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Timing of seasonal reproduction by flying-foxes is apparently dependent on an endogenous circannual rhythm, coded in their genome. Ultimately, evolution of an endogenous rhythm aligns an important reproductive stage, such as lactation, with resource availability such as the occurrence of maximum plant productivity; animals then do not have to rely on proximate factors to predict conditions nine months in advance. External influences that re-align reproduction to match a phase-shift in environmental conditions have to either adjust the period of the biological clock, or else induce a phase-shift, to bring breeding back into line with prevailing conditions. These are non-genomic factors: they influence the expression of genes, and therefore phenotype, without altering the DNA.

Stages of reproduction relate temporally with the endogenous rhythm, but individual flying-foxes may need to make fine adjustments in their own timing. To do this they probably monitor a suite of environmental conditions. It has been proposed that if a signal changed in isolation from other factors it would be ignored. For example, it is important that a nomadic species be not directly responsive to photoperiod since this differs when they move between latitudes. A reproductive stage would, however, be inhibited if several cues warned against proceeding, e.g. inadequate forage combined with long commuting distances at a time of unfavourable temperatures.

What non-genomic factors regulate flying-fox reproduction? It is likely that rainfall is part of the regulation for the overall rhythm, while current energy balance is probably important for individual animals during many stages of their reproduction.

Baker, J.R. and Baker, Z. 1936. The seasons in a tropical rainforest (New Hebrides).-Part 3. Fruit-bats (Pteropidae). Journal of the Linnaean Society, Zoology 40: 123-141.
Barclay, R.M.R. 1995. Does energy or calcium availability constrain reproduction by bats? Symposium of the Zoological Society, London 67: 245-258.
Bronson, F.H. 1998. Energy balance and ovulation: small cages versus natural habitats. Reproduction, Fertility and Development 10: 127-137.
Bronson, F.H. and Heideman, P.D. 1994. Seasonal regulation of reproduction in mammals. Pp. 541-584 in The Physiology of Reproduction(2nd ed.), edited by E. Knobil and J.D. Neill. Raven, New York.
Caillol, M., Meunier, M., Mondain-Monval, M., and Simon, P. 1986. Seasonal variations in the pituitary response to LHRH in the brown hare ( Lepus europaeus). Journal of Reproduction and Fertility, 78: 479-486.
Connell, K.A., Munro, U. and Torpy, F.R. 2006. Daytime behaviour of the grey-headed flying fox Pteropus poliocephalus Temminck (Pteropodidae: Megachiroptera) at an autumn/winter roost. Australian Mammalogy 28: 7-14.
Eby, P. 1991. Seasonal movements of grey-headed flying foxes, Pteropus poliocephalus(Chiroptera: Pteropodidae), from two maternity camps in northern New South Wales. Wildlife Research 18: 547-559.
Eby, P. 1995 The biology and management of flying foxes in NSW. Species Management Report. Hurstville, NSW: NSW NPWS. 18: 72pp. ISBN 0 7310 0829 4.
Eby, P. 2000. Low reproductive success in grey-headed flying foxes associated with a short period of food scarcity. Australasian Bat Society Newsletter No. 14, pp.17-20. ISSN: 1448-5877.
Eby, P. 2008. Overview of flying-fox biology and ecology. Pp. 3-55 in Managing Flying-fox Camps for Land Managers: Workshop Proceedings. Department of Environment and Climate Change (NSW).
Eby, P., Richards, G., Collins, L. and Parry-Jones, K. 1999. The distribution, abundance and vulnerability to population reduction of a nomadic nectarivore, the grey-headed flying-fox, Pteropus poliocephalus in NSW during a period of resource concentration. Australian Zoologist 31: 240-253.
Fox, S., Spencer, H. and O'Brien, G.M. 2008. Analysis of twinning in flying-foxes (Megachiroptera) reveals superfoetation and multiple-paternity. Acta Chiropterologica 10: 271-278.
Heideman, P.D. 1989. Delayed development in Fischer's pygmy fruit bat, Haplonycteris fischeri, in the Philippines. Journal of Reproduction and Fertility 85: 363-382
Heideman, P.D. 1995. Synchrony and seasonality of reproduction in tropical bats. Symposium of the Zoological Society, London 67: 151-165.
Heideman, P.D. 2000. Environmental regulation of reproduction. Pp. 469-499 in Reproductive Biology of Bats, edited by E.G. Crichton and P.H. Krutzsch. Academic Press, London.
Heideman, P.D. and Bronson, F.H. 1994. An endogenous circannual rhythm of reproduction in a tropical bat, Anoura geoffroyi, is not entrained by photoperiod. Biology of Reproduction 50: 607-614.
Kennedy, J.H. 1992 Regulation of Ovarian Function in Australian Flying-foxes. PhD thesis, The University of Queensland, Brisbane.
Macdonald, A.A. 2007 Follicle stimulating hormone regulation of reproduction in Australian flying-foxes. BSc(Hons) Thesis, University of New England, Armidale, NSW.
Macdonald, A.A., Gray, K.A. and O'Brien, G.M. 2007. Gonadotrophin hormones in flying-fox plasma during key reproductive stages. Proceedings of the Australian Physiological Society 38: 87P. http://www.apps.org.au/Proceedings/38/87P/
Marcus, N. 2002. Behaviour of the black flying fox Pteropus alecto: 2. Territoriality and courtship. Acta Chiropterologica 4: 153-166.
Martin, L. 1997. What regulates seasonal breeding in Australian flying foxes (genus Pteropus) ? Proceedings of the Australian Society for Reproductive Biology 28: 49.
Martin, L. and Bernard, R.T.F. 2000. Endocrine regulation of reproduction in bats: the role of circulating gonadal hormones. Pp. 27-64 in Reproductive Biology of Bats, edited by E.G. Crichton and P.H. Krutzsch. Academic Press, London.
Martin, L., Kennedy, J.H., Little, L., Luckhoff, H.C., O'Brien, G.M., Pow, C.S.T., Towers, P.A., Waldon, A.K. and Wang, D.Y. 1995. The reproductive biology of Australian flying-foxes (genus Pteropus). Symposium of the Zoological Society, London 67: 167-184.
McGuckin, M.A. and Blackshaw, A.W. 1992. Effects of photoperiod on the reproductive physiology of male flying foxes, Pteropus poliocephalus. Reproduction, Fertility and Development 4: 43-53.
McWilliam, A.N. 1985. The feeding ecology of Pteropus in north-eastern New South Wales, Australia. Myotis 23-24: 201-208.
Milligan, S. R. 1982. Induced ovulation in mammals. Pp. 1-46 in Oxford Reviews of Reproductive Biology, edited by C.A. Finn, volume 4. Oxford University Press, Oxford.
Nelson, J.E. 1965. Behaviour of Australian Pteropodidae (Megachiroptera). Animal Behaviour 13: 544-557.
O'Brien, G.M. 1993. Seasonal reproduction in flying foxes, reviewed in the context of other tropical mammals. Reproduction, Fertility and Development 5: 499-521.
O'Brien, G.M. 1999. What is the timecourse of courtship in Pteropus scapulatus, little red flying foxes? Proceedings of the Australian and New Zealand Society for Comparative Physiology and Biochemistry 16: 16. ISBN 1 86389 610 4.
O'Brien, G.M. 2007. Prevention is better than cure when managing flying-fox camps. Australasian Bat Society Newsletter No. 28, pp.47-53 ISSN: 1448-5877.
O'Brien, G.M., Curlewis, J.D. and Martin, L. 1990. Plasma prolactin levels in male grey-headed flying foxes. Proceedings of the Australian Physiological and Pharmacological Society 21: 65P. ISSN 0067-2084.
O'Brien, G.M., Curlewis, J.D. and Martin, L. 1991. Unusual reproductive photoresponsiveness of male greyheaded flying foxes ( Pteropus poliocephalus). Proceedings of the Australian Society for Reproductive Biology 23: 160.
O'Brien, G.M., Curlewis, J.D. and Martin, L. 1993. Effect of photoperiod on the annual cycle of testis growth in a tropical mammal, the little red flying fox, Pteropus scapulatus. Journal of Reproduction and Fertility 98: 121-127.
O'Brien, G.M. and Gray, K-A. 2003. Central program and ovarian feedback both influence LH secretion in flying-foxes. Proceedings of the Australian Physiological and Pharmacological Society 33: 77P. ISSN 0067-2084.
O'Brien, G.M., McFarlane, J.R. and Kearney, P.J. 1999. New LH assay casts light on the riddle of flying fox reproduction. Proceedings of the Australian Physiological and Pharmacological Society 30: 33P. ISSN 0067-2084.
O'Brien, G.M., McFarlane, J.R. and Kearney, P.J. 2001. Pituitary production of LH in female flying foxes, Genus Pteropus. Abstracts for the 32nd Annual Conference of the Society for Reproductive Biology, Gold Coast, Qld, 9-12 September 2001, Abstract 82 ISSN 0812-7662.
O'Brien, G.M. and Nankervis, R.F. 1994. Coital behavior of male Pteropus scapulatus(little red flying foxes) in captivity. Physiology and Behavior 56: 471-478.
Pow, C.S.T. and Martin, L. 1994. The ovarian-uterine vasculature in relation to unilateral endometrial growth in flying foxes (genus Pteropus, suborder Megachiroptera, order Chiroptera). Journal of Reproduction and Fertility 101: 247-255.
Puddicombe, R. 1981 A behavioural study of the grey-headed flying fox Pteropus poliocephalus ( Megachiroptera). BSc(Hons) Thesis, University of New England, Armidale NSW.
Racey, P.A. and Entwistle, A.C. 2000. Life-history and reproductive strategies of bats. Pp. 363-414 in Reproductive Biology of Bats, edited by E.G. Crichton and P.H. Krutzsch. Academic Press, London.
Spencer, H.J., Palmer, C. and Parry-Jones, K. 1991. Movements of fruit-bats in eastern Australia, determined by using radio-tracking. Wildlife Research 18: 463-468.
Tidemann, C.R. and Nelson, J.E. 2004. Long-distance movements of the grey-headed flying-fox ( Pteropus poliocephalus). Journal of Zoology, London 263: 141-146.
Towers, P.A. and Martin, L. 1985. Some aspects of female reproduction in the Grey-headed Flying-fox, Pteropus poliocephalus(Megachiroptera: Pteropodidae). Australian Mammalogy 8: 257-63.
Vardon, M.J. and Tidemann, C.R. 1998. Reproduction, growth and maturity in the black flying-fox, Pteropus alecto(Megachiroptera: Pteropodidae). Australian Journal of Zoology 46: 329-344.
Welbergen, J.A., Klose, S.M., Markus, N. and Eby, P. 2008. Climate change and the effects of temperature extremes on Australian flying-foxes. Proceedings. Biological sciences / The Royal Society 275: 419-425 doi:10.1098/rspb.2007.1385.
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References

Baker, J.R. and Baker, Z. 1936. The seasons in a tropical rainforest (New Hebrides).-Part 3. Fruit-bats (Pteropidae). Journal of the Linnaean Society, Zoology 40: 123-141.
Barclay, R.M.R. 1995. Does energy or calcium availability constrain reproduction by bats? Symposium of the Zoological Society, London 67: 245-258.
Bronson, F.H. 1998. Energy balance and ovulation: small cages versus natural habitats. Reproduction, Fertility and Development 10: 127-137.
Bronson, F.H. and Heideman, P.D. 1994. Seasonal regulation of reproduction in mammals. Pp. 541-584 in The Physiology of Reproduction(2nd ed.), edited by E. Knobil and J.D. Neill. Raven, New York.
Caillol, M., Meunier, M., Mondain-Monval, M., and Simon, P. 1986. Seasonal variations in the pituitary response to LHRH in the brown hare ( Lepus europaeus). Journal of Reproduction and Fertility, 78: 479-486.
Connell, K.A., Munro, U. and Torpy, F.R. 2006. Daytime behaviour of the grey-headed flying fox Pteropus poliocephalus Temminck (Pteropodidae: Megachiroptera) at an autumn/winter roost. Australian Mammalogy 28: 7-14.
Eby, P. 1991. Seasonal movements of grey-headed flying foxes, Pteropus poliocephalus(Chiroptera: Pteropodidae), from two maternity camps in northern New South Wales. Wildlife Research 18: 547-559.
Eby, P. 1995 The biology and management of flying foxes in NSW. Species Management Report. Hurstville, NSW: NSW NPWS. 18: 72pp. ISBN 0 7310 0829 4.
Eby, P. 2000. Low reproductive success in grey-headed flying foxes associated with a short period of food scarcity. Australasian Bat Society Newsletter No. 14, pp.17-20. ISSN: 1448-5877.
Eby, P. 2008. Overview of flying-fox biology and ecology. Pp. 3-55 in Managing Flying-fox Camps for Land Managers: Workshop Proceedings. Department of Environment and Climate Change (NSW).
Eby, P., Richards, G., Collins, L. and Parry-Jones, K. 1999. The distribution, abundance and vulnerability to population reduction of a nomadic nectarivore, the grey-headed flying-fox, Pteropus poliocephalus in NSW during a period of resource concentration. Australian Zoologist 31: 240-253.
Fox, S., Spencer, H. and O'Brien, G.M. 2008. Analysis of twinning in flying-foxes (Megachiroptera) reveals superfoetation and multiple-paternity. Acta Chiropterologica 10: 271-278.
Heideman, P.D. 1989. Delayed development in Fischer's pygmy fruit bat, Haplonycteris fischeri, in the Philippines. Journal of Reproduction and Fertility 85: 363-382
Heideman, P.D. 1995. Synchrony and seasonality of reproduction in tropical bats. Symposium of the Zoological Society, London 67: 151-165.
Heideman, P.D. 2000. Environmental regulation of reproduction. Pp. 469-499 in Reproductive Biology of Bats, edited by E.G. Crichton and P.H. Krutzsch. Academic Press, London.
Heideman, P.D. and Bronson, F.H. 1994. An endogenous circannual rhythm of reproduction in a tropical bat, Anoura geoffroyi, is not entrained by photoperiod. Biology of Reproduction 50: 607-614.
Kennedy, J.H. 1992 Regulation of Ovarian Function in Australian Flying-foxes. PhD thesis, The University of Queensland, Brisbane.
Macdonald, A.A. 2007 Follicle stimulating hormone regulation of reproduction in Australian flying-foxes. BSc(Hons) Thesis, University of New England, Armidale, NSW.
Macdonald, A.A., Gray, K.A. and O'Brien, G.M. 2007. Gonadotrophin hormones in flying-fox plasma during key reproductive stages. Proceedings of the Australian Physiological Society 38: 87P. http://www.apps.org.au/Proceedings/38/87P/
Marcus, N. 2002. Behaviour of the black flying fox Pteropus alecto: 2. Territoriality and courtship. Acta Chiropterologica 4: 153-166.
Martin, L. 1997. What regulates seasonal breeding in Australian flying foxes (genus Pteropus) ? Proceedings of the Australian Society for Reproductive Biology 28: 49.
Martin, L. and Bernard, R.T.F. 2000. Endocrine regulation of reproduction in bats: the role of circulating gonadal hormones. Pp. 27-64 in Reproductive Biology of Bats, edited by E.G. Crichton and P.H. Krutzsch. Academic Press, London.
Martin, L., Kennedy, J.H., Little, L., Luckhoff, H.C., O'Brien, G.M., Pow, C.S.T., Towers, P.A., Waldon, A.K. and Wang, D.Y. 1995. The reproductive biology of Australian flying-foxes (genus Pteropus). Symposium of the Zoological Society, London 67: 167-184.
McGuckin, M.A. and Blackshaw, A.W. 1992. Effects of photoperiod on the reproductive physiology of male flying foxes, Pteropus poliocephalus. Reproduction, Fertility and Development 4: 43-53.
McWilliam, A.N. 1985. The feeding ecology of Pteropus in north-eastern New South Wales, Australia. Myotis 23-24: 201-208.
Milligan, S. R. 1982. Induced ovulation in mammals. Pp. 1-46 in Oxford Reviews of Reproductive Biology, edited by C.A. Finn, volume 4. Oxford University Press, Oxford.
Nelson, J.E. 1965. Behaviour of Australian Pteropodidae (Megachiroptera). Animal Behaviour 13: 544-557.
O'Brien, G.M. 1993. Seasonal reproduction in flying foxes, reviewed in the context of other tropical mammals. Reproduction, Fertility and Development 5: 499-521.
O'Brien, G.M. 1999. What is the timecourse of courtship in Pteropus scapulatus, little red flying foxes? Proceedings of the Australian and New Zealand Society for Comparative Physiology and Biochemistry 16: 16. ISBN 1 86389 610 4.
O'Brien, G.M. 2007. Prevention is better than cure when managing flying-fox camps. Australasian Bat Society Newsletter No. 28, pp.47-53 ISSN: 1448-5877.
O'Brien, G.M., Curlewis, J.D. and Martin, L. 1990. Plasma prolactin levels in male grey-headed flying foxes. Proceedings of the Australian Physiological and Pharmacological Society 21: 65P. ISSN 0067-2084.
O'Brien, G.M., Curlewis, J.D. and Martin, L. 1991. Unusual reproductive photoresponsiveness of male greyheaded flying foxes ( Pteropus poliocephalus). Proceedings of the Australian Society for Reproductive Biology 23: 160.
O'Brien, G.M., Curlewis, J.D. and Martin, L. 1993. Effect of photoperiod on the annual cycle of testis growth in a tropical mammal, the little red flying fox, Pteropus scapulatus. Journal of Reproduction and Fertility 98: 121-127.
O'Brien, G.M. and Gray, K-A. 2003. Central program and ovarian feedback both influence LH secretion in flying-foxes. Proceedings of the Australian Physiological and Pharmacological Society 33: 77P. ISSN 0067-2084.
O'Brien, G.M., McFarlane, J.R. and Kearney, P.J. 1999. New LH assay casts light on the riddle of flying fox reproduction. Proceedings of the Australian Physiological and Pharmacological Society 30: 33P. ISSN 0067-2084.
O'Brien, G.M., McFarlane, J.R. and Kearney, P.J. 2001. Pituitary production of LH in female flying foxes, Genus Pteropus. Abstracts for the 32nd Annual Conference of the Society for Reproductive Biology, Gold Coast, Qld, 9-12 September 2001, Abstract 82 ISSN 0812-7662.
O'Brien, G.M. and Nankervis, R.F. 1994. Coital behavior of male Pteropus scapulatus(little red flying foxes) in captivity. Physiology and Behavior 56: 471-478.
Pow, C.S.T. and Martin, L. 1994. The ovarian-uterine vasculature in relation to unilateral endometrial growth in flying foxes (genus Pteropus, suborder Megachiroptera, order Chiroptera). Journal of Reproduction and Fertility 101: 247-255.
Puddicombe, R. 1981 A behavioural study of the grey-headed flying fox Pteropus poliocephalus ( Megachiroptera). BSc(Hons) Thesis, University of New England, Armidale NSW.
Racey, P.A. and Entwistle, A.C. 2000. Life-history and reproductive strategies of bats. Pp. 363-414 in Reproductive Biology of Bats, edited by E.G. Crichton and P.H. Krutzsch. Academic Press, London.
Spencer, H.J., Palmer, C. and Parry-Jones, K. 1991. Movements of fruit-bats in eastern Australia, determined by using radio-tracking. Wildlife Research 18: 463-468.
Tidemann, C.R. and Nelson, J.E. 2004. Long-distance movements of the grey-headed flying-fox ( Pteropus poliocephalus). Journal of Zoology, London 263: 141-146.
Towers, P.A. and Martin, L. 1985. Some aspects of female reproduction in the Grey-headed Flying-fox, Pteropus poliocephalus(Megachiroptera: Pteropodidae). Australian Mammalogy 8: 257-63.
Vardon, M.J. and Tidemann, C.R. 1998. Reproduction, growth and maturity in the black flying-fox, Pteropus alecto(Megachiroptera: Pteropodidae). Australian Journal of Zoology 46: 329-344.
Welbergen, J.A., Klose, S.M., Markus, N. and Eby, P. 2008. Climate change and the effects of temperature extremes on Australian flying-foxes. Proceedings. Biological sciences / The Royal Society 275: 419-425 doi:10.1098/rspb.2007.1385.
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