Predicting species‐specific responses of fungi to climatic variation using historical records

Although striking changes have been documented in plant and animal phenology over the past century, less is known about how the fungal kingdom's phenology has been changing. A few recent studies have documented changes in fungal fruiting in Europe in the last few decades, but the geographic and taxonomic extent of these changes, the mechanisms behind these changes, and their relationships to climate are not well understood. Here, we analyzed herbarium data of 274 species of fungi from Michigan to test the hypotheses that fruiting times of fungi depend on annual climate and that responses depend on taxonomic and functional groups. We show that the fungal community overall fruits later in warmer and drier years, which has led to a shift toward later fruiting dates for autumn‐fruiting species, consistent with existing evidence. However, we also show that these effects are highly variable among species and are partly explained by basic life‐history characteristics. Resulting differences in climate sensitivities are expected to affect community structure as climate changes. This study provides a unique picture of the climate dependence of fungal phenology in North America and an approach for quantifying how individual species and broader fungal communities will respond to ongoing climate change.     

Unraveling environmental drivers of a recent increase in Swiss fungi fruiting

Disentangling biotic and abiotic drivers of wild mushroom fruiting is fraught with difficulties because mycelial growth is hidden belowground, symbiotic and saprotrophic supply strategies may interact, and myco‐ecological observations are often either discontinuous or too short. Here, we compiled and analyzed 115 417 weekly fungal fruit body counts from permanent Swiss inventories between 1975 and 2006. Mushroom fruiting exhibited an average autumnal delay of 12 days after 1991 compared with before, the annual number of fruit bodies increased from 1801 to 5414 and the mean species richness doubled from 10 to 20. Intra‐ and interannual coherency of symbiotic and saprotrophic mushroom fruiting, together with little agreement between mycorrhizal yield and tree growth suggests direct climate controls on fruit body formation of both nutritional modes. Our results contradict a previously reported declining of mushroom harvests and propose rethinking the conceptual role of symbiotic pathways in fungi‐host interaction. Moreover, this conceptual advancement may foster new cross‐disciplinary research avenues, and stimulate questions about possible amplifications of the global carbon cycle, as enhanced fungal production in moist mid‐latitude forests rises carbon cycling and thus increases greenhouse gas exchanges between terrestrial ecosystems and the atmosphere.     

Mushroom's spore size and time of fruiting are strongly related: is moisture important?

Most basidiomycete fungi produce annual short-lived sexual fruit bodies from which billions of microscopic spores are spread into the air during a short time period. However, little is known about the selective forces that have resulted in some species fruiting early and others later in the fruiting season. This study of relationships between morphological and ecological characteristics, climate factors and time of fruiting are based upon thorough statistical analyses of 66 520 mapped records from Norway, representing 271 species of autumnal fruiting mushroom species. We found a strong relationship between spore size and time of fruiting; on average, a doubling of spore size (volume) corresponded to 3 days earlier fruiting. Small-spored species dominate in the oceanic parts of Norway, whereas large-spored species are typical of more continental parts. In separate analyses, significant relationships were observed between spore size and climate factors. We hypothesize that these relationships are owing to water balance optimization, driven by water storage in spores as a critical factor for successful germination of primary mycelia in the drier micro-environments found earlier in the fruiting season and/or in continental climates.     

Drought-induced changes in the phenology,productivity and diversity of Spanish fungi

Mushrooms are amongst the most important of non-timber forest products, with growing economic value in many rural areas of the Mediterranean region. At the same time, the effects of climate variability on fungal ecology and productivity are insufficiently understood, because the belowground life cycle of fungi is mediated in many different ways and observational field surveys at the community level are generally too short. Here, we assess records of 48, 348 mycorrhizal and saprotrophic fungal fruit bodies that were recorded at weekly intervals between 1995 and 2013 in Pinar Grande, the largest Spanish Scots pine forest. Autumnal fruiting was delayed by one week after 2004 compared with the period before, the mean annual number of sporocarps dropped from 2 880 to 2 045, and mean species richness declined from 55 to 51. Trends in the phenology and productivity of Boletus edulis and Lactarius spp., the most profitable edible species, were associated with decreasing Jul.–Sep. precipitation totals, whereas the mean fruit body weight of B. edulis significantly increased from 71 to 123 g (pre and post 2004). In tandem with declining Spanish tree growth and truffle harvest since the 1970s, this study reveals a strong dependency of drought-prone Iberian forest ecosystem productivity on hydroclimatic variability. In light of a predicted drier Mediterranean climate, our results further emphasize the importance of long and well-replicated field inventories at high spatiotemporal resolution for informing forest service and management strategies, as well as gastronomy and tourist industries.     

Topography-specific emergence of fungal fruiting bodies in warm temperate evergreen broad-leaved forests on Yakushima Island,Japan

We conducted line route censuses of fungal fruiting bodies from August to September in 2005 and 2006 along ridges and valleys and compared the differences in the encounter rates of fungal fruiting bodies (= fruiting bodies seen per census kilometer) between types of topography and between fungal functional groups (i.e., ectomycorrhizal and saprobic fungi) in warm temperate evergreen broad-leaved forests on Yakushima Island, Japan. We found 251 fungal fruiting bodies (26 families, 50 genera, and 65 species) in total, including 51 bodies from Tricholomataceae, 41 from Russulaceae, 25 from Boletaceae, and 19 from Amanitaceae. The encounter rate of ectomycorrhizal fungi was greater at the ridge route (26.7 unit/km) than at the valley route (8.7 unit/km) and that of saprobic fungi was greater at the valley route (25.0 unit/km) than at the ridge route (12.5 unit/km). In addition, we conducted 7-year intermittent sampling and identified 40 families, 96 genera, and 142 species. The topography-specific emergence pattern of the intermittent sampling method was similar to that of the line census method. The fungal species composition in this study was possibly affected by a topographic gradient for both fungal functional groups through soil moisture, nutrient availability, and host tree distribution.     

Increased evapotranspiration demand in a Mediterranean climate might cause a decline in fungal yields under global warming

Wild fungi play a critical role in forest ecosystems, and its recollection is a relevant economic activity. Understanding fungal response to climate is necessary in order to predict future fungal production in Mediterranean forests under climate change scenarios. We used a 15‐year data set to model the relationship between climate and epigeous fungal abundance and productivity, for mycorrhizal and saprotrophic guilds in a Mediterranean pine forest. The obtained models were used to predict fungal productivity for the 2021–2080 period by means of regional climate change models. Simple models based on early spring temperature and summer–autumn rainfall could provide accurate estimates for fungal abundance and productivity. Models including rainfall and climatic water balance showed similar results and explanatory power for the analyzed 15‐year period. However, their predictions for the 2021–2080 period diverged. Rainfall‐based models predicted a maintenance of fungal yield, whereas water balance‐based models predicted a steady decrease of fungal productivity under a global warming scenario. Under Mediterranean conditions fungi responded to weather conditions in two distinct periods: early spring and late summer–autumn, suggesting a bimodal pattern of growth. Saprotrophic and mycorrhizal fungi showed differences in the climatic control. Increased atmospheric evaporative demand due to global warming might lead to a drop in fungal yields during the 21st century.     

Combining high-throughput sequencing with fruit body surveys reveals contrasting life-history strategies in fungi

Before the recent revolution in molecular biology, field studies on fungal communities were mostly confined to fruit bodies, whereas mycelial interactions were studied in the laboratory. Here we combine high-throughput sequencing with a fruit body inventory to study simultaneously mycelial and fruit body occurrences in a community of fungi inhabiting dead wood of Norway spruce. We studied mycelial occurrence by extracting DNA from wood samples followed by 454-sequencing of the ITS1 and ITS2 regions and an automated procedure for species identification. In total, we detected 198 species as mycelia and 137 species as fruit bodies. The correlation between mycelial and fruit body occurrences was high for the majority of the species, suggesting that high-throughput sequencing can successfully characterize the dominating fungal communities, despite possible biases related to sampling, PCR, sequencing and molecular identification. We used the fruit body and molecular data to test hypothesized links between life history and population dynamic parameters. We show that the species that have on average a high mycelial abundance also have a high fruiting rate and produce large fruit bodies, leading to a positive feedback loop in their population dynamics. Earlier studies have shown that species with specialized resource requirements are rarely seen fruiting, for which reason they are often classified as red-listed. We show with the help of high-throughput sequencing that some of these species are more abundant as mycelium in wood than what could be expected from their occurrence as fruit bodies.     

Fine‐scale spatiotemporal dynamics of fungal fruiting: prevalence,amplitude, range and continuity

Despite the critical importance of fungi as symbionts with plants, resources for animals, and drivers of ecosystem function, the spatiotemporal distributions of fungi remain poorly understood. The belowground life cycle of fungi makes it difficult to assess spatial patterns and dynamic processes even with recent molecular techniques. Here we offer an explicit spatiotemporal Bayesian inference of the drivers behind spatial distributions from investigation of a Swiss inventory of fungal fruit bodies. The unique inventory includes three temperate forest sites in which a total of 73 952 fungal fruit bodies were recorded systematically in a spatially explicit design between 1992 and 2006. Our motivation is to understand how broad‐scale climate factors may influence spatiotemporal dynamics of fungal fruiting within forests, and if any such effects vary between two functional groups, ectomycorrhizal (ECM) and saprotrophic fungi. For both groups we asked: 1) how consistent are the locations of fruiting patches, the sizes of patches, the quantities of fruit bodies, and of prevalence (occupancy)? 2) Do the annual spatial characteristics of fungal fruiting change systematically over time? 3) Are spatial characteristics of fungal fruiting driven by climatic variation? We found high inter‐annual continuity in fruiting for both functional groups. The saprotrophic species were characterised by small patches with variable fruit body counts. In contrast, ECM species were present in larger, but more distinctly delimited patches. The spatial characteristics of the fungal community were only indirectly influenced by climate. However, climate variability influenced overall yields and prevalence, which again links to spatial structure of fruit bodies. Both yield and prevalence were correlated with the amplitudes of occurrence and of fruit body counts, but only prevalence influenced the spatial range. Summarizing, climatic variability affects forest‐stand fungal distributions via its influence on yield (amount) and prevalence (occupancy), whereas fungal life‐history strategies dictate fine‐scale spatial characteristics.     

Impact of climate change on plant phenology in Mediterranean ecosystems

Plant phenology is strongly controlled by climate and has consequently become one of the most reliable bioindicators of ongoing climate change. We used a dataset of more than 200 000 records for six phenological events of 29 perennial plant species monitored from 1943 to 2003 for a comprehensive assessment of plant phenological responses to climate change in the Mediterranean region. Temperature, precipitation and North Atlantic Oscillation (NAO) were studied together during a complete annual cycle before phenological events to determine their relative importance and potential seasonal carry‐over effects. Warm and dry springs under a positive phase of NAO advance flowering, leaf unfolding and fruiting dates and lengthen the growing season. Spatial variability of dates (range among sites) was also reduced during warm and dry years, especially for spring events. Climate during previous weeks to phenophases occurrence had the greatest impact on plants, although all events were also affected by climate conditions several months before. Immediate along with delayed climate effects suggest dual triggers in plant phenology. Climatic models accounted for more than 80% of variability in flowering and leaf unfolding dates, and in length of the growing season, but for lower proportions in fruiting and leaf falling. Most part of year‐to‐year changes in dates was accounted for temperature, while precipitation and NAO accounted for <10% of dates' variability. In the case of flowering, insect‐pollinated species were better modelled by climate than wind‐pollinated species. Differences in temporal responses of plant phenology to recent climate change are due to differences in the sensitivity to climate among events and species. Spring events are changing more than autumn events as they are more sensitive to climate and are also undergoing the greatest alterations of climate relative to other seasons. In conclusion, climate change has shifted plant phenology in the Mediterranean region.     

Trait‐dependent distributional shifts in fruiting of common British fungi

Despite the dramatic phenological responses of fungal fruiting to recent climate warming, it is unknown whether spatial distributions of fungi have changed and to what extent such changes are influenced by fungal traits, such as ectomycorrhizal (ECM) or saprotrophic lifestyles, spore characteristics, or fruit body size. Our overall aim was to understand how climate and fungal traits determine whether and how species‐specific fungal fruit body abundances have shifted across latitudes over time, using the UK national database of fruiting records. The data employed were recorded over 45 yr (1970–2014), and include 853 278 records of Agaricales, Boletales and Russulales, though we focus only on the most common species (with more than 3000 records each). The georeferenced observations were analysed by a Bayesian inference as a Gaussian additive model with a specification following a joint species distribution model. We used an offset, random contributions and fixed effects to isolate different potential biases from the trait‐specific interactions with latitude/climate and time. Our main aim was assessed by examination of the three‐way‐interaction of trait, predictor (latitude or climate) and time. The results show a strong trait‐specific shift in latitudinal abundance through time, as ECM species have become more abundant relative to saprotrophic species in the north. Along precipitation gradients, phenology was important, in that species with shorter fruiting seasons have declined markedly in abundance in oceanic regions, whereas species with longer seasons have become relatively more common overall. These changes in fruit body distributions are correlated with temperature and rainfall, which act directly on both saprotrophic and ECM fungi, and also indirectly on ECM fungi, through altered photosynthate allocation from their hosts. If these distributional changes reflect fungal activity, there will be important consequences for the responses of forest ecosystems to changing climate, through effects on primary production and nutrient cycling.     

Rainfall homogenizes while fruiting increases diversity of spore deposition in Mediterranean conditions

There is a lack of knowledge regarding the main factors modulating fungal spore deposition in forest ecosystems. We have described the local spatio-temporal dynamics of fungal spore deposition along a single fruiting season and its relation with fruit body emergence and rainfall events. Passive spore traps were weekly sampled during autumn and analysed by metabarcoding of the ITS2 region in combination with qPCR. There were larger compositional changes of deposited spores across sampling weeks than amongst sampling plots. Spore diversity and abundance correlated with mushroom emergence and weekly rainfall. Spore compositional changes were related to rainfall, with lower spatial compositional heterogeneity across plots during weeks with higher rainfall. Soil saprotrophs, and amongst them, puffball species, showed the strongest positive correlation with rainfall across fungal guilds. We saw high fine-scale temporal changes of deposited spores, and both mushroom emergence and rainfall may be important factors driving airborne spore deposition.     

Temperature affects the timing and duration of fungal fruiting patterns across major terrestrial biomes

The Earth's ecosystems are affected by a complex interplay of biotic and abiotic factors. While global temperatures increase, associated changes in the fruiting behaviour of fungi remain unknown. Here, we analyse 6.1 million fungal fruit body (mushroom) records and show that the major terrestrial biomes exhibit similarities and differences in fruiting events. We observed one main fruiting peak in most years across all biomes. However, in boreal and temperate biomes, there was a substantial number of years with a second peak, indicating spring and autumn fruiting. Distinct fruiting peaks are spatially synchronized in boreal and temperate biomes, but less defined and longer in the humid tropics. The timing and duration of fungal fruiting were significantly related to temperature mean and variability. Temperature-dependent aboveground fungal fruiting behaviour, which is arguably also representative of belowground processes, suggests that the observed biome-specific differences in fungal phenology will change in space and time when global temperatures continue to increase.     

Long-term temporal changes of plant phenology in the Western Mediterranean

Plants are altering their life cycles in response to current climatic change around the globe. More than 200 000 records for six phenological events (leaf unfolding, flowering, fruit ripening, fruit harvesting, leaf falling and growing season) of 29 perennial species for the period 1943–2003 recorded throughout Spain provide the longest temporal and the broadest spatial assessment of plant phenology changes in the Mediterranean region. The overwhelming majority of the 118 studied phenophases shifted their dates in recent decades. Such changes differed among phenological events. Leaf unfolding, flowering and fruiting are markedly advancing (?0.48, ?0.59 and ?0.32 days yr^?1, respectively), but only since the mid‐1970s. Anemophilous have advanced more days their flowering than entomophilous. However, some species have delayed and others have advanced their leaf falling dates and as a result only a weak shift was observed in this event for the whole of the studied species (+0.12 days yr^?1). The growing season lengthened by 18 days, which implies an increase of 8% in the life of annual leaves. Such an increase was achieved mainly through the advance of leaf unfolding dates in the spring, one of the most productive times of year for vegetation in the Mediterranean. Shifts in the plant calendar were accompanied as well by long‐term changes in the range of onset dates in 39% of studied phenophases. Leaf unfolding, flowering and growing season tended to reduce spatial variability, reflecting a faster and more synchronized onset (or duration) of phenophases across the study area. Changes in spatial variability may aggravate calendar mismatching with other trophic levels resulting from changes in dates. Because temporal responses differed markedly among species, calendar guilds of plants have changed, which suggests alterations of interspecific relationships in plant communities from Mediterranean ecosystems.     

Detailed information on fruiting phenology provides new insights on wood-inhabiting fungal detection

Fruiting phenology traits may have a large effect on the detection of fungal species. Detailed studies considering these biologically important traits are, however, surprisingly scarce. We conducted a rigorous fruit body monitoring of wood-inhabiting fungal occurrences over one fruiting season. Taxon-specific longevity of the fruiting was different between different morphological groups. This was mainly due to agaric fruiting being shorter than other groups. Different number and timing of surveys are needed to detect the majority of the fruiting taxa of different wood-inhabiting fungal groups.     

Host plants and edaphic factors influence the distribution and diversity of ectomycorrhizal fungal fruiting bodies within rainforests from Tshopo,Democratic Republic of the Congo

Ectomycorrhizal fungi constitute an important component of forest ecosystems that enhances plant nutrition and resistance against stresses. Diversity of ectomycorrhizal (EcM) fungi is, however, affected by host plant diversity and soil heterogeneity. This study provides information about the influence of host plants and soil resources on the diversity of ectomycorrhizal fungal fruiting bodies from rainforests of the Democratic Republic of the Congo. Based on the presence of fungal fruiting bodies, significant differences in the number of ectomycorrhizal fungi species existed between forest stand types (p < 0.001). The most ectomycorrhizal species‐rich forest was the Gilbertiodendron dewevrei‐dominated forest (61 species). Of all 93 species of ectomycorrhizal fungi, 19 demonstrated a significant indicator value for particular forest stand types. Of all analysed edaphic factors, the percentage of silt particles was the most important parameter influencing EcM fungi host plant tree distribution. Both host trees and edaphic factors strongly affected the distribution and diversity of EcM fungi. EcM fungi may have developed differently their ability to successfully colonise root systems in relation to the availability of nutrients.     

Phenological variation in fruit characteristics in vertebrate-dispersed plants

Summary We investigated inter-specific variation in fruit characteristics — fruit size, seed number per fruit, seed weight, nutritional content, fruit persistence, and fruit synchronization — in relation to flowering and fruiting phenology in 34 species of fleshy fruited plants. Except for aspects of fruit synchrony and persistence, the results in general were inconsistent with previous suggestions about adaptive variation in phenologically related fruit traits. The main results were as follows: (1) Late flowering, late fruiting, lengthy development time from flower to fruit, and highly persistent fruits constitute a complex of correlated characteristics among the species. (2) Synchronization of fruiting within individuals increased from early ripening fruits to late ripening fruits. Fruiting synchrony was more pronounced in species with a small crop size than in species with a large fruit crop, whereas synchrony was not significantly related to flowering synchronization, nor to life form. (3) Nitrogen and carbohydrate content of fruit pulp did not vary in relation to phenology, whereas lipid content decreased from early to late ripening fruits. (4) No seasonal trends were found for variation in seed size or seed number per fruit. (5) Interactions with flowering phenology and developmental constraints are important in phenological fruiting patterns. Temporal variation in start of fruiting was partly (36%) explained by variation in flowering time. Seed weight variation explained 17% of variation in development time from flower to fruit. (6) Despite constraints from flowering and seed development, some adaptive adjustment in fruiting phenology is likely to be allowed for among the investigated species. Such an adaptive variation in fruiting phenology was suggested by intra-generic comparisons of Prunus and Vaccinium species.     

ECOLOGICAL CORRELATES OF REPRODUCTIVE TRAITS OF MEXICAN RAIN FOREST TREES

Sexual systems of 139 tree species from a tropical rain forest at Los Tuxtlas, Mexico were investigated to: 1) estimate the relative proportions of hermaphroditic, monoecious, and dioecious species; 2) describe flowers, fruits, and seeds in terms of size and weight; 3) describe flowering and fruiting phenology; and 4) correlate sexuality to pollination and dispersal syndromes, and the successional status occupied in the forest. Hermaphroditism occurred in 63% of the species, monoecism in 9%, and dioecy in 27%. Nondioecious species had larger flowers, but dioecious species had more seeds per fruit. The dioecious condition was associated with small flowers pollinated with unspecialized insects and fleshy fruits dispersed by animals at both species and generic levels. Reproductive traits were more correlated among nondioecious species than dioecious species. Pioneer species had more seeds per fruit, and longer flowering and fruiting periods, but persistent species produced heavier seeds and fruits. Flower and fruit morphological traits, sexual systems, and tree guilds are related in a comprehensive way, and a flow model based on data from this study is presented.     

Fruiting patterns of macrofungi in tropical and temperate land use types in Yunnan Province,China

Despite the important contribution of fungi to forest health, biomass turnover and carbon cycling, little is known about the factors that influence fungal phenology. Therefore, in order to further our understanding on how macrofungal fruiting patterns change along a gradient from temperate to tropical climate zones, we investigated the phenological patterns of macrofungal fruiting at five sites along a combined altitudinal and latitudinal gradient in SW China and NW Laos, ranging from temperate to tropical climates. Observations were conducted in the dominant land use types at these study sites: mixed forest (all sites), coniferous forest (temperate sites) and grassland (temperate sites). In total, 2866 specimens were collected, belonging to 791 morpho species, 162 genera, and 71 families. At the site level, the fruiting of ectomycorrhizal (EcMF) and saprotrophic fungi (SapF) occurred at the same time among all land use types. The fruiting season of fungi in the tropical sites began earlier and ended later compared to that of fungi in the temperate sites, which we attribute mainly to the higher temperature and more abundant rainfall of the tropical areas. EcMF taxa richness in temperate forests (both coniferous and mixed forest) showed a distinct peak at the end of the rainy season in August and September, while no significant peak was observed for SapF taxa richness. Neither functional fungal groups showed significant seasonal fluctuations in tropical areas. The temporal turnover of fungal fruiting significantly increased with the shift from tropical to temperate forests along the elevation gradient. In the grasslands, macrofungal abundance was less than 22% of that of corresponding forest sites, and taxa richness was 42% of that of corresponding forest sites. Fungal fruiting showed no significant fluctuations across the rainy season. This work represents a case study carried out over one year, and further measurements will be needed to test if these results hold true in the longer term.     

Reproductive phenology of two Mimusops species in relation to climate,tree diameter and canopy position in Benin (West Africa)

Assessing species phenology provides useful understanding about their autecology, to contribute to management strategies. We monitored reproductive phenology of Mimusops andongensis and Mimusops kummel, and its relationship with climate, tree diameter and canopy position. We sampled trees in six diameter classes and noted their canopy position. For both species flowering began in the dry season through to the rainy season, but peaked in the dry season, whilst fruiting occurred in the rainy season and peaked during the most humid period. Flowering was positively correlated with temperature. Conversely, fruiting was negatively correlated with temperature and positively with rainfall, only in the Guineo‐Sudanian zone. For M. andongensis, flowering and fruiting prevalences were positively linked to stem diameter, while only flowering was significantly related to canopy position. For M. kummel, the relationship with stem diameter was significant for flowering prevalence only and in the Guineo‐Sudanian zone. Results suggest that phylogenetic membership is an important factor restricting Mimusops species phenology. Flowering and fruiting of both species are influenced by climate, and consequently climate change might shift their phenological patterns. Long‐term investigations, considering flowering and fruiting abortion, will help to better understand the species phenology and perhaps predict demographic dynamics.