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RESEARCH ARTICLE (Open Access)

The dingo (Canis familiaris) as a secondary disperser of mycorrhizal fungal spores

Todd F. Elliott https://orcid.org/0000-0001-9304-7040 A * , C. E. Timothy Paine A , Guy-Anthony Ballard A B , Heath Milne A , Josh Van der Eyk A , Kelsey Elliott C , Paul Meek https://orcid.org/0000-0002-3792-5723 A D , Jeremy J. Bruhl https://orcid.org/0000-0001-9112-4436 E and Karl Vernes https://orcid.org/0000-0003-1635-9950 A
+ Author Affiliations
- Author Affiliations

A Ecosystem Management, School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia.

B Vertebrate Pest Research Unit, Biosecurity NSW, NSW Department of Primary Industries, University of New England, PO Box U86, Armidale, NSW 2351, Australia.

C Integrative Studies Department, Warren Wilson College, Swannanoa, NC 28778, USA.

D Vertebrate Pest Research Unit, New South Wales Department of Primary Industries, Corner Gordon and Hood Street, Coffs Harbour, NSW 2450, Australia.

E Botany, School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia.

* Correspondence to: toddfelliott@gmail.com

Handling Editor: Thomas Newsome

Wildlife Research 51, WR22057 https://doi.org/10.1071/WR22057
Submitted: 23 March 2022  Accepted: 7 March 2023  Published: 4 April 2023

© 2024 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

Context

Many mycorrhizal fungi are vital to nutrient acquisition in plant communities, and some taxa are reliant on animal-mediated dispersal. The majority of animals that disperse spores are relatively small and have short-distance movement patterns, but carnivores – and especially apex predators – eat many of these small mycophagists and then move greater distances. No studies to date have assessed the ecosystem services carnivores provide through long-distance spore dispersal.

Aims

In this study, we aimed to investigate whether Australia’s free-ranging dogs (Canis familiaris), including dingoes, act as long-distance spore dispersers by predating smaller mycophagous animals and then secondarily dispersing the fungi consumed by these prey species.

Methods

To answer this question, we collected dingo scats along 40 km of transects in eastern Australia and analysed the scats to determine the presence of fungal spores and prey animals. Using telemetry and passage rate data, we then developed a movement model to predict the spore dispersal potential of dingoes.

Key results

We found 16 species of mammalian prey to be eaten by dingoes, and those dingo scats contained spores of 14 genera of mycorrhizal fungi. These fungi were more likely to appear in the scats of dingoes if primary mycophagist prey mammals had been consumed. Our model predicted dingo median spore dispersal distance to be 2050 m and maximum dispersal potential to be 10 700 m.

Conclusions

Our study indicates that dingoes are providing a previously overlooked ecosystem service through the long-distance dispersal of mycorrhizal fungi. Many of the fungi found in this study form hypogeous (underground) fruiting bodies that are unable to independently spread spores via wind. Because dingoes move over larger areas than their prey, they are especially important to these ecosystem functions.

Implications

Our novel approach to studying an overlooked aspect of predator ecology is applicable in most terrestrial ecosystems. Similar modelling approaches could also be employed to understand the dispersal potential of both primary and secondary spore dispersers globally. Because this study highlights an unrecognised ecosystem service provided by dingoes, we hope that it will stimulate research to develop a more comprehensive understanding of other apex predators’ ecosystem functions.

Keywords: canids, carnivore ecology, diplochory, free-ranging dog, fungal ecology, mycophagy, mycorrhizae, predator ecology, spore dispersal.

References

Aguirre F, Nouhra E, Urcelay C (2021) Native and non-native mammals disperse exotic ectomycorrhizal fungi at long distances from pine plantations. Fungal Ecology 49, 101012.
| Crossref | Google Scholar |

Allen MF, Hipps LE, Wooldridge GL (1989) Wind dispersal and subsequent establishment of VA mycorrhizal fungi across a successional arid landscape. Landscape Ecology 2, 165-171.
| Crossref | Google Scholar |

Banta CA, Clemens ET, Krinsky MM, Sheffy BE (1979) Sites of organic acid production and patterns of digesta movement in the gastrointestinal tract of dogs. The Journal of Nutrition 109, 1592-1600.
| Crossref | Google Scholar |

Bradshaw AJ, Autumn KC, Rickart EA, Dentinger BTM (2022) On the origin of feces: fungal diversity, distribution, and conservation implications from feces of small mammals. Environmental DNA 2022, 608-626.
| Crossref | Google Scholar |

Brunner H, Coman BJ (1974) ‘The Identification of Mammalian Hair.’ (Inkata Press: Melbourne, Vic. Australia)

Burrows CF, Kronfeld DS, Banta CA, Merritt AM (1982) Effects of fiber on digestibility and transit time in dogs. The Journal of Nutrition 112, 1726-1732.
| Crossref | Google Scholar |

Caiafa MV, Jusino MA, Wilkie AC, Díaz IA, Sieving KE, Smith ME (2021) Discovering the role of Patagonian birds in the dispersal of truffles and other mycorrhizal fungi. Current Biology 31, 5558-5570.e3.
| Crossref | Google Scholar |

Childs-Sanford SE, Angel CR (2006) Transit time and digestibility of two experimental diets in the maned wolf (Chrysocyon brachyurus) and domestic dog (Canis lupus). Zoo Biology 25, 369-381.
| Crossref | Google Scholar |

Claridge AW, May TW (1994) Mycophagy among Australian mammals. Austral Ecology 19, 251-275.
| Crossref | Google Scholar |

Cloutier VB, Piché Y, Fortin JA, Bérubé JA, Glémet H, Desrochers A (2019) A novel approach for tracing mycophagous small mammals and documenting their fungal diets. Botany 97, 475-785.
| Crossref | Google Scholar |

Danks MA (2012) Gut-retention time in mycophagous mammals: a review and a study of truffle-like fungal spore retention in the swamp wallaby. Fungal Ecology 5, 200-210.
| Crossref | Google Scholar |

Danks M, Lebel T, Vernes K, Andrew N (2013) Truffle-like fungi sporocarps in a eucalypt-dominated landscape: patterns in diversity and community structure. Fungal Diversity 58, 143-157.
| Crossref | Google Scholar |

Danks MA, Simpson N, Elliott TF, Paine CET, Vernes K (2020) Modeling mycorrhizal fungi dispersal by the mycophagous swamp wallaby (Wallabia bicolor). Ecology and Evolution 10, 12920-12928.
| Crossref | Google Scholar |

De Cuyper A, Hesta M, Tibosch S, Wanke C, Clauss M, Janssens GPJ (2018) How does dietary particle size affect carnivore gastrointestinal transit: a dog model. Journal of Animal Physiology and Animal Nutrition 102, e615-e622.
| Crossref | Google Scholar |

Doherty TS, Davis NE, Dickman CR, Forsyth DM, Letnic M, Nimmo DG, et al. (2019) Continental patterns in the diet of a top predator: Australia’s dingo. Mammal Review 49, 31-44.
| Crossref | Google Scholar |

Dundas SJ, Hopkins AJM, Ruthrof KX, Tay NE, Burgess TI, Hardy GESJ, Fleming PA (2018) Digging mammals contribute to rhizosphere fungal community composition and seedling growth. Biodiversity and Conservation 27, 3071-3086.
| Crossref | Google Scholar |

Elliott TF, Vernes K (2019) Superb lyrebird Menura novaehollandiae mycophagy, truffles and soil disturbance. Ibis 161, 198-204.
| Crossref | Google Scholar |

Elliott TF, Jusino MA, Trappe JM, Lepp H, Ballard G-A, Bruhl JJ, Vernes K (2019a) A global review of the ecological significance of symbiotic associations between birds and fungi. Fungal Diversity 98, 161-194.
| Crossref | Google Scholar |

Elliott TF, Bower DS, Vernes K (2019b) Reptilian mycophagy: a global review of mutually beneficial associations between reptiles and macrofungi. Mycosphere 10, 776-797.
| Crossref | Google Scholar |

Elliott TF, Truong C, Jackson SM, Zúñiga CL, Trappe JM, Vernes K (2022) Mammalian mycophagy: a global review of ecosystem interactions between mammals and fungi. Fungal Systematics and Evolution 9, 99-159.
| Crossref | Google Scholar |

Geml J, Tulloss RE, Laursen GA, Sazanova NA, Taylor DL (2008) Evidence for strong inter- and intracontinental phylogeographic structure in Amanita muscaria, a wind-dispersed ectomycorrhizal basidiomycete. Molecular Phylogenetics and Evolution 48, 694-701.
| Crossref | Google Scholar |

Hernot DC, Biourge VC, Martin LJ, Dumon HJ, Nguyen PG (2005) Relationship between total transit time and faecal quality in adult dogs differing in body size. Journal of Animal Physiology and Animal Nutrition 89, 189-193.
| Crossref | Google Scholar |

Holland GJ, Bennett AF (2009) Differing responses to landscape change: implications for small mammal assemblages in forest fragments. Biodiversity and Conservation 18, 2997-3016.
| Crossref | Google Scholar |

Hopkins AJM, Tay NE, Bryant GL, Ruthrof KX, Valentine LE, Kobryn H, Burgess TI, Richardson BB, Hardy GESJ, Fleming PA (2021) Urban remnant size alters fungal functional groups dispersed by a digging mammal. Biodiversity and Conservation 30, 3983-4003.
| Crossref | Google Scholar |

Jackson SM, Groves CP, Fleming PJS, Aplin KP, Eldridge MDB, Gonzalez A, Helgen KM (2017) The wayward dog: is the Australian native dog or dingo a distinct species? Zootaxa 4317, 201-224.
| Crossref | Google Scholar |

Jackson SM, Fleming PJS, Eldridge MDB, Archer M, Ingleby S, Johnson RN, Helgen KM (2021) Taxonomy of the dingo: it’s an ancient dog. Australian Zoologist 41, 347-357.
| Crossref | Google Scholar |

Jonsson L, Dahlberg A, Nilsson M-C, Kårén O, Zackrisson O (1999) Continuity of ectomycorrhizal fungi in self-regenerating boreal Pinus sylvestris forests studied by comparing mycobiont diversity on seedlings and mature trees. New Phytologist 142, 151-162.
| Crossref | Google Scholar |

Li D-W (2005) Release and dispersal of basidiospores from Amanita muscaria var. alba and their infiltration into a residence. Mycological Research 109, 1235-1242.
| Crossref | Google Scholar |

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 Ecology 27, 1-13.
| Crossref | Google Scholar |

Nuske SJ, Anslan S, Tedersoo L, Congdon BC, Abell SE (2019) Ectomycorrhizal fungal communities are dominated by mammalian dispersed truffle-like taxa in north-east Australian woodlands. Mycorrhiza 29, 181-193.
| Crossref | Google Scholar |

O’Malley A (2013) Spatial patterns in the distribution of truffle-like fungi, mutualistic interactions with mammals, and spore dispersal dynamics. PhD Thesis, University of New England, Armidale, NSW, Australia.

Ori F, Menotta M, Leonardi M, Amicucci A, Zambonelli A, Covès H, Selosse M-A, Schneider-Maunoury L, Pacioni G, Iotti M (2021) Effect of slug mycophagy on Tuber aestivum spores. Fungal Biology 125, 796-805.
| Crossref | Google Scholar |

Peay KG, Schubert MG, Nguyen NH, Bruns TD (2012) Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Molecular Ecology 21, 4122-4136.
| Crossref | Google Scholar |

Pires AS, Koeler Lira P, Fernandez FAS, Schittini GM, Oliveira LC (2002) Frequency of movements of small mammals among Atlantic Coastal Forest fragments in Brazil. Biological Conservation 108, 229-237.
| Crossref | Google Scholar |

R Core Team (2020) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria)

Specht RL (1970) Vegetation. In ‘The Australian Environment’. 4th edn. (Ed. GW Leeper) pp. 44–67. (CSIRO and Melbourne University Press: Melbourne, Vic., Australia)

Strahan R (1983) ‘Complete Book of Australian Mammals.’ (Angus & Robertson: Sydney, NSW, Australia)

Swihart RK, Slade NA, Bergstrom BJ (1988) Relating body size to the rate of home range use in mammals. Ecology 69, 393-399.
| Crossref | Google Scholar |

Tay NE, Hopkins AJM, Ruthrof KX, Burgess T, Hardy GES, Fleming PA (2018) The tripartite relationship between a bioturbator, mycorrhizal fungi, and a key Mediterranean forest tree. Austral Ecology 43, 742-751.
| Crossref | Google Scholar |

Trappe JM (1988) Lessons from alpine fungi. Mycologia 80, 1-10.
| Crossref | Google Scholar |

Trappe JM, Strand RF (1969) Mycorrhizal deficiency in a Douglas-fir region nursery. Forest Science 15, 381-389.
| Google Scholar |

Triggs B (2004) ‘Tracks, Scats, and Other Traces: a Field Guide to Australian Mammals.’ Revised edn. (Oxford University Press: Melbourne, Vic., Australia)

Vašutová M, Mleczko P, López-García A, Maček I, Boros G, Ševčík J, Fujii S, Hackenberger D, Tuf IH, Hornung E, Páll-Gergely B, Kjøller R (2019) Taxi drivers: the role of animals in transporting mycorrhizal fungi. Mycorrhiza 29, 413-434.
| Crossref | Google Scholar |

Vogilino P (1895) Richerche intorno all’ azione delle lumache e dei rospi nello sviluppo di Agaricini. Nuovo Giornale Botanico 27, 181-185 [In Italian].
| Google Scholar |

Warner NJ, Allen MF, MacMahon JA (1987) Dispersal agents of vesicular–arbuscular mycorrhizal fungi in a disturbed arid ecosystem. Mycologia 79, 721-730.
| Crossref | Google Scholar |

Watson DM, Shaw D (2018) Veiled polypore (Cryptoporus volvatus) as a foraging substrate for the white-headed woodpecker (Picoides albolarvatus). Northwestern Naturalist 99, 58-62.
| Crossref | Google Scholar |

Zambonelli A, Ori F, Hall I (2017) Mycophagy and spore dispersal by vertebrates. In ‘The Fungal Community: its Organization and Role in the Ecosystem, Vol. 32’. 4th edn. (Eds J Dighton, JF White) pp. 347–358. (CRC Press: Boca Raton, FL, USA)