Food composition of the European pond turtle (Emys orbicularis) in Lake Sülu klu (Western Anatolia, Turkey)

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1 Journal of Freshwater Ecology Vol. 26, No. 4, December 2011, Food composition of the European pond turtle (Emys orbicularis) in Lake Sülu klu (Western Anatolia, Turkey) Kerim C ic ek and Dinç er Ayaz * Zoology Section, Department of Biology, Faculty of Science, Ege University, TR Bornova, Izmir, Turkey (Received 13 January 2011; final version received 14 March 2011) We examined the seasonal changes in the food composition of the European pond turtle, Emys orbicularis in Lake Sülu klu (Manisa, Turkey) during spring and summer The stomach contents of 110 (40 <<, 62,,, eight juveniles) E. orbicularis individuals were analyzed, and 461 prey items were found. Gastropods (2.2%), earthworms (0.4%), insects (67.2%), fishes (6.9%), amphibians (15.0%), and plant material (8.2%) constituted the food of the species. Food consisted primarily of insects and other invertebrates during the breeding season and of vertebrate and plant material (especially seeds and roots) during the post-breeding season. Based on these results, the European pond turtle is a generalist opportunistic omnivore whose diet is most strongly influenced by prey availability. Keywords: European pond turtle; Emys orbicularis; food habitat; Western Anatolia; Turkey Introduction The European pond turtle (Emys orbicularis) is one of the world s most widely distributed freshwater turtles (Fritz 2003) and is legally protected over much of its range (Fritz and Andreas 2000). The species is classified as lower risk/near threatened in the IUCN Red List (Tortoise and Freshwater Turtle Specialist Group 1996), in the list of Annex II of the EU Habitats Directive 92/43/EEC, and in the list of Annex II of the Bern Convention. The European pond turtle generally lives in slow-moving waterbodies with soft bottoms (mud or sand) and abundant aquatic vegetation, especially overhanging the banks (Bas og lu and Baran 1977; Ernst and Barbour 1989). Ernst and Barbour (1989) stated that E. orbicularis is carnivorous, feeding on insects, crustaceans, mollusks, worms, salamanders, frogs, and fishes. Stephens and Wiens (2003) treated the European pond turtle as a strictly aquatic and carnivorous species. The food of the European pond turtle is poorly known, especially in the Mediterranean region (Ottonello et al. 2005). Studies on food composition of the European pond turtle have been conducted for some European populations (e.g. Bulgaria, Kovacˇev 1912; France, Rollinat 1934; the Ukraine, Sˇcˇerbak and Sˇcˇerbanj 1980; Spain, Gonzalez De La Vega 1988; *Corresponding author. dincer.ayaz@ege.edu.tr ISSN print/issn online ß 2011 Taylor & Francis

2 572 K. Çiçek and D. Ayaz Italy, Lebboroni and Chelazzi 1991; Drobenkov 1999; Kotenko 2000; Ottonello et al. 2005); however, available data for eastern populations of its range (e.g. Bannikov 1951; Alekperov 1978; Guskow et al. 1983; Badmajewa et al. 1985) are still incomplete. The objective of this study was to collect detailed information on the food habits and describe temporal patterns of food composition of the European pond turtle population inhabiting Lake Su lu klu (Western Anatolia, Turkey). Materials and methods Lake Su lu klu (Manisa, Turkey) is located on the northeastern slope of Mt. Spil ( N, E, 612 m a.s.l.). The surface of the lake is nearly 1.58 ha, and its depth 2 4 m. A detailed description of the study area was given by C ic ek and Ayaz (2011). We caught turtles during daytime between 08:00 10:00 and 15:00 18:00 h by net, hand, or using fish traps set at six different locations on eight occasions from the first half of April to the end of September To compare the seasonal change in food habits, we divided the sampling regimen into two periods the spring breeding season (April June) and the summer post-breeding season (July September). Within 30 min of capture, we extracted stomach contents by gastric lavage with pressurized water in the field. The stomach contents were preserved in 70% ethanol. We measured straight carapace length (SCL) and plastron length (PL) using a caliper to the nearest 0.1 mm, and body mass (BM) was recorded to the nearest 0.1 g. After these procedures, we marked each captured individual by notching its marginal scutes (Gibbons 1990) and released all turtles at the places where they had been captured. The prey items were identified to the lowest possible taxonomic level. To calculate the similarity in food for sexes, the Pianka (1973) overlap index was used. This index varies between 0 (no similarity) and 1 (totally similar). Food-niche breadth was calculated using Shannon s index (Shannon 1948). All niche calculations were done using the EcoSim 700 program (Gotelli and Entsminger 2010). The t-test and the Mann Whitney U test were used to compare the sexes; statistical analyses were performed using SPSS 10.0, and the alpha level was set at Results are presented as means with their standard deviations. Results We captured 118 (42 <<, 68,,, eight juveniles) individuals of European pond turtle from Lake Su lu klu. The stomachs of six females and two males were empty in the post-breeding morning sampling. The average SCLs were ( ) mm for juveniles, ( ) mm for males, and ( ) mm for females. The average PLs were ( ) mm in juveniles, ( ) mm in males, and ( ) mm in females. The average BMs were ( ) g for juveniles, ( ) g for males, and ( ) g for females. Females were larger than males (t-test, for SCL: t ¼ 3.43, p 0.001; for PL: t ¼ 5.56, p 0.000; for BM: t ¼ 5.04, p 0.000). From the stomach contents of 110 (40 <<, 62,,, eight juveniles) individuals, 461 prey items, with body lengths ranging from 0.5 to 12 cm, were found with a median number of 2.0 (range ¼ 1 54). Some 362 prey items were found in the stomach

3 Journal of Freshwater Ecology 573 contents of 38 individuals (12 <<, 24,,, two juveniles) in the breeding season, whereas 99 prey items were observed in the food contents of 72 individuals (28 <<, 38,,, six juveniles) in the post-breeding season. Depending on season, the median number of prey items extracted from the stomach was 6.0 (2 54) during the breeding season, while it was 1.0 (1 4) in the post-breeding season (Mann Whitney U test, Z ¼ 9.044, p 0.000). As regards the sexes, the median number of prey items extracted from the stomachs of females was 2.0 (1 29), and that from the stomachs of males was 1.0 (1 54) (Mann Whitney U test, Z ¼ 2.819, p ¼ 0.005). Gastropoda (N% ¼ 2.2%), Oligocheta (0.4%), Insecta (67.2%), Cypriniformes (6.9%), Amphibia (15.0%), and plant material (Typha angustifolia, Phragmites australis, Juncus sp., Carex sp., Potamogeton sp., seeds, roots, leaves, and algae) (8.2%) were the prey groups included in the stomach contents (Table 1). By number, the food composition in the breeding season consisted of Gastropoda (2.5%), Oligocheta (0.3%), Insecta (84.8%), Cypriniformes (1.1%), Amphibia (6.9%), and plant material (4.4%), while the stomach contents in the post-breeding season consisted of Gastropoda (1.0%), Insecta (3.0%), Cypriniformes (28.3%), Amphibia (44.4%), and plant material (22.2%). Terrestrial prey items (adult Odonata, Anisolabididae, Cicadidae, adult Hymenoptera, Formicidae, Cerambycidae, Staphylinidae, Muscidae, and Culicidae) constituted only 8.7% of the stomach contents. The plant material (especially seeds and roots) consisted extensively of the roots and seeds of aquatic forms. Among the prey taxa, insects (frequency% ¼ 79.1%), amphibians (62.7%), plant material (34.5%), and fishes (28.2%) were frequently consumed by European pond turtles. Insects (84.2%), amphibians (65.8%), and plant material (42.1%) in the breeding season and amphibians (50.0%), fishes (38.9%), and plant material (20.6%) in the post-breeding season were the most frequently observed prey groups in the food content. As suggested by Pianka s niche overlap index, the two sexes and juveniles shared a large similarity in their diet (males vs. females ¼ 0.771, males vs. juveniles ¼ 0.816, females vs. juveniles ¼ 0.756). Food niche breadth (Shannon s index) values were 1.79, 1.95, and 1.39 in males, females, and juveniles, respectively. Furthermore, although the prey diversity of females (1.95) was higher, no difference was observed between the sexes (Mann Whitney U test, Z ¼ 0.075, p ¼ 0.613). Discussion Our study revealed that European pond turtle feeds on a variety of invertebrates, vertebrates, and plants, and that insects, fishes, amphibians, and plant material partially constitute an important part of its diet. The previous studies on European pond turtle showed that food composition of individuals comprised mollusks, arachnids, crustaceans, terrestrial and aquatic insects, fishes, amphibians, birds, and plants (Kovačev 1912; Rollinat 1934; Bannikov 1951; Lukina 1966; Alekperov 1978; Sˇčerbak and Sˇcˇerbanj 1980; Guskow et al. 1983; Tertysnikow and Gorowaja 1984; Badmajewa et al. 1985; Gonzalez De La Vega 1988; Lebboroni and Chelazzi 1991; Drobenkov 1999; Kotenko 2000; Fritz 2001; Ottonello et al. 2005; Ficetola and De Bernardi 2006; Ayres et al. 2010). Some authors (Lanza 1983; Ernst and Barbour 1989; Stephens and Wiens 2003) reported that the species was carnivorous. Bannikov (1951) stated that the Dagestan

4 574 K. Çiçek and D. Ayaz Table 1. Food composition of E. orbicularis from Lake Su lu klu. Males Females Juveniles All turtles Prey taxon N Percent N Percent N Percent Frequency Percent Gastropoda Planorbidae Planorbis sp Oligocheta Lumbricidae Lumbricus terrestris Insecta Ephemeroptera Nymphs Odonata Nymphs Adults Dermaptera Anisolabididae Euborellia sp Plecoptera Nymphs Hemiptera Nymphs Notonectidae Notonecta glauca Cicadidae Cicada orni Hymenoptera Adults Formicidae Formica sp Coleoptera Adults Dytiscidae Acillius sp Noteridae Noterus clavicornis Hydrophilidae Enochrus sp Cerambycidae Staphylinidae Staphylinus sp (continued )

5 Journal of Freshwater Ecology 575 Table 1. Continued. Males Females Juveniles All turtles Prey taxon N Percent N Percent N Percent Frequency Percent Diptera Muscidae Musca sp Culicidae Cypriniformes Cyprinidae Cyprinus carpio Adults Larvae Urodela Salamandridae Lissotriton vulgaris Adults Larvae Triturus karelinii Anura Ranidae Pelophylax bedriagae Adults Larvae Plant material (seeds, roots, leaves, and algae) Notes: N ¼ total number of this food item occurring in stomach samples of male, female, and juvenile turtles; the associated percentage value is the relative proportion of occurrence. Frequency ¼ the total frequency of occurrence of the food item in the 110 examined stomachs; the associated percentage value is the relative frequency of occurrence.

6 576 K. Çiçek and D. Ayaz population fed particularly on aquatic and terrestrial invertebrates and that its food consisted mostly of insects (94 100%) and terrestrial prey items in the steppes and mountainous regions, while isopods and plant material were also included in the woodland areas. Ayres et al. (2010) detected considerable quantities of water lily seeds in the food composition of the Spanish population of European pond turtle in the summer months. Although the stomach contents of the Lake Su lu klu population consisted of aquatic invertebrates and vertebrates, plant material was also frequently encountered especially in the summer months. Honigmann (1921) and Manteifel et al. (1992) stated that the European pond turtle hunts in water. Nevertheless, Bannikov (1951) reported that it hunts on land as well. Our data also support the fact that the species hunts mostly in water and both on land and in water. Ottonello et al. (2005) and Clark and Gibbons (1969) suggested that the plant food items consumed during the breeding season were randomly taken, and also depended on environmental factors. The percentage of food with plant material consumed during the breeding season in the Lake Su lu klu population of E orbicularis was 4.4%, while this increased to 22.2% in the post-breeding season. In terms of frequency, it was observed as 42.1% in the breeding season and 30.6% in the postbreeding season. The fact that the difference between the breeding and post-breeding seasons is not very great when the frequency of consumption is considered, makes one think of the possibility that the species consciously consumes plant material. We observed that of the two hatchling individuals we kept in captivity from Lake Su lu klu for a short period of time, one preferred animal prey items, while the other preferred plant items. This observation does not support the fact that food with plant material in the breeding season is random. The lower energy requirements and hunting skills associated with post-breeding periods of lower activity could favor a preference for prey items that have lower energy values but are easier to obtain, according to the optimal foraging theory (MacArthur and Pianka 1966). During the breeding season, the majority of stomach contents consisted of insects (84.8%), while the food composition in the post-breeding season showed increases in fishes (28.3%), amphibians (44.4%), and plant material (22.2%). During the breeding season, aquatic ephemeropterans, odonates, and hemipteran nymphs were quite abundant in the lake. Indeed, 44.2% of the food content during the breeding season consisted of nymphs. Our results demonstrated that the European pond turtle is an opportunistic predator as found in other populations (Ottonello et al. 2005) and other freshwater turtle species (e.g. Clark and Gibbons 1969; Hart 1983; Chessman 1986; Dreslik 1999). The feeding regimes of individuals throughout the year range from carnivorous to omnivorous depending on environmental conditions (Ottonello et al. 2005). This also showed that food spectrum of individuals was strongly affected by habitat conditions, such as season and prey availability. Our study also confirms the findings of other studies on this species, namely that the European pond turtle is an opportunistic predator. Despite small differences in percentages, no statistically significant difference was found between the sexes with respect to food composition. This stems from the fact that females and males use the same microhabitat during foraging. However, differences were particularly observed in the breeding season in terms of the number of prey items extracted from the stomach. This might be because females are larger and require more energy for breeding than males. In a recent evaluation of ecological diversity and phylogeny of emydid turtles, Stephens and Wiens (2003) included E. orbicularis in the strictly aquatic and

7 Journal of Freshwater Ecology 577 carnivorous category. Nevertheless, our findings demonstrate that the species display considerable carnivorous feeding in the breeding season and omnivorous feeding in the post-breeding season. Acknowledgement The authors thank Hasan Serdar Mutlu and Yusuf Bayrakci for helping them in field studies. References Alekperov AM Zemnovodnnie i Presmikayushchiesya Azerbaidzhana SSR. Akademija Nauk Azerbaidzan SSR, Elm, Baku. 264p. (in Russian). Ayres C, Calvin o-cancela M, Cordero-Rivera A Water lilies, Nymphaea alba, in the summer diet of Emys orbicularis in northwestern Spain: use of emergent resources. Chelonian Conservation and Biology. 9: Badmajewa EI, Korsakowa ND, Curjumova EJ Jekologia bolotnoj cerepachi Sarpinskoj inzmennosti Kalmyzkoj ASSR. Woprosy Gerpetologii 1985:17 (in Russian). Bannikov AG Materialy k poznaniyu biologii kavkazkikh cherepakh. Uchebnye Zapiski Moskovskogo Gorodskogo Pedagogicheskogo Instituta imeni V. P. Potemkina 18: (in Russian). Bas og lu M, Baran _I Tu rkiye su ru ngenleri, K{s{m I. kaplumbag a ve kertenkeleler. Ege U niv., Fen Fak. Kitaplar Serisi no: 76, Bornova-_Izmir, (_Ilker Matbaas{), 272p. (in Turkish). Chessman BC Diet of the murray terrapin, Emydura macquarii (Gray) (Testudines: chelidae). Australian Wildlife Research. 13: C iç ek K, Ayaz D New data on facultative paedomorphism of the smooth newt, Lissotriton vulgaris, in western Anatolia, Turkey. Journal of Freshwater Ecology. 26: Clark DB, Gibbons JW Dietary shift in the terrapin Pseudemys scripta (Schoepff) from youth to maturity. Copeia. 1969: Dreslik MJ Dietary notes on the red-eared slider (Trachemys scripta) and river cooter (Pseudemys concinna) from southern Illinois. Transactions of the Illinois State Academy of Science. 92: Drobenkov SM Characteristic features of the pond turtle (Emys orbicularis) ecology and morphology in the north of the range area. V: Abstracts, 2nd International Symposium on Emys orbicularis; Le Blanc; 1999 June p. 10. Ernst CH, Barbour RW Turtles of the world. Washington, DC: Smithsonian Institution Press. p Ficetola GF, De Bernardi F Is the European pond turtle Emys orbicularis strictly aquatic and carnivorous? Amphibia-Reptilia. 27: Fritz U Emys orbicularis (Linnaeus, 1758) Europa ische Sumpfschildkro te. In: Fritz U, editor. Handbuch der reptilien und amphibien Europas, band 3/IIIA: Schildkro ten I. Wiesbaden/Wiebelsheim: AULA-Verlag. p. 595 (in German). Fritz U Die Europa ische Sumpfschildkro te. Bielefeld, Laurenti. 224p. (in German). Fritz U, Andreas B Distribution, variety of forms and conservation of the European pond turtle. In: SOPTOM (ed.), Proceedings of the 2nd International Symposium on Emys orbicularis; 1999 June; Chelonii; Vol. 2, p Gibbons JW Turtle studies at SREL: a research perspective. In: Gibbons JW, editor. Life history and ecology of the slider turtle. Washington, DC: Smithsonian Institution Press. p

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