New evidence of seed dispersal identified in Australian mammals
Bryony J. Palmer A C , Gabrielle Beca A , Todd E. Erickson A B , Richard J. Hobbs A and Leonie E. Valentine AA School of Biological Sciences, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
B Kings Park Science, Department of Biodiversity, Conservation and Attractions, Kings Park, WA 6005, Australia.
C Corresponding author. Email: bryony.palmer@research.uwa.edu.au
Wildlife Research 48(7) 635-642 https://doi.org/10.1071/WR21015
Submitted: 13 January 2021 Accepted: 15 April 2021 Published: 18 June 2021
Abstract
Context: Mammal–seed interactions are important for structuring vegetation communities across a diverse range of ecosystems worldwide. In Australia, mammals are typically considered to be seed predators and to play insignificant roles in seed dispersal. However, very few studies have investigated endozoochorous seed dispersal in Australian species. The translocation of Australian mammals for the purposes of ecosystem restoration is increasing. Digging mammals (i.e. species that dig to obtain food or create shelter) are commonly the focus of these translocations because they are considered to be ecosystem engineers, but an understanding of their role in seed dispersal is lacking.
Aims: The aim of the present study was to expand the understanding of endozoochory in Australian digging mammals by determining whether seeds consumed by select species remain viable and able to germinate.
Methods: Scat samples were collected from five digging mammal species, known to consume seeds or fruit, across nine sites in Western and South Australia. The samples were searched for seeds, with the recovered seeds identified and tested for viability and germination capacity.
Key results: The abundance of intact seeds in scats was generally low, but 70% of the retrieved seeds appeared viable. Five species of seed germinated under laboratory conditions. These seeds were retrieved from bilby (Macrotis lagotis), boodie (Bettongia lesueur), golden bandicoot (Isoodon auratus) and quenda (I. fusciventer) scats.
Conclusions: Seeds consumed by Australian digging mammals can remain viable and germinate, indicating that digging mammals play a more important role in seed dispersal than previously considered.
Implications: Digging mammals have the potential to contribute to ecosystem restoration efforts through the dispersal of viable seeds, but there is also a risk that non-native species could be dispersed. These costs and benefits should be considered by practitioners when planning reintroductions of digging mammals.
Keywords: Bettongia, endozoochory, germination, Isoodon, Macrotis, marsupial, reintroduction, restoration, translocation.
References
Auld, T. D., and Denham, A. J. (1999). The role of ants and mammals in dispersal and post-dispersal seed predation of the shrubs Grevillea (Proteaceae). Plant Ecology 144, 201–213.| The role of ants and mammals in dispersal and post-dispersal seed predation of the shrubs Grevillea (Proteaceae).Crossref | GoogleScholarGoogle Scholar |
Auld, T. D., Denham, A. J., and Turner, K. (2007). Dispersal and recruitment dynamics in the fleshy-fruited Persoonia lanceolata (Proteaceae). Journal of Vegetation Science 18, 903–910.
| Dispersal and recruitment dynamics in the fleshy-fruited Persoonia lanceolata (Proteaceae).Crossref | GoogleScholarGoogle Scholar |
Ballardie, R. T., and Whelan, R. J. (1986). Masting, seed dispersal and seed predation in the cycad Macrozamia communis. Oecologia 70, 100–105.
| Masting, seed dispersal and seed predation in the cycad Macrozamia communis.Crossref | GoogleScholarGoogle Scholar | 28311292PubMed |
Beca, G., Palmer, B., Valentine, L. E., Erickson, T. E., and Hobbs, R. J. (2020). Gut passage time and viability of seeds consumed by Australian marsupials. Australian Mammalogy , .
| Gut passage time and viability of seeds consumed by Australian marsupials.Crossref | GoogleScholarGoogle Scholar |
Bice, J., and Moseby, K. (2008). Diets of the re-introduced greater bilby (Macrotis lagotis) and burrowing bettong (Bettongia lesueur) in the Arid Recovery Reserve, Northern South Australia. Australian Mammalogy 30, 1–12.
| Diets of the re-introduced greater bilby (Macrotis lagotis) and burrowing bettong (Bettongia lesueur) in the Arid Recovery Reserve, Northern South Australia.Crossref | GoogleScholarGoogle Scholar |
Burbidge, A. A., Harrison, P. L., and Woinarski, J. (2014) ‘The Action Plan for Australian Mammals 2012.’ (CSIRO Publishing: Melbourne, Vic., Australia.)
Carlo, T. A., Aukema, J. E., and Morales, J. M. (2007). Plant–frugivore interactions as spatially explicit networks: integrating frugivore foraging with fruiting plant spatial patterns. In ‘Seed Dispersal: Theory and its Application in a Changing World’. (Eds A. J. Dennis, E. W. Schupp, R. J. Green and D. A. Westcott.) pp. 369–390. (CABI: Reading, UK.)
Chapman, T. F. (2015). Reintroduced burrowing bettongs (Bettongia lesueur) scatter hoard sandalwood (Santalum spicatum) seed. Australian Journal of Zoology 63, 76–79.
| Reintroduced burrowing bettongs (Bettongia lesueur) scatter hoard sandalwood (Santalum spicatum) seed.Crossref | GoogleScholarGoogle Scholar |
Cochrane, J. A., Friend, J. A., and Hill, S. J. E. (2005). Endozoochory and the Australian bluebell: consumption of Billardiera fusiformis (Labill.) Payer (Pittosporaceae) seeds by three mammal species at Two Peoples Bay Nature Reserve, Western Australia. Journal of the Royal Society of Western Australia 88, 191–196.
Denham, A. J. (2008). Seed predation limits post-fire recruitment in the waratah (Telopea speciosissima). Plant Ecology 199, 9–19.
| Seed predation limits post-fire recruitment in the waratah (Telopea speciosissima).Crossref | GoogleScholarGoogle Scholar |
Dennis, A. J. (2003). Scatter-hoarding by musky rat-kangaroos, Hypsiprymnodon moschatus, a tropical rain-forest marsupial from Australia: implications for seed dispersal. Journal of Tropical Ecology 19, 619–627.
| Scatter-hoarding by musky rat-kangaroos, Hypsiprymnodon moschatus, a tropical rain-forest marsupial from Australia: implications for seed dispersal.Crossref | GoogleScholarGoogle Scholar |
Erickson, T. E., and Merritt, D. J. (2016). Seed collection, cleaning, and storage procedures. In ‘Pilbara Seed Atlas and Field Guide: Plant Restoration in Australia’s Arid Northwest’. (Eds T. E. Erickson, R. L. Barrett, D. J. Merritt, and K. W. Dixon.) pp. 7–16. (CSIRO Publishing: Melbourne, Vic., Australia.)
Erickson, T. E., Barrett, R. L., Symons, D. R., Turner, S. R., and Merritt, D. J. (2016). An atlas to the plants and seeds of the Pilbara region. In ‘Pilbara Seed Atlas and Field Guide: Plant Restoration in Australia’s Arid Northwest’. (Eds T. E. Erickson, R. L. Barrett, D. J. Merritt, and K. W. Dixon.) pp. 43–256. (CSIRO Publishing: Melbourne, Vic., Australia.)
Farwig, N., and Berens, D. G. (2012). Imagine a world without seed dispersers: a review of threats, consequences and future directions. Basic and Applied Ecology 13, 109–115.
| Imagine a world without seed dispersers: a review of threats, consequences and future directions.Crossref | GoogleScholarGoogle Scholar |
Fleming, P. A., Anderson, H., Prendergast, A. S., Bretz, M. R., Valentine, L. E., and Hardy, G. E. S. (2014). Is the loss of Australian digging mammals contributing to a deterioration in ecosystem function? Mammal Review 44, 94–108.
| Is the loss of Australian digging mammals contributing to a deterioration in ecosystem function?Crossref | GoogleScholarGoogle Scholar |
Garkaklis, M. J., Bradley, J. S., and Wooller, R. D. (2003). The relationship between animal foraging and nutrient patchiness in south-west Australian woodland soils. Australian Journal of Soil Research 41, 665–673.
| The relationship between animal foraging and nutrient patchiness in south-west Australian woodland soils.Crossref | GoogleScholarGoogle Scholar |
Gibson, L. A. (2001). Seasonal changes in the diet, food availability and food preference of the greater bilby (Macrotis lagotis) in south-western Queensland. Wildlife Research 28, 121–134.
| Seasonal changes in the diet, food availability and food preference of the greater bilby (Macrotis lagotis) in south-western Queensland.Crossref | GoogleScholarGoogle Scholar |
Gordon, C. E., and Letnic, M. (2016). Functional extinction of a desert rodent: implications for seed fate and vegetation dynamics. Ecography 39, 815–824.
| Functional extinction of a desert rodent: implications for seed fate and vegetation dynamics.Crossref | GoogleScholarGoogle Scholar |
Hulme, P. E. (2002). Seed-eaters: seed dispersal, destruction and demography. In ‘Seed Dispersal & Frugivory: Ecology, Evolution and Conservation’. (Eds D. Levey, W. R. Silva, and M. Galetti.) pp. 257–274. (CABI: Wallingford, UK.)
James, A. I., Eldridge, D. J., and Moseby, K. E. (2010). Foraging pits, litter and plant germination in an arid shrubland. Journal of Arid Environments 74, 516–520.
| Foraging pits, litter and plant germination in an arid shrubland.Crossref | GoogleScholarGoogle Scholar |
Lipsey, M. K., and Child, M. F. (2007). Combining the fields of reintroduction biology and restoration ecology. Conservation Biology 21, 1387–1390.
| Combining the fields of reintroduction biology and restoration ecology.Crossref | GoogleScholarGoogle Scholar | 18173457PubMed |
Mallen-Cooper, M., Nakagawa, S., and Eldridge, D. J. (2019). Global meta-analysis of soil-disturbing vertebrates reveals strong effects on ecosystem patterns and processes. Global Ecology and Biogeography 28, 661–679.
| Global meta-analysis of soil-disturbing vertebrates reveals strong effects on ecosystem patterns and processes.Crossref | GoogleScholarGoogle Scholar |
Marshall, V. M., Lewis, M. M., and Ostendorf, B. (2012). Buffel grass (Cenchrus ciliaris) as an invader and threat to biodiversity in arid environments: a review. Journal of Arid Environments 78, 1–12.
| Buffel grass (Cenchrus ciliaris) as an invader and threat to biodiversity in arid environments: a review.Crossref | GoogleScholarGoogle Scholar |
Merritt, D. (2006). Seed storage and testing. In ‘Australian Seeds: A Guide to their Collection, Identification and Biology’. (Eds L. Sweedman, and D. Merritt.) pp. 53–60. (CSIRO Publishing: Melbourne, Vic., Australia.)
Merritt, D., Turner, S., Clarke, S., and Dixon, K. (2007). Seed dormancy and germination stimulation syndromes for Australian temperate species. Australian Journal of Botany 55, 336–344.
| Seed dormancy and germination stimulation syndromes for Australian temperate species.Crossref | GoogleScholarGoogle Scholar |
Mills, C. H., and Letnic, M. (2018). Reversing functional extinction of mammals prompts a rethink of paradigms about seed fate in arid Australia. Royal Society Open Science 5, .
| Reversing functional extinction of mammals prompts a rethink of paradigms about seed fate in arid Australia.Crossref | GoogleScholarGoogle Scholar | 29410877PubMed |
Mills, C. H., Gordon, C. E., and Letnic, M. (2018). Rewilded mammal assemblages reveal the missing ecological functions of granivores. Functional Ecology 32, 475–485.
| Rewilded mammal assemblages reveal the missing ecological functions of granivores.Crossref | GoogleScholarGoogle Scholar |
Morton, S. R. (1985). Granivory in arid regions: comparison of Australia with North and South America. Ecology 66, 1859–1866.
| Granivory in arid regions: comparison of Australia with North and South America.Crossref | GoogleScholarGoogle Scholar |
Murphy, M., Howard, K., Hardy, G. E. S. J., and Dell, B. (2015). When losing your nuts increases your reproductive success: sandalwood (Santalum spicatum) nut caching by the woylie (Bettongia penicillata). Pacific Conservation Biology 21, 243–252.
| When losing your nuts increases your reproductive success: sandalwood (Santalum spicatum) nut caching by the woylie (Bettongia penicillata).Crossref | GoogleScholarGoogle Scholar |
Palmer, B. J., Valentine, L. E., Page, M., and Hobbs, R. J. (2020). Translocations of digging mammals and their potential for ecosystem restoration: a review of goals and monitoring programmes. Mammal Review 50, 382–398.
| Translocations of digging mammals and their potential for ecosystem restoration: a review of goals and monitoring programmes.Crossref | GoogleScholarGoogle Scholar |
Petre, C.-A., Tagg, N., Beudels-Jamar, R. C., Haurez, B., and Doucet, J.-L. (2015). Western lowland gorilla seed dispersal: are seeds adapted to long gut retention times? Acta Oecologica 67, 59–65.
| Western lowland gorilla seed dispersal: are seeds adapted to long gut retention times?Crossref | GoogleScholarGoogle Scholar |
Quin, D. G. (1985). Observations on the diet of the southern brown bandicoot, Isoodon obesulus (Marsupialia: Peramelidae), in southern Tasmania. Australian Mammalogy 11, 15–25.
Ross, C. E., McIntyre, S., Barton, P. S., Evans, M. J., Cunningham, S. A., and Manning, A. D. (2020). A reintroduced ecosystem engineer provides a germination niche for native plant species. Biodiversity and Conservation 29, 817–837.
| A reintroduced ecosystem engineer provides a germination niche for native plant species.Crossref | GoogleScholarGoogle Scholar |
South Australian Seed Conservation Centre (2018). Seeds of South Australia. (South Australian Seed Conservation Centre.) Available at https://spapps.environment.sa.gov.au/seedsofsa/ [verified 15 March 2020].
Southgate, R., and Carthew, S. M. (2006). Diet of the bilby (Macrotis lagotis) in relation to substrate, fire and rainfall characteristics in the Tanami Desert. Wildlife Research 33, 507–519.
| Diet of the bilby (Macrotis lagotis) in relation to substrate, fire and rainfall characteristics in the Tanami Desert.Crossref | GoogleScholarGoogle Scholar |
Sweedman, L. (2006). Australian seeds: a photographic guide. In ‘Australian Seeds: A Guide to their Collection, Identification and Biology’. (Eds L. Sweedman, and D. J. Merritt.) pp. 128–233. (CSIRO Publishing: Melbourne, Vic., Australia.)
Tay, N. E., Hopkins, A. J. M., Ruthrof, K. X., Burgess, T., Hardy, G. E. S., and Fleming, P. A. (2018). The tripartite relationship between a bioturbator, mycorrhizal fungi, and a key Mediterranean forest tree. Austral Ecology 43, 742–751.
| The tripartite relationship between a bioturbator, mycorrhizal fungi, and a key Mediterranean forest tree.Crossref | GoogleScholarGoogle Scholar |
Theimer, T. C., and Gehring, C. A. (2007). Mycorrhizal plants and vertebrate seed and spore dispersal: incorporating mycorrizas into the seed dispersal paradigm. In ‘Seed Dispersal: Theory and its Application in a Changing World’. (Eds A. J. Dennis, E. W. Schupp, R. J. Green, and D. A. Westcott.) pp. 463–478. (CABI: Reading, UK.)
Thums, M., Klaassen, M., and Hume, I. D. (2005). Seasonal changes in the diet of the long-nosed bandicoot (Perameles nasuta) assessed by analysis of faecal scats and of stable isotopes in blood. Australian Journal of Zoology 53, 87–93.
| Seasonal changes in the diet of the long-nosed bandicoot (Perameles nasuta) assessed by analysis of faecal scats and of stable isotopes in blood.Crossref | GoogleScholarGoogle Scholar |
Torres, D. A., Castaño, J. H., and Carranza‐Quiceno, J. A. (2020). Global patterns in seed germination after ingestion by mammals. Mammal Review 50, 278–290.
| Global patterns in seed germination after ingestion by mammals.Crossref | GoogleScholarGoogle Scholar |
Traveset, A., and Verdú, M. (2002). A meta-analysis of the effect of gut treatment on seed germination. In ‘Seed Dispersal and Frugivory: Ecology, Evolution and Conservation’. (Eds D. Levey, W. R. Silva and M. Galetti.) pp. 339–350. (CABI: Wallingford, UK.)
Traveset, A., Robertson, A. W., and Rodriguez-Perez, J. (2007). A reveiw on the role of endozoochory in seed germination. In ‘Seed Dispersal: Theory and its Application in a Changing World’. (Eds A. J. Dennis, E. W. Schupp, R. J. Green and D. A. Westcott.) pp. 78–103. (CABI: Reading, UK.)
Valentine, L. E., Bretz, M., Ruthrof, K. X., Fisher, R., Hardy, G. E. S. J., and Fleming, P. A. (2017). Scratching beneath the surface: bandicoot bioturbation contributes to ecosystem processes. Austral Ecology 42, 265–276.
| Scratching beneath the surface: bandicoot bioturbation contributes to ecosystem processes.Crossref | GoogleScholarGoogle Scholar |
Valentine, L. E., Ruthrof, K. X., Fisher, R., Hardy, G. E. S. J., Hobbs, R. J., Fleming, P. A., and Stevens, C. (2018). Bioturbation by bandicoots facilitates seedling growth by altering soil properties. Functional Ecology 32, 2138–2148.
| Bioturbation by bandicoots facilitates seedling growth by altering soil properties.Crossref | GoogleScholarGoogle Scholar |
Valiente‐Banuet, A., Aizen, M. A., Alcántara, J. M., Arroyo, J., Cocucci, A., Galetti, M., García, M. B., García, D., Gómez, J. M., Jordano, P., Medel, R., Navarro, L., Obeso, J. R., Oviedo, R., Ramírez, N., Rey, P. J., Traveset, A., Verdú, M., Zamora, R., and Johnson, M. (2015). Beyond species loss: the extinction of ecological interactions in a changing world. Functional Ecology 29, 299–307.
| Beyond species loss: the extinction of ecological interactions in a changing world.Crossref | GoogleScholarGoogle Scholar |
Wotton, D. M., and McAlpine, K. G. (2015). Seed dispersal of fleshy-fruited environmental weeds in New Zealand. New Zealand Journal of Ecology 39, 155–169.
Wright, B. R., Zuur, A. F., and Chan, G. C. K. (2014). Proximate causes and possible adaptive functions of mast seeding and barren flower shows in spinifex grasses (Triodia spp.) in arid regions of Australia. The Rangeland Journal 36, 297–308.
| Proximate causes and possible adaptive functions of mast seeding and barren flower shows in spinifex grasses (Triodia spp.) in arid regions of Australia.Crossref | GoogleScholarGoogle Scholar |
Zosky, K. L., Wayne, A. F., Bryant, K. A., Calver, M. C., and Scarff, F. R. (2017). Diet of the critically endangered woylie (Bettongia penicillata ogilbyi) in south-western Australia. Australian Journal of Zoology 65, 302–312.
| Diet of the critically endangered woylie (Bettongia penicillata ogilbyi) in south-western Australia.Crossref | GoogleScholarGoogle Scholar |