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ISRN Zoology  2012 

Interspecific Variation in Temperature Effects on Embryonic Metabolism and Development in Turtles

DOI: 10.5402/2012/846136

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Abstract:

We measured temperature-induced differences in metabolic rates and growth by embryos of three turtle species, Macrochelys temminckii, Trachemys scripta, and Apalone spinifera, at different, constant, temperatures. Oxygen consumption rate (VO2) was measured during development and used to characterize changes in metabolism and calculate total O2 consumption. Results from eggs incubated at different temperatures were used to calculate Q10s at different stages of development and to look for evidence of metabolic compensation. Total O2 consumption over the course of incubation was lowest at high incubation temperatures, and late-term metabolic rate Q10s were <2 in all three species. Both results were consistent with positive metabolic compensation. However, incubation temperature effects on egg mass-corrected hatchling size varied among species. Apalone spinifera hatchling mass was unaffected by temperature, whereas T. scripta mass was greatest at high temperatures and M. temminckii mass was lowest at high temperatures. Hatchling mass?:?length relationships tended to correlate negatively with temperature in all three species. Although we cannot reject positive metabolic compensation as a contributor to the observed VO2 patterns, there is precedence for drawing the more parsimonious conclusion that differences in yolk-free size alone produced the observed incubation temperature differences without energetic canalization by temperature acclimation during incubation. 1. Introduction Although the suite of biochemical activities that contributes to an organism’s metabolism is complex and therefore challenging to model [1], strong relationships exist between body temperature and whole-organism metabolic rate [2]. Various thermoregulatory mechanisms are employed by animals to dissociate body temperature from ambient temperature. Endothermy has evolved repeatedly as a physiological means of surviving suboptimal thermal conditions, but ectothermic species often rely primarily on behavioral strategies to regulate body temperature. In addition to behavior, however, ectotherms may exhibit physiological mechanisms to address thermal constraints of their environment. Solutions for surviving inhospitable temperatures may include manipulating biochemical reaction rates by varying enzyme concentrations or receptor densities, production of chaperone proteins to increase the range of temperatures over which target enzymes remain functional [3], changing the composition of cell membranes to affect permeability and (rarely) producing temperature-specific isozymes [4–6]. In

References

[1]  A. Clarke, “Is there a universal temperature dependence of metabolism?” Functional Ecology, vol. 18, no. 2, pp. 252–256, 2004.
[2]  J. F. Gillooly, J. H. Brown, G. B. West, V. M. Savage, and E. L. Charnov, “Effects of size and temperature on metabolic rate,” Science, vol. 293, no. 5538, pp. 2248–2251, 2001.
[3]  M. E. Feder and G. E. Hofmann, “Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology,” Annual Review of Physiology, vol. 61, pp. 243–282, 1999.
[4]  J. R. Hazel and C. L. Prosser, “Molecular mechanisms of temperature compensation in poikilotherms,” Physiological Reviews, vol. 54, no. 3, pp. 620–677, 1974.
[5]  J. J. Lin, S. MacLeod, and C. M. Kuo, “Qualitative and quantitative strategies of thermal adaptation of grass carp (Ctenopharyngodon idella) cytoplasmic malate dehydrogenases,” Fish Physiology and Biochemistry, vol. 15, no. 1, pp. 71–81, 1996.
[6]  G. N. Somero, “Adaptation of enzymes to temperature: searching for basic ‘strategies’,” Comparative Biochemistry and Physiology, vol. 139, no. 3, pp. 321–333, 2004.
[7]  C. L. Morjan, “Variation in nesting patterns affecting nest temperatures in two populations of painted turtles (Chrysemys picta) with temperature-dependent sex determination,” Behavioral Ecology and Sociobiology, vol. 53, no. 4, pp. 254–261, 2003.
[8]  J. J. Bull and E. L. Charnov, “Enigmatic sex ratios,” Evolution, vol. 43, pp. 1561–1566, 1989.
[9]  D. Crews, J. M. Bergeron, J. J. Bull et al., “Temperature-dependent sex determination in reptiles: proximate mechanisms, ultimate outcomes, and practical applications,” Developmental Genetics, vol. 15, no. 3, pp. 297–312, 1994.
[10]  C. Ciofi and I. R. Swingland, “Environmental sex determination in reptiles,” Applied Animal Behaviour Science, vol. 51, no. 3-4, pp. 251–265, 1997.
[11]  R. J. Brooks, M. L. Bobyn, D. A. Galbraith, J. A. Layfield, and E. G. Nancekivell, “Maternal and environmental influences on growth and survival of embryonic and hatchling snapping turtles (Chelydra serpentina),” Canadian Journal of Zoology, vol. 69, no. 10, pp. 2667–2676, 1991.
[12]  J. R. Spotila, L. D. Spotila, and N. F. Kaufer, “Molecular mechanisms of TSD in reptiles: a search for the magic bullet,” Journal of Experimental Zoology, vol. 270, no. 1, pp. 117–127, 1994.
[13]  W. M. Roosenburg and K. C. Kelley, “The effect of egg size and incubation temperature on growth in the turtle, Malaclemys terrapin,” Journal of Herpetology, vol. 30, no. 2, pp. 198–204, 1996.
[14]  S. O'Steen, “Embryonic temperature influences juvenile temperature choice and growth rate in snapping turtles Chelydra serpentina,” The Journal of Experimental Biology, vol. 201, no. 3, pp. 439–449, 1998.
[15]  J. P. Demuth, “The effects of constant and fluctuating incubation temperatures on sex determination, growth, and performance in the tortoise Gopherus polyphemus,” Canadian Journal of Zoology, vol. 79, no. 9, pp. 1609–1620, 2001.
[16]  W. G. Du and X. Ji, “The effects of incubation thermal environments on size, locomotor performance and early growth of hatchling soft-shelled turtles, Pelodiscus sinensis,” Journal of Thermal Biology, vol. 28, no. 4, pp. 279–286, 2003.
[17]  K. M. Ryan, J. R. Spotila, and E. A. Standora, “Incubation temperature and post-hatching growth and performance in snapping turtles,” American Zoologist, vol. 30, article 112A, 1990.
[18]  C. M. McKnight and W. H. N. Gutzke, “Effects of embryonic environment and of hatchling housing conditions on growth of young snapping turtles (Chelydra serpentina),” Copeia, vol. 1993, pp. 475–482, 1993.
[19]  M. L. Bobyn and R. J. Brooks, “Interclutch and interpopulation variation in the effects of incubation conditions on sex, survival and growth of hatchling turtles (Chelydra serpentina),” Journal of Zoology, vol. 233, no. 2, pp. 233–257, 1994.
[20]  T. Rhen and J. W. Lang, “Phenotypic plasticity for growth in the common snapping turtle: effects of incubation temperature, clutch, and their interaction,” American Naturalist, vol. 146, no. 4, pp. 726–747, 1995.
[21]  T. Rhen and J. W. Lang, “Temperature during embryonic and juvenile development influences growth in hatchling snapping turtles, Chelydra serpentina,” Journal of Thermal Biology, vol. 24, no. 1, pp. 33–41, 1999.
[22]  A. C. Steyermark and J. R. Spotila, “Effects of maternal identity and incubation temperature on snapping turtle (Chelydra serpentina) growth,” Functional Ecology, vol. 15, no. 5, pp. 624–632, 2001.
[23]  D. A. Warner and R. Shine, “The adaptive significance of temperature-dependent sex determination: experimental tests with a short-lived lizard,” Evolution, vol. 59, no. 10, pp. 2209–2221, 2005.
[24]  F. J. Janzen, “The influence of incubation temperature and family on eggs, embryos, and hatchlings of the smooth softshell turtle (Apalone mutica),” Physiological Zoology, vol. 66, no. 3, pp. 349–373, 1993.
[25]  F. J. Janzen, “Expermental evidence for the evolutionary significance of temperature-dependent sex determination,” Evolution, vol. 49, no. 5, pp. 864–873, 1995.
[26]  J. S. Doody, “A test of the comparative influences of constant and fluctuating incubation temperatures on phenotypes of hatchling turtles,” Chelonian Conservation and Biology, vol. 3, pp. 529–531, 1999.
[27]  S. O'Steen and F. J. Janzen, “Embryonic temperature affects metabolic compensation and thyroid hormones in hatchling snapping turtles,” Physiological and Biochemical Zoology, vol. 72, no. 5, pp. 520–533, 1999.
[28]  A. C. Steyermark and J. R. Spotila, “Effects of maternal identity and incubation temperature on snapping turtle (Chelydra serpentina) metabolism,” Physiological and Biochemical Zoology, vol. 73, no. 3, pp. 298–306, 2000.
[29]  D. T. Booth, “Influence of incubation temperature on hatchling phenotype in reptiles,” Physiological and Biochemical Zoology, vol. 79, no. 2, pp. 274–281, 2006.
[30]  M. B. Thompson, “Patterns of metabolism in embryonic reptiles,” Respiration Physiology, vol. 76, no. 2, pp. 243–256, 1989.
[31]  M. B. Thompson, “Oxygen consumption and energetics of development in eggs of the leatherback turtle, Dermochelys coriacea,” Comparative Biochemistry and Physiology A, vol. 104, no. 3, pp. 449–453, 1993.
[32]  G. F. Birchard and C. L. Reiber, “Growth, metabolism, and chorioallantoic vascular density of developing snapping turtles (Chelydra serpentina): influence of temperature,” Physiological Zoology, vol. 68, no. 5, pp. 799–811, 1995.
[33]  M. J. Angilletta, R. S. Winters, and A. E. Dunham, “Thermal effects on the energetics of lizard embryos: implications for hatchling phenotypes,” Ecology, vol. 81, no. 11, pp. 2957–2968, 2000.
[34]  D. T. Booth, “Incubation of eggs of the Australian broad-shelled turtle, Chelodina expansa (Testudinata: Chelidae), at different temperatures: effects on pattern of oxygen consumption and hatchling morphology,” Australian Journal of Zoology, vol. 48, no. 4, pp. 369–378, 2000.
[35]  I. G. Vladimirova, T. A. Alekseeva, and M. V. Nechaeva, “Effect of temperature on the rate of oxygen consumption during the second half of embryonic and early postembryonic development of European pond turtle Emys orbicularis (Reptilia: Emydidae),” Biology Bulletin, vol. 32, no. 5, pp. 484–489, 2005.
[36]  I. G. Vladimirova, T. A. Alekseeva, and M. V. Nechaeva, “Growth and oxygen consumption in embryonic and early postembryonic development of European pond turtle Emys orbicularis (Reptilia: Emydidae),” Biology Bulletin, vol. 32, no. 2, pp. 172–178, 2005.
[37]  P. J. Whitehead and R. S. Seymour, “Patterns of metabolic rate in embryonic crocodilians Crocodylus johnstoni and Crocodylus porosus,” Physiological Zoology, vol. 63, pp. 334–352, 1990.
[38]  A. Leshem, A. Ar, and R. A. Ackerman, “Growth, water, and energy metabolism of the soft-shelled turtle (Trionyx triunguis) embryo: effects of temperature,” Physiological Zoology, vol. 64, pp. 568–594, 1991.
[39]  D. T. Booth, “Incubation of turtle eggs at different temperatures: do embryos compensate for temperature during development?” Physiological Zoology, vol. 71, no. 1, pp. 23–26, 1998.
[40]  D. T. Booth and K. Astill, “Incubation temperature, energy expenditure and hatchling size in the green turtle (Chelonia mydas), a species with temperature-sensitive sex determination,” Australian Journal of Zoology, vol. 49, no. 4, pp. 389–396, 2001.
[41]  P. W. Hochachka and G. N. Someri, Strategies of Biochemical Adaptation, Saunders, Philadelphia, Pa, USA, 1973.
[42]  C. H. Ernst, J. E. Lovich, and R. W. Barbour, Turtles of the United States and Canada, Smithsonian Institute Press, Washington, DC, USA, 1994.
[43]  D. B. Ligon and M. B. Lovern, “Temperature effects during early life stages of the alligator snapping turtle (Macrochelys temminckii),” Chelonian Conservation and Biology, vol. 8, no. 1, pp. 74–83, 2009.
[44]  M. A. Ewert, D. R. Jackson, and C. E. Nelson, “Patterns of temperature-dependent sex determination in turtles,” Journal of Experimental Zoology, vol. 270, pp. 3–15, 1994.
[45]  X. Ji, F. Chen, W. G. Du, and H. L. Chen, “Incubation temperature affects hatchling growth but not sexual phenotype in the Chinese soft-shelled turtle, Pelodiscus sinensis (Trionychidae),” Journal of Zoology, vol. 261, no. 4, pp. 409–416, 2003.
[46]  M. A. Ewert and J. M. Legler, “Hormonal induction of oviposition in turtles,” Herpetologica, vol. 34, pp. 314–318, 1978.
[47]  G. J. W. Webb, S. C. Manolis, P. J. Whitehead, and K. Dempsey, “The possible relationship between embryo orientation, opaque banding and the dehydration of albumen in crocodile eggs,” Copeia, vol. 1987, pp. 252–257, 1987.
[48]  G. C. Packard, M. J. Packard, K. Miller, and T. J. Boardman, “Influence of moisture, temperature, and substrate on snapping turtle eggs and embryos,” Ecology, vol. 68, no. 4, pp. 983–993, 1987.
[49]  D. Vleck, “Measurement of O2 consumption, CO2 production, and water vapor production in a closed system,” Journal of Applied Physiology, vol. 62, no. 5, pp. 2103–2106, 1987.
[50]  C .C. Peterson, “Paradoxically low metabolic rate of the diurnal gecko Rhoptropus afer,” Copeia, vol. 1990, pp. 233–237, 1990.
[51]  R. E. Gatten, “Aerobic metabolism in snapping turtles, Chelydra serpentina, after thermal acclimation,” Comparative Biochemistry and Physiology A, vol. 61, no. 2, pp. 325–337, 1978.
[52]  T. A. Alekseeva, “Effect of temperature on oxygen consumption by rainbow trout,” Ontogenez, vol. 18, pp. 308–311, 1987.
[53]  W. R. Barrionuevo and W. W. Burggren, “O2 consumption and heart rate in developing zebrafish (Danio rerio): influence of temperature and ambient O2,” American Journal of Physiology, vol. 276, no. 2 45-2, pp. R505–R513, 1999.
[54]  C. Díaz-Paniagua and M. Cuadrado, “Influence of incubation conditions on hatching success, embryo development and hatchling phenotype of common chameleon (Chamaeleo chamaeleon) eggs,” Amphibia Reptilia, vol. 24, no. 4, pp. 429–440, 2003.
[55]  M. J. Angilletta, V. Lee, and A. C. Silva, “Energetics of lizard embryos are not canalized by thermal acclimation,” Physiological and Biochemical Zoology, vol. 79, no. 3, pp. 573–580, 2006.
[56]  Z. H. Lin, X. Ji, L. G. Luo, and X. M. Ma, “Incubation temperature affects hatching success, embryonic expenditure of energy and hatchling phenotypes of a prolonged egg-retaining snake, Deinagkistrodon acutus (Viperidae),” Journal of Thermal Biology, vol. 30, no. 4, pp. 289–297, 2005.
[57]  G. W. Ferguson and C. H. Bohlen, “Demographic analysis: a tool for the study of natural selection of behavioral traits,” in Behavior and Neurology of Lizards, N. Greenberg and P. D. Maclean, Eds., pp. 227–243, Department of Health, Education and Welfare, NIMH, Rockville, Md, USA, 1978.
[58]  S. F. Fox, “Natural selection on behavioral phenotypes of the lizard Uta stansburiana,” Ecology, vol. 59, pp. 834–847, 1978.
[59]  I. R. Swingland and M. J. Coe, “The natural regulation of giant tortoise populations on Aldabra Atoll: recruitment,” Philosophical Transactions of the Royal Society B, vol. 28, pp. 177–188, 1979.
[60]  G. W. Ferguson and S. F. Fox, “Annual variation of survival advantage of large juvenile side- blotched lizards, Uta stansburiana: its causes and evolutionary significance,” Evolution, vol. 38, no. 2, pp. 342–349, 1984.
[61]  G. C. Packard, “The physiological and ecological importance of water to embryos of oviparous reptiles,” in Egg Incubation: Its Effects on Embryonic Development in Birds and Reptiles, D. C. Deeming and M. W. J. Ferguson, Eds., pp. 213–228, Cambridge University Press, Cambridge, Mass, USA, 1991.
[62]  R. Van Damme, D. Bauwens, F. Brana, and R. F. Verheyen, “Incubation temperature differentially affects hatching time, egg survival, and hatchling performance in the lizard Podarcis muralis,” Herpetologica, vol. 48, no. 2, pp. 220–228, 1992.
[63]  F. Bra?a and X. Ji, “Influence of incubation temperature on morphology, locomotor performance, and early growth of hatchling wall lizards (Podarcis muralis),” Journal of Experimental Zoology, vol. 286, no. 4, pp. 422–433, 2000.
[64]  D. A. Warner and R. M. Andrews, “Laboratory and field experiments identify sources of variation in phenotypes and survival of hatchling lizards,” Biological Journal of the Linnean Society, vol. 76, no. 1, pp. 105–124, 2002.
[65]  A. Haskell, T. E. Graham, C. R. Griffin, and J. B. Hestbeck, “Size related survival of headstarted redbelly turtles (Pseudemys rubriventris) in Massachusetts,” Journal of Herpetology, vol. 30, no. 4, pp. 524–527, 1996.
[66]  F. J. Janzen, J. K. Tucker, and G. L. Paukstis, “Experimental analysis of an early life-history stage: selection on size of hatchling turtles,” Ecology, vol. 81, no. 8, pp. 2290–2304, 2000.
[67]  F. J. Janzen, J. K. Tucker, and G. L. Paukstis, “Experimental analysis of an early life-history stage: avian predation selects for larger body size of hatchling turtles,” Journal of Evolutionary Biology, vol. 13, no. 6, pp. 947–954, 2000.
[68]  J. K. Tucker, “Body size and migration of hatchling turtles: inter- and intraspecific comparisons,” Journal of Herpetology, vol. 34, no. 4, pp. 541–546, 2000.
[69]  J. J. Kolbe and F. J. Janzen, “The influence of propagule size and maternal nest-site selection on survival and behaviour of neonate turtles,” Functional Ecology, vol. 15, no. 6, pp. 772–781, 2001.
[70]  J. D. Congdon, J. W. Gibbons, and J. L. Greene, “Parental investment in the chicken turtle (Deirochelys reticularia),” Ecology, vol. 64, no. 3, pp. 419–425, 1983.
[71]  N. I. Filoramo and F. J. Janzen, “Effects of hydric conditions during incubation on overwintering hatchlings of the red-eared slider turtle (Trachemys scripta elegans),” Journal of Herpetology, vol. 33, no. 1, pp. 29–35, 1999.

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