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Is small mammal mycophagy relevant for trufe 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 trufe 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 trufe species by mammal
vectors, or about the potential role of mycophagy in trufe plantations. We hypothesize that
small mammal mycophagy contributes to the productivity of trufe plantations by providing
inoculum for trufe mycelium establishment and mating. Spread of non-desired competitors
of gourmet trufes 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
Polish Botanical Society
Elektronicznie podpisany przez Polish Botanical Society
DN: c=IE, st=Warszawa, o=ditorPolish Bot, ou=Standard Certificate,
ou=anical SocietySupport, serialNumber=PT2110520970.1,
title=Managing E, sn=Otreba, givenName=org.plPiotr,
email=p.otreba@pbsociety., cn=Polish Botanical Society
Data: 2014.01.02 12:10:04 +01'00'
140 A. Urban et al.
gourmet trufe 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 trufe 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 trufe plantations. Newly established trufe 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 trufe 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 trufe 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 trufe plantations and need to be excluded.
Effects on trufe populations. Little is known about effects of mycophagy on
trufe populations in managed plantations. The small rodent species common in
habitats like trufe 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 trufes or host tree roots.
From the trufe growers perspective, mycophagy may be regarded as a waste of
valuable crop. Small mammals are important dispersal agents for trufe 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 trufe 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 trufe plantations: 1) Trufe spores in faeces of small mammals
are a viable source of inoculum (Schickmann et al. 2012). 2) Articial inoculation
of soil with trufe spores is reported to inrease yields of Tuber aestivum (P. Sourzat,
unpublished). 3) Sexual reproduction and outcrossing has been proven in some
gourmet trufe 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.
Trufe 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 trufe within the plantation.
CONCLUSIONS
Currently, information on the role of small mammal mycophagists in trufe planta-
tions is scarce, despite the signicance of mycophagy in the trufe life cycle. Small
mammals, at least if present in excess, are typically regarded as pests, by foresters
and trufe-growers. Some trufe 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 difcult to assess than the inuence of
abiotic factors, such as climate. Experimental work on mycophagy in trufe planta-
tion and natural trufe sites is needed to obtain reliable data on the role of small
mammals in the dispersal and reproduction of trufe species.
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