Assessing the Cost of Helping: The Roles of Body Condition and Oxidative Balance in the Seychelles Warbler (Acrocephalus sechellensis)

In cooperatively breeding species, helping close relatives may provide important fitness benefits. However, helping can be energetically expensive and may result in increased generation of reactive oxygen species. Consequently, an oxidant/antioxidant imbalance can lead to higher oxidative stress susceptibility. Given the potential costs of helping, it may be that only individuals with a sufficiently good body condition and/or stable oxidative balance can afford to help. Knowledge about relationships between social status and oxidative balance in cooperatively breeding systems is still limited. Studying these relationships is important for understanding the costs of helping and physiological pressures of reproduction. Here we evaluate the relationship between helping behaviour, body condition and oxidative balance in a wild population of the cooperatively breeding Seychelles warbler (Acrocephalus sechellensis). In this species, some subordinate individuals help dominant birds with the rearing of young, while others refrain from any assistance. We assessed body condition and oxidative parameters of birds of different social status caught during different breeding stages. We found that, prior to breeding, female subordinates that did not subsequently help (non-helpers) had significantly lower body condition and higher ROMs (reactive oxygen metabolites) than helpers and dominants. During the later stages of breeding, body condition was low in dominants and helpers, but high in non-helpers. Differences in oxidative balance between individuals of different social status were found only during nest care: Dominant males occupied with guarding behaviours tended to have relatively high oxidative stress susceptibility. Furthermore, dominant and helper females showed elevated antioxidant capacity (measured as OXY) in the weeks just prior to egg-laying, possibly representing a change in their reproductive physiology. The results imply that an individuals' oxidative balance may be influenced by factors related to reproduction, which can differ with sex and—within cooperative breeding systems—social status.

[1]  T. Burke,et al.  Spatio-temporal variation in territory quality and oxidative status: a natural experiment in the Seychelles warbler (Acrocephalus sechellensis) , 2011, The Journal of animal ecology.

[2]  J. Meade,et al.  No direct fitness benefits of helping in a cooperative breeder despite higher survival of helpers , 2010 .

[3]  Neil B. Metcalfe,et al.  Oxidative stress as a life‐history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death , 2010 .

[4]  T. Burke,et al.  MHC‐dependent survival in a wild population: evidence for hidden genetic benefits gained through extra‐pair fertilizations , 2010, Molecular ecology.

[5]  B. Silverin Seasonal development of reproductive organs in the female Pied flycatcher Ficedula hypoleuca and experimental studies on duration of her re-nesting ability , 2010 .

[6]  D. Costantini Complex trade-offs in the pigeon (Columba livia): egg antioxidant capacity and female serum oxidative status in relation to diet quality , 2010, Journal of Comparative Physiology B.

[7]  R. Mateo,et al.  Age and Breeding Effort as Sources of Individual Variability in Oxidative Stress Markers in a Bird Species , 2009, Physiological and Biochemical Zoology.

[8]  S. Verhulst,et al.  Does high antioxidant capacity indicate low oxidative stress , 2009 .

[9]  T. Groothuis,et al.  Do Primary Males Physiologically Suppress Subordinate Males? An Experiment in a Cooperatively Breeding Passerine , 2009 .

[10]  C. Both,et al.  Experimental evidence for density-dependent reproduction in a cooperatively breeding passerine. , 2009, Ecology.

[11]  H. Crick Load‐lightening in cooperatively breeding birds and the cost of reproduction , 2008 .

[12]  R. Mulder,et al.  Can we measure the benefits of help in cooperatively breeding birds: the case of superb fairy-wrens Malurus cyaneus? , 2008, The Journal of animal ecology.

[13]  G. Dell’Omo,et al.  Effects of corticosteroids on oxidative damage and circulating carotenoids in captive adult kestrels (Falco tinnunculus) , 2008, Journal of Comparative Physiology B.

[14]  J. Koolhaas,et al.  Aggressive and non-aggressive personalities differ in oxidative status in selected lines of mice (Mus musculus) , 2008, Biology Letters.

[15]  T. Burke,et al.  GRANDPARENT HELPERS: THE ADAPTIVE SIGNIFICANCE OF OLDER, POSTDOMINANT HELPERS IN THE SEYCHELLES WARBLER , 2007, Evolution; international journal of organic evolution.

[16]  T. Zglinicki,et al.  A continuous correlation between oxidative stress and telomere shortening in fibroblasts , 2007, Experimental Gerontology.

[17]  R. Pamplona,et al.  Life and death: metabolic rate, membrane composition, and life span of animals. , 2007, Physiological reviews.

[18]  G. Barja Mitochondrial oxygen consumption and reactive oxygen species production are independently modulated: implications for aging studies. , 2007, Rejuvenation research.

[19]  N. Metcalfe,et al.  Green swordtails alter their age at maturation in response to the population level of male ornamentation , 2007, Biology Letters.

[20]  B. Faivre,et al.  Testosterone and oxidative stress: the oxidation handicap hypothesis , 2007, Proceedings of the Royal Society B: Biological Sciences.

[21]  T. Clutton‐Brock,et al.  Intrasexual competition and sexual selection in cooperative mammals , 2006, Nature.

[22]  G. Hill,et al.  Yolk Antioxidants Vary with Male Attractiveness and Female Condition in the House Finch (Carpodacus mexicanus) , 2006, Physiological and Biochemical Zoology.

[23]  G. Dell’Omo,et al.  Effects of T-cell-mediated immune response on avian oxidative stress. , 2006, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[24]  N. Saino,et al.  Early maternal, genetic and environmental components of antioxidant protection, morphology and immunity of yellow‐legged gull (Larus michahellis) chicks , 2006, Journal of evolutionary biology.

[25]  B. Faivre,et al.  AN EXPERIMENTAL MANIPULATION OF LIFE‐HISTORY TRAJECTORIES AND RESISTANCE TO OXIDATIVE STRESS , 2006, Evolution; international journal of organic evolution.

[26]  Nigel C. Bennett,et al.  Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats , 2006, Proceedings of the National Academy of Sciences.

[27]  B. Faivre,et al.  Carotenoids modulate the trade-off between egg production and resistance to oxidative stress in zebra finches , 2006, Oecologia.

[28]  B. Miroux,et al.  Mitochondrial Uncoupling Proteins: New Perspectives for Evolutionary Ecologists , 2005, The American Naturalist.

[29]  R. Sapolsky The Influence of Social Hierarchy on Primate Health , 2005, Science.

[30]  M. Gross The Evolution of Parental Care , 2005, The Quarterly Review of Biology.

[31]  H. Lin,et al.  Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus) 2. Short-term effect. , 2004, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[32]  H. Lin,et al.  Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus) 1. Chronic exposure. , 2004, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[33]  E. Abellán,et al.  Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver. , 2004, Comparative biochemistry and physiology. Toxicology & pharmacology : CBP.

[34]  R. Sapolsky Social Status and Health in Humans and Other Animals , 2004 .

[35]  J. Speakman,et al.  Birds sacrifice oxidative protection for reproduction , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[36]  P. Redman,et al.  Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer , 2004, Aging cell.

[37]  T. Groothuis,et al.  Testosterone, cuckoldry risk and extra–pair opportunities in the Seychelles warbler , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[38]  B. Faivre,et al.  Increased susceptibility to oxidative stress as a proximate cost of reproduction , 2004 .

[39]  David M. Richardson,et al.  Sex‐specific associative learning cues and inclusive fitness benefits in the Seychelles warbler , 2003, Journal of evolutionary biology.

[40]  P. Buston,et al.  Social hierarchies: Size and growth modification in clownfish , 2003, Nature.

[41]  T. Clutton‐Brock,et al.  Breeding success in cooperative meerkats: effects of helper number and maternal state , 2003 .

[42]  K. Yeum,et al.  Carotenoid-radical interactions. , 2003, Biochemical and biophysical research communications.

[43]  T. Burke,et al.  Plant ecology (communication arising): Tree-species competition and coexistence , 2003, Nature.

[44]  T. H. Clutton-Brock,et al.  Cost minimization by helpers in cooperative vertebrates , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[45]  G. Flachowsky Natural Antioxidants in Avian Nutrition and Reproduction , 2003 .

[46]  Terry Burke,et al.  DIRECT BENEFITS AND THE EVOLUTION OF FEMALE‐BIASED COOPERATIVE BREEDING IN SEYCHELLES WARBLERS , 2002, Evolution; international journal of organic evolution.

[47]  A. Møller,et al.  Patterns of yolk enrichment with dietary carotenoids in gulls: the roles of pigment acquisition and utilization , 2002 .

[48]  R. Fiocchi,et al.  Evaluation of an Automated Spectrophotometric Assay for Reactive Oxygen Metabolites in Serum , 2002, Clinical chemistry and laboratory medicine.

[49]  J. Speakman,et al.  Living fast, dying when? The link between aging and energetics. , 2002, The Journal of nutrition.

[50]  J. Speakman,et al.  Antioxidant enzyme activities, lipid peroxidation, and DNA oxidative damage: the effects of short-term voluntary wheel running. , 2002, Archives of biochemistry and biophysics.

[51]  Tim Clutton-Brock,et al.  Breeding together: kin selection and mutualism in cooperative vertebrates. , 2002, Science.

[52]  A. Møller,et al.  Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[53]  T. Burke,et al.  Parentage assignment and extra‐group paternity in a cooperative breeder: the Seychelles warbler (Acrocephalus sechellensis) , 2001, Molecular ecology.

[54]  S. Creel,et al.  Social dominance and stress hormones , 2001 .

[55]  D. Marx,et al.  A COST OF REPRODUCTION IN DROSOPHILA MELANOGASTER: STRESS SUSCEPTIBILITY , 2001, Evolution; international journal of organic evolution.

[56]  C. Leeuwenburgh,et al.  Oxidative stress and antioxidants in exercise. , 2001, Current medicinal chemistry.

[57]  A. Green MASS/LENGTH RESIDUALS: MEASURES OF BODY CONDITION OR GENERATORS OF SPURIOUS RESULTS? , 2001 .

[58]  Peter F Surai,et al.  Carotenoids in Avian Nutrition and Embryonic Development. 2. Antioxidant Properties and Discrimination in Embryonic Tissues , 2001 .

[59]  Hanna Kokko,et al.  The evolution of cooperative breeding through group augmentation , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[60]  N. Holbrook,et al.  Oxidants, oxidative stress and the biology of ageing , 2000, Nature.

[61]  M. Brand Uncoupling to survive? The role of mitochondrial inefficiency in ageing , 2000, Experimental Gerontology.

[62]  T. E. Martin,et al.  EVOLUTION OF PASSERINE INCUBATION BEHAVIOR: INFLUENCE OF FOOD, TEMPERATURE, AND NEST PREDATION , 2000, Evolution; international journal of organic evolution.

[63]  T. Clutton‐Brock,et al.  Individual contributions to babysitting in a cooperative mongoose, Suricata suricatta , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[64]  D. Houston,et al.  Why egg yolk is yellow. , 2000, Trends in ecology & evolution.

[65]  V. Polo,et al.  Status signalling, metabolic rate and body mass in the siskin: the cost of being a subordinate , 2000, Animal Behaviour.

[66]  L L Ji,et al.  Antioxidants and oxidative stress in exercise. , 1999, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[67]  J. Komdeur,et al.  Predation risk affects trade-off between nest guarding and foraging in Seychelles warblers , 1999 .

[68]  R. Heinsohn,et al.  The cost of helping. , 1999, Trends in ecology & evolution.

[69]  M. Taborsky,et al.  Behavioural time–energy budgets of cooperatively breedingNeolamprologus pulcher(Pisces: Cichlidae) , 1998, Animal Behaviour.

[70]  A. Cockburn EVOLUTION OF HELPING BEHAVIOR IN COOPERATIVELY BREEDING BIRDS , 1998 .

[71]  R. Griffiths,et al.  A DNA test to sex most birds , 1998, Molecular ecology.

[72]  J. Komdeur Long‐term fitness benefits of egg sex modification by the Seychelles warbler , 1998 .

[73]  I. Owens,et al.  Cooperative breeding in birds: a comparative test of the life history hypothesis , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[74]  B. Ames,et al.  The free radical theory of aging matures. , 1998, Physiological reviews.

[75]  R. Browne,et al.  Correlates of markers of oxidative status in the general population. , 1998, American journal of epidemiology.

[76]  T. Clutton‐Brock,et al.  Costs of cooperative behaviour in suricates (Suricata suricatta) , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[77]  D. Houston Nutritional constraints on egg production in birds , 1997, Proceedings of the Nutrition Society.

[78]  D. Wilmore,et al.  Starvation enhances hepatic free radical release following endotoxemia. , 1997, The Journal of surgical research.

[79]  J. Komdeur Inter-island transfers and population dynamics of Seychelles Warblers Acrocephalus sechellensis , 1997, Bird Conservation International.

[80]  J. Komdeur Influence of age on reproductive performance in the Seychelles warbler , 1996 .

[81]  J. Komdeur Seasonal Timing of Reproduction in a Tropical Bird, the Seychelles Warbler: A Field Experiment Using Translocation , 1996, Journal of biological rhythms.

[82]  L. Knudsen,et al.  Oxidative stress associated with exercise, psychological stress and life-style factors. , 1996, Chemico-biological interactions.

[83]  R. Weindruch,et al.  Oxidative Stress, Caloric Restriction, and Aging , 1996, Science.

[84]  A. Cockburn,et al.  Food supplementation induces provisioning of young in cooperatively breeding White-winged Choughs , 1996 .

[85]  R. Cowie,et al.  Differential response by males and females to brood manipulations in the Pied Flycatcher : Energy expenditure and nestling diet , 1995 .

[86]  I. Pen,et al.  Parental energy expenditure in relation to manipulated brood size in the European kestrel Falco tinnunculus , 1995 .

[87]  Andrew Cockburn,et al.  Helping is costly to young birds in cooperatively breeding white-winged choughs , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[88]  A. Astrup,et al.  Oxidative DNA damage correlates with oxygen consumption in humans , 1994, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[89]  J. Komdeur Experimental evidence for helping and hindering by previous offspring in the cooperative-breeding Seychelles warbler Acrocephalus sechellensis , 1994, Behavioral Ecology and Sociobiology.

[90]  I. Cuthill,et al.  The ecological costs of avian fat storage. , 1993, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[91]  R. Mulder,et al.  Dominant males punish helpers for temporary defection in superb fairy-wrens , 1993, Animal Behaviour.

[92]  R. Mumme Do helpers increase reproductive success? , 1992, Behavioral Ecology and Sociobiology.

[93]  R. Heinsohn,et al.  Cooperative enhancement of reproductive success in white-winged choughs , 1992, Evolutionary Ecology.

[94]  S. Schoech,et al.  Reproductive endocrinology and mechanisms of breeding inhibition in cooperatively breeding Florida Scrub Jays Aphelocoma C. coerulescens) , 1991 .

[95]  S. Creel,et al.  Energetics, reproductive suppression and obligate communal breeding in carnivores , 1991, Behavioral Ecology and Sociobiology.

[96]  S. Daan,et al.  Avian basal metabolic rates: their association with body composition and energy expenditure in nature. , 1990, The American journal of physiology.

[97]  W. Arnold The evolution of marmot sociality ii. costs and benefits of joint hibernation , 1990 .

[98]  K. N. Rabenold Cooperative Breeding in Birds: Campylorhynchus wrens: the ecology of delayed dispersal and cooperation in the Venezuelan savanna , 1990 .

[99]  R. H. Wiley,et al.  The relationship between social dominance, subcutaneous fat, and annual survival in wintering white-throated sparrows (Zonotrichia albicollis) , 1990, Behavioral Ecology and Sociobiology.

[100]  J. Moreno Strategies of mass change in breeding birds , 1989 .

[101]  M. Petrie Helping and communal breeding in birds. Ecology and evolution By Jerram L. Brown. Princeton, New Jersey: Princeton University Press (1987). Pp. xviii 354. Price £28.20 hardback, £10.40 paperback , 1989, Animal Behaviour.

[102]  S. Emlen,et al.  The role of kinship in helping decisions among white-fronted bee-eaters , 1988, Behavioral Ecology and Sociobiology.

[103]  S. F. Eden When do helpers help? Food availability and helping in the moorhen, Gallinula chloropus , 1987, Behavioral Ecology and Sociobiology.

[104]  B. Halliwell,et al.  Free radicals in biology and medicine , 1985 .

[105]  S. Austad,et al.  Reproductive enhancement by helpers and an experimental inquiry into its mechanism in the bicolored wren , 1985, Behavioral Ecology and Sociobiology.

[106]  M. Taborsky Broodcare helpers in the cichlid fish Lamprologus brichardi: Their costs and benefits , 1984, Animal Behaviour.

[107]  H. Reyer Investment and relatedness: A cost/benefit analysis of breeding and helping in the pied kingfisher (Ceryle rudis) , 1984, Animal Behaviour.

[108]  E. R. Brown,et al.  Morphological variation in a population of grey-crowned babblers: Correlations with variables affecting social behavior , 1982, Behavioral Ecology and Sociobiology.

[109]  Leonard A. Freed,et al.  LOSS OF MASS IN BREEDING WRENS: STRESS OR ADAPTATION? , 1981 .

[110]  H. Reyer Flexible helper structure as an ecological adaptation in the pied kingfisher (Ceryle rudis rudis L.) , 1980, Behavioral Ecology and Sociobiology.

[111]  Ivan D. Chase,et al.  Cooperative and Noncooperative Behavior in Animals , 1980, The American Naturalist.

[112]  Anthony J. Gaston,et al.  The Evolution of Group Territorial Behavior and Cooperative Breeding , 1978, The American Naturalist.

[113]  B. G. Murray Ecological Adaptations for Breeding in Birds , 1969 .

[114]  D. Harman Aging: a theory based on free radical and radiation chemistry. , 1956, Journal of gerontology.

[115]  N. Metcalfe,et al.  Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. , 2009, Ecology letters.

[116]  Jan KOMDEURt The effect of kinship on helping in the cooperative breeding Seychelles warbler ( Acrocephalus sechellensis ) , 2009 .

[117]  J. Komdeur,et al.  Molecular ecology reveals the hidden complexities of the seychelles warbler , 2007 .

[118]  T. Clutton‐Brock Cooperative breeding in mammals , 2006 .

[119]  A. Walter The evolution of marmot sociality: II. Costs and benefits of joint hibernation , 2004, Behavioral Ecology and Sociobiology.

[120]  J. Dickinson,et al.  Ecology and evolution of cooperative breeding in birds , 2004 .

[121]  J. Rasbash,et al.  A User's Guide to MLwiN version 2.0 , 2004 .

[122]  J. S. Quinn,et al.  Ecology and Evolution of Cooperative Breeding in Birds: Joint laying systems , 2004 .

[123]  T. von Zglinicki Oxidative stress shortens telomeres. , 2002, Trends in biochemical sciences.

[124]  Peter F Surai Natural Antioxidants in Avian Nutrition and Reproduction , 2002 .

[125]  L. Bolognini,et al.  The radical cation of N,N-diethyl-para-phenylendiamine: A possible indicator of oxidative stress in biological samples , 2000 .

[126]  M. Taborsky,et al.  Paying to stay or paying to breed? Field evidence for direct benefits of helping behavior in a cooperatively breeding fish , 1998 .

[127]  S. Verhulst,et al.  Clutch size and parental effort in the Great Tit Parus major , 1997 .

[128]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[129]  M. Taborsky Sneakers, Satellites, and Helpers: Parasitic and Cooperative Behavior in Fish Reproduction , 1994 .

[130]  J. Komdeur Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler , 1992, Nature.

[131]  B. Ames,et al.  DNA DAMAGE BY ENDOGENOUS OXIDANTS AS A CAUSE OF AGING AND CANCER , 1991 .

[132]  C. M. Lessells,et al.  The Evolution of Life Histories , 1994 .

[133]  S. Emlen Cooperative Breeding in Birds: White-fronted Bee-eaters: helping in a colonially nesting species , 1990 .

[134]  W. Koenig,et al.  Reproductive Sociality. (Book Reviews: Cooperative Breeding in Birds. Long-Term Studies of Ecology and Behavior.) , 1990 .

[135]  D. Crews Psychobiology of reproductive behavior : an evolutionary perspective , 1987 .

[136]  J. Krebs,et al.  Behavioural ecology: An evolutionary approach , 1978 .