Turtle Biology Research Articles

Assessing the phenology and reproductive output of loggerhead turtles in relation to climatic variables at Patara Beach, Türkiye

AbstractLoggerhead turtles (Caretta caretta), being ectothermic organisms, could be especially susceptible to climate change effects, and may exhibit climate‐related variation in their reproductive behaviours such as phenology, annual nest numbers, clutch size, hatching success, incubation period and sex ratio. This study investigated the reproductive phenology and outputs of loggerhead turtles and their relationships with climatic variables over a 5‐year period (2019–2023) at Patara Beach, Türkiye. We found significant fluctuations in atmospheric temperature, sea surface temperature and relative humidity, and that female turtle emergences on Patara Beach could temporarily adjust their phenology in response to these minor environmental changes. We highlight the importance of understanding the impacts of phenological shifts on the ability to satisfy the conditions over the nesting season that determine reproductive output. Our statistical analyses also showed that increasing sea water temperatures and atmospheric temperatures, as well as decreasing precipitation and relative humidity, had direct and/or indirect effects on the nesting phenology and reproductive output of loggerhead turtles. The findings from this study indicate that atmospheric temperature significantly affected incubation period, hatching success rate, the number of dead embryos and the number of empty eggshells. Additionally, relative humidity had a significant impact on the incubation period and the number of empty eggshells. In this context, rising temperatures led to drier nest conditions, decreased incubation periods and increased nest temperatures, resulting in higher proportions of female offspring. In conclusion, there are still gaps in our understanding of the effects of climate change on the reproductive biology of loggerhead turtles, and more studies are needed at both the Mediterranean and global scales to better understand these effects.

The tongue of the red-eared slider (Trachemys scripta elegans): morphological characterization through gross, light, scanning electron, and immunofluorescence microscopic examination

The red-eared slider (Trachemys scripta elegans) is renowned for its remarkable adaptations, yet much of its complex biology remains unknown. In this pioneering study, we utilized a combination of gross anatomy, scanning electron microscopy (SEM), light microscopy, and immunofluorescence techniques to examine the tongue’s omnivorous adaptation in this species. This research bridges a critical knowledge gap, enhancing our understanding of this intriguing reptile. Gross examination revealed a unique arrowhead-shaped tongue with a median lingual fissure and puzzle-piece-shaped tongue papillae. SEM unveiled rectangular filiform, conical, and fungiform papillae, with taste pores predominantly on the dorsal surface and mucous cells on the lateral surface of the papillae. Histologically, the tongue’s apex featured short rectangular filiform and fungiform papillae, while the body exhibited varying filiform shapes and multiple taste buds on fungiform papillae. The tongue’s root contained lymphatic tissue with numerous lymphocytes surrounding the central crypt, alongside lingual skeletal musculature, blood and lymph vessels, and Raffin corpuscles in the submucosa. The lingual striated muscle bundles had different orientations, and the lingual hyaline cartilage displayed a bluish coloration of the ground substance, along with a characteristic isogenous group of chondrocytes. Our research represents the first comprehensive application of immunofluorescence techniques to investigate the cellular intricacies of the red-eared slider’s tongue by employing seven distinct antibodies, revealing a wide array of compelling and significant findings. Vimentin revealed the presence of taste bud cells, while synaptophysin provided insights into taste bud and nerve bundle characteristics. CD34 and PDGFRα illuminated lingual stromal cells, and SOX9 and PDGFRα shed light on chondrocytes within the tongue’s cartilage. CD20 mapped B-cell lymphocyte distribution in the lingual tonsil, while alpha smooth actin (α-SMA) exposed the intricate myofibroblast and smooth muscle network surrounding the lingual blood vessels and salivary glands. In conclusion, our comprehensive study advances our knowledge of the red-eared slider’s tongue anatomy and physiology, addressing a significant research gap. These findings not only contribute to the field of turtle biology but also deepen our appreciation for the species’ remarkable adaptations in their specific ecological niches.

Assessing and Screening of Female Fertility in Artificially Bred Asian Yellow Pond Turtles (Mauremys mutica) Based on Parentage Assignment

The Asian yellow pond turtle (Mauremys mutica) is widely traded in China, and its artificial breeding has now become a major industry. However, the insufficient offspring supply and reproductive decline of farmed turtles make the wild turtles more vulnerable. The present study was mainly designed to quantify the fecundity of M. mutica and attempt to screen for good reproductive performance in females. The genetic variability of the population and its genetic structure were also analysed. The parent–offspring relationships of all offspring in four consecutive years were confirmed using sixteen microsatellite loci. The genetic variability between the parents and offspring was low, and offspring of different years also showed little variability. We summarised the reproductive results of all females and counted the annual number of offspring and the variation in the number of offspring. The females were then divided into three types (stable, undulating and levelling off) according to the continuity. We selected seven females with good reproductive ability, which provided 16.94% of the annual contributions, while there were two females that had no offspring in four years. We also analysed the possible reasons for this difference and the importance of carrying out a family survey. This research can provide the basis and materials for the creation of a good reproductive group and the study of the reproductive biology of turtles in M. mutica aquaculture.

Saving the endangered Mary River turtle: Enhancing conservation outcomes through community engagement

AbstractAustralian biodiversity is facing an extinction crisis; yet, government spending on conservation is wholly inadequate. The involvement of local communities in fundraising, direct actions, and habitat restoration is becoming vital in the fate of threatened species. Here, we review the research outputs and impact generated from 22 years of conservation‐driven collaboration between researchers and a local community focused on saving the endangered Mary River turtle (Elusor macrurus). The study found that this collaboration generated a significant body of research that advanced the ecological knowledge of the species and ensured the findings were being applied towards the conservation of the turtle, locally and nationally. While the national listing status of E. macrurus as endangered has not changed over the past 22 years, the knowledge gained about the turtle's biology and its use to better advise development and water resources in the catchment suggests that the species' future is brighter than when it was first discovered in 1994. This review demonstrates the potential of local communities in driving and supporting conservation initiatives and provides a blueprint for scientific endeavours that inform adaptive community conservation programmes for threatened species.

Characterization of 25 new microsatellite markers for the green turtle (Chelonia mydas) and cross-species amplification in other marine turtle species

The green sea turtle, Chelonia mydas, is a migratory species with a strong natal homing behavior leading to a complex population structure worldwide. The species has suffered severe declines in local populations; it is therefore crucial to understand its population dynamics and genetic structure to adopt appropriate management policies. Here, we describe the development of 25 new microsatellite markers specific to C. mydas and suitable for these analyses. They were tested on 107 specimens from French Polynesia. An average allelic diversity of 8 alleles per locus was reported and observed heterozygosity ranged from 0.187 to 0.860. Ten loci were significantly deviant from the Hardy-Weinberg equilibrium, and 16 loci showed a moderate to high level of linkage disequilibrium (4-22%). The overall Fis was positive (0.034, p-value < 0.001), and sibship analysis revealed 12 half- or full-sibling dyads, suggesting possible inbreeding in this population. Cross-amplification tests were performed on two other marine turtle species, Caretta caretta and Eretmochelys imbricata. All loci successfully amplified on these two species, though 1 to 5 loci were monomorphic. These new markers will not only be relevant for further analyses on the population structure of the green turtle and the two other species, but they will also be invaluable for parentage studies, for which a high number of polymorphic loci are necessary. This can provide important insight into male reproductive behavior and migration, an aspect of sea turtle biology that is of critical importance for the conservation of the species.

CORRIGENDUM: Biology and conservation of marine turtles in the northwestern Indian Ocean: a review

CORRIGENDUM: Biology and conservation of marine turtles in the northwestern Indian Ocean: a review

Photo‐identification confirms polyandry in loggerhead sea turtles

AbstractWhile polyandry in sea turtles is indicated through multiple‐paternity analyses of offspring, confirmed observations of the same female mating with multiple males are extremely challenging to obtain. To contribute to this discussion, we analysed a long‐term photo‐identification database (&gt;20 years) of adult male and female loggerhead sea turtles frequenting the breeding area of Zakynthos, Greece, Mediterranean. A total of 38 records of mating individuals within and across seasons were assimilated via field surveys and citizen science records between 2003 and 2020. For one female, we recorded it mating with two different males within a 5.5‐h interval on the same day in 2015. This observation constitutes the first direct evidence of polyandry in sea turtles, in addition to highlighting the potential for photo‐identification to contribute information on less well‐known aspects of sea turtle biology, such as validating outputs of genetic studies.

Biology and conservation of marine turtles in the northwestern Indian Ocean: a review

The northwestern Indian Ocean hosts globally crucial marine biodiversity, which is relatively understudied. There has, however, been significant research and conservation effort focused on marine turtles across the region in recent decades. We undertook an exhaustive review of 251 relevant publications to extract and collate the current information concerning marine turtles. To ensure completeness, we received input on a preliminary draft from a large group of experts who have worked extensively in the region. Data presented here are from all 13 countries with significant coastlines in the region (Bahrain, Djibouti, Egypt, Eritrea, Iran, Kuwait, Oman, Qatar, Saudi Arabia, Somalia, Sudan, United Arab Emirates, and Yemen) on occurrence, nesting biology, morphology, foraging areas, population status, threats, and relevant national legislation and international conservation strategies. The experts independently provided details on what they felt were the (1) most significant threats to marine turtles, (2) most critical knowledge gaps for marine turtle ecology, (3) impediments to practical conservation, and (4) essential strengths and opportunities in the region.

Comparison of UAV and Boat Surveys for Detecting Changes in Breeding Population Dynamics of Sea Turtles

Surveying the breeding population of a given species can be difficult for many logistic reasons. Marine turtles are a challenging taxon for the study of reproductive ecology and breeding strategies, because turtles aggregate off-shore and males remain exclusively at sea. For successful management of sea turtle populations, determining operational sex ratios (OSRs) on a continuing basis is critical for determining long-term population viability, particularly in the context of changing hatchling sex ratios due to temperature-dependent sex determination in a warming climate. To understand how survey technique and stage of the breeding season might influence the ability to detect turtles and determine OSRs, we surveyed the presence and identified the sex of adult male and female green sea turtles (Chelonia mydas) using a boat and small commercial unoccupied/unmanned aerial vehicle (UAV), at the start (October) and peak (December) of a nesting season at an important breeding site at Heron Island, Great Barrier Reef, Australia. The ratio of males to females within the breeding ground detected by both survey methods changed from being male-biased in October to heavily female-biased in December, indicating that most males cease their reproductive effort and depart before the peak of the nesting season. Surveying with a UAV more than doubled the rate of turtles seen per minute of survey effort compared with surveying solely from the boat and allowed surveys to be conducted at times and/or places unsafe or inaccessible for boats. The sex of a slightly greater proportion of turtles seen could not be identified by observers using a UAV versus a boat, although more turtles were detected using the UAV. The departure of many males during the peak of the nesting season is likely due to an increasing biological cost of residency in the area because males encounter fewer receptive females as the season progresses and the limited foraging opportunity is insufficient to support the number of males present. Overall, we found that UAVs are an effective tool for studying important but difficult to observe aspects of sea turtle biology.

Measuring of the effects of a sea turtle conservation education program on children's knowledge and attitudes in Grenada, West Indies

Grenada, a multi-island country in the Caribbean Sea, supports aggregates of critically endangered hawksbill turtles (Eretmochelys imbricata), endangered green turtles (Chelonia mydas) and vulnerable leatherback turtles (Dermochelys coriacea). These species play an integral role within the marine ecosystem and are important to ecotourism in Grenada. They are also negatively impacted by anthropogenic factors in Grenada such as legal and illegal hunting, habitat loss, pollution, and by-catch. Conservation educational programs represent a powerful approach for increasing public knowledge about sea turtles and engaging stakeholders to improve management of sea turtle populations. However, little data is available that quantifies the impact that these programs have on participants. A 10 day, active-learning sea turtle education program was developed for 22, nine to twelve-year old children who were selected for participation by their school principles, on the island of Carriacou, a dependency of Grenada. Knowledge and attitude changes towards sea turtle biology and conservation were quantified with pre- and post-curriculum test scores consisting of multiple-choice basic biology questions (n = 15) and Likert-scale questions (n = 16) that assessed the variables understanding and concern, locus of control, and level of verbal commitment. Student's knowledge of sea turtle biology significantly increased 12.3 percentage points, including a 16.3 percentage point increase for females (n = 11) and 7.9 for males (n = 11). Likert-scale scores demonstrated that students held and maintained a positive attitude towards sea turtle conservation. Score changes were not significant but females trended towards a more positive attitude change for each variable post-curriculum while males trended towards less positive attitudes. Possible influences driving these gender differences are discussed. Public education remains central to engaging communities in sea turtle conservation and ocean resource management efforts in the Caribbean region. Understanding the effects of conservation education programs on participant knowledge and attitudes is central to our ability to progress the curriculum and better engage communities in conservation efforts.

Effects of global warming on species with temperature-dependent sex determination: Bridging the gap between empirical research and management.

Global warming could threaten over 400 species with temperature‐dependent sex determination (TSD) worldwide, including all species of sea turtle. During embryonic development, rising temperatures might lead to the overproduction of one sex and, in turn, could bias populations’ sex ratios to an extent that threatens their persistence. If climate change predictions are correct, and biased sex ratios reduce population viability, species with TSD may go rapidly extinct unless adaptive mechanisms, whether behavioural, physiological or molecular, exist to buffer these temperature‐driven effects. Here, we summarize the discovery of the TSD phenomenon and its still elusive evolutionary significance. We then review the molecular pathways underpinning TSD in model species, along with the hormonal mechanisms that interact with temperatures to determine an individual's sex. To illustrate evolutionary mechanisms that can affect sex determination, we focus on sea turtle biology, discussing both the adaptive potential of this threatened TSD taxon, and the risks associated with conservation mismanagement.

DNA barcode analysis of the endangered green turtle (Chelonia mydas) in Mexico1.

Technological and analytical advances to study evolutionary biology, ecology, and conservation of green turtles (Chelonia mydas) are realized through molecular approaches including DNA barcoding. We characterized the usefulness of COI DNA barcodes in green turtles in Mexico to better understand genetic divergence and other genetic parameters of this species. We analyzed 63 sequences, including 25 from green turtle field specimens collected from the Gulf of Mexico and from the Mexican Pacific and 38 already present in the Barcode of Life Data Systems (BOLD). A total of 13 haplotypes were identified with four novel haplotypes from the Pacific Ocean and three novel haplotypes from the Atlantic Ocean. Intraspecific distance values among COI gene sequences by two different models were 0.01, demonstrating that there is not a subdivision for green turtle species. Otherwise, the interspecific distance interval ranged from 0.07 to 0.13, supporting a clear subdivision among all sea turtle species. Haplotype and total nucleotide diversity values of the COI gene reflect a medium genetic diversity average. Green turtles of the Mexican Pacific showed common haplotypes to some Australian and Chinese turtles, but different from the haplotypes of the Mexican Atlantic. COI analysis revealed new haplotypes and confirmed that DNA barcodes were useful for evaluation of the population diversity of green turtles in Mexico.

Advances in the Biology and Conservation of Turtles

The approximately 356 species of testudines (turtles) are remarkable for their blend of phylogenetic conservatism and diversity [...]

A Dynamic Energy Budget Model of Ornate Box Turtle Shell Growth

Many aspects of box turtle development may depend on size rather than age. Notable examples include sexual maturity and the development of the fully closing hinge in the shell that allows box turtles to completely hide in their shells. Thus, it is important to understand how turtles grow in order to have a complete understanding of turtle biology. Previous studies show that turtle shell growth behaves in a logistic manner. These studies use functional models that fit the data well but do little to explain mechanisms. In this work we use the ideas found in dynamic energy budget theory to build a model of box turtle shell growth. We show this model fits the data as well as previous models for ornate box turtles Terrapene ornata ornata, but also offers explanations for observed phenomena, such as maximum sizes and the appearance of biphasic growth.

Preserved collagen reveals species identity in archaeological marine turtle bones from Caribbean and Florida sites.

Advancements in molecular science are continually improving our knowledge of marine turtle biology and evolution. However, there are still considerable gaps in our understanding, such as past marine turtle distributions, which can benefit from advanced zooarchaeological analyses. Here, we apply collagen fingerprinting to 130 archaeological marine turtle bone samples up to approximately 2500 years old from the Caribbean and Florida's Gulf Coast for faunal identification, finding the vast majority of samples (88%) to contain preserved collagen despite deposition in the tropics. All samples can be identified to species-level with the exception of the Kemp's ridley (Lepidochelys kempii) and olive ridley (L. olivacea) turtles, which can be separated to genus level, having diverged from one another only approximately 5 Ma. Additionally, we identify a single homologous peptide that allows the separation of archaeological green turtle samples, Chelonia spp., into two distinct groups, which potentially signifies a difference in genetic stock. The majority of the archaeological samples are identified as green turtle (Chelonia spp.; 63%), with hawksbill (Eretmochelys imbricata; 17%) and ridley turtles (Lepidochelys spp.; 3%) making up smaller proportions of the assemblage. There were no molecular identifications of the loggerhead turtle (Caretta caretta) in the assemblage despite 9% of the samples being morphologically identified as such, highlighting the difficulties in relying on morphological identifications alone in archaeological remains. Finally, we present the first marine turtle molecular phylogeny using collagen (I) amino acid sequences and find our analyses match recent phylogenies based on nuclear and mitochondrial DNA. Our results highlight the advantage of using collagen fingerprinting to supplement morphological analyses of turtle bones and support the usefulness of this technique for assessing their past distributions across the Caribbean and Florida's Gulf Coast, especially in these tropical environments where DNA preservation may be poor.

Characterizing a Sea Turtle Developmental Habitat Using Landsat Observations of Surface-Pelagic Drift Communities in the Eastern Gulf of Mexico

Compared with our understanding of most aspects of sea turtle biology, knowledge of the surface-pelagic juvenile life stages remains limited. Young North Atlantic cheloniids (hard-shelled sea turtles) are closely associated with surface-pelagic drift communities (SPDCs), which are dominated by macroalgae of the genus Sargassum . We quantified SPDCs in the eastern Gulf of Mexico, a region that hosts four species of cheloniids during their surface-pelagic juvenile stage. Landsat satellite imagery was used to identify and measure the areal coverage of SPDCs in the eastern Gulf during 2003–2011 (1323 images). Although the SPDC coverage varied annually, seasonally, and spatially, SPDCs were present year-round, with an estimated mean area of SPDC in each Landsat image of 4.9 km2 (SD = 10.1). The area of SPDCs observed was inversely proportional to sea-surface wind velocity (Spearman's r = −0.33, p < 0.001). The SPDC coverage was greatest during 2005, 2009, and 2011 and least during 2004 and 2010, but the 2010 analysis was affected by the Deepwater Horizon oil spill, which occurred within the study region. In the eastern Gulf, the area of SPDC peaked during June–August of each year. Although the SPDC coverage appeared lower in the eastern Gulf than in other regions of the Gulf and the North Atlantic, surface-pelagic juvenile green, hawksbill, Kemp's ridley, and loggerhead turtles were found to be using this habitat, suggesting that eastern Gulf SPDCs provide developmental habitats that are critical to the recovery of four sea turtle species.

A full life cycle Dynamic Energy Budget (DEB) model for the green sea turtle (Chelonia mydas) fitted to data on embryonic development

The complex life history of sea turtles presents challenges for researchers. These slow-growing, long-lived reptiles occupy several habitats throughout their life cycle, including oceanic environments where they are difficult to study. Consequently, much research on sea turtle biology has focussed on the nesting environment. Yet, to effectively manage sea turtle populations, the documentation of processes such as growth, maturation and reproductive output is critical to understanding their population dynamics. Dynamic Energy Budget (DEB) theory provides a mechanistic framework for investigating such processes. Here we developed a full life cycle DEB model for a green turtle (Chelonia mydas) population from Western Australia, where the model was based primarily on data collected on the embryonic life stage. The model provided a good fit to empirical data, including the limited data on juvenile and adult growth, and suggested that it is practical to investigate full life cycle energetics based on embryonic data that are comparatively easy to collect. Maternal effects on embryonic development and patterns of energy allocation throughout the life cycle were inferred from the DEB model. This is the first DEB model developed for C. mydas, and its potential applications include demonstrating how maturation, maintenance and reproduction of wild individuals depend on food availability and temperature. Such applications are especially valuable for understanding future impacts of climate change, and how best to manage this iconic species that plays a key role in marine ecosystems across the globe.

Filling the gaps in sea turtle research and conservation in the region where it began: Latin America

The first documented long-term sea turtle research and conservation project in the world was officially launched in Latin America (Tortuguero, Costa Rica) in 1955. Despite the enormous advances in research and conservation in the nearly seven decades since, many questions still remain unanswered about fundamental aspects of ecology and population dynamics that hinder the conservation of sea turtles in the region. To catalyze further dissemination of information and improvement of sea turtle conservation, this Special Issue presents 10 papers solely focused on studies conducted in Latin America. This Special Issue resulted from an initiative launched to celebrate the 36th Annual Symposium on Sea Turtle Biology and Conservation, held in Peru in March 2016 -the first time this event was held in South America. The articles featured present novel results for four of the five species of sea turtles present in this region, with data collected as far back as 1971 and as recent as 2016. The studies cover diverse subjects including the nesting ecology for the most endangered populations of sea turtles in the world -the Eastern Pacific hawksbill turtle (Eretmochelys imbricata) and leatherback turtle (Dermochelys coriacea); the origins and connectivity of nesting and foraging populations of hawksbills and green turtles (Chelonia mydas); the detection of a new foraging ground for hawksbills in the Eastern Pacific; and the pervasive occurrence of incidental capture as well as illegal retention of sea turtles. The recovery of these imperiled marine reptiles relies on information to design and implement sound conservation actions; in this regard, the papers in this Special Issue are making a vital contribution, following the initial efforts launched nearly 70 years ago.

Advances in the Application of Genetics in Marine Turtle Biology and Conservation

Marine turtles migrate across long distances, exhibit complex life histories, and occupy habitats that are difficult to observe. These factors present substantial challenges to understanding fundamental aspects of their biology or assessing human impacts, many of which are important for the effective conservation of these threatened and endangered species. The early development and application of genetic tools made important contributions to understanding marine turtle population and evolutionary biology, such as providing evidence of regional natal homing by breeding adults, establishing connectivity between rookeries and foraging habitats, and determining phylogeography and broad scale stock structure for most marine turtle species. Recent innovations in molecular technologies, statistical methods, and creative application of genetic tools have significantly built upon this knowledge to address key questions in marine turtle biology and conservation management. Here, we evaluate the latest major advances and potential of marine turtle genetic applications, including improved resolution and large-scale syntheses of population structure, connectivity and phylogeography, estimation of key demographic rates such as age to maturity and operational or breeding sex ratios, insight into reproductive strategies and behavior, and assessment of differential human impacts among populations. We then discuss remaining challenges and emerging capabilities, such as rapid, multiplexed genotyping and investigation of the genomic underpinnings of adaptive variation afforded by high-throughput sequencing technologies.

Research and Conservation Priorities for Tortoises and Freshwater Turtles of Colombia

The objective of our study was to review and quantify the level of knowledge of the biology of tortoise and freshwater turtle species of Colombia based on studies conducted in the country. We used the resulting rankings in knowledge, in combination with IUCN threat category, presence in protected areas, and endemism, to propose conservation priorities. This process also allowed us to evaluate which aspects of turtle biology have been least studied. Four species obtained total values of zero or one over the 21 knowledge criteria employed, so they were ranked as the highest priority for research based on the lack of knowledge of their biology: Black-lined Toad-headed Turtle ( Mesoclemmys raniceps), Amazon Toad-headed Turtle ( Mesoclemmys heliostemma), Gibba Toad-headed Turtle ( Mesoclemmys gibba), and Dunn’s Mud Turtle ( Kinosternon dunni). Moreover, species in the family Chelidae in general were found to have limited levels of knowledge, which makes this group a priority for investigation. Evaluation of the distinct criteria used in the knowledge assessment revealed that the best-known criteria were geographic distribution (modeled), presence or absence in protected areas, and clutch size. The most poorly known biological characteristics, which constitute research priorities, are the frequency of nesting, longevity and generation time, and population parameters. According to the criteria used, the priority species for conservation were the Magdalena River Turtle ( Podocnemis lewyana), Dahl’s Toad-headed Turtle ( Mesoclemmys dahli), K. dunni, and Maracaibo Wood Turtle ( Rhinoclemmys diademata), three of which are endemic or semiendemic ( R. diademata only occurs in Colombia and Venezuela), followed by two species of Mesoclemmys.