Citizen science data reveal ecological, historical and evolutionary factors shaping interactions between woody hosts and wood‐inhabiting fungi

Heilmann‐Clausen, Jacob; Maruyama, Pietro Kiyoshi; Bruun, Hans Henrik; Dimitrov, Dimitar; Læssøe, Thomas; Frøslev, Tobias Guldberg; Dalsgaard, Bo

doi:10.1111/nph.14194

Cited by 46 publications

(37 citation statements)

References 66 publications

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“…However, Heilmann‐Clausen et al. () recently found that major clades of aphyllophoroid fungi are less host specialist than several other fungal lineages, especially in the Ascomycota, probably reflecting a much stronger signal of co‐evolution with hosts. It is, hence, likely that host distribution patterns may have a stronger impact on the biogeography of fungi in other lineages than aphyllophoroid fungi, as it has been found in Lepidoptera with strong co‐evolution with their plant hosts (Auger‐Rozenberg et al., ; Triponez et al., ).…”

Section: Discussionmentioning

confidence: 99%

“…The close associations to live or dead plants in many species suggest that vegetation types greatly influence community composition, but it still remains unknown to which degree vegetation zones structure aphyllophoroid fungal communities. A better understanding of how fungal communities depend on their host communities provides the possibility to gain insights into co‐evolutionary relationships between fungi and plants (Heilmann‐Clausen et al., ) and how biogeographical legacies affect current distribution and host‐specificity patterns (Auger‐Rozenberg, Torres‐Leguizamon, Courtin, Rossi, & Kerdelhué, ; Triponez, Arrigo, Espíndola, & Alvarez, ).…”

Section: Introductionmentioning

confidence: 99%

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Do plant‐based biogeographical regions shape aphyllophoroid fungal communities in Europe?

Ordynets

Heilmann‐Clausen

Savchenko

et al. 2018

Journal of Biogeography

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Aim Aphyllophoroid fungi are associated with plants, either using plants as a resource (as parasites or decomposers) or as symbionts (as mycorrhizal partners). In spite of their strong association with plants, it is unknown how much plant distributions determine their biogeographical patterns compared with environmental factors such as climate and human land use. In this study, our aims are to (1) describe the spatial diversity patterns of aphyllophoroid fungi in Europe and (2) identify the factors shaping these patterns. Location Europe, as well as the adjacent Subarctic to Arctic islands (Greenland, Faroe Islands, Iceland, Svalbard), Palestine and the south‐east coast of the Caspian Sea. Methods We compiled a dataset consisting of 14,030 fruitbody occurrences of 1,491 aphyllophoroid fungal species from 39 geographical areas (17 countries) belonging to eight biogeographical regions. We assessed the differences in fungal species richness and overall diversity and its nestedness and turnover components across biogeographical regions of Europe, as well as between southern and northern Europe (based on geographical latitude of 50° as threshold). We used cluster and ordination analyses to classify the European aphyllophoroid communities biogeographically and evaluated the importance of climate, host‐tree species, topography and human land‐use intensity in explaining biogeographical variation. Results The importance of biogeographical regions in determining European aphyllophoroid fungal communities varies for different diversity components. Species richness and nestedness are best explained by plant‐based biogeographical regions, whereas overall beta diversity and species turnover are driven mostly by variation in climate, and nestedness mostly by tree species occupancy. Beta‐diversity patterns of aphyllophoroid fungi do not differ between southern and northern Europe. Main conclusions At the continental scale, aphyllophoroid fungi are less shaped by historical legacies than vascular plant and animal communities, and trends of overall beta diversity in southern and northern Europe are similar to patterns found for bryophytes.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Do plant‐based biogeographical regions shape aphyllophoroid fungal communities in Europe?

Ordynets

Heilmann‐Clausen

Savchenko

et al. 2018

Journal of Biogeography

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“…Taxa in this residual interaction pool may also be responding to unmeasured characteristics of the environment in this study. For instance, some studies have found that pH, which we did not measure, is important for explaining variation in fungal community composition in decaying wood (Baldrian et al 2016, Heilmann-Clausen et al 2016, Purahong et al 2016. Additionally, wood secondary chemistry is difficult to measure, but is an important way in which plants regulate pathogens.…”

Section: Many Positively Associated Taxamentioning

confidence: 90%

Good neighbors aplenty: fungal endophytes rarely exhibit competitive exclusion patterns across a span of woody habitats

Lee

Powell

Oberle

et al. 2019

Ecology

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Environmental forces and biotic interactions, both positive and negative, structure ecological communities, but their relative roles remain obscure despite strong theory. For instance, ecologically similar species, based on the principle of limiting similarity, are expected to be most competitive and show negative interactions. Specious communities that assemble along broad environmental gradients afford the most power to test theory, but the communities often are difficult to quantify. Microbes, specifically fungal endophytes of wood, are especially suited for testing community assembly theory because they are relatively easy to sample across a comprehensive range of environmental space with clear axes of variation. Moreover, endophytes mediate key forest carbon cycle processes, and although saprophytic fungi from dead wood typically compete, endophytic fungi in living wood may enhance success through cooperative symbioses. To classify interactions within endophyte communities, we analyzed fungal DNA barcode variation across 22 woody plant species growing in woodlands near Richmond, New South Wales, Australia. We estimated the response of endophytes to the measured wood environment (i.e., 11 anatomical and chemical wood traits) and each other using latent‐variable models and identified recurrent communities across wood environments using model‐based classification. We used this information to evaluate whether (1) co‐occurrence patterns are consistent with strong competitive exclusion, and (2) a priori classifications by trophic mode and phylum distinguish taxa that are more likely to have positive vs. negative associations under the principle of limiting similarity. Fungal endophytes were diverse (mean = 140 taxa/sample), with differences in community composition structured by wood traits. Variation in wood water content and carbon concentration were associated with especially large community shifts. Surprisingly, after accounting for wood traits, fungal species were still more than three times more likely to have positive than negative co‐occurrence patterns. That is, patterns consistent with strong competitive exclusion were rare, and positive interactions among fungal endophytes were more common than expected. Confirming the frequency of positive vs. negative interactions among fungal taxa requires experimental tests, and our findings establish clear paths for further study. Evidence to date intriguingly suggests that, across a wide range of wood traits, cooperation may outweigh combat for these fungi.

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“…Despite the importance and diversity of wood‐inhabiting fungi, our understanding of the factors driving the spatial and temporal patterns of their diversity is limited. It has been suggested that characteristics of the colonized dead‐wood object (host) and the environment surrounding an object are important drivers of the diversity of wood‐inhabiting fungi (Heilmann‐Clausen et al., ; Seibold, Bässler, Brandl, et al., ; Seibold et al., and therein). However, how the host and the environment individually affect fungal diversity on dead‐wood objects is unknown (Bradford et al., ).…”

Section: Introductionmentioning

confidence: 99%

Independent effects of host and environment on the diversity of wood‐inhabiting fungi

et al. 2018

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Dead wood is a habitat for numerous fungal species, many of which are important agents of decomposition. Previous studies suggested that wood‐inhabiting fungal communities are affected by climate, availability of dead wood in the surrounding landscape and characteristics of the colonized dead‐wood object (e.g. host tree species). These findings indicate that different filters structure fungal communities at different scales, but how these factors individually drive fungal fruiting diversity on dead‐wood objects is unknown. We conducted an orthogonal experiment comprising 180 plots (0.1 ha) in a random block design and measured fungal fruit body richness and community composition on 720 dead‐wood objects over the first 4 years of succession. The experiment allowed us to disentangle the effects of the host (beech and fir; logs and branches) and the environment (microclimate: sunny and shady plots; local dead wood: amount and heterogeneity of dead wood added to plot). Variance partitioning revealed that the host was more important than the environment for the diversity of wood‐inhabiting fungi. A more detailed model revealed that host tree species had the highest independent effect on richness and community composition of fruiting species of fungi. Host size had significant but low independent effects on richness and community composition of fruiting species. Canopy openness significantly affected the community composition of fruiting species. By contrast, neither local amount nor heterogeneity of dead wood significantly affected the fungal diversity measures. Synthesis. Our study identified host tree species as a more important driver of the diversity of wood‐inhabiting fungi than the environment, which suggests a host‐centred filter of this diversity in the early phase of the decomposition process. For the conservation of wood‐inhabiting fungi, a high variety of host species in various microclimates is more important than the availability of dead wood at the stand level.

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Citizen science data reveal ecological, historical and evolutionary factors shaping interactions between woody hosts and wood‐inhabiting fungi

Cited by 46 publications

References 66 publications

Do plant‐based biogeographical regions shape aphyllophoroid fungal communities in Europe?

Do plant‐based biogeographical regions shape aphyllophoroid fungal communities in Europe?

Good neighbors aplenty: fungal endophytes rarely exhibit competitive exclusion patterns across a span of woody habitats

Independent effects of host and environment on the diversity of wood‐inhabiting fungi

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