Skip to main content
SpringerLink
Log in

Costs and benefits of communal rearing to female prairie voles (Microtus ochrogaster)

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Communal rearing of offspring may help mothers maximize their investment in offspring at a reduced cost to their own bodily condition, thus maximizing their potential for reproductive success. The objective of this study was to quantify the costs and benefits of communal rearing to prairie vole (Microtus ochrogaster) pups and mothers. Mothers were assigned to one of three social units: solitary mothers, singularly breeding groups (i.e. one mother and one non-reproductive sister) and plurally breeding groups (i.e. two lactating sisters). For each type of social unit, some replicates were provided with food ad libitum, while others were provided with limited food. The body mass of focal mothers (i.e. the first mother to produce a litter) was a significant predictor of pup growth. Regardless of food availability, litters of focal mothers in plurally breeding groups gained more weight than litters reared by solitary mothers. Pups reared in singularly breeding groups were intermediate in weight gain, but did not gain significantly more weight than solitary offspring. There was no difference in the body mass of focal mothers from each type of social unit, regardless of food availability. Within plurally breeding groups, the weight gain of the two litters and body mass of focal and second mothers did not differ. However, focal mothers from plurally breeding groups nursed fewer pups than solitary mothers and also fewer pups than their nestmates when food was limited. Our results suggest that plural breeding results in greater fitness to mothers than solitary and singular breeding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Blumstein DT, Armitage KB (1999) Cooperative breeding in marmots. Oikos 84:369–382

    Google Scholar 

  • Brant CL, Schwab TM, Vandenbergh JG, Schaefer RL, Solomon NG (1998) Behavioural suppression of female pine voles after replacement of the breeding male. Anim Behav 55:615–627

    Article  PubMed  Google Scholar 

  • Cameron EZ (1998) Is suckling behaviour a useful predictor of milk intake? A review. Anim Behav 56:521–532

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Derrickson EM (1988) The effect of experimental termination of lactation on subsequent growth in Peromyscus leucopus. Can J Zool 66:2507–2512

    Google Scholar 

  • Ebensperger LA, Cofré H (2001) On the evolution of group-living in the New World cursorial hystricognath rodents. Behav Ecol 12:227–236

    Article  Google Scholar 

  • Elwood RW, Broom DM (1978) The influence of litter size and parental behaviour on the development of Mongolian gerbil pups. Anim Behav 26:438–454

    Google Scholar 

  • Festa-Bianchet M, Jorgenson JT, Réale D (2000) Early development, adult mass, and reproductive success in bighorn sheep. Behav Ecol 11:633–639

    Article  Google Scholar 

  • Gerlach G, Bartmann S (2002) Reproductive skew, costs and benefits of cooperative breeding in female wood mice (Apodemus sylvaticus). Behav Ecol 13:408–418

    Article  Google Scholar 

  • Getz LL, Simms LE, McGuire B, Snarski ME (1997) Factors affecting life expectancy of the prairie vole, Microtus ochrogaster. Oikos 80:362–370

    Google Scholar 

  • Getz LL, McGuire B, Pizzuto T, Hofmann JE, Frase B (1993) Social organization of the prairie vole (Microtus ochrogaster). J Mammal 74:44–58

    Google Scholar 

  • Getz LL, McGuire B (1997) Communal nesting in prairie voles (Microtus ochrogaster): formation, composition and persistence of communal groups. Can J Zool 75:525–534

    Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour. J Theor Biol 7:1–51

    CAS  PubMed  Google Scholar 

  • Hayes LD (2000) To nest communally or not to nest communally: a review of rodent communal nesting and nursing. Anim Behav 59:677–688

    Article  PubMed  Google Scholar 

  • Haywood S, Perrins CM (1992) Is clutch size in birds affected by environmental conditions during growth? Proc R Soc Lond B 249:195–197

    CAS  PubMed  Google Scholar 

  • Hoffmann RS, Koeppl JW (1985) Zoogeography. In: Tamarin RH (ed) Biology of New World Microtus. Am Soc Mamm Spec Publ No. 8, pp 84–115

  • Huber S, Millesi E, Walzl M, Dittami J, Arnold W (1999) Reproductive effort and costs of reproduction in female European ground squirrels. Oecologia 121:19–24

    Article  Google Scholar 

  • Huber S, Hoffmann IE, Millesi E, Dittami J, Arnold W (2001) Explaining the seasonal decline in litter size in European ground squirrels. Ecography 24:205–211

    Article  Google Scholar 

  • Innes DGL, Millar JS (1981) Body weight, litter size, and energetics of reproduction in Chlethrionomys gapperi and Microtus pennsylvanicus. Can J Zool 59:785–789

    Google Scholar 

  • Jonsson P, Agrell J, Koskela E, Mappes T (2002) Effects of litter size on pup defence and weaning success of neighbouring bank vole females. Can J Zool 80:1–5

    Article  Google Scholar 

  • Koivula M, Koskela E, Mappes T, Oksanen TA (2003) Cost of reproduction in the wild: manipulation of reproductive effort in the bank vole. Ecology 84:398–405

    Google Scholar 

  • König B (1994) Components of lifetime reproductive success in communally and solitarily nursing house mice—a laboratory study. Behav Ecol Sociobiol 34:275–283

    Article  Google Scholar 

  • König B (1997) Cooperative care of young in mammals. Naturwissenschaften 84:95–104

    Article  PubMed  Google Scholar 

  • Koskela E (1998) Offspring growth, survival and reproductive success in the bank vole: a litter size manipulation experiment. Oecologia 115:379–384

    Article  Google Scholar 

  • Lacey EA (2004) Sociality reduces individual direct fitness in a communally breeding rodent, the colonial tuco-tuco (Ctenomys sociabilis). Behav Ecol Sociobiol (in press)

  • Lacey EA, Sherman PW (1997) Cooperative breeding in naked mole-rats: implications for vertebrate and invertebrate sociality. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 267–301

  • Lima SL (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Adv Stud Behav 27:215–290

    Google Scholar 

  • Lindström J (1999) Early development and fitness in birds and mammals. Trends Evol Ecol 14:343–348

    Article  Google Scholar 

  • Madison DM (1984) Group nesting and its ecological and evolutionary significance in overwintering microtine rodents. In: Merritt JF (ed) Winter ecology of small mammals. Carnegie Mus Spec Publ, vol. 10, pp 267–274

  • McGuire B, Getz LL (1995) Communal nesting in prairie voles (Microtus ochrogaster): an evaluation of costs and benefits based on patterns of dispersal and settlement. Can J Zool 73:383–391

    Google Scholar 

  • McGuire B, Novak M (1984) A comparison of maternal behaviour in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum). Anim Behav 32:1132–1141

    Google Scholar 

  • McGuire B, Heller H, Novak M (1988) Milk composition and volume in meadow voles and prairie voles. Acta Theriol 33(26–43):537–544

    Google Scholar 

  • McGuire B, Getz LL, Oli MK (2002) Fitness consequences of sociality in prairie voles, Microtus ochrogaster: influence of group size and composition. Anim Behav 64:645–654

    Article  Google Scholar 

  • Mennella JA, Blumberg MS, McClintock MK, Moltz H (1990) Inter-litter competition and communal nursing among Norway rats: advantages of birth synchrony. Behav Ecol Sociobiol 27:183–190

    Google Scholar 

  • Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Evol Ecol 16:254–260

    Article  Google Scholar 

  • Neuhaus P (2000) Weight comparisons and litter size manipulation in Columbian ground squirrels (Spermophilus columbianus) show evidence of costs of reproduction. Behav Ecol Sociobiol 48:75–83

    Article  Google Scholar 

  • Pilastro A, Missiaglia E, Marin G (1996) Age-related reproductive success in solitarily and communally nesting female dormice (Glis glis). J Zool 239:601–608

    Google Scholar 

  • Powell RA, Fried JJ (1992) Helping by juvenile pine voles (Microtus pinetorum), growth and survival of younger siblings, and the evolution of pine vole sociality. Behav Ecol 3:325–333

    Google Scholar 

  • Richmond ME, Conaway CH (1969) Management, breeding and reproductive performance of the vole, Microtus ochrogaster in a laboratory colony. Lab Anim Care 19:80–87

    CAS  PubMed  Google Scholar 

  • Rogowitz GL (1996) Trade-offs in energy allocation during lactation. Am Zool 36:197–204

    Google Scholar 

  • Roulin A, Heeb P (1999) The immunological function of allosuckling. Ecol Lett 2:319–324

    Article  Google Scholar 

  • Russell AF, Clutton-Brock TH, Brotherton PNM, Sharpe LL, Mcilrath GM, Dalerum FD, Cameron EZ, Barnard JA (2002) Factors affecting pup growth and survival in co-operatively breeding meerkats Suricata suricatta. J Anim Ecol 71:700–709

    Article  Google Scholar 

  • Sayler A, Salmon M (1969) Communal nursing in mice: influence of multiple mothers on the growth of the young. Science 164:1309–1310

    CAS  PubMed  Google Scholar 

  • Sayler A, Salmon M (1971) An ethological analysis of communal nursing by the house mouse (Mus musculus). Behaviour 40:60–85

    Google Scholar 

  • Schanberg SM, Evoniuk G, Kuhn CM (1984) Tactile and nutritional aspects of maternal care-specific regulators of neuroendocrine function and cellular development. Proc Soc Exp Biol Med 175:135–146

    CAS  PubMed  Google Scholar 

  • Sheridan M, Tamarin RH (1988) Space use, longevity, and reproductive success in meadow voles. Behav Ecol Sociobiol 22:85–90

    Google Scholar 

  • Solomon NG (1991) Current indirect fitness benefits associated with philopatry in juvenile prairie voles. Behav Ecol Sociobiol 29:277–282

    Google Scholar 

  • Solomon NG (1993) Body size and social preferences of male and female prairie voles, Microtus ochrogaster. Anim Behav 45:1031–1033

    Article  Google Scholar 

  • Solomon NG (1994) Effect of the pre-weaning environment on subsequent reproduction in prairie voles, Microtus ochrogaster. Anim Behav 48:331–341

    Article  Google Scholar 

  • Solomon NG, Getz LL (1997) Examination of alternative hypotheses for cooperative breeding in rodents. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 199–230

  • Thompson SD (1992) Gestation and lactation in small mammals: basal metabolic rate and the limits of energy use. In: Tomasi TE, Horton TH (eds) Mammalian energetics: interdisciplinary views of metabolism and reproduction. Comstock, Ithaca, N.Y., pp 213–259

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago

  • Werboff J, Steg M, Barnes L (1970) Communal nursing in mice: strain-specific effects of multiple mothers on growth and behavior. Psychon Sci 19:269–271

    Google Scholar 

  • Wolff JO (1994) Reproductive success of solitarily and communally nesting white-footed and deer mice. Behav Ecol 5:206–209

    Google Scholar 

Download references

Acknowledgements

We thank V. Barko, C. Buckholtz and G. Feldhamer for helping us locate prairie voles. Several undergraduate students helped us with project, most notably E. O’Bryant. We thank P. Callahan, Y.K. Lin, A. Rypstra and R. Schaefer for their advice. B. Keane, E. Lacey and D. Meikle read an earlier version of this manuscript. L.D.H. was funded by an Animal Behavior Society Grant-in-Aid of Research, a Sigma Xi Grant-in-Aid of Research and a National Science Foundation Doctoral Dissertation Improvement Grant (IBN no. 0309068). N.G.S. was funded by the National Institute of Health (NIMH grant no. MH57115). The research was approved by the Miami University All University Animal Care Committee (Protocol no. 486) and was conducted in compliance with U.S. laws for the use of animals in research.

Author information

Authors and Affiliations

  1. Department of Zoology, Miami University, 212 Pearson Hall, Oxford, OH 45056, USA

    Loren Donald Hayes & Nancy Gail Solomon

Authors
  1. Loren Donald Hayes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nancy Gail Solomon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Loren Donald Hayes.

Additional information

Communicated by E. Korpimäki

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hayes, L.D., Solomon, N.G. Costs and benefits of communal rearing to female prairie voles (Microtus ochrogaster). Behav Ecol Sociobiol 56, 585–593 (2004). https://doi.org/10.1007/s00265-004-0815-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-004-0815-4

Keywords

Search

Navigation