Reproductive allocation strategies: A long-term study on proximate factors and temporal adjustments in a viviparous lizard

Oecologia

Volumn 171, Issue 1, 2013, Pages 141-151

  Bleu, Josefa ^a,b   Le Galliard, Jean François ^a,c   Fitze, Patrick S ^d,e   Meylan, Sandrine ^a,f   Clobert, Jean ^c   Massot, Manuel ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b UNIVERSITÉ DE SAVOIE   (France)

^c CNRS   (France)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

^e FUNDACIÓN ARAID   (Spain)

^f SORBONNE UNIVERSITÉ   (France)

Author keywords

Capital breeder; Energy allocation; Phenotypic plasticity; Trade off; Viviparity

Indexed keywords

EVOLUTIONARILY STABLE STRATEGY; FITNESS; LIFE HISTORY TRAIT; LIZARD; LONG-TERM CHANGE; OPTIMIZATION; PARENT-OFFSPRING INTERACTION; PHENOTYPIC PLASTICITY; REPRODUCTIVE COST; TRADE-OFF; VIVIPARITY;

SQUAMATA; ZOOTOCA VIVIPARA;

EID: 84872140282     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-012-2401-1     Document Type: Article

References (65)

1. Adolph SC, Porter WP (1993) Temperature, activity, and lizard life histories. Am Nat 142: 273-295. doi: 10. 1086/285538.
2. Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, Sorci G (2004) Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol Lett 7: 363-368. doi: 10. 1111/j. 1461-0248. 2004. 00594. x.
3. Avery RA (1974) Storage lipids in the lizard Lacerta vivipara: a quantitative study. J Zool 173: 419-425. doi: 10. 1111/j. 1469-7998. 1974. tb04124. x.
4. Avery RA (1975) Clutch size and reproductive effort in the lizard Lacerta vivipara Jacquin. Oecologia 19: 165-170. doi: 10. 1007/BF00369099.
5. Bauwens D (1981) Survivorship during hibernation in the European common lizard, Lacerta vivipara. Copeia 1981: 741-744. doi: 10. 2307/1444592.
6. Bauwens D, Verheyen RF (1985) The timing of reproduction in the lizard Lacerta vivipara: differences between individual females. J Herpetol 19: 353-364. doi: 10. 2307/1564263.
7. Berglund A, Rosenqvist G (1986) Reproductive costs in the prawn Palaemon adspersus: effects on growth and predator vulnerability. Oikos 46: 349-354. doi: 10. 2307/3565833.
8. Bleu J, Le Galliard J-F, Meylan S, Massot M, Fitze PS (2011) Mating does not influence reproductive investment, in a viviparous lizard. J Exp Zool 315A: 458-464. doi: 10. 1002/jez. 693.
9. Bleu J, Massot M, Haussy C, Meylan S (2012) Experimental litter size reduction reveals costs of gestation and delayed effects on offspring in a viviparous lizard. Proc R Soc B 279: 489-498. doi: 10. 1098/rspb. 2011. 0966.
10. 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. doi: 10. 1034/j. 1600-0706. 2001. 920212. x.
11. Brown CA (2003) Offspring size-number trade-offs in scorpions: an empirical test of the van Noordwijk and de Jong model. Evolution 57: 2184-2190. doi: 10. 1111/j. 0014-3820. 2003. tb00397. x.
12. Cadby CD, While GM, Hobday AJ, Uller T, Wapstra E (2010) Multi-scale approach to understanding climate effects on offspring size at birth and date of birth in a reptile. Integr Zool 5: 164-175. doi: 10. 1111/j. 1749-4877. 2010. 00201. x.
13. Chamaillé-Jammes S, Massot M, Aragón P, Clobert J (2006) Global warming and positive fitness response in mountain populations of common lizards Lacerta vivipara. Global Change Biol 12: 392-402. doi: 10. 1111/j. 1365-2486. 2005. 01088. x.
14. Charnov EL, Downhower JF, Brown LP (1995) Optimal offspring sizes in small litters. Evol Ecol 9: 57-63. doi: 10. 1007/BF01237697.
15. Christians JK (2000) Trade-offs between egg size and number in waterfowl: an interspecific test of the van Noordwijk and de Jong model. Funct Ecol 14: 497-501. doi: 10. 1046/j. 1365-2435. 2000. 00444. x.
16. Clobert J, Massot M, Lecomte J, Sorci G, De Fraipont M, Barbault R (1994) Determinants of dispersal behavior: the common lizard as a case study. In: Vitt LJ, Pianka ER (eds) Lizard ecology: historical and experimental perspectives. Princeton University Press, Princeton, pp 183-206.
17. Clutton-Brock TH, Guinness FE, Albon SD (1983) The costs of reproduction to red deer hinds. J Anim Ecol 52: 367-383. doi: 10. 2307/4560.
18. Cox RM, Calsbeek R (2010) Severe costs of reproduction persist in Anolis lizards despite the evolution of a single-egg clutch. Evolution 64: 1321-1330. doi: 10. 1111/j. 1558-5646. 2009. 00906. x.
19. Cox RM, Parker EU, Cheney DM, Liebl AL, Martin LB, Calsbeek R (2010) Experimental evidence for physiological costs underlying the trade-off between reproduction and survival. Funct Ecol 24: 1262-1269. doi: 10. 1111/j. 1365-2435. 2010. 01756. x.
20. Doughty P, Shine R (1997) Detecting life history trade-offs: measuring energy stores in "capital" breeders reveals costs of reproduction. Oecologia 110: 508-513. doi: 10. 1007/s004420050187.
21. Doughty P, Shine R (1998) Reproductive energy allocation and long-term energy stores in a viviparous lizard (Eulamprus tympanum). Ecology 79: 1073-1083. doi: 10. 1890/0012-9658(1998)079[1073: REAALT]2. 0. CO; 2.
22. Festa-Bianchet M (1998) Condition-dependent reproductive success in bighorn ewes. Ecol Lett 1: 91-94. doi: 10. 1046/j. 1461-0248. 1998. 00023. x.
23. French SS, DeNardo DF, Moore MC (2007) Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction? Am Nat 170: 79-89. doi: 10. 1086/518569.
24. Glazier DS (1999) Trade-offs between reproductive and somatic (storage) investments in animals: a comparative test of the van Noordwijk and De Jong model. Evol Ecol 13: 539-555. doi: 10. 1023/A: 1006793600600.
25. González-Suárez M, Mugabo M, Decencière B, Perret S, Claessen D, Le Galliard J-F (2011) Disentangling the effects of predator body size and prey density on prey consumption in a lizard. Funct Ecol 25: 158-165. doi: 10. 1111/j. 1365-2435. 2010. 01776. x.
26. Gregory PT (2006) Influence of income and capital on reproduction in a viviparous snake: direct and indirect effects. J Zool 270: 414-419. doi: 10. 1111/j. 1469-7998. 2006. 00149. x.
27. Gustafsson L, Nordling D, Andersson MS, Sheldon BC, Qvarnström A (1994) Infectious diseases, reproductive effort and the cost of reproduction in birds. Philos Trans R Soc Lond B 346: 323-331. doi: 10. 1098/rstb. 1994. 0149.
28. Hadley GL, Rotella JJ, Garrott RA (2007) Evaluation of reproductive costs for Weddell seals in Erebus Bay, Antarctica. J Anim Ecol 76: 448-458. doi: 10. 1111/j. 1365-2656. 2007. 01219. x.
29. Hanssen SA, Hasselquist D, Folstad I, Erikstad KE (2005) Cost of reproduction in a long-lived bird: incubation effort reduces immune function and future reproduction. Proc R Soc B 272: 1039-1046. doi: 10. 1098/rspb. 2005. 3057.
30. Hare KM, Cree A (2010) Exploring the consequences of climate-induced changes in cloud cover on offspring of a cool-temperate viviparous lizard. Biol J Linn Soc 101: 844-851. doi: 10. 1111/j. 1095-8312. 2010. 01536. x.
31. Houston AI, Stephens PA, Boyd IL, Harding KC, McNamara JM (2007) Capital or income breeding? A theoretical model of female reproductive strategies. Behav Ecol 18: 241-250. doi: 10. 1093/beheco/arl080.
32. Huey RB (1982) Temperature, physiology, and the ecology of reptiles. In: Gans C, Pough FH (eds) Biology of the reptilia. Academic Press, New-York, pp 25-91.
33. 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. doi: 10. 1007/s004420100776.
34. Koivula M, Koskela E, Mappes T, Oksanen TA (2003) Cost of reproduction in the wild: manipulation of reproductive effort in the bank vole. Ecology 84: 398-405. doi: 10. 1890/0012-9658(2003)084[0398: CORITW]2. 0. CO; 2.
35. Landwer AJ (1994) Manipulation of egg production reveals costs of reproduction in the tree lizard (Urosaurus ornatus). Oecologia 100: 243-249. doi: 10. 1007/BF00316951.
36. Le Galliard J-F, Cote J, Fitze PS (2008) Lifetime and intergenerational fitness consequences of harmful male interactions for female lizards. Ecology 89: 56-64. doi: 10. 1890/06-2076. 1.
37. Le Galliard J-F, Marquis O, Massot M (2010) Cohort variation, climate effects and population dynamics in a short-lived lizard. J Anim Ecol 79: 1296-1307. doi: 10. 1111/j. 1365-2656. 2010. 01732. x.
38. Le Galliard J-F, Massot M, Baron J-P, Clobert J (2012) Ecological effects of climate change on European reptiles. In: Brodie JF, Post E, Doak D (eds) Conserving wildlife populations in a changing climate. University of Chicago Press, Chicago.
39. Lourdais O, Bonnet X, Shine R, Denardo D, Naulleau G, Guillon M (2002) Capital-breeding and reproductive effort in a variable environment: a longitudinal study of a viviparous snake. J Anim Ecol 71: 470-479. doi: 10. 1046/j. 1365-2656. 2002. 00612. x.
40. Lourdais O, Bonnet X, Shine R, Taylor EN (2003) When does a reproducing female viper (Vipera aspis) "decide" on her litter size? J Zool 259: 123-129. doi: 10. 1017/s0952836902003059.
41. Lourdais O, Shine R, Bonnet X, Guillon M, Naulleau G (2004) Climate affects embryonic development in a viviparous snake, Vipera aspis. Oikos 104: 551-560. doi: 10. 1111/j. 0030-1299. 2004. 12961. x.
42. Marquis O, Massot M, Le Galliard J-F (2008) Intergenerational effects of climate generate cohort variation in lizard reproductive performance. Ecology 89: 2575-2583. doi: 10. 1890/07-1211. 1.
43. Massot M, Clobert J (1995) Influence of maternal food availability on offspring dispersal. Behav Ecol Sociobiol 37: 413-418. doi: 10. 1007/BF00170589.
44. Massot M, Clobert J, Montes-Poloni L, Haussy C, Cubo J, Meylan S (2011) An integrative study of ageing in a wild population of common lizards. Funct Ecol 25: 848-858. doi: 10. 1111/j. 1365-2435. 2011. 01837. x.
45. Mugabo M, Marquis O, Perret S, Le Galliard J-F (2011) Direct and socially mediated effects of food availability late in life on life-history variation in a short-lived lizard. Oecologia 166: 949-960. doi: 10. 1007/s00442-011-1933-0.
46. Panigel M (1956) Contribution à l'étude de l'ovoviviparité chez les reptiles: gestation et parturition chez le lézard vivipare Zootoca vivipara. Ann Sci Nat Zool 18: 569-668.
47. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New-York.
48. Qualls CP, Shine R (1995) Maternal body-volume as a constraint on reproductive output in lizards: evidence from the evolution of viviparity. Oecologia 103: 73-78. doi: 10. 1007/BF00328427.
49. Reading CJ (2004) The influence of body condition and prey availability on female breeding success in the smooth snake (Coronella austriaca Laurenti). J Zool 264: 61-67. doi: 10. 1017/S0952836904005515.
50. Richner H, Tripet F (1999) Ectoparasitism and the trade-off between current and future reproduction. Oikos 86: 535-538. doi: 10. 2307/3546657.
51. Roff DA (2002) Life history evolution. Sinauer Assoc, Sunderland.
52. Shine R (2005) Life-history evolution in reptiles. Annu Rev Ecol Evol Syst 36: 23-46. doi: 10. 1146/annurev. ecolsys. 36. 102003. 152631.
53. Shine R, Downes SJ (1999) Can pregnant lizards adjust their offspring phenotypes to environmental conditions? Oecologia 119: 1-8. doi: 10. 1007/s004420050754.
54. Shine R, Harlow P (1993) Maternal thermoregulation influences offspring viability in a viviparous lizard. Oecologia 96: 122-127. doi: 10. 1007/BF00318039.
55. Stephens PA, Boyd IL, McNamara JM, Houston AI (2009) Capital breeding and income breeding: their meaning, measurement, and worth. Ecology 90: 2057-2067. doi: 10. 1890/08-1369. 1.
56. Stewart JR, Ecay TW, Heulin B (2009) Calcium provision to oviparous and viviparous embryos of the reproductively bimodal lizard Lacerta (Zootoca) vivipara. J Exp Biol 212: 2520-2524. doi: 10. 1242/jeb. 030643.
57. Swain R, Jones SM (2000) Maternal effects associated with gestation conditions in a viviparous lizard, Niveoscincus metallicus. Herpetol Monogr 14: 432-440. doi: 10. 2307/1467056.
58. Uller T, Olsson M (2005) Trade-offs between offspring size and number in the lizard Lacerta vivipara: a comparison between field and laboratory conditions. J Zool 265: 295-299. doi: 10. 1017/s0952836904006326.
59. Uller T, While GM, Wapstra E, Warner DA, Goodman BA, Schwarzkopf L, Langkilde T, Doughty P, Radder RS, Rohr DH, Bull CM, Shine R, Olsson M (2009) Evaluation of offspring size-number invariants in 12 species of lizard. J Evol Biol 22: 143-151. doi: 10. 1111/j. 1420-9101. 2008. 01629. x.
60. Uller T, While GM, Cadby CD, Harts A, O'Connor K, Pen I, Wapstra E (2011) Altitudinal divergence in maternal thermoregulatory behaviour may be driven by differences in selection on offspring survival in a viviparous lizard. Evolution 65: 2313-2324. doi: 10. 1111/j. 1558-5646. 2011. 01303. x.
61. van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128: 137-142. doi: 10. 1086/284547.
62. Wapstra E (2000) Maternal basking opportunity affects juvenile phenotype in a viviparous lizard. Funct Ecol 14: 345-352. doi: 10. 1046/j. 1365-2435. 2000. 00428. x.
63. Warner DA, Bonnet X, Hobson KA, Shine R (2008) Lizards combine stored energy and recently acquired nutrients flexibly to fuel reproduction. J Anim Ecol 77: 1242-1249. doi: 10. 1111/j. 1365-2656. 2008. 01442. x.
64. Webb JK, Shine R, Christian KA (2006) The adaptive significance of reptilian viviparity in the tropics: testing the maternal manipulation hypothesis. Evolution 60: 115-122. doi: 10. 1554/05-460. 1.
65. Winkler DW, Wallin K (1987) Offspring size and number: a life history model linking effort per offspring and total effort. Am Nat 129: 708-720. doi: 10. 1086/284667.