Unlike most vipers, female rattlesnakes (Crotalus atrox) continue to hunt and feed throughout pregnancy

Journal of Zoology

Volumn 289, Issue 2, 2013, Pages 101-110

  Schuett, G W ^a,b   Repp, R A ^c   Amarello, M ^d   Smith, C F ^b,e  

^a GEORGIA STATE UNIVERSITY   (United States)

^b The Copperhead Institute   (United States)

^c NATIONAL OPTICAL ASTRONOMY OBSERVATORY   (United States)

^d ARIZONA STATE UNIVERSITY   (United States)

^e WOFFORD COLLEGE   (United States)

Author keywords

Anorexia; Deserts; Life history; Reproduction; Reptile; Snake; Spatial ecology; Trade offs; Water balance.

Indexed keywords

ADULT; BODY SIZE; BREEDING SEASON; DESERT; DROUGHT; EMBRYO; FECUNDITY; FEEDING; FOOD CONSUMPTION; HIGH TEMPERATURE; LIFE HISTORY; NUTRIENT USE; PREGNANCY; RADIOTELEMETRY; RANGE SIZE; SNAKE; SURVIVAL; TRADE-OFF; WATER BUDGET;

ARIZONA; SONORAN DESERT; UNITED STATES;

ARIZONA (SNAKE); CICHLIDAE; CROTALUS; CROTALUS ATROX; MIROUNGA; REPTILIA; SERPENTES; VERTEBRATA; VIPERIDAE; VIPERINAE;

EID: 84872485932     PISSN: 09528369     EISSN: 14697998     Source Type: Journal    
DOI: 10.1111/j.1469-7998.2012.00969.x     Document Type: Article

References (89)

1. Adamo, S.A., Bartlett, A., Le, J., Spencer, N. & Sullivan, K. (2010). Illness-induced anorexia may reduce trade-offs between digestion and immune function. Anim. Behav. 79, 3-10.
2. Amarello, M., Nowak, E.M., Taylor, E.N., Schuett, G.W., Repp, R.A., Rosen, P.C. & Hardy, D.L. (2010). Potential environmental influences on variation in body size and sexual size dimorphism among Arizona populations of the western diamond-backed rattlesnake (Crotalus atrox). J. Arid Environ. 74, 1443-1449.
3. Bates, D. & Maechler, M. (2009). lme4: linear mixed-effects models using S4 classes. R package version 0.999375-32. http://CRAN.Rproject.org/package=lme4.
4. Beaupre, S.J. (2002). Modeling time-energy allocation in vipers: individual responses to environmental variation and implications for populations. In Biology of the vipers: 463-482. Schuett, G.W., Höggren, H., Douglas, M.E. & Greene, H.W. (Eds). Eagle Mountain: Eagle Mountain Publishing, LC.
5. Beaupre, S.J. & Duvall, D. (1998). Variation in oxygen consumption of the western diamondback rattlesnake (Crotalus atrox): implications for sexual size dimorphism. J. Comp. Physiol. B. 168, 497-506.
6. Beck, D.D. (1995). Ecology and energetics of three sympatric rattlesnake species in the Sonoran Desert. J. Herpetol. 29, 211-223.
7. Birchard, G.F., Black, C.P., Schuett, G.W. & Black, V.D. (1984). Influence of pregnancy on oxygen consumption, heart rate, and hematology in the garter snake: implication for the cost of reproduction in live-bearing reptiles. Comp. Biochem. Physiol. A 77, 519-523.
8. Blackburn, D.G. & Flemming, A.F. (2012). Invasive implantation and intimate placental associations in a placentotrophic African lizard, Trachylepis ivensi (Scincidae). J. Morphol. 273, 137-159.
9. Blackburn, D.G. & Stewart, J.R. (2011). Viviparity and placentation in snakes. In Reproductive biology and phylogeny of snakes: 119-181. Aldridge, R.D. & Sever, D.M. (Eds). Enfield: Science Publishers.
10. Bonnet, X., Bradshaw, D. & Shine, R. (1998). Capital versus income breeding: an ectothermic perspective. Oikos 83, 333-342.
11. Bonnet, X., Naulleau, G., Shine, R. & Lourdais, O. (1999). What is the appropriate timescale for measuring costs of reproduction in a 'capital breeder' such as the aspic viper? Evol. Ecol. 13, 485-497.
12. Bonnet, X., Naulleau, G., Shine, R. & Lourdais, O. (2001). Short-term versus long-term effects of food intake on reproductive output in a viviparous snake, Vipera aspis. Oikos 92, 297-308.
13. Bradshaw, S.D. (1997). Homeostasis in desert reptiles. New York: Springer.
14. Brischoux, F., Bonnet, X. & Shine, R. (2011). Conflicts between feeding and reproduction in amphibious snakes (sea kraits, Laticauda spp.). Austral Ecol. 36, 46-52.
15. Brivio, F., Grignolio, F. & Apollonio, M. (2010). To feed or not to feed? Testing different hypotheses on rut-induced hypophagia in a mountain ungulate. Ethology 116, 406-415.
16. Brodie, E.D., III (1989). Behavioral modification as a means of reducing the cost of reproduction. Am. Nat. 134, 225-238.
17. Brown, D.E. (1994). Biotic communities of the American southwest-United States and Mexico. Salt Lake City: University of Utah Press.
18. Bull, J. & Shine, R. (1979). Iteroparous animals that skip opportunities for reproduction. Am. Nat. 114, 296-303.
19. Campbell, J.A. & Lamar, W.W. (2004). The venomous reptiles of the western hemisphere, two vols. Ithaca: Cornell University Press.
20. Castoe, T.A., Spencer, C.L. & Parkinson, C.L. (2007). Phylogeographic structure and historical demography of the western diamondback rattlesnake (Crotalus atrox): a perspective on North American desert biogeography. Mol. Phylogenet. Evol. 42, 193-212.
21. Charland, M.B. & Gregory, P.T. (1990). The influence of female reproductive status on thermoregulation in a viviparous snake, Crotalus viridis. Copeia 1990, 1089-1098.
22. Cloudsley-Thompson, J.L. (1971). The temperature and water relations of reptiles. London: Merrow Publishing.
23. Clutton-Brock, T. & Sheldon, B.C. (2010). Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends Ecol. Evol. 25, 562-573.
24. Cox, R.M., Parker, E.U., Cheney, D.M., Liebl, A.L., Martin, L.B. & Calsbeek, R. (2010). Experimental evidence for physiological costs underlying the trade-off between reproduction and survival. Funct. Ecol. 24, 1262-1269.
25. Crane, A.L. & Greene, B.D. (2008). The effect of reproductive condition on thermoregulation in female Agkistrodon piscivorus near the northwestern range limit. Herpetologica 64, 156-157.
26. Dunham, A.E., Miles, D.B. & Reznick, D.N. (1988). Life history patterns in reptiles. In Biology of the Reptilia, vol 16, ecology B, defense and life history: 441-522. Gans, C. & Huey, R.B. (Eds). Ann Arbor: Branta.
27. Duvall, D., Arnold, S.J. & Schuett, G.W. (1992). Pitviper mating systems: ecological potential, sexual selection, and microevolution. In Biology of the pitvipers: 321-336. Campbell, J.A. & Brodie, E.D., Jr (Eds). Tyler: Selva.
28. Epple, A.E. & Epple, L.E. (1995). Plants of Arizona. Helena: Falcon Publishing.
29. Fitch, H.S. (1960). Autecology of the copperhead. Univ. Kansas Publ. Mus. Nat. Hist. 13, 85-288.
30. Fitch, H.S. (1970). Reproductive cycles of lizards and snakes. Univ. Kansas Publ. Mus. Nat. Hist. Publ. 52, 1-247.
31. Fitch, H.S. & Pisani, G.R. (1993). Life history traits of the western diamondback rattlesnake (Crotalus atrox) studied from roundup samples in Oklahoma. Occ. Pap. Univ. Kansas Mus. Nat. Hist. 156, 1-24.
32. Gardner-Santana, L.C. & Beaupre, S.J. (2009). Timber rattlesnakes (Crotalus horridus) exhibit elevated and less variable body temperatures during pregnancy. Copeia 2009, 363-368.
33. Gignac, A. & Gregory, P.T. (2005). The effects of body size, age, and food intake during pregnancy on reproductive traits of a viviparous snake, Thamnophis ordinoides. Ecoscience 12, 236-243.
34. Graves, B.M. & Duvall, D. (1995). Aggregation of squamate reptiles associated with gestation, oviposition, and parturition. Herpetol. Monogr. 9, 102-119.
35. Greene, H.W., May, P.G., Hardy, D.L., Sr, Sciturro, J.M. & Farrell, T.M. (2002). Parental behavior by vipers. In Biology of the vipers: 179-206. Schuett, G.W., Höggren, M., Douglas, M.E. & Greene, H.W. (Eds). Eagle Mountain: Eagle Mountain Publishing.
36. Gregory, P.T., Crampton, L.H. & Skebo, K.M. (1999). Conflicts and interactions among reproduction, thermoregulation and feeding in viviparous reptiles: are gravid females anorexic? J. Zool. 248, 231-241.
37. Harrison, X.A., Blount, J.D., Inger, R., Norris, D.R. & Bearhop, S. (2011). Carry-over effects as drivers of fitness differences in animals. J. Anim. Ecol. 80, 4-18.
38. Harshman, L.G. & Zera, A.J. (2006). The cost of reproduction: the devil in the details. Trends Ecol. Evol. 22, 80-86.
39. Hooge, P.N., Eichenlaub, W. & Solomon, E. (1999). The animal movement program. Anchorage: USGS, Alaska Biological Science Center.
40. Johnson, M.A., Caton, J.L., Cohen, R.E., Vandecar, J.R. & Wade, J. (2010). The burden of motherhood: the effect of reproductive load on female lizard locomotor, foraging, and social behavior. Ethology 116, 1217-1225.
41. Jönsson, I. (1997). Capital and income breeding as alternative tactics of resources use in reproduction. Oikos 78, 57-66.
42. Keenlyne, K.D. (1972). Sexual differences in feeding habits of Crotalus horridus horridus. J. Herpetol. 6, 234-237.
43. Kenward, R.E. (2001). A manual for wildlife radio tagging. San Diego: Academic Press.
44. Klauber, L.M. (1956). Rattlesnakes: their habits, life histories, and influence on mankind, two vols. Berkeley and Los Angeles: University of California Press.
45. Ladyman, M. & Bradshaw, D. (2003). The influence of dehydration on the thermal preferences of the western tiger snake, Notechis scutatus. J. Comp. Physiol. B 173, 239-246.
46. Lourdais, O., Bonnet, X. & Doughty, P. (2002). Costs of anorexia during pregnancy in a viviparous snake (Vipera aspis). J. Exp. Zool. 292, 487-493.
47. Macartney, J.M. & Gregory, P.T. (1988). Reproductive biology of female rattlesnakes (Crotalus viridis) in British Columbia. Copeia 1988, 47-57.
48. McCue, M.D. (2007). Snakes survive starvation by employing supply- and demand-side economic strategies. Zoology 110, 318-327.
49. Mock, C.J. (1996). Climatic controls and spatial variation of precipitation in the western United States. J. Climate 9, 1111-1125.
50. Mrosovsky, N. & Sherry, D.F. (1980). Animal anorexias. Science 207, 837-842.
51. Murphy, B.F. & Thompson, M.B. (2011). A review of the evolution of viviparity in squamate reptiles: the past, present and future role of molecular biology and genomics. J. Comp. Physiol. B 181, 575-594.
52. Nagy, K.A. (1987). How do desert animals get enough water? Progress in desert research: 89-98. Berkofsky, L. & Wertele, M.G. (Eds). Totowa: Roman and Littlefield.
53. Nowak, E.M., Theimer, T.C. & Schuett, G.W. (2008). Functional and numerical responses of predators: where do vipers fit in the traditional paradigms? Biol. Rev. 83, 601-620.
54. Phillips, S.J. & Comus, P.W. (2000). A natural history of the Sonoran Desert. Berkeley and Los Angeles: The University of California Press.
55. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & the R Development Core Team (2010). nlme: linear and nonlinear mixed effects models. R package version 3, 1-97.
56. R Development Core Team (2010). R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. ISBN 3-900051-07-0, URL http://www.R-project.org.
57. Reinert, H.K. (1992). Radiotelemetric field studies of pitvipers: data acquisition and analysis. In Biology of the pitvipers: 185-198. Campbell, J.A. & Brodie, E.D., Jr (Eds). Tyler: Selva.
58. Reiserer, R.S. (2001). Evolution of life histories in rattlesnakes. Unpublished dissertation, University of California, Berkeley, 256 pp.
59. Reiserer, R.S., Schuett, G.W. & Earley, R.L. (2008). Dynamic aggregations of newborn sibling rattlesnakes exhibit stable thermoregulatory properties. J. Zool. 274, 277-283.
60. Repp, R.A. & Schuett, G.W. (2008). Western diamond-backed rattlesnakes, Crotalus atrox (Serpentes: Viperidae), gain water by harvesting and drinking rain, sleet, and snow. Southwest. Nat. 53, 108-114.
61. Repp, R.A. & Schuett, G.W. (2009). Natural history notes. Crotalus atrox (western diamond-backed rattlesnake). Adult predation on lizards. Herpetol. Rev. 40, 353-354.
62. Roff, D.A. (2002). Life history evolution. 2nd edn. Sunderland: Sinauer Associates.
63. Rosen, P.C. & Goldberg, S.R. (2002). Female reproduction in the western diamond-backed rattlesnake, Crotalus atrox (Serpentes: Viperidae), from Arizona. Texas J. Sci. 54, 347-356.
64. Ross, M.G. & Desai, M. (2005). Gestational programming: population survival effects of drought and famine during pregnancy. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R25-R33.
65. Row, J.R. & Blouin-Demers, G. (2006). Kernels are not accurate estimators of home range size for herpetofauna. Copeia 2006, 797-802.
66. Schuett, G.W., Repp, R.A. & Hoss, S.K. (2011). Frequency of reproduction in female western diamond-backed rattlesnakes (Crotalus atrox) from the Sonoran Desert of Arizona is variable in individuals: potential role of rainfall and prey densities. J. Zool. 284, 105-113.
67. Schultz, T.J., Webb, J.K. & Christian, K.A. (2008). The physiological cost of pregnancy in a tropical viviparous snake. Copeia 2008, 637-642.
68. Seigel, R.A., Huggins, M.M. & Ford, N.B. (1987). Reduction in locomotor ability as a cost of reproduction in gravid snakes. Oecologia 73, 481-485.
69. Shine, R. (1980). 'Costs' of reproduction in reptiles. Oecologia 46, 92-100.
70. Shine, R. (2005). Life-history evolution in reptiles. Ann. Rev. Ecol. Evol. Syst. 36, 23-46.
71. Shine, R. & Schwarzkopf, L. (1992). The evolution of reproductive effort in lizards and snakes. Evolution 46, 62-75.
72. Smith, C.F., Schuett, G.W., Earley, R.L. & Schwenk, K. (2009). The spatial and reproductive ecology of the copperhead (Agkistrodon contortrix) at the northeastern extreme of its range. Herpetological Monographs 23, 45-73.
73. Spencer, C.L. (2003). Geographic variation in the morphology, diet and reproduction of a widespread pitviper, the western diamondback rattlesnake (Crotalus atrox). Unpublished dissertation, University of Texas at Arlington.
74. Spencer, C.L. (2008). Geographic variation in western diamond-backed rattlesnake (Crotalus atrox) morphology. In The biology of rattlesnakes: 55-78. Hayes, W.K., Beaman, K.R., Cardwell, M.D. & Bush, S.P. (Eds). Linda: Loma Linda Press.
75. Stearns, S.C. (1992). The evolution of life histories. Oxford: Oxford University Press.
76. Stephens, P.A., Boyd, I.L., McNamara, J.M. & Houston, A.I. (2009). Capital breeding and income breeding: their meaning, measurement, and worth. Ecology 90, 2057-2067.
77. Stewart, J.R., Blackburn, D.G., Baxter, D.C. & Hoffman, L.H. (1990). Nutritional provision to embryos in a predominantly lecithotrophic placental reptile, Thamnophis ordinoides (Squamata: Serpentes). Physiol. Zool. 63, 722-734.
78. Tate, K.B., Eme, J., Swart, J., Conlon, J.M. & Crossley, D.A., II (2012). Effects of dehydration on cardiovascular development in the embryonic American alligator (Alligator mississipiensis). Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 162, 252-258.
79. Taylor, E.N. & DeNardo, D.F. (2005). Reproductive ecology of western diamond-backed rattlesnakes (Crotalus atrox) in the Sonoran Desert. Copeia 2005, 152-158.
80. Taylor, E.N. & DeNardo, D.F. (2011). Hormone and reproductive cycles in snakes. In Hormones and reproduction in vertebrates, vol. 2, reptiles: 355-372. Norris, D.O. & Lopez, K.H. (Eds). San Diego: Academic Press.
81. Taylor, E.N., Malawy, M.A., Browning, D.M., Lemar, S.V. & DeNardo, D.F. (2005). Effects of food supplementation on the physiological ecology of female western diamond-backed rattlesnakes (Crotalus atrox). Oecologia 144, 206-213.
82. Thompson, M.B. & Speake, B.K. (2006). A review of the evolution of viviparity in lizards: structure, function, and physiology of the placenta. J. Comp. Physiol. B 176, 179-189.
83. Van Dyke, J.U. & Beaupre, S.J. (2011). Bioenergetic components of reproductive effort in viviparous snakes: costs of vitellogenesis exceed costs of pregnancy. Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 160, 504-515.
84. Van Dyke, J.U. & Beaupre, S.J. (2012). Stable isotope tracer reveals that viviparous snakes transport amino acids to offspring during gestation. J. Exp. Biol. 215, 760-765.
85. Webber, M.M., Glaudas, X. & Rodriguez-Robles, J.A. (2012). Do sidewinder rattlesnakes (Crotalus cerastes, Viperidae) cease feeding during the breeding season? Copeia 2012, 100-105.
86. Weeks, S.C. (1996). The hidden cost of reproduction: reduced food intake caused by spatial constraints in the body cavity. Oikos 75, 345-349.
87. Wickham, H. (2009). ggplot2: an implementation of the grammar of graphics. http://had.co.nz/ggplot2.
88. Winne, C.T. & Hopkins, W.A. (2006). Influence of sex and reproductive condition on terrestrial and aquatic locomotor performance in the semi-aquatic snake Seminatrix pygaea. Funct. Ecol. 20, 1054-1061.
89. Winne, C.T., Willson, J.D. & Gibbons, J.W. (2006). Income breeding allows an aquatic snake Seminatrix pygaea to reproduce normally following prolonged drought-induced aestivation. J. Anim. Ecol. 75, 1352-1360.