The fungal rat race: mycophagy among rodent communities in eastern Australia
Todd F. Elliott A * , Kelsey Elliott B and Karl Vernes AA Ecosystem Management, School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia.
B Integrative Studies Department, Warren Wilson College, Swannanoa, NC 28778, USA.
Wildlife Research 50(7) 526-536 https://doi.org/10.1071/WR22062
Submitted: 28 March 2022 Accepted: 3 July 2022 Published: 26 July 2022
© 2023 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: Rodents in many parts of the world perform an important ecosystem function as dispersers of mycorrhizal fungal spores. These fungi are vital to nutrient uptake in plant communities, but many of the fungal taxa that form these associations have fruiting bodies that are reliant on animals for their spore dispersal.
Aims: Numerous studies have focused on the ecological importance of Australian marsupials (especially members of the Potoroidae) for the dispersal of these ecologically important fungi. We chose to focus this study on the role of murid rodents in the dispersal of these fungi in eastern Australia.
Methods: To compare fungal taxa in murid diets, we trapped rodents in three regions of eastern Australia; our study sites spanned over 2000 km from temperate eucalypt forests to tropical eucalypt and tropical rainforest habitats. We performed microanalysis on all scats to determine whether fungi were consumed and which taxa were being eaten. Statistical analysis was conducted to investigate trends in levels of mycophagy among species and habitats.
Key results: We examined 10 rodent species, and all were shown to ingest mycorrhizal fungi to varying degrees. The diversity, abundance and specific fungal taxa consumed varied depending on the site and forest type. In drier forests dominated by Eucalyptus spp., the fungal taxa consumed and dispersed were primarily ectomycorrhizal; in wetter rainforest habitats, the fungal diversity consumed was far lower and included primarily vesicular arbuscular fungi. We provide the first evidence of mycophagy by grassland melomys (Melomys burtoni) and Cape York melomys (Melomys capensis).
Conclusions: Our findings highlight the importance of rodents as dispersers of mycorrhizal fungi across a variety of habitats from temperate to tropical forests of eastern Australia.
Implications: This study increases the existing knowledge of rodent diets and habitat requirements. It also provides a new angle for mammal conservation efforts, given the vital nature of the ecosystem service provided by these small and frequently overlooked mammals.
Keywords: hypogeous fungi, mammal diets, mammal ecology, Melomys, mycorrhizae, Pseudomys oralis, Rattus, spore dispersal, Uromys, Zyzomys argurus.
References
Caiafa, MV, Jusino, MA, Wilkie, AC, Díaz, IA, Sieving, KE, and Smith, ME (2021). Discovering the role of Patagonian birds in the dispersal of truffles and other mycorrhizal fungi. Current Biology 31, 5558–5570.e3.| Discovering the role of Patagonian birds in the dispersal of truffles and other mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |
Caldwell, I, Vernes, KA, and Barlocher, F (2005). The northern flying squirrel (Glaucomys sabrinus) as a vector for inoculation of red spruce (Picea rubens) seedlings with ectomycorrhizal fungi. Sydowia 57, 166–178.
Cázares, E, and Trappe, JM (1994). Spore dispersal of ectomycorrhizal fungi on a glacier forefront by mammal mycophagy. Mycologia 86, 507–510.
| Spore dispersal of ectomycorrhizal fungi on a glacier forefront by mammal mycophagy.Crossref | GoogleScholarGoogle Scholar |
Claridge, AW, and May, TW (1994). Mycophagy among Australian mammals. Australian Journal of Ecology 19, 251–275.
| Mycophagy among Australian mammals.Crossref | GoogleScholarGoogle Scholar |
Colgan, W, and Claridge, AW (2002). Mycorrhizal effectiveness of Rhizopogon spores recovered from faecal pellets of small forest-dwelling mammals. Mycological Research 106, 314–320.
| Mycorrhizal effectiveness of Rhizopogon spores recovered from faecal pellets of small forest-dwelling mammals.Crossref | GoogleScholarGoogle Scholar |
Comport, SS, and Hume, ID (1998). Gut morphology and rate of passage of fungal spores through the gut of a tropical rodent, the giant white-tailed rat (Uromys caudimaculatus). Australian Journal of Zoology 46, 461–471.
| Gut morphology and rate of passage of fungal spores through the gut of a tropical rodent, the giant white-tailed rat (Uromys caudimaculatus).Crossref | GoogleScholarGoogle Scholar |
Cove, MV, Simons, TR, Gardner, B, Maurer, AS, and O’Connell, AF (2017). Evaluating nest supplementation as a recovery strategy for the endangered rodents of the Florida Keys. Restoration Ecology 25, 253–260.
| Evaluating nest supplementation as a recovery strategy for the endangered rodents of the Florida Keys.Crossref | GoogleScholarGoogle 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.
| Gut-retention time in mycophagous mammals: a review and a study of truffle-like fungal spore retention in the swamp wallaby.Crossref | GoogleScholarGoogle Scholar |
Danks, MA, Simpson, N, Elliott, TF, Paine, CET, and Vernes, K (2020). Modeling mycorrhizal fungi dispersal by the mycophagous swamp wallaby (Wallabia bicolor). Ecology and Evolution 10, 12920–12928.
| Modeling mycorrhizal fungi dispersal by the mycophagous swamp wallaby (Wallabia bicolor).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 |
Elliott, TF, and Marshall, PA (2016). Animal-fungal interactions 1: notes on bowerbird’s use of fungi. Australian Zoologist 38, 59–61.
| Animal-fungal interactions 1: notes on bowerbird’s use of fungi.Crossref | GoogleScholarGoogle Scholar |
Elliott, TF, and Vernes, K (2021). Notes on the diets of four rodent species from Goodenough Island. Australian Mammalogy 43, 256–259.
| Notes on the diets of four rodent species from Goodenough Island.Crossref | GoogleScholarGoogle Scholar |
Elliott, TF, Jusino, MA, Trappe, JM, Lepp, H, Ballard, G-A, Bruhl, JJ, and Vernes, K (2019a). A global review of the ecological significance of symbiotic associations between birds and fungi. Fungal Diversity 98, 161–194.
| A global review of the ecological significance of symbiotic associations between birds and fungi.Crossref | GoogleScholarGoogle Scholar |
Elliott, TF, Bower, DS, and Vernes, K (2019b). Reptilian mycophagy: a global review of mutually beneficial associations between reptiles and macrofungi. Mycosphere 10, 776–797.
| Reptilian mycophagy: a global review of mutually beneficial associations between reptiles and macrofungi.Crossref | GoogleScholarGoogle Scholar |
Elliott, TF, Townley, S, Johnstone, C, Meek, P, Gynther, I, and Vernes, K (2020). The endangered Hastings River mouse (Pseudomys oralis) as a disperser of ectomycorrhizal fungi in eastern Australia. Mycologia 112, 1075–1085.
| The endangered Hastings River mouse (Pseudomys oralis) as a disperser of ectomycorrhizal fungi in eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Elliott, TF, Truong, C, Jackson, S, Zúñiga, CL, Trappe, JM, and Vernes, K (2022). Mammalian mycophagy: a global review of ecosystem interactions between mammals and fungi. Fungal Systematics and Evolution 9, 99–159.
| Mammalian mycophagy: a global review of ecosystem interactions between mammals and fungi.Crossref | GoogleScholarGoogle Scholar |
Firth, RSC, Brook, BW, Woinarski, JCZ, and Fordham, DA (2010). Decline and likely extinction of a northern Australian native rodent, the Brush-tailed Rabbit-rat Conilurus penicillatus. Biological Conservation 143, 1193–1201.
| Decline and likely extinction of a northern Australian native rodent, the Brush-tailed Rabbit-rat Conilurus penicillatus.Crossref | GoogleScholarGoogle Scholar |
Fogel, R, and Trappe, JM (1978). Fungus consumption (mycophagy) by small animals. Northwest Science 52, 1–31.
Gasparini, B (2014). Cortinarius (Agaricales) revised taxonomy: new species names or combinations. Mycosphere 5, 541–544.
| Cortinarius (Agaricales) revised taxonomy: new species names or combinations.Crossref | GoogleScholarGoogle Scholar |
Hamilton, MJ, and Leslie, DM (2021). Celebrating five decades of Mammalian Species, highlighted by the publication of the 1,000th account. Journal of Mammalogy 102, 681–684.
| Celebrating five decades of Mammalian Species, highlighted by the publication of the 1,000th account.Crossref | GoogleScholarGoogle Scholar |
Johnson, CN (1996). Interactions between mammals and ectomycorrhizal fungi. Trends in Ecology & Evolution 11, 503–507.
| Interactions between mammals and ectomycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |
Maser C, Claridge AW, Trappe JM (2008) ‘Trees, truffles, and beasts: how forests function.’ (Rutgers University Press: New Brunswick, NJ, USA)
McGee, PA, and Baczocha, N (1994). Sporocarpic Endogonales and Glomales in the scats of Rattus and Perameles. Mycological Research 98, 246–249.
| Sporocarpic Endogonales and Glomales in the scats of Rattus and Perameles.Crossref | GoogleScholarGoogle Scholar |
Miranda, V, Rothen, C, Yela, N, Aranda-Rickert, A, Barros, J, Calcagno, J, and Fracchia, S (2019). Subterranean desert rodents (genus Ctenomys) create soil patches enriched in root endophytic fungal propagules. Microbial Ecology 77, 451–459.
| Subterranean desert rodents (genus Ctenomys) create soil patches enriched in root endophytic fungal propagules.Crossref | GoogleScholarGoogle Scholar |
Nouhra, E, Kuhar, F, Truong, C, Pastor, N, Crespo, E, Mujic, A, Caiafa, MV, and Smith, ME (2021). Thaxterogaster revisited: a phylogenetic and taxonomic overview of sequestrate Cortinarius from Patagonia. Mycologia 113, 1022–1055.
| Thaxterogaster revisited: a phylogenetic and taxonomic overview of sequestrate Cortinarius from Patagonia.Crossref | GoogleScholarGoogle Scholar |
Nuske, SJ, Vernes, K, May, TW, Claridge, AW, Congdon, BC, Krockenberger, A, and Abell, SE (2017a). Redundancy among mammalian fungal dispersers and the importance of declining specialists. Fungal Ecology 27, 1–13.
| Redundancy among mammalian fungal dispersers and the importance of declining specialists.Crossref | GoogleScholarGoogle Scholar |
Nuske, SJ, Vernes, K, May, TW, Claridge, AW, Congdon, BC, Krockenberger, A, and Abell, SE (2017b). Data on the fungal species consumed by mammal species in Australia. Data in Brief 12, 251–260.
| Data on the fungal species consumed by mammal species in Australia.Crossref | GoogleScholarGoogle Scholar |
Nuske, SJ, Anslan, S, Tedersoo, L, Congdon, BC, and Abell, SE (2019). Ectomycorrhizal fungal communities are dominated by mammalian dispersed truffle-like taxa in north-east Australian woodlands. Mycorrhiza 29, 181–193.
| Ectomycorrhizal fungal communities are dominated by mammalian dispersed truffle-like taxa in north-east Australian woodlands.Crossref | GoogleScholarGoogle Scholar |
Oksanen J, Guillaume Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2020) vegan: community ecology package. R package version 2.5-7. Available at https://CRAN.R-project.org/package=vegan
Ori, F, Trappe, J, Leonardi, M, Iotti, M, and Pacioni, G (2018). Crested porcupines (Hystrix cristata): mycophagist spore dispersers of the ectomycorrhizal truffle Tuber aestivum. Mycorrhiza 28, 561–565.
| Crested porcupines (Hystrix cristata): mycophagist spore dispersers of the ectomycorrhizal truffle Tuber aestivum.Crossref | GoogleScholarGoogle Scholar |
Pastor, N, Chiapella, J, Kuhar, F, Mujic, AB, Crespo, EM, and Nouhra, ER (2019). Unveiling new sequestrate Cortinarius species from northern Patagonian Nothofagaceae forests based on molecular and morphological data. Mycologia 111, 103–117.
| Unveiling new sequestrate Cortinarius species from northern Patagonian Nothofagaceae forests based on molecular and morphological data.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2020) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria). Available at https://www.R-project.org/
Reddell, P, Spain, AV, and Hopkins, M (1997). Dispersal of spores of mycorrhizal fungi in scats of native mammals in tropical forests of northeastern Australia. Biotropica 29, 184–192.
| Dispersal of spores of mycorrhizal fungi in scats of native mammals in tropical forests of northeastern Australia.Crossref | GoogleScholarGoogle Scholar |
Roycroft, E, MacDonald, AJ, Moritz, C, Moussalli, A, Portela Miguez, R, and Rowe, KC (2021). Museum genomics reveals the rapid decline and extinction of Australian rodents since European settlement. Proceedings of the National Academy of Sciences 118, e2021390118.
| Museum genomics reveals the rapid decline and extinction of Australian rodents since European settlement.Crossref | GoogleScholarGoogle Scholar |
Shevill DI (1999) ‘The ecology of the Rufus Spiny Bandicoot, Echymipera rufescens australis (Peters and Doria) (Marsupialia: Peramelidae) in Lowland Rainforest of Iron Range National Park, Cape York Peninsula.’ (James Cook University, School of Tropical Biology)
Shevill, DI, and Johnson, CN (2007). Diet and breeding of the rufous spiny bandicoot Echymipera rufescens australis, Iron Range, Cape York Peninsula. Australian Mammalogy 29, 169–175.
| Diet and breeding of the rufous spiny bandicoot Echymipera rufescens australis, Iron Range, Cape York Peninsula.Crossref | GoogleScholarGoogle Scholar |
Smith, AP, and Quin, DG (1996). Patterns and causes of extinction and decline in Australian conilurine rodents. Biological Conservation 77, 243–267.
| Patterns and causes of extinction and decline in Australian conilurine rodents.Crossref | GoogleScholarGoogle Scholar |
Stephens, RB, and Rowe, RJ (2020). The underappreciated role of rodent generalists in fungal spore dispersal networks. Ecology 101, e02972.
| The underappreciated role of rodent generalists in fungal spore dispersal networks.Crossref | GoogleScholarGoogle Scholar |
Stephens, RB, Trowbridge, AM, Ouimette, AP, Knighton, WB, Hobbie, EA, Stoy, PC, and Rowe, RJ (2020). Signaling from below: rodents select for deeper fruiting truffles with stronger volatile emissions. Ecology 101, e02964.
| Signaling from below: rodents select for deeper fruiting truffles with stronger volatile emissions.Crossref | GoogleScholarGoogle Scholar |
Swihart, RK, Slade, NA, and Bergstrom, BJ (1988). Relating body size to the rate of home range use in mammals. Ecology 69, 393–399.
| Relating body size to the rate of home range use in mammals.Crossref | GoogleScholarGoogle Scholar |
Taylor, RJ (1992). Seasonal changes in the diet of the Tasmanian bettong (Bettongia gaimardi), a mycophagous marsupial. Journal of Mammalogy 73, 408–414.
| Seasonal changes in the diet of the Tasmanian bettong (Bettongia gaimardi), a mycophagous marsupial.Crossref | GoogleScholarGoogle Scholar |
Tedersoo, L, May, TW, and Smith, ME (2010). Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20, 217–263.
| Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages.Crossref | GoogleScholarGoogle Scholar |
Thiers, HD (1984). The secotioid syndrome. Mycologia 76, 1–8.
| The secotioid syndrome.Crossref | GoogleScholarGoogle Scholar |
Trappe, JM, and Maser, C (1976). Germination of spores of Glomus macrocarpus (Endogonaceae) after passage through a rodent digestive tract. Mycologia 68, 433–436.
| Germination of spores of Glomus macrocarpus (Endogonaceae) after passage through a rodent digestive tract.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 |
Vašutová, M, Mleczko, P, López-García, A, Maček, I, Boros, G, Ševčík, J, Fujii, S, Hackenberger, D, Tuf, IH, Hornung, E, Páll-Gergely, B, and Kjøller, R (2019). Taxi drivers: the role of animals in transporting mycorrhizal fungi. Mycorrhiza 29, 413–434.
| Taxi drivers: the role of animals in transporting mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |
Vernes, K (2014). Seasonal truffle consumption by long-nosed bandicoots (Perameles nasuta) in a mixed rainforest–open forest community in north-eastern New South Wales. Australian Mammalogy 36, 113–115.
| Seasonal truffle consumption by long-nosed bandicoots (Perameles nasuta) in a mixed rainforest–open forest community in north-eastern New South Wales.Crossref | GoogleScholarGoogle Scholar |
Vernes, K, and Dunn, L (2009). Mammal mycophagy and fungal spore dispersal across a steep environmental gradient in eastern Australia. Austral Ecology 34, 69–76.
| Mammal mycophagy and fungal spore dispersal across a steep environmental gradient in eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Vernes, K, and McGrath, K (2009). Are introduced black rats (Rattus rattus) a functional replacement for mycophagous native rodents in fragmented forests? Fungal Ecology 2, 145–148.
| Are introduced black rats (Rattus rattus) a functional replacement for mycophagous native rodents in fragmented forests?Crossref | GoogleScholarGoogle Scholar |
Vernes, K, Castellano, M, and Johnson, CN (2001). Effects of season and fire on the diversity of hypogeous fungi consumed by a tropical mycophagous marsupial. Journal of Animal Ecology 70, 945–954.
| Effects of season and fire on the diversity of hypogeous fungi consumed by a tropical mycophagous marsupial.Crossref | GoogleScholarGoogle Scholar |
Vernes, K, Cooper, T, and Green, S (2015). Seasonal fungal diets of small mammals in an Australian temperate forest ecosystem. Fungal Ecology 18, 107–114.
| Seasonal fungal diets of small mammals in an Australian temperate forest ecosystem.Crossref | GoogleScholarGoogle Scholar |
Vernes, K, Elliott, TF, and Jackson, SM (2021). 150 years of mammal extinction and invasion at Koonchera Dune in the Lake Eyre Basin of South Australia. Biological Invasions 23, 593–610.
| 150 years of mammal extinction and invasion at Koonchera Dune in the Lake Eyre Basin of South Australia.Crossref | GoogleScholarGoogle Scholar |
Waller, NL, Gynther, IC, Freeman, AB, Lavery, TH, and Leung, LK-P (2017). The Bramble Cay melomys Melomys rubicola (Rodentia: Muridae): a first mammalian extinction caused by human-induced climate change? Wildlife Research 44, 9–21.
| The Bramble Cay melomys Melomys rubicola (Rodentia: Muridae): a first mammalian extinction caused by human-induced climate change?Crossref | GoogleScholarGoogle Scholar |
Wellesley-Whitehouse H (1983) White-tailed rat Uromys caudimaculatus. In ‘The Australian Museum complete book of Australian Mammals’. (Ed. R Strahan) pp. 371. (Angus and Robertson: Sydney, NSW, Australia)
Wildi O (2017) ‘Data analysis in vegetation ecology.’ 3rd edn. (CABI: Wallingford, UK)
Wilson DE, Lacher TE, Mittermeier RA (Eds) (2017) ‘Handbook of the mammals of the world. Vol. 7. Rodents II.’ (Lynx Editions: Barcelona, Spain)