Oecologia

pp 1–12 | Cite as

Birth date promotes a tortoise or hare tactic for body mass development of a long-lived male ungulate

  • Eric S. Michel
  • Stephen Demarais
  • Bronson K. Strickland
  • Guiming Wang
Population ecology – original research

Abstract

Maternal and early-life influences may affect life-long individual phenotype, potentially influencing reproductive success. However, some individuals may compensate for a poor start to life, which may improve longevity and reproductive success later in life. We developed four models to assess whether maternal characteristics (age, body mass and previous year cumulative lactation demand) and/or birth date influenced a long-lived mammal’s phenotype to maturity. We used a directional separation analysis to assess the relative influence of each maternal characteristic and birth date on captive male white-tailed deer (Odocoileus virginianus) body mass and antler size. We found that birth date was the only characteristic that persistently influenced male body mass. Depending on when offspring were born, they used alternative tactics to increase their body mass. Birth date positively influenced body mass at 1, 2 and 3 years of age-indicating males displayed faster growth and compensated for late birth (hare tactic). However, early-, heavy-born males were heavy juveniles, and juvenile body mass positively influenced mature body mass (slow but steady growth; tortoise tactic). Our findings provide a first evidence that a long-lived ungulate can display alternative tactics to achieve heavy body mass; individuals are either born early and heavy and are heavy throughout life (tortoise), or light, late-born individuals compensate for a poor start in life by growing at a faster rate to equal or surpass the body mass of early-born individuals (hare). Either tactic may be viable if it influences reproductive success as body mass positively influences access to mates in ungulates.

Keywords

Birth date Compensatory growth Life history theory Maternal effects Path analysis White-tailed deer 

Notes

Acknowledgements

We thank the Mississippi Department of Wildlife, Fisheries and Parks (MDWFP) for financial support using resources from the Federal Aid in Wildlife Restoration Act. We thank MDWFP biologists W. McKinley, A. Blaylock, A. Gary and L. Wilf for their extensive involvement in data collection. We also thank S. Tucker as facility coordinator and multiple graduate students and technicians for their help collecting data. We also thank J. M. Gaillard and two anonymous reviewers for their helpful comments. This manuscript is contribution WFA-412 of the Mississippi State Forest and Wildlife Research Center.

Author contribution statement

ESM, SD, BKS and GW conceived the research idea. ESM collected and analyzed the data. ESM wrote the manuscript with SD, BKS and GW providing editorial advice.

Compliance with ethical standards

Ethical approval

All applicable institutional guidelines for the care and use of animals were followed.

Supplementary material

442_2017_4013_MOESM1_ESM.pdf (114 kb)
Supplementary material 1 (PDF 113 kb)

References

  1. Abbott MJ, Ullrey DE, Ku PK, Schmitt SM, Romsos DR, Tucker HA (1984) Effect of photoperiod on growth and fat accretion in white-tailed doe fawns. J Wildlife Manage 48:776–787CrossRefGoogle Scholar
  2. Ali M, Nicieza A, Wootton RJ (2003) Compensatory growth in fishes: a response to growth depression. Fish Fish 4:147–190CrossRefGoogle Scholar
  3. Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 72:149–177CrossRefGoogle Scholar
  4. Bates D, Maechler M, Bolker B, Walker S (2014) Lme4: linear mixed-effects models using eigen and s4. R package version 1.1-7. http://cran.r-project.org/package=lme4. Accessed Sept 2015
  5. Bernardo J (1996) Maternal effects in animal ecology. Am Zool 36:83–105CrossRefGoogle Scholar
  6. Blaylock AC (2007) Effects of soil region, litter size, and gender on morphometrics of white-tailed deer fawns. Master thesis, Department of Wildlife Fisheries and Aquaculture, Mississippi State University, Mississippi State, Mississippi, USAGoogle Scholar
  7. Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach. Springer, New YorkCrossRefGoogle Scholar
  8. Clutton-Brock TH, Guinness FE, Albon SD (1982) Red Deer: behavior and ecology of two sexes. The University of Chicago Press, IllinoisGoogle Scholar
  9. Coltman DW, Festa-Bianchet M, Jorgenson JT, Strobeck C (2001) Age-dependent sexual selection in bighorn rams. P Roy Soc Lond B Bio 269:165–172CrossRefGoogle Scholar
  10. Cook JG, Johnson BK, Cook RC, Riggs RA, Delcurto T, Bryant LD, Irwin LL (2004) Effects of summer-autumn nutrition and parturition date on reproduction and survival of elk. Wildlife Monogr 155:1–61Google Scholar
  11. Côté SD, Festa-Bianchet M (2001) Birthdate, mass and survival in mountain got kids: effects of maternal characteristics and forage quality. Oecologia 127:230–238CrossRefPubMedGoogle Scholar
  12. Crocker DE, Houser DS, Webb PM (2012) Impact of body reserves on energy expenditure, water flux, and mating success in breeding male northern elephant seals. Physiol Biochem Zool 85:11–20CrossRefPubMedGoogle Scholar
  13. Demarais S, Strickland BK (2011) Antlers. In: Hewitt DG (ed) Biology and management of white-tailed deer. Florida CRC Press, Florida, pp 107–146Google Scholar
  14. Demarais S, Miller KV, Jacobson HA (2000) White-tailed deer. In: Demarais S, Krausman PR (eds) Ecology and management of large mammals in North America. Prentice Hall Inc., New Jersey, pp 601–628Google Scholar
  15. DeYoung RW, Miller KV (2011) White-tailed deer behavior. In: Hewitt DG (ed) Biology and management of white-tailed deer. Florida CRC Press, Florida, pp 311–354Google Scholar
  16. Ditchkoff SS (2011) Anatomy and physiology. In: Hewitt DG (ed) Biology and management of white-tailed deer. Florida CRC Press, Florida, pp 43–74Google Scholar
  17. Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116CrossRefPubMedGoogle Scholar
  18. Douhard F, Gaillard JM, Pellerin M, Jacob L, Lemaître JF (2017) The cost of growing large: costs of post-weaning growth on body mass senescence in a wild mammal. Oikos 126:1329–1338CrossRefGoogle Scholar
  19. Favre M, Martin JG, Festa-Bianchet M (2008) Determinants and life-history consequences of social dominance in bighorn ewes. Anim Behav 76:1373–1380CrossRefGoogle Scholar
  20. Feder C, Martin JGA, Festa-Bianchet M, Bérubé C, Jorgenson J (2008) Never too late? Consequences of late birthdate for mass and survival of bighorn lambs. Oecologia 156:773–781CrossRefPubMedGoogle Scholar
  21. Festa-Bianchet M, Jorgenson JT, Wishart WD (1995) Life history consequences of variation in age of primiparity in bighorn ewes. Ecology 76:871–881CrossRefGoogle Scholar
  22. Festa-Bianchet M, Jorgenson JT, Réale D (2000) Early development, adult mass, and reproductive success in bighorn sheep. Behav Ecol 11:633–639CrossRefGoogle Scholar
  23. Flinn EB, Strickland BK, Demarais S, Chistiansen D (2013) Age and gender affect epiphyseal closure in white-tailed deer. Southeast Nat 12:297–306CrossRefGoogle Scholar
  24. Gaillard JM, Delorme D, Jullien JM (1993) Effects of cohort, sex, and birth date on body development of roe deer (Capreolus capreolus) fawns. Oecologia 94:57–61CrossRefPubMedGoogle Scholar
  25. Gotthard K (2000) Increased risk of predation as a cost of high growth rate: an experimental test in a butterfly. J Anim Ecol 69:896–902CrossRefGoogle Scholar
  26. Green WCH, Rothstein A (1991) Trade-offs between growth and reproduction in female bison. Oecologia 86:521–527CrossRefPubMedGoogle Scholar
  27. Green WCH, Rothstein A (1993) Persistent influences of birth date on dominance, growth and reproductive success in bison. J Zool 230:177–186CrossRefGoogle Scholar
  28. Gurney WSC, Jones W, Veitch AR, Nisbet RM (2003) Resource allocation, hyperphagia, and compensatory growth in juveniles. Ecology 84:2777–2787CrossRefGoogle Scholar
  29. Hamel S, Côté SD, Gaillard JM, Festa-Bianchet M (2009) Individual variation in reproductive costs of reproduction: high-quality females always do better. J Anim Ecol 78:143–151CrossRefPubMedGoogle Scholar
  30. Hewison AJM, Gaillard JM (1999) Successful sons or advantaged daughters? The Trivers-Willard model and sex-biased maternal investment in ungulates. Trends Ecol Evol 14:229–234CrossRefPubMedGoogle Scholar
  31. Hewitt DG (2011) Nutrition. In: Hewitt DG (ed) Biology and management of white-tailed deer. CRC Press, Florida, pp 5–106Google Scholar
  32. Iossa G, Soulsbury CD, Baker PJ, Harris S (2008) Body mass, territory size, and life- history tactics in a socially monogamous canid, the red fox Vulpes vulpes. J Mammal 89:1480–1490CrossRefGoogle Scholar
  33. Kie JG, Johnson BK, Noyes JH, Williams CL, Dick BL, Rhodes OE, Stussy RJ, Bowyer RT (2013) Reproduction in North American elk Cervus elaphus: paternity of calves sired by males of mixed age classes. Wildlife Biol 19:302–310CrossRefGoogle Scholar
  34. Kreeger TJ (1996) Handbook of wildlife chemical immobilization. International Wildlife Veterinary Services, WyomingGoogle Scholar
  35. Kruuk LEB, Clutton-Brock TH, Slate J, Pemberton JM, Brotherstone S, Guiness F (2000) Heritability of fitness in a wild mammal population. P Natl Acad Sci USA 97:698–703CrossRefGoogle Scholar
  36. Lang SLC, Iverson SJ, Bowen WD (2011) The influence of reproductive experience on milk energy output and lactation performance in the grey seal (Halichoerus grypus). PLoS ONE 6:e19487CrossRefPubMedPubMedCentralGoogle Scholar
  37. Loehr J, Carey J, Hoefs M, Suhonen J, Ylönen H (2007) Horn growth rate and longevity: implications for natural and artificial selection in thinhorn sheep (Ovis dalli). Evol Biol 20:818–828CrossRefGoogle Scholar
  38. Loison A, Langvatn R, Solberg EJ (1999) Body mass and winter mortality in red deer calves: disentangling sex and climate effects. Ecography 22:20–30CrossRefGoogle Scholar
  39. Loison A, Solberg EJ, Yoccoz NG, Langvatn R (2004) Sex differences in the interplay of cohort and mother quality on body mass of red deer calves. Ecology 85:1992–2002CrossRefGoogle Scholar
  40. Mangel M, Munch SB (2005) A life-history perspective on short- and long-term consequences of compensatory growth. Am Nat 166:E155–E176CrossRefPubMedGoogle Scholar
  41. Margraf N, Gotthard K, Rahier M (2003) The growth strategy of an alpine beetle: maximization or individual growth adjustment in relation to seasonal time horizons? Funct Ecol 17:605–610CrossRefGoogle Scholar
  42. McAdam AG, Boutin S, Réale D, Berteaux D (2002) Maternal effects and the potential for evolution in a natural population of animals. Evolution 56:846–851CrossRefPubMedGoogle Scholar
  43. Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260CrossRefPubMedGoogle Scholar
  44. Michel ES, Demarais S, Strickland BK, Belant JL (2015) Contrasting the effects of maternal and behavioral characteristics on fawn birth mass in white-tailed deer. PLoS One 10:e0136034CrossRefPubMedPubMedCentralGoogle Scholar
  45. Michel ES, Flinn EB, Demarais S, Strickland BK, Wang G, Dacus CM (2016) Improved nutrition cues switch from efficiency to luxury phenotypes for a long-lived ungulate. Ecol Evol 20:7276–7285CrossRefGoogle Scholar
  46. Miller BF, Muller LI, Doherty T, Osborn DA, Miller KV, Warren RJ (2004) Effectiveness of antagonists for tiletamine-zolazepam/xylazine immobilization in female white-tailed deer. J Wildlife Dis 40:533–537CrossRefGoogle Scholar
  47. Mitchell RJ (2001) Path analysis: pollination. In: Scheiner SM, Gurevitc J (eds) Design and analysis of ecological experiments. Oxford University Press, New York, pp 217–234Google Scholar
  48. Monteith KL, Schmitz LE, Jenks JA, Delger JA, Bowyer RT (2009) Growth of male white-tailed deer: consequences of maternal effects. J Mammal 90:651–660CrossRefGoogle Scholar
  49. Monteith KL, Stephenson TR, Bleich VC, Conner MM, Pierce BM, Bowyer RT (2013) Risk-sensitive allocation in seasonal dynamics of fat and protein reserves in a long-lived mammal. J Anim Ecol 82:377–388CrossRefPubMedGoogle Scholar
  50. Nesbitt WH, Wright PL, Buckner EL, Byers CR, Reneau J (2009) Measuring and scoring North American big game trophies, 3rd edn. Boone and Crockett Club, MontanaGoogle Scholar
  51. Orizaola G, Dahl E, Laurila A (2010) Compensating for delayed hatching across consecutive life-history stages in an amphibian. Okios 119:980–987CrossRefGoogle Scholar
  52. Palomares F, Ferreras P, Travaini A, Delibes M (1998) Co-existence between Iberian lynx and Egyptian mongooses: estimating interaction strength by structural equation modeling and testing by an observational study. J Anim Ecol 67:967–978CrossRefPubMedGoogle Scholar
  53. Parker KL, Barboza PS, Gillingham MP (2009) Nutrition integrates environmental responses of ungulates. Funct Ecol 23:57–69CrossRefGoogle Scholar
  54. Plard F, Gaillard JM, Coulson T, Hewison AJM, Douhard M, Klein F, Delorme D, Warnant C, Bonenfant C (2015) The influence of birth date via body mass on individual fitness in a long-lived mammal. Ecology 96:1516–1528CrossRefGoogle Scholar
  55. Räsänen K, Kruuk LEB (2007) Maternal effects and evolution at ecological time-scales. Funct Ecol 21:408–421CrossRefGoogle Scholar
  56. 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 60:2168–2181CrossRefPubMedGoogle Scholar
  57. Rughetti M, Festa-Bianchet M (2010) Compensatory growth limits opportunities for artificial selection in alpine chamois. J Wildlife Manage 74:1024–1029CrossRefGoogle Scholar
  58. Saether BE, Solberg EJ, Heim M (2003) Effects of altering sex ratio structure on the demography of an isolated moose population. J Wildlife Manage 67:455–466CrossRefGoogle Scholar
  59. Schultz SR, Johnson MK (1995) Effects of birth date and body mass at birth on adult body mass of male white-tailed deer. J Mammal 76:575–579CrossRefGoogle Scholar
  60. Schumacker RE, Lomax RG (2004) A beginner’s guide to structural equation modeling. Lawrence Erlbaum Associates, New JerseyGoogle Scholar
  61. Shama LNS, Robinson CT (2006) Sex-specific life-history responses to seasonal time constraints in an alpine caddisfly. Evol Ecol Res 8:169–180Google Scholar
  62. Shipley B (2000a) A new inferential test for path models based on directed acyclic graphs. Struct Equ Model 7:206–218CrossRefGoogle Scholar
  63. Shipley B (2000b) Cause and correlation in biology: a user’s guide to path analysis, structural equations and causal inference. Cambridge University Press, New YorkCrossRefGoogle Scholar
  64. Shipley B (2003) Testing recursive path models with correlated errors using d-separation. Struct Equ Model 10:214–221CrossRefGoogle Scholar
  65. Shipley B (2009) Confirmatory path analysis in a generalized multilevel context. Ecology 90:363–368CrossRefPubMedGoogle Scholar
  66. Shipley B (2013) The AIC model selection method applied to path analytic models compared using a d-separation test. Ecology 94:560–564CrossRefPubMedGoogle Scholar
  67. Simard MA, Huot J, de Bellefeuille D, Côté SD (2014) Linking conception and weaning success with environmental variation and female body condition in a northern ungulate. J Mammal 95:311–327CrossRefGoogle Scholar
  68. Skalski GT, Picha ME, Gilliam JF, Borski RJ (2005) Variable intake, compensatory growth, and increased growth efficiency in fish: models and mechanisms. Ecology 86:1452–1462CrossRefGoogle Scholar
  69. Solberg EJ, Heim M, Grøtan V, Saether BE, Garel M (2007) Annual variation in maternal age and calving date generate cohort effects in moose (Alces alces) body mass. Oecologia 154:259–271CrossRefPubMedGoogle Scholar
  70. Solberg EJ, Garel M, Heim M, Grøtan V, Saether BE (2008) Lack of compensatory body growth in a high performance moose Alces alces population. Oecologia 158:485–498CrossRefPubMedGoogle Scholar
  71. Stearns SC (2000) Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87:476–486CrossRefPubMedGoogle Scholar
  72. Steiger S (2013) Bigger mothers are better mothers: disentangling size-related prenatal and postnatal maternal effects. P Roy Soc Lond B Bio 280:20131225CrossRefGoogle Scholar
  73. Stier A, Viblanc VA, Massemin-Challet S, Handrich Y, Zahn S, Rojas ER, Saraux C, Le Vaillant M, Prud’homme O, Grosbellet E, Robin JP, Bize P, Criscuolo F (2014) Starting with a handicap: phenotypic differences between early- and late-born king penguin chicks and their survival correlates. Funct Ecol 28:601–611CrossRefGoogle Scholar
  74. Strickland BK, Demarais S (2000) Age and regional differences in antlers and mass of white-tailed deer. J Wildlife Manage 64:903–911CrossRefGoogle Scholar
  75. Therrien JF, Côté SD, Festa-Bianchet M, Ouellet JP (2008) Maternal care in white-tailed deer: trade-off between maintenance and reproduction under food restriction. Anim Behav 75:235–243CrossRefGoogle Scholar
  76. Thomas DW, Shipley B, Blonde J, Perret P, Simon A, Lambrects MM (2007) Common paths link food abundance and ectoparasite loads to physiological performance and recruitment in nestling blue tits. Funct Ecol 21:947–955CrossRefGoogle Scholar
  77. Thompson CB, Holter JB, Hayes HH, Silver H, Urban WE (1973) Nutrition of white-tailed deer. 1. Energy requirements of fawns. J Wildlife Manage 37:301–311CrossRefGoogle Scholar
  78. Verme LJ (1989) Maternal investment in white-tailed deer. J Mammal 70:438–442CrossRefGoogle Scholar
  79. Verme LJ, Ozoga JJ (1980) Effects of diet on growth and lipogenesis in deer fawns. J Wildlife Manage 44:315–324CrossRefGoogle Scholar
  80. Verme LJ, Ullrey DE (1984) Physiology and nutrition. In: Halls LK, House C (eds) White-tailed deer ecology and management. Stackpole Books, Pennsylvania, pp 91–118Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Eric S. Michel
    • 1
    • 3
  • Stephen Demarais
    • 1
  • Bronson K. Strickland
    • 1
  • Guiming Wang
    • 2
  1. 1.Deer Ecology and Management Laboratory, Department of Wildlife, Fisheries and Aquaculture, Forest and Wildlife Research CenterMississippi State UniversityMississippi StateUSA
  2. 2.Department of Wildlife, Fisheries and AquacultureMississippi State UniversityMississippi StateUSA
  3. 3.Department of Natural Resource ManagementSouth Dakota State UniversityBrookingsUSA

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