discussion"). Three beaches along the eastern part were
(MARGARITOULIS et al., 1995 ; MARGARITOULIS & DRE-
resurveyed in 1999 (HADDOUD & EL GOMATI, in press).
TAKIS, 1991). Recent estimates of the overall nesting
activity of C. caretta in Greece contain no reference to
Lebanon 2001
nesting in that area (MARGARITOULIS, 2000). Occasional
"diffuse" nesting, however, may occur but on a very small
During summer 2001, an assessment was carried out in
scale.
order to locate potential nesting sites along the Lebanon
coast (Table 1). Evidence of marine turtle nesting was
Syria, 1991
recorded for five sites: On one of these, nesting by both
C. caretta and C.mydas was confirmed. Egg predation
The entire Syrian coast was surveyed for the first time
especially by canids was heavy at all sites. A number of
in June 1991 (Table 1). Most evidence of nesting was
beaches where past nesting had been reported, were found
recorded between Jablah and Latakia. The predation rate
to be the subject of severe erosion, and in some cases had
was 100%, mostly due to stray dogs and humans. Sea-
disappeared completely; sand extraction from beaches,
borne plastic garbage contamination was found, as well as
dunes, offshore sand dredging and unplanned sediment
raw sewage being piped directly into the sea.
removal from river beds for construction and military
To our knowledge, since the 1991 survey no compara-
purposes were seen as definitive causes of erosion along
tive data have appeared. Information on nesting species in
the Lebanese coast. Sea-borne garbage pollution was also
Syria is still speculative.
recorded in some areas.
Egypt (northwest coast), 1993
DISCUSSION
A comprehensive survey with ground patrols along the
western part of the Egyptian Mediterranean coastline took
Through several years of research, we have achieved
place in June and July 1993 (Table 1). Despite several
greater insight into the nesting beaches of Caretta caretta
informal reports by fishermen and others of C. caretta
and Chelonia mydas (Fig. 3). Although Greece and Tur-
occurrence in the sea, nesting evidence was scarce. This
key host a large percentage of the Mediterranean C.
research indicated the exploitation of both C. caretta and
caretta nesting population (MARGARITOULIS, 2000 ; YERLI
C. mydas products in Alexandria and contributed to the
& DEMIRAYAK, 1996) and C. mydas nesting sites are
formulation of Egypt's first conservation law 4/1994,
mainly confined to Cyprus and Turkey (KASPAREK et al.,
which includes protection of marine turtles.
2001), there is now substantial evidence of small nesting
The entire Egyptian coastline, including the part
populations for both species in other countries of the
between Alexandria and El-Salum, was reassessed for
Mediterranean.
nesting evidence in 1998 (data reviewed in CAMPBELL et
In Sardinia, the absence of any signs of nesting activity
al., 2001). Fieldwork confirmed the 1993 survey conclu-
suggests that nesting there is improbable although fisher-
sion, that nesting activity at the north-western part of the
men commonly report
Egyptian Mediterranean coast is negligible, whereas most
C. caretta by-catch. Nesting in the northern Aegean is
nesting occurs in the area to the east of Port Said (North
equally unlikely. Evidence from Syria is confined to the
Sinai) (Table 1).
1993 data, which is insufficient for adequate classifica-
Enforcement of the law against trade in marine turtle
tion of the beaches; further research is advisable, espe-
products in Egypt has now increased following a recent
cially in view of the encouraging recent discovery of C.
campaign by MEDASSET and local NGOs (VENIZELOS &
mydas nesting on the neighbouring Lebanon coast, and
NADA, 2000).
the important nesting beaches over the Turkish border. In
Egypt, it appears that few turtles nest to the west of Alex-
Libya 1995 & 1998
andria, and small numbers of C. caretta and C. mydas
The north-eastern part of the Libyan coast, between
breed in Sinai, although offshore populations are report-
Sirte and the Egyptian border (1195 km) was inspected
edly significant.
during June - July 1995, the first survey of the area out-
The situation in Libya remains debatable. Past assess-
side the Kouf National Park (SCHLEICH 1987). The major-
ments that employed extrapolation to determine the status
ity of the beaches were inspected only once with evidence
of the nesting population of C. caretta (LAURENT et al.,
of C. caretta nesting (Table 1). The authors speculated,
1995 ; 1999), have attracted criticism as this methodology
after extrapolating from the data collected, that the total
implies random or regularly spaced nesting in order to
annual number of C. caretta nests made in Libya could be
give rise to realistic estimations, and opposes the general
estimated at around 9000 nests per season (LAURENT &
trend of aggregated emergence and nesting observed in
AL, 1995). The northwest part of the Libyan coast
long-term datasets. C. caretta for example, displays a
between Misratah and the Tunisian border was inspected
highly aggregated distribution of nesting in Kyparissia,
Marine turtle research in some previously unsurveyed marine turtle nesting sites of the Mediterranean
275
Greece (Fig.1) and temporal variation in nesting density
Except for some cases of sporadic nesting, we are not
correlates positively between beaches, indicating a con-
aware of any data from within the Mediterranean indicat-
sistent trend in time and non-random nesting (r = 1,
ing random or regularly spaced nesting patterns. There-
s
p<0.05). C. caretta nesting density comparisons between
fore, we feel that there is insufficient evidence to employ
adjacent coastal zones along the northern shore of Cyprus
extrapolation of nesting densities from one beach to
also indicate a similar trend, although not in all cases
another; nesting numbers produced in this way are, in our
(Fig.2, Table 2). Analogous patterns are reported from
opinion, unrealistic (see also comments in MARGARI-
other geographical areas e.g. Florida, U.S.A. (MATTISON
TOULIS & REES, 2001).
et al., 1994) and Turkey (TÜRKOZAN & BARAN, 1996).
Fig. 3. Marine turtle nesting surveys in the Mediterranean (drawing not to scale).
With the exception of the major loggerhead nesting
Although they very rarely change their nesting site,
sites in Greece, important nesting sites in Cyprus (BROD-
marine turtles are known to occasionally migrate to other
ERICK & GODLEY, 1996, DEMETROPOULOS & HATZIHRISTO-
nesting beaches as a result of disturbance (MARGARI-
FOROU, 1995) and certain beaches in Turkey (YERLI &
TOULIS, 1998) or natural causes. Because of the possibility
DEMIRAYAK, 1996), we are aware of only a few longterm
of natural disasters etc. wiping out a nesting area, it is of
projects monitoring marine turtle nesting in the Mediter-
paramount importance that the future viability of marine
ranean. It is suggested that research should shift towards
turtle populations in the Mediterranean does not solely
more elaborate research projects with standardized moni-
rely on the few major rookeries, but includes protection of
toring procedures for the rest of the significant breeding
some areas with comparatively low nesting numbers such
sites within the basin, with further studies of pelagic pop-
as the Kuriat Islands in Tunisia, where 13 nests were
ulations. Conservation priorities include enforcement of
recorded in 2000 (JRIBI et al., 2002). There is an urgent
protective legislation, management of nesting areas, pro-
need to establish zones of maximum protection at inter-
tection of foraging and wintering areas and migratory
vals around the entire Mediterranean coastline on beaches
routes, and a limit to the impact of fisheries (Action Plan
favourable to turtle nesting, and in important pelagic for-
aging areas. A well-managed international network of
for the Conservation of Mediterranean Marine Turtles,
protected areas would go a long way towards assuring the
UNEP/MAP-RAC/SPA). These efforts, however, are
survival of all life stages of marine turtles. Currently, an
undermined by difficulties in the implementation of pro-
attempt is being made to set up a Mediterranean Sea Tur-
tective legislation, and lack of knowledge of foraging area
tle Conservation Network in a regional effort to enhance
ecology and the pelagic stages of these species. It is espe-
collaboration between sea turtle research and conserva-
cially important that international cooperation efforts
tion organizations around the Mediterranean.
should go beyond mere protection of nesting beaches :
Foraging habitats of the Mediterranean populations are
marginally known but recent satellite data agree with
REFERENCES
older information, mainly derived indirectly from arti-
sanal fisheries by-catch (V
BENTIVEGNA, F. (2002). Intra-Mediterranean migrations of log-
ENIZELOS & NADA, 2000),
gerhead sea turtles (Caretta caretta) monitored by satellite
showing that North Africa is probably an important forag-
telemetry. Marine Biology, 141 : 795-800.
ing area where turtles may hold distinct home ranges
BRODERICK A.C. & B.J. GODLEY (1993). Glasgow University
(GODLEY & AL, 2002).
turtle conservation expedition to northern Cyprus : 1993
276
Lily Venizelos, Kalliopi Papapavlou, Marc-Antoine Dunais and Calliope Lagonika
expedition report. Marine Turtle Research Group, Division
KASPAREK M. (1991). Marine turtles in Greece Results of a
of Environmental and Evolutionary Biology, University of
survey of potential nesting beaches in the northern Aegean
Glasgow, Glasgow Scotland.
Sea. Report submitted to the EEC by MEDASSET under
BRODERICK A.C. & B.J. GODLEY (1995). Glasgow University
Contract No. 6610 (90) 4313.
turtle conservation expedition to northern Cyprus : 1995
KASPAREK M. (1993). Marine turtles conservation in the Medi-
expedition report.
terranean Marine turtles in Egypt. Phase I, Survey of the
BRODERICK A.C. & B.J. GODLEY (1996). Population and nesting
Mediterranean coast between Alexandria and El-Salum.
ecology of the green turtle, Chelonia mydas, and the logger-
Project by : MEDASSET, National Centre of Oceanography
head turtle, Caretta caretta, in northern Cyprus. Zoology in
and Fisheries (Alexandria, Egypt) & RAC/SPA.
the Middle East, 13 : 27-46.
KASPAREK M. (1994). Marine turtles conservation in the Medi-
BRODERICK, A.C., F.GLEN, B.J. GODLEY, A. KELLY & G. C. HAYS
terranean Marine turtles in Syria. Survey of the Syrian
(2002). Estimating the number of green and loggerhead tur-
coast. Project by : MEDASSET & HCI.
tles nesting annually in the Mediterranean Oryx, 36 : 227-
KASPAREK, M., B.J. GODLEY & A.C.BRODERICK (2001). Nesting
235.
of the Green Turtle Chelonia mydas, in the Mediterranean : a
BRODERICK, A.C., B.J. GODLEY, A. KELLY & A. MCGOWAN
review of status and conservation needs. Zoology in the Mid-
(1997). Glasgow University turtle conservation expedition to
dle East, 24 : 45-74.
northern Cyprus 1997 : Expedition Report.
KREBS C.J. (1989) : Ecological methodology. Harper Collin
BRUNDTLAND G. H. (1997). The scientific underpinning of pol-
Publishers, USA.
icy. Science, 277 : 457.
LAURENT L. (1998) : Review and analysis of the available
CAMPBELL, A.C., M. CLARKE, S. GHONEIM, W.S. HAMEID,
knowledge of marine turtle nesting and population dynamics
C. SIMMS & C. EDWARDS (2001). On status and conservation
in the Mediterranean. UNEP (OCA) MED WG. 145/Inf.3,
of marine turtles along the Egyptian Mediterranean Sea
RAC/SPA, Tunis, Tunisia.
coast : results of the Darwin Initiative Sea Turtle Conserva-
LAURENT, L., M.N. BRADAI, D.A. HADOUD & H.M. EL-GOMATI
tion Project 1998-2000. Zoology in the Middle East, 24 : 19-
(1995). Marine turtle nesting activity assessment on Libyan
29.
coasts. Phase 1 : survey of the coasts between the Egyptian
DEMETROPOULOS A. & M. HADJICHRISTOPHOROU (1995). Manual
border and Sirte. Report of a joint project by : Marine Biol-
on marine turtle conservation in the Mediterranean. MAP-
ogy Research Centre (Tajura, Libya), MEDASSET, RAC/
UNEP, IUCN, Ministry of Agriculture, Natural Resources
SPA (MAP-UNEP), Technical Centre for Environmental
and Environment Cyprus Cyprus Wildlife Society.
Protection (TCEP, Tripoli), WWF International Mediterra-
DEMIRAYAK, F., L. VENIZELOS, R. SADEK, S. HRAOUI-BLOQUET &
nean Programme.
M. KHALIL (2003). Marine turtle conservation in the
LAURENT, L., M.N. BRADAI, D.A. HADOUD, H.M. EL-GOMATI &
Mediterranean Lebanon : a first survey for Chelonia
A.A. HAMZA (1999). Marine turtle nesting activity assess-
mydas and Caretta caretta nesting in Lebanon. In : Proceed-
ment on Libyan coasts. Phase 3 : survey of the coast to the
ings of the 22nd Annual Symposium on Sea Turtle Biology
west of Misratah. Report of a joint project by : Marine Biol-
and Conservation, 4-7 April 2002, Miami U.S.A., NOAA
ogy Research Centre (Tajura, Libya), MEDASSET, RAC/
Technical Memorandum NMFS-SEFSC-503 : 24-25.
SPA (MAP-UNEP), Technical Centre for Environmental
GODLEY B.J., S.RICHARDSON, A.C. BRODERICK, M.S.COYNE,
Protection (TCEP, Tripoli), WWF International Mediterra-
F.GLEN & G.C. HAYS (2002) : Long-term satellite telemetry
nean Programme.
of the movements and habitat utilization by green turtles in
MARGARITOULIS, D. (1998). Interchange of nesting loggerheads
the Mediterranean. Ecography, 25 : 352-326.
among Greek beaches. In : EPPERLY S.P. & J.BRAUN (com-
GODLEY, B.J., R. THOMPSON & A.C. BRODERICK (1998) : Glas-
pilers), Proceedings from the 17th Annual Workshop on Sea
gow University turtle conservation expedition to northern
Turtle Biology and Conservation, 4-8 March 1997, Florida -
Cyprus 1998 : Expedition Report.
U.S.A, NOAA Technical Memorandum NMFS-SEFSC-
GODLEY B.J. & A.C. BRODERICK (1992) : Glasgow University
415 : 225-227.
turtle conservation expedition to northern Cyprus 1992 :
MARGARITOULIS, D. (2000). An estimation of the overall nesting
Expedition Report. Marine Turtle Research Group, Division
activity of the loggerhead turtle in Greece. In : ABREU
of Environmental and Evolutionary Biology, University of
GROBOIS F.A., R. BRISEÑODUEÑAS, R. MARQUES & S. SARTI
Glasgow, Glasgow Scotland.
(eds), Proceedings of the 18th International Sea Turtle Sym-
GODLEY B.J. & A.C. BRODERICK (1994) : Glasgow University
posium U.S. Department of Commerce, NOAA Technical
turtle conservation expedition to northern Cyprus 1994 :
Memorandum : 48-50.
Expedition Report.
MARGARITOULIS, D. & M. DRETAKIS (1991). Determination of
GODLEY B.J. & A. KELLY (1996) : Glasgow University turtle
nesting habitats of Caretta caretta in Greece 1990-1991.
conservation expedition to northern Cyprus 1996 : Expedi-
Final report submitted to the EEC (DGXI) on contract
tion Report.
B6610(90) 3588.
GROOMBRIDGE B. (1990). Marine turtles in the Mediterranean :
MARGARITOULIS, D. & A.F. REES (2001). The loggerhead turtle,
distribution, population status, conservation. Nature and
Caretta caretta, population nesting in Kyparissia Bay, Pelo-
Environment Series, No 48.
ponnesus, Greece : Results of beach surveys over seventeen
HADDOUD D. A. & H.M. EL-GOMATI : A general assessment of
seasons and determination of the core nesting habitat. Zool-
marine turtle nesting activity on the whole Libyan coast. In :
ogy in the Middle East, 24 : 75-90.
Proceedings of the 1st Mediterranean Conference on marine
MARGARITOULIS, D., R. ARGANO, I. BARAN, F. BENTIVEGNA,
turtles, Rome, 24-28 October 2001 (in press).
M.N. BRADAI, J.A. CAMIÑAS, P. CASALE, G. DE METRIO, A.
HILTON TAYLOR C. 2000 (COMP.) (2000). IUCN Red List of
DEMETROPOULOS, G. GEROSA, B.J. GODLEY, D.A. HADDOUD,
Threatened species. IUCN Gland Switzerland.
J. HOUGHTON, L. LAURENT & B. LAZAR (2003). Loggerhead
JRIBI, I., M.N. BRADAI & A. BOUAIN (2002). Marine turtle nest-
turtles in the Mediterranean : present knowledge and conser-
ing in Kuriat Islands, Tunisia, 2000. Marine turtle newslet-
vation perspectives. In : Proceedings from the 20th Annual
ter, 96 : 4-6.
Workshop on Sea Turtle Biology and Conservation, 4-8
KASPAREK M. (1995). The nesting of marine turtles on the coast
March 1997, Florida U.S.A., NOAA Technical Memoran-
of Syria. Zoology in the Middle East, 11 : 51-62
dum NMFS-SEFSC-503 : 175-197.
Marine turtle research in some previously unsurveyed marine turtle nesting sites of the Mediterranean
277
MARGARITOULIS, D., M. DRETAKIS & A. KOTITSAS (1995). Dis-
NOAA Technical Memorandum NMFS-SEFSC-503 : 166-
covering new nesting areas of Caretta caretta in Greece. In :
167.
RICHARDSON J.I. & T.H. RICHARDSON (compilers), Proceed-
TÜRKOZAN O. & I. BARAN (1996). Research on the loggerhead
ings of the 12th International Sea turtle Symposium, 25-19
Caretta caretta of Fethiye Beach. Turkish Journal of Zool-
February 1992, Georgia U.S.A., NOAA Technical Memo-
ogy, 20 : 183-188.
randum NMFS-SEFC-361 : 214-216.
VENIZELOS L. (1993). MEDASSET's marine turtle research
MATTISON, C., C.BURNEY & L.FISHER (1994). Trends in the spa-
projects in six Mediterranean areas : results, recommenda-
tial distribution of sea turtle activity on an urban beach
tions for conservation and recovery. Testudo, 3 : 54-64.
(1981-1992). In : SCHROEDER B.A. & B.W. WITHERINGTON
VENIZELOS L. & M.A. NADA (2000). Exploitation of loggerhead
(compilers), Proceedings of the 13th Annual Sea turtle Sym-
and green turtles in Egypt : good news? Marine turtle News-
posium on Sea Turtle Biology and Conservation, 23-27 Feb-
letter, 87 : 12.
ruary 1993, Jekyll Island, Georgia U.S.A., NOAA Techni-
VENIZELOS L. & M. KASPAREK (1996). Marine turtles in Egypt :
cal Memorandum NMFS-SEFC-341 : 102-104.
results of a coastal assessment by MEDASSET of the Medi-
M
terranean coast between Alexandria and El-Salum (1993).
ILLER J.D. (1997). Reproduction in sea turtles In : LUTZ &
In : K
M
EINATH J.A., D.E. BARNARD, J.A.MUSICK & B.A. BELL.
USICK (eds), The biology of sea turtles, CRC Marine Sci-
ence Series : 51-81.
(compilers), Proceedings of the 15th International Sea turtle
Symposium, 20-25 February 1995, South Carolina U.S.A.,
SCHLEICH H.H. (1987). Contributions to the herpetology of Kouf
NOAA Technical Memorandum NMFS-SEFC-387 : 329-
national Park (NE-Libya) and adjacent areas. Spixiana,
333.
10(1) : 37-80.
WHITMORE C., R. JESU & P. REYNOLDS (1991). Sardinia an
TOMÁS J., J.L.MONS, J.J.MARTÍN, J.J.BELLIDO & J.J.CASTILLO
assessment of beaches for loggerhead turtle nesting. Report
(2003). First nesting activity of the loggerhead sea turtle,
submitted to the EEC by MEDASSET under Contract No.
Caretta caretta, in the Spanish Mediterranean coast. In :
6610 (90) 4313.
Proceedings of the 22nd Annual Symposium on Sea Turtle
YERLI S. & F. DEMIRAYAK (1996). Marine turtles in Turkey : a
Biology and Conservation, 4-7 April 2002, Miami U.S.A.,
survey on nesting site status. DHKD.
Belg. J. Zool., 135 (2) : 279-286
July 2005
Origin and vectors of introduction of exotic molluscs in
greek waters
A. Zenetos1, D. Koutsoubas2* and E. Vardala-Theodorou3
1 Hellenic Centre for Marine Research, Institute of Oceanography, GR-19013, Greece
2 Department of Marine Science, Fac. of Environment, University of the Aegean, GR-81100, Mytilene, Greece
3 Goulandris Natural History Museum, 14562, GR-Kifissia, Athens, Greece
Corresponding author : Drosos Koutsoubas, e-mail address : drosos@aegean.gr
ABSTRACT. Exotic species of macrophytes, invertebrates and fish have become increasingly prominent in most
coastal habitats in the Mediterranean Sea, the Greek waters included, over the last decades. It is well established
that the introduction of non-indigenous species has significant ecological as well as economic impact in the Medi-
terranean Sea. A review of the exotic molluscan records in Greek waters revealed a total of 26 species (16 Gastrop-
oda, 10 Bivalvia). Nine species are of Indo-Pacific and Erythrean origin, and are already well established in the
Eastern Mediterranean. The occurrence of these species in the Greek Seas is attributed to progressive penetration
through the Suez Canal, the so-called Lessepsian migration. Four species, namely the gastropods Nerita sanguino-
lenta, Haminoea cyanomarginata, Melibe fimbriata and the bivalve Pseudochama corbieri, are Red Sea endemic
and Indo-Pacific biota, which have been first sighted in Greek waters and to date have a limited distribution in the
entire Mediterranean. Another four species, the gastropods Crepidula fornicata and Polycerella emertoni and the
bivalves Petricola pholadiformis and Mya arenaria, which originate from the Atlantic and occur in ports/lagoons,
may have entered via shipping and/or aquaculture. The gastropods Strombus persicus and Rapana venosa and the
bivalves Anadara demiri and Crassostrea gigas are of Pacific, Indian Ocean or Persian Gulf origin and the vector of
their introduction, though not documented, is presumed to be shipping or aquaculture. The rate of molluscan intro-
ductions in Greek waters is increasing exponentially with time : 13 out of the 26 species have been recorded since
1990, and further studies may reveal many more.
KEY WORDS : Mollusca, Exotic Species, Introduction, Greek Seas, Mediterranean
INTRODUCTION
increased from 44 (POR, 1978) to 137 (GOFAS & ZENETOS,
2003).
The vectors of introduction of exotic species to the
Mediterranean are diverse : migration through the Suez
A review of the Greek marine exotic biota has revealed
Canal, thoroughly analyzed by P
that molluscs predominate among the 78 exotic species
OR (1978, 1990) also
termed `lessepsian migration' ; migration through the
that have been recorded to date (PANCUCCI - PAPADOPOU-
Gibraltar Straits (C
LOU et al., 2003). The first exotic mollusc reported from
ATTANEO-VIETTI & THOMPSON, 1989) ;
transport on ship hulls and with ballast waters ; inten-
the Greek seas is the Erythrean bivalve species Pseudo-
tional introductions (mariculture) and accidental intro-
chama corbieri (Jonas, 1946) found in Saronikos Gulf in
ductions accompanying intentionally introduced species ;
the South Aegean (RALLI-TZELEPI, 1946). The CIESM
market discards ; escape from aquaria (Z
atlas enumerates 26 exotic molluscs (ZENETOS et al.,
IBROWIUS, 1992).
The Suez Canal has been the largest pathway for the entry
2003).
of invaders in the Mediterranean Sea and more than 300
The majority of the exotic Gastropod species recorded
Erythrean species principally molluscs, fish, decapod
from the Greek Seas has arrived as Lessepsian invaders
crustaceans, polychaetes and algae - have become estab-
(KOUTSOUBAS, 1992). However, other ways of invasion of
lished in the Eastern Mediterranean, primarily in the
these species should also be taken into consideration, e.g.
Levantine Basin. The rate of these biological invasions
invasion through human activities and/or entrance via the
has increased in recent decades, and "they collectively
Gibraltar Straits (see review by KOUTSOUBAS & CINELLI,
have significant ecological and economic impacts in the
1997). Considering the rate of introduction, an updated
Mediterranean Sea" (GALIL, 2000).
inventory is needed of exotic molluscs, to include recent
Given the rate and extent of the phenomenon, some
findings and extend the zoogeographical distributions,
national monitoring projects in countries bordering the
thus providing further insight to the modes of introduc-
Mediterranean have focused on introduced species. The
tion. Furthermore, and despite intensive research effort
International Commission for the Scientific Exploration
into the marine biodiversity in the Greek Seas, especially
of the Mediterranean Sea (CIESM) has published a digital
during the last two decades, which has resulted in reliable
atlas of exotic species in the Mediterranean (fish, crusta-
molluscan inventories (e.g. ZENETOS, 1996 ; KOUTSOUBAS
ceans and molluscs). According to the updated informa-
et al., 1997, 2000a, b ; DELAMOTTE & VARDALA-THEOD-
tion, the number of exotic molluscan species has
OROU, 2001) the ecological and economic impacts of the
280
A. Zenetos, D. Koutsoubas and E. Vardala-Theodorou
molluscan invaders in the Greek Seas have not been rec-
Origin and vectors of introduction of exotic mollusc
ognized so far.
species in the Greek seas
The present review aims to : 1) present an updated
checklist of the exotic mollusc species in Greek Waters,
Considering the origin of the exotic mollusc species
2) discuss in detail their origins, vectors and their rates of
recorded from the Greek Seas (Table 1) the majority are
introduction, 3) examine zoogeographical patterns of
Erythrean ones (five species from Red Sea, three from
these species in the Greek Seas and in the Eastern Medi-
Indian Ocean and Red Sea, four from Indo-Pacific Ocean
terranean.
and Red Sea), followed by those from the Indo-Pacific
oceans (five species). Very few species (four) originate
MATERIAL AND METHODS
from the Atlantic Ocean.
The work is a combined effort to compile all past and
Many of the Erythrean species, either well established
recent records of exotic molluscs in the Greek Seas up
in the Eastern Mediterranean (Cylichna girardi, Burs-
until April 2002. To this end, part of the information is
atella leachi, Brachidontes pharaoni, Malfuvundus regu-
derived from : the ongoing CIESM ATLAS project (see
lus, Gastrochaena cymbium), or accidental (Cellana rota,
www.ciesm.org/atlas) ; unpublished data of the authors'
Trochus erythraeus, Murex forskoehli, Pseudochama cor-
research efforts on molluscs in the Greek Seas over the
bieri) occur in the Suez Canal and therefore their finding
last 20 years ; data originated from the gray literature (e.g.
in the Greek coasts should be attributed to progressive
Technical Reports). Of the many terms (aliens, intro-
penetration through the Suez Canal (Lessepsian migra-
duced, invaders, exotic, non-indigenous species) cur-
tion) (Fig. 1). The same pathway (?Lessepsian) is sus-
rently used to define species introduced from one sea to
pected to be the mode of introduction of another seven
another via any vector of introduction, we have chosen to
mollusc species that are either Red Sea endemics (Nerita
adopt the term exotic in the sense used by CIESM. The
sanguinolenta, Acteocina mucronata, Haminoea
taxonomy used in this study is that used for Red Sea mol-
cyanomarginata) or Indo-Pacific species (Smaragdia sou-
lusc species (OLIVER, 1992 ; DEKKER & ORLIN, 2000). In
order to define the rate of introduction of the exotic mol-
verbiana, Rapana rapiformis, Bulla ampulla, Melibe fim-
luscs a special effort was made through the Goulandris
briata) (Fig. 1). These species, however, are absent from
Natural History Museum collections, the authors'
the Suez Canal and have, to date, a limited distribution in
research collections, and amateur collectors collections
the Eastern Mediterranean. The Indo-Pacific oyster spe-
available to the authors to trace, to the degree possible,
cies Crassostrea gigas is the most widely distributed oys-
the true dates of appearance of the species in Greek
ter introduced word-wide in temperate to tropical seas
waters. On presenting the zoogeographical distribution of
and its presence in the Greek Seas should be attributed to
the exotics within the Greek Seas, different physicochem-
aquaculture. The opisthobranch Atlantic species Polycer-
ical and dynamic processes were encountered leading to
ella emertoni has been found in the Mediterranean in
the division suggested by THEOCHARIS et al. (1993) i.e.
ports or lagoons close to ports, and shipping is speculated
Ionian Sea, the Sea of Kythira, the Aegean Sea and the
to be the most likely introduction vector. Finally certain
Libyan Sea. Given the importance of ports, a more
species may have followed more than one route. In other
detailed division included Saronikos and Thermaikos
cases pathways of introduction remain unknown, even if
Gulfs (in the South and North Aegean correspondingly)
shipping is assumed to be the most likely vector of their
where the main Greek ports are situated.
transport since their occurrence is patchy and associated
with ports and/or they are fouling organisms on ship hulls
RESULTS
or ballast tanks (Fig. 1). The species with a two-mode
introduction or introduction via shipping are presented in
Records and composition of exotic mollusc species in
detail below :
the Greek seas
The examined material in authors' collections along
SH
with a review of the relevant literature has revealed that to
?LES
4%
AQ
UN/SH
date 26 exotic mollusc species have been recorded from
24%
4%
24%
the Greek Seas. These species are presented in phyloge-
netic order in Table 1. Very few species, namely the gas-
tropods Strombus persicus, Bursatella leachi, Melibe fim-
Unknown
briata and the bivalves Brachidontes pharaonis, Pinctada
31%
radiata, are well established in the Greek Seas. Certain
other species i.e. Crepidula fornicata, Rapana venosa,
LES/SH
Bulla ampulla, Anadara demiri and Fulvia fragilis are
LES
LES/AQ
4%
36%
4%
met in large populations but are locally established. The
remaining species have been reported from a single site
and usually from a single individual indicating that their
Fig. 1. Vectors of introduction of exotic mollusc species
presence in the Greek Seas could be considered as acci-
recorded in Greek Seas. LES = Lessepsian migration ; AQ =
dental.
Aquaculture ; SH = Shipping ; UN = Unknown
Origin and vectors of introduction of exotic molluscs in Greek waters
281
TABLE 1
Findings, Records, Composition and Origin of Exotic Mollusc species in Greek Seas. o : Species in authors'
collections ; * : Additional record in the Greek Seas this study ; is. = island ; G = Gulf
1st
Citations
Sites of Greek Seas
Exotic Mollusc Species
Origin
Finding
in the Greek Seas
Reported
GASTROPODA
PROSOBRANCHIA
NACELLIDAE
Cellana rota (Gmelin, 1791)
1989
Fountoulakis & Sabelli, 1999
Saronikos G.
IO, RS
NERITIDAE
Smaragdia souverbiana (Montrouzier, 1863)
1994
Buzzurro & Greppi, 1994
Rhodes is.
IP, RS
Nerita sanguinolenta Menke, 1829
1968
Nordsieck, 1973
Karpathos is.
RS
TROCHIDAE
Trochus erythraeus Brocchi, 1821
1994
Cosenza & Fasulo, 1997
Crete is.
RS
STROMBIDAE
oStrombus persicus Swainson, 1821
1986
Nicolay, 1986
Rhodes is, **Argolikos G.,
PG, AS
**Lakonikos G.
CALYPTRAEIDAE
oCrepidula fornicata (Linnaeus, 1758)
1994
Delamotte & Vardala-Theodorou, 1994 Saronikos G., Evoikos G.
WA
MURICIDAE
Murex forskoehli Roeding, 1798
1966
Settepassi, 1967
Saronikos G.
RS, AS
oRapana venosa (Valenciennes, 1846)
1991
Koutsoubas & Voultsiadou-Koukoura
Thermaikos G.
PO
1991
Rapana rapiformis (Von Born, 1778)
1970
Barash & Danin, 1988/89
Rhodes is.
IP
OPISTHOBRANCHIA
BULLIDAE
oBulla ampulla Linnaeus, 1758
1999
Vardala-Theodorou, 1999
Saronikos G., **Argolikos G. IP
HAMINOEIDAE
Haminoea cyanomarginata Heller & Thompson, 1983
2001
Gosliner & Mollo (unpublished data)
**Korinthiakos G.
RS
CYLICHNIDAE
Acteocina mucronata (Philippi, 1849)
1997
Storsberg, 1997
Naxos is.
RS
RETUSIDAE
Cylichna girardi (Audouin, 1826)
1994
Cosenza & Fasulo, 1997
Crete island
IP
APLYSIIDAE
oBursatella leachi De Blainville, 1817
1986
Barash & Danin, 1986; Koutsoubas,
Chios is., Lesvos is., **Ther- IP
1992
maikos G., **Chalkidiki
POLYCERIDAE
oPolycerella emertoni Verrill, 1881
1995
Koutsoubas et al, 2000a
Gialova lagoon
EA
TETHYIDAE
oMelibe fimbriata Alder & Hancock, 1864
1982
Thompson & Crampton, 1984; Kout-
Astakos G., Kefallonia is.,
IP
soubas & Cinelli, 1997
Korinthiakos G., Milos is.
BIVALVIA
PTEROMORPHIA
ARCIDAE
oAnadara demiri (Piani, 1981)
**1993 Zenetos, 1994
Thermaikos G.
IO
MYTILIDAE
oBrachidontes pharaonis (Fischer P., 1870)
**1975 Koroneos, 1979; Tenekides, 1989
Rhodes is., Saronikos G.,
IO, RS
Evoikos G.
OSTREIDAE
Crassostrea gigas (Thunberg, 1793)
1989
Dimitrakis, 1989
Patraikos G., Korinthiakos G. PO
PTERIIDAE
oPinctada radiata (Leach, 1814)
1963
Serbetis, 1963; Nordsieck, 1969; Kallo- Rhodes is., Karpathos is.,
IP, RS
pissis, 1981; Kinzelbach, 1985; Barash Saronikos G., Evoikos G.,
& Danin, 1988/89; Zenetos, 1996
Lesvos is., **Lakonikos G.
MALLEIDAE
Malvufundus regulus (Forskål, 1775)
2001
Giannuzzi-Savelli et al., 2001
Simi is.
IP, RS
HETERODONTA
CHAMIIDAE
Pseudochama corbieri (Jonas, 1846)
1946
Ralli-Tzelepi, 1946
Saronikos G.
RS
CARDIIDAE
oFulvia fragilis (Forsskål in Niebuhr, 1775)
1999
Vardala-Theodorou, 1999
Saronikos G.
IO, RS
PETRICOLIDAE
oPetricola pholadiformis Lamarck, 1818
1994
Delamotte & Vardala-Theodorou, 1994 Evoikos G.
WA
MYIIDAE
oMya arenaria Linnaeus, 1758
**1984 Zenetos et al. 2003
Saronikos G.
EA
GASTROCHAENIDAE
oGastrochaena cymbium (Spengler, 1783)
**1974 Tenekides, 1989
Saronikos G.
IP, RS
Lessepsian migration Shipping
However, its recent finding in Saronikos Gulf, and in par-
ticular in Peiraew port, suggests transport via shipping, as
The Indo-Pacific bivalve Fulvia fragilis seems to have
all other areas in the Mediterranean from where it has
followed the typical distribution of a Lessepsian migrant.
reported are also in the vicinity of ports.
It has been recorded in the Suez Canal, in the coasts of
Israel, Tunisia and S. Turkey (www.ciesm.org/atlas).
282
A. Zenetos, D. Koutsoubas and E. Vardala-Theodorou
Lessepsian migration Aquaculture
should be rather attributed to shipping since the records of
the species are from areas near ports and away from areas
The pearl oyster Pinctada radiata was intentionally
where marine farms are located.
introduced to Greece for mariculture purposes, and has
since established thriving populations in the sites where it
Rate of introduction of exotic mollusc species in the
was firstly imported for aquaculture (i.e. Lesvos island,
Greek seas
Evoikos Gulf, Saronikos Gulf), but its recent finding in
Rhodes island and Lakonikos Gulf, where aquaculture
Thirteen out of the 26 exotic mollusc species have been
activities are absent, supports the Lessepsian mode of
recorded in the Greek Seas in the last decade (50% of the
introduction.
total number of exotic molluscs recorded so far from
these seas) thus implying an exponential rate of introduc-
Unknown Shipping
tion of these species in the Greek waters (Fig. 2). It is
worth mentioning that only during last year two species,
The gastropod Strombus persicus from the Persian Gulf
namely the gastropod Haminoea cyanomarginata and the
and Arabian Sea, was first recorded in the Mediterranean
bivalve Malvufundus regulus, have been recorded from
not far from the oil terminal in the south Turkish Bay of
the Greek Seas (GOSLINER & MOLO unpublished data and
Iskenderun. The species has not been recorded from the
GIANNUZZI-SAVELLI et al., 2001 correspondingly).
Red Sea, and its introduction in the Mediterranean could
be attributed to ships coming from the Persian Gulf
(OLIVERIO, 1995). However, the species has plank-
Cumulative Number of Species Per Year
totrophic larvae thus ensuring long-distance dispersal.
GALIL & ZENETOS (2002) argue that the rapid geographic
s 30
expansion and successful establishment of this species in
2
25
the Levantine basin is typical of a Lessepsian invader.
The slipper limpet Crepidula fornicata is assumed to have
20
been introduced in the Mediterranean by shipping related
15
to oyster/mussel commerce for farming. Its occurrence is
10
rather local in the Mediterranean (e.g. French coasts near
Toulon, Sicily - ZIBROWIUS, 1992). Presumably there
5
were separate introductions of cultivated bivalves from
Cumulative Number of Specie
0
the French Atlantic coast to the French Mediterranean
1940
1950
1960
1970
1980
1990
2000
2010
lagoons, and from unknown origin to the Italian and Mal-
Years
tese sites (GALIL & ZENETOS, 2002). The species has a
broad adaptive ability, extensive period of reproduction
Fig. 2. Rate of introduction of exotic mollusc species in the
with direct fecundation (through piling), together with the
Greek Seas.
absence of specific predators (BLANCHARD & ERHOLD,
1999). Its record from Saronikos Gulf and in particular
Comparing the appearance of the exotic mollusc spe-
close to Peiraeus port is related rather to shipping, as there
cies in the Greek Seas vs the Mediterranean Sea, we note
is no oyster/mussel farming in the broader area. Rapana
that six species (Smaragdia souverbiana, Nerita sangui-
venosa a gastropod native to the Sea of Japan was intro-
nolenta, Rapana rapiformis, Haminoea cyanomarginata,
duced in the Black Sea accidentally in the 40s and most
Melibe fimbriata, Pseudochama corbieri) are Red Sea
possibly independently in the Adriatic in the 70s. It has
endemic and Indo-Pacific biota that have been firstly
been speculated that the planktonic larvae of the species
sighted in Greek waters and then in the rest of the Medi-
arrived through ballast water in commercial ships, but a
terranean Sea. With the exception of Melibe fimbriata,
more likely scenario is that egg masses may have been
these species have a limited distribution in the entire
transported with the products of marine farming i.e. oys-
Mediterranean to date. On the contrary some of the very
ters or mussels. Its discovery in the northern Aegean Sea
first exotic mollusc species in the Mediterranean Sea that
near natural oyster and mussel banks in the bay of Thes-
entered that sea via the Suez Canal, colonized its eastern
saloniki (major port in the North Aegean) in the 90s
part and became locally abundant in the Levantine basin
(KOUTSOUBAS & VOULTSIADOU - KOUKOURA, 1991) is most
i.e. Lessepsian migrants, such as Murex forskoehli, Bra-
possibly related to shipping but transfer via the Darda-
chidontes pharaonis, Pinctada radiata and Malvufundus
nelle's strait should not be excluded. The bivalve Anad-
regulùs then later appeared in Greek waters after a time
ara demiri, originating from the China Seas, was reported
lapse of 60 to 98 years.
to dominate the degraded benthic ecosystems in Izmir
Bay (DEMIR, 1977) and Thessaloniki Gulf (ZENETOS,
Zoogeographical patterns of the exotic mollusc species
1994). The species seems to be well established in these
in the Greek seas
areas but its distribution in the Mediterranean remains
spotty. Though shipping seems to be the most likely vec-
Twenty one exotic mollusc species have been recorded
tor of introduction since the species, at least in the
from the Aegean Sea, four from the Ionian Sea, two from
Aegean, had been found in ports, its recent finding in the
the Sea of Kythira and one from the Libyan Sea (Fig. 3).
Central Adriatic does not exclude other introduction
Within the Aegean, the southern part is richer (19 spe-
modes. Petricola pholadiformis and Mya arenaria are
cies), and two major centres can be distinguished there :
bivalves imported for mariculture in Mediterranean
a) the Saronikos and Argolikos Gulfs, which are in the
lagoons. However, their occurrence in Greek waters
route of many ships towards Peiraeus (the biggest Greek
Origin and vectors of introduction of exotic molluscs in Greek waters
283
port), where 11 species have been recorded and b) the
nating from the Atlantic, which have extended their distri-
Dodekannese islands, which are located close to the
bution via different pathways into the Mediterranean.
Levantine basin, the main area of distribution of exotic
This point strengthens the statements of previous authors
species within the Mediterranean, where seven species
that although the major pool of exotic species invading
have been recorded. Also in the North Aegean, two major
the Mediterranean is Erythrean biota, the discovery of
centres can be seen ; a) Thermaikos Gulf (three species)
each species new to the inventory of the exotic flora and
and b) Evoikos Gulf (four species), which are both areas
fauna species should be interpreted with caution and its
where major ports are located.
origin be carefully examined (ZIBROWIUS, 1992 ; GALIL,
2000).
Molluscs are one of the `leading' groups of the Lessep-
sian migration, together with decapod crustaceans and
fishes (POR & DIMENTMAN, 1989). OLIVERIO (1995) has
discussed the use of the term "Lessepsian migration" and
concluded that this should not be used indiscriminately
for any species of Indo-Pacific origin found in the Medi-
21
terranean. A sensible use of the term is for species that
4
have worked their way through the Suez Canal and then
spread progressively into the Mediterranean. It is in this
2
sense that almost 35% of the Greek exotic mollusc spe-
cies (Cellana rota, Trochus erythraeus, Murex forskoehli,
1
Cylichna girardi, Bursatella leachi, Brachidontes
pharaoni, Pseudochama corbieri, Malvufundus regulus,
Gastrochaena cymbium), which are also successful in the
Canal itself, could be considered as true Lessepsian
Fig. 3. Number of exotic mollusc species recorded from the
migrants. Another seven Erythrean origin species (Nerita
different Greek Seas
sanguinolenta, Acteocina mucronata, Haminoea
cyanomarginata, Smaragdia souverbiana, Rapana rapi-
DISCUSSION
formis, Bulla ampulla, Melibe fimbriata) are suspected to
have penetrated via the same pathway, but because of no
Twenty six exotic molluscan species (16 Gastropoda
up-to-date records in the Suez Canal and their limited dis-
and 10 Bivalvia) have been collected in the Greek Seas
tribution in the entire Mediterranean, they are classified
during the last decades. These comprise less than 2.4% of
as suspected Lessepsian migrants.
the total number of mollusc species recorded so far in
Besides introduction through the Suez Canal, the next
Greek Waters (1095 species DELAMOTTE &. VARDALA-
major vectors of introductions of exotic marine biota in
THEODOROU, 2001).
the Eastern Mediterranean are shipping and then aquacul-
ture (GALIL & ZENETOS, 2002). This pattern is also valid
The majority of the exotic mollusc species in Greek
for the exotic molluscs recorded in Greek waters,
waters (61%) originate from the Indo-Pacific region or
although to be able to draw the line further investigation
are distributed in these oceans and the Red Sea. The next
is needed. Shipping has been considered the vector of
major component are Red Sea endemics (19%). This is
introduction for the opisthobranch mollusc Polycerella
also the case for other marine taxa with exotic representa-
emertoni and aquaculture for the bivalve species Crassos-
tives in the Mediterranean (POR, 1978). A major problem
trea gigas. However, transport via shipping routes and
when dealing with exotic mollusc species is to dismiss the
mariculture are considered to be the most likely vectors of
Mediterranean species that occur also in the Indo-Pacific
introduction of exotic mollusc species in the Greek waters
region, as `tethyan relicts' (CATTANEO-VIETTI & THOMP-
in certain cases for which a two-mode introduction
SON, 1989). A review of the palaeontological records
scheme has been assumed, where the true vector is still
shows that none of the exotic mollusc species reported so
unknown. Even if these two vectors are not the true vec-
far from the Greek waters were present in the area during
tors of introduction of exotic mollusc species in different
the Pleistocene. Were the aforementioned species present
parts of the Greek Seas, they may have been involved in
in the Mediterranean at earlier geological periods, they
combination with other pathways of introductions. For
should be found as fossils either under the recent mean
Strombus persicus and Fulvia fragilis Lessepsian migra-
sea level, if they lived during the last glaciation, or above
tion has been suggested by PASSAMONTI (1996), GALIL &
mean sea level, if they lived during warm periods. On
ZENETOS (2002) and shipping by OLIVERIO (1995).
reviewing the literature referring to the Upper Pleistocene
Although in the present study their vector of introduction
marine fossil Mollusca, from the warm periods of Tyrrhe-
has been characterized as unknown, Crepidula fornicata,
nian-Eutyrrhenian and Neotyrrhenian in Greek Seas, the
Rapana venosa, Anadara demiri, Petricola pholadiformis
aforementioned species did not occur as fossils (VARD-
and Mya arenaria were sampled in areas close to major
ALA-THEODOROU, 1999). This implies that the exotic mol-
ports, therefore shipping should be considered as the true
lusc species found so far in the Greek Seas are not relicts
vector of their introduction in the Greek waters. The pearl
of the past.
oyster Pinctada radiata has been imported in Greek
Only four out of the 26 exotic molluscs in the Greek
waters for aquaculture (KALOPISSIS, 1981) and viable pop-
Seas (Crepidula fornicata, Polycerella emertoni, Petri-
ulations have successfully established in the wild, but
cola pholadiformis and Mya arenaria) are species origi-
progressive penetration through the Suez Canal should
284
A. Zenetos, D. Koutsoubas and E. Vardala-Theodorou
not be excluded as the species has been recorded in other
or Red Sea origin, which have already been established in
areas of the Eastern Mediterranean ; recently it was found
the Levantine Basin. (iii) the more intensive research car-
in Rhodes island in the South Aegean where aquaculture
ried out in the South Aegean. Despite the fact that the
is absent. To further extend the discussion on the subject,
number of exotic mollusc species in the North Aegean
new findings suggest caution even when dealing with
has increased over the last decade, it seems that the
species that have been considered without doubt as true
Lessepsian migration the major vector of introduction
Lessepsian migrants. For example the small mussel Bra-
of exotic mollusc species in the Greek Seas has not yet
chidontes pharaonis, a species that originates from the
proceeded to that part of the Aegean Sea. Only two out of
Indian Ocean and is widely spread throughout the Red
the seven species recorded in the North Aegean i.e. the
Sea (OLIVER, 1992), was among the first migrants noticed
opisthobranch gastropod Bursatella leachi and the
in the Eastern Mediterranean. Based on the origin of the
bivalve Brachidontes pharaonis could be considered as
species and its present distribution, progressive penetra-
true Lessepsian migrants, while the presence of the other
tion through the Suez Canal was considered obvious and
species in this area is in most cases connected with
hence its characterization as a Lessepsian migrant was not
anthropogenic activities i.e. shipping and/or aquaculture.
questioned. However, preliminary results of molecular
The scarcity of Lessepsian migrants in the North Aegean
studies have shown that although Red Sea genotypes are
Sea has also been noticed for other benthic groups such as
present in the Mediterranean Sea, non-Red Sea genotypes
anthozoans (VAFIDIS et al., 1994) and crustaceans (KOUK-
are fairly common in that sea also, and the frequency of
OURAS et al., 1992).
the latter increases as we get further from the Suez Canal
(ABELSON, pers. commun.). This suggests that ship trans-
The number of exotic mollusc species recorded from
port from elsewhere may have occurred for this species
the Greek Seas is moderate when compared with that
rather that natural migration through the Suez Canal. The
recorded from other areas of the Eastern Mediterranean.
importance of these two vectors and in particular shipping
The areas with the largest number of exotic species are
in introduction of mollusc species in an area of the Greek
the Israeli coasts (95 species), the coasts of SE Turkey (68
seas extends beyond the issue of exotic species, since
species), Cyprus (32 species), the coasts of Egypt (31 spe-
these vectors may have also contributed to spread of spe-
cies) and the coasts of Lebanon and Syria (29 species).
cies originally native in a restricted part of the Mediterra-
All these areas are located in the Levantine Basin, which
nean. Such a case is that of the pulmonate gastropod
constitutes a separate subsystem in the Eastern Mediterra-
Siphonaria pectinata (Linnaeus, 1758), originally
nean (POR & DIMENTMAN, 1989). It has been assumed that
restricted to the Alboran Sea and the Western coasts of
the prevailing environmental conditions in that basin i.e.
Algeria and now thriving in Saronikos gulf in the South
high temperature and salinity, make this area unsuitable
Aegean (GOFAS & ZENETOS, 2003).
for many western Mediterranean species (SARA, 1985)
The rate of invasion of exotic mollusc species in the
and presumably species of Atlantic origin as well. Conse-
quently this area of the Mediterranean is a favourable
Greek waters has increased in recent decades, in agree-
place for the tropical species that arrive there, since there
ment with data for the rate of biological invasions in the
whole Mediterranean (G
are few ecological obstacles to prevent their establish-
ALIL, 2000). The increased rate of
ment (G
invasion in the Greek Seas could be the result of a syn-
ALIL, 2000). Indeed the Erythrean biota, coming
mainly through the Suez Canal in that sea, accentuates its
ergy of different reasons, the most important of which are
the following : a) the intensive research on the marine
subtropical character (TORTONESE, 1985). POR (1978) was
the first to suggest that Lessepsian migrants represent at
biota of the Greek Seas during the last 20 years and espe-
least 10% of the species inventory of the Levantine Basin,
cially after 90s, which led to the discovery of many mol-
luscs not reported previously in this area of the Mediterra-
while a similar ratio (9.4%) has been suggested by BAR-
nean, b) the increased anthropogenic activities in the
ASH & DANIN (1986) for the molluscs. Similarly, the intro-
duction of exotics has increased by about 10% the biodi-
Greek Seas over the last decade such as aquaculture and
tourism (contributing factors to increase of maritime traf-
versity of molluscs along the Lebanese coasts where out
of 298 recorded species 29 are exotics (B
fic).
ITAR & KOULI-
BITAR, 1999, 2001) and SE Turkey coasts where from a
Among the Greek Seas, the Aegean and in particular
restricted area (Tasuçu area) out of 371 mollusc species
the South Aegean is the area where the majority of the
40 belong to exotics (BUZZURRO & GREPPI, 1996). In
exotic mollusc species is distributed. This difference
Cyprus however, the exotic molluscs contribute only 5%
between the two parts of the Aegean should be attributed
to the malacofauna diversity. Out of the 627 species
to : (i) the prevailing environmental conditions (e.g.
known to date (CECALUPO & QUADRI, 1996 ; BUZZURRO &
higher temperatures and salinities in relation to the North
GREPPI, 1997) only 32 are exotics (www.ciesm.org/atlas).
Aegean - POULOS et al., 1997), which are favourable for
the distribution and settlement of these species, (ii) the
Another reason that has been suggested for the low
vicinity of the South Aegean with the Levantine Basin in
number of exotic mollusc species in other areas than the
connection with the hydrological regime within the East-
Levantine Basin of the Eastern Mediterranean (KOUTSOU-
ern Mediterranean i.e. sea currents running from the
BAS, 1992), is the restricted period of life for the mollus-
coasts of Egypt anticlockwise south of the Turkey coasts
can planktonic larvae when referring to their natural
up to Rhodes island and then to the South Aegean. The
spreading capacities which restricts the distribution of
influx of the Levantine Intermediate Water in the South
such species over long distances. Areas isolated (due to
Aegean through the Kassos straits and then to the other
deep trenches) from the continental coasts, such as
Greek Seas (KONTOYIANNIS et al., 1999) certainly
islands, are difficult for non-indigenous species to
enriches these waters with elements of Indo-Pacific and/
approach.
Origin and vectors of introduction of exotic molluscs in Greek waters
285
It is well documented that the presence of exotic spe-
DELAMOTTE, M. & E. VARDALA-THEODOROU (2001). Shells from
cies in the Mediterranean has significant ecological and
the Greek Seas. The Goulandris Natural History Museum,
economic impacts in that sea (POR & DIMENTMAN, 1989 ;
Athens, 323 pp.
ZIBROWIUS, 1992 ; GALIL, 2000). TOM & GALIL (1991)
DEMIR, M. (1977). On the presence of Arca (Scapharca) amy-
have pointed out the impact of certain exotic mollusc spe-
gdalum Philippi, 1847 in the harbour of Izmir, Turkey. Istan-
cies, which have entered the Mediterranean via Lessep-
bul Universitesi Fen Fakultesi Mecmuasi, Sér. B, 42 : 197-
202.
sian migration, on benthic communities in the Israeli
DIMITRAKIS, K. G. (1989). Shells from the Greek Seas. Orfanides
coasts. Of the exotic mollusc species distributed in the
Press, Athens, 67pp. (in Greek)
Greek Seas, the prosobranch gastropod Rapana venosa
FOUNTOULAKIS, E. & B. SABELLI (1999). Observations on the
first established in Thermaikos Gulf (KOUTSOUBAS &
Malacofauna of the littoral of Saronikos Gulf. In : HELLENIC
VOULTSIADOU-KOUKOURA, 1991), and has since spread
ZOOLOGICAL SOCIETY (eds), Contributions to the Zoogeogra-
out. According to the local Fisheries and Aquaculture
phy and Ecology of the Eastern Mediterranean Region : 465-
Associations it has become a considerable nuisance in the
472.
oyster and mussel beds in the area in a similar way to
GALIL, B. (2000). A sea under siege - alien species in the Medi-
what has been reported for the Black Sea where the spe-
terranean. Biol. Inv., 2 : 177-186.
cies was first noticed and progressively established
GALIL, B. & A. ZENETOS (2002). A sea change - exotics in the
(Z
Eastern Mediterranean. In : L
IBROWIUS, 1992). The bivalve Anadara demiri has been
EPPÄKOSKI, E., OLENIN, S. & S.
reported to dominate the degraded benthic ecosystems in
GOLLASCH (eds), Invasive Aquatic Species Of Europe : Dis-
tributions, Impacts and Management : 325-326. Kluwer Sci-
Thessaloniki Gulf (ZENETOS, 1994), a fact strengthening
entific Publishers
the opinion of GALIL (2000) that polluted or physically
GIANNUZZI-SAVELLI R., PUSATERI F., PALMERI A. & C. EBREO
degraded environments are more prone to invasion than
(2001). Atlante delle conchiglie marine del Mediterraneo.
are pristine sites. However, in order to precisely track and
Edizioni La Conchiglia, Roma, Vol.7 : Bivalvia, 246 pp.
better understand the changes in the Greek marine biota,
GOFAS S. & A. ZENETOS (2003). Exotic Molluscs in the Mediter-
and in particular Mollusca, both its autochthonous and
ranean Basin : Current Status and Perspectives. Ocean. &
allochthonous components should be further investigated.
Mar. Biol. : An Annual Review, (in press)
KALOPISSIS, J. (1981). Individus perliers de Pinctada radiata
LITERATURE
Leach dans les eaux du Golfe de Saronique. Thal. Sal., 11 :
105-108.
BARASH, A. & Z. DANIN (1986). Further additions to the knowl-
KINZELBACH, R. (1985). Lesseps'sche Wanderung : neue statio-
edge of Indo-Pacific Mollusca in the Mediterranean Sea.
nen von Muscheln (Bivalvia : Anisomyaria). Arch. Mollusk.,
Spixiana, 9 : 117-141.
115 : 273-278.
B
K
ARASH, A.& Z. DANIN (1988/1989). Marine Mollusca at
ONTOYIANNIS, H., IONA, A., PAPADOPOULOS, V., PAPAGEORGIOU
Rhodes. Isr. J. Zool., 35 :1-74.
E., GOTSIS-SKRETAS O., PAVLIDOU A. & BALOPOULOS E.
B
(1999). The Hydrology and Biochemistry of the Cretan
ITAR, G. & S. KOULI-BITAR (1999). Inventaire des mollusques
marin benthiques du Liban en remarques biogeographique
Straits (Antikithira and Kassos Straits) revisited in June/97,
sur quelques espéses nouvellement signaless. Mesogee, 56 :
January/98 and May/98. International Conference on Ocea-
37-44.
nography of the Eastern Mediterranean and Black Sea, Ath-
ens, 23-26 February 1999.
BITAR, G. & S. KOULI-BITAR (2001). Nouvelles donnees sur la
KORONEOS, J. (1979). Les Mollusques de la Grèce, Athens,
faune et la flore benthiques de la cote Libanaise. Migration
36 p., 48 pl.
Lessepsienne. Thal. Sal., 25 : 71-74.
KOUKOURAS, A., DOUNAS, C., TURKAY, M. & E. VOULTSIADOU-
BLANCHARD, M. & A. ERHOLD (1999). Cartographies et évalua-
KOUKOURA (1992). Decapod Crustacean Fauna of the
tion du stock de crépidules Crepidula fornicata (L.) en Baie
Aegean Sea : New Information, Checklist, Affinities. Senk-
du Mont Saint-Michel. Haliotis, 28 : 11-20.
enbergiana marit., 22 : 217-244.
BUZZURRO, G. & E. GREPPI (1994). Presenza di Smaragdia
KOUTSOUBAS, D. (1992). Contribution to the study of the gastro-
(Smaragdella) souverbiana (Montrouzier, 1863) nel Medi-
pod molluscs of the continental shelf of the North Aegean
terraneo orientale. Boll. Malacol., 29 : 319-321.
Sea. Ph.D. Thesis, Biology Department, Aristotle University
BUZZURRO, G. & E. GREPPI (1996). The Lessepsian Molluscs of
of Thessaloniki, 585 pp. (in Greek with English summary).
Tasuçu (South-East Turkey). La Conchiglia, (Supplement to
KOUTSOUBAS, D. & F. CINELLI (1997). Indo-Pacific origin gas-
279) : 3-22.
tropod species in the Aegean Sea. Melibe fimbriata Alder
BUZZURRO, G. & E. GREPPI (1997). Notes on the Molluscs of
and Hancock, 1864 a new invader. Boll. Malacol., 32 : 1-6.
Cyprus, with special attention to the allocthone species. La
KOUTSOUBAS, D., KOUKOURAS, A. & E. VOULTSIADOU-KOUK-
Conchiglia, 283 : 21-31, 61-62.
OURA (1997). Prosobranch Mollusc Fauna of the Aegean
C
Sea : New information, checklist, distribution. Isr. J. Zool.,
ATTANEO-VIETTI, R. & T.E. THOMPSON (1989). Mediterranean
Opisthobranch Molluscs : A zoogeographic approach. Boll.
43 : 19-54.
Malacol., 25 : 183-204.
KOUTSOUBAS D., ARVANITIDIS, C., DOUNAS, C. & L. DRUMMOND
(2000a). Community and dynamics of the molluscan fauna
CECALUPO, A. & P. QUADRI (1996). Contributo alla conoscenza
in a Mediterranean lagoon (Gialova lagoon, SW Greece).
Malacologica per il nord dell' isola di Cipro. Boll. Malacol.,
Belg. J. Zool., 130 (Supplement) : 135-142.
31 : 95-118.
KOUTSOUBAS D., TSELEPIDES, A. & A. ELEFTHERIOU (2000b).
COSENZA, G. & G. FASULO (1997). The littoral shelled Mollusks
Deep Sea Molluscan Fauna of the Cretan Sea (Eastern
of the Island of Crete. La Conchiglia, 284 : 51-58.
Mediterranean) : Faunal, Ecological and Zoogeographical
DEKKER, H. & Z. ORLIN (2000). Check list of Red Sea Mollusca.
Remarks. Senkenbergiana marit., 30 : 85-98.
Spirula, 47 (suppl.) : 1-46.
KOUTSOUBAS, D. & E. VOULTSIADOU-KOUKOURA (1991). The
DELAMOTTE, M. & E. VARDALA-THEODOROU (1994). Shells from
occurrence of Rapana venosa (Valenciennes, 1846) (Gastro-
the Greek Seas. The Goulandris Natural History Museum,
poda, Thaididae) in the Aegean Sea. Boll. Malacol., 26 :
Athens, (in Greek), 320 pp.
201-204.
286
A. Zenetos, D. Koutsoubas and E. Vardala-Theodorou
NICOLAY, K. (1986). Sempre piu diffuso il strombo del Mediter-
STORSBERG, J. (1997). Ein weiterer Fund von Acteocina mucro-
raneo. La Conchiglia, 202-203 : 29.
nata (Philippi, 1849) im östlichen Mittelmeer (Gastropoda :
NORDSIECK, F. (1969). Die europäischen Meeresmuscheln. Vom
Cylichnidae). Sch. Mal. Haus Natur-Cismar, 10 : 7-9.
Eismeer bis Kapverden, Mittelmeer und Schwarzes Meer.
TENEKIDES, N.S. (1989). On a collection of shells from the Greek
Gustav Fischer, Stuttgart, XIII + 256 pp.
Seas. Protopapa Press, Athens, 187 pp. (in Greek)
NORDSIECK, F. (1973). A new Neritidae in the Mediterranean. La
THEOCHARIS, A., GEORGOPOULOS D., LASKARATOS A. & K. NIT-
Conchiglia, 5 : 4.
TIS (1993). Water masses and circulation in the central region
OLIVER, P.G. (1992.) Bivalved seashells of the Red Sea. Verlag
of the Eastern Mediterranean : Eastern Ionian, South Aegean
Christa Hemmen & National Museum of Wales, Cardiff,
and Northwest Levantine, 1986-1987. Deep-Sea Res.. 40 :
330 pp.
1121-1142.
OLIVERIO, M. (1995). The status of the living Mediterranean
THOMPSON, T.E. & D.M. CRAMPTON (1984). Biology of Melibe
Strombus, or : What is a lessepsian migrant ? Notiz. CISMA,
fimbriata, a conspicuous opistobranch Mollusc of the Indian
16 : 35-40.
Ocean, which has now invaded the Mediterranean Sea. J.
P
moll. Studies, 50 : 113-121.
ANCUCCI-PAPADOPOULOU, M.A., ZENETOS, A., SIMBOURA, N. &
M. C
T
ORSINI (2002). Updating the Greek marine exotic fauna.
OM, M. & B. GALIL (1991). The macrobenthic associations of
7th Hellenic Symposium on Oceanography and Fisheries,
Haifa Bay, Mediterranean Coast of Israel. Mar. Ecol., 12 :
Hersonisson, Crete, 6-9 May 2003 : 138.
75-86.
P
TORTONESE, E. (1985). Distribution and ecology of endemic ele-
ASSAMONTI, M. (1996). Nuova segnalazione per le coste Tuni-
sine di Papyridea papyracea (Gmelin,1791) (Bivalvia : Car-
ments in the Mediterranean fauna (fishes and echinoderms).
didae). Boll. Malacol., 32 : 153-156.
In : MORAITOU-APOSTOLOPOULOU, M. & V. KIORTSIS (eds)
Mediterranean Marine Ecosystems, Plenum Press, New
POR, F.D. (1978). Lessepsian migration - the influx of Red Sea
biota into the Mediterranean Sea by way of the Suez Canal.
York : 57-83.
viii + 228 p. Springer, Berlin.
VAFIDIS, D., KOUKOURAS, A. & E. VOULTSIADOU-KOUKOURA
(1994). Octocoral fauna of the Aegean Sea with a checklist
POR, F.D. & C. DIMENTMAN (1989). The legacy of Tethys : an
of the Mediterranean species : New information, faunal
aquatic biogeography of the Levant. Monographiae Biologi-
comparisons. Ann. Inst. Océanogr., Paris, 70 :217-229
cae 63, Kluwer Academic Publ., Dordecht, 215 pp.
VARDALA-THEODOROU, G.E. (1998). Study of the recent and fos-
POR, F.D. (1990). Lessepsian migration. An appraisal and new
sil (Quaternary) benthic Mollusca of Vouliagmeni Lake at
data. Bull.Inst. Océan., Monaco, Special No 7 : 1-10.
Perachora. Ph. D. Thesis University of Athens, 404 pp. (in
POULOS, S.E., DRAKOPOULOS P. & M.B. COLLINS (1997). Sea-
Greek)
sonal variability in sea surface oceanographic conditions in
VARDALA-THEODOROU, G.E. (1999). The occurrence of the Indo-
the Aegean Sea (Eastern Mediterranean) : An Overview. J.
Pacific molluscan species Fulvia fragilis (Forsskal, 1775)
Mar. Syst., 13 : 225-244.
and Bulla ampulla L., 1758 in Elefsis Bay. Newsl. Hell.
RALLI-TZELEPI, Z.N. (1946). Contribution a l'etude conchyliol-
Zool. Soc., Fasc. 31 : 10-11.
ogique du littoral de l'Attique (Grèce). Ph.D. Thesis, Uni-
ZENETOS, A. (1994). Scapharca demiri (Piani, 1981) : First find-
versity of Athens.
ing in the North Aegean Sea. La Conchiglia, 271 : 37-38.
SARA, M. (1985). Ecological factors and their biogeographic
ZENETOS, A. (1996). The Marine Bivalvia (Mollusca) of Greece.
consequences in the Mediterranean ecosystems. In : MORAI-
Fauna graeciae : Volume VII. Hellenic Zoological Society &
TOU-APOSTOLOPOULOU M. & V. KIORTSIS (eds), Mediterra-
NCMR (eds), Athens, 1996, 319 pp.
nean Marine Ecosystems, Plenum Press, New York : 1-17.
ZENETOS, A., GOFAS S., RUSSO, G. & TEMPLADO, J. (2003).
SERBETIS, C.D. (1963). L'acclimatation de la Meleagrina
CIESM Atlas of Exotic Species in the Mediterranean. Vol. 3.
(Pinctada) margaritifera (Lam.) en Grèce. Rapp. Comm. int.
Molluscs. (F. BRIAND, Eds). CIESM, Monaco : 376 pp.
Medit., 17 : 271-272.
ZIBROWIUS, H. (1992). Ongoing modifications of the Mediterra-
SETTEPASSI, F. (1967). Atlante malacologico.Molluschi viventi
nean marine fauna and flora by the establishment of exotic
nel Mediterraneo Vol. 1. Corporazione Atti Grafiche, Roma
species. Mesogee, 51 : 83-107.
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