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Reproductive success related to uropygial gland volume varies with abundance of conspecifics in barn swallows Hirundo rustica

  • Sergio Magallanes
  • Cosme López-Calderón
  • Javier Balbontín
  • Anders P. Møller
  • Florentino de Lope
  • Alfonso MarzalEmail author
Original Article

Abstract

Pathogens have negative effects on the fitness of their hosts, reducing survival and/or decreasing their reproductive success. To cope with pathogen challenge, animals have developed a variety of defensive traits to evade parasite infection and minimize their detrimental effects. Uropygial gland secretion has been proposed to have antimicrobial and antifungal properties, which may potentially influence bird fitness. However, whether uropygial gland secretion may affect the breeding success of birds remains unknown. Here, we explore whether the relationship between uropygial gland volume and reproductive success could be determined by the abundance of conspecific barn swallows (Hirundo rustica), a small colonial migratory hirundine. Because a larger number of swallows nesting within the same building may boost abundance and transmission of pathogens, we predicted that the anti-pathogen properties of uropygial gland secretion may enhance bird reproductive success in environments with high density of conspecifics. We showed that barn swallows with larger uropygial glands had higher breeding success (greater total number of fledglings reared) when living in environments with higher abundance of conspecifics. In contrast, barn swallows with larger uropygial glands had lower reproductive success when breeding in environments with lower abundance of conspecifics. Furthermore, we found that the same individuals did not modify uropygial glands in response to different pathogen pressure experienced across consecutive years. These outcomes suggest that benefits of uropygial secretion are host density dependent, thus consistent with this being a heritable trait that has evolved as a consequence of divergent selection imposed by pathogens.

Significance statement

To face pathogen challenges, animals have evolved a broad range of barriers and defense mechanisms to avoid parasite infection and/or to minimize negative effects. Uropygial gland secretion has been proposed to have antimicrobial and antifungal properties, but also act as a defensive mechanism against malaria infection. However, whether uropygial gland secretions may affect the reproductive success of birds remains poorly studied. In this study, we explore, for the first time, whether the relationship between uropygial gland volume and reproductive success could be determined by the abundance of conspecifics. We found that barn swallows with larger uropygial glands had higher breeding success when living in environments with higher abundance of conspecifics. Because a larger number of swallows nesting within the same building may boost abundance and transmission of pathogens, this novel outcome is consistent with a heritable trait that has evolved as a consequence of divergent selection imposed by pathogens.

Keywords

Barn swallow Defensive traits Hirundo rustica Host-pathogen interaction Preen gland Reproductive success 

Notes

Acknowledgments

Charles R. Brown and two anonymous reviewers provided suggestions to improve the article. We thank Juan Sangran and his family, Borja Lora and his family, Plácido, and Marzal family for allowing us to work on their properties. Thanks also to Martin, Manuel, Antonio, Fernando, Javier, Gabriel, and all the other staff that work in the farms. We also thank Marina Bollo, Celia Vinagre-Izquierdo, and all students that participated through their help during fieldwork.

Funding

This study was funded by research projects of the Spanish Ministry of Economy and Competitiveness (CGL2015-64650P), Junta de Extremadura (IB16121), and Junta of Andalucía (P12-RNM-2144). SM was supported by a PhD grant from Ministry of Economy and Competition of Spain. CLC was supported by an operating grant from the Junta of Andalucía (P12-RNM-2144).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All the experiments comply with the current laws of Spain, where the experiments were performed. Methods were evaluated and approved by institutional Commission of Bioethics of University of Extremadura (CBUE 49/2011) and by Junta de Extremadura Local Government (72/2016).

Supplementary material

265_2018_2598_MOESM1_ESM.docx (120 kb)
ESM 1 (DOCX 120 kb)

References

  1. Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, Poss M, Pulliam JRC (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu Rev Ecol Evol Syst 34:517–547Google Scholar
  2. Anderson RM, May RM (1978) Regulation and stability of host-parasite population interaction. J Anim Ecol 47:249–267Google Scholar
  3. Asghar M, Hasselquist D, Bensch S (2011) Are chronic avian haemosporidian infections costly in wild birds? J Avian Biol 42:530–537Google Scholar
  4. Asghar M, Hasselquist D, Hansson B, Zehtindjiev P, Westerdahl H, Bensch S (2015) Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347:436–438PubMedGoogle Scholar
  5. Baggott GK, Graeme-Cook K (2002) Microbiology of natural incubation. In: Deeming DC (ed) Avian incubation behaviour, environment and evolution. Oxford University Press, Oxford, pp 179–191Google Scholar
  6. Balbontín J, Hermosell IG, Marzal A, Reviriego M, de Lope F, Møller AP (2007) Age-related change in breeding performance in early life is associated with an increase in competence in the migratory barn swallow Hirundo rustica. J Anim Ecol 76:915–925PubMedGoogle Scholar
  7. Balbontín J, Møller AP, Hermosell IG, Marzal A, Reviriego M, de Lope F (2009) Geographic patterns of natal dispersal in barn swallows Hirundo rustica from Denmark and Spain. Behav Ecol Sociobiol 63:1197–1205Google Scholar
  8. Balbontín J, Møller AP, Hermosell IG, Marzal A, Reviriego M, de Lope F (2012a) Lifetime individual plasticity in body condition of a migratory bird. Biol J Linn Soc 105:420–434Google Scholar
  9. Balbontín J, Møller AP, Hermosell IG, Marzal A, Reviriego M, de Lope F (2012b) Geographical variation in reproductive ageing patterns and life-history strategy of a short-lived passerine bird. J Evol Biol 25:2298–2309PubMedGoogle Scholar
  10. Bandyopadhyay A, Bhattacharyya SP (1999) Influence of fowl uropygial gland and its secretory lipid components on the growth of skin surface fungi of fowl. Indian J Exp Biol 37:1218–1222PubMedGoogle Scholar
  11. Barton K (2015) Package MuMIn: multi-model inference. R Package version 1.15.1., https://cran.r-project.org/web/packages/MuMIn/index.html
  12. Bates D, Maechler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–51Google Scholar
  13. Begon M, Bennett M, Bowers RG, French NP, Hazel SM, Turner J (2002) A clarification of transmission terms in host-microparasite models: numbers, densities and areas. Epidemiol Infect 129:147–153PubMedPubMedCentralGoogle Scholar
  14. BirdLife International (2018) Species factsheet: Hirundo rustica, http://www.birdlife.org. Accessed 02 April 2018
  15. Brown CR, Brown MB (1996) Coloniality in the cliff swallow: the effect of group size on social behavior. University of Chicago Press, ChicagoGoogle Scholar
  16. Brown CR, Brown MB (2004) Empirical measure- ment of parasite transmission between groups in a colonial bird. Ecology 85:1619–1626Google Scholar
  17. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information theoretic approach. Springer, New YorkGoogle Scholar
  18. Calero-Riestra M, García JT (2016) Sex-dependent differences in avian malaria prevalence and consequences of infections on nestling growth and adult condition in the Tawny pipit, Anthus campestris. Malaria J 15:178Google Scholar
  19. Cook MI, Beissinger SR, Toranzos GA, Arendt WJ (2005a) Incubation reduces microbial growth on eggshells and the opportunity for trans-shell infection. Ecol Lett 8:532–537PubMedGoogle Scholar
  20. Cook MI, Beissinger SR, Toranzos GA, Rodriguez RA, Arendt WJ (2005b) Microbial infection affects egg viability and incubation behavior in a tropical passerine. Behav Ecol 16:30–36Google Scholar
  21. Dimitrov D, Palinauskas V, Iezhova TA, Bernotienė R, Ilgūnas M, Bukauskaitė D, Zehtindjiev P, Ilieva M, Shapoval AP, Bolshakov CV, Markovets MY, Bensch S, Valkiūnas G (2015) Plasmodium spp.: an experimental study on vertebrate host susceptibility to avian malaria. Exp Parasitol 148:1–16PubMedGoogle Scholar
  22. Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W (2008) Homage to Linnaeus: how many parasites? How many hosts? Proc Natl Acad Sci U S A 105:11482–11489PubMedPubMedCentralGoogle Scholar
  23. Eizaguirre C, Lenz TL, Kalbe M, Milinski M (2012) Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nat Commun 3:621–627PubMedPubMedCentralGoogle Scholar
  24. Fülöp A, Vágási CI, Pap PL (2017) Cohabitation with farm animals rather than breeding effort increases the infection with feather-associated bacteria in the barn swallow Hirundo rustica. J Avian Biol 48:1005–1014Google Scholar
  25. Gaidet N, Caron A, Cappelle J, Cumming GS, Balanca G, Hammoumi S, Cattoli G, Abolnik C, Servan de Almeida R, Gil P, Fereidouni SR, Grosbois V, Tran A, Mundava J, Fofana B, Ould el Mamy AB, Ndlovu M, Mondain-Monval JY, Triplet P, Hagemeijer W, Karesh WB, Newman SH, Dodman T (2012) Understanding the ecological drivers of avian influenza virus infection in wildfowl: a continental-scale study across Africa. Proc R Soc Lond B 279:1131–1141Google Scholar
  26. Galván I, Sanz JJ (2006) Feather mite abundance increases with uropygial gland size and plumage yellowness in Great Tits Parus major. Ibis 148:687–697Google Scholar
  27. Gelman A (2008) Scaling regression inputs by dividing by two standard deviations. Stat Med 27:2865–2873PubMedGoogle Scholar
  28. Gelman A, Su YS (2015) Arm: data analysis using regression and multilevel/hierarchical models. R Package version 1.8–5, https://cran.r-project.org/web/packages/arm/index.html
  29. Giraudeau M, Czirják GÁ, Duval C, Bretagnolle V, Eraud C, McGraw KJ, Heeb P (2010) Effect of restricted preen-gland access on maternal self maintenance and reproductive investment in mallards. PLoS One 5:e13555PubMedPubMedCentralGoogle Scholar
  30. Golüke S, Caspers BA (2017) Sex-specific differences in preen gland size of zebra finches during the course of breeding. Auk 134:821–831Google Scholar
  31. Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711PubMedGoogle Scholar
  32. Han BA, Park AW, Jolles AE, Altizer S (2015) Infectious disease transmission and behavioural allometry in wild mammals. J Anim Ecol 84:637–646PubMedGoogle Scholar
  33. Hansen CM, Meixell BW, Van Hemert C, Hare RF, Hueffer K (2015) Microbial infections are associated with embryo mortality in arctic-nesting geese. Appl Environ Microbiol 81:5583–5592PubMedPubMedCentralGoogle Scholar
  34. Hasselquist D, Nilsson J (2012) Physiological mechanisms mediating costs of immune responses: what can we learn from studies of birds? Anim Behav 83:1303–1312Google Scholar
  35. Hermosell IG, Balbontín J, Marzal A, Reviriego M, de Lope F (2007) Sex determination in barn swallows Hirundo rustica by means of discriminant analysis in two European populations. Ardeola 54:93–100Google Scholar
  36. Jacob J, Ziswiler V (1982) The uropygial gland. In: Farner DS, King JR (eds) Avian biology, vol VI. Academic Press, London, pp 199–324Google Scholar
  37. Jacob J, Eigener U, Hoppe U (1997) The structure of preen gland waxes from pelecaniform birds containing 3,7-dimethyloctan-1-ol - an active ingredient against dermatophytes. A J Biosci 52:114–123Google Scholar
  38. Jacob S, Immer A, Leclaire S, Parthuisot N, Ducamp C, Espinasse G, Heeb P (2014) Uropygial gland size and composition varies according to experimentally modified microbiome in great tits. BMC Evol Biol 14:134PubMedPubMedCentralGoogle Scholar
  39. 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 29:1048–1058Google Scholar
  40. Johnson MB, Lafferty KD, van Oosterhout C, Cable J (2011) Parasite transmission in social interacting hosts: monogenean epidemics in guppies. PLoS One 6:e22634PubMedPubMedCentralGoogle Scholar
  41. Klasing KC (2004) The cost of immunity. Acta Zool Sin 50:961–969Google Scholar
  42. Krist M (2011) Egg size and offspring quality: a meta-analysis in birds. Biol Rev 86:692–716PubMedGoogle Scholar
  43. Law-Brown J (2001) Chemical defence in the red billed woodhoopoe Phoeniculus purpureus. MSc thesis, University of Cape Town, Cape Town, South AfricaGoogle Scholar
  44. Magallanes S, Møller AP, García-Longoria L, de Lope F, Marzal A (2016) Volume and antimicrobial activity of secretions of the uropygial gland are correlated with malaria infection in house sparrows. Parasite Vector 9:232Google Scholar
  45. Magallanes S, García-Longoria L, López-Calderón C, Reviriego M, de Lope F, Møller AP, Marzal A (2017) Uropygial gland volume and malaria infection are related to survival in migratory house martins. J Avian Biol 48:1355–1359Google Scholar
  46. Marri V, Richner H (2014) Differential effects of vitamins E and C and carotenoids on growth, resistance to oxidative stress, fledging success and plumage colouration in wild great tits. J Exp Biol 217:1478–1484PubMedGoogle Scholar
  47. Martínez-de la Puente J, Merino S, Tomás G, Moreno J, Morales J, Lobato E, García-Fraile S, Belda EJ (2010) The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment. Biol Lett 6:663–665Google Scholar
  48. Martínez-García A, Soler JJ, Rodríguez-Ruano SM, Martínez-Bueno M, Martín-Platero AM, Juárez-García N, Martín-Vivaldi M (2015) Preening as a vehicle for key bacteria in hoopoes. Microbial Ecol 70:1024–1033Google Scholar
  49. Martín-Vivaldi M, Ruiz-Rodríguez M, Soler JJ, Peralta-Sánchez JM, Méndez M, Valdivia E, Martín-Platero AM, Martínez-Bueno M (2009) Seasonal, sexual and developmental differences in hoopoe Upupa epops preen gland morphology and secretions: evidence for a role of bacteria. J Avian Biol 40:191–205Google Scholar
  50. Martin-Vivaldi M, Soler JJ, Peralta-Sánchez JM, Arco L, Martin-Platero AM, Martinez-Bueno M, Ruiz-Rodríguez M, Valdivia E (2014) Special structures of hoopoe eggshells enhance the adhesion of symbiont-carrying uropygial secretion that increase hatching success. J Anim Ecol 83:1289–1301PubMedGoogle Scholar
  51. Marzal A, de Lope F, Navarro C, Møller AP (2005) Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142:541–545PubMedGoogle Scholar
  52. Marzal A, Bensch S, Reviriego M, Balbontín J, de Lope F (2008) Effects of malaria double infection in birds: one plus one is not two. J Evol Biol 21:979–987PubMedGoogle Scholar
  53. Marzal A, Reviriego M, Hermosell IG, Balbontín J, Bensch S, Relinque C, Rodríguez L, Garcia-Longoria L, de Lope F (2013) Malaria infection and feather growth rate predict reproductive success in house martins. Oecologia 171:853–861PubMedGoogle Scholar
  54. Marzal A, Balbontín J, Reviriego M, García-Longoria L, Relinque C, Hermosell IG, Magallanes S, López-Calderón C, de Lope F, Møller AP (2016) A longitudinal study of age-related changes in Haemoproteus infection in a passerine bird. Oikos 125:1092–1099Google Scholar
  55. Marzal A, Møller AP, Espinoza K et al (2018) Variation in malaria infection and immune defence in invasive and endemic house sparrows. Anim Conserv, published online,  https://doi.org/10.1111/acv.12423
  56. Maxted AM, Luttrell MP, Goekjian VH, Brown JD, Niles LJ, Dey AD, Kalasz KS, Swayne DE, Stallknecht DE (2012) Avian influenza virus infection dynamics in shorebird hosts. J Wildl Dis 48:322–335PubMedGoogle Scholar
  57. Merino S, Moreno J, Sanz JJ, Arriero E (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proc R Soc Lond B 9:2507–2510Google Scholar
  58. Møller AP (1992) Swallowing ornamental asymmetry. Nature 359:488Google Scholar
  59. Møller AP (1994a) Sexual selection and the barn swallow. Oxford University Press, OxfordGoogle Scholar
  60. Møller AP (1994b) Phenotype-dependent arrival time and its consequences in a migratory bird. Behav Ecol Sociobiol 35:115–122Google Scholar
  61. Møller AP (2005) Parasitism and the regulation of host populations. In: Thomas F, François R (eds) Parasitism and ecosystems. Oxford University Press, Oxford, pp 43–53Google Scholar
  62. Møller AP, Erritzøe J (2001) Dispersal, vaccination and regression of immune defence organs. Ecol Lett 4:484–490Google Scholar
  63. Møller AP, de Lope F, Saino N (2005) Reproduction and migration in relation to senescence in the barn swallow Hirundo rustica: a study of avian “centenarians”. Age 27:1–12Google Scholar
  64. Møller AP, Czirjak GÁ, Heeb P (2009) Feather micro-organisms and uropygial antimicrobial defences in a colonial passerine bird. Funct Ecol 23:1097–1102Google Scholar
  65. Moore J (2002) Parasites and the behavior of animals. Oxford University Press, OxfordGoogle Scholar
  66. Moreno-Rueda G (2010) Uropygial gland size correlates with feather holes, body condition and wingbar size in the house sparrow Passer domesticus. J Avian Biol 41:229–236Google Scholar
  67. Moreno-Rueda G (2011) House Sparrows Passer domesticus with larger uropygial glands show reduced feather wear. Ibis 153:195–198Google Scholar
  68. Moreno-Rueda G (2015) Body-mass-dependent trade-off between immune response and uropygial gland size in house sparrows Passer domesticus. J Avian Biol 46:40–45Google Scholar
  69. Moreno-Rueda G (2017) Preen oil and bird fitness: a critical review of the evidence. Biol Rev 92:2131–2143PubMedGoogle Scholar
  70. Müller W, Groothuis TGG, Dijkstra C, Siitari H, Alatalo R (2004) Maternal antibody transmission and breeding densities in the black-headed gull Larus ridibundus. Funct Ecol 18:719–724Google Scholar
  71. Muriel J, Salmón P, Nunez-Buiza A, de Salas F, Pérez-Rodríguez L, Puerta M, Gil D (2015) Context-dependent effects of yolk androgens on nestling growth and immune function in a multibrooded passerine. J Evol Biol 28:1476–1488PubMedGoogle Scholar
  72. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  73. Nallar R, Papp Z, Leighton FA, Epp T, Pasick J, Berhane Y, Lindsay R, Soos C (2016) Ecological risk factors of avian influenza virus, West Nile virus and avian paramyxovirus infection and antibody status in blue-winged teal (Anas discors) in the Canadian prairies. J Wildl Dis 52:33–46PubMedGoogle Scholar
  74. Nussey DH, Froy H, Lemaître JF, Gaillard JM, Austad SN (2013) Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology. Ageing Res Rev 12:214–225PubMedGoogle Scholar
  75. Olea L, San Miguel A (2006) The Spanish dehesa: a traditional Mediterranean silvopastoral system linking production and nature conservation. In: 21st General Meeting of the European Grassland Federation, Badajoz. Sociedad Española para el Estudio de los Pastos (SEEP), MadridGoogle Scholar
  76. Pap PL, Vágási CI, Osváth G, Mureșan C, Barta Z (2010) Seasonality in the uropygial gland size and feather mite abundance in house sparrows Passer domesticus: natural covariation and an experiment. J Avian Biol 41:653–661Google Scholar
  77. Pap PL, Adam C, Vágási CI, Benkő Z, Vincze O (2013) Sex ratio and sexual dimorphism of three lice species with contrasting prevalence parasitizing the house sparrow. J Parasitol 99:24–30PubMedGoogle Scholar
  78. Peralta-Sánchez JM, Martín-Platero AM, Wegener-Parfrey L et al (2018) Bacterial density rather than diversity correlates with hatching success across different avian species. Microb Ecol 94:022Google Scholar
  79. Piault R, Gasparini J, Bize P, Paulet M, McGraw KJ, Roulin A (2008) Experimental support for the makeup hypothesis in nestling tawny owls (Strix aluco). Behav Ecol 19:703–709Google Scholar
  80. Pinowski J, Barkowska M, Kruszewicz AH, Kruszewicz AG (1994) The causes of the mortality of eggs and nestlings of Passer sp. J Biosci 19:441–451Google Scholar
  81. Poulin R (1998) Evolutionary ecology of parasites. Chapman & Hall, New YorkGoogle Scholar
  82. R Development Core Team (2017) R: A language and environment for statistical computing. R Foundation for statistical Computing, Vienna, Austria, https://www.R-project.org/
  83. Richards SA (2008) Dealing with overdispersed count data in applied ecology. J Appl Ecol 45:218–227Google Scholar
  84. Ricklefs RE (1990) Evolution of life histories, 3rd edn. W. H. Freeman, New YorkGoogle Scholar
  85. Rifkin JL, Nunn CL, Garamszegi LZ (2012) Do animals living in larger groups experience greater parasitism? A meta-analysis. Am Nat 180:70–82PubMedGoogle Scholar
  86. Rodríguez-Ruano SM, Martín-Vivaldi M, Martín-Platero AM, López-López JP, Peralta-Sánchez JM, Ruiz-Rodríguez M, Soler JJ, Valdivia E, Martínez-Bueno M (2015) The hoopoe’s uropygial gland hosts a bacterial community influenced by the living conditions of the bird. PLoS One 10:e0139734PubMedPubMedCentralGoogle Scholar
  87. Ruiz-Rodríguez M, Valdivia E, Soler JJ (2009) Symbiotic bacteria living in the hoopoe’s uropygial gland prevent feather degradation. J Exp Biol 212:3621–3626PubMedGoogle Scholar
  88. Saino N, Ferrari R, Romano M, Martinelli R, Møller AP (2003) Experimental manipulation of egg carotenoids affects immunity of barn swallow nestlings. Proc R Soc Lond B 270:2485–2489Google Scholar
  89. Saino N, Szep T, Ambrosini R, Romano M, Møller AP (2004) Ecological conditions during winter affect sexual selection and breeding in a migratory bird. Proc R Soc Lond B 271:681–686Google Scholar
  90. Schmid-Hempel P (2011) Evolutionary parasitology: the integrated study of infections, immunology, ecology and genetics. Oxford University Press, OxfordGoogle Scholar
  91. Shawkey MD, Pillai SR, Hill GE (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J Avian Biol 34:345–349Google Scholar
  92. Svensson L (1992) Identification guide to European passerines, 4th edn. Svensson, StockholmGoogle Scholar
  93. Tian R, Chen M, Chai S, Rong X, Chen B, Ren W, Xu S, Yang G (2018) Divergent selection of pattern recognition receptors in mammals with different ecological characteristics. J Mol Evol 86:138–149PubMedGoogle Scholar
  94. Turner AK (1994) The swallow. Hamlyn, LondonGoogle Scholar
  95. Turner AK, Rose C (1989) A handbook to the swallows and martins of the world. Christopher Helm, LondonGoogle Scholar
  96. Valkiūnas G (2005) Avian malaria parasites and other Haemosporidia. CRC Press, Boca RatonGoogle Scholar
  97. Vincze O, Vágási CI, Kovács I, Galván I, Pap PL (2013) Sources of variation in uropygial gland size in European birds. Biol J Linn Soc 110:543–563Google Scholar
  98. Wagner EC, Williams TD (2007) Experimental (antiestrogen-mediated) reduction in egg size negatively affects offspring growth and survival. Physiol Biochem Zool 80:293–305PubMedGoogle Scholar
  99. Wakelin D (1996) Immunity to parasites: how parasitic infections are controlled. Cambridge University Press, CambridgeGoogle Scholar
  100. Wegner KM, Reusch TBH, Kalbe M (2003) Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J Evol Biol 16:224–232PubMedGoogle Scholar
  101. Whittaker DJ, Gerlach NM, Soini HA, Novotny MV, Ketterson ED (2013) Bird odour predicts reproductive success. Anim Behav 86:697–703Google Scholar
  102. Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666Google Scholar

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Authors and Affiliations

  1. 1.Department of Anatomy, Cellular Biology and ZoologyUniversity of ExtremaduraBadajozSpain
  2. 2.Department of Zoology, Faculty of BiologyGreen BuildingSevilleSpain
  3. 3.Laboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079Université Paris-SudOrsay CedexFrance

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