PhD Candidate, Monash University
I study how embryos of turtles develop with changing environmental variables
Leatherback sea turtle eggs consistently experience lower hatching success (~50%) than those of other sea turtle species. The majority of embryonic death (>50%) occurs at early stages of development, possibly because embryos fail to break pre-ovipositional embryonic arrest after they are oviposited (laid). Pre-ovipositional arrest is maintained by hypoxia (low-oxygen) in the oviduct and increased oxygen availability is the trigger that breaks the arrest after oviposition in all turtle species studied to date. Here, we examined the impact of pre-ovipositional embryonic arrest on reproductive success in leatherbacks. We conducted an incubator experiment and a hatchery experiment. After oviposition eggs were exposed to either normoxia (21% O2), hyperoxia (32-42% O2) for five days, or hypoxia (1% O2) for three or five days. As has been found for other turtles, hypoxic incubation maintained embryos in arrest, equivalent to the time spent in hypoxia. However, extending arrest for five days resulted in greater early-stage embryonic death and a significant decrease in hatching success (68% lower than normoxic treatment). Eggs placed in incubators experienced greater hatching success than those placed into hatchery nests (67% vs 47%). We found no impact of hyperoxia on stage of embryonic death, hatching success, hatchling phenotype or fitness. Our findings indicate that delayed nesting and the subsequent extension of embryonic arrest may negatively impact embryonic development and therefore the reproductive success of endangered leatherback turtles. They also indicate that incubation under hyperoxic conditions is unlikely to be a useful method to improve hatching success in this species.
Abstract: Leatherback turtles have an average global hatching success rate of ~50%, lower than other marine turtle species. Embryonic death has been linked to environmental factors such as precipitation and temperature, although, there is still a lot of variability that remains to be explained. We examined how nesting season, the time of nesting each season, the relative position of each clutch laid by each female each season, maternal identity and associated factors such as reproductive experience of the female (new nester versus remigrant) and period of egg retention between clutches (interclutch interval) affected hatching success and stage of embryonic death in failed eggs of leatherback turtles nesting at Playa Grande, Costa Rica. Data were collected during five nesting seasons from 2004/05 to 2008/09. Mean hatching success was 50.4%. Nesting season significantly influenced hatching success in addition to early and late stage embryonic death. Neither clutch position nor nesting time during the season had a significant affect on hatching success or the stage of embryonic death. Some leatherback females consistently produced nests with higher hatching success rates than others. Remigrant females arrived earlier to nest, produced more clutches and had higher rates of hatching success than new nesters. Reproductive experience did not affect stage of death or the duration of the interclutch interval. The length of interclutch interval had a significant affect on the proportion of eggs that failed in each clutch and the developmental stage they died at. Intrinsic factors such as maternal identity are playing a role in affecting embryonic death in the leatherback turtle.
Pub.: 23 Jun '11, Pinned: 15 Oct '17
Abstract: Although viviparity (live birth) has evolved from oviparity (egg laying) at least 140 times in vertebrates, nearly 120 of these independent events occurred within a single reptile taxon. Surprisingly, only squamate reptiles (lizards and snakes) are capable of facilitating embryonic development to increasingly advanced stages inside the mother during extended periods of oviducal egg retention. Viviparity has never evolved in turtle lineages, presumably because embryos enter and remain in an arrested state until after eggs are laid, regardless of the duration of egg retention. Until now, the limiting factor that initiates and maintains developmental arrest has remained elusive. Here, we show that oviducal hypoxia arrests embryonic development. We demonstrate that hypoxia can maintain developmental arrest after oviposition and that subsequent exposure of arrested embryos to normoxia triggers resumption of their development. We discovered remarkably low oxygen partial pressure in the oviducts of gravid turtles and found that secretions produced by the oviduct retard oxygen diffusion. Our results suggest that an extremely hypoxic environment in the oviduct arrests embryonic development and may constrain the evolution of viviparity in turtles, with the reduced diffusive capacity of oviducal secretions possibly creating or contributing to this hypoxia. We anticipate that these findings will allow us to better understand the mechanisms underlying the evolutionary transition between reproductive modes.
Pub.: 26 Jan '13, Pinned: 15 Oct '17
Abstract: Turtle embryos pause development before oviposition in a process known as preovipositional arrest. Embryonic development arrests due to hypoxia (low oxygen) in the maternal oviducts and resumes only after exposure to normoxia when eggs are laid. Recently, several studies have hypothesized that the prolonged periods of preovipositional arrest may have a detrimental effect on embryo survival and development after eggs are laid. We tested this hypothesis by comparing embryo survival (determined by white spot formation and hatching success) and hatchling fitness (measured by self-righting, crawling, and swimming ability) of flatback sea turtle (Natator depressus) eggs following incubation in hypoxic (∼ 1%) and normoxic (∼ 21%) treatments for 5 d immediately following oviposition. We also measured embryo survival and hatchling fitness when eggs were incubated in hyperoxic conditions (42% oxygen), to determine whether hyperoxia could improve developmental outcome or whether some consequence of oxidative stress might manifest. Eggs incubated in hypoxia remained arrested during the 5-d treatment, and 97.5% of the eggs successfully recommenced development after exposure to normoxia when the treatment finished. At treatment commencement, 100% and 97.5% of eggs in the hyperoxic and normoxic treatments, respectively, began developing. Although hatching success was significantly lower following hypoxia (15%) compared to normoxia (80%) and hyperoxia (85%), hatchings from the hypoxic treatment were larger (carapace length and width and plastron length) than normoxic hatchlings. Similarly, hypoxic hatchings also swam significantly faster than hyperoxic hatchlings. Considering larger hatchlings may have a greater chance of survival, the production of larger hatchings may offset the high cost (lower hatching success) when preovipositional arrest is prolonged. Hyperoxia does not appear to have deleterious consequences for development.
Pub.: 03 Mar '15, Pinned: 15 Oct '17
Abstract: Turtle embryos enter a state of arrested development in the oviduct, allowing the mother greater flexibility in her reproductive schedule. Development recommences once eggs transition from the hypoxic oviduct to the normoxic nest. Significant mortality can occur if turtle eggs are moved between 12 h and 20 d after oviposition, and this is linked to the recommencement of embryonic development. To better understand the timing of developmental arrest and to determine how movement-induced mortality might be avoided, we determined the latency (i.e., time elapsed since oviposition) to recommencement of development following oviposition by exposing the eggs of green turtles (Chelonia mydas) to hypoxia (oxygen tension <8 mmHg) for 3 d, commencing 30 min to 48 h after oviposition. Embryonic development-including development of the characteristic opaque white spot on the eggshell-was halted by hypoxic incubation. When the delay before hypoxic incubation was 12 h or less, hatching success did not differ from a control group. If the hypoxic treatment began after 16 h or more in normoxia, then all embryos died. Thus, by returning eggs to a hypoxic environment before they have broken from arrest (i.e., within 12 h of oviposition), it is possible to extend embryonic arrest for at least 3 d, with no apparent detriment to hatching success. Therefore, hypoxic incubation may provide a new approach for avoidance of movement-induced mortality when conservation or research efforts require the relocation of eggs. Our findings also suggest that movement-induced mortality may have constrained the evolution of viviparity in turtles.
Pub.: 22 Jun '17, Pinned: 15 Oct '17
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