Assessing the cost of helping: The roles of body condition and oxidative balance in the seychelles warbler (acrocephalus sechellensis)

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  van de Crommenacker, Janske ^a   Komdeur, Jan ^a   Richardson, David S ^b,c  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^c NATURE SEYCHELLES   (Seychelles)

Author keywords

[No Author keywords available]

Indexed keywords

REACTIVE OXYGEN METABOLITE;

AEROBIC METABOLISM; ARTICLE; BIRD; BODY CONSTITUTION; BREEDING; CONTROLLED STUDY; COOPERATION; EGG LAYING; FEMALE; MALE; NESTING; NONHUMAN; OXIDATIVE STRESS; REARING; REPRODUCTION; SEYCHELLES WARBLER; SOCIAL STATUS; ANIMAL; METABOLISM; PHYSIOLOGY; SONGBIRD;

ACROCEPHALUS SECHELLENSIS; AVES;

ANIMALS; BREEDING; COOPERATIVE BEHAVIOR; FEMALE; HELPING BEHAVIOR; MALE; NESTING BEHAVIOR; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; REPRODUCTION; SONGBIRDS;

EID: 80055033754     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026423     Document Type: Article

References (135)

1. Brown JL, (1987) Helping and communal breeding in birds. Princeton, NJ Princeton University Press.
2. Taborsky M, (1994) Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction. Adv Stud Behav 23: 1-100.
3. Emlen ST, Wrege PH, (1988) The role of kinship in helping decisions among white-fronted bee-eaters. Behav Ecol Sociobiol 23: 305-315.
4. Jennions MD, Macdonald DW, (1994) Cooperative breeding in mammals. Trends Ecol Evol 9: 89-93.
5. Gaston AJ, (1987) The evolution of group territorial behavior and cooperative breeding. Am Nat 112: 1091-1100.
6. Reyer HU, (1984) Investment and relatedness: a cost/benefit analysis of breeding and helping in the pied kingfisher (Ceryle rudis). Anim Behav 32: 1163-1178.
7. Kokko H, Johnstone RA, Clutton-Brock TH, (2001) The evolution of cooperative breeding through group augmentation. P Roy Soc B- Biol Sci 268: 187-196.
8. Clutton-Brock T, (2002) Breeding Together: kin selection and mutualism in cooperative vertebrates. Science 296: 69-72.
9. Richardson DS, Burke T, Komdeur J, (2002) Direct benefits and the evolution of female-biased cooperative breeding in Seychelles warblers. Evolution 56: 2313-2321.
10. Vehrencamp SL, Quinn JS, (2004) Joint laying systems. In: Koenig WD, Dickinson JL, editors. Ecology and Evolution of Cooperative Breeding in Birds 177-197 Cambridge Cambridge University Press In:.
11. Komdeur J, (1996) Influence of age on reproductive performance in the Seychelles warbler. Behav Ecol 7: 417-425.
12. Emlen ST, (1990) White-fronted bee-eaters: helping in a colonially nesting species. In: Stacey PB, koenig WB, editors. Cooperative breeding in birds: long-term studies of ecology and behavior 487-526 Cambridge Cambridge University Press.
13. Arnold KE, Owens IPF, (1998) Cooperative breeding in birds: a comparative test of the life history hypothesis. P Roy Soc B- Biol Sci 265: 739-745.
14. Richardson DS, Burke T, Komdeur J, (2003) Sex-specific associative learning cues and inclusive fitness benefits in the Seychelles warbler. J Evol Biol 16: 854-861.
15. Richardson DS, Komdeur J, Burke T, (2003) Animal behaviour: Altruism and infidelity among warblers. Nature 422: 580.
16. Reyer HU, (1980) Flexible helper structure as an ecological adaptation in the pied kingfisher (Ceryle rudis rudis L.). Behav Ecol Sociobiol 6: 219-227.
17. Heinsohn RG, (1992) Cooperative enhancement of reproductive success in white-winged choughs. Evol Ecol 6: 97-114.
18. Mumme RL, (1992) Do helpers increase reproductive success? Behav Ecol Sociobiol. 31: 319-328.
19. Austad SN, Rabenold KN, (1985) Reproductive enhancement by helpers and an experimental inquiry into its mechanism in the bicolored wren. Behav Ecol Sociobiol 17: 19-27.
20. Crick HQP, (1992) Load-lightening in cooperatively breeding birds and the cost of reproduction. Ibis 134: 56-61.
21. Cockburn A, Sims RA, Osmond HL, Green DJ, Double MC, et al. (2008) Can we measure the benefits of help in cooperatively breeding birds: the case of superb fairy-wrens Malurus cyaneus? J Anim Ecol 77: 430-438.
22. Russell AF, Brotherton PNM, McIlrath GM, Sharpe LL, Clutton-Brock TH, (2003) Breeding success in cooperative meerkats: effects of helper number and maternal state. Behav Ecol 14: 486-492.
23. Emlen ST, (1991) Evolution of cooperative breeding in birds and mammals. In: Behavioural ecology: an evolutionary approach. Oxford: Blackwell Scientific, 301-337.
24. Cockburn A, (1998) Evolution of helping behavior in cooperatively breeding birds. Annu Rev Ecol Syst 29: 141-177.
25. Heinsohn R, Legge S, (1999) The cost of helping. Trends Ecol Evol 14: 53-57.
26. Rabenold KN, (1990) Campylorhynchus wrens: the ecology of delayed dispersal and cooperation in the Venezuelan savanna. In: Stacey PB, Koenig WD, editors. Cooperative breeding in birds 157-196 Cambridge Cambridge University Press.
27. Clutton-Brock TH, (1991) The evolution of parental care. Princeton, NJ Princeton University Press.
28. Russell AF, Sharpe LL, Brotherton PNM, Clutton-Brock TH, (2003) Cost minimization by helpers in cooperative vertebrates. Proc Natl Acad Sci U S A 100: 3333-3338.
29. Taborsky M, (1984) Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits. Anim Behav 32: 1236-1252.
30. Buston P, (2003) Social hierarchies: size and growth modification in clownfish. Nature 424: 145-146.
31. Walling CA, Royle NJ, Metcalfe NB, Lindström J, (2007) Green swordtails alter their age at maturation in response to the population level of male ornamentation. Biol Lett 3: 144-146.
32. Schoech SJ, Mumme RL, Moore MC, (1991) Reproductive endocrinology and mechanisms of breeding inhibition in cooperatively breeding Florida scrub jays (Aphelocoma c. coerulescens). Condor 93: 354-364.
33. Creel S, (2001) Social dominance and stress hormones. Trends Ecol Evol 16: 491-497.
34. Young AJ, Carlson AA, Monfort SL, Russell AF, Bennett NC, et al. (2006) Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proc Natl Acad Sci U S A 103: 12005-12010.
35. Brown JL, Brown ER, Brown SD, (1982) Morphological variation in a population of grey-crowned babblers: Correlations with variables affecting social behavior. Behav Ecol Sociobiol. 10: 281-287.
36. Arnold W, (1990) The evolution of marmot sociality: costs and benefits of joint hibernation. Behav Ecol Sociobiol 27: 239-246.
37. Heinsohn R, Cockburn A, (1994) Helping is costly to young birds in cooperatively breeding white-winged choughs. P Roy Soc B- Biol Sci 256: 293-298.
38. Clutton-Brock TH, Gaynor D, Kansky R, MacColl AD, McIlrath G, et al. (1998) Costs of cooperative behaviour in suricates (Suricata suricatta). Proc Biol Sci 265: 185-190.
39. Taborsky M, Grantner A, (1998) Behavioural time-energy budgets of cooperatively breeding Neolamprologus pulcher (Pisces: Cichlidae). Anim Behav 56: 1375-1382.
40. Eden SF, (1987) When do helpers help? Food availability and helping in the moorhen, Gallinula chloropus. Behav Ecol Sociobiol 21: 191-195.
41. Clutton-Brock TH, Brotherton PN, O'Riain MJ, Griffin AS, Gaynor D, et al. (2000) Individual contributions to babysitting in a cooperative mongoose, Suricata suricatta. Proc Biol Sci 267: 301-305.
42. Meade J, Hatchwell BJ, (2010) No direct fitness benefits of helping in a cooperative breeder despite higher survival of helpers. Behav Ecol 21: 1186-1194.
43. Harman D, (1956) Aging: A theory based on free radical and radiation chemistry. J Gerontol 11: 298-300.
44. Sohal RS, Weindruch R, (1987) Oxidative stress, caloric restriction, and aging. Nature 327: 725.
45. Speakman JR, Selman C, McLaren JS, Harper EJ, (2002) Living fast, dying when? The link between aging and energetics. J Nutr 132: 1583S-1597S.
46. Hulbert AJ, Pamplona R, Buffenstein R, Buttemer WA, (2007) Life and death: metabolic rate, membrane composition, and life span of animals. Physiol Rev 87: 1175-1213.
47. von Zglinicki T, (2002) Oxidative stress shortens telomeres. Trends Biochem Sci 27: 339-344.
48. Richter T, von Zglinicki T, (2007) A continuous correlation between oxidative stress and telomere shortening in fibroblasts. Exp Gerontol 42: 1039-1042.
49. 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.
50. Leeuwenburgh C, Heinecke JW, (2001) Oxidative stress and antioxidants in exercise. Curr Med Chem 8: 829-838.
51. Finkel T, Holbrook NJ, (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408: 239-247.
52. Barja G, (2007) Mitochondrial oxygen consumption and reactive oxygen species production are independently modulated: implications for aging studies. Rejuv Res 10: 215-224.
53. Beckman KB, Ames BN, (1998) The free radical theory of aging matures. Physiol Rev 78: 547-581.
54. Ozawa T, (1999) Understanding the process of aging. New York Marcel Dekker.
55. Halliwell B, Gutteridge JMC, (1999) Free radicals in biology and medicine. Oxford Oxford University Press.
56. Ames BN, Shingenaga MK, Park EM, (1991) DNA damage by endogenous oxidants as a cause of ageing and cancer. In: Davies KJA, editors. Oxidation Damage and Repair: Chemical, Biological, and Medical Aspects 181-187 New York Pergamon, Elmstad.
57. Krinsky NI, Yeum KJ, (2003) Carotenoid-radical interactions. Biochem Bioph Res Co 305: 754-760.
58. Costantini D, Verhulst S, (2009) Does high antioxidant capacity indicate low oxidative stress? Funct Ecol 23: 506-509.
59. Deerenberg C, Pen I, Dijkstra C, Arkies BJ, Visser GH, et al. (1995) Parental energy expenditure in relation to manipulated brood size in the European kestrel. Zool Ana Compl Syst 99: 38-47.
60. Moreno J, Cowie RJ, Sanz JJ, Williams RSR, (1995) Differential response by males and females to brood manipulations in the pied flycatcher: energy expenditure and nestling diet. J Anim Ecol 64: 721-732.
61. Verhulst S, Tinbergen JM, (1997) Clutch size and parental effort in the great tit Parus major. Ardea 85: 111-126.
62. Wiersma P, Selman C, Speakman JR, Verhulst S, (2004) Birds sacrifice oxidative protection for reproduction. P Roy Soc B- Biol Sci 271: 360-363.
63. Loft S, Astrup A, Buemann B, Poulsen HE, (1994) Oxidative DNA damage correlates with oxygen consumption in humans. FASEB J 8: 534-537.
64. Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, et al. (2004) Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol Lett 7: 363-368.
65. Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, et al. (2006) An experimental manipulation of life-history trajectories and resistance to oxidative stress. Evolution 60: 1913-1924.
66. Stearns SC, (1992) The evolution of life histories. Oxford Oxford University Press.
67. Sapolsky RM, (2004) Social status and health in humans and other animals. Ann Rev Anthropol 33: 393-418.
68. Sapolsky RM, (2005) The influence of social hierarchy on primate health. Science 308: 648-652.
69. Salmon AB, Marx DB, Harshman LG, (2001) A cost of reproduction in Drosophila melanogaster: stress susceptibility. Evolution 55: 1600-1608.
70. Bertrand S, Alonso-Alvarez C, Devevey G, Faivre B, Prost J, et al. (2006) Carotenoids modulate the trade-off between egg production and resistance to oxidative stress in zebra finches. Oecologia 147: 576-584.
71. Alonso-Alvarez C, Pérez-Rodríguez L, García JT, Viñuela J, Mateo R, (2010) Age and breeding effort as sources of individual variability in oxidative stress markers in a bird species. Physiol Biochem Zool 83: 110-118.
72. Metcalfe NB, Alonso-Alvarez C, (2010) Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct Ecol 24: 984-996.
73. Richardson DS, Jury FL, Blaakmeer K, Komdeur J, Burke T, (2001) Parentage assignment and extra-group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis). Mol Ecol 10: 2263-2273.
74. Komdeur J, Richardson DS, (2007) Molecular ecology reveals the hidden complexities of the Seychelles warbler. Adv Stud Behav 37: 147-187.
75. Brouwer L, Barr I, van de Pol M, Burke T, Komdeur J, et al. (2010) MHC-dependent survival in a wild population: evidence for hidden genetic benefits gained through extra-pair fertilizations. Mol Ecol 19: 3444-3455.
76. Komdeur J, (1994) The effect of kinship on helping in the cooperative breeding Seychelles warbler (Acrocephalus sechellensis). P Roy Soc B- Biol Sci 256: 47-52.
77. Komdeur J, (1998) Long-term fitness benefits of egg sex modification by the Seychelles warbler. Ecol Lett 1: 56-62.
78. Komdeur J, (1991) Cooperative breeding in the Seychelles warbler. PhD Thesis Cambridge University, Cambridge.
79. Komdeur J, (1996) Seasonal timing of reproduction in a tropical bird, the Seychelles warbler: A field experiment using translocation. J Biol Rhythms 11: 333-346.
80. Komdeur J, (1992) Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler. Nature 358: 493-495.
81. Komdeur J, (1997) Inter-island transfers and population dynamics of Seychelles warblers, Acrocephalus sechellensis. Bird Cons Intl 7: 7-26.
82. Brouwer L, Tinbergen JM, Both C, Bristol R, Richardson DS, et al. (2009) Experimental evidence for density-dependent reproduction in a cooperatively breeding passerine. Ecology 90: 729-741.
83. van de Crommenacker J, Komdeur J, Burke T, Richardson DS, (2011) Spatio-temporal variation in territory quality and oxidative status: a natural experiment in the Seychelles warbler (Acrocephalus sechellensis). J Anim Ecol 80: 668-680.
84. Griffiths R, Double MC, Orr K, Dawson RJG, (1998) A DNA test to sex most birds. Mol Ecol 7: 1071-1075.
85. Trevisan M, Browne R, Ram M, Muti P, Freudenheim J, et al. (2001) Correlates of markers of oxidative status in the general population. Am J Epidemiol 154: 348-356.
86. Alberti A, Bolognini L, Macciantelli D, Caratelli M, (2000) The radical cation of N,N-diethyl-para-phenylendiamine: A possible indicator of oxidative stress in biological samples. Res Chem Intermed 26: 253-267.
87. Iamele L, Fiocchi R, Vernocchi A, (2002) Evaluation of an automated spectrophotometric assay for reactive oxygen metabolites in serum. Clin Chem Lab Med 40: 673-676.
88. Costantini D, Dell'Omo G, (2006) Effects of T-cell-mediated immune response on avian oxidative stress. Comp Biochem Phys A 145: 137-142.
89. Rasbash J, Steele F, Browne W, Prosser B, (2004) A user's guide to MLwiN version 2.0. London Institute of Education.
90. Brouwer L, Groothuis TGG, Vedder O, Eikenaar C, Richardson DS, et al. (2009) Do primary males physiologically suppress subordinate males? An experiment in a cooperatively breeding passerine. Ethology 115: 576-587.
91. Green AJ, (2001) Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82: 1473-1483.
92. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57: 289-300.
93. Costantini D, Carere C, Caramaschi D, Koolhaas JM, (2008) Aggressive and non-aggressive personalities differ in oxidative status in selected lines of mice (Mus musculus). Biol Lett 4: 119-122.
94. Cullen NJ, Heinsohn R, Cockburn A, (1996) Food supplementation induces provisioning of young in cooperatively breeding white-winged choughs. J Avian Biol 27: 92-94.
95. Chase ID, (1980) Cooperative and noncooperative behavior in animals. Am Nat 115: 827-857.
96. Komdeur J, (1994) Experimental evidence for helping and hindering by previous offspring in the cooperative-breeding Seychelles warbler Acrocephalus sechellensis. Behav Ecol Sociobiol 34: 175-186.
97. Komdeur J, Kats RKH, (1999) Predation risk affects trade-off between nest guarding and foraging in Seychelles warblers. Behav Ecol 10: 648-658.
98. Piper WH, Wiley RH, (1990) The relationship between social dominance, subcutaneous fat, and annual survival in wintering white-throated sparrows (Zonotrichia albicollis). Behav Ecol Sociobiol 26: 201-208.
99. Creel SR, Creel NM, (1991) Energetics, reproductive suppression and obligate communal breeding in carnivores. Behav Ecol Sociobiol 28: 263-270.
100. Clutton-Brock TH, Hodge SJ, Spong G, Russell AF, Jordan NR, et al. (2006) Intrasexual competition and sexual selection in cooperative mammals. Nature 444: 1065-1068.
101. Lack DL, (1968) Ecological adaptations for breeding in birds. London Methuen.
102. Daan S, Masman D, Groenewold A, (1990) Avian basal metabolic rates: their association with body composition and energy expenditure in nature. Am J Physiol- Reg Integr Comp Physiol 259: R333-R340.
103. Conway CJ, Martin TE, (2000) Evolution of passerine incubation behavior: influence of food, temperature, and nest predation. Evolution 54: 670-685.
104. Moreno J, (1989) Strategies of mass change in breeding birds. Biol J Linn Soc 37: 297-310.
105. Witter MS, Cuthill IC, (1993) The ecological costs of avian fat storage. Phil Trans Biol Sci 340: 73-92.
106. Houston DC, (1997) Nutritional constraints on egg production in birds. P Nutr Soc 56: 1057-1065.
107. Nilsson J-Å, Råberg L, (2001) The resting metabolic cost of egg laying and nestling feeding in great tits. Oecologia 128: 187-192.
108. Navara KJ, Badyaev AV, Mendonça MT, Hill GE, (2006) Yolk antioxidants vary with male attractiveness and female condition in the house finch (Carpodacus mexicanus). Physiol Biochem Zool 79: 1098-1105.
109. Silverin B, (1980) Seasonal development of reproductive organs in the female pied flycatcher Ficedula hypoleuca and experimental studies on duration of her re-nesting ability. J Zool 190: 241-257.
110. Freed LA, (1981) Loss of mass in breeding wrens: stress or adaptation? Ecology 62: 1179-1186.
111. Richardson DS, Burke T, Komdeur J, Wedell N, (2007) Grandparent helpers: the adaptive significance of older, postdominant helpers in the Seychelles warbler. Evolution 61: 2790-2800.
112. Wingfield JC, Moore MC, (1987) Hormonal, social, and environmental factors in the reproductive biology of free-living male birds. In: D Krews, editor. Psychobiology of reproductive behavior: an evolutionary perspective. New Jersey, Prentice Hall, 149-175.
113. van de Crommenacker J, Richardson DS, Groothuis TGG, Eising CM, Dekker L, et al. (2004) Testosterone, cuckoldry risk and extra-pair opportunities in the Seychelles warbler. P Roy Soc B- Biol Sci 271: 1023-1031.
114. Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G, (2007) Testosterone and oxidative stress: the oxidation handicap hypothesis. P Roy Soc B- Biol Sci 274: 819-825.
115. Ji LL, (1999) Antioxidants and oxidative stress in exercise. Exp Biol Med 222: 283-292.
116. Brand MD, (2000) Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp Gerontol 35: 811-820.
117. Selman C, McLaren JS, Collins AR, Duthie GG, Speakman JR, (2002) Antioxidant enzyme activities, lipid peroxidation, and DNA oxidative damage: the effects of short-term voluntary wheel running. Arch Biochem Biophys 401: 255-261.
118. Speakman JR, Talbot DA, Selman C, Snart S, McLaren JS, et al. (2004) Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3: 87-95.
119. Criscuolo F, Gonzalez-Barroso MM, Bouillaud F, Ricquier D, Miroux B, et al. (2005) Mitochondrial uncoupling proteins: new perspectives for evolutionary ecologists. Am Nat 166: 686-699.
120. Robinson MK, Rustum RR, Chambers EA, Rounds JD, Wilmore DW, et al. (1997) Starvation enhances hepatic free radical release following endotoxemia. J Surg Res 69: 325-330.
121. Morales AE, Pérez-Jiménez A, Hidalgo MC, Abellán E, Cardenete G, (2004) Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver. Comp Biochem Phys C 139: 153-161.
122. Møller P, Wallin H, Knudsen LE, (1996) Oxidative stress associated with exercise, psychological stress and life-style factors. Chem-Biol Interact 102: 17-36.
123. Senar JC, Polo V, Uribe F, Camerino M, (2000) Status signalling, metabolic rate and body mass in the siskin: the cost of being a subordinate. Anim Behav59: 103-110.
124. Mulder RA, Langmore NE, (1993) Dominant males punish helpers for temporary defection in superb fairy-wrens. Anim Behav 45: 830-833.
125. Balshine-Earn S, Neat FC, Reid H, Taborsky M, (1998) Paying to stay or paying to breed? Field evidence for direct benefits of helping behavior in a cooperatively breeding fish. Behav Ecol 9: 432-458.
126. Lin H, Decuypere E, Buyse J, (2004) Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus): 2. Short-term effect. Comp Biochem Phys B 139: 745-751.
127. Lin H, Decuypere E, Buyse J, (2004) Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus): 1. Chronic exposure. Comp Biochem Phys B 139: 737-744.
128. Costantini D, Fanfani A, Dell'Omo G, (2008) Effects of corticosteroids on oxidative damage and circulating carotenoids in captive adult kestrels (Falco tinnunculus). J Comp Phys B 178: 829-835.
129. Surai PF, (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham Nottingham University Press.
130. Blount JD, Houston DC, Møller AP, (2000) Why egg yolk is yellow. Trends Ecol Evol 15: 47-49.
131. 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 Evolution Biol 19: 1571-1584.
132. Blount JD, Surai PF, Houston DC, Møller AP, (2002) Patterns of yolk enrichment with dietary carotenoids in gulls: the roles of pigment acquisition and utilization. Funct Ecol 16: 445-453.
133. Blount JD, Surai PF, Nager RG, Houston DC, Møller AP, et al. (2002) Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. P Roy Soc B- Biol Sci 269: 29-36.
134. Costantini D, (2010) Complex trade-offs in the pigeon (Columba livia): egg antioxidant capacity and female serum oxidative status in relation to diet quality. J Comp Physiol B 180: 731-739.
135. Surai PF, Speake BK, Sparks NHC, (2001) Carotenoids in avian nutrition and embryonic development. 2. Antioxidant properties and discrimination in embryonic tissues. J Poult Sci 38: 117-145.