The use of emergent or seasonal resources during shortage of preferred prey is well known in many species. For instance, the Eurasian otter, Lutra lutra, has shifted its diet due to the presence of an introduced crayfish (Delibes and Adrián 1987; Beja 1996); other species also use this emergent resource (Peris et al. 1994; Correia 2001) in the Iberian Peninsula. The otter is also able to feed on turtles if there is a shortage of fish (Lanszki et al. 2006; García and Ayres 2007). For turtles, the seasonal use of aquatic insects and amphibian eggs has recently been described for the Spanish pond turtle, Mauremys leprosa (Alarcos et al. 2008; De Vries and Marco 2008). This paper describes the use of another seasonal resource by Emys orbicularis in northwestern Spain.

Emys orbicularis is widely distributed across Europe, parts of Asia, and Northern Africa (Fritz 2001). In the Iberian Peninsula, this species is common in some areas, while northern populations are clearly in decline (Ayres Fernández and Cordero Rivera 2004). Nevertheless, with the exception of the work of Keller (1997), very little is known about its regional ecology and behavior.

As Ottonello et al. (2005) noted, information about the diet of E. orbicularis across its distribution is sparse, especially in the Mediterranean region. Some authors have treated E. orbicularis as strictly carnivorous (Ernst and Barbour 1989; Stephen and Wiens 2003), and Bannikov (1951) showed that in Daghestan the species feeds mainly on aquatic and terrestrial invertebrates. However, other studies (Lebboroni and Chelazzi 1991; Kotenko 2000; and references in Fritz 2001) found plant matter in the diet, but this was considered accidental intake. Even in the Iberian Peninsula, E. orbicularis has been viewed as strictly carnivorous, while the Spanish pond turtle is considered to feed largely on plants (Keller and Busack 2001; Gómez-Mestre and Keller 2003). Recent studies by Ottonello et al. (2005) and Ficetola and De Bernardi (2006) presented data of high prevalence of plant matter in the diet of E. orbicularis, casting doubt on its having a strictly carnivorous diet.

In this work we present new data supporting adaptability of E. orbicularis to habitat resources, suggesting a dietary shift to plant matter in the summer.

Methods

The population of E. orbicularis studied is located in Centeáns ponds, in the valley of the Louro River (northwest Spain, lat 42°10′N, long 8°37′W). The species survives in a protected area (Gándaras de Budiño e Ribeiras do Louro) that is part of the Spanish Natura 2000 network, which is endangered by heavy industrial pressure (Ayres Fernández and Cordero Rivera 2001). This population inhabits abandoned clay pits, which are common in the area, and also natural ponds. The Centeáns ponds are clay pits at least 20 years old and include a group of 7 ponds of variable size with a mean diameter of 60.6 m (range 19 to 125 m). The ponds are also deep (to 30 m) with high slopes. Some of these ponds are still being used for clay extraction, while others are now naturalized and have a dense cover of aquatic vegetation, including water lilies, Nymphaea alba.

Pond turtles were captured by hand or with eel traps baited with canned sardines from mid-June to October between 2003 and 2008, and then placed in individual containers with water for at least 1 day, in order to obtain fecal samples. Samples were stored in plastic tubes and their contents identified. The number of water lily nuphar seeds per sample was counted and other dietary items noted. Means are presented with their standard errors.

Results

Fecal samples contained water lily seeds, ranging from 12 seeds from a juvenile, to more than 2000 seeds from an immature turtle. The mean value for the global sample was 695.2 ± 606.8 (N  =  34). There was high variability in the fruit intake by individuals (Fig. 1). The mean for adults was 821.1 ± 524.6 seeds (N  =  16), and the mean for immature turtles was 1068.7 ± 752.6 (N  =  8). Two small juveniles captured in 2006 had 12 and 60 seeds each in their fecal samples, and the mean for juveniles was 195.2 ± 144.8 seeds (N  =  10).

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Using a Kruskal–Wallis test, significant differences in the presence of seeds in fecal samples between age classes were detected (15.73, df  =  3, p  =  0.001). Nearly all individuals had fecal samples composed only of N. alba seeds (100% in volume), which could be detected in the digestive tract by inguinal palpation, as is done to detect the presence of shelled eggs (Bertolero and Marin 2005). Only one individual also had remains of an unidentified water snail in its fecal sample. No direct observations of N. alba fruit consumption by turtles were made, but juveniles were observed eating petals of nuphar flowers, and adults were observed eating common cattail leaves (Typha latifolia) (C. Ayres, pers. obs.).

Discussion

There is a lack of information about the feeding ecology of E. orbicularis as noted by Otonello et al. (2005) and Ficetola and De Bernardi (2006). Although most authors (Bannikov 1951; Lanza 1983; Ernst and Barbour 1989) considered this species to be a carnivore, some work in the Mediterranean region (Lebboroni and Chelazzi 1992, 1998) suggested that E. orbicularis is not entirely carnivorous. There are few long-term studies that cover year-round feeding behavior of E. orbicularis. In the study area we also detected some predation on American crayfish (Procambarus clarkii). Emys orbicularis in our study area is capable of changing its diet, shifting to an almost completely vegetarian diet during summer months.

Otonello et al. (2005) proposed that the differences in the abundance of plant matter in the diet of E. orbicularis could be related to 2 different phases of the year, reproductive and postreproductive, associated with seasonal migrations of individuals to different habitats. In our area there is no evidence of migration to summer areas, but the dietary shift could be linked to the aestivation period since there is typically a decline in the activity of E. orbicularis in summer. The lower energy requirements and hunting skills associated with these periods of lower activity may favor a preference for food items that have a lower energy value but are easier to obtain, according to the optimal foraging theory (MacArthur and Pianka 1966).

Ficetola and Di Bernardi (2006) suggested that this behavior could be an ontogenetic dietary shift, changing to a more herbivorous diet as it grows, as has been described for other emydid species (Clark and Gibbons 1969; Hart 1983). Nevertheless, results from this study do not coincide with that suggestion. In this population we recorded nuphar fruit consumption in all age classes, and some animal matter was also present in the spring and autumn diet.

Most studies in the past assumed that plant matter in the diet was an accidental intake while feeding on insects or other food (Lebboroni and Chelazzi 1991; Kotenko 2000; also see Fritz 2001), but in our work it is clear that the presence of N. alba seeds was not accidental. Calviño-Cancela et al. (2007) stated that nuphar fruits contained an average of 392 ± 70.7 seeds; thus, it is clear that only specific consumption of N. alba fruits could result in the high number of seeds detected in the fecal samples.

Emys orbicularis acts as a disperser of N. alba seeds, functioning as a nonstandard agent, i.e., one for which the plant apparently lacks any adaptation (Calviño-Cancela et al. 2007). Further studies will be necessary to understand the relationship between these species.