Bioturbation by echidna (Tachyglossus aculeatus) in a forest habitat, south-western Australia
Shannon J. Dundas
A B * , Lara Osborne A , Anna J. M. Hopkins A C , Katinka X. Ruthrof A D and Patricia A. Fleming A D
+ Author Affiliations
- Author Affiliations
A Terrestrial Ecosystem Science and Sustainability, Harry Butler Institute, Murdoch University, Murdoch, WA 6150, Australia.
B NSW Department of Primary Industries, 1447 Forest Road, Orange, NSW 2800, Australia.
C Conservation and Biodiversity Research Centre, School of Science, Edith Cowan University, 270 Joondalup Drive, Joondalup, WA 6027, Australia.
D Biodiversity and Conservation Sciences, Department of Biodiversity, Conservation and Attractions, Kensington, WA 6151, Australia.
Australian Journal of Zoology 69(5) 197-204 https://doi.org/10.1071/ZO22019
Submitted: 8 February 2022 Accepted: 30 June 2022 Published: 3 August 2022
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Bioturbation by digging animals is important for key forest ecosystem processes such as soil turnover, decomposition, nutrient cycling, water infiltration, seedling recruitment, and fungal dispersal. Despite their widespread geographic range, little is known about the role of the short-beaked echidna (Tachyglossus aculeatus) in forest ecosystems. We measured the density and size of echidna diggings in the Northern Jarrah Forest, south-western Australia, to quantify the contribution echidna make to soil turnover. We recorded an overall density of 298 echidna diggings per hectare, 21% of which were estimated to be less than 1 month old. The average size of digs was 50 ± 25 mm in depth and 160 ± 61 mm in length. After taking into account seasonal digging rates, we estimated that echidnas turn over 1.23 tonnes of soil ha−1 year−1 in this forest, representing an important role in ecosystem dynamics. Our work contributes to the growing body of evidence quantifying the role of these digging animals as critical ecosystem engineers. Given that the echidna is the only Australian digging mammal not severely impacted by population decline or range reduction, its functional contribution to health and resilience of forest ecosystems is increasingly important due to the functional loss of most Australian digging mammals.
Keywords: animal digging, biopedturbation, echidna, ecosystem engineering, ecosystem processes, Jarrah forest, soil turnover, Tachyglossus aculeatus.
References
Abensperg-Traun, M (1991). Survival strategies of the echidna Tachyglossus aculeatus Shaw 1792 (Monotremata: Tachyglossidae). Biological Conservation 58, 317–328.| Survival strategies of the echidna Tachyglossus aculeatus Shaw 1792 (Monotremata: Tachyglossidae).Crossref | GoogleScholarGoogle Scholar |
Abensperg-Traun, M, and Boer, ESD (1992). The foraging ecology of a termite- and ant-eating specialist, the echidna Tachyglossus aculeatus (Monotremata: Tachyglossidae). Journal of Zoology 226, 243–257.
| The foraging ecology of a termite- and ant-eating specialist, the echidna Tachyglossus aculeatus (Monotremata: Tachyglossidae).Crossref | GoogleScholarGoogle Scholar |
Andrys, J, Lyons, TJ, and Kala, J (2015). Multidecadal evaluation of WRF downscaling capabilities over Western Australia in simulating rainfall and temperature extremes. Journal of Applied Meteorology and Climatology 54, 370–394.
| Multidecadal evaluation of WRF downscaling capabilities over Western Australia in simulating rainfall and temperature extremes.Crossref | GoogleScholarGoogle Scholar |
Augee M, Gooden B, Musser A (2006) ‘Echidna: extraordinary egg laying mammal.’ (CSIRO Publishing: Victoria)
Bartle J, Slessar GC (1989) Mining and rehabilitation. In ‘The jarrah forest: a complex mediterranean ecosystem’. (Ed. B Dell, JJ Havel, N Malajczuk) pp. 357–377. (Springer: Dordrecht, The Netherlands)
| Crossref |
Bates, BC, Hope, P, Ryan, B, Smith, I, and Charles, S (2008). Key findings from the Indian Ocean climate initiative and their impact on policy development in Australia. Climatic Change 89, 339–354.
| Key findings from the Indian Ocean climate initiative and their impact on policy development in Australia.Crossref | GoogleScholarGoogle Scholar |
BOM (2022) Bureau of meteorology. Available at http://www.bom.gov.au/climate/data/stations/
Churchward HM, Dimmock GM (1989) The soils and landforms of the Northern Jarrah Forest. In ‘The Jarrah Forest: a complex mediterranean ecosystem’. (Ed. B Dell, JJ Havel, N Malajczuk) pp. 13–21. (Springer: Dordrecht, The Netherlands).
| Crossref |
Clemente, CJ, Cooper, CE, Withers, PC, Freakley, C, Singh, S, and Terrill, P (2016). The private life of echidnas: using accelerometry and GPS to examine field biomechanics and assess the ecological impact of a widespread, semi-fossorial monotreme. The Journal of Experimental Biology 219, 3271–3283.
| The private life of echidnas: using accelerometry and GPS to examine field biomechanics and assess the ecological impact of a widespread, semi-fossorial monotreme.Crossref | GoogleScholarGoogle Scholar |
Cowan, T, Purich, A, Perkins, S, Pezza, A, Boschat, G, and Sadler, K (2014). More frequent, longer, and hotter heat waves for Australia in the twenty-first century. Journal of Climate 27, 5851–5871.
| More frequent, longer, and hotter heat waves for Australia in the twenty-first century.Crossref | GoogleScholarGoogle Scholar |
CSIRO (2018) ‘Australian soil resource information system (ASRIS).’ (Australian Collaborative Land Evaluation Program, CSIRO Land and Water: Canberra, ACT)
Davies, GTO, Kirkpatrick, JB, Cameron, EZ, Carver, S, and Johnson, CN (2019). Ecosystem engineering by digging mammals: effects on soil fertility and condition in Tasmanian temperate woodland. Royal Society Open Science 6, 180621.
| Ecosystem engineering by digging mammals: effects on soil fertility and condition in Tasmanian temperate woodland.Crossref | GoogleScholarGoogle Scholar |
Decker, O, Leonard, S, and Gibb, H (2019). Rainfall-dependent impacts of threatened ecosystem engineers on organic matter cycling. Functional Ecology 33, 2254–2266.
| Rainfall-dependent impacts of threatened ecosystem engineers on organic matter cycling.Crossref | GoogleScholarGoogle Scholar |
Dell B, Havel JJ (1989) The Jarrah Forest, an introduction. In ‘The Jarrah Forest: a complex mediterranean ecosystem’. (Ed. B Dell, JJ Havel, N Malajczuk) pp. 1–10. (Springer: Dordrecht, The Netherlands).
| Crossref |
Diffenbaugh, NS, and Field, CB (2013). Changes in ecologically critical terrestrial climate conditions. Science 341, 486–492.
| Changes in ecologically critical terrestrial climate conditions.Crossref | GoogleScholarGoogle Scholar |
Dundas, SJ, Hopkins, AJM, Ruthrof, KX, Tay, NE, Burgess, TI, Hardy, GESJ, and Fleming, PA (2018). Digging mammals contribute to rhizosphere fungal community composition and seedling growth. Biodiversity and Conservation 27, 3071–3086.
| Digging mammals contribute to rhizosphere fungal community composition and seedling growth.Crossref | GoogleScholarGoogle Scholar |
Eldridge, DJ (2011). The resource coupling role of animal foraging pits in semi-arid woodlands. Ecohydrology 4, 623–630.
| The resource coupling role of animal foraging pits in semi-arid woodlands.Crossref | GoogleScholarGoogle Scholar |
Eldridge, DJ, and James, AI (2009). Soil-disturbance by native animals plays a critical role in maintaining healthy Australian landscapes. Ecological Management & Restoration 10, S27–S34.
| Soil-disturbance by native animals plays a critical role in maintaining healthy Australian landscapes.Crossref | GoogleScholarGoogle Scholar |
Eldridge, DJ, and Koen, TB (2021). Temporal changes in soil function in a wooded dryland following simulated disturbance by a vertebrate engineer. CATENA 200, 105166.
| Temporal changes in soil function in a wooded dryland following simulated disturbance by a vertebrate engineer.Crossref | GoogleScholarGoogle Scholar |
Eldridge, DJ, and Kwok, ABC (2008). Soil disturbance by animals at varying spatial scales in a semi-arid Australian woodland. The Rangeland Journal 30, 327–337.
| Soil disturbance by animals at varying spatial scales in a semi-arid Australian woodland.Crossref | GoogleScholarGoogle Scholar |
Eldridge, DJ, and Mensinga, A (2007). Foraging pits of the short-beaked echidna (Tachyglossus aculeatus) as small-scale patches in a semi-arid Australian box woodland. Soil Biology and Biochemistry 39, 1055–1065.
| Foraging pits of the short-beaked echidna (Tachyglossus aculeatus) as small-scale patches in a semi-arid Australian box woodland.Crossref | GoogleScholarGoogle Scholar |
Eldridge, DJ, Koen, TB, Killgore, A, Huang, N, and Whitford, WG (2012). Animal foraging as a mechanism for sediment movement and soil nutrient development: evidence from the semi-arid Australian woodlands and the Chihuahuan desert. Geomorphology 157–158, 131–141.
| Animal foraging as a mechanism for sediment movement and soil nutrient development: evidence from the semi-arid Australian woodlands and the Chihuahuan desert.Crossref | GoogleScholarGoogle Scholar |
Eldridge, DJ, Woodhouse, JN, Curlevski, NJA, Hayward, M, Brown, MV, and Neilan, BA (2015). Soil-foraging animals alter the composition and co-occurrence of microbial communities in a desert shrubland. The ISME Journal 9, 2671–2681.
| Soil-foraging animals alter the composition and co-occurrence of microbial communities in a desert shrubland.Crossref | GoogleScholarGoogle Scholar |
Eldridge, DJ, Delgado-Baquerizo, M, Woodhouse, JN, and Neilan, BA (2017). Contrasting effects of two mammalian soil engineers on microbial communities. Austral Ecology 42, 380–384.
| Contrasting effects of two mammalian soil engineers on microbial communities.Crossref | GoogleScholarGoogle Scholar |
Field JB, Anderson GR (2003) Biological agents in regolith processes: case study on the southern tablelands, NSW. In ‘Advances in Regolith – Proceedings of the Cooperative Research Centre for Landscape Environments and Mineral Exploration (CRC LEME) Regional Regolith Symposia’. (Ed. I Roach) pp. 119–121. (CRC LEME)
Fleming, PA, Anderson, H, Prendergast, AS, Bretz, MR, Valentine, LE, and Hardy, GESJ (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, MJ, Bradley, JS, and Wooller, RD (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, MJ, Bradley, JS, and Wooller, RD (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, MJ, Bradley, JS, and Wooller, RD (2003). The relationship between animal foraging and nutrient patchiness in south-west Australian woodland soils. Soil Research 41, 665–673.
| The relationship between animal foraging and nutrient patchiness in south-west Australian woodland soils.Crossref | GoogleScholarGoogle Scholar |
Garkaklis, MJ, Bradley, JS, and Wooller, RD (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 |
Gentilli J (1989) Climate of the jarrah forest. In ‘The Jarrah Forest: a complex mediterranean ecosystem’. (Eds B Dell, JJ Havel, N Malajczuk) pp. 23–40. (Springer: Dordrecht, The Netherlands)
Gioia, P, and Hopper, SD (2017). A new phytogeographic map for the Southwest Australian Floristic Region after an exceptional decade of collection and discovery. Botanical Journal of the Linnean Society 184, 1–15.
| A new phytogeographic map for the Southwest Australian Floristic Region after an exceptional decade of collection and discovery.Crossref | GoogleScholarGoogle Scholar |
Harper, RJ, McKissock, I, Gilkes, RJ, Carter, DJ, and Blackwell, PS (2000). A multivariate framework for interpreting the effects of soil properties, soil management and landuse on water repellency. Journal of Hydrology 231–232, 371–383.
| A multivariate framework for interpreting the effects of soil properties, soil management and landuse on water repellency.Crossref | GoogleScholarGoogle Scholar |
Hopkins, AJM, Tay, NE, Bryant, GL, Ruthrof, KX, Valentine, LE, Kobryn, H, Burgess, TI, Richardson, BB, Hardy, GESJ, and Fleming, PA (2021). Urban remnant size alters fungal functional groups dispersed by a digging mammal. Biodiversity and Conservation 30, 3983–4003.
| Urban remnant size alters fungal functional groups dispersed by a digging mammal.Crossref | GoogleScholarGoogle Scholar |
James, AI, and Eldridge, DJ (2007). Reintroduction of fossorial native mammals and potential impacts on ecosystem processes in an Australian desert landscape. Biological Conservation 138, 351–359.
| Reintroduction of fossorial native mammals and potential impacts on ecosystem processes in an Australian desert landscape.Crossref | GoogleScholarGoogle Scholar |
Le Dantec S (2016) Soil mapping Mulloon Creek catchment-research project. Available at https://static1.squarespace.com/static/5600deebe4b07aebe017c6d2/t/61385e90ce34b858daa3fb05/1631084185925/Soil+Mapping+Mulloon+Creek+Catchment+Report_19Jan2018.pdf
Mallen-Cooper, M, Nakagawa, S, and Eldridge, DJ (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 |
Martin, ML, Travouillon, KJ, Sherratt, E, Fleming, PA, and Warburton, NM (2019a). Covariation between forelimb muscle anatomy and bone shape in an Australian scratch-digging marsupial: comparison of morphometric methods. Journal of Morphology 280, 1900–1915.
| Covariation between forelimb muscle anatomy and bone shape in an Australian scratch-digging marsupial: comparison of morphometric methods.Crossref | GoogleScholarGoogle Scholar |
Martin, ML, Warburton, NM, Travouillon, KJ, and Fleming, PA (2019b). Mechanical similarity across ontogeny of digging muscles in an Australian marsupial (Isoodon fusciventer). Journal of Morphology 280, 423–435.
| Mechanical similarity across ontogeny of digging muscles in an Australian marsupial (Isoodon fusciventer).Crossref | GoogleScholarGoogle Scholar |
Matusick, G, Ruthrof, KX, Fontaine, JB, and Hardy, GESJ (2016). Eucalyptus forest shows low structural resistance and resilience to climate change-type drought. Journal of Vegetation Science 27, 493–503.
| Eucalyptus forest shows low structural resistance and resilience to climate change-type drought.Crossref | GoogleScholarGoogle Scholar |
McKenzie, NL, Burbidge, AA, Baynes, A, Brereton, RN, Dickman, CR, Gordon, G, Gibson, LA, Menkhorst, PW, Robinson, AC, Williams, MR, and Woinarski, JCZ (2007). Analysis of factors implicated in the recent decline of Australia’s mammal fauna. Journal of Biogeography 34, 597–611.
| Analysis of factors implicated in the recent decline of Australia’s mammal fauna.Crossref | GoogleScholarGoogle Scholar |
Mulcahy, MJ (1960). Laterites and lateritic soils in south-western Australia. Journal of Soil Science 11, 206–225.
| Laterites and lateritic soils in south-western Australia.Crossref | GoogleScholarGoogle Scholar |
Munro, NT, McIntyre, S, Macdonald, B, Cunningham, SA, Gordon, IJ, Cunningham, RB, and Manning, AD (2019). Returning a lost process by reintroducing a locally extinct digging marsupial. PeerJ 7, e6622.
| Returning a lost process by reintroducing a locally extinct digging marsupial.Crossref | GoogleScholarGoogle Scholar |
Myers, N, Mittermeier, RA, Mittermeier, CG, da Fonseca, GAB, and Kent, J (2000). Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
| Biodiversity hotspots for conservation priorities.Crossref | GoogleScholarGoogle Scholar |
Nichols OG, Muir B (1989) Vertebrates of the Jarrah Forest. In ‘The Jarrah Forest: a complex mediterranean ecosystem’. (Eds B Dell, JJ Havel, N Malajczuk) pp. 133–153. (Springer: Dordrecht, The Netherlands).
| Crossref |
Paine, RT (1995). A conversation on refining the concept of keystone species. Conservation Biology 9, 962–964.
| A conversation on refining the concept of keystone species.Crossref | GoogleScholarGoogle Scholar |
Pearce RH (1989) Pre-colonial usage of Jarrah Forest by Indigenous people. In ‘The Jarrah Forest: a complex mediterranean ecosystem’. (Eds B Dell, JJ Havel, N Malajczuk) pp. 219–228. (Springer: Dordrecht, The Netherlands)
| Crossref |
R Core Team (2022) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria)
Smith, AP, Wellham, GS, and Green, SW (1989). Seasonal foraging activity and microhabitat selection by echidnas (Tachyglossus aculeatus) on the New England tablelands. Australian Journal of Ecology 14, 457–466.
| Seasonal foraging activity and microhabitat selection by echidnas (Tachyglossus aculeatus) on the New England tablelands.Crossref | GoogleScholarGoogle Scholar |
Stoneman GL, Bradshaw FJ, Christensen P (1989) Silviculture. In ‘The Jarrah Forest: a complex mediterranean ecosystem’. (Ed. B Dell, JJ Havel, N Malajczuk) pp. 335–355. (Springer: Dordrecht, The Netherlands)
Tay, NE, Hopkins, AJM, Ruthrof, KX, Burgess, T, Hardy, GESJ, and Fleming, PA (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 |
Travers, SK, Eldridge, DJ, Koen, TB, and Soliveres, S (2012). Animal foraging pit soil enhances the performance of a native grass under stressful conditions. Plant and Soil 352, 341–351.
| Animal foraging pit soil enhances the performance of a native grass under stressful conditions.Crossref | GoogleScholarGoogle Scholar |
Valentine, LE, Anderson, H, Hardy, GESJ, and Fleming, PA (2012). Foraging activity by the southern brown bandicoot (Isoodon obesulus) as a mechanism for soil turnover. Australian Journal of Zoology 60, 419–423.
| Foraging activity by the southern brown bandicoot (Isoodon obesulus) as a mechanism for soil turnover.Crossref | GoogleScholarGoogle Scholar |
Valentine, LE, Bretz, M, Ruthrof, KX, Fisher, R, Hardy, GESJ, and Fleming, PA (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, LE, Ruthrof, KX, Fisher, R, Hardy, GESJ, Hobbs, RJ, and Fleming, PA (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 |
Van Dyck S, Strahan R (Eds) (2008) ‘The mammals of australia.’ (Reed New Holland: Sydney, Australia)
Warburton, NM, Grégoire, L, Jacques, S, and Flandrin, C (2013). Adaptations for digging in the forelimb muscle anatomy of the southern brown bandicoot (Isoodon obesulus) and bilby (Macrotis lagotis). Australian Journal of Zoology 61, 402–419.
| Adaptations for digging in the forelimb muscle anatomy of the southern brown bandicoot (Isoodon obesulus) and bilby (Macrotis lagotis).Crossref | GoogleScholarGoogle Scholar |
Woinarski J, Burbidge A, Harrison P (2014) ‘The action plan for Australian mammals 2012.’ (CSIRO Publishing)
Woinarski, JCZ, Burbidge, AA, and Harrison, PL (2015). Ongoing unraveling of a continental fauna: decline and extinction of Australian mammals since European settlement. Proceedings of the National Academy of Sciences of the United States of America 112, 4531–4540.
| Ongoing unraveling of a continental fauna: decline and extinction of Australian mammals since European settlement.Crossref | GoogleScholarGoogle Scholar |
Wood, SN (2011). Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society: Series B 73, 3–36.
| Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models.Crossref | GoogleScholarGoogle Scholar |
Zosky KL (2011) Food resources and the decline of woylies Bettongia penicillata ogilbyi in southwestern Australia. PhD thesis, Murdoch University, Perth, WA, Australia.
