Herpetology Notes, volume 13: 875-881 (2020) (published online on 22 October 2020)

Feeding habits of the European pond orbicularis (Linnaeus, 1758) in the Lake Tonga, Algeria

Nadia Ziane1, Samira Fediras1, Rachid Rouag2,*, Anthony Olivier3, and Slim Benyacoub4

Abstract. We studied the feeding habits of Emys orbicularis in the Lake Tonga, situated in north-eastern Algeria. The ecology of this turtle is little known in Maghreb, and in this study, detailed data on the diet composition are presented. Food data were recovered by faecal pellet analysis. In total, 43 faecal pellets were collected in 2017 and analysed, and 353 prey items were identified from 22 females, 21 males. The food habits of this population seemed more specific than those of other Emys orbicularis populations in other regions. Emys orbicularis feeds on a wide range of food categories and is also a specialist of freshwater snails. The ate more than plant material, aquatic molluscs being the most conspicuous. There were no differences in the consumption of food items between the sexes categories.

Keywords. Emys orbicularis, diet, food habits, El Kala National Park, freshwater turtle

Introduction we study the feeding ecology of the Emys orbicularis. This species is one of the most In any study of evolutionary ecology, food relations widely distributed water turtle species ranging from appear as one of the most important aspects of the North-western Africa in the west to the former Aral Sea system of animate nature (Hutchinson, 1959). Studies of in the east, and from the Moscow region in the north food relations are centrally important to understanding to the Turkish-Syrian border in the south (Fritz 2001, the ecology of population and community and can 2003). However, populations of the European pond provide insight on the evolution and dynamics of turtle are considered endangered in several parts of its biological systems (Madsen and Shine, 1996; Ford et range (Farkas and Sasvári, 1999; Sommer et al., 2009; al., 1998; Caldwell and Vitt, 1999; Rodríguez-Robles Fritz and Chiari, 2013). and de Jesús-Escobar, 1999). Animal foraging and The ecology of the European populations of Emys feeding ecology are influenced complexly by many orbicularis has been studied by many authors during factors, including several abiotic and biotic elements the last two decades (Fritz et al., 2017). Biological of the animal’s environment (Stephens and Krebs, characteristics of the species, including feeding habits, 1986; Berdoy and Mac Donald, 1991). In this paper, require extensive research to provide the information to apply proper conservation measures. The diet of the European pond terrapin Emys orbicularis is poorly known, especially in the Mediterranean region (Ottonello et al., 2005). Some studies showed that this species 1 Laboratoire de biosurveillance environnementale. Université mainly feeds on aquatic and terrestrial invertebrates Badji Mokhtar. Département de (Bannikov, 1951). Others noticed the predominance of Biologie. BP. 12. El Hadjar. 23000 Annaba, Algeria. invertebrates but a high occurrence of plant matter in the 2 Laboratoire de recherche sur la biodiversité et la pollution des diet. (Lebboroni and Chelazzi, 1991; Kotenko, 2000). écosystèmes. Université Chadli Only a few studies on the Maghreb populations have Bendjedid. 36100 El Tarf, Algeria. been conducted especially on phylogeography (Stuckas 3 Station Biologique de la Tour du Valat, Le Sambuc, 13200 et al., 2014), distribution (Fahd et al., 2009; Donaire Arles, France. 4 Université Badji Mokhtar. Département de Biologie. BP. 12. et al., 2011; Velo-Anton et al. 2015) and recently on El Hadjar. 23000 Annaba, Algeria. population structure (Tiar Saadi et al., 2017; Fediras et * Corresponding author. ������� ��������������������� al., 2018) and parasitism (Fediras et al., 2017). 876 Nadia Ziane et al.

In this paper, we study the feeding ecology of E. period to drain the lake. This lotic ecosystem is limited Orbicularis and we evaluate the dietary variation by the Mediterranean Sea to the north, Tonga Lake to between (males, females). The diet of the European the south, the plains of Souarekh to the west and pine pond turtle is poorly known (Ottonello et al., 2005, forests to the east. It stretches for a distance of 3 km, 2018). The results are interesting biogeographically, with an average width of 12 m. The study site contains since this is the first time that feeding habits are studied high plant diversity; we noted the presence of Typha in the southern limits of the range of this species where angustifolia, Phragmites australis, Scirpus lacustris, the environmental conditions are different from those of Iris pseudacorus, Nymphaea alba and many other European populations. aquatic species. The fauna is very diverse; we notice the presence of several rare birds such as Gallinula Materials and methods chloropus, Porphyrio porphyrio, and the Heron Bubulcus ibis (Fig. 1). Study area.—This study was carried out in the National Park of El Kala, in north-eastern Algeria. This protected Fieldwork.—The field study was carried out between territory is ecologically very important because it 01 March and 28 July 2017. Each month, four research includes some waterbodies which are intensively used days were conducted, i.e. a total of 20 research days by birds and other faunistic group as they are among were spent in the field during the whole study. Each the few wet areas situated inside the overall dry day, research was conducted from 09:00 to 17:00 h; environments of northern Algeria (Benyacoub et al., approximately 160 man-hours of research were spent in 1998). Overall, the national park has a surface of 78,400 carrying out this study. Individuals were hand captured ha, and is characterised by an alternation of lakes, during visual searches. During the study, the European marshes, and hilly territories (up to 600 m elevation), pond turtles were marked by notching their marginal covered with relatively dense vegetation (De Belair, scutes (Gibbons, 1990). On every specimen caught, 1990). The climate is Mediterranean (Seltzer, 1946; seven morphometrical variables were measured and then Toubal, 1986); rainfall is moderate, and concentrated each individual was released at the site of capture. The during the winter months. Total annual rainfall is about carapace length (CL) was measured by a digital calliper 630 mm, and the mean monthly rainfall is about 52 mm (precision ± 0.1 mm) with the same measurement (Benyacoub et al., 1998). The study was carried in the criteria of Stubbs and Swingland (1984). The body “Canal Messida”. The area is about 5 ha situated in the mass of the turtles was measured by a digital balance north of Lake Tonga (36°53’N, 8°31’E). The “Messida (precision ± 1 g). Sex was determined by secondary canal” is an artificial canal that connects Tonga Lake sexual characteristics (e.g., plastral concavity, the length to the sea. It was dug by the French during the colonial of tail) (Rossler, 2000). We quantified E. orbicularis diet by analysing faecal pellets because it is non-invasive. However, this method may pose biases in that softer materials may be digested so they are unidentifiable in the faecal fragments (Demuth and Buhlmann, 1997; Gunzburger, 1999). Turtles typically defecated during capture and manipulation. Their faecal pellets were collected, placed in ethanol (50% v/v), and stored in plastic vials for subsequent analysis. To avoid pseudo-replication, only one pellet was collected per turtle. The faecal samples collected were washed with water and filtered with a 500-micrometre sieve, stored in 70% alcohol and examined under a dissecting microscope. For each food type, the number of items was recorded. Data analyses.—Data on faecal pellets were analysed by sex (females and males). The diet was analysed according to several descriptors. Prey type richness, Figure 1. Location of Lac Tonga with major vegetation types Number of prey items (N), relative frequency (F%) and study area. and frequency of occurrence (Fo%) of the food item. Feeding habits of the European pond turtle in the Lake Tonga, Algeria 877

Shannon–Weaver diversity index (H) to calculate a was dominated by molluscs and especially gastropods measure of the prey species diversity for each turtle which contains 4 orders of freshwater snails. In the pellet; Food niche overlap (Ojk) between sexes was order Basommatophores four families were identified: quantified using Pianka’s (1986) symmetric equation. Physidae, Ancylidae, Planorbidae and Lymnaeidae To test for dietary differences among males and females, (Table 1). Prey that were not determined were classified we used the t-test on the number of individual turtles that together as unidentified prey. ate the different items. Statistical analyses, with all tests The diet was dominated by molluscs which occupy being two-tailed and alpha set at 5%, were performed 40.52% (n = 143) of the food range of the turtles and using Statistica (Version 7.0) software. which are represented by 5 Orders, the most important is the Basommatophores 21.81% (n = 77) followed by Results aquatic beetles in insects which hold a high proportion General diet.—We analysed faeces from 43 E. 18.13% (n = 64) compared to other insects. Tadpoles orbicularis: 21 adult males (mean carapace length, CL = were an important food for turtles 15.58% (n = 130.65 ± 10.57 mm; range 110.01-161.20 mm), 22 adult 55). Other categories such as bivalves, Hemiptera, females (mean carapace length, CL = 151.00 ± 18.96 Ephemeroptera, Spiders, Odonata or Hymenoptera mm; range 110.10-179.67 mm), and we categorised are the less consumed preys by the European Pond 353 faecal fragments. 21 prey items were identified Turtle. With 15.01 % (n = 53), vegetation is present in in the faeces of the European pond turtle and were turtle faeces. The identification of scales confirms the distributed among Molluscs, Arthropods, Annelids, consumption of fish by turtles, however, it is unknown vertebrate and plant material. The diet was diverse and if this species is a fish predator or scavenger.

Table 1. Diversity of diet and abundance of prey items in the faeces of the European Pond Turtle Emys orbicularis from Tonga Lake. Table 1. Diversity of diet and abundance of prey items in the faeces of the European Pond Turtle Emys orbicularis from Tonga Lake

Prey taxon N F (%) Fo (%) Heterostropha 6 1.70 6.82 27 7.65 31.82 Class 8 2.27 11.36 Basommatophora 77 21.81 95.45 Architaenioglossa 20 5.67 22.73 Veneroida 2 0.57 4.55 Class Bivalvia Unionida 3 0.85 2.27 Total 143 40.52 Coleoptera (aquatic) 64 18.13 31.82 Hemiptera 8 2.27 11.36 Class Insecta Ephemeroptera 4 1.13 4.55 Arthropoda Odonata 9 2.55 11.36 Hymenoptera (ants) 3 0.85 9.09 Class Arachnida Araneae 1 0.28 2.27 Total 89 25.21 Class Clitellata Arhynchobdellida 1 0.28 2.27 Annelida Class Polychaeta Polychaeta 4 1.13 2.27 Class Amphibia Unidentified tadpole 55 15.58 65.91 Vertebra Unidentified fish 2 0.57 2.27 Unidentified prey 6 1.70 11.36 Plant material Unidentified 53 15.01 63.64 Total 353 100

878 Nadia Ziane et al.

In terms of frequency of occurrence, the diet of the The food spectrum of males was larger than females European pond turtle is also dominated by Gastropods with four more categories (Unionid, Hymenopter, Spider in particular Basommatophora with 95.45% of ingested and fish). Hymenoptera represented 16.66% of the food prey, followed by the tadpoles and the plants with 65.91% range and plant material 8.35%. Basommatophores were and 63.64% respectively. In insects, Coleoptera is the the most consumed prey. The application of Student’s t- most ingested prey (31.82%). Hemiptera, Hymenoptera test to compare the diet of males and females revealed no and Odonata are accessory prey. Bivalves, spiders and significantly difference (t-test, t = 0.195, p = 0.8476). fish are accidental prey in the European Pond Turtle. Shannon’s diversity and Equitability indexes did not differ between females and males. The application of Sexual differences in diet.—Females consumed a total Hutcheson t-test to compare Shannon diversity index of 191 prey items with an average of 8.68 prey/faeces; between males and females revealed no significantly males with 150 prey items and consumed an average of difference (t = 0.109, p = 0.9128, df = 271). Equitability 7.14 prey/faeces. Among males, Basommatophores were is high and is almost identical between males and the most consumed prey. They accounted for 22.65% females (0.80 and 0.82). of ingested prey followed by tadpoles with 18.67%. This means that all the prey is distributed almost Coleoptera and plants each occurred at 14.67%. The equitably among the different species that form the other categories of prey are poorly represented in the food spectrum of the European pond turtle. The value diet. For females, Coleoptera was the most frequently of overlapping food niches is very high between males consumed prey with a relative abundance of 21.99%. and females (O = 0.938; P = 0.999), rejecting the Basommatophores had a frequency of 18.85%; followed jk obs

Table 2. Prey frequencies (F%) and diversity indexes and sex for the European pond turtle�. Table 2. Prey frequencies (F%) and diversity indexes and sex for the European pond turtle

Prey taxon Female (N = 22) Male (N = 21) Population Basommatophora 18.85 22.65 Heterostropha 2.09 1.33 Neotaenioglossa 10.99 4 Littorinimorpha 2.62 2 Architaenioglossa 7.33 4 Veneroida 0.52 0.67 Unionides - 2 Coleoptera 21.99 14.67 Hemiptera 1.57 3.33 Ephemeroptera 2.09 - Odonata 1.57 4 Hymenoptera - 0.67 Araneae - 0.67 Arhynchobdellida 0.52 - Polychaeta 2.67

Unidentified tadpole 14.14 18.67 Unidentified fish - 1.33 Unidentified prey - - Plant material 15.72 14.67 Shannon Diversity (H) 3.02 3.19 3.25 Equitability (H/Hmax) 0.82 0.80 0.88

Feeding habits of the European pond turtle in the Lake Tonga, Algeria 879

Discussion has already been reported by Vilizzi et al. (2015) for E. orbicularis and Ottonello et al. (2016) for Emys Only a few studies have analysed the diet of Emys trinacris and is probably related to its low availability orbicularis. This turtle is an opportunistic predator in the environment due to the presence of fish. Females with a large food niche similar to many other tend to ingest a few more Gastropods and insects freshwater turtles (Clark and Gibbons, 1969; Georges, (especially Coleoptera) than males, but we found no 1982; Chessman, 1986). This species is considered a statistically significant difference in the composition of carnivore (Bannikov, 1951; Lanza, 1983; Ernst and the diet between the two sexes. The same observation Barbour, 1989); it also changes its regime according to was made for (Ottonello et al., different habitats that are related to differences in the 2016). In Doñana (Spain), the adult diet was based on availability of prey (Ottonello et al., 2005, 2018). Its with a small proportion of plants. Animal prey diet is opportunistic in which the animal component predominates but also includes plants (Fritz, 2001). was dominated by crustaceans and, to a lesser extent, However, it is often difficult to determine whether plant by Heteroptera, Odonata, Hymenoptera, Diptera, material is accidentally ingested with animal prey or is Coleoptera, Annelidae and fishes (Pérez-Santigosa et an elementary food (Lindeman, 1996). Several studies al., 2011). have found plant remains in their faeces. However, it has The feeding strategy of our population is not similar to been considered that plant remains should be considered those found for other populations of Emys orbicularis “mistakenly consumed” (Lebboroni and Chelazzi, (Ficetola and De Bernardi, 2006) or its counterpart 1991; Kotenko, 2000). For our population, the plants Emys trinacris (Ottonello et al., 2017) whose main are present in more than 60% of the faeces analysed. prey are aquatic invertebrates. Our population showed The plant material can be consumed voluntarily and a tendency to specialise in gastropods and especially is an important part of the food spectrum. A very high freshwater snails. The choice of prey is a question of the number of water lily seeds (Nymphaea alba) was found availability of the prey and also of the characteristics in fecal samples in the diet of the population of the of the environment (George, 1982; Chessman, 1986; Louro River (Pontevedra - Spain). Further analysis of Demuth and Buhlmann, 1997; Ottonello et al., 2005). samples indicated that E. orbicularis uses water lilies In addition, we believe that the European pond as an emergent food resource during summer. It is turtle consumes prey in proportion to their relative proposed that E. orbicularis should no longer be viewed abundances in the environment. Annual sampling would as strictly carnivorous (Ayres et al., 2010). be desirable to have the variation of the diet during the In the Camargue (France), the diet of the species was different seasons depending on the variation in aquatic based in the spring on invertebrates and in summer there fauna and trophic availability. The comparison between is a greater use of plant material. They found the remains several populations will undoubtedly make it possible of plants in 89% of the faeces of adult E. orbicularis to understand whether the European basin turtle is an (Ottonello et al., 2005). The same results were found in opportunistic species, feeding on prey available in each a restocked population of the European pond turtle in environment or, on the contrary, it has its own food northwest Italy (Ottonello et al., 2018). needs and preferences. The diet of our population was specialised on molluscs and especially gastropods which occupied 39.1% of the Acknowledgments. We are grateful to Dr. P. Grillas, Program food spectrum followed by insects 24.93%, then by Director in the research center for the conservation of Mediterranean wetlands (Tour du Valat) for receiving us in the plants with 15%. Tadpoles were identified when not research station and for the use of their facilities during our stay. completely digested. They were readily available in This research was funded by the Hubert Curien Programme; the aquatic environment and constituted an important PHC Maghreb N°19MAG50 / 41431WD. Permits to capture and source of protein for turtles. A tadpole represented about analyse the turtles (N°: 418/SD/PNEK/2016) used in this study 15% of the food spectrum and is consistent with reports were released by the Director of the National Park of El Kala. from other populations (Skibinski, 1954). Tadpoles are one of the main categories of prey of E. orbicularis in References Turkey (Çiçek and Ayaz, 2011) Ayres, C., Calviño-Cancela, M, Cordero-Rivera, A. (2010): Water Plants are important for both sexes with almost equal lilies, Nymphaea alba, in the summer diet of Emys orbicularis proportions, 14.67% in males and 15.72% in females. in northwestern Spain: use of emergent resources. Chelonian The reduction of invertebrate diversity and abundance Conservation Biology 9: 128–131. 880 Nadia Ziane et al.

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Accepted by Eric Munscher