The importance of declining mammalian fungal specialists for ectomycorrhizal fungal dispersal

Nuske, Susan Joy (2017) The importance of declining mammalian fungal specialists for ectomycorrhizal fungal dispersal. PhD thesis, James Cook University.

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Conservation is more than just preserving biodiversity but also preserving ecosystem processes. Understanding how loss of diversity can affect the functioning of ecosystems requires understanding of the system's functional redundancy. That is, how many species in the system perform similar roles and can compensate for the loss of similar species? In this thesis, I investigate the functional redundancy among mammal species involved in an important, yet poorly understood, interaction between three very different organisms; fungi, plants and mammals.

Mycorrhizal fungi associate mutualistically with the roots of many plant species. In exchange for nutrients accessed by the fungi, the plants provide the fungus with sugars (carbohydrates) from their photosynthesis. Many mycorrhizal species form below-ground fruit-bodies (truffles) that rely on mammals for spore dispersal. This interaction led to the hypothesis that mammals are important for fungal species diversity, plant-fungal interactions and ecosystem functioning. However, little is known about how truffles contribute to the structure of mycorrhizal communities. For instance, are truffle taxa that mammals disperse important components of the mycorrhizal community as a whole and thus, can mammals influence mycorrhizal community structure?

Globally, many different mammals are known to consume and disperse truffles, some to a much greater degree than others. For example, the term 'fungal specialists' is used for mammals that consume fungi for the majority of their diet (>50%, relative to other food types). Often as a consequence, fungal specialists can also consume (and disperse) a diversity of truffle species. Many mammals with generalist diets, on the other hand, frequently consume truffle fungi opportunistically. Hence, individual mammals with generalist diets often consume a lower diversity of truffle fungal species than mammals with fungal specialist diets. However, currently it is unknown whether the combined fungal dispersal role of mammals with generalist diets equates to that of a specialist (i.e.: is there functional redundancy in the system?). In other words, if a fungal specialist were to become extinct in an ecosystem, is there enough functional redundancy that the dispersal roles for truffle fungi will be fulfilled by the remaining mammals with generalist diets?

Understanding this interaction is particularly relevant to Australian ecosystems. Unfortunately, Australia has the highest rate of mammal extinction and decline, including fungal specialists within the family Potoroidae. Additionally, the majority of Australia's native forests are dominated by woodland trees that host truffle-producing ectomycorrhizal (ECM) fungi (for instance, Eucalyptus, Corymbia, Allocasuarina, Melaleuca). In this thesis, I addressed a number of research questions aimed at better understanding how the loss of mammalian diversity could potentially impact on truffle populations and mycorrhizal communities. These research results pave the way to understanding how loss of mammal diversity could influence fungus-plant interactions and ecosystem functioning.

In Chapter Two, a meta-analysis brings together discordant data on fungal diets of mammals across Australia. These data were used to ask whether there is functional redundancy in fungal dispersal roles among mammalian fungal specialists and mammals with generalist diets. Despite detecting a sampling bias in the literature, on average, fungal specialists consumed fungi at a higher diversity and abundance, and more consistently across seasons than mycophagous mammals with generalist diets, indicating little functional redundancy in general. However, some generalist mammals ate a fungal species diversity on par with specialists (Rattus fuscipes, Perameles nasuta and Wallabia bicolor) indicating that there may be functional redundancy in some systems. Studies presented in this meta-analysis utilised differences in morphological characters of spores to identify fungal species, however, this technique has limited resolution with some groups (e.g. Russulaceae). Additionally, much of the data could not be compared between studies because many taxa were undescribed (e.g. Unknown species 1).

Results from Chapter Two are built on in Chapter Three, by directly comparing fungal diets of a specialist and nine co-occurring generalist fungal diets using modern DNA sequencing techniques. This direct comparison eliminated the biases associated with using data collected from different studies and allowed a higher resolution of fungal species diversity to be measured. I found that the fungal specialist, Bettongia tropica (northern bettong), consumed a significantly higher diversity and more unique mycorrhizal and truffle fungal taxa than the combined diets of the generalists. Bettongia tropica also had a significantly different fungal community in their diets. These trends were consistent across sites and seasons. These data suggest that there is little functional redundancy in this ecosystem and indicates that truffle fungi populations may be detrimentally impacted by the loss of the endangered B. tropica.

To further understand whether potential loss of truffle taxa, via loss of specialists, would have detrimental impacts on fungal-plant interactions, a good understanding of the structure of the mycorrhizal community must first be obtained. Yet, particularly in Australia, little is known about the structure of mycorrhizal communities and how truffle diversity contributes to it. In Chapter Four, this knowledge gap was addressed by measuring the mycorrhizal community at different scales using molecular methods. I found that the dominant mycorrhizal fungal taxa associating with plant roots were truffle taxa found in mycophagous mammalian diets. Over 80% of truffle taxa associating with roots were within the diet of the fungal specialist, and this percentage was just over half (52%) for generalist mammals. These data indicate that mammals, particularly those with specialist fungal diets, are important in shaping ECM fungal communities. This adds credence to the hypothesis that the loss of mammals could have detrimental effects on ECM communities and fungal-plant relationships.

Overall, my thesis addressed key knowledge gaps in the interactions between mycophagous mammals, ECM fungi and their host plants. This work also highlights previously overlooked ramifications of native mammal loss in Australia, drawing particular attention to specialist mycophagists whose role in maintaining the diversity of ECM truffle fungal taxa may be irreplaceable.

Item ID: 51587
Item Type: Thesis (PhD)
Keywords: conservation, diet, ecosystem function, Ectomycorrhizae, ectomycorrhizal fungi, functional redundancy, fungal generalist, fungal specialists, fungi, mammal loss, mammal, mycophagous mammals, mycophagy, mycorrhizal, potoroidae, rat-kangaroo, sequestrate fungi, spore dispersal, spore, truffle-like fungi
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Nuske, S.J., Vernes, K., May, T.W., Claridge, A.W., Congdon, B.C., Krockenberger, A., and Abell, S.E. (2017) Redundancy among mammalian fungal dispersers and the importance of declining specialists. Fungal Ecology, 27. pp. 1-13.

Chapter 2: Nuske, S.J., Vernes, K., May, T.W., Claridge, A.W., Congdon, B.C., Krockenberger, A., and Abell, S.E. (2017) Data on the fungal species consumed by mammal species in Australia. Data in Brief, 12. pp. 251-260.

Date Deposited: 20 Nov 2017 03:42
FoR Codes: 05 ENVIRONMENTAL SCIENCES > 0502 Environmental Science and Management > 050202 Conservation and Biodiversity @ 60%
05 ENVIRONMENTAL SCIENCES > 0501 Ecological Applications > 050102 Ecosystem Function @ 20%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060208 Terrestrial Ecology @ 20%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960806 Forest and Woodlands Flora, Fauna and Biodiversity @ 45%
96 ENVIRONMENT > 9613 Remnant Vegetation and Protected Conservation Areas > 961306 Remnant Vegetation and Protected Conservation Areas in Forest and Woodlands Environments @ 45%
97 EXPANDING KNOWLEDGE > 970105 Expanding Knowledge in the Environmental Sciences @ 10%
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