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Pacific Conservation Biology Pacific Conservation Biology Society
A journal dedicated to conservation and wildlife management in the Pacific region.
RESEARCH ARTICLE (Open Access)

Synchronous abortion events in the grey-headed flying-fox (Pteropus poliocephalus)

Matthew Mo https://orcid.org/0000-0003-2099-6020 A * , Jessica Meade https://orcid.org/0000-0003-1082-9907 B , Janina Price C , Jacquie Maisey C and Justin A. Welbergen B
+ Author Affiliations
- Author Affiliations

A Department of Planning, Industry and Environment, Biodiversity, Conservation and Science, Saving our Species program, 4 Parramatta Square, 12 Darcy Street, Parramatta, NSW 2150, Australia.

B Hawkesbury Institute for the Environment, Western Sydney University, Richmond, NSW 2751, Australia.

C Northern Tablelands Wildlife Carers, Armidale, NSW 2350, Australia.


Handling Editor: Mike Calver

Pacific Conservation Biology 29(2) 110-118 https://doi.org/10.1071/PC21060
Submitted: 16 September 2021  Accepted: 20 December 2021   Published: 20 January 2022

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context: The grey-headed flying-fox (Pteropus poliocephalus) is a vulnerable species endemic to eastern and south-eastern Australia. Environmental stressors are important contributors to physiological stress, leading to synchronous abortions.

Aims: We investigate the possibilities of weather conditions and anthropogenic disturbances contributing to synchronous abortion events in a grey-headed flying-fox (Pteropus poliocephalus) roost.

Methods: We recorded observations of two synchronous abortion events in a flying-fox roost in Tamworth, New South Wales (NSW), Australia, during October 2017 and August 2019.

Key results: Roost searches found ∼200 (October 2017) and 41 (August 2019) foetuses, equating to ∼0.5% and >0.1% of adults present at the time, respectively. Neither event was associated with significantly colder than average temperatures nor hot extremes (>42°C). Synchronous abortions cannot be easily attributed to unusually cold or hot site conditions. However, the surrounding region suffered from rainfall deficiencies, known to cause failure of flowering in diet plants, in the 6 months preceding both abortion events. Notably, no rainfall deficiency occurred in 6 months preceding August 2015 when colony size was also large, and no synchronous abortions occurred.

Conclusions: Natural background rates of abortions are unlikely to explain the abortion events. The 2017 abortion event coincided with intense harassment of flying-foxes using noise agents; thus, it is possible that physiological stress was a contributor. The 2019 abortion event was associated with harassment of lesser intensity but coincided with a severe food shortage throughout surrounding regions.

Implications: While it is not possible to attribute the synchronous abortion events conclusively to a single factor, the results suggest that the combination of chronic physiological stress from food shortage and acute stress from anthropogenic disturbance may have precipitated both synchronous abortion events.

Keywords: abortion, anthropogenic disturbance, bats, environmental stressors, flying-fox roost, foetal loss, Pteropodidae, reproductive failure.


References

Adams, KR, Fetterplace, LC, Davis, AR, Taylor, MD, and Knott, NA (2018). Sharks, rays and abortion: the prevalence of capture-induced parturition in elasmobranchs. Biological Conservation 217, 11–27.
Sharks, rays and abortion: the prevalence of capture-induced parturition in elasmobranchs.Crossref | GoogleScholarGoogle Scholar |

Australian Bureau of Meteorology (2021a) Climate data online. Available at http://www.bom.gov.au/climate/data. [Accessed 1 April 2021]

Australian Bureau of Meteorology (2021b) Recent and historical rainfall maps. Available at http://www.bom.gov.au/climate/maps/rainfall. [Accessed 1 April 2021]

Beydoun, H, and Saftlas, AF (2008). Physical and mental health outcomes of prenatal maternal stress in human and animal studies: a review of recent evidence. Paediatric and Perinatal Epidemiology 22, 438–466.
Physical and mental health outcomes of prenatal maternal stress in human and animal studies: a review of recent evidence.Crossref | GoogleScholarGoogle Scholar |

Budasha, NH, Gonzalez, J-P, Sebhatu, TT, and Arnold, E (2018). Rift Valley fever seroprevalence and abortion frequency among livestock of Kisoro district, South Western Uganda (2016): a prerequisite for zoonotic infection. BMC Veterinary Research 14, 271.
Rift Valley fever seroprevalence and abortion frequency among livestock of Kisoro district, South Western Uganda (2016): a prerequisite for zoonotic infection.Crossref | GoogleScholarGoogle Scholar |

Connell, KA, Munro, U, and Torpy, FR (2006). Daytime behaviour of the grey-headed flying fox Pteropus poliocephalus Temminck (Pteropodidae: Megachiroptera) at an autumn/winter roost. Australian Mammalogy 28, 7–14.
Daytime behaviour of the grey-headed flying fox Pteropus poliocephalus Temminck (Pteropodidae: Megachiroptera) at an autumn/winter roost.Crossref | GoogleScholarGoogle Scholar |

Cox L (2019) Flying-foxes found dead and emaciated across eastern Australia as dry weather bites. The Guardian, 17 October 2019. Available at https://www.theguardian.com/environment/2019/oct/17/flying-foxes-found-deadand-emaciated-across-eastern-australia-as-dry-weather-bites

Department of Agriculture, Water and the Environment (2021a) National recovery plan for the grey-headed flying-fox Pteropus poliocephalus. (Department of Agriculture, Water and the Environment: Canberra)

Department of Agriculture, Water and the Environment (2021b) National flying-fox monitoring viewer. Available at http://www.environment.gov.au/webgis-framework/apps/ffc-wide/ffc-wide.jsf. [Accessed 17 May 2021]

Dolman S, Moore M (2017) Welfare implications of cetacean bycatch and entanglements. In ‘Marine mammal welfare: human induced change in the marine environment and its impacts on marine mammal welfare’. (Ed. A Butterworth) pp. 41–65. (Springer: Cham, Switzerland) 10.1007/978-3-319-46994-2_4

Eby P (1995). The biology and management of flying-foxes in NSW. Species management report number 18. (NSW National Parks and Wildlife Service: Sydney)

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 New South Wales, during a period of resource concentration. Australian Zoologist 31, 240–253.
The distribution, abundance and vulnerability to population reduction of a nomadic nectarivore, the grey-headed flying-fox Pteropus poliocephalus in New South Wales, during a period of resource concentration.Crossref | GoogleScholarGoogle Scholar |

Edson, D, Field, H, McMichael, L, Jordan, D, Kung, N, Mayer, D, and Smith, C (2015). Flying-fox roost disturbance and Hendra virus spillover risk. PLoS ONE 10, e0125881.
Flying-fox roost disturbance and Hendra virus spillover risk.Crossref | GoogleScholarGoogle Scholar |

Fontaine, E (2012). Food intake and nutrition during pregnancy, lactation and weaning in the dam and offspring. Reproduction in Domestic Animals 47, 326–330.
Food intake and nutrition during pregnancy, lactation and weaning in the dam and offspring.Crossref | GoogleScholarGoogle Scholar |

Gallagher, CA, Grimm, V, Kyhn, LA, Kinze, CC, and Nabe-Nielsen, J (2021). Movement and seasonal energetics mediate vulnerability to disturbance in marine mammal populations. The American Naturalist 197, 296–311.
Movement and seasonal energetics mediate vulnerability to disturbance in marine mammal populations.Crossref | GoogleScholarGoogle Scholar |

Gharekhani, J, and Yakhchali, M (2019). Neospora caninum infection in dairy farms with history of abortion in West of Iran. Veterinary and Animal Science 8, 100071.
Neospora caninum infection in dairy farms with history of abortion in West of Iran.Crossref | GoogleScholarGoogle Scholar |

Giles, JR, Eby, P, Parry, H, Peel, AJ, Plowright, RK, Westcott, DA, and McCallum, H (2018). Environmental drivers of spatiotemporal foraging intensity in fruit bats and implications for Hendra virus ecology. Scientific Reports 8, 9555.
Environmental drivers of spatiotemporal foraging intensity in fruit bats and implications for Hendra virus ecology.Crossref | GoogleScholarGoogle Scholar |

Guinet, C, Roux, JP, Bonnet, M, and Mison, V (1998). Effect of body size, body mass, and body condition on reproduction of female South African fur seals (Arctocephalus pusillus) in Namibia. Canadian Journal of Zoology 76, 1418–1424.
Effect of body size, body mass, and body condition on reproduction of female South African fur seals (Arctocephalus pusillus) in Namibia.Crossref | GoogleScholarGoogle Scholar |

Hall, LS, Martin, L, O’Brien, G, Kelly, R, and Luckoff, H (1991). Flying fox populations in crisis in southeast Queensland. Proceedings of the Australian Mammal Society 37, 18.

Heathcote A (2019) Community unites to provide ‘apple kebabs’ for starving flying-foxes. Australian Geographic, 26 September 2019. Available at https://www.australiangeographic.com.au/topics/wildlife/2019/09/community-unites-to-provide-apple-kebabs-for-starving-flying-foxes

Hoh A (2017) Sydney flying-fox backyard rescues at record high due to food shortage, heat. ABC News, 22 February 2017. Available at https://www.abc.net.au/news/2017-02-22/sydney-flying-fox-rescues-at-record-high/8293004

Ladyman, SR (2008). Leptin resistance during pregnancy in the rat. Journal of Neuroendocrinology 20, 269–277.
Leptin resistance during pregnancy in the rat.Crossref | GoogleScholarGoogle Scholar |

Ladyman, SR, Augustine, RA, and Grattan, DR (2010). Hormone interactions regulating energy balance during pregnancy. Journal of Neuroendocrinology 22, 805–817.
Hormone interactions regulating energy balance during pregnancy.Crossref | GoogleScholarGoogle Scholar |

Martin L, McIlwee AP (2002) The reproductive biology and intrinsic capacity for increase of the grey-headed flying-foxes Pteropus poliocephalus (Megachiroptera), and the implications of culling. In ‘Managing the Grey-headed Flying-fox as a Threatened Species in New South Wales’. (Eds P Eby, D Lunney) pp. 91–108. (Royal Zoological Society of New South Wales: Mosman, NSW) 10.7882/FS.2002.042

Martin, L, Towers, PA, McGuckin, MA, Little, L, Luckhoff, H, and Blackshaw, AW (1987). Reproductive biology of flying-foxes (Chiroptera: Pteropodidae). Australian Mammalogy 10, 115–118.

Martin, L, Kennedy, JH, Little, L, Luckhoff, HC, O’Brien, GM, Pow, CST, Towers, PA, Waldon, AK, and Wang, DY (1996). The reproductive biology of Australian flying-foxes (genus Pteropus). Symposia of the Zoological Society of London 67, 167–184.

Mo, M, Roache, M, Haering, R, and Kwok, A (2021). Using wildlife carer records to identify patterns in flying-fox rescues: a case study in New South Wales, Australia. Pacific Conservation Biology 27, 61–69.
Using wildlife carer records to identify patterns in flying-fox rescues: a case study in New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |

Mo, M, Roache, M, Davies, J, Hopper, J, Pitty, H, Foster, N, Guy, S, Parry-Jones, K, Francis, G, Koosmen, A, Colefax, L, Costello, C, Stokes, J, Curran, S, Smith, M, Daly, G, Simmons, C-M, Hansen, R, Prophet, D, Judge, S, Major, F, Hogarth, T, McGarry, C-A, Pope, L, Brend, S, Coxon, D, Baker, K, Kaye, K, Collins, L, Wallis, M, Brown, R, Roberts, L, Taylor, S, Pearson, T, Bishop, T, Dunne, P, Coutts-McClelland, K, Oliver, L, Dawe, C, and Welbergen, JA (2021). Estimating flying-fox mortality associated with abandonments of pups and extreme heat events during the austral summer of 2019-20. Pacific Conservation Biology , .
Estimating flying-fox mortality associated with abandonments of pups and extreme heat events during the austral summer of 2019-20.Crossref | GoogleScholarGoogle Scholar |

Moberg GP (2000) Biological response to stress: implications for animal welfare. In ‘The biology of animal stress: basic principles and implications for animal welfare’. (Eds GP Moberg, JA Mench) pp. 1–20. (CAB International Publishing: UK) 10.1079/9780851993591.0001

Moshkin, MP, Gerlinskaya, LA, Zavjalov, EL, Kolosova, IE, Rogovin, KA, and Randall, JA (2003). Stress and nutrition in the wild. Recent Advances in Animal Nutrition in Australia 14, 11–22.

Nelson, JE (1965). Movements of Australian flying foxes (Pteropodidae: Megachiroptera). Australian Journal of Zoology 13, 53–73.
Movements of Australian flying foxes (Pteropodidae: Megachiroptera).Crossref | GoogleScholarGoogle Scholar |

Parry-Jones, K, Webster, KN, and Divljan, A (2016). Baseline levels of faecal glucocorticoid metabolites and indications of chronic stress in the vulnerable grey-headed flying-fox, Pteropus poliocephalus. Australian Mammalogy 38, 195–203.
Baseline levels of faecal glucocorticoid metabolites and indications of chronic stress in the vulnerable grey-headed flying-fox, Pteropus poliocephalus.Crossref | GoogleScholarGoogle Scholar |

Roberts, BJ, Catterall, CP, Eby, P, and Kanowski, J (2012). Long-distance and frequent movements of the flying-fox Pteropus poliocephalus: implications for management. PLoS ONE 7, e42532.
Long-distance and frequent movements of the flying-fox Pteropus poliocephalus: implications for management.Crossref | GoogleScholarGoogle Scholar | 22880021PubMed |

Szott, ID, Pretorius, Y, Ganswindt, A, and Koyama, NF (2019). Physiological stress response of African elephants to wildlife tourism in Madikwe Game Reserve, South Africa. Wildlife Research 47, 34–43.
Physiological stress response of African elephants to wildlife tourism in Madikwe Game Reserve, South Africa.Crossref | GoogleScholarGoogle Scholar |

Tamworth Regional Council (2017) Flying-fox camp management plan: Peel River camp. (Tamworth Regional Council: Tamworth, NSW).

Taylor K, Field H, Harrison C, Durrheim D, Cox-Witton K (2017) ‘Flying-fox mass mortality event – spring/summer 2016–17’. (Wildlife Health Australia: Sydney). Available at https://wildlifehealthaustralia.com.au/Portals/0/Documents/Ongoing%20Incidents/Flying-fox_mass_mortality_2016-17_-_report_V2.pdf. [Accessed 2 August 2021]

Tennessen JB, Parks SE, Langkilde TL (2016) Anthropogenic noise and physiological stress in wildlife. In ‘The effects of noise on aquatic life II. Advances in experimental medicine and biology’. (Eds A Popper, A Hawkins) pp. 1145–1148. (Springer: New York) 10.1007/978-1-4939-2981-8_142

Waldner, CL (2014). Cow attributes, herd management, and reproductive history events associated with abortion in cow-calf herds from Western Canada. Theriogenology 81, 840–848.
Cow attributes, herd management, and reproductive history events associated with abortion in cow-calf herds from Western Canada.Crossref | GoogleScholarGoogle Scholar | 24472651PubMed |

Welbergen, JA (2011). Fit females and fat polygynous males: seasonal body mass changes in the grey-headed flying-fox. Oecologia 165, 629–637.
Fit females and fat polygynous males: seasonal body mass changes in the grey-headed flying-fox.Crossref | GoogleScholarGoogle Scholar | 21153744PubMed |

Welbergen, JA, Klose, SM, Markus, N, and Eby, P (2008). Climate change and the effects of temperature extremes on Australian flying-foxes. Proceedings of the Royal Society B: Biological Sciences 275, 419–425.
Climate change and the effects of temperature extremes on Australian flying-foxes.Crossref | GoogleScholarGoogle Scholar | 18048286PubMed |

Welbergen, JA, Meade, J, Field, HE, Edson, D, McMichael, L, Shoo, LP, Praszczalek, J, Smith, C, and Martin, JM (2020). Extreme mobility of the world’s largest flying mammals creates key challenges for management and conservation. BMC Biology 18, 101.
Extreme mobility of the world’s largest flying mammals creates key challenges for management and conservation.Crossref | GoogleScholarGoogle Scholar | 32819385PubMed |

Wildlife Health Australia (2021) Report an incident. Available at https://wildlifehealthaustralia.com.au/DiseaseIncidents/ReportanIncident.aspx. [Accessed 2 August 2021]

Wilmut, I, Sales, DI, and Ashworth, CJ (1986). Maternal and embryonic factors associated with prenatal loss in mammals. Reproduction 76, 851–864.
Maternal and embryonic factors associated with prenatal loss in mammals.Crossref | GoogleScholarGoogle Scholar |