Abstract
A life history strategy that favours somatic growth over reproduction is well known for long-lived iteroparous species, especially in unpredictable environments. Risk-sensitive female reproductive allocation can be achieved by a reduced reproductive effort at conception, or the subsequent adjustment of investment during gestation or lactation in response to unexpected environmental conditions or resource availability. We investigated the relative importance of reduced investment at conception compared with later in the reproductive cycle (i.e. prenatal, perinatal or neonatal mortality) in explaining reproductive failure in two high-density moose (Alces alces) populations in southern Norway. We followed 65 multiparous, global positioning system (GPS)-collared females throughout the reproductive cycle and focused on the role of maternal nutrition during gestation in determining reproductive success using a quasi-experimental approach to manipulate winter forage availability. Pregnancy rates in early winter were normal (≥0.8) in all years while spring calving rates ranged from 0.4 to 0.83, with prenatal mortality accounting for most of the difference. Further losses over summer reduced autumn recruitment rates to 0.23–0.69, despite negligible predation. Over-winter mass loss explained variation in both spring calving and autumn recruitment success better than absolute body mass in early or late winter. Although pregnancy was related to body mass in early winter, overall reproductive success was unrelated to pre-winter body condition. We therefore concluded that reproductive success was limited by winter nutritional conditions. However, we could not determine whether the observed reproductive allocation adjustment was a bet-hedging strategy to maximise reproduction without compromising survival or whether females were simply unable to invest more resources in their offspring.
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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
Albon SD, Mitchell B, Huby BJ, Brown D (1986) Fertility in female red deer (Cervus elaphus): the effects of body composition, age and reproductive status. J Zool 209:447–460
Arnemo JM, Kreeger TJ, Soveri T (2003) Chemical immobilization of free-ranging moose. Alces 39:243–253
Bårdsen B-J, Fauchald P, Tveraa T, Langeland K, Yoccoz NG, Ims RA (2008) Experimental evidence of a risk-sensitive reproductive allocation in a long-lived mammal. Ecology 89:829–837
Bårdsen BJ, Tveraa T, Fauchald P, Langeland K (2010) Observational evidence of risk-sensitive reproductive allocation in a long-lived mammal. Oecologia 162:627–639
Barnowe-Meyer KK, White PJ, Byers JA (2011) Maternal investment by Yellowstone pronghorn following winter habitat deterioration. West North Am Nat 71:222–233
Clutton-Brock TH (ed) (1988) Reproductive success: Studies of individual variation in contrasting breeding systems. University of Chicago Press Chicago, Illinois
Clutton-Brock TH, Guinness FE, Albon SD (1983) The costs of reproduction to red deer hinds. J Anim Ecol 52:367–383
Clutton-Brock TH, Albon SD, Guinness FE (1987) Interactions between population density and maternal characteristics affecting fecundity and juvenile survival in red deer. J Anim Ecol 56:857–871
Clutton-Brock TH, Albon SD, Guinness FE (1989) Fitness costs of gestation and lactation in wild mammals. Nature 337:260–262
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
Danielsen J (2001) Local community based moose management plans in Norway. Alces 37:55–60
Ericsson G, Wallin K, Ball JP, Broberg M (2001) Age-related reproductive effort and senescence in free-ranging moose, Alces alces. Ecology 82:1613–1620
Festa-Bianchet M (1998) Condition-dependent reproductive success in bighorn ewes. Ecol Lett 1:91–94
Festa-Bianchet M, Gaillard J-M, Jorgenson JT (1998) Mass- and density-dependent reproductive success and reproductive costs in a capital breeder. Am Nat 152:367–379
Gaillard J-M (2007) Are moose only a large deer?: some life history considerations. Alces 43:1–11
Gaillard J-M, 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
Garel M, Solberg EJ, Sæther B-E, Grøtan V, Tufto J, Heim M (2009) Age, size, and spatiotemporal variation in ovulation patterns of a seasonal breeder, the Norwegian moose (Alces alces). Am Nat 173:89–104
Grøtan V, Sæther B-E, Lillegård M, Solberg EJ, Engen S (2009) Geographical variation in the influence of density dependence and climate on the recruitment of Norwegian moose. Oecologia 161:685–695
Hamel S, Côté SD, Gaillard J-M, Festa-Bianchet M (2009) Individual variation in reproductive costs of reproduction: high-quality females always do better. J Anim Ecol 78:143–151
Hamel S, Côté SD, Festa-Bianchet M (2010) Maternal characteristics and environment affect the costs of reproduction in female mountain goats. Ecology 91:2034–2043
Keech MA, Bowyer RT, Ver Hoef JM, Boertje RD, Dale BW, Stephenson TR (2000) Life-history consequences of maternal condition in Alaskan moose. J Wildl Manage 64:450–462
Kozak HM, Hudson RJ, French N, Renecker LA (1995) Winter feeding, lactation and calf growth in farmed wapiti. Rangelands 17:116–120
Kruuk LEB, Clutton-Brock TH, Albon SD, Pemberton JM, Guinness FE (1999) Population density affects sex ratio variation in red deer. Nature 399:459–461
Langvatn R (1992) Analysis of ovaries in studies of reproduction in red deer (Cervus elaphus, L.): application and limitations. Rangifer 12:67–91
Long RA, Kie JG, Bowyer RT, Hurley MA (2009) Resource selection and movements by female mule deer Odocoileus hemionus: effects of reproductive stage. Wildl Biol 15:288–298
Markgren G (1969) Reproduction of moose in Sweden. Viltrevy 6:127–299
Martin JGA, Festa-Bianchet M (2010) Bighorn ewes transfer the costs of reproduction to their lambs. Am Nat 176:414–423
Milner JM, Stien A, Irvine RJ, Albon SD, Langvatn R, Ropstad E (2003) Body condition in Svalbard reindeer and the use of blood parameters as indicators of condition and fitness. Can J Zool 81:1566–1578
Milner JM, Storaas T, Van Beest FM, Lien G (2012) Sluttrapport for elgfôringsprosjektet. Oppdragsrapport no. 1–2012. Hedmark University College, Norway
Murtaugh PA (2009) Performance of several variable-selection methods applied to real ecological data. Ecol Lett 12:1061–1068
Mysterud A, Coulson T, Stenseth NC (2002) The role of males in the dynamics of ungulate populations. J Anim Ecol 71:907–915
National Cervid Register (2011) Norwegian national register for wild ungulate monitoring data www.Hjortevilt.No
Newton I (1989) Lifetime reproduction in birds. Academic Press, London
Ozoga JJ, Verme LJ (1982) Physical and reproductive characteristics of a supplementally-fed white-tailed deer herd. J Wildl Manage 46:281–301
Parker KL, Gillingham MP, Hanley TA, Robbins CT (1999) Energy and protein balance of free-ranging black-tailed deer in a natural forest environment. Wildl Monogr 143:1–48
Parker KL, Barboza PS, Gillingham MP (2009) Nutrition integrates environmental responses of ungulates. Funct Ecol 23:57–69
Peek JM, Schmidt KT, Dorrance MJ, Smith BL (2002) Supplemental feeding and farming of elk. In: Toweill DE, Thomas JW (eds) Elk of North America: ecology and management, 2nd edn. Smithsonian Institute Press, Washington, pp 614–647
Pelletier F, Reale D, Garant D, Coltman DW, Festa-Bianchet M (2007) Selection on heritable seasonal phenotypic plasticity of body mass. Evolution 61:1969–1979
Putman RJ, Staines BW (2004) Supplementary winter feeding of wild red deer Cervus elaphus in Europe and North America: justifications, feeding practice and effectiveness. Mammal Rev 34:285–306
Rodriguez-Hidalgo P, Gortazar C, Tortosa FS, Rodriguez-Vigal C, Fierro Y, Vicente J (2010) Effects of density, climate, and supplementary forage on body mass and pregnancy rates of female red deer in Spain. Oecologia 164:389–398
Rolandsen CM, Solberg EJ, Heim M, Holmstrøm F, Solem MI, Sæther B-E (2008) Accuracy and repeatability of moose (Alces alces) age as estimated from dental cement layers. Eur J Wildl Res 54:6–14
Sæther B-E (1997) Environmental stochasticity and population dynamics of large herbivores : a search for mechanisms. Trends Ecol Evol 12:143–149
Sæther B-E, Haagenrud H (1983) Life history of the moose (Alces alces): fecundity rates in relation to age and carcass weight. J Mammal 64:226–232
Sand H (1996a) Life history patterns in female moose (Alces alces): the relationship between age, body size, fecundity and environmental conditions. Oecologia 106:212–220
Sand H (1996b) Life history strategies in moose (Alces alces): Geographical and temporal variation in body growth and reproduction. PhD, Swedish University of Agricultural Sciences, Uppsala
Sand H (1998) Costs of reproduction in female moose (Alces alces) as measured by means of phenotypic correlations. Can J Zool 76:187–193
Sand H, Cederlund G, Danell K (1995) Geographical and latitudinal variation in growth patterns and adult body size of Swedish moose (Alces alces). Oecologia 102:433–442
Schwartz CC, Hundertmark KJ (1993) Reproductive characteristics of Alaskan moose. J Wildl Manage 57:454–468
Schwartz CC, Regelin WL, Franzmann AW (1987) Seasonal weight dynamics of moose. Swed Wildl Res Suppl 1:301–310
Sentrallaboratoriet (2011) Methods—progesterone. Norges Veterinærhøgskole. http://www.sentrallaboratoriet.no/metoder_j_r.htm#p
Simms M, Elston DA, Larkham A, Nussey DH, Albon SD (2007) Identifying when weather influences life-history traits of grazing herbivores. J Anim Ecol 76:761–770
Skogland T (1984) The effects of food and maternal conditions in fetal growth and size in wild reindeer. Rangifer 4:39–46
Smith BL, Robbins RL, Anderson SH (1997) Early development of supplementally fed, free-ranging elk. J Wildl Manage 61:26–38
Solberg EJ, Heim M, Arnemo JM, Sæther BE, Os Ø (2003) Does rectal palpation of pregnant moose cows affect pre- and neo-natal mortality of their calves? Alces 39:65–77
Solberg EJ, Rolandsen CM, Heim M, Grøtan V, Garel M, Sæther B-E, Nilsen EB, Austrheim G, Herfindal I (2006) Elgen i norge sett med jegerøyne - en analyse av jaktmaterialet fra overvåkeningsprogrammet for elg og det samlede sett elg-materialet for perioden 1966–2004, vol 125. NINA, Trondheim
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Stephens PA, Boyd IL, McNamara JM, Houston AI (2009) Capital breeding and income breeding: their meaning, measurement, and worth. Ecology 90:2057–2067
Stubsjøen T, Saether B-E, Solberg EJ, Heim M, Rolandsen CM (2000) Moose (Alces alces) survival in three populations in northern Norway. Can J Zool 78:1822–1830
Tavecchia G, Coulson T, Morgan BJT, Pemberton JM, Pilkington JG, Gulland FMD, Clutton-Brock TH (2005) Predictors of reproductive cost in female Soay sheep. J Anim Ecol 74:201–213
Testa JW (2004) Interaction of top-down and bottom-up life history trade-offs in moose (Alces alces). Ecology 85:1453–1459
Testa JW, Adams GP (1998) Body condition and adjustments to reproductive effort in female moose (Alces alces). J Mammal 79:1345–1354
Thorne ET, Dean RE, Hepworth WG (1976) Nutrition during gestation in relation to successful reproduction in elk. J Wildl Manage 40:330–335
Tveraa T, Fauchald P, Henaug C, Yoccoz NG (2003) An examination of a compensatory relationship between food limitation and predation in semi-domestic reindeer. Oecologia 137:370–376
van Beest FM, Gundersen H, Mathisen KM, Milner JM, Skarpe C (2010a) Long-term browsing impact around diversionary feeding stations for moose in southern Norway. For Ecol Manage 259:1900–1911
van Beest FM, Loe LE, Mysterud A, Milner JM (2010b) Comparative space use and habitat selection of moose around feeding stations. J Wildl Manage 74:219–227
van Beest FM, Mysterud A, Loe LE, Milner JM (2010c) Forage quantity, quality and depletion as scale-dependent mechanisms driving habitat selection of a large browsing herbivore. J Anim Ecol 79:910–922
Visscher DR, Merrill EH, Fortin D, Frair JL (2006) Estimating woody browse availability for ungulates at increasing snow depths. For Ecol Manage 222:348–354
Wam HK, Hjeljord O, Solberg EJ (2010) Differential forage use makes carrying capacity equivocal on ranges of Scandinavian moose (Alces alces). Can J Zool 88:1179–1191
Williams GC (1966) Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am Nat 100:687–690
Acknowledgments
We thank Fritzöe Skoger and Løvenskiold-Fossum in Telemark and Stor-Elvdal Landowners’ Association in Hedmark for collaborating as partners in this project. Thanks to all who helped with the collection of field data and in particular to Bent Thorkildsen, Staffan Klasson, Knut B. Nicolaysen and Tor Taraldsrud for their assistance during capturing and hunting. We thank Bram van Moorter, Jon M. Arnemo and Scott Becker for useful discussions, and Marco Festa-Bianchet and an anonymous reviewer for useful comments on an earlier version of the manuscript. Funding was provided by the Norwegian Research Council (173868/AREAL), Innovation Norway, Telemark County, Hedmark County and municipalities in Telemark, Vestfold and Hedmark. All work carried out during this study conforms to the legal requirements set by Forsøksdyrutvalget (Animal Research Committee) in Norway.
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Milner, J.M., van Beest, F.M., Solberg, E.J. et al. Reproductive success and failure: the role of winter body mass in reproductive allocation in Norwegian moose. Oecologia 172, 995–1005 (2013). https://doi.org/10.1007/s00442-012-2547-x
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DOI: https://doi.org/10.1007/s00442-012-2547-x