Abstract
Many internal and environmental factors influence the growth of birds. Here we ask whether the reversed sexual dimorphism in the classically polyandrous black coucal is reflected in differential growth and fledging parameters of females and males. We also investigate whether androgen concentrations were higher in females than males during the nestling development, thus, providing a potential mechanism for the ‘behavioural masculinization’ of female black coucals. Furthermore, we give a detailed description of the breeding biology of this little studied and unusual bird species. Black coucal eggs were smaller, and the incubation and nestling periods were shorter than expected for a bird of that size. In absolute terms female black coucals grew faster than males and left the nest with a larger body mass, suggesting that females are the more expensive sex to rear in this species. However, in relation to adult body size, females grew slower and reached a smaller proportion of their adult body size than males upon fledging. ‘Testosterone’ concentrations were significantly higher in male than in female nestlings, hence not supporting a role of circulating androgens in the ontogeny of sex-role reversal. To our knowledge, the early sex differences in ‘testosterone’ levels of black coucals represent the first evidence that such differences exist in nestlings of altricial birds. We present anecdotal evidence that the differences may be related to an early maturation of male reproductive organs in black coucals. In females but not in males, ‘testosterone’ concentrations were related to structural growth rates.
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References
Adkins-Regan E, Abdelnabi M, Mobarak M, Ottinger MA (1990) Sex steroid levels in developing and adult male and female zebra finches (Poephila guttata). Gen Comp Endocrinol 78:93–109
Anderson DJ, Reeve J, Gomez JEM, Weathers WW, Hutson S, Cunningham HV, Bird DM (1993) Sexual size dimorphism and food requirements of nestling birds. Can J Zool 71:2541–2545
Anderson DJ, Reeve J, Bird DM (1997) Sexually dimorphic eggs, nestling growth and sibling competition in American kestrels Falco sparverius. Funct Ecol 11:331–335
Ashmole NP (1963) The biology of the wideawake or sooty tern Sterna fuscata on Ascension island. Ibis 103b:297–364
Becker P, Wink M (2003) Influences of sex, sex composition of brood and hatching order on mass growth in common terns Sterna hirundo. Behav Ecol Sociobiol 54:136–146
Bhasin S (2003) Androgen effects in Mammals. In: Henry HL, Norman AW (eds) Encyclopedia of hormones. Academic Press, San Diego, pp 70–83
Clark AB, Wilson DS (1981) Avian breeding adaptations: hatching asynchrony, brood reduction, and nest failure. Q Rev Biol 56:253–277
Clutton-Brock TH, Albon SD, Guinness FE (1981) Parental investment in male and female offspring in polygynous mammals. Nature 289:487–489
Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton
Daunt F, Monaghan P, Wanless S, Harris MP, Griffiths R (2001) Sons and daughters: age-specific differences in parental rearing capacities. Funct Ecol 15:211–216
De la Mora AN, Drummond H, Wingfield JC (1996) Hormonal correlates of dominance and starvation-induced aggression in chicks of the blue-footed booby. Ethology 102:748–761
Ferree ED, Wikelski MC, Anderson DJ (2004) Hormonal correlates of siblicide in Nazca boobies: support for the Challenge Hypothesis. Horm Behav 46:655–662
Fiala KL, Congdon JD (1983) Energetic consequences of sexual size dimorphism in nestling red-winged blackbirds. Ecology 64:642–647
Frith CB (1975) Field observations on Centropus tolou insularis on Aldabra Atoll. Ostrich 46:251–257
Gebhardt-Henrich S, Richner H (1998) Causes of growth variation and its consequences for fitness. In: Starck JM, Ricklefs RE (eds) Avian growth and development. Evolution within the altricial-precocial spectrum. Oxford University Press, Oxford, pp 324–339
Goymann W, Wittenzellner A, Wingfield JC (2004) Competing females and caring males. Polyandry and sex-role reversal in African black coucals, Centropus grillii. Ethology 110:807–823
Goymann W (2004) Wetteifernde Weibchen und fürsorgliche Männchen - Geschlechterrollentausch beim Afrikanischen Grillkuckuck. Jahrbuch der Max-Planck-Gesellschaft , pp 513–518
Goymann W, Wingfield JC (2004) Competing females and caring males. Sex steroids in African black coucals, Centropus grillii. Anim Behav 64:733–740
Griffiths R (1992) Sex-biased mortality in the lesser black-backed gull Larus fuscus during the nestling stage. Ibis 134:237–244
Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075
Groothuis TGG, Muller W, von Engelhardt N, Carere C, Eising C (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29:329–352
Gwinner E (1972) Frühe Geschlechtsreife beim Fichtenkreuzschnabel (Loxia curvirostra). Die Vogelwarte 26:356–357
Hoyt DF (1979) Practical methods of estimating volume and fresh weight of bird eggs. Auk 96:73–77
Hutchison J, Wingfield J, Hutchison R (1984) Sex differences in plasma concentrations of steroids during the sensitive period for brain differentiation in the zebra finch. J Endocrinol 103:363–369
Kitaysky AS, Piatt JF, Wingfield JC, Romano M (1999) The adrenocortical stress-response of black-legged Kittiwake chicks in relation to dietary restrictions. J Comp Physiol B 169:303–310
Kitaysky AS, Kitaiskaia EV, Wingfield JC, Piatt JF (2001) Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks. J Comp Physiol B 171:701–709
Krijgsveld KL, Dijkstra C, Visser GH, Daan S (1998) Energy requirements for growth in relatioin to sexual size dimorphism in marsh harrier Circus aeruginosus nestlings. Physiol Zool 71:693–702
Lack D (1968) Ecological adaptations for breeding in birds. Methuen, London
Magrath RD (1990) Hatching asynchrony in altricial birds. Biol Rev Cambridge Phil Soc 65:587–622
Marchant S (1960) The breeding of some S.W. Ecuadorian birds. Ibis 102:349–382
McNabb FMA, Scanes CG, Zeman M (1998) The endocrine system. In: Starck JM, Ricklefs RE (eds) Avian growth and development. Evolution within the altricial-precocial spectrum. Oxford University Press, Oxford, pp 174–202
Naguib M, Riebel KAM, Gil D (2004) Nestling immunocompetence and testosterone covary with brood size in a songbird. Proc R Soc B 271:833–838
Newton I (1978) Feeding and development of sparrowhawk nestlings. J Zool 184:465–487
Oring LW (1982) Avian mating systems. In: Farner DS, King JR, Parkes KC (eds) Avian biology, vol 6. Academic Press, New York, pp 1–92
Ottinger MA, Bakst MR (1981) Peripheral androgen concentrations and testicular morphology in embryonic and young male Japanese quail. Gen Comp Endocrinol 43:170–177
Payne RB (1997) Family Cuculidae (Cuckoos). In: del Hoyo J, Elliott A, Sargatal J (eds) Handbook of the birds of the world, vol 4. Lynx Editions, Barcelona, pp 508–545
Ricklefs RE (1969) An analysis of nesting mortality in birds. Smithsonian Contrib Zool 9:1–48
Ricklefs RE (1980) Geographical variation in clutch size among passerine birds: ashmole’s hypothesis. Auk 97:38–49
Ricklefs RE, Starck JM, Konarzewski M (1998) Internal constraints on growth in birds. In: Starck JM, Ricklefs RE (eds) Avian growth and development. Evolution within the altricial-precocial spectrum. Oxford University Press, Oxford, pp 266–287
Ricklefs RE, Starck JM (1998) Embryonic growth and development. In: Starck JM, Ricklefs RE (eds) Avian growth and development. Evolution within the altricial-precocial spectrum. Oxford University Press, Oxford, pp 31–58
Riedstra B, Dijkstra C, Daan S (1999) Daily energy expenditure of male and female marsh harrier nestlings. Auk 115:635–641
Ros AFH, Groothuis TGG, Apanius V (1997) The relation among gonadal steroids, immunocompetence, body mass, and behavior in young black-headed gulls (Larus ridibundus). Am Nat 150:201–219
Schlinger B (1998) Sexual differentiation of avian brain and behavior: current views on gonadal hormone dependent and independent mechanisms. Ann Rev Physiol 60:407–29
Schlinger B, Arnold A (1992) Plasma sex steroids and tissue aromatization in hatchling zebra finches: implications for the sexual differentiation of singing behavior. Endocrinology 130:289–299
Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90:11446–11450
Skutch AF (1966) A breeding census and nesting success in Central America. Ibis 108:1–16
Slotow R (1996) Black Coucal Centropus grillii egg volume predicts their polyandrous mating system. J Avian Biol 27:171–173
van Someren VGL (1956) Days with birds. Fieldiana Zool 38:1–520
Starck JM, Ricklefs RE (1998a) Data set of avian growth parameters. In: Starck JM, Ricklefs RE (eds) Avian growth and development. Evolution within the altricial-precocial spectrum. Oxford University Press, Oxford, pp 381–423
Starck JM, Ricklefs RE (1998b) Variation, constraints, and phylogeny. Comparative analysis of variation in growth. In: Starck JM, Ricklefs RE (eds) Avian growth and development. Evolution within the altricial-precocial spectrum. Oxford University Press, Oxford, pp 247–265
Steyn P (1972) The development of Senegal coucal nestlings. Ostrich 43:56–59
Taplin A, Beurteaux Y (1992) Aspects of the breeding biology of the pheasant coucal Centropus phaisaninus. Emu 92:141–146
Tarlow EM, Wikelski M, Anderson DJ (2001) Hormonal correlates of siblicide in Galapagos Nazca Boobies. Horm Behav 40:14–20
Teather KL, Weatherhead PJ (1994) Allometry, adaptation, and the growth and development of sexually dimorphic birds. Oikos 71:515–525
Torres R, Drummond H (1999) Does large size make daughters of the blue-footed booby more expensive than sons? J Anim Ecol 68:1133–1141
Vanderschueren D, Vandenput L, Boonen S, Lindberg MK, Bouillon R, Ohlsson C (2004) Androgens and bone. Endocr Rev 25:389–425
Vernon CJ (1971) Notes on the biology of the black coucal. Ostrich 42:242–258
Weimerskirch H, Barbraud C, Lys P (2000) Sex differences in parental investment and chick growth in wandering albatrosses: fitness consequences. Ecology 81:309–318
Woods JE, Simpson RM, Moore PL (1975) Plasma testosterone levels in the chick embryo. Gen Comp Endocrinol 27:543–547
Woods JE, Weeks RL (1969) Ontogenesis of the pituitary-gonadal axis in the chick embryo. Gen Comp Endocrinol 13:242–254
Acknowledgements
We are grateful to the Tanzania Commission of Science and Technology (COSTECH), the Tanzania Wildlife Research Institute (TAWIRI), Dr Felister Urasa from the University of Dar es Salaam, Tanzania, and the management of the Kapunga Rice Project, in particular Mr Melkizedek Saro and Mr Heke, for the permits to conduct this study. We are especially grateful to Wolfgang Wickler from the former Max Planck Institute for Behavioural Physiology for his continuous support and to the late Ebo Gwinner for giving WG the opportunity to continue the Black Coucal Project. We thank Veit Eitner, Dieter Schmidl, Sabine Tebbich, Andrea Wittenzellner and especially Musa Makomba for assistance in the field, Kim Teltscher for invaluable help to molecularly sex the birds, Barbara Helm and Michael Raess for improving an earlier version of the manuscript, Liz and Neil Baker, Sonja and Andreas Kümmerle and Petra and Peter Neubert for logistic support, and Nicole Hoiss for editorial help with the manuscript. This study was funded by grants no. Go 985/2-1 and Go 985/2-2 from Deutsche Forschungsgemeinschaft (DFG) and the Max Planck Society to WG and by grants OPP-9911333 and IBN-9905679 from the National Science Foundation to JCW. This study complies with the current laws of Tanzania.
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Goymann, W., Kempenaers, B. & Wingfield, J. Breeding biology, sexually dimorphic development and nestling testosterone concentrations of the classically polyandrous African black coucal, Centropus grillii . J Ornithol 146, 314–324 (2005). https://doi.org/10.1007/s10336-005-0004-x
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DOI: https://doi.org/10.1007/s10336-005-0004-x