Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Variation in fur properties may explain differences in heat-related mortality among Australian flying-foxes

Himali Udeshinie Ratnayake https://orcid.org/0000-0003-2463-4764 A B E , Justin Arno Welbergen C , Rodney van der Ree A D and Michael Ray Kearney A
+ Author Affiliations
- Author Affiliations

A School of BioSciences, The University of Melbourne, Parkville, Vic. 3010, Australia.

B Department of Zoology and Environment Sciences, University of Colombo, PO Box 1490, Colombo 00300, Sri Lanka.

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

D Ecology and Infrastructure International Pty Ltd, PO Box 6031, Wantirna, Vic. 3152, Australia.

E Corresponding author. Email: h.u.ratnayake@gmail.com

Australian Journal of Zoology - https://doi.org/10.1071/ZO20040
Submitted: 1 June 2020  Accepted: 29 March 2021   Published online: 26 April 2021

Abstract

Fur properties play a critical role in the thermoregulation of mammals and are becoming of particular interest as the frequency, intensity, and duration of extreme heat events are increasing under climate change. Australian flying-foxes are known to experience mass die-offs during extreme heat events, yet little is known about how different fur properties affect their thermoregulatory needs. In this study, we examined the differences and patterns in fur properties among and within the four mainland Australian flying-fox species: Pteropus poliocephalus, P. alecto, P. conspicillatus, and P. scapulatus. Using museum specimens, we collected data on fur solar reflectance, fur length and fur depth from the four species across their distribution. We found that P. poliocephalus had significantly longer and deeper fur, and P. alecto had significantly lower fur solar reflectivity, compared with the other species. Across all species, juveniles had deeper fur than adults, and females of P. alecto and P. conspicillatus had deeper fur than males. The biophysical effects of these fur properties are complex and contingent on the degree of exposure to solar radiation, but they may help to explain the relatively higher mortality of P. alecto and of juveniles and females that is commonly observed during extreme heat events.

Keywords: extreme heat events, flying-foxes, fruit bats, fur, hair, heat budget, heat stress, Pteropus


References

Bartholomew, G. A., Leitner, P., and Nelson, J. E. (1964). Body temperature, oxygen consumption, and heart rate in three species of Australian flying foxes. Physiological Zoology 37, 179–198.
Body temperature, oxygen consumption, and heart rate in three species of Australian flying foxes.Crossref | GoogleScholarGoogle Scholar |

Bates, D., Mächler, M., Bolker, B., and Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |

Bicca-Marques, J. C., and Calegaro-Marques, C. (1998). Behavioral thermoregulation in a sexually and developmentally dichromatic neotropical primate, the black-and-gold howling monkey (Alouatta caraya). American Journal of Physical Anthropology 106, 533–546.
Behavioral thermoregulation in a sexually and developmentally dichromatic neotropical primate, the black-and-gold howling monkey (Alouatta caraya).Crossref | GoogleScholarGoogle Scholar | 9712481PubMed |

Briscoe, N. J., Krockenberger, A., Handasyde, K. A., and Kearney, M. R. (2015). Bergmann meets Scholander: geographical variation in body size and insulation in the koala is related to climate. Journal of Biogeography 42, 791–802.
Bergmann meets Scholander: geographical variation in body size and insulation in the koala is related to climate.Crossref | GoogleScholarGoogle Scholar |

Buckley, L. B., and Huey, R. B. (2016). Temperature extremes: geographic patterns, recent changes, and implications for organismal vulnerabilities. Global Change Biology 22, 3829–3842.
Temperature extremes: geographic patterns, recent changes, and implications for organismal vulnerabilities.Crossref | GoogleScholarGoogle Scholar | 27062158PubMed |

Caro, T. (2009). Contrasting coloration in terrestrial mammals. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 364, 537–548.
Contrasting coloration in terrestrial mammals.Crossref | GoogleScholarGoogle Scholar | 18990666PubMed |

Churchill, S. (2009) ‘Australian Bats.’ 2nd edn. (Allen & Unwin: Sydney.)

Conley, K. E., and Porter, W. P. (1986). Heat loss from deer mice (Peromyscus): evaluation of seasonal limits to thermoregulation. The Journal of Experimental Biology 126, 249–269.
| 3805994PubMed |

Currey, K., Kendal, D., Van der Ree, R., and Lentini, P. E. (2018). Land manager perspectives on conflict mitigation strategies for urban flying-fox camps. Diversity 10, 39.
Land manager perspectives on conflict mitigation strategies for urban flying-fox camps.Crossref | GoogleScholarGoogle Scholar |

Dawson, W. R. (1982). Evaporative losses of water by birds. Comparative Biochemistry and Physiology. Part A, Physiology 71, 495–509.
Evaporative losses of water by birds.Crossref | GoogleScholarGoogle Scholar |

Dawson, T. J., and Fanning, F. D. (1981). Thermal and energetic problems of semiaquatic mammals: a study of the Australian water rat, including comparisons with the platypus. Physiological Zoology 54, 285–296.
Thermal and energetic problems of semiaquatic mammals: a study of the Australian water rat, including comparisons with the platypus.Crossref | GoogleScholarGoogle Scholar |

Dawson, T. J., and Maloney, S. K. (2004). Fur versus feathers: the different roles of red kangaroo fur and emu feathers in thermoregulation in the Australian arid zone. Australian Mammalogy 26, 145–152.
Fur versus feathers: the different roles of red kangaroo fur and emu feathers in thermoregulation in the Australian arid zone.Crossref | GoogleScholarGoogle Scholar |

Dawson, T. J., Webster, K. N., and Maloney, S. K. (2014). The fur of mammals in exposed environments; do crypsis and thermal needs necessarily conflict? The polar bear and marsupial koala compared. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 184, 273–284.
The fur of mammals in exposed environments; do crypsis and thermal needs necessarily conflict? The polar bear and marsupial koala compared.Crossref | GoogleScholarGoogle Scholar | 24366474PubMed |

Diamond, M. E., and Arabzadeh, E. (2013). Whisker sensory system – from receptor to decision. Progress in Neurobiology 103, 28–40.
Whisker sensory system – from receptor to decision.Crossref | GoogleScholarGoogle Scholar | 22683381PubMed |

Dominoni, D., Smit, J. A. H., Visser, M. E., and Halfwerk, W. (2020). Multisensory pollution: artificial light at night and anthropogenic noise have interactive effects on activity patterns of great tits (Parus major). Environmental Pollution 256, 113314.
Multisensory pollution: artificial light at night and anthropogenic noise have interactive effects on activity patterns of great tits (Parus major).Crossref | GoogleScholarGoogle Scholar | 31761596PubMed |

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.
Seasonal movements of grey-headed flying-foxes, Pteropus poliocephalus (Chiroptera: Pteropodidae), from two maternity camps in northern New South Wales.Crossref | GoogleScholarGoogle Scholar |

Gates, D. M. (1980). ‘Biophysical Ecology.’ (Springer-Verlag: New York, Heidelberg, Berlin.)

Hall, L. S., and Richards, G. (2000). ‘Flying Foxes: Fruit and Blossom Bats of Australia.’ (UNSW Press: Sydney.)

Hammel, H. T. (1955). Thermal properties of fur. The American Journal of Physiology 182, 369–376.
Thermal properties of fur.Crossref | GoogleScholarGoogle Scholar | 13258817PubMed |

Huey, R. B., Kearney, M. R., Krockenberger, A., Holtum, J. A. M., Jess, M., and Williams, S. E. (2012). Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 367, 1665–1679.
Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation.Crossref | GoogleScholarGoogle Scholar | 22566674PubMed |

Hutchinson, J. C. D., and Brown, G. D. (1969). Penetrance of cattle coats by radiation. Journal of Applied Physiology 26, 454–464.
Penetrance of cattle coats by radiation.Crossref | GoogleScholarGoogle Scholar |

Kearney, M. R., and Porter, W. P. (2017). NicheMapR – an R package for biophysical modelling: the microclimate model. Ecography 40, 664–674.
NicheMapR – an R package for biophysical modelling: the microclimate model.Crossref | GoogleScholarGoogle Scholar |

Kearney, M. R., Porter, W. P., and Huey, R. B. (2021). Modelling the joint effects of body size and microclimate on heat budgets and foraging opportunities of ectotherms. Methods in Ecology and Evolution 12, 458–467.
Modelling the joint effects of body size and microclimate on heat budgets and foraging opportunities of ectotherms.Crossref | GoogleScholarGoogle Scholar |

Klir, J. J., and Heath, J. E. (1992). An infrared thermographic study of surface temperature in relation to external thermal stress in three species of foxes: the red fox (Vulpes vulpes), Arctic fox (Alopex lagopus), and kit fox (Vulpes macrotis). Physiological Zoology 65, 1011–1021.
An infrared thermographic study of surface temperature in relation to external thermal stress in three species of foxes: the red fox (Vulpes vulpes), Arctic fox (Alopex lagopus), and kit fox (Vulpes macrotis).Crossref | GoogleScholarGoogle Scholar |

Madej, J. P., Mikulová, L., Gorošová, A., Mikula, Š., Řehák, Z., Tichý, F., and Buchtová, M. (2013). Skin structure and hair morphology of different body parts in the common pipistrelle (Pipistrellus pipistrellus). Acta Zoologica 94, 478–489.

Mathewson, P. D., and Porter, W. P. (2013). Simulating polar bear energetics during a seasonal fast using a mechanistic model. PLoS One 8, e72863.
Simulating polar bear energetics during a seasonal fast using a mechanistic model.Crossref | GoogleScholarGoogle Scholar | 24019883PubMed |

McKechnie, A. E., Hockey, P. A. R., and Wolf, B. O. (2012). Feeling the heat: Australian landbirds and climate change. Emu 112, i–vii.
Feeling the heat: Australian landbirds and climate change.Crossref | GoogleScholarGoogle Scholar |

Meehl, G. A., and Tebaldi, C. (2004). More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305, 994–997.
More intense, more frequent, and longer lasting heat waves in the 21st century.Crossref | GoogleScholarGoogle Scholar | 15310900PubMed |

Noll, U. (1979). Postnatal growth and development of thermogenesis in Rousettus aegyptiacus. Comparative Biochemistry and Physiology. A. Comparative Physiology 63, 89–93.
Postnatal growth and development of thermogenesis in Rousettus aegyptiacus.Crossref | GoogleScholarGoogle Scholar |

Porter, W. P., and Gates, D. M. (1969). Thermodynamic equilibria of animals with environment. Ecological Monographs 39, 227–244.
Thermodynamic equilibria of animals with environment.Crossref | GoogleScholarGoogle Scholar |

Porter, W. P., and Mitchell, J. W. (2006). Method and system for calculating the spatial–temporal effects of climate and other environmental conditions on animals. Patent no. US9938196. In ‘Wisconsin Alumni Research Foundation.’ (United States of America.)

Porter, W. P., Munger, J. C., Stewart, W. E., Budaraju, S., and Jaeger, J. (1994). Endotherm energetics – from a scalable individual-based model to ecological applications. Australian Journal of Zoology 42, 125–162.
Endotherm energetics – from a scalable individual-based model to ecological applications.Crossref | GoogleScholarGoogle Scholar |

R Core Team (2017). R: a language and environment for statistical computing. Version 3.4.1 (R Foundation for Statistical Computing: Vienna, Austria.)

Racey, P. A., and Speakman, J. R. (1987). The energy costs of pregnancy and lactation in heterothermic bats. Symposia of the Zoological Society of London 57, 107–125.

Ratnayake, H. U. (2018). Understanding how extreme heat events affect the heat budgets of Australian flying-foxes (Pteropus spp.): roles of morphology, physiology and behaviour. Ph.D. Thesis, The University of Melbourne, Parkville, Australia.

Ratnayake, H. U., Kearney, M. R., Govekar, P., Karoly, D., and Welbergen, J. A. (2019). Forecasting wildlife die‐offs from extreme heat events. Animal Conservation 22, 386–395.
Forecasting wildlife die‐offs from extreme heat events.Crossref | GoogleScholarGoogle Scholar |

Roberts, B., Eby, P., Tsang, S. M., and Sheherazade (2017). Pteropus alecto. The IUCN Red List of Threatened Species 2017: e.T18715A22080057.

Rymer, T. L., Kinahan, A. A., and Pillay, N. (2007). Fur characteristics of the African ice rat Otomys sloggetti robertsi: modifications for an alpine existence. Journal of Thermal Biology 32, 428–432.
Fur characteristics of the African ice rat Otomys sloggetti robertsi: modifications for an alpine existence.Crossref | GoogleScholarGoogle Scholar |

Schmidt-Nielsen, K. (1997). ‘Animal Physiology: Adaptation and Environment.’ (Cambridge University Press.)

Scholander, P. F. (1955). Evolution of climatic adaptation in homeotherms. Evolution 9, 15–26.
Evolution of climatic adaptation in homeotherms.Crossref | GoogleScholarGoogle Scholar |

Scholander, P. F., Hock, R., Walters, V., and Irving, L. (1950a). Adaptation to cold in Arctic and tropical mammals and birds in relation to body temperature, insulation, and basal metabolic rate. The Biological Bulletin 99, 259–271.
Adaptation to cold in Arctic and tropical mammals and birds in relation to body temperature, insulation, and basal metabolic rate.Crossref | GoogleScholarGoogle Scholar | 14791423PubMed |

Scholander, P. F., Hock, R., Walters, V., Johnson, F., and Irving, L. (1950b). Heat regulation in some Arctic and tropical mammals and birds. The Biological Bulletin 99, 237–258.
Heat regulation in some Arctic and tropical mammals and birds.Crossref | GoogleScholarGoogle Scholar | 14791422PubMed |

Scholander, P. F., Walters, V., Hock, R., and Irving, L. (1950c). Body insulation of some Arctic and tropical mammals and birds. The Biological Bulletin 99, 225–236.
Body insulation of some Arctic and tropical mammals and birds.Crossref | GoogleScholarGoogle Scholar | 14791421PubMed |

Steffen, W., Hughes, L., and Perkins, S. (2014). ‘Heatwaves: Hotter, Longer, More Often.’ (Climate Council of Australia Ltd: Australia.)

Underwood, L. S., and Reynolds, P. (1980). Photoperiod and fur lengths in the Arctic fox (Alopex lagopus L.). International Journal of Biometeorology 24, 39–48.
Photoperiod and fur lengths in the Arctic fox (Alopex lagopus L.).Crossref | GoogleScholarGoogle Scholar |

Wacker, C. B., McAllan, B. M., Körtner, G., and Geiser, F. (2016). The functional requirements of mammalian hair: a compromise between crypsis and thermoregulation? Naturwissenschaften 103, 53.
The functional requirements of mammalian hair: a compromise between crypsis and thermoregulation?Crossref | GoogleScholarGoogle Scholar | 27287044PubMed |

Wagner, J. (2008) Glandular secretions of male Pteropus (flying-foxes): preliminary chemical comparisons among species. Independent Study Project (ISP) Collection 559.

Walsberg, G. E. (1988a). Consequences of skin color and fur properties for solar heat gain and ultraviolet irradiance in two mammals. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 158, 213–221.
Consequences of skin color and fur properties for solar heat gain and ultraviolet irradiance in two mammals.Crossref | GoogleScholarGoogle Scholar | 3170827PubMed |

Walsberg, G. E. (1988b). The significance of fur structure for solar heat gain in the rock squirrel, Spermophilus variegatus. The Journal of Experimental Biology 138, 243–257.
| 3193058PubMed |

Walsberg, G. E., and Schmidt, C. A. (1989). Seasonal adjustment of solar heat gain in a desert mammal by altering coat properties independently of surface coloration. The Journal of Experimental Biology 142, 387–400.

Walsberg, G. E., Weaver, T., and Wolf, B. O. (1997). Seasonal adjustment of solar heat gain independent of coat coloration in a desert mammal. Physiological Zoology 70, 150–157.
Seasonal adjustment of solar heat gain independent of coat coloration in a desert mammal.Crossref | GoogleScholarGoogle Scholar | 9231387PubMed |

Weigold, H. (1973). Jugendentwicklung der Temperaturregulation bei der Mausohrfledermaus, Myotis myotis (Borkhausen, 1797). Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 85, 169–212.

Welbergen, J. A. (2005). The social organisation of the grey-headed flying-fox. Ph.D. Thesis, University of Cambridge.

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 275, 419–425.
Climate change and the effects of temperature extremes on Australian flying-foxes.Crossref | GoogleScholarGoogle Scholar | 18048286PubMed |

West, P. M., and Packer, C. (2002). Sexual selection, temperature, and the lion’s mane. Science 297, 1339–1343.
Sexual selection, temperature, and the lion’s mane.Crossref | GoogleScholarGoogle Scholar | 12193785PubMed |

Wolf, B. O., and Walsberg, G. E. (2000). The role of the plumage in heat transfer processes of birds. American Zoologist 40, 575–584.
The role of the plumage in heat transfer processes of birds.Crossref | GoogleScholarGoogle Scholar |