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Plasma levels of androgens and gonadal development of breeders and helpers in the bell miner (Manorina melanophrys)

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Abstract

Plasma concentration of androgens and gonad development were studied in wild cooperatively breeding bell miners (Manorina melanophrys) of different age, sex and social status. Plasma levels of androgens increased with age of birds. For sexually mature (SM) bell miners, androgen levels were higher in breeders than in nonbreeding (NB) helpers (P < 0.005), and they were marginally higher in females than in males (P < 0.10). Thus female breeders showed the highest plasma levels of androgens. This pattern may be explained by an asymmetry between the sexes in the levels of competition needed to reach and defend breeding status; the degree of intra-sexual competition seems to be higher among female bell miners than among males. In general, male breeders had larger gonads than male SMNB helpers; male breeder gonads produced spermatozoa whereas most helpers' gonads did not. However, old (i.e. ≧ 34 months) SMNB male helpers had large gonads producing spermatozoa in spite of having low plasma levels of androgens. We suggest that young male bell miners may be under a “voluntary” mechanism of reproductive suppression perhaps favoured by inbreeding avoidance; although some aggressive interactions observed between very young helpers (about 2 months) and adult members of the breeding unit suggests that a certain degree of imposition also occurs at young ages. Older male helpers may avoid aggression with the male breeder and imposed reproductive suppression, hence the low circulating levels of androgens, but they have the potential to sneak extra-pair copulations. Gonad size decreased during the non-breeding season in both sexes.

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References

  • Abraham GE, Gaza A, Manlimos FS (1977) Radioimmunoassay of steroids. In: Abraham GE (ed) Handbook of radioimmunoassay. Marcel Dekker, New York, pp 591–656

    Google Scholar 

  • 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

    Google Scholar 

  • Arctander P (1988) Comparative studies of avian DNA by restriction fragment length polymorphism analysis: convenient procedures based on blood samples from live birds. J Ornithol 129:205–216

    Google Scholar 

  • Balthazart J (1983) Hormonal correlates of behavior. In: Farner DS, King JR, Parkes KC (eds) Avian biology, vol 7. Academic Press, New York, pp 221–365

    Google Scholar 

  • Baptista LF, Le Wolfe BB, Avery-Beausoleil L (1987) Testosterone, aggression, and dominance in Gambel's white-crowed sparrows. Wilson Bull 99:86–91

    Google Scholar 

  • Barholomew GA (1949) The effect of light and day length on reproduction in the English sparrow. Bull Mus Comp Zool 101:433–476

    Google Scholar 

  • Bell HL, Ford HA (1986) A comparison of social organization of three syntopic species of Australian thornbill, Acanthiza. Behav Ecol Sociobiol 19:381–392

    Google Scholar 

  • Bowman LA, Dilley SR, Keverne EB (1978) Suppression of oestrogen-induced LH surges by social subordination in talapoin monkeys. Nature 275:56–58

    Google Scholar 

  • Brooker MG, Rowley I, Adams M, Baverstock PR (1990) Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species? Behav Ecol Sociobiol 26: 191–199

    Google Scholar 

  • Brown JL (1974) Alternative routes to sociality in jays — with a theory for the evolution of altruism and communal breeding. Am Zool 14:63–80

    Google Scholar 

  • Brown JL (1978) Avian communal breeding systems. Annu Rev Ecol Syst 9:123–155

    Google Scholar 

  • Brown JL (1985) The evolution of helping behavior — an ontogenetic and comparative perspective. In: Gollins ES (ed) The comparative development of adaptive skills: evolutionary implications. LEA Publishers, New Jersey, pp 137–171

    Google Scholar 

  • Brown JL (1987) Helping and communal breeding in birds. Princeton University Press, Princeton

    Google Scholar 

  • Brown JL, Horvath EG (1989) Geographic variation of group size, ontogeny, rattle calls, and body size in Aphelocoma ultramarina. Auk 106:124–128

    CAS  PubMed  Google Scholar 

  • Burger HG, Lee VWK, Rennie GC (1972) A generalized computer program for the treatment of data from competitive proteinbinding assays including radioimmunoassays. J Lab Clin Med 80:302–312

    Google Scholar 

  • Burke T, Davies NB, Bruford MW, Hatchwell BJ (1989) Parental care and mating behaviour of polyandrous dunnocks Prunella modularis related to paternity by DNA fingerprinting. Nature 338:249–251

    Article  Google Scholar 

  • Chard T (1987) An introduction to radioimmunoassay and related techniques. Elsevier, Amsterdam

    Google Scholar 

  • Clarke MF (1984) Co-operative breeding by the Australian bell miner Manorina melanophrys Latham: a test of kin selection theory. Behav Ecol Sociobiol 14:137–146

    Google Scholar 

  • Clarke MF (1988) The reproductive behaviour of the bell miner Manorina melanophrys. Emu 88:88–100

    Google Scholar 

  • Clarke MF (1989) The pattern of helping in the bell miner (Manorina melanophrys). Ethology 80:292–306

    Google Scholar 

  • Clarke MF, Heathcote CF (1988) Methods for sexing and ageing the bell miner Manorina melanophrys. Emu 88:118–121

    Google Scholar 

  • Clarke MF, Heathcote CF (1990) Dispersal, survivorship and demography in the co-operatively breeding bell miner Manorina melanophrys. Emu 90:15–23

    Google Scholar 

  • Clayden EC (1962) Practical section cutting and staining. J & A Churchill

  • Collins K, Borgia G (1992) Age-related effects of testosterone, plumage, and experience on aggression and social dominance in juvenile male satin bowerbirds (Ptilonorhynchus violaceus). Auk 109:422–434

    Google Scholar 

  • Creel SR, Creel NM (1991) Energetics, reproductive suppression and obligate communal breeding in carnivores. Behav Ecol Sociobiol 28:263–270

    Google Scholar 

  • Creel SR, Waser PM (1991) Failures of reproductive suppression in dwarf mongooses (Helogale parvula): accident or adaptation? Behav Ecol 2:7–15

    Google Scholar 

  • Crook JH, Butterfield PA (1968) Effects of testosterone propionate and luteinizing hormone on agonistic and nest building behaviour of Quelea quelea. Anim Behav 16:370–384

    Google Scholar 

  • Davies NB (1985) Cooperation and conflict among dunnocks, Prunella modularis, in a variable mating system. Anim Behav 33:628–648

    Google Scholar 

  • Donham RS, Wingfield JC, Mattocks PWJr, Farner DS (1982) Changes in testicular and plasma androgens with photoperiodically induced increase in plasma LH in the House Sparrow. Gen Comp Endocrinol 48:342–347

    Google Scholar 

  • Dow DD (1975) Displays of the honey-eater Manorina melanocephala. Z Tierpsychol 38:70–96

    Google Scholar 

  • Dow DD (1978) Breeding biology and development of the young of Manorina melanocephala, a communally breeding honeyeater. Emu 78:207–222

    Google Scholar 

  • Dufty AMJr (1989) Testosterone and survival: a cost of aggressiveness? Horm Behav 23:185–193

    CAS  PubMed  Google Scholar 

  • Dunbar RIM (1988) Primate social systems. Croom Helm, London

    Google Scholar 

  • Elwood RW, Ostermeyer MC (1984) Does copulation inhibit infanticide in male rodents? Anim Behav 32:293–294

    Google Scholar 

  • Farner DS, Wilson AC (1957) A quantitative examination of testicular growth in the white-crowned sparrow. Biel Bull 113:254–267

    Google Scholar 

  • Farner DS, Follett BK, King JR, Morton ML (1966) A quantitative examination of ovarian growth in the white-crowned sparrow. Biol Bull 130:67–75

    Google Scholar 

  • Francis RC (1988) On the relationship between aggression and social dominance. Ethology 78:223–237

    Google Scholar 

  • Francis RC, Jacobson B, Wingfield JC, Fernald RD (1992) Castration lowers aggression but not social dominance in male Haplochromis burtoni (Ciclidae). Ethology 90:247–255

    Google Scholar 

  • Grant R (1990) The significance of subadult plumage in Darwin's finches, Geospiza fortis. Behav Ecol 1:161–170

    Google Scholar 

  • Gratto-Trevor CL, Oring LW, Fivizzani AJ (1991) Effects of blood sampling stress on hormone levels in the Semipalmated Sandpiper. J Field Ornithol 62:19–27

    Google Scholar 

  • Harvey S, Phillips JG, Rees A, Hall TR (1984) Stress and adrenal function. J Exp Zool 232:633–645

    Google Scholar 

  • Hegner RE, Wingfield JC (1987a) Effects of brood-size manipulations on parental investment, breeding success, and reproductive endocrinology of house sparrows. Auk 104:470–480

    Google Scholar 

  • Hegner RE, Wingfield JC (1987b) Effects of experimental manipulation of testosterone levels on parental investment and breeding success in male house sparrows. Auk 104:462–469

    Google Scholar 

  • Hinde RA (ed) (1983) Primate social relationships. Blackwell Scientific, Oxford

    Google Scholar 

  • Hoysak DJ, Weatherhead PJ (1991) Sampling blood from birds: a technique and an assessment of its effect. Condor 93:746–752

    Google Scholar 

  • Kerlan JT, Jaffe RB (1974) Plasma testosterone levels during the testicular cycle of the redwinged blackbird (Agelaius phoeniculus). Gen Comp Endocrinol 22:428–432

    Google Scholar 

  • Ketterson ED, Nolan VJr, Wolf L, Ziegenfus C, Dufty AMJr, Ball GF, Johnsen TS (1991) Testosterone and avian life histories: the effect of experimentally elevated testosterone and corticosterone on body mass in dark-eyed juncos. Horm Behav 25:489–503

    Google Scholar 

  • Koenig WD, Pitelka FA (1979) Relatedness and inbreeding avoidance: counterploys in the communally nesting acorn woodpecker. Science 206:1103–1105

    Google Scholar 

  • Lawton M, Guindon CF (1981) Flock composition, breeding success, and learning in the brown jay. Condor 83:27–33

    Google Scholar 

  • Lawton MF, Lawton RO (1985) Heterochrony, deferred breeding, and avian sociality. Curr Ornithol 3:187–222

    Google Scholar 

  • Ligon JD (1988) The question of parent-pffspring conflict in cooperatively breeding birds. In: Quellet H (ed) Proceedings of the 19th international ornithological congress, Ottawa, Ottawa Press, pp 1231–1243

    Google Scholar 

  • Lovegrove BG (1991) The evolution of eusociality in molerats (Bathyergidae): a question of risks, numbers, and costs. Behav Ecol Sociobiol 28:37–45

    Google Scholar 

  • Masters-Vleck C, Dobrott SJ (1993) Testosterone, antiandrogen, and alloparental behavior in bobwhite quail foster fathers. Horm Behav 27:92–107

    Google Scholar 

  • Mays NA, Masters-Vleck C, Dawson J (1991) Plasma luteinizing hormone, steroid hormones, behavioral role, and nest stage in cooperatively breeding Harris' hawks (Parabuteo unicinctus). Auk 108:619–637

    Google Scholar 

  • Moehlman P (1986) Ecology of cooperation in canids. In: Rubenstein DI, Wrangham RW (eds) Ecological aspects of social evolution. Princeton University Press, Princeton, pp 64–86

    Google Scholar 

  • Morton ML, Peterson LE, Burns DM, Allan N (1990) Seasonal and age-related changes in plasma testosterone levels in mountain white-crowned sparrows. Condor 92:166–173

    Google Scholar 

  • Mumme RL, Koenig WD, Zink RM, Marten JA (1985) Genetic variation and parentage in a California population of acorn woodpeckers. Auk 102:305–312

    Google Scholar 

  • Peterson AT (1991) Sociality and ontogeny of coloration in the blue-and-black jays. Wilson Bull 103:59–67

    Google Scholar 

  • Poiani A (1992a) Hormonal, behavioural and ecological aspects of cooperative breeding in the bell miner (Manorina melanophrys, Meliphagidae). PhD Thesis, Department of Zoology, La Trobe University, Victoria, Australia

    Google Scholar 

  • Poiani A (1992b) Feeding of the female breeder by male helpers in the bell miner Manorina melanophrys. Emu 92:233–237

    Google Scholar 

  • Poiani A (1993a) Social structure and the development of helping in the bell miner (Manorina melanophrys, Meliphagidae). Ethology 93:62–80

    Google Scholar 

  • Poiani A (1993b) Reproductive biology of the bell miner (Manorina melanophrys, Meliphagidae) at Healesville, South-eastern Victoria. Wildl Res 20 (in press)

  • Poiani A (1993c) Effects of clutch size manipulation on reproductive behavior and nesting success in the cooperatively breeding bell miner (Manorina melanophrys). Evol Ecol 7:329–356

    Google Scholar 

  • Poiani A (1993d) A possible case of intra-specific brood parasitism in the bell miner. Corella 17:61–62

    Google Scholar 

  • Poiani A, Rogers A, Rogers K, Rogers D (1990) Asymmetrical competition between the bell miner (Manorina melanophrys, Meliphagidae) and other honeyeaters: evidence from southeastern Victoria, Australia. Oecologia 85:250–256

    Google Scholar 

  • Procter-Gray E, Holmes RT (1981) Adaptive significance of delayed attainment of plumage in male American redstarts: tests of two hypotheses. Evolution 35:742–751

    Google Scholar 

  • Rabenold KN (1985) Cooperation in breeding by nonreproductive wrens: kinship, reciprocity and demography. Behav Ecol Sociobiol 17:1–17

    Google Scholar 

  • Rabenold PP, Rabenold KN, Piper WH, Haydock J, Zack SW (1990) Shared paternity revealed by genetic analysis in cooperatively breeding tropical wrens. Nature 348:538–540

    Google Scholar 

  • Reyer H-U, Dittami JP, Hall MR (1986) Avian helpers at the nest: are they psychologically castrated? Ethology 71:216–228

    Google Scholar 

  • Rood JP (1980) Mating relationships and breeding suppression in the dwarf mongoose. An Behav 28:143–150

    Google Scholar 

  • Rowell TE (1966) Hierarchy in the organization of a captive baboon group. Anim Behav 14:430–443

    Google Scholar 

  • Rowley I (1965) The life history of the superb blue wren Malurus cyaneus. Emu 64:250–297

    Google Scholar 

  • Rowley I, Russell E, Payne RB, Payne LL (1989) Plural breeding in the splendid fairy-wren, Malurus splendens (Aves: Maluridae), a cooperative breeder. Ethology 83:229–247

    Google Scholar 

  • Saitoh T (1990) Lifetime reproductive success in reproductively suppressed female voles. Res Popul Ecol 32:391–406

    Google Scholar 

  • Schilling A, Perret M, Predine J (1984) Sexual inhibition in a prosimian primate: a pheromone-like effect. J Endocrinol 102:143–151

    Google Scholar 

  • Schmidt LG, Bradshaw SD, Follett BK (1991) Plasma levels of luteinizing hormone and androgens in relation to age and breeding status among cooperatively breeding Australian magpies (Gymnorhina tibicen Latham). Gen Comp Endocrinol 83:48–55

    Google Scholar 

  • 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

    Google Scholar 

  • Scott DM, Middleton ALA (1968) The annual testicular cycle of the brown-headed cowbird (Molothrus ater). Can J Zool 46:77–87

    Google Scholar 

  • Siegel HS (1980) Physiological stress in birds. Bioscience 30:529–534

    Google Scholar 

  • Silverin B (1980) Effects of long-acting testosterone treatment on free-living pied flycatchers, Ficedula hypoleuca, during the breeding period. Anim Behav 28:906–912

    Google Scholar 

  • Silverin B (1982) Endocrine correlates of brood size in adult pied flycatchers, Ficedula hypoleuca. Gen Comp Endocrinol 47:18–23

    Google Scholar 

  • Silverin B (1991) Behavioral, hormonal, and morphological responses of free-living male pied flycatchers to estradiol treatment of their mates. Horm Behav 25:38–56

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman, New York

    Google Scholar 

  • Sossinka R (1980) Ovarian development in an opportunistic breeder, the zebra finch Poephila guttata castanotis. J Exp Zool 211:225–230

    Google Scholar 

  • Tsutsui K, Wingfield JC, Bottjer SW (1991) Adenohypophysectomy in the zebra finch. Gen Comp Endocrinol 81:163–173

    Google Scholar 

  • Vehrencamp SL (1983) A model for the evolution of despotic versus egalitarian societies. Anim Behav 31:667–682

    Google Scholar 

  • Vogel C (1985) Helping, cooperation, and altruism in primate societies. In: Holldobler B, Lindauer M (eds) Experimental behavioral ecology. Fisher, New York, pp 375–389

    Google Scholar 

  • Walsberg GE (1983) Avian ecological energetics. In: Farner DS, King JR, Parkes KC (eds) Avian biology vol 7. Academic Press, New York, pp 161–220

    Google Scholar 

  • Wasser SK, Barash DP (1983) Reproductive suppression among female mammals: implications for biomedicine and sexual selection theory. Q Rev Biol 58:513–538

    Google Scholar 

  • Wingfield JC (1980) Fine temporal adjustment of reproductive functions. In: Epple A, Stetson MH (eds) Avian endocrinology. Academic Press, New York, pp 367–389

    Google Scholar 

  • Wingfield JC (1984a) Environmental and endocrine control of reproduction in the song sparrow, Melospiza melodia. I Temporal organizaton of the breeding cycle. Gen Comp Endocrinol 56:406–416

    Google Scholar 

  • Wingfield JC (1984b) Environmental and endocrine control of reproduction in the song sparrow, Melospiza melodia. II Agonistic interactions as environmental information stimulating secretion of testosterone. Gen Comp Endocrinol 56:417–424

    Google Scholar 

  • Wingfield JC, Farner DS (1976) Avian endocrinology — field investigations and methods. Condor 78:570–573

    Google Scholar 

  • Wingfield JC, Lewis DM (1993) Hormonal and behavioural responses to simulated territorial intrusion in the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali. Anim Behav 45:1–11

    Article  Google Scholar 

  • Wingfield JC, Smith JP, Farner DS (1982) Endocrine responses of white-crowned sparrows to environmental stress. Condor 8:399–409

    Google Scholar 

  • Wingfield JC, Ball GF, Dufty AM Jr, Hegner RE, Ramenofsky M (1987) Testosterone and aggression in birds. Am Sci 75:602–608

    Google Scholar 

  • Wingfield JC, Hegner RE, Dufty AM Jr, Ball GF (1990) The “challenge hypothesis”: theoretical implications for patterns of testosterone secretions, mating systems, and breeding strategies. Am Nat 136:829–846

    Article  Google Scholar 

  • Wingfield JC, Hegner RE, Lewis DM (1991) Circulating levels of luteinizing hormone and steroid hormones in relation to social status in the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali. J Zool London 225:43–58

    Google Scholar 

  • Wingfield JC, Hegner RE, Lewis DM (1992) Hormonal responses to removal of a breeding male in the cooperatively breeding white-browed sparrowweaver, Plocepasser mahali. Horm Behav 26:145–155

    Google Scholar 

  • Winterstein SR (1985) Ecology and sociobiology of black-throated magpie-jay. Ph.D. thesis, New Mexico State University, New Mexico, USA

    Google Scholar 

  • Wolff JO (1992) Parents suppress reproduction and stimulate dispersal in opposite-sex juvenile white-footed mice. Nature 359:409–410

    Google Scholar 

  • Wrege PH, Emlen ST (1987) Biochemical determination of parental uncertainty in white-fronted bee-eaters. Behav Ecol Sociobiol 20:153–160

    Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice Hall, New Jersey

    Google Scholar 

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  1. Terry Fletcher

    Present address: Prince Henry's Institute of Medical Research, P.O. Box 152, 3168, Clayton, Victoria, Australia

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  1. Department of Zoology, La Trobe University, 3083, Bundoora, Victoria, Australia

    Aldo Poiani

  2. Department of Anatomy, Monash University, 3168, Clayton, Victoria, Australia

    Terry Fletcher

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Poiani, A., Fletcher, T. Plasma levels of androgens and gonadal development of breeders and helpers in the bell miner (Manorina melanophrys). Behav Ecol Sociobiol 34, 31–41 (1994). https://doi.org/10.1007/BF00175456

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