Cranial variation amongst independent lineages of the alligator snapping turtle (Macrochelys temminckii)

Recent interest in diagnoses and relationships between lineages of the alligator snapping turtle (Macrochelys temminckii) present conflicting patterns of molecular variation across the taxon's range. This study uses geometric morphometric techniques to test molecular hypotheses. We analyse alligator snapping turtle cranial variation amongst populations (i.e. drainages) with the hypothesis that populations of turtles recovered as monophyletic by previous molecular studies are more similar to each other in cranial shape. Dorsal, lateral and ventral cranial shape analyses corroborate the uniqueness of populations recovered by molecular genetic hypotheses. Additionally, analyses reveal near equal separation between drainages that were assigned to monophyletic clades by previous phylogenetic studies. These results reveal the potential for more independent lineages that have yet to be diagnosed, and unique cranial shapes are described for our three most heavily sampled drainages.     

Modeling the emergence of migratory corridors and foraging hot spots of the green sea turtle

Environmental factors shape the spatial distribution and dynamics of populations. Understanding how these factors interact with movement behavior is critical for efficient conservation, in particular for migratory species. Adult female green sea turtles, Chelonia mydas, migrate between foraging and nesting sites that are generally separated by thousands of kilometers. As an emblematic endangered species, green turtles have been intensively studied, with a focus on nesting, migration, and foraging. Nevertheless, few attempts integrated these behaviors and their trade‐offs by considering the spatial configurations of foraging and nesting grounds as well as environmental heterogeneity like oceanic currents and food distribution. We developed an individual‐based model to investigate the impact of local environmental conditions on emerging migratory corridors and reproductive output and to thereby identify conservation priority sites. The model integrates movement, nesting, and foraging behavior. Despite being largely conceptual, the model captured realistic movement patterns which confirm field studies. The spatial distribution of migratory corridors and foraging hot spots was mostly constrained by features of the regional landscape, such as nesting site locations, distribution of feeding patches, and oceanic currents. These constraints also explained the mixing patterns in regional forager communities. By implementing alternative decision strategies of the turtles, we found that foraging site fidelity and nesting investment, two characteristics of green turtles' biology, are favorable strategies under unpredictable environmental conditions affecting their habitats. Based on our results, we propose specific guidelines for the regional conservation of green turtles as well as future research suggestions advancing spatial ecology of sea turtles. Being implemented in an easy to learn open‐source software, our model can coevolve with the collection and analysis of new data on energy budget and movement into a generic tool for sea turtle research and conservation. Our modeling approach could also be useful for supporting the conservation of other migratory marine animals.     

大鳄龟感染蛙病毒的PCR检测及组织病理分析

2013年3月成都市某海洋馆送检2只发病大鳄龟(Macrochelys temminckii),临床特征表现为:精神状态萎靡,爬行无力,对外界刺激反应迟钝;颈部和四肢局部红肿,腹甲溃烂,严重部位甚至穿孔,最后死亡。为明确患病大鳄龟的病因,进行了细菌学、组织病理学和PCR检查。细菌学检查阴性;病理组织学观察发现,大鳄龟多组织、器官均发生严重病变,尤其是肾、肝、肺和心的损伤最为严重,表现为明显的变性、坏死和炎症细胞浸润,并在一些病变组织细胞浆内见嗜酸性或嗜碱性包涵体。针对蛙病毒(Ranavirus)病毒的特异性PCR检测扩增出蛙病毒主要衣壳蛋白(MCP)基因500 bp目的片段,测序后的DNA序列与Gen Bank中已知核酸序列进行Blast比对,发现其与Gen Bank中的蛙病毒主要衣壳蛋白基因同源性达95%~99%。根据组织病理特点及PCR检测结果推测大鳄龟的死亡是感染蛙病毒所致。     

Incidental nest predation in freshwater turtles: inter- and intraspecific differences in vulnerability are explained by relative crypsis

There has long been interest in the influence of predators on prey populations, although most predator–prey studies have focused on prey species that are targets of directed predator searching. Conversely, few have addressed depredation that occurs after incidental encounters with predators. We tested two predictions stemming from the hypothesis that nest predation on two sympatric freshwater turtle species whose nests are differentially prone to opportunistic detection—painted turtles (Chrysemys picta) and snapping turtles (Chelydra serpentina)—is incidental: (1) predation rates should be density independent, and (2) individual predators should not alter their foraging behavior after encountering nests. After monitoring nest survival and predator behavior following nest depredation over 2 years, we confirmed that predation by raccoons (Procyon lotor), the primary nest predators in our study area, matched both predictions. Furthermore, cryptic C. picta nests were victimized with lower frequency than more detectable C. serpentina nests, and nests of both species were more vulnerable in human-modified areas where opportunistic nest discovery is facilitated. Despite apparently being incidental, predation on nests of both species was intensive (57% for painted turtles, 84% for snapping turtles), and most depredations occurred within 1 day of nest establishment. By implication, predation need not be directed to affect prey demography, and factors influencing prey crypsis are drivers of the impact of incidental predation on prey. Our results also imply that efforts to conserve imperiled turtle populations in human-modified landscapes should include restoration of undisturbed conditions that are less likely to expose nests to incidental predators.     

Genetic effects of landscape,habitat preference and demography on three co‐occurring turtle species

Expanding the scope of landscape genetics beyond the level of single species can help to reveal how species traits influence responses to environmental change. Multispecies studies are particularly valuable in highly threatened taxa, such as turtles, in which the impacts of anthropogenic change are strongly influenced by interspecific differences in life history strategies, habitat preferences and mobility. We sampled approximately 1500 individuals of three co‐occurring turtle species across a gradient of habitat change (including varying loss of wetlands and agricultural conversion of upland habitats) in the Midwestern USA. We used genetic clustering and multiple regression methods to identify associations between genetic structure and permanent landscape features, past landscape composition and landscape change in each species. Two aquatic generalists (the painted turtle, Chrysemys picta, and the snapping turtle Chelydra serpentina) both exhibited population genetic structure consistent with isolation by distance, modulated by aquatic landscape features. Genetic divergence for the more terrestrial Blanding's turtle (Emydoidea blandingii), on the other hand, was not strongly associated with geographic distance or aquatic features, and Bayesian clustering analysis indicated that many Emydoidea populations were genetically isolated. Despite long generation times, all three species exhibited associations between genetic structure and postsettlement habitat change, indicating that long generation times may not be sufficient to delay genetic drift resulting from recent habitat fragmentation. The concordances in genetic structure observed between aquatic species, as well as isolation in the endangered, long‐lived Emydoidea, reinforce the need to consider both landscape composition and demographic factors in assessing differential responses to habitat change in co‐occurring species.     

Evidence of counter‐gradient growth in western pond turtles (Actinemys marmorata) across thermal gradients

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Commercial harvest and export of snapping turtles (Chelydra serpentina) in the United States: trends and the efficacy of size limits at reducing harvest

As Asian turtle populations have crashed, China has increasingly turned to international import to meet domestic demand, which has increased pressure on global turtle populations. Snapping turtles (Chelydra serpentina) are being harvested in unprecedented numbers in the United States (US) to meet the needs of this international market. Here we report US snapping turtle live export from 1999 to 2013, and for the first time test the effectiveness of size limits in reducing commercial harvest numbers. Over three million live snapping turtles from farm and wild caught stock were exported from the US to Asia in 2012–14 alone. Increases in the export of wild caught snapping turtles to over 200,000 individuals in 2012 and 2014, compared to under 50,000 in other years, may indicate that farms are becoming unable to keep up with increasing demand. Annual harvest pressure at the state level increased linearly from 1998 to 2013, mirroring trends in federal export over the same time period. Our model estimates that size-limits were effective at reducing harvest by 30–87% in years with high harvest pressure. However, the majority of size limit regulations result in the removal of larger breeding adults, which has been shown to be detrimental to long term population viability. Regulatory approaches dedicated to the long term management of this iconic species will need to balance the short term gains, in the form of reduced harvest rates, with long term population viability.     

Juvenile proportion as a predictor of freshwater turtle population change

The extreme longevity of turtles and tortoises can make it difficult to determine the conservation status of their populations because high annual adult survival may mask gradual attrition due to low levels of recruitment. When long-term demographic trends are unknown and available data are insufficient for population modelling, it may be assumed that a scarcity of juveniles indicates low recruitment that will result in population ageing and numerical decline. However, the reliability with which the proportion of juveniles foreshadows demographic change is uncertain. We tested the hypothesis that a low proportion of juveniles in a turtle population presages its ageing by analysing over 20 years of survey data for five discrete populations of the Australian western saw-shelled turtle (Myuchelys bellii: Chelidae), a listed threatened species. The analysis tested whether the initial proportion of juvenile turtles in each population was related to its temporal trend in average body size. The five populations had varied structure and trends, with the initial proportion of juvenile turtles ranging from 10% to 39% and average body size increasing over time in some populations and decreasing in others. Contrary to expectation, the initial proportion of juveniles was unrelated to the trend in average body size and, by inference, average age, indicating that effective trend forecasting requires more detailed demographic information than merely population structure.     

Identifying Hot Moments in Road-Mortality Risk for Freshwater Turtles

ABSTRACT Risk assessments can be used to identify threats, which vary both in space and time, to declining species. Just as hot spots describe locations where threat processes operate at a higher rate than in surrounding areas, hot moments refer to periods when threat rates are highest. However, the identification of hot moments can be challenging because the temporal complexity of some threat processes makes their effects on population viability difficult to predict. Declining throughout much of their range, Blanding's turtle (Emydoidea blandingii) populations are potentially most vulnerable to road mortality where road densities and traffic volumes are high. The temporal variations in road-mortality risk faced by these and other semiaquatic turtles at the population level are a consequence of several factors, including sex-specific movement characteristics and seasonal changes in traffic volume. We examined these risk factors for Blanding's turtle populations in Maine, USA, by integrating temporally explicit roadkill probabilities with demographic parameters informed by local and range-wide studies. Specifically, we used population simulations to estimate the relative risk for 14 2-week periods during the turtles’ active season. Our analysis clearly identified early summer as a period of elevated risk, with June through mid-July signaling a road-mortality hot moment for Blanding's turtles (for both M and F). These findings provide guidance for the implementation of temporally explicit conservation measures such as cautionary road signage, traffic management, and public outreach that, if timed strategically, could help to mitigate population impacts from road mortality.     

Characterization of microsatellite DNA markers for the alligator snapping turtle,Macrochelys temminckii

Two trinucleotide and seven tetranucleotide microsatellite loci were isolated from an alligator snapping turtle Macrochelys temminckii. To assess the degree of variability in these nine microsatellite loci, we genotyped 174 individuals collected from eight river drainage basins in the southeastern USA. These markers revealed a moderate degree of allelic diversity (six to 16 alleles per locus) and observed heterozygosity (0.166–0.686). These polymorphic microsatellite loci provide powerful tools for population genetic studies for a species that is afforded some level of conservation protection in every state in which it occurs.     

Road avoidance and its energetic consequences for reptiles

Roads are one of the most widespread human‐caused habitat modifications that can increase wildlife mortality rates and alter behavior. Roads can act as barriers with variable permeability to movement and can increase distances wildlife travel to access habitats. Movement is energetically costly, and avoidance of roads could therefore impact an animal's energy budget. We tested whether reptiles avoid roads or road crossings and explored whether the energetic consequences of road avoidance decreased individual fitness. Using telemetry data from Blanding's turtles (Emydoidea blandingii; 11,658 locations of 286 turtles from 15 sites) and eastern massasaugas (Sistrurus catenatus; 1,868 locations of 49 snakes from 3 sites), we compared frequency of observed road crossings and use of road‐adjacent habitat by reptiles to expected frequencies based on simulated correlated random walks. Turtles and snakes did not avoid habitats near roads, but both species avoided road crossings. Compared with simulations, turtles made fewer crossings of paved roads with low speed limits and more crossings of paved roads with high speed limits. Snakes made fewer crossings of all road types than expected based on simulated paths. Turtles traveled longer daily distances when their home range contained roads, but the predicted energetic cost was negligible: substantially less than the cost of producing one egg. Snakes with roads in their home range did not travel further per day than snakes without roads in their home range. We found that turtles and snakes avoided crossing roads, but road avoidance is unlikely to impact fitness through energetic expenditures. Therefore, mortality from vehicle strikes remains the most significant impact of roads on reptile populations.     

Predicted distributions and abundances of the sea turtle ‘lost years’ in the western North Atlantic Ocean

Oceanic dispersal characterizes the early juvenile life-stages of numerous marine species of conservation concern. This early stage may be a ‘critical period’ for many species, playing an overriding role in population dynamics. Often, relatively little information is available on their distribution during this period, limiting the effectiveness of efforts to understand environmental and anthropogenic impacts on these species. Here we present a simple model to predict annual variation in the distribution and abundance of oceanic-stage juvenile sea turtles based on species’ reproductive output, movement and mortality. We simulated dispersal of 25 cohorts (1993–2017) of oceanic-stage juveniles by tracking the movements of virtual hatchling sea turtles released in a hindcast ocean circulation model. We then used estimates of annual hatchling production from Kemp's ridley Lepidochelys kempii (n = 3), green Chelonia mydas (n = 8) and loggerhead Caretta caretta (n = 5) nesting areas in the northwestern Atlantic (inclusive of the Gulf of Mexico, Caribbean Sea and eastern seaboard of the U.S.) and their stage-specific mortality rates to weight dispersal predictions. The model's predictions indicate spatial heterogeneity in turtle distribution across their marine range, identify locations of increasing turtle abundance (notably along the U.S. coast), and provide valuable context for temporal variation in the stranding of young sea turtles across the Gulf of Mexico. Further effort to collect demographic, distribution and behavioral data that refine, complement and extend the utility of this modeling approach for sea turtles and other dispersive marine taxa is warranted. Finally, generating these spatially-explicit predictions of turtle abundance required extensive international collaboration among scientists; our findings indicate that continued conservation of these sea turtle populations and the management of the numerous anthropogenic activities that operate in the northwestern Atlantic Ocean will require similar international coordination.     

Effect of acclimation temperature and substrate type on selected temperature,movement and activity of juvenile spiny softshell turtles (Apalone spinifera) in an aquatic thermal gradient

In some turtle species, temperature selection may be influenced by environmental conditions, including acclimation temperature and substrate quality. These factors may be particularly important for softshell turtles that are highly aquatic and often thermoregulate by burying in the substrate in shallow water microhabitats. We tested for effects of acclimation temperature (22 °C or 27 °C) and substrate type (sand or gravel) on the selected temperature and movement patterns of 20 juvenile spiny softhshell turtles (Apalone spinifera; Reptilia: Trionychidae) in an aquatic thermal gradient of 14–34 °C. Among 7–11 month old juvenile softshell turtles, acclimation temperature and substrate type did not influence temperature selection, nor alter activity and movement patterns. During thermal gradient tests, both 22- and 27 °C-acclimated turtles selected the warmest temperature (34 °C) available most frequently, regardless of substrate type (sand or gravel). Similarly, acclimation temperature and substrate type did not influence movement patterns of turtles, nor the number of chambers used in the gradient tests. These results suggest that juvenile Apalone spinifera are capable of detecting small temperature increments and prefer warm temperatures that may positively influence growth and metabolism, and that thermal factors more significantly influence aquatic thermoregulation in this species than does substrate type.     

Survival and Causes of Mortality of Head-Started Western Pond Turtles on Pierce National Wildlife Refuge,Washington

ABSTRACT The western pond turtle (Actinemys marmorata) is a species of conservation concern over much of its range and is listed as endangered in Washington State. From 2000 to 2004, we used radiotelemetry to document survival and mortality factors of head-started western pond turtles (n = 68) released into Pierce National Wildlife Refuge in southwestern Washington. Survival estimates for first year and older turtles ranged from 86% to 97% and overlapping confidence intervals indicated no detectible differences among age classes or among years. Subadult turtles released at ≥90-mm carapace length apparently avoided capture by most aquatic predators, indicating that terrestrial predators should be the focus of research and management where predation on larger age-classes is a concern. High annual survival combined with the documented nesting by ≥7-year-old female head-started turtles in Washington suggest that recruitment of adults is being achieved; however, head-starting is only practical as an interim solution and strategies for effective removal of aquatic predators must be developed and implemented where natural recruitment is inadequate to maintain populations.     

Long-term behavioral repeatability in wild adult and captive juvenile turtles (Terrapene carolina): Implications for personality development

Animal personality can be defined as conspecific individuals consistently differing in behavioral tendencies. Personality is typically identified by behavioral repeatability, which occurs when within-individual variance is low relative to among-individual variance in the population. Intraspecific comparisons of behavioral repeatability in juveniles and adults within and across years are rare, but would be useful for testing hypotheses related to origins of animal personality and whether individuals exhibit stable or diverging behavior with ontogeny. To examine within- and across-year behavioral repeatability for eastern box turtles (Terrapene carolina), we assessed boldness (movement latency after brief confinement) of captive-born juveniles twice within three days when eight months old. We then repeated these tests for the same individuals one year later. Juveniles exhibited repeatable boldness within and across years. Although increasing body temperature was slightly associated with decreased movement latency, test year (1 or 2), or housing experience (being raised in an enriched or unenriched condition) had no effects on boldness. We also assessed across-year repeatability of boldness (head emergence from the shell after brief confinement) for wild adults at 1–3 year intervals. Adults also exhibited repeatable across-year boldness that was of similar magnitude to juveniles. We found no indication that sex class or whether adults had been radio-tracked influenced boldness. Our results suggest eastern box turtles demonstrate consistent individuality in boldness from an early age that is largely unaffected by temporal or environmental variation, and these behavioral differences can be maintained for multiple years in captivity and the wild, contrasting with theoretical expectations for personality development. These findings add to recent accumulating evidence demonstrating juvenile and adult box turtles exhibit multiple repeatable behaviors over the short- and long-term. We suggest this species is quickly gaining traction as a model organism for studying the proximate and ultimate causes of personality development within long-lived animals.     

Oviductal morphology in relation to hormonal levels in the snapping turtle, Chelydra serpentina

Microscopic and in situ visual observations were used to relate circulating hormone levels to morphological changes in the oviduct of the snapping turtle Chelydra serpentina throughout the ovarian cycle. Increase in levels of progesterone (P), estradiol (E2) and testosterone (T) levels coincide with an increase in number and growth of endometrial glands, luminal epithelial cells and secretory droplets throughout the oviduct. Testosterone and estradiol levels rose significantly (P < 0.05) after the May-June period and remained high throughout the rest of the summer. Progesterone levels remained stable throughout the summer, with a brief decline in July due to luteolysis. Hormonal values declined significantly (P < 0.001) at the end of the ovarian cycle in the fall. In situ visual observation of fresh oviducts at different stages of gravidity in recently ovulated turtles revealed that proteinaceous like components from the endometrial glands were released into the lumen to form fibers. The morphological features of the oviduct remained active throughout the summer months even though the snapping turtle is a monoclutch species which deposits all the eggs in late-May to mid-June. The high steroid levels correlate with and may be responsible for the secretory activity present throughout the summer and their decline correlates with change to low secretory activity in the fall. Calcium deposition accompanied by morphological changes in luminal cells are suggestive of secretory activity. In the egg-bearing turtles, uterine Ca2+ concentrations measured by flame atomic absorption spectrophotometry revealed significantly higher Ca2+ concentrations (P < 0.001) in eggs with soft shell than eggs without shell. There was a significant increase in calcium granules and proteinaceous fibers in luminal surface of the uterus during the period of eggshelling. This supports the fact that in the snapping turtle like in other reptiles, eggshelling process occurs in the uterus.     

Eimeria filamentifera sp. n. from the Snapping Turtle, Chelydra serpentina (Linné), in Iowa

SYNOPSIS. Oocysts of Eimeria filamentifera sp. n. were isolated from 2 of 2 snapping turtles, Chelydra serpentina (Linné), in Iowa. The ovoid to ellipsoid oocysts of this species averaged 23.2 × 18.6 μm and had a length/width ratio ranging from 1.1 to 1.6. The ellipsoid sporocysts averaged 14.0 × 7.7 μm and had papillose, filament-bearing Stieda bodies. Oocyst and sporocyst residua were present, but micropyle and polar granule were not. This appears to be the 2nd species of Eimeria reported from snapping turtles, with E. chelydrae being the first.     

Disruption of magnetic orientation in hatchling loggerhead sea turtles by pulsed magnetic fields

Loggerhead sea turtles (Caretta caretta) derive both directional and positional information from the Earths magnetic field, but the mechanism underlying magnetic field detection in turtles has not been determined. One hypothesis is that crystals of biogenic, single-domain magnetite provide the physical basis of the magnetic sense. As a first step toward determining if magnetite is involved in sea turtle magnetoreception, hatchling loggerheads were exposed to pulsed magnetic fields (40 mT, 4 ms rise time) capable of altering the magnetic dipole moment of biogenic magnetite crystals. A control group of turtles was treated identically but not exposed to the pulsed fields. Both groups of turtles subsequently oriented toward a light source, implying that the pulsed fields did not disrupt the motivation to swim or the ability to maintain a consistent heading. However, when swimming in darkness under conditions in which turtles normally orient magnetically, control turtles oriented significantly toward the offshore migratory direction while those that were exposed to the magnetic pulses did not. These results are consistent with the hypothesis that at least part of the sea turtle magnetoreception system is based on magnetite. In principle, a magnetite-based magnetoreception system might be involved in detecting directional information, positional information, or both.     

Mixed-stock aging analysis reveals variable sea turtle maturity rates in a recovering population

Quantifying demographic parameters and variable vital rates, such as somatic growth rates, time to maturity, and reproductive longevity, is important for effective management of threatened and endangered populations such as sea turtles (Cheloniidae). To address these knowledge gaps, we applied skeletochronology to analyze and compare somatic growth rates and variation in life-history traits such as age and size at sexual maturity for 65 green turtles (Chelonia mydas) in the eastern Pacific Ocean (EP), along the west coast of the United States; turtles belonged to ≥2 nesting subpopulations that differed in body size (mean nesting size). Green turtles in the EP spend approximately 5 years in the oceanic stage before recruiting to nearshore habitats, males may be smaller and younger than females at maturation (x̅ = 17.7 ± 5.5 yr vs. 28.0 ± 8.2 yr), and younger age at sexual maturity was associated with smaller size at sexual maturity, suggesting that mean nesting body size may be reflective of maturation timing for subpopulations. Smaller body sizes for females nesting at Michoacán, Mexico (continental) rookeries, yielded a younger predicted age at sexual maturity (x̅ = ~17 yr) compared to females from Revillagigedo Islands, Mexico rookeries, which displayed larger body sizes and older age at sexual maturity (x̅ = ~30 yr). We consider possible mechanisms driving the observed divergence in life-history traits, including the possibility that earlier maturation (reduced generation length) for turtles in the Michoacán nesting subpopulation may be a response to intense harvesting in the past 50 years, and consideration of such anthropogenic impacts is warranted by population managers. Finally, our results indicate green turtles moved into nearshore neritic habitats at a young age (4–6 yr), emphasize the importance of protecting neritic habitats along the southwestern United States and northwestern Mexican coasts, and encourage the incorporation of variable maturation time in population recovery assessments.     

Not all management is equal: a comparison of methods to increase wood turtle population viability

Management generally targets the most tractable life stage to rescue declining populations; however, that stage may not have the largest influence on recovery. Freshwater turtles are declining globally and early stages are frequently targeted for management, although the effectiveness of these actions on population growth are relatively unknown because of incomplete demographic data. We estimated the hatchling yearly survival rate for a freshwater turtle in the field using in situ enclosures to collect missing demographic information. We used these data to develop demographic models to calculate growth rate for a hypothetical, declining population of wood turtles (Glyptemys insculpta) in Wisconsin, USA, 2014–2019. We modeled growth for populations across a range of scenarios from no management to combinations of nest protection and head-starting at varying levels of effort. Nest protection alone did not increase population growth rate, while head-starting alone increased population growth by 0.07, with the largest increase in growth rate, 0.11, resulting from combinations of both approaches. No combination of nest protection and head-starting, without an increase in adult survival rate from the observed 0.88 to ≥0.95, led to population stabilization or increase. Populations of freshwater turtles, like the wood turtle, will likely only recover with a multi-faceted approach that targets multiple life stages simultaneously.