Eighteen years of saturation tagging data reveal a significant increase in nesting hawksbill sea turtles (Eretmochelys imbricata) on Long Island, Antigua

Hawksbill sea turtle Eretmochelys imbricata nesting on Long Island, Antigua, West Indies (also known as Jumby Bay) has been monitored since 1987. Although the numbers of nesting females remained relatively constant for the first 11 survey seasons (1987–1997), inclusion of more recent data (1998–2004) in the analysis reveals a statistically significant upward trend. In particular, neophytes have shown a significant upturn in numbers, whereas the remigrant subpopulation has remained stationary. This indicates that recruitment is driving the upward trend in the total number of nesters. Predictive models based on the Poisson distribution suggest that the neophyte subpopulation will continue to grow in size by an average of 10% per annum. Model-based predictions and their limitations are discussed. The Jumby Bay Hawksbill Project, which has monitored and protected nesting hawksbills and their eggs since the project's onset, is one among several factors that may contribute to the recent increase in nesting females.     

Extensive hybridization in hawksbill turtles (Eretmochelys imbricata) nesting in Brazil revealed by mtDNA analyses

Bahia state hosts over 90% of hawksbill (Eretmochelys imbricata) nests registered in the main nesting sites monitored by Projeto Tamar-IBAMA in Brazil. The genetic diversity of this hawksbill population (n=119) was assayed through the analyses of 752 bp of the mitochondrial DNA control region in nesting females. Seven distinct haplotypes, defined by 125 polymorphic sites, were found. Most of the individuals (n=67) display four typical hawksbill haplotypes, 50 individuals display two haplotypes characteristic of the loggerhead turtle (Caretta caretta) and two individuals had a haplotype affiliated with the olive ridley (Lepidochelys olivacea). These results demonstrate hybridization between the hawksbills and two species that nest along the Bahia coast. Of special interest is the high occurrence of loggerhead × hawksbill hybrids (42%), which display loggerhead mtDNA haplotypes but are characterized morphologically as hawksbills. The true hawksbill haplotypes present only three variable sites and low genetic diversity values (h=0.358±0.069; π=0.0005±0.0001). The occurrence of several nesting individuals with identical mtDNA from another species may also suggest a long history of introgression between species producing likely F2 or further generation hybrids. Marine turtle hybrids have been previously reported, but the high frequency observed in Bahia is unprecedented. Such introgression may influence evolutionary pathways for all three species, or may introduce novel morphotypes that develop apart from the parental species. The presence of a unique hybrid swarm has profound conservation implications and will significantly influence the development and implementation of appropriate management strategies for these species.     

Multiple paternity in egg clutches of hawksbill turtles (Eretmochelys imbricata)

We present the first data collected on the genetic mating system of the hawksbill turtle Eretmochelys imbricata, the only marine turtle not studied to date. We examined paternity within 12 egg clutches from ten female hawksbill turtles from Sabah Turtle Islands, Malaysia. A total of 375 hatchlings were analysed using five microsatellite markers. Results demonstrated that clutches from two out of ten females were sired by multiple males (maximum of two). Although at a low frequency, observation of multiple paternity indicates that hawksbill turtles exhibit the same genetic mating system (polyandry) as observed for other species of marine turtles. Consistent paternity across multiple clutches laid by individual females in one breeding season supports the hypothesis that sperm are stored from mating prior to nesting and are then used to fertilize all subsequent clutches of eggs that season.     

Diving behavior of immature hawksbill turtles (Eretmochelys imbricata) in a caribbean reef habitat

 Time-depth recorders were deployed on immature hawksbill turtles at the southwestern reefs of Mona Island, Puerto Rico, to examine patterns of diving behavior. Diving profiles of 10–12 day duration were obtained from five turtles ranging in carapace length from 27–52 cm. Turtles exhibited contrasting diurnal and nocturnal diving behaviors. During daylight hours, dives were made 92% of the time, featured continuous depth variation and were attributed to foraging activity. Foraging dive duration increased with turtle size; individual mean dive durations ranged from 19–26 min; mean post-dive surface intervals ranged from 37–64 s; mean depths ranged from 8–10 m. At night, dives were made 86% of the time to constant depths and were interpreted as resting behavior. Resting dive durations were not dependent on turtle size; individual mean dive durations ranged from 35–47 min; mean post-dive surface intervals ranged from 36–60 s; and mean depths from 7–10 m. Immature hawksbill turtles maintained short term home ranges several hundred meters in extension. Accepted: 2 July 1996     

Mixed-stock analysis reveals the migrations of juvenile hawksbill turtles (Eretmochelys imbricata) in the Caribbean Sea

Hawksbill turtles (Eretmochelys imbricata) migrate between nesting beaches and feeding habitats that are often associated with tropical reefs, but it is uncertain which nesting colonies supply which feeding habitats. To address this gap in hawksbill biology, we compile previously published and new mitochondrial DNA (mtDNA) haplotype data for 10 nesting colonies (N = 347) in the western Atlantic and compare these profiles to four feeding populations and four previously published feeding samples (N = 626). Nesting colonies differ significantly in mtDNA haplotype frequencies (Phi(ST) = 0.588, P < 0.001), corroborating earlier conclusions of nesting site fidelity and setting the stage for mixed-stock analysis. Feeding aggregations show lower but significant structure (Phi(ST) = 0.089, P < 0.001), indicating that foraging populations are not homogenous across the Caribbean Sea. Bayesian mixed-stock estimates of the origins of juveniles in foraging areas show a highly significant, but shallow, correlation with nesting population size (r = 0.378, P = 0.004), supporting the premise that larger rookeries contribute more juveniles to feeding areas. A significant correlation between the estimated contribution and geographical distance from nesting areas (r = -0.394, P = 0.003) demonstrates the influence of proximity on recruitment to feeding areas. The influence of oceanic currents is illustrated by pelagic stage juveniles stranded in Texas, which are assigned primarily (93%) to the upstream rookery in Yucatan. One juvenile had a haplotype previously identified only in the eastern Atlantic, invoking rare trans-oceanic migrations. The mixed-stock analysis demonstrates that harvests in feeding habitats will impact nesting colonies throughout the region, with the greatest detriment to nearby nesting populations.     

Diving behavior and movements of juvenile hawksbill turtles Eretmochelys imbricata on a Caribbean coral reef

As historically abundant spongivores, hawksbill turtles Eretmochelys imbricata likely played a key ecological role on coral reefs. However, coral reefs are now experiencing global declines and many hawksbill populations are critically reduced. For endangered species, tracking movement has been recognized as fundamental to management. Since movements in marine vertebrates encompass three dimensions, evaluation of diving behavior and range is required to characterize marine turtle habitat. In this study, habitat use of hawksbill turtles on a Caribbean coral reef was elucidated by quantifying diel depth utilization and movements in relation to the boundaries of marine protected areas. Time depth recorders (TDRs) and ultrasonic tags were deployed on 21 Cayman Islands hawksbills, ranging in size from 26.4 to 58.4 cm straight carapace length. Study animals displayed pronounced diel patterns of diurnal activity and nocturnal resting, where diurnal dives were significantly shorter, deeper, and more active. Mean diurnal dive depth (±SD) was 8 ± 5 m, range 2–20 m, mean nocturnal dive depth was 5 ± 5 m, range 1–14 m, and maximum diurnal dive depth was 43 ± 27 m, range 7–91 m. Larger individuals performed significantly longer dives. Body mass was significantly correlated with mean dive depth for nocturnal but not diurnal dives. However, maximum diurnal dive depth was significantly correlated with body mass, suggesting partitioning of vertical habitat by size. Thus, variable dive capacity may reduce intraspecific competition and provide resistance to degradation in shallow habitats. Larger hawksbills may also represent important predators on deep reefs, creating a broad ecological footprint over a range of depths. Communicated by Biology Editor Dr Mark McCormick     

mtDNA variation of the critically endangered hawksbill turtle (Eretmochelys imbricata) nesting on Iranian islands of the Persian Gulf

Genetic diversity of sea turtles (hawksbill turtle) was studied using sequencing of mitochondrial DNA (mtDNA, D-loop region). Thirty dead embryos were collected from the Kish and Qeshm Islands in the Persian Gulf. Analysis of sequence variation over 890 bp of the mtDNA control region revealed five haplotypes among 30 individuals. This is the first time that Iranian haplotypes have been recorded. Nucleotide and haplotype diversity was 0.77 and 0.001 for Qeshm Island and 0.64 and 0.002 for Kish Island, respectively. Total haplotype diversity was calculated as 0.69, which demonstrates low genetic diversity in this area. The data also indicated very high rates of migration between the populations of these two islands. A comparison of our data with data from previous studies downloaded from a gene bank showed that turtles of the Persian Gulf migrated from the Pacific and the Sea of Oman into this area. On the other hand, evidence of migration from populations to the West was not found.     

Antigua revisited: the impact of climate change on sand and nest temperatures at a hawksbill turtle (Eretmochelys imbricata) nesting beach

Whether a turtle embryo develops into a male or a female depends, as with many other reptiles, on the temperature during incubation of the eggs. With sea turtles, warm temperatures produce 100% females. Therefore, global warming has the potential to drastically alter their sex ratios. Air temperatures on Antigua have increased by 0.7°C over the last 35 years. Measurements in both the sand and the clutches laid by hawksbill turtles (Eretmochelys imbricata) at Pasture Bay, Antigua, show that for important parts of the nesting season temperatures are already above the level producing 50% of each sex (pivotal level). Comparisons are made to sand temperature measurements taken on this beach in 1989 and 1990. It is estimated that fewer males were produced in 2003 than in the previous years. Recommendations are made for close monitoring of the fertility of eggs and for research on any turtles nesting at cooler times of year.     

Interplay between plasma hormone profiles, sex and body condition in immature hawksbill turtles (Eretmochelys imbricata) subjected to a capture stress protocol

We investigated plasma hormone profiles of corticosterone and testosterone in immature hawksbill turtles (Eretmochelys imbricata) in response to a capture stress protocol. Further, we examined whether sex and body condition were covariates associated with variation in the adrenocortical response of immature turtles. Hawksbill turtles responded to the capture stress protocol by significantly increasing plasma levels of corticosterone over a 5 h period. There was no significant sex difference in the corticosterone stress response of immature turtles. Plasma testosterone profiles, while significantly different between the sexes, did not exhibit a significant change during the 5 h capture stress protocol. An index of body condition was not significantly associated with a turtle's capacity to produce plasma corticosterone both prior to and during exposure to the capture stress protocol. In summary, while immature hawksbill turtles exhibited an adrenocortical response to a capture stress protocol, neither their sex nor body condition was responsible for variation in endocrine responses. This lack of interaction between the adrenocortical response and these internal factors suggests that the inactive reproductive- and the current energetic- status of these immature turtles are important factors that could influence plasma hormone profiles during stress.     

Efficient establishment of primary fibroblast cultures from the hawksbill sea turtle (Eretmochelys imbricata)

The hawksbill sea turtle (Eretmochelys imbricata) is a critically endangered species at a risk of extinction. Preservation of the genomic and cellular information of endangered animals is important for future genetic and biological studies. Here, we report the efficient establishment of primary fibroblast cultures from skin tissue of the hawksbill sea turtle. We succeeded in establishing 19 primary cultures from 20 hawksbill sea turtle individuals (a success rate of 95%). These cells exhibited a fibroblast-like morphology and grew optimally at a temperature of 26°C, but experienced a loss of viability when cultured at 37°C. Chromosomal analysis using the primary cells derived here revealed that hawksbill sea turtles have a 2n?=?56 karyotype. Furthermore, we showed that our primary cell cultures are free of several fish-related viruses, and this finding is important for preservation purposes. To our knowledge, this report is the first to describe primary cell cultures established from normal tissues of the hawksbill sea turtle. The results will contribute to the preservation of biodiversity, especially for the sea turtles that are critically endangered owing to human activities.     

Isolation and characterization of novel microsatellites from the critically endangered hawksbill sea turtle (Eretmochelys imbricata)

We isolated and characterized 12 microsatellite loci from the hawksbill sea turtle (Eretmochelys imbricata). The loci exhibited a variable number of alleles that ranged from three to 14 with an average observed heterozygosity of 0.70 (SD 0.18) across 40 hawksbill turtles from the Caribbean. The polymorphism exhibited individually and in combination makes them suitable for fine-scale genetic studies. In particular, the low probability of identity and high paternity exclusion of these markers makes them highly useful for parentage and relatedness studies. These new markers greatly increase the power of genetic studies directed towards the conservation of this endangered species.     

Genetic variation,multiple paternity,and measures of reproductive success in the critically endangered hawksbill turtle (Eretmochelys imbricata)

The Yucatán Peninsula in Mexico contains some of the largest breeding groups of the globally distributed and critically endangered hawksbill turtle (Eretmochelys imbricata). An improved understanding of the breeding system of this species and how its genetic variation is structured among nesting areas is required before the threats to its survival can be properly evaluated. Here, we genotype 1195 hatchlings and 41 nesting females at 12 microsatellite loci to assess levels of multiple paternity, genetic variation and whether individual levels of homozygosity are associated with reproductive success. Of the 50 clutches analyzed, only 6% have multiple paternity. The distribution of pairwise relatedness among nesting localities (rookeries) was not random with elevated within‐rookery relatedness, and declining relatedness with geographic distance indicating some natal philopatry. Although there was no strong evidence that particular rookeries had lost allelic variation via drift, younger turtles had significantly lower levels of genetic variation than older turtles, suggesting some loss of genetic variation. At present there is no indication that levels of genetic variation are associated with measures of reproductive success such as clutch size, hatching success, and frequency of infertile eggs.     

A survey of the epibiota of Eretmochelys imbricata (Testudines: Cheloniidae) of Mona Island, Puerto Rico

Epibiotic organisms inhabiting non-nesting hawksbill sea turtles, Eretmochelys imbricata (Linnaeus, 1766), are described from Mona and Monito Islands, Puerto Rico. Epibiont samples from 105 turtles of shallow (< 40 m) water foraging habitats were collected and identified to the lowest possible taxon. This epibiotic assemblage consisting of at least 4 algal functional groups and 12 animal phyla represents the greatest phylogenetic diversity for marine turtle epibiota. Six groups are considered new reports for marine turtles. Most epibiont colonization was found on posterior marginal scutes and under overlapping scutes. Ecological attributes of epibiota and their symbiosis with E. imbricata provide a tool to understand basi and epibiont populations.     

Testing models of female reproductive migratory behaviour and population structure in the Caribbean hawksbill turtle, Eretmochelys imbricata, with mtDNA sequences

Information on the reproductive behaviour and population structure of female hawksbill turtles, Eretmochelys imbricata , is necessary to define conservation priorities for this highly endangered species. Two hypotheses to explain female nest site choice, natal homing and social facilitation, were tested by analyzing mtDNA control region sequences of 103 individuals from seven nesting colonies in the Caribbean and western Atlantic. Under the social facilitation model, newly mature females follow older females to a nesting location, and subsequently use this site for future nesting. This model generates an expectation that female lineages will be homogenized among regional nesting colonies. Contrary to expectations of the social facilitation model, mtDNA lineages were highly structured among western Atlantic nesting colonies. These analyses identified at least 6 female breeding stocks in the Caribbean and western Atlantic and support a natal homing model for recruitment of breeding females. Reproductive populations are effectively isolated over ecological time scales, and recovery plans for this species should include protection at the level of individual nesting colonies.     

Population subdivision in hawksbill turtles nesting on Barbados, West Indies, determined from mitochondrial DNA control region sequences

A new mitochondrial DNA control region survey of the Barbados hawksbill nesting population was undertaken using larger sample sizes, reanalysis of previously reported samples, and new primers that increase the fragment length sequenced. This work revealed that haplotypes originally identified as endemic to Barbados were misread sequences. Genetic variants and a geographic subdivision on a finer scale than has previously been recorded for sea turtles were identified between the Barbados leeward and windward coasts, indicating the need for sampling at multiple sites to reveal comprehensive genetic variation at national scales. Using the updated haplotype profiles to re-estimate Barbados’ contribution to Caribbean hawksbill foraging grounds indicated a presence several-fold larger than previously calculated; a result congruent with the breeding population being one of the largest in the region.     

Plesiochorus irwinorum n. sp. (Trematoda: Gorgoderidae) from the urinary bladder of the hawksbill turtle,Eretmochelys imbricata (Testudines: Cheloniidae), off the east coast of Australia

Plesiochorus Looss, 1901 is a genus of Gorgoderidae infecting the urinary bladders of marine turtles globally. Currently, just two morphologically similar species are recognised, Plesiochorus cymbiformis (Rudolphi, 1819) Looss, 1901 and Plesiochorus elongatus Pigulevsky, 1953, which have been distinguished by molecular data and subtle morphological differences. Here we describe a new species, Plesiochorus irwinorum n. sp., infecting hawksbill turtles (Eretmochelys imbricata (L.)), which is primarily distinguished from the other two species of Plesiochorus on the basis of ITS2, cox1 and 28S sequence data. Morphometric data for specimens examined during this study overlap between P. cymbiformis and P. irwinorum n. sp. for every measured feature, rendering them functionally cryptic. However, principal components analysis clearly distinguishes the two species. Additionally, we report new specimens of P. cymbiformis, and provide new sequence data for specimens from Australian loggerhead (Caretta caretta (L.)) and hawksbill turtles. There is little understanding of the host-specificity or geographical distribution of the three species of Plesiochorus, and it remains possible that some of the previously reported sequences have been attributed to the wrong species.

     

Spermiogenesis in the imbricate alligator lizard,Barisia imbricata (Reptilia,Squamata, Anguidae)

Although the events of spermiogenesis are commonly studied in amniotes, the amount of research available for Squamata is lacking. Many studies have described the morphological characteristics of mature spermatozoa in squamates, but few detail the ultrastructural changes that occur during spermiogenesis. This study's purpose is to gain a better understanding of the subcellular events of spermatid development within the Imbricate Alligator Lizard, Barisia imbricata. The morphological data presented here represent the first complete ultrastructural study of spermiogenesis within the family Anguidae. Samples of testes from four specimens collected on the northwest side of the Nevado de Toluca, México, were prepared using standard techniques for transmission electron microscopy. Many of the ultrastructural changes occurring during spermiogenesis within B. imbricata are similar to that of other squamates (i.e., early acrosome formation, chromatin condensation, flagella formation, annulus present, and a prominent manchette). However, there are a few unique characteristics within B. imbricata spermatids that to date have not been described during spermiogenesis in other squamates. For example, penetration of the acrosomal granule into the subacrosomal space to form the basal plate of the perforatorium during round spermatid development, the clover‐shaped morphology of the developing nuclear fossa of the flagellum, and the bulbous shape to the perforatorium are all unique to the Imbricate Alligator Lizard. These anatomical character differences may be valuable nontraditional data that along with more traditional matrices (such as DNA sequences and gross morphological data) may help elucidate phylogenetic relationships, which are historically considered controversial within Squamata. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.