Geographic variation in reproductive traits and trade-offs between size and number of eggs of the Chinese cobra (Naja atra)

Biological Journal of the Linnean Society

Volumn 85, Issue 1, 2005, Pages 27-40

  Ji, Xiang ^a,b   Wang, Zu Wang ^c  

^a NANJING NORMAL UNIVERSITY   (China)

^b HANGZHOU NORMAL COLLEGE   (China)

^c INSTITUTE OF ZOOLOGY   (China)

Author keywords

Clutch size; Egg size; Reproductive investment; Size number trade off

Indexed keywords

CLUTCH SIZE; EGG SIZE; GEOGRAPHICAL VARIATION; REPRODUCTIVE COST; SNAKE; TRADE-OFF;

ASIA; CHINA; EASTERN HEMISPHERE; EURASIA; FAR EAST; WORLD;

ATRA; ELAPIDAE; NAJA ATRA; SERPENTES;

EID: 18644365277     PISSN: 00244066     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2005.00470.x     Document Type: Article

References (59)

1. Adolph SC, Porter WP. 1996. Growth, seasonality, and lizard life histories: age and size at maturity. Oikos 77: 267-278.
2. Agrawall AF, Brodie ED, Brown J. 2001. Parent-offspring coadaptation and the dual genetic control of maternal care. Science 292: 1710-1712.
3. Andrews RM. 1982. Patterns of growth in reptiles. In: Gans C, Pough FH, eds. Biology of the Reptilia, Vol. 12. New York: Academic Press, 273-320.
4. Ballinger RE. 1977. Reproductive strategies: food availability as a source of proximal variation in a lizard. Ecology 58: 628-635.
5. Ballinger RE. 1983. Life-history variations. In: Huey RB, Pianka ER, Tinkle TW, eds. Lizard ecology: studies of a model organism. Cambridge: Harvard University Press, 241-260.
6. Bernardo J. 1996. The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. American Zoologist 36: 216-236.
7. Berven KA, Gill DE. 1983. Interpreting geographic variation in life history traits. American Zoologist 23: 85-97.
8. Charnov EL, Downhower JF. 1995. A trade-off-invariant life history rule for optimal offspring size. Nature 376: 418-419.
9. Downhower JF, Charnov EL. 1998. A resource range invariant rule for optimal offspring size predicts of variability in parental phenotypes. Proceedings of the National Academy of Sciences, USA 95: 6028-6211.
10. Dunham AE, Miles DB, Reznick DN. 1988. Life history: life-history patterns in squamate reptiles. In: Gans C, Huey RB, eds. Biology of the Reptilia, Vol. 16. New York: Alan R. Liss, 443-515.
11. Einum S, Fleming IA. 1999. Maternal effects of egg size in brown trout (Salmo trutta): norms of reaction to environmental quality. Proceedings of the Royal Society, London B 266: 2095-2100.
12. Einum S, Fleming IA. 2000. Highly fecundity mothers sacrifice offspring survival to maximize fitness. Nature 405: 565-567.
13. Ferguson GW, Bohlen CH, Wooley HP. 1980. Sceloporus undulates: comparative life history and regulation of a Kansas population. Ecology 61: 312-322.
14. Ferguson GW, Fox SF. 1984. Annual variation of survival advantage of large juvenile side-blotched lizards, Uta stansburiana: its causes and evolutionary significance. Evolution 38: 342-349.
15. Ferguson GW, Snell HL. 1986. Endogenous control of seasonal change of egg, hatchling, and clutch size of the lizard Sceloporus undulatus garmani. Herpetologica 42: 185-191.
16. Fitch HS. 1985. Variation in clutch and litter size in New World reptiles. University of Kansas Museum of Natural History, Miscellaneous Publications. 76: 1-76.
17. Ford NB, Seigel RA. 1989. Phenotypic plasticity in reproductive traits: evidence from a viviparous snake. Ecology 70: 1768-1774.
18. Ford NB, Seigel RA. 1994. An experimental study of the trade-offs between age and size at maturity: effects of energy availability. Functional Ecology 8: 91-96.
19. Forsman A, Shine R. 1995. Parallel geographic variation in body shape and reproductive life history within the Australian scincid lizard Lampropholis delicata. Functional Ecology 9: 818-828.
20. Hu BQ, Huang MH, Ho SS, Chou SA, Hsieh TT, Tsai B. 1966. A preliminary report on some ecological observations of Akistrodon halys and Naja naja atra. Acta Zoologica Sinica 18: 187-194.
21. Huang MH, Jin YL. 1990. Reptilia. In: Huang MH, Jin YL, Cai CM, eds. Fauna of Zhejiang (Amphibia and Reptilia). Hangzhou: Zhejiang Science and Technology Publishing House, 153-281.
22. Ji X, Braña F. 2000. Among clutch variation in reproductive output and egg size in the wall lizard (Podarcis muralis) from a low land population of northern Spain. Journal of Herpetology 34: 54-60.
23. Ji X, Du WG. 2001. The effects of thermal and hydric conditions on incubating eggs and hatchling traits in the cobra, Naja naja atra. Journal of Herpetology 35: 186-194.
24. Ji X, Xu YG, Zheng XZ. 1994. Major energy reserves in the Chinese skink, Eumeces chinensis. Zoological Research 15: 59-64.
25. Ji X, Chen HL, Du WG, Zhu BQ. 2002a. Radiotelemetry of thermoregulation and thermal tolerance on Chinese cobras (Naja atra) overwintering in a laboratory enclosure. Acta Zoologica Sinica 48: 591-598.
26. Ji X, Sun PY, Xu XF, Du WG. 2000. Relationships among body size, clutch size, and egg size in five species of oviparous colubrid snakes from Zhoushan Islands, Zhejiang, China. Acta Zoologica Sinica 46: 138-145.
27. Ji X, Huang HY, Hu XZ, Du WG. 2002b. Geographic variation in female reproductive characteristics and egg incubation in the Chinese skink, Eumeces chinensis. Chinese Journal of Applied Ecology 13: 680-684.
28. Jordan MA, Snell HL. 2002. Life history trade-offs and phenotypic plasticity in the reproduction of Galapagos lava lizards (Microlophus delanonis). Oecologia 130: 44-52.
29. Lloyd DG. 1987. Selection of offspring size at independence and other size-versus-number strategies. American Naturalist 129: 800-817.
30. Mathies T, Andrews RM. 1995. Thermal and reproductive biology of high and low elevation populations of the lizard Sceloporus scalaris: implications for the evolution of viviparity. Oecologia 104: 101-111.
31. McGinley MA, Temme DH, Geber MA. 1987. Parental investment in offspring in variable environments: theoretical and empirical considerations. American Naturalist 130: 370-398.
32. National Research Council. 1985. Guide for the care and use of laboratory animals. NIH publication no. 85-23. Bethesda, MD: Public Health Service.
33. Niewiarowski PH, Dunham AE. 1994. The evolution of reproductive effort in squamate reptiles: costs, trade-offs, and assumptions reconsidered. Evolution 48: 137-145.
34. Olsson M, Shine R. 1997. The limits to reproductive output: offspring size versus number in the sand lizard (Lacerta agilis). American Naturalist 149: 179-188.
35. Parker GA, Begon M. 1986. Optimal egg size and clutch size: effects of environmental and maternal phenotype. American Naturalist 128: 573-592.
36. Reznick DN. 1991. Maternal effects in fish life histories. In: Dudley EC, ed. The unity of evolutionary biology: proceedings of the fourth IC-SEB. Oregon: Dioscorides Press, 780-793.
37. Roff DA. 1992. The evolution of life histories: theory and analysis. New York: Chapman & Hall.
38. Rohr DH. 1997. Demographic and life-history variation in two proximate populations of viviparous skink separated by a steep altitudinal gradient. Journal of Animal Ecology 66: 567-578.
39. Sakai S, Harada Y. 2004. Size-number trade-off and optimal offspring size for offspring produced sequentially using a fixed amount of reserves. Journal of Theoretical Biology 226: 253-264.
40. Sargent RC, Taylor PD, Gross MR. 1987. Parental care and the evolution of egg size in fishes. American Naturalist 129: 32-46.
41. Schwarzkopf L. 1994. Measuring trade-offs: A review of studies of costs of reproduction in lizard. In: Vitt LJ, Pianka ER, eds. Lizard ecology: historical and experimental perspectives. Princeton: Princeton University Press, 7-29.
42. Seigel RA, Fitch HS. 1985. Annual variation in reproduction in snakes in a fluctuating environment. Journal of Animal Ecology 54: 497-505.
43. Seigel RA, Ford NB. 1991. Phenotypic plasticity in the reproductive characteristics of an oviparous snake, Elaphe guttata: implications for life history studies. Herpetologica 47: 301-307.
44. Seigel RA, Ford NB. 1992. Effects of energy input on variation in clutch size and offspring size in a viviparous reptile. Functional Ecology 6: 382-385.
45. Shine R, Charnov EL. 1992. Patterns of survival, growth, and maturation in snakes and lizards. American Naturalist 139: 1257-1269.
46. Shine R, Schwarzkopf L. 1992. The evolution of reproductive effort in lizards and snakes. Evolution 46: 62-75.
47. Shine R, Seigel RA. 1996. A neglected life-history trait: clutch-size variance in snakes. Journal of Zoology, London 239: 209-223.
48. Sinervo B. 1990. The evolution of maternal investment in lizards: an experimental and comparative analysis of egg size and its effects on offspring performance. Evolution 44: 279-294.
49. Sinervo B, Adolph SC. 1989. Thermal sensitivity of growth rate in hatchling Sceloporus lizards: environmental, behavioral and genetic aspects. Oecologia 78: 11-419.
50. Sinervo B, Doughty P. 1996. Interactive effects of offspring size and timing of reproduction on offspring reproduction: experimental, maternal, and quantitative genetic aspects. Evolution 50: 1314-1327.
51. Sinervo B, Licht P. 1991. Proximate constraints on the evolution of egg size, number, and total clutch mass in lizards. Science 252: 1300-1302.
52. Smith CC, Fretwell SD. 1974. The optimal balance between size and number of offspring. American Naturalist 108: 499-506.
53. Stearns SC. 1989. The evolutionary significance of phenotype plasticity. Bioscience 39: 436-445.
54. Stearns SC. 1992. The evolutionary of life histories. Oxford: Oxford University Press.
55. Stearns SC, Crandall RE. 1981. Quantitative predictions of delayed maturity. Evolution 35: 455-463.
56. Tinkle DW, Wilbur HM, Tilley SC. 1970. Evolutionary strategies in lizard reproduction. Evolution 24: 55-74.
57. Wapstra E, Swain R. 2001. Geographic and annual variation in life-history traits in a temperate zone Australian skink. Journal of Herpetology 35: 194-203.
58. Winkler DW, Wallin K. 1987. Offspring size and offspring number: a life history model linking effort per offspring and total effort. American Naturalist 129: 708-720.
59. Wüster W, Golay P, Warrell DA. 1997. Synopsis of recent developments in venomous snake systematics. Toxicon 35: 319-340.