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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?
1Department of Systematic and Evolutionary Botany, Faculty of Life Sciences
University of Vienna, Rennweg 14, A-1030 Vienna,
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
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
Vol. 47 (2): 139–143
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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).
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).
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.
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 ). ...
Full-text available
Successful and efficient dispersal of fungi is crucial to the survival of the fungi, balance of ecosystems and stability of biodiversities. Dispersal strategies of microfungi and other fungi are reviewed in detail based on the literature published in the last four decades. It covers the latest development of research on the dispersal process: liberation, transporation, deposition, resuspension, and survival of fungal spores and other propagules from microscale to macroscale. The characters of dispersal strategies of fungi from different habitats are elucidated. The fungal habitats include litter, soil, plants, insects, other animals, and aquatic and marine environments etc. For each strategy, the associated mechanisms are discussed for their ecological significance. The significance of new technology used in the recent studies on dispersal strategies is presented. At the same time current and future applications of dispersal strategies of microfungi are discussed in the chapter.
... 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. ...
Trained dogs can detect many biochemical traces, from the most hostile, such as COVID-19, to the most expensive, such as truffles. However, it is still unclear how the interplay of genetic disposition, education, experience, personality, and environmental conditions influences the performance of dogs. Here, we combine published evidence with the knowledge of truffle hunters to assess direct and indirect factors that affect the hunting performance of truffle dogs. Since the transport of truffle aroma into the canine nasal cavity is most puzzling, we propose five experiments to further investigate the role of weather conditions, soil parameters, and bacterial composition on the dispersal of truffle volatiles perceived by trained dogs. We also suggest exploring whether the application of multiple dogs increases the success of truffle hunting. Moreover, we argue that interdisciplinary research on dog behavior and performance, including insights from veterinary science and comparative psychology as well as the experience of truffle hunters and farmers, is needed to improve the quantity and quality of truffle harvests.
Shrews, Chromosomes and Speciation - edited by Jeremy B. Searle February 2019
The diversity of small mammals reported to feed on true truffles is revised. Potential adaptations and specific capacities linked to mycophagy are discussed. The nutritional qualities of true truffles are summarized and confronted with digestive capacities and food preferences of small mammals. The recent discovery that the primarily insectivorous shrews (Sorex spp.) feed on true truffles, apparently in a selective manner, led to the hypothesis that allometric constraints on acceptable food quality limit mycophagy in extremely small mammal species and may be at the origin of more selective mycophagy. Foraging behaviour, hoarding and hibernation are recognized as factors influencing the spatial and temporal patterns of truffle spore dispersal. Case studies of the interrelationships between habitat preferences of small mammals, the spatial distribution of truffle species and the plant community succession are reported. The potential role of truffle spore dispersal by small mammals in the truffle life cycle is briefly discussed, hypothesizing that the dispersal of ascospores and/or microconidia contributes to mating in true truffles.
Full-text available
The diets of small mammals in different hemiboreal spruce-dominated, oak-dominated and mixed forests in western part of Lithuania were studied by examination of fungal spores in fresh fecal pellets of caught animals. In the diets of mice (Apodemus spp.), bank voles (Myodes glareolus), and common and pygmy shrews (Sorex araneus and S. minutus), 22 different fungal taxa were identified, 15 of which were hypogeous fungi. The sporocarp abundance and the spores in fecal samples of Elaphomyces fungi prevailed in study area during this investigation. Although most of the captured individuals consumed fungi, the consumption varied among small mammal species. The data show that the fungi were more frequent and taxonomically diverse in Myodes glareolus than in Apodemus spp. diets. The study provided evidence that the fungal component in the diets of insectivorous Sorex species is more diverse than previously known. The availability of sporocarps and the fungal component in the diets of small mammals showed seasonal effects. Annual hypogeous and epigeous sporocarp abundances did not vary significantly across forest types. The significant difference in mycophagy was observed across all forest cover types, with the greatest fungal diversity in fecal samples collected in mixed coniferous-deciduous tree stands.
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Mycophagy is often underestimated as dietary strategy, but forms an important part of the webs of life, especially in forest ecosystems. The identification of consumed fungal species is crucial to gain more knowledge about food web structures. DNA based methods are the way of choice to overcome limitations of species determination by microscopic analysis. DNA extraction from fungal spores in faecal samples requires specific methodology, due to the resistance of fungal spores and due to the properties of the faecal matrix. We tested two open source extraction buffers, as well as one widely used commercial extraction kit in combination with a mechanical disruption procedure optimised for fungal spores in faecal samples. The efficiency of the DNA extraction was assessed by comparing DNA yield after amplification by PCR with fungus-specific primers. All three protocols were successful in extracting amplifiable fungal DNA. The CTAB protocol yielded the highest amounts of DNA after PCR and gave the most constant results, but the differences among protocols were not significant. The establishment of reliable protocols for DNA extraction from small quantities of fungal spores in faecal samples paves the way for high resolution non-invasive studies in the dietary ecology of wild-living mammals.
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A Turdus migratorius (American Robin) nest was found in southern New Brunswick, Canada, containing 52 mature sporocarps (“truffles”) of Elaphomyces granulatus (false truffle), a species of hypogeous fungus common across North America. Teeth marks on the truffles indicated they had been cached in the nest by a Tamiasciurus hudsonicus (red squirrel). The truffles appeared to have been air-dried before caching and were well preserved. Mean (± SD) weight of each truffle was 3.3 ± 1.4 g, with a total weight of cached material of 173 g. Although caching of epigeous fungus by squirrels is well documented in the literature, records of cached hypogeous fungi are relatively uncommon, and caches involving disused bird nests appear to be rarely encountered.
The consumption of epigeous and hypogeous fungi by red squirrels Sciurus vulgaris in subalpine conifer forests in the Alps was studied by determining the presence and taxa (genus level) of fungal spores in fecal samples. Nearly all live-trapped squirrels in summer and autumn had eaten fruit bodies of hypogeous fungi, but only some animals had consumed epigeous fungi of the genus Boletus and/or Laccaria. From two (spring) up to nine (summer–autumn) genera of hypogeous fungi were eaten. The mean number of genera of fungi and the mean number of spores per mg fecal material differed between study areas and seasons. Fruit bodies of hypogeous, and to a lesser extent epigeous, fungi seem to present an important seasonal food resource for red squirrels in conifer forests of the Alps. We suggest that squirrels, having large home range size and dispersal distances, are likely to play a major role as spore dispersal agent for hypogeous fungi.
Spores of hypogeous fungi found in stomach contents of mice and voles trapped in high and low-elevation forests were identified and recorded with estimates of frequency of fungal genera. The data show differences between sites in the number of fungal taxa consumed. A similar taxa frequency was noted on plots with regenerations adjacent to mature stands. Spores of Endogonaceae were found to occur more often within reforestation sites linked with qualitative changes in ground vegetation.
In today's world of specialization, people are attempting to protect the Earth's fragile state by swapping limousines for hybrids and pesticide-laced foods for organic produce. At other times, environmental awareness is translated into public relations gimmicks or trendy commodities. Moreover, simplistic policies, like single-species protection or planting ten trees for every tree cut down, are touted as bureaucratic or industrial panaceas. Because today's decisions are tomorrow's consequences, every small effort makes a difference, but a broader understanding of our environmental problems is necessary to the development of sustainable ecosystem policies. In Trees, Truffles, and Beasts, Chris Maser, Andrew W. Claridge, and James M. Trappe make a compelling case that we must first understand the complexity and interdependency of species and habitats from the microscopic level to the gigantic. Comparing forests in the Pacific Northwestern United States and Southeastern mainland of Australia, the authors show how easily observable speciesùtrees and mammalsùare part of a complicated infrastructure that includes fungi, lichens, and organisms invisible to the naked eye, such as microbes. Eminently readable, this important book shows that forests are far more complicated than most of us might think, which means simplistic policies will not save them. Understanding the biophysical intricacies of our life-support systems just might. Copyright © 2008 by Chris Maser, Andrew W. Claridge, and James M. Trappe. All rights reserved.
The impact of small rodents on Polish forest trees was examined at both the national and regional levels. Detailed information based on a questionnaire was collected at the national level in 1993. Field studies at the regional level were carried out from 1994 through to 1997. The damage due to rodents constituting a significant economic problem occurred in only 4% of the Forest Districts in Poland. The tree species that small rodents preferred most were larch, ash, beech and maple, whereas birch, Norway spruce, Scots pine and black alder were the least preferred. Regional field studies were conducted in localities with the highest levels of damage situated in the Sudety Mountains (southern Poland). In this region, the most common rodent species was the field vole. Levels of tree-seedling damage were correlated with vole population density in the Autumn. I conclude that: (1) at the national level, the damage caused by small rodents has limited impact on Polish forestry; (2) at the regional level small rodents may exert considerable pressure on the over-wintering survival of tree seedlings.
(1) Small saplings of Tilia cordata, when planted in deciduous woodlands, are damaged or destroyed by rodents. (2) Experiments with captive animals show that the damage is identical with that caused by bank voles. (3) Bank voles are present at all sites where damage occurs. (4) Small saplings of Betula spp. established naturally in the sites are very rarely damaged. (5) Seedlings of Quercus spp. and Fagus silvatica are damaged or destroyed but small saplings suffer little or no damage attributable to voles. (6) Experiments with captive bank voles demonstrate marked differences between species of tree in their susceptibility to damage. (7) Tilia cordata is often severely damaged or destroyed. (8) Betula spp. suffer little or no damage. (9) Damage and destruction of small saplings is an important factor in the failure of regeneration of T. cordata in English woodlands because of the low density of seedlings and low frequency of large crops of fertile fruits.
The Australian continent is characterised by a harsh climate and highly weathered, nutrient-poor soils. Trees and shrubs in these stressful environmental conditions typically form ectomycorrhizae with a variety of fungi, many of which form hypogeous (underground) fruit-bodies. The total number of hypogeous fungi Australia-wide is unknown, although recent systematic studies in the far south-eastern corner of the country suggest that they may number well over a thousand. Similar surveys elswhere are urgently required to clarify the situation. The precise ecological role of many hypogeous fungi remains to be determined, although most presumably facilitate nutrient and water uptake on behalf of their mycorrhizal partners. Others may also protect their plant host from root pathogens. One key function of hypogeous fungi is the role their fruit-bodies play as a food resource for a large range of terrestrial mammals. For a few animals, hypogeous fungi form the single most important dietary item year-round, whereas for others they may only be of seasonal or supplementary value. The extent to which fungi form part of the diet of any mammal species is reflected in the various levels of adaptation toward acquiring, then processing and digesting these cryptic and nutritionally challenging foodstuffs.