Pond Turtle Research Articles

Unintended Entrainment of Western Pond Turtle (Actinemys marmorata) during Algae Control on a Newly Restored Wetland

Unintended Entrainment of Western Pond Turtle (<i>Actinemys marmorata</i>) during Algae Control on a Newly Restored Wetland

Pharmacokinetics of Nebulized Terbinafine in Plasma and Keratin of Northwestern Pond Turtles (Actinemys marmorata) Associated with Emydomycosis

The Northwestern pond turtle ( Actinemys marmorata ) is native to Washington State, USA and has developed a grossly evident form of shell disease affecting a large percentage of the free-ranging population in this state. Emydomyces testavorans is a novel fungus in the order Onygenales that is the presumed causative agent for shell disease in the Northwestern pond turtle. Terbinafine hydrochloride is a lipophilic allylamine broad spectrum antifungal that penetrates keratin and concentrates in the stratum corneum. This study evaluated the drug concentration in the plasma and keratin of 18 Northwestern pond turtles after nebulization with 18 mg terbinafine solution (2 mg/ml) once a day for 28 days. Blood and keratin samples were collected serially during the course of treatment, and for 14 days following the last dose. Plasma and keratin were analyzed by high-performance liquid chromatography. No significant concentrations of terbinafine were found in the plasma of the turtles. Terbinafine in turtle keratin peaked after 16 days of treatment and maintained therapeutic concentrations for 14 days post treatment. Turtle shell lesions also showed signs of clinical improvement post-therapy. Nebulization of terbinafine is recommended for the treatment of shell disease secondary to Emydomyces testavorans , however pulse antifungal therapy is likely needed to prevent disease from reoccurring.

On the Brink of Extinction: Results of a 20-Year Quest for Eiselt's Pond Turtle (Emys orbicularis eiselti) in Southeastern Turkey

Eiselt's pond turtle (Emys orbicularis eiselti) was described in 1998, based on only 4 museum specimens collected in the 1960s and 1970s. Its distribution range has been massively reduced by large-scale drainage measures and only little suitable habitat remains near the Turkish–Syrian border. During 20-yr-long fieldwork we could locate only 18 individuals of this subspecies. We estimate the number of surviving Eiselt's pond turtles to be less than 100 mature individuals in the wild. The distribution range (area of occupancy) in the Amik Maraş Rift Valley shrank from originally 11,612 km2 to only 206 km2 at present (approx. 2%), qualifying E. o. eiselti as a Critically Endangered taxon. Without immediate conservation measures and the strict protection of the remaining habitat, the subspecies will soon be extinct.

Geometric morphometrics and anatomical network analyses reveal ecospace partitioning among geoemydid turtles from the Uinta Formation, Utah.

We present new fossil records of the geoemydid turtle Bridgeremys pusilla from the Uinta Formation of Utah. Turtles are abundant throughout the unit, and known taxa are similar to those from the older strata in the Upper Green River Basin in Wyoming from the Bridger and Washakie Formations. B. pusilla is known from Bridgerian deposits but was not previously known from after the Turtle Bluff Member of the Bridger Formation. The taxon was coveal with two species of the geoemydid Echmatemys (E. callopyge and E. wyomingensis), a common genus of extinct pond turtles known primarily from lacustrine and fluvial deposits in western North America, including the Uinta Basin. In addition to previously documented morphological differences, our geometric morphometric analyses revealed significant differences in epiplastral morphology between B. pusilla and the two coeval Echmatemys species. Bridgeremys pusilla shared several morphological characters with Testudinidae. However, our anatomical network analysis suggests that the carapace of B. pusilla distributed stress forces in a manner more similar to emydids (basal and derived) than to derived testudinoids (Testudinidae and Emydidae), including Echmatemys species. This finding changes our understanding of the ecology of the species and sheds light onto how geoemydid turtles of the Uinta Formation may have partitioned the available ecospace. These new Uintan records extend the geographic range of B. pusilla into the Uinta Basin and stratigraphically through the top of the Uinta Formation, extending the temporal range of the taxon by more than 4 million years through the Uintan North American Land Mammal Age to the base of the Duchesne River Formation.

Turtle Shell Disease Fungus (Emydomyces testavorans): First Documented Occurrence in California and Prevalence in Free-Living Turtles

Pond Turtle Shell Disease is an emerging infectious disease associated with the fungus Emydomyces testavorans (Emte). Here, we report the first documented case of Emte in free-ranging Californian turtles. We assayed Emte in nine Western Pond Turtles (Emys = Actinemys marmorata; WPT) and three non-native Red-eared Slider turtles (Trachemys scripta elegans; RES) from the same pond in Santa Cruz County, California. Despite several WPT exhibiting significant shell lesions, scute defects, and pliable scutes, all tested negative for Emte. However, all three RES were Emte-positive, although two of these showed no shell defects. Given all tested RES were Emte-positive, it is possible that some WPT results are false negatives, either due to assay performance or insufficient shell tissue sampling. However, our Emte results in WPT are likely true negatives, and thus our observations contrast the high prevalence of Emte and shell disease in WPT from Washington. The emergence of Emte in California poses a previously unaccounted conservation concern for imperiled WPT. Emte's presence in California is also an important opportunity to study the epidemiology and ecology of this pathogen in a contrasting environmental context to Washington state where shell disease has had pronounced conservation consequences. Given the recent discovery of Snake Fungal Disease in California and the substantial impact the amphibian chytrid fungus has had on California's amphibians, there is an urgent need to understand the spread, prevalence, and impacts of Emte and other emerging wildlife diseases in California and elsewhere.

Comparative transcriptomic analysis reveals the gonadal development-related gene response to environmental temperature in Mauremys mutica

The Asian yellow pond turtle (Mauremys mutica) displays temperature-dependent sex determination (TSD), in which incubation temperature during embryonic development determines the sexual fate of the individual. However, the mechanism of the sex determination/differentiation of Mauremys mutica remains a mystery. Here, we first analyzed the temperature-specific gonadal transcriptomes of Mauremys mutica prior to gonad formation and gonads during the thermosensitive period. We uncovered a list of candidates that respond to temperature stimuli enriched in several categories, such as heat shock protein family members dnajb6a, dnaja4, hspa8 and hsp90aa1, temperature sensor genes mmp17 and mmp28, and putative novel temperature-responsive genes tmco6, gria3 and eif3f. Notably, striking differences were identified in the expression profiles of genes underlying sexual development, such as tex15, insr, igf1r, cirbp, esr1, dmrt2 and Serpinh1. Moreover, we analyzed the similarity and divergence of the timecourse of gene expression among Mauremys mutica and two other reported TSD turtles (Trachemys scripta and Chrysemys picta). The shared genes revealed the common gonad-specific regulatory mechanisms existing in these three TSD turtles that initiate their sexual development. Therefore, our findings could provide basic data to elucidate the mechanisms of sex determination/differentiation of M. mutica, even contributing to further understanding of these mechanisms in other TSD turtles.

Fine scale behaviour and time-budget in the cryptic ectotherm European pond turtle Emys orbicularis.

For ectotherms, behaviour and associated energetic costs are directly related to thermal conditions. In the present context of global change, estimating time-budget for these species is relevant to assess and predict their capacity to adapt to near future. We tested the hypothesis that in ectotherms where reproduction is highly energy consuming, energy expenditure should vary throughout the breeding season with a maximum around nesting events. To test this hypothesis, we assessed the fine-scale behaviour, time-budget and estimated energetic costs in eight adult female European pond turtles Emys orbicularis equipped with data-loggers recording ambient temperature, pressure, light and the animals’ 3-axis acceleration. Deployments occurred over four months throughout the nesting season 2017 in semi-natural captive conditions in Alsace, France. All study turtles showed a clear daily pattern over the 24h cycle, with four distinct phases (referred to as Night, Morning, Midday and Evening), associated with different behaviours and activity levels. Before oviposition, turtles were mostly active during Morning, and activity was positively driven by ambient temperature. Activity levels doubled during the nesting period, mostly due to the increased activity in the Evening, when nesting events occurred. Throughout the active season, basking occurrence at Midday was related to air temperature but cloud coverage was an even more important factor. Our results are a first step in predicting the seasonal time and energy budgets of the European pond turtle, and demonstrate the usefulness of animal-borne accelerometers to study free living freshwater turtles over extended periods of time.

Distribution range and population viability of Emys orbicularis in Slovakia: a review with conservation implications

The European pond turtle (Emys orbicularis) is the only native freshwater turtle species in Slovakia. Due to watercourse regulations in the middle of the 20th century, its range became fragmented and, currently, there are only two isolated populations. From a total of 1,236 historical records in Slovakia, most observations (782 records) came from the area of the Tajba National Nature Reserve (NNR). Three of the population viability analysis models (‘baseline’, ‘catastrophe’, ‘nest protection during a catastrophe’) indicated the extinction of the population in Tajba, with the highest probability of extinction occurring during a catastrophic event (probability of extinction 1.00). We also evaluated information about the activity patterns of seven radio-tracked individuals and about the number of destroyed nests from the area. During the period 2017–2021, we recorded only two turtles leaving the aquatic habitat of Tajba. An alarming fact is the massive number of destroyed nests found in the area during the study period (Tajba 524; Poľany 56). Our results indicate that the population in the Tajba NNR require immediate application of management steps to ensure its long-term survival.

Virulence and Antimicrobial Resistance Pattern of Aeromonas spp. Colonizing European Pond Turtles Emys orbicularis and Their Natural Environment. First Study from Poland.

Simple SummaryAeromonas species are Gram-negative facultative anaerobic bacteria with a wide distribution in nature. The genus comprises bacteria which can cause different types of diseases in many warm- and cold-blooded animals. Moreover, exposure to these bacteria can cause gastroenteritis or localized skin infections in humans. In the current study, Aeromonas species were identified in samples from water sources and European pond turtles (Emys orbicularis) from Eastern Poland. Our results revealed a high prevalence of Aeromonas isolates (43.2%) in the turtles and 66.7% in the water samples. All isolates were resistant to ampicillin, 62% to sulfamethoxazole, 40.5% to erythromycin, and 40.5% to colistin. Eight strains were intermediately resistant to meropenem. Additionally, most Aeromonas isolates (from 90.5% to 45.2%) were found to possess the following virulence genes: fla, aer, hlyA, act, ela, alt, and ast. This report indicated that European pond turtles were colonized by Aeromonas spp. While acting as reservoirs for these pathogens, they may play an important role in the etiology of Aeromonas-associated animal infections. Moreover, the undesirable properties of water quality caused by the presence of drug-resistant aeromonads could exert a negative impact on human health.The aim of the study was to isolate and identify species belonging to the Aeromonas genus and evaluate the antimicrobial resistance and virulence patterns of isolates colonizing European pond turtles (Emys orbicularis) from natural environment of Eastern Poland. In total, 74 turtles and 15 samples of water from their natural environment were examined. More than 40 strains were isolated and identified: A. bestiarum (n = 1), A. hydrophila (n = 13), A. allosaccharophila (n = 2), A. salmonicida (n = 3), and A. veronii (n = 23). The highest incidence of resistance was noted for ampicillin (100%) and sulfamethoxazole (62.0%), followed by erythromycin and colistin (both 40.5%). Moreover, eight strains were intermediately resistant to meropenem (19%). Most Aeromonas isolates were found to possess more than one virulence gene among fla, aer, hlyA, act, ela, alt, and ast. We showed that the population of free-living European pond turtles was highly colonized by Aeromonas spp. Such strains may be an infectious agent not only for the population of turtles but also for other species of animals inhabiting their natural environment. Moreover, the undesirable properties of water quality caused by the presence of drug-resistant aeromonads could have a negative impact on human health.

So close so different: what makes the difference?

The introduction of alien fish species in wetland ecosystems could have a great impact on freshwater communities and ecological processes. Despite fish introduction has been noticed as one of the principal cause of freshwater extinctions, ecosystem processes alteration, and change in aquatic community assemblage, very few data about impact on freshwater reptiles are available. As study model we used two neighbour sub-populations of the endangered Sicilian pond turtle, Emys trinacris, inhabiting two small, close each other and very similar lakes, except for the presence of allocthonous fish, Cyprinus carpio and Gambusia hoolbroki in one of the two. The multi-year study allowed highlighting significant differences in abundance, growth and reproductive output between the two freshwater turtle sub-populations, suggesting their influence on phenotypic plasticity of the studied population. These results are discussed in the light of previous evidence about the impact of these alien species on abundance and assemblage of the invertebrate community with an evident impact on niche width, diet composition and therefore energy intake by Emys trinacris. These data may provide important information to address management strategies and conservation actions of small wetland areas inhabited by pond turtles, pointing out a threats never highlighted up to now.

A case of Emys orbicularis (L.) feeding on newts from Bulgaria

Different amphibians and amphibian larvae were already observed and described as part of the diet of the European pond turtle. Few studies report body parts from adult newts in the stomach content of Emys orbicularis (Linnaeus, 1758) or newts predated by the same pond turtle species. We observed remains of Triturus dobrogicus (Kiritzescu, 1903) and Trituris ivanbureschi Arntzen &amp; Wielstra, 2013 eaten by E. orbicularis inside funnel traps, which strongly suggests, that newts are part of the diet, although not typical and often eaten food by this pond turtle.

Conservation of Northwestern and Southwestern Pond Turtles: Threats, Population Size Estimates, and Population Viability Analysis

Abstract Accurate status assessments of long-lived, widely distributed taxa depend on the availability of long-term monitoring data from multiple populations. However, monitoring populations across large temporal and spatial scales is often beyond the scope of any one researcher or research group. Consequently, wildlife managers may be tasked with utilizing limited information from different sources to detect range-wide evidence of population declines and their causes. When assessments need to be made under such constraints, the research and management communities must determine how to extrapolate from variable population data to species-level inferences. Here, using three different approaches, we integrate and analyze data from the peer-reviewed literature and government agency reports to inform conservation for northwestern pond turtles (NPT) Actinemys marmorata and southwestern pond turtles (SPT) Actinemys pallida. Both NPT and SPT are long-lived freshwater turtles distributed along the west coast of the United States and Mexico. Conservation concerns exist for both species; however, SPT may face more severe threats and are thought to exist at lower densities throughout their range than NPT. For each species, we ranked the impacts of 13 potential threats, estimated population sizes, and modeled population viability with and without long-term droughts. Our results suggest that predation of hatchlings by invasive predators, such as American bullfrogs Lithobates catesbeianus and Largemouth Bass Micropterus salmoides, is a high-ranking threat for NPT and SPT. Southwestern pond turtles may also face more severe impacts associated with natural disasters (droughts, wildfires, and floods) than do NPT. Population size estimates from trapping surveys indicate that SPT have smaller population sizes on average than do NPT (P = 0.0003), suggesting they may be at greater risk of local extirpation. Population viability analysis models revealed that long-term droughts are a key environmental parameter; as the frequency of severe droughts increases with climate change, the likelihood of population recovery decreases, especially when census sizes are low. Given current population trends and vulnerability to natural disasters throughout their range, we suggest that conservation and recovery actions first focus on SPT to prevent further population declines.

Basking Site Selection and Usage Strategies of the European Pond Turtle, &lt;i&gt;Emys orbicularis&lt;/i&gt; (Linnaeus, 1758) in Babat valley (Gödöllő, Hungary)

Sun basking is the most common method for freshwater turtles, such as the European pond turtle, to maintain optimal body temperature. The attributes of the macro- and microhabitat features around the basking sites affect the basking site selection of the European pond turtle. To protect the European pond turtle, it is important to know the basking habits among the biological characteristics of the species, along with the effects of the habitat characteristics and the choice of the type of basking sites. The purpose of our research was to detect the effects of macro- and microhabitat features on the selection of basking sites. We wanted to determine basking site type selection according to the carapace length classes and if there is any difference in the choice of basking trunks and branches with different thicknesses. Turtles choose basking sites with less closed vegetation in their environment. We have detected seasonal differences in the microhabitat features. The closing reed and Typha sp. had a negative effect on the number of observed basking turtles. The most popular type of basking sites in the pond system was the commonly occurred fallen tree trunks and branches in the water, regardless of turtle body size. Most turtles used thinner tree trunks and branches for basking. In the meantime, we found differences in the choice of basking trunks between the turtles with different body sizes. Younger turtles with smaller bodies appeared in larger numbers on emergent branches with smaller diameters.

The first case of Spiroxys contortus in European pond turtle (Emys orbicularis) in the wild in Poland.

During standard parasitological dissection of 4 individuals of European pond turtle (E. orbicularis) (Linneaus, 1758) one nematode was found. In a morphological examination the parasite was identified as Spiroxys contortus (Rudolphi, 1819) and confirmed by DNA analysis based on sequencing of the small subunit ribosomal RNA gene. The partial 18S rDNA gene was deposited to NCBI GenBank with the accession number MN629917. This is the first molecular evidence of S. contortus in E. orbicularis from wild from Poland. The analyzed sample genotype sequence shows 100% similarity to the reference specimen from Argentina.

Morphometric measurements of the European pond turtle (Emys orbicularis)(L., 1758) in Lithuania

In Lithuania, the number of European pond turtles Emys orbicularis decreased between 1975 and 2010, but increased significantly between 2010 and 2014, when the LIFE project was implemented. During this project, an ecological network was created, habitats were restored in protected areas, and European pond turtle nesting areas were protected from predators. Very few morphometric measurements of European pond turtles are carried out in Lithuania. The purpose of this study was to perform morphometric measurements, assess migration, spread, and morphometric size variation. Morphometric measurements of juvenile European pond turtles showed that the morphometric indicators depended on the place of habitation: males from Juodabalė Zoological Reserve (Meteliai Regional Park) are smaller than females. Also, female turtles from Meteliai Regional Park are larger than both males and females from Kučiuliškė Herpetological Reserve. When comparing the morphometric indicators of males and females at ten months of age, sexual dimorphism is already observed: the shell height, the width of the head, carapace, and plastron of a females are already bigger than those of males.

Optimal body mass-length ratio during hibernation for Emys orbicularis (Linnaeus, 1758) – European Pond Turtle

The aim of this study was to determine optimal body mass/length ratios of Emys orbicularis before hibernation. We obtained 213 measurements of wild-caught and captive-bred turtles during 9 years (2011–2019) and determined regression curves that show intervals for optimal or suboptimal body mass/length ratios before winter dormancy. Using this data we designed an online calculator that facilitates the process of establishing if a turtle has an optimal body mass/length ratio before hibernation. We also gathered 45 measurements at the end of the hibernation period which showed an average body mass loss of 5.32%. The present study offers practical means of assessing if an Emys orbicularis individual is fit for hibernation.

Distribution and Potential Limiting Factors of the European Pond Turtle (Emys orbicularis) in Eastern Europe

In order to use an integrated approach for studying the influence of risk factors on the distribution of the native turtle species E. orbicularis and accompanying invasive species (T. scripta and N. procyonoides) in the northeast of their range, we used GIS modelling and a database (GAEZ, human footprint, CliMond) of 55 preselected variables, which represent a system of bioclimatic and anthropogenic factors. The main variables that influenced the results were factors related to temperature. There was a high correlation (r = 0.6) between the species distribution model’s habitat suitability for E. orbicularis and the corresponding “human footprint” values within the European part of the species’ natural range. Its unpretentiousness towards anthropogenic factors would likely help the further expansion of its range in eastern Europe, because the areas with the highest habitat suitability (r &gt; 0.7) were projected to increase 3.3-fold. When comparing the E. orbicularis model to those obtained for N. procyonoides and T. scripta, we concluded that N. procyonoides could be dangerous because it occupies similar habitats (the degree of correlation is reasonably high in the north of their range (r = 0.5) in Latvia). An expansion of the range of Trachemys scripta is also possible in the future within the northern territories. Therefore, when developing the turtles’ protection algorithms, it is also necessary to take into account the influence of invasive species.

The Early Pleistocene ectothermic vertebrates of Pietrafitta (Italy) and the last Western European occurrence of Latonia Meyer, 1843

The Early Pleistocene site of Pietrafitta (central Italy) produced a rich vertebrate assemblage from the Late Villafranchian Land Mammal Age (late MN18). Geological and paleobotanical data from Pietrafitta indicate a lacustrine environment, surrounded by a humid deciduous broadleaved forest with a temperate climate. The vertebrate assemblage consists of at least 40 taxa including actinopterygians, amphibians, reptiles, birds, and mammals. Here, we concentrate on the ichthyofaunal and herpetofaunal remains. The ichthyofauna includes Barbus Cuvier and Cloquet, 1816, Scardinius Bonaparte, 1837, aff. Squalius Cuvier, 1817, and Tinca Cuvier, 1817. The two anuran genera are the large-sized alytid frog Latonia Meyer, 1843 and the “green frog” Pelophylax Fitzinger, 1843. Three snake precloacal vertebrae were recognized, one attributed to Colubrines indet., another one to ­Natrix sp. Laurenti, 1768, and the largest and most complete vertebra is referred to the genus Vipera s.l. Laurenti, 1768 (cf. gr. “Oriental vipers”). The chelonian fossils, including some complete carapaces and plastrals, are attributed to the European pond turtle (Emys gr. Orbicularis Linnaeus, 1758) and Hermann’s tortoise (Testudo hermanni Gmelin, 1789).

EVALUATION OF CALCIUM CARBONATE CONTENT IN EGGSHELLS OF AVIAN, TURTLE, SNAIL, AND OSTRICH USING CHEMICAL ANALYSIS AND SCANNING ELECTRON MICROSCOPY

In the present study, different eggs were collected and analyzed from five various animal species: European pond turtle (Emys orbicularis (Linnaeus, 1758)), giant African land snail (Achatina fulica (Bowdich, 1822)), common ostrich (Struthio camelus (Linnaeus, 1758)), white, light-brown, and dark-brown laying hen (Gallus gallus domesticus (Linnaeus, 1758) and European quail (Coturnix coturnix (Linnaeus, 1758). The typical mineral shell mainly composed of the calcite polymorph of CaCO3 but the eggshell consists of membranes, that composed mainly of proteins. The shell quality also could be assigned by several external and internal factors such as oviposition time, animal genotype and age, housing system (for poultry), and mineral nutrition complex. The CaCO3 content was determined by the standard titration method, coz the titration could provide a reliable method for evaluation of CaCO3 content in different types of eggshells. The structural surface characterization of eggshells was performed by scanning electron microscopy (SEM) with a field emission gun. In terms of chemical composition, ostrich eggshells generally did not differ much from those of laying hen, turtles, giant snails, or quail eggs, but the concentration of calcium carbonate was the highest. The average calcium carbonate content of various eggshells is between 84 and 98%. The thickness of the eggshell ranges from 0.08 to 1.89 mm, and it is not the same over the entire surface of the egg. At the sharp end of the egg, the shell is slightly thicker than at the blunt end. The purpose of this study was to study the quantitative content of calcium carbonate in various eggshells of different animals to draw further conclusions in which animals the eggshell contains the maximum amount of biological calcium carbonate.

Effects of Simulated Heat Wave on Oxidative Physiology and Immunity in Asian Yellow Pond Turtle (Mauremys mutica)

Global warming has led to an increase in the frequency, duration, and intensity of heat waves in the summer, which can cause frequent and acute heat stress on ectotherms. Thus, determining how ectothermic animals respond to heat waves has been attracting growing interest among ecologists. However, the physiological and biochemical responses to heat waves in reptiles, especially aquatic reptiles, are still poorly understood. The current study investigated the oxidant physiology, immunity, and expression levels of heat shock proteins (HSP) mRNA after exposure to a simulated heat wave (1 week, 35 ± 4°C), followed by a recovery period (1 week, 28 ± 4°C) in juvenile Asian yellow pond turtle (Mauremys mutica), a widely farmed aquatic turtle in East Asia. The contents of malondialdehyde (MDA) in the liver and muscle were not significantly affected by the heat wave or recovery. Of all antioxidant enzymes, only the activity of glutathione peroxidase (GSH-Px) in muscles increased after heat wave, while the total superoxide dismutase (T-SOD), catalase activity (CAT), and total antioxidant capacity (T-AOC) did not change during the study. The organo-somatic index for the liver and spleen of M. mutica decreased after the heat wave but increased to the initial level after recovery. In contrast, plasma lysozyme activity and serum complement C4 levels increased after the heat wave, returning to the control level after recovery. In addition, heat waves did not alter the relative expression of HSP60, HSP70, and HSP90 mRNA in the liver. Eventually, heat wave slightly increased the IBR/n index. Therefore, our results suggested that heat waves did not lead to oxidative damage to lipids in M. mutica, but deleteriously affected the turtles’ immune organs. Meanwhile, the constitutive levels of most antioxidative enzyme activities, HSPs and enhanced blood immune functions might protect the turtles from the threat of heat waves under the current climate scenarios.