Turtle Research Articles

Eggshell composition of Amazon turtle (Podocnemis expansa) is altered after incubation in substrates containing glyphosate and fipronil formulations

Besides its crucial role during embryo development, eggshells are an essential bioindicator of environmental contaminants. However, the effects of contaminant exposure during incubation on the eggshell composition remain poorly known for freshwater turtles. Accordingly, we tested the effects of incubating the eggs of Podocnemis expansa in substrates containing glyphosate and fipronil formulations on the eggshell's level of mineral and dry matter, crude protein, nitrogen, and ethereal extract. Eggs were incubated in sand moistened with water contaminated with glyphosate Atar 48 at concentrations of 65 or 6500 μg/L, fipronil Regent 800 WG at concentrations of 4 or 400 μg/L, or the combination of 65 μg/L glyphosate and 4 μg/L fipronil and 6500 μg/L glyphosate with 400 μg/L fipronil. Exposure to the tested pesticides, alone or in association, altered the chemical composition of the eggshell of P. expansa, reducing the eggshell's moisture and crude protein content and increasing levels of ethereal extract. These changes may cause significant deficiencies in the mobilization of water and nutrients to the embryo, affecting the development and reproductive success of P. expansa.

Molecular Phylogenies of Leeches and Haemoparasites Infecting Freshwater Turtles in Aquatic Ecosystems of Northern Africa Suggest Phylogenetic Congruence between Placobdella costata Sensu Lato and Haemogregarina stepanowi Sensu Lato.

Haemogregarines are blood parasites with a life-cycle involving a vertebrate as the intermediate host and an invertebrate as the definitive host and vector. Extensive phylogenetic investigations based on 18S-rRNA gene sequences have shown that Haemogregarina stepanowi (Apicomplexa: Haemogregarinidae) is able to infest a large diversity of freshwater turtle species, including the European pond turtle Emys orbicularis, the Sicilian pond turtle Emys trinacris, the Caspian turtle Mauremys caspica, the Mediterranean pond turtle Mauremys leprosa, and the Western Caspian turtle Mauremys rivulata, among others. From the same molecular markers, H. stepanowi is further considered to be a complex of cryptic species predisposed to infect the same host species. While Placobdella costata is known to be the unique vector of H. stepanowi, it is only recently that independent lineages within P. costata have been illustrated-suggesting the presence of at least five unique leech species across Western Europe. The aims of our study were therefore to investigate from mitochondrial markers (COI) the genetic diversity within haemogregarines and leeches infecting freshwater turtles of the Maghreb, in order to identify processes of parasite speciation. We showed that H. stepanowi consists of at least five cryptic species in the Maghreb, while two Placobella species were identified in the same area. Although an Eastern-Western speciation pattern was apparent for both leeches and haemogregarines, we cannot make definitive conclusions regarding co-speciation patterns between parasites and vectors. However, we cannot reject the hypothesis of a very strict host-parasite specificity within leeches.

Nesting Emergences and Other Terrestrial Movements of Macrochelys (Testudines: Chelydridae)

Alligator snapping turtles (genus Macrochelys) are the largest freshwater turtles in North America. Despite strong interest in their conservation, we still lack a comprehensive understanding of their natural history, including behaviors associated with terrestrial activity. We reviewed the literature and solicited unpublished observations of terrestrial movements of these highly aquatic turtles. We compiled 206 observations of terrestrial activity from 9 states. The majority of observations were associated with nesting behavior. Observations expanded our knowledge regarding the spatial extent and timing of terrestrial movements and the nesting season. In addition, we compiled observations of terrestrially foraging animals, as well as males and juveniles traveling overland and crossing roads. Collectively, this information clarifies the extent of terrestrial movement by Macrochelys, behaviors that should be considered in conservation plans.

Maximum Body Size of the Suwannee Alligator Snapping Turtle (Macrochelys suwanniensis)

The published literature does not provide a consensus regarding maximum body sizes of North America's largest wild freshwater turtles (genus Macrochelys). The largest known wild M. suwanniensis (Suwannee Alligator Snapping Turtle) currently exists as a curated specimen measuring 713 mm straight-midline carapace length, 801 mm maximum carapace length, 619 mm maximum carapace width, and 236 mm maximum head width. The turtle was never weighed, but we used morphometric data from our studies in the Santa Fe and Suwannee rivers to estimate that it weighed ∼76.4 kg (168 lbs) when captured. Our 95% prediction interval (67.6–86.3 kg [149–190 lbs]) suggests that speculative estimates and anecdotal reports of M. suwanniensis that weigh ≥90 kg (≥200 lbs) are dubious.

Big Turtles Start Small: Trapping Juvenile Alligator Snapping Turtles in South Mississippi and Implications for Conservation

Macrochelys (alligator snapping turtles), the largest freshwater turtles in North America, were recently proposed for threatened status under the US Endangered Species Act. Many previous surveys have focused on catching these large turtles in large river systems, but few surveys have focused on targeting hatchlings and juveniles, particularly in smaller rivers and creeks. I trapped extensively within the Pascagoula River drainage using small, baited crayfish traps, and a considerable focus of the study was in small rivers and streams. Juvenile Macrochelys temminckii (Alligator Snapping Turtle; 42.2–192 mm) were detected in small streams and large rivers (30.4 km2–22,000 km2), and the small traps were effective at capturing young alligator snapping turtles. Smaller streams are logistically harder to trap from a boat, but small streams should not be overlooked when sampling for this species, as these streams may have served as refugia during commercial harvest over the past century.

ESTIMATION OF SALMONELLA SPP. PREVALENCE AND DIVERSITY AMONG FREE-LIVING TURTLES AND A ZOO COLLECTION

Salmonellosis infection is caused by bacteria of the genus Salmonella. There are many pathways for the pathogenic bacteria to spread which is through contaminated food, water, and contact with animals. The research was conducted to detect Salmonella spp. carriage in free-living aquatic turtles and zoo turtles. Turtles are frequent inhabitants of zoos and the owners of a large number of bacteria in their outer skin and shell surfaces that under adverse conditions can multiply and lead to the development of infection. However, they are known to be a frequent source of Salmonella infection without showing signs of disease. The risk of human infection exists if personal hygiene is not followed after contact with a turtle. Identification of bacteria of the genus Salmonella, the main causative agent of the disease was determined by the standard method on chromogenic Salmonella LAB-Agarᵀᴹ (BIOMAXIMA, Poland) agar. The inoculation was incubated under aerobic conditions at 37 ± 1°C for 72 h. Serotype (D serotype) was determined by serotyping in 11 from 16 (68.75%) Zoo inhabitants but not found in 25 free-living turtles. Our present research is of theoretical and practical value for the study of free-living turtles as well as from the collections of zoos under protection in Latvia and Europe. It is necessary to remember the possibility of infection with pathogenic bacteria.

Systemic Caryospora-like coccidiosis in a clutch of hatchling red-eared slider turtles (Trachemys scripta elegans).

Caryospora-like organisms (CLOs) form a clade of at least 11 genotypes of related coccidia that can cause epizootic mortality in marine turtles. The biology, transmission, host species range, and host cell tropism of these organisms are still largely unknown. The goal of this study was to characterize the host cell tropism, pathologic and ultrastructural features, and phylogeny associated with the first report of a mortality event due to CLO in the freshwater red-eared slider turtle (Trachemys scripta elegans). Sudden mortalities within a clutch of captive-raised red-eared slider hatchlings (n = 8) were recorded, and deceased animals had severe segmental to diffuse, transmural, fibrinonecrotic enterocolitis and multifocal to coalescing hepatic necrosis, among other lesions associated with numerous intracytoplasmic developing stages of intralesional coccidia. Among the different developmental stages, merozoites were ultrastructurally characterized by an apical complex. A pan-apicomplexan polymerase chain reaction (PCR) yielded a 347 bp-amplicon matching the Schellackia/Caryospora-like clade with 99.1% identity to the US3 strain from green sea turtles (Chelonia mydas) and 99.1% identity to Schellackia sp. Isolate OC116. Surviving hatchlings were treated with toltrazuril sulfone (ponazuril) but were subsequently euthanized due to the risk of spreading the parasite to other chelonids in the collection. The ponazuril-treated hatchlings (n = 4) had mild proliferative anterior enteritis, with few intraepithelial coccidia in one hatchling confirmed as CLO by PCR. This is the first report of Caryospora-like coccidiosis in non-cheloniid turtles, highlighting the relevance of this disease as an emerging highly pathogenic intestinal and extra-intestinal form of coccidiosis of turtles with potential cross-species infectivity.

Mepimbat tedul proujek: Indigenous knowledge of culturally significant freshwater turtles addresses species knowledge gaps in Northern Australia

AbstractIndigenous biocultural knowledge offers valuable insights for species conservation; however, like biological diversity, associated cultural knowledge is also often threatened. This paper demonstrates how Indigenous biocultural knowledge of species can contribute to addressing gaps in species occurrence data and conservation knowledge using a case study from the South East Arnhem Land Indigenous Protected Area (SEAL IPA), northern Australia. Using a series of mapping workshops and interviews this collaborative project recorded Indigenous biocultural knowledge of the distribution, ecology, cultural significance and threats to freshwater turtles (freshwoda teduls in the local Indigenous language, Roper River Kriol). Based on past freshwoda tedul hunting experiences, 74 Indigenous knowledge holders identified 753 past freshwoda tedul occurrences, significantly adding to the 12 occurrences previously listed for the SEAL IPA in Australia's online species database, the Atlas of Living Australia. Importantly, these were the first ‘memory’ records of past species sightings by Indigenous people to be recognized and added to Australia's national species database. In addition, a blog summarizing this research was promoted through the Atlas of Living Australia, raising awareness of the Indigenous biocultural knowledge associated with these species. The Mepimbat tedul proujek revealed the cultural significance of freshwoda teduls and reported declines in abundance since the turn of the century, implicating invasive hard‐hooved ungulates (buffalo, pig) and reduced rainfall. The addition of non‐sacred Indigenous knowledge to free online species databases may offer innovative solutions for storage, interaction and sharing of indigenous knowledge, with opportunities for intergenerational and cross‐cultural learning and broader application in conservation management and decision‐making.

Nocturnal basking in freshwater turtles: A global assessment

Nocturnal basking in freshwater turtles: A global assessment

A preliminary assessment of chelonian diversity in the montane forests of two areas in northern Vietnam

Very little is known of the ecology and distribution of Vietnamese tortoises and freshwater turtles, even though Vietnam is one of the world’s hotspots of chelonian diversity and, according to the International Union for the Conservation of Nature (IUCN), almost all its species are threatened. We report the diversity of chelonians for two distinct areas of northern Vietnam (in three provinces) characterised by forested hills and mountains, with ponds and streams. We observed ten species in Lang Son/Bac Giang provinces and 11 species in Lao Cai province. Reportedly, the two most frequently recorded species were Pelodiscus sinensis and Cuora mouhotii. Most species were Endangered or Critically Endangered according to IUCN, thus making the protection of the forest habitats of these provinces of crucial relevance for the survival of these species. Reliable records for the almost extinct Rafetus swinhoei were collected, but all of them refer to the end of the 1970s.

HEALTH ASSESSMENT OF PAINTED TURTLES (CHRYSEMYS PICTA) IN A RESTORED WETLAND HABITAT IN NORTHWESTERN INDIANA, USA.

Freshwater turtles are sensitive to environmental changes and can serve as sentinel species for ecosystem health assessments. The Efroymson Restoration at Kankakee Sands in northwestern Indiana, USA has been restored in the past 25 yr from primarily agricultural land to a mosaic of prairie and wetland habitats. Health assessments of 40 free-ranging painted turtles (Chrysemys picta) at Kankakee Sands were performed in May 2021 to evaluate overall health status, screen for infectious diseases, and obtain baseline clinical pathology values in this population. Assessment of each turtle included a physical examination, complete blood count, plasma biochemistry panel, blood lactate level, venous blood gas analysis, serum trace mineral panel, serum vitamin D3 level, and plasma protein electrophoresis. Oral and cloacal swabs were tested for adenoviruses, herpesviruses, frog virus 3, and Mycoplasmopsis species by PCR in 39 painted turtles. Four turtles were positive for adenovirus, which shared 100% homology to Sulawesi tortoise adenovirus. Two turtles were herpesvirus-positive with 100% homology to emydid herpesvirus 1. No Mycoplasmopsis spp. or frog virus 3 was detected. Female turtles had significantly higher manganese, prealbumin, uric acid, triglycerides, and ionized calcium levels, while male turtles had significantly higher cholesterol, glutamate dehydrogenase, and CO2 levels. These baseline data can be used for future research into freshwater turtle health in restored wetland habitats.

PVA-based assessment of resiliency, redundancy, and representation in an imperiled freshwater turtle

PVA-based assessment of resiliency, redundancy, and representation in an imperiled freshwater turtle

Embryonic development, hatchling performance and metabolic profile after egg exposure to environmentally relevant levels of chlorpyrifos in an aquatic turtle

The extensive use of organophosphorus insecticides poses a threat to the survival of non-target organisms. Ecotoxicological outcomes of embryonic exposure to insecticides are rarely evaluated in various oviparous species. In this study, soft-shelled turtle (Pelodiscus sinensis) eggs were incubated in moist substrate containing different levels (0, 2, 20 and 200 μg/kg) of chlorpyrifos to investigate its toxic effects on embryonic development and survival, and hatchling physiological performance. Chlorpyrifos exposure had no significant impacts on embryonic development rate and egg survival in P. sinensis. Similarly, embryonic chlorpyrifos exposure neither obviously affected the size and locomotor performance of hatchlings, nor changed the activities of superoxide dismutase and catalase, and content of malondialdehyde in their erythrocytes. Based on liquid chromatography-mass spectrometry analysis, minor metabolic perturbations related to amino acid, lipid and energy metabolism in hatchlings after embryonic chlorpyrifos exposure were revealed by hepatic metabolite profiling. Overall, our results suggested that embryonic exposure to environmentally relevant levels of chlorpyrifos had only a limited impact on physiological performances of hatchlings, although it would result in a potential risk of hepatotoxicity in P. sinensis.

Distribution, habitat and population structure of the threatened Manning River helmeted turtle, Myuchelys purvisi

AbstractMany freshwater turtle species are threatened with extinction, but the implementation of effective conservation measures may be hindered by ignorance of their biology and ecology. We analysed the available monitoring data for a listed Endangered but poorly known species, the Manning River helmeted turtle (Myuchelys purvisi: Chelidae), to elucidate its geographic distribution and evaluate its relationships to broad‐scale environmental factors. We found M. purvisi to be common and widely distributed in the Manning River system, with a balanced population structure including a wide mix of size classes and a substantial juvenile component. The occurrence of the species was significantly positively associated with a larger stream size, which probably confers greater habitat availability and lower vulnerability to drying during drought. Mean carapace length was significantly lower in stream segments with higher average annual air temperature, suggesting that warmer conditions favour recruitment. However, occurrence and mean carapace length were not related to the proportion of conservation land in the immediate stream environs, suggesting that persistence of the species is not favoured simply by occurrence in protected areas, and threats may need active management. We provide some suggestions for further investigation of the species' ecology and vulnerability to potential threats.

Using baited remote underwater videos to survey freshwater turtles

AbstractNew and innovative techniques utilizing underwater cameras have the potential to track changes in turtle populations whilst being less invasive and time intensive than traditional trapping surveys. In this study, we trialled the use of Baited Remote Underwater Videos (BRUVs) in five upland streams to test if BRUVs could be used for abundance, size and sex estimates of freshwater turtles. We also compared BRUVs to cathedral traps and identified key considerations for future use of this method, such as whether the time of day influenced results. Our study successfully detected 83 turtles from 52 h of footage and identified all species known to occur in the study area. The deployment time did not significantly influence relative abundance. BRUVs also produced statistically similar catch per unit effort estimates to cathedral trapping techniques. No small turtles (i.e. juveniles) were detected, and difficulties with visibility, sex accuracy and carapace measurements are discussed for future BRUV use. Our study shows that BRUVs are a useful, time effective, non‐invasive technique to collect relative abundance and species richness estimates for freshwater turtles.

A NEW SPECIES OF PNEUMOATRACTIS (COSMOCERCOIDEA: ATRACTIDAE) FROM TWO SPECIES OF FRESHWATER TURTLES FROM THE BRAZILIAN AMAZON.

The monotypic genus PneumoatractisBursey, Reavill, and Greiner, 2009 was erected to allocate nematodes collected from the lungs of the freshwater turtle Podocnemis unifilis Troschel. During a helminthological survey of parasites from freshwater turtles of Tocantins and Xingu rivers, Pará State, eastern Amazon, Brazil, we found nematodes parasitizing the stomach and large intestine of Po. unifilis and Podocnemis expansa Schweigger. We assigned them to a new species of Pneumoatractis, which is described herein. Pneumoatractis gibbonsae n. sp. resembles Pneumoatractis podocnemis by the morphology of the oral opening, the position of the excretory pore, and the lanceolate shape of the spicules, but differs from it in males by having 10 pairs of caudal papillae plus 1 unpaired anterior to cloacal lip, different length of the right spicule, and short gubernaculum; it differs in females by the distances of vulva and anus from the posterior end respectively. We found the new species in a different infection site from that of the type species. Thus, this is the second species of Pneumoatractis described in Po. unifilis and the first in Po. expansa.

Alien Freshwater Turtles in Greece: Citizen Science Reveals the Hydra-Headed Issue of the Pet Turtle Trade

Citizen science is emerging as a powerful tool for the early detection of biological invasions. The exotic pet trade has been deemed as the most significant cause of establishment for reptiles, and among them, turtles have the highest number of introduction events. In Europe, at least 13 species of alien freshwater turtles have been recorded in the wild. In Greece, only two species of alien turtles have been reported, namely the American pond slider Trachemys scripta and the Florida cooter Pseudemys floridana. In this study, we provide an updated checklist of the alien freshwater turtles recorded in Greece, using citizen science, personal observations, and literature. Our results provide the first records for the country of five species, namely the Florida red-bellied cooter Pseudemys nelsoni, the Eastern river cooter Pseudemys concinna, the Chinese stripe-necked turtle Mauremys sinensis, the Chinese soft-shelled turtle Pelodiscus sinensis, and the Common snapping turtle Chelydra serpentina and new localities for T. scripta. Similar to the myth of the Lernaean Hydra (i.e., for every head chopped off, more would regrow), the pet turtle trade has been proven to have multiple heads.

Ineffectiveness of plastic mesh for protecting artificial freshwater turtle nests from red fox (Vulpes vulpes) predation

AbstractInvasive mammalian predators are efficient at driving native animal declines. The red fox (Vulpes vulpes) kills millions of endemic reptiles in Australia each year. In areas of south‐eastern Australia, the eastern long‐necked turtle (Chelodina longicollis) and Murray River turtle (Emydura macquarii) have declined by more than 50%. High rates of nest predation by foxes limit the recruitment of young turtles in these populations, but previous methods of fox control have been ineffective at protecting turtle nests. Here, we tested the effectiveness of plastic mesh for protecting artificial turtle nests from predation by foxes, in the mid‐Murray catchment, Victoria. We also tested whether protecting a large number of artificial nests in a given area encourages foxes to give up foraging following predictions from giving‐up density theory. We made a series of plots, each containing 32 artificial turtle nests. In each plot, we covered a percentage (0%, 25%, 50%, 81% or 100%) of the nests with either 1 or 2 sheets of plastic mesh. We used remote cameras to photograph and identify any predator that attacked nests in the plots. The cameras also allowed us to estimate the amount of time a fox was visible on each plot, as a metric of how much effort foxes expended on protected nests. Nest survival rate was not increased by either 1 or 2 sheets of mesh, and increasing the number of protected nests on a plot did not reveal a giving‐up density (GUD) value for fox foraging behaviour. Our study demonstrates that plastic mesh is not effective for protecting artificial turtle nests from foxes in this region.

Activity of a freshwater turtle varies across a latitudinal gradient: Implications for the success of assisted colonisation

Abstract The value of assisted colonisation as a response to climate change can only be realised if focal species are well suited to their new habitats. For ectotherms, new habitats must offer microclimates that promote crucial behaviours such as thermoregulation and foraging. The Western swamp turtle Pseudemydura umbrina, a Critically Endangered species from south‐western Australia, serves as a global case‐study of assisted colonisation in action. Initial trials where juvenile P. umbrina were released into wetter and cooler climates found that individuals spent considerable time at body temperatures that apparently limited their growth. Using high‐resolution biologging data (temperature and depth), here we tested if turtle activity is thermally constrained in cooler latitudes by releasing 48 juveniles into seasonal swamps at three sites. One site was core natural habitat, and the other sites were wetlands 380 km apart that offered either warmer or cooler microclimates. Generalised additive mixed models were used to evaluate behaviours and time spent at optimal temperatures for approximately 1 month following release, and growth rates were measured and analysed after release until the end of the hydroperiod 4–5 months later. We found that turtles released into the most poleward (southern) wetland spent significantly less time active and basking and grew significantly less compared to turtles released further north. When analysed together, behavioural and growth datasets showed that activity was positively correlated with growth rates. We conclude that poor growth of turtles in the southern wetland was likely a result of lower body temperatures, stemming from a reduced ability to thermoregulate in water. Consequently, for assisted colonisation of juvenile P. umbrina to be successful, recipient wetlands must offer aquatic microclimates that are sufficiently warm to promote foraging activity that leads to growth, and ultimately to maturation. Read the free Plain Language Summary for this article on the Journal blog.

Low coverage sequencing provides insights into the key features of the nuclear and mitochondrial genomes of the Alligator Snapping Turtle Macrochelys temminckii

The alligator snapping turtle Macrochelys temminckii is a culturally, ecologically, and evolutionary relevant species of conservation concern. In this study, we conducted a genome survey of M. temminckii. Using a low-coverage short read sequencing strategy, this study estimated the genome size, repetitive genome content, annotated and quantified repetitive elements, assembled the 45S rRNA DNA operon, and characterized in detail the mitochondrial genome of M. temminckii. Using a k-mer strategy, the estimated haploid genome size varied between 3.77 and 3.19 Gbp, which is within the range previously reported for other representatives of the family Chelydridae. Repetitive genome content estimates using different k-mers (21 to 51) indicated that more than 75 % of the genome of M. temminckii comprised repetitive elements. Taking into account only annotated repetitive elements, the most common repetitive elements were classified as Class I - Long Interspersed Nuclear Element (LINE) which were more abundant than Class I – Penelope and Class I - Long Terminal Repeat (LTR) Ty3 mobile elements. Less abundant repeat element families in the nuclear genome of M. temminckii included Class I - DIRS mobile elements and Satellite DNA. The nuclear ribosomal operon was partially assembled into three contigs, one encoding the complete ssrRNA gene, a second encoding the complete 5.8S rRNA gene, and a third comprising the full lsrRNA gene. The AT-rich complete mitochondrial genome was 16,570 bp long. These new genomic resources are of utmost importance to aid in the development of conservation plans for this iconic freshwater turtle.