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Mammalian Mycophagy: a Global Review of Ecosystem Interactions Between Mammals and Fungi

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Mammalian Mycophagy: a Global Review of Ecosystem Interactions Between Mammals and Fungi

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The consumption of fungi by animals is a significant trophic interaction in most terrestrial ecosystems, yet the role mammals play in these associations has been incompletely studied. In this review, we compile 1 154 references published over the last 146 years and provide the first comprehensive global review of mammal species known to eat fungi (508 species in 15 orders). We review experimental studies that found viable fungal inoculum in the scats of at least 40 mammal species, including spores from at least 58 mycorrhizal fungal species that remained viable after ingestion by mammals. We provide a summary of mammal behaviours relating to the consumption of fungi, the nutritional importance of fungi for mammals, and the role of mammals in fungal spore dispersal. We also provide evidence to suggest that the morphological evolution of sequestrate fungal sporocarps (fruiting bodies) has likely been driven in part by the dispersal advantages provided by mammals. Finally, we demonstrate how these interconnected associations are widespread globally and have far-reaching ecological implications for mammals, fungi and associated plants in most terrestrial ecosystems.
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© 2022 Westerdijk Fungal Biodiversity Instute 99
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal Biodiversity Institute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
Fungal Systemacs and Evoluon
doi.org/10.3114/fuse.2022.09.07
VOLUME 9
JUNE 2022
PAGES 99–159
INTRODUCTION
Fungi have many dierent strategies for spore dispersal. The
most widespread mechanism among macrofungi involves
liberang spores into air currents via forcible discharge
(ballistospory among Basidiomycetes and bursng of the asci
among Ascomycetes) (Buller 1909, Money 1998, Trail 2007).
Other fungi rely on mutualisms with organisms that ingest their
sporocarps as a food reward for subsequent dispersal. The term
"mycophagy" refers to the consumpon of fungi by vertebrates
and invertebrates. Animals consume many groups of fungi that
form macroscopic sporocarps both above ground (epigeous, e.g.
mushrooms, brackets or cups) and below ground (hypogeous,
e.g. trues). These animals oen act as important vectors for the
spread of fungal spores across landscapes. Mammals, reples
and birds are signicant fungal dispersers (Fogel & Trappe 1978,
Claridge & May 1994, Maser et al. 2008, Ellio et al. 2019a, b,
Caiafa et al. 2021), but specialised dispersal associaons have
been most thoroughly studied among invertebrates (Fogel
1975, Hammond & Lawrence 1989, Schigel 2012, Kitabayashi
et al. 2022). For example, in one of its developmental stages,
the entomopathogenic fungal genus Massospora alters the
behaviour of male cicadas by using cathinone (an amphetamine)
and psilocybin (a tryptamine) to cause males to simulate the
behaviour of sexually recepve females (Boyce et al. 2018,
Cooley et al. 2018). This chemical manipulaon causes males
to aempt copulaon with the infected pseudo-female, leading
to further transmission of fungal spores. There are numerous
other examples of specialised invertebrate-fungal associaons.
The polypore Cryptoporus volvatus has a veil enclosing its
ferle surface; a diversity of insects live between these layers
and disperse spores by entering and exing via a portal hole
through the veil (Ingold 1953, Kadowaki 2010, Ellio 2020).
Members of the Phallaceae (snkhorns and relaves) release
pungent aromas that aract spore dispersing ies (Tuno 1998),
while some shelf fungi (e.g. Cerrena unicolor) have incredibly
specialised associaons with wood-boring Hymenoptera that
disperse spores as oidial inoculum transmied into the wood via
the wasp’s ovipositors (Ingold 1953, Bunyard 2015). Other fungi
(e.g. Guyanagaster necrorhizus as well as some members of the
Leucocoprineae, Lepiotaceae, Mycosphaerella, Phaeosphaeria,
Termitomyces and Tricholomataceae) rely enrely on termites,
Mammalian mycophagy: A global review of ecosystem interacons between mammals and
fungi
T.F. Ellio1*, C. Truong2,3, S.M. Jackson4,5,6, C.L. Zúñiga3, J.M. Trappe7, K. Vernes1
1Ecosystem Management, School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia
2Royal Botanic Gardens Victoria, Birdwood Ave, Melbourne, VIC 3004, Australia
3Instuto de Biología, Universidad Nacional Autónoma de México, Tercer Circuito s/n, Ciudad Universitaria, 04510 Ciudad de México, Mexico
4Australian Museum Research Instute, Australian Museum, 1 William St., Sydney, NSW 2010, Australia
5School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia
6Division of Mammals, Naonal Museum of Natural History, Smithsonian Instuon, Washington, DC 20013-7012, USA
7Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon 97331, USA
*Corresponding author: toddfellio@gmail.com
Abstract: The consumpon of fungi by animals is a signicant trophic interacon in most terrestrial ecosystems, yet the
role mammals play in these associaons has been incompletely studied. In this review, we compile 1 154 references
published over the last 146 years and provide the rst comprehensive global review of mammal species known to eat
fungi (508 species in 15 orders). We review experimental studies that found viable fungal inoculum in the scats of at least
40 mammal species, including spores from at least 58 mycorrhizal fungal species that remained viable aer ingeson
by mammals. We provide a summary of mammal behaviours relang to the consumpon of fungi, the nutrional
importance of fungi for mammals, and the role of mammals in fungal spore dispersal. We also provide evidence to
suggest that the morphological evoluon of sequestrate fungal sporocarps (fruing bodies) has likely been driven in
part by the dispersal advantages provided by mammals. Finally, we demonstrate how these interconnected associaons
are widespread globally and have far-reaching ecological implicaons for mammals, fungi and associated plants in most
terrestrial ecosystems.
Key words:
fungivory
mammal diets
mammal ecology
nutrion
sequestrate fungi
true
Citaon: Ellio TF, Truong C, Jackson S, Zúñiga CL, Trappe JM, Vernes K (2022). Mammalian mycophagy: a global review of ecosystem interacons
between mammals and fungi. Fungal Systemacs and Evoluon 9: 99–159. doi: 10.3114/fuse.2022.09.07
Received: 13 October 2021; Accepted: 2 April 2022; Effectively published online: 21 June 2022
Corresponding editor: P.W. Crous
© 2022 Westerdijk Fungal Biodiversity Instute
Elliott et al.
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
100
ants and snails for their dispersal (Chapela et al. 1994, Silliman &
Newell 2003, Nobre et al. 2011, Koch & Aime 2018). In addion
to the many specialised associaons with invertebrates, fungi
have also evolved a diversity of reproducve morphologies that
are well adapted to mammalian dispersal. Although associaons
between fungi and vertebrates are not as specialised as those
between fungi and invertebrates, many fungi consumed by
mammals have evolved a sequestrate sporocarp morphology
(spores are enclosed in a persistent skin called the pileus or
peridium). This skin makes it dicult for the spores of sequestrate
fungi to disperse without being eaten by animals. Sequestrate
sporocarp morphologies include some epigeous fungi and a
great diversity of hypogeous fungi (commonly referred to as
trues or true-like fungi) that have independently arisen in
mulple fungal linages and have evolved more than 100 mes
(Bonito et al. 2013, Sheedy et al. 2015, Truong et al. 2017, Ellio
& Trappe 2018, Ellio et al. 2020a, Palfner et al. 2020). While
there is some debate about what evoluonary factors may have
driven the rise of sequestrate morphologies (Sheedy et al. 2015),
the high diversicaon of sequestrate species in many fungal
groups may reect the dispersal advantages of mycophagy and
the major role that mammals played in the process (Trappe
1988, Trappe & Claridge 2005, Maser et al. 2008, Trappe et al.
2009, Beever & Lebel 2014).
Fungi with sequestrate sporocarp structures have numerous
reproducve benets, including substanal protecon from
extreme climac condions (temperature and humidity) and a
reduced likelihood of being eaten by mammals before spores are
mature (Maser et al. 2008, Beever & Lebel 2014). These factors
have likely contributed to the loss of forcible discharge among
sequestrate taxa and encouraged the transion away from
producing a stalk (which is usually not composed of spore-bearing
ssue). The loss of these traits allows sporocarps to opmise
spore producon in a larger percentage of reproducve ssue.
On the other hand, trade-os include suscepbility to saturated
soil (e.g. rong in place) and the reliance on other organisms to
disperse spores. To remedy this, many sequestrate fungi have
developed strategies to increase the probability of discovery by
animals, such as the producon of aromac aractants (Maser et
al. 2008). The mammals that excavate and consume hypogeous
fungi will subsequently disperse spores through their faeces.
Soil disturbance (bioturbaon) from digging for hypogeous
fungi increases fungal dispersal within the soil and improves soil
aeraon and organic maer decomposion (Fleming et al. 2014,
Davies et al. 2018, Palmer et al. 2020).
Sequestrate fungi are predominantly ectomycorrhizal
(ECM), so their successful dispersal is key to plant nutrion,
regeneraon and survival in many forest systems (Tedersoo et
al. 2010). In exchange for a carbon source, these fungi form
benecial associaons with the roots of their hosts and are vital
to plant nutrient uptake and water movement (Allen 1991, 2007
Agerer 2001, Peay et al. 2008, Tedersoo & Smith 2013). In the
rhizosphere, connuous mycelia of mulple ECM fungal species
form a “mycorrhizal network” linking plants of the same or
dierent species; within the network, fungal and plant species
interact, compete and provide posive/negave feedbacks that
can aect both plant and fungal communies (Gorzelak et al.
2015). Disrupons of mycorrhizal networks (e.g. through impacts
on biodiversity that result in the loss of mammal dispersers) can
therefore negavely aect regeneraon of ECM plant species
and forest resilience aer disturbance (Dundas et al. 2018, Liang
et al. 2020).
Previous work on animal-fungal interacons has provided
in-depth study and/or reviews on the ecological impacts
and importance of fungal consumpon by birds (Ellio et al.
2019a, Caiafa et al. 2021), reples (Ellio et al. 2019b) and
invertebrates (Fogel 1975, Hammond & Lawrence 1989, Schigel
2012). Given these previous works, we chose to focus this
review on the associaons between fungi and their mammal
consumers and how these interacons are benecial to fungal
dispersal, mammal nutrion, host plant communies and
overall ecosystem health. As highlighted below, these dispersal
modes and their interconnected associaons are widespread
yet remain incompletely studied in comparison to other elds,
such as pollinaon and seed dispersal ecology. Reproducve
success oen depends on interconnecons between
organisms, and these associaons can range from specialist to
generalist (Wheelwright & Orians 1982, Richardson et al. 2000,
Schiestl 2004, Schupp et al. 2010). Ecosystem processes are
complex and mulfaceted, and there are inevitably mulple
evoluonary factors aridicaon in parcular that have
contributed to the rise of sequestrate sporocarp morphologies.
Considering the dispersal advantages facilitated by vertebrate
vectors through the consumpon of fungi, we argue that
mammalian mycophagy has likely been a major contribung
factor to the rise of a wide range of sequestrate sporocarp
morphologies.
MATERIAL AND METHODS
This review is part of a series examining the associaons between
macrofungi and vertebrates; the two previous reviews examined
interacons between fungi and birds (Ellio et al. 2019a) and
between fungi and reples (Ellio et al. 2019b). In this study,
we carefully reviewed references of relevant publicaons and
conducted methodical searches in relevant journals, databases
and search engines for publicaons detailing the behaviours
and diets of hundreds of mammal species. We concentrated
our search eort on dietary studies based on known behaviours
of mammal species, including a focus on terrestrial rather than
oceanic mammal groups. For praccal reasons, we restricted
our literature search to publicaons wrien in English,
French, German, Portuguese and Spanish. Sources wrien in
a few other languages were included when we were able to
determine the mammal species reported to eat fungi, but we
did not systemacally review the literature beyond these ve
languages. We incorporated many of the references cited in the
review of small mammal mycophagy by Fogel & Trappe (1978),
but we could not locate all of the literature they cite. In total,
we compiled 1 154 references published over the last 146 years
(Fig. 1) reporng fungal consumpon by 508 mammal species
belonging to 15 orders (Fig. 2).
The number of publicaons on mammalian mycophagy is
substanally greater than that on birds and reples combined.
To make this review as comprehensive as possible in regard
to the mammal species that eat fungi, we omied imprecise
notes (e.g. those that menon a “squirrel” or a “mouse” eang
a mushroom) when we could not determine which mammal
species was being discussed. Some publicaons (e.g. Berkeley
& Broome 1887, Reess & Fisch 1887, Chan 1892, Thaxter 1922,
Zeller 1939, Dowding 1959, Hilton 1980) used general names
like bandicoot, potoroo, shrew, mole, rock rabbit, dormouse,
mouse, pine squirrel, jerboa, eld mouse, chipmunk, wood rat,
© 2022 Westerdijk Fungal Biodiversity Instute
Mammalian mycophagy
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
101
Fig. 1. Illustration of the number of publications reporting mammal mycophagy
published each decade between 1880 and 2020.
Fig. 1. Illustraon of the number of publicaons reporng mammal mycophagy published each decade between 1880 and 2020.
Fig. 2. Percentage of extant members of each order that has been reported to consume fungi. Numbers at end of graph bars indicate number of
extant mycophagous species we found reported in the literature. Number of species in each order is based on Hamilton & Leslie (2021). Note that this
gure only includes extant species. Two species that appear in the tables are not included in this graph and those are American mastodon (Mammut
americanum) and neanderthal (Homo neanderthalensis).
Fig. 2. Percentage of extant members of each order that has been reported to consume fungi.
Numbers at end of graph bars indicate number of extant mycophagous species we found
reported in the literature. Number of species in each order is based on Hamilton and Leslie
(2021). Note that this figure only includes extant species. Two species that appear in the
tables are not included in this graph and those are American mastodon (Mammut
americanum) and neanderthal (Homo neanderthalensis).
© 2022 Westerdijk Fungal Biodiversity Instute
Elliott et al.
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
102
deer and game animal. In these instances, we did our best to
determine what mammal species the authors were referring to,
but we somemes disregarded reports due to lack of taxonomic
clarity about the mammal species involved. Groups such as
mice or squirrels are among the most thoroughly documented
mycophagous mammals, so no value was lost by discarding
imprecise species reports.
Where necessary, we updated names from their original
citaon to reect current nomenclature. The taxonomy and
common names of mammals included in this review follow the
nomenclature of Wilson & Miermeier (2009, 2011, 2014),
Miermeier et al. (2013), Jackson & Groves (2015), and Wilson
et al. (2016, 2017, 2018, 2019). Total number of mammal
species in each order is based on Hamilton & Leslie (2021). Rates
of mycophagy may dier among subspecies, but we did not
consider subspecies due to the large number of mammal species
covered. In many instances, there was not enough informaon
for us to determine which subspecies was involved and its
taxonomic validity. Researchers interested in these parcular
issues can easily refer to the primary references provided under
cited species in Supplementary Tables S1–S11.
Some mammalogists incorrectly assume that fungi are eaten
mostly by rodents or other small mammals. This misconcepon
led us to focus this review on the diversity of mammals that eat
fungi rather than the diversity of fungal taxa eaten. Although
some studies idenfy what fungi are eaten, most only menon
“fungi” or “mushrooms” in the mammal diet. Terms used in
cited references range from formal species names to general
terms like toadstool, shelf mushroom, bracket fungus, true
and puall. When authors did provide idencaon, it was
rarely possible to determine how accurately they had idened
the fungal species; thus, it was not realisc for us to verify fungal
idencaons. We have not included lichens or myxomycetes
in this review. We discarded the informaon from Maser et al.
(1988) because they listed spores of three ECM true genera
that were consumed by a range of mammals, but the habitats
they sampled did not contain ECM host plants that are likely
to associate with these fungi. Apart from this case, we have no
reason to believe that the fungi and mammals reported were
inaccurately idened. Researchers interested specically in
the diversity of fungal taxa eaten by mammals can consult the
following reviews as starng points: Fogel & Trappe (1978),
Claridge & May (1994), Claridge et al. (1996), Piaoni et al.
(2016), and Nuske et al. (2017a, b). We also compiled a list of
fungal species that are consumed and whose spores remain
viable aer passage through the gut of mammals (Table 2).
Our review does not include literature related to animal
poisoning as a result of eang fungi. Although there is a
substanal body of work in veterinary literature related to pet
poisoning (e.g. Cleland 1934, Cole 1993, Naude & Berry 1997,
Puschner et al. 2007, Beug & Shaw 2009, Bates et al. 2014,
Möönen et al. 2014, Bates 2016 and Seljetun 2017), this area
of research has lile relevance to mycophagy in wild animals.
The behaviour and food choices of capve individuals does not
necessarily represent their wild relaves, and we are unaware of
any evidence of poisoning cases among wild individuals.
RESULTS
Diversity of mammal mycophagists by order
The following secon provides tables lisng a brief overview of
the mammal groups that contain the 508 species reported to eat
fungi. For anyone interested in the full lists and references for
mammal mycophagy compiled by this review please also refer
to the data provided in Supplementary Tables S1–11. Because
we have updated the nomenclature to current taxonomy, names
we list are not necessarily the same as in the cited references.
This secon is broken into subsecons organised phylogenecally
by mammalian order. Each of the 15 orders reported to eat
fungi is briey introduced. Any order containing three or more
mycophagous species has a supplementary table where families,
genera and species are organised alphabecally.
Mycophagy has been studied in great detail for some orders
(e.g. rodents), whereas studies of other orders are limited.
Likewise, some mammal species are included in numerous
reports describing their roles as mycophagists and spore
dispersal vectors, whereas other species have seldom or never
been studied to determine whether or not they consume fungi.
It is important to note that the number of cited references does
not necessarily reect the level of fungal consumpon for a given
species. There are undoubtedly many seldom studied species
not on these lists that frequently eat fungi, and some of those
may rely on fungi for a higher percentage of their diet than do
the species for which we cite dozens of references. Some groups
of terrestrial mammals with highly specialised diets, such as ant
or termite feeding specialists (e.g. the families Tachyglossidae,
Myrmecobiidae, Manidae and Myrmecophagidae), likely
never deliberately consume fungi. It is also possible that some
mammals – including species of cats (Felidae) – lack the ability
to produce chinases (Cornelius et al. 1975) that allow them to
digest fungi, and this may lead to their avoidance of fungi as
food. More studies are needed to understand the link between
mammalian biosynthesis of chinases and mycophagy.
In order to disnguish how important fungi are for mammal
consumpon, Claridge & Trappe (2005) proposed four
categories of mammal mycophagists: obligate, preferenal,
casual or accidental. In the context of this review, we aimed to
compile a comprehensive list of all mammal species that have
ever been reported to ulise fungi as food. Unfortunately, the
level of mycophagy of the vast majority of the 508 listed species
has not been suciently studied for us to accurately classify
most species we list within one of these four categories. With
connued research, we hope it will become possible to classify
more mammals within these categories; but in the context of
this review, we use only the taxonomic categories listed below.
Marsupials
Didelphimorphia
The opossums are a relavely small order of marsupials nave
to the Americas. The diets of many members of the group are
poorly studied, but we found reports of fungi in the diets of
three species all within the family Didelphidae (Supplementary
Table S1). Based on our review, we show that approximately
2.4 % of the extant members of this order have been shown to
eat fungi (Fig 2).
© 2022 Westerdijk Fungal Biodiversity Instute
Mammalian mycophagy
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
103
Paucituberculata
The shrew-opossums of South America have been relavely
poorly studied. To date, only the long-nosed shrew-opossum
(Rhyncholestes raphanurus) has been reported to eat fungi
(Meserve et al. 1988). Based on our review, we show that
approximately 14.3 % of the extant members of this order have
been shown to eat fungi (Fig. 2).
Microbiotheria
The Monito del Monte (Dromiciops gliroides) is one of three
species in the order Microbiotheria. It is found in southern
South America and has been reported to eat small amounts of
fungi (Meserve et al. 1988). Based on our review, we show that
at least a third of the extant members of this order have been
shown to eat fungi (Fig. 2).
Dasyuromorphia
These carnivorous marsupials are endemic to Australia, New
Guinea and several neighbouring islands and include animals
such as: antechinus, dunnarts, the kowari, mulgaras, quolls and
the Tasmanian devil. They are primarily carnivores or insecvores,
but we found reports of fungi in the diets of ve species in the
family Dasyuridae (Supplementary Table S2, Fig 3D). Based on our
review, we show that approximately 6.5 % of the extant members
of this order have been shown to eat fungi (Fig. 2).
Peramelemorphia
The bandicoots and bilbies are endemic to Australia, New
Guinea, and several surrounding islands. Although many of the
New Guinean species remain poorly studied, most species in
this order that have been studied have been shown to eat fungi.
Some species that were once thought to have large geographic
distribuons have also been recently shown to be disnct
species. We found reports of fungi in the diets of 13 species in
three families (Supplementary Table S3). Based on our review,
we show that approximately 59 % of the extant members of this
order have been shown to eat fungi (Fig. 2).
Diprotodona
The diprotodont marsupials are the largest and most diverse
group of marsupial mammals and include koala, wombats,
possums, gliders and macropods (the laer includes all
kangaroos, wallabies, potoroos, beongs, rat-kangaroos and
their relaves). They are nave only to Australia, New Guinea and
several surrounding islands. This group has a diversity of dietary
specialisaons, and some members of the order rely heavily on
fungi for large porons of their diet. We found reports of fungi
in the diets of 33 species in eight families (Supplementary Table
S4, Fig. 3C). Based on our review, we show that approximately
22 % of the extant members of this order have been shown to
eat fungi (Fig. 2).
Placental Mammals
Cingulata
Armadillos are a relavely small order of placental mammals and
are nave to the Americas. There has been limited research on
the overall importance of fungi in armadillo diets, but we found
reports of fungi in the diets of three species in two families
(Supplementary Table S5). Based on our review, we show that
approximately 14.3 % of the extant members of this order have
been shown to eat fungi (Fig. 2).
Proboscidea
The elephants comprise only three extant species that are
restricted to Africa and southern Asia. The members of this group
are primarily herbivores, with fungi playing only a very limited
role in their diets. We only found menon of trace amounts
of fungi in the diets of the living African Elephant (Loxodonta
africana) (Paugy et al. 2004) and the exnct American Mastodon
(Mammut americanum) that once occurred in North America
(Newsom & Mihlbachler 2006). Given the size of both animals
and the fungi that were reported, it is hard to denively know if
this represents deliberate mycophagy or incidental consumpon
of spores. But in this instance and unl further studies are
conducted on elephants, we are considering mycophagy to be
any evidence of fungi in the diet. Based on our review, we show
that approximately a third of the extant members of this order
have been shown to eat fungi (Fig. 2).
Primates
Primates are a widely distributed and diverse group of placental
mammals. If humans (Homo sapiens) are included, they can
be found in virtually every habitat on Earth and are one of the
most adaptable and successful species of mammals. Over the
past hundred years, waste management systems used by many
modern humans have changed our role as spore dispersers,
but undoubtedly hardly more than 100 years ago, almost all
humans that ingested fungi were playing a role in the dispersal
of fungal spores. Although it has been shown that early humans
and neanderthals (H. neanderthalensis) consumed fungi as
food, their role as spore dispersers has not been as thoroughly
studied as that of some other hominids (see Supplementary
Table S6). Excluding all the plant pathogens and diseases that
humans have accidentally spread, modern humans deliberately
transport and culvate numerous mycorrhizal and saprotrophic
fungi as well as their associated plant species (Stamets 1993,
Coer 2014, Zambonelli et al. 2015, Guerin-Laguee et al.
2020). Modern humans have been documented to harvest more
than 2 100 edible mushroom species both for personal use and
commercial sale (Li et al. 2021), which is more species than has
been documented by any other mammal in this review. In the
process of picking, cleaning, carrying and somemes shipping
sporocarps, spores are inevitably being dispersed. There are
obviously numerous ways - both posive and negave - that
humans contribute to spore dispersal, and given that there
have been hundreds of papers and books published about
ethnomycology, this topic warrants a review of its own and is
beyond the scope of this study. In Supplementary Table S6 we
only cite a selecon of papers that we think are most relevant to
fungi consumpon by humans, but it is important to note that
this is the only mammal species that we have deliberately le
incomplete.
There have been two previous reviews specically relang
to primate mycophagy. We encourage readers who are
parcularly interested in primate mycophagy to also refer to the
earlier reviews by Hanson et al. (2003) and Sawada (2014). For
our study, we found reports of fungi in the diets of 105 primate
species in 13 families (Supplementary Table S6, Fig. 3B). This
is more species than has been previously compiled. Hanson et
al. (2003) reported just over 20 species, and Sawada (2014)
showed nearly 60 species. Despite the diversity of primate
species that consume fungi, they are frequently overlooked in
primate dietary studies or are lumped in with plants, “other” or
unidened; this is the case even in major reviews on primate
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104
Fig. 3. A selecon of mycophagous mammals with fungal fruing bodies. A. Mount Graham red squirrel with a parally dried fungus in its mouth
on Mount Graham in Arizona, USA. B. In northwestern Cambodia, a Germain’s langur holds a mushroom that it is eang. C. A northern beong eats
an unidened true in northern Queensland, Australia. D. A brown Antechinus pauses near the fruing body of a sequestrate species of Descolea
(lower right corner of image) in eastern New South Wales, Australia. Image A © Eirini Pajak. Image B © Brenda de Groot. Image C © Stephanie Todd.
Image D © Stephen Mahony.
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Mammalian mycophagy
Editor-in-Chief
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E-mail:p.crous@westerdijkinstitute.nl
105
nutrion and diets (e.g. Lambert & Rothman 2015). Unlike the
majority of references, we cite that have reported mycophagy
in other orders of mammals, almost all papers cited in this
secon are based on observaonal studies. There is much
merit in observaonal methods to improve understanding of
the biology and behaviour of mammals; but as has been shown
with ornithological studies (Ellio et al. 2019a), using these
methods in isolaon makes it exceedingly easy to overlook,
misidenfy or underesmate the importance of the fungal
components of diets. We suspect that if primate researchers
employed the typical scat analysis methods commonly used in
groups that are harder to observe, a far greater diversity of
primates would be shown to ulise fungi for food and likely at
a higher rate than is currently esmated among some species.
Based on our review, we show that approximately 20.2 % of
the extant members of this order have been shown to eat fungi
(Fig. 2).
Lagomorpha
The hares, rabbits and pikas are a relavely small group of
widely distributed placental mammals. They primarily eat plant
material, but we found reports of fungi in the diets of 12 species
in three families (Supplementary Table S7). Based on our review,
we show that approximately 11.1 % of the extant members of
this order have been shown to eat fungi (Fig. 2).
Rodena
The rodents are a highly diverse and widespread order of
placental mammals with nave members found in most regions
except the coldest porons of the Arcc and Antarcc and
some islands (e.g. New Zealand). The members of this order are
arguably some of the most important dispersers of fungal spores,
and for some species, fungi represent large porons of their
diet. We found reports of fungi in the diets of 221 species in 14
families (Supplementary Table S8, Fig. 3A). Based on our review,
we show that approximately 8.5 % of the extant members of this
order have been shown to eat fungi (Fig. 2).
Eulipotyphla
The Eulipotyphla are a diverse order of widely distributed
placental mammals that includes hedgehogs, moonrats, shrews,
moles and solenodons. They are oen considered to be primarily
insecvorous, but we found reports of fungi in the diets of 21
species in three families (Supplementary Table S9). Based on
our review, we show that approximately 3.9 % of the extant
members of this order have been shown to eat fungi (Fig. 2).
Carnivora
The carnivores are widely distributed, and while many members
of this order are primarily carnivorous, a wide diversity of
species augment their diet with many other food types. We
found reports of fungi in the diets of 27 species in nine families
(Supplementary Table S10). Based on our review, we show that
approximately 10.1 % of the extant members of this order have
been shown to eat fungi (Fig. 2).
Perissodactyla
The odd-toed ungulates of the order Perissodactyla are a
relavely small order of placental mammals that are mostly
grazers; the order includes horses, asses, zebras, rhinos and
tapirs. Though they show lile reliance on fungi, we found
reports of fungi in the diets of the horse (Equus caballus)
(Hasngs & Moram 1915, Cleland 1934) and the mountain
tapir (Tapirus pinchaque) (Downer 1996, 2003). Other than
these two species, we found no indicaon of fungi consumpon
by this order. Based on our review, we show that approximately
11.1 % of the extant members of this order have been shown to
eat fungi (Fig. 2).
Arodactyla
The even-toed ungulates are a diverse and widespread group
of placental mammals (e.g. cale, sheep, deer, pigs, giraes,
camels and llamas). Most species in this group are relavely
large-bodied, so fungi oen do not comprise a bulk of their diet;
however, fungi do appear to be nutrionally important to them.
We found reports of fungi in the diets of 59 species in seven
families (Supplementary Table S11). Based on our review, we
show that approximately 23 % of the extant members of this
order have been shown to eat fungi (Fig. 2).
DISCUSSION
Feeding on fungi
Feeding preferences between fungal taxa, morphologies and
porons of sporocarps
Several factors likely contribute to fungal food choices and
species selecon. It is possible that toxicity may be a factor in
species selecon, but there is very limited data on fungal toxins
in relaon to wild mammals. Sawada et al. (2014) studied fungal
species preference in relaon to their toxicity among Japanese
macaques (Macaca fuscata) and found that this species of
primate eats a diversity of fungi. They suggested that individuals
use dierent methods to avoid poisonous mushrooms, including
previous knowledge and on-site assessment of taste (but not
smell). The macaques generally ate fungi without examining
them; but when they were hesitant and tasted the sporocarps
before eang, Sawada et al. (2014) determined the fungus was
more likely to be a toxic species. Since almost all knowledge
of fungal toxicity is in relaon to humans and a few species of
mammalian pets, it is dicult to determine the toxicity of fungi
for specic mammal species. For the most part, what – if any –
role fungal toxins play in food selecon is sll unknown.
Mammals are likely to prefer nutrionally rich fungal taxa
that produce easily detectable aromas or colours. In response
to these selecon pressures, some fungi may produce chemicals
and/or compounds to make certain parts of their sporocarps
desirable. Even though mycophagy may have contributed to the
success of certain fungal groups and sporocarp morphologies,
there has been limited research that directly invesgates
the selecon pressure from mammal food choices on fungal
reproducve paerns and morphologies. Herbivores oen
selecvely feed on certain species or parts of plants, somemes
preferenally selecng the tender new growth (Wilsey 1996,
Pérez-Harguindeguy et al. 2003), and we suspect that preferenal
feeding strategies likely occur in fungi as well. There is evidence
of dierent nutrional value within the sporocarps of some
fungi. The chemical composion and nutrional value of desert
trues in the genera Terfezia and Tirmania vary between taxa
and the dierent layers of sporocarps, depending upon whether
or not the peridium (outer skin) of these trues was removed
or le on the exterior (Hussain & Al-Ruqaie 1999). Grönwall &
Pehrson (1984) also found variaon in nutrional value between
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E-mail:p.crous@westerdijkinstitute.nl
106
the peridium and spores of the sequestrate ECM species
Elaphomyces granulatus, while Vogt et al. (1981) detected
dierences in nutrient concentraons between mycorrhizal and
decomposer fungal species.
Among the numerous members of the family Russulaceae
that are important foods for mammals, some species/genera
produce latex (including the genera Arcangeliella, Lactarius,
Lacuus, Mulfurca and Zelleromyces), while members of the
closely related genus Russula do not. The latex is produced in
laciferous hyphae, and in some species these hyphae also serve
to store precursors of pungent dialdehydes (Camazine & Lupo
1984). The chemistry of the latex varies between species, and this
may impact animal consumpon. For example, the latex produced
by Lactarius volemus contains polyisoprene, which is also found
in rubber (Ohya et al. 1998) and appears to deter invertebrates
from feeding. Therefore, invertebrates are less likely to feed
on the latex-producing genus Lactarius than the closely related
Russula species that do not produce latex (Taskirawa & Tuno
2016). Latex is most abundant in young sporocarps and deterred
slugs in experimental feeding studies; once the sporocarp aged,
latex producon slowed or stopped and slugs ate Lactarius and
Russula species at similar rates (Taskirawa & Tuno 2016). There
may also be a nite number of latex-producing hyphae within
each sporocarp, and as the sporocarp expands, it becomes more
dispersed/diluted for the feeding animal. It is therefore possible
that latex protects young sporocarps from being consumed by
animals before spore maturaon, at which point latex producon
is reduced and the sporocarps of lactang members of the family
Russulaceae become more desirable to invertebrates. Latex
producon in fungi is restricted to a relavely small number of
genera, so its impact on food preferences has limited relevance
across the enre fungal kingdom. Nevertheless, we suspect a
similar negave correlaon between small mammal mycophagy
and latex producon.
Among many groups of animals, evidence suggests that the
hymenium (spore-bearing surface) is preferenally selected for
food instead of other porons of the sporocarp. Vogilino (1895)
and Buller (1909) rst suggested that gastropods preferenally
eat gills/reproducve surfaces before other structures, an
observaon that we also made in slugs and other invertebrates
(Fig. 4). Due to their large nature and faster movements (at
least compared to slugs), mammals’ feeding preferences are
more dicult to observe. However, a few studies suggest that
mammals also show a preference toward dierent porons of
fungal sporocarps. For example, brown lemurs (Eulemur spp.)
seem to preferenally eat the cap while discarding other parts
of mushrooms (Overdor 1993), and Humboldt’s ying squirrels
(Glaucomys oregonensis) preferenally feed on the reproducve
ssues of epigeous fungi (Thysell et al. 1997). The volcano
deermouse (Neotomodon alstoni) and the North American
deermouse (Peromyscus maniculatus) are both known to eat
enre fungal sporocarps but have a preference for the hymenium
(Casllo-Guevara et al. 2012). Walton (1903) noted that North
American red squirrels (Tamiasciurus hudsonicus) regularly ate
the gills of mushrooms and rejected the rest of the sporocarp.
Using camera trapping, Ellio & Vernes (2021a) showed that
several species of Australian vertebrates (both mammals and
birds) fed on Amanita mushrooms, with a preference for the caps
of sporocarps. We observed that many small mammals (especially
rodents) preferenally eat the hymenium before other porons
of the fungal sporocarp (Fig. 5A–F), but larger mammals (e.g.
deer) oen ingest any parts they can nd (Fig. 5G–H).
As outlined in the Introducon, sequestrate fungi have
sporocarps with reproducve ssues enclosed within one or
more layers of skin. In many cases, they are also hypogeous (i.e.
sporulang below ground). It is not known when and where the
rst sequestrate fungi appeared, but esmates suggest that the
rst Australian sequestrate taxa emerged 34–13 million years
ago during the Oligocene and Miocene, while many Australian
mycophagous mammals appeared around 16 million years ago
(Sheedy et al. 2015). In sequestrate basidiomycete species, the
energy used for producing sporocarps with a stalk and cap can
be relocated toward producing more sporocarps and/or spores;
for cup fungi relaves (Ascomycota), the increased layering and
folding of the hymenium increases the volume of spore-bearing
ssue. Among these morphologies, spore dispersal relies
heavily on animal consumpon instead of air currents or water.
Therefore, sequestrate sporulang morphologies likely evolved
in paral response to feeding preferences toward dierent parts
of the sporocarp. There are inevitably mulple factors that have
contributed to the rise of sequestrate sporulang habits, e.g. as a
response to major climac changes such as aridicaon (Sheedy
et al. 2016). Some groups, such as the Mesophelliaceae, predate
the rise of mycophagy specialist mammals and may therefore
have inially formed associaons with early invertebrates or
more generalist feeders (Sheedy et al. 2016).
Among sequestrate species with eshy (non-powdery)
sporocarps, the enre sporocarp is generally consumed;
but in groups such as the genus Elaphomyces and the family
Mesophelliaceae, powdery spores appear to be the least
desirable poron (Figs 6, 7). Many small animals favour the
exterior of Elaphomyces sporocarps by selecvely eang the
peridium (Fig. 6). Research on North American red squirrels by
Vernes et al. (2014) showed that when Elaphomyces trues
are unearthed, the squirrel cleans the outer peridium by
“shucking” adherent soil and mycelium from the true before
it is eaten or cached (see Supplementary Video S1). Members
of the family Mesophelliaceae dier in having a thin and non-
nutrious outer layer surrounding a nutrious central core,
with spores packed in between the two (Fig. 7). Animals
typically peel the outer layer and focus on eang the central
core; this is especially the case aer re when Mesophelliaceae
trues can become more fragrant and are oen more easily
discovered by foraging mammals (Trappe et al. 1996, Maser et
al. 2008). Vernes (2000) noted that the discarded outer peridia
and spore-bearing mass of Mesophellia clelandi liered the
ground around beong digs on burnt ground, but this was never
recorded on unburnt ground. Spores of both Elaphomyces and
Mesophelliaceae are common in faecal pellets of a broad range
of mammals, and both groups are partly reliant on animals for
their dispersal. Even though the spore-producing porons of
sporocarps are not necessarily targeted, mammals inevitably
ingest spores in the process and spill spores onto their fur. The
leovers of sporocarps are oen le exposed on the ground or
a log (Figs 6, 7), from where they can be carried away by wind
or water.
Caching and hoarding of fungi
A diversity of mammal species cache and hoard foods to varying
degrees (Vander Wall 1990). These behaviours have been
arguably best studied among rodents, parcularly in squirrels
that bury nuts and/or cache cones. Fungal caching behaviours
have been most frequently noted among North American red
squirrels, but similar behaviours occur in rodents from other
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Mammalian mycophagy
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
107
Fig. 4. Invertebrates display dietary preferences toward the reproducve porons of fungal fruing bodies. A. Arion subfuscus feeds on the hymenium
of several eyelash cups (Scutellinia scutellata) in Rusk County, Wisconsin, USA. Note the light-coloured secons of the ferle surface where the slug
has eaten the reproducve ssues but not the rest of the fruing body. B. An Arion sp. eats the gills on a Russula sp. in the Tucker County, West
Virginia, USA. C. The gills of three Hygrophorus hypothejus fruing bodies have succumbed to the feeding acvies of a gastropod in Rutherford
County, North Carolina, USA. The upper surfaces of the caps of these three fruing bodies had been le untouched. D. Springtails hollowed out
and ate the enrety of the spore-containing surfaces of the sequestrate fungus Leraomyces erythrocephalus near Wellington, New Zealand. Note
the visible brown line down the middle of the springtails that shows evidence of their digesve tracts lled with spores. E. The hollowed out skin
of a sequestrate Descolea sp. that has had spores eaten by a lilac-coloured Brachystomella sp. in Barrington Tops Naonal Park, New South Wales,
Australia. Images © Todd F. Ellio.
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Elliott et al.
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
108
Fig. 5. Examples showing how mammalian mycophagists oen selecvely feed on the reproducve ssues of fruing bodies. A. The upper surface of
a Lactarius corrugis fruing body from Buncombe County, North Carolina, USA. Note there is a lile evidence of feeding on the margin of the cap. B.
The same fruing body as previous image but almost all of the gills have been removed by a feeding rodent. C. The remnants of a Boletellus russellii
fruing body le on a sck by a feeding rodent (likely a squirrel) Broward County, Florida, USA. The stem was virtually untouched, but all of the
reproducve ssues and part of the cap were removed before the fruing body was discarded. D. A Russula fruing body with all of the gills removed
by a feeding rodent in Randolph County, West Virginia, USA. Only part of the stem and a very thin secon of the upper poron of the fruing body
remained. E. An unidened bolete fruing body ravaged by a feeding rodent in Tucker County, West Virginia. Most of the sterile poron of the cap
remained, and the stem and other sterile porons were le in a chewed pile (visible in the right corner of the image). The rodent appeared to have
ingested every bit of the pore surface. F. Stems and part of the cap surface of one fruing body is all that remains of these two Amanita jacksonii
fruing bodies in Rutherford County, North Carolina. G. Immature Calvaa craniiformis fruing bodies eaten before spore maturity by white-tailed
deer in York County, Pennsylvania, USA. H. Enre Ischnoderma resinosum fruing bodies eaten up to the maximum browse height of a white-tailed
deer in Rusk County, Wisconsin, USA. Images © Todd F. Ellio.
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Mammalian mycophagy
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
109
Fig. 6. The widely distributed sequestrate genus Elaphomyces is an important food source for mammals wherever it has been studied. A. The eastern
North American endemic E. macrosporus and many other members of this genus have thick outer peridial layers that are sought out by mammals.
B. Elaphomyces favosus, a tropical African species eaten by mammals that also illustrates the thick outer layers. C. An unidened Elaphomyces sp.
from Rutherford Coungy, North Carolina, USA that has been parally excavated by the foraging acvies of a small mammal. Note the dark spot
where several small bites have been taken. D. A single Elaphomyces fruing body from Transylvania County, North Carolina that was excavated and
parally eaten by a small rodent. Note the teeth marks on much of the peridium. E. While true hunng in Rutherford County, North Carolina, the
rst author encountered an area lled with extensive animal digs; a nearby log had this pile of powdery black Elaphomyces spores placed on top.
True raking near the digs uncovered this fruing body of E. americanum, and microscopic examinaon revealed that the black spores le piled
on the log matched those of the collected fruing body. A chipmunk or squirrel was likely responsible for this tailings pile. Images © Todd F. Ellio.
© 2022 Westerdijk Fungal Biodiversity Instute
Elliott et al.
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
110
Fig. 7. Examples of members of the re-adapted mycorrhizal family Mesophelliaceae. Widespread in Eucalyptus forests across Australia and an
important food source for a diversity of mammals. A. Mesophellia (Reidsdale, New South Wales, Australia) fruing bodies are oen located deeper
in the soil than other groups of sequestrate fungi and oen grow in nearly conuent clusters. Note that the exterior of the fruing body incorporates
soil and mycorrhizal roots. The next layer is lled with powdery, greenish grey spores, and the central white core is the desired food of foraging
mammals. B. Andebbia pachythrix (Braidwood, New South Wales), shares similar fruing morphology and requires mammals to peel the exterior
before they can eat the core. C. Three exposed fruing bodies of a member of the Mesophelliaceae that were burned in a re (Victoria, Australia).
These fruing bodies were close to the surface and exposed to excessive heat, which likely caused them to be overlooked by mammals foraging post
re. Fruing bodies that are located deeper in the soil and are exposed to re oen produce a highly pungent aroma reminiscent of rong onions.
D. In the aermath of the intense 2019/2020 Bee’s Nest Fire near Dundurrabin, New South Wales, the rst author was exnguishing a burning log
and found the skins and spores of these three Mesophellia fruing bodies in the tailings pile of a small mammal excavaon approximately 20 m away
from what was sll burning. The mammal responsible for the tailings pile had successfully extracted the core and le behind the skin and spores. Due
to the recent re, there was lile other food within several kilometers of this site, which highlights the importance of this family of fungi as post-re
food for Australian mammals. Images © Todd F. Ellio.
© 2022 Westerdijk Fungal Biodiversity Instute
Mammalian mycophagy
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
111
regions of the world that experience cold winters or other
environmental/climac factors that can lead to seasonal food
shortages. Though their fungal caching behaviours have been far
less thoroughly studied than nut/seed dispersal, rodents likely
perform ecosystem funcons that are of similar importance.
Early naturalists frequently wrote with amusement about the
labours and physical feats of small squirrels as they built their
fungal caches and struggled to haul large fungal sporocarps into
the canopy to dry them for winter. Merriam (1884: 214) noted
the following about a North American red squirrel:
“From his liking for mushrooms some would consider him
an epicure, but in whatever light we regard this taste, it is a
droll spectacle to see him drag a large ‘toadstool’ to one of
his storehouses. If the ‘umbrella’ happens to catch on some
sck or log and is broken from the stem, as is frequently
the case, he is prey sure to scold and spuer for a while,
and then take the pieces separately to their desnaon”.
Most squirrels that have been studied were observed to dry
fungal sporocarps on branches and later hide these in caches
(Fig. 8). In some areas, squirrels dry so many mushrooms in tree
branches that it has been described to look like a decorated
Christmas tree (Odell 1925, Murie 1927). Some authors have
reported only the drying behaviour, but given that squirrels
are typically secreve about their caches, it is easy to overlook
where they may have stored the dried mushrooms. It is also
possible that in some regions or among some squirrel species,
mushrooms are le in their original drying sites; however, further
studies are needed to conrm this. Buller (1917, 1922) reported
that North American red squirrels store dried sporocarps in
hollow trees, crow nests, woodpecker nests and even boxes in
old houses. Laursen et al. (2003) noted that in Alaska, northern
ying squirrels and North American red squirrels hollowed out
witches’ brooms that were produced by spruce broom rust
or yellow witches’ broom rust (Chrysomyxa arcotostaphyli);
the squirrels then used these cavies to raise their young and
cache dried mycorrhizal fungi (both epigeous and hypogeous
species). Jung et al. (2010) noted that North American red
squirrels also used witches’ brooms as nests, lining them with
American bison (Bison bison) hair and storing dried fungi for the
winter. Vernes & Poirier (2007) noted that a North American red
squirrel lled a robin nest with more than 50 dried sporocarps
from the hypogeous genus Elaphomyces (Fig. 8C). Caches made
by North American red squirrels can oen be quite large. Buller
(1922) examined a box found in an abandoned house that was
used as a North American red squirrel cache, and he reported
it to weigh nearly 0.5 kg and contain 116 fungal sporocarps;
another cache contained up to 300 sporocarps. Hardy (1949)
studied a large North American red squirrel cache in a hollow
tree containing 59 fungal specimens. He was able to idenfy at
least 13 fungal species, most of which were ECM taxa; the most
numerous species (30 specimens) was the sequestrate fungus
Hymenogaster tener.
Kato (1985) noted that the Japanese squirrel (Sciurus lis)
cached walnuts and pinecones in trees and underground,
while fungi were only cached in trees. He also reported that
underground food was eaten mainly in the spring. Foods
stored below ground are naturally harder for thieves to nd,
but squirrels struggle to access them under deep snow. It is
therefore usually important for squirrels to also cache food in
elevated locaons; however, Lampio (1967) reported that in
Finland, Eurasian red squirrels (Sciurus vulgaris) dug cached
fungi from under the snow. The amount of fungi and other
foods cached likely correlates with climate and food availability
in winter and inevitably varies between regions, habitats and
species. Buller (1922) suggested that Great Britain’s winters
might be too wet for rodents to store fungi, and this may explain
the higher frequency of reports on caching behaviours from the
colder and drier parts of North America and Eurasia. In Scotland,
for example, the Eurasian red squirrel was esmated to cache
a minimum of 42 sporocarps across its home range (Lurz &
South 1998); this is a much lower number than what has been
generally reported among squirrel species in northern North
America (Buller 1917, 1922, Dice 1921, Murie 1927, Ha 1929,
Hardy 1949, Smith 1965, 1968a). On the other hand, caches of
Eurasian red squirrels in northern Finland have been esmated
to contain approximately 440 stored fungi per hectare and
possibly as many as 1 800 sporocarps per individual (Sulkava &
Nyholm 1987). These studies show that caching rates vary both
within the same species of squirrel from dierent latudes and
between squirrel species across the Northern Hemisphere, and
may correlate with the length of winter, snow cover and other
climac condions.
Fungi typically require air drying and subsequent storage
in very dry caches (Fig. 8), while other foods preserve beer
in varying weather condions. Despite the wide array of
foods eaten by the North American red squirrel, their fungal
caches typically do not contain other food items (Hardy 1949).
Quality of drying and storage locaons for fungi appear to be
important to squirrels. Experimental studies suggest that most
mushrooms stored in caches for a long period of me tend to
lose nutrional value, parcularly with exposure to freezing and
thawing cycles (Frank 2009). This nutrional degradaon may
explain why squirrels are typically very diligent in making sure
that stored fungi are dry, saving the driest and best insulated
storage sites for fungi and/or to build their nests. Dice (1921)
described a North American red squirrel nest on a shelf in an
old Alaskan cabin where, by October, the squirrel had collected
a large number of fungi. He reported that every open can was
packed with dried mushrooms, while sporocarps that were not
fully dry were spread out on the shelves. Hendricks & Hendricks
(2015) observed that North American red squirrels in Montana
preferred to dry/cache mushrooms on dead branches, possibly
because they have beer airow.
Learning to dry a mushroom and cache it in an appropriate
locaon for long-term storage is a relavely complex skill that
squirrels progressively acquire with pracce. Smith (1968a)
observed that young North American red squirrels began to
aempt this acvity as early as three days out of the nest. He
reported that in the rst 10 days out of the nest, three young
squirrels dropped 12 of the 32 fungi they aempted to hang on
branches. They only dropped 10 out of 70 by their third week,
while their mother only dropped three out of the 165 fungi that
she hung to dry.
The full diversity of mammals that cache fungi is poorly
known. As discussed earlier, most studies have focused on
North American red squirrels, the Eurasian red squirrel and the
Japanese squirrel, while there are few reports of other rodents
caching fungi. Two studies reported the Siberian chipmunk
(Tamias sibiricus) and the Uinta chipmunk (T. umbrinus) to cache
fungi (Ognev 1966, Bergstrom 1986), but we were unable to nd
any addional informaon about other chipmunk species caching
fungi. Most researchers who have studied the nests and behaviour
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Elliott et al.
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
112
Fig. 8. Examples of fungi hung or cached by rodents. A. An enre bolete fruing body carefully hung by a North American red squirrel in Tucker
County, West Virginia, USA. B. A species of Amanita hung to dry by an unidened squirrel (likely a Douglas’s squirrel based on the species frequently
observed in that area) in Chelan County, Washington, USA. C. A North American red squirrel in New Brunswick, Canada cached more than 50
Elaphomyces fruing bodies inside of this abandoned robin nest (see: Vernes and Poirier 2007). D. A large Allegheny woodrat cache of dried fungi
(likely mostly members of the Russulaceae) found inside of a cave in Adams County, Ohio, USA. Images A & B © Todd F. Ellio. Image C © Karl Vernes.
Image D © Laura S. Hughes.
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Mammalian mycophagy
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
113
of various North American woodrats (Neotoma spp.) have
reported that they frequently cache and collect fungi along with
other seemingly random non-food objects (see papers reporng
mycophagy for this genus in Supplementary Table S8 and Fig.
8D). Neotoma species, somemes called pack rats, are notorious
hoarders. They certainly use the stored fungi for food, but it is
dicult to determine how reliant they are on the food value of
cached fungi or whether this behaviour is simply an extension of
their predisposion for hoarding random objects. Further study
of fungal caching behaviours among various Neotoma species
is needed to fully understand these interacons. Kangaroo rats
frequently cache food, but we only found one study reporng
fungi caching behaviours, and this was in the banner-tailed
kangaroo rat (Dipodomys spectabilis) (Vorhies & Taylor 1922).
Species of the shrew family, Soricidae, have very fast
metabolisms that require them to cache food (Moore 1943,
Maser & Hooven 1974, Marn 1981, Robinson & Brodie 1982,
Carraway 1985, Merri 1986, Vander Wall 1990, Schwartz
& Schwartz 2001, Rychlik & Jancewicz 2002, Urban 2016).
Although this aspect of shrew biology remains relavely
incompletely studied, many species are reported to eat fungi
(Supplementary Table S9). Though we could not nd any
reports of caching fungi by shrews, further research may reveal
such behaviour in some species. Some species of pocket mice
(Heteromyidae), voles (Cricedae), lemmings (Cricedae) and
gophers (Geomyidae) cache food (Vander Wall 1990, Schwartz
& Schwartz 2001, Connior 2011), and members of these groups
have been reported to eat fungi (Supplementary Table S8).
However, we have so far been unsuccessful in locang explicit
reports of these groups caching fungi, likely due to insucient
research having been undertaken on this topic.
Reports of fungal caching behaviours have focused on cold
regions of the Northern Hemisphere. In regions where fungal
caching does not occur, it is possible that fungi sporulate for
a larger poron of the season, the climate is not conducive
to fungal storage, or animals are adapted to seasonal fungal
consumpon and periodically rely on other food sources.
It seems probable that mycophagous mammals in the
Southern Hemisphere also cache fungi, though we could not
nd any evidence of such events even in the large volume
of mycophagy literature published in Australia; we could
also nd no evidence in the literature for South America or
Southern Africa. In Australia, some mycophagous mammals
including brush-tailed beongs (Beongia penicillata), musky
rat-kangaroos (Hypsiprymnodon moschatus) and giant white-
tailed rats (Uromys caudimaculatus) have been reported
to cache seeds (Forget & Vander Wall 2001, Theimer 2001,
Theimer 2003, Murphy et al. 2005). Musky rat-kangaroos
and giant white-tailed rats primarily reside in wet tropical
habitats in northeastern Queensland, Australia. This type of
wet tropical habitat is not conducive to storing fungi since they
would quickly rot in humid warm condions. Since brush-tailed
beongs reside in areas that would be beer suited to storing
fungi (compared to the tropics of northern Queensland),
it is possible that they may be caching fungi on occasion or
some fungi may be available throughout the season, but to
our knowledge this has not been specically studied. Further
research may uncover that this behaviour is more widespread
both geographically and among more mammal species.
For animals that store fungi, these caches provide an
important food for seasons when the resource is less readily
available. In addion to the species that make stores, other
mammals and birds may depend on raiding the caches. For
example, Andreev (1978) noted that Siberian jays (Perisoreus
infaustus) survived Eurasian winters in part by feeding heavily on
fungi stolen from rodent caches. Carey (1991) noted that during
the night, Humboldt’s ying squirrels raid caches of fungi made
by diurnal squirrels. Stealing food from squirrel caches comes at
a risk to the thief, since some squirrels can be violent (Seagears
1949–1950) and are usually highly defensive of their stores.
Occasionally they have been reported to ght to the death over
cache ownership (Smith 1968a). The diversity of mammals that
cache fungi or raid these caches is sll poorly understood, and
more studies are needed to understand their importance as
winter food.
The ecological implicaons of mammal caching behaviours
for fungal dispersal are not fully understood. By placing fungi to
dry several metres o the ground, rodents help with the release
of fungal spores higher into air currents. Connor (1960) noted
that North American red squirrels bury “small pualls” in pits;
he unfortunately did not idenfy the fungal species involved, but
it is likely some type of hypogeous fungi. It is therefore possible
that squirrels may dig hypogeous fungi in one locaon and bury
them somewhere else. Regardless of whether squirrels really
store fungi below ground or simply forget them, this behaviour
has potenally important implicaons for fungal dispersal.
Nutrional advantage of fungi consumpon
Since fungal cell walls are primarily composed of chin (Cork &
Kenagy 1989a, Balestrini et al. 2000) that is dicult for humans
to digest when raw, there is a widespread myth that fungi are
nutrionally insignicant; however, cooking fungi makes them
highly digesble and nutrionally benecial to humans (Wani
et al. 2010). While cooking fungi is irrelevant in the context of
wildlife nutrion, many mammals are capable of biosynthesizing
chinases and digesng raw fungal ssues to access nutrients
(Cornelius et al. 1975, Boot et al. 2001, Wallis et al. 2012,
Polatyńska 2014). The Abert’s squirrel (Sciurus aber) carries
mushrooms to its nest as one of the rst non-milk foods its young
eat (Keith 1956), suggesng that fungi are highly digesble for
this species. Fungi also do not require the processing oen
carried out on other foods (e.g. husking nuts, peeling fruit,
extracng seeds). Young mammals such as the juvenile Tana
River mangabey (Cercocebus galeritus) take advantage of this
simple source of nutrion before they learn to process more
energy intensive foods (Kivai 2018). Some arboreal mammals
even risk predaon by descending from the canopy to feed
on highly desirable fungi. Germain’s langurs (Trachypithecus
germaini) have been found to come to the ground to pick fungal
sporocarps and then immediately retreat into the trees to
consume them (de Groot & Nekaris 2016; Fig 3D). Among other
primates such as the grivet monkey (Chlorocebus aethiops),
higher ranking members of troops tend to eat higher porons
of fungi while lower ranking members eat more fruit (Isbell
et al. 1999). The use of troop status to acquire fungi indicates
that they are highly desirable; this is likely due to nutrional
advantages, avour or aroma. Japanese macaques (Macaca
fuscata), which are known to eat at least 67 fungal species, can
be so enthusiasc about fungi that ghts frequently break out
over possession and consumpon of sporocarps (Sawada et al.
2014). Eastern gorillas (Gorilla beringei) apparently have similar
disagreements within the troop over ownership of a highly
valued species of Ganoderma fungus, as noted by Fossey (1983:
76) in the following:
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Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
114
“Sll another special food is bracket fungus (Ganoderma
applanatum), a parasical tree growth resembling a large
solidied mushroom. The shelike projecon is dicult to
break free from a tree, so younger animals oen have to
wrap their arms and legs awkwardly around a trunk and
content themselves by only gnawing at the delicacy. Older
animals who succeed in breaking the fungus loose have
been observed carrying it several hundred feet from its
source, all the while guarding it possessively from more
dominant individuals’ aempts to take it away. Both the
scarcity of the fungus and the gorillas’ liking of it cause
many intragroup squabbles, a number of which are seled
by the silverback, who simply takes the item of contenon
for himself”.
Fungal biochemistry is complex and varies between taxonomic
groups (Mendel 1898, Kinnear et al. 1979, Vogt et al. 1981,
Blair et al. 1984, Grönwall & Pehrson 1984, Jabaji-Hare 1988,
Hussain & Al-Ruqaie 1999, Claridge & Trappe 2005, Barros
et al. 2007, 2008, Kalač 2009, Ouzouni et al. 2009, Wani et
al. 2010, Wallis et al. 2012, Zambonelli et al. 2017, Lucchesi
et al. 2021). The nutrional value for mammals also varies
between fungal species and between dierent parts of the
sporocarp. The nutrional role that fungi play in mammals’
diets therefore varies between individuals, species, seasons,
and the availability of other foods. Grönwall & Pehrson (1984)
esmate that Eurasian red squirrels can reach up to half of
their daily energec requirements by eang fungi. As previous
studies and reviews on mycophagy have typically shown, fungi
are a signicant source of nutrion and biomass for small
mammals (Fogel & Trappe 1978, Claridge & May 1994, Claridge
et al. 1996, Johnson 1996, Luoma et al. 2003, Polatyńska 2014,
Nuske et al. 2017a, b, Zambonelli et al. 2017). Fungi are also
important for some larger mammal species, including deer in
the family Cervidae that rely heavily on fungi as a large poron
of their diet (Strode 1954, Lovaas 1958, Kirkpatrick et al.
1969, Hungerford 1970, Launchbaugh & Urness 1992, also see
Supplementary Table S11). The white-tailed deer (Odocoileus
virginianus) has been reported to eat as many as 580 fungal
species (Cadoe 2018). Ungulates generally eat larger fungal
species, and since these taxa tend to sporulate most prolically
in the autumn and early winter, they are oen more seasonally
important. In cold regions of Eastern and Northern Europe,
various ungulate species have been reported to excavate frozen
mushrooms from under the snow (Blank 2003, Inga 2007).
Water constutes up to 80–95 % of the biomass of fungal
sporocarps (Claridge & Trappe 2005, Barros et al. 2007) and
represents an important source of hydraon for small mammals.
In some cases, fungal sporocarps can be the major or only source
of water for small mammals (Getz 1968). Using fungi as a water
source therefore increase the adaptability of some mammals
to marginal habitats where available surface water is scarce.
This may explain the high diversity of mycophagous mammals
in Australian dry woodlands and other similar environments
around the world.
Fungal sporocarps generally contain more proteins and
nutrients than plant material (Wallis et al. 2012) and can be an
important source of essenal amino acids (Blair et al. 1984). In
larger mammals, fungi are not necessarily an important source
of dietary biomass but can provide key nutrients that are oen
scarce or inaccessible in other food sources. Selenium, for
example, is an important microelement in mammal diets that
is found in relavely high levels in some fungi (Watkinson 1964,
Quinche 1983a, b, Claridge & Trappe 2005, Falandysz 2008,
Costa-Silva et al. 2011, Kabuyi et al. 2017). Selenium deciency
can lead to nutrional muscular dystrophy (white muscle
disease), and many livestock feeding mixes include selenium
supplements (Gupta & Gupta 2000, Claridge & Trappe 2005,
Falandysz 2008). Fungi are likely one of the primary sources of
selenium for wild mammals, thus making fungi an important
food even if only small quanes are ingested.
In addion to selenium, fungi contain a wide array of essenal
amino acids, fats, fay acids, carbohydrates, minerals, nutrients
and proteins (Claridge & Trappe 2005). Some groups of fungi,
including members of the families Glomeraceae, Gigasporaceae
and Mesophelliaceae, also have high lipid and fay acid content
(Kinnear et al. 1979, Jabaji-Hare 1988). Many aspects of the
chemical composion of various fungal species can boost animal
health even in very small quanes. Studies on livestock and
poultry feeds have experimentally shown the high value of fungi
as a dietary supplement even in low dosages. When fungi were
given to broiler chickens, for example, the chickens generally
experienced increased weight gain and improved resistance
to pathogens (Bederska-Łojewska et al. 2017). These benets
were detected even when fungi were added at levels of as low
as 2 % in poultry diets. In addion to the use of sporocarps in
the livestock feed industry, research has suggested that using
mycelium as a fermenng agent can also provide anoxidants
and improve the overall quality of livestock feeds (Ukpebor et al.
2007, Abdullah et al. 2016).
Most informaon about the nutrional composion of
fungi is known from species culvated for human or livestock
feed, so there is very lile informaon on the nutrional value
of most wild fungal species. Deciphering the impacts of fungal
consumpon by wild animals is also more complex than in
capve populaons. Studies of wild populaons of the heavily
mycophagous eastern beong (Beongia gaimardi) suggested
that an increase in fungi in the marsupial’s diet correlated
with an improved body condion (Johnson 1994b). Female
eastern beongs are more heavily mycophagous than males,
and the growth rate of pouch young is posively correlated
to the abundance of fungal sporocarps (Johnson 1994b).
However, it remains dicult to measure the direct physiological
impacts of fungal species in the diet of a given individual or
species since there are many co-occurring variables. The idea
of mammals “self-medicangby using fungi and plants with
certain pharmacological properes is sll speculave, but
research into some foods used by animals including fungi
has uncovered compounds with promising pharmacological
properes (Human 1997, 2003, Cousins & Human 2002).
These studies compare some of the medicinal compounds
found in pharmacological studies with food choice in primates;
however, it is more dicult to relate medicinal compounds used
for medical applicaons to the diets of mammals more distantly
related to humans.
Fungi consumpon has a variety of posive impacts for
many mammals, but some fungal species are bioaccumulators
that can absorb environmental toxins when they are growing in
contaminated areas (Ernst 1985, Colpaert & Van Assche 1987,
Gast et al. 1988, Brown & Hall 1989, Gadd 1994, Gonzalez-Chavez
et al. 2004, Pokorny et al. 2004, Fomina et al. 2005, Soylak et al.
2005, Shavit & Shavit 2010, Dulay et al. 2015). Isotope studies in
Europe have shown that fungi absorb radiocesium, which can be
transmied to animals that ingest contaminated sporocarps and
© 2022 Westerdijk Fungal Biodiversity Instute
Mammalian mycophagy
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
115
then move up the food chain to eventually contaminate humans
and other apex predators that have eaten these mycophagous
game animals (Johnson & Nayeld 1970, Hove et al. 1990,
Karlén et al. 1991, Fielitz 1992, Johanson 1994, Strandberg &
Knudsen 1994, Avila et al. 1999, Zibold et al. 2001, Hohmann
& Huckschlag 2005, Steiner & Fielitz 2009, Dvořák et al. 2010,
Škrkal et al. 2015). Environmental contaminants are oen the
by-products of human acvies such as agriculture, mining,
bombing and manufacturing. The movement of these toxins
through food webs from primary to secondary consumers is
undoubtedly more widespread than is currently known, and
further studies are needed to thoroughly understand the role
that fungi play in the bioaccumulaon and magnicaon of
toxins through the food chain.
Evoluonary signicance of mammal mycophagy
The role of mycophagy in fungal spore dispersal
Fungi disperse across ecosystems either vegetavely (through
mycelium growth or asexual propagules) or sexually (via spore
dispersal). Mycelium is the non-reproducve part of a fungus and
is composed of a network of ne root-like laments. In habitats
with similar or compable plant communies, mycorrhizal fungi
commonly colonise seedlings through mycelial spread (Jonsson
et al. 1999). In fragmented, highly disturbed or degraded areas,
mycelial spread tends to be less eecve, and spores are the
primary means of establishment (Trappe & Strand 1969, Bruns
et al. 2009, Okada et al. 2022).
Even though spores theorecally enable fungi to disperse
over greater distances than mycelial spread does, only a
small percentage of spores generally disperse successfully at
signicant distances. Many widespread mycorrhizal fungal
species successfully disperse through air currents (Warner et al.
1987, Allen et al. 1989, Geml et al. 2008), but a high percentage
of spores land very close to their source and very few spores are
able to colonise new areas. Esmates suggest that only about
2 % of spores from wind-dispersed basidiomycete species travel
beyond 5.2 m of the parent sporocarps (Li 2005), while about
5 % of spores travel beyond one metre (Galante et al. 2011).
Among ectomycorrhizal fungi, density and diversity of wind-
dispersed spores decrease with distance from forest edges,
with few spores detected at distances over 1 km from the forest
edge (Peay et al. 2012). Once landed, spores must nd suitable
substrates (for saprophyc species) or hosts (for mycorrhizal
and parasic species) to germinate. For sexual reproducon,
individuals need to meet nearby compable genec strains.
Therefore, spores landing closer to their parent sporocarps
have a greater probability of nding suitable habitat and mang
types (Kytöviita 2000, Peay et al. 2012, Horton 2017); however,
proximity to the parent may also reduce the genec diversity
(thus the adaptability and resilience) of the species in the area.
For example, low genec diversity detected in populaons of
the hypogeous commercial true Tuber melanosporum is likely
due to dicules in long-distance spore dispersal (Taschen et
al. 2016). Such genec bolenecks could be a result of too few
animal dispersers.
Fungal sporocarps are oen ephemeral and delicate, but
their spores are far more resilient. Spores typically survive the
enzymac tribulaons of the mammalian digesve tract and
regularly germinate once deposited in scats (See next secon
and Tables 1, 2). Since mammals can eat enre sporocarps,
mycophagy would account for the dispersal of a greater
percentage of spores from a single sporocarp than would wind
dispersal. Some rodents also co-disperse bacteria that interact
with root-associated fungi and play important roles in nitrogen
xaon (Li et al. 1986, Li & Maser 1986). Since an individual
mammal oen consumes mulple sporocarps, their scats
may contain spores from mulple individuals and species of
fungi that are deposited within close proximity to each other.
Mycophagy is therefore an eecve means of long-distance
dispersal of fungal spores and improving genec diversity within
fungal populaons.
Fungal spore dispersal through mycophagy can greatly impact
the species composion, genec diversity and adaptability of
mycorrhizal fungal communies (Gehring et al. 2002, Nuske 2017,
Dundas et al. 2018, Valenne et al. 2018, Miranda et al. 2019,
Nuske et al. 2019). Mycophagous mammals may have played a role
in the movement and recolonisaon of mycorrhizal fungi under
major climac changes such as glaciaon, with obvious impacts
on the current distribuon of fungal species and associated plants
(Murat et al. 2004, Piaoni et al. 2016). It is dicult to esmate
the long-term biogeographic impact of mycophagy at a global
scale, but several studies have addressed these quesons on
a smaller scale, e.g. in degraded, newly forming or transional
systems. For example, mammals play a vital role in the transport
of mycorrhizal inoculant into newly forming soils at the forefront
of receding glaciers in the alpine zone of the North Cascades
Mountains, USA (Cázares & Trappe 1994). Scats of mycophagous
animals enable ectomycorrhizal tree establishment in nutrient-
poor sandy dune environments in Oregon, USA (Ashkannejhad
2003, Ashkannejhad & Horton 2006). Aer the volcanic erupon
of Mount Saint Helens in Washington, USA, the spore-containing
scats of mammals served as vectors of mycorrhizal spores into
newly formed sterile soils within the blast zone (MacMahon &
Warner 1984, Allen 1987). In newly produced coal mine spoils,
mycorrhizal spores can be dispersed by grasshoppers and rabbits
(Ponder 1980). Small mycophagous mammals such as voles are
key to habitat succession engineered by North American beavers
(Castor canadensis), a species that causes more ecosystem-level
change than any other non-human mammal. When beaver
ponds eventually silt in, they become meadows dominated by
herbaceous communies that typically associate with arbuscular
mycorrhizal fungi, while the surrounding forests are dominated
by ECM plants. Southern red-backed voles (Myodes gapperi)
regularly eat hypogeous ECM fungi on the forested edges
of beaver meadows and inadvertently carry spores into the
meadows in their scats; this behaviour builds up a spore bank
that assists ECM tree species in recolonising areas aected by
beavers (Terwilliger & Pastor 1999). Similar meadow colonisaon
by ECM spores was observed in Oregon as a result of western
pocket gophers (Thomomys mazama) deposing ingested fungal
spores in below ground faecal chambers (Maser et al. 1978b).
In regions where non-nave pines (Pinus spp.) are farmed in
plantaons, a variety of mycophagous animals spread the spores
of pine-associated mycorrhizal fungi outside the bounds of pine
plantaons, potenally contribung to the spread of these trees
(Nuñez et al. 2013, Wood et al. 2015, Policelli et al. 2019, 2022,
Aguirre et al. 2021).
Spore viability
Fungal spores tend to be very robust and remain viable aer passage
through the digesve system of a diverse range of invertebrates
(Tuno 1998, Trappe & Claridge 2005, Kitabayashi & Tuno 2018,
Vašutová et al. 2019, Ori et al. 2021) and birds (Caiafa et al. 2021).
© 2022 Westerdijk Fungal Biodiversity Instute
Elliott et al.
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
116
Table 1. Mammal species experimentally shown to disperse viable mycorrhizal fungal spores.
Genus and species of mammals Common Name Method* Viable Rate* Citaon
Aepyprymnus rufescens Rufous Beong IT Yes ?Reddell et al. (1997)
Beongia penicillata Brush-tailed Beong IT Yes +Lamont et al. (1985)
Beongia tropica Northern Beong IT Yes ?Reddell et al. (1997)
Bison bison American Bison IT Yes ?Lekberg et al. (2011)
Callospermophilus saturatus Cascade Golden-mantled Ground
Squirrel
MYes +Cork & Kenagy (1989a)
Cervus canadensis Wapi/Elk IT Yes ?Allen (1987)
Cervus elaphus Western Red Deer IT Yes ?Wood et al. (2015)
Ctenomys knigh Catamarca Tuco-tuco IT Yes ?Fracchia et al. (2011)
Glaucomys oregonensis Humboldt’s Flying Squirrel M, IT Yes - Colgan & Claridge (2002)
Glaucomys sabrinus Northern Flying squirrel IT Yes +Caldwell et al. (2005)
Hystrix cristata Crested Porcupine MYes ?Ori et al. (2018)
Isoodon fusciventer Dusky-bellied Bandicoot IT Yes +, ? Smith (2018), Tay et al. (2018)
Isoodon macrourus Northern Brown Bandicoot IT Yes ?Reddell et al. (1997)
Lepus europaeus European Hare IT Yes ?Aguirre et al. (2021)
Loxodonta africana African Elephant IT Yes ? Paugy et al. (2004)
Melomys cervinipes Fawn-footed Melomys IT Yes ?Reddell et al. (1997)
Microtus oregoni Creeping Vole GYes ?Trappe & Maser (1976)
Mus musculus House Mouse IT Yes +Ori et al. (2021)
Myodes californicus Western Red-backed Vole M, IT Yes - Colgan & Claridge (2002)
Myodes gapperi Southern Red-backed Vole IT Yes - Terwilliger & Pastor (1999)
Neotomodon alstoni Mexican Volcano Mouse MYes +, = Casllo-Guevara et al. (2011,
2012), Pérez et al. (2012)
Odocoileus hemionus Mule Deer IT Yes ?Ashkannejhad & Horton (2006)
Perameles nasuta Long-nosed Bandicoot IT Yes ?McGee & Baczocha (1994),
Reddell et al. (1997), McGee &
Trappe (2002)
Peromyscus leucopus White-footed Deermouse IT Yes ?Rothwell & Holt (1978), Miller
(1985)
Peromyscus maniculatus North American Deermouse IT, M Yes ?,+,= Rothwell & Holt (1978), Casllo-
Guevara et al. (2011, 2012),
Pérez et al. (2012)
Potorous tridactylus Long-nosed Potoroo IT Yes +Claridge et al. (1992)
Proechimys semispinosus Tome’s Spiny-rat IT Yes ?Mangan & Adler (2002)
Pseudalopex gymnocercus Pampas Fox IT Yes ?Aguirre et al. (2021)
Raus fuscipes Bush Rat IT Yes ?Reddell et al. (1997)
Raus raus Black Rat IT Yes ?McGee & Baczocha (1994),
McGee & Trappe (2002)
Reithrodontomys humulis Eastern Harvest Mouse IT Yes ?Rothwell & Holt (1978)
Rupicapra rupicapra Alpine Chamois IT Yes ?Wiemken & Boller (2006)
Sciurus aber Abert’s Squirrel IT Yes = Koer & Farennos (1984)
Sus scrofa Eurasian Wild Pig M, IT Ye s +,? Nuñez et al. (2013), Piaoni et
al. (2014), Livne-Luzon et al.
(2017), Aguirre et al. (2021)
Sylvilagus oridanus Eastern Coontail IT Yes +Ponder (1980)
Tamias townsendii Townsend’s Chipmunk M, IT Yes +Colgan & Claridge (2002)
Thomomys talpoides Northern Pocket Gopher IT Yes ?Allen & MacMahon (1988)
Trichosurus vulpecula Common Brush-tail Possum IT Yes ?Wood et al. (2015)
Uromys caudimaculatus Giant White-tailed Rat IT Yes ?Reddell et al. (1997)
Two species of deer Cervus elaphus (Western Red Deer) Dama dama (Common
Fallow Deer)
IT Yes ?Nuñez et al. (2013)
© 2022 Westerdijk Fungal Biodiversity Instute
Mammalian mycophagy
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
117
Table 1. (Connued).
Genus and species of mammals Common Name Method* Viable Rate* Citaon
Mixed scats from Raus fuscipes, R. raus, R. villosissimus and Perameles
nasuta were shown to contain viable VAM spores, but it is unclear which
species were actually tested for viability
IT Yes ?McGee & Baczocha (1994)
Ten species of small European mammals were examined in this study but it is
unclear if viability was tested in all mammals
IT Yes ?Schickmann (2012)
A list of at least 40 mammal species that have been experimentally shown to disperse viable fungal spores through their scats. *Method: M:
microscopic assessment, IT: Inoculaon Trials, G: germinaon trial in vitro. *Rate: +: improved viability when consumed by animals compared to
control, =: equal viability from scats to control, -: reduced viability compared to control, ?: no comparave viability data.
Table 2. Species of mycorrhizal fungi whose spores have been experimentally shown to remain viable aer mammal consumpon.
Fungal species Method* Viability Rate* Citaon
Acaulospora morrowiae IT Yes ?Lekberg et al. (2011)
Amphinema sp. IT Yes ?Nuñez et al. (2013)
Archaeospora trappei IT Yes ?Lekberg et al. (2011)
Densospora tubiformis IT Yes ?McGee & Baczocha (1994)
Descolea angusspora IT Ye s ?Tay et al. (2018)
Elaphomyces granulatus MYes +Cork & Kenagy (1989a)
Endogone aggregata IT Yes ?McGee & Baczocha (1994)
Glomus atrouva IT Yes ?McGee & Baczocha (1994), McGee & Trappe (2002)
Glomus australe IT Yes ?McGee & Baczocha (1994)
Glomus fuegianum IT Yes ?McGee & Baczocha (1994)
Glomus intraradices IT Ye s ?Lekberg et al. (2011)
Glomus macrocarpum G, IT Yes ?Trappe & Maser (1976), Allen & MacMahon (1988),
McGee & Baczocha (1994)
Glomus pellucidum IT Yes ?McGee & Baczocha (1994), McGee & Trappe (2002)
Glomus spp. IT Yes ?Allen (1987), McGee & Baczocha (1994)
Hebeloma mesophaeum IT Yes ?Nuñez et al. (2013)
Laccaria trichodermophora M, IT Yes +,- Casllo-Guevara et al. (2011), Pérez et al. (2012)
Melanogaster sp. IT Yes ?Nuñez et al. (2013)
Pyronemataceae IT Yes ?Tay et al. (2018)
Rhizophagus fasciculatus IT Yes ?Rothwell & Holt (1978)
Rhizopogon cf. arctostaphyli IT Yes ?Nuñez et al. (2013)
Rhizopogon evadens IT Yes ?Ashkannejhad & Horton (2006)
Rhizopogon fuscorubens IT Yes ?Ashkannejhad & Horton (2006)
Rhizopogon occidentalis IT Ye s ?Ashkannejhad & Horton (2006)
Rhizopogon pseudoroseolus IT Yes ?Aguirre et al. (2021)
Rhizopogon cf. rogersii IT Yes ?Nuñez et al. (2013)
Rhizopogon roseolus IT Yes ?Nuñez et al. (2013)
Rhizopogon salebrosus (group) IT Ye s ?Ashkannejhad & Horton (2006)
Rhizopogon truncatus M, IT Yes ?Colgan & Claridge (2002)
Rhizopogon vinicolor M, IT Yes varied Colgan & Claridge (2002)
Rhizopogon spp. (3 unidened species) IT Yes ?Wood et al. (2015)
Russula a. cuprea MYes = Casllo-Guevara et al. (2012)
Suillus brevipes IT Ye s ?Ashkannejhad & Horton (2006)
Suillus granulatus IT Yes ?Wiemken & Boller (2006), Aguirre et al. (2021)
Suillus luteus IT Yes ?Nuñez et al. (2013), Wood et al. (2015)
Suillus tomentosus M, IT Yes +Casllo-Guevara et al. (2011), Pérez et al. (2012)
© 2022 Westerdijk Fungal Biodiversity Instute
Elliott et al.
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
118
Table 2. (Connued).
Fungal species Method* Viability Rate* Citaon
Suillus umbonatus IT Yes ?Ashkannejhad & Horton (2006)
Thelephora americana IT Ye s ?Ashkannejhad & Horton (2006)
Thelephoraceae T73.1 IT Yes ?Ashkannejhad & Horton (2006)
Tomentella sublilicina IT Yes ?Ashkannejhad & Horton (2006)
Tuber aesvum M, IT Ye s +Piaoni et al. (2014), Ori et al. (2018, 2021)
Tuber borchii IT Yes ?Livne-Luzon et al. (2017)
Tuber canaliculatum IT Yes ?Miller (1985)
Tuber oligospermum IT Yes ?Livne-Luzon et al. (2017)
Tuber shearii IT Yes ?Miller (1985)
Tuberaceae IT Yes ?Tay et al. (2018)
Unidened (27 ECM taxa including
Ascomycetes and Basidiomycetes)
IT Yes +Claridge et al. (1992)
Unidened taxa (including: Elaphomyces
spp., Glomus sp., Hysterangium separabile,
Rhizopogon spp., Sclerogaster xerophilum and
Sedecula pulvinata)
IT Yes (unclear
which taxa)
= Koer & Farennos (1984)
Colonisaon by one or more of the following
VAM taxa: Glomus spp., Scutellospora gregaria
and S. verrucosa
IT Yes (unclear
which taxa)
? Paugy et al. (2004)
A preliminary examinaon of the scats
indicated that at least Hysterangium, Descolea
and Reddellomyces, but a full list was beyond
the scope of the study. Based on the results
both ECM and VAM taxa remained viable
IT Yes (unclear
which taxa)
+Smith (2018)
Dark septate endophytes and VAM fungi IT Ye s ?Fracchia et al. (2011)
Unidened (at least 7 ECM taxa) IT Yes +Lamont et al. (1985)
VAM fungi IT Yes +Ponder (1980)
VAM fungi including Glomus spp. (3
unidened species) and Sclerocyss
coremioides unclear if all or some were viable
IT Yes ?Mangan & Adler (2002)
Unidened ECM and VAM taxa IT Yes ?Reddell et al. (1997)
Unidened ECM fungi IT Yes - Terwilliger & Pastor (1999)
Unidened ECM fungi IT Yes ?McGee & Baczocha (1994)
Unidened ECM fungi IT Yes +Caldwell et al. (2005)
Unidened ECM fungi IT Yes ?Schickmann (2012)
A list of at least 58 taxa of mycorrhizal fungi that have been experimentally shown to remain viable aer passage through the digesve systems of
mammals. *Method: M: microscopic assessment, IT: inoculaon trials, G: germinaon trial in vitro. *Rate: +: improved viability when consumed
by animals compared to control, =: equal viability from scats to control, -: reduced viability compared to control, ?: no comparave viability data,
varied: dierent rates depending on mammal species. (Note: the names of the fungi listed in this table in some cases have been updated to reect
recent taxonomic/nomenclatural changes and may dier from the name listed in the original publicaon.)
Reess & Fisch (1887) and Hasngs & Moram (1915) rst
suggested that hypogeous fungi such as Elaphomyces may
benet from mammal dispersal, although they were not able
to demonstrate spore viability. The concept of spore dispersal
through mammal mycophagy assumes that spores remain
viable aer passage through the mammalian digesve system.
To fully understand how frequently spores remain viable and
among how many dierent mammal species, we reviewed the
literature that tested spore viability in mammal faeces. Reess &
Fisch (1887) tried mulple approaches with Elaphomyces spores
extracted from scats of the common fallow deer (Dama dama),
but both their controls and spores extracted from scats proved
unsuccessful. Considering that mycorrhizae research was in its
infancy in the 1880’s, they were likely facing methodological
limitaons. Aside from this early aempt, we found mulple
studies focusing on dierent groups of mycorrhizal fungi and
using various microscopy techniques or inoculaon/germinaon
trials. These studies detected viable spores from more than
58 mycorrhizal fungal species aer their passage through the
digesve system of at least 40 mammal species (Tables 1, 2). We
were unable to nd any studies showing that fungal spores were
no longer viable aer ingeson by mammals.
Spore resilience may be due in part to melanins that limit the
disintegraon (lysis) of spore cell walls (Bloomeld & Alexander
1967, Zambonelli et al. 2017). Although further studies are
needed to fully understand the relaonship between melanins
© 2022 Westerdijk Fungal Biodiversity Instute
Mammalian mycophagy
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
119
and mammalian digesve enzymes, the digesve enzymes of
mammals appear to be no match for the melanins in fungal
spores. It has been suggested that spores with ornamentaon or
thicker walls are more adept at surviving the digesve systems
of animals (Korf 1973). Although there may be situaons where
this hypothesis holds true, there are fungi with smooth, thin-
walled spores (e.g. the genera Suillis and Rhizopogon) that have
been thoroughly documented to survive mammalian digesve
systems (Table 2).
Although further empirical tesng is needed, our review
also revealed that at least 10 species of mammals may increase
spore germinaon/viability aer ingeson (Table 1). Colgan &
Claridge (2002) suggested that several factors, such as body
temperature, passage me and digesve anatomy, may impact
spore viability. Nuñez et al. (2013) showed that twice as many
seedlings inoculated with Eurasian wild pig (Sus scrofa) faeces
formed mycorrhizal colonisaon when compared with seedlings
inoculated with western red deer (Cervus elaphus) and common
fallow deer (Dama dama) faeces. The authors were unable to
decipher whether these dierences were due to the digesve
system of deer decreasing spore viability, or if the digesve
enzymes of wild pigs caused scaricaon that alleviates
spore dormancy and increases germinaon. Scaricaon of
fungal spores (i.e. erosion or breaking down of spore wall
microstructures) aer transit through mammalian digesve
systems has only been studied in a few fungal taxa and is probably
more common than presently known. For example, asci of Tuber
aesvum break apart and the spore ornamentaon is worn
down aer passage through digesve systems of Eurasian wild
pigs (Piaoni et al. 2014, 2016). Despite this apparent damage,
spores from faeces formed heavier mycorrhizal colonisaon
than non-ingested spores in inoculaon trials. Dierent animals
cause dierent amounts of spore scaricaon, and in general,
longer passage rates among larger animals likely increase
spore liberaon from asci and/or scaricaon. For example,
when comparing Tuber spores ingested by wild pigs with those
ingested by the long-tailed eld mouse (Apodemus sylvacus),
Zambonelli et al. (2017) suggested that the digesve system of
the long-tailed eld mice had liberated far fewer spores from
their asci than did that of wild pigs.
There are likely situaons where both seeds and associated
fungal spores are dispersed in the same scat (Pirozynski &
Malloch 1988), and it is possible that both are simultaneously
being scaried, thus increasing their chance to match with
suitable mycorrhizal symbionts. These studies are analogous
to animal ingeson of fruits that can facilitate the disrupon
of seed dormancy and increases seed germinaon rates (Sles
1992, Traveset et al. 2007). In mycology, similar studies remain
scarce but are necessary to improve our understanding of these
trophic interacons.
The role of aromas in mycophagy and fungal evoluon
Evidence suggests that some bird species may encounter fungi
simply by chance while others select them based on colour or
aroma (Ellio & Marshall 2016, Ellio & Vernes 2019). Although
terrestrial nave mammals are absent from New Zealand,
the country has a diversity of exceponally colourful endemic
trues that may be a result of selecve pressure from visually
cued foraging birds (Beever & Lebel 2014, Ellio et al. 2019a).
There are numerous reports of mammals eang epigeous fungi,
but since these fungal sporocarps are easily visible above the
surface of the soil, it is dicult to determine if mammals detect
them by visual or olfactory cues or a combinaon of both.
Fossey (1983: 131) provided an example of two young eastern
gorillas named Pucker and Coco seeking out “bracket fungi” for
food using what appears to be visual cues:
“One day while walking in a new area, Pucker suddenly ran
toward a large cluster of Hagenia trees on the edge of the
forest leading to the mountain. Coco leapt from my arms
in rapid pursuit — which was unusual. I thought they were
making a dash for the mountain and was hasly taking out
the bananas when both infants halted below one of the
larger trees. They peered up at the tree like children looking
up a chimney on Christmas eve. I had never seen them so
fascinated by a tree, nor could I determine what it was
that so strongly aracted them. Suddenly the two began
frenziedly climbing the huge trunk, leaving me even more
puzzled. About thirty feet above the ground they stopped,
pig-grunted at one another, and avidly started bing into a
large bracket fungus. Previously I had noted these shelike
growths, which protrude from Hagenia tree trunks and
rather resemble overgrown solidied mushrooms[...] Try
as they might, neither Coco nor Pucker could pry the fungus
from its anchorage on the trunk, so they had to content
themselves with gnawing chunks out of it. A half-hour later
only a remnant remained. Reluctantly they descended, but
as we walked on they gazed longingly back at the tree with
the fungus elixir”.
The role of aroma is more obvious in hypogeous fungi, where the
selecve advantage of mycophagy contributed to the convergent
rise of sequestrate sporulang morphologies in mulple fungal
lineages (Sheedy et al. 2016, Truong et al. 2017, Ellio &
Trappe 2018, Ellio et al. 2020a). Sequestrate sporocarps can
be parally emergent or hidden enrely below the soil surface,
placing the reproducve success of sporocarps and the species
at the whim of animal detecon. Many sequestrate fungi have
lost their ability for the forcible discharge of spores (Thiers 1984)
and therefore rely on the producon of volale olfactory cues to
aract animal dispersers (Maser et al. 1978a, Talou et al. 1987,
1990, Donaldson & Stoddart 1994, Stephens et al. 2020).
Due to the culinary/economic importance of many members
of the sequestrate genus Tuber, the chemistry of sequestrate
fungal aromas has been most thoroughly studied in this genus
(Splivallo et al. 2011, Molinier et al. 2015, Splivallo et al. 2015,
Vita et al. 2018, Mustafa et al. 2020). Based on experiments with
domesc dogs and pigs, Talou et al. (1990) suggested that dimethyl
sulphide was the primary aroma responsible for the detecon
of mature T. melanosporum sporocarps. Dimethyl sulphide is
also the primary odour that aracts true specialist arthropods
(Pacioni et al. 1991). These relaonships are analogous to plants
aracng pollinators with nectar and seed dispersers with sugary
fruits, but animal-fungal interacons remain less thoroughly
studied. We argue that similarly interdependent associaons have
been developed by sequestrate fungi through the producon
of strong aromas that ence animals to nd them when spores
reach maturity. The level of specialisaon and specicity in these
aromas is sll up for debate, and it is currently unknown whether
some fungi can mimic pheromones to target certain species or
sexes of mammalian dispersers. Claus et al. (1981) suggested that
the ability of pigs to detect T. melanosporum may be linked to
a steroidal pheromone (5α-androst-16-en-3α-ol) that is similar to
sex chemicals produced by the mammal. Ulmately, it is hard to
© 2022 Westerdijk Fungal Biodiversity Instute
Elliott et al.
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
120
prove whether wild pigs are so passionately interested in trues
merely because they are tasty and nutrious or as a result of some
sexual pheromonal trickery. Unlike analogous co-evoluonary
associaons involved in seed dispersal and pollinaon, we are
unaware of any highly specialised associaons that are exclusive
between a mammal and a fungal species. However, it would be
interesng to explore further whether the selecve advantages
oered by mycophagy could lead to more specialised dispersal
associaons.
There are many observaonal reports of mammals detecng
hypogeous fungi by sense of smell, such as deer digging up
hypogeous fungi hidden below the soil surface (Cowan 1945).
Bermejo et al. (1994: 888) described a bonobo (Pan paniscus)
seemingly using smell to locate an unidened “true” species
in the Democrac Republic of Congo:
“…standing quadrupedally, digs up the earth, rst with
one hand, then with the other, in search of subterranean
trues. She puts her face closer to the hole that she has
dug and looks closely. Then she carefully puts one hand into
the hole and withdraws it immediately, pung her ngers
to her nose to detect the scent of trues. She faithfully
repeats this operaon again and again”.
This type of behaviour is not restricted solely to this species
of primate. On mulple occasions, we have observed humans
displaying nearly idencal foraging behaviours while aempng
to locate commercially valuable trues in the wild and on
culvated true farms.
Smith (1968a) made extensive observaons of the behaviour
of young North American red squirrels in their rst few days
out of the nest as they learned what to eat. Smith (1968a: 42)
described the following observaon:
“On the third day one of the young travelled over 100
from the nest, at which point it snied along the ground
and dug up a false true (Hymenogastrales). It ate all of
the rst false true, dug up another, and ate half of that
before making an unsuccessful aempt to cache the rest
in a tree”.
Based on this observaon, squirrels appear to have an innate
knowledge about using their sense of smell to detect hypogeous
fungi and subsequently caching sporocarps. By making careful
daylight observaons from the day this squirrel was born, Smith
(1968a) demonstrated that the behaviour of this young squirrel
was truly innate and was not acquired from observing a parent
or other individual (also see secon: Caching and hoarding of
fungi). He suggested that the young would gradually become
more adept at this task, since it took over two minutes for this
juvenile to dig up the rst true and another nine minutes
to eat it, while its mother could perform the same acvity in
approximately one minute.
Brown hyenas (Hyaena brunnea) in the southern Kalahari
Desert are primarily scavengers of vertebrate remains, but they
reportedly also use their acute sense of smell to detect and eat
the hypogeous desert true Kalaharituber pfeilii (Mills 1978).
Brown hyenas are heavily reliant on odours when foraging, and
Mills (1978) reported in great detail how they ulised wind
direcon to detect and locate food, including desert trues. In
April of 1975, Mills reported brown hyenas picking up a scent on
the breeze on 21 occasions, making upwind turns of up to 200
m and then digging for a few seconds in the sand before they
uncovered specimens of K. pfeilii. We (TFE, JMT and KV) have
observed similar behaviours among domescated dogs trained
to hunt Tuber melanosporum, Lucangium carthusiana and other
commercially harvested trues. On mulple occasions, we
have seen highly trained true dogs step on parally emergent
immature trues, totally unaware of their presence, while
signalling their handlers toward a ripe true nearby.
These examples suggest that aroma can be an important
factor in controlling true consumpon and prevenng them
from being discovered before spores are mature/ready to
germinate. In western North America, the dusky-footed woodrat
(Neotoma fuscipes) regularly eats hypogeous fungi of the genera
Gaueria and Hysterangium (Parks 1919, 1922). Parks (1922)
noted that in the process of digging up ripe sporocarps, woodrats
oen overlooked or even discarded unripe specimens. The
more strong-smelling species were more regularly consumed,
suggesng a preferenal selecon for mature hypogeous
sporocarps likely due to the strength of the aromas. Parks
(1922) also noted that when dierent hypogeous fungal species
sporulated in close proximity to one another, dusky-footed
woodrats preferenally ate more aromac species and ignored
other readily accessible taxa, even if they were signicantly
larger. The diversity and abundance of trues (parcularly the
genus Gaueria) was also higher near dusky-footed woodrat
nests, but without a randomised survey method it is not possible
to prove if this is a meaningful correlaon. Based on this early
naturalist’s observaons, it is possible that when dusky-footed
woodrats defecate in close proximity to their nests, they might
inadvertently “farm” trues close to the security and safety of
their homes. More in-depth and rigorous studies are needed to
follow up on Parks’ observaons.
These examples illustrate some of the reproducve and
dispersal advantages of sequestrate fungi that produce aromac
compounds. How specialised these associaons are and whether
certain aromas are more appealing to dierent individuals, sexes
or taxonomic groups of animals remains to be directly assessed.
In a study invesgang the interacons between sporulang
depths, volale producon and rodent mycophagy of the
genus Elaphomyces, Stephens et al. (2020) showed that deeper
sporulang Elaphomyces species had disnct volale organic
compound proles and produced signicantly higher quanes of
aromac compounds compared to other members of the genus
that sporulated closer to the soil surface. They also concluded that
rodents were selecng for species that sporulated deeper in the soil
but produced stronger volales. The aromas of some hypogeous
fungi are potent enough to be detected with portable electronic
gas detectors such as ame ionisaon or explosimeters (Talou et
al. 1988). Thus, some hypogeous species produce aromas that
are so strong-smelling that they may be detected by animals that
do not typically rely on olfactory abilies when foraging. Stronger
aromas potenally translate into more frequent consumpon and
beer dispersal, but more complex interacons also occur. Pacioni
(1986) suggests that in Europe, domesc true dogs trained
to detect white true species (Tuber borchii and T. magnatum)
are less eecve at nding black true species (T. aesvum, T.
brumale, T. macrosporum, T. melanosporum, T. mesentericum and
T. uncinatum), and vice versa. The aroma composion of these
two groups diers only in the presence of one or more atoms of
sulphur (Pacioni 1986), indicang that aromac specialisaon
is possibly aimed at dierent animal dispersers. Donaldson &
Stoddart (1994) showed that acetaldehyde, ethyl acetate, n-propyl
© 2022 Westerdijk Fungal Biodiversity Instute
Mammalian mycophagy
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
121
acetate, isobutyl acetate, ethyl isobutanoate, ethyl butanoate and
ethyl propanoate were the compounds responsible for eastern
beongs’ aracon to and detecon of species of Mesophellia.
Ulmately, it is sll unknown whether it is the combinaon of
dierent aromac compounds or the strength of the compounds
themselves that is more impacul on mammalian sporocarp
detecon.
Mammal movements and impacts of primary versus secondary
spore dispersal
Fungal spores ingested by mammals are generally only dispersed
within the home range of an individual, and for most mammals,
there is a direct relaonship between larger body size and
larger home range (Lindstedt et al. 1986, Swihart et al. 1988).
The dispersal potenal of any vertebrate species depends on
three factors: passage rate (i.e. transit me through the animal’s
gastrointesnal tract); movement paern (i.e. how far the
individual will move as well as the size of its home range); and
speed (i.e. how fast the animal will travel within its home range).
These three factors are key to esmang the dispersal potenal
of fungi ingested by any animal.
Due to the small size and vast numbers of spores produced
by fungal sporocarps, spores can linger in the mammalian gut
for longer periods than other larger dietary components (Danks
2012). The passage rate of macrofungal spores has been directly
studied in ve mammal species: two Murids, one Sciurid, one
Macropodid and domesc pigs (Sus scrofa) (Danks 2012, Piaoni
et al. 2016). This small sub-sample does not reect the large
diversity of mammal mycophagists, and there is likely variability
between species and individuals of the same species depending
on weight, size, intesnal morphology, sex, age, health,
movement, other dietary components and season/temperature
(Cork & Kenagy 1989b, Comport & Hume 1998, Danks 2012,
Piaoni et al. 2016, Ellio et al. 2020b). This area of research
is sll in its infancy in comparison to the extensive botanical
research regarding vertebrate seed dispersal. More studies on
spore passage rates in many groups of mammals are needed to
beer understand the processes behind fungal spore dispersal in
various mammal species and to develop modelling applicaons
similar to those widely used by plant ecologists. One modelling
study showed that swamp wallabies (Wallabia bicolor) regularly
disperse fungal spores hundreds of metres (in some instances
up to 1 265 m) from where the sporocarp was inially ingested
(Danks et al. 2020). Such long-distance dispersal events have
strong ecological signicance for fungal taxa, parcularly those
with sequestrate sporocarp morphologies. To our knowledge,
this is the only study of its kind, and such modelling approaches
show promise in their potenal to demonstrate that a diversity
of animal species carry spores for similar or even greater
distances than does the swamp wallaby.
Secondary dispersal (diplochory) by predators that consume
primary mycophagists is another important mode of fungal
spore dispersal. This concept was rst invesgated more than
a century ago in toads that dispersed viable fungal spores by
eang slugs that had eaten fungi (Vogilino 1895, Buller 1909).
Since then, very lile modern research has directly invesgated
secondary dispersal, and it is sll unclear how widespread
it is. Numerous animals are likely playing a role, including
the white-headed woodpecker (Picoides albolarvatus) that
feeds on insects known to disperse spores of the veiled
polypore (Cryptoporus volvatus) (Watson & Shaw 2018). These
woodpeckers – as well as numerous other insecvorous birds
and mammals – can inadvertently act as secondary dispersers
of fungi. In most cases, secondary dispersal of fungal spores
can greatly increase their dispersal distance, as insecvorous
birds and mammals typically move over much larger distances
than the primary consumers they prey upon (Schickmann
2012, Schickmann et al. 2012). Predators such as eagles, owls
and hawks frequently prey on mycophagous rodents, and their
aerial journeys inevitably disperse spores far more widely than
those of the small earthbound mammals (Trappe 1988, Colgan
1997, Luoma et al. 2003, Halbwachs & Bässler 2015). Larger
mammalian carnivores such as canids regularly feed on smaller
mycophagous mammals. Because predators have much larger-
scale movement paerns than their prey, these carnivores
have the potenal to provide a vital yet overlooked ecosystem
funcon through secondary dispersal of mycorrhizal fungi. The
pampas fox (Lycalopex gymnocercus) has been reported to
disperse mycorrhizal fungal spores, but it is currently unclear
if this is an example of primary or secondary dispersal (Aguirre
et al. 2021). Many bats are also likely acng as secondary
dispersers of fungi by ingesng insects that eat fungi (O’Malley
2013). New Zealand’s ightless bats (Mystacina) may ingest
fungi (Lloyd 2001); but this group of bats are atypical, and
there is sll insucient data to conrm if they are fungal
dispersers. Given the resiliency of fungal spores (see Tables
1, 2), it is unlikely that secondary dispersal negavely impacts
their viability, but further studies are needed to address these
quesons.
When a scat is deposited by a primary or secondary
disperser, it is not necessarily at the end of its journey.
Numerous organisms interact with scats and may further impact
spore dispersal. Some mammals eat scats (coprophagy) and may
therefore further disperse spores or improve spore germinaon
rates (Zambonelli et al. 2017). In many terrestrial ecosystems,
scarab beetles move and bury animal dung, including that from
mycophagous mammal species. Scarab beetles can further
disperse or bury seeds (Vander Wall & Longland 2004), but
very lile research has assessed dung beetles as dispersal
vectors of fungal spores in mammal scats. At least three
species of scarab beetles (Onthophagus ferox, O. rupicra and
Thyregis spp.) disperse spores from the brush-tailed beong
(Beongia penicillata) aer feeding on the scats of this mammal
(Christensen 1980). Several Australian species of Orthophagus
have claws on their legs that are modied for grasping the fur
of mammals, including mycophagous wallabies and beongs.
This adaptaon allows the beetle to cling to the animal unl it
defecates; upon defecaon, the beetle drops from the animal
and immediately buries the dung to use as a brood chamber for
its larvae (Mahews 1972). Although it has yet to be directly
studied, this behaviour in many scarab beetles likely improves
the success of mycorrhizal fungal spores by burying them in the
rhizosphere and thus facilitang mycorrhizal root colonisaon.
Ecosystem implicaons of mammal mycophagy
Bioturbaon resulng from mycophagy
The digging acvies of animals excavang hypogeous fungi
contribute to bioturbaon (soil disturbance) and provide
important soil aeraon for water penetraon and organic maer
decomposion (Lamont 1995, Garkaklis et al. 1998, 2000, 2003,
2004, Newell 2008, James et al. 2009, Valenne et al. 2013,
2018, 2021, Fleming et al. 2014, Clarke et al. 2015, Davies et al.
2018, Palmer et al. 2020, 2021). Various mycophagous animals
© 2022 Westerdijk Fungal Biodiversity Instute
Elliott et al.
Editor-in-Chief
Prof. dr P.W. Crous,Westerdijk Fungal BiodiversityInstitute, P.O. Box 85167, 3508 AD Utrecht, The Netherlands.
E-mail:p.crous@westerdijkinstitute.nl
122
perform bioturbaon to varying degrees, and the relave
importance of animal-mediated soil turnover is also dependant
on the region and soil type. In Australia, the role of mycophagous
vertebrates in soil turnover has been relavely well studied
in some regions. Many Australian forests are dominated by
Eucalyptus species and their relaves (Holliday 1989). Leaves in
these groups oen contain high levels of oils that leach into the
soil, creang a hydrophobic lm on the soil surface that impairs
water penetraon (Garkaklis et al. 1998). The combinaon of soil
dryness and oil concentraon at the soil surface creates a layer of
ammable material that increases the sensivity of these forests
to res. In a healthy system, a multude of vertebrates forage in
the lier and dig down into the mineral soil in search of trues
and other subterranean foods. These acvies contribute to
the breaking up of the hydrophobic layer at the soil surface and
create micro catchments, thus improving water penetraon
and assisng with organic maer decomposion (Lamont 1995,
Garkaklis et al. 1998, 2000, 2003, 2004, Newell 2008, James et
al. 2009, Valenne et al. 2013, 2018, Fleming et al. 2014, Davies
et al. 2018, Palmer et al. 2020, Maisey et al. 2021).
The degree of bioturbaon depends on the size of the
animal and its foraging habits. Superb lyrebirds (Menura
novaehollandiae) eat a diversity of hypogeous fungi (Ellio &
Vernes 2019), and each individual is esmated to displace an
average of 155.7 tonnes of soil per hectare per year (Maisey
et al. 2021). Mammals typically turn over less soil than ground
foraging birds, likely due to their keen olfactory abilies that
allow them to pinpoint the locaons of subterranean food (Ellio
et al. 2019a). Ground foraging birds need to scratch larger areas
to nd food that they cannot necessarily detect by smell. Sll,
mammals contribute greatly to soil turnover. The brush-tailed
beong digs between 38 and 114 excavaons per night, and each
individual is esmated to displace an average of 4.8 tonnes of soil
per year (Garkaklis et al. 2004). The southern brown bandicoot
(Isoodon obesulus) has been esmated to dig about 45 foraging
excavaons per day and in the process displace about 10.74 kg
of soil, resulng in a soil turnover of approximately 3.9 tonnes
per year per individual (Valenne et al. 2013). Some of the larger
desert species such as the greater bilby (Macros lagos) and
the burrowing beong (Beongia lesueur) are esmated to turn
over approximately 30 tonnes of soil per year per individual
(Newell 2008). These examples demonstrate the wide range in
the rate/quanty of soil disturbance by various mammal species.
Given that Australia is believed to have the greatest diversity of
hypogeous fungi (Bougher & Lebel 2001, Claridge 2002) and is
also home to numerous mycophagous mammal species, it is
very likely that these interacons have coevolved.
In healthy systems, many individuals and species co-occur,
and their combined foraging eorts are key to maintaining
healthy forest soils. Due to the introducon of foxes and
cats to Australia, many of these bioturbang mammals have
disappeared from much of their historic ranges or became
exnct (Bilney 2014, Fleming et al. 2014, Vernes et al. 2021).
We suspect that the loss of mycophagous mammal species
and the subsequent loss of their soil turnover capacies may
be a contribung factor in the increased frequency/intensity
of res, as well as in the desercaon of some regions of the
connent. Though early foresters recognised the importance of
well-aerated soil for the health of Australian forests and for the
reducon of intense wildres (Hutchins 1916), these aspects of
forest ecology are unfortunately rarely considered in current
forest management plans.
Ecosystem impact on below ground and above ground
communies
The examples described in the previous secon illustrate how
mammal-mediated dispersal plays a major role in shaping
the composion of soil-fungal communies. The mycorrhizal
interacons between these fungi and plant roots can also
directly </