Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Pacific Conservation Biology Pacific Conservation Biology Society
A journal dedicated to conservation and wildlife management in the Pacific region.
RESEARCH ARTICLE

When losing your nuts increases your reproductive success: sandalwood (Santalum spicatum) nut caching by the woylie (Bettongia penicillata)

Marie Murphy A , Kay Howard A , Giles E. St J. Hardy A and Bernard Dell A B
+ Author Affiliations
- Author Affiliations

A School of Veterinary and Life Sciences, Murdoch University, South Street, Murdoch, WA 6150, Australia.

B Corresponding author. Email: B.Dell@murdoch.edu.au

Pacific Conservation Biology 21(3) 243-252 https://doi.org/10.1071/PC14924
Submitted: 18 March 2015  Accepted: 17 August 2015   Published: 9 October 2015

Abstract

To regenerate sandalwood (Santalum spicatum) stands in south-western Australia it is necessary to understand the complex relationship between woylies (Bettongia penicillata ogilbyi) and sandalwood. Sandalwood requires a seed disperser for successful recruitment and in the past the critically endangered woylie played an important role in dispersing and caching seeds, but it is not clear whether this mutualistic and antagonistic relationship is beneficial to regeneration efforts. An enclosure in a woodland and 46Scandium-labelled seeds, enabled study of the in situ predation of seeds, caching, the fate of cached seeds, the detection of cached seeds and predation of germinated seeds. Woylies preferentially cached sandalwood, then S. acuminatum seeds, before any interest was shown in Acacia acuminata and Gastrolobium microcarpum seeds, which were virtually all eaten in situ. Of a further 500 radiolabelled and individually numbered sandalwood seeds deployed, 42.2% were eaten in situ, 20.8% had an unknown fate and 37% were cached, with some seeds being recached up to four times. After nine months, only four cached seeds remained undisturbed. Olfaction appeared to be the primary method of cache detection. To examine the recruitment rate of cached seeds, the fate of 89 transplanted sandalwood seedlings at two study sites was followed. After one month 38% were intact and growing, but half of the transplanted seedlings were dug up and the remaining endosperm was eaten in situ or taken away. The results highlight the potential of providing seed supplies, including sandalwood seeds and seeds of their hosts, to seed-dispersal marsupials for passive ecosystem repair.

Additional keywords: caching, dispersal, regeneration, 46Scandium, scatter hoarding.


References

Abbott, H. G., and Quink, T. F. (1970). Ecology of eastern pine seed caches made by small forest mammals. Ecology 51, 271–278.
Ecology of eastern pine seed caches made by small forest mammals.Crossref | GoogleScholarGoogle Scholar |

Brand, J. E. (2000). The effects of management regime and host species on sandalwood (Santalum spicatum) recruitment near Paynes Find, Western Australia. The Rangeland Journal 22, 243–255.
The effects of management regime and host species on sandalwood (Santalum spicatum) recruitment near Paynes Find, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Brand, J. E., Sawyer, B., and Evans, D. R. (2014). The benefits of seed enrichment on sandalwood (Santalum spicatum) populations, after 17 years, in semi-arid Western Australia. The Rangeland Journal 36, 475–482.
The benefits of seed enrichment on sandalwood (Santalum spicatum) populations, after 17 years, in semi-arid Western Australia.Crossref | GoogleScholarGoogle Scholar |

Brand-Miller, J. C., and Holt, S. H. A. (1998). Australian Aboriginal plant foods: a consideration of their nutritional composition and health implications. Nutrition Research Reviews 11, 5–23.
Australian Aboriginal plant foods: a consideration of their nutritional composition and health implications.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M%2FjsF2ktQ%3D%3D&md5=a4f7f55a30d36b8539ff6adabac2606dCAS | 19087457PubMed |

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 |

Christensen, P. E. S. (1980). The biology of Bettongia penicillata (Grey, 1837) and Macropus eugenii (Desmarest 1817) in relation to fire. Forests Department of Western Australia Bulletin 91, 1–90.

Christensen, P., and Leftwich, T. (1980). Observations on the nest-building habits of the brush-tailed rat-kangaroo or woylie (Bettongia penicillata). Journal of the Royal Society of Western Australia 63, 33–38.

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 |

Department of the Environment (2015). Bettongia penicillata ogilbyi – woylie. Biodiversity – species profile and threats database. Australian Government, Department of the Environment. Available at: http://www.environment.gov.au/cgi-bin/sprat/public/publicspecies.pl?taxon_id= 66844 [accessed August 2015].

Erickson, R., George, A. S., Marchant, N. G., and Morcombe, M. K. (1973). ‘Australian Flora in Colour: Flowers and Plants of Western Australia.’ (A.H. and A.W. Reed: Sydney.)

Forget, P.-M. (1993). Post-dispersal predation and scatterhoarding of Dipteryx panamensis (Papilionaceae) seeds by rodents in Panama. Oecologia 94, 255–261.
Post-dispersal predation and scatterhoarding of Dipteryx panamensis (Papilionaceae) seeds by rodents in Panama.Crossref | GoogleScholarGoogle Scholar |

Forget, P.-M., and Wenny, D. (2005). How to elucidate seed fate? A review of marking methods used to study seed removal and secondary seed dispersal. In ‘Seed Fate: Predation, Dispersal and Seedling Establishment’. (Eds P. M. Forget, J. Lambert, P. Hulme, and S. B. Vander Wall.) pp. 379–393. (CABI Publishing: Wallingford, UK.)

Garkaklis, M. J., Bradley, J. S., and Wooller, R. D. (1998). The effects of woylie (Bettongia penicillata) foraging on soil water repellency and water infiltration in heavy textured soils in southwestern Australia. Australian Journal of Ecology 23, 492–496.
The effects of woylie (Bettongia penicillata) foraging on soil water repellency and water infiltration in heavy textured soils in southwestern Australia.Crossref | GoogleScholarGoogle Scholar |

Garkaklis, M. J., Bradley, J. S., and Wooller, R. D. (2000). Digging by vertebrates as an activity promoting the development of water-repellent patches in sub-surface soil. Journal of Arid Environments 45, 35–42.
Digging by vertebrates as an activity promoting the development of water-repellent patches in sub-surface soil.Crossref | GoogleScholarGoogle Scholar |

Garkaklis, M. J., Bradley, J. S., and Wooller, R. D. (2004). Digging and soil turnover by a mycophagous marsupial. Journal of Arid Environments 56, 569–578.
Digging and soil turnover by a mycophagous marsupial.Crossref | GoogleScholarGoogle Scholar |

Hadj-Chikh, L. Z., Steele, M. A., and Smallwood, P. D. (1996). Caching decisions by grey squirrels: a test of the handling time and perishability hypotheses. Animal Behaviour 52, 941–948.
Caching decisions by grey squirrels: a test of the handling time and perishability hypotheses.Crossref | GoogleScholarGoogle Scholar |

Hettiarachchi, D. S., Liu, Y. D., Boddy, M. R., Fox, J. E. D., and Sunderland, V. B. (2013). Contents of fatty acids, selected lipids and physicochemical properties of Western Australian sandalwood seed oil. Journal of the American Oil Chemists’ Society 90, 285–290.
Contents of fatty acids, selected lipids and physicochemical properties of Western Australian sandalwood seed oil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFeqtbs%3D&md5=8013b573621f978c795d9b97be283042CAS |

Howe, H. F. (1989). Scatter- and clump-dispersal and seedling demography: hypothesis and implications. Oecologia 79, 417–426.
Scatter- and clump-dispersal and seedling demography: hypothesis and implications.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3sfnsFShtw%3D%3D&md5=9213e588185a7fa99afee35ca03e9971CAS | 23921409PubMed |

Hulme, P. E. (2002). Seed-eaters: dispersal, destruction and demography. In ‘Seed Dispersal and Frugivory: Ecology, Evolution and Conservation’. (Eds D. J. Levey, W. R. Silva and M. Galetti.) pp. 257–273. (CAB International: New York.)

Hulme, P. E., and Borelli, T. (1999). Variability in post-dispersal seed predation in deciduous woodland: relative importance of location, seed species, burial and density. Plant Ecology 145, 149–156.
Variability in post-dispersal seed predation in deciduous woodland: relative importance of location, seed species, burial and density.Crossref | GoogleScholarGoogle Scholar |

Irlbeck, N. A., and Hume, I. D. (2003). The role of acacia in the diets of Australian marsupials – a review. Australian Mammalogy 25, 121–134.
The role of acacia in the diets of Australian marsupials – a review.Crossref | GoogleScholarGoogle Scholar |

Jansen, P. A., Bongers, F., and Hemerik, L. (2004). Seed mass and mast seeding enhance dispersal by a Neotropical scatterhoarding rodent. Ecological Monographs 74, 569–589.
Seed mass and mast seeding enhance dispersal by a Neotropical scatterhoarding rodent.Crossref | GoogleScholarGoogle Scholar |

Jansen, P. A., Bongers, F., and Prins, H. H. T. (2006). Tropical rodents change rapidly germinating seeds into long-term food supplies. Oikos 113, 449–458.
Tropical rodents change rapidly germinating seeds into long-term food supplies.Crossref | GoogleScholarGoogle Scholar |

Jensen, T. S. (1985). Seed–seed predator interactions of European beech (Fagus silvatica L) and forest rodents, Clethrionomys glareolus and Apodemus flavicollis. Oikos 44, 149–156.
Seed–seed predator interactions of European beech (Fagus silvatica L) and forest rodents, Clethrionomys glareolus and Apodemus flavicollis.Crossref | GoogleScholarGoogle Scholar |

Jones, G. P., Watson, T. G., Sinclair, A. J., Birkett, A., Dunt, N., Nair, S., and Tonkin, S. Y. (1999). Santalbic acid from quandong kernels and oil fed to rats affects kidney and liver P450. Asia Pacific Journal of Clinical Nutrition 8, 211–215.
Santalbic acid from quandong kernels and oil fed to rats affects kidney and liver P450.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntFSksLg%3D&md5=28f38fd2a97869188c4baecad5ca6f16CAS | 24394165PubMed |

Kealley, I. (1991). The management of sandalwood. Wildlife Management Program 8. Department of Conservation and Land Management, Western Australia.

Liu, Y. D., Longmore, R. B., and Kailis, S. G. (1997). Proximate and fatty acid composition changes in developing sandalwood (Santalum spicatum) seeds. Journal of the Science of Food and Agriculture 75, 27–30.
Proximate and fatty acid composition changes in developing sandalwood (Santalum spicatum) seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtFags7w%3D&md5=bc47429ba589bf9f75493f3495b171adCAS |

LoGiudice, K., and Ostfeld, R. S. (2002). Interactions between mammals and trees: predation on mammal-dispersed seeds and the effects of ambient food. Oecologia 130, 420–425.
Interactions between mammals and trees: predation on mammal-dispersed seeds and the effects of ambient food.Crossref | GoogleScholarGoogle Scholar |

Longland, W. S., and Clements, C. (1995). Use of fluorescent pigments in studies of seed caching by rodents. Journal of Mammalogy 76, 1260–1266.
Use of fluorescent pigments in studies of seed caching by rodents.Crossref | GoogleScholarGoogle Scholar |

Longland, W. S., and Ostoja, S. M. (2013). Ecosystem services from keystone species: diversionary seeding and seed-caching desert rodents can enhance Indian ricegrass seedling establishment. Restoration Ecology 21, 285–291.
Ecosystem services from keystone species: diversionary seeding and seed-caching desert rodents can enhance Indian ricegrass seedling establishment.Crossref | GoogleScholarGoogle Scholar |

MacDonald, I. M. V. (1997). Field experiments on duration and precision of grey and red squirrel spatial memory. Animal Behaviour 54, 879–891.
Field experiments on duration and precision of grey and red squirrel spatial memory.Crossref | GoogleScholarGoogle Scholar |

McKinnell, F. H. (1990). Status of management and silviculture research on sandalwood in Western Australia and Indonesia. In ‘USDA Forest Service General Technology Report PSW-122’. (Ed. F. H. McKinnell.) pp. 19–29. (Department of Conservation and Land Management: Western Australia.)

Moore, J. E., McEuen, A. B., Swihart, R. K., Contreras, T. A., and Steele, M. A. (2007). Determinants of seed removal distance by scatter-hoarding rodents in deciduous forests. Ecology 88, 2529–2540.
Determinants of seed removal distance by scatter-hoarding rodents in deciduous forests.Crossref | GoogleScholarGoogle Scholar | 18027756PubMed |

Murphy, M. T., Garkaklis, M. J., and Hardy, G. E. St. J. (2005). Seed caching by woylies Bettongia penicillata can increase sandalwood Santalum spicatum regeneration in Western Australia. Austral Ecology 30, 747–755.
Seed caching by woylies Bettongia penicillata can increase sandalwood Santalum spicatum regeneration in Western Australia.Crossref | GoogleScholarGoogle Scholar |

Noble, J. C. (1993). Relict surface-soil features in semi-arid mulga (Acacia aneura) woodlands. The Rangeland Journal 15, 48–70.
Relict surface-soil features in semi-arid mulga (Acacia aneura) woodlands.Crossref | GoogleScholarGoogle Scholar |

Pacioni, C., Wayne, A. F., and Spencer, P. B. S. (2011). Effects of habitat fragmentation on population structure and long distance gene flow in an endangered marsupial: the woylie. Journal of Zoology 283, 98–107.
Effects of habitat fragmentation on population structure and long distance gene flow in an endangered marsupial: the woylie.Crossref | GoogleScholarGoogle Scholar |

Pearson, K. M., and Theimer, T. C. (2004). Seed caching and pilfering by two species of Peromyscus: implications for pinyon pine establishment. Oecologia 141, 76–83.
Seed caching and pilfering by two species of Peromyscus: implications for pinyon pine establishment.Crossref | GoogleScholarGoogle Scholar | 15258848PubMed |

Primack, R. B., and Levy, C. K. (1988). A method to label seeds and seedlings using gamma-emitting radionuclides. Ecology 69, 796–800.
A method to label seeds and seedlings using gamma-emitting radionuclides.Crossref | GoogleScholarGoogle Scholar |

Puerta-Piñero, C., Gómez, J. M., and Schupp, E. W. (2010). Spatial patterns of acorn dispersal by rodents: do acorn crop size and ungulate presence matter? Oikos 119, 179–187.
Spatial patterns of acorn dispersal by rodents: do acorn crop size and ungulate presence matter?Crossref | GoogleScholarGoogle Scholar |

Pyare, S., and Longland, W. S. (2000). Seedling-aided cache detection by heteromyid rodents. Oecologia 122, 66–71.
Seedling-aided cache detection by heteromyid rodents.Crossref | GoogleScholarGoogle Scholar |

Sampson, J. C. (1971). The biology of Bettongia penicillata Grey, 1837. Ph.D. Thesis. The University of Western Australia, Western Australia.

Sawyer, B. (2013). Sandalwood (Santalum spicatum) establishment in the semi-arid and arid regions of Western Australia. The Rangeland Journal 35, 109–115.
Sandalwood (Santalum spicatum) establishment in the semi-arid and arid regions of Western Australia.Crossref | GoogleScholarGoogle Scholar |

Smallwood, P. D., and Peters, W. D. (1986). Grey squirrel food preferences: the effects of tannin and fat concentration. Ecology 67, 168–174.
Grey squirrel food preferences: the effects of tannin and fat concentration.Crossref | GoogleScholarGoogle Scholar |

Stapanian, M. A., and Smith, C. C. (1978). A model for seed scatterhoarding: coevolution of fox squirrels and black walnuts. Ecology 59, 884–896.
A model for seed scatterhoarding: coevolution of fox squirrels and black walnuts.Crossref | GoogleScholarGoogle Scholar |

Start, A. N., Burbidge, A. A., and Armstrong, D. (1995). Woylie recovery plan. Wildlife Management Program No. 16. Department of Conservation and Land Management, Western Australia.

Subasinghe, S. M. C. U. P. (2013). Sandalwood research: a global perspective. Journal of Tropical Forestry and Environment 3, 1–8.

Suselbeek, L., Jansen, P. A., Prins, H. H. T., and Steele, M. A. (2013). Tracking rodent-dispersed large seeds with passive Integrated Transponder (PIT) tags. Methods in Ecology and Evolution 4, 513–519.
Tracking rodent-dispersed large seeds with passive Integrated Transponder (PIT) tags.Crossref | GoogleScholarGoogle Scholar |

Taraborelli, P., Borruel, N., and Mangeaud, A. (2009). Ability of murid rodents to find buried seeds in the Monte Desert. Ethology 115, 201–209.
Ability of murid rodents to find buried seeds in the Monte Desert.Crossref | GoogleScholarGoogle Scholar |

Theimer, T. H. (2001). Seed scatter-hoarding by white-tailed rats: consequences for seedling recruitment by an Australian rain forest tree. Journal of Tropical Ecology 17, 177–189.
Seed scatter-hoarding by white-tailed rats: consequences for seedling recruitment by an Australian rain forest tree.Crossref | GoogleScholarGoogle Scholar |

Vander Wall, S. B. (1990). ‘Food Hoarding in Animals.’ (The University of Chicago Press: Chicago.)

Vander Wall, S. B. (1995). The effects of seed value on the caching behavior of yellow pine chipmunks. Oikos 74, 533–537.
The effects of seed value on the caching behavior of yellow pine chipmunks.Crossref | GoogleScholarGoogle Scholar |

Vander Wall, S. B. (2000). The influence of environmental conditions on cache recovery and cache pilferage by yellow pine chipmunks (Tamias amoenus) and deer mice (Peromyscus maniculatus). Behavioral Ecology 11, 544–549.
The influence of environmental conditions on cache recovery and cache pilferage by yellow pine chipmunks (Tamias amoenus) and deer mice (Peromyscus maniculatus).Crossref | GoogleScholarGoogle Scholar |

Vander Wall, S. B. (2003). Masting in pines alters the use of cached seeds by rodents and causes increased seed survival. Ecology 84, 3508–3516.

Vander Wall, S. B. (2008). On the relative contributions of wind vs. animals to seed dispersal of four Sierra Nevada pines. Ecology 89, 1837–1849.
On the relative contributions of wind vs. animals to seed dispersal of four Sierra Nevada pines.Crossref | GoogleScholarGoogle Scholar | 18705371PubMed |

Vander Wall, S. B. (2010). How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals. Philosophical Transactions of Royal Society B 365, 989–997.
How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals.Crossref | GoogleScholarGoogle Scholar |

Vander Wall, S. B., Kuhn, K. M., and Beck, M. J. (2005). Seed removal, seed predation and secondary dispersal. Ecology 86, 801–806.
Seed removal, seed predation and secondary dispersal.Crossref | GoogleScholarGoogle Scholar |

Waitman, B. A., Vander Wall, S. B., and Esque, T. C. (2012). Seed dispersal and seed fate in Joshua tree (Yucca brevifolia). Journal of Arid Environments 81, 1–8.
Seed dispersal and seed fate in Joshua tree (Yucca brevifolia).Crossref | GoogleScholarGoogle Scholar |

Wang, B. C., and Smith, T. B. (2002). Closing the seed dispersal loop. Trends in Ecology & Evolution 17, 379–385.
Closing the seed dispersal loop.Crossref | GoogleScholarGoogle Scholar |

Wayne, A. F., Maxwell, M. A., Ward, C., Vellios, C., Ward, B., Liddelow, G. L., Wilson, I., Wayne, J. C., and Williams, M. R. (2013). The importance of getting the numbers right: quantifying the rapid and substantial decline of an abundant marsupial, Bettongia penicillata. Wildlife Research 40, 169–183.
The importance of getting the numbers right: quantifying the rapid and substantial decline of an abundant marsupial, Bettongia penicillata.Crossref | GoogleScholarGoogle Scholar |

Wayne, A. F., Maxwell, M., Ward, C. G., Vellios, C. V., Wilson, I., Wayne, J. C., and Williams, M. R. (2015). Sudden and rapid decline of the abundant marsupial, Bettongia penicillata in Australia. Oryx 49, 175–185.
Sudden and rapid decline of the abundant marsupial, Bettongia penicillata in Australia.Crossref | GoogleScholarGoogle Scholar |

Winterrowd, M. F., and Weigl, P. D. (2006). Mechanisms of cache retrieval in the group nesting Southern Flying Squirrel (Glaucomys volans). Ethology 112, 1136–1144.
Mechanisms of cache retrieval in the group nesting Southern Flying Squirrel (Glaucomys volans).Crossref | GoogleScholarGoogle Scholar |

Wróbel, A., and Zwolak, R. (2013). The choice of seed tracking method influenced fate of beech seeds dispersed by rodents. Plant Ecology 214, 471–475.
The choice of seed tracking method influenced fate of beech seeds dispersed by rodents.Crossref | GoogleScholarGoogle Scholar |

Yeatman, G. J., and Groom, C. J. (2012). National Recovery Plan for the woylie Bettongia penicillata. Wildlife Management Program No. 51. (Department of Environment and Conservation: Perth.)

Zhang, Z. B., Xiao, Z. S., and Li, H. J. (2005). Impact of small rodents on tree seeds in temperate and subtropical forests, China. In ‘Seed Fate: Seed Predation, Seed Dispersal and Seedling Establishment’. (Eds P. M. Forget, J. Lambert, P. E. Hulme and S. B. Vander Wall.) pp. 269–282. (CABI Publishing: Wallingford, UK.)