Does the hydric environment affect the incubation of small rigid-shelled turtle eggs?

Hydric environments are hypothesized to have minor effects on the embryonic development of rigid-shelled turtle eggs due to the low water permeability of the eggshell. However, the water reserve in the eggs may still influence their resistance to environmentally induced dehydration. We incubated rigid-shelled turtle eggs (Pelodiscus sinensis) on different moist substrates (from ? 12 to ? 750 kPa) to test the hypothesis that small rigid-shelled eggs would be sensitive to hydric environments. The hydric treatment significantly affected the incubation period, with eggs incubated in the moistest and driest substrates taking longer to hatch than those on the medium-moisture substrates. Hatching success was slightly lower for eggs incubated in dry conditions than those in wet conditions, but the difference was not statistically significant. The heart rates of early embryos were lower on moist substrates than those on dry substrates, but this difference disappeared in late embryos. Hatchlings from the moistest substrate were larger (in carapace length and width) and heavier than those from drier substrates. However, the dry body mass of the hatchlings did not differ among the hydric treatments. The functional performance (righting response) of the hatchlings was affected by the hydric environment. The time to right was shorter for the hatchlings from the substrate of ? 12 kPa than those from ? 220 kPa. These results are consistent with the hypothesis that the hydric environment may significantly affect developing embryos and the resulting hatchlings in turtle species, such as P. sinensis, with small rigid-shelled eggs.     

Does maternal oviposition site influence offspring dispersal to suitable habitat?

Orientation and dispersal to suitable habitat affects fitness in many animals, but the factors that govern these behaviors are poorly understood. In many turtle species, hatchlings must orient and disperse to suitable aquatic habitat immediately after emergence from subterranean nests. Thus, the location of nest sites relative to aquatic habitats ideally should be associated with the direction of hatchling dispersal. At our study site, painted turtles (Chrysemys picta) nest to the west (on an island) and east (on the mainland) of a wetland, which determines the direction that hatchlings must travel to reach suitable aquatic habitat. To determine if hatchling orientation is intrinsically influenced by the location where their mothers nest, we employed a two-part cross-fostering experiment in the field, whereby half the eggs laid in mainland nests were swapped with half the eggs laid in island nests. Moreover, because C. picta hatchlings overwinter inside their nests, we performed a second cross-fostering experiment to fully decouple the effects of (1) the maternally chosen nest location, (2) the embryonic developmental location, and (3) the overwinter location. We released hatchlings into a circular arena in the field and found that turtles generally dispersed in a westerly direction, regardless of the maternally chosen nest location and independent of the locations of embryonic development and overwintering. Although this westerly direction was towards suitable aquatic habitat, we could not distinguish whether naïve hatchling turtles (i) use environmental cues/stimuli to orient their movement, or (ii) have an intrinsic bias to orient west in the absence of stimuli. Nevertheless, these findings suggest that the orientation behavior of naïve hatchling turtles during terrestrial dispersal is not dependent upon the location of maternally-chosen nest sites.     

First fossil gravid turtle provides insight into the evolution of reproductive traits in turtles

Here we report on the first discovery of shelled eggs inside the body cavity of a fossil turtle and on an isolated egg clutch, both referable to the Cretaceous turtle Adocus. These discoveries provide a unique opportunity to gain insight into the reproductive traits of an extinct turtle and to understand the evolution of such traits among living turtles. The gravid adult and egg clutch indicate that Adocus laid large clutches of rigid-shelled spherical eggs and established their nests near rivers, traits that are shared by its closest living relatives, the soft-shelled turtles. Adocus eggshell, however, was probably more rigid than that of living turtles, based on its great thickness and structure, features that may represent unique adaptations to intense predation or to arid nest environments. In light of the reproductive traits observed in Adocus, the distribution of reproductive traits among turtles reveals that large clutches of rigid-shelled eggs are primitive for hidden-necked turtles (cryptodirans) and that spherical eggs may have evolved independently within this group.     

The influence of hydric environments during egg incubation on embryonic heart rates and offspring phenotypes in a scincid lizard (Lampropholis guichenoti)

Extensive evidence shows that incubation conditions can affect phenotypic traits of hatchling reptiles, but the relative importance of thermal versus hydric factors, and the proximate mechanisms by which such factors influence hatchling phenotypes, remain unclear for most species. We incubated eggs of an Australian scincid lizard, Lampropholis guichenoti, at four different moisture contents ranging from -500 to 0 kPa. Drier substrates reduced water uptake of eggs and resulted in smaller hatchlings, but other phenotypic traits (incubation periods, hatchling sex, body proportions, running speeds, growth rates post-hatching) were not affected by the hydric environment during incubation. Contrary to our prediction, lower water uptake during incubation (and hence, presumably, more viscous blood) did not affect embryonic heart rates. Thus, as in many other squamate species, hatchling phenotypes and embryonic developmental rates of L. guichenoti are less sensitive to hydric conditions in the nest than to thermal regimes.     

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.     

Water exchange of flexible-shelled eggs and its effect on hatchling traits in the Chinese skink,<Emphasis Type="Italic"> Eumeces chinensis</Emphasis>

Flexible-shelled eggs of the Chinese skink (Eumeces chinensis) were used to determine the routes of water exchange with the environment and the effects of water exchange on hatchling traits. Eggs were incubated under three different hydric conditions at 28 °C. One group (ground eggs) was half-buried in incubation substrate. The second group (upper eggs) rested on the ground eggs but did not contact the substrate directly, and the third group was placed on a plastic platform above the substrate. Ground and upper eggs increased in mass and hatched successfully, while all eggs resting on the plastic platform lost mass and died within a week. Hence, E. chinensis eggs cannot sustain water balance through exchange of water vapor in air alone, but can absorb water from the substrate and other eggs and develop well. Water gained by upper eggs was only 20% of that absorbed by ground eggs, but hatchlings from the two treatments did not differ in morphology or locomotor performance. Therefore, the degree of water exchange of E. chinesis eggs has little effect on embryonic development and hatchling traits. The insensitivity of the eggs to variations in water exchange may be an adaptation against extreme hydric conditions in a species that deposits its eggs close to the soil surface.Communicated by I.D. Hume     

The effects of thermal and hydric environments on hatching success, embryonic use of energy and hatchling traits in a colubrid snake, Elaphe carinata.

We examined the effects of thermal and hydric environments on hatching success, the embryonic use of energy and hatchling traits in a colubrid snake, Elaphe carinata. The eggs were incubated at four temperatures ranging from 24 to 32 degrees C on substrates with water potentials of 0 and -220 kPa using a 4x2 factorial design. Both thermal and hydric environments affected the water exchange between eggs and their surroundings. Eggs incubated in wetter substrates gained mass throughout the course of incubation, whereas eggs in drier substrates gained mass during the first half of incubation and lost mass thereafter. Hatching success was noticeably higher at 26 and 30 degrees C than at 24 and 32 degrees C, but among treatments, differences in hatching success were not significant. Temperature significantly affected the duration of incubation and most hatchling traits examined. Deformed hatchlings were found in all temperature treatments, with more deformities observed at 32 degrees C. Hatchlings from eggs incubated at different temperatures differed in wet body mass, but the differences stemmed mainly from variation in water contents. Embryos at different temperatures completed development at nearly the same expenditure of energy and catabolized nearly the same amount of lipids, but hatchlings from different temperatures differed in the development condition of carcass at hatching. Hatchlings from eggs incubated at 26 degrees C were larger in SVL than those from other higher or lower incubation temperatures, characteristically having larger carcasses; hatchlings from 32 degrees C eggs were smaller in SVL and had smaller carcasses but larger residual yolks than those from lower incubation temperatures. Hatchlings from eggs incubated at 24 degrees C were shorter in tail length but greater in size (SVL)-specific body wet mass than those from higher incubation temperatures. Within the range from -220 to 0 kPa, the substrate water potential did not affect hatching success, the embryonic use of energy and all hatchling traits examined, and the effects of temperature were independent of the effects of substrate water potential. Therefore, our data add evidence showing that embryonic development in reptiles with pliable-shelled eggs is relatively insensitive to variation in hydric environments during incubation.     

孵化温度对赤链蛇胚胎代谢和幼体行为的影响

研究了赤链蛇(Dinodon rufozonatum)在孵化过程中卵的生长、孵化期、胚胎代谢和孵出幼体行为表现的热依赖性。结果显示:孵化温度对孵化期、卵增重、孵化过程中消耗的总能量和孵出幼体的运动表现有显著影响,但不影响胚胎代谢率、孵化成功率和幼体吐信频次。孵化期随着孵化温度的升高而缩短,孵化过程中,24℃终末卵重和胚胎代谢率显著大于30℃,而27℃与其他两个温度没有差异;27℃孵出幼体游速较24℃快,30℃孵出幼体与其他两个温度孵出幼体的游速无显著差异。上述结果显示:24—30℃是赤链蛇适合的孵化温度范围,与赤链蛇所处的生境温度相近。     

Influence of incubation temperature on hatching success,energy expenditure for embryonic development,and size and morphology of hatchlings in the oriental garden lizard,Calotes versicolor (Agamidae)

We incubated eggs of Calotes versicolor at four constant temperatures ranging from 24 degrees C to 33 degrees C to assess the effects of incubation temperature on hatching success, embryonic use of energy, and hatchling phenotypes that are likely to affect fitness. All viable eggs increased in mass throughout incubation due to absorption of water, and mass gain during incubation was dependent on initial egg mass and incubation temperature. The average duration of incubation at 24 degrees C, 27 degrees C, 30 degrees C, and 33 degrees C was 82.1 days, 60.5 days, 51.4 days, and 50.3 days, respectively. Incubation temperature affected hatching success, energy expenditure for embryonic development, and several hatchling traits examined, but it did not affect the sex ratio of hatchlings. Hatching success was lowest (3.4%) at 33 degrees C, but a higher incidence of deformed embryos was recorded from eggs incubated at this temperature compared to eggs incubated at lower temperatures. Most of the deformed embryos died at the last stage of incubation. Energy expenditure for embryonic development was, however, higher in eggs incubated at 33 degrees C than those similarly incubated at lower temperatures. A prolonged exposure of eggs of C. versicolor at 33 degrees C appears to have an adverse and presumably lethal effect on embryonic development. Hatching success at 24 degrees C was also low (43.3%), but hatchlings incubated at 24 degrees C did not differ in any of the examined traits from those incubated at two intermediate temperatures (27 degrees C and 30 degrees C). Hatchlings incubated at 33 degrees C were smaller (snout-vent length, SVL) than those incubated at lower incubation temperatures and had larger mass residuals (from the regression on SVL) as well as shorter head length, hindlimb length, tympanum diameter, and eye diameter relative to SVL. Hatchlings from 33 degrees C had significantly lower scores on the first axis of a principal component analysis representing mainly SVL-free head size (length and width) and fore- and hindlimb lengths, but they had significantly higher scores on the second axis mainly representing SVL-free wet body mass. Variation in the level of fluctuating asymmetry in eye diameter associated with incubation temperatures was quite high, and it was clearly consistent with the prediction that environmental stress associated with the highest incubation temperatures might produce the highest level of asymmetry. Newly emerged hatchlings exhibited sexual dimorphism in head width, with male hatchlings having larger head width than females.     

Effects of incubation temperature on the energetics of embryonic development and hatchling morphology in the Brisbane river turtle Emydura signata

Incubation temperature and the amount of water taken up by eggs from the substrate during incubation affects hatchling size and morphology in many oviparous reptiles. The Brisbane river turtle Emydura signata lays hard-shelled eggs and hatchling mass was unaffected by the amount of water gained or lost during incubation. Constant temperature incubation of eggs at 24 °C, 26 °C, 28 °C and 31 °C had no effect on hatchling mass, yolk-free hatchling mass, residual yolk mass, carapace length, carapace width, plastron length or plastron width. However, hatchlings incubated at 26 °C and 28 °C had wider heads than hatchlings incubated at 24 °C and 31 °C. Incubation period varied inversely with incubation temperature, while the rate of increase in oxygen consumption during the first part of incubation and the peak rate of oxygen consumption varied directly with incubation temperature. The total amount of oxygen consumed during development and hatchling production cost was significantly greater at 24 °C than at 26 °C, 28 °C and 31 °C. Hatchling mass and dimensions and total embryonic energy expenditure was directly proportional to initial egg mass. Accepted: 18 March 1998     

Geographic variation in thermal sensitivity of early life traits in a widespread reptile

Taxa with large geographic distributions generally encompass diverse macroclimatic conditions, potentially requiring local adaptation and/or phenotypic plasticity to match their phenotypes to differing environments. These eco‐evolutionary processes are of particular interest in organisms with traits that are directly affected by temperature, such as embryonic development in oviparous ectotherms. Here we examine the spatial distribution of fitness‐related early life phenotypes across the range of a widespread vertebrate, the painted turtle (Chrysemys picta). We quantified embryonic and hatchling traits from seven locations (in Idaho, Minnesota, Oregon, Illinois, Nebraska, Kansas, and New Mexico) after incubating eggs under constant conditions across a series of environmentally relevant temperatures. Thermal reaction norms for incubation duration and hatchling mass varied among locations under this common‐garden experiment, indicating genetic differentiation or pre‐ovulatory maternal effects. However, latitude, a commonly used proxy for geographic variation, was not a strong predictor of these geographic differences. Our findings suggest that this macroclimatic proxy may be an unreliable surrogate for microclimatic conditions experienced locally in nests. Instead, complex interactions between abiotic and biotic factors likely drive among‐population phenotypic variation in this system. Understanding spatial variation in key life‐history traits provides an important perspective on adaptation to contemporary and future climatic conditions.     

Eggshell Types and Their Evolutionary Correlation with Life-History Strategies in Squamates

The eggshell is an important physiological structure for the embryo. It enables gas exchange, physical protection and is a calcium reserve. Most squamates (lizards, snakes, worm lizards) lay parchment-shelled eggs, whereas only some gekkotan species, a subgroup of lizards, have strongly calcified eggshells. In viviparous (live-bearing) squamates the eggshell is reduced or completely missing (hereafter “shell-less”). Recent studies showed that life-history strategies of gekkotan species differ between species with parchment- and rigid-shelled eggshells. Here we test if the three different eggshell types found in the squamates are also associated with different life-history strategies. We first investigated the influence of the phylogeny on the trait “eggshell type” and on six life-history traits of 32 squamate species. Phylogenetic principal component analysis (pPCA) was then conducted to identify an association between life-history strategies and eggshell types. Finally, we also considered adult weight in the pPCA to examine its potential effect on this association. Eggshell types in squamates show a strong phylogenetic signal at a low taxonomical level. Four out of the six life-history traits showed also a phylogenetic signal (birth size, clutch size, clutches per year and age at female maturity), while two had none (incubation time, maximum longevity). The pPCA suggested an association of life-history strategies and eggshell types, which disappeared when adult weight was included in the analysis. We conclude that the variability seen in eggshell types of squamates is weakly influenced by phylogeny. Eggshell types correlate with different life-history strategies, and mainly reflect differences in adult weights of species.     

Thermal acclimation of heart rates in reptilian embryos

In many reptiles, the thermal regimes experienced by eggs in natural nests vary as a function of ambient weather and location, and this variation has important impacts on patterns of embryonic development. Recent advances in non-invasive measurement of embryonic heart rates allow us to answer a long-standing puzzle in reptilian developmental biology: Do the metabolic and developmental rates of embryos acclimate to local incubation regimes, as occurs for metabolic acclimation by post-hatching reptiles? Based on a strong correlation between embryonic heart rate and oxygen consumption, we used heart rates as a measure of metabolic rate. We demonstrate acclimation of heart rates relative to temperature in embryos of one turtle, one snake and one lizard species that oviposit in relatively deep nests, but found no acclimation in another lizard species that uses shallow (and hence, highly thermally variable) nests. Embryonic thermal acclimation thus is widespread, but not ubiquitous, within reptiles.     

Climate change and temperature‐linked hatchling mortality at a globally important sea turtle nesting site

The study of temperature‐dependent sex determination (TSD) in vertebrates has attracted major scientific interest. Recently, concerns for species with TSD in a warming world have increased because imbalanced sex ratios could potentially threaten population viability. In contrast, relatively little attention has been given to the direct effects of increased temperatures on successful embryonic development. Using 6603 days of sand temperature data recorded across 6 years at a globally important loggerhead sea turtle rookery—the Cape Verde Islands—we show the effects of warming incubation temperatures on the survival of hatchlings in nests. Incorporating published data (n = 110 data points for three species across 12 sites globally), we show the generality of relationships between hatchling mortality and incubation temperature and hence the broad applicability of our findings to sea turtles in general. We use a mechanistic approach supplemented by empirical data to consider the linked effects of warming temperatures on hatchling output and on sex ratios for these species that exhibit TSD. Our results show that higher temperatures increase the natural growth rate of the population as more females are produced. As a result, we project that numbers of nests at this globally important site will increase by approximately 30% by the year 2100. However, as incubation temperatures near lethal levels, the natural growth rate of the population decreases and the long‐term survival of this turtle population is threatened. Our results highlight concerns for species with TSD in a warming world and underline the need for research to extend from a focus on temperature‐dependent sex determination to a focus on temperature‐linked hatchling mortalities.     

Geographic variation in hatchling size in an oviparous skink: effects of maternal investment and incubation thermal environment

Geographic variation in offspring size can be viewed as an adaptive response to local environmental conditions, but the causes of such variation remain unclear. Here, we compared the size and composition of eggs laid by female Chinese skinks (Plestiodon chinensis) from six geographically distinct populations in southeastern China to evaluate geographic variation in hatchling size. We also incubated eggs from these six populations at three constant temperatures (24, 28 and 32 °C) to evaluate the combined effects of incubation temperature and population source on hatchling size. Egg mass and composition varied among populations, and interpopulation differences in yolk dry mass and energy content were still evident after accounting for egg mass. Population mean egg mass and thus hatchling mass were greater in the colder localities. Females from three northern populations increased offspring size by laying larger eggs relative to their own size. Females from an inland population in Rongjiang could increase offspring size by investing relatively more dry materials and thus more energy into individual eggs without enlarging the size of their eggs. The degree of embryonic development at oviposition was almost the same across the six populations, so was the rate of embryonic development and thus incubation length at any given temperature. Both incubation temperature and population source affected hatchling traits examined, but the relative importance of these two factors varied between traits. Our data show that in P. chinensis hatchling traits reflecting overall body size (body mass, snout‐vent length and tail length) are more profoundly affected by population source. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 283–296.     

Success of Delayed Translocation of Loggerhead Turtle Nests

ABSTRACT Sea turtle embryo mortality in natural nests due to environmental and anthropogenic factors can be very high. To increase hatching success of these endangered species, nest translocation to hatcheries immediately after egg-laying is a common management tool. To test the viability of delayed translocation, we moved 50 loggerhead sea turtle (Caretta caretta) nests to a beach hatchery after various times (0–96 hr) after egg-laying at Boavista Island (Republic of Cabo Verde, western Africa). We transported eggs in a rigid plastic container, being careful to maintain their original vertical orientation. Delayed translocation times of 0 hours, 12 hours, 24 hours, 84 hours, or 96 hours after egg-laying did not have any effect on hatching success, incubation period, or hatchling size and mass. Delayed translocation slightly increased the duration of the translocation process because of extra precautions taken (e.g., maintaining axial orientation, protecting eggs from mechanical shocks). We conclude that delayed nest translocation can be done in a safe and effective way, thereby increasing the efficiency of the whole monitoring program. Finally, delayed translocation, accompanied by an evaluation of fertility, would seem to permit the removal of undeveloped eggs and to facilitate their subsequent exploitation by local communities without affecting turtle nesting success.