The exposure of green turtles (Chelonia mydas) to tumour promoting compounds produced by the cyanobacterium Lyngbya majuscula and their potential role in the aetiology of fibropapillomatosis

Lyngbya majuscula, a benthic filamentous cyanobacterium found throughout tropical and subtropical oceans, has been shown to contain the tumour promoting compounds lyngbyatoxin A (LA) and debromoaplysiatoxin (DAT). It grows epiphytically on seagrass and macroalgae, which also form the basis of the diet of the herbivorous green turtle (Chelonia mydas). This toxic cyanobacterium has been observed growing in regions where turtles suffer from fibropapillomatosis (FP), a potentially fatal neoplastic disease. The purpose of this study was to determine whether green turtles consume L. majuscula in Queensland, Australia and the Hawaiian Islands, USA, resulting in potential exposure to tumour promoting compounds produced by this cyanobacterium. L. majuscula was present, though not in bloom, at nine sites examined and LA and DAT were detected in variable concentrations both within and between sites. Although common in green turtle diets, L. majuscula was found to contribute less than 2% of total dietary intake, indicating that turtles may be exposed to low concentrations of tumour promoting compounds during non-bloom conditions. Tissue collected from dead green turtles in Moreton Bay tested positive for LA. An estimated dose, based on dietary intake and average toxin concentration at each site, showed a positive correlation for LA with the proportion of the population observed with external FP lesions. No such relationship was observed for DAT. This does not necessarily demonstrate a cause and effect relationship, but does suggest that naturally produced compounds should be considered in the aetiology of marine turtle FP.     

Distribution of mitochondrial haplotypes (cytb) in Polish populations of Emys orbicularis (L., 1758)

The European pond turtle, Emys orbicularis, inhabits a wide distribution area in the western Palaearctic. Polish populations of pond turtle represent the nominotypical subspecies Emys orbicularis orbicularis. The mitochondrial DNA haplotype (cytb gene) variation among 131 turtles from 26 locations in five regions of Poland was investigated. Five haplotypes belonging to three distinct lineages were identified. Two clades (I and II) were represented by two haplotypes each, while the other clade (IV) was represented by one haplotype. Three haplotypes were reported for the first time in E. orbicularis. The eastern part of Poland is inhabited exclusively by turtles bearing haplotype Ia. The remaining four sequence variants were recorded in western Poland where only the IIb haplotype is considered endemic. The distribution of the other haplotypes in western Poland could thus reflect past introductions or accidental releases. The authors regarded the two locations (Drzeczkowo and Karpicko) that were first included in the western Poland populations as autochthonous catchment areas of haplotype Ia.     

Effect of graded hypoxic and acidotic stress on contractile force of heart muscle from hypoxia-tolerant and hypoxia-intolerant turtles

Previous studies have shown that isometric contractile force of in vitro cardiac muscle from the anoxia-tolerant painted turtle, Chrysemys picta bellii, decreases when anoxic and when acidotic. This study sought to define the thresholds for these responses in the isolated ventricular strips of the painted turtle and in the anoxia-intolerant softshell turtles, Apalone spinifera. The ventricular strips were exposed to HCO3- Ringer's solution equilibrated at P(O2) 156, 74, 37, 19, and 0 mmHg (45 min at each grade), at both pH 7.0 and at pH 7.8. Strips were also exposed to graded lactic acidosis with intervals between pH 6.8 and pH 7.8 at P(O2) 156 mmHg (softshell) or 37 mmHg (painted). In painted turtle strips at pH 7.8, force remained at control levels until it decreased by 30% at P(O2) 19 mmHg. No further significant decrease occurred at P(O2) 0. In contrast, softshell turtle muscle force did not fall significantly until P(O2) reached 0. When graded hypoxia was imposed at pH 7.0, strips from both species were more sensitive to hypoxia, but the softshell force decreased at a higher P(O2) than the painted turtle (P(O2) 156 mmHg vs. 37 mmHg), its force fell to a lower level at P(O2) 0 (22 % of control vs. 40 % of control), and unlike painted turtle heart muscle, softshell muscle did not recover fully. In summary, these data indicate that ventricular strips of the painted turtle are no more tolerant of hypoxia alone than strips from the softshell turtle, but that when hypoxia is combined with acidosis, the painted turtle heart muscle functions significantly better during the exposure and recovers more fully after exposure.     

The role of the integument as a barrier to penetration of ice into overwintering hatchlings of the painted turtle (Chrysemys picta)

Hatchlings of the North American painted turtle (Chrysemys picta) spend their first winter of life inside a shallow, subterranean hibernaculum (the natal nest) where they may be exposed for extended periods to ice and cold. Hatchlings seemingly survive exposure to such conditions by becoming supercooled (i.e., by remaining unfrozen at temperatures below the equilibrium freezing point for body fluids), so we investigated the role of their integument in preventing ice from penetrating into body compartments from surrounding soil. We first showed that hatchlings whose epidermis has been damaged are more likely to be penetrated by growing crystals of ice than are turtles whose cutaneous barrier is intact. We next studied integument from a forelimb by light microscopy and discovered that the basal part of the alpha-keratin layer of the epidermis contains a dense layer of lipid. Skin from the forelimb of other neonatal turtles lacks such a layer of lipid in the epidermis, and these other turtles also are highly susceptible to inoculative freezing. Moreover, epidermis from the neck of hatchling painted turtles lacks the lipid layer, and this region of the skin is readily penetrated by growing crystals of ice. We therefore conclude that the resistance to inoculation imposed by skin on the limbs of hatchling painted turtles results from the presence of lipids in the alpha-keratin layer of the epidermis. Neonates apparently are able to avoid freezing during winter by drawing much of the body inside the shell, leaving only the ice-resistant integument of the limbs exposed to ice in the environment. The combination of behavior and skin morphology enables overwintering hatchlings to exploit an adaptive strategy based on supercooling.     

Relationship between tropical cyclones and the distribution of sea turtle nesting grounds

Aim This study examines the relationship between the distribution of existing sea turtle nesting sites and historical patterns of tropical cyclone events to investigate whether cyclones influence the current distribution of sea turtle nesting sites. The results, together with information on predicted cyclone activity and other key environmental variables, will help in the identification and prediction of future nesting sites for sea turtles as changes to the coastal environment continue. Location Queensland, Australia. Methods We used data on the nesting distribution of seven populations of four species of sea turtles [green (Chelonia mydas), flatback (Natator depressus), hawksbill (Eretmochelys imbricata) and loggerhead (Caretta caretta)] from the eastern Queensland coast, and tropical cyclone track data from 1969 to 2007 to explore the relationship between (1) sea turtle nesting phenology and cyclone season, and (2) sea turtle nesting sites and cyclone distribution. Furthermore, using two green turtle populations as a case study, we investigated the relationship between cyclone disturbance and sea turtle reproductive output, nesting site and season. Bootstrapping was used to explore if current sea turtle nesting sites are located in areas with lower or higher cyclone frequency than areas where turtles are currently not nesting. Results All populations of sea turtles studied here were disturbed by cyclone activity during the study period. The exposure (frequency) of tropical cyclones that crossed each nesting site varied greatly among and within the various sea turtle populations. This was mainly a result of the spatial distribution of each population’s nesting sites. Bootstrapping indicated that nesting sites generally have experienced lower cyclone activity than other areas that are available for nesting. Main conclusions Tropical cyclones might have been sufficiently detrimental to sea turtle hatching success on the eastern Queensland coast that through a natural selection process turtles in this region are now nesting in areas with lower cyclone activity. Therefore, it is important that future studies that predict climate or range shifts for sea turtle nesting distributions consider future cyclone activity as one of the variables in their model.     

A bloom of Lyngbya majuscula in Shoalwater Bay, Queensland, Australia: An important feeding ground for the green turtle (Chelonia mydas)

Lyngbya majuscula, a toxic cyanobacterium, was observed blooming during June–July (winter) 2002 in Shoalwater Bay, Queensland, Australia, an important feeding area for a large population of green turtles (Chelonia mydas). The bloom was mapped and extensive mats of L. majuscula were observed overgrowing seagrass beds along at least 18 km of coast, and covering a surface area of more than 11 km². Higher than average rainfall preceded the bloom and high water temperatures in the preceding summer may have contributed to the bloom. In bloom samples, lyngbyatoxin A (LA) was found to be present in low concentration (26 μg kg⁻¹_{(dry weight)}), but debromoaplysiatoxin (DAT) was not detected. The diet of 46 green turtles was assessed during the bloom and L. majuscula was found in 51% of the samples, however, overall it contributed only 2% of the animals’ diets. L. majuscula contribution to turtle diet was found to increase as the availability of the cyanobacterium increased. The bloom appeared to have no immediate impact on turtle body condition, however, the presence of a greater proportion of damaged seagrass leaves in diet in conjunction with decreases in plasma concentrations of sodium and glucose could suggest that the turtles may have been exposed to a substandard diet as a result of the bloom. This is the first confirmed report of L. majuscula blooming in winter in Shoalwater Bay, Queensland, Australia and demonstrates that turtles consume the toxic cyanobacterium in the wild, and that they are potentially exposed to tumour promoting compounds produced by this organism.     

Accumulation of lactate by supercooled hatchlings of the painted turtle (Chrysemys picta): implications for overwinter survival

Hatchlings of the North American painted turtle (Chrysemys picta) typically spend their first winter of life inside the shallow, subterranean nest where they completed embryogenesis the preceding summer. Neonates at northern localities consequently may be exposed during winter to subzero temperatures and frozen soil. Hatchlings apparently survive exposure to such conditions by supercooling, but the physiological consequences of this adaptive strategy have not been examined. We measured lactate in hatchling painted turtles after exposure to each of three temperatures (0 °C, −4 °C, and −8 °C) for three time periods (5 days, 15 days, and 25 days) to determine the extent to which overwintering hatchlings might rely on anaerobic metabolism to regenerate ATP. Whole-body lactate increased with increasing duration of exposure and decreasing temperature, and the highest levels were associated with the group that experienced the highest mortality. These results indicate that animals may develop a considerable lactic acidosis during a winter in which temperatures fall below 0 °C for weeks or months and that accumulation of lactate may contribute to mortality of overwintering animals. Accepted: 20 October 1999     

Do Roads Reduce Painted Turtle (Chrysemys picta) Populations?

Road mortality is thought to be a leading cause of turtle population decline. However, empirical evidence of the direct negative effects of road mortality on turtle population abundance is lacking. The purpose of this study was to provide a strong test of the prediction that roads reduce turtle population abundance. While controlling for potentially confounding variables, we compared relative abundance of painted turtles (Chrysemys picta) in 20 ponds in Eastern Ontario, 10 as close as possible to high traffic roads (Road sites) and 10 as far as possible from any major roads (No Road sites). There was no significant effect of roads on painted turtle relative abundance. Furthermore, our data do not support other predictions of the road mortality hypothesis; we observed neither a higher relative frequency of males to females at Road sites than at No Road sites, nor a lower average body size of turtles at Road than at No Road sites. We speculate that, although roads can cause substantial adult mortality in turtles, other factors, such as release from predation on adults and/or nests close to roads counter the negative effect of road mortality in some populations. We suggest that road mitigation for painted turtles can be limited to locations where turtles are forced to migrate across high traffic roads due, for example, to destruction of local nesting habitat or seasonal drying of ponds. This conclusion should not be extrapolated to other species of turtles, where road mortality could have a larger population-level effect than on painted turtles.     

Incidental nest predation in freshwater turtles: inter- and intraspecific differences in vulnerability are explained by relative crypsis

There has long been interest in the influence of predators on prey populations, although most predator–prey studies have focused on prey species that are targets of directed predator searching. Conversely, few have addressed depredation that occurs after incidental encounters with predators. We tested two predictions stemming from the hypothesis that nest predation on two sympatric freshwater turtle species whose nests are differentially prone to opportunistic detection—painted turtles (Chrysemys picta) and snapping turtles (Chelydra serpentina)—is incidental: (1) predation rates should be density independent, and (2) individual predators should not alter their foraging behavior after encountering nests. After monitoring nest survival and predator behavior following nest depredation over 2 years, we confirmed that predation by raccoons (Procyon lotor), the primary nest predators in our study area, matched both predictions. Furthermore, cryptic C. picta nests were victimized with lower frequency than more detectable C. serpentina nests, and nests of both species were more vulnerable in human-modified areas where opportunistic nest discovery is facilitated. Despite apparently being incidental, predation on nests of both species was intensive (57% for painted turtles, 84% for snapping turtles), and most depredations occurred within 1 day of nest establishment. By implication, predation need not be directed to affect prey demography, and factors influencing prey crypsis are drivers of the impact of incidental predation on prey. Our results also imply that efforts to conserve imperiled turtle populations in human-modified landscapes should include restoration of undisturbed conditions that are less likely to expose nests to incidental predators.