Herpetological Conservation and Biology 15(1):41–48. Submitted: 27 March 2019; Accepted: 27 November 2019; Published: 30 April 2020. DEMOGRAPHICS AND SURVIVORSHIP IN THE EUROPEAN POND TURTLE (EMYS ORBICULARIS): A 31–YEAR STUDY DANIEL ESCORIZA1,2,7, MARC FRANCH3,4, SANTIAGO RAMOS5, PAU SUNYER-SALA6, AND DANI BOIX1 1GRECO, Institute of Aquatic Ecology, University of Girona, Campus Montilivi, Girona, Spain 2 Institut Català de la Salut, Barcelona, Spain 3CICGE-Centro de Investigaçâo em Ciências Geo-Espaciais, Universidade do Porto, Vila Nova de Gaia, Portugal 4PECAT-Departament de Ciències Ambientals, Universitat de Girona, Campus Montillivi, Girona, Spain 5Parc Natural Montgrí, les Illes Medes i Baix Ter, L’Estartit, Spain 6Fundació Emys, Riudarenes, Spain 7Corresponding author, e-mail address: [email protected] Abstract.—Two populations of the European Pond Turtle (Emys orbicularis) separated by a distance of 4 km were studied in the tributaries of the Tordera River in northeast Spain. One population was observed from 1987–2018 (Zone 1) and the other from 2008–2018 (Zone 2). We captured turtles using baited funnel traps and we marked turtles individually. We used capture-recapture and radio-tracking techniques to determine population structure and dispersal movements. The sex ratio favored females in Zone 1 (males/males + females = 0.25) and males in Zone 2 (males/males + females = 0.57). The sex ratio remained stable for 21 y in Zone 1. Using a capture-recapture model, we found a high probability of turtle survival in Zone 1 and 2 (females 0.91–0.92; males 0.84–0.86). The population growth is fundamentally supported by a low adult mortality in both zones. We estimated the adult population size as 148 in Zone 1 and 155 in Zone 2. In Zone 1, we recaptured one female 31 y after being first marked and one male and another four females after 30 y. The recaptured turtles showed an important fidelity to the capture sites, and only 19% of the females and 30% of the males moved between successive recaptures. The mean displacement distances were 0.09 km for females and 0.15 km for males. Key Words.—capture-recapture; Emydidae; long-term study; population size; radio-tracking INTRODUCTION study periods between 20 and 38 y (Wilbur 1975; Stickel 1978; Williams and Parker 1987). These long-term The European Pond Turtle (Emys orbicularis) is studies allow the evaluation of temporal fluctuations one of three species of native freshwater turtles found in turtle populations and have important implications in Europe and occupies a wide geographical region for conservation, such as detecting factors that could (Speybroeck et al. 2016). Despite this, in Western negatively influence survival (Stickel 1978; Williams Europe, a large part of the population is fragmented, has and Parker 1987). a low number of individuals, or has become extinct in We analyzed a temporal series of data obtained some countries (Hofer 2001; Keller and Andreu 2002; over 31–y in the upper Tordera River system. We used Vamberger and Fritz 2018). This species shows high capture-recapture and radio-tracking methods to study longevity, estimated to reach or exceed 50 y (Gibbons population structure, dispersal patterns, and survivorship. 1987; Schneeweiss 2004); however, previous studies This population is considered the most important for the carried out in Europe encompassed comparatively species in the northeast of Spain given the population size short periods of time: e.g., Cordero-Rivera and Ayres and the expanse it occupies (Mascort and Budó 2017); (2004) in Galicia, northwest Spain (6 y); Mitrus and however, it could be threatened due to the loss of habitat Zemanek (2004) in central Poland (13 y); Schneeweiss quality and the increasing presence of invasive species (2004) in northeast Germany (8 y); Mazzotti (1995) in in the fluvial systems of the region (Escoriza 2018). We northeast Italy (3 y); and Vamberger and Kos (2011) measured several population parameters collected from and Vamberger et al. (2017) in central Slovenia (2 1987–2018 and placed special emphasis on survival y). Although studies of this type could be suitable to rates and population size trends, which are difficult to evaluate the population structure at a single time point, discern from short-term studies. These analyses allowed they are clearly insufficient to evaluate demographic us to estimate demographics and patterns of space use to trends in long-lived species. Long-term studies have define better management and conservation strategies for been carried out with other turtle species, involving this regionally threatened species. Copyright © 2020. Daniel Escoriza 41 All Rights Reserved. Escoriza et al.—Demographics in Emys orbicularis. FIGURE 1. Map of the study area in Spain, showing the main hydrographic network (blue lines), sampling points (red circles, size is proportional to the number of specimens found) and dispersal movements (black bidirectional arrows, numbers indicate the number of dispersion events greater than five). The green background represents forest cover per km2 according to Tuanmu and Jetz (2014). The abbreviations Z1 = Zone 1 and Z2 = Zone 2. MATERIALS AND METHODS however, sampling could not be carried out continuously throughout this period for reasons unrelated to the design Study area.—The study area included the Riera de of the study. In 1995, 2001, and 2004, we did not sample Santa Coloma and its tributaries: Riera de Santa Maria, Zone 1, and in 2010, 2013, and 2014, we did not sample Riera de l’Esparra, and Sèquia de Sils. This network of Zone 2. We performed surveys twice a year in spring intermittent streams flows into the Tordera River (Riba (April-June) and early autumn (October), coinciding et al. 1980). The climate of the basin is Mediterranean with the periods of maximum activity of E. orbicularis (Csa; Köppen-Geiger classification), with an average (Ramos et al. 2009). We marked turtles using unique annual temperature of 15.5º C and average accumulated combinations of holes drilled in the marginal scutes rainfall of 741 mm y–1. The landscape consists of of the carapace (Plummer 1979). Once the pattern forest patches (mean cover = 39.7% km2; Tuanmu and was established, we determined the sex of a turtle and Jetz 2014) alternating with fields and small villages. measured total carapace length. We determined sex of In the Girona area, E. orbicularis occurs in small and adult individuals based on external dimorphic traits, isolated populations, with the population of the Riera such as plastron morphology, color of the irises and de Santa Coloma completely isolated (Mascort and the head, relative size of the tail, and the presence of Budó 2017). a precloaca (Zuffi and Gariboldi 1995), although we In the study area, E. orbicularis occurs in two disjunct did not determine sex of turtles from 1987–1997. We populations: one occupies a system of permanent and classified most individuals that did not show secondary temporary ponds structured around several seasonal sexual traits and with an axial carapace length of < 103 streams (Riera de Santa Coloma, Barranc de Vilarràs, mm as juveniles (Mazzotti 1995; Ramos et al. 2009). and Riera de l’Esparra; hereafter Zone 1) and the other After handling, all the captured turtles were released at in the Riera de Santa Maria and Sèquia de Sils (Zone 2; the capture spot. Fig. 1). These two zones are geographically separated Additionally, we assessed terrestrial movement by by 4 km (Fig. 1); therefore, they were studied as radio-tracking the specimens in Zone 1. We attached independent units because this range of distance is only radio tags (model TW3 10/28 and TW4 Ag 391/357; covered rarely by this turtle (Gariboldi and Zuffi 1994; Biotrack Ltd., Wareham, UK) to the carapace of 11 Mitrus and Zemanek 2004). individuals (two juveniles, seven females, and two males). The weight of the radio tags represented 2‒4% Sampling procedures.—We captured turtles of the weight of the individuals. We determined the using nets and floating baited net traps (110 × 50 cm; location of a turtle by triangulation, and we followed McDiarmid et al. 2012). We placed the traps in all individuals for 12 mo (autumn 1999 to autumn 2000), available types of aquatic habitats including permanent taking one location per month. (natural and artificial) ponds, temporary ponds, and seasonal streams. Depending on the size of the aquatic Data analyses.—We evaluated demographic habitat, we placed one to five traps separated by 10 m at parameters based on capture-recapture methods each station. We conducted surveys between 1987 and (Mazzotti 1995) and dispersal patterns based on the 2018 in Zone 1 and between 2008 and 2018 in Zone 2; distances covered between successive recaptures 42 Herpetological Conservation and Biology (Gariboldi and Zuffi 1994). Demographic parameters TABLE 1. Survey and demographic statistics (mean and standard included indexes directly calculated from the recapture deviation) of the European Pond Turtle (Emys orbicularis) in Riera data (sex ratio and relative frequency of population de Santa Coloma (Girona, north-eastern Spain). Variables are Total unique specimens = total of specimens marked during the sampling groups: females, males, and juveniles) and other data period and Specimens year–1 = mean number of specimens captured derived from statistical models. We calculated sex ratio per year. Interzone dispersal is the percentage of unique specimens as the relative male proportion (male/male + females), that migrated from Zone 1 to Zone 2 (first box) and from Zone 2 following similar studies in Spain (Keller 1997; to Zone 1 (second box). Sex ratio year–1 is the mean sex ratio Cordero-Rivera and Ayres 2004). To assess whether the (males/males+females) per year. Group year–1 is the mean relative frequency (group/total captures) per year. The total of specimens sex proportion differed from parity, we used a Single marked of the Mediterranean Stripe-necked Terrapin (Mauremys Proportion test (Julious 2005).