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Is small mammal mycophagy relevant for truffle cultivation? Acta Mycol. 47 (2): 139–143, 2012. The role of mycophagous small mammals as vectors of hypogeous fungi is well established. However, little is known about dispersal of gourmet truffle species by mammal vectors, or about the potential role of mycophagy in truffle plantations. We hypothesize that small mammal mycophagy contributes to the productivity of truffle plantations by providing inoculum for truffle mycelium establishment and mating. Spread of non-desired competitors of gourmet truffles is a potential adverse effect of small mammal mycophagy. INTRODUCTION Hypogeous fungi and other macrofungi are part of the diet of small rodents (Ro-dentia) such as voles (Arvicolinae, Cricetidae, Myomorpha), mice (Murinae, Muridae, Myomorpha), dormice (Gliridae, Sciuromorpha) and sqirrels (Sciuridae, Sciuromor-pha) (Maser, Claridge and Trappe 2008). Recently it was found that insectivorous shrews (Sorex spp., Soricidae, Eulipotyphla) frequently feed on hypogeous fungi as well (Kataržytė, Kutorga 2011; Schickmann et al. 2012). The nutritional ecology of most small mammal species seems to be rather flexible, highly adaptive and more diverse than commonly assumed. Spore dispersal in hypogeous fungi including ACTA MYCOLOGICA Vol. 47 (2): 139–143 2012
Is small mammal mycophagy relevant for trufe cultivation?
ALEXANDER URBAN1, MARIJA KATARŽYTĖ2, SUSANNE SCHICKMANN3,
KATHARINA KRÄUTLER4 and TONY PLA1,5
1Department of Systematic and Evolutionary Botany, Faculty of Life Sciences
University of Vienna, Rennweg 14, A-1030 Vienna, alexander.urban@univie.ac.at
2Coastal Research and Planning Institute, Klaipėda University, LT-92294, Klaipėda
3Department of Integrative Biology and Biodiversity Research, Institute of Wildlife Biology
and Game Management, University of Natural Resources and Life Sciences,
Gregor-Mendel-Strasse 33, A-1180 Vienna
4Department of Forest and Soil Sciences, Institute of Forest Entomology,
Forest Pathology and Forest Protection
University of Natural Resources and Life Sciences, Hasenauerstraße 38, A-1180 Vienna
5 TrüffelGarten Urban & Pla OG, Burwegstr. 88, A-3034 Eichgraben
Urban A., Kataržytė M., Schickmann S., Kräutler K., Pla T.: Is small mammal mycophagy
relevant for trufe cultivation? Acta Mycol. 47 (2): 139–143, 2012.
The role of mycophagous small mammals as vectors of hypogeous fungi is well
established. However, little is known about dispersal of gourmet trufe species by mammal
vectors, or about the potential role of mycophagy in trufe plantations. We hypothesize that
small mammal mycophagy contributes to the productivity of trufe plantations by providing
inoculum for trufe mycelium establishment and mating. Spread of non-desired competitors
of gourmet trufes is a potential adverse effect of small mammal mycophagy.
Keywords: Tuber aestivum, Tuber melanosporum, mutualism, symbiosis, mycorrhiza, ectomycorrhiza
INTRODUCTION
Hypogeous fungi and other macrofungi are part of the diet of small rodents (Ro-
dentia) such as voles (Arvicolinae, Cricetidae, Myomorpha), mice (Murinae, Muridae,
Myomorpha), dormice (Gliridae, Sciuromorpha) and sqirrels (Sciuridae, Sciuromor-
pha) (Maser, Claridge and Trappe 2008). Recently it was found that insectivorous
shrews (Sorex spp., Soricidae, Eulipotyphla) frequently feed on hypogeous fungi as
well (Kataržytė, Kutorga 2011; Schickmann et al. 2012). The nutritional ecology of
most small mammal species seems to be rather exible, highly adaptive and more
diverse than commonly assumed. Spore dispersal in hypogeous fungi including
ACTA MYCOLOGICA
Vol. 47 (2): 139–143
2012
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140 A. Urban et al.
gourmet trufe species depends entirely on animal vectors, and the mutualistic re-
lationship between mycophagous animals and hypogeous fungi can be considered
obligate for the latter. Small mammal mycophagy was extensively studied in North
America and Australia, since it was recognized as a process potentially important
for the maintenance of fungal and mammal biodiversity and for forest regeneration
(Claridge 2002; Maser et al. 2008). In Europe, relatively few studies demonstrated
the role of mycophagy in bank vole, (Myodes glareolus, Blaschke and Bäumler 1989),
red squirrel (Sciurus vulgaris, Grönwall, Pehrson 1984; Bertolino et al. 2004) and
wood mice (Apodemus spp., Blaschke, Bäumler 1989).
During a study conducted in primary and secondary forests in two regions of
the eastern alps we found that all mammal species native to Central Europe moun-
tainous forests investigated feed on hypogeous fungi, albeit with different inten-
sity (Schickmann et al. 2012). Based on frequency, quantity and diversity of fungal
spores detected in faeces by microscopy and with molecular tools, we concluded
that at least one native small mammal species, the bank vole (Myodes glareolus) is
preferentially mycophagous. All other species captured, including wood mice (Ap-
odemus avicollis and A. sylvaticus), other vole species, shrews (Sorex spp.) and the
fat doormouse (Glis glis) were found to be opportunistically mycophagous. All small
mammal species were found to feed on a diversity of fungal species. Similar results
were reported from hemiboreal forests in Lithuania (Kataržytė, Kutorga 2011).
METHODS
Here we synthesize available information to infer potential roles of small mammals
in trufe plantations. A descriptinon of methods used for life trapping of small mam-
mals, fecal pellet sample collection and microscopical analysis is found in (Schick-
mann et al. 2012). A protocol optimized for DNA extraction from fungal spores in
fecal pellets of small mammals was developed (Schickmann et al. 2011).
RESULTS
POTENTIAL ROLES OF SMALL MAMMALS IN TRUFFLE PLANTATIONS
Effects on host trees. Small mammal communities differ with habitat types. Rodent
species are more or less herbivorous, and some species are known to damage host
trees, at least at high population densities. Red squirrels are likely to occur in ma-
ture plantations, especially if hazelnuts (Corylus spp.) or conifer seeds are avail-
able. Squirrels are very effective seed predators, hoarding of excess food in caches
contributes to seed dispersal. Sqirrels can damage trees by bark stripping, however,
this behaviour is a major issue in the invasive grey squirrel (Sciurus carolinensis)
but not in the native red squirrel (Bertolino, Genovesi 2003). Voles can cause se-
vere damage in young trufe plantations. Newly established trufe plantations in
Small mammal mycophagy 141
agricultural environmenments are more likely to be colonized by common voles
(Microtus arvalis) than by species ocurring in more natural habitats such as eld
vole (Microtus agrestis) and bank vole (Myodes glareolus). An invasion of voles into
an experimental trufe plantation was observed when a neighbouring maize eld
was harvested and the animals lost shelter (Ronald Vogl, personal communication).
Debarking of the stem base killed one Corylus colurna tree (4 yrs after outplanting).
It appears that some tree species are less preferred by voles, e.g., pine species are
avoided (Borowski 2007). Lime tree (Tilia cordata) seedlings were reported to be
preferentially attacked by bank voles (Pigott 1985).
Planting a diversity of tree species may the best strategy to limit overall damage,
given the diversity of potential pest species. According to our experience, voles are
rarely a cause of excessive tree mortality in trufe plantations, but pressure can vary
considerably. If the risk of loosing tree seedlings due to damage by voles is high, the
roots and stem bases can be protected with a non-galvanized wire-basket which will
decompose by corrosion. Mulching can provide shelter for small mammals depend-
ing on the material used and should be avoided or adapted if pressure is critical.
Small mammal species are an important source of prey for predators such as
various species of birds of prey, owls, red fox (Vulpes vulpes), wildcat (Felis silvestris),
and various mustelids such as weasel (Mustela nivalis), European polecat (Mustela
putorius) and European badger (Meles meles). Providing habitat for predators and
protecting them from beeing hunted is an effective way to keep small mammal popu-
lations at levels compatible with plantation management objectives.
According to our experience, game species, like European hare (Lepus euro-
paeus) and roe deer (Capreolus capreolus) usually impose much higher pressure on
young trufe plantations and need to be excluded.
Effects on trufe populations. Little is known about effects of mycophagy on
trufe populations in managed plantations. The small rodent species common in
habitats like trufe plantations, e.g., voles, wood mice (Apodemus syvaticus and A.
avicollis) and squirrels are well known to be mycophagous (Maser et al. 2008).
Sqirrels even cache hypogeous fungi (Vernes, Poirier 2007). Recently it was shown
that also insectivores such as shrews (Sorex spp.) frequently feed on hypogeous fungi
(Kataržytė, Kutorga 2011; Schickmann et al. 2012). This result is of interest for two
reasons: 1) Shrews are not herbivorous and they are very unlikely to harm host trees.
2) Shrews are insectivorous and ground-dwelling, and may contribute to controlling
insects parasitic on trufes or host tree roots.
From the trufe growers perspective, mycophagy may be regarded as a waste of
valuable crop. Small mammals are important dispersal agents for trufe spores, but
no data are available which proof that there is a role for mycophagist in plantations
established with mycorrhized trees. Once established, genets of trufe mycelium can
grow and and extend, without apparent need of additional spores. However, three
lines of evidence suggest that mycophagy may be essential for the long term fertility
and productivity of trufe plantations: 1) Trufe spores in faeces of small mammals
are a viable source of inoculum (Schickmann et al. 2012). 2) Articial inoculation
of soil with trufe spores is reported to inrease yields of Tuber aestivum (P. Sourzat,
unpublished). 3) Sexual reproduction and outcrossing has been proven in some
gourmet trufe species (Paolocci et al. 2006; Riccioni et al. 2008), and ascopore or
142 A. Urban et al.
conidiospore (Urban et al. 2004) dispersal is likely to play a role in fertilisation of
opposing mating types.
Trufe spore dispersal by small mammal vectors has one potential drawback:
mycophagists use to feed on a variety of species of hypogeous fungi. Thereby, they
likely vector non-marketable or low-value species which may compete with the tar-
get gourmet trufe within the plantation.
CONCLUSIONS
Currently, information on the role of small mammal mycophagists in trufe planta-
tions is scarce, despite the signicance of mycophagy in the trufe life cycle. Small
mammals, at least if present in excess, are typically regarded as pests, by foresters
and trufe-growers. Some trufe growers use to combat small mammals by different
means of pest control, but systematic experimentation is still lacking. At present we
do not know whether the contribution of spore dispersal by small mammals to pro-
ductivity is comparable to the relevance of pollination in fruit orchards. The impact
of biotic interactions on productivity is more difcult to assess than the inuence of
abiotic factors, such as climate. Experimental work on mycophagy in trufe planta-
tion and natural trufe sites is needed to obtain reliable data on the role of small
mammals in the dispersal and reproduction of trufe species.
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... Masses of spores and sticky sap droplet exuded form pycnidial and perithecial cirrhi or often on the top of an elongated stalk are carried away by arthropods passing through colonies. Microfungi such as Gliocladium , Graphium , Leptographium , Myrothecium , Pesotum , Stilbella , and Stachybotrys develop complex conidiophores and utilize this dispersal mode (Ingold 1953 ;Abbott 2000 ;Seifert 1985 ;Upadhyay 1981 ;Wingfi eld et al. 1993 ). These relatively large, complex structures develop vertically from t he substrates and are tall enough to hitchhike onto large insects moving over the surface. ...
... Ascospores are developed in wet spore masses at the apices of the perithecial necks in Ophiostoma , Ceratocystis , and Sphaeronaemella . The long-necked ascomata and long-stalked conidiophores stick out into the insect passing routes and effi ciently force the insects to touch the spore masses as they pass through the restricted spaces and to pick up spores (Upadhyay 1981 ;Wingfi eld et al. 1993 ). ...
... Bark beetles, Dendroctonus and Ips , are well documented for their roles in dispersal of the ascospores and the conidia of blue-stain fungi (e.g., Leptographium and Pesotum ) (Upadhyay 1981 ;Wingfi eld et al. 1993 ). One classic example is the dispersal of Dutch elm disease caused by Ophiostoma ulmi and O. novo-ulmi by specialized bark beetle vectors ( Scolytus and Hylurgopinus ). ...
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... In addition to well-known smuggled goods ( Jezierski et al., 2014 ) and COVID-19 ( D'Aniello et al., 2021 ), dogs can find truffles, one of the most expensive gourmet foods. While the hidden life cycle of these belowground fungi ( Callot, 1999 ) challenges our ecological and phenological understanding in space and time ( Büntgen et al., 2017 ), the specific volatiles of ripe fruiting bodies attract many animals ( Urban et al., 2012 ). Apart from insects that feed on truffles ( Martin-Santafe et al., 2014 ), their fruiting bodies are an important source of carbohydrates (derived from the host plant) for many animals, such as mice, squirrels, and wild boars ( Maser et al., 2008 ). ...
... From our experience, even highly trained dogs cannot always distinguish between different truffle species and other underground fungi (e.g., Genea spp., Choiromyces meandriformis ). Moreover, overpopulated mycophagous rodents such as mice and squirrels reduce the seasonal harvest ( Urban et al., 2012 ) and, from our perspective, also confuse dogs by scattering feces ( Gsell et al., 2010 ). Further scent confusion for dogs may arise in orchards, where gopher and mouse tunnels in the soil transport the aroma away from truffles. ...
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