The plant pathogen Phytophthora cinnamomi influences habitat use by the obligate nectarivore honey possum (Tarsipes rostratus)
Shannon J. Dundas A B C , Giles E. St J. Hardy A and Patricia A. Fleming A
+ Author Affiliations
- Author Affiliations
A School of Veterinary and Life Sciences, Murdoch University, South Street, Murdoch, WA 6152, Australia.
B Present address: NSW Department of Primary Industries, Locked Bag 6006, Orange, NSW 2800, Australia.
C Corresponding author. Email: S.Dundas@murdoch.edu.au
Australian Journal of Zoology 64(2) 122-131 https://doi.org/10.1071/ZO16019
Submitted: 15 March 2016 Accepted: 6 July 2016 Published: 12 August 2016
Abstract
Introduced plant pathogens can devastate susceptible plant communities, and consequently impact on animal communities reliant on plants for food and habitat. Specifically, plant pathogens change the floristic diversity of vegetation communities, thereby reducing availability of food sources for fauna (e.g. pollen and nectar) and result in major changes to habitat structure when canopy and understorey plant species succumb to disease. Phytophthora cinnamomi poses a threat to flowering plant species (e.g. Banksia species) which are important food sources for nectarivorous fauna. The honey possum (Tarsipes rostratus) is the only obligate nectarivorous non-flying mammal living on a restrictive diet of nectar and pollen; consequently, these tiny mammals are likely to be particularly vulnerable to the landscape-wide devastation caused by P. cinnamomi. We investigated habitat selection by honey possums in a vegetation community infested with P. cinnamomi to determine how these mammals respond to habitat affected by this pathogen. Over four seasons, 18 honey possums were fitted with radio-transmitters and tracked to identify habitat preferences. Vegetation surveys were compared for locations selected by honey possums (as determined from tracking) and randomly selected sites. Radio-tracking revealed that sites selected by honey possums were significantly taller, denser, and more floristically diverse than their paired random locations. The presence of P. cinnamomi influences habitat use by honey possums, but animals show resilience in terms of using the best of what is available in both P. cinnamomi–affected and unaffected locations. Habitat patches comprising less susceptible species, or plants that have yet to succumb to infection, provide refuge and food resources for honey possums. Management to reduce the spread of existing P. cinnamomi infestations and prevent contamination of new locations will benefit vegetation communities and associated faunal communities, while identifying honey possum food plant species that are resilient to the pathogen may support revegetation attempts.
Additional keywords: Banksia plumosa, dieback, diet, food plants, habitat selection, pollination, VHF tracking.
References
Allen, C. D., Macalady, A. K., Chenchouni, H., Bachelet, D., McDowell, N., Vennetier, M., Kitzberger, T., Rigling, A., Breshears, D. D., Hogg, E. H., Gonzalez, P., Fensham, R., Zhang, Z., Castro, J., Demidova, N., Lim, J.-H., Allard, G., Running, S. W., Semerci, A., and Cobb, N. (2010). A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management 259, 660–684.| A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests.Crossref | GoogleScholarGoogle Scholar |
Armistead, R. J. (2008). The impact of Phytophthora cinnamomi on the distribution of the yellow-footed antechinus (mardo) (Antechinus flavipes leucogaster) (Marsupialia: Dasyuridae). Ph.D. Thesis, Murdoch University, Perth.
Arrese, C., and Runham, P. B. (2001). Redefining the activity pattern of the honey possum (Tarsipes rostratus). Australian Mammalogy 23, 169–172.
| Redefining the activity pattern of the honey possum (Tarsipes rostratus).Crossref | GoogleScholarGoogle Scholar |
Bradshaw, S. D., and Bradshaw, F. J. (1999). Field energetics and the estimation of pollen and nectar intake in the marsupial honey possum, Tarsipes rostratus, in heathland habitats of south-western Australia. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 169, 569–580.
| Field energetics and the estimation of pollen and nectar intake in the marsupial honey possum, Tarsipes rostratus, in heathland habitats of south-western Australia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2FpvFekuw%3D%3D&md5=0625ecfa3b1f11eef8a1ae67012f6900CAS | 10633562PubMed |
Bradshaw, S. D., and Bradshaw, F. J. (2002). Short-term movements and habitat use of the marsupial honey possum (Tarsipes rostratus). Journal of Zoology 258, 343–348.
| Short-term movements and habitat use of the marsupial honey possum (Tarsipes rostratus).Crossref | GoogleScholarGoogle Scholar |
Bradshaw, S. D., Phillips, R. D., Tomlinson, S., Holley, R. J., Jennings, S., and Bradshaw, F. J. (2007). Ecology of the honey possum, Tarsipes rostratus, in Scott National Park, Western Australia. Australian Mammalogy 29, 25–38.
| Ecology of the honey possum, Tarsipes rostratus, in Scott National Park, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Brouwers, N., Matusick, G., Ruthrof, K., Lyons, T., and Hardy, G. (2013). Landscape-scale assessment of tree crown dieback following extreme drought and heat in a Mediterranean eucalypt forest ecosystem. Landscape Ecology 28, 69–80.
| Landscape-scale assessment of tree crown dieback following extreme drought and heat in a Mediterranean eucalypt forest ecosystem.Crossref | GoogleScholarGoogle Scholar |
Clancy, R. L. (2011). The dispersal of honey possums, Tarsipes rostratus, in relation to habitat fragmentation and fire. Ph.D. Thesis, University of Western Australia, Nedlands.
Clarke, K. R., and Warwick, R. M. (1994). ‘Change in Marine Communities: an Approach to Statistical Analysis and Interpretation.’ (Natural Environment Research Council: Plymouth Marine Laboratory, Plymouth, UK.)
Davis, R. A., Valentine, L. E., Craig, M. D., Wilson, B., Bancroft, W. J., and Mallie, M. (2014). Impact of Phytophthora-dieback on birds in Banksia woodlands in south west Western Australia. Biological Conservation 171, 136–144.
| Impact of Phytophthora-dieback on birds in Banksia woodlands in south west Western Australia.Crossref | GoogleScholarGoogle Scholar |
Dundas, S. J., Fleming, P. A., and Hardy, G. E. S. J. (2013). Flower visitation by honey possums (Tarsipes rostratus) in a coastal banksia heathland infested with the plant pathogen Phytophthora cinnamomi. Australian Mammalogy 35, 166–174.
| Flower visitation by honey possums (Tarsipes rostratus) in a coastal banksia heathland infested with the plant pathogen Phytophthora cinnamomi.Crossref | GoogleScholarGoogle Scholar |
Dunstan, W. A., Rudman, T., Shearer, B. L., Moore, N. A., Paap, T., Calver, M. C., Dell, B., and Hardy, G. E. S. J. (2010). Containment and spot eradication of a highly destructive, invasive plant pathogen (Phytophthora cinnamomi) in natural ecosystems. Biological Invasions 12, 913–925.
| Containment and spot eradication of a highly destructive, invasive plant pathogen (Phytophthora cinnamomi) in natural ecosystems.Crossref | GoogleScholarGoogle Scholar |
Everaardt, A. (2003). The impact of fire on the honey possum Tarsipes rostratus in the Fitzgerald River National Park, Western Australia. Ph.D. Thesis, Murdoch University, Perth.
Garavanta, C. A. M. (1997). A mark-recapture study of the social organisation of the honey possum Tarsipes rostratus in the Fitzgerald River National Park, Western Australia. Ph.D. Thesis, Murdoch University, Perth.
Garavanta, C. A. M., Wooller, R. D., and Richardson, K. C. (2000). Movement patterns of honey possums, Tarsipes rostratus, in the Fitzgerald River National Park, Western Australia. Wildlife Research 27, 179–183.
| Movement patterns of honey possums, Tarsipes rostratus, in the Fitzgerald River National Park, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Garkaklis, M., Calver, M., Wilson, B., and Hardy, G. E. S. J. (2004). Habitat alteration caused by an introduced plant disease, Phytophthora cinnamomi: a potential threat to the conservation of Australian forest fauna. In ‘Conservation of Australias Forest Fauna’. pp. 899–913. (Royal Zoological Society of New South Wales: Sydney.)
Hammer, Ø., Harper, D. A. T., and Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis version 3.10. Palaeontologia Electronica 4, 9.
Hardy, G. E. S. J., Barrett, S., and Shearer, B. L. (2001). The future of phosphite as a fungicide to control the soilborne plant pathogen Phytophthora cinnamomi in natural ecosystems. Australasian Plant Pathology 30, 133–139.
| The future of phosphite as a fungicide to control the soilborne plant pathogen Phytophthora cinnamomi in natural ecosystems.Crossref | GoogleScholarGoogle Scholar |
Hüberli, D, Tommerup, I. C., and Hardy, G. E. S. J. (2000). False negative isolations or absence of lesions may cause mis-diagnosis of diseased plants infected with Phytophthora cinnamomi. Australasian Plant Pathology 29, 164–169.
Jurskis, V. (2005). Eucalypt decline in Australia, and a general concept of tree decline and dieback. Forest Ecology and Management 215, 1–20.
| Eucalypt decline in Australia, and a general concept of tree decline and dieback.Crossref | GoogleScholarGoogle Scholar |
Kennedy, J., and Weste, G. (1986). Vegetation changes associated with invasion by Phytophthora cinnamomi on monitored sites in the Grampians, Western Victoria. Australian Journal of Botany 34, 251–279.
| Vegetation changes associated with invasion by Phytophthora cinnamomi on monitored sites in the Grampians, Western Victoria.Crossref | GoogleScholarGoogle Scholar |
Kenward, R. E. (2001). ‘A Manual for Wildlife Radio Tagging.’ (Academic Press: San Diego.)
Laidlaw, W. S., and Wilson, B. A. (2006). Habitat utilisation by small mammals in a coastal heathland exhibiting symptoms of Phytophthora cinnamomi infestation. Wildlife Research 33, 639–649.
| Habitat utilisation by small mammals in a coastal heathland exhibiting symptoms of Phytophthora cinnamomi infestation.Crossref | GoogleScholarGoogle Scholar |
Law, B. S. (1993). Roosting and foraging ecology of the Queensland blossom bat (Syconycteris australis) in north-eastern New South Wales: flexibility in response to seasonal variation. Wildlife Research 20, 419–431.
| Roosting and foraging ecology of the Queensland blossom bat (Syconycteris australis) in north-eastern New South Wales: flexibility in response to seasonal variation.Crossref | GoogleScholarGoogle Scholar |
Matusick, G., Ruthrof, K. X., Brouwers, N. C., and Hardy, G. S. J. (2014). Topography influences the distribution of autumn frost damage on trees in a Mediterranean-type Eucalyptus forest. Trees 28, 1449–1462.
| Topography influences the distribution of autumn frost damage on trees in a Mediterranean-type Eucalyptus forest.Crossref | GoogleScholarGoogle Scholar |
McFarland, D. C. (1986). Seasonal changes in the abundance and body condition of honeyeaters (Meliphagidae) in response to inflorescence and nectar availability in the New England National Park, New South Wales. Australian Journal of Ecology 11, 331–340.
| Seasonal changes in the abundance and body condition of honeyeaters (Meliphagidae) in response to inflorescence and nectar availability in the New England National Park, New South Wales.Crossref | GoogleScholarGoogle Scholar |
Mercer, J., and Leighton, S. (1999). Cheyne Bay coastal survey: Cape Riche to Pallinup River. Report for Wellstead Land Conservation District Committee, Western Australia.
Myers, N., Mittermeier, R. A., Mittermeier, C. C., da Fonseca, G. A., and Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
| Biodiversity hotspots for conservation priorities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhs1Olsr4%3D&md5=06b11d676d9cb9dfe97ce49fbcc90744CAS | 10706275PubMed |
Newell, G. R., and Wilson, B. A. (1993). The relationship between cinnamon fungus (Phytophthora cinnamomi) and the abundance of Antechinus stuartii (Dasyuridae: Marsupialia) in the Brisbane Ranges, Victoria. Wildlife Research 20, 251–259.
| The relationship between cinnamon fungus (Phytophthora cinnamomi) and the abundance of Antechinus stuartii (Dasyuridae: Marsupialia) in the Brisbane Ranges, Victoria.Crossref | GoogleScholarGoogle Scholar |
Pyšek, P., and Richardson, D. M. (2010). Invasive species, environmental change and management, and health. Annual Review of Environment and Resources 35, 25–55.
| Invasive species, environmental change and management, and health.Crossref | GoogleScholarGoogle Scholar |
Russell, E. M., and Renfree, M. B. (1989). Tarsipedidae. In ‘Fauna of Australia Volume 1B’. (Ed. W. W. Walton.) pp. 769–782. (Australian Government Publishing Service: Canberra.)
Saffer, V. M. (1998). A comparison of foodplant utilisation by nectar-feeding marsupials and birds in the Fitzgerald River National Park, Western Australia. Ph.D. Thesis, Murdoch University, Perth.
Shearer, B. L., Crane, C. E., and Cochrane, A. (2004). Quantification of the susceptibility of the native flora of the South-West Botanical Province, Western Australia, to Phytophthora cinnamomi. Australian Journal of Botany 52, 435–443.
| Quantification of the susceptibility of the native flora of the South-West Botanical Province, Western Australia, to Phytophthora cinnamomi.Crossref | GoogleScholarGoogle Scholar |
Shearer, B. L., Crane, C. E., Barrett, S., and Cochrane, A. (2007). Phytophthora cinnamomi invasion, a major threatening process to conservation of flora diversity in the South-west Botanical Province of Western Australia. Australian Journal of Botany 55, 225–238.
| Phytophthora cinnamomi invasion, a major threatening process to conservation of flora diversity in the South-west Botanical Province of Western Australia.Crossref | GoogleScholarGoogle Scholar |
Shearer, B., Crane, C., Fairman, R., and Dunne, C. (2009). Ecosystem dynamics altered by pathogen-mediated changes following invasion of Banksia woodland and Eucalyptus marginata forest biomes of south-western Australia by Phytophthora cinnamomi. Australasian Plant Pathology 38, 417–436.
| Ecosystem dynamics altered by pathogen-mediated changes following invasion of Banksia woodland and Eucalyptus marginata forest biomes of south-western Australia by Phytophthora cinnamomi.Crossref | GoogleScholarGoogle Scholar |
Shearer, B., Crane, C., and Dunne, C. (2012). Variation in vegetation cover between shrubland, woodland and forest biomes invaded by Phytophthora cinnamomi. Australasian Plant Pathology 41, 413–424.
| Variation in vegetation cover between shrubland, woodland and forest biomes invaded by Phytophthora cinnamomi.Crossref | GoogleScholarGoogle Scholar |
Statsoft Inc (2006). ‘STATISTICA (Data Analysis Software System). Version 7.1.’
Swei, A., Ostfeld, R. S., Lane, R. S., and Briggs, C. J. (2011). Effects of an invasive forest pathogen on abundance of ticks and their vertebrate hosts in a California Lyme disease focus. Oecologia 166, 91–100.
| Effects of an invasive forest pathogen on abundance of ticks and their vertebrate hosts in a California Lyme disease focus.Crossref | GoogleScholarGoogle Scholar | 20941513PubMed |
Tempel, D. J., and Tietje, W. D. (2006). Potential effects of sudden oak death on small mammals and herpetofauna in coast live oak (Quercus agrifolia) woodlands. In ‘Proceedings of the Sudden Oak Death Second Science Symposium: the State of Our Knowledge, Albany, California, USA’. (Eds S. J. Frankel, P. J. Shea and M. I. Haverty.) pp. 233–236.
Whelan, J. K. (2003). The impact of Phytophthora cinnamomi on the abundance and mycophagous diet of the bush rat (Rattus fuscipes). B.Sc.(Honours) Thesis, Murdoch University, Perth.
Wills, R. T. (1993). The ecological impact of Phytophthora cinnamomi in the Stirling Range National Park, Western Australia. Australian Journal of Ecology 18, 145–159.
| The ecological impact of Phytophthora cinnamomi in the Stirling Range National Park, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Withers, P. C., Richardson, K. C., and Wooller, R. D. (1989). Metabolic physiology of euthermic and torpid honey possums, Tarsipes rostratus. Australian Journal of Zoology 37, 685–693.
| Metabolic physiology of euthermic and torpid honey possums, Tarsipes rostratus.Crossref | GoogleScholarGoogle Scholar |
Wooller, R. D., Renfree, M. B., Russell, E. M., Dunning, A., Green, S. W., and Duncan, P. (1981). Seasonal changes in a population of the nectar-feeding marsupial Tarsipes spencerae (Marsupialia: Tarsipedidae). Journal of Zoology 195, 267–279.
| Seasonal changes in a population of the nectar-feeding marsupial Tarsipes spencerae (Marsupialia: Tarsipedidae).Crossref | GoogleScholarGoogle Scholar |
Wooller, R. D., Russell, E. M., and Renfree, M. B. (1984). Honey possums and their food plants. In ‘Possums and Gliders’. (Eds A. P. Smith and I. D. Hume.) pp. 439–443. (Surrey Beatty: Sydney.)
Wooller, R. D., Richardson, K. C., and Collins, B. G. (1993). The relationship between nectar supply and the rate of capture of a nectar-dependent small marsupial Tarsipes rostratus. Journal of Zoology 229, 651–658.
| The relationship between nectar supply and the rate of capture of a nectar-dependent small marsupial Tarsipes rostratus.Crossref | GoogleScholarGoogle Scholar |
Zentmyer, G. A. (1988). Origin and distribution of four species of Phytophthora. Transactions of the British Mycological Society 91, 367–378.
| Origin and distribution of four species of Phytophthora.Crossref | GoogleScholarGoogle Scholar |
