Effects of temperature and moisture during incubation on carcass composition of hatchling snapping turtles (Chelydra serpentina)

Summary Flexible-shelled eggs of common snapping turtles (Chelydra serpentina) were incubated on each of two substrates (vermiculite, sand) at each of three temperatures (26.0°C, 28.5°C, 31.0°C) and three moisture regimes (wet, intermediate, dry). Embryos developing in cool, wet environments mobilized the largest amounts of protein from their yolk and attained the largest size before hatching, whereas turtles developing in warm, dry environments mobilized the smallest quantities of protein and were the smallest in body size at hatching. Embryos on wet substrates mobilized more lipid from their yolk than did embryos on dry media, but ambient temperature had no demonstrable influence on patterns of lipid mobilization. The total reserve of neutral lipid available in residual yolk plus carcass to sustain neonates in the interval prior to the beginning of feeding was largest in hatchlings from dry environments and smallest in animals from wet environments, but was unaffected by temperature during incubation. Hydration of tissues in hatchlings was higher when incubation was in cool, moist conditions than when incubation was in warm, dry settings, thereby indicating that some of the effects of moisture and temperature on mobilization of nutrients by embryos may be mediated by differences in intracellular water. Patterns of response to temperature and moisture recorded for turtles emerging from eggs on sand were similar to those recorded for hatchlings on vermiculite, so no important conclusion would have been affected by incubating eggs on one medium instead of the other.     

Environmental modulation of calcium and phosphorus metabolism in embryonic snapping turtles (Chelydra serpentina)

Summary Eggs of common snapping turtles (Chelydra serpentina) were incubated on wet (–150 kPa water potential) and dry (–950 kPa) substrates in a laboratory study assessing the effects of the hydric environment on patterns of mobilization of calcium and phosphorus by developing embryos. We found that embryos developing in wet environments withdrew nutrients from their yolk faster, grew more rapidly, and incubated longer than embryos exposed to dry environments. Turtles developing in both environments absorbed calcium from the yolk at similar rates and depleted the yolk of almost its entire reserve of calcium prior to hatching. Calcium withdrawn from the yolk was supplemented with calcium mobilized from the eggshell, but embryos in wet environments obtained substantially more calcium from the eggshell than did those in dry settings. Embryos obtained all of the phosphorus used in skeletogenesis from the yolk, but those incubating in wet environments mobilized phosphorus from this compartment more rapidly than did those in dry settings. Exposing embryonic snapping turtles to wet environments apparently allows them to make more efficient use of the transitory source of calcium in the eggshell than is possible in dry environments. However, the residual yolk in hatchlings from both wet and dry environments contains too little calcium to support the growth of hard and soft tissues in neonates at rates similar to those characterizing the growth phase of development in embryogenesis.     

Wetness of the nest environment influences cardiac development in pre- and post-natal snapping turtles (Chelydra serpentina)

We dissected hearts from near-term embryos and hatchlings of common snapping turtles (Chelydridae: Chelydra serpentina) whose eggs had incubated on wet or dry substrates, and then dried and individually weighed the heart and yolk-free carcass from each animal. Hearts and carcasses of prenatal and neonatal animals grew at different rates, and the patterns of growth by both heart and carcass differed between wet and dry environments. Hearts grew faster, both in actual mass and in mass adjusted for variation in body size, in embryos and hatchlings whose eggs were incubated on dry substrates than in animals whose eggs were held on wet media. This finding is consistent with a hypothesis that embryos incubating in dry settings experience hypovolemia secondary to dehydration and that enlargement of the heart compensates, in part, for the associated increase in viscosity of the blood. Embryonic turtles seemingly exhibit the same plasticity and response that would be expected from other vertebrate ectotherms subjected to the physiological challenges associated with desiccation and an associated reduction in blood volume.     

An experimental analysis of the water relations of eggs of Blanding's turtles (Emydoidea blandingii)

Eggs of Blanding's turtles ( Emydoidea blandingii ) were incubated in the laboratory under hydric conditions eliciting different patterns of net water exchange between eggs and surrounding air and substrate. Eggs incubated on wet and intermediate substrates increased in mass during the first half of incubation and decreased in mass during the second half, and their mass just before hatching was slightly lower than at oviposition. Eggs incubated on dry substrates and on platforms above substrates declined in mass throughout incubation, with a rate of decline greater in the second half of incubation than in the first. The size of hatchlings was related to the hydric environment in which eggs were incubated and, possibly, to the net flux of water across eggshells. However, variation in size of hatchlings was not as great as has been reported for other species with flexible-shelled eggs, owing presumably to the constraints on water exchange imposed by the more complex eggshells of Blanding's turtles.     

Changes in mass of eggs of softshell turtless (Trionyx spiniferus) incubated under hydric conditions simulating those of natural nests

Rigid-shelled eggs of softshell turtles ( Trionyx spiniferus ) incubated at 29C under hydric conditions simulating those at the interior of natural nests (i.e. eggs not contacting the substrate) declined in mass during incubation owing to the continuous escape of water vapour to air trapped inside the chambers, with eggs incubated in relatively dry chambers declining more in mass than eggs held in relatively wet chambers. Eggs held under hydric conditions approximating those at the periphery of natural nests (i.e. eggs partly buried in the substrate) also declined in mass during incubation, but at lower rates than characterized eggs not contacting the substrate, indicating that absorption of liquid water from the substrate compensated for part of the water vapour escaping to the air inside the chambers. There was no relationship between hatching success and either the position of eggs in the chambers or the wetness of substrates, nor was there any variation among experimental groups in the size of hatchlings. Thus, development of embryos of Trionyx spiniferus seems not to be closely coupled with the hydric environment of the nest, a situation contrasting with that of embryos of those species of turtles producing pliable-shelled eggs.     

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.     

Influence of water availability during incubation on hatchling size, body composition, desiccation tolerance, and terrestrial locomotor performance in the snapping turtle Chelydra serpentina

The effects of water availability during incubation on the water contents of neonatal snapping turtles at hatching were examined, along with the influence of hatchling water content on desiccation tolerance and terrestrial locomotor performance. The water contents of hatchlings from eggs incubated on wet substrates were both absolutely and proportionally greater than were those of hatchlings from eggs incubated on dry substrates. Hatchlings with greater water contents at hatching were able to survive longer and to lose more water before physiological performance was adversely affected by desiccation. Increased water contents in hatchlings with greater water availability during incubation may enhance survival by increasing the amount of water the animal can afford to lose before dehydration begins to adversely affect whole animal performance.     

Embryonic communication in the nest: metabolic responses of reptilian embryos to developmental rates of siblings

Incubation temperature affects developmental rates and defines many phenotypes and fitness characteristics of reptilian embryos. In turtles, eggs are deposited in layers within the nest, such that thermal gradients create independent developmental conditions for each egg. Despite differences in developmental rate, several studies have revealed unexpected synchronicity in hatching, however, the mechanisms through which synchrony are achieved may be different between species. Here, we examine the phenomenon of synchronous hatching in turtles by assessing proximate mechanisms in an Australian freshwater turtle (Emydura macquarii). We tested whether embryos hatch prematurely or developmentally compensate in response to more advanced embryos in a clutch. We established developmental asynchrony within a clutch of turtle eggs and assessed both metabolic and heart rates throughout incubation in constant and fluctuating temperatures. Turtles appeared to hatch at similar developmental stages, with less-developed embryos in experimental groups responding to the presence of more developed eggs in a clutch by increasing both metabolic and heart rates. Early hatching did not appear to reduce neuromuscular ability at hatching. These results support developmental adjustment mechanisms of the 'catch-up hypothesis' for synchronous hatching in E. macquarii and implies some level of embryo-embryo communication. The group environment of a nest strongly supports the development of adaptive communication mechanisms between siblings and the evolution of environmentally cued hatching.     

Residual yolk energetics and postnatal shell growth in Smooth Softshell Turtles,Apalone mutica

We examined functions of residual yolk (RY¹) in hatchling Smooth Softshell Turtles (Apalone mutica). Removal of RY did not affect survival, shell growth, or resting metabolic rates of turtles for 40 d after hatching. Our estimates of metabolic rate suggest that RY can fuel maintenance and activity metabolism for approximately 25 days. A. mutica absorb more than 1 g of water in the first 2 weeks of life, which appears to be the basis of post-hatch shell expansion rather than yolk-provisioned growth. Post-hatch growth may be limited by the magnitude of RY remaining at hatching, but RY protein and lipid proportions do not differ from those of freshly-laid eggs. In addition, A. mutica did not use RY to fuel nest emergence. Our results suggest that RY does not fulfill several hypothetical functions in A. mutica, including postnatal growth, catabolic fuel for nest emergence, and long-term nutritional sustenance for maintenance, activity, or hibernation. Instead, A. mutica appear to absorb most yolk prior to hatching, and are left with a minimum of RY. Variation in RY mass with incubation regime in other species suggests that mothers may overprovision their eggs to ensure successful development across a diversity of possible incubation conditions.     

The relationship between gut contents and supercooling capacity in hatchling painted turtles (Chrysemys picta)

Painted turtles (Chrysemys picta) typically spend their first winter of life in a shallow, subterranean hibernaculum (the natal nest) where they seemingly withstand exposure to ice and cold by resisting freezing and becoming supercooled. However, turtles ingest soil and fragments of eggshell as they are hatching from their eggs, and the ingestate usually contains efficient nucleating agents that cause water to freeze at high subzero temperatures. Consequently, neonatal painted turtles have only a modest ability to undergo supercooling in the period immediately after hatching. We studied the limit for supercooling (SCP) in hatchlings that were acclimating to different thermal regimes and then related SCPs of the turtles to the amount of particulate matter in their gastrointestinal (GI) tract. Turtles that were transferred directly from 26 degrees C (the incubation temperature) to 2 degrees C did not purge soil from their gut, and SCPs for these animals remained near -4 degrees C for the 60 days of the study. Animals that were held at 26 degrees C for the duration of the experiment usually cleared soil from their GI tract within 24 days, but SCPs for these turtles were only slightly lower after 60 days than they were at the outset of the experiment. Hatchlings that were acclimating slowly to 2 degrees C cleared soil from their gut within 24 days and realized a modest reduction in their SCP. However, the limit of supercooling in the slowly acclimating animals continued to decline even after all particulate material had been removed from their GI tract, thereby indicating that factors intrinsic to the nucleating agents themselves also may have been involved in the acclimation of hatchlings to low temperature. The lowest SCPs for turtles that were acclimating slowly to 2 degrees C were similar to SCPs recorded in an earlier study of animals taken from natural nests in late autumn, so the current findings affirm the importance of seasonally declining temperatures in preparing animals in the field to withstand conditions that they will encounter during winter.     

Phenotypic variation in smooth softshell turtles (<Emphasis Type="Italic">Apalone mutica</Emphasis>) from eggs incubated in constant versus fluctuating temperatures

Temperatures experienced during embryonic development elicit well-documented phenotypic variation in embryonic and neonatal animals. Most research, however, has only considered the effects of constant temperatures, even though developmental temperatures in natural settings fluctuate considerably on a daily and seasonal basis. A laboratory study of 15 clutches of smooth softshell turtles (Apalone mutica) was conducted to explicitly examine the influence of thermal variance on phenotypic variation. Holding mean temperature constant and eliminating substrate moisture effects permitted a clear assessment of the impact of thermal variance on hatching success, incubation length, hatchling body size, swimming speed, and righting time. Incubation length and swimming speed varied significantly among temperature treatments. Both traits tended to increase with increasing thermal variance during embryonic development. Clutch significantly affected all traits examined, except righting time, even after accounting for the effects of initial egg mass. These results highlight the importance of accounting for the impact of both thermal mean and variance on phenotypic variation. The findings also strengthen the increasing recognition of maternal clutch effects as critical factors influencing phenotypic variation in neonatal animals.     

孵化水热环境对渔异色蛇孵化卵和孵出幼体的影响

渔异色蛇卵孵化时能从环境中吸收水分导致质量增加,卵质量的增加与初始卵质量和孵化基质湿度有关。较大幅度的孵化基质湿度变化对孵化期、孵化成功率、胚胎动用孵内物质和能量、孵出幼体的性比、大小和质量无显著影响。孵化期随温度升高而缩短,并显示极强的窝间差异。温度对孵出幼体的性别无影响,但显著影响孵化成功率、胚胎对卵内物质和能量的动用、幼体的大小和质量、躯干和剩余卵黄的质量。孵出幼体总长的两性差异不显著,但雌体体长大于雄体而尾长小于雄体。３２℃不适于孵化渔异色蛇卵,该温度下孵出的幼体躯干发育不良,剩余孵黄较多,尾部均呈畸形,孵化过程中能量转化率较低。２４℃和２６℃中孵出的幼体躯干发育良好,孵化过程中能量转化率较高,各项被测定的幼体特征指标均极相似。     

Breeding limits foraging time: evidence of interrupted foraging response from body mass variation in a tropical environment

Birds should store body reserves if starvation risk is anticipated; this is known as an ‘interrupted foraging response’. If foraging remains unrestricted, however, body mass should remain low to limit the predation risk that gaining and carrying body reserves entails. In temperate environments mass gain in female birds during breeding is often attributed to egg formation and mass loss after incubation to flight adaptation or the effect of reproductive workload, rather than as a result of an adaptive interrupted foraging response to the limited foraging time or unpredictable foraging conditions that breeding demands. In tropical environments, foraging conditions vary more within the breeding season than in temperate environments, and so studies in tropical environments are more suited to decouple the potentially confounded effects of increase in body reserves versus egg formation on the body mass of breeding birds. In this study, we test whether breeding results in an interrupted foraging response in a tropical savannah system using body mass data collected over a 15‐year period from female common bulbuls Pycnonotus barbatus. This species breeds both in the wet and dry season, despite fewer resources being available in the dry season. Breeding stage predicted female body mass: body mass peaked abruptly during incubation, but was not closely associated with the egg‐laying stage, and declined during brood rearing. Breeding females were heavier in the dry season than in the wet season. In the dry season, heavier birds were more likely to incubate eggs or brood chicks. These observations suggest that increased body reserves are required to buffer the consequence of limited foraging time or impoverished foraging conditions, which may be most pronounced during incubation and in the dry season, respectively. Such mass increases are consistent with an interrupted foraging response, which may apply to temperate zone birds experiencing foraging restrictions during breeding.     

Patterns of interspecific variation in the heart rates of embryonic reptiles

New non-invasive technologies allow direct measurement of heart rates (and thus, developmental rates) of embryos. We applied these methods to a diverse array of oviparous reptiles (24 species of lizards, 18 snakes, 11 turtles, 1 crocodilian), to identify general influences on cardiac rates during embryogenesis. Heart rates increased with ambient temperature in all lineages, but (at the same temperature) were faster in lizards and turtles than in snakes and crocodilians. We analysed these data within a phylogenetic framework. Embryonic heart rates were faster in species with smaller adult sizes, smaller egg sizes, and shorter incubation periods. Phylogenetic changes in heart rates were negatively correlated with concurrent changes in adult body mass and residual incubation period among the lizards, snakes (especially within pythons) and crocodilians. The total number of embryonic heart beats between oviposition and hatching was lower in squamates than in turtles or the crocodilian. Within squamates, embryonic iguanians and gekkonids required more heartbeats to complete development than did embryos of the other squamate families that we tested. These differences plausibly reflect phylogenetic divergence in the proportion of embryogenesis completed before versus after laying.     

中华鳖新孵幼体的热耐受性、体温昼夜变化和运动能力的热依赖性

研究中华鳖新孵幼体的热耐受性、体温及温度对运动能力的影响 .结果表明 ,在干燥和潮湿环境下 ,选择体温分别为 2 8.0℃和 30 .3℃ ;潮湿环境下 ,临界高温和低温分别为 40 .9℃和 7.8℃ .在缺乏温度梯度的热环境中 ,水温对幼鳖体温的影响比气温更直接 ,体温和环境温度的昼夜变化相一致 ,说明幼鳖生理调温能力很弱 .在有温度梯度的热环境中 ,幼鳖能通过行为调温将体温维持到较高且较恒定的水平 ,导致体温昼夜变化不明显 .幼鳖运动能力有显著的热依赖性 ,在一定温度范围内随体温升高而增强 .体温31.5℃时 ,幼鳖的运动表现最好 ,最大续跑距离、单位时间跑动距离和单位时间停顿次数分别为 1.87m、4 92m·min-1和 6 .2次·min-1.体温过高时 ,运动能力下降 .当体温为 33 .0℃时 ,最大续跑距离、单位时间跑动距离和单位时间停顿次数分别为 1.30m、4.2 8m·min-1和 7.7次·min-1.     

High rates of growth recorded for hawksbill sea turtles in Anegada,British Virgin Islands

Management of species of conservation concern requires knowledge of demographic parameters, such as rates of recruitment, survival, and growth. In the Caribbean, hawksbill turtles (Eretmochelys imbricata) have been historically exploited in huge numbers to satisfy trade in their shells and meat. In the present study, we estimated growth rate of juvenile hawksbill turtles around Anegada, British Virgin Islands, using capture–mark–recapture of 59 turtles over periods of up to 649 days. Turtles were recaptured up to six times, having moved up to 5.9 km from the release location. Across all sizes, turtles grew at an average rate of 9.3 cm year⁻¹ (range 2.3–20.3 cm year⁻¹), and gained mass at an average of 3.9 kg year⁻¹ (range 850 g–16.1 kg year⁻¹). Carapace length was a significant predictor of growth rate and mass gain, but there was no relationship between either variable and sea surface temperature. These are among the fastest rates of growth reported for this species, with seven turtles growing at a rate that would increase their body size by more than half per year (51–69% increase in body length). This study also demonstrates the importance of shallow water reef systems for the developmental habitat for juvenile hawksbill turtles. Although growth rates for posthatching turtles in the pelagic, and turtles larger than 61 cm, are not known for this population, the implications of this study are that Caribbean hawksbill turtles in some areas may reach body sizes suggesting sexual maturity in less time than previously considered.     

Seasonal flexibility in organ size in the Andean lizard Liolaemus moradoensis

The understanding of animal functioning in fluctuating environments is a major goal of physiological and evolutionary ecology. In temperate terrestrial habitats, one of the most pervasive changes in environmental conditions is that associated with the seasonal change along the year. In this study, we describe the pattern of seasonal variation in the size of nine internal organs in the lizard Liolaemus moradoensis from the Andes Mountains of Central Chile. We observed that the size of digestive organs was greater during summer in comparison to other seasons. Dry masses of liver and fat bodies reached maximum values during summer and minimum during spring. We suspect that lowest spring values are related with build‐up costs of energetically expensive organs (e.g., digestive, muscle mass) at the end of the hibernation period. Dry mass of the heart and lungs did not show a clear pattern of variation, suggesting that cardiac and pulmonary performance were maintained throughout the year. The dry mass of kidneys was greater during winter than during summer, a result observed in other hibernating lizards but for which there is no clear explanation. Finally, the dry mass of testes showed a maximum value during autumn and a progressive reduction toward summer, indicating that reproduction occurs during autumn. When represented in a bivariate space, acquisition (digestive), distribution (heart, lungs and kidneys), storage (liver and fat bodies), and expenditure (testes) organs generate four clusters. In general terms, observed seasonal pattern of change in organ size is in agreement with those reported for other lizard species that inhabit highly fluctuating environments. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

The physiology of hibernation in common map turtles (Graptemys geographica).

Map turtles from Wisconsin were submerged at 3 degrees C in normoxic and anoxic water to simulate extremes of potential respiratory microenvironments while hibernating under ice. In predive turtles, and in turtles submerged for up to 150 days, plasma PO2, PCO2) pH, [Cl-], [Na+], [K+], total Mg, total Ca, lactate, glucose, and osmolality were measured; hematocrit and body mass were determined, and plasma [HCO3-] was calculated. Turtles in anoxic water developed a severe metabolic acidosis, accumulating lactate from a predive value of 1.7 to 116 mmol/l at 50 days, associated with a fall in pH from 8.010 to 7.128. To buffer lactate increase, total calcium and magnesium rose from 3.5 and 2.0 to 25.7 and 7.6 mmol/l, respectively. Plasma [HCO3-] was titrated from 44.7 to 4.3 mmol/l in turtles in anoxic water. Turtles in normoxic water had only minor disturbances of their acid-base status and ionic statuses; there was a marked increase in hematocrit from 31.1 to 51.9%. This study and field studies suggest that map turtles have an obligatory requirement for a hibernaculum that provides well-oxygenated water (e.g. rivers and large lakes rather than small ponds and swamps) and that this requirement is a major factor in determining their microdistribution.