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Will forest conservation areas protect functionally important diversity of fungi and lichens over time?

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Incorporating functional values in biodiversity monitoring systems could add novel perspectives of the status of biodiversity in conservation areas. Stable frequencies of large foliose nitrogen-fixing cyanolichens likely have positive effects on the nitrogen budget of forests and provide food, material and shelter for invertebrates, gastropods and birds. Stable volumes of deadwood and frequencies of associated fungi provide an important supporting function for ecosystem services such as nutrient cycling, carbon storage and soil formation. Based on regional monitoring data from boreal old-growth forest nature reserves and key habitats, we tested for changes in the frequency of various functionally important substrates and species over time. We detected significant reductions in the frequency of indicator cyanolichens occurring on deciduous trees already after 10 years in key habitats, despite non-significant changes in their host substrates. Frequencies of indicator pendulous lichens Alectoria sarmentosa and Bryoria nadvornikiana had also decreased in key habitats, despite overall stable volumes of large conifer host trees. Lichen reductions were more pronounced in the smaller key habitats compared to the larger formally protected nature reserves, likely due to degrading fragmentation and isolation effects. In contrast to these lichens, the average frequencies of old-growth forest indicator fungi decaying coniferous deadwood and common fungi on deciduous trees (Fomes fomentarius) and coniferous trees (Fomitopsis pinicola) remained unchanged. The studied cyanolichens and fruiting fungi generally had similar extinction rates over 10 years, whilst only cyanolichens had substantially lower colonization rates. Amid a severely fragmented landscape, conservation areas seem to struggle in preserving some of the basic old-growth forest values.
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ORIGINAL PAPER
Will forest conservation areas protect functionally
important diversity of fungi and lichens over time?
Mari T. Jo
¨nsson
1
Alejandro Ruete
1
Olle Kellner
2
Urban Gunnarsson
3
Tord Sna
¨ll
1
Received: 24 June 2015 / Revised: 24 November 2015 / Accepted: 6 December 2015 /
Published online: 21 January 2016
ÓSpringer Science+Business Media Dordrecht 2016
Abstract Incorporating functional values in biodiversity monitoring systems could add
novel perspectives of the status of biodiversity in conservation areas. Stable frequencies of
large foliose nitrogen-fixing cyanolichens likely have positive effects on the nitrogen
budget of forests and provide food, material and shelter for invertebrates, gastropods and
birds. Stable volumes of deadwood and frequencies of associated fungi provide an
important supporting function for ecosystem services such as nutrient cycling, carbon
storage and soil formation. Based on regional monitoring data from boreal old-growth
forest nature reserves and key habitats, we tested for changes in the frequency of various
functionally important substrates and species over time. We detected significant reductions
in the frequency of indicator cyanolichens occurring on deciduous trees already after
10 years in key habitats, despite non-significant changes in their host substrates. Fre-
quencies of indicator pendulous lichens Alectoria sarmentosa and Bryoria nadvornikiana
had also decreased in key habitats, despite overall stable volumes of large conifer host
trees. Lichen reductions were more pronounced in the smaller key habitats compared to the
larger formally protected nature reserves, likely due to degrading fragmentation and iso-
lation effects. In contrast to these lichens, the average frequencies of old-growth forest
indicator fungi decaying coniferous deadwood and common fungi on deciduous trees
Communicated by Eckehard Brockerhoff, Herve
´Jactel and Ian Thompson.
This is part of the special issue on ‘Forest biodiversity and ecosystem services’.
Electronic supplementary material The online version of this article (doi:10.1007/s10531-015-1035-0)
contains supplementary material, which is available to authorized users.
&Mari T. Jo
¨nsson
mari.jonsson@slu.se
1
Swedish Species Information Centre, Swedish University of Agricultural Sciences (SLU),
P.O. 7007, 750 07 Uppsala, Sweden
2
County Administrative Board of Ga
¨vleborg, 801 70 Ga
¨vle, Sweden
3
County Administrative Board of Dalarna, 791 84 Falun, Sweden
123
Biodivers Conserv (2017) 26:2547–2567
DOI 10.1007/s10531-015-1035-0
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Supplementary resource (1)

... The weak effect of fragment characteristics is not unexpected, because fragments were originally selected such that their forest characteristics would be similar. Although we did not measure forest characteristics in 2017, we presume that they did not change markedly as key characteristics result from site productivity and thus tend to remain without stand-replacing disturbances (Jönsson et al. 2017). ...
... First of all, wood-decaying fungi can persist in small old-growth forest fragments for decades, and thus the importance of small fragments should be acknowledged. Our species-specific results regarding extinctions, colonizations and declines are consistent with the studies of the same species in Sweden (Berglund and Jonsson 2008;Jönsson et al. 2008;Ruete et al. 2016;Jönsson et al. 2017). Taken together, all these studies underscore that rare species generally seem to decline following fragmentation, but abundant species become more abundant. ...
Article
Full-text available
According to ecology theory, isolated habitat fragments cannot maintain populations of specialized species. Yet, empirical evidence based on monitoring of the same fragments over time is still limited. We studied the colonization–extinction dynamics of eight wood-decaying fungal species in 16 old-growth forest fragments (<14 ha) over a 20-year period (1997–2017). We observed 19 extinctions and 5 colonizations; yet, the distribution of extinctions and colonizations did not differ from the one expected by chance for any of the species. Twenty-six percent of the extinctions took place in two natural fragments amid large forest–peatland complexes. (Romell) Bourdot and Galzin decreased and (P. Karst.) Bourdot increased in abundance (number of logs occupied). The volume of living spruce trees in the forest fragments correlated positively with the number of logs inhabited in five of the study species. Because fragment characteristics did not affect species turnover, it seems that stochastic processes governed colonizations and extinctions. Although the least abundant species in 1997 had declined, and the most abundant species had become more abundant, it appears that specialized wood-decaying fungi can persist for decades in isolated old-growth forest fragments, if suitable dead wood is continuously available. Phellinus nigrolimitatus Phellinus ferrugineofuscus
... Indeed, most biodiversity conservation research has focused on high-profile, yet relatively species-poor groups such as vertebrates, plants, and some groups of insects, often neglecting fungi (Lonsdale et al. 2008;Heilmann-Clausen et al. 2015). Even the fungal conservation biology literature is more concerned with saproxylic fungi than with tree fungal pathogens, although tree diseases are an important provider of deadwood (Jönsson et al. 2017). A forest without a sufficient amount of tree diseases is thus today recognized as not entirely healthy (Ostry and Laflamme 2008;Holdenrieder and Pautasso 2014;Szwagrzyk 2020). ...
Chapter
Tree diseases are important agents of ecological disturbance in wooded ecosystems. Native tree diseases create forest gaps, thus diversifying forest structure and creating habitat for many organisms. Tree diseases are also part of biodiversity, but they have seldom been considered from a conservation biology perspective. More diverse forests are generally less susceptible to tree disease epidemics. Tree diseases can in turn modify the resilience of forests against other stresses. Because of increased plant trade and other global change drivers, exotic tree diseases are becoming more frequent. Interactions between tree diseases and other ecological disturbances need more public awareness and integration into forest simulation models.KeywordsDeadwoodDisease triangleEcosystem engineersEmerging tree diseasesForest healthForest pathologyInteracting disturbancesTree diversityTree fungal pathogensTree health
... The decline on remeasured trees and similarly recorded declines in protected forests (Jönsson et al., 2017) show that other drivers also affected the lichens. Although thallus length increased slightly in some regions, we found no increase in occurrence in southern-central regions in response to the reduced anthropogenic N deposition since ~1980 (Engardt et al., 2017). ...
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Thin, hair‐like lichens (Alectoria, Bryoria, Usnea) form conspicuous epiphyte communities across the boreal biome. These poikilohydric organisms provide important ecosystem functions and are useful indicators of global change. We analyse how environmental drivers influence changes in occurrence and length of these lichens on Norway spruce (Picea abies) over 10 years in managed forests in Sweden using data from >6000 trees. Alectoria and Usnea showed strong declines in southern‐central regions, whereas Bryoria declined in northern regions. Overall, relative loss rates across the country ranged from 1.7% per year in Alectoria to 0.5% in Bryoria. These losses contrasted with increased length of Bryoria and Usnea in some regions. Occurrence trajectories (extinction, colonization, presence, absence) on remeasured trees correlated best with temperature, rain, nitrogen deposition, and stand age in multinomial logistic regression models. Our analysis strongly suggests that industrial forestry, in combination with nitrogen, is the main driver of lichen declines. Logging of forests with long continuity of tree cover, short rotation cycles, substrate limitation and low light in dense forests are harmful for lichens. Nitrogen deposition has decreased but is apparently still sufficiently high to prevent recovery. Warming correlated with occurrence trajectories of Alectoria and Bryoria, likely by altering hydration regimes and increasing respiration during autumn/winter. The large‐scale lichen decline on an important host has cascading effects on biodiversity and function of boreal forest canopies. Forest management must apply a broad spectrum of methods, including uneven‐aged continuous cover forestry and retention of large patches, to secure the ecosystem functions of these important canopy components under future climates. Our findings highlight interactions among drivers of lichen decline (forestry, nitrogen, climate), functional traits (dispersal, lichen colour, sensitivity to nitrogen, water storage), and population processes (extinction/colonization).
... To the best of our knowledge, there have been no studies investigating the impact of fungal community composition on tree establishment or tree community composition, however, there have been multiple studies investigating the impact of trees (and plantations in particular) on fungal communities. There is evidence to suggest that tree species composition and biodiversity-promoting forest management strategies do affect the species composition of fungal communities in forests (Asplund et al., 2019;Brazee et al., 2014;Gunina et al., 2017;Jönsson et al., 2017;Kutszegi et al., 2015Kutszegi et al., , 2020Müller et al., 2007;O'Hanlon & Harrington, 2012a, 2012bPurahong et al., 2018;Rodriguez-Ramos et al., 2021;Tomao et al., 2020;Varenius et al., 2016). However, the overall fungal richness is often not affected by tree species composition, and a number of studies have demonstrated the potential of plantation forests (including non-native tree species) to support and maintain fungal populations (Humphrey, 2005;Humphrey et al., 2000;Komonen et al., 2016;Leski et al., 2019;Newton et al., 2002;O'Hanlon & Harrington, 2012a;Quine & Humphrey, 2010). ...
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Tree planting now forms a major part of the UK climate mitigation strategy, with targets to increase the forest cover from the current 13% to 17%–20% by 2050. A tree planting strategy on this scale requires a significant amount of planning, bringing together expertise from a wide range of practitioners. We highlight four key reasons why fungi should be considered in tree planting strategies: 1. Fungi can cause severe tree disease. 2. Fungi can cause significant human health burdens. 3. Forest soil carbon and nutrient cycling is controlled by fungi. 4. Climate change is already affecting fungi. Following from these four reasons, we explore the ways in which the negative effects of fungi, such as plant and human disease, can be mitigated against, whilst also protecting and promoting the benefits of fungi in carbon storage and biodiversity. Based on this, we outline seven guidelines which should be integrated into existing tree planting guidelines and UK policy: A. Monitor tree fungal disease emergence and spread, including in source material trade (e.g. seeds and saplings). B. Choose tree species combinations appropriate to the specific habitat and appropriate for biodiversity and carbon storage goals. C. Develop and implement a widely accessible fungal spore forecast to complement existing pollen forecasts. D. Protect existing ancient and mature woodlands. E. Promote planting on suitable land types, avoiding grasslands and wetlands. F. Assess proposed and existing forest sites, ideally using a combination of fungal fruit body surveys and eDNA techniques. G. Develop and implement the UK Fungi Red List into UK law. Tree planting now forms a major part of the UK climate mitigation strategy, with targets to increase the forest cover from the current 13% to 17%–20% by 2050. We highlight four key reasons why fungi should be considered in tree planting strategies, with a following seven policy recommendations to maximise the carbon sequestration and biodiversity benefits of fungi, whilst mitigating against plant and human disease risks.
... 4,17,24 ) there is a need to comprehensively assess how different fungal groups respond to forest naturalness. Fungal traits, such as nutritional modes as well as fruitbody and spore characteristics, can affect species response to environmental changes and explain concomitant changes in species diversity 23,[25][26][27][28] . Fungal fruitbodies function as a structure for spore (or other dispersal structure) formation and release in reproduction. ...
Article
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The general negative impact of forestry on wood-inhabiting fungal diversity is well recognized, yet the effect of forest naturalness is poorly disentangled among different fungal groups inhabiting dead wood of different tree species. We studied the relationship between forest naturalness, log characteristics and diversity of different fungal morpho-groups inhabiting large decaying logs of similar quality in spruce dominated boreal forests. We sampled all non-lichenized fruitbodies from birch, spruce, pine and aspen in 12 semi-natural forest sites of varying level of naturalness. The overall fungal community composition was mostly determined by host tree species. However, when assessing the relevance of the environmental variables separately for each tree species, the most important variable varied, naturalness being the most important explanatory variable for fungi inhabiting pine and aspen. More strikingly, the overall species richness increased as the forest naturalness increased, both at the site and log levels. At the site scale, the pattern was mostly driven by the discoid and pyrenoid morpho-groups inhabiting pine , whereas at the log scale, it was driven by pileate and resupinate morpho-groups inhabiting spruce. Although our study demonstrates that formerly managed protected forests serve as effective conservation areas for most wood-inhabiting fungal groups, it also shows that conservation planning and management should account for group- or host tree -specific responses.
... However, not enough is known about the fungal composition of forest formations to be able to use them widely as biological indicators of forest health [61]. In addition, some authors considered that joint studies with the dynamics and diversity of lichen-forming fungi [62] would be necessary for a more correct assessment of their degree of preservation, especially for forest habitats with older individuals [63]. In any case, the relevance of fungal species as a tool for assessing the health of habitats has been stressed [64], subject to further contributions that should be made in this field [65]. ...
Article
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The use of bioindicators to assess the conservation status of various ecosystems is becoming increasingly common, although fungi have not been widely used for this purpose. The aim was to use the analysis of the macromycetes fruiting bodies in the area of a natural reserve and the degree of preservation of its different zones combined with the use of geographical information systems (GIS). For this purpose, quantitative and qualitative fungal samples were carried out in plots of the middle-west of the Iberian Peninsula previously delimited and characterised thanks to GIS during the springs and autumns of the 2009–2012 period. In addition, the lifestyles of the fungal species were analysed as well as the influence of the main meteorological parameters on fungal fruiting. A total of 10,125 fruiting bodies belonging to 148 species were counted on 20 plots with four vegetation units (holm oak dehesas, mixed holm oaks and Pyrenean oak dehesas with different abundance and grasslands). The distribution of the different species, their lifestyles and the number of fruiting bodies in the different plots of the reserve indicated that the eastern part was best conserved, showing that the combination of fungal diversity studies and the use of GIS could be useful in the management of areas with environmental relevance.
Chapter
Ecosystem services are the benefits people obtain from ecosystems. Disturbances can have multiple, often negative, effects on ecosystem services. Primary production is temporarily reduced by disturbances, while water and nutrient cycles are stimulated by disturbances. Consequently, the production of plant biomass (wood, animal fodder) may be temporarily decreased. In the context of climate regulation, disturbances reduce carbon storage (warming effect) but simultaneously increase albedo (cooling effect). Furthermore, disturbances reduce the protection function of forests against natural hazards. The way disturbances affect cultural services, such as the recreational function of ecosystems, depends on the subjective perception of people.KeywordsFire Wind Bark beetles Drought Supporting services Provisioning services Regulating services Cultural services
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Functional diversity refers to those components of biodiversity that influence how an ecosystem operates or functions. The biological diversity, or biodiversity, of a habitat is much broader and includes all the species living in a site, all of the genotypic and phenotypic variation within each species, and all the spatial and temporal variability in the communities and ecosystems that these species form. Functional diversity, which is a subset of this, is measured by the values and range in the values, for the species present in an ecosystem, of those organismal traits that influence one or more aspects of the functioning of an ecosystem. Functional diversity is of ecological importance because it, by definition, is the component of diversity that influences ecosystem dynamics, stability, productivity, nutrient balance, and other aspects of ecosystem functioning.
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Exploration of tree crowns worldwide often reveals rich epiphyte communities composed of lichens, bryophytes, and vascular plants. In very old, wet forests, nearly every tree surface, from outermost twigs to thick branches and the main trunk, is covered by epiphytes. An arboreal botanist faced with this diversity quickly realizes that these plants are not uniformly distributed across tree surfaces and that most of the species seldom, if ever, grow on the forest floor below. Many epiphytes, including all of the lichens and bryophytes, are poikilohydric organisms. Their survival in the canopy depends on an ability to become dormant when humidity is low, with physiological activity resuming only upon rehydration by atmospheric moisture. The chapter focuses on the ecology of epiphytic lichens and bryophytes. After introducing the organisms, it describes their distributions along environmental gradients, summarizes biotic interactions, discusses the strong associations between some species and old-growth forests, evaluates their roles in forest ecosystems, and considers their conservation in an uncertain future.
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To maintain biodiversity in managed forests we must understand the patterns and processes that regulate the occurrence and dynamics of species in undisturbed ecosystems. We compared biomass and species composition of canopy lichens on 180 lower branches of Norway spruce (Picea abies) in three pairs of old-growth and managed (selectively logged) stands in northern Sweden (30 branches per stand). The purpose was to evaluate the effect of substrate quality (branch characteristics) on patterns of lichen biomass for two different growth forms (foliose and fruticose). Old-growth stands had six times higher lichen mass per spruce branch, and two times higher expressed as percentage of branch mass, compared to mature stands of managed forest. Lichen mass was strongly related to mass, diameter, and age of branches. Fruticose, pendulous species (Alectoria sarmentosa and Bryoria spp.) were highly sensitive to forest practices. In contrast, type of forest had no significant effect on foliose species. Species number per stand was the same (15 species) in both types of forest, but there were marked differences in the relative abundance of different lichen groups. Results suggest that limited amount of substrate (i.e., small branches) available to lichens, and young branches, providing only a short time for lichen colonization and growth, are important factors limiting epiphytic lichen abundance in managed forests. Conversion of old-growth forest into young, managed stands will lead to a significant reduction in epiphytic lichen mass. This in turn may probably affect nutrient cycling in forests and has negative consequences for animals that utilize canopy lichens as food, shelter, or nesting material.
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