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Fit females and fat polygynous males: seasonal body mass changes in the grey-headed flying fox

  • Behavioral ecology - Original Paper
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Abstract

When females and males differ in their timing of maximum reproductive effort, this can result in sex-specific seasonal cycles in body mass. Such cycles are undoubtedly under strong selection, particularly in bats, where they affect flying ability. Flying foxes (Old World fruit bats, Pteropus spp.) are the largest mammals that can sustain powered flight and therefore face critical trade-offs in managing body reserves for reproduction, yet little is known about body mass dynamics in this group. I investigated body mass changes in relation to reproductive behaviour in a large colony of grey-headed flying foxes (Pteropus poliocephalus). In this polygynous mammal, females were predicted to maximise reproductive effort during lactation and males during the breeding season. As predicted, female body condition declined during the nursing period, but did not vary in relation to sexual activity. By contrast, males accumulated body reserves prior to the breeding season, but subsequently lost over 20% of their body mass on territory defence and courtship, and lost foraging opportunities as they also defended their day roost territories at night. Males in better condition had larger testes, particularly during territory establishment, prior to maximum sexual activity. Thus, the seasonality of female mass reflected the high metabolic load that lactation imposes on mothers. However, male mass followed a pattern akin to the “fatted male phenomenon”, which is commonly observed in large polygynous mammals with seasonal reproduction, but not in bats. This shows the importance of body reserves for reproduction in flying foxes, despite their severe constraints on body mass.

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References

  • Adkins-Regan E (2005) Hormones and animal social behavior. Princeton University Press, Princeton

    Google Scholar 

  • Archer J (2006) Testosterone and human aggression: an evaluation of the challenge hypothesis. Neurosci Biobehav Rev 30:319–345

    Article  CAS  PubMed  Google Scholar 

  • Atkinson SN, Ramsay MA (1995) The effects of prolonged fasting of the body composition and reproductive success of female polar bears (Ursus maritimus). Funct Ecol 9:559–567

    Article  Google Scholar 

  • Baptista TL, Richardson CS, Kunz TH (2000) Post-natal growth and age estimation in free-ranging bats: a comparison of longitudinal and cross-sectional sampling methods. J Mammal 81:709–718

    Article  Google Scholar 

  • Barclay RMR, Harder LD (2003) Life histories of bats: life in the slow lane. In: Fenton MB (ed) Ecology of bats. University of Chicago Press, Chicago, pp 209–253

    Google Scholar 

  • Beck CA, Bowen WD, Iverson SJ (2003) Sex differences in the seasonal patterns of energy storage and expenditure in a phocid seal. J Anim Ecol 72:280–291

    Article  Google Scholar 

  • Bell G (1980) The costs of reproduction and their consequences. Am Nat 116:45–76

    Article  Google Scholar 

  • Brody S (1974) Bioenergetics and growth: with special reference to the efficiency complex in domestic animals. Hafner/Collier Macmillan, New York/London

  • Clutton-Brock TH, Parker GA (1992) Potential reproductive rates and the operation of sexual selection. Q Rev Biol 67:437–456

    Article  Google Scholar 

  • Clutton-Brock TH, Albon SD, Guinness FE (1989) Fitness costs of gestation and lactation in wild mammals. Nature 337:260–262

    Article  CAS  PubMed  Google Scholar 

  • Crichton EG, Krutzsch PH (eds) (2000) Reproductive biology of bats. Academic, San Diego

  • Deutsch CJ, Haley MP, Le Boeuf BJ (1990) Reproductive effort of male northern elephant seals: estimates from mass loss. Can J Zool 68:2580–2593

    Article  Google Scholar 

  • Du Mond FV, Hutchinson TC (1967) Squirrel monkey reproduction: the “fatted” male phenomenon and seasonal spermatogenesis. Science 158:1067–1070

    Article  CAS  PubMed  Google Scholar 

  • Duncan A, Baker GB, Montgomery N (1999) The action plan for Australian bats. Environment Australia, Canberra

    Google Scholar 

  • Eby P (1991) Seasonal movements of grey-headed flying foxes, Pteropus poliocephalus (Chiroptera: Pteropodidae), from two maternity camps in northern New South Wales. Wildl Res 18:547–549

    Article  Google Scholar 

  • Eby P, Lunney D (2002) Managing the grey-headed flying fox, Pteropus poliocephalus as a threatened species: a context for the debate. In: Eby P, Lunney D (eds) Managing the grey-headed flying fox Pteropus poliocephalus as a threatened species in NSW. Royal Zoological Society of New South Wales, Mosman, pp 1–15

    Google Scholar 

  • Encarnação JA, Dietz M, Kierdorf U, Wolters V (2004) Body mass changes in male Daubenton’s bats Myotis daubentonii (Chiroptera, Vespertilionidae) during the seasonal activity period. Mammalia 68:291–297

    Article  Google Scholar 

  • Forsyth DM, Duncan RP, Tustin KG, Gaillard J-M (2005) A substantial energetic cost to male reproduction in a sexually dimorphic ungulate. Ecology 86:2154–2163

    Article  Google Scholar 

  • Fujita MS, Tuttle MD (1991) Flying-foxes (Chiroptera: Pteropodidae): threatened animals of key ecological and economic importance. Conserv Biol 5:455–463

    Article  Google Scholar 

  • Gittleman JL, Thompson SD (1988) Energy allocation in mammalian reproduction. Am Zool 28:863–875

    Google Scholar 

  • Gopalakrishna A, Chaudhari PN (1977) Breeding habits and associated phenomena in some Indian bats. Part 1. Rousettus leschenaulti (Desmarest). Megachiroptera. J Bombay Nat Hist Soc 74:1–16

    Google Scholar 

  • Hall LS, Richards GC (2000) Flying foxes: fruit and blossom bats. University of New South Wales Press, Sydney

    Google Scholar 

  • Hamilton IM, Barclay RMR (1998) Ontogenetic influences on foraging and mass accumulation by big brown bats (Eptesicus focus). J Anim Ecol 67:930–940

    Article  Google Scholar 

  • Hayssen V, Kunz TH (1996) Allometry of litter mass in bats: maternal size, wing morphology, and phylogeny. J Mammal 77:476–490

    Article  Google Scholar 

  • Hosken DJ (1998) Testes mass in megachiropteran bats varies in accordance with sperm competition theory. Behav Ecol Sociobiol 44:169–178

    Article  Google Scholar 

  • Hosken DJ, O’Shea JE (2001) Sperm production and immune function in two Australian bats, Chalinolobus morio and Nyctophilus geoffroyi. Ethol Ecol Evol 13:173–180

    Article  Google Scholar 

  • Kenagy GC (1976) The periodicity of daily activity and its seasonal changes in free-ranging and captive kangaroo rats. Oecologia 24:105–140

    Article  Google Scholar 

  • Klose SM, Welbergen JA, Goldizen AW, Kalko EKV (2009a) Spatio-temporal vigilance architecture of an Australian flying-fox colony. Behav Ecol Sociobiol 63:371–380

    Article  Google Scholar 

  • Klose SM, Welbergen JA, Kalko EKV (2009b) Testosterone is associated with harem maintenance ability in free-ranging grey-headed flying-foxes, Pteropus poliocephalus. Biol Lett 5:758–761

    Article  PubMed  Google Scholar 

  • Koprowski JL (2005) Annual cycles in body mass and reproduction of endangered Mt. Graham red squirrels. J Mammal 86:309–313

    Article  Google Scholar 

  • Korine C, Speakman J, Arad Z (2004) Reproductive energetics of captive and free-ranging Egyptian fruit bats (Rousettus aegyptiacus). Ecology 85:220–230

    Article  Google Scholar 

  • Kunz TH, Parsons S (eds) (2009) Ecological and behavioral methods for the study of bats. Johns Hopkins Press, Baltimore

  • Kunz TH, Stern AA (1995) Maternal investment and post-natal growth in bats. In: Swift SM, Racey PA (eds) Symposia of the Zoological Society of London, vol 67. Clarendon, Oxford, pp 123–138

  • Kunz TH, Wrazen JA, Burnett CD (1998) Changes in body mass and fat reserves in prehibernating little brown bats (Myotis lucifugus). Ecoscience 5:8–17

    Google Scholar 

  • Kurta A, Kunz TH, Nagy KA (1990) Energetics and water flux of free-ranging Big Brown Bats (Eptesicus fuscus) during pregnancy and lactation. J Mammal 71:59–65

    Article  Google Scholar 

  • Lindstedt SL, Boyce MS (1985) Seasonality, fasting endurance, and body size in mammals. Am Nat 125:873–878

    Article  Google Scholar 

  • Loudon ASI, Racey PA (eds) (1987) Reproductive energetics of mammals. Oxford University Press, Oxford

    Google Scholar 

  • Lunney D, Richards G, Dickman C (2008) Pteropus poliocephalus. In: IUCN (ed) IUCN Red List of Threatened Species. IUCN, Gland

  • Maina JN (2000) What it takes to fly: the structural and functional respiratory refinements in birds and bats. J Exp Biol 203:3045–3064

    CAS  PubMed  Google Scholar 

  • Malo AF et al (2009) What does testosterone do for red deer males? Proc R Soc Biol Sci Ser B 276:971–980

    Article  CAS  Google Scholar 

  • Markus N (2002) Behaviour of the black flying fox Pteropus alecto. 2. Territoriality and courtship. Acta Chiropt 4:153–166

    Google Scholar 

  • Markus N, Blackshaw JK (2002) Behaviour of the black flying fox, Pteropus alecto. 1. An ethogram of behaviour, and preliminary characterisation of mother-infant interactions. Acta Chiropt 4:137–152

    Google Scholar 

  • Martin L et al (1995) The reproductive biology of Australian flying-foxes (genus Pteropus). In: Swift SM, Racey PA (eds) Symposia of the Zoological Society of London, vol 67. Clarendon, Oxford, pp 167–184

  • McGuckin MA, Blackshaw AW (1987) Seasonal changes in spermatogenesis (including germ cell degeneration) and plasma testosterone concentration in the Grey-headed fruit bat, Pteropus poliocephalus. Aust J Biol Sci 40:211–220

    CAS  Google Scholar 

  • McGuckin MA, Blackshaw AW (1991a) Mating-associated peak in plasma testosterone concentration in wild male grey-headed flying foxes (Pteropus poliocephalus). J Reprod Fert 92:347–352

    Article  CAS  Google Scholar 

  • McGuckin MA, Blackshaw AW (1991b) Seasonal changes in testicular size, plasma testosterone concentration and body weight in captive flying foxes (Pteropus poliocephalus and P. scapulatus). J Reprod Fert 92:339–346

    Article  CAS  Google Scholar 

  • McLean JA, Speakman JR (1999) Energy budgets of lactating and non-reproductive brown long-eared bats (Plecotus auritus) suggest females use compensation in lactation. Funct Ecol 13:360–372

    Article  Google Scholar 

  • McNab BK (1976) Seasonal fat reserves of bats in two tropical environments. Ecology 57:332–338

    Article  Google Scholar 

  • Michener GR, Locklear L (1990) Differential costs of reproductive effort for male and female Richardson’s ground squirrels. Ecology 71:855–868

    Article  Google Scholar 

  • Miquelle DG (1990) Why don’t bull moose eat during the rut? Behav Ecol Sociobiol 27:145–151

    Article  Google Scholar 

  • Mitchell B, McCowan D, Nicholson IA (1976) Annual cycles of body weight and condition in Scottish red deer, Cervus elaphus. J Zool (Lond) 180:107–127

    Article  Google Scholar 

  • Nelson JEW (1964) Vocal communication in Australian flying foxes (Pteropodidae; Megachiroptera). Z Tierpsychol 27:857–870

    Google Scholar 

  • Nelson JEW (1965a) Behavior of Australian pteropodidae (Megachiroptera). Anim Behav 13:544–557

    Article  CAS  PubMed  Google Scholar 

  • Nelson JEW (1965b) Movements of Australian flying foxes (Pteropodidae: Megachiroptera). Aust J Zool 13:53–73

    Article  Google Scholar 

  • Norberg UM, Rayner JMV (1987) Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philos Trans R Soc Lond B Biol Sci 316:335–427

    Article  Google Scholar 

  • O’Brien GM (1993) Seasonal reproduction in flying foxes, reviewed in the context of other tropical mammals. Reprod Fertil Dev 5:499–521

    Article  PubMed  Google Scholar 

  • Olsson M, Madsen T, Shine R (1997) Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proc R Soc Lond B Biol Sci 264:455–459

    Article  Google Scholar 

  • Parry-Jones KA, Augee ML (1992) Movements of grey-headed flying-foxes (Pteropus poliocephalus) to and from a colony site on the central coast of New South Wales. Wildl Res 19:331–340

    Article  Google Scholar 

  • Puddicombe R (1981) A behavioural study of the Grey-Headed Flying Fox, Pteropus poliocephalus (Megachiroptera) (BSc Hons thesis). University of New England, Armidale

  • Racey PA (1982) The ecology of bat reproduction. In: Kunz TH (ed) The ecology of bats. Plenum, New York, pp 57–104

  • Racey PA, Speakman JR (1987) The energy costs of pregnancy and lactation in heterothermic bats. Symp Zool Soc Lond 54:107–125

    Google Scholar 

  • Ratcliffe F (1932) Notes on the fruit bats (Pteropus spp.) of Australia. J Anim Ecol 1:32–57

    Article  Google Scholar 

  • Reeder DM, Kosteczko NS, Kunz TH, Widmaier EP (2006) The hormonal and behavioral response to group formation, seasonal changes, and restraint stress in the highly social Malayan Flying Fox (Pteropus vampyrus) and the less social Little Golden-mantled Flying Fox (Pteropus pumilus) (Chiroptera: Pteropodidae). Horm Behav 49:484–500

    Google Scholar 

  • Schulte-Hostedde AI, Millar JS, Hickling GJ (2005a) Condition dependence of testis size in small mammals. Evol Ecol Res 7:143–149

    Google Scholar 

  • Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005b) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163

    Article  Google Scholar 

  • Speakman J, Racey P (1986) The influence of body condition on sexual development of male brown long-eared bats (Plecotus auritus) in the wild. J Zool (Lond) 210:515–525

    Article  Google Scholar 

  • Speakman JR, Rowland A (1999) Preparing for inactivity: how insectivorous bats deposit a fat store for hibernation. Proc Nutr Soc 58:123–131

    Article  CAS  PubMed  Google Scholar 

  • Spencer HJ, Palmer C, Parry-Jones K (1991) Movements of fruit bats in eastern Australia, determined by using radio-tracking. Wildl Res 18:463–468

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Temminck CJ (1825) Vues générales sur l’ordre des cheiroptères. In: Temminck CJ (ed) Monographies de mammalogie, ou description de quelques genres de mammifères, dont les espèces dont été observées dans les différens musées de l’Europe. G. Dufour & E. D’Ocagne, Paris, pp 157–204

    Google Scholar 

  • Thomas DW, Marshall AG (1984) Reproduction and growth in three species of West African fruit bats. J Zool (Lond) 202:265–281

    Article  Google Scholar 

  • Vardon MJ, Tidemann CR (1998) Reproduction, growth and maturity in the black flying-fox, Pteropus alecto (Megachiroptera: Pteropodidae). Aust J Zool 46:329–344

    Article  Google Scholar 

  • Voigt CC (2003) Reproductive energetics of the nectar-feeding bat Glossophaga soricina (Phyllostomidae). J Comp Physiol B Biochem Syst Environ Physiol 173:79–85

    CAS  Google Scholar 

  • Welbergen JA (2005) The social organisation of the grey-headed flying-fox (Ph.D thesis). University of Cambridge, Cambridge

  • Welbergen JA (2006) Timing of the evening emergence from day roosts of the grey-headed flying-fox, Pteropus poliocephalus: the effects of predation risk, foraging needs and social context. Behav Ecol Sociobiol 60:311–322

    Article  Google Scholar 

  • Welbergen JA (2008) Variation in twilight predicts the duration of the evening emergence of fruit bats from a mixed-species roost. Anim Behav 75:1543–1550

    Article  Google Scholar 

  • Welbergen JA (2010) Growth, bimaturation and sexual size dimorphism in wild gray-headed flying-foxes (Pteropus poliocephalus). J Mammal 91:38–47

    Article  Google Scholar 

  • Welbergen JA, Klose SM, Markus N, Eby P (2008) Climate change and the effects of temperature extremes on Australian flying-foxes. Proc R Soc Biol Sci Ser B 275:419–425

    Article  Google Scholar 

  • Wolff JO (1998) Breeding strategies, mate choice, and reproductive success in American bison. Oikos 83:529–544

    Article  Google Scholar 

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Acknowledgments

I am very grateful to N. Davies, T. H. Clutton-Brock, and P. Racey for their constructive comments on earlier versions of the manuscript. I thank S. Klose and T. Sinclair-Taylor for their help in the field; A. Goldizen for her academic support; and G. H. Williams for access to the Dallis Park property. This work was supported in part by studentships from the Natural Environment Research Council, King’s College, the Isaac Newton Trust, and the Cambridge European Trust. All procedures used in this study were under permit and in accordance with the principles and guidelines of the Australian Bird and Bat Banding Scheme, NSW Parks and Wildlife Service, and NSW Department of Agriculture.

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  1. Justin A. Welbergen

    Present address: Division of Evolution, Ecology and Genetics, Research School of Biology, Australian National University, Canberra, ACT, 0200, Australia

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  1. Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ, UK

    Justin A. Welbergen

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Communicated by Elisabeth Kalko.

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Welbergen, J.A. Fit females and fat polygynous males: seasonal body mass changes in the grey-headed flying fox. Oecologia 165, 629–637 (2011). https://doi.org/10.1007/s00442-010-1856-1

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