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Biodiversity and Conservation

, Volume 27, Issue 12, pp 3071–3086 | Cite as

Digging mammals contribute to rhizosphere fungal community composition and seedling growth

  • Shannon J. DundasEmail author
  • Anna J. M. Hopkins
  • Katinka X. Ruthrof
  • Natasha E. Tay
  • Treena I. Burgess
  • Giles E. St. J. Hardy
  • Patricia A. Fleming
Original Paper

Abstract

Bioturbation is an important ecosystem process, and the loss of native digging mammals due to introduced predators and habitat loss may have detrimental consequences for ecosystem health. The mycophagous woylie (Bettongia penicillata ogilbyi) was once widespread across the Australian continent and currently exists in a greatly reduced range, while the omnivorous quenda (Isoodon fusciventer), which once occurred across the southern part of Western Australia (WA), remains common in south west WA over a reduced range. Populations of these two digging marsupials are currently maintained within sanctuaries where they can reach high densities. To assess the influence these digging marsupials have on fungal assemblages, we investigated fungal root associations among seedlings of a key mycorrhizal forest canopy species, Corymbia calophylla, R. Br. K. D. Hill and L. A. S. Johnson. Seedlings were grown in soil collected from inside (heavily-dug soil) and outside (minimally-dug soil) two predator-proof sanctuaries. Our results showed that above-ground seedling biomass was significantly greater for seedlings grown in soil collected from inside the sanctuaries. There were no differences in the diversity or species richness of rhizosphere fungal communities isolated from these seedlings; however, the community composition was significantly different. This was most obvious for the predator-proof enclosure that had been in place for 20 years (Karakamia Sanctuary) compared with the more recently-installed Perup Sanctuary (fenced in 2010; 4 years before this study). At Karakamia, there were greater numbers of putatively hypogeous ectomycorrhizal fungi inside the enclosure and four times the number of operational taxonomic units of arbuscular mycorrhizal fungi outside the enclosure. The differences in fungal communities suggest that digging mammals play a pivotal role in ecosystem functioning by influencing the rhizosphere of this key forest canopy species, which has implications for maintaining the health and persistence of forests.

Keywords

Bioturbation Mammal reintroductions Brush-tailed bettong Marsupial Mycorrhiza Biopedturbation Rhizosphere fungi 

Notes

Acknowledgements

The authors would like to thank Bryony Palmer and Mike Smith from the Australian Wildlife Conservancy (AWC), and Adrian Wayne, Julia Wayne and Mark Virgo from the Department of Biodiversity, Conservation and Attractions for facilitating entry into the sanctuaries and for providing unpublished trapping data. We would also like to thank Pat Dundas, Judy Gardner (Scion, New Zealand) and Yvonne Lau for help collecting soil samples in the field. Thank you to the two anonymous reviewers who provided constructive comments to improve the manuscript. Support for this project was received through a Murdoch University Small Grants Scheme. SD, AH and KR were funded through the State Centre of Excellence for Climate Change, Woodland and Forest Health, which is a partnership between private industry, community groups, universities and the Government of Western Australia.

Supplementary material

10531_2018_1575_MOESM1_ESM.pdf (81 kb)
Supplementary material 1 (PDF 82 kb)

References

  1. Abbott I (2008) Historical perspectives of the ecology of some conspicuous vertebrate species in south-west Western Australia. Conserv Sci West Aust 6:1–214Google Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  3. Beare MH, Parmelee RW, Hendrix PF, Cheng W, Coleman DC, Crossley DA (1992) Microbial and faunal interactions and effects on litter nitrogen and decomposition in agroecosystems. Ecol Monogr 62:569–591CrossRefGoogle Scholar
  4. Brundrett MC (2008) Mycorrhizal associations: The Web ResourceGoogle Scholar
  5. Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77CrossRefGoogle Scholar
  6. Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol.  https://doi.org/10.1111/nph.14976 PubMedCrossRefGoogle Scholar
  7. Bryant GL, Kobryn HT, Hardy GES, Fleming PA (2017) Habitat islands in a sea of urbanisation. Urban For Urban Green 28:131–137CrossRefGoogle Scholar
  8. Burbidge AA, McKenzie NL (1989) Patterns in the modern decline of Western Australia’s vertebrate fauna: causes and conservation implications. Biol Conserv 50:143–198CrossRefGoogle Scholar
  9. Christensen PES (1980) The biology of Bettongia penicillata Gray, 1837, and Macropus eugenii (Desmarest, 1817) in relation to fire. Forests Department of Western Australia. Bulletin 91Google Scholar
  10. Claridge AW, May TW (1994) Mycophagy among Australian mammals. Aust J Ecol 19:251–275CrossRefGoogle Scholar
  11. Clarke LJ, Weyrich LS, Cooper A (2015) Reintroduction of locally extinct vertebrates impacts arid soil fungal communities. Mol Ecol 24:3194–3205CrossRefPubMedGoogle Scholar
  12. Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lindahl BD (2015) Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests. New Phytol 205:1525–1536CrossRefPubMedGoogle Scholar
  13. Courty P-E, Buée M, Diedhiou AG, Frey-Klett P, Le Tacon F, Rineau F, Turpault M-P, Uroz S, Garbaye J (2010) The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. Soil Biol Biochem 42:679–698CrossRefGoogle Scholar
  14. DBCA (2013) Perup Sanctuary. (ed C. a. A. Western Australian Department of Biodiversity)Google Scholar
  15. Dunn RR, Harris NC, Colwell RK, Koh LP, Sodhi NS (2009) The sixth mass coextinction: are most endangered species parasites and mutualists? Proc R Soc B 276:3037–3045CrossRefPubMedGoogle Scholar
  16. Eldridge DJ, James AI (2009) Soil-disturbance by native animals plays a critical role in maintaining healthy Australian landscapes. Ecol Manage Restor 10:S27–S34CrossRefGoogle Scholar
  17. Eldridge DJ, Woodhouse JN, Curlevski NJA, Hayward M, Brown MV, Neilan BA (2015) Soil-foraging animals alter the composition and co-occurrence of microbial communities in a desert shrubland. ISME J 9:2671–2681CrossRefPubMedPubMedCentralGoogle Scholar
  18. Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115–1126CrossRefPubMedGoogle Scholar
  19. Finlayson HH (1958) On Central Australian mammals (with notice of related species from adjacent tracts). Part III. The Potoroinae. Rec South Aust Mus 13:235–302Google Scholar
  20. Fleming PA, Anderson H, Prendergast AS, Bretz MR, Valentine LE, Hardy GESJ (2014) Is the loss of Australian digging mammals contributing to a deterioration in ecosystem function? Mamm Rev 44:94–108CrossRefGoogle Scholar
  21. Fogel R, Trappe JM (1978) Fungus consumption (Mycophagy) by small animals. Northwest Sci 52:1–31Google Scholar
  22. Garkaklis MJ, Bradley JS, Wooller RD (2000) Digging by vertebrates as an activity promoting the development of water-repellent patches in sub-surface soil. J Arid Environ 45:35–42CrossRefGoogle Scholar
  23. Garkaklis MJ, Bradley JS, Wooller RD (2003) The relationship between animal foraging and nutrient patchiness in south-west Australian woodland soils. Soil Res 41:665–673CrossRefGoogle Scholar
  24. Garkaklis MJ, Bradley JS, Wooller RD (2004) Digging and soil turnover by a mycophagous marsupial. J Arid Environ 56:569–578CrossRefGoogle Scholar
  25. Gehring CA, Wolf JE, Theimer TC (2002) Terrestrial vertebrates promote arbuscular mycorrhizal fungal diversity and inoculum potential in a rain forest soil. Ecol Lett 5:540–548CrossRefGoogle Scholar
  26. Hammer Ø, Harper DAT (2013) PAST: version 2.17c http://folk.uio.no/ohammer/past
  27. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 41:1–9Google Scholar
  28. Hillman A, Thompson RCA (2016) Interactions between humans and urban-adapted marsupials on private properties in the greater Perth region. Aust Mammal 38:253–255CrossRefGoogle Scholar
  29. Ihrmark K, Bödeker ITM, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandström-Durling M, Clemmensen KE (2012) New primers to amplify the fungal ITS2 region–evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol 82:666–677CrossRefPubMedGoogle Scholar
  30. Ishaq L, Barber PA, Hardy GESJ, Calver M, Dell B (2013) Seedling mycorrhizal type and soil chemistry are related to canopy condition of Eucalyptus gomphocephala. Mycorrhiza 23:359–371CrossRefPubMedGoogle Scholar
  31. Ishaq L, Barber PA, Hardy GESJ, Dell B (2018) Diversity of fungi associated with roots of Eucalyptus gomphocephala seedlings grown in soil from healthy and declining sites. Australas Plant Pathol 47:155–162CrossRefGoogle Scholar
  32. Johnson CN (1995) Interactions between fire, mycophagous mammals, and dispersal of ectomycorrhizal fungi in Eucalyptus forests. Oecologia 104:467–475CrossRefPubMedGoogle Scholar
  33. Johnson CN (1996) Interactions between mammals and ectomycorrhizal fungi. Trends Ecol Evol 11:503–507CrossRefPubMedGoogle Scholar
  34. Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith VS (2004) Species Coextinctions and the Biodiversity Crisis. Science 305:1632–1634CrossRefPubMedGoogle Scholar
  35. Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiss M, Larsson K-H (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277CrossRefPubMedGoogle Scholar
  36. Lamont BB, Ralph CS, Christensen PES (1985) Mycophagous marsupials as dispersal agents for ectomycorrhizal fungi on Eucalyptus calophylla and Gastrolobium bilobum. New Phytol 101:651–656CrossRefGoogle Scholar
  37. Lindahl BD, Nilsson RH, Tedersoo L, Abarenkov K, Carlsen T, Kjøller R, Kõljalg U, Pennanen T, Rosendahl S, Stenlid J, Kauserud H (2013) Fungal community analysis by high-throughput sequencing of amplified markers—a user’s guide. New Phytol 199:288–299CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lodge DJ (2000) Ecto- or arbuscular mycorrhizas—which are best? New Phytol 146:353–354CrossRefGoogle Scholar
  39. Martin G (2003) The role of small ground-foraging mammals in topsoil health and biodiversity: implications to management and restoration. Ecol Manage Restor 4:114–119CrossRefGoogle Scholar
  40. McGuire KL, Treseder KK (2010) Microbial communities and their relevance for ecosystem models: decomposition as a case study. Soil Biol Biochem 42:529–535CrossRefGoogle Scholar
  41. McIlwee AP, Johnson C (1998) The contribution of fungus to the diets of three mycophagous marsupials in eucalyptus forests, revealed by stable isotope analysis. Funct Ecol 12:223–231CrossRefGoogle Scholar
  42. Moore TL, Craig MD, Valentine LE, Hardy GESJ, Fleming PA (2014) Signs of wildlife activity and Eucalyptus wandoo condition. Aust Mammal 36:146–153CrossRefGoogle Scholar
  43. Nguyen VP, Needham AD, Friend JA (2005) A quantitative dietary study of the ‘critically endangered’ Gilbert’s potoroo Potorous gilbertii. Aust Mammal 27:1–6CrossRefGoogle Scholar
  44. Nguyen NH, Song ZW, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248CrossRefGoogle Scholar
  45. Nguyen D, Boberg J, Cleary M, Bruelheide H, Hönig L, Koricheva J, Stenlid J (2017) Foliar fungi of Betula pendula: impact of tree species mixtures and assessment methods. Sci Rep 7:41801CrossRefPubMedPubMedCentralGoogle Scholar
  46. Nuske SJ, Vernes K, May TW, Claridge AW, Congdon BC, Krockenberger A, Abell SE (2017) Redundancy among mammalian fungal dispersers and the importance of declining specialists. Fungal Ecol 27:1–13CrossRefGoogle Scholar
  47. Ottosson E, Kubartová A, Edman M, Jönsson M, Lindhe A, Stenlid J, Dahlberg A (2015) Diverse ecological roles within fungal communities in decomposing logs of Picea abies. FEMS Microbiol Ecol 91:fiv012CrossRefPubMedGoogle Scholar
  48. Pacioni C, Wayne AF, Spencer PBS (2013) Genetic outcomes from the translocations of the critically endangered woylie. Curr Zool 59:294–310CrossRefGoogle Scholar
  49. Quin DG (1985) Observations on the diet of the southern brown bandicoot, Isoodon obesulus (Marsupialia: peramelidae), in southern Tasmania. Aust Mammal 11:15–25Google Scholar
  50. Sapsford SJ (2017) Factors predisposing Corymbia calophylla to canker disease caused by Quambalaria coyrecup. PhD Thesis. Murdoch University, PerthGoogle Scholar
  51. Short J, Smith A (1994) Mammal decline and recovery in Australia. J Mammal 75:288–297CrossRefGoogle Scholar
  52. Shortridge GC (1909) An account of the geographical distribution of the marsupials and monotremes of south-west Australia, having special reference to the specimens collected during the Balston Expedition of 1904–1907. Proc Zool Soc Lond 79:803–848CrossRefGoogle Scholar
  53. Start AN, Burbidge AA, Armstrong D (1998) A review of the conservation status of the woylie, Bettongia penicillata ogilbyi (Marsupialia: Potoroidae) using IUCN criteria. CALMScience 2:277–289Google Scholar
  54. Tay N, Hopkins AJM, Ruthrof KX, Burgess T, Hardy GESJ, Fleming PA (2018) The tripartite relationship between a bioturbator, mycorrhizal fungi, and a key Mediterranean-type forest tree. Austral Ecol.  https://doi.org/10.1111/aec.12598 CrossRefGoogle Scholar
  55. Tommerup IC, Bougher NL (2000) The role of ectomycorrhizal fungi in nutrient cycling in temperate Australian woodlands. Surrey Beatty & Sons Pty., Ltd., Chipping NortonGoogle Scholar
  56. Travers SK, Eldridge DJ, Koen TB, Soliveres S (2012) Animal foraging pit soil enhances the performance of a native grass under stressful conditions. Plant Soil 352:341–351CrossRefGoogle Scholar
  57. Valentine LE, Anderson H, Hardy GESJ, Fleming PA (2013) Foraging activity by the southern brown bandicoot (Isoodon obesulus) as a mechanism for soil turnover. Aust J Zool 60:419–423CrossRefGoogle Scholar
  58. Valentine LE, Bretz M, Ruthrof KX, Fisher R, Hardy GESJ, Fleming PA (2017) Scratching beneath the surface: bandicoot bioturbation contributes to ecosystem processes. Austral Ecol 42:265–276CrossRefGoogle Scholar
  59. Valentine LE, Ruthrof KX, Fisher R, Hardy GESJ, Hobbs RJ, Fleming PA (2018) Bioturbation by bandicoots facilitates seedling growth by altering soil properties. Funct Ecol.  https://doi.org/10.1111/1365-2435.13179 CrossRefGoogle Scholar
  60. Van Der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310CrossRefPubMedGoogle Scholar
  61. Vernes K, Castellano M, Johnson CN (2001) Effects of season and fire on the diversity of hypogeous fungi consumed by a tropical mycophagous marsupial. J Anim Ecol 70:945–954CrossRefGoogle Scholar
  62. Wayne A, Maxwell MA, Ward CG, Vellios CV, Wilson I, Wayne JC, Williams MR (2015) Sudden and rapid decline of the abundant marsupial Bettongia penicillata in Australia. Onyx 49(1):175–185Google Scholar
  63. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Academic Press, San DiegoCrossRefGoogle Scholar
  64. Woinarski JCZ, Burbidge AA, Harrison PL (2014) The action plan for Australian mammals 2012. CSIRO Publishing, CollingwoodGoogle Scholar
  65. Zosky K, Bryant K, Calver M, Wayne A (2010) Do preservation methods affect the identification of dietary components from faecal samples? A case study using a mycophagous marsupial. Aust Mammal 32:173–176CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.School of Veterinary and Life SciencesMurdoch UniversityMurdochAustralia
  2. 2.NSW Department of Primary IndustriesOrangeAustralia
  3. 3.Centre for Ecosystem Management, School of ScienceEdith Cowan UniversityJoondalupAustralia
  4. 4.Kings Park ScienceDepartment of Biodiversity, Conservation and AttractionsKings ParkAustralia

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