Belg. J. Zool., 138 (2) : 146-148 July 2008
Feeding behaviour of the Columbretes lizard Podarcis atrata,
1 Estación Biológica de Sanaüja, Museo Nacional de Ciencias Naturales (CSIC). Ap. Correos nº 35, E-25280 Solsona, Lleida, España. e-mail: aurora@mncn.csic.es
2 Dept. Biodiversity and Evolutionary Biology, National Museum of Natural Sciences (CSIC), C/ José Gutiérrez Abascal 2, E28006 Madrid, Spain. e-mail: aurora@mncn.csic.es
3 Laboratory of Functional Morphology, Department of Biology, University of Antwerp, Campus Drie Eiken, B-2610 Antwerp, Belgium e-mail: bieke.vanhooydonck@ua.ac.be
4 Integrative Biology, University of California Berkeley, 3060 Valley Life Sciences Bldg #3140, Berkeley CA 94720, USA e-mail: acatenazzi@gmail.com
Corresponding author : * Aurora M. Castilla. Estación Biológica de Sanaüja, Museo Nacional de Ciencias Naturales (CSIC). Ap. Correos nº 35, E-25280 Solsona, Lleida, España. e-mail: aurora@mncn.csic.es
ABSTRACT. The lizard Podarcis atrata, endemic to the Columbretes archipelago (Mediterranean, Spain) occupies very small islands characterized by extreme aridity and a reduced availability of potential insect prey. The results of an experimental study have shown that adult lizards offered individuals of Ligia italica and Armadillo officinalis (marine and terrestrial isopods, respectively) consumed at high frequencies; with males consuming them at significantly higher frequencies than females. The results are discussed in light of the importance of the inclusion of marine prey into the diet in arid insular ecosystems.
KEY WORDS : island, intertidal trophic resources, endemic lizard, arid zones
The endemic lizard Podarcis atrata from the Columbretes archipelago (Mediterranean, Castellón, Spain), inhabits very small islands ranging from 0.5 to 13 hectares. The islands are characterized by extreme aridity and by the scarcity of terrestrial insects (see CASTILLA & BAUWENS, 1991). Adult lizards have been observed near shore feeding on seabird regurgitates, and scavenging on carcasses and gull eggs on several islands of the archipelago (CASTILLA et al., 1987). Lizards from arid coastal areas across the world are important consumers of marine and intertidal trophic resources (amphipods, crabs, shells, flies, etc) (Table 1). It is generally assumed that the inclusion of marine resources into the diet is promoted by the lack of other food resources (POLIS & HURD, 1996; BARRET el al., 2005; CATENAZZI et al., 2005; CATENAZZI & DONNELLY, 2007).
The isopod Ligia italica is very abundant on Columbretes, and inhabits rocky substrates from 0 to 12 meters above sea level. In some areas, lizards and isopods utilize the same rocks, thus facilitating predator-prey interactions. However, observations of the consumption of L. italica by P. atrata individuals under natural conditions are difficult because both species are very wary on exposed rocks without vegetation cover and a high abundance of bird predators. Moreover, lizards are very difficult to capture on vertical, eroded cliffs. Consequently, no data are available on stomach contents for animals living near shore. We decided to use an experimental approach similar to that employed in a previous study to examine the cannibalistic propensities of lizards on the same island (CASTILLA & VAN DAMME, 1996). We measured the willingness of P. atrata individuals to consume the marine isopod Ligia italica and the terrestrial one Armadillo officinalis, which is morphologically similar and has been found in the stomach contents of P. atrata (CASTILLA et al., 1987).
The study was conducted on the island Columbrete Grande during the fist week of June 2006. We captured adult isopods of L. italica at the sea shore and offered them to free ranging adults of P. atrata living in vegetated areas of the island near human habitation where the lizards are abundant and used to human presence. Observations were conducted between 0900-1200 hours, with ambient temperature ranging from 20–22ºC, and relative humidity from 72-84%.
To be sure lizards were hungry at the time of the experiment we first offered them a mealworm (a preferred prey) attached to a noose. If the reaction of the lizard to the mealworm was positive (e.g. direct attack), we removed the mealworm from the noose and replaced it with an individual of L. italica (length x width ca. 15 x 6mm; 0.15g). We tested only adult lizards (svl=60-70mm, mass=5-9g) of both sexes. After each presentation we observed the reaction of the lizard and registered its behaviour (Table 2). We also recorded the handling time, as the time from the moment the lizard captured its prey to the moment the lizard completed ingestion. After three days we repeated the same experiment using terrestrial isopods, A. officinalis (length x width ca. 10x5mm; 0.05g) that were captured under rocks near human habitation.
Feeding behaviour of the Columbretes lizard Podarcis atrata 147
TABLE 1
Insular and coastal lizards that include marine input in their diet. Note that there are only data for one species from the Mediterranean (present study).
| Species (Reptilia: Squamata) | Zone | Reference |
|---|---|---|
| Amblyrhynchus cristatus Callisaurus draconoides Cryptoblepharus bautony Leiolopisma suteri Microlophus peruvianus Phyllodactilus angustidigitu Uta spp. Uta antiqua Uta encantadae Uta lowei Uta palmeri Uta stansburiana Uta tumidarostra Podarcis dugesii Podarcis atrata | Galapagos Baja California Madagascar New Zealand Peru Peru Gulf of California Gulf of California Gulf of California Gulf of California Gulf of California Gulf of California Gulf of California Atlantic, Madeira Mediterranean, Columbretes | DUNSON, 1969 QUIJADA-MASCAREÑAS, 1992 FRICKE, 1970 TOWNS, 1975 VOGT, 1939 CATENAZZI & DONNELLY, 2007 SOULÉ, 1966 BALLINGER & TINKLE, 1972 GRISMER, 1994 GRISMER, 1994 WILCOX, 1980 BARRETT et al., 2005 GRISMER, 1994 DAVENPORT & DELLINGER, 1995 present study |
TABLE 2
Behavioural response of free living adult males and females of Podarcis atrata following presentation of individuals of two different Isopoda (Crustacea) prey attached to a noose. For each different lizard the first immediate reaction was recorded. The results are expressed in percentages (%), and sample size given (n).
| P. atrata response | Ligia italica | Armadillo officinalis | |||||||
|---|---|---|---|---|---|---|---|---|---|
| Males (n=18) | Females (n=10) | Males (n=20) | Females (n=18) | ||||||
| n | % | n | % | n | % | n | % | ||
| Ignore Observe-ignoreObserve-attack-eat Direct attack- eat Direct attack- not eat | 0 0 4 40 1 6 2 20 3 17 1 10 13 72 3 30 1 6 0 0 | 2 10 5 28 1 5 2 11 5 25 1 6 11 55 10 56 1 5 0 0 | |||||||
Differences in response (consumption of the prey or not) towards the two different prey items (L. italica or A. officinalis) by lizards of both sexes were analysed with a binomial regression (i.e., generalized linear model) with a probit link function to examine the putative effects of prey, sex and their interaction, using the program S-Plus. We also tested for differences in handling time between prey species using an analysis of variance. Prior to performing the one way ANOVA's we logarithmically transformed (log10) handling times.
In all cases (n=66) males and females reacted to the mealworm by directly attacking it. After that, most males consumed the isopod L. italica (89%), 72% attacking the prey directly without previous observation (Table 2). Most females (60%) ignored the specimen of L. italica offered, and only 40% of the females actually consumed them. Most males consumed the offered individuals of A. officinalis (80%), 55% attacking them directly without previous observation. Some females (39%) ignored this prey while 61% consumed the terrestrial isopod (Table 2).
We did not find a significant interaction effect between sex and prey (t=1.2909; P>0.05). However, the analysis showed a significant effect of sex (t=2.8711; P<0.01): males consumed both isopods species at higher proportions (L. italica=89%, A. officinalis=80%) than did females (L. italica=40%, A. officinalis=61%).
Handling time for consumption of the isopod L. italica was only measured for male lizards, and ranged from 22 seconds to 1 minute (mean=40.1sec; sd=13.6; n=13). Handling time of specimens of A.officinalis by male lizards ranged from 12 to 38sec (mean=23.9sec; sd=7.7; n=9), and the difference was significant (F1, 26=9.38; p=0.005). The mean ingestion time of specimens A. officinalis was longer for female lizards (mean=27.6sec; sd=14.1; n=7) than it was for males (23.9sec) but the difference was not significant (F1, 14=0.11; p=0.75).
The results of our study show that, in our experimental conditions, both sexes of the lizard P. atrata consumed the marine isopod L. italica in the same proportion as the terrestrial A. officinalis. However, males were more inclined to consume both prey types than females. In June, 80% of the females were pregnant, and they may be more selective for food during that stage. Additional experiments outside the breeding season would help to better interpret our results.
Handling time for males was lower for specimens of A. officinalis (24sec) than those of L. italica (40sec). In addition we observed one male ingesting three specimens of
148 Aurora M. Castilla, Bieke Vanhooydonck & Alessandro Catenazzi
A. officinalis, one after the other. For this individual, ingestion time was variable (22.41sec; 31.91sec and 24.64sec), suggesting that a larger sample size may be needed.
A longer handling time for specimens of L. italica could be related to the larger size of this species (ca. 5mm larger than individuals of A. officinalis). However, we believe that these differences were mainly due to the fact that a specimen of L. italica was sometimes thrown to the ground and picked up again by both males and females. Unfortunately, we could not quantify the “rejection behaviour” shown by six individuals. Interestingly, rejection behaviours were not observed with offered individuals of A. officinalis. Terrestrial isopods such as A. officinalis are abundant species in the vegetated and humid zones of the island, and are frequently consumed by P. atrata (CASTILLA et al., 1987) and other lizards (CARRETERO, 2004).
To test the importance of marine prey resources in the diet of P. atrata, future studies should include the analysis of stomach contents of lizards living near the seashore. Alternatively, stable isotope analysis could be used (e.g., CATENAZZI & DONNELLY, 2007) to test for the importance of the marine subsidies into the terrestrial ecosystem at the Columbretes islands. The only other data on European lizards utilising marine resources are for Podarcis dugesi on Madeira Island (Atlanic, Portugal; see DAVENPORT & DELLINGER, 1995). However, as there are many islands in the Atlantic and the Mediterranean seas holding lizard populations, the use of marine trophic resources to survive or complement the diet of lizards is likely more common. Indeed, our observations suggest that marine invertebrates may be an important food source for lizards living in harsh conditions on small islands.
We would like to thank the Generalitat Valenciana and the Secretaria General de Pesca Marítima (Ministerio de Agricultura, Pesca y Alimentación) for permission to work on the islands. Thanks to Diego Kersting (MAPA), Marta Aguiló (GV) and Guim Llacuna (Escuela de Capacitación Agraria de Solsona) for their help during the field work and to Pep Perolet and the boats CAT-CAT, Clavel I and Super Bonanza for transportation. We thank A. Herrel and D. Bauwens for comments. This paper is a contribution of the Bio-Ecological Station of the Museum of National Sciences (CSIC). This work was conducted on a contract “Ramón and Cajal” from the Spanish National Science Foundation (CSIC, Ministerio de Educación y Ciencia) (to AMC), and the Project MEC CGL2005-00391/ BOS (J. Martín & P. López, MNCN-CSIC).
BALLINGER RE & TINKLE DW (1972). Systematics and evolution of the genus Uta (Sauria: Iguanidae). Miscellaneous Publications of the Museum of Zoology at the University of Michigan, 145: 1-83.
BARRETT K, ANDERSON WB, WAIT AD, GRISMER LL, POLIS GA & ROSE MD (2005). Marine subsidies alter the diet and abundance of insular and coastal lizard populations. Oikos,
109: 145-153.
CASTILLA AM, JIMÉNEZ J & LACOMBA I (1987). Los reptiles de Columbretes. In: ALONSO MATILLA LA, CARRETERO JL & GARCIA-CARRASCOSA AM (eds), Islas Columbretes. Contribución al estudio de su medio natural, Generalitat Valenciana, Valencia: 181-194.
CASTILLA AM & BAUWENS D (1991). Observations on the natural history, present status, and conservation of the insular lizard Podarcis hispanica atrata. Biological Conservation, 58: 69-84.
CASTILLA AM & VAN DAMME R (1996). Cannibalistic propensities in the lizard Podarcis hispanica atrata. Copeia, 1996: 991-994.
CARRETERO MA (2004). From set menu to a la carte. Linking issues in throphic ecology of Mediterranean lacertids. Italian Journal of Zoology, 2: 121-133.
CATENAZZI A, CARRILLO J & DONNELLY MA (2005). Seasonal and geographic eurythermy in a coastal Peruvian lizard. Copeia, 4: 713-723.
CATENAZZI A & DONNELLY MA (2007). The Ulva connection. Marine green algae subsidize terrestrial consumers in coastal Peru. Oikos, 116: 75-86.
DAVENPORT J & DELLINGER T (1995). Melanism and foraging behavior in an intertidal population of the Madeiran lizard Podarcis (=Lacerta) dugesii (Milne-Edwards, 1829). Herpetological Journal, 5: 200-203.
DUNSON WA (1969). Electrolyte excretion by the salt gland of the Galapagos marine iguana. American Journal of Physiology, 216: 995-1002.
FRICKE HW (1970). Die ökologische Spezialisierung der Eidechse Cryptoblepharus boutoni cognatus (Boettger) auf das Leben in der Gezeitenzone (Reptilia, Skinkidae). Oecologia, 5: 380-391.
GRISMER LL (1994). Three New Species of Intertidal Side-blotched Lizards (Genus Uta) from the Gulf of California, Mexico. Herpetologica, 50: 451-474.
POLIS GA & HURD SD (1996). Linking marine and terrestrial food webs: allochthonous input from the ocean supports high secondary productivity on small islands and coastal land communities. American Naturalist, 147: 396-423.
QUIJADA-MASCAREÑAS A (1992). Feeding and foraging of Callisaurus draconoides (Sauria: Phrynosomatidae) in the intertidal zone of coastal Sonora. Southwestern Naturalist, 37: 311-314.
SOULÉ M (1966). Trends in the insular radiation of a lizard. American Naturalist, 100: 47-64.
TOWNS DR (1975). Ecology of the black shore skink, Leiolopisma suteri (Lacertilia: Scincidae), in boulder beach habitats. New Zealand Journal of Zoology, 2: 389-407.
VOGT W (1939). Las lagartijas y las aves guaneras. Boletín de la Compañía Administradora del Guano [VOLUME?]: 346
348.
WILCOX BA (1980). Species number, stability, and equilibrium status of reptile faunas on the california Islands. In: POWER DM (ed), The California Islands. Proceedings of a multidisciplinary symposium, Museum of Natural History, Santa Barbara, California: 551-564.
Received: March 31, 2007 Accepted: April 16, 2008