Skip to main content
SpringerLink
Log in

Foraging competition in larger groups overrides harassment avoidance benefits in female reindeer (Rangifer tarandus)

  • Behavioral ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Male harassment toward females during the breeding season may have a negative effect on their reproductive success by disturbing their foraging activity, thereby inducing somatic costs. Accordingly, it is predicted that females will choose mates based on their ability to provide protection or will aggregate into large groups to dilute per capita harassment level. Conversely, increasing group size may also lead to a decrease in foraging activity by increasing foraging competition, but this effect has rarely been considered in mating tactic studies. This study examined the importance of two non-exclusive hypotheses in explaining the variations of the female activity budget during the breeding season: the male harassment hypothesis, and the female foraging competition hypothesis. We used focal observations of female activity from known mating groups collected during the breeding season from a long-term (15 years) study on reindeer Rangifer tarandus. We found that females were more disturbed (i.e., spent less time feeding) in the presence of young dominant males, and marginally disturbed in the presence of satellite males, which supports the male harassment hypothesis. We also found that female disturbance level increased with group size, being independent of the adult sex ratio. Consequently, these results rejected the dilution effect, but strongly supported the foraging competition hypothesis. This study therefore highlights a potential conflict in female behaviour. Indeed, any gains from harassment protection were negated by an increase of 6–7 females, since adult males lead larger groups than young males.

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
Fig. 3

Similar content being viewed by others

References

  • Berger J (1978) Group size, foraging, and antipredator ploys: an analysis of bighorn sheep decisions. Behav Ecol Sociobiol 4:91–99. doi:10.1007/BF00302563

    Article  Google Scholar 

  • Bierbach D, Sassmannshausen V, Streit B, Arias-Rodriguez L, Plath M (2013) Females prefer males with superior fighting abilities but avoid sexually harassing winners when eavesdropping on male fights. Behav Ecol Sociobiol 67:675–683. doi:10.1007/s00265-013-1487-8

    Article  Google Scholar 

  • Body G, Weladji RB, Holand Ø, Nieminen M (2014) Highly competitive reindeer males control female behavior during the rut. PLoS ONE 9:e95618

    Article  PubMed Central  PubMed  Google Scholar 

  • Body G, Weladji RB, Holand Ø, Nieminen M (2015) Fission-fusion group dynamics in reindeer reveal an increase of cohesiveness at the beginning of the peak rut. Acta Ethol 18:101–110. doi:10.1007/s10211-014-0190-8

    Article  Google Scholar 

  • Bro-Jørgensen J (2011) Intra- and intersexual conflicts and cooperation in the evolution of mating strategies: lessons learnt from ungulates. Evol Biol 38:28–41. doi:10.1007/s11692-010-9105-4

    Article  Google Scholar 

  • Burnham K, Anderson D (2002) Model selection and multimodel inference: a practical information-theoretical approach. Springer, New York

    Google Scholar 

  • Byers JA, Moodie JD, Hall N (1994) Pronghorn females choose vigorous mates. Anim Behav 47:33–43

    Article  Google Scholar 

  • Cameron EZ, Setsaas TH, Linklater WL (2009) Social bonds between unrelated females increase reproductive success in feral horses. Proc Natl Acad Sci USA 106:13850–13853. doi:10.1073/pnas.0900639106

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carranza J (1995) Female attraction by males versus sites in territorial rutting red deer. Anim Behav 50:445–453. doi:10.1006/anbe.1995.0258

    Article  Google Scholar 

  • Carranza J, Valencia J (1999) Red deer females collect on male clumps at mating areas. Behav Ecol 10:525–532. doi:10.1093/beheco/10.5.525

    Article  Google Scholar 

  • Clutton-Brock TH, McAuliffe K (2009) Female mate choice in mammals. Q Rev Biol 84:3–27

    Article  PubMed  Google Scholar 

  • Clutton-Brock TH, Parker GA (1992) Potential reproductive rates and the operation of sexual selection. Q Rev Biol 67:437–456

    Article  Google Scholar 

  • Clutton-Brock TH, Vincent ACJ (1991) Sexual selection and the potential reproductive rates of males and females. Nature 351:58–60

    Article  CAS  PubMed  Google Scholar 

  • Clutton-Brock TH, Price OF, MacColl ADC (1992) Mate retention, harassment, and the evolution of ungulate leks. Behav Ecol 3:234–242. doi:10.1093/beheco/3.3.234

    Article  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, Chichester

    Book  Google Scholar 

  • Danchin E, Giraldeau L-A, Cézilly F (2008) Behavioural ecology. Oxford University Press, Oxford

    Google Scholar 

  • De Jong K, Forsgren E, Sandvik H, Amundsen T (2012) Measuring mating competition correctly: available evidence supports operational sex ratio theory. Behav Ecol 23:1170–1177. doi:10.1093/beheco/ars094

    Article  Google Scholar 

  • Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223

    Article  CAS  PubMed  Google Scholar 

  • Festa-Bianchet M (1998) Condition-dependent reproductive success in bighorn ewes. Ecol Lett 1:91–94. doi:10.1046/j.1461-0248.1998.00023.x

    Article  Google Scholar 

  • Focardi S, Pecchioli E (2005) Social cohesion and foraging decrease with group size in fallow deer (Dama dama). Behav Ecol Sociobiol 59:84–91. doi:10.1007/s00265-005-0012-0

    Article  Google Scholar 

  • Fortin D, Fortin M-E, Beyer HL, Duchesne T, Courant S, Dancose K (2009) Group-size-mediated habitat selection and group fusion–fission dynamics of bison under predation risk. Ecology 90:2480–2490

    Article  PubMed  Google Scholar 

  • Gittleman JL, Thompson SD (1988) Energy allocation in mammalian reproduction. Am Zool 28:863–875. doi:10.1093/icb/28.3.863

    Article  Google Scholar 

  • Hewison AJM, Vincent JP, Reby D (1998) Social organization of European roe deer. In: Andersen R, Duncan P, Linnell JDC (eds) The European roe deer: the biology of success. Scandinavian University Press, Oslo, pp 189–219

    Google Scholar 

  • Holand Ø, Weladji RB, Røed KH, Gjøstein H, Kumpula J, Gaillard J-M, Smith ME, Nieminen M (2006) Male age structure influences females’ mass change during rut in a polygynous ungulate: the reindeer (Rangifer tarandus). Behav Ecol Sociobiol 59:682–688. doi:10.1007/s00265-005-0097-5

    Article  Google Scholar 

  • Isvaran K (2005) Variation in male mating behaviour within ungulate populations : patterns and processes. Curr Sci 89:1192–1199

    Google Scholar 

  • Kojola I (1986) Rutting behaviour in an enclosured group of wild forest reindeer. Rangifer 1:173–179

    Article  Google Scholar 

  • Kojola I, Nieminen M (1988) Aggression and nearest neighbour distances in female reindeer during the rut. Ethology 77:217–224. doi:10.1111/j.1439-0310.1988.tb00205.x

    Article  Google Scholar 

  • Komers PE, Birgersson B, Ekvall K (1999) Timing of estrus in fallow deer is adjusted to the age of available mates. Am Nat 153:431–436

    Article  Google Scholar 

  • L’Italien L, Weladji RB, Holand Ø, Røed KH, Nieminen M, Côté SD (2012) Mating group size and stability in reindeer Rangifer tarandus: the effects of male characteristics, sex ratio and male age structure. Ethology 118:783–792. doi:10.1111/j.1439-0310.2012.02073.x

    Article  Google Scholar 

  • Lent P (1965) Rutting behaviour in a barren-ground caribou population. Anim Behav 13:259–264. doi:10.1016/0003-3472(65)90044-8

    Article  CAS  PubMed  Google Scholar 

  • Linklater W, Cameron E, Minot E, Stafford K (1999) Stallion harassment and the mating system of horses. Anim Behav 58:295–306. doi:10.1006/anbe.1999.1155

    Article  PubMed  Google Scholar 

  • Lipetz VE, Bekoff M (1982) Group size and vigilance in pronghorns. Z Tierpsychol 58:203–216

    Article  Google Scholar 

  • Makowicz AM, Schlupp I (2013) The direct costs of living in a sexually harassing environment. Anim Behav 85:569–577. doi:10.1016/j.anbehav.2012.12.016

    Article  Google Scholar 

  • Marshall HH, Carter AJ, Rowcliffe JM, Cowlishaw G (2012) Linking social foraging behaviour with individual time budgets and emergent group-level phenomena. Anim Behav 84:1295–1305. doi:10.1016/j.anbehav.2012.09.030

    Article  Google Scholar 

  • Martin P, Bateson P (2007) Measuring behaviour: an introductory guide, 3rd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • McMahon CR, Bradshaw CJA (2004) Harem choice and breeding experience of female southern elephant seals influence offspring survival. Behav Ecol Sociobiol 55:349–362. doi:10.1007/s00265-003-0721-1

    Article  Google Scholar 

  • Melnycky N, Weladji RB, Holand Ø, Nieminen M (2013) Scaling of antler size in reindeer (Rangifer tarandus): sexual dimorphism and variability in resource allocation. J Mammal 6:1371–1379. doi:10.1644/12-MAMM-A-282.1

    Article  Google Scholar 

  • Nieminen M (2013) Response distances of wild forest reindeer (Rangifer tarandus fennicus Lönnb.) and semi-domestic reindeer (R.t. tarandus L.) to direct provocation by a hu- man on foot/snowshoes. Rangifer 33:1–15

    Article  Google Scholar 

  • Pays O, Fortin D, Gassani J, Duchesne J (2012) Group dynamics and landscape features constrain the exploration of herds in fusion–fission societies: the case of European roe deer. PLoS ONE 7:e34678. doi:10.1371/journal.pone.0034678

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • R Development Core Team (2013) R: A language and environment for statistical computing. R foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org/

  • Réale D, Boussès P, Chapuis J (1996) Female-biased mortality induced by male sexual harassment in a feral sheep population. Can J Zool 74:1812–1818

    Article  Google Scholar 

  • Reimers E, Røed KH, Colman JE (2012) Persistence of vigilance and flight response behaviour in wild reindeer with varying domestic ancestry. J Evol Biol 25:1543–1554. doi:10.1111/j.1420-9101.2012.02538.x

    Article  CAS  PubMed  Google Scholar 

  • Rodney D, Boert J (1985) Seasonal activity of the Denali caribou herd, Alaska. Rangifer 5:32–42

    Article  Google Scholar 

  • Ropstad E (2000) Reproduction in female reindeer. Anim Reprod Sci 60–61:561–570

    Article  PubMed  Google Scholar 

  • Stephens DW, Brown JS, Ydenberg RC (2007) Foraging: behavior and ecology. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Symonds MRE, Moussalli A (2010) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21. doi:10.1007/s00265-010-1037-6

    Article  Google Scholar 

  • Tennenhouse EM, Weladji RB, Holand Ø, Røed KH, Nieminen M (2011) Mating group composition influences somatic costs and activity in rutting dominant male reindeer (Rangifer tarandus). Behav Ecol Sociobiol 65:287–295. doi:10.1007/s00265-010-1043-8

    Article  Google Scholar 

  • Tennenhouse EM, Weladji RB, Holand Ø, Nieminen M (2012) Timing of reproductive effort differs between young and old dominant male reindeer. Ann Zool Fenn 49:152–160

    Article  Google Scholar 

  • Tettamanti F, Viblanc VA (2014) Influences of mating group composition on the behavioral time-budget of male and female Alpine Ibex (Capra ibex) during the rut. PLoS ONE 9:e86004. doi:10.1371/journal.pone.0086004

    Article  PubMed Central  PubMed  Google Scholar 

  • Tobler M, Schlupp I, Plath M (2011) Costly interactions between the sexes: combined effects of male sexual harassment and female choice? Behav Ecol 22:723–729. doi:10.1093/beheco/arr044

    Article  Google Scholar 

  • Weir LK (2013) Male–male competition and alternative male mating tactics influence female behavior and fertility in Japanese medaka (Oryzias latipes). Behav Ecol Sociobiol 67:193–203. doi:10.1007/s00265-012-1438-9

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank Mika Tervonen of the Finnish Reindeer Herder’s Association for the management of Reindeer in Finland, and Heikki Törmänen of the Reindeer Research Station for compiling this long-term database. We thank Hallvard Gjøstein, Eliana Pintus, Sacha Engelhardt and numerous field crew members who helped with data collection over the years, and Juan Carranza, Denis Réale and two anonymous reviewers for comments. Handling of animals and data collection was done in agreement with the Animal Ethics and Care certificate provided by Concordia University (AREC-2010-WELA and AREC-2011-WELA) and by the Finnish National Advisory Board on Research Ethics.

Author contribution statement

GB, RBW, ØH and MN conceived and designed the experiments. SU, GB, RBW, ØH performed the experiments. SU, GB analyzed the data. SU, GB, RBW wrote the manuscript. ØH, MN provided editorial advices.

Author information

Authors and Affiliations

  1. Department of Biology, Concordia University, 7141 Sherbrooke Street West, Montreal, QC, H4B 1R6, Canada

    Stefania Uccheddu, Guillaume Body & Robert B. Weladji

  2. Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås, Norway

    Øystein Holand

  3. Finnish Game and Fisheries Research Institute, Reindeer Research Station, Kaamanen, Finland

    Mauri Nieminen

Authors
  1. Stefania Uccheddu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guillaume Body
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert B. Weladji
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Øystein Holand
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mauri Nieminen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Robert B. Weladji.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Ilpo Kojola.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Uccheddu, S., Body, G., Weladji, R.B. et al. Foraging competition in larger groups overrides harassment avoidance benefits in female reindeer (Rangifer tarandus). Oecologia 179, 711–718 (2015). https://doi.org/10.1007/s00442-015-3392-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3392-5

Keywords

Search

Navigation