Behavioral Ecology and Sociobiology

, Volume 70, Issue 2, pp 277–283 | Cite as

Parasites, mate attractiveness and female feather corticosterone levels in a socially monogamous bird

  • François Mougeot
  • Ádám Z. Lendvai
  • Jesús Martínez-Padilla
  • Lorenzo Pérez-Rodríguez
  • Mathieu Giraudeau
  • Fabián Casas
  • Ignacio T. Moore
  • Steve Redpath
Original Article


Stress is ubiquitous in the life of animals and a key determinant of their well-being and fitness. By quantifying levels of feather corticosterone in growing feathers (CORTf), we measured integrated stress responses in a monogamous game bird, the red grouse Lagopus lagopus scoticus. We investigated the effects of parasites and social mate choice on female CORTf levels during pairing, and tested the hypothesis that females with more parasites and paired with less attractive males have higher CORTf. We experimentally reduced nematode parasite abundance during pairing in females and investigated the effect of treatment on CORTf, while also considering the social mate’s phenotype (male comb size, as a proxy of sexual attractiveness). The treatment was effective at contrasting parasite loads between control and dosed females, but had no apparent effect on CORTf. In experimental females, reinfection rate after a month positively correlated with CORTf. We found no evidence of assortative mating based on size, condition or ornament size, but females paired with more attractive males (displaying bigger combs) had lower CORTf during pairing. Females for which parasite load was reduced had lower CORTf than control females at all levels of male attractiveness. Social mate choice therefore appears to be an important determinant of female integrated stress responses, which may in turn modulate reinfection rate and parasitism risk. An influence of male attractiveness on female stress may be part of an adaptive response allowing females to adjust reproductive investment to their achieved social mate choice.


Feather corticosterone Red grouse Lagopus lagopus scoticus Nematode Trichostrongylus tenuis Mate choice Sexual ornament 



We thank Pablo Vergara, Jessica Haines and Sonia Ludwig for help during fieldwork, and two anonymous referees for helping us to improve the manuscript.

Compliance with ethical standards


This work was funded by NERC (NE/D014352/1) and by NSF (IOS-1145625). FM was supported by a distinguish visitor award from the University of Cape Town (2015). LP-R was supported by a postdoctoral contract from MINECO (Severo Ochoa Programme; (SEV-2012-0262). FC and JM-P were supported by a JAE-Doc contract funded by CSIC and ESF. ÁZL was supported by an Eötvös Grant from the Hungarian Scholarship Board and an OTKA grant (K113108).

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

All procedures on animals were carried out under a UK Home Office license (PPL 60/3824)


  1. Alonso-Alvarez C, Perez-Rodriguez L, Ferrero E, García de Blas E, Casas F, Mougeot F (2012) Adjustment of female breeding investment according to male carotenoid-based ornamentation in a Gallinacean bird. Behav Ecol Sociobiol 66:731–742CrossRefGoogle Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  3. Bart J, Earnst SL (1999) Relative importance of male and territory quality in pairing success of male rock ptarmigan (Lagopus mutus). Behav Ecol Sociobiol 45:355–359CrossRefGoogle Scholar
  4. Bortolotti GR, Marchant TA, Blas J, German T (2008) Corticosterone in feathers is a long-term, integrated measure of avian stress physiology. Funct Ecol 22:494–500CrossRefGoogle Scholar
  5. Bortolotti GR, Marchant T, Blas J, Cabezas S (2009a) Tracking stress: localisation, deposition and stability of corticosterone in feathers. J Exp Biol 212:1477–1482PubMedCrossRefGoogle Scholar
  6. Bortolotti GR, Mougeot F, Martinez-Padilla J, Webster LMI, Piertney SB (2009b) Physiological stress mediates the honesty of social signals. PLoS ONE 4:e4983PubMedPubMedCentralCrossRefGoogle Scholar
  7. Carrete M, Bortolotti GR, Sanchez-Zapata JA, Delgado A, Cortes-Avizanda A, Grande JM, Donazar JA (2013) Stressful conditions experienced by endangered Egyptian vultures on African wintering areas. Anim Conserv 16:353–358CrossRefGoogle Scholar
  8. Fairhurst GD, Frey MD, Reichert JF, Szelest I, Kelly DM, Bortolotti GR (2011) Does environmental enrichment reduce stress? An integrated measure of corticosterone from feathers provides a novel perspective. PLoS ONE 6:e17663PubMedPubMedCentralCrossRefGoogle Scholar
  9. Fairhurst GD, Navarro J, Gonzalez-Solis J, Marchant TA, Bortolotti GR (2012) Feather corticosterone of a nestling seabird reveals consequences of sex-specific parental investment. Proc R Soc Lond B 279:177–184CrossRefGoogle Scholar
  10. Fairhurst GD, Dawson RD, van Oort H, Bortolotti GR (2014) Synchronizing feather-based measures of corticosterone and carotenoid-dependent signals: what relationships do we expect? Oecologia 174:689–698PubMedCrossRefGoogle Scholar
  11. Griffith SC, Pryke SR, Buttemer WA (2011) Constrained mate choice in social monogamy and the stress of having an unattractive partner. Proc R Soc Lond B 278:2798–2805CrossRefGoogle Scholar
  12. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds—a role for parasites. Science 218:384–387PubMedCrossRefGoogle Scholar
  13. Harriman VB, Dawson RD, Clark RG, Fairhurst GD, Bortolotti GR (2014) Effects of ectoparasites on seasonal variation in quality of nestling tree swallows (Tachycineta bicolor). Can J Zool 92:87–96CrossRefGoogle Scholar
  14. Hudson PJ (1986) The red grouse: the biology and management of a wild gamebird. The Game Conservancy Trust, FordingbridgeGoogle Scholar
  15. Jenni-Eiermann S, Helfenstein F, Vallat A, Glauser G, Jenni L (2015) Corticosterone: effects on feather quality and deposition into feathers. Meth Ecol Evol 6:237–246CrossRefGoogle Scholar
  16. Koren L, Nakagawa S, Burke T, Soma KK, Wynne-Edwards KE, Geffen E (2012) Non-breeding feather concentrations of testosterone, corticosterone and cortisol are associated with subsequent survival in wild house sparrows. Proc R Soc Lond B 279:1560–1566CrossRefGoogle Scholar
  17. Lattin CR, Reed JM, DesRochers DW, Romero LM (2011) Elevated corticosterone in feathers correlates with corticosterone-induced decreased feather quality: a validation study. J Avian Biol 42:247–252CrossRefGoogle Scholar
  18. Lendvai AZ, Giraudeau M, Nemeth J, Bako V, McGraw KJ (2013) Carotenoid-based plumage coloration reflects feather corticosterone levels in male house finches (Haemorhous mexicanus). Behav Ecol Sociobiol 67:1817–1824CrossRefGoogle Scholar
  19. Martinez-Padilla J, Vergara P, Perez-Rodriguez L, Mougeot F, Casas F, Ludwig SC, Haines JA, Zeineddine M, Redpath SM (2011) Condition- and parasite-dependent expression of a male-like trait in a female bird. Biol Lett 7:364–367PubMedPubMedCentralCrossRefGoogle Scholar
  20. Martinez-Padilla J, Vergara P, Mougeot F, Redpath SM (2012) Parasitized mates increase infection risk for partners. Am Nat 179:811–820PubMedCrossRefGoogle Scholar
  21. Martinez-Padilla J, Mougeot F, Garcia JT, Arroyo B, Bortolotti GR (2013) Feather corticosterone levels and carotenoid-based coloration in common buzzard (Buteo buteo) nestlings. J Raptor Res 47:161–173CrossRefGoogle Scholar
  22. Martinez-Padilla J, Redpath SM, Zeineddine M, Mougeot F (2014) Insights into population ecology from long-term studies of red grouse Lagopus lagopus scoticus. J Anim Ecol 83:85–98PubMedCrossRefGoogle Scholar
  23. Møller AP, Alatalo RV (1999) Good-genes effects in sexual selection. Proc R Soc Lond B 266:85–91CrossRefGoogle Scholar
  24. Mougeot F, Evans SA, Redpath SM (2005a) Interactions between population processes in a cyclic species: parasites reduce autumn territorial behaviour of male red grouse. Oecologia 144:289–298PubMedCrossRefGoogle Scholar
  25. Mougeot F, Redpath SM, Piertney SB, Hudson PJ (2005b) Separating behavioral and physiological mechanisms in testosterone-mediated trade-offs. Am Nat 166:158–168PubMedCrossRefGoogle Scholar
  26. Mougeot F, Redpath SM, Piertney SB (2006) Elevated spring testosterone increases parasite intensity in male red grouse. Behav Ecol 17:117–125CrossRefGoogle Scholar
  27. Mougeot F, Perez-Rodriguez L, Martinez-Padilla J, Leckie F, Redpath SM (2007) Parasites, testosterone and honest carotenoid-based signalling of health. Funct Ecol 21:886–898CrossRefGoogle Scholar
  28. Mougeot F, Martinez-Padilla J, Webster LMI, Blount JD, Perez-Rodriguez L, Piertney SB (2009) Honest sexual signalling mediated by parasite and testosterone effects on oxidative balance. Proc R Soc Lond B 276:1093–1100CrossRefGoogle Scholar
  29. Mougeot F, Martinez-Padilla J, Bortolotti GR, Webster LMI, Piertney SB (2010) Physiological stress links parasites to carotenoid-based colour signals. J Evol Biol 23:643–650PubMedCrossRefGoogle Scholar
  30. Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891CrossRefGoogle Scholar
  31. Pryke SR, Rollins LA, Buttemer WA, Griffith SC (2011) Maternal stress to partner quality is linked to adaptive offspring sex ratio adjustment. Behav Ecol 22:717–722CrossRefGoogle Scholar
  32. Redpath SM, Mougeot F, Leckie FM, Evans SA (2006) The effects of autumn testosterone on survival and productivity in red grouse, Lagopus lagopus scoticus. Anim Behav 71:1297–1305CrossRefGoogle Scholar
  33. Rintamaki PT, Hoglund J, Karvonen E, Alatalo RV, Bjorklund N, Lundberg A, Ratti O, Vouti J (2000) Combs and sexual selection in black grouse (Tetrao tetrix). Behav Ecol 11:465–471CrossRefGoogle Scholar
  34. Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255PubMedCrossRefGoogle Scholar
  35. Seivwright LJ, Redpath SM, 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 Helminth 78:69–76PubMedCrossRefGoogle Scholar
  36. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321PubMedCrossRefGoogle Scholar
  37. Sild E, Meitern R, Männiste M, Karu U, Hõrak P (2014) High feather corticosterone indicates better coccidian infection resistance in greenfinches. Gen Comp Endocrinol 204:203–210PubMedCrossRefGoogle Scholar
  38. von Schantz T, Wittzell H, Goransson G, Grahn M, Persson K (1996) MHC genotype and male ornamentation: Genetic evidence for the Hamilton-Zuk model. Proc R Soc Lond Lond B 263:265–271CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • François Mougeot
    • 1
    • 8
  • Ádám Z. Lendvai
    • 2
  • Jesús Martínez-Padilla
    • 3
  • Lorenzo Pérez-Rodríguez
    • 3
  • Mathieu Giraudeau
    • 4
  • Fabián Casas
    • 5
    • 6
  • Ignacio T. Moore
    • 2
  • Steve Redpath
    • 7
  1. 1.Instituto de Investigación en Recursos Cinegéticos IREC (CSIC-UCLM-JCCM)Ciudad RealSpain
  2. 2.Department of Biological SciencesVirginia TechBlacksburgUSA
  3. 3.Estación Biológica de Doñana (EBD-CSIC)SevilleSpain
  4. 4.School of Life sciencesArizona State UniversityPhoenixUSA
  5. 5.Department of BiologyUniversity of MarylandCollege ParkUSA
  6. 6.Estacion Experimental de Zonas AridasAlmeriaSpain
  7. 7.Institute of Biological and Environmental SciencesUniversity of AberdeenAberdeenUK
  8. 8.Percy FitzPatrick Institute of African OrnithologyUniversity of Cape TownCape TownSouth Africa

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