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.     

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.     

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     

Respiratory responses to short term hypoxia in the snapping turtle, Chelydra serpentina

Among vertebrates, turtles are able to tolerate exceptionally low oxygen tensions. We have investigated the compensatory mechanisms that regulate respiration and blood oxygen transport in snapping turtles during short exposure to hypoxia. Snapping turtles started to hyperventilate when oxygen levels dropped below 10% O(2). Total ventilation increased 1.75-fold, essentially related to an increase in respiration frequency. During normoxia, respiration occurred in bouts of four to five breaths, whereas at 5% O(2), the ventilation pattern was more regular with breathing bouts consisting of a single breath. The increase in the heart rate between breaths during hypoxia suggests that a high pulmonary blood flow may be maintained during non-ventilatory periods to improve arterial blood oxygenation. After 4 days of hypoxia at 5% O(2), hematocrit, hemoglobin concentration and multiplicity and intraerythrocytic organic phosphate concentration remained unaltered. Accordingly, oxygen binding curves at constant P(CO(2)) showed no changes in oxygen affinity and cooperativity. However, blood pH increased significantly from 7.50+/-0.05 under normoxia to 7.72+/-0.03 under hypoxia. The respiratory alkalosis will produce a pronounced in vivo left-shift of the blood oxygen dissociation curve due to the large Bohr effect and this is shown to be critical for arterial oxygen saturation.     

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.     

Oviductal morphology in relation to hormonal levels in the snapping turtle, Chelydra serpentina

Microscopic and in situ visual observations were used to relate circulating hormone levels to morphological changes in the oviduct of the snapping turtle Chelydra serpentina throughout the ovarian cycle. Increase in levels of progesterone (P), estradiol (E2) and testosterone (T) levels coincide with an increase in number and growth of endometrial glands, luminal epithelial cells and secretory droplets throughout the oviduct. Testosterone and estradiol levels rose significantly (P < 0.05) after the May-June period and remained high throughout the rest of the summer. Progesterone levels remained stable throughout the summer, with a brief decline in July due to luteolysis. Hormonal values declined significantly (P < 0.001) at the end of the ovarian cycle in the fall. In situ visual observation of fresh oviducts at different stages of gravidity in recently ovulated turtles revealed that proteinaceous like components from the endometrial glands were released into the lumen to form fibers. The morphological features of the oviduct remained active throughout the summer months even though the snapping turtle is a monoclutch species which deposits all the eggs in late-May to mid-June. The high steroid levels correlate with and may be responsible for the secretory activity present throughout the summer and their decline correlates with change to low secretory activity in the fall. Calcium deposition accompanied by morphological changes in luminal cells are suggestive of secretory activity. In the egg-bearing turtles, uterine Ca2+ concentrations measured by flame atomic absorption spectrophotometry revealed significantly higher Ca2+ concentrations (P < 0.001) in eggs with soft shell than eggs without shell. There was a significant increase in calcium granules and proteinaceous fibers in luminal surface of the uterus during the period of eggshelling. This supports the fact that in the snapping turtle like in other reptiles, eggshelling process occurs in the uterus.     

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.     

The physiology of overwintering in a turtle that occupies multiple habitats,the common snapping turtle (Chelydra serpentina)

Common snapping turtles, Chelydra serpentina (Linnaeus), were submerged in anoxic and normoxic water at 3 degrees C. Periodic blood samples were taken, and PO(2), PCO(2), pH, [Na(+)], [K(+)], [Cl(-)], total Ca, total Mg, [lactate], [glucose], hematocrit, and osmolality were measured; weight gain was determined; and plasma [HCO(3)(-)] was calculated. Submergence in normoxic water caused a decrease in PCO(2) from 10.8 to 6.9 mmHg after 125 d, partially compensating a slight increase in lactate and allowing the turtles to maintain a constant pH. Submergence in anoxic water caused a rapid increase in lactate from 1.8 to 168.1 mmol/L after 100 d. Associated with the increased lactate were decreases in pH from 8.057 to 7.132 and in [HCO(3)(-)] from 51.5 to 4.9 mmol/L and increases in total Ca from 2.0 to 36.6 mmol/L, in total Mg from 1.8 to 12.1 mmol/L, and in [K(+)] from 3.08 to 8.45 mmol/L. We suggest that C. serpentina is tolerant of anoxic submergence and therefore is able to exploit habitats unavailable to some other species in northern latitudes.     

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.     

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.     

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     

Secretory proteins in the reproductive tract of the snapping turtle, Chelhydra serpentina

SDS-polyacrylamide gel electrophoresis was used to separate the secretory proteins produced by the epithelial and endometrial glands of the uterine tube and uterus in the snapping turtle Chelydra serpentina. The proteins were analyzed throughout the phases of the reproductive cycle from May to August, including preovulatory, ovulatory, postovulatory or luteal, and vitellogenic phases. The pattern of secretory proteins is quite uniform along the length of the uterine tube, and the same is true of the uterus, but the patterns for uterine tube and uterus are clearly different. We identify 13 major proteins in C. serpentina egg albumen. Bands co-migrating with 11 of these are found in the uterine tube, but at most 4 are found in the uterus, suggesting that the majority of the albumen proteins are most likely secreted in the uterine tube, not in the uterus. Although some of the egg albumen proteins are present in the uterine tube only at the time of ovulation, most of the bands corresponding to albumen proteins are present throughout the breeding season even though the snapping turtle is a monoclutch species. These results suggest that the glandular secretory phase in the uterine tube is active and quite homogeneous in function regardless of location or phase of the reproductive cycle.     

Effect of thermal acclimation on thermal preference,resistance and locomotor performance of hatchling soft-shelled turtle

The significant influence of thermal acclimation on physiological and behavioral performance has been documented in many ectothermic animals, but such studies are still limited in turtle species. We acclimated hatchling soft-shelled turtles Pelodiscus sinensis under three thermal conditions （10, 20 and 30~C） for 4 weeks, and then measured selected body temperature （Tsel）, critical thermal minimum （CTMin） and maximum （CTM~x）, and locomotor performance at different body temperatures. Thermal acclimation significantly affected thermal preference and resistance of P sinensis hatchlings. Hatchling turtles accli- mated to 10~C selected relatively lower body temperatures and were less resistant to high temperatures than those acclimated to 20~C and 30~C. The turtles＇ resistance to low temperatures increased with a decreasing acclimation temperature. The thermal re- sistance range （i.e. the difference between CTM~x and CTMin, TRR） was widest in turtles acclimated to 20~C, and narrowest in those acclimated to 10~C. The locomotor performance of turtles was affected by both body temperature and acclimation tem- perature. Hatchling turtles acclimated to relatively higher temperatures swam faster than did those acclimated to lower temperatures. Accordingly, hatchling turtles acclimated to a particular temperature may not enhance the performance at that temperature. Instead, hatchlings acclimated to relatively warm temperatures have a better performance, supporting the ＂hotter is better＂ hypothesis.