Behavioral Ecology and Sociobiology

, Volume 61, Issue 3, pp 423–433

Armaments and ornaments in the rock sparrow: a possible dual utility of a carotenoid-based feather signal

  • Matteo Griggio
  • Lorenzo Serra
  • Davide Licheri
  • Alessia Monti
  • Andrea Pilastro
Original Article

Abstract

Females often base their mating preferences on male sexual secondary traits that are used to settle contests among males. Such traits are likely to be honest indicators of male quality if they are constantly used during costly male–male agonistic interactions. Carotenoid signals have been shown to work as a handicap because they are costly to produce. However, the role of carotenoids as “honest” signals during male contests is less clear, and it is not known whether a carotenoid-based trait can serve in both male–male competition and female choice. In this study, we studied the dual function of a carotenoid feather ornament in the rock sparrow (Petronia petronia), a bird species in which both sexes have a yellow throat patch whose size positively correlates with phenotypic measures. First, we investigated, in a field study, whether the size of a male’s yellow patch correlates with his ability to acquire a territory. Second, we tested the signal function of the yellow patch in two male–male interaction in captivity experiments. Finally, we measured female preference for males differing in throat patch size in a mate choice experiment. Our experiments revealed that the size of a male’s throat patch positively correlated with the number of nest boxes he was able to defend. Moreover, in controlled conditions, males with relatively large yellow patches had earlier access to food than those with small patches. Also, in an experiment in which a dummy rock sparrow with an experimentally manipulated yellow patch was positioned near a feeder, latency to feed by focal birds positively correlated with dummy patch size. Lastly, in a dichotomous mate choice experiment, females showed a proximity preference for males whose patch was experimentally enlarged. Taken together, these results suggest that the same carotenoid feather signal may be used in both male–male competition and female choice in this passerine bird.

Keywords

Male–male competition Female choice Mutual selection Status signaling Condition-dependent traits 

References

  1. Alonso-Alvarez C, Doutrelant C, Sorci G (2004) Ultraviolet reflectance affects male–male interactions in the blue tit (Parus caeruleus ultramarinus). Behav Ecol 15:805–809CrossRefGoogle Scholar
  2. Amundsen T (2000) Why are female birds ornamented? Trends Ecol Evol 15:149–155PubMedCrossRefGoogle Scholar
  3. Andersson M (1994) Sexual selection. Princeton University Press, Princeton, New JerseyGoogle Scholar
  4. Andersson S, Ahlund M (1991) Hunger affects dominance among strangers in house sparrows. Anim Behav 41:895–897CrossRefGoogle Scholar
  5. Belthoff JR, Dufty AM, Gauthreaux SA (1994) Plumage variation, plasma steroids and social-dominance in male house finches. Condor 96:614–625Google Scholar
  6. Berglund A, Bisazza A, Pilastro A (1996) Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol J Linn Soc 58:385–399CrossRefGoogle Scholar
  7. Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127PubMedCrossRefGoogle Scholar
  8. Borgia G, Coleman SW (2000) Co-option of male courtship signals from aggressive display in bowerbirds. Proc R Soc Lond B 267:1735–1740CrossRefGoogle Scholar
  9. Bright A, Waas JR, King CM, Cuming PD (2004) Bill colour and correlates of male quality in blackbirds: an analysis using canonical ordination. Behav Processes 65:123–132PubMedCrossRefGoogle Scholar
  10. Brown MB, Brown CR (1988) Access to winter food resources by bright-versus dull-colored house finches. Condor 90:729–731Google Scholar
  11. Burley NT (1988) Wild zebra finches have band-color preferences. Anim Behav 36:1235–1237CrossRefGoogle Scholar
  12. Burley NT, Price DK, Zann RA (1992) Bill color, reproduction and condition effects in wild and domesticated zebra finches. Auk 109:12–23Google Scholar
  13. Candolin U (2000) Male–male competition ensures honest signaling of male parental ability in the three-spined stickleback (Gasterosteus aculeatus). Behav Ecol Sociobiol 49:57–61CrossRefGoogle Scholar
  14. Chew BP (1996) Importance of antioxidant vitamins in immunity and health in animals. Anim Feed Sci Technol 59:103–114CrossRefGoogle Scholar
  15. Cramp S, Perrins CM (1994) Handbook of the birds of the Western Palearctic. Oxford University Press, OxfordGoogle Scholar
  16. Etman EJ, Lelieveld HM, Ten Cate C (2001) Male bill colour and competition in zebra finches. Behav Processes 55:119–124PubMedCrossRefGoogle Scholar
  17. Evans MR, Norris K (1996) The importance of carotenoids in signaling during aggressive interactions between male firemouth cichlids (Cichlasoma meeki). Behav Ecol 7:1–6Google Scholar
  18. Faivre B, Gregoire A, Preault M, Cezilly F, Sorci G (2003) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103PubMedCrossRefGoogle Scholar
  19. Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546PubMedGoogle Scholar
  20. Gray DA (1996) Carotenoids and sexual dichromatism in North American passerine birds. Am Nat 148:453–480CrossRefGoogle Scholar
  21. Griffith SC, Parker TH, Olson VA (2006) Melanin- versus carotenoid-based sexual signals: is the difference really so black and red? Anim Behav 71:749–763CrossRefGoogle Scholar
  22. Griggio M, Matessi G, Pilastro A (2003a) Male rock sparrow (Petronia petronia) nest defence correlates with female ornament size. Ethology 109:659–669CrossRefGoogle Scholar
  23. Griggio M, Tavecchia G, Biddau L, Mingozzi T (2003b) Mating strategies in the rock sparrow Petronia petronia: the role of female quality. Ethol Ecol Evol 15:389–398CrossRefGoogle Scholar
  24. Griggio M, Valera F, Casas A, Pilastro A (2005) Males prefer ornamented females: a field experiment of male choice in the rock sparrow. Anim Behav 69:1243–1250CrossRefGoogle Scholar
  25. Hartley RC, Kennedy MW (2004) Are carotenoids a red herring in sexual display? Trends Ecol Evol 19:353–354PubMedCrossRefGoogle Scholar
  26. Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339CrossRefGoogle Scholar
  27. Hill GE (1994) Geographic-variation in male ornamentation and female mate preference in the house finch—a comparative test of models of sexual selection. Behav Ecol 5:64–73Google Scholar
  28. Hill GE (1999a) Is there an immunological cost to carotenoid-based ornamental coloration? Am Nat 154:589–595PubMedCrossRefGoogle Scholar
  29. Hill GE (1999b) Mate choice, male quality and carotenoid-based plumage coloration. In: Adams N, Slotow R (eds) Proceedings of the 22nd international ornithology congress. University of Natal, Durban, pp 1654–1668Google Scholar
  30. Hill GE, Farmer KL (2005) Carotenoid-based plumage coloration predicts resistance to a novel parasite in the house finch. Naturwissenschaften 92:30–34PubMedCrossRefGoogle Scholar
  31. Hill GE, Nolan PM, Stoehr AM (1999) Pairing success relative to male plumage redness and pigment symmetry in the house finch: temporal and geographic constancy. Behav Ecol 10:48–53CrossRefGoogle Scholar
  32. Holland B, Rice WR (1998) Perspective: chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52:1–7CrossRefGoogle Scholar
  33. Hudon J (1994) Showiness, carotenoids, and captivity—a comment on Hill (1992). Auk 111:218–221Google Scholar
  34. Jones IL, Hunter FM (1993) Mutual sexual selection in a monogamous seabird. Nature 362:238–239CrossRefGoogle Scholar
  35. Jones IL, Hunter FM (1999) Experimental evidence for mutual inter- and intrasexual selection favouring a crested auklet ornament. Anim Behav 57:521–528PubMedCrossRefGoogle Scholar
  36. Kodric-Brown A (1989) Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Behav Ecol Sociobiol 25:393–401CrossRefGoogle Scholar
  37. Leitao A, Riebel K (2003) Are good ornaments bad armaments? Male chaffinch perception of songs with varying flourish length. Anim Behav 66:161–167CrossRefGoogle Scholar
  38. Liker A, Székely T (1997) Aggression among female lapwings, Vanellus vanellus. Anim Behav 54:797–802PubMedCrossRefGoogle Scholar
  39. Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311CrossRefGoogle Scholar
  40. MacDougall AK, Montgomerie (2003) Assortative mating by carotenoid-based plumage colour: a quality indicator in American goldfinches, Carduelis tristis. Naturwissenschaften 90:464–467PubMedCrossRefGoogle Scholar
  41. Manly BFJ (1991) Randomization and Monte Carlo methods in biology. Chapman & Hall, LondonGoogle Scholar
  42. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  43. Mateos C, Carranza J (1999) Effects of male dominance and courtship display on female choice in the ring-necked pheasant. Behav Ecol Sociobiol 45:235–244CrossRefGoogle Scholar
  44. McGraw KJ, Hill GE (2000) Carotenoid-based ornamentation and status signaling in the house finch. Behav Ecol 11:520–527CrossRefGoogle Scholar
  45. Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N, Surai PF (2000) Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian Poult Biol Rev 11:137–159Google Scholar
  46. Navara KJ, Hill GE (2003) Dietary carotenoid pigments and immune function in a songbird with extensive carotenoid-based plumage coloration. Behav Ecol 14:909–916CrossRefGoogle Scholar
  47. Nicoletto PF (1995) Offspring quality and female choice in the guppy, Poecilia reticulata. Anim Behav 49:377–387CrossRefGoogle Scholar
  48. Norušis MJ (1993) SPSS for Windows Base System User’s Guide Release 6.0. SPSS, ChicagoGoogle Scholar
  49. Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514CrossRefGoogle Scholar
  50. Olson VA, Owens IPF (2005) Interspecific variation in the use of carotenoid-based coloration in birds: diet, life history and phylogeny. J Evol Biol 18:1534–1546PubMedCrossRefGoogle Scholar
  51. Payne RW, Arnold GM (2003) GenStat® Release 7.1 Reference Manual. VSN International, OxfordGoogle Scholar
  52. Peters A, Denk AG, Delhey K, Kempenaers B (2004) Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards. J Evol Biol 17:1111–1120PubMedCrossRefGoogle Scholar
  53. Pilastro A, Biddau L, Marin G, Mingozzi T (2001) Female brood desertion increases with the number of available mates in the Rock Sparrow. J Avian Biol 32:68–72CrossRefGoogle Scholar
  54. Pilastro A, Griggio M, Biddau L, Mingozzi T (2002) Extrapair paternity as a cost of polygyny in the rock sparrow: behavioural and genetic evidence of the ‘trade-off’ hypothesis. Anim Behav 63:967–974CrossRefGoogle Scholar
  55. Pilastro A, Griggio M, Matessi G (2003) Male rock sparrows adjust their breeding strategy according to female ornamentation: parental or mating investment? Anim Behav 66:265–271CrossRefGoogle Scholar
  56. Preault M, Deregnaucourt S, Sorci G, Faivre B (2002) Does beak coloration of male blackbirds play a role in intra and/or intersexual selection? Behav Processes 58:91–96PubMedCrossRefGoogle Scholar
  57. Pryke SR, Andersson S (2003a) Carotenoid-based epaulettes reveal male competitive ability: experiments with resident and floater red-shouldered widowbirds. Anim Behav 66:217–224CrossRefGoogle Scholar
  58. Pryke SR, Andersson S (2003b) Carotenoid-based status signalling in red-shouldered widowbirds (Euplectes axillaris): epaulet size and redness affect captive and territorial competition. Behav Ecol Sociobiol 53:393–401Google Scholar
  59. Pryke SR, Andersson S, Lawes MJ (2001a) Sexual selection of multiple handicaps in the red-collared widowbird: female choice of tail length but not carotenoid display. Evolution 55:1452–1463PubMedCrossRefGoogle Scholar
  60. Pryke SR, Lawes MJ, Andersson S (2001b) Agonistic carotenoid signalling in male red-collared widowbirds: aggression related to the colour signal of both the territory owner and model intruder. Anim Behav 62:695–704CrossRefGoogle Scholar
  61. Senar JC, Camerino M (1998) Status signalling and the ability to recognize dominants: an experiment with siskins (Carduelis spinus). Proc R Soc Lond B 265:1515–1520CrossRefGoogle Scholar
  62. Senar JC, Escobar D (2002) Carotenoid-derived plumage coloration in the siskin Carduelis spinus is related to foraging ability. Avian Sci 2:19–24Google Scholar
  63. Senar JC, Domenech J, Camerino M (2005) Female siskins choose mates by the size of the yellow wing stripe. Behav Ecol Sociobiol 57:465–469CrossRefGoogle Scholar
  64. Sokal RR, Rohlf FJ (1995) Biometrics. Freeman, San Francisco, CAGoogle Scholar
  65. Svensson L (1992) Identification guide to European passerines, 4th edn. British Trust for Ornithology, ThetfordGoogle Scholar
  66. Tarof SA, Dunn PO, Whittingham LA (2005) Dual functions of a melanin-based ornament in the common yellowthroat. Proc R Soc Lond B Biol Sci 272:1121–1127CrossRefGoogle Scholar
  67. von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proc R Soc Lond B 266:1–12CrossRefGoogle Scholar
  68. Wedekind C, Meyer P, Frischknecht M, Niggli UA, Pfander H (1998) Different carotenoids and potential information content of red coloration of male three-spined stickleback. J Chem Ecol 24:787–801CrossRefGoogle Scholar
  69. Wong BBM, Candolin U (2005) How is female mate choice affected by male competition? Biol Rev 80:559–571PubMedCrossRefGoogle Scholar
  70. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Matteo Griggio
    • 1
  • Lorenzo Serra
    • 2
  • Davide Licheri
    • 2
  • Alessia Monti
    • 2
  • Andrea Pilastro
    • 1
  1. 1.Dipartimento di BiologiaUniversità di PadovaPadovaItaly
  2. 2.Istituto Nazionale per la Fauna SelvaticaOzzano dell’Emilia BOItaly

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