Is the European “pond” turtle Emys orbicularis strictly aquatic and carnivorous?

Gentile Francesco Ficetola, Fiorenza De Bernardi

In their recent, straightforward overview of have an important influence on the management the evolution of Emydid Turtles, Stephens and of this threatened species. Wiens (2003) treat Emys orbicularis (Linnaeus, 1758) as a strictly “aquatic” and “carnivorous” turtle. This interpretation directly draws from Is E. orbicularis strictly carnivore? the current point of view about the ecology of E. orbicularis. Interestingly, E. orbicularis is Only a few studies analysed the diet of E. or- the only species within the subfamily Emydinae bicularis. This species is classically consid- considered to be both strictly aquatic and car- ered a carnivore (Bannikov, 1951; Lanza, 1983; nivorous. As a consequence, within emydid tur- Ernst and Barbour, 1989). Instead, several stud- tles, two simultaneous changes in diet and habi- ies found vegetable remains in their faeces. tat have been invoked in the evolution of E. or- However, it has been disputed whether veg- bicularis: the recent ancestors of E. orbicularis etable remains should be considered as eaten were likely omnivore and semi-terrestrial (habi- “by mistake” (e.g., Lebboroni and Chelazzi, tat and dietary generalist), thus it has been hy- 1992; Kotenko, 2000). In their recent paper, Ot- pothesized that E. orbicularis evolved a more tonello et al. (2005) found plant remains in 89% specialised ecology, becoming strictly carniv- of faeces of adult E. orbicularis. This amount orous and aquatic, and thus a habitat and di- of plant items can hardly be considered to be etary specialist (Stephens and Wiens, 2003). It eaten by mistake: plants are among the most is worth noting that, following this reconstruc- common food items, furthermore adults feed tion, E. orbicularis is the only taxon (out of 64 more frequently on plants than juveniles, and analysed by Stephens and Wiens) in which a si- the amount of ingested plants increases dur- multaneous change in habitat and diet seems to ing the post breeding period (Ottonello et al., have occurred. 2005). These results are consistent with those However, evidences from recent studies sug- found in other Mediterranean populations (Leb- gest that E. orbicularis is not strictly carniv- boroni and Chelazzi, 1992, 1998), and suggest orous or aquatic: these findings suggest that that E. orbicularis is not entirely carnivorous. the “simultaneous changes” hypothesis could be Emys orbicularis seems to shift from a carni- caused by a bias in the existing literature about vore to a more herbivorous diet as it grows, E. orbicularis. A reanalysis of available data about the ecology of E. orbicularis can also similarly to other omnivore emydid turtles (e.g., Trachemys scripta: Hart 1983), and it could pre- fer less energetic food, such as plants, during Dipartimento di Biologia, Università degli Studi di Mi- the post breeding season, when the energetic re- lano, Via Celoria 26, 200133 Milano, Italy e-mail: francesco.fi[email protected]; quirements are less intense. It should also be fi[email protected] noted that a mixed diet, including both plant and

© Koninklijke Brill NV, Leiden, 2006. Amphibia-Reptilia 27 (2006): 445-447 Also available online - www.brill.nl 446 Short Notes animal matter, can increase the efficiency of the bicularis found by Ottonello et al. (2005) sug- digestive process (Bjorndal, 1991). gests that upland environment can be important also for feeding, since E. orbicularis can feed also in an upland environment (Lanza, 1983). Is E. orbicularis a strictly aquatic species? The importance of the upland environment for this species can be detected also at a landscape Terrestrial environment is important for all scale. Emys orbicularis is more frequent and freshwater turtles, as they lay eggs on land. lives at higher densities in wetlands surrounded However, species using the upland environment by a large proportion of natural, wooded, land- only for nesting are usually considered strictly scape (Ficetola et al., 2004). The composition of aquatic, while those using upland habitat also terrestrial environment could affect the presence for other activities are considered semi-aquatic and abundance of populations of E. orbicularis (or terrestrial). In which category should E. or- also at distances greater than 1500 m, and can bicularis be classified? Usually, E. orbicularis explain most of the variation in their abundance is considered to be an aquatic species (e.g., (Ficetola et al., 2004). Ernst and Barbour, 1989), since some of their Finally, it is possible that the importance of most conspicuous behaviours (such as bask- terrestrial behaviour is variable among popula- ing or mating) occur in or very close to the tions. For example, terrestrial activity could be water (e.g., Di Trani and Zuffi, 1997; Rovero more important for populations that live in wet- et al., 1999). However, following a quantita- lands suffering seasonal draughts (e.g., Utzeri tive approach, E. orbicularis is among Emy- and Serra, 2001). did turtles the one that can move furthest from wetlands. Semlitsh and Bodie (2003) review the data about the use of terrestrial habitat in Conclusion 28 species of freshwater turtles, mainly from North America. They reported no cases of dis- Altogether, these studies suggest that E. orbicu- tances exceeding ∼1600 m from wetlands. For laris is not more strictly carnivorous or aquatic the close relatives of E. orbicularis (Emydoidea than closely related species: plants are impor- blandingii and Clemmis spp.), usually consid- tant food items for adults, and the upland envi- ered semi-aquatic species, the overland move- ronment is very important for this species. At ments span up to 1620 m (Joyal et al., 2001). least two main implications can be drawn from However, Jablonski and Jablonska (1998) re- this analysis. port that E. orbicularis can move up to 4 km First, it is not necessary to hypothesize two far from their wetland for nesting, and reports recent, simultaneous changes in the evolution of terrestrial migrations exceeding 1 km are of ecology of E. orbicularis. This observation not uncommon (Lebboroni and Chelazzi, 1998; makes more clear cut the hypotheses about the Schneeweiss and Steinhauer, 1998). evolution of ecological traits in Emydid turtles Maybe more importantly than any record (Stephens and Wiens, 2003): it is consistent of exceptional terrestrial movements, E. orbic- with the observation that habitat changes occur ularis uses upland environment for activities prior to dietary changes, that habitat and diet other than nesting migration. Terrestrial activity do not change on the same branch, and that is frequently performed also by males (Nalleau, changes in ecology are very rare in the evolution 1992); for example the upland environment is of Emydid turtles, both in Emydinae and in used for aestivation, hibernation and for travel- Deirochelynae (Stephens and Wiens, 2003). ling (Naulleau, 1992; Fritz and Gunther, 1996; Second, plans for the conservation of habitat Utzeri and Serra, 2001). Moreover, the abun- of E. orbicularis usually focus on the manage- dance of terrestrial insects in the diet of E. or- ment of wetlands or of wetland systems (e.g.,