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Reproductive phenology of a food-hoarding mast-seed consumer: resource- and density-dependent benefits of early breeding in red squirrels

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Abstract

The production of offspring by vertebrates is often timed to coincide with the annual peak in resource availability. However, capital breeders can extend the energetic benefits of a resource pulse by storing food or fat, thus relaxing the need for synchrony between energy supply and demand. Food-hoarding red squirrels (Tamiasciurus hudsonicus) breeding in the boreal forest are reliant on cones from a masting conifer for their nutrition, yet lactation is typically completed before the annual crop of cones is available for consumption such that peaks in energy supply and demand are not synchronized. We investigated the phenological response of red squirrels to annual variation in environmental conditions over a 20-year span and examined how intra- and inter-annual variation in the timing of reproduction affected offspring recruitment. Reproductive phenology was strongly affected by past resource availability with offspring born earlier in years following large cone crops, presumably because this affected the amount of capital available for reproduction. Early breeders had higher offspring survival and were more likely to renest following early litter loss when population density was high, perhaps because late-born offspring are less competitive in obtaining a territory when vacancies are limited. Early breeders were also more likely to renest after successfully weaning their first litter, but renesting predominantly occurred during mast years. Because of their increased propensity to renest and the higher survival rates of their offspring, early breeders contribute more recruits to the population but the advantage of early breeding depends on population density and resource availability.

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References

  • Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Caski F (eds) Proceedings of the Second International Symposium on Information Theory. Akademiai Kiado, Budapest, pp 267–281

  • Aloha MP, Laaksonen T, Eeva T, Lehikoinen E (2012) Selection on laying date is connected to breeding density in the pied flycatcher. Oecologia 168:703–710

    Article  Google Scholar 

  • Baker JR (1938) The evolution of breeding seasons. In: DeBeer J (ed) Evolution, essays on aspects of evolutionary biology. Clarendon, Oxford, pp 161–177

    Google Scholar 

  • Berteaux D, Boutin S (2000) Breeding dispersal in female North American red squirrels. Ecology 81:1311–1326

    Article  Google Scholar 

  • Bieber C, Juškaitis R, Turbill C, Ruf T (2012) High survival during hibernation affects onset and timing of reproduction. Oecologia 169:155–166

    Article  PubMed  Google Scholar 

  • Both C, Visser ME (2001) Adjustment to climate change is constrained by arrival date in a long-distance migrant bird. Nature 411:296–298

    Article  CAS  PubMed  Google Scholar 

  • Boutin S, Wauters LA, McAdam AG, Humphries MM, Tosi G, Dhondt AA (2006) Anticipatory reproduction and population growth in seed predators. Science 314:1928–1930

    Article  CAS  PubMed  Google Scholar 

  • Boyce MS (1979) Seasonality and patterns of natural selection for life histories. Am Nat 114:569–583

    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 

  • Coltman DW, Smith JA, Bancroft DR, Pilkington J, MacColl ADC, Clutton-Brock TH, Pemberton JM (1999) Density-dependent variation in lifetime breeding success and natural and sexual selection in Soay Rams. Am Nat 154:730–746

    Article  CAS  PubMed  Google Scholar 

  • Crick HQP, Wingfield D, Gibbons D, Magrath RD (1993) Seasonal changes in clutch size in British birds. J Anim Ecol 62:263–273

    Article  Google Scholar 

  • Daan S, Dijkstra C, Drent R, Meijer T (1989) Food supply and the annual timing of avian reproduction. Acta XIX Congressus Internationalis Ornithologici, Ottawa, Ontario, Canada, pp 392–407

  • Dantzer B, Newman AE, Boonstra R, Palme R, Boutin S, Humphries MM, McAdam AG (2013) Density triggers maternal hormones that increase adaptive offspring growth in a wild mammal. Science 340:1215–1217

    Article  CAS  PubMed  Google Scholar 

  • Descamps S, Boutin S, Berteaux D, Gaillard JM (2008) Age-specific variation in survival, reproductive success and offspring quality in red squirrels: evidence of senescence. Oikos 117:1406–1416

    Article  Google Scholar 

  • Dunn PO, Winkler DW, Whittingham LA, Hannon SJ, Robertson RJ (2011) A test of the mismatch hypothesis: how is timing of reproduction related to food abundance in an aerial insectivore? Ecology 92:450–461

    Article  PubMed  Google Scholar 

  • Durant JM, Hjermann DØ, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Climate Res 33:271–283

    Article  Google Scholar 

  • Eeva T, Veistola S, Lehikoinen E (2000) Timing of breeding in subarctic passerines in relation to food availability. Can J Zool 78:67–78

    Article  Google Scholar 

  • Erikstad KE, Fauchald P, Tveraa T, Steen H (1998) On the cost of reproduction in long-lived birds: the influence of environmental variability. Ecology 79:1781–1788

    Article  Google Scholar 

  • Farner DS (1985) Annual rhythms. Annu Rev Physiol 47:65–82

    Google Scholar 

  • Fletcher QE, Boutin S, Lane JE, LaMontagne JM, McAdam AG, Krebs CJ, Humphries MM (2010) The functional response of a hoarding seed predator to mast seeding. Ecology 91:2673–2683

    Article  PubMed  Google Scholar 

  • Fletcher QE, Speakman JR, Boutin S, McAdam AG, Woods SB, Humphries MM (2012) Seasonal stage differences overwhelm environmental and individual factors as determinants of energy expenditure in free-ranging red squirrels. Funct Ecol 26:677–687

    Article  Google Scholar 

  • Fletcher QE, Landy-Currier M, Boutin S, McAdam AG, Speakman JR, Humphries MM (2013) Reproductive timing and reliance on hoarded capital resources by lactating red squirrels. Oecologia. doi:10.1007/s00442-013-2699-3

    Google Scholar 

  • Gwinner E (1986) Circannual rhythms. Springer, Berlin

  • Harrison XA, Blount JD, Inger R, Norris DR, Bearhop S (2011) Carry-over effects as drivers of fitness differences in animals. J Anim Ecol 80:4–18

    Article  PubMed  Google Scholar 

  • Humphries MM, Boutin S, Thomas DW, Ryan JD, Selman C, McAdam AG, Berteaux D, Speakman JR (2005) Expenditure freeze: the metabolic response of small mammals to cold environments. Ecol Lett 8:1326–1333

    Article  Google Scholar 

  • Husby A, Kruuk LEB, Visser ME (2009) Decline in the frequency and benefits of multiple brooding in great tits as a consequence of a changing environment. Proc R Soc B 276:1845–1854

    Article  PubMed  Google Scholar 

  • Inouye DW, Barr B, Armitage KB, Inouye BD (2000) Climate change is affecting altitudinal migrants and hibernating species. Proc Natl Acad Sci 97:1630–1633

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Kerby J, Post E (2013) Capital and income breeding traits differentiate trophic match–mismatch dynamics in large herbivores. Philos Trans R Soc B 368:20120484

    Article  Google Scholar 

  • Kerr TD, Boutin S, LaMontagne JL, McAdam AG, Humphries MM (2007) Persistent maternal effects on juvenile survival in North American red squirrels. Biol Lett 3:289–291

    Article  PubMed Central  PubMed  Google Scholar 

  • Krebs CJ, Lamontagne JM, Kenney AJ, Boutin S (2012) Climatic determinants of white spruce cone crops in the boreal forest of southwestern Yukon. Botany 90:113–119

    Article  Google Scholar 

  • Lack D (1954) The natural regulation of animal numbers. Clarendon, Oxford

    Google Scholar 

  • LaMontagne JM, Peters S, Boutin S (2005) A visual index for estimating cone production for individual white spruce trees. Can J For Res 35:3020–3026

    Article  Google Scholar 

  • LaMontagne JM, Williams CT, Donald JL, Humphries MM, McAdam AG, Boutin S (2013) Linking intraspecific variation in territory size, cone supply, and survival of North American red squirrels. J Mammal 94:1048–1058

    Article  Google Scholar 

  • Lehikoinen A, Ranta E, Pietiäinen H, Byholm P, Saurola P, Valkama J, Huitu O, Henttonen H, Korpimäki E (2011) The impact of climate and cyclic food abundance on the timing of breeding and brood size in four boreal owl species. Oecologia 165:349–355

    Article  PubMed  Google Scholar 

  • Lewis RJ, Kappeler PM (2005) Seasonality, body condition, and timing of reproduction in Propithecus verreauxi verreauxi in the Kirindy Forest. Am J Primatol 67:347–364

    Article  CAS  PubMed  Google Scholar 

  • McAdam AG, Boutin S (2003) Variation in viability selection among cohorts of juvenile red squirrels (Tamiasciurus hudsonicus). Evolution 57:1689–1697

    PubMed  Google Scholar 

  • McAdam AG, Boutin S, Sykes AK, Humphries MM (2007) Life histories of female red squirrels and their contributions to population growth and lifetime fitness. Écoscience 14:362–369

    Article  Google Scholar 

  • Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Philos Trans R Soc B 365:3177–3186

    Article  Google Scholar 

  • Moyes K, Nussey D, Clements M, Guinness F, Morris A, Morris S, Pemberton J, Kruuk L, Clutton-Brock T (2011) Advancing breeding phenology in response to environmental change in a wild red deer population. Global Change Biol 17:2455–2469

    Article  Google Scholar 

  • Ostfeld RS, Keesing F (2000) Pulsed resources and community dynamics of consumers in terrestrial ecosystems. Trends Ecol Evol 15:232–237

    Article  PubMed  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42

    Article  CAS  PubMed  Google Scholar 

  • Perrins CM (1970) The timing of birds’ breeding seasons. Ibis 112:242–255

    Article  Google Scholar 

  • Post E, Forchhammer MC (2008) Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Philos Trans R Soc Lond B 363:2369–2375

    Article  Google Scholar 

  • Price T, Kirkpatrick M, Arnold SJ (1988) Directional selection and the evolution of breeding date in birds. Science 240:798–799

    Article  CAS  PubMed  Google Scholar 

  • Price K, Boutin S, Ydenberg R (1990) Intensity of territorial defense in red squirrels: an experimental test of the asymmetric war of attrition. Behav Ecol Sociobiol 27:217–222

    Article  Google Scholar 

  • Raudenbush SW, Bryk AS (2002) Hierarchical linear models: applications and data analysis methods, 2nd edn. Sage, Newbury Park

    Google Scholar 

  • Réale D, McAdam AG, Boutin S, Berteaux D (2003) Genetic and plastic responses of a northern mammal to climate change. Proc R Soc B 270:591–596

    Article  PubMed  Google Scholar 

  • Richard AF, Dewar RE, Schwartz M, Ratsirarson J (2000) Mass change, environmental variability and female fertility in wild Propithecus verreauxi. J Human Evol 39:381–391

    Article  CAS  Google Scholar 

  • Richard AF, Dewar RE, Schwartz M, Ratsirarson J (2002) Life in the slow lane? Demography and life histories of male and female sifaka. J Zool 256:421–436

    Article  Google Scholar 

  • Roellig K, Goeritz F, Fickel J, Hermes R, Hofer H, Hildebrandt TB (2010) Superconception in mammalian pregnancy can be detected and increases reproductive output per breeding season. Nat Commun 1:78

    Article  PubMed  Google Scholar 

  • Rohwer FC, Eisenhauer DJ (1989) Egg mass and clutch size relationships in geese, eiders, and swans. Ornis Scand 20:43–48

    Article  Google Scholar 

  • Shultz MT, Piatt JF, Harding AMA, Kettle AB, Van Pelt TI (2009) Timing of breeding and reproductive performance in murres and kittiwakes reflect mismatched seasonal prey dynamics. Mar Ecol Prog Ser 393:247–258

    Article  Google Scholar 

  • Smith CC (1968) The adaptive nature of social organization in the genus of tree squirrels Tamiasciurus. Ecol Monogr 38:31–63

    Article  Google Scholar 

  • Stephens PA, Boyd IL, McNamara JM, Houston AI (2009) Capital breeding and income breeding: their meaning, measurement, and worth. Ecology 90:2057–2067

    Article  PubMed  Google Scholar 

  • Studd E (2012) Environmental and biological correlates of maternal investment in red squirrels. MSc thesis. McGill University, Montreal

  • Thackeray SJ, Sparks TH, Frederiksen M, Burthe S, Bacon PJ, Bell JR, Wanless S (2010) Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob Change Biol 16:3304–3313

    Article  Google Scholar 

  • Verboven N, Verhulst S (1996) Seasonal variation in the incidence of double broods: the date hypothesis fits better than the quality hypothesis. J Anim Ecol 65:264–273

    Article  Google Scholar 

  • Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc R Soc Lond B 272:2561–2569

    Article  Google Scholar 

  • Williams CT, Barnes BM, Kenagy GJ, Buck CL (2013) Phenology of hibernation and reproduction in squirrels: integration of environmental cues with endogenous programming. J Zool (in press)

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Acknowledgments

The work was funded by grants from the Natural Sciences and Engineering Research Council to S. B., A. G. M., and M. M. H. and a grant from the National Science Foundation to A. G. M. We are grateful to the many students and crew members for data collection and to Ainsley Sykes for data and field management. This is contribution no. 72 of the Kluane Red Squirrel Project.

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Correspondence to Cory T. Williams.

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Communicated by Jörg U. Ganzhorn.

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Williams, C.T., Lane, J.E., Humphries, M.M. et al. Reproductive phenology of a food-hoarding mast-seed consumer: resource- and density-dependent benefits of early breeding in red squirrels. Oecologia 174, 777–788 (2014). https://doi.org/10.1007/s00442-013-2826-1

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