The ectomycorrhizal fungi Tuber melanosporum Vittad. and Tuber aestivum Vittad. produce highly valuable truffles, but little is known about the soil fungal communities associated with these truffle species in places where they co-occur. Here, we compared soil fungal communities present in wild and planted truffle sites, in which T. melanosporum and T. aestivum coexist, in Mediterranean and temperate regions over three sampling seasons spanning from 2018 to 2019. We showed that soil fungal community composition and ectomycorrhizal species composition are driven by habitat type rather than climate regions. Also, we observed the influence of soil pH, organic matter content and C:N ratio structuring total and ectomycorrhizal fungal assemblages. Soil fungal communities in wild sites revealed more compositional variability than those of plantations. Greater soil fungal diversity was found in temperate compared to Mediterranean sites when considering all fungal guilds. Ectomycorrhizal diversity was significantly higher in wild sites compared to plantations. Greater mould abundance at wild sites than those on plantation was observed while tree species and seasonal effects were not significant predictors in fungal community structure. Our results suggested a strong influence of both ecosystem age and management on the fungal taxa composition in truffle habitats.
Recent global warming affects species compositions at an unprecedented rate. To predict climate-induced changes in species assemblages, a better understanding of the link between species occurrence and climate is needed. Macrofungal fruit body assemblages are correlated with the thermal environment at the European scale. However, it is still unknown whether macrofungal communities are also phylogenetically structured by thermal environments. Thermal environments are characterized by annual temperature means but also by intra-annual temperature variability (hereafter termed temperature seasonality), which are both considered in this study. Here, we used distribution data of 2882 species based on fruit body records across Europe to address two main questions: 1) are mushroom assemblages at the extremes of the mean (warm and cold) and seasonal (high intra-annual variability, i.e. continental) climate gradient phylogenetically more similar than expected (phylogenetic alpha diversity); 2) are mushroom assemblages, that are subject to different mean and seasonal temperature conditions, composed of different lineages (phylogenetic beta diversity). Our phylogenetic alpha diversity analysis shows that mushroom assemblages are phylogenetically structured by warm and cold environments, indicating that phylogenetically related species with similar traits thrive under more extreme conditions. In contrast, assemblages are phylogenetically more dissimilar (overdispersed) in temperature seasonal environments, indicating limiting similarity. Phylogenetic beta diversity was significantly correlated with mean and seasonal temperature differences, a response mainly driven by a few genera. Our results show that macrofungal assemblages are phylogenetically structured by temperature across Europe, suggesting phylogenetically constrained specialization towards temperature extremes. Predicted anthropogenic warming is likely to affect species composition and phylogenetic diversity with additional consequences for the carbon- and nutrient cycles.
Global warming is pushing populations outside their range of physiological tolerance. According to the environmental envelope framework, the most vulnerable populations occur near the climatic edge of their species' distributions. In contrast, populations from the climatic center of the species range should be relatively buffered against climate warming. We tested this latter prediction using a combination of linear mixed effects and machine learning algorithms on an extensive, citizen-scientist generated dataset on the fruitbody productivity of the Burgundy (aka summer) truffle (Tuber aestivum Vittad.), a keystone, ectomycorrhizal tree-symbiont occurring on a wide range of temperate climates. T. aestivum's fruitbody productivity was monitored at 3-week resolution over up to 8 continuous years at 20 sites distributed in the climatic center of its European distribution in southwest Germany and Switzerland. We found that T. aestivum fruitbody production is more sensitive to summer drought than would be expected from the breadth of its species' climatic niche. The monitored populations occurring nearly 5°C colder than the edge of their species' climatic distribution. However, interannual fruitbody productivity (truffle mass year-1 ) fell by a median loss of 22% for every 1°C increase in summer temperature over a site's 30-year mean. Among the most productive monitored populations, the temperature sensitivity was even higher, with single summer temperature anomalies of 3°C sufficient to stop fruitbody production altogether. Interannual truffle productivity was also related to the phenology of host trees, with ~22 g less truffle mass for each 1-day reduction in the length of the tree growing season. Increasing summer drought extremes are therefore likely to reduce fruiting among summer truffle populations throughout Central Europe. Our results suggest that European T. aestivum may be a mosaic of vulnerable populations, sensitive to climate-driven declines at lower thresholds than implied by its species distribution model.
Climate change exposes ecosystems to strong and rapid changes in their environmental boundary conditions mainly due to the altered temperature and precipitation patterns. It is still poorly understood how fast interlinked ecosystem processes respond to altered environmental conditions, if these responses occur gradually or suddenly when thresholds are exceeded, and if the patterns of the responses will reach a stable state. We conducted an irrigation experiment in the Pfynwald, Switzerland from 2003-2018. A naturally dry Scots pine (Pinus sylvestris L.) forest was irrigated with amounts that doubled natural precipitation, thus releasing the forest stand from water limitation. The aim of this study was to provide a quantitative understanding on how different traits and functions of individual trees and the whole ecosystem responded to increased water availability, and how the patterns and magnitudes of these responses developed over time. We found that the response magnitude, the temporal trajectory of responses, and the length of initial lag period prior to significant response largely varied across traits. We detected rapid and stronger responses from above-ground tree traits (e.g., tree-ring width, needle length, and crown transparency) compared to below-ground tree traits (e.g., fine root biomass). The altered above-ground traits during the initial years of irrigation increased the water demand and trees adjusted by increasing root biomass during the later years of irrigation, resulting in an increased survival rate of Scots pine trees in irrigated plots. The irrigation also stimulated ecosystem-level foliar decomposition rate, fungal fruit body biomass, and regeneration abundances of broadleaved tree species. However, irrigation did not promote the regeneration of Scots pine trees which are reported to be vulnerable to extreme droughts. Our results provide extensive evidence that treeand ecosystem-level responses were pervasive across a number of traits on long-term temporal scales. However, after reaching a peak, the magnitude of these responses either decreased or reached a new stable state, providing important insights into how resource alterations could change the system functioning and its boundary conditions.
OBJECTIVE:The aim of this study was to investigate the contralateral hearing of patients with sporadic vestibular schwannoma (VS).STUDY DESIGN:Retrospective cohort study.SETTING:Pure-tone audiograms of the contralateral ear from patients with a wait-and-scan strategy were compared to the ones who received therapy. Due to a possible bias caused by the therapy, hearing thresholds before and after radiotherapy or surgery were compared separately with the wait-and-scan group.METHODS:From 1979 to 2017, 508 patients with sporadic VS could be included in the study. Of these, 240 received regular controls in the sense of wait-and-scan, 72 underwent radiotherapy (63 audiograms before and 43 after radiotherapy), and 196 had a surgery (186 audiograms before and 146 after surgery). Age-normalized hearing thresholds of the contralateral ear from patients with a wait-and-scan strategy were compared to ones who received therapy. In addition, hearing thresholds were compared to norm values.RESULTS:There was no evidence for a difference in the contralateral hearing of patients with sporadic VS between the wait-and-scan and therapy groups. The mean difference of hearing thresholds in our sample to norm values was found to be larger for the high frequencies and more pronounced in male patients.CONCLUSION:There was no evidence for a difference in the contralateral hearing loss of patients with sporadic VS between the wait-and-scan and therapy groups. However, there was some indirect indication of poorer contralateral hearing in all patients with sporadic VS compared to normative values.
Climate change has been described as the main threat for the cultivation and growth of truffles, but hydroclimate variability and model uncertainty challenge regional projections and adaptation strategies of the emerging sector. Here, we conduct a literature review to define the main Périgord truffle growing regions around the world and use 20 global climate models to assess the impact of future trends and extremes in temperature, precipitation and soil moisture on truffle production rates and price levels in all cultivation regions in the Americas, Europe, South Africa, and Australasia. Climate model simulations project 2.3 million km2 of suitable land for truffle growth will experience 50% faster aridification than the rests of the global land surface, with significantly more heat waves between 2070 and 2099 CE. Overall, truffle production rates will decrease by ∼15%, while associated price levels will increase by ∼36%. At the same time, a predicted increase in summer precipitation and less intense warming over Australasia will likely alleviate water scarcity and support higher yields of more affordable truffles. Our findings are relevant for truffle farmers and businesses to adapt their irrigation systems and management strategies to future climate change.
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 5 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.
Burgundy truffles are heterothallic ascomycetes that grow in symbiosis with trees. Despite their esteemed belowground fruitbodies, the species' complex lifecycle is still not fully understood. Here, we present the genetic patterns in three natural Burgundy truffle populations based on genotyped fruitbodies, ascospore extracts and ectomycorrhizal root tips using microsatellites and the mating-type locus. Distinct genetic structures with high relatedness in close vicinity were found for females (forming the fruitbodies) and males (fertilizing partner as inferred from ascospore extracts), with high genotypic diversity and annual turnover of males, suggesting that ephemeral male mating partners are germinating ascospores from decaying fruitbodies. The presence of hermaphrodites and the interannual persistence of a few males suggest that persistent mycelia may sporadically also act as males. Only female or hermaphroditic individuals were detected on root tips. At one site, fruitbodies grew in a fairy ring formed by a large female individual that showed an outward growth rate of 30 cm per year, with the mycelium decaying within the ring and being fertilized by over 50 male individuals. While fairy ring structures have never been shown for truffles, the genetics of Burgundy truffle populations support a similar reproductive biology as those of other highly prized truffles.
Despite its status as a highly-prized and coveted fungi in gastronomy, many aspects of the subterranean life cycle of the Burgundy truffle (Tuber aestivum) are still unknown, because in situ observations of the formation and maturation of truffle fruitbodies remain difficult. Here, we adopted a suite of archaeological fine-scale excavating techniques to provide unique spatiotemporal snapshots of Burgundy truffle growth at three sites in southern Germany. We also recorded the relative position, fresh weight, maturity level and genotype composition of all excavated fruitbodies. Varying by a factor of thousand, the fresh weight of 73 truffle ranged from 0.1 to 103.2 g, with individual maturity levels likely representing different life cycle stages from completely unripe to fully ripe and even decaying. While only a slightly positive relationship between fruitbody weight and maturity level was found, our results suggest that genetically distinct specimens can exhibit different life cycle stages at the same period of time and under the same environmental conditions. We therefore argue that truffles are likely able to grow, mature and ripe simultaneously between early summer and late winter of the following year. Our case study should encourage further eco-archaeological truffle excavations under different biogeographic settings and at different seasons of the year to gain deeper insights into the fungi's subterranean ecology. The expected cross-disciplinary findings will help truffle hunters and farmers to improve their harvest practices and management strategies.
Many plant and animal species are changing their latitudinal and/or altitudinal distributions in response to climate change, but whether fungi show similar changes is largely unknown. Here, we use historical fungal fruit body records from the European Alps to assess altitudinal changes in fungal fruiting between 1960 and 2010. We observe that many fungal species are fruiting at significantly higher elevations in 2010 compared to 1960, and especially so among soil-dwelling fungi. Wood-decay fungi, being dependent on the presence of one or a few host trees, show a slower response. Species growing at higher elevations changed their altitudinal fruiting patterns significantly more than lowland species. Environmental changes in high altitudes may lead to proportionally stronger responses, since high-altitude species live closer to their physiological limit. These aboveground changes in fruiting patterns probably mirror corresponding shifts in below-ground fungal communities, suggesting parallel shifts in important ecosystem functions.
The sudden interruption of recurring larch budmoth (LBM; Zeiraphera diniana or griseana Gn.) outbreaks across the European Alps after 1982 was surprising, because populations had regularly oscillated every 8-9 years for the past 1200 years or more. Although ecophysiological evidence was limited and underlying processes remained uncertain, climate change has been indicated as a possible driver of this disruption. An unexpected, recent return of LBM population peaks in 2017 and 2018 provides insight into this insect's climate sensitivity. Here, we combine meteorological and dendrochronological data to explore the influence of temperature variation and atmospheric circulation on cyclic LBM outbreaks since the early 1950s. Anomalous cold European winters, associated with a persistent negative phase of the North Atlantic Oscillation, coincide with four consecutive epidemics between 1953 and 1982, and any of three warming-induced mechanisms could explain the system's failure thereafter: (1) high egg mortality, (2) asynchrony between egg hatch and foliage growth, and (3) upward shifts of outbreak epicentres. In demonstrating that LBM populations continued to oscillate every 8-9 years at sub-outbreak levels, this study emphasizes the relevance of winter temperatures on trophic interactions between insects and their host trees, as well as the importance of separating natural from anthropogenic climate forcing on population behaviour.
Truffles are ectomycorrhizal fungi of which several species can be commercially produced in man-made plan-tations using trees inoculated with their mycelia. The production in tree plantations is meant to increase the availability of economically valued ascocarps on the market and, in the same time preserve natural habitats from an excessive pressure of truffle hunters, as well as limit the damage that they may face due to the inadequate management of truffle-producing regions. Even though plantations of summer truffle (Tuber aestivum Vittad.) are the most ubiquitous in France and Italy, the Jaszsag region in Hungary has been recently recognized as one of the most productive areas in Europe. Forestry practice in this region often assumes the renovation of autochthonous tree stands by massive sowing of the tree seeds. One of these plantations of oaks (Quercus robur and Q. cerris), spontaneously colonized without artificial inoculation, appeared to produce the highest officially reported amounts of summer truffles in Europe. Therefore, the managing forestry company decided to apply practice that aimed at maintenance of high truffle production. Assuming that climatic and vegetation factors have no impact on ascocarp production within the stand, the plantation provided perfect experimental setup for investigating the influence of very localised soil properties and terrain morphology on truffle abundance. Therefore, in this contribution selected soil properties have been investigated in the entire plantation using specifically designed protocols to characterize the site and find out if the spatial variation in the truffle production can be explained by short-distance differences in soil properties. In the Chernozem soil type that dominated the entire forest stand, soil organic matter (SOM), soluble nitrogen (TN) and properties influenced by SOM and biological activity were positively correlated with high ascocarp production, whereas increased soil aggregate size and clay content was negatively correlated with productivity. The spatial distribution of these parameters appeared strongly related to ascocarp abundance distribution. Chernozem seems to be an ideal type of soil for Tuber aestivum ascocarp production, but terrain morphology and soil properties spatial pattern, which may have been historically influenced by fluvial and aeolian processes, can significantly influence the rate of production. In the case of non wood products such as truffles, forest management will necessarily have to consider the conditions of the soil environment that, influencing the presence of the truffle species, can make their production interesting in terms of income for the forest owner.
Despite being one of the most expensive gourmet foods, it remains unclear if the iconic White Truffle (Tuber magnatum Pico; hereinafter WT) accumulates radioactivity at harmful levels comparable to other fungal species. Here, we measure the active radiocaesium-137 concentration (137Cs) in ten hypogeous WT fruitbodies from southern Hungary, and the soils in which they were growing. All WTs reveal non-significant 137Cs values, thus providing an 'all clear' for WT hunters in the species' northernmost habitats, where corresponding soil samples occasionally exhibit slight 137Cs concentrations. Our results are particularly relevant in the light of a rapidly increasing global demand for WTs and their subsequent trading extent and price inflation, because up to 600 kg of fresh fruitbodies are harvested each year in southern Hungary. Moreover, some of Europe's forest ecosystems, in which mushroom picking is common practise, are still contaminated with 137Cs from the Chernobyl fallout more than 30 years ago, posing a serious threat to human health.
The unprecedented price inflation of Black truffles, recently exceeding 5000 Euro kg(-1) (in Zurich), is a combined result of increasing global demands and decreasing Mediterranean harvests. Since the effects of long-term irrigation and climate variation on symbiotic fungus-host interaction and the development of belowground microbes are poorly understood, the establishment and maintenance of truffle plantations remains a risky venture. Using 49 years of continuous harvest and climate data from Spain, France and Italy, we demonstrate how truffle production rates, between November and March, significantly rely on previous June-August precipitation totals, whereas too much autumnal rainfall affects the subsequent winter harvest negatively. Despite a complex climate-host-fungus relationship, our findings show that southern European truffle yields can be predicted at highest probability (r = 0.78, t-stat = 5.645, prob = 0.000 01). Moreover, we demonstrate the reliability of national truffle inventories since 1970, and question the timing and dose of many of the currently operating irrigation systems. Finally, our results suggest that Black truffle mycorrhizal colonization of host fine roots, the sexualisation of mycelium, and the formation of peridium are strongly controlled by natural summer rainfall. Recognising the drought-vulnerability of southern Europe's rapidly growing truffle sector, we encourage a stronger liaison between farmers, politicians and scientists to maintain ecological and economic sustainability under predicted climate change in the Mediterranean basin.
Truffle fungi are well known for their enticing aromas partially emitted by microbes colonizing truffle fruiting bodies. The identity and diversity of these microbes remain poorly investigated, because few studies have determined truffle-associated bacterial communities while considering only a small number of fruiting bodies. Hence, the factors driving the assembly of truffle microbiomes are yet to be elucidated. Here we investigated the bacterial community structure of more than 50 fruiting bodies of the black truffle Tuber aestivum in one French and one Swiss orchard using 16S rRNA gene amplicon high-throughput sequencing. Bacterial communities from truffles collected in both orchards shared their main dominant taxa: while 60% of fruiting bodies were dominated by α-Proteobacteria, in some cases the β-Proteobacteria or the Sphingobacteriia classes were the most abundant, suggesting that specific factors (i.e., truffle maturation and soil properties) shape differently truffle-associated microbiomes. We further attempted to assess the influence in truffle microbiome variation of factors related to collection season, truffle mating type, degree of maturation, and location within the truffle orchards. These factors had differential effects between the two truffle orchards, with season being the strongest predictor of community variation in the French orchard, and spatial location in the Swiss one. Surprisingly, genotype and fruiting body maturation did not have a significant effect on microbial community composition. In summary, our results show, regardless of the geographical location considered, the existence of heterogeneous bacterial communities within T. aestivum fruiting bodies that are dominated by three bacterial classes. They also indicate that factors shaping microbial communities within truffle fruiting bodies differ across local conditions.
Although it is logical to think that mycorrhizal mushroom production should be somehow related to the growth of the trees from which the fungi obtain carbohydrates, little is known about how mushroom yield patterns are related to tree performance. In this study, we delved into the understanding of the relationships between aboveground fungal productivity, tree radial growth patterns and climatic conditions across three latitudinally different bioclimatic regions encompassing Mediterranean, temperate and boreal forest ecosystems in Europe. For this purpose, we used a large assemblage of long-term data of weekly or biweekly mushroom yield monitoring in Spain, Switzerland and Finland. We analysed the relationships between annual mushroom yield (considering both biomass and number of sporocarps per unit area), tree ring features (tree ring, earlywood and latewood widths), and meteorological conditions (i.e. precipitation and temperature of summer and autumn) from different study sites and forest ecosystems, using both standard and partial correlations. Moreover, we fitted predictive models to estimate mushroom yield from mycorrhizal and saprotrophic fungal guilds based on climatic and dendrochronological variables. Significant synchronies between mushroom yield and climatic and dendrochronological variables were mostly found in drier Mediterranean sites, while few or no significant correlations were found in the boreal and temperate regions. We observed positive correlations between latewood growth and mycorrhizal mushroom biomass only in some Mediterranean sites, this relationship being mainly mediated by summer and autumn precipitation. Under more water-limited conditions, both the seasonal wood production and the mushroom yield are more sensitive to precipitation events, resulting in higher synchrony between both variables. This comparative study across diverse European forest biomes and types provides new insights into the relationship between mushroom productivity, tree growth and weather conditions.
PREMISE OF THE STUDY:Fungal diversity (richness) trends at large scales are in urgent need of investigation, especially through novel situations that combine long-term observational with environmental and remotely sensed open-source data.METHODS:We modeled fungal richness, with collections-based records of saprotrophic (decaying) and ectomycorrhizal (plant mutualistic) fungi, using an array of environmental variables across geographical gradients from northern to central Europe. Temporal differences in covariables granted insight into the impacts of the shorter- versus longer-term environment on fungal richness.RESULTS:Fungal richness varied significantly across different land-use types, with highest richness in forests and lowest in urban areas. Latitudinal trends supported a unimodal pattern in diversity across Europe. Temperature, both annual mean and range, was positively correlated with richness, indicating the importance of seasonality in increasing richness amounts. Precipitation seasonality notably affected saprotrophic fungal diversity (a unimodal relationship), as did daily precipitation of the collection day (negatively correlated). Ectomycorrhizal fungal richness differed from that of saprotrophs by being positively associated with tree species richness.DISCUSSION:Our results demonstrate that fungal richness is strongly correlated with land use and climate conditions, especially concerning seasonality, and that ongoing global change processes will affect fungal richness patterns at large scales.
Thermal melanism theory states that dark-colored ectotherm organisms are at an advantage at low temperature due to increased warming. This theory is generally supported for ectotherm animals, however, the function of colors in the fungal kingdom is largely unknown. Here, we test whether the color lightness of mushroom assemblages is related to climate using a dataset of 3.2 million observations of 3,054 species across Europe. Consistent with the thermal melanism theory, mushroom assemblages are significantly darker in areas with cold climates. We further show differences in color phenotype between fungal lifestyles and a lifestyle differentiated response to seasonality. These results indicate a more complex ecological role of mushroom colors and suggest functions beyond thermal adaption. Because fungi play a crucial role in terrestrial carbon and nutrient cycles, understanding the links between the thermal environment, functional coloration and species' geographical distributions will be critical in predicting ecosystem responses to global warming.