Demographic and genetic status of an isolated population of bog turtles (<Emphasis Type="Italic">Glyptemys muhlenbergii</Emphasis>): implications for managing small populations of long-lived animals

In this study, we sought to determine the population stability and genetic diversity of one isolated population of the federally-threatened bog turtle (Glyptemys muhlenbergii) in North Carolina. Using capture–recapture data, we estimated adult survival and population growth rate from 1992 to 2007. We found that the population decreased from an estimated 36 adult turtles in 1994 to approximately 11 adult turtles in 2007. We found a constant adult survival of 0.893 (SE = 0.018, 95% confidence interval, 0.853–0.924) between 1992 and 2007. Using 18 microsatellite markers, we compared the genetic status of this population with five other bog turtle populations. The target population displayed allelic richness (4.8 ± 0.5) and observed heterozygosity (0.619 ± 0.064) within the range of the other bog turtle populations. Coalescent analysis of population growth rate, effective population size, and timing of population structuring event also indicated the genetics of the target population were comparable to the other populations studied. Estimates of effective population size were a proportion of the census size in all populations except the target population, in which the effective population size was larger than the census size (30 turtles vs. 11 turtles). We attribute the high genetic diversity in the target population to the presence of multiple generations of old turtles. This study illustrates that the demographic status of populations of long-lived species may not be reflected genetically if a decline occurred recently. Consequently, the genetic integrity of populations of long-lived animals experiencing rapid demographic bottlenecks may be preserved through conservation efforts effective in addressing demographic problems.     

Impacts of river alteration for flood control on freshwater turtle populations

The impacts of artificial river alteration for flood control on the dynamics of freshwater turtle populations were studied in small urban and rural river systems in northwestern Chiba Prefecture, Japan, from 2003 to 2006. The population density of the Reeve’s turtle, Chinemys reevesii, decreased markedly, from 279 turtles km⁻¹ in 2003 to 43 turtles km⁻¹ in 2006 in association with the artificial river alteration practices implemented by 2006. Low turtle population densities in other river sections where flood control measures have already been implemented suggest slow population recovery. River alteration practices also altered the age structures, sex ratios, and demographic characteristics of the turtle populations, although the exact consequences for population viability have not yet been determined. Because the turtles select concave submerged riverbanks or bottoms with slow or no current velocity, increased current velocity in the altered river section make the entire riverbank and bottom unsuitable for hibernation. Overall, river alteration for flood control during the winter season when turtles are inactive due to low water temperature negatively impacted freshwater turtle populations.     

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.     

Population Ecology of the Eastern Box Turtle in a Fragmented Landscape

Abstract: In the mid-Atlantic region, urban sprawl and development have resulted in habitat alterations and fragmentation; however, the effects on eastern box turtle (Terrapene carolina carolina) populations are unclear. To investigate the status of eastern box turtle populations in a fragmented landscape, we used mark—recapture and radiotelemetry to estimate population density, sex ratio, age structure, and survival on 4 study areas with differing degrees of isolation and human disturbance in northern New Castle County, Delaware, USA. We estimated adult population densities ranging from 0.81 turtles/ha to 3.62 turtles/ha among our 4 study areas. Sex ratios were male-biased at 2 study areas and balanced at 2 study areas. Proportion of juveniles ranged from 0% to 31%. Estimated annual survival rate ranged from 0.813 to 0.977. Mortality of radiotagged and marked turtles was primarily due to natural causes, but mowing was the primary cause of human-induced mortality. We found evidence of population decline at one study area due to low survival and recruitment. Human disturbances, isolation, and habitat composition appear to have the greatest influence on the box turtle populations we studied. To minimize mortality from human disturbance, we suggest planting crops adjacent to forest habitat that require no mowing or mowing at a height ≥15 cm. (JOURNAL OF WILDLIFE MANAGEMENT 72(3):745–753; 2008)     

Bigger is better: age class-specific survival rates in long-lived turtles increase with size

Vital rates for small, non-breeding individuals are important components of population dynamics for many species, but often individuals of these sizes are difficult to locate, capture, and track. As such, biologists frequently lack reliable estimates of juvenile survival because sample sizes and recapture rates for this life stage are low. Long-lived animals often take many years to reach sexual maturity and spend much of this time in the smaller size classes, making them sensitive to changes in survival rates. We estimated the survival rates of all size classes for the northern map turtle (Graptemys geographica) using a mark-recapture dataset with >3,500 captures from 2019–2021 and 210 nests from 2018–2021. As turtle size increased, annual survival probability increased regardless of sex. Estimated annual survival probability for turtles >18 cm long (i.e., adult females >15 years) was about 0.95, over 4 times higher than turtles that were 3 cm long (i.e., hatchlings <1 year; 0.22 annual survival probability). Although we did not observe a difference in survival probability between sexes of any size class, adult females are nearly twice the size of adult males, leading to an increased annual survival probability for females of 0.95, compared to 0.80 for males. Changes in adult survival had the greatest influence on population estimates over time, with temporary decreases, such as those due to poaching or an environmental disaster, potentially leading to unrecoverable decreases in the overall population size. Our study provides detailed survival rates for all size classes in a long-lived turtle, which are necessary to assess population stability and can be used to determine the most effective conservation or management practices.     

The leaf turtle population of Phnom Kulen National Park (northwestern Cambodia) has genetic and morphological signatures of hybridization

Cambodia is known to harbour three distinct species of Southeast Asian leaf turtles (Cyclemys spp.), which are heavily traded and common in seizures of wildlife. Confiscated leaf turtles are often released to natural habitats. Thus, an exact knowledge of the distribution of the individual species is of great importance to avoid the introduction of non‐native turtles, posing the risk of competition and hybridization. In this study, we examine a recently discovered leaf turtle population from Phnom Kulen National Park using external morphology, 17 unlinked microsatellite loci and the mitochondrial cytochrome b gene. Leaf turtles from the Phnom Kulen National Park morphologically resemble C. oldhamii, but harbour mitochondrial haplotypes of C. atripons. With respect to microsatellite loci, the turtles are distinct from C. atripons. Unfortunately no material of C. oldhamii was available from Cambodia. We propose that the Phnom Kulen population represents either a natural hybrid swarm of C. atripons and C. oldhamii or a distinct undescribed species with introgressed mitochondria of C. atripons. This underlines that genetic differentiation of wild leaf turtle populations in Cambodia is complex and suggests that this differentiation pattern becomes increasingly threatened by translocations of confiscated individuals. For drawing a definite conclusion about the taxonomic status of the Phnom Kulen population, denser sampling of other Cambodian leaf turtle populations would be required, in particular of C. oldhamii.     

Genetic diversity and population differentiation of the Chinese soft-shelled turtle (Pelodiscus sinensis) in three geographical populations

The Chinese soft-shelled turtle (Pelodiscus sinensis) is one of the most important economical chelonians in the world. To understand the genetic variations of the Chinese soft-shelled turtle in China, 62 individuals were sampled from three localities and 18 polymorphic microsatellite loci tested were used to detect genetic diversity and population structure. Results showed that the genetic diversity of the wild P. sinensis was high. Except for the Wuhu populations, the majority of microsatellite loci are not deviation from Hardy–Weinberg equilibrium in the other two populations. AMOVA analysis indicated that genetic variations occurred mainly within populations (97.4%) rather than among populations (2.6%). The gene flow estimates (Nm) among three geographic populations demonstrated that strong gene flow existed (Nm > 1, mean 6). The present study supported that different habitats, breed turtles escaped, multiple paternity and long evolutionary history may be responsible for the current genetic diversity and differentiation in the wild Chinese soft-shelled turtle.     

Effects of road proximity on genetic diversity and reproductive success of the painted turtle (Chrysemys picta)

Roads have a severe impact on wildlife. Reptiles are particularly susceptible due to their attraction to roads and their low car-avoidance capacity. For example, a high number of road killed freshwater turtles resulted from females selecting the unpaved side of roads as nesting sites. However, roads are harmful not only for adults, but are also expected to affect egg survival and recruitment. In this work, we indirectly determined whether the proximity to roads affects the reproductive success of freshwater turtles. The painted turtle (Chrysemys picta) was chosen for its population density, which is higher than most turtle species considered endangered. Locations near roads (<100 m) and in natural areas (>500 m) were sampled in three geographically distant ecoregions. We estimated the diversity of microsatellite loci from nuclear and mitochondrial genomes to assess the size of the kin groups as a proxy of the reproductive success of females. Similar diversity at nuclear markers suggested a comparable historical and demographic background among populations. However, lower mitochondrial diversity, higher mean and variance in the size of kin groups as well as a lower number of kin groups were strongly associated with the proximity to roads. Results indicated that a lower proportion of females participated in the recruitment of populations close to the roads than in natural areas, resulting in fewer but larger families near roads. We expect similar results for species nesting on the roadside. Barriers or fences that prevent individuals from reaching the road may help reduce their impacts on these populations.     

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.     

How far do adult turtles move? Home range and dispersal of Kinosternon integrum

We describe the home range and movements of a population of Kinosternon integrum in Tonatico, Estado de México, México, over 3.5 years (during rainy and dry season months) using radiotelemetry in 37 adult turtles. The results showed that the home range of K. integrum was 0.151 ± 0.051 ha using 50% kernel density estimator (KDE), and 0.657 ± 0.214 ha using 95% KDE; the home range did not vary between sexes. Kinosternon integrum showed low distances traveled 51.44 ± 4.50 m, where 87.3% (n = 373) of movements were <100 m. The distance traveled differed by season, and movement category (aquatic and terrestrial movements). The shortest distance occurred during the dry season, during which some individuals move to estivation sites, and these movements were shorter than movements to artificial ponds (cattle ponds). In this population, home range and movement are similar to other species of the genus Kinosternon. Overall, the results indicate than K. integrum are highly dependent on aquatic habitats, but also utilize the terrestrial habitats for different biological activities, and to maintain viable populations. Therefore, the conservation of the entire inhabited area is fundamental. This study highlights the need to increase the studies, in Central México, concerning habitat use of freshwater turtles in order to increase the efficiency of conservation strategies.     

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.     

Basking Activity is Modulated by Health State but is Constrained by Conspicuousness to Predators in Male Spanish Terrapins

Aerial basking may have several benefits for freshwater turtles in addition to thermoregulation such as removing parasites from the skin, which would improve health state. However, basking outside of water may be risky because it may expose freshwater turtles to terrestrial predators. Here, we monitored the basking activity of male Spanish terrapins (Mauremys leprosa) in a wild population of the south‐western of the Iberian Peninsula. We also measured body size, health state parameters, parasite prevalence, and limb coloration of these individuals. We aimed to examine whether basking may improve health state of turtles. The results showed that male turtles with higher basking activity were those parasitized by Hepatozoon and that had lower total white blood cell (WBC). This might indicate that turtles in worse health condition increase their time spent basking to improve their immune system. In addition, because basking might be risky, we also expected that turtles with more conspicuous coloration should reduce their basking activity to avoid being detected by potential predators. We found that infected turtles, but not uninfected ones, that spent more time basking also had less bright coloration in limb stripes. Our study provides evidence that basking activity may improve health state of terrapins, but that color conspicuity may increase costs of basking, especially for parasitized individuals. Understanding the balance between the benefits and the costs of basking might be essential for the conservation of freshwater turtle populations.     

Patterns of nuclear and mitochondrial DNA variation in Iberian populations of <Emphasis Type="Italic">Emys orbicularis</Emphasis> (Emydidae): conservation implications

The European pond turtle (Emys orbicularis) is threatened and in decline in several regions of its natural range, due to habitat loss combined with population fragmentation. In this work, we have focused our efforts on studying the genetic diversity and structure of Iberian populations with a fine-scale sampling (254 turtles in 10 populations) and a representation from North Africa and Balearic island populations. Using both nuclear and mitochondrial markers (seven microsatellites, ∼1048 bp nDNA and ∼1500 bp mtDNA) we have carried out phylogenetic and demographic analyses. Our results show low values of genetic diversity at the mitochondrial level although our microsatellite dataset revealed relatively high levels of genetic variability with a latitudinal genetic trend decreasing from southern to northern populations. A moderate degree of genetic differentiation was estimated for Iberian populations (genetic distances, F _ST values and clusters in the Bayesian analysis). The results in this study combining mtDNA and nDNA, provide the most comprehensive population genetic data for E. orbicularis in the Iberian Peninsula. Our results suggest that Iberian populations within the Iberian–Moroccan lineage should be considered as a single subspecies with five management units, and emphasize the importance of habitat management rather than population reinforcement (i.e. captive breeding and reintroduction) in this long-lived species.     

Long-term trends in abundance of green sea turtles (Chelonia mydas) assessed by non-lethal capture rates in a coastal fishery

Sea turtle populations underwent severe decline in historical times, mainly through harvesting eggs and adults on nesting beaches. With the reduction of this threat in many areas, coupled with other conservation actions, some populations have demonstrated encouraging recovery, although remaining below their previous levels and undergone additional modern threats such as incidental capture in fisheries and pollution. Trends in sea turtle populations have usually been assessed through monitoring of females or nests on nesting beaches. Here we present data from a 22-year monitoring period for a juvenile green sea turtle Chelonia mydas mixed-stock in southeastern Brazil that were incidentally captured in passive non-lethal pound nets. A total of 3639 green turtles were captured in 5323 fishing days.pound⁻¹ with mortality rate of 2%. Captures occurred in all months, but bycatch rates, excluding recapture events, were higher in September and October, probably due to the recruitment of turtles migrating from southern areas, as well as recruits from the oceanic zone. Capture rates increased by 9.2% per year in the period from 1995 to 2016, in line with increasing source populations, particularly the main source contributor at Ascension Island, but also Trindade Island (Brazil) and Aves Island (Venezuela). Mean Curved Carapace Length of green turtles was higher during austral summer/early autumn and decreased markedly in May, probably due to the small-sized individuals that recruited to the study site. We show that the incidental capture of sea turtles in non-lethal fisheries, such as Brazilian pound nets, could also provide data on trends of populations nesting in distant places, and can contribute to the assessment of population status of sea turtles within Regional Management Units throughout the Atlantic Ocean.     

Driftnet fishery threats sea turtles in the Atlantic Ocean

Fisheries are recognised as a major threat to sea turtles worldwide. Oceanic driftnets are considered the main cause of the steep decline in Pacific Ocean populations of the leatherback sea turtle Dermochelys coriacea. The world’s largest leatherback population nests in West Africa and migrates across the Atlantic Ocean to feed off the South American coast. There, the turtles encounter a range of fisheries, including the Brazilian driftnet fishery targeting hammerhead sharks. From 2002 to 2008, 351 sea turtles were incidentally caught in 41 fishing trips and 371 sets. Leatherbacks accounted for 77.3% of the take (n = 252 turtles, capture rate = 0.1405 turtles/km of net), followed by loggerheads Caretta caretta (47 individuals, capture rate = 0.0262 turtles/km of net), green turtles Chelonia mydas (27 individuals, capture rate = 0.0151 turtles/km of net) and unidentified hard-shelled turtles (25 individual, capture rate = 0.0139 turtles/km of net) that fell off the net during hauling. Immediate mortality (i.e., turtles that were dead upon reaching the vessel, excluding post-release mortality) was similar among the species and accounted for 22.2 to 29.4% of turtles hauled onboard. The annual catch by this fishery ranged from 1,212 to 6,160 leatherback turtles, as estimated based on bootstrap procedures under different fishing effort scenarios in the 1990s. The present inertia in law and enforcement regarding gillnet regulations in Brazil could result in the reestablishment of the driftnet fishery, driving rates of leatherback mortality to levels similar to those observed in previous decades. This development could potentially lead to the collapse of the South Atlantic leatherback population, mirroring the decline of the species in the Pacific. In light of these potential impacts and similar threats to other pelagic mega fauna, we recommend banning this type of fishery in the region.     

Monitoring and conservation of critically reduced marine turtle nesting populations: lessons from the Cayman Islands

Historically, nesting marine turtles were abundant in the Cayman Islands and were an integral part of the economy and culture. Today, nesting of loggerhead turtle Caretta caretta and green turtles Chelonia mydas takes place at very low levels. Hawksbill Eretmochelys imbricata nesting has not been recorded since 1999. We overview highly detailed monitoring data gathered over a 6-year period allowing insight into the magnitude and spatial and temporal patterns of marine turtle nesting, cost-effectiveness of monitoring such reduced populations, impacts of development on reproductive success and current threats to the recovery of the population. Nesting is diffuse and widely distributed for both nesting species on Grand and Little Cayman. Modelled nesting detection profiles for Grand Cayman show that in order to maintain data resolution, most sandy coastline must be surveyed throughout each season. However, in Little Cayman it may be possible to reduce effort. Legal take of adults and illegal take of eggs may be significantly impacting the remaining population. Surprisingly, we observed no significant correlation between density of coastal development and clutch density, adult emergence success or hatching success for either species. A significant relationship exists however, between density of coastal development and incidence of misorientation events in loggerhead hatchlings but not in green turtle hatchlings. Effective protection of known nesting habitat and the elimination of exploitation of remaining adults and eggs within the population are critical to its recovery.     

Massive transoceanic gene flow in a freshwater turtle (Testudines: Geoemydidae: Mauremys rivulata)

The freshwater turtle Mauremys rivulata ranges from the Adriatic coast of the Balkan Peninsula through the Aegean region and coastal western and southern Turkey southwards to Israel. In addition, it occurs on several Aegean islands, Crete and Cyprus. Previous investigations using mtDNA sequences found virtually no genetic differentiation across its distribution range, despite some major biogeographical barriers for terrestrial and freshwater biota. Thus, the absence of any phylogeographical differentiation would be unexpected. To re‐examine genetic differentiation within M. rivulata, here we use a comprehensive rangewide sampling and information of 13 unlinked polymorphic microsatellite loci and compare these data against mtDNA variation. Our microsatellite analyses reveal a weak population structuring which conflicts, however, with most biogeographical barriers. We conclude that the genetic structure in the vast majority of the species' range has been shaped by massive transoceanic gene flow. This explanation is unlikely for the northernmost populations, which seem rather to be genetically impacted by intentionally released foreign turtles.     

Large‐scale connectivity,cryptic population structure,and relatedness in Eastern Pacific Olive ridley sea turtles (Lepidochelys olivacea)

Endangered species are grouped into genetically discrete populations to direct conservation efforts. Mitochondrial control region (mtCR) haplotypes are used to elucidate deep divergences between populations, as compared to nuclear microsatellites that can detect recent structuring. When prior populations are unknown, it is useful to subject microsatellite data to clustering and/or ordination population inference. Olive ridley sea turtles (Lepidochelys olivacea) are the most abundant sea turtle, yet few studies have characterized olive ridley population structure. Recently, clustering results of olive ridleys in the Eastern Tropical Pacific Ocean suggested weak structuring (F_ST = 0.02) between Mexico and Central America. We analyzed mtCR haplotypes, new microsatellite genotypes from Costa Rica, and preexisting microsatellite genotypes from olive ridleys across the Eastern Tropical Pacific, to further explore population structuring in this region. We subjected inferred populations to multiple analyses to explore the mechanisms behind their structuring. We found 10 mtCR haplotypes from 60 turtles nesting at three sites in Costa Rica, but did not detect divergence between Costa Rican sites, or between Central America and Mexico. In Costa Rica, clustering suggested one population with no structuring, but ordination suggested four cryptic clusters with moderate structuring (F_ST = 0.08, p < .001). Across the Eastern Tropical Pacific, ordination suggested nine cryptic clusters with moderate structuring (F_ST = 0.103, p < .001) that largely corresponded to Mexican and Central American populations. All ordination clusters displayed significant internal relatedness relative to global relatedness (p < .001) and contained numerous sibling pairs. This suggests that broadly dispersed family lineages have proliferated in Eastern Tropical Pacific olive ridleys and corroborates previous work showing basin‐wide connectivity and shallow population structure in this region. The existence of broadly dispersed kin in Eastern Tropical Pacific olive ridleys has implications for management of olive ridleys in this region, and adds to our understanding of sea turtle ecology and life history, particularly in light of the natal‐homing paradigm.