Home range, movements, and habitat use of the European pond turtle (Emys orbicularis) in the Rhône-Alpes region, France

Biologia, Bratislava, 59/Suppl. 14: 89 94, 2004 Home range, movements, and habitat use of the European pond turtle (Emys orbicularis) in the Rhône-Alpes region, France Antoine Cadi 1,2,MélanieNemoz 3, Stéphanie Thienpont 3 & Pierre Joly 1 1 UMR CNRS 5023, Ecologie des Hydrosystèmes Fluviaux, Université Claude Bernard Lyon 1, F 69622 Villeurbanne Cedex, France; e-mail:a.cadi@fnh.org 2 Conservatoire Rhône-Alpes des Espaces Naturels, 2 rue des Vallières, F 69390 Vourles, France 3 Lo Parvi Association, F 38890 Saint Chef, France CADI, A.,NEMOZ, M.,THIENPONT, S.&JOLY, P., Home range, movements, and habitat use of the European pond turtle (Emys orbicularis) intherhône- Alpes region, France. Biologia, Bratislava, 59/Suppl. 14: 89 94, 2004; ISSN 0006-3088. The European pond turtle (Emys orbicularis) isconsideredasanumbrella species for nature conservation. Its biological cycle requires the conservation of both aquatic and terrestrial habitats. In order to design efficient management actions for an endangered species a solid knowledge of the biological and ecological requirements is needed. To achieve this objective, the population parameters, movement pattern and home range size were estimated for a wild population in the French department Isère, inhabiting areas of mixed natural and agricultural habitat. We monitored 10 males and 10 females using radiotelemetry. We also trapped turtles to obtain additional data on population structure (450 capture events in 2000 and 2001). We present evidence of a seasonal pattern in the habitat use of the European pond turtle (overwintering, growth, foraging and nesting sites) in the study area and underline the importance of determining habitat types. Our results highlight the importance of large-scale protection of mixed habitats for Central European pond turtle populations. Linking aquatic habitats and nesting sites is crucial for the survival of populations under human environmental pressure. Key words: Emys orbicularis, habitat use, telemetry, conservation, habitat management, France. Introduction Freshwater turtles usually inhabit lentic and lotic habitats with stable hydroperiods. Wetlands are used for basking, feeding, mating, and overwintering (SERVAN, 1986, 1988; LEBBORONI & CHELAZZI, 1991; DALL ANTONIA et al., 2001). The annual cycles of some species are well documented, e. g. for Trachemys scripta (Schoepff, 1792) (GIBBONS, 1990). Males of Emys orbicularis (L., 1758) rarely leave their habitat except to emigrate, search for females, or for terrestrial hibernation (DUGUY & BARON, 1998). Females may leave the wetland to emigrate, overwinter, and for egglaying which occurs once to several times a year (ROVERO & CHELAZZI, 1996; DALL ANTONIA et al., 2001). T. scripta hatchlings, after emergence from terrestrial nests, migrate to the wetland to feed and grow (GIBBONS et al., 1990). Feeding activity apparently decreases in this species when 89

Table 1. Capture session dates from 2000 to 2001 in both La Serre and Lemps ponds. Sessions La Serre Lemps June 2000 1 4 June 2000 2 5 June 2000 July 2000 4 7 July 2000 11 14 July 2000 September 2000 19 22 September 2000 12 15 September 2000 March 2001 20 23 March 2001 25 February 28 March 2001 May 2001 1 4 May 2001 7 10 May 2001 June 2001 19 22 June 2001 26 29 June 2001 August 2001 25 28 July 2001 1 4 August 2001 September 2001 15 18 September 2001 26 29 September 2001 mean temperature is decreasing (CAGLE, 1946). Feeding and basking become more frequent in freshwater turtles when ambient temperatures rise to 20 to 30 C (BURY, 1979). In Italian E. orbicularis, courtship and mating occur in spring, egg-laying in June (ROVERO & CHELAZZI, 1996). Numbers and activity levels are both highest in summer. Protecting freshwater turtles depends directly on the quality of both aquatic and surrounding terrestrial habitats. Nowadays, a high proportion of freshwater turtle species is in need of conservation because of the alteration and exploitation of freshwater habitats. These threats are major causes of decline for many species. Among the vertebrates that inhabit aquatic systems, turtles are a pervasive group whose semi-aquatic behaviour makes them especially important for understanding the link between aquatic and terrestrial habitats (BODIE & SEMLITSCH, 2000). The European pond turtle occurs over a wide distribution range, from North Africa to East Europe and Central Asia, as far as the Aral Sea (FRITZ, 1996). As E. orbicularis is listed in the Habitat Directive of the European Commission (Annexes II and IV) and in the Bern Convention (Annexe II), a number of conservation programmes have been started in France. However, little is known about habitat use in wild French populations. This may result in difficulties when designing effective management plans. We investigated the use of aquatic and terrestrial habitats by European pond turtles in the French Isère department. In particular, we tested whether sexes have different habitat preferences. Material and methods Study area Data were collected from March to October 2000 and 2001 in a large area in the Isère department, France. The site of La Serre (45 43 42 N, 5 25 25 E) comprises five ponds connected to each other by ditches or separated by dikes (45 ha submerged area); part of the site is protected. Capture The site was sampled monthly from May 2000 to September 2001 (Tab. 1). Drifting traps made of a 5 m-long net were stretched perpendicularly to the shoreline, with a hoop trap fastened to the end of the net, so that turtles swimming in either direction along the shoreline were driven towards the traps. Traps were placed in the water along the shoreline (1 trap every 50 m). Traps were checked and rebaited daily. The site was trapped continuously for four nights. A minimum interval of 30 days was left between two sessions in the same site (for more details see CADI, 2003). Turtles were individually marked by marginal notching. Sex and age (juvenile vs. adult) were recorded. For recaptured individuals, date, individual number, and trap number were recorded. Turtles were released into the water at the end of the session, near thetrapinwhichtheywerecaught. Radiotelemetry Monitored individuals were located by telemetry. Because habitat use is potentially different between sexes in some freshwater turtles (VOGT, 1980), we monitored both males and females. Transmitters were too heavy for hatchlings. Hence, hatchlings were not studied. Ten adult female and ten adult male Emys orbicularis were captured, measured, marked, fitted with radiotransmitters (TW-3, Biotracks, UK, Receiver Mariner 57, 148 149 MHz and Yagi antenna), and released within 1 24 h (from 17 May 2000 to 31 May 2001). Radiotransmitters were attached to the anterior upper carapace margin with aluminium machine screws, and plumber s epoxy was used for streamlining. Transmitter packages weighed less than 5% of the turtle body mass. Transmitter frequencies were searched daily from the end of March to the beginning of October, then once a week during the rest of the year. As females usually dig their egg chambers in the afternoon or evening (KOTENKO, 2000; MITRUS & ZE- MANEK, 2000), all individual transmitter frequencies were searched each day during the afternoon; then twice in the beginning and the middle of the night. Occasional long-range (> 1 km) movements by some 90

Fig. 1. Daily movements (grey) and distances from the overwintering site (black) from May 2000 to July 2001. Both sexes were combined as no significant differences exist. individuals required searches by four wheel drive vehicle or boat. Results Population structure 450 captures were performed in the course of eight sessions. We identified a total of 226 individuals (juveniles n = 104, males n = 70, females n = 52). Distances Distances between two consecutive locations changed simultaneously in both sexes (Spearman rank correlation test: ρ = 0.491, P < 0.0001). Changes in daily movements over the study period are summarizedinfigure1.movementsstartinmayand end in November; they strongly increase in May, and decrease from August onwards. This cycle was found in all three activity periods. During hibernation, 15 of 20 monitored individuals (75%) were located in the same area. Distances between each location and the previous hibernation spot increase simultaneously with the values of everyday distances (Fig. 1), indicating post-hibernation dispersal (Spearman rank correlation test: ρ = 0.820, P < 0.0001). Short range movement Home range was computed for each sex over two activity cycles (from one hibernation to the next, including all terrestrial and aquatic locations). We obtained home ranges of 7.74 ± 3.63 ha for males and 12.51 ± 8.38 ha for females (home range, polygon convex method with 95% of the locations). Male and female home range sizes are not different (Mann-Whitney U test: U = 48, P = 0.87). Home ranges computed in the 2001/2002 period overlay those of 2000/2001 by 72 ± 15%. Long range movement Long distance movements (for egg-laying or changing ponds) require crossing dry land if aquatic pathways are lacking. 8 (3 males and 5 females) out of 20 turtles changed ponds during foraging periods (average distance moved on land: 143 ± 217 m, min-max: 5 520 m; May and June). All turtles returned between mid-august and mid- September, i. e., before hibernation. We observed egg-laying movements of 124 ± 90 m (min-max: 10 300; n = 16). During the nesting season (June), most females were reported to nest at night (n = 21, 76%). The longer the distance between pond and egg-laying site, the earlier in the afternoon turtles came out of the water. Discussion Our data of movement patterns indicate that the annual cycle of Emys orbicularis can be divided into two phases: an activity period from April to October and a lethargic, hibernation period from November to March. Similar observations have been reported for other parts of the range (Italy: ROVERO & CHELAZZI, 1996; Hungary: FARKAS, 2000; Ukraine: KOTENKO, 2000). The duration of these periods is influenced by climatic conditions. Our studied turtles migrated significant distances in response to seasonal changes. In the temperate zone, all turtle species hibernate (ROLLI- NAT, 1934; GIBBONS et al., 1990; PARDE et al., 1999), E. orbicularis mostly under water (our results). Movements are restricted during hibernation; they increase as soon as weather conditions allow (increase in temperature and insolation). A very long hibernation period in the 2000/2001 winter is explained by the presence of a thick ice layer that prohibited any movement for more than a month. Overwintering is essential for turtles living 91

in regions where winter temperatures approach or fall below freezing. Some overwintering individuals become active on sunny days, if their body temperatures can be raised sufficiently by aquatic or aerial basking. In spring, probably strongly influenced by the need of food, turtles move back to shallow, well-vegetated areas. The progressive scattering of locations over the whole wetland area during the activity period corresponds to spreading to all surrounding aquatic biotopes. This is probably linked to an optimization of resource acquisition or avoidance of competition for food and basking sites. In La Serre, the habitat is richly structured, with small patches of reeds, Carex, and water lilies, harbouring important food items for turtles, such as snails and larvae of water insects. For South American mud turtles (Kinosternon leucostomum), MORALES-VERDEJA & VOGT (1997) believe that the irregular distribution of such small plant patches, and hence of food resources, explains the observed wide scattering of turtles. According to BURY (1979), home range size is limited by physical barriers (dikes, canals). The commonly observed wide spreading of turtles suggests that each individual utilizes as much of the wetland as possible within these limitations. Movements over dry land to change ponds are known to be fast and direct in E. orbicularis (NAULLEAU, 1991; LEBBORONI &CHELAZZI, 2000). Females can travel overland several hundred metres during egg-laying, in some parts of the range even over kilometres (SERVAN, 1988; ROVERO & CHELAZZI, 1996; KOTENKO, 2000). We found a strong homing behaviour for most individuals, particularly for the hibernation site. We suppose the survival rate during hibernation is much higher than during an overland or aquatic travel to the hibernation site. Several studies have shown that emydid turtles are able to home after experimental displacement (Chrysemys picta: CAGLE, 1944; Clemmys guttata: ERNST, 1968; Emys orbicularis: LEBBORONI & CHELAZZI, 2000). Moreover, a water-finding ability (orientation towards aquatic habitats outside the home range and beyond the field of view) has been demonstrated for T. scripta (YEOMANS, 1995). This strong habitat fidelity highlights the risks resulting from short-term landscape modification on individual survivorship. Italian E. orbicularis are known to use their complete home range (including wetlands of several hundred square metres) during an annual cycle (LEBBORONI &CHELAZZI, 1999). Freshwater turtles are long-lived organisms and habitat disturbances may not be immediately obvious (CONGDON et al., 1993, 1994). Every component of the annual cycle of turtles is at risk in human-dominated landscapes. The failure of protecting a single annual or life cycle stage habitat will ultimately doom the entire population to extinction (BUHLMANN et al., 1997; BODIE &SEM- LITSCH, 2000). Hence, complete habitat protection, acquisition, and maintenance should be basic priorities in conservation programmes. An ideal reserve must include a large breeding nucleus along with optimal nesting and feeding habitats. In Central French pond turtle populations, a terrestrial buffer zone must be at least 200 m around all the wetland. The objective is to protect the breeding nucleus so that it can continually supply recruitment to the population both inside and outside the sanctuary. Ideally, the protected population grows to a level at which population pressures force excess individuals out of the sanctuary. Special attention must be brought to small wetlands. Our investigations suggest that many E. orbicularis populations survive in particularly small wetlands (only a few hundred square metres), which are usually not considered in any conservation measures. The importance of such small wetlands has already been pointed out for other species by GIBBS (1993). Moreover, it is necessary to raise public awareness of the importance of wetlands to biodiversity conservation. Wherever and whenever marshes, sloughs, swamps, and similar habitats are threatened, conservationists must take a strong stand against unbridled development and misuse. Biologists must make conservationists, educators, community leaders, and politicians aware of the habitat needs of freshwater turtles and their aquatic associates. Even fish and game departments, which would seem to be logical allies, may need to be educated regarding the effects of angling on turtles. With regard to the public, arguments based on aesthetics and awareness that the turtles are part of the biodiversity, should be emphasized. Acknowledgements The authors thank J. SERVAN (National Museum of Natural History), R. QUESADA (Association Lo Parvi), M. CHEYLAN (EPHE Montpellier) for their advise and support. We thank the Conseil Général de l Isère and SIVAL for permitting our investigations. We also thank C. REYNAUD and F. MICOULOUD for the technical help. We are indebted to E. PATTEE for some English corrections. Many thanks to the students who assisted us during three years (Romain, Elise, Pauline, Ivan, Guillaume, Yann, Céline, and Benjamin). This work 92

was supported by the Rhône-Alpes Region, the DI- REN, the Agence de l Eau and the Conseil Général de l Isère. References BODIE, J. R.& SEMLITSCH, R. 2000. Spatial and temporal use of foodplain habitats by lentic and lotic species of aquatic turtles. Oecologia 122: 138 146. BUHLMANN, K.A.,MITCHELL, J.C.&ROLLINS, M. G. 1997. New approaches for the conservation of bog turtles, Clemmys muhlenbergii, in Virginia, pp. 359 363. In: VAN ABBEMA, J. (ed.) Proceedings: Conservation, Restoration, and Management of Tortoises and Turtles An international Conference, July 1993, New York Turtle and Tortoise Society, New York. BURY, R. B. 1979. Population ecology of freshwater turtles, pp. 571 602. In: HARLESS, M. & MOR- LOCK, H. (eds) Turtles Perspectives and Research, John Wiley & Sons, New York and Chichester. CADI, A. 2003. Ecologie de la Cistude d Europe (Emys orbicularis): aspects spatiaux et démographiques, application à la conservation. PhD Thesis, Université Lyon 1, Lyon, France, 310 pp. CAGLE, F. R. 1944. Home range, homing behavior, and migrations in turtles. Misc. Publ. Mus. Zool. 61: 1 34. CAGLE, F. R. 1946. The growth of the slider turtle, Pseudemys scripta elegans. Amer.Midl.Nat.36: 685 739. CONGDON, J. D., DUNHAM, A. E. & VAN LOBEN SELS, R. C. 1993. Delayed sexual maturity and demographics of Blanding s turtles (Emydoidea blandingii): implications for conservation and management of long-lived organisms. Conserv. Biol. 7: 826 833. CONGDON, J. D., DUNHAM, A. E. & VAN LOBEN SELS, R. C. 1994. Demographics of common snapping turtles (Chelydra serpentina): implications for conservation and management of long-lived organisms. Amer. Zool. 34: 397 408. DALL ANTONIA, L., LEBBORONI,M.,BENVENUTI,M.&CHELAZZI, G. 2001. Data loggers to monitor activity in wild freshwater turtles. Ethol. Ecol. Evol. 13: 81 88. DUGUY, R.& BARON, J.-P. 1998. La cistude d Europe, Emys orbicularis, dans les marais de Brouage (Char.-Mar.): cycle d activité, thermorégulation, déplacements, reproduction et croissance. Ann. Soc. Sci. Nat. Charente-Maritime 8: 781 803. ERNST, C. H. 1968. Homing ability in the spotted turtle, Clemmys guttata (Schneider). Herpetologica 24: 77 78. FARKAS, B. 2000. The European Pond turtle Emys orbicularis (L.) in Hungary, pp. 127-132. In: HÖDL, W. & RÖSSLER, M. (eds) Die Europäische Sumpfschildkröte, Stapfia 69. FRITZ, U. 1996. Zur innerartlichen Variabilität von Emys orbicularis (Linnaeus, 1758) 5b. Intraspezifische Hierarchie und Zoogeographie (Reptilia, Testudines: Emydidae). Zool. Abh. Mus. Tierkd. Dresden 49: 31 71. GIBBONS, J. W. (ed.) 1990. The Slider Turtle. Life History and Ecology of the Slider Turtle. Smithsonian Institution Press, Washington, D. C. and London, 396 pp. GIBBONS, J.W.,GREENE, J.L.&CONGDON, J.D. 1990. Temporal and spatial movement patterns of sliders and other turtles, pp. 201 215. In: GIB- BONS, J. W. (ed.) The Slider Turtle. Life History and Ecology of the Slider Turtle, Smithsonian Institution Press, Washington, D. C. and London. GIBBS, J. P. 1993. Importance of small wetlands for the persistence of local populations of wetland associated animals. Wetlands 13: 25 31. KOTENKO, T. I. 2000. The European pond turtle (Emys orbicularis) in the steppe zone of the Ukraine, pp. 87 106. In: HÖDL, W.& RÖSSLER, M. (eds) Die Europäische Sumpfschildkröte, Stapfia 69. LEBBORONI, M.& CHELAZZI, G. 1991. Activity patterns of Emys orbicularis L. (Chelonia Emydidae) in central Italy. Ethol. Ecol. Evol. 3: 257 268. LEBBORONI, M.& CHELAZZI, G. 1999. Habitat use, reproduction and conservation of Emys orbicularis in a central pond system in central Italy, pp. 169 173. In: BOOTHBY, J. (ed.) Ponds and ponds landscapes of Europe, Liverpool. LEBBORONI, M.& CHELAZZI, G. 2000. Waterward orientation and homing after experimental displacement in the European pond turtle, Emys orbicularis. Ethol. Ecol. Evol. 12: 83 88. MITRUS, S.& ZEMANEK, M. 2000. Distribution and biology of Emys orbicularis (L.) in Poland, pp. 107 118. In: HÖDL, W.& RÖSSLER, M.(eds) Die Europäische Sumpfschildkröte, Stapfia 69. MORALES-VERDEJA, A.& VOGT, C. 1997. Terrestrial movements in relation to aestivation and the annual reproductive cycle of Kinosternon leucostomum. Copeia1997: 123 130. NAULLEAU, G. 1991. Adaptations écologiques d une population de cistudes (Emys orbicularis L.) (Reptilia, Chelonii) aux grandes variations de niveau d eau et à l assèchement naturel du milieu aquatique fréquenté. Bull. Soc. Herpétol. Fr. 58: 11 19. PARDE, J.-M.,HURSTEL, S.&LEFEVRE, A.-C. 2000. Etude éco-éthologique de la Cistude d Europe dans le Bas-Armagnac (Gers, France), en vue de sa conservation, pp. 73 79. In: Proceedings of the 2 nd International Symposium on Emys orbicularis, Chelonii 2. ROLLINAT, R. 1934. La vie des reptiles de la France centrale. Delagrave, Paris, 337 pp. ROVERO, F.& CHELAZZI, G. 1996. Nesting migrations in a population of the European pond turtle Emys orbicularis (L) (Chelonia Emydidae) from central Italy. Ethol. Ecol. Evol. 8: 297 304. 93

SERVAN, J. 1986. Utilisation d un nouveau piège pour l étude des populations de Cistude d Europe Emys orbicularis. Rev.Ecol.TerreVie41: 111 117. SERVAN, J. 1988. La cistude d Europe, Emys orbicularis, dans les étangs de Brenne, France. Mésogée 48: 91 95. VOGT, R. C. 1980. Natural History of the map turtle Graptemys pseudogeographica and G. ouachitensis in Wisconsin. Tulane Stud. Zool. Bot. 22: 17 48. YEOMANS, S. R. 1995. Water-finding in adult turtles: random search or oriented behaviour? Animal Behav. 49: 977 987. 94