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The Effects of Thermal and Hydric Environments on Hatching Success, Embryonic Use of Energy and Hatchling Traits in a Colubrid Snake, Elaphe Carinata

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The Effects of Thermal and Hydric Environments on Hatching Success, Embryonic Use of Energy and Hatchling Traits in a Colubrid Snake, Elaphe Carinata Comparative Biochemistry and Physiology Part A 129Ž. 2001 461᎐471 The effects of thermal and hydric environments on hatching success, embryonic use of energy and hatchling traits in a colubrid snake, Elaphe carinata Xiang JiU, Wei-Guo Du Department of Biology, Hangzhou Normal College, Hangzhou 310036, Zhejiang, PR China Received 18 October 2000; received in revised form 10 December 2000; accepted 31 December 2000 Abstract 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 32ЊC on substrates with water potentials of 0 and y220 kPa using a 4=2 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 30ЊC than at 24 and 32ЊC, 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 32ЊC. 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 26ЊC were larger in SVL than those from other higher or lower incubation temperatures, characteristically having larger carcasses; hatchlings from 32ЊC eggs were smaller in SVL and had smaller carcasses but larger residual yolks than those from lower incubation temperatures. Hatchlings from eggs incubated at 24ЊC were shorter in tail length but greater in sizeŽ. SVL -specific body wet mass than those from higher incubation temperatures. Within the range from y220 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. ᮊ 2001 Elsevier Science Inc. All rights reserved. Keywords: Reptilia; Squamata; Colubridae; Elaphe carinata; Egg; Incubation; Hatching success; Calorimetry; Hatchling trait U Corresponding author. Tel.: q86-571-8082506; fax: q86-571-8804145. E-mail address: [email protected]Ž. X. Ji . 1095-6433r01r$ - see front matter ᮊ 2001 Elsevier Science Inc. All rights reserved. PII: S 1 0 9 5 - 6 4 3 3Ž. 0 1 00271-9 462 X. Ji, W. Du rComparati¨e Biochemistry and Physiology Part A 129() 2001 461᎐471 1. Introduction different species respond differently to variations in hydric environments encountered during in- Thermal and hydric environments affect em- cubation. In addition, investigators using different bryogenesis in reptilesŽ Packard, 1991; Overall, experimental designs and types of eggs might 1994. Theoretically, embryos can develop suc- reach different conclusions on the same topic. cessfully at temperatures between the upper and Reptiles lay either pliable-shelled eggs or lower limits of incubation temperatures, yielding rigid-shelled eggs, and most squamate reptiles lay viable hatchlingsŽ. Vinegar, 1974 . A high inci- pliable-shelled eggs. Unlike rigid-shelled eggs, pli- dence of abnormalities and failure of embryonic able-shelled eggs gain or lose mass rapidly due to development occurs at extreme temperatures, so the active exchange of water with their surround- the proportion of abnormal hatchlings and hatch- ingsŽ. Vleck and Hoyt, 1991; Vleck, 1991 . Conse- ing success can be used to assess the range of quently, pliable-shelled eggs show greater tem- viable incubation temperatures for any given poral changes in mass during incubation than do speciesŽ Ji and Brana,˜ 1999; Lin and Ji, 1998; Ji et rigid-shelled eggs, providing a greater variation in al., 1999b. The range of viable incubation tem- hydric conditions inside the eggŽ Vleck, 1991; Ji, peratures may vary among and within species that 1992; Overall, 1994; Ji et al., 1996, 1997a,b; Lin differ in distribution and habitat use, and is gen- and Ji, 1998; Ji and Brana,˜ 1999. Due to this erally wider in reptiles than in birdsŽ Ferguson, difference, we hypothesized that pliable-shelled 1985; Deeming and Ferguson, 1991; Lin and Ji, eggs would be more sensitive to variations in 1998; Ji et al., 1999b. Within this range, tempera- hydric conditions than rigid-shelled eggs and ture may subtly affect the embryonic use of en- would, therefore, be more suitable to test for the ergy and thermally plastic traits of hatchlingsŽ Lin subtle influence of incubation hydric environ- and Ji, 1998; Ji and Brana,˜ 1999; Ji et al., 1999b; ments. Brana˜ and Ji, 2000. Some influence could be Elaphe carinata is a large sized colubrid snake, ecologically and biologically important, and would, and females normally lay a single clutch with therefore, have a long-term effect on an individ- 5᎐17 pliable-shelled eggsŽ.Ž means9.7 Ji et al., ual’s fitnessŽ Webb and Cooper-Preston, 1989; 2000. per breeding season. The snake is widely Burger, 1991, 1998; Van Damme et al., 1992; distributed in southern China, including Taiwan, Allstead and Lang, 1995; Shine, 1995; Shine et al., northward to the provinces of Henan, Shaanxi 1997a,b; Brana˜ and Ji, 2000. In species with TSD and Gansu; it is also found in northern Vietnam Ž.temperature sex determination , temperature and JapanŽ Ryukyu Island, including the Senkaku also influences the sex ratio of hatchlingsŽ Bull, Group.Ž Zhao and Adler, 1993 . Previous work on 1980; Deeming and Ferguson, 1988; Janzen and egg incubation of this species focused on the Paukstis, 1991; Mrosovsky and Pieau, 1991. embryonic use of energy and nutrients and the Studies examining the effects of hydric environ- function of residual yolk. Results showed that E. ments on eggs and the hatchlings of reptiles are carinata embryos use yolk as the source of all limited, and the conclusions reached seem to be organic and most inorganic nutrients, and the contradictory. Some studies have shown pervasive eggshell as the additional source of calcium, and effects of incubation hydric environments on the residual yolk could be used to support the hatching success, duration of incubation and some subsequent growth of newly emerged hatchlings important hatchling traitsŽ e.g. mass and linear during their first days of lifeŽ. Ji et al., 1997a . measurements of hatchlings and size of residual However, the eggs used in previous work were yolk.Ž Lutz and Dunbar-Cooper, 1984; Packard incubated using just one combination of tempera- and Packard, 1984, 1986, 1988; Gutzke and ture and moisture, so the extent to which temper- Packard, 1987; Packard, 1991. Others, however, ature, moisture and their interaction affect eggs considered that the influence of hydric environ- and hatchlings remains unclear. Thus, we in- ments on egg incubation in reptiles, if any, was cubated E. carinata eggs at four temperatures less importantŽ Tracy, 1980; Hotaling et al., 1985; ranging from 24 to 32ЊC on substrates with water Plummer and Snell, 1988; Ratterman and Acker- potentials of 0 and y220 kPa using a 4=2 fac- man, 1989; Lin and Ji, 1998; Ji and Brana,˜ 1999; torial design. These temperatures and water po- Ji et al., 1999b. This contradiction is not so tentials were selected because they were mostly surprising, however, and suggests that the eggs of within the range of thermal and hydric environ- X. Ji, W. Du rComparati¨e Biochemistry and Physiology Part A 129() 2001 461᎐471 463 ments found in the E. carinata nests that were We moved containers every day among shelves located, although in natural nests, the thermal in the incubators according to a predetermined and hydric conditions normally fluctuateŽ Ji et al., schedule to minimize any influence of thermal unpublished data. Our aims were to examine the gradients inside the incubator. Incubation tem- effects of incubation temperature, substrate mois- peratures in close proximity to eggs were moni- ture and their interaction on the embryonic use tored twice daily using a digital thermometer. of energy and mass, linear measurements, mor- Eggs were weighed at 5-day intervals. Containers phology and the composition of newly emerged were weighed daily and, if necessary, distilled hatchlings. water was mixed evenly into substrates to com- pensate for small evaporative losses and water absorbed by eggs, thereby maintaining the sub- 2. Materials and methods strate water potential at a constant. When eggs were found to have pipped, we Forty-seven gravid female snakesw snout-vent moved them individually into covered glass con- lengthŽ. SVL : 95.0᎐144.0 cm; post-oviposition tainersŽ. 250 ml , thereby assuring positive identi- body mass: 276.5᎐788.0 gx were collected in mid- fication of emergent young. The duration of in- June 1998 from Lishui and Jiande, Zhejiang, east- cubation, measured as the number of days to ern China. The snakes were subsequently pipping, was recorded for each egg. Upon emer- transported to our laboratory at Hangzhou Nor- gence, mass, SVL and tail length were measured mal College, where they were randomly assigned on each hatchling. Deformed hatchlings were ex- 50=45=35 cm3 Ž. length=width=height wire cluded from further statistical analyses. Hatch- cages of which each contained 1᎐2 individuals. lings Ž.Ns204 were then killed by freezing to We fed snakes with commercial quail ŽTurnix y15ЊC for later study.
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