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Heterogeneity in individual quality overrides costs of reproduction in female reindeer

  • Behavioral Ecology - Original Paper
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Abstract

Reproductive allocation at one age is predicted to reduce the probability of surviving to the next year or to lead to a decrease in future reproduction. This prediction assumes that reproduction involves fitness costs. However, few empirical studies have assessed whether such costs may vary with the age at primiparity or might be overridden by heterogeneities in individual quality. We used data from 35 years’ monitoring of individually marked semi-domestic reindeer females to investigate fitness costs of reproduction. Using multi-state statistical models, we compared age-specific survival and reproduction among four reproductive states (never reproduced, experienced non-breeders, reproduced but did not wean offspring, and reproduced and weaned offspring) and among contrasted age at primiparity. We assessed whether reproductive costs occurred, resulting in a trade-off between current reproduction and future reproduction or survival, and whether early maturation was costly or rather reflected differences in individual quality of survival and reproduction capabilities. We did not find any evidence for fitness costs of reproduction in female reindeer. We found no cost of gestation and lactation in terms of future reproduction and survival. Conversely, successful breeders had higher survival and subsequent reproductive success than experienced non-breeders and unsuccessful breeders, independently of the age at primiparity. Moreover, it was beneficial to mature earlier, especially for females that successfully weaned their first offspring. Successful females at early primiparity remained successful throughout their life, clearly supporting the existence of marked among-female differences in quality. The weaning success peaked for multiparous females and was lower for first-time breeders, indicating a positive effect of experience on reproductive performance. Our findings emphasize an overwhelming importance of individual quality and experience to account for observed variation in survival and reproductive patterns of female reindeer that override trade-offs between current reproduction and future performance, at least in the absence of harsh winters.

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References

  • Albon SD, Mitchell B, Staines BW (1983) Fertility and body weight in female red deer: a density-dependent relationship. J Anim Ecol 52:969–980

    Article  Google Scholar 

  • Albon SD, Mitchell B, Huby BJ, Brown V (1986) Fertility in female red deer (Cervus elaphus): the effects of body composition, age and reproductive status. J Zool 209:447–460

    Google Scholar 

  • Bailey RC (1992) Why we should stop trying to measure the cost of reproduction correctly. Oikos 65:349–352

    Article  Google Scholar 

  • Barbraud C, Weimerskirch H (2005) Environmental conditions and breeding experience affect costs of reproduction in blue petrels. Ecology 86:682–692

    Article  Google Scholar 

  • Beauplet G, Barbraud C, Dabin W, Kussener C, Guinet C (2006) Age-specific survival and reproductive performances in fur seals: evidence of senescence and individual quality. Oikos 112:430–441

    Article  Google Scholar 

  • Bérubé CH, Festa-Bianchet M, Jorgenson JT (1996) Reproductive cost of sons and daughters in Rocky Mountain bighorn sheep. Behav Ecol 7:60–68

    Article  Google Scholar 

  • Bize P, Roulin A, Richner H (2002) Covariation between egg size and rearing condition determine offspring quality: an experiment with the Alpine swift. Oecologia 132:231–234

    Article  Google Scholar 

  • Bonnet X, Naulleau G, Shine R, Lourdais O (1999) What is the appropriate time scale for measuring costs of reproduction in a capital breeder such as the aspic viper? Evol Ecol 13:485–497

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Cam E, Link WA, Cooch EG, Monnat JY, Danchin E (2002) Individual covariation between life-history traits: seeing the trees despite the forest. Am Nat 159:96–105

    Article  PubMed  Google Scholar 

  • Cameron MR (1994) Reproductive pause by female caribou. J Mamm 75:10–13

    Article  Google Scholar 

  • Choquet R, Reboulet AM, Pradel R, Gimenez O, Lebreton JD (2005a) M-SURGE 1.7 user’s manual. CEFE, Montpellier, France

    Google Scholar 

  • Choquet R, Reboulet AM, Lebreton JD, Gimenez O, Pradel R (2005b) U-CARE 2.2 user’s manual. CEFE, Montpellier, France

    Google Scholar 

  • Clutton-Brock TH (1984) Reproductive effort and terminal investment in iteroparous animals. Am Nat 123:212–229

    Article  Google Scholar 

  • Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Oxford

    Google Scholar 

  • Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer. Behavior and ecology of two sexes. Wildlife behavior and ecology series. The University of Chicago Press, Chicago

    Google Scholar 

  • Clutton-Brock TH, Guinness FE, Albon SD (1983) The costs of reproduction to red deer hinds. J Anim Ecol 52:367–383

    Article  Google Scholar 

  • Clutton-Brock TH, Albon SD, Guinness FE (1989) Fitness costs of gestation and lactation in wild mammals. Nature 337:260–262

    Article  PubMed  CAS  Google Scholar 

  • Clutton-Brock TH, Stevenson IR, Marrow P, MacColl AD, Houston AI, McNamara JM (1996) Population fluctuations, reproductive costs and life-history tactics in female Soay sheep. J Anim Ecol 65:675–689

    Article  Google Scholar 

  • Clutton-Brock TH, Illius A, Wilson K, Grenfell BT, MacColl A, Albon SD (1997) Stability and instability in ungulate populations: an empirical analysis. Am Nat 149:195–219

    Article  Google Scholar 

  • Cobley ND, Croxall JP, Prince PA (1998) Individual quality and reproductive performance in the grey-headed albatross Diomedea chrysostoma. Ibis 140:315–322

    Article  Google Scholar 

  • Cody ML (1966) A general theory of clutch size. Evolution 20:174–184

    Article  Google Scholar 

  • Crocker DE, Williams JD, Costa DP, Le Boeuf BJ (2001) Maternal traits and reproductive effort in northern elephant seals. Ecology 82:3541–3555

    Google Scholar 

  • Descamps S, Boutin S, Berteaux D, Gaillard JM (2006) Best squirrels trade a long life for an early reproduction. Proc R Soc Lond Ser B 273:2369–2374

    Article  Google Scholar 

  • Doughty PD, Shine R (1997) Detecting life-history tradeoffs: measuring energy stores in “capital” breeders reveals costs of reproduction. Oecologia 110:508–513

    Article  Google Scholar 

  • Eloranta E, Nieminen M (1986) Calving of the experimental reindeer herd in Kaamanen during 1970–85. Rangifer Spec Issue 1:115–121

    Google Scholar 

  • Festa-Bianchet M (1989) Individual differences, parasites, and the costs of reproduction for bighorn ewes (Ovis canadensis). J Anim Ecol 58:755–795

    Google Scholar 

  • Festa-Bianchet M (1998) Condition-dependent reproductive success in bighorn ewes. Ecol Lett 1:91–94

    Article  Google Scholar 

  • Festa-Bianchet M, Jorgenson JT (1998) Selfish mothers: reproductive expenditure and resource availability in bighorn ewes. Behav Ecol 9:144–150

    Article  Google Scholar 

  • Festa-Bianchet M, Jorgenson JT, Lucherini M, Wishart WD (1995) Life-history consequences of variation in age of primiparity in bighorn ewes. Ecology 76:871–881

    Article  Google Scholar 

  • Festa-Bianchet M, Gaillard JM, Jorgenson JT (1998) Mass- and density-dependent reproductive success and reproductive costs in a capital breeder. Am Nat 152:367–379

    Article  PubMed  CAS  Google Scholar 

  • Fleming IA, Lamberg A, Jonsson B (1997) Effects of early experience on the reproductive performance of Atlantic salmon. Behav Ecol 8:470–480

    Article  Google Scholar 

  • Forslund P, Pärt T (1995) Age and reproduction in birds—hypotheses and test. Trends Ecol Evol 10:374–378

    Article  Google Scholar 

  • Gaillard JM, Sempere AJ, Boutin JM, Van Laere G, Boisaubert B (1992) Effects of age and body weight on the proportion of females breeding in a population of roe deer (Capreolus capreolus). Can J Zool 70:1541–1545

    Google Scholar 

  • Gaillard JM, Festa-Bianchet M, Yoccoz NG (1998) Population dynamics of large herbivores: variable recruitment with constant adult survival. Trends Ecol Evol 13:58–63

    Article  Google Scholar 

  • Gaillard JM, Festa-Bianchet M, Yoccoz NG, Loison A, Toïgo C (2000) Temporal variation in fitness components and population dynamics of large herbivores. Annu Rev Ecol Syst 31:367–393

    Article  Google Scholar 

  • Gaillard JM, Loison A, Festa-Bianchet M, Yoccoz NG, Solberg E (2003) Ecological correlates of life span in populations of large herbivores mammals. Pop Dev Rev (Suppl) 29:39–56

    Google Scholar 

  • Gerhart KL, Russell DE, van de Wetering D, White RG, Cameron RG (1997) Pregnancy of adult caribou (Rangifer tarandus): evidence for lactational infertility. J Zool 242:17–30

    Google Scholar 

  • Holand Ø, Røed KH, Mysterud A, Kumpula JM, Nieminen M, Smith ME (2003) The effect of sex ratio and male age structure on reindeer calving. J Wildl Manage 67:25–33

    Article  Google Scholar 

  • Holand Ø, Weladji RB, Gjøstein H, Kumpula J, Smith ME, Nieminen M, Røed KH (2004) Reproductive effort in relation to maternal social rank in reindeer (Rangifer tarandus). Behav Ecol Sociobiol 57:69–76

    Article  Google Scholar 

  • Holand Ø, Weladji RB, Røed KH, Gjøstein H, Kumpula J, Gaillard J-M, Smith ME, Nieminen M (2006) Male age structure influences females’ mass change during rut in a polygynous ungulate: the reindeer (Rangifer tarandus). Behav Ecol Sociobiol 59:682–688

    Article  Google Scholar 

  • Huber HR (1987) Natality and weaning success in relation to age of first reproduction in northern elephant seals. Can J Zool 65:1311–1316

    Google Scholar 

  • Jonsson KI (1997) Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 78:57–66

    Article  Google Scholar 

  • Kumpula J (2001) Winter grazing of reindeer in woodland lichen pasture: effect of lichen availability on the condition of reindeer. Small Rumin Res 39:121–130

    Article  PubMed  Google Scholar 

  • Laaksonen T, Korpimäki E, Hakkarainen H (2002) Interactive effects of parental age and environmental variation on the breeding performance of Tengmalms owls. J Anim Ecol 71:23–31

    Article  Google Scholar 

  • Langvatn R, Albon SD, Burkey T, Clutton-Brock TH (1996) Climate, plant phenology and variation in age at first reproduction in a temperate herbivore. J Anim Ecol 65:653–670

    Article  Google Scholar 

  • Langvatn R, Mysterud A, Stenseth NC, Yoccoz NG (2004) Timing and synchrony of ovulation in red deer constrained by short northern summers. Am Nat 163:763–772

    Article  PubMed  Google Scholar 

  • Loison A, Festa-Bianchet M, Gaillard JM, Jorgenson JT, Jullien JM (1999a) Age-specific survival in five populations of ungulates: evidence of senescence. Ecology 80:2539–2554

    Article  Google Scholar 

  • McNamara JM, Houston AI (1996) State-dependent life histories. Nature 380:215–221

    Article  PubMed  CAS  Google Scholar 

  • Millar JS (1994) Senescence in a population of small mammals? Ecoscience 1:317–321

    Google Scholar 

  • Millar JS, Derrickson EM, Sharpe STP (1992) Effects of reproduction on maternal survival and subsequent reproduction in northern Peromyscus-maniculatus. Can J Zool 70:1129–1134

    Google Scholar 

  • Mysterud A, Yoccoz NG, Stenseth NC, Langvatn R (2001a) Effects of age, sex, and density on body weight of Norwegian red deer: evidence of density-dependent senescence. Proc R Soc Lond Ser B 268:911–919

    Article  CAS  Google Scholar 

  • Mysterud A, Stenseth NC, Yoccoz NG, Langvatn R, Steinheim G (2001b) Nonlinear effects of large-scale climatic variability on wild and domestic herbivores. Nature 410:1096–1099

    Article  PubMed  CAS  Google Scholar 

  • Neuhaus P, Broussard DR, Murie JO, Dobson FS (2004) Age of primiparity and implications of early reproduction on life history in female Columbian ground squirrels. J Anim Ecol 73:36–43

    Article  Google Scholar 

  • Nichols JD, Kendall WL (1995) The use of multistate capture–recapture models to address questions of evolutionary ecology. J Appl Stat 22:835–846

    Article  Google Scholar 

  • Oftedal OT (1985) Pregnancy and lactation. In: Hudson R, White RG (eds) Bioenergetics of wild herbivores. CRC Press, Boca Raton, pp 215–238

    Google Scholar 

  • Orell M, Belda EJ (2002) Delayed cost of reproduction and senescence in the willow tit Parus montanus. J Anim Ecol 71:55–64

    Article  Google Scholar 

  • Orell M, Koivula K, Rytkonen S, Lahti K (1994) To breed or not to breed: causes and implications of non-breeding habit in the willow tit Parus montanus. Oecologia 77:339–346

    Article  Google Scholar 

  • Orell M, Rytkonen S, Koivula K, Ronkainen M, Rahlala M (1996) Brood size manipulations within the natural range did not reveal intragenerational cost of reproduction in the Willow Tit Parus montanus. Ibis 138:630–637

    Google Scholar 

  • Partridge L, Harvey PH (1985) Costs of reproduction. Nature 316:20

    Article  Google Scholar 

  • Partridge L, Harvey PH (1988) The ecological context of life-history evolution. Science 241:1449–1455

    Article  PubMed  Google Scholar 

  • Pease CM, Bull JJ (1988) A critique of methods for measuring life history trade-offs. J Evol Biol 1:293–303

    Article  Google Scholar 

  • Pomeroy PP, Fedak MA, Rothery P, Anderson S (1999) Consequences of maternal size for reproductive expenditure and pupping success of grey seals at North Rona, Scotland. J Anim Ecol 68:235–253

    Article  Google Scholar 

  • Pradel R, Gimenez O, Lebreton JD (2005) Principles and interest of GOF tests for multistate capture-recapture models. Anim Biodivers Conserv 28:189–204

    Google Scholar 

  • Pyle P, Nur V, Sydeman WJ, Emslie SD (1997) Cost of reproduction and the evolution of deferred breeding in the western gull. Behav Ecol 8:140–147

    Article  Google Scholar 

  • Reimers E (1983) Reproduction in wild reindeer in Norway. Can J Zool 61:211–217

    Article  Google Scholar 

  • Reimers E, Holmengen N, Mysterud A (2005) Life history variation of wild reindeer in the highly productive North Ottadalen region, Norway. J Zool 265:53–62

    Article  Google Scholar 

  • Reiter J, Le Boeuf BJ (1991) Life history consequences of variation in age at primiparity in northern elephant seals. Behav Ecol Sociobiol 28:153–160

    Article  Google Scholar 

  • Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257–267

    Article  Google Scholar 

  • Robbins CT, Robbins BL (1979) Fetal and neonatal growth-patterns and maternal reproductive effort in ungulates and sub-ungulates. Am Nat 114:101–116

    Article  Google Scholar 

  • Robinson MR, Pilkington JG, Clutton-Brock TH, Pemberton JM, Kruuk LEB (2006) Live fast, die young: trade-offs between fitness components and sexually antagonistic selection on weaponry in Soay sheep. Evolution 60:2168–2181

    PubMed  Google Scholar 

  • Roff DA (1992) The evolution of life histories. Chapman & Hall, London

    Google Scholar 

  • Rönnegård L, Forslund P, Danell Ö (2002) Lifetime patterns in adult female mass, reproduction and offspring mass in semidomesticated reindeer (Rangifer tarandus tarandus). Can J Zool 80:2047–2055

    Article  Google Scholar 

  • Sadleir RMFS (1987) Reproduction of female cervids. In: Wemmer CM (ed) Biology and management of the cervidae. Smithsonian Institution Press, Washington DC, pp 123–144

    Google Scholar 

  • Sinervo B, DeNardo DF (1996) Costs of reproduction in the wild: path analysis of natural selection and experimental tests of causation. Evolution 50:1299–1313

    Article  Google Scholar 

  • Skogland T (1983) The effects of density dependent resource limitation on size of wild reindeer. Oecologia 60:156–168

    Article  Google Scholar 

  • Skogland T (1989) Comparative social organisation of wild reindeer in relation to food, mates and predator avoidance. Adv Ethol 29:1–74

    Google Scholar 

  • Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Suttie JM, Webster JR (1995) Extreme seasonal growth in Arctic deer: comparisons and control mechansims. Am Zool 135:215–222

    Google Scholar 

  • Sydeman WJ, Nur N (1994) Life history strategies of female northern elephant seals. In: Le Boeuf BJ, Laws RM (eds) Elephant seals: population ecology, behavior, and physiology. University of California Press, Berkeley, pp 121–136

    Google Scholar 

  • Tavecchia G, Coulson T, Morgan BJT, Pemberton JM, Pilkington JC, Gulland FMD, Clutton-Brock TH (2005) Predictors of reproductive cost in female Soay sheep. J Anim Ecol 74:201–213

    Article  Google Scholar 

  • Testa JW (1987) Long-term reproductive patterns and sighting bias in Weddell seals (Leptonychotes weddelli). Can J Zool 65:1091–1099

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Weladji RB, Gaillard JM, Yoccoz NG, Holand Ø, Mysterud A, Loison A, Nieminen M, Stenseth NC (2006) Good reindeer mothers live longer and become better at raising offspring. Proc R Soc Lond Ser B 273:1239–1244

    Article  Google Scholar 

  • Wesolowski T, Rowinski P (2006) Is there a cost of reproduction for Marsh Tits Parus palustris in a primeval forest? Ibis 148:126–132

    Article  Google Scholar 

  • Williams GC (1966) Adaptation and natural selection. Princeton University Press, NJ

    Google Scholar 

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Acknowledgements

The authors are grateful to the Finnish Game and Fisheries Research Institute and V. Tervonen and his crew at Kutuharju Reindeer Research Station for the data. Funding from the Norwegian Research Council to R. B. W. and N. G. Y., and from the Natural Sciences and Engineering Research Council of Canada to R. B. W. supported this work. The authors are also grateful to the French–Norway Network funded by CNRS and the CLIMPOP Network funded by the GICC2.

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Authors and Affiliations

  1. Department of Biology, Concordia University, 7141 Sherbrooke St. West, Montreal, QC, H4B 1R6, Canada

    Robert B. Weladji

  2. UMR-CNRS 5558, Laboratoire de Biométrie et de Biologie Evolutive, Université Lyon 1, 69622, Villeurbanne Cedex, France

    Anne Loison & Jean-Michel Gaillard

  3. Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, P.O. Box 5003, 1432, Ås, Norway

    Øystein Holand

  4. Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biology, University of Oslo, P.O. Box 1066, 0316, Oslo, Norway

    Atle Mysterud & Nils C. Stenseth

  5. Department of Biology, University of Tromsø, 9037, Tromsø, Norway

    Nigel G. Yoccoz

  6. Finnish Game and Fisheries Research Institute, Reindeer Research Station, 99910, Kaamanen, Finland

    Mauri Nieminen

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  1. Robert B. Weladji
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  2. Anne Loison
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  3. Jean-Michel Gaillard
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  4. Øystein Holand
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  6. Nigel G. Yoccoz
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  7. Mauri Nieminen
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  8. Nils C. Stenseth
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Correspondence to Robert B. Weladji.

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Communicated by Hannu Ylonen.

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Weladji, R.B., Loison, A., Gaillard, JM. et al. Heterogeneity in individual quality overrides costs of reproduction in female reindeer. Oecologia 156, 237–247 (2008). https://doi.org/10.1007/s00442-008-0961-x

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