Mitochondrial phylogeography of the European pond turtle, Emys orbicularis (Linnaeus 1758)

The phylogeny and phylogeography of Emys orbicularis was inferred from mitochondrial nucleotide sequences of the cytochrome b gene analysed by DNA sequencing and RNA heteroduplex analysis. Within the family Emydidae the monotypic genus Emys is affiliated with the nearctic taxa Emydoidea blandingii and Clemmys marmorata. The analysis of 423 individuals of E. orbicularis, originating throughout its distribution range, revealed a remarkable intraspecific differentiation in 20 different haplotypes with distinct geographical ranges. Maximum parsimony analysis produced a star-like phylogeny with seven main lineages which may reflect separations in the late Pliocene. The haplotype distribution examined by partial Mantel tests and analysis of molecular variance revealed a substantial effect of glacial periods. This historical perspective suggests the existence of multiple glacial refugia and considerable Holocene range expansion which was modulated by climatic traits. Further support is gained for the occurrence of long-term parapatry in glacial refugia.     

Factors affecting the predation of otter (Lutra lutra) on European pond turtle (Emys orbicularis)

In this case study, the ecological background of an unusual hunting behaviour was investigated, when otters Lutra lutra preyed upon European pond turtles Emys orbicularis in a Hungarian fish pond system during an 18-month period. Predation on turtle was found only during cold periods (established by spraint analysis and also by the collection of 182 turtle carcasses in 2003). The relationship was not close between fish availability and turtle consumption ( r _P =−0.325, P =0.19). The crude protein content of the turtle head and leg was higher than that of fish, frog and turtle body, whereas the energy content of the samples was similar. The mean body weight of the killed turtles (460 g) fell within the range of the optimal prey size of the otter. Turtles were used as cache foods by otters during extreme environmental conditions (as in the long winter), but occurred only rarely as buffer foods during moderate winter. In fish ponds, the conservation of the coexistent otter and turtle depends on pond management. The maintenance of a higher fish availability in ponds during winter makes it possible to avoid the need to acquire a proper hunting technique on turtle, indicated by the scarcity of primary fish food.     

The morphometrics and colouration of the European pond turtle Emys orbicularis in Lubuskie province (West Poland)

The European pond turtle Emys orbicularis, is an endangered species in Poland. The region of the Ilanka River, in the western part of the country (Lubuskie province), is the most densely inhabited area by the species. Several populous sites are dispersed over the whole area of the province. Over the past 10 years, 279 turtles were captured at 11 sites. In 218 individuals, those with a straight carapace length (SCL) between 2.10–12.10 cm, sex was not determined; the remaining 61 with SCL 13.33–19.85 cm were sexed. Females had bigger bodies and were heavier than males. The SCL of females was 17.10 ± 1.7 cm (average ± SD, n = 33), their body mass (BM) was 790.6 ± 228.7 g (n = 27), and in the case of males SCL was 15.44 ± 1.5 cm and BM was 554.2 ± 138.8 g (n = 28). SCL of the smallest egg laying female was 15.30 cm, and SCL of the smallest mating male was 13.33 cm. The colouration of the turtles which undergoes change with age can be varied.     

Blood parasite diversity (Apicomplexa: Haemogregarinidae) within the western populations of the European pond turtle Emys orbicularis

Systematic Parasitology - Molecular tools have revolutionized assessments of blood parasites in freshwater turtles. In the Iberian Peninsula and North Africa, two native species of terrapins occur,...     

Reproductive strategies and body shape in the European pond turtle (Emys orbicularis) from contrasting habitats in Italy

Comparisons within and among populations offer important insights into variation in life-history traits and possible adaptive patterns to environmental conditions. We present the results of observed differences in body size, body shape and patterns of reproduction in four separate populations of the European pond turtle Emys orbicularis in central and southern Italy – coastal ( n =3) and mountainous ( n =1) sites and pond ( n =2) and canal ( n= 2) habitats – to determine whether phenotypic plasticity affects reproductive output. Although we did not find any significant latitudinal variation in body size, we observed significant differences in body shape between canal (rounded body shape) and pond (elongated body shape) systems and smaller size with rounded shape in the mountainous population. Reproductive output is similar among populations (median=5 eggs per clutch), whereas reproductive investment (relative clutch mass to maternal body mass) is higher in the mountain population (one clutch per year) than in coastal populations (two clutches per year), suggesting differential trade-offs between geographic locality, elevation and habitat type. Turtle shell shape and geographic location together affect reproductive output in E. orbicularis in Italy.     

Eimeria species from the European pond turtle, Emys orbicularis (Reptilia: Testudines), in Galicia (NW Spain), with description of two new species

Parasitological examination of feces from 44 Emys orbicularis from Galicia (NW Spain) revealed the presence of 2 new eimerian species, Eimeria gallaeciaensis sp. n. and E. emydis sp. n., as well as E. mitraria (Laveran and Mesnil, 1902) Doflein, 1909. Oocysts of E. gallaeciaensis n. sp. were found in 20 of 44 (45.4%) turtles and are subspherical to lightly ovoid-ellipsoid, 19.3 x 16.0 (17-22 x 15-18) microm, shape index 1.2 (1.1-1.3), with a smooth, single-layered wall. Micropyle and polar granule are absent, but an oocyst residuum is present. Sporocysts are ellipsoid, 9.7 x 5.1 (9-10 x 5-6) microm, shape index 1.9 (1.7-2.0), each with a sporocyst residuum and a conical Stieda body usually bearing 1-4 short and thin projections. Oocysts of E. emydis n. sp. were found in the feces of 5 of 44 (11.4%) turtles and are ovoid, rarely pear-shaped, 22.6 x 17.0 (20-25 x 15.5-18) microm, shape index 1.3 (1.2-1.5), with a smooth, single-layered wall with a slight thinning at the pointed end. Micropyle and polar granule are absent, and an oocyst residuum is present. Sporocysts are ellipsoid, 11.4 x 6.0 (9-13 x 5-7) microm, shape index 1.9 (1.6-2.2), each with sporocyst residuum and a prominent Stieda body bearing 3-5 club-shaped projections. In addition to the new species described, this is the first report of E. mitraria parasitizing E. orbicularis.     

Unexpected early extinction of the European pond turtle (Emys orbicularis) in Sweden and climatic impact on its Holocene range

Using ancient DNA sequences of subfossil European pond turtles ( Emys orbicularis ) from Britain, Central and North Europe and accelerator mass spectrometry radiocarbon dating for turtle remains from most Swedish sites, we provide evidence for a Holocene range expansion of the pond turtle from the southeastern Balkans into Britain, Central Europe and Scandinavia, according to the 'grasshopper pattern' of Hewitt. Northeastern Europe and adjacent Asia were colonized from another refuge located further east. With increasing annual mean temperatures, pond turtles reached southern Sweden approximately 9800 years ago. Until approximately 5500 years ago, rising temperatures facilitated a further range expansion up to Östergötland, Sweden (approximately 58°30'N). However, around 5500 years ago pond turtle records suddenly terminate in Sweden, some 1500 years before the Holocene thermal maximum ended in Scandinavia and distinctly earlier than previously thought. This extinction coincides with a temporary cooling oscillation during the Holocene thermal maximum and is likely related to lower summer temperatures deteriorating reproductive success. Although climatic conditions improved later again, recolonization of Sweden from southern source populations was prevented by the Holocene submergence of the previous land connection via the Danish Straits that occurred approximately 8500 years ago.     

Oxygen consumption as related to the development of the extraembryonic membranes and cardiovascular system in the European pond turtle (Emys orbicularis) embryogenesis

The rate of oxygen consumption (V(O2)), embryo mass, distribution and mass of the chorioallantoic membrane (CAM), heart rate (HR), heart mass, and amnion rhythmic contractions (ARC) were studied in eggs of the European pond turtle (Emys orbicularis) incubated at 28 degrees C for 62.5+/-0.3 days. The V(O2) rapidly increased beginning from incubation day 19 (D19) to a maximum on D50 and then decreased until pipping. The rapid V(O2) rise was correlated with an increase in the CAM surface and mass, heart mass, and ARC amplitude, whereas the functional parameters such as HR and ARC frequency remained unchanged. The drop in V(O2) before pipping was accompanied by a decrease in HR, while the heart and CAM masses were almost constant. In the cases of short-term temperature deviations of +/-3 degrees C from 28 degrees C, changes in (O2) were significant until D50 and nonsignificant after that, the changes in ARC frequency and HR being significant at all stages studied. Thus, the developmental V(O2) changes were contributed mainly by the slow morphogenetic processes during D19-D50, whereas changes in functional parameters began to play a role at later stages. The response to temperature fluctuations was mediated by a rapid change in functional parameters at all these stages.     

Creation of a nature reserve, its effects on hunting management and waterfowl distribution in the Camargue (southern France)

The eastern portion of the Camargue in southern France is divided into two parts: a natural wetland area of 2800 ha and an agricultural area of 5045 ha. In 1984 and 1989, a new protected area (1000 ha) was created on two contiguous former hunting estates. Analysis of aerial photographs (1968–1998) in conjunction with a field survey revealed, from 1984 to 1998, an increase of management for waterfowl hunting in natural wetlands located on the periphery of the new reserve, and a similar increase in the agricultural area amongst residual wetlands and former rice fields. Based on monthly aerial censuses, the size of the waterfowl population in the winter increased in this part of the delta by a factor of 3.8 following the creation of the reserve. Our results suggest that the creation of a reserve on former hunting estates resulted in greater attractiveness for ducks but also in the development of commercial hunting activity around the edge. This development increased fragmentation and uniformity of natural areas, including the loss of the unique Cladium mariscus habitat in the Camargue and resulted in the spatial expansion of waterfowl hunting areas in agricultural areas. It is associated with an increase in financial profit from waterfowl hunting. Our study highlights unexpected costs for nature conservation associated with the creation of a reserve. It illustrates the need for new models of wetland conservation where protection goals are not restricted to reserves, but also integrate conservation and economic development outside the protected areas.     

Survival and population growth of a long-lived threatened snake species, Drymarchon couperi (Eastern Indigo Snake)

Demographic data provide a basis for understanding the life history and ecology of species, factors which are vital for informing conservation efforts; however, little is known regarding the population ecology of most snake species, including the threatened Eastern Indigo Snake (Drymarchon couperi). We used 11 years (1999–2009) of capture-mark-recapture (CMR) and 2.5 years (2003–2005) of radiotelemetry data from southeastern Georgia, USA, in a CMR modeling framework to estimate apparent survival, capture and transition probabilities, and evaluate factors influencing these parameters. The model-averaged estimate of overall apparent annual survival probability was 0.700 (±0.030 SE) and is comparable to that obtained from known fate analysis (radiotelemetry) at the same site. Body size positively influenced survival, regardless of sex. Capture probability differed seasonally by sex, suggesting lower capture probability for females in fall and males in winter. There was no evidence for effect of precipitation or site-specific differences in survival. Model averaged estimate of annual adult survival estimated using multistate CMR models was 0.738 ± 0.030 and 0.515 ± 0.189 for subadults. We estimated population growth rate (λ) and elasticity (proportional sensitivity) of λ to vital rates using a stage-structured matrix population model. Population growth rate ranged from 0.96 to 1.03 depending on the value of the probability of transitioning from subadult to adult stage. The λ was proportionally most sensitive to changes in adult survival rate, followed by subadult survival. Our results suggest that protecting adult snakes and their habitats would result in the highest likelihood of long-term population stability and growth.     

A new cryptic species of pond turtle from southern Italy, the hottest spot in the range of the genus Emys (Reptilia, Testudines, Emydidae)

Geographic variation in the mtDNA haplotypes (cytochrome b gene) of 127 European pond turtles from Italy was investigated. Thirty‐eight of the Italian samples were also studied by nuclear fingerprinting (ISSR PCR) and compared with samples from other parts of the range representing all nine currently known mtDNA lineages of Emys orbicularis. Our genetic findings were compared against morphological data sets (measurements, colour pattern) for 109 adult turtles from southern Italy. Italy is displaying on a small geographical scale the most complicated variation known over the entire distributional area of Emys (North Africa over Europe and Asia Minor to the Caspian and Aral Seas). The Tyrrhenic coast of the Apennine Peninsula, the Mt. Pollino area and Basilicata are inhabited by Emys orbicularis galloitalica, a subspecies harbouring a distinct mtDNA lineage. The same lineage is also found in Sardinia. Along the Adriatic coast of Italy and on the Salentine Peninsula (Apulia, southern Italy), another morphologically distinctive subspecies (Emys orbicularis hellenica) occurs, which also bears a different mtDNA lineage. A higher diversity of mtDNA haplotypes in the south of the Apennine Peninsula suggests that the glacial refugia of E. o. galloitalica and E. o. hellenica were located here. A further refuge of E. o. hellenica probably existed in the southern Balkans. The west coasts of the Balkans and Corfu have probably been colonized from Italy and not from the geographically closer southern Balkanic refuge. In Sicily, a third mtDNA lineage is distributed, which is sister to all other known lineages of Emys. Morphologically, Sicilian pond turtles resemble E. o. galloitalica. However, nuclear fingerprinting revealed a clear distinctiveness of the Sicilian taxon, whereas no significant divergence was detected between representatives of the other eight mtDNA lineages of Emys. Furthermore, nuclear fingerprinting provided no evidence for current or past gene flow between the Sicilian taxon and the mainland subspecies of E. orbicularis. Therefore, Sicilian pond turtles are described here as a species new to science. Some populations in Calabria and on the Salentine Peninsula comprise individuals of different mtDNA lineages. We interpret this as a natural contact. However, we cannot exclude that these syntopic occurrences are the result of human activity. For example, in other parts of Italy, the natural distribution pattern of Emys is obscured by allochthonous turtles. This could also be true for southern Italy. The discovery of the complex taxonomic differentiation in southern Italy requires reconsidering conservation strategies.     

Sexual dimorphism of the European Pond Turtle,Emys orbicularis (Linnaeus, 1758), in Anzali Lagoon,Iran (Reptilia: Emydidae)

The morphometric characteristics of the European Pond Turtle, Emys orbicularis, were studied at Anzali lagoon on the southern coast of the Caspian Sea. Males were on average (N=249) with 272.0?g significantly lighter than females with 447.0?g, and average carapace length was significantly smaller (123.0?mm in males, 139.0 in females). Females exceeded males also in all other studied characters (carapace width, plastron length, plastron width, and scute height). The sex ratio of male to female was 1 to 1.03, and the comparison of total tail length and cloaca-tail tip length revealed a difference between the position of the cloaca in both sexes, a character useful for sex determination in this species.     

Range-wide molecular analysis of the western pond turtle (Emys marmorata): cryptic variation, isolation by distance, and their conservation implications

We analysed phylogeography and population genetic variation across the range of the western pond turtle (Emys marmorata) using rapidly evolving mitochondrial and nuclear DNA sequence data. Nuclear DNA sequences from two unlinked introns displayed extremely low levels of variation, but phylogenetic analyses based on mtDNA recovered four well-supported and geographically coherent clades. These included a large Northern clade composed of populations from Washington south to San Luis Obispo County, California, west of the Coast Ranges; a San Joaquin Valley clade from the southern Great Central Valley; a geographically restricted Santa Barbara clade from a limited region in Santa Barbara and Ventura counties; and a Southern clade that occurs south of the Tehachapi Mountains and west of the Transverse Range south to Baja California, Mexico. An analysis of molecular variance (amova) based on regional hydrographic units revealed that populations from the Sacramento Valley north to Washington were virtually invariant, with no evidence of population substructure among northern river drainage basins. In other areas, E. marmorata contains considerable unrecognized variation, particularly in central and southern California and in northern Baja California, Mexico. Our northern clade is congruent with the distribution of the subspecies Emys marmorata marmorata (Washington-central California). However, no clade is congruent with the distribution of the southern subspecies Emys marmorata pallida from central California-Baja. Thus, recognition of the current subspecies split is not warranted, based on the available genetic evidence. Our amova and phylogenetic results, in conjunction with a growing comparative database for other codistributed aquatic taxa, confirm the occurrence of genetic breaks across the Tehachapi Mountains and Transverse Range bounding the southern end of the Great Central Valley, and point to southern California as a rich source of cryptic genetic variation.     

Sand smelt (Atherina boyeri) migration within the water system of the Camargue,southern France

In the coastal lagoons of Southern France, sand smelt Atherina boyeri, is known as a sedentary species. However part of the sand smelt population living in the brackish water Vaccarès lagoon in the Camargue annually migrates to fresh waters. The movements of sand smelts within the watersystem of the Camargue were studied from 1986 to 1990. Fish traps and fyke nets were set and catches were standardised to Catch Per Unit Effort (CPUE). A Stepwise Multiple Correlation analysis was carried out to link fish abundance with various environmental factors. Between September and November, sand smelts living in the Vaccarès start to colonize fresh waters (drainage canals and then temporary marshes), until March. Spawning occurs from April to June, both in the shallow branches of the canal and in the marshes. From June onwards adults and young-of-the year leave the fresh waters and return to the Vaccarès lagoon where they remain until the next migration. This autumnal migration to freshwater habitats involves mainly fish less than 3 years old, the oldest individuals remaining all year in the Vaccarès. Water level and photoperiod contribute to 20.7% of the variation of CPUE within the drainage canal, while date, water temperature, and rainfall combined, only account for 2.5% of CPUE variations. Date and photoperiod contribute significantly to explaining the patterns of fish migrations between the canal and the marshes. The density of mature sand smelt in the marshes before spawning, varies between 4 and 4346 fish ha^–1. Fry mortality (against number of eggs spawned) over the first two months of life was assessed to vary between 97.5% and 99.9%. Physiological factors such as osmoregulation linked to water temperature are possibly the ultimate factors explaining these unusual annual migrations of sand smelt in the Camargue.     

Comparative population structure of three snook species (Teleostei: Centropomidae) from the eastern central Pacific

Three snook species, Centropomus viridis, Centropomus medius, and Centropomus robalito, from the eastern central Pacific, representing three of the four proposed phyletic lineages in the genus, were analyzed for genetic variability by means of allozyme and RAPD to evaluate the divergence between populations at different levels of dispersal ability and to evaluate the importance of barriers to dispersal in the population subdivision and genetic diversity. Levels of genetic diversity among species estimated by allozymes were similar and consistent with the observed levels of differentiation in marine fish species. Mean heterozygosity ranged from 0.089 for C. viridis to 0.10 for C. robalito. Genetic diversity for the snook species studied was slightly higher than the mean estimation reported in allozymes for 106 marine fish (0.055) and for anadromous fish species (0.043 to 0.057). Multilocus allele frequency homogeneity tests and population-subdivision estimates for both allozyme and RAPD markers revealed the existence of population structure in C. viridis and C. medius, in coincidence with geographic separation of samples, whereas no divergence was detected in C. robalito. This finding may be attributed to the greater population size of C. robalito, which originated by a recent population range expansion, and hence the potential for dispersal is mediated by larval drift. Fluctuations in population size and population range expansion are used to explain discrepancies between levels of genetic diversity and population structure in the studied species. Supplementary material to this paper is available in electronic format at     

Competition between an introduced and an indigenous species: the case of Paspalum paspalodes (Michx) Schribner and Aeluropus littoralis (Gouan) in the Camargue (southern France)

Paspalum paspalodes, an introduced grass species, and Aeluropus littoralis, an indigenous species, develop abundantly in seasonally-flooded marshes in the Camargue (Rhône Delta, France). Although they occur together in many multispecies communities, neither species occurs when the other is dominat. The cultivation of cuttings of P. paspalodes and A. littoralis in a replacement series in a combination of five proportions (0/100, 25/75, 50/50, 75/25 and 100/0) and four salinities (0,2 4, and 6 g Cl^- · 1^-1) gave contrasting results for the two species: (1) strong asymmetrical competition in favour of P. paspalodes at 0 g Cl^- · 1^-1, (2) no significant effect of salinity on the mean above-ground and underground yields per plant for A. littoralis over the range tested, (3) a major decrease in the mean above-ground and belowground yields per plant for P. paspalodes with increasing salinity, (4) a reversal of the competitive balance between the species with increasing salinity. The cultivation of cuttings at high temperatures in a greenhouse in a combination of the same five proportions at two salinities (0 and 4 g Cl^- · 1^-1) refuted the hypothesis that the introduced species is better adapted to summer temperatures. Because it is not salt-tolerant, P. paspalodes cannot be considered as a potentially invasive species in the Camargue. Its abundance depends on newly created and artificially maintained habitats.     

Response of Juniperus phoenicea on sandy dunes in the Camargue (France) to water and saline constraint in summer

The ‘Bois des Rièges’ woodland occurs on the relic littoral dunes in the National Reserve of the Camargue. Although surrounded by brackish ponds and saline lands with very salt groundwater close to the surface, the dunes are covered with non-halophytic vegetation of herbaceous shrubs and trees, including the dominant shrub Juniperus phoenicea. This is due to the presence of a freshwater lens beneath the dunes supplied by rains, and floating in hydrodynamic equilibrium upon the saline aquifer. The importance and duration of the freshwater stock depends on the precipitation-evapotranspiration balance as well as on the size of the dune. From the end of the spring to the autumn rain period this freshwater stock is considerably reduced, while the capillary potential in the zone of aeration of soil and the osmotic potential of the soil solution, influenced by capillary rise of the brackish groundwater, decrease. In summer the vegetation is thus subjected to severe drought caused by lack of water or salt excess, to which it must adjust its biological activity. The water relationships in the soil-plant system have been studied along a transect between the top and the borders of a dune surrounded by saline lands. Using simultaneous water potential measurements of the sunny and shady sides of Juniperus trees daily and seasonal transpiration regulations were studied. The preliminary results indicate that trees on the border of the dune as well as on tops are absorbing water from the same freshwater lens in the middle of the dune.     

Feeding ecology of the Sicilian pond turtle <Emphasis Type="Italic">Emys trinacris</Emphasis> (Testudines,Emydidae) influenced by seasons and invasive aliens species

Feeding ecology of a species is the result of its evolutionary history, biology, physiology and local constraints, such as prey availability, intra- and inter-specific interactions and environmental characteristics. In this study we investigated the still unknown diet of the Sicilian pond turtle, with special emphasis to the relationships with recently introduced alien species in the “Lake Preola and Gorghi Tondi” Nature Reserve (Sicily, Italy). A total of 83 faecal samples were collected in three different periods. Emys trinacris seems an opportunistic and generalist species. The main prey taxa were aquatic invertebrates, including the invasive Procambarus clarkii, while non-aquatic preys are found sporadically. Plant matter, mainly leaves and roots of aquatic forms, was also found in high frequency with a high occurrence of fruits and seeds in spring. We did not find a significant difference in diet composition within sex and age, while an evident divergence was found between periods and sites. In particular, we noticed a decrease in prey abundance and in food-niche breadth from pre-reproductive period to post-reproductive period. Moreover a very clear difference was found between a site with allochthonous fishes and a site fish-free, with a more abundant and wide diet spectrum in the last one, as a result of the increased availability of prey. We highlighted the importance to take any possible actions to avoid the spread of fishes in other basins and to study the indirect impact of Procambarus clarkii, as possible vector of harmful trace element.