Male Turtles Research Articles

Treatment of Multifocal Cutaneous Squamous Cell Carcinoma with Strontium-90 and Cryotherapy in a Midland Painted Turtle (Chrysemys picta marginata)

Abstract A 16-yr-old male midland painted turtle (Chrysemys picta marginata) presented for evaluation of a crusted cervical lesion and conjunctivitis. The patient initially underwent several treatm...

Discovery and description of a novel sexual weapon in the world’s most widely-studied freshwater turtle

Sexually coercive reproductive tactics are widespread among animals, where one sex employs specialized structures, called sexual weapons, to harass, intimidate, and/or physically force the other sex to mate. Painted turtles (Chrysemys picta) have been extremely well-studied over the last two centuries, and their mating system has been described as female choice based on male courtship display. The present study arises from observation that males seemingly have more protracted and serrated anterior marginal scutes than females. We hypothesized that the anterior carapace is sexually dimorphic, and that this morphology is a weapon used by males in coercive mating. We quantified anterior carapacial morphology using geometric morphometric analysis of digital photographs, drawing on samples of painted turtles from North American museum collections and our field site in Algonquin Provincial Park. We found that the anterior carapace of males had a significantly more serrated and projected shape compared to females, consistent with the sexual weapon hypothesis. Additionally, anterior carapacial shape was more strongly related to body size in males. Behavioural field observations strongly suggest that males use this morphology as a weapon to harm females during reproduction. The present study complements and strengthens the recent hypothesis that male painted turtles engage in coercion as an alternative reproductive tactic, questioning the long-understood paradigm of exclusive female choice in this well-studied species. Our study invites new avenues of research on the evolution of female harm in a system with extreme selection on female longevity and for which operational sex ratios vary among populations. Further, our work underlines how basic natural history observations can transform our understanding of well-studied systems.

HABITAT USE, MOVEMENT PATTERNS, AND NEST SITE SELECTION BY WESTERN POND TURTLES (ACTINEMYS MARMORATA) IN A MANAGED CENTRAL CALIFORNIA RANGELAND POND

The Western Pond Turtle (Actinemys marmorata) has been declining throughout its range due to several stressors, including habitat degradation and loss, exotic competitors, nonnative predators, and epidemic disease. California's only native turtle is listed as a Species of Special Concern and a candidate species for listing under the federal Endangered Species Act. Few studies have examined their population ecology in lentic environments subject to livestock grazing. From 2011 through 2016, staff and volunteers from the East Bay Regional Park District used radiotelemetry or tracked visually the seasonal movement patterns, habitat use, and nest site selection of Western Pond Turtles (n = 38) in eastern Contra Costa County, California. Statistical analyses of this multiple-year database showed that male and female turtles used the pond environment differently; however, they all overwintered in the same relative location. Gravid females on average moved 24.4 m (s = 17.5 m.) away from the ponds during the first 2 wk of June to oviposit on south-facing slopes (aspect = 134°, s = 31.9°), with mean residual-dry-matter levels of 1345 lbs/ac (1510 kg/ha) and vegetation heights ranging between 26.6 and 39.5 cm. These findings on how Western Pond Turtles used their pond and upland environments may have significant conservation and management implications for rangelands.

Revisiting the hypothesis of sex-biased turtle road mortality

Road mortality poses a major threat to turtle populations. Several studies have suggested that the terrestrial movements associated with nesting increase this risk for females. The Ontario Turtle Conservation Centre (OTCC) is home to the Kawartha Turtle Trauma Centre, which admits 900 or more turtles a year, with road injuries the primary cause of admission. We tested the hypothesis that road mortality in turtles is female-biased using data from injured Midland Painted Turtles (Chrysemys picta marginata), Snapping Turtles (Chelydra serpentina), Blanding’s Turtles (Emydoidea blandingii), and Northern Map Turtles (Graptemys geographica) collected over about 126 000 km2 and admitted to OTCC’s hospital from January 2013 to October 2017. There was no difference in the number of male and female admissions of Midland Painted, Blanding’s, or Snapping Turtles (P > 0.05); however, more female Northern Map Turtles than males were admitted (P < 0.001). Admission of female turtles peaked in June during the nesting season, but male admissions were more evenly distributed throughout the season. Our admissions data provide a temporally unbiased and geographically broad snapshot of turtle–vehicle interactions that can directly inform conservation and management policies. Although our data are not equivalent to mortality rates, these results demonstrate that vehicle strikes can have a substantial impact on both female and male turtles.

Evaluating Heavy Metal Contamination Effects on the Caspian Pond Turtle Health (Mauremys caspica caspica) Through Analyzing Oxidative Stress Factors

Background and aims: Antioxidant defense plays a vital part in organism protection against oxidative stress which is produced by reactive oxygen species (ROS). Oxidative stress represents a serious threat to the animals facing with heavy metals. This study was designed to analyze the habitat suitability for Caspian pond turtles, namely, Mauremys caspica in Mazandaran province by measuring lead (Hg) and mercury (Pb) tissues concentrations and heavy metals’ effects on the health status of Caspian pond turtles through quantifying the oxidative stress factors. Methods: Hg and Pb were measured in kidney and liver tissues of 20 sampled Caspian pond male turtles (treatment group) using atomic absorption spectrometry (AAS) and a Caspian pond male turtle was included in the control group. Moreover, glutathione (GSH) level, catalase (CAT), and superoxide dismutase (SOD) activities were investigated in kidney and liver tissues. Results: The mean (SD) concentration of Pb and Hg were 35.83 (4.20), and 0.604 (0.03) mg/kg for the sampled livers and also 31.01 (3.42) mg/kg and 0.316 (0.04) mg/kg for the sampled kidneys, respectively. Levels of trace elements, CAT, and SOD activities were found to be higher in the liver. Totally, GSH levels, as well as, CAT, and SOD activities were found to be higher and lower, respectively, in the control turtle as compared with the contaminated Caspian pond turtles. Trace-element levels had a positive correlation with CAT and SOD activities while having a negative association with GSH levels in contaminated Caspian pond sampled turtles. Conclusion: According to the results, it was inferred that high Hg and Pb concentrations in the turtles were due to the heavy metal contamination of their habitat in Mazandaran province. Based on the positive correlation between the heavy metal concentration of the tissue and dysfunction of oxidative stress defense markers, it can be concluded when the Caspian pond turtles are faced with heavy metal contamination risk, these markers can act as a bioindicator of their health status. No doubt, more studies are required to prove this hypothesis.

The effect of dietary carotenoid increase on painted turtle spot and stripe color.

Determination of how carotenoid-based color patches change with pigmentary access is important to understanding color patch function in animals. We performed a carotenoid addition experiment on male painted turtles (Chrysemys picta) to determine if an increase in dietary carotenoids led to location-specific changes in painted turtle spot and stripe color. Turtles fed large quantities of carotenoids had increased yellow chroma in chin stripes and increased red chroma in the neck and carapace stripes, as well as reduced ultraviolet (UV) chroma in the neck (orange to the human eye) and fore -limb (red to the human eye) stripes. Turtles fed large quantities of carotenoid had reduced brightness (B1) in the hind-limb stripes (red to the human eye) as well as reduced red and UV chroma in the post orbital spot of turtles (yellow to the human eye) compared to turtles fed moderate amounts of carotenoid. These results imply that integumentary spot and stripe colors are dependent upon carotenoid access, and increased lutein access leads to increased yellow and red chroma, as well as reduced ultra-violet chroma and brightness in male painted turtles. These results are discussed with respect to dietary access to carotenoids and color in other model systems, and the possibility that spot and stripe color functions as a visual signal.

Evaluating outcomes of long-term satellite tag attachment on leatherback sea turtles

Attachment methods for satellite tags deployed on marine animals must optimize data collection and minimize potential adverse effects on the study subjects. The smooth, oily carapace of the leatherback turtle contrasts with the keratinized scutes of other sea turtles and has required the development of novel approaches to tag attachment. Early leatherback satellite tracking work focused on non-invasive methods, namely the use of custom-fitted harnesses, which have now largely been replaced by the direct attachment of tags to the carapace. The present study represents the first long-term assessment of satellite tag retention, recovery, and attachment site condition for leatherback sea turtles. We compare outcomes for female, male, and sub-adult turtles tagged using both harness (n = 43) and direct attachment methods (n = 43) in a foraging area off Nova Scotia, Canada. We demonstrate that the typical operational lifespan of harness-attached tags (median 227 days) was similar to that of directly-attached tags (median 235 days). However, harness tags may be more likely to be lost at high latitudes than directly-attached tags. Mating interactions may be a primary source of tag loss for female leatherbacks because, irrespective of tag attachment method, tracking data suggest that females are more likely to lose their tags at low latitudes than either males or sub-adult turtles. High re-encounter rates (~ 50%) on nesting beaches after tagging in Canadian waters indicate that both female turtles with harness tags and directly-attached tags continue to nest successfully, many in the first nesting season following tagging. Differences in tag attachment methodologies did not appear to affect turtle survival or nesting success; however, follow-up examinations suggested divergence in the scale of impact to contact tissue. Direct attachment was characterized as a benign tagging method, as associated impacts were typically superficial, limited to the footprint of the tag itself, and nearly imperceptible following tag loss. This stands in contrast to harness tags, which have been characterized by impact to multiple body parts in contact with harness materials and potential long-term or permanent disfigurement and/or scarring of the body. Moving forward, we encourage all wildlife telemetry practitioners to continue to optimize tag characteristics and attachment methods to improve animal welfare.

Sex-biased seasonal capture rates in Painted Turtle (<i>Chrysemys picta</i>)

We examined captures of Painted Turtle (Chrysemys picta) in Algonquin Provincial Park, Ontario, Canada, during the understudied summer–autumn transition period (August–September). The proportion of captured male turtles increased relative to the proportion of females during the late summer and early autumn sampling period, leading to male-biased capture rates in a population with a strongly female-biased sex ratio. We consider explanations for the capture bias in relation to sex-specific activity patterns and briefly discuss the implications of sampling period on the outcome of population structure studies.

Prevalence of polygyny in a critically endangered marine turtle population

Genetic analyses of nuclear DNA (e.g., microsatellites) are a primary tool for investigating mating systems in reptiles, particularly marine turtles. Whereas studies over the past two decades have demonstrated that polyandry (i.e., females mating with multiple males) is common in marine turtles, polygyny (i.e., males mating with multiple females) has rarely been reported. In this study we investigated the mating structure of Critically Endangered hawksbill turtles (Eretmochelys imbricata) at Bahía de Jiquilisco in El Salvador, one of the largest rookeries in the eastern Pacific Ocean. We collected genetic samples from 34 nesting females and hatchlings from 41 clutches during the 2015 nesting season, including one nest from each of 27 females and two nests from seven additional females. Using six highly polymorphic microsatellite loci, we reconstructed the paternal genotypes for 22 known male turtles and discovered that seven (31.8%) sired nests from multiple females, which represents the highest polygyny level reported to date for marine turtles and suggests that this is a common mating structure for this population. We also detected multiple paternity in four (11.8%) clutches from the 34 females analyzed, confirming polyandrous mating strategies are also employed. The high level of polygyny we documented suggests there may be a limited number of sexually mature males at Bahía de Jiquilisco; a scenario supported by multiple lines of empirical evidence. Our findings highlight key management uncertainties, including whether polygynous mating strategies can compensate for potential ongoing feminization and the low number of adult males found for this and possibly other marine turtle populations.

Intimate Navigations, Refracted Perspectives

Intimate Navigations, Refracted Perspectives

Gonadal and extragonadal sperm reserves in the African sideneck Turtle (Pelusios castaneus)

Introduction: The African sideneck turtle (Pelusios castaneus), a freshwater turtle found in sub-Saharan Africa, recently became the focus of a number of biomedical research apart from its numerous trado-medical uses and very little consumption as meat in some quarters. This study was designed to investigate the gonadal and extragonadal sperm reserves of the African sideneck turtle, thereby generating data useful in the improved breeding of the animal. Methods: The gonadal and extragonadal sperm reserves of the African sideneck turtle were investigated using twenty adult male African sideneck turtles. Following anaesthesia and turtle dissection, the testis and epididymis were harvested and spermiogram investigated using standard techniques. Results: The mean testicular (gonadal) spermatozoa concentration of the P. castaneus was 48.50 ± 2.13 x 106/ ml, accounting for 27.5% of the total spermatozoa reserves, while that of the epididymis (extragonadal) was 127.61 ± 12.28 x 106/ml being 72.5% of the total sperm reserves with a significant difference (p < 0.05). The mean distribution of spermatozoa in the proximal, mid and posterior regions of the epididymis were 35.17 ± 8.23 x 106 /ml, 38.38 ± 5.85 x 106/ml and 54.06 ± 7.39 x 106/ml respectively, representing 27.56%, 30.01% and 42.36% respectively, of the total extragonadal sperm reserves of the P. castaneus. Significance: This report, being the first of its kind in this turtle, provides baseline data essential for a more productive selection of male turtles for breeding purposes as well as effective utilization of the sperm resources of the P. castaneus.

Assessing potential limitations when characterising the epibiota of marine megafauna: Effect of gender, sampling location, and inter-annual variation on the epibiont communities of olive ridley sea turtles

The epibionts of marine megafauna can serve as valuable indicators of the host's health or behaviour; however, only a few studies have attempted to determine how and why epibiont communities vary between host individuals, populations, or even species. Further complicating efforts to compare epibiont communities of marine megafaunas is that measures of epibiont abundance and diversity may be influenced by the sampling methods and timing of the assessment. Here, we examined how host gender, geographic location, and sampling year affect measures of epibiont community structure in olive ridley sea turtles, Lepidochelys olivacea, in the East Pacific Ocean. To achieve this, we identified, enumerated, and then statistically compared the epibiont communities of (1) nesting female turtles sampled over different nesting seasons, (2) female turtles sampled on nesting beaches and at sea, and (3) female and male turtles, both sampled at sea. We did not discover statistically significant differences between the epibiont communities of nesting female turtles sampled on different years nor between females sampled on nesting beaches and at sea. However, we did observe a statistically significant difference between the epibiont communities of female and male turtles. Thus, we conclude that while sampling epibionts from nesting sea turtles may be an accurately and more logistically straight-forward method than sampling turtle at sea, it should not be assumed that epibiont communities of male and female hosts are identical. We also suggest that knowledge of the factors that drive intra-specific variation in the epibiont communities of marine megafauna, be it biological or methodological factors, is necessary before broader-scale meta-analyses are made to determine spatial and temporal patterns in the distribution of epibiont communities worldwide.

Genetic fingerprinting reveals natal origins of male leatherback turtles encountered in the Atlantic Ocean and Mediterranean Sea

Understanding population dynamics in broadly distributed marine species with cryptic life history stages is challenging. Information on the population dynamics of sea turtles tends to be biased toward females, due to their accessibility for study on nesting beaches. Males are encountered only at sea; there is little information about their migratory routes, residence areas, foraging zones, and population boundaries. In particular, male leatherbacks (Dermochelys coriacea) are quite elusive; little is known about adult and juvenile male distribution or behavior. The at-sea distribution of male turtles from different breeding populations is not known. Here, 122 captured or stranded male leatherback turtles from the USA, Turkey, France, and Canada (collected 1997–2012) were assigned to one of nine Atlantic basin populations using genetic analysis with microsatellite DNA markers. We found that all turtles originated from western Atlantic nesting beaches (Trinidad 55%, French Guiana 31%, and Costa Rica 14%). Although genetic data for other Atlantic nesting populations were represented in the assignment analysis (St. Croix, Brazil, Florida, and Africa (west and south), none of the male leatherbacks included in this study were shown to originate from these populations. This was an unexpected result based on estimated source population sizes. One stranded turtle from Turkey was assigned to French Guiana, while others that were stranded in France were from Trinidad or French Guiana breeding populations. For 12 male leatherbacks in our dataset, natal origins determined from the genetic assignment tests were compared to published satellite and flipper tag information to provide evidence of natal homing for male leatherbacks, which corroborated our genetic findings. Our focused study on male leatherback natal origins provides information not previously known for this cryptic, but essential component of the breeding population. This method should provide a guideline for future studies, with the ultimate goal of improving management and conservation strategies for threatened and endangered species by taking the male component of the breeding population into account.

Direct Observation of Mating Behavior Involving One Female and Two Male Loggerhead Turtles in the Wild

Abstract: In March 2015, we observed mating behavior of loggerhead turtles in the western coastal waters of Okinawa Island, Japan. Two males and one female were initially involved, of which one of the males (M1) was attempting to mount the other male (M2) that had already mounted the female. Shortly after the onset of observation, M1 dismounted from M2 and swam away. At that time, the female, initially seemingly resisting copulation with M2, became receptive. This is the first report of loggerhead turtle mating behavior that involves more than two individuals. This observation suggests that the mating season of loggerheads around Okinawa Island includes the early spring.

Comparison of biological indices and nutritional composition of male Chinese soft-shelled turtle, Trionyx sinensis , reared in a greenhouse and eco-pond for Chinese mitten crab, Eriocheir sinensis

Comparison of biological indices and nutritional composition of male Chinese soft-shelled turtle, <i>Trionyx sinensis</i> , reared in a greenhouse and eco-pond for Chinese mitten crab, <i>Eriocheir sinensis</i>

Polyandrous behavior in an overexploited giant South American turtle (Podocnemis expansa) population in Central Amazon, Brazil.

The aim of the present study was to investigate the reproductive behavior of the giant Amazon River turtle (Podocnemis expansa) in the Amazon. This was carried out by estimating the degree of polymorphism in five DNA microsatellites in a sample of 359 hatchlings from 12 nests in the Mamirauá Sustainable Development Reserve in the municipality of Tefé, state of Amazonas, Brazil. An analysis of allele frequency and variation in the five microsatellite loci allowed for determination of multiple paternity in all nests sampled. Contributions of at least four male turtles to one nest, three male turtles to six nests, and two male turtles to five nests were identified. Knowledge on the reproductive behavior of P. expansa can assist in the establishment of management and conservation strategies for the population in the Mamirauá Reserve.

Dissemination of Zoonotic Antibiotic Resistant Serotypes of Salmonella by Caspian Pond Turtles, Golestan and Mazandaran Provinces, Iran

Background: Salmonella spp. are widespread zoonotic pathogens with economic importance for both humans and animals. They are categorized as the natural flora of the gastrointestinal tract of many reptiles. Human salmonellosis acquired from contact with reptiles is a well-recognized medical problem. Objective: The frequency of Salmonella contamination in Caspian pond turtles was surveyed to evaluate the danger of exposure or disease risk for humans as these species are abundant around the villages in Golestan and Mazandaran provinces. Materials and Methods: One hundred fifty fecal samples from Caspian pond turtles were tested by standard bacteriological methods and positive samples were serotyped. Antimicrobial susceptibility tests on isolated Salmonella strains were also performed. Results: Out of 150 samples, 54 turtles were detected to be contaminated with Salmonella. Of the 54 Salmonella isolates, 38.8% (21/54) were serotyped as S. typhimurium; 35.1% (19/54) as S. enterica subsp. enterica; 9.2% (5/54) as S. enterica subsp. salamae; 9.2% (5/54) as S. enterica subsp. arizona; and 7.4% (4/54) as S. enterica subsp. houtenae. Female (28/80, 35%) and male (26/74, 35.1%) turtles showed equal incidence of Salmonella spp. contamination. Resistance was mostly observed against ampicillin (37%) followed by tetracycline (33.3%), nalidixic acid (7.4%), ciprofloxacin (5.5%), and cotrimoxazole (3.7%). The highest susceptibility was observed against gentamicin (100%) and trimethoprim (98.1%). Conclusion: Our findings confirmed that people who are in close exposure to Caspian pond turtles and their feces are at the risk of Salmonella contamination. Accordingly, fundamental principles of hygiene should be applied in human contact with Caspian pond turtles. Furthermore, people should be educated about the Salmonella contamination which may occur through Caspian pond turtles.

Genetic markers provide insight on origins of immature green turtles Chelonia mydas with biased sex ratios at foraging grounds in Sabah, Malaysia

An understanding of population dynamics is needed to assess the viability of migra- tory species. Monitoring of marine turtles at foraging grounds may detect changes in population trends that would take decades to be seen at nesting beaches. Mixed Stock Analysis using molec- ular markers provides a tool for estimating the origin of turtles sampled at foraging grounds. Here, we analysed mitochondrial DNA sequences of 90 immature green turtles at 2 foraging grounds in northwestern Sabah, Malaysia. We used data from 30 Indo-Pacific green turtle rookeries as the baseline for tracing the origin of turtles at the 2 foraging grounds. The inferred origins of turtles at the 2 locations were not different and indicated that the majority originated from 3 major popula- tions in Southeast Asia, the Turtle Islands of Sarawak in northwestern Borneo (29%), the Turtle Islands Heritage Protected Area (TIHPA) (28%) and Peninsular Malaysia (25%). Previous analy- ses indicated a 1:4 female-biased sex ratio at the foraging grounds, and based on our results, this largely reflects the use of unshaded beach hatcheries at some of the source rookeries for decades, which resulted in mostly female hatchlings. This result is supported by differences in the origins of male and female turtles. The result suggests a greater proportion of males originating from Peninsular Malaysia and fewer males originating from Sarawak and possibly the TIHPA com- pared to females. We discuss the implications of hatchery practices that influence sex ratios of hatchlings and recommend future research to improve the management of marine turtles in the region.

Histochemical and immunohistochemical studies of the gonads and paramesonephric ducts of male and female hatchlings of loggerhead sea turtles (Caretta caretta)

The sex of neonatal sea turtles is difficult to determine, because neonates lack heteromorphic sex chromosomes and dimorphic external characteristics; internal dimorphic morphology is defined at hatching. We used histochemical staining and made measurements in the gonads and paramesonephric ducts (PD) of both sexes to determine structural differences in female and male loggerhead sea turtle (Caretta caretta) hatchlings. We detected differences in the gonads and PD between the sexes including the amounts of mucopolysaccharides, collagen and elastic fibers. We determined that the thickness of the gonadal cortex and the diameter of the PD lumen are reliable sex-specific characteristics. We also assessed immunolocalization of aromatase, an enzyme complex that converts androgens to estrogens, and found differences in the localization and intensity of aromatase immunostaining in the gonads and PD of female and male hatchlings. Comprehensive studies of the sexual differences of sea turtles are important for conservation programs.

Golf courses as habitat for aquatic turtles in urbanized landscapes

Golf courses host some of the only semi-natural aquatic habitats in urban areas. We assessed whether golf course wetlands could provide habitat refuges for freshwater turtles, which are threatened worldwide by wetland loss and degradation associated with urbanization. In 2009 and 2010 we examined populations of snapping turtles (Chelydra serpentina) and painted turtles (Chrysemys picta) and their habitats in 88 wetlands near Syracuse, New York, USA in golf courses, urban areas, and wildlife refuges. We tested two null hypotheses: (1) golf courses provide habitats comparable to nearby urban and protected areas, and (2) turtle populations in these contexts are comparable. Golf course wetlands were surrounded by low road density and were distinct from protected area wetlands only in that they were surrounded by less forest and grassland and had more homogenous aquatic plant communities. In terms of turtle populations, relative abundance was equivalent in protected area and golf course wetlands and female fraction was closer to parity in golf course wetlands. Painted turtles were of similar size across contexts and snapping turtles were smaller in urban and golf course contexts. Additionally, male turtles in golf courses were relatively heavier and both species had less severe indicators of poor health. Golf course wetlands apparently supported viable turtle populations similar to those observed in protected areas in the region. Nevertheless, turtle habitat on golf courses can be improved by increasing the area of wetlands, increasing their shape complexity, promoting vegetative diversity in and around wetlands, and increasing surrounding forest and grassland.