Wood-inhabiting fungal communities : Opportunities for integration of empirical and theoretical community ecology

Publisher Copyright: © 2021 The AuthorThe interest in studying wood-inhabiting fungal communities has grown in recent years. This interest has mainly been motivated by the important roles of wood-inhabiting fungi in ecosystem functioning (e.g. nutrient cycling) and conservation biology (e.g. their sensitivity to forest management). In this paper, I argue that another important, but yet largely unexplored motivation for studying wood-inhabiting fungal communities, is their potential to advance fundamental community ecology. One major advantage of wood-inhabiting fungi as model systems is that they are organized as spatially well-defined metacommunities, thus conforming to the assumptions of many theoretical frameworks. Another major advantage is that they allow observations and manipulations over large numbers of local communities (habitat patches). After reviewing recent approaches in theoretical community ecology, I discuss how past empirical studies on wood-inhabiting fungal communities relate to community assembly processes, and provide future research directions on how the still unstudied assembly processes could be tackled using wood-inhabiting fungi as a model system.Peer reviewe

What can observational data reveal about metacommunity processes?

A key challenge for community ecology is to understand to what extent observational data can be used to infer the underlying community assembly processes. As different processes can lead to similar or even identical patterns, statistical analyses of non-manipulative observational data never yield undisputable causal inference on the underlying processes. Still, most empirical studies in community ecology are based on observational data, and hence understanding under which circumstances such data can shed light on assembly processes is a central concern for community ecologists. We simulated a spatial agent-based model that generates variation in metacommunity dynamics across multiple axes, including the four classic metacommunity paradigms as special cases. We further simulated a virtual ecologist who analysed snapshot data sampled from the simulations using eighteen output metrics derived from beta-diversity and habitat variation indices, variation partitioning and joint species distribution modelling. Our results indicated two main axes of variation in the output metrics. The first axis of variation described whether the landscape has patchy or continuous variation, and thus was essentially independent of the properties of the species community. The second axis of variation related to the level of predictability of the metacommunity. The most predictable communities were niche-based metacommunities inhabiting static landscapes with marked environmental heterogeneity, such as metacommunities following the species sorting paradigm or the mass effects paradigm. The most unpredictable communities were neutral-based metacommunities inhabiting dynamics landscapes with little spatial heterogeneity, such as metacommunities following the neutral or patch sorting paradigms. The output metrics from joint species distribution modelling yielded generally the highest resolution to disentangle among the simulated scenarios. Yet, the different types of statistical approaches utilized in this study carried complementary information, and thus our results suggest that the most comprehensive evaluation of metacommunity structure can be obtained by combining them.Peer reviewe

What can observational data reveal about metacommunity processes?

A key challenge for community ecology is to understand to what extent observational data can be used to infer the underlying community assembly processes. As different processes can lead to similar or even identical patterns, statistical analyses of non‐manipulative observational data never yield undisputable causal inference on the underlying processes. Still, most empirical studies in community ecology are based on observational data, and hence understanding under which circumstances such data can shed light on assembly processes is a central concern for community ecologists. We simulated a spatial agent‐based model that generates variation in metacommunity dynamics across multiple axes, including the four classic metacommunity paradigms as special cases. We further simulated a virtual ecologist who analysed snapshot data sampled from the simulations using eighteen output metrics derived from beta‐diversity and habitat variation indices, variation partitioning and joint species distribution modelling. Our results indicated two main axes of variation in the output metrics. The first axis of variation described whether the landscape has patchy or continuous variation, and thus was essentially independent of the properties of the species community. The second axis of variation related to the level of predictability of the metacommunity. The most predictable communities were niche‐based metacommunities inhabiting static landscapes with marked environmental heterogeneity, such as metacommunities following the species sorting paradigm or the mass effects paradigm. The most unpredictable communities were neutral‐based metacommunities inhabiting dynamics landscapes with little spatial heterogeneity, such as metacommunities following the neutral or patch sorting paradigms. The output metrics from joint species distribution modelling yielded generally the highest resolution to disentangle among the simulated scenarios. Yet, the different types of statistical approaches utilized in this study carried complementary information, and thus our results suggest that the most comprehensive evaluation of metacommunity structure can be obtained by combining them

Traits and phylogenies modulate the environmental responses of wood-inhabiting fungal communities across spatial scales

Identifying the spatial scales at which community assembly processes operate is fundamental for gaining a mechanistic understanding of the drivers shaping ecological communities. In this study, we examined whether and how traits and phylogenetic relationships structure fungal community assembly across spatial scales. We applied joint species distribution modelling to a European-scale dataset on 215 wood-inhabiting fungal species, which includes data on traits, phylogeny and environmental variables measured at the local (log-level) and regional (site-level) scales. At the local scale, wood-inhabiting fungal communities were mostly structured by deadwood decay stage, and the trait and phylogenetic patterns along this environmental gradient suggested the lack of diversifying selection. At regional scales, fungal communities and their trait distributions were influenced by climatic and connectivity-related variables. The fungal climatic niches were not phylogenetically structured, suggesting that diversifying selection or stabilizing selection for climatic niches has played a strong role in wood-inhabiting communities. In contrast, we found a strong phylogenetic signal in the responses to connectivity-related variables, revealing phylogenetic homogenization in small and isolated forests. Synthesis. Altogether, our results show that species-level traits and phylogenies modulate the responses of wood-inhabiting fungi to environmental processes acting at different scales. This result suggests that the evolutionary histories of fungal traits diverge along different environmental axes.Peer reviewe

Environmental responses of fruiting fungal communities are phylogenetically structured

Through their ephemeral reproductive structures (fruiting bodies), ectomycorrhizal forest soil fungi provide a resource for a plethora of organisms. Thus, resolving what biotic and abiotic factors determine the occurrence and abundance of fruiting bodies is fundamental for understanding the dynamics of forest trophic networks. While the influence of abiotic factors such as moisture and temperature on fungal fruiting are relatively well established, little is known about how these processes interact with the evolutionary history of fungal species to determine when, where, and in which abundance fungal fruiting bodies will emerge. A specific knowledge gap relates to whether species' responses to their environment are phylogenetically structured. Here, we ask whether related fungal taxa respond similarly to climatic factors and forest habitat characteristics, and whether such correlated responses will affect the assembly of fungal fruiting communities. To resolve these questions, we fitted joint species distribution models combining data on the species composition and abundance of fungal fruiting bodies, environmental variation, and phylogenetic relationships among fungal taxa. Our results show that both site-level forest characteristics (dominant tree species and forest age) and climatic factors related to phenology (effective heat sum) greatly influence the occurrence and abundance of fruiting bodies. More importantly, while different fungal species responded unequally to their shared environment, there was a strong phylogenetic signal in their responses, so that related fungal species tended to fruit under similar environmental conditions. Thus, not only are fruiting bodies short-lived and patchily distributed, but the availability of similar resources will be further aggregated in time and space. These strong constraints on resource availability for fungus-associated taxa highlight the potential of fungus-based networks as a model system for studies on the ecology and evolution of resource-consumer relations in ephemeral systems of high spatiotemporal patchiness

Microclimate structures communities, predation and herbivory in the High Arctic

1. In a warming world, changes in climate may result in species-level responses as well as changes in community structure through knock-on effects on ecological interactions such as predation and herbivory. Yet, the links between these responses at different levels are still inadequately understood. Assessing how microclimatic conditions affect each of them at local scales provides information essential for understanding the consequences of macroclimatic changes projected in the future.2. Focusing on the rapidly changing High Arctic, we examine how a community based on a common resource species (avens, Dryas spp.), a specialist insect herbivore (Sympistis zetterstedtii) and natural enemies of lepidopteran herbivores (parasitoids) varies along a multidimensional microclimatic gradient. We ask (a) how parasitoid community composition varies with local abiotic conditions, (b) how the community-level response of parasitoids is linked to species-specific traits (koino- or idiobiont life cycle strategy and phenology) and (c) whether the effects of varying abiotic conditions extend to interaction outcomes (parasitism rates on the focal herbivore and realized herbivory rates).3. We recorded the local communities of parasitoids, herbivory rates on Dryas flowers and parasitism rates in Sympistis larvae at 20 sites along a mountain slope. For linking community-level responses to microclimatic conditions with parasitoid traits, we used joint species distribution modelling. We then assessed whether the same abiotic variables also affect parasitism and herbivory rates, by applying generalized linear and additive mixed models.4. We find that parasitism strategy and phenology explain local variation in parasitoid community structure. Parasitoids with a koinobiont strategy preferred high-elevation sites with higher summer temperatures or sites with earlier snowmelt and lower humidity. Species of earlier phenology occurred with higher incidence at sites with cooler summer temperatures or later snowmelt. Microclimatic effects also extend to parasitism and herbivory, with an increase in the parasitism rates of the main herbivore S. zetterstedtii with higher temperature and lower humidity, and a matching increase in herbivory rates.5. Our results show that microclimatic variation is a strong driver of local community structure, species interactions and interaction outcomes in Arctic ecosystems. In view of ongoing climate change, these results predict that macroclimatic changes will profoundly affect arctic communities

Spatiotemporal snowmelt patterns within a high Arctic landscape, with implications for flora and fauna

Snow conditions are important drivers of the distribution and phenology of Arctic flora and fauna, but the extent and effects of local variation in snowmelt are still inadequately studied. We analyze snowmelt patterns within the Zackenberg valley in northeast Greenland. Drawing on landscape-level snowmelt dates and meteorological data from a central climate station, we model snowmelt trends during 1998-2014. We then use time-lapse photographs to examine consistency in spatiotemporal snowmelt patterns during 2006-2014. Finally, we use monitoring data on arthropods and plants for 1998-2014 to investigate how snowmelt date affects the phenology of Arctic organisms. Despite large interannual variation in snowmelt timing, we find consistency in the relative order of snowmelt among sites within the landscape. With a slight overall advancement in snowmelt during the study period, early melting locations have advanced more than late-melting ones. Individual organism groups differ greatly in how their phenology shifts with snowmelt, with much variance attributable to variation in life history and diet. Overall, we note that local variation in snowmelt patterns may drive important ecological processes, and that more attention should be paid to variability within landscapes. Areas optimal for a given taxon vary between years, thereby creating spatial structure in a seemingly uniform landscape.Peer reviewe

Dead wood profile of a semi-natural boreal forest - implications for sampling

Dead wood profile of a forest is a useful tool for describing forest characteristics and assessing forest disturbance history. Nevertheless, there are few studies on dead wood profiles, including both coarse and fine dead wood, and on the effect of sampling intensity on the dead wood estimates. In a semi-natural boreal forest, we measured every dead wood item over 2 cm in diameter from 80 study plots. From eight plots, we further recorded dead wood items below 2 cm in diameter. Based on these data we constructed the full dead wood profile, i.e. the overall number of dead wood items and their distribution among different tree species, volumes of different size and decay stage categories. We discovered that while the number of small dead wood items was immense, their number dropped drastically from the diameter below 1 cm to diameters 2-3 cm. Different tree species had notably different abundance-diameter distribution patterns: spruce dead wood comprised most strikingly the smallest diameter fractions, whereas aspen dead wood comprised a larger share of large-diameter items. Most of the dead wood volume constituted of large pieces (>10 cm in diameter), and 62% of volume was birch. The variation in the dead wood estimates was small for the numerically dominant tree species and smallest diameter categories, but high for the sub-dominant tree species and larger size categories. In conclusion, the more the focus is on rare tree species and large dead wood items, the more comprehensive should the sampling be.Peer reviewe

Microclimate structures communities, predation and herbivory in the High Arctic

In a warming world, changes in climate may result in species-level responses as well as changes in community structure through knock-on effects on ecological interactions such as predation and herbivory. Yet, the links between these responses at different levels are still inadequately understood. Assessing how microclimatic conditions affect each of them at local scales provides information essential for understanding the consequences of macroclimatic changes projected in the future. Focusing on the rapidly changing High Arctic, we examine how a community based on a common resource species (avens, Dryas spp.), a specialist insect herbivore (Sympistis zetterstedtii) and natural enemies of lepidopteran herbivores (parasitoids) varies along a multidimensional microclimatic gradient. We ask (a) how parasitoid community composition varies with local abiotic conditions, (b) how the community-level response of parasitoids is linked to species-specific traits (koino- or idiobiont life cycle strategy and phenology) and (c) whether the effects of varying abiotic conditions extend to interaction outcomes (parasitism rates on the focal herbivore and realized herbivory rates). We recorded the local communities of parasitoids, herbivory rates on Dryas flowers and parasitism rates in Sympistis larvae at 20 sites along a mountain slope. For linking community-level responses to microclimatic conditions with parasitoid traits, we used joint species distribution modelling. We then assessed whether the same abiotic variables also affect parasitism and herbivory rates, by applying generalized linear and additive mixed models. We find that parasitism strategy and phenology explain local variation in parasitoid community structure. Parasitoids with a koinobiont strategy preferred high-elevation sites with higher summer temperatures or sites with earlier snowmelt and lower humidity. Species of earlier phenology occurred with higher incidence at sites with cooler summer temperatures or later snowmelt. Microclimatic effects also extend to parasitism and herbivory, with an increase in the parasitism rates of the main herbivore S. zetterstedtii with higher temperature and lower humidity, and a matching increase in herbivory rates. Our results show that microclimatic variation is a strong driver of local community structure, species interactions and interaction outcomes in Arctic ecosystems. In view of ongoing climate change, these results predict that macroclimatic changes will profoundly affect arctic communities.</p

Imprints of latitude, host taxon, and decay stage on fungus-associated arthropod communities

Interactions among fungi and insects involve hundreds of thousands of species. While insect communities on plants have formed some of the classic model systems in ecology, fungus-based communities and the forces structuring them remain poorly studied by comparison. We characterize the arthropod communities associated with fruiting bodies of eight mycorrhizal basidiomycete fungus species from three different orders along a 1200-km latitudinal gradient in northern Europe. We hypothesized that, matching the pattern seen for most insect taxa on plants, we would observe a general decrease in fungal-associated species with latitude. Against this backdrop, we expected local communities to be structured by host identity and phylogeny, with more closely related fungal species sharing more similar communities of associated organisms. As a more unique dimension added by the ephemeral nature of fungal fruiting bodies, we expected further imprints generated by successional change, with younger fruiting bodies harboring communities different from older ones. Using DNA metabarcoding to identify arthropod communities from fungal fruiting bodies, we found that latitude left a clear imprint on fungus-associated arthropod community composition, with host phylogeny and decay stage of fruiting bodies leaving lesser but still-detectable effects. The main latitudinal imprint was on a high arthropod species turnover, with no detectable pattern in overall species richness. Overall, these findings paint a new picture of the drivers of fungus-associated arthropod communities, suggesting that latitude will not affect how many arthropod species inhabit a fruiting body but, rather, what species will occur in it and at what relative abundances (as measured by sequence read counts). These patterns upset simplistic predictions regarding latitudinal gradients in species richness and in the strength of biotic interactions.Peer reviewe