Effects of maternal identity and incubation temperature on snapping turtle (Chelydra serpentina) metabolism

Individual variation in physiological traits may have important consequences for offspring survivorship and adult fitness. Variance in offspring phenotypes is due to interindividual differences in genotype, environment, and/or maternal effects. This study examined the contributions of incubation environment, maternal effects, and clutch identity to individual variation in metabolic rates in the common snapping turtle, Chelydra serpentina. We measured standard metabolic rate, as determined by oxygen consumption, for 246 individuals representing 24 clutches at 15 degrees and 25 degrees C, and we measured standard metabolic rates additionally for 34 individuals at 20 degrees and 30 degrees C. Standard metabolic rate for 34 snapping turtles measured at 15 degrees, 20 degrees, 25 degrees, and 30 degrees C increased with increasing temperature. Mean standard metabolic rate for 246 individuals was 0.247 microL O(2) min(-1) g(-1) at 15 degrees C and 0.919 microL O(2) min(-1) g(-1) at 25 degrees C. At 15 degrees C, mass at hatching, individual mass, and egg mass had no significant effects on metabolic rate, but at 25 degrees C, mass at hatching, individual mass, and egg mass did have significant effects on metabolic rate. Incubation temperature had no significant effect on metabolic rate at 15 degrees, but it did have a significant effect at 25 degrees C. Clutch identity had a significant effect on metabolic rate at both 15 degrees and 25 degrees C. Interindividual variation in standard metabolic rate due to incubation temperature, and especially clutch identity, could have large effects on energy budgets. Results suggest that there were both environmental and genetic effects on standard metabolic rate.     

Behavioral responses of hatchling painted turtles (Chrysemys picta) and snapping turtles (Chelydra serpentina) at subzero temperatures

We monitored behavioral responses of cold-acclimated hatchling painted turtles (Chrysemys picta) indigenous to Nebraska and hatchling snapping turtles (Chelydra serpentina) indigenous to Nebraska and Arkansas during cooling (0.1°C/min) to temperatures as low as −19°C. All turtles made exploratory movements during cooling and locomotion occurred at temperatures as low as −2 to −4°C, but C. picta maintained relatively higher levels of locomotor activity than C. serpentina, and no differences in motility occurred between northern and southern groups of C. serpentina. Slow movements of the head and limbs were observed in supercooled hatchling C. picta at temperatures as low as −10°C, whereas at about −5°C, C. serpentina exhibited an increase in spontaneous motor activity followed by muscle contracture, immobility, and spontaneous freezing. C. picta spontaneously froze at about −16°C without exhibiting cold contracture, suggesting that they are better adapted to survive exposure to extreme cold.     

Temperature during embryonic and juvenile development influences growth in hatchling snapping turtles,Chelydra serpentina

Embryonic temperature influenced subsequent growth in juvenile snapping turtles, Chelydra serpentina: incubation temperatures of 24 and 26.5°C enhanced growth relative to a temperature of 29°C. Although embryonic temperature normally determines gonadal sex in this species, experimental manipulations revealed that temperature effects on growth were independent of sex. Ambient temperature also affected growth: juvenile turtles grew slowly in a cool (19°C) versus a warm (28°C) environment. In a parallel experiment, turtles from different embryonic temperatures displayed different patterns of temperature choice in response to nutritional status or time of day. We tentatively conclude that embryonic temperature has both direct and indirect (i.e., through temperature choice) effects on growth in snapping turtles.     

Aerial and aquatic oxygen uptake by freely-diving snapping turtles (Chelydra serpentina)

Summary Aerial oxygen consumption of unrestrained, freely-diving warm-and cold-acclimated snapping turtles, Chelydra serpentina, was measured at 10, 20, and 30°C. Also, simultaneous determinations of aerial and aquatic oxygen uptake by voluntarilydiving animals were made at 4 and 20°C. The standard rates of aerial oxygen consumption are equivalent in cold-and warm-acclimated animals in water and in cold-acclimated ones in air; these rates are all lower than those of warm-acclimated animals in air. Thus either cold acclimation or voluntary submergence reduces the standard metabolic rate of snapping turtles but the effects are not additive. Aquatic oxygen uptake during voluntary submergence is more important at low than at moderate temperatures and probably contributes significantly to gas exchange in these animals as they overwinter beneath the ice of ponds and streams.     

Cardiovascular correlates of exercise in snapping turtles, Chelydra serpentina

1. Heart rate increased with a rise in body temperature (10-30 degrees C) and with induced physical exercise in snapping turtles. 2. Maximum heart rate increment occurred at 30 degrees C. 3. Standard oxygen pulse did not change with a rise in temperature. 4. Oxygen pulse during exercise and oxygen pulse increment were maximal at 10 degrees C and minimal at 20 degrees C. 5. The increase in heart rate with exercise accounted for only 9-22% of the increase in oxygen transport during activity; the remainder was provided by a rise in cardiac stroke volume and/or A-V difference.     

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.     

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.     

Availability of water affects organ growth in prenatal and neonatal snapping turtles (Chelydra serpentina)

We manipulated the amount of water that was available to prenatal and neonatal snapping turtles (Chelydra serpentina) in order to assess the impact of water on growth by different organs in these animals. Three treatments were used: (1) turtles that completed their incubation on a wet substrate, (2) turtles that completed their incubation on a dry substrate, and (3) turtles that spent a few days in water after completing incubation on a dry substrate. Turtles hatching on a dry substrate (treatment 2) were smaller than animals in the other two treatments (which did not differ in size), so data for mass of different organs were adjusted by ANCOVA to remove effects of body size. Scaled masses of liver, stomach, lungs, kidneys, and small intestine did not differ between turtles emerging in wet environments and those hatching in dry environments, but hearts of turtles hatching in dry settings were substantially larger than those of animals hatching in wet ones. Thus, the mass of most organs in turtles developing in wet and dry environments scaled to body size, whereas the heart was hypertrophied in embryos developing in dry environments. Turtles that spent a few days in water after hatching from eggs in dry environments grew rapidly in size, and the increase in body size was accompanied by disproportionately rapid growth in the liver, stomach, lungs, kidneys, and small intestine. The heart did not increase in size during this period, despite the substantial increase in body mass over that at hatching. The enlarged heart of turtles hatching on dry substrates may have been caused by a circulatory hypovolemia late in incubation; the rapid growth of organs other than the heart when these animals were placed in water may reflect a release from constraints on growth once circulatory volume was restored. Accepted: 2 November 1999     

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.     

Ultrastructural morphology of the shell and shell membrane of eggs of common snapping turtles (Chelydra serpentina)

Common snapping turtles (Chelydra serpentina) lay nearly spherical, flexible-shelled eggs having an outer mineral layer composed of calcium carbonate in the aragonite form. The mineral layer is arranged into loosely organized groups of nodular shell units, with numerous spaces (or pores) between adjacent shell units. Shell units are structurally complex, consisting of an inner tip that is morphologically distinct from the main body of the shell unit. Contained within an intact shell unit at the interface of the tip and the main part of the shell unit is the central plaque, an apparent modification of the shell membrane that may serve to nucleate calcification of shell units during shell formation. The tips of shell units are firmly attached to a single, multilayered shell membrane throughout much of incubation. The calcareous layer begins to detach from the shell membrane about half-way through incubation, and changes in shell morphology attending this detachment indicate that snapping turtles may use the shell as a source of calcium during embryogenesis. The arrangement of the mineral layer into groups of shell units, the large number of spaces between shell units, and little or no interlocking of crystallites of adjacent shell units apparently are factors contributing to the ability of these eggs to swell as they absorb water.     

The effect of incubation media on the water exchange of snapping turtle (Chelydra serpentina) eggs and hatchlings

Summary The effect of two different incubation media, sand and vermiculite, on the water exchange of eggs and the mass of hatchlings of snapping turtles (Chelydra serpentina) was assessed. The eggs were incubated fully buried in either sand or vermiculite at 30 °C and egg mass was measured periodically throughout incubation. The wet and dry masses of each hatchling and its residual yolk were measured at the end of incubation. The media had similar water potentials () but their thermal conductivities differed 2.8-fold. The eggs experienced a net water gain during incubation. The rates of water uptake between treatments were not statistically different throught the first 36 days of incubation but were statistically different thereafter, with eggs incubating in sand taking up water at about twice the rate of eggs incubating in vermiculite. Hatchling masses were similar to both media but hatchling water contents were significantly different. Hatchlings incubated in sand had lower water contents than hatchlings incubated in vermiculite even though the eggs in sand took up more water. Hatchling mass was correlated with egg water exchange for eggs incubated in vermiculite but not for eggs incubated in sand. The difference in egg water exchange in the two media appears to be attributable to differences in the thermal conductivity of the media. The presence of such a thermal effect supports the hypothesis that the eggs exchanged water with the media as water vapor. Egg water exchange was limited by the shell and shell membranes and not by the media. The shell and shell membranes appear to present an effective barrier to water uptake.Abbreviations M _{H 2 O} water flux (cm³·day^-1) - L _p hydraulic conductivity (cm·day^-1·kPa^-1) - A shell area (cm²) - A _p pore area (cm²) - l shell thickness (cm) - r pore radius (cm) - viscosity (kPa·day) - P _{EH 2 O} egg water potential (kPa) - P _{AH 2 O} medium water potential (kPa) - G _{H 2 O} water vapor conductance (cm³·day^-1·kPa^-1) - D _{H 2 O} diffusion coefficient (cm²·day^-1) - R gas constant (cm³·kPa·K^-1·cm^-3) - T temperature (K) - P _{EH 2 O} egg water vapor pressure (kPa) - P _{AH 2 O} medium water vapor pressure (kPa) - d egg diameter - K soil hydraulic conductivity (cm²·day^-1·kPa^-1) - DHM hatchling dry mass - WHM hatchiling wet mass - WU water uptake - IM initial egg mass     

The relationship of body size to survivorship of hatchling snapping turtles (Chelydra serpentina): an evaluation of the “bigger is better” hypothesis

In many organisms, body size is positively correlated with traits that are presumably related to fitness. If directional selection frequently favors larger offspring (the “bigger is better” hypothesis), the results of such selection should be detectable with field experiments. We tested the “bigger is better” hypothesis in hatchling snapping turtles (Chelydra serpentina) by conducting one long-term and three short-term experiments on the University of Michigan E.S. George Reserve in southeastern Michigan. In the fall of 1995 and 1996, we released hatchlings at artificial nests separated from the nearest wetland by fences. We recorded the proportion of hatchlings recaptured, the time it took hatchlings to move to fences from artificial nests 45, 55, and 80 m away, and dispersion along the fence. We determined whether the response variables and probability of recapture at fences were associated with hatchling body size. During 1995, average travel times of hatchlings from the experimental nests were not related to distance from the fence; however, time to recapture was positively correlated with dispersion from the zero point on the fence, and the maximum time to reach the fence was almost twice as long for hatchlings from the 80-m nest compared to those from the 45-m nest. Sixty-seven percent of the hatchlings reached the fence and the proportions doing so from each nest were not different. Body size was not significantly related to probability of recapture in either of the 1995 experiments. In 1996, 59% of released hatchlings were recaptured. Time to recapture was not related to dispersion from the zero point or to body size. Cubic spline analysis suggested stabilizing selection on body size. We also conducted a set of long-term hatchling release experiments between 1980–1993 to compare the survival of hatchlings released at nest sites to that of hatchlings released directly into marshes, and we looked for relationships between survivorship and hatchling body size. During 7 years in which more than 30 hatchlings were released, 413 hatchlings were released directly into the marsh and 262 were released at nests: their probability of survival did not differ. Over all years, for both release groups combined and for each group separately, survival was not related to body size. In 1983 alone, survival was also not related to body size for either group or for both groups combined. In our three short-term experiments and one long-term experiment, we found no evidence to support the “bigger is better” hypothesis. When selection on body size did occur, selection was stabilizing, not directional for larger size. Received: 4 June 1998 / Accepted: 24 June 1999     

Embryonic temperature affects metabolic compensation and thyroid hormones in hatchling snapping turtles.

Temperature acclimation of adult vertebrates typically induces changes in metabolic physiology. During early development, such metabolic compensation might have profound consequences, yet acclimation of metabolism is little studied in early life stages. We measured the effect of egg incubation temperature on resting metabolic rate (RMR) and blood thyroid hormone levels of hatchling snapping turtles (Chelydra serpentina). Like many reptiles, snapping turtles have temperature-dependent sex determination (TSD), in which embryonic temperature determines sex. Therefore, we designed the experiments to separately measure effects of temperature and of sex on the response variables. We incubated eggs in the laboratory at 21. 5 degrees, 24.5 degrees, 27.5 degrees, and 30.5 degrees C, producing both sexes, all males, both sexes, and all females, respectively. Hatchling RMR, when measured at a common temperature (either 25 degrees or 31 degrees C), was negatively correlated with egg temperature in both males and females, such that RMR of turtles from 21.5 degrees C-incubated eggs averaged 160% that of turtles from 30.5 degrees C-incubated eggs. These results indicate that egg temperatures induced positive metabolic compensation in both sexes. Thyroid hormone levels of hatchlings showed similar correlations with egg temperature; thyroxine level of turtles from 21.5 degrees C-incubated eggs averaged 220% that of turtles from 30.5 degrees C-incubated eggs. To examine the possibility that thyroid hormones contribute to positive metabolic compensation, we added triiodothyronine to eggs during mid-incubation. RMR of hatchlings from these treated eggs averaged 131% that of controls, consistent with the previous possibility. Moreover, the effects of embryonic temperature on metabolic physiology, in combination with effects on sex, can result in differences in RMR and thyroid hormone levels between male and female hatchling turtles. Such differences may be important to the ecology and evolution of TSD.     

Mechanics of respiration in the snapping turtle,Chelydra serpentina (Linné)

The mechanism of lung ventilation in chelonians has been much debated. Electromyographic studies show that the basic mechanism in the snapping turtle, Chelydra serpentina, is dependent on the activities of four major respiratory muscles that are capable of varying the volume of the visceral cavity. The precise mechanism utilized varies in response to environmental factors, especially the depth to which the animal is submerged. Chelydra tends to reduce muscular activity to a minimum, and hydrostatic pressure or gravity replaces muscular effort whenever possible. The response is subject to hysteresis. Both the mechanics and pattern of ventilation in Chelydra differ from those of Testudo. The differences appear to be attributable in part to Chelydra's markedly reduced plastron and more extensive respiratory musculature and in part to the different habitats occupied by the two species.     

Swimming performance of hatchling green turtles is affected by incubation temperature

In an experiment repeated for two separate years, incubation temperature was found to affect the body size and swimming performance of hatchling green turtles (Chelonia mydas). In the first year, hatchlings from eggs incubated at 26°C were larger in size than hatchlings from 28 and 30°C, whilst in the second year hatchlings from 25.5°C were similar in size to hatchings from 30°C. Clutch of origin influenced the size of hatchlings at all incubation temperatures even when differences in egg size were taken into account. In laboratory measurements of swimming performance, in seawater at 28°C, hatchlings from eggs incubated at 25.5 and 26°C had a lower stroke rate frequency and lower force output than hatchlings from 28 and 30°C. These differences appeared to be caused by the muscles of hatchlings from cooler temperatures fatiguing at a faster rate. Clutch of origin did not influence swimming performance. This finding that hatchling males incubated at lower temperature had reduced swimming ability may affect their survival whilst running the gauntlet of predators in shallow near-shore waters, prior to reaching the relative safety of the open sea.     

Temperature effects on snapping performance in the common snapper Chelydra serpentina (Reptilia, Testudines)

Studies on the effect of temperature on whole-animal performance traits other than locomotion are rare. Here we investigate the effects of temperature on the performance of the turtle feeding apparatus in a defensive context. We measured bite force and the kinematics of snapping in the Common Snapping Turtle (Chelydra serpentina) over a wide range of body temperatures. Bite force performance was thermally insensitive over the broad range of temperatures typically experienced by these turtles in nature. In contrast, neck extension (velocity, acceleration, and deceleration) and jaw movements (velocity, acceleration, and deceleration) showed clear temperature dependence with peak acceleration and deceleration capacity increasing with increasing temperatures. Our results regarding the temperature dependence of defensive behavior are reflected by the ecology and overall behavior of this species. These data illustrate the necessity for carefully controlling T(b) when carrying out behavioral and functional studies on turtles as temperature affects the velocity, acceleration, and deceleration of jaw and neck extension movements. More generally, these data add to the limited but increasing number of studies showing that temperature may have important effects on feeding and defensive performance in ectotherms.     

Effects of incubation temperatures on sexual differentiation in the turtle,Chelydra serpentina

Eggs of the common snapping turtle, Chelydra serpentina, were incubated at constant temperatures ranging from 20°C to 30°C, At hatching, the oviducts were absent or incomplete in males; the testes were differentiated. In females at hatching, the oviduct was intact hut in some cases the gonad retained bisexual characteristics. Three months after hatching, the ovary was differentiated and contained follicles. Eggs incubated at 20°C and at 30°C developed into females in 100% of the cases. At 26°C, 99% of the individuals were males; at 24°C, 100% were males. More males than females developed at incubation temperatures of 22°C and 28°C.     

An ontogenetic shift in the response of heart rates to temperature in the developing snapping turtle (Chelydra serpentina)

The affect of acute changes in temperature on heart rates was investigated for the first time in a developing reptile. Heart rates were determined early and late in incubation in snapping turtle (Chelydra serpentina) eggs. Late in incubation heart rates at any given temperature were lower than those observed early in incubation. The results of temperature switching experiments late in incubation were consistent with thermal acclimation.