Behavioral Ecology and Sociobiology

, Volume 66, Issue 1, pp 135–143 | Cite as

Safe betting: males help dull females only when they raise high-quality offspring

Original Paper


In evolutionary biology, whether parents should enhance or reduce parental care according to mate ornamentation is a subject of great debate. However, the evolution of female ornaments can shed light on this question. In theory, female ornamentation should be traded off against fecundity and thus cannot be wholly informative to males without a direct indication of fecundity. Hence, direct cues of offspring quality should affect the relationship between male investment and female ornamentation. Under this hypothesis, we manipulated two direct cues of offspring quality (egg size and color) after first egg laying in the blue-footed booby and registered male incubation patterns. In this species, foot color is a dynamic signal of current condition and in females is traded off with egg size. We found that males spent more time incubating when paired with dull females but only in nests with large eggs. Males also spent less time incubating small dull eggs. Results indicate that egg size, a direct cue of reproductive value, affected the relationship between male effort and female ornamentation. Males may be willing to help females that have invested in offspring at the expense of ornamentation, which suggests compensation when females are in low condition. Another possibility is that males relax their effort when paired with highly ornamented and fecund females because they have high parenting abilities. Our findings suggest that the information conveyed by female ornaments may depend on direct cues of fecundity. Results also highlight that parental decisions are complex, modulated by a combination of information sources.


Differential allocation Eggshell color Information exchange Life history tradeoffs Parental care Reproductive compensation Reproductive value Sula nebouxii 



We are grateful to four anonymous reviewers for valuable and constructive comments. We thank René Beamonte-Barrientos, Natalia Lifshitz, and Alejandro Mendez for help in the field. We thank the fisherman from San Blas and Camichín, the staff from Parque Nacional Isla Isabel, and the Armada de México for logistic support. SEMARNAT gave working permissions and approved the research. This work was supported by the Universidad Nacional Autónoma de México (PAPIIT IN211406, IN228309), Consejo Nacional de Ciencia y Tecnología (47599, 81823) of México, Ministerio de Ciencia e Innovación (CGL2006-10357-C02-01/CGL2009-10883-C02-01 and Juan de la Cierva fellowship to JM) of Spain, and a research grant (2007) from the Association for the Study of Animal Behaviour to JM.


  1. Ancona S, Sánchez-Colón S, Rodríguez C, Drummond H (2011) El niño in the warm tropics: local sea temperature predicts breeding parameters and growth of blue-footed boobies. J Anim Ecol 80:799–808PubMedCrossRefGoogle Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  3. Barta Z, Houston AI, McNamara JM, Székely T (2002) Sexual conflict about parental care: the role of reverses. Am Nat 159:687–705PubMedCrossRefGoogle Scholar
  4. Bolund E, Schielzeth H, Forstmeier W (2009) Compensatory investment in zebra finches: females lay larger eggs when paired to sexually unattractive males. Proc R Soc Lond B 276:707–715CrossRefGoogle Scholar
  5. Braga-Goncalves I, Mobley KB, Ahnesjö I, Sagebakken G, Jones AG, Kvarnemo C (2010) Reproductive compensation in broad-nose pipefish females. Proc R Soc Lond B 277:1581–1587CrossRefGoogle Scholar
  6. Burley N (1986) Sexual selection for aesthetic traits in species with biparental care. Am Nat 127:415–445CrossRefGoogle Scholar
  7. Burley N (1988) The differential allocation hypothesis: an experimental test. Am Nat 132:611–628CrossRefGoogle Scholar
  8. Byers JA, Waits L (2006) Good genes sexual selection in nature. Proc Natl Acad Sci U S A 103:16343–16345PubMedCrossRefGoogle Scholar
  9. Chenoweth SF, Doughty P, Kokko H (2006) Can non-directional male mating preferences facilitate honest female ornamentation? Ecol Lett 9:179–184PubMedCrossRefGoogle Scholar
  10. Cunningham EJA, Russell AF (2000) Egg investment is influenced by male attractiveness in the mallard. Nature 404:74–77PubMedCrossRefGoogle Scholar
  11. 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
  12. Davis JN, Todd PM, Bullock S (1999) Environmental quality predicts parental provisioning decisions. Proc R Soc Lond B 266:1791–1797CrossRefGoogle Scholar
  13. Dentressangle F, Boeck L, Torres R (2008) Maternal investment in eggs is affected by male feet colour and breeding conditions in the blue-footed booby, Sula nebouxii. Behav Ecol Sociobiol 62:1899–1908CrossRefGoogle Scholar
  14. Fitzpatrick S, Berglund A, Rosenqvist G (1995) Ornaments or offspring: costs to reproductive success restrict sexual selection processes. Biol J Linn Soc 55:251–260CrossRefGoogle Scholar
  15. Folstad I, Carter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622CrossRefGoogle Scholar
  16. Fox J (1997) Applied regression analysis, linear models, and related methods. Sage, Thousand OaksGoogle Scholar
  17. García-Peña GE (2005) Efectos y costos de la termorregulación durante la incubación del ave marina Sula nebouxii. Mater thesis, Universidad Autónoma Nacional de México, MéxicoGoogle Scholar
  18. Gowaty PA (2008) Reproductive compensation. J Evol Biol 21:1189–1200PubMedCrossRefGoogle Scholar
  19. Gowaty PA, Anderson WW, Bluhm CK, Drickamer LC, Kim YK, Moore AJ (2007) The hypothesis of reproductive compensation and its assumptions about mate preferences and offspring viability. Proc Natl Acad Sci U S A 104:15023–15027PubMedCrossRefGoogle Scholar
  20. Harris WE, Uller T (2009) Reproductive investment when mate quality varies: differential allocation versus reproductive compensation. Phil Trans R Soc B 364:1039–1048PubMedCrossRefGoogle Scholar
  21. Hill JA, Enstrom DA, Ketterson ED, Nolan V Jr, Ziegenfus C (1999) Mate choice based on static versus dynamic secondary sexual traits in the dark-eyed junco. Behav Ecol 10:1–96CrossRefGoogle Scholar
  22. Hinde CA, Kilner RM (2007) Negotiations within the family over the supply of parental care. Proc R Soc Lond B 274:53–60CrossRefGoogle Scholar
  23. Hoelzer GA (1989) The good parent process of sexual selection. Anim Behav 38:1067–1078CrossRefGoogle Scholar
  24. Krebs EA, Hunte W, Green D (2004) Plume variation, breeding performance and extra-pair copulations in the cattle egret. Behaviour 141:479–499CrossRefGoogle Scholar
  25. Lessells CM (1999) Sexual conflict in animals. In: Keller L (ed) Levels of selection in evolution. Princeton University Press, Princeton, pp 75–99Google Scholar
  26. Matessi G, Carmagnani C, Griggio M, Pilastro A (2009) Male rock sparrows differentially allocate nest defence but not food provisioning to offspring. Behaviour 146:209–223CrossRefGoogle Scholar
  27. Morales J, Alonso-Álvarez C, Pérez C, Torres R, Serafino E, Velando A (2009a) Families on the spot: sexual signals influence parent–offspring negotiations. Proc R Soc Lond B 276:2477–2483CrossRefGoogle Scholar
  28. Morales J, Velando A, Torres R (2009b) Fecundity compromises attractiveness when pigments are scarce. Behav Ecol 20:117–123CrossRefGoogle Scholar
  29. Morales J, Velando A, Torres R (2010a) Biliverdin-based egg coloration is enhanced by carotenoid supplementation. Behav Ecol Sociobiol 65:197–203CrossRefGoogle Scholar
  30. Morales J, Torres R, Velando A (2010b) Parental conflict and blue egg coloration in a seabird. Naturwissenschaften 97:173–180PubMedCrossRefGoogle Scholar
  31. Moreno J, Osorno JL (2003) Avian egg color and sexual selection: does eggshell pigmentation reflect female condition and genetic quality? Ecol Lett 6:803–806CrossRefGoogle Scholar
  32. Nelson JB (1978) The Sulidae: gannets and boobies. Oxford University Press, OxfordGoogle Scholar
  33. Osorno JL, Székely T (2004) Sexual conflict and parental care in magnificent frigatebirds: full compensation by deserted females. Anim Behav 68:337–342CrossRefGoogle Scholar
  34. Pérez-Staples D, Drummond H (2005) Tactics, effectiveness and avoidance of mate guarding in the blue-footed booby. Behav Ecol Sociobiol 59:115–119CrossRefGoogle Scholar
  35. 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
  36. Ratikainen II, Kokko H (2010) Differential allocation and compensation: who deserves the silver spoon? Behav Ecol 21:195–200CrossRefGoogle Scholar
  37. Reed JR (1987) Scotopic and photopic spectral sensitivities of boobies. Ethology 76:33–55CrossRefGoogle Scholar
  38. Reznick D, Nunney L, Tessier A (2000) Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol Evol 15:421–425PubMedCrossRefGoogle Scholar
  39. Roff DA, Fairbairn DJ (2007) The evolution of trade-offs: where are we? J Evol Biol 20:433–447PubMedCrossRefGoogle Scholar
  40. Roulin A (1999) Non-random pairing by male barn owls (Tyto alba) with respect to a female plumage trait. Behav Ecol 10:688–695CrossRefGoogle Scholar
  41. Roulin A, Altwegg R, Jensen H, Steinsland I, Schaub M (2010) Sex-dependent selection on an autosomal melanic female ornament promotes the evolution of sex ratio bias. Ecol Lett 13:616–626PubMedCrossRefGoogle Scholar
  42. Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, Stradi R (2002) 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
  43. Sheldon B (2000) Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 15:398–402CrossRefGoogle Scholar
  44. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  45. Stocker R, Yorihiro Y, McDonagh AF, Glazer AN, Ames BN (1987) Bilirubin is an antioxidant of possible physiological properties. Science 235:1043–1046PubMedCrossRefGoogle Scholar
  46. Torres R, Drummond H (1999) Does large size make daughters of the blue-footed booby more expensive than sons? J Anim Ecol 68:1133–1141CrossRefGoogle Scholar
  47. 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
  48. Torres R, Velando A (2005) Male preference for female foot color in the socially monogamous blue-footed booby Sula nebouxii. Anim Behav 69:59–65CrossRefGoogle Scholar
  49. Torres R, Velando A (2010) Color in a long-lived tropical seabird: sexual selection in a life-history context. Advances 42:155–188Google Scholar
  50. Trivers RL (1972) Parental investment and sexual selection 1871–1971. In: Campbell BG (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179Google Scholar
  51. 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
  52. 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 149:535–542PubMedCrossRefGoogle Scholar
  53. Wiebe KL (2010) Negotiation of parental care when the stakes are high: experimental handicapping of one parent during incubation leads to short-term generosity. J Anim Ecol 79:63–70PubMedCrossRefGoogle Scholar
  54. Williams GC (1966) Natural selection, the costs of reproduction and a refinement of Lack's principle. Am Nat 100:687–690CrossRefGoogle Scholar
  55. Winkler DW (1987) A general model of parental care. Am Nat 130:526–543CrossRefGoogle Scholar
  56. Winkler DW, Wallin K (1987) Offspring size and number: a life history model linking effort per offspring and total effort. Am Nat 129:709–720CrossRefGoogle Scholar
  57. Zavalaga CB, Benvenuti S, Dall'Antonia L, Emslie SD (2007) Diving behavior of blue-footed boobies Sula nebouxii in northern Peru in relation to sex body size and prey type. Mar Ecol Prog Ser 336:291–303CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Judith Morales
    • 1
    • 2
  • Roxana Torres
    • 3
  • Alberto Velando
    • 1
  1. 1.Departamento de Ecoloxía e Bioloxía Animal, Facultade de CienciasUniversidade de VigoVigoSpain
  2. 2.Departamento de Ecología EvolutivaMuseo Nacional de Ciencias Naturales (CSIC)MadridSpain
  3. 3.Departamento de Ecología Evolutiva, Laboratorio de Conducta Animal, Instituto de EcologíaUniversidad Nacional Autónoma de MéxicoMéxicoMexico

Personalised recommendations