Skip to main content

Skin and flange colour, but not ectoparasites, predict condition and survival in starling nestlings

Abstract

Parents are expected to strategically partition their limited resources among the current and future progeny in order to maximize their fitness. Since an equal investment in offspring of different reproductive value entails fitness costs, natural selection has promoted the evolution of reliable signals of offspring condition, allowing parents to invest in their progeny accordingly. In birds, mouth and skin colouration are hypothesized to be honest signals of offspring condition, because they are affected by diverse factors. Among these, ectoparasite load has been shown to affect nestling condition, but its influence on visual components of begging is poorly known. We experimentally investigated whether nest ectoparasite removal affected flange and skin reflectance of first- and second-brood European starling (Sturnus vulgaris) nestlings. We also tested whether high reflectance in visual components of begging mirrored other aspects of nestling condition, such as morphological (high stature) and physiological (high haematocrit and immune response) traits, and pre-fledging mortality. Ectoparasite removal did not affect visual components of begging in first or second broods. However, larger nestlings from both broods displayed higher ultraviolet (UV) reflectance of skin and higher flange reflectance in the visible-wavelength region (but lower flange UV reflectance) than their siblings. A higher skin UV reflectance relative to siblings also positively predicted pre-fledging survival within-brood. Therefore, visual components of begging did not mirror ectoparasite infestation in this species. However, they provide parents with reliable information about individual quality, thus affecting resource allocation and promoting survival of the most valuable offspring during the entire breeding season.

Significance statement

In species with parental care, natural selection favours the evolution of reliable signals of offspring quality, thus allowing parents to invest in their progeny accordingly. We experimentally show that skin and beak flange colour does not mirror ectoparasite infection in European starling nestlings. However, begging visual signals predict nestling body size and survival until fledging. A seasonal variation in the strength of the association between begging visual signals and nestling condition is also shown, indicating that change ecological conditions can affect the association between different condition-dependent traits.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Arnold KE, Ramsay SL, Henderson L, Larcombe SD (2010) Seasonal variation in diet quality: antioxidants, invertebrates and blue tits Cyanistes caeruleus. Biol J Linn Soc 99:708–717

    Article  Google Scholar 

  2. Avery ML, Primus TM, Mihaich EM, Decker DG, Humphrey JS (1998) Consumption of fipronil-treated rice seed does not affect captive blackbirds. Pestic Sci 52:91–96

    CAS  Article  Google Scholar 

  3. de Ayala RM, Saino N, Møller AP, Anselmi C (2007) Mouth coloration of nestlings covaries with offspring quality and influences parental feeding behaviour. Behav Ecol 18:26–534

    Article  Google Scholar 

  4. Badyaev AV, Hamstra TL, Oh KP, Seaman DAA (2006) Sex-biased maternal effects reduce ectoparasite-induced mortality in a passerine bird. P Natl Acad Sci USA 103:14406–14411

    CAS  Article  Google Scholar 

  5. Bize P, Piault R, Moureau B, Heeb P (2006) A UV signal of offspring condition mediates context-dependent parental favouritism. Proc R Soc Lond B 273:2063–2068

    Article  Google Scholar 

  6. Brown CR, Brown MB (1992) Ectoparasitism as a cause of natal dispersal in cliff swallows. Ecology 73:1718–1723

  7. Candolin U (2000) Changes in expression and honesty of sexual signalling over the reproductive lifetime of sticklebacks. Proc R Soc Lond B 267:2425–2430

    CAS  Article  Google Scholar 

  8. Cantarero A, López-Arrabé J, Redondo AJ, Moreno J (2013) Behavioural responses to ectoparasites in pied flycatchers Ficedula hypoleuca: an experimental study. J Avian Biol 44:591–599

    Article  Google Scholar 

  9. Caro SM, Griffin AS, Hinde CA, West SA (2016) Unpredictable environments lead to the evolution of parental neglect in birds. Nat Commun 7:10985

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Christe P, Richner H, Oppliger A (1996) Begging, food provisioning, and nestling competition in great tit broods infested with ectoparasites. Behav Ecol 7:127–131

    Article  Google Scholar 

  11. Clark L, Mason JR (1988) Effect of biologically active plants used as nest material and the derived benefit to starling nestlings. Oecologia 77:174–180

    Article  PubMed  Google Scholar 

  12. Costantini D, Møller AP (2008) Carotenoids are minor antioxidants for birds. Funct Ecol 22:367–370

    Article  Google Scholar 

  13. Cotton S, Fowler K, Pomiankowski A (2004) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc R Soc Lond B 271:771–783

    Article  Google Scholar 

  14. Cramp S (1998) The complete birds of the western Palearctic on CD-ROM. Oxford University Press, Oxford

  15. Davis JN, Todd PM, Bullock S (1999) Environment quality predicts parental provisioning decisions. Proc R Soc Lond B 266:1791–1797

    Article  Google Scholar 

  16. Dawson RD, Bortolotti GR (1997) Are avian hematocrits indicative of condition? American kestrels as a model. J Wildlife Manage 61:1297–1306

    Article  Google Scholar 

  17. Doutrelant C, Grégoire A, Grnac N, Gomez D, Lambrechts MM, Perret P (2008) Female coloration indicates female reproductive capacity in blue tits. J Evol Biol 21:226–233

    CAS  PubMed  Google Scholar 

  18. Dugas MB (2009) House sparrow (Passer domesticus) parents preferentially feed nestlings with mouth colours that appear carotenoid-rich. Anim Behav 78:767–772

    Article  Google Scholar 

  19. Dugas MB (2012) Cross-fostering reveals that among-brood differences in ornamental mouth colouration mostly reflect rearing conditions in nestling house sparrows. Biol J Linn Soc 106:169–179

    Article  Google Scholar 

  20. Dugas MB (2015) Commentary: parental care and the proximate links between maternal effects and offspring fitness. Oecologia 177:1089–1092

    Article  PubMed  Google Scholar 

  21. Dugas MB, Doumas LT (2014) Ectoparasite density is associated with mouth colour and size in nestling house sparrows Passer domesticus. Ibis 156:682–686

    Article  Google Scholar 

  22. Dugas MB, McGraw KJ (2011) Proximate correlates of carotenoid-based mouth coloration in nestlings house sparrow. Condor 113:691–700

    Article  Google Scholar 

  23. Dugas MB, Rosenthal GG (2010) Carotenoid-rich mouth colors influence the conspicuousness of nestling birds. Behav Ecol Sociobiol 64:455–462

    Article  Google Scholar 

  24. Ewen GE, Thorogood R, Karadas F, Cassey P (2008) Condition dependence of nestling mouth colour and effect of supplementing carotenoids on parental behaviour in the hihi (Notiomystis cinta). Oecologia 157:361–368

    Article  PubMed  Google Scholar 

  25. Fair J, Whitaker S, Pearson B (2007) Sources of variation in haematocrit in birds. Ibis 149:535–552

    Article  Google Scholar 

  26. Gil D, Bulmer E, Celis P, Lopez-Rull I (2008) Adaptive developmental plasticity in growing nestlings: sibling competition induces differential gape growth. Proc R Soc Lond B 275:549–554

    Article  Google Scholar 

  27. Godfray HCJ (1991) Signaling of need by offspring to their parents. Nature 352:328–330

    Article  Google Scholar 

  28. Griffiths R, Double MC, Orr K, Dawson RJ (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075

    CAS  Article  PubMed  Google Scholar 

  29. Griggio M, Morosinotto C, Pilastro A (2009) Nestlings’ carotenoid feather ornament affects parental allocation strategy and reduces maternal survival. J Evol Biol 22:2077–2085

    CAS  Article  PubMed  Google Scholar 

  30. Gwinner H, Oltrogge M, Trost L, Nienaber U (2000) Green plants in starling nests: effects on nestlings. Anim Behav 59:301–309

    CAS  Article  PubMed  Google Scholar 

  31. Hartley RC, Kennedy MW (2004) Are carotenoids a red herring in sexual display? Trends Ecol Evol 19:353–354

    Article  PubMed  Google Scholar 

  32. Hill G, McGraw K (2006) Bird coloration. Mechanisms and measurements. Harvard University Press, Cambridge Vol. 1

  33. Hunt S, Kilner RM, Langmore NE, Bennett ATD (2003) Conspicuous, ultraviolet-rich mouth colours in begging chicks. Proc R Soc Lond B 270:S25–S28

    Article  Google Scholar 

  34. Jacob S, Heeb P (2013) Mouth colour components of begging are dynamic signals of quality in European starling nestlings. J Avian Biol 44:39–44

    Article  Google Scholar 

  35. Jacob S, Rieucau G, Heeb P (2011) Multimodal begging signals reflect independent indices of nestling condition in European starlings. Behav Ecol 22:1249–1255

    Article  Google Scholar 

  36. Jacob S, Parthuisot N, Vallat A, Ramon-Portugal F, Helfenstein F, Heeb P (2015) Microbiome affects egg carotenoid investment, nestling development and adult oxidative costs of reproduction in great tits. Funct Ecol 29:1048–1058

    Article  Google Scholar 

  37. Johnstone RA (1999) Signalling of need, sibling competition and the cost of honesty. P Natl Acad Sci USA 96:12644–12649

    CAS  Article  Google Scholar 

  38. Jourdie V, Moureau B, Bennet ATD, Heeb P (2004) Ultraviolet reflectance by the skin of nestlings. Nature 431:262

    CAS  Article  PubMed  Google Scholar 

  39. Kacelnik A, Cotton PA, Stirling L, Wright J (1995) Food allocation among nestling starlings: sibling competition and the scope of parental choice. Philos T Roy Soc B 259:259–263

    Article  Google Scholar 

  40. Kilner RM (1997) Mouth colour is a reliable signal of need in begging canary nestlings. Proc R Soc Lond B 264:963–968

    Article  Google Scholar 

  41. Kilner RM (2002) The evolution of complex begging displays. In: Wright J, Leonard ML (eds) The evolution of begging: competition, cooperation and communication. Kluwer Academic, Dordrecht, pp 87–106

    Chapter  Google Scholar 

  42. Kilner RM, Johnstone RA (1997) Begging the question: are offspring solicitation behaviours signals of need? Trends Ecol Evol 12:11–15

    CAS  Article  PubMed  Google Scholar 

  43. Leonard ML, Horn AG, Parks E (2003) The role of posturing and calling in the begging display of nestling birds. Behav Ecol Sociobiol 54:188–193

    Article  Google Scholar 

  44. Lessells CM (2002) Parentally biased favouritism: why should parents specialize in caring for different offspring? Philos T Roy Soc B 357:381–403

    CAS  Article  Google Scholar 

  45. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 1:116–121

    Article  Google Scholar 

  46. Liker A, Márkus M, Vozár Á, Zemankovics E, Rózsa L (2001) Distribution of Carnus hemapterus in a starling colony. Can J Zool 79:574–580

    Article  Google Scholar 

  47. Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348

    Article  PubMed  Google Scholar 

  48. Loiseau C, Fellous S, Haussy C (2008) Condition-dependent effects of corticosterone on a carotenoid-based begging signal in house sparrows. Horm Behav 53:266–273

    CAS  Article  PubMed  Google Scholar 

  49. Lyon BE, Eadie JM, Hamilton LD (1994) Parental choice selects for ornamental plumage in American coot chicks. Nature 371:240–243

    Article  Google Scholar 

  50. Marri V, Richner H (2014) Yolk carotenoids increase fledging success in great tit nestlings. Oecologia 176:371–377

    Article  PubMed  Google Scholar 

  51. Martínez-de la Puente J, Merino S, Tomás G, Moreno J, Morales J, Lobato E, Martínez J (2011) Nest ectoparasites increase physiological stress in breeding birds: an experiment. Naturwissenschaften 98:99–106

    Article  PubMed  Google Scholar 

  52. Mazgajski TD (2007) Effect of old nest material in nestboxes on ectoparasite abundance and reproductive output in the European Starling Sturnus vulgaris. Pol J Ecol 55:377–385

    Google Scholar 

  53. Merino S, Potti J (1995) Mites and blowflies decrease growth and survival in nestling pied flycatchers. Oikos 73:95–103

    Article  Google Scholar 

  54. Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, New York

  55. Mock DW, Dugas MB, Strickler SA (2011) Honest begging: expanding from signal of need. Behav Ecol 22:909–917

    Article  Google Scholar 

  56. Møller AP (1989) Parasites, Predators and nest boxes: Facts and artefacts in nest box studies of birds? Oikos 56:421–423

  57. Møller AP (1993) Ectoparasites increase the cost of reproduction in their hosts. J Anim Ecol 62:309–322

    Article  Google Scholar 

  58. Møller AP, Erritzøe J (1996) Parasite virulence and host immune defense: host immune response is related to nest reuse in birds. Evolution 50:2066–2072

    Article  Google Scholar 

  59. Møller AP, Arriero E, Lobato E, Merino S (2009) A meta-analysis of parasite virulence in nestling birds. Biol Rev 84:567–588

    Article  PubMed  Google Scholar 

  60. Moreno-Rueda G, Redondo T, Ochoa D, Camacho C, Canal D, Potti J (2016) Nest-dwelling ectoparasites reduce begging effort in pied flycatcher Ficedula hypoleuca nestlings. Ibis 158:881–886

    Article  Google Scholar 

  61. O’Connor JA, Sulloway FJ, Robertson J, Kleindorfer S (2010) Philornis downsi parasitism is the primary cause of nestling mortality in the critically endangered Darwin’s medium tree finch (Camarhynchus pauper). Biodivers Conserv 19:853–866

    Article  Google Scholar 

  62. Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 12:510–514

    Article  Google Scholar 

  63. Parker GA, Royle NJ, Hartley IR (2002) Intrafamilial conflict and parental investment: a synthesis. Philos T Roy Soc B 357:295–307

    Article  Google Scholar 

  64. Pinxten R, Eens M, Verheyen RF (1990) Intermediate clutches in the Starling (Sturnus vulgaris): replacement clutches, additional clutches of polygynous males or late first clutches? J Ornithol 131:141–150

  65. Pirrello S, Pilastro A, Serra L (2015) Nest-dwelling ectoparasites influence the start and duration of the first pre-basic moult in the European starling Sturnus vulgaris. J Avian Biol 46:412–418

    Article  Google Scholar 

  66. van de Pol M, Wright J (2009) A simple method for distinguishing within- versus between-subject effects using mixed models. Anim Behav 77:753–758

    Article  Google Scholar 

  67. Powlesland RG (1977) Effects of the haematophagous mite Ornithonyssus bursa on nestling starlings in New Zealand. New Zeal J Zool 4:85–94

    Article  Google Scholar 

  68. Romano A, Rubolini D, Caprioli M, Boncoraglio G, Ambrosini R, Saino N (2011) Sex-related effects of an immune challenge on growth and begging behavior of barn swallow nestlings. PLoS One 6:e22805

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. Romano A, Bazzi G, Caprioli M, Corti M, Costanzo A, Rubolini D, Saino (2016) Nestling sex and plumage color predict food allocation by barn swallow parents. Behav Ecol 27:1198–1205

    Article  Google Scholar 

  70. Royle NJ, Smiseth PT, Kölliker M (2012) The evolution of parental care. Oxford University Press, Oxford

  71. Ruiz-Castellano C, Soler M, Rösler A, Martín-Gálvez D, Soler JJ (2016) Context-dependent effects of an experimental increase of hunger level in house sparrow nestlings. Behav Ecol Sociobiol 70:939–949

    Article  Google Scholar 

  72. Saino N, Ninni P, Calza S, Martinelli R, De Bernardi F, Møller AP (2000) Better red than dead: corotenoid based mouth coloration reveals infection in barn swallow nestlings. Proc R Soc Lond B 267:57–61

    CAS  Article  Google Scholar 

  73. Saino N, Romano M, Scandolara C, Rubolini D, Ambrosini R, Caprioli M, Costanzo A, Romano A (2014) Brownish, small and lousy barn swallows have greater natal dispersal propensity. Anim Behav 87:137–146

    Article  Google Scholar 

  74. SAS Institute (2006) The GLIMMIX procedure. SAS Institute, Cary, NC

  75. Serra L, Pirrello S, Caprioli M et al. (2012) Seasonal decline of off spring quality in the European starling Sturnus vulgaris: an immune challenge experiment. Behav Ecol Sociobiol 66:697–709

    Article  Google Scholar 

  76. Seth A, Pradhan S, Purkait S, Sinha S, Chowdhury A (2016) Effects of fipronil, a pyrazole insecticide, on microbial biomass carbon, soil respiration, FDA and dehydrogenase activity of soil. Int J Adv Biol Res 6:352–356

    Google Scholar 

  77. Soler JJ, Avilés JM, Cuervo JJ, Perez-Contreras T (2007) Is the relation between colour and immune response mediated by nutritional condition in spotless starling nestlings? Anim Behav 74:1139–1145

    Article  Google Scholar 

  78. Svensson PA, Wong BBM (2011) Carotenoid-based signals in behavioural ecology: a review. Behaviour 148:131–189

    Article  Google Scholar 

  79. Szép T, Møller AP (1999) Cost of parasitism and host immune defence in the sand martin Riparia riparia: a role for parent-off spring conflict? Oecologia 119:9–15

    Article  PubMed  Google Scholar 

  80. Tella JL, Lemus JA, Carrete M, Blanco G (2008) The PHA test reflects acquired T-cell mediated immunocompetence in birds. PLoS One 3:e3295

    Article  PubMed  PubMed Central  Google Scholar 

  81. Thorogood R, Kilner RM, Karadas F, Ewen JG (2008) Spectral mouth colour of nestlings changes with carotenoid availability. Funct Ecol 22:1044–1051

    Article  Google Scholar 

  82. Tomás G, Merino S, Martínez-de la Puente J, Moreno J, Morales J, Lobato E (2008) Determinants of abundance and effects of blood-sucking flying insects in the nest of a hole-nesting bird. Oecologia 156:305–312

    Article  PubMed  Google Scholar 

  83. Trivers RL (1974) Parent-offspring conflict. Am Zool 14:249–264

    Article  Google Scholar 

  84. Tschirren B, Fitze PS, Richner H (2003) Proximate mechanisms of variation in the carotenoid-based plumage coloration of nestling great tits (Parus major L.) J Evol Biol 16:91–100

    CAS  Article  PubMed  Google Scholar 

  85. Vergara P, Martinez-Padilla J, Mougeot F, Leckie F, Redpath SM (2012) Environmental heterogeneity influences the reliability of secondary sexual traits as condition indicators. J Evol Biol 25:20–28

    Article  PubMed  Google Scholar 

  86. Verhulst S, Nilsson JÅ (2008) The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Philos T Roy Soc B 363:399–410

    Article  Google Scholar 

  87. Wright J, Leonard ML (2002) The evolution of begging: competition, cooperation and communication. Kluwer Academic, Dordrecht, The Netherlands

Download references

Acknowledgements

We are grateful to L. Zangari and G. Viscardi who greatly helped during field work. Three anonymous referees also provided very useful comments to previous versions of the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Andrea Romano.

Ethics declarations

This research was undertaken (capture and experimental treatments) under the combined prescriptions of Art. 4 (1) and Art. 7 (5) of the Italian law 157/1992, which regulates studies on wild bird species. This law also regulates taking, keeping and manipulating procedures to be followed for the study of wild birds. Standard procedures for capturing and handling nestlings in the nest-box were used. The duration of handling nestlings was kept to a minimum to minimize stress.

Funding

SP and AP were partially supported by a grant from the Fondazione CARIPARO (Progetto di eccellenza 2007). AR was funded by the Postdoctoral Fellowship Program of the Ministero dell’Istruzione, dell’Università e della Ricerca (MIUR). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by K. McGraw

Electronic supplementary material

ESM 1

(DOCX 40 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pirrello, S., Colombo, E., Pilastro, A. et al. Skin and flange colour, but not ectoparasites, predict condition and survival in starling nestlings. Behav Ecol Sociobiol 71, 63 (2017). https://doi.org/10.1007/s00265-017-2292-6

Download citation

Keywords

  • Begging behaviour
  • Ectoparasites
  • Flange colour
  • Parent-offspring communication
  • Skin colour
  • Seasonal variation