Hazards Associated with the Consumption of Sea Turtle Meat and Eggs: A Review for Health Care Workers and the General Public

Sea turtle products (e.g., meat, adipose tissue, organs, blood, eggs) are common food items for many communities worldwide, despite national regulations in some countries prohibiting such consumption. However, there may be hazards associated with this consumption due to the presence of bacteria, parasites, biotoxins, and environmental contaminants. Reported health effects of consuming sea turtles infected with zoonotic pathogens include diarrhea, vomiting, and extreme dehydration, which occasionally have resulted in hospitalization and death. Levels of heavy metals and organochlorine compounds measured in sea turtle edible tissues exceed international food safety standards and could result in toxic effects including neurotoxicity, kidney disease, liver cancer, and developmental effects in fetuses and children. The health data presented in this review provide information to health care providers and the public concerning the potential hazards associated with sea turtle consumption. Based on past mortality statistics from turtle poisonings, nursing mothers and children should be particularly discouraged from consuming all sea turtle products. We recommend that individuals choose seafood items lower in the food chain that may have a lower contaminant load. Dissemination of this information via a public health campaign may simultaneously improve public health and enhance sea turtle conservation by reducing human consumption of these threatened and endangered species.     

How do hatcheries influence embryonic development of sea turtle eggs? Experimental analysis and isolation of microorganisms in leatherback turtle eggs

Many conservation programs consider translocation of turtle nests to hatcheries as a useful technique. The repeated use of the same incubation substrate over several seasons in these hatcheries could, however, be harmful to embryos if pathogens were able to accumulate or if the physical and chemical characteristics of the incubation environment were altered. However, this hypothesis has yet to be tested. We conducted two field experiments to evaluate the effects of hatchery sand and eggshell decay on the embryonic development of leatherback sea turtle eggs in Colombia. We identified the presence of both fungi and bacteria species on leatherback turtle eggs. Sea turtle eggs exposed to previously used hatchery substrates or to decaying eggshells during the first and middle third of the embryonic development produced hatchlings that were smaller and/or weighed less than control eggs. However, this did not negatively influence hatching success. The final third of embryonic development seems to be less susceptible to infection by microorganisms associated with decaying shells. We discuss the mechanisms that could be affecting sea turtle egg development when in contact with fungi. Further studies should seek to understand the infection process and the stages of development in which the fungi are more virulent to the eggs of this critically endangered species.     

Fungal infection of sea turtle eggs in the sea turtle hatcheries in Peninsular Malaysia

Fungal infection in sea turtle nests has become a potential threat to sea turtle embryos. We screened the hatchery nest sand, eggshells of failed eggs, and stillbirths of green turtles and hawksbills collected from hatcheries in Malacca, Pahang, Perak and Terengganu for the presence of fungi. The DNA sequence of the ITS region of the three highest occurring isolated fungi confirmed that these species were Pseudallescheria ellipsoidea (35.4%), Scedosporium aurantiacum (27.2%), and Fusarium solani (22.0%). Morphological characteristics of these fungi were recorded. Although the total fungi abundance had no significant effect on hatching success (p > 0.05), the abundance of P. ellipsoidea significantly increased mortality in the nests (r = 0.70, p < 0.05). Future research should focus on understanding the biological aspects of this species to establish a more effective mitigation technique for the prevention of fungal infection of sea turtle eggs and hatchery employees.     

Detection of multiple paternity in the Kemp's ridley sea turtle with limited sampling

An important question in sea turtle biology is the number of males that contribute to the fertilization of a clutch of eggs. Previous studies on other sea turtle species have indicated little to no multiple paternity. We conclude here that female Kemp's ridleys, Lepidochelys kempi , are polyandrous. DNA from 26 mother and offspring groups was analysed at three microsatellite loci to identify paternal alleles. Three paternal alleles were observed among 14 of the clutches; four paternal alleles were observed among the offspring of an additional female. A maximum likelihood analysis not only rejects the model of single paternity, but also rejects the model of equal paternal contribution to the clutch. By explicitly addressing the high mutation rate of microsatellite markers, our analysis rejected mutation as the sole cause of multiple paternal alleles.     

To Eat or not to Eat an Endangered Species: Views of Local Residents and Physicians on the Safety of Sea Turtle Consumption in Northwestern Mexico

Sea turtles have historically been an important food resource for many coastal inhabitants of Mexico. Today, the consumption of sea turtle meat and eggs continues in northwestern Mexico despite well-documented legal protection and market conditions providing easier access to other more reliable protein sources. Although there is growing evidence that consuming sea turtles may be harmful to human health due to biotoxins, environmental contaminants, viruses, parasites, and bacteria, many at-risk individuals, trusted information sources, and risk communicators may be unaware of this information. Therefore, we interviewed 134 residents and 37 physicians in a region with high rates of sea turtle consumption to: (1) examine their knowledge and perceptions concerning these risks, as a function of sex, age, occupation, education and location; (2) document the occurrence of illness resulting from consumption; and (3) identify information needs for effective risk communication. We found that 32% of physicians reported having treated patients who were sickened from sea turtle consumption. Although physicians believed sea turtles were an unhealthy food source, they were largely unaware of specific health hazards found in regional sea turtles, regardless of location. By contrast, residents believed that sea turtles were a healthy food source, regardless of sex, age, occupation, and education, and they were largely unaware of specific health hazards found in regional sea turtles, regardless of age, occupation, and education. Although most residents indicated that they would cease consumption if their physician told them it was unhealthy, women were significantly more likely to do so than men. These results suggest that residents may lack the necessary knowledge to make informed dietary decisions and physicians do not have enough accurate information to effectively communicate risks with their patients.     

Loggerhead turtle eggshells as a source of maternal nuclear genomic DNA for population genetic studies

Tagging studies on nesting beaches are commonly used to estimate nesting frequency, remigration interval and nesting population size for marine turtle rookeries. Estimates of these demographic parameters from tagging projects may be biased because of the small scale of tagging efforts relative to female nest site fidelity and the logistical difficulty of intercepting all nesting females. Therefore, alternative and supplemental means of individual identification of nesting females are required. We demonstrate that maternal nuclear microsatellite DNA can be isolated from unincubated eggshells of the loggerhead sea turtle (Caretta caretta) through comparison of DNA extracted from 59 eggs collected within 15 h of oviposition and DNA derived from skin samples from respective nesting females. Scorable microsatellite genotypes were produced in 897 of 994 (90.2%) single-locus egg amplifications attempted. Among eggs from known females, 730 of 748 (97.6%) single-locus, egg-derived genotypes matched the respective skin-derived genotypes. Allelic dropout was the most common type of error, followed by the presence of nonmaternal, presumably paternal, alleles. Genotypes derived from unincubated eggshells permit individual assignment of nests and therefore demographic parameter estimates for loggerhead turtle nesting populations, despite genotyping errors that require further optimization. Although sampling unincubated eggs is destructive, this technique is noninvasive to nesting females and is applicable in marine turtle population genetics studies when individual resolution is required but direct interception of nesting females is undesirable or logistically infeasible.     

Global Distribution of Two Fungal Pathogens Threatening Endangered Sea Turtles

Nascent fungal infections are currently considered as one of the main threats for biodiversity and ecosystem health, and have driven several animal species into critical risk of extinction. Sea turtles are one of the most endangered groups of animals and only seven species have survived to date. Here, we described two pathogenic species, i.e., Fusarium falciforme and Fusarium keratoplasticum, that are globally distributed in major turtle nesting areas for six sea turtle species and that are implicated in low hatch success. These two fungi possess key biological features that are similar to emerging pathogens leading to host extinction, e.g., high virulence, and a broad host range style of life. Their optimal growth temperature overlap with the optimal incubation temperature for eggs, and they are able to kill up to 90% of the embryos. Environmental forcing, e.g., tidal inundation and clay/silt content of nests, were correlated to disease development. Thus, these Fusarium species constitute a major threat to sea turtle nests, especially to those experiencing environmental stressors. These findings have serious implications for the survival of endangered sea turtle populations and the success of conservation programs worldwide.     

Development of species-specific primers for rapid identification by PCR of the ecologically important pathogen Fusarium keratoplasticum from isolated and environmental samples

The genus Fusarium contains many fungal species known to be pathogenic to animals and plants alike. One species complex within this genus, the Fusarium solani species complex (FSSC), is of particular concern due to its high numbers of pathogenic members. FSSC members are known to contribute significantly to plant, human and other animal fungal disease. One member of the FSSC, Fusarium keratoplasticum, is of particular ecological concern and has been implicated in low hatching success of endangered sea turtle eggs, as well as contribute to human and other animal Fusarium pathogenesis. Species-specific primers for molecular identification of F. keratoplasticum currently do not exist to our knowledge, making rapid identification, tracking and quantitation of this pathogenic fungus difficult. The objective of this study was to develop primers specific to F. keratoplasticum that could be applied to DNA from isolated cultures as well as total (mixed) DNA from environmental samples. RPB2 sequence from 109 Fusarium isolates was aligned and analysed to determine nucleotide polymorphisms specific to F. keratoplasticum useful for primer design. A set of primers were generated and found to be effective for identification of F. keratoplasticum from total DNA extracted from sand surrounding sea turtle nesting sites.     

Unravelling the Microbiome of Eggs of the Endangered Sea Turtle Eretmochelys imbricata Identifies Bacteria with Activity against the Emerging Pathogen Fusarium falciforme

Habitat bioaugmentation and introduction of protective microbiota have been proposed as potential conservation strategies to rescue endangered mammals and amphibians from emerging diseases. For both strategies, insight into the microbiomes of the endangered species and their habitats is essential. Here, we sampled nests of the endangered sea turtle species Eretmochelys imbricata that were infected with the fungal pathogen Fusarium falciforme. Metagenomic analysis of the bacterial communities associated with the shells of the sea turtle eggs revealed approximately 16,664 operational taxonomic units, with Proteobacteria, Actinobacteria, Firmicutes and Bacteroidetes as the most dominant phyla. Subsequent isolation of Actinobacteria from the eggshells led to the identification of several genera (Streptomyces, Amycolaptosis, Micromomospora Plantactinospora and Solwaraspora) that inhibit hyphal growth of the pathogen F. falciforme. These bacterial genera constitute a first set of microbial indicators to evaluate the potential role of microbiota in conservation of endangered sea turtle species.     

Some analyses of artificially incubated eggs and hatchlings of Green and Loggerhead sea turtles

Eggs of the Green sea turtle ( Chelonia mydas ) and the Loggerhead sea turtle ( Caretta caretta ) were incubated in coral sand or silica sand moistened with distilled water. The eggs and hatchlings were analysed for calcium, magnesium and phosphorus. There was less magnesium but more calcium in the hatchlings than in the original egg contents but this was not influenced by the type of sand used during incubation. The results are interpreted as indicating that the eggshell is the major source of calcium for the developing embryos. The Logger-head sea turtle shows a greater efficiency in the incorporation of yolk magnesium and phosphorus into the embryo than does the Green sea turtle.     

A gravid fossil turtle from the Early Cretaceous reveals a different egg development strategy to that of extant marine turtles

Extant sea turtles develop and lay pliable (flexible) eggs; however, it is unknown whether they inherited this reproductive strategy from their closer fossil relatives or if it represents an evolutionary novelty. Here, we describe the first undisputable gravid marine fossil turtle ever found, from the early Cretaceous of Colombia, belonging to Desmatochelys padillai Cadena & Parham, which constitutes a representative of the Protostegidae. Using thin sectioning of one of the eggs, as well as scanning electron microscopy coupled with elemental characterization, cathodoluminescence, and computer tomography, we established that Desmatochelys padillai produced rigid eggs similar to those associated with some extant and fossil freshwater and terrestrial turtles. At least 48 spherical eggs were preserved inside this gravid turtle. We suggest that the development of rigid eggs in the extinct marine turtle Desmatochelys padillai resulted as an adaptation for egg‐embryo requirements dictated by the physical attributes of the nesting site.     

Diversity and status of sea turtle species in the Gulf of Guinea islands

In West Africa, the Gulf of Guinea islands are important nesting places for four sea turtle species. The Green turtle (Chelonia mydas), the Hawksbill (Eretmochelys imbricata), the Olive Ridley (Lepidochelys olivacea) and the Leatherback (Dermochelys coriacea) turtles nest on Bioko's southern beaches. The Green, Hawksbill and Leatherback turtles breed on Príncipe and São Tomé. The Leatherback turtle nests, at least, on Annobón. The Leatherback turtle is reported on the four islands for the first time, and the Olive Ridley turtle for Bioko. Bioko is probably the most important island in terms of number of species and nesting individuals; the Green turtle being the most abundant species. However, the nesting places are at present restricted to barely 20 km along the coastline. On Príncipe and São Tomé, the most common species is the Hawksbill turtle. Sea turtle nesting populations are being severely depleted on the four islands. The main causes of cverexploitation are the meat and egg trade on Bioko and the Hawksbill shell-craft trade on São Tomé and Príncipe.     

Influence of diminished respiratory surface area on survival of sea turtle embryos

It has been suggested that fungal presence on sea turtle eggs may impede gas exchange. To investigate the influence of diminished gas exchange surface upon embryo survivorship, flatback (Natator depressus) and green (Chelonia mydas) eggs were painted with petroleum jelly. Variable proportions of the egg surface were covered, including both respiratory and nonrespiratory domains. Embryo survival varied with site inhibited, proportion of eggshell affected, and species of turtle. If fungi on the exterior of the eggshell are able to impede respiratory gas exchange, their presence on the upper hemisphere (primary gas exchange area in early incubation) will result in the highest embryo mortality. Large eggs are likely to demonstrate a higher survivorship than small eggs, due to their larger available respiratory area and/or to variation in weight or stage-specific embryonic metabolic demands. Interspecific differences in egg size may therefore be a contributory factor to observed mortality rate differences in the natural presence of fungi.     

On Sea Turtle‐associated Craspedostauros (Bacillariophyta), with Description of Three Novel Species

The current study focuses on four species from the primarily marine diatom genus Craspedostauros that were observed growing attached to numerous sea turtles and sea turtle‐associated barnacles from Croatia and South Africa. Three of the examined taxa, C. danayanus sp. nov., C. legouvelloanus sp. nov., and C. macewanii sp. nov., are described based on morphological and, whenever possible, molecular characteristics. The new taxa exhibit characters not previously observed in other members of the genus, such as the presence of more than two rows of cribrate areolae on the girdle bands, shallow perforated septa, and a complete reduction of the stauros. The fourth species, C. alatus, itself recently described from museum sea turtle specimens, is reported for the first time from loggerhead sea turtles rescued in Europe. A 3‐gene phylogenetic analysis including DNA sequence data for three sea turtle‐associated Craspedostauros species and other marine and epizoic diatom taxa indicated that Craspedostauros is monophyletic and sister to Achnanthes. This study, being based on a large number of samples and animal specimens analyzed and using different preservation and processing methods, provides new insights into the ecology and biogeography of the genus and sheds light on the level of intimacy and permanency in the host–epibiont interaction within the epizoic Craspedostauros species.     

Metabolic heat estimation of the sea turtle Lepidochelys olivacea embryos

Several studies have reported the importance of metabolic heat on the increment of temperature in the sea turtle nests; however, the metabolic heat has not been calculated for sea turtle eggs. In this study, the metabolic heat generated by embryos of the sea turtle Lepidochelys olivacea was estimated from a thermal balance model by means of three measured temperatures—one in the center of the nest, and the others in the sand above and beside the nest. An experiment was conducted with a sample of 100 eggs from a Lepidochelys olivacea nest collected in the Baja Peninsula, Mexico. The results showed that during the incubation period, no metabolic heat was detected before day 19 but it increased from that day until a maximum of 0.84 W at day 34, when the incubation process was interrupted due to rain. This value corresponds to 31 emerged hatchlings. The novel model is a suitable framework to predict the temperature and metabolic heat within the nest.     

Developing ultraviolet illumination of gillnets as a method to reduce sea turtle bycatch

Fisheries bycatch of marine animals has been linked to population declines of multiple species, including many sea turtles. Altering the visual cues associated with fishing gear may reduce sea turtle bycatch. We examined the effectiveness of illuminating gillnets with ultraviolet (UV) light-emitting diodes for reducing green sea turtle (Chelonia mydas) interactions. We found that the mean sea turtle capture rate was reduced by 39.7% in UV-illuminated nets compared with nets without illumination. In collaboration with commercial fishermen, we tested UV net illumination in a bottom-set gillnet fishery in Baja California, Mexico. We did not find any difference in overall target fish catch rate or market value between net types. These findings suggest that UV net illumination may have applications in coastal and pelagic gillnet fisheries to reduce sea turtle bycatch.     

Sea Turtle Nesting as a Process Influencing a Sandy Beach Ecosystem

Sea turtle egg mortality, egg predation, and small organisms associated with turtle nests were studied at Playa Ostional, Costa Rica. Sites with concentrated sea turtle nesting were compared with solitary nesting sites as a function of place and time based on ANOVA, Akaike's Information Criterion, and Bayesian analyses. Results indicate that sea turtle egg mortality was significantly associated (P < 0.005) with flowing water that erodes or saturates nesting sites, and with overlapped nesting in which sea turtles disturb each other's nests. Sarcophagid and calliphorid fly larvae (Bayesian prior = 1.19; posterior = 2.27), fungi (prior = 1.14; posterior = 1.92), mites (prior = 0.51; posterior = 1.15), and several other types of small organisms increased in number after turtle egg laying (N= 303 nests; 34,451 turtle eggs). During peak sea turtle nesting periods, visitation to nesting sites by poachers and vertebrate predators was high, and relative number of nests disturbed by these predators was low (P < 0.02). In multimodel analysis, the three most parsimonious models were: (1) turtle egg mortality and distance from mean high tide; (2) turtle egg predation and distance from mean high tide; and (3) turtle egg mortality and nesting density, with Akaike weights of 0.224, 0.203, and 0.153 respectively. Intensive sea turtle nesting might result in upwelling and turnover of nesting debris and nest organisms, and may influence biotic community structure of sandy beach ecosystems.