Seasonal decline of offspring quality in the European starling Sturnus vulgaris: An immune challenge experiment

Behavioral Ecology and Sociobiology

Volumn 66, Issue 5, 2012, Pages 697-709

  Serra, Lorenzo ^a   Pirrello, Simone ^a,d   Caprioli, Manuela ^b   Griggio, Matteo ^c   Andreotti, Alessandro ^a   Romano, Andrea ^b   Pilastro, Andrea ^d   Saino, Nicola ^b   Sacchi, Roberto ^e   Galeotti, Paolo ^e   Fasola, Mauro ^e   Spina, Fernando ^a   Rubolini, Diego ^b  

^a INSTITUTE FOR ENVIRONMENTAL PROTECTION AND RESEARCH ISPRA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^d UNIVERSITY OF PADOVA   (Italy)

^e UNIVERSITY OF PAVIA   (Italy)

Author keywords

Antioxidants; Immune challenge; LPS; Oxidative stress; Seasonal variation; Sex biased investment

Indexed keywords

ANTIOXIDANT; BACTERIUM; EGG SIZE; ENVIRONMENTAL CHANGE; EXPERIMENTAL STUDY; FITNESS; GROWTH RESPONSE; IMMUNE RESPONSE; METABOLITE; PARENTAL INVESTMENT; PASSERINE; PHYSIOLOGICAL RESPONSE; RECRUITMENT (POPULATION DYNAMICS); REPRODUCTIVE POTENTIAL; SEASONAL VARIATION; SEXUAL DIMORPHISM; SURVIVAL; TOXIN;

AVES; BACTERIA (MICROORGANISMS); STURNUS VULGARIS;

EID: 84859732604     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-012-1318-3     Document Type: Article

References (98)

1. 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: 651-659.
2. Badyaev AV (2002) Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol Evol 17: 369-378.
3. Berthouly A, Cassier A, Richner H (2008) Carotenoid-induced maternal effects interact with ectoparasite burden and brood size to shape the trade-off between growth and immunity in nestling great tits. Funct Ecol 22: 854-863.
4. Bertrand S, Criscuolo F, Faivre B, Sorci G (2006) Immune activation increases susceptibility to oxidative tissue damage in Zebra Finches. Funct Ecol 20: 1022-1027.
5. Bhattacharyya J, Biswas S, Datta AG (2004) Mode of action of endotoxin: role of free radicals and antioxidants. Curr Med Chem 11: 359-368.
6. Bize P, Devevey G, Monaghan P, Doligez B, Christe P (2008) Fecundity and survival in relation to resistance to oxidative stress in a free-living bird. Ecology 89: 2584-2593.
7. Boncoraglio G, Martinelli R, Saino N (2008) Sex-related asymmetry in competitive ability of sexually monomorphic barn swallow nestlings. Behav Ecol Sociobiol 62: 729-738.
8. Bonisoli-Alquati A, Martinelli R, Rubolini D, Saino N (2008) Sex-specific effects of albumen removal and nest environment manipulation on barn swallow nestlings. Ecology 89: 2315-2324.
9. Bonisoli-Alquati A, Boncoraglio G, Caprioli M, Saino N (2011) Birth order, individual sex and sex of competitors determine the outcome of conflict among siblings over parental care. Proc R Soc B 278: 1273-1279.
10. Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, Sorci G (2003) Assessing the cost of mounting an immune response. Am Nat 161: 367-379.
11. Bourgeon S, Guindre-Parker S, Williams TD (2011) Effects of sibling competition on growth, oxidative stress, and humoral immunity: a two-year brood-size manipulation. Physiol Biochem Zool 84: 429-437.
12. Brinkhof MWG, Cavé AJ, Hage FJ, Verhulst S (1993) Timing of reproduction and fledging success in the Coot Fulica atra: evidence for a causal relationship. J Anim Ecol 62: 577-587.
13. Brinkhof MWG, Cave AJ, Perdeck AC (1997) The seasonal decline in the first-year survival of juvenile coots: an experimental approach. J Anim Ecol 66: 73-82.
14. Casagrande S, Dell'Omo G, Costantini D, Tagliavini J (2006) Genetic differences between early- and late-breeding Eurasian kestrels. Evol Ecol Res 8: 1029-1038.
15. Catoni C, Peters A, Martin Schaefer H (2008) Life history trade-offs are influenced by the diversity, availability and interactions of dietary antioxidants. Anim Behav 76: 1107-1119.
16. Chin EH, Love OP, Clark AM, Williams TD (2005) Brood size and environmental conditions sex-specifically affect nestling immune response in the European starlings Sturnus vulgaris. J Avian Biol 36: 549-554.
17. Christe P, de Lope F, Gonzalez G, Saino N, Møller AP (2001) The influence of environmental conditions on immune responses, morphology and recapture probability of nestling house martins (Delichon urbica). Oecologia 126: 333-338.
18. Clark AB, Wilson DS (1981) Avian breeding adaptations: hatching asynchrony, brood reduction, and nest failure. Q Rev Biol 56: 253-277.
19. Clutton-Brock TH (1988) Reproductive success. University of Chicago Press, Chicago.
20. Clutton-Brock TH, Albon SD, Guinness FE (1985) Parental investment and sex differences in juvenile mortality in birds and mammals. Nature 313: 131-133.
21. Cordero PJ, Vinuela J, Aparicio JM, Veiga JP (2001) Seasonal variation in sex ratio and sexual egg dimorphism favouring daughters in first clutches of the spotless starling. J Evol Biol 14: 829-834.
22. Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11: 1238-1251.
23. Costantini D, Dell'Omo G (2006a) Environmental and genetic components of oxidative stress in wild kestrel nestlings (Falco tinnunculus). J Comp Physiol B 176: 575-579.
24. Costantini D, Dell'Omo G (2006b) Effects of T-cell-mediated immune response on avian oxidative stress. Comp Biochem Physiol A 145: 137-142.
25. Costantini D, Møller AP (2009) Does immune response cause oxidative stress in birds? A meta-analysis. Comp Biochem Physiol A 153: 339-344.
26. Costantini D, Carello L, Fanfani A (2010) Relationships among oxidative status, breeding conditions and life-history traits in free-living Great Tits Parus major and Common Starlings Sturnus vulgaris. Ibis 152: 793-802.
27. Cotton PA, Wright J, Kacelnik A (1999) Chick begging strategies in relation to brood hierarchies and hatching asynchrony. Am Nat 153: 412-420.
28. Cramp S (1998) The complete birds of the western Palearctic on CD-ROM. Oxford University Press, Oxford.
29. Crick HQP, Gibbons DW, Magrath RD (1993) Seasonal changes in clutch size in British birds. J Anim Ecol 62: 263-273.
30. Dubiec A, Cichoñ M (2001) Seasonal decline in health status of Great Tit (Parus major) nestlings. Can J Zool 79: 1829-1833.
31. Fair J, Whitaker S, Pearson B (2007) Sources of variation in haematocrit in birds. Ibis 149: 535-552.
32. Feare CJ, Burham SE (1978) Lack of nest site tenacity and mate fidelity in the starling. Bird Study 25: 189-191.
33. Griffiths R (1992) Sex-biased mortality in the lesser black-backed gull Larus fuscus during the nestling stage. Ibis 134: 237-244.
34. Griffiths R, Double MC, Orr K, Dawson RJ (1998) A DNA test to sex most birds. Mol Ecol 7: 1071-1075.
35. Grindstaff JL (2008) Maternal antibodies reduce costs of an immune response during development. J Exp Biol 211: 654-660.
36. Grindstaff JL, Hasselquist D, Nilsson JK, Sandell M, Smith HG, Stjernman M (2006) Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity. Proc R Soc B 273: 2551-2557.
37. Grüebler MU, Naef-Daenzer B (2008) Fitness consequences of pre- and post-fledging timing decisions in a double-brooded passerine. Ecology 89: 2736-2745.
38. Grüebler MU, Naef-Daenzer B (2010) Fitness consequences of timing of breeding in birds: date effects in the course of a reproductive episode. J Avian Biol 41: 282-291.
39. Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. Oxford University Press, Oxford.
40. Hendry AP, Day T (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol 14: 901-916.
41. Hochachka W (1990) Seasonal decline in reproductive performance of song sparrows. Ecology 71: 1279-1288.
42. Hochachka W, Smith JNM (1991) Determinants and consequences of nestling condition in song sparrows. J Anim Ecol 60: 995-1008.
43. Horak P, Zilmer M, Saks L, Ots I, Karu U, Zilmer K (2006) Antioxidant protection, carotenoids and the costs of immune challenge in greenfinches. J Exp Biol 209: 4329-4338.
44. Iwasa Y, Levin SA (1995) The timing of life history events. J Theor Biol 172: 33-42.
45. Janeway CA, Travers P (1999) Immunobiology: the immune system in health and disease, 4th edn. Current Biology, London.
46. Klomp H (1970) The determination of clutch size in birds. Ardea 58: 1-124.
47. Krist M (2011) Egg size and offspring quality: a meta-analysis in birds. Biol Rev 86: 692-716.
48. Lack D (1947) The significance of clutch size. Ibis 89: 302-352.
49. Lack D (1954) The natural regulation of animal numbers. Clarendon, Oxford.
50. Lee KA, Martin LB II, Wikelski MC (2005) Responding to inflammatory challenges is less costly for a successful avian invader, the house sparrow (Passer domesticus), than its less-invasive congener. Oecologia 145: 244-251.
51. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models, 2nd edn. SAS, Cary.
52. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88: 87-98.
53. López-Rull I, Salaberria C, Gil D (2010) Seasonal decline in egg size and yolk androgen concentration in a double brooded passerine. Ardeola 57: 321-332.
54. López-Rull I, Celis P, Salaberria C, Puerta M, Gil D (2011) Post-fledging recruitment in relation to nestling plasma testosterone and immunocompetence in the spotless starling. Funct Ecol 25: 500-508.
55. Magrath RD (1991) Nestling weight and juvenile survival in the blackbird, Turdus merula. J Anim Ecol 60: 335-351.
56. Mainwaring M, Dickens M, Hartley IR (2010) Sexual dimorphism and growth trade-offs in Blue Tit Cyanistes caeruleus nestlings. Ibis 153: 175-179.
57. Merino S, Potti J (1998) Growth, nutrition, and blowfly parasitism in nestling pied flycatchers. Can J Zool 76: 936-941.
58. Merino S, Møller AP, de Lope F (2000) Seasonal changes in cell-mediated immunocompetence and mass gain in nestling barn swallows: a parasite-mediated effect? Oikos 90: 327-332.
59. Møller AP (2002) North Atlantic Oscillation (NAO) effects of climate on the relative importance of first and second clutches in a migratory passerine bird. J Anim Ecol 71: 201-210.
60. 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.
61. Møller AP, Saino N (2004) Immune response and survival. Oikos 104: 299-304.
62. Møller AP, de Lope F, Saino N (2004) Parasitism, immunity, and arrival date in a migratory bird, the barn swallow. Ecology 85: 206-219.
63. Møller AP, Arriero E, Lobato E, Merino S (2009) A meta-analysis of parasite virulence in nestling birds. Biol Rev 84: 567-588.
64. Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12: 75-92.
65. Moreno J, Merino S, Sanz JJ, Arriero E, Morales J, Tomas G (2005) Nestling cell-mediated immune response, body mass and hatching date as predictors of local recruitment in the pied flycatcher Ficedula hypoleuca. J Avian Biol 36: 251-260.
66. Morishita TY, Aye PP, Ley EC, Harr BS (1999) Survey of pathogens and blood parasites in free-living passerines. Avian Dis 43: 549-552.
67. Naef-Daenzer B, Widmer F, Nuber M (2001) Differential post-fledging survival of great and coal tits in relation to their condition and fledging date. J Anim Ecol 70: 730-738.
68. Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11: 19-26.
69. Norte AC, Sheldon BC, Sousa JP, Ramos JA (2009) Environmental and genetic variation in body condition and blood profile of great tit Parus major nestlings. J Avian Biol 40: 157-165.
70. Oddie KR (2000) Size matters: competition between male and female great tit offspring. J Anim Ecol 69: 903-912.
71. Owen-Ashley NT, Wingfield JC (2007) Acute phase responses of passerine birds: characterization and seasonal variation. J Ornithol 148: 583-591.
72. Owen-Ashley NT, Turner M, Hahn TP, Wingfield JC (2006) Hormonal, behavioral, and thermoregulatory responses to bacterial lipopolysaccharide in captive and free-living white-crowned sparrows (Zonotrichia leucophrys gambelii). Horm Behav 49: 15-29.
73. Parsons J (1975) Seasonal variation in the breeding success of the herring gull: an experimental approach to pre-fledging success. J Anim Ecol 44: 553-573.
74. Perrins CM (1970) The timing of birds' breeding seasons. Ibis 112: 242-255.
75. 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.
76. Potti J, Moreno J, Merino S, Frias O, Rodriguez R (1999) Environmental and genetic variation in the haematocrit of fledgling pied flycatchers Ficedula hypoleuca. Oecologia 120: 1-8.
77. Price K, Ydenberg RC (1995) Begging and provisioning in broods of asynchronously-hatched yellow-headed blackbird nestlings. Behav Ecol Sociobiol 37: 201-208.
78. Råberg L, Stjernman M, Nilsson J-Å (2005) Sex and environmental sensitivity in blue tit nestlings. Oecologia 145: 496-503.
79. Richner H, Oppliger A, Christe P (1993) Effect of ectoparasites on reproduction in great tits. J Anim Ecol 62: 703-710.
80. 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.
81. Rowe L, Ludwig D, Schluter D (1994) Condition, and the seasonal decline of avian clutch size. Am Nat 143: 698-722.
82. Rubolini D, Romano M, Bonisoli-Alquati A, Saino N (2006) Early maternal, genetic and environmental components of antioxidant protection, morphology and immunity of yellow-legged gull (Larus michahellis) chicks. J Evol Biol 19: 1571-1584.
83. Saino N, Calza S, Møller AP (1997) Immunocompetence of nestling barn swallows in relation to brood size and parental effort. J Anim Ecol 66: 827-836.
84. Saino N, Caprioli M, Romano M, Boncoraglio G, Rubolini D, Ambrosini R, Bonisoli-Alquati A, Romano A (2011) Antioxidant defenses predict long-term survival in a passerine bird. PLoS One 6: e19593.
85. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11: 317-321.
86. Simon A, Thomas DW, Bourgault P, Blondel J, Perret P, Lambrechts MM (2005) Between-population differences in nestling size and hematocrit level in blue tits (Parus caeruleus): a cross-fostering test for genetic and environmental effects. Can J Zool 83: 694-701.
87. Slagsvold T, Sandvik J, Rofstad G, Lorentsen Ö, Husby M (1984) On the adaptive value of intraclutch egg size variation in birds. Auk 101: 685-697.
88. Slagsvold T, Amundsen T, Dale S (1995) Costs and benefits of hatching asynchrony in Blue Tits Parus caeruleus. J Anim Ecol 64: 563-578.
89. Sorci G, Soler JJ, Møller AP (1997) Reduced immunocompetence of nestlings in replacement clutches of the European magpie (Pica pica). Proc R Soc B 264: 1593-1598.
90. Soszynski D, Krajewska M (2002) Time-course of changes in plasma nitric oxide following lipopolysaccharide and turpentine injection in rats. J Therm Biol 27: 387-391.
91. Uller T (2006) Sex-specific sibling interactions and offspring fitness in vertebrates: patterns and implications for maternal sex ratios. Biol Rev 81: 207-217.
92. Verboven N, Verhulst S (1996) Seasonal variation in the incidence of double broods: the date hypothesis fits better than the quality hypothesis. J Anim Ecol 65: 264-273.
93. Verboven N, Visser ME (1998) Seasonal variation in local recruitment of great tits: the importance of being early. Oikos 81: 511-524.
94. Verhulst S, Nilsson JÅ (2008) The timing of birds' breeding seasons: a review of experiments that manipulated timing of breeding. Phil Trans R Soc Lond B 363: 399-410.
95. Whittingham MJ, Stephens PA, Bradbury RB, Freckleton RP (2006) Why do we still use stepwise modelling in ecology and behaviour? J Anim Ecol 75: 1182-1189.
96. Wilk T, Dubiec A, Cichoń M (2006) Seasonal decline in cell-mediated immunity of collared flycatcher Ficedula albicollis nestlings: does the sex of offspring matter? J Ornithol 148: 199-205.
97. Williams TD (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev 68: 35-59.
98. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York.