Behavioral Ecology and Sociobiology

, Volume 62, Issue 12, pp 1899–1908 | Cite as

Maternal investment in eggs is affected by male feet colour and breeding conditions in the blue-footed booby, Sula nebouxii

  • Fabrice Dentressangle
  • Lourdes Boeck
  • Roxana TorresEmail author
Original Paper


Females are expected to vary investment in offspring according to variables that may influence the offspring fitness in a way that optimises her inclusive fitness for a particular context. Thus, when sexual ornaments signal the quality of the male, females might invest in reproduction as a function of the attractiveness of their mate. We tested whether breeding conditions and male feet colour influence reproductive decisions of blue-footed booby females. In the blue-footed booby, male feet colour is a dynamic condition-dependent sexually selected trait that is related to paternal effort. During two consecutive years, an El Niño year (poor breeding conditions) and a year with good breeding conditions, we experimentally reduced male attractiveness by modifying their feet colour after the first egg was laid and recorded female investment in the second egg. We found that, relative to the first egg in the clutch, females laid heavier second eggs during the poor year than during the good year. Females paired with males with duller feet colour reduced second-egg mass and volume and delayed the laying of the second egg, independently of the year. Absolute yolk androstenedione (A4) concentration (but not testosterone, T) in second eggs was higher during a poor year than during a good year. Only during a year with poor breeding conditions, females paired with experimental males decreased the relative A4 concentration (but not T) in the second egg compared to control females. Thus, blue-footed booby females probably favour brood reduction by decreasing egg quality and increasing size asymmetry between chicks when the breeding and the mate conditions are poor.


Sexual traits Egg quality Laying asynchrony Yolk androgens Sula nebouxii Maternal effects 



We are grateful to M. Cerbón, A. Córdoba, H. Drummond, D. Gil, A. Velando, K. Renton, two anonymous Referees and J. Graves for helpful comments and discussion during the study, to E. Villaseñor, D. Gonzalez and A. Nava Sánches for their great help during field work and to the Laboratorio de Hormonas Esteroides del Instituto Nacional de Ciencias de la Salud y de Nutrición for logistic support for the androgen determination. The project was supported by the Universidad Nacional Autónoma de México (UNAM, PAPIIT IN211406) and CONACYT (47599). Logistic support was provided by the Armada de México, the staff from the Parque Nacional Isla Isabel and the fisherman from San Blas, Nayarit. The experiments comply with the current laws of Mexico; permissions were granted by SEMARNAT and the Parque Nacional Isla Isabel. During the study, F. Dentressangle was supported by a scholarship for graduate studies from UNAM.


  1. Burley N (1986) Sexual selection for aesthetic traits in species with biparental care. Am Nat 127(4):415–445CrossRefGoogle Scholar
  2. Burley N (1988) The differential allocation hypothesis: an experimental test. Am Nat 132(5):611–628CrossRefGoogle Scholar
  3. Cariello MO, Macedo RHF, Schwabl HG (2006) Maternal androgens in eggs of communally breeding guira cuckoos (Guira guira). Horm Behav 49:654–662PubMedCrossRefGoogle Scholar
  4. Christians JK (2002) Avian egg size: variation within species and inflexibility within individuals. Biol Rev 77:1–26PubMedGoogle Scholar
  5. Cunningham EJA, Russell AF (2000) Egg investment is influenced by male attractiveness in the mallard. Nature 404:74–76PubMedCrossRefGoogle Scholar
  6. D’Alba L, Torres R (2007) Seasonal egg mass variation and laying sequence in a bird with facultative brood reduction. Auk 124:643–652CrossRefGoogle Scholar
  7. Drummond H (2006) Dominance in vertebrate broods and litters. Q Rev Biol 81:3–32PubMedCrossRefGoogle Scholar
  8. Drummond H, Gonzalez E, Osorno JL (1986) Parent–offspring cooperation in the blue-footed booby (Sula nebouxii). Behav Ecol Sociobiol 19:365–372CrossRefGoogle Scholar
  9. Drummond H, Osorno JL, Torres R, Garcia Chavelas C, Merchant Larios H (1991) Sexual size dimorphism and sibling competition: implications for avian sex. Am Nat 138(3):623–641CrossRefGoogle Scholar
  10. Drummond H, Rodriguez C, Schwabl H (2008) Do mothers regulate facultative and obligate siblicide by differentially provisioning eggs with hormones? J Avian Biol 39:139–143CrossRefGoogle Scholar
  11. Eising C, Groothuis T (2003) Yolk androgens and begging behaviour in black-headed gull chicks: an experimental field study. Anim Behav 66(6):1027–1034CrossRefGoogle Scholar
  12. Eising CM, Eikenaar C, Schwabl H, Groothuis TGG (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc Lond B 268:839–846CrossRefGoogle Scholar
  13. Gasparini J, Boulinier T, Gill VA, Gil D, Hatch SA, Roulin A (2007) Food availability affects the maternal transfer of androgens and antibodies into eggs of a colonial bird seabird. J Evol Biol 20(3):874–880PubMedCrossRefGoogle Scholar
  14. Gil D (2003) Golden eggs: maternal manipulation of offspring phenotype by egg androgen in birds. Ardeola 50(2):281–294Google Scholar
  15. Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128PubMedCrossRefGoogle Scholar
  16. Gil D, Heim C, Bulmer E, Rocha M, Puerta M, Naguib M (2004a) Negative effects of early developmental stress on yolk testosterone levels in a passerine bird. J Exp Biol 207:2215–2220PubMedCrossRefGoogle Scholar
  17. Gil D, Leboucher G, Lacroix A, Cue R, Kreutzer M (2004b) Female canaries produce eggs with greater amounts of testosterone when exposed to preferred male song. Horm Behav 45:64–70PubMedCrossRefGoogle Scholar
  18. Gil D, Biard C, Lacroix A, Spottiswoode CN, Saino N, Puerta M, Møller AP (2007) Evolution of yolk androgens in birds: development, coloniality, and sexual dichromatism. Am Nat 169:802–819PubMedCrossRefGoogle Scholar
  19. Groothuis TGG, Müller W, von Engelhardt N, Carere C, Eising C (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neuro Biobehav Rev 29:329–352CrossRefGoogle Scholar
  20. Hoyt DF (1979) Practical methods for estimating volume and fresh weight of bird eggs. Auk 96:73–77Google Scholar
  21. Lack D (1954) The natural regulation of animal numbers. Oxford University Press, OxfordGoogle Scholar
  22. Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, CaryGoogle Scholar
  23. Loyau A, Saint Jalme M, Mauget R, Sorci G (2007) Male sexual attractiveness affects the investment of maternal resources into the eggs in peafowl (Pavo cristatus). Behav Ecol Sociobiol 61:1043–1052CrossRefGoogle Scholar
  24. Marshall RC, Leisler B, Catchpole CK, Schwabl H (2005) Male song quality affects circulating but not yolk steroid concentrations in female canaries (Serinus canaria). J Exp Biol 208:4593–4598PubMedCrossRefGoogle Scholar
  25. Mazuc J, Bonneaud C, Chastel O, Sorci G (2003) Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus). Ecol Lett 6:1084–1090CrossRefGoogle Scholar
  26. Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, OxfordGoogle Scholar
  27. Mousseau TA, Fox CW (1998a) The adaptive significance of maternal effects. TREE 13(10):403–407Google Scholar
  28. Mousseau TA, Fox CW (1998b) Maternal effects as adaptations. Oxford University Press, OxfordGoogle Scholar
  29. Müller W, Dijkstra C, Groothuis TGG (2003) Inter-sexual differences in T-cell-mediated immunity of black-headed gull chicks (Larus ridibundus) depend on the hatching order. Behav Ecol Sociobiol 55:80–86CrossRefGoogle Scholar
  30. Müller W, Groothuis TGG, Dijkstra C, Siitari H, Alatalo RV (2004) Maternal antibody transmission and breeding densities in the black-headed gull, Larus ridibundus. Funct Ecol 18:719–724CrossRefGoogle Scholar
  31. Müller W, Groothuis TGG, Kasprzik A, Dijkstra C, Alatalo RV, Siitari H (2005) Prenatal androgen exposure modulates cellular and humoral immune function of black headed gull chicks. Proc R Soc Lond B 272:1971–1977CrossRefGoogle Scholar
  32. Navara KJ, Hill GE, Mendonça MT (2005) Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiol Biochem Zool 78:570–578PubMedCrossRefGoogle Scholar
  33. Navara KJ, Hill GE, Mendonça MT (2006) Yolk testosterone stimulates growth and immunity in house finch chicks. Physiol Biochem Zool 79(3):550–555PubMedCrossRefGoogle Scholar
  34. Osorno JL, Drummond H (1995) The function of hatching asynchrony in the blue-footed booby. Behav Ecol Sociobiol 37:265–273CrossRefGoogle Scholar
  35. Rubolini D, Romano M, Martinelli R, Saino N (2006) Effects of elevated yolk testosterone levels on survival, growth and immunity of male and female yellow-legged gull chicks. Behav Ecol Sociobiol 59(3):344–352CrossRefGoogle Scholar
  36. Rutstein AN, Gilbert L, Slater PJB, Graves JA (2004) Mate attractiveness and primary resource allocation in the zebra finch. Anim Behav 68(5):1087–1094CrossRefGoogle Scholar
  37. Saino N, Ferrari RP, Martinelli R, Romano M, Rubolini D, Møller AP (2002a) Early maternal effects mediated by immunity depend on sexual ornamentation of the male partner. Proc R Soc Lond B 269:1005–1009CrossRefGoogle Scholar
  38. Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, Stradi R (2002b) Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proc R Soc Lond B 269:1729–1733CrossRefGoogle Scholar
  39. Saino N, Romano M, Ferrari RP, Martinelli R, Møller AP (2003) Maternal antibodies but not carotenoids in barn swallow eggs covary with embryo sex. J Evol Biol 16:516–522PubMedCrossRefGoogle Scholar
  40. Sandell MI, Adkins-Regan E, Ketterson ED (2007) Pre-breeding diet affects the allocation of yolk hormones in zebra finches Taeniopygia guttata. J Avian Biol 38:284–290Google Scholar
  41. Schwabl H (1993) Yolk is source of testosterone for developing birds. Proc Natl Acad Sci USA 90:11446–11450PubMedCrossRefGoogle Scholar
  42. Schwabl H (1996) Maternal testosterone in the avian egg enhances post natal growth. Comp Biochem Physiol 114A:271–276CrossRefGoogle Scholar
  43. Schwabl H (1997) A hormonal mechanism for parental favouritism. Nature 386:231CrossRefGoogle Scholar
  44. Sheldon B (2000) Differential allocation: tests, mechanism and implications. Trends Ecol Evol 15(10):397–402PubMedCrossRefGoogle Scholar
  45. Sockman KW, Schwabl H (2000) Yolk androgens reduce offspring survival. Proc R Soc Lond B 267:1451–1456CrossRefGoogle Scholar
  46. Sockman KW, Sharp PJ, Schwabl H (2006) Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases for flexibility in clutch size, incubation behaviour, and yolk androgen deposition. Biol Rev 81:629–666PubMedCrossRefGoogle Scholar
  47. Tanvez A, Beguin N, Chastel O, Lacroix A, Leboucher G (2004) Sexually attractive phrases increase yolk androgen deposition in canaries, (Serinus canaria). Gen Comp Endocrinol 138:113–120PubMedCrossRefGoogle Scholar
  48. Tobler M, Nilsson JA, Nilsson JF (2007) Costly steroids: egg testosterone modulates nestling metabolic rate in the zebra finch. Biol Lett 3:408–410, doi: 10.1098/rsbl.2007.0127 PubMedCrossRefGoogle Scholar
  49. Torres R, Drummond H (1999) Does large size make daughters of the blue-footed booby more expensive than sons? J Anim Ecol 68:1–10CrossRefGoogle Scholar
  50. 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
  51. Uller T, Eklöf J, Andersson S (2005) Female egg investment in relation to male sexual traits and the potential for transgenerational effects in sexual selection. Behav Ecol Sociobiol 57:584–590CrossRefGoogle Scholar
  52. 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
  53. 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
  54. Velando A, Beamonte-Barrientos R, Torres R (2006) Pigment-based skin colour in the blue-footed booby: an honest signal of current condition used by females to adjust reproductive investment. Oecologia 149(3):535–542PubMedCrossRefGoogle Scholar
  55. Verboven N, Monaghan P, Evans DM, Schwabl H, Evans N, Whitelaw C, Nager RG (2003) Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the lesser black-backed gull (Larus fuscus). Proc R Soc Lond B 270:2223–2232CrossRefGoogle Scholar
  56. Von Engelhardt N, Carere C, Dijkstra C, Groothuis TGG (2006) Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches. Proc R Soc Lond B 273:65–70CrossRefGoogle Scholar
  57. Wagner E, Williams T (2007) Experimental (antiestrogen-mediated) reduction in egg size negatively affects offspring growth and survival. Physiol Biochem Zool 80(3):293–305PubMedCrossRefGoogle Scholar
  58. Wiebe KL, Bortolotti GR (1995) Food dependent benefits of hatching asynchrony in American kestrels Falco sparverius. Behav Ecol Sociobiol 36:49–57CrossRefGoogle Scholar
  59. Wiebe KL, Korpimäki E, Wiehn J (1998) Hatching asynchrony in Eurasian kestrels in relation to the abundance and predictability of cyclic prey. J Anim Ecol 67:908–917CrossRefGoogle Scholar
  60. Williams TD (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev Camb Philos Soc 69(1):35–59PubMedCrossRefGoogle Scholar
  61. Williamson KA, Surai PF, Graves JA (2006) Yolk antioxidants and mate attractiveness in the zebra finch. Funct Ecol 20(2):354–359CrossRefGoogle Scholar
  62. Wingfield JC, Farner DS (1975) The determination of five steroids in avian plasma by radioimmunoassay and competitive protein-binding. Steroids 26:311–327PubMedCrossRefGoogle Scholar
  63. Wingfield JC, Ramos-Fernández G, Nuñez de la Mora A, Drummond H (1999) The effect of an “El Niño” event on reproduction in male and female blue-footed boobies, Sula nebouxii. Gen Comp Endocrinol 114:163–172PubMedCrossRefGoogle Scholar
  64. Yao G, Shang XJ (2005) A comparison of proliferation of thymocyte by testosterone, dehydroisoandrosterone and androstenedione in vitro. Arch Androl 51:257–265PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Fabrice Dentressangle
    • 1
  • Lourdes Boeck
    • 2
  • Roxana Torres
    • 1
    Email author
  1. 1.Instituto de Ecología, Departamento de Ecología Evolutiva, Laboratorio de Conducta AnimalUniversidad Nacional Autónoma de MéxicoMéxicoMéxico
  2. 2.Laboratorio de Hormonas Esteroides, Biología de la ReproducciónInstituto Nacional de Ciencias Médicas y de la Nutrición, Salvador ZubiránMéxicoMéxico

Personalised recommendations