Torn limb from limb: the ethology of prey-processing in Tasmanian devils (Sarcophilus harrisii)
Tahlia I. Pollock
A G , David P. Hocking A B , Daniel O. Hunter C , Marissa L. Parrott D , Monika Zabinskas E and Alistair R. Evans A F
+ Author Affiliations
- Author Affiliations
A School of Biological Sciences, Monash University, Melbourne, Vic. 3800, Australia.
B Zoology, Tasmanian Museum and Art Gallery, Hobart, Tas. 7000, Australia.
C Anglesea, Vic. 3230, Australia.
D Wildlife Conservation and Science, Zoos Victoria, Parkville, Vic. 3052, Australia.
E Threatened Mammals Life Sciences, Zoos Victoria, Parkville, Vic. 3052, Australia.
F Geosciences, Museums Victoria, Melbourne, Vic. 3001, Australia.
G Corresponding author. Email: tahlia.pollock@monash.edu
Australian Mammalogy 44(1) 126-138 https://doi.org/10.1071/AM21006
Submitted: 29 January 2021 Accepted: 21 June 2021 Published: 9 August 2021
Abstract
The success of carnivorous mammals is determined not only by their ability to locate and kill prey, but also their efficiency at consuming it. Breaking large prey into small pieces is challenging due to the strong and tough materials that make up a carcass (e.g. hide, muscle, and bone). Carnivores therefore require a diverse suite of prey-processing behaviours to utilise their catch. Tasmanian devils are Australia’s only large marsupial scavengers and have the ability to consume almost all of a carcass. To determine how they do this we analysed 5.5 hours of footage from 21 captive and wild devils feeding at carcasses. We documented 6320 bouts of 12 distinct prey-processing behaviours, performed at frequencies that varied throughout feeds and between groups. The time point in the feed influenced the types of behaviours used. This is likely due to changing prey size, as different techniques appear better suited to handling whole carcasses or large pieces (pulling and pinning) or smaller pieces (holding and manipulating). Group size impacted the frequency of social pulling behaviours, which increased with the number of animals. Our findings highlight the range of prey-processing behaviours performed by scavenging devils when handling, breaking down, and consuming a carcass. The devils’ repertoire shares similarities with large carnivores that handle and consume whole carcasses as well as small carnivores that are adept in grasping and handling smaller prey.
Keywords: carcass feed, carnivore, diet, ethology, feeding behaviour, marsupial, prey processing, Sarcophilus harrisii, Tasmanian devil.
References
Andersen, G. E., Johnson, C. N., Barmuta, L. A., and Jones, M. E. (2017). Dietary partitioning of Australia’s two marsupial hypercarnivores, the Tasmanian devil and the spotted-tailed quoll, across their shared distributional range. PLoS One 12, e0188529.| Dietary partitioning of Australia’s two marsupial hypercarnivores, the Tasmanian devil and the spotted-tailed quoll, across their shared distributional range.Crossref | GoogleScholarGoogle Scholar | 29176811PubMed |
Bell, O., Jones, M. E., Ruiz‐Aravena, M., Hamede, R. K., Bearhop, S., and McDonald, R. A. (2020). Age‐related variation in the trophic characteristics of a marsupial carnivore, the Tasmanian devil Sarcophilus harrisii. Ecology and Evolution 10, 7861–7871.
| Age‐related variation in the trophic characteristics of a marsupial carnivore, the Tasmanian devil Sarcophilus harrisii.Crossref | GoogleScholarGoogle Scholar | 32760570PubMed |
Buchmann, O. L., and Guiler, E. R. (1977). Behaviour and ecology of the Tasmanian devil, Sarcophilus harrisii. In ‘The biology of marsupials.’ pp. 155–168. (Springer.)
Cunningham, C. X., Comte, S., McCallum, H., Hamilton, D. G., Hamede, R., Storfer, A., Hollings, T., Ruiz‐Aravena, M., Kerlin, D. H., and Brook, B. W. (2021). Quantifying 25 years of disease‐caused declines in Tasmanian devil populations: host density drives spatial pathogen spread. Ecology Letters 24, 958–969.
| Quantifying 25 years of disease‐caused declines in Tasmanian devil populations: host density drives spatial pathogen spread.Crossref | GoogleScholarGoogle Scholar | 33638597PubMed |
Elbroch, L. M., and Quigley, H. (2017). Social interactions in a solitary carnivore. Current Zoology 63, 357–362.
| 29491995PubMed |
Ewer, R. F. (1968). ‘Ethology of mammals.’ (Logos Press Limited: London.)
Ewer, R. F. (1969). Some observations on the killing and eating of prey by two dasyurid marsupials: the Mulgara, Dasycercus cristicauda, and the Tasmanian devil, Sarcophilus harrisi. Zeitschrift für Tierpsychologie 26, 23–38.
| Some observations on the killing and eating of prey by two dasyurid marsupials: the Mulgara, Dasycercus cristicauda, and the Tasmanian devil, Sarcophilus harrisi.Crossref | GoogleScholarGoogle Scholar |
Ewer, R. (1973). ‘The carnivores.’ (Cornell University Press: Ithaca, NY.)
Friard, O., and Gamba, M. (2016). BORIS: a free, versatile open‐source event‐logging software for video/audio coding and live observations. Methods in Ecology and Evolution 7, 1325–1330.
| BORIS: a free, versatile open‐source event‐logging software for video/audio coding and live observations.Crossref | GoogleScholarGoogle Scholar |
Fujii, J. A., McLeish, D., Brooks, A. J., Gaskell, J., and Van Houtan, K. S. (2018). Limb-use by foraging marine turtles, an evolutionary perspective. PeerJ 6, e4565.
| Limb-use by foraging marine turtles, an evolutionary perspective.Crossref | GoogleScholarGoogle Scholar | 29610708PubMed |
Gilchrist, J., Jennings, A., Veron, G., and Cavallini, P. (2009). Family Herpestidae (mongooses). In ‘Handbook of mammals of the world. Vol. 1. Carnivores’. (Eds D.E. Wilson and R.A. Mittermeier.) pp. 262–328. (Lynx Edicions: Barcelona)
Green, R. H. (1967). Notes on the devil (Sarcophilus harrisi) and the quoll (Dasyurus viverrinus) in north-eastern Tasmania. Records of the Queen Victoria Museum Launceston 27, 1–13.
Guilder, J., Barca, B., Arroyo-Arce, S., Gramajo, R., and Salom-Pérez, R. (2015). Jaguars (Panthera onca) increase kill utilization rates and share prey in response to seasonal fluctuations in nesting green turtle (Chelonia mydas mydas) abundance in Tortuguero National Park, Costa Rica. Mammalian Biology 80, 65–72.
| Jaguars (Panthera onca) increase kill utilization rates and share prey in response to seasonal fluctuations in nesting green turtle (Chelonia mydas mydas) abundance in Tortuguero National Park, Costa Rica.Crossref | GoogleScholarGoogle Scholar |
Guiler, E. (1970). Obsevations on the Tasmanian devil, Sarcophilus harrisii (Marsupialia: Dasyuridae) I. Numbers, home, range, movements and food in two populations. Australian Journal of Zoology 18, 49–62.
| Obsevations on the Tasmanian devil, Sarcophilus harrisii (Marsupialia: Dasyuridae) I. Numbers, home, range, movements and food in two populations.Crossref | GoogleScholarGoogle Scholar |
Hall, K., and Schaller, G. B. (1964). Tool-using behavior of the California sea otter. Journal of Mammalogy 45, 287–298.
| Tool-using behavior of the California sea otter.Crossref | GoogleScholarGoogle Scholar |
Hamede, R. K., Mccallum, H., and Jones, M. (2008). Seasonal, demographic and density‐related patterns of contact between Tasmanian devils (Sarcophilus harrisii): Implications for transmission of devil facial tumour disease. Austral Ecology 33, 614–622.
| Seasonal, demographic and density‐related patterns of contact between Tasmanian devils (Sarcophilus harrisii): Implications for transmission of devil facial tumour disease.Crossref | GoogleScholarGoogle Scholar |
Hawkins, C. E., McCallum, H., Mooney, N., Jones, M., and Holdsworth, M. (2008). Sarcophilus harrisii. The IUCN Red List of Threatened Species 2008(e.T40540A10331066).
Hocking, D. P., Ladds, M. A., Slip, D. J., Fitzgerald, E. M., and Evans, A. R. (2017). Chew, shake, and tear: prey processing in Australian sea lions (Neophoca cinerea). Marine Mammal Science 33, 541–557.
| Chew, shake, and tear: prey processing in Australian sea lions (Neophoca cinerea).Crossref | GoogleScholarGoogle Scholar |
Hogg, C., and Hockley, J. (2013). DPIPWE/ZAA husbandry guidelines for Tasmanian devil, Sarcophilus harrisii. Australia: Zoo and Aquarium Association.
Hogg, C., Fox, S., Pemberton, D., and Belov, K. (2019). ‘Saving the Tasmanian devil: recovery through science-based management.’ (CSIRO Publishing: Melbourne, Vic., Australia.)
Holekamp, K., and Kolowski, J. (2009). Family Hyaenidae (hyenas). In ‘Handbook of mammals of the world. Vol. 1. Carnivores’. (Eds D.E. Wilson and R.A. Mittermeier.) pp. 234–260. (Lynx Edicions: Barcelona)
Hunter, D. O., Britz, T., Jones, M., and Letnic, M. (2015). Reintroduction of Tasmanian devils to mainland Australia can restore top-down control in ecosystems where dingoes have been extirpated. Biological Conservation 191, 428–435.
| Reintroduction of Tasmanian devils to mainland Australia can restore top-down control in ecosystems where dingoes have been extirpated.Crossref | GoogleScholarGoogle Scholar |
Iwaniuk, A. N., and Whishaw, I. Q. (2000). On the origin of skilled forelimb movements. Trends in neurosciences 23, 372–376.
| On the origin of skilled forelimb movements.Crossref | GoogleScholarGoogle Scholar | 10906801PubMed |
Izzard, S., Barnard, O., and Schaap, D. (2019). Managing and maintaining wild temperament and behaviours in captivity. In ‘Saving the Tasmanian devil: recovery through science-based management’. pp. 207–221. (CSIRO Publishing: Melbourne, Vic., Australia.)
Johnson, C. N., and Wroe, S. (2003). Causes of extinction of vertebrates during the Holocene of mainland Australia: arrival of the dingo, or human impact? The Holocene 13, 941–948.
| Causes of extinction of vertebrates during the Holocene of mainland Australia: arrival of the dingo, or human impact?Crossref | GoogleScholarGoogle Scholar |
Jones, M. (1995). Guild structure of the large marsupial carnivores in Tasmania. PhD thesis, Zoology Department, University of Tasmania, Hobart, Tas., Australia.
Jones, M., Archer, M., and Dickman, C. (2003). ‘Predators with pouches: the biology of carnivorous marsupials.’ (CSIRO Publishing: Melbourne, Vic., Austrlaia.)
Kruuk, H. (1972). ‘The spotted hyena: a study of predation and social behavior.’ (University of Chicago Press: Chicago, IL.)
Larivière, S., and Jennings, A. (2009). Family Musterlidae (weasels and relatives). In ‘Handbook of the mammals of the world. Vol. 1 Carnivores’. (Eds D.E. Wilson and R.A. Mittermeier.) pp. 564–656. (Lynx Edicions: Barcelona.)
Lazenby, B. T., Tobler, M. W., Brown, W. E., Hawkins, C. E., Hocking, G. J., Hume, F., et al. (2018). Density trends and demographic signals uncover the longâ€term impact of transmissible cancer in Tasmanian devils. Journal of Applied Ecology 55, 1368–1379.
| Density trends and demographic signals uncover the longâ€term impact of transmissible cancer in Tasmanian devils.Crossref | GoogleScholarGoogle Scholar |
Leyhausen, P. (1979). ‘Cat behaviour. The predatory and social behaviour of domestic and wild cats.’ (Garland STPM Press.: New York.)
Lucas, P., and Luke, D. (1984). Chewing it over: basic principles of food breakdown. In ‘Food acquisition and processing in primates’. (Eds D. J. Chivers, B. A. Wood, A. Bilsborough.) pp. 283–301. (Springer: Boston, MA.)
Lucas, P. W. (2004). ‘Dental functional morphology: how teeth work.’ (Cambridge University Press: New York.)
Mech, L. D., Smith, D. W., and MacNulty, D. R. (2015). ‘Wolves on the hunt: the behavior of wolves hunting wild prey.’ (University of Chicago Press: Chicago, IL.)
Mills, S. (2004). ‘Tiger.’ (Firefly Books: North America)
Napier, J. R. (1956). The prehensile movements of the human hand. The Journal of Vone and Joint Surgery. British volume 38, 902–913.
| The prehensile movements of the human hand.Crossref | GoogleScholarGoogle Scholar |
Newberry, R. C. (1995). Environmental enrichment: increasing the biological relevance of captive environments. Applied Animal Behaviour Science 44, 229–243.
| Environmental enrichment: increasing the biological relevance of captive environments.Crossref | GoogleScholarGoogle Scholar |
Pemberton, D. (1990). Social organisation and behaviour of the Tasmanian devil, Sarcophilus harrisii. PhD thesis, Zoology Department, University of Tasmania, Hobart, Australia.
Pemberton, D., and Renouf, D. (1993). A field-study of communication and social-behavior of the Tasmanian devil at feeding sites. Australian Journal of Zoology 41, 507–526.
| A field-study of communication and social-behavior of the Tasmanian devil at feeding sites.Crossref | GoogleScholarGoogle Scholar |
Pemberton, D., Gales, S., Bauer, B., Gales, R., Lazenby, B., and Medlock, K. (2008). The diet of the Tasmanian devil, Sarcophilus harrisii, as determined from analysis of scat and stomach contents. Papers and Proceedings of the Royal Society of Tasmania 142, 13–22.
| The diet of the Tasmanian devil, Sarcophilus harrisii, as determined from analysis of scat and stomach contents.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2018). R: A language and environment for statistical computing. (R Foundation for Statistical Computing: Vienna, Austria.) Available at http://www.R-project.org
Robbins, J. R., Poncet, D., Evans, A. R., and Hocking, D. P. (2019). A rare observation of group prey processing in wild leopard seals (Hydrurga leptonyx). Polar Biology 42, 1625–1630.
| A rare observation of group prey processing in wild leopard seals (Hydrurga leptonyx).Crossref | GoogleScholarGoogle Scholar |
Rogers, T., Fox, S., Pemberton, D., and Wise, P. (2016). Sympathy for the devil: captive-management style did not influence survival, body-mass change or diet of Tasmanian devils 1 year after wild release. Wildlife Research 43, 544–552.
| Sympathy for the devil: captive-management style did not influence survival, body-mass change or diet of Tasmanian devils 1 year after wild release.Crossref | GoogleScholarGoogle Scholar |
Rosewarne, T. (2011). Understanding animal behaviours in captive insurance populations: the Tasmanian devil as a case study. BSc Honours thesis, School of Life and Environmental Sciences, Deakin University, Melbourne, Vic., Australia.
Rovinsky, D. S., Evans, A. R., Martin, D. G., and Adams, J. W. (2020). Did the thylacine violate the costs of carnivory? Body mass and sexual dimorphism of an iconic Australian marsupial. Proceedings of the Royal Society B 287, 20201537.
| Did the thylacine violate the costs of carnivory? Body mass and sexual dimorphism of an iconic Australian marsupial.Crossref | GoogleScholarGoogle Scholar | 32811303PubMed |
Rowe-Rowe, D. (1977). Prey capture and feeding behaviour of South African otters. Lammergeyer 23, 13–21.
Sandell, M. (1989). The mating tactics and spacing patterns of solitary carnivores. In ‘Carnivore behavior, ecology, and evolution’. (Ed J. L. Gittleman.) pp. 164–182. (Springer: Boston, MA.)
Schaller, G. B. (1967). ‘The deer and the tiger: a study of wildlife in India.’ (University of Chicago Press: Chicago, IL.)
Schaller, G. B. (1972). ‘The Serengeti lion: a study of predator-prey relations.’ (University of Chicago Press: Chicago, IL.)
Shepherdson, D. J., and Mellen, J. D. (1999). ‘Second nature: Environmental enrichment for captive animals.’ (Smithsonian: Washington DC.)
Sincerbox, S. N., and DiGangi, E. A. (2017). ‘Forensic taphonomy and ecology of North American scavengers.’ (Academic Press: San Diego, CA.)
Skelton, C. J., and Stannard, H. J. (2018). Preliminary investigation of social interactions and feeding behavior in captive group-housed Tasmanian devils (Sarcophilus harrisii). Journal of Applied Animal Welfare Science 21, 295–303.
| Preliminary investigation of social interactions and feeding behavior in captive group-housed Tasmanian devils (Sarcophilus harrisii).Crossref | GoogleScholarGoogle Scholar | 29350542PubMed |
Sunquist, M., and Sunquist, F. (2002). ‘Wild cats of the world.’ (University of Chicago Press: Chicago, IL.)
Sustaita, D., Pouydebat, E., Manzano, A., Abdala, V., Hertel, F., and Herrel, A. (2013). Getting a grip on tetrapod grasping: form, function, and evolution. Biological Reviews 88, 380–405.
| Getting a grip on tetrapod grasping: form, function, and evolution.Crossref | GoogleScholarGoogle Scholar | 23286759PubMed |
Van Valkenburgh, B. (1996). Feeding behavior in free-ranging, large African carnivores. Journal of Mammalogy 77, 240–254.
| Feeding behavior in free-ranging, large African carnivores.Crossref | GoogleScholarGoogle Scholar |
Wroe, S., McHenry, C., and Thomason, J. (2005). Bite club: comparative bite force in big biting mammals and the prediction of predatory behaviour in fossil taxa. Proceedings of the Royal Society of London B: Biological Sciences 272, 619–625.
| Bite club: comparative bite force in big biting mammals and the prediction of predatory behaviour in fossil taxa.Crossref | GoogleScholarGoogle Scholar |
