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.
Similar content being viewed by others
References
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 48:776–787
Ali M, Nicieza A, Wootton RJ (2003) Compensatory growth in fishes: a response to growth depression. Fish Fish 4:147–190
Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 72:149–177
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
Bernardo J (1996) Maternal effects in animal ecology. Am Zool 36:83–105
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, USA
Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach. Springer, New York
Clutton-Brock TH, Guinness FE, Albon SD (1982) Red Deer: behavior and ecology of two sexes. The University of Chicago Press, Illinois
Coltman DW, Festa-Bianchet M, Jorgenson JT, Strobeck C (2001) Age-dependent sexual selection in bighorn rams. P Roy Soc Lond B Bio 269:165–172
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 155:1–61
Côté SD, Festa-Bianchet M (2001) Birthdate, mass and survival in mountain got kids: effects of maternal characteristics and forage quality. Oecologia 127:230–238
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 85:11–20
Demarais S, Strickland BK (2011) Antlers. In: Hewitt DG (ed) Biology and management of white-tailed deer. Florida CRC Press, Florida, pp 107–146
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 601–628
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 311–354
Ditchkoff SS (2011) Anatomy and physiology. In: Hewitt DG (ed) Biology and management of white-tailed deer. Florida CRC Press, Florida, pp 43–74
Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116
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 126:1329–1338
Favre M, Martin JG, Festa-Bianchet M (2008) Determinants and life-history consequences of social dominance in bighorn ewes. Anim Behav 76:1373–1380
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 156:773–781
Festa-Bianchet M, Jorgenson JT, Wishart WD (1995) Life history consequences of variation in age of primiparity in bighorn ewes. Ecology 76:871–881
Festa-Bianchet M, Jorgenson JT, Réale D (2000) Early development, adult mass, and reproductive success in bighorn sheep. Behav Ecol 11:633–639
Flinn EB, Strickland BK, Demarais S, Chistiansen D (2013) Age and gender affect epiphyseal closure in white-tailed deer. Southeast Nat 12:297–306
Gaillard JM, Delorme D, Jullien JM (1993) Effects of cohort, sex, and birth date on body development of roe deer (Capreolus capreolus) fawns. Oecologia 94:57–61
Gotthard K (2000) Increased risk of predation as a cost of high growth rate: an experimental test in a butterfly. J Anim Ecol 69:896–902
Green WCH, Rothstein A (1991) Trade-offs between growth and reproduction in female bison. Oecologia 86:521–527
Green WCH, Rothstein A (1993) Persistent influences of birth date on dominance, growth and reproductive success in bison. J Zool 230:177–186
Gurney WSC, Jones W, Veitch AR, Nisbet RM (2003) Resource allocation, hyperphagia, and compensatory growth in juveniles. Ecology 84:2777–2787
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 78:143–151
Hewison AJM, Gaillard JM (1999) Successful sons or advantaged daughters? The Trivers-Willard model and sex-biased maternal investment in ungulates. Trends Ecol Evol 14:229–234
Hewitt DG (2011) Nutrition. In: Hewitt DG (ed) Biology and management of white-tailed deer. CRC Press, Florida, pp 5–106
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 89:1480–1490
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 19:302–310
Kreeger TJ (1996) Handbook of wildlife chemical immobilization. International Wildlife Veterinary Services, Wyoming
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 97:698–703
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:e19487
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 20:818–828
Loison A, Langvatn R, Solberg EJ (1999) Body mass and winter mortality in red deer calves: disentangling sex and climate effects. Ecography 22:20–30
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 85:1992–2002
Mangel M, Munch SB (2005) A life-history perspective on short- and long-term consequences of compensatory growth. Am Nat 166:E155–E176
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 17:605–610
McAdam AG, Boutin S, Réale D, Berteaux D (2002) Maternal effects and the potential for evolution in a natural population of animals. Evolution 56:846–851
Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260
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:e0136034
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 20:7276–7285
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 40:533–537
Mitchell RJ (2001) Path analysis: pollination. In: Scheiner SM, Gurevitc J (eds) Design and analysis of ecological experiments. Oxford University Press, New York, pp 217–234
Monteith KL, Schmitz LE, Jenks JA, Delger JA, Bowyer RT (2009) Growth of male white-tailed deer: consequences of maternal effects. J Mammal 90:651–660
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 82:377–388
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, Montana
Orizaola G, Dahl E, Laurila A (2010) Compensating for delayed hatching across consecutive life-history stages in an amphibian. Okios 119:980–987
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 67:967–978
Parker KL, Barboza PS, Gillingham MP (2009) Nutrition integrates environmental responses of ungulates. Funct Ecol 23:57–69
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 96:1516–1528
Räsänen K, Kruuk LEB (2007) Maternal effects and evolution at ecological time-scales. Funct Ecol 21:408–421
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
Rughetti M, Festa-Bianchet M (2010) Compensatory growth limits opportunities for artificial selection in alpine chamois. J Wildlife Manage 74:1024–1029
Saether BE, Solberg EJ, Heim M (2003) Effects of altering sex ratio structure on the demography of an isolated moose population. J Wildlife Manage 67:455–466
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 76:575–579
Schumacker RE, Lomax RG (2004) A beginner’s guide to structural equation modeling. Lawrence Erlbaum Associates, New Jersey
Shama LNS, Robinson CT (2006) Sex-specific life-history responses to seasonal time constraints in an alpine caddisfly. Evol Ecol Res 8:169–180
Shipley B (2000a) A new inferential test for path models based on directed acyclic graphs. Struct Equ Model 7:206–218
Shipley B (2000b) Cause and correlation in biology: a user’s guide to path analysis, structural equations and causal inference. Cambridge University Press, New York
Shipley B (2003) Testing recursive path models with correlated errors using d-separation. Struct Equ Model 10:214–221
Shipley B (2009) Confirmatory path analysis in a generalized multilevel context. Ecology 90:363–368
Shipley B (2013) The AIC model selection method applied to path analytic models compared using a d-separation test. Ecology 94:560–564
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 95:311–327
Skalski GT, Picha ME, Gilliam JF, Borski RJ (2005) Variable intake, compensatory growth, and increased growth efficiency in fish: models and mechanisms. Ecology 86:1452–1462
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 154:259–271
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 158:485–498
Stearns SC (2000) Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87:476–486
Steiger S (2013) Bigger mothers are better mothers: disentangling size-related prenatal and postnatal maternal effects. P Roy Soc Lond B Bio 280:20131225
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 28:601–611
Strickland BK, Demarais S (2000) Age and regional differences in antlers and mass of white-tailed deer. J Wildlife Manage 64:903–911
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 75:235–243
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 21:947–955
Thompson CB, Holter JB, Hayes HH, Silver H, Urban WE (1973) Nutrition of white-tailed deer. 1. Energy requirements of fawns. J Wildlife Manage 37:301–311
Verme LJ (1989) Maternal investment in white-tailed deer. J Mammal 70:438–442
Verme LJ, Ozoga JJ (1980) Effects of diet on growth and lipogenesis in deer fawns. J Wildlife Manage 44:315–324
Verme LJ, Ullrey DE (1984) Physiology and nutrition. In: Halls LK, House C (eds) White-tailed deer ecology and management. Stackpole Books, Pennsylvania, pp 91–118
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 information
Authors and Affiliations
Contributions
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.
Corresponding author
Ethics declarations
Ethical approval
All applicable institutional guidelines for the care and use of animals were followed.
Additional information
Communicated by Jean-Michel Gaillard.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Michel, E.S., Demarais, S., Strickland, B.K. et al. Birth date promotes a tortoise or hare tactic for body mass development of a long-lived male ungulate. Oecologia 186, 117–128 (2018). https://doi.org/10.1007/s00442-017-4013-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-017-4013-2