, Volume 144, Issue 2, pp 289–298 | Cite as

Interactions between population processes in a cyclic species: parasites reduce autumn territorial behaviour of male red grouse

  • Franccois Mougeot
  • Sharon A. Evans
  • Stephen M. Redpath
Population Ecology


The causes of population cycles fascinate and perplex ecologist. Most work have focused on single processes, whether extrinsic or intrinsic, more rarely on how different processes might interact to cause or mould the unstable population dynamics. In red grouse (Lagopus lagopus scoticus), two causal mechanisms have been supported: territorial behaviour (changes in autumn aggressiveness) and parasites (parasite induced reduction in fecundity). Here, we report on how these two regulatory processes might interact, by testing whether the parasite suspected to cause the grouse cycles, the nematode Trichostrongylus tenuis, reduces male autumn territorial behaviour. We either treated males with an anthelmintic, to remove parasites (dosed or D-males), or challenged them with infective T. tenuis larvae, to increase parasite intensity (challenged or C-males). We first show that dosing was effective in removing T. tenuis parasites, while parasite intensities increased in challenged birds during the autumn. Because old males initially had more parasites than young males, the treatments generated greater differences in parasite intensity in old than in young males. We also show that various aspects of territorial behaviour (increase in testosterone-dependent comb size in autumn, territorial call rate, likelihood of winning territorial interactions and over-winter survival) were significantly higher in dosed than in challenged males, but in old birds only. Our data thus supported the hypothesis that parasites reduce male aggressiveness during the autumn territorial contests, and could thereby influence recruitment. Our results also highlight that the territorial behaviour of young males, which have fewer parasites, is not as limited by parasites as that of old, previously territorial males. We discuss the implications of these findings for our understanding of the processes regulating red grouse populations and causing their complex, unstable population dynamics.


Aggression Lagopus lagopus scoticus Population regulation Unstable dynamics Trichostrongylus tenuis 


  1. Berryman AA (2002) Population cycles: the case for trophic interactions. Oxford University Press, OxfordGoogle Scholar
  2. Cramp S, Simmons KEL (1980) The birds of the western palearctic, vol 2. Oxford University Press, OxfordGoogle Scholar
  3. Dobson AP, Hudson PJ (1992) Regulation and stability of a free-living host-parasite system—Trichostrongylus tenuis in red grouse. II. Population models. J Anim Ecol 61:487–498CrossRefGoogle Scholar
  4. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622CrossRefGoogle Scholar
  5. Fox A, Hudson PJ (2001) Parasites reduce territorial behaviour in red grouse (Lagopus lagopus scoticus). Ecol Lett 4:139–143CrossRefGoogle Scholar
  6. Haydon DT, Shaw DJ, Cattadori IM, Hudson PJ, Thirgood SJ (2002) Analysing noisy time-series: describing regional variation in the cyclic dynamics of red grouse. Proc R Soc Lond B 269:1609–1617CrossRefGoogle Scholar
  7. Hillgarth N, Wingfield JC (1997) Parasite-mediated sexual selection: endocrine aspects. In: Clayton DH, Moore J (eds) Host-parasite evolution. General Principles and Avian Models. Oxford University Press, Oxford, pp 78–104Google Scholar
  8. Hudson PJ (1986) The red grouse: the biology and management of a wild gamebird. The Game Conservancy Trust, FordingbridgeGoogle Scholar
  9. Hudson PJ, Newborn D, Dobson AP (1992) Regulation and stability of a free-living host-parasite system—Trichostrongylus tenuis in red grouse. I. Monitoring and parasite reduction experiments. J Anim Ecol 61:477–486CrossRefGoogle Scholar
  10. Hudson PJ, Dobson AP (1997) Transmission dynamics and host-parasite interactions of Trichostrongylus tenuis in red grouse (Lagopus lagopus scoticus). J Parasitogy 83:194–202CrossRefGoogle Scholar
  11. Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258CrossRefPubMedGoogle Scholar
  12. Hudson PJ et al. (2002) Trophic interactions and population growth rates: describing patterns and identifying mechanisms. Phil Trans R Soc Lond B357:1259–1271CrossRefGoogle Scholar
  13. Klemola T, Koivula M, Korpimaki E, Norrdahl K (2000) Experimental tests of predation and food hypotheses for population cycles of voles. Proc R Soc Lond B 267:351–356CrossRefGoogle Scholar
  14. Krebs CJ et al. (1995) Impact of food and predation on the snowshoe hare cycle. Science 269:1112–1115PubMedCrossRefGoogle Scholar
  15. MacColl ADC, Piertney SB, Moss R, Lambin X (2000) Spatial arrangement of kin affects recruitment success in young male red grouse. Oikos 90:261–270CrossRefGoogle Scholar
  16. Matthiopoulos J, Moss R, Lambin X (1998) Models of red grouse cycles: a family affair? Oikos 82:574–590CrossRefGoogle Scholar
  17. Matthiopoulos J, Moss R, Mougeot F, Lambin X, Redpath SM (2003) Territorial behaviour and population dynamics in red grouse Lagopus lagopus scoticus. II. Population models. J Anim Ecol 72:1083–1096CrossRefGoogle Scholar
  18. Matthiopoulos J, Halley J.M., Moss R (2005) Socially-induced population cycles in red grouse require abrupt transitions between tolerant and aggressive behaviour. Ecology (in press)Google Scholar
  19. Moss R et al (1979) Aggressiveness and dominance in captive cock red grouse. Aggr Behav 5:58–84CrossRefGoogle Scholar
  20. Moss R, Watson A, Parr R (1988) Mate choice by hen red grouse Lagopus lagopus with an excess of cocks—role of territory size and food quality. Ibis 130:545–552Google Scholar
  21. Moss R, Trenholm IB, Watson A, Parr R (1990) Parasitism, predation and survival of hen red grouse Lagopus lagopus scoticus in spring. J Anim Ecol 59:631–642CrossRefGoogle Scholar
  22. Moss R, Watson A (2001) Population cycles in birds of the grouse family (Tetraonidae). Adv Ecol Res 32:53–111CrossRefGoogle Scholar
  23. Mougeot F, Redpath SM, Leckie F, Hudson PJ (2003a) The effect of aggressiveness on the population dynamics of a territorial bird. Nature 421:737–739PubMedCrossRefGoogle Scholar
  24. Mougeot F, Redpath SM, Moss R, Matthiopoulos J, Hudson PJ (2003b) Territorial behaviour and population dynamics in red grouse Lagopus lagopus scoticus. I. Population experiments. J Anim Ecol 72:1073–1082CrossRefGoogle Scholar
  25. Mougeot F, Redpath S (2004) Sexual ornamentation relates to immune function in male red grouse Lagopus lagopus scoticus. J Avian Biol 35:425–433CrossRefGoogle Scholar
  26. Mougeot F, Irvine J, Seivwright LJ, Redpath S, Piertney SB (2004) Testosterone, immunocompetence and honest sexual signaling in male red grouse. Behav Ecol 15:630–637CrossRefGoogle Scholar
  27. Mougeot F, Dawson A, Redpath S, Leckie F (2005a) Testosterone and autumn territorial behaviour in male red grouse Lagopus lagopus scoticus. Horm Behav (in press)Google Scholar
  28. Mougeot F, Piertney S, Leckie F, Evans S, Moss R, Redpath S, Hudson PJ (2005b) Experimentally increased aggressiveness reduces population kin structure and subsequent recruitment in red grouse Lagopus lagopus scoticus. J Anim Ecol (in press)Google Scholar
  29. Mountford MD, Watson A, Moss R, Parr R, Rothery P (1990) Land inheritance and population cycles of red grouse. In: Lance AN, Lawton JH (eds) Red Grouse Population Processes. Royal Society for the Protection of Birds, Sandy, Bedfordshire, pp 78–83Google Scholar
  30. Packer C, Holt RD, Hudson PJ, Lafferty KD, Dobson AP (2003) Keeping the herds healthy and alert: implications of predator control for infectious disease. Ecol Lett 6:797–802CrossRefGoogle Scholar
  31. Park KJ, Hurley MM, Hudson PJ (2002) Territorial status and survival in red grouse Lagopus lagopus scoticus: hope for the doomed surplus? J Avian Biol 33:56–62CrossRefGoogle Scholar
  32. Peters A, Delhey K, Denk AG, Kempenaers B (2004) Trade-offs between immune investment and sexual signaling in male mallards. Am Nat 164:51–59CrossRefPubMedGoogle Scholar
  33. SAS (2001) SAS/STAT User’s guide, version 8.01. SAS Insitute Inc., CaryGoogle Scholar
  34. Seivwright LJ (2004) Pattern of Trichostrongylus tenuis infection in individual red grouse Lagopus lagopus scoticus. PhD dissertation. University of StirlingGoogle Scholar
  35. Seivwright LJ, Redpath S, Mougeot F, Watt L, Hudson PJ (2004) Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. J Helm 78:69–76CrossRefGoogle Scholar
  36. Seivwright LJ, Redpath S, Mougeot F, Leckie F, Hudson PJ (2005) Interactions between population processes in a cyclic species: testosterone increases parasite intensity, (submitted)Google Scholar
  37. Shaw JL (1988) Arrested development of Trichostrongylus tenuis as 3rd stage larvae in red grouse. Res Vet Sci 45:256–258PubMedGoogle Scholar
  38. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321CrossRefGoogle Scholar
  39. Stenseth NC, Bjornstad ON, Falck W (1996) Is spacing behaviour coupled with predation causing the microtine density cycle? A synthesis of current process-oriented and pattern-oriented studies. Proc R Soc Lond B 263:1423–1435CrossRefGoogle Scholar
  40. Turchin P (2003) Complex population dynamics: a theoritical/empirical synthesis. University Press, PrincetonGoogle Scholar
  41. Verhulst S, Dieleman SJ, Parmentier HK (1999) A trade-off between immunocompetence and sexual ornamentation in domestic fowl. PNAS 96:4478–4481CrossRefPubMedGoogle Scholar
  42. Watson A (1985) Social class, socially-induced loss, recruitment and breeding of red grouse. Oecologia 67:493–498CrossRefGoogle Scholar
  43. Watson A, Jenkins D (1964) Notes on the behaviour of red grouse. Br Birds 57:137–170Google Scholar
  44. Watson A, Miller GR (1971) Territory size and aggression in a fluctuating red grouse population. J Anim Ecol 40:367–383CrossRefGoogle Scholar
  45. Watson A, Moss R, Parr R, Mountford MD, Rothery P (1994) Kin landownership, differential aggression between kin and non-kin, and population fluctuations in red grouse. J Anim Ecol 63:39–50CrossRefGoogle Scholar
  46. Wilson GR, Wilson LP (1978) Haematology, weight and condition of captive red grouse (Lagopus lagopus scoticus) infected with caecal threadworm (Trichostrongylus tenuis). Res Vet Sci 25:331–336PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Franccois Mougeot
    • 1
  • Sharon A. Evans
    • 1
  • Stephen M. Redpath
    • 1
  1. 1.Centre for Ecology and HydrologyBanchoryScotland, UK

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