Oecologia

, Volume 149, Issue 3, pp 535–542

Pigment-based skin colour in the blue-footed booby: an honest signal of current condition used by females to adjust reproductive investment

  • Alberto Velando
  • René Beamonte-Barrientos
  • Roxana Torres
Behavioural Ecology

Abstract

In monogamous species, the value of present reproduction is affected by the current condition of the mate, and females may use male ornaments to evaluate his condition and adjust their level of investment according. Many animals display colour in fleshy structures which may be accurate indicators of quality due to their potentially rapid response to changes in condition. Here we show that in the blue-footed booby, Sula nebouxii, male foot colour is structurally (collagen arrays) and pigment based. In 48 h foot colour became duller when males were food deprived and brighter when they were re-fed with fresh fish. Variation of dietary carotenoids induced comparable changes in cell-mediated immune function and foot colour, suggesting that carotenoid-pigmentation reveals the immunological state of individuals. These results suggest that pigment-based foot colour is a rapid honest signal of current condition. In a second experiment, we found that rapid variation in male foot colour caused parallel variation in female reproductive investment. One day after the first egg was laid we captured the males and modified the foot colour of experimental males with a non-toxic and water resistant duller blue intensive make-up, mimicking males in low condition. Females decreased the size of their second eggs, relative to the second egg of control females, when the feet of their mates were experimentally duller. Since brood reduction in this species is related to size differences between brood mates at hatching, by laying lighter second eggs females are facilitating brood reduction. Our data indicate that blue-footed booby females are continuously evaluating their mates and can perform rapid adjustments of reproductive investment by using dynamic sexual traits. We suggest that this fine-tuned adjustment may be widespread in socially monogamous animals.

Keywords

Dynamic trait Differential allocation Sexual signal Carotenoids Brood reduction 

References

  1. Adams NJ, Abrams WR, Siegfried R, Nagy KA, Kaplan IR (1991) Energy expenditure and food consumption by breeding Cape Gannets (Morus capensis). Mar Ecol Prog Ser 70:1–9CrossRefGoogle Scholar
  2. Alonso-Alvarez C, Bertrand S, Devevey G, Gaillard M, Prost J, Faivre B, Sorci G (2004) An experimental test of the dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. Am Nat 164:651–659PubMedCrossRefGoogle Scholar
  3. Andersson M (1994) Sexual Selection. Princeton University Press, New YorkGoogle Scholar
  4. Auber L (1957) The distribution of structural colors and unusual pigments in the Class Aves. Ibis 99:463–476CrossRefGoogle Scholar
  5. 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
  6. Burley N (1986) Sexual selection for aesthetic traits in species with biparental care. Am Nat 127:415–445CrossRefGoogle Scholar
  7. Clifford L, Anderson DJ (2001) Food limitation explains most clutch size variation in the Nazca booby. J Anim Ecol 70:539–545CrossRefGoogle Scholar
  8. Cunningham EJA, Russell A (2000) Egg investment is influenced by male attractiveness in the mallard. Nature 404:74–77PubMedCrossRefGoogle Scholar
  9. D’Alba L (2000) Efecto de la asignación de recursos de huevos sobre la sobrevivencia de crías de diferente sexo y orden de puesta en el bobo de patas azules (Sula nebouxii). Bachelor Thesis, Universidad Nacional Autónoma de MéxicoGoogle Scholar
  10. David P, Bjorsksten T, Fowler K, Pomiankowski A (2000) Condition-dependent signalling of genetic variation in stalk-eyed flies. Nature 406:186–188PubMedCrossRefGoogle Scholar
  11. Drummond H, González E, Osorno JL (1986) Parent-offspring cooperation in the blue-footed booby (Sula nebouxii): social roles in infanticidal brood reduction. Behav Ecol Sociobiol 19:365–372CrossRefGoogle Scholar
  12. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: A role for parasites? Science 218:384–387PubMedCrossRefGoogle Scholar
  13. Hill GE (2002) A red bird in a brown bag: the function and evolution of colorful plumage coloration in the house finch. Oxford University Press, NewYorkGoogle Scholar
  14. Faivre B, Gregoire A, Preault M, Cezilly F, Sorci G (2003) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:29–31CrossRefGoogle Scholar
  15. Finkler MS, Van Orman JB, Sotherland PR (1998) Experimental manipulation of egg quality in chickens: influence of albumen and yolk on the size and body composition of near-term embryos in a precocial bird. J Comp Physiol B 168:17–24PubMedCrossRefGoogle Scholar
  16. Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128PubMedCrossRefGoogle Scholar
  17. Grattagliano I, Vendemiale G, Caraceni P, Domenicali M, Nardo B, Cavallari A, Trevisani F, Bernardi M, Altomare E (2000) Starvation impairs antioxidant defense in fatty livers of rats fed a choline-deficient diet. J Nutr 130:2131–2136PubMedGoogle Scholar
  18. Grether GF, Kasahara S, Kolluru GR, Cooper EL (2004) Sex-specific effects of carotenoid intake on the immunological response to allografts in guppies (Poecilia reticulata). Proc R Soc Lond B 271:45–49CrossRefGoogle Scholar
  19. Klasing KC (1998) Comparative avian nutrition. CABI PublishingGoogle Scholar
  20. de Lope F, Møller AP (1993) Female reproductive effort depends on the degree of ornamentation of their mates. Evolution 47:1152–1160CrossRefGoogle Scholar
  21. Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311CrossRefGoogle Scholar
  22. Limbourg T, Mateman AC, Andersson S, Lessells CM (2004) Female blue tits adjust parental effort to manipulated male UV attractiveness. Proc R Soc Lond B 271:1903–1908CrossRefGoogle Scholar
  23. Martensson J (1986) The effect of fasting on leukocyte and plasma glutathione and sulfur amino acid concentrations. Metabolism 35:118–121PubMedCrossRefGoogle Scholar
  24. McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712PubMedCrossRefGoogle Scholar
  25. McGraw KJ, Hudon J, Hill GE, Parker RS (2005a) A simple and inexpensive chemical test for behavioral ecologists to determine the presence of carotenoid pigments in animal tissues. Behav Ecol Sociobiol 57:391–397CrossRefGoogle Scholar
  26. McGraw KJ, Hill GE, Parker RS (2005b) The physiological costs of being colourful: nutritional control of carotenoid utilization in the American goldfinch, Carduelis tristis. Anim Behav 69:653–660CrossRefGoogle Scholar
  27. Nelson B (1978) The Sulidae: gannets and boobies. Oxford University Press, OxfordGoogle Scholar
  28. Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514CrossRefGoogle Scholar
  29. Osorio-Beristain M, Drummond H (1998) Non-aggressive mate guarding by the blue-footed booby: a balance of female and male control. Behav Ecol Sociobiol 43:307–315CrossRefGoogle Scholar
  30. Peters A, Delhey K, Denk AG, Kempenaers B (2004) Trade-offs between immune investment and sexual signaling in male mallards. Am Nat 164:51–59PubMedCrossRefGoogle Scholar
  31. Prum RO, Torres R (2003) Structural coloration of avian skin: convergent evolution or coherently scattering dermal colagen arrays. J Exp Biol 206:2409–2429PubMedCrossRefGoogle Scholar
  32. Reed JR (1987) Scotopic and photopic spectral sensitivities of boobies. Ethology 76:33–55CrossRefGoogle Scholar
  33. Safran RJ, Neuman CR, McGraw KJ, Lovette IJ (2005) Dynamic paternity allocation as a function of male plumage color in barn swallows. Science 309:2210–2212PubMedCrossRefGoogle Scholar
  34. Sheldon BC (2000) Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 15:397–402PubMedCrossRefGoogle Scholar
  35. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohemagglutinin skin testing technique in studies of avian immunocompetence. Funct Ecol 13:567–577CrossRefGoogle Scholar
  36. Solomon NW, Bulux J (1993) Effects of nutritional status on carotene uptake and bioconversion. Ann NY Acad Sci 691:96–109CrossRefGoogle Scholar
  37. Stearns SC (1992) The Evolution of Life Histories. Oxford University Press, OxfordGoogle Scholar
  38. Svensson E, Sheldon BC (1998) The social context of life history evolution. Oikos 83:466–477CrossRefGoogle Scholar
  39. Torres R, Velando A (2003) A dynamic trait affects continuous pair assessment in the blue-footed booby, Sula nebouxii. Behav Ecol Sociobiol 55:65–72CrossRefGoogle Scholar
  40. Torres R, Velando A (2005) Male preference for female foot colour in the socially monogamous blue-footed booby, Sula nebouxii. Anim Behav 69:59–65CrossRefGoogle Scholar
  41. Velando A, Alonso-Alvarez C (2003) Differential body condition regulation by males and females in response to experimental manipulations of brood size and parental effort in the Blue-footed Booby. J Anim Ecol 72:846–856CrossRefGoogle Scholar
  42. Velando A, Torres R, Espinosa I (2005) Male coloration and chick condition in blue-footed booby: a cross-fostering experiment. Behav Ecol Sociobiol 58:175–180CrossRefGoogle Scholar
  43. Williams TD (1994) Intra-specific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev 68:35–59CrossRefGoogle Scholar
  44. Winkler DW (1987) A general model for parental care. Am Nat 130:526–543CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Alberto Velando
    • 1
  • René Beamonte-Barrientos
    • 2
  • Roxana Torres
    • 2
  1. 1.Departamento de Ecoloxía e Bioloxía Animal, Campus Lagoas-MarcosendeUniversidade de VigoVigoSpain
  2. 2.Departamento de Ecología Evolutiva, Instituto de EcologíaUniversidad Nacional Autónoma de MéxicoMexicoMexico

Personalised recommendations