Article

Old trees as a key source of epiphytic lichen persistence and spatial distribution in mountain Norway spruce forests

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Habitat loss and fragmentation can negatively impact the persistence of dispersal-limited lichen species with narrow niches. Rapid change in microclimate due to canopy dieback exposes species to additional stressors that may limit their capacity to survive and colonize. We studied the importance of old trees as micro-refuges and microclimate stability in maintaining lichen survival and diversity. The study was situated in mountain Norway spruce (Picea abies) forests of the Gorgany Mountains of the Ukrainian Carpathian mountain belt. Lichens were collected on 13 circular study plots (1000 m²). Dendrochronological methods were used to reconstruct age structure and maximum disturbance event history. A linear mixed effects model and general additive models were used to explain patterns and variability of lichens based on stand age and disturbance history for each plot. Tree age was the strongest variable influencing lichen diversity and composition. Recent (<80 years ago) severely disturbed plots were colonized only by the most common species, however, old trees (>200 years old) that survived the disturbances served as microrefuges for the habitat-specialized and/or dispersal limited species, thus epiphytic lichen biodiversity was markedly higher on those plots in comparison to plots without any old trees. Most species were able to survive microclimatic change after disturbances, or recolonize disturbed patches from surrounding old-growth forests. We concluded that the survival of old trees after disturbances could maintain and/or recover large portions of epiphytic lichen biodiversity even in altered microclimates.
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ORIGINAL PAPER
Old trees as a key source of epiphytic lichen persistence
and spatial distribution in mountain Norway spruce
forests
Lucie Zemanova
´
1
Volodymyr Trotsiuk
2
Robert C. Morrissey
2
Radek Bac
ˇe
2
Martin Mikola
´s
ˇ
2
Miroslav Svoboda
2
Received: 1 April 2016 / Revised: 18 March 2017 / Accepted: 30 March 2017 /
Published online: 22 April 2017
ÓSpringer Science+Business Media Dordrecht 2017
Abstract Habitat loss and fragmentation can negatively impact the persistence of dis-
persal-limited lichen species with narrow niches. Rapid change in microclimate due to
canopy dieback exposes species to additional stressors that may limit their capacity to
survive and colonize. We studied the importance of old trees as micro-refuges and
microclimate stability in maintaining lichen survival and diversity. The study was situated
in mountain Norway spruce (Picea abies) forests of the Gorgany Mountains of the
Ukrainian Carpathian mountain belt. Lichens were collected on 13 circular study plots
(1000 m
2
). Dendrochronological methods were used to reconstruct age structure and
maximum disturbance event history. A linear mixed effects model and general additive
models were used to explain patterns and variability of lichens based on stand age and
disturbance history for each plot. Tree age was the strongest variable influencing lichen
diversity and composition. Recent (\80 years ago) severely disturbed plots were colonized
only by the most common species, however, old trees ([200 years old) that survived the
disturbances served as microrefuges for the habitat-specialized and/or dispersal limited
species, thus epiphytic lichen biodiversity was markedly higher on those plots in com-
parison to plots without any old trees. Most species were able to survive microclimatic
change after disturbances, or recolonize disturbed patches from surrounding old-growth
forests. We concluded that the survival of old trees after disturbances could maintain and/
or recover large portions of epiphytic lichen biodiversity even in altered microclimates.
Communicated by Pradeep Kumar Divakar.
This article belongs to the Topical Collection: Forest and plantation biodiversity.
&Lucie Zemanova
´
zluxie@gmail.com
1
Department of Ecology, Faculty of Environmental Sciences, Czech University of Life Sciences,
Kamy
´cka
´1176, 16521 Prague, Czech Republic
2
Department of Forest Ecology, Faculty of Forestry and Wood Science, Czech University of Life
Sciences, Kamy
´cka
´1176, 16521 Prague, Czech Republic
123
Biodivers Conserv (2017) 26:1943–1958
DOI 10.1007/s10531-017-1338-4
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Conti and Cecchetti 2001;Thormann 2006;Kuldeep and Prodyut 2015), are highly effective for diagnosing many aspects of forest quality since they are regarded as substrate or habitat specialists (Resl et al. 2018). For example, some lichens are characterized by their strong preference to old woodland stands (Marmor et al. 2011;Zemanová et al. 2017;Williams and Ellis 2018), being associated with over-mature senescent trees (Nascimbene et al. 2009) and large trees (Kruys et al. 1999), i.e. substrates that are poorly represented in managed forests. ...
... Concerning the species richness, our results are not exceptional in context of other studies focused on a comparison of managed, unmanaged and old-growth forest with Picea abies. The studies emphasize higher species richness of lichens in unmanaged stands that is conditioned mainly by forest age (Holien 1996;Hilmo et al. 2009;Lie et al. 2009;Marmor et al. 2011;Dittrich et al. 2013;Zemanová et al. 2017), light availability (Gauslaa et al. 2008;Marmor et al. 2012) and dispersal limitations of some old-growth forest species (Sillett et al. 2000;Hilmo and Såstad 2001). Species richness is also positively correlated with elevation (Holien 1996;Nascimbene and Marini 2015;Bässler et al. 2016), admixture of other tree species (Kuusinen and Siitonen 1998) and microclimatic factors like a higher humidity in swamp forests (Kuusinen 1996). ...
... Species richness is also positively correlated with elevation (Holien 1996;Nascimbene and Marini 2015;Bässler et al. 2016), admixture of other tree species (Kuusinen and Siitonen 1998) and microclimatic factors like a higher humidity in swamp forests (Kuusinen 1996). A stand age of 200 years seems to be the lower limit for species-rich communities, for species with limited dispersal abilities and niche specialists (Dittrich et al. 2013;Zemanová et al. 2017). Intensity of forest management has a strong negative impact on the number of Red-listed lichens and substrate specialists (Boch et al. 2013;Ardelean et al. 2015). ...
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Natural spruce forests are restricted to the highest mountain ranges in the Czech Republic. Spruce is also the commonest tree species in managed forests. Owing to a massive decline of spruce forests in Central Europe, caused by recent climatic fluctuations and disturbances, the lichen diversity and species composition was compared between ten representative natural mountain old-growth forests in the Czech Republic and their counterparts in mature managed forests. The old-growth forests are characterized by a higher species richness, abundance, number of Red-listed species, functional, taxonomic and phylogenetic diversities. Plots with the highest species richness are situated in the Šumava Mountains, an area with a relatively low sulphur deposition in the past. Bioindication analysis searching for lichen indicators supported several species (e.g. Xylographa vitiligo, Chaenotheca sphaerocephala) and genera (e.g. Calicium, Xylographa) with a strong preference for old-growth forests. Analysis of lichen functional traits revealed a higher abundance of species with a vegetative reproduction in managed forests that may be explained by a higher efficiency in colonization by young successional stages. Lichens with stalked apothecia, pigmented ascospores and large ascospores are more frequent in old-growth forests. Our results are briefly discussed in terms of nature conservation, focusing on national refugees of old-growth forest species, biodiversity hot-spots, practical use of indicator species and representative measures for an evaluation of forest quality.
... Therefore, different tree species may constitute refuges for different lichens. The number of lichen species is often positively related to tree size, and greater species richness can be expected on older and larger trees (Gustafsson et al. 1992, Uliczka & Angelstam 2000, Johansson & Ehrlén 2003, Zemanová et al. 2017). Thus, tree avenues (especially those including multiple species) comprising aged and lofty individuals possess vast potential as habitats for many endangered epiphytic lichens. ...
... (2) 1-5 %; (3) 5 -12.5 %; (4) 12.5 -50 %; (5) > 50 % (see also Hofmeister et al. 2015, Kubiak & Osyczka 2017, Zemanová et al. 2017. ...
... Generally, older trees are usually inhabited by more species of lichens (e.g. Fritz et al. 2009, Hofmeister et al. 2016, Zemanová et al. 2017. However, this is not a strict rule, and sometimes an inverse relationship is observed (Jüriado et al. 2009b). ...
Article
Kubiak, D. & Osyczka, P. 2019. Tree avenues as reservoir for epiphytic lichens in deforested landscapes. – Herzogia 32: 398 – 420.Old tree avenues are a disappearing traditional element in European landscapes. Roadside trees constitute an important habitat for many groups of organisms and support the maintenance of biodiversity in deforested areas, but they are often neglected in conservation strategies. This study describes and analyses the conservation value of planted trees along rural roads in NE Poland for epiphytic lichens. A total of 105 trunks of seven deciduous tree species were examined. Lichen species inventories were assembled for trunks at a height up to two meters from the ground. A total of 99 lichen species was recorded. Lichen species richness and cover were dependent primarily on tree species. Diameter of trees was not significantly correlated with the number of species. Ulmus laevis and, to a lesser extent, Fraxinus excelsior and Acer platanoides, were be the most valuable tree species in terms of lichen species richness. Quercus robur as a roadside tree did not have above-average species numbers. Lichen species with a preference for eutrophicated or alkaline bark occurred in their largest numbers on Populus nigra agg. Betula pendula hosted the largest number of species avoiding eutrophication. Each tree species had its own set of exclusive lichens and hosted taxa which are red-listed in Poland; however, no single tree species alone guarantees preservation of the entire range of epiphytic lichens on roadside trees in the study area. Since tree avenues, especially those composed of multiple species, provide a suitable habitat for various rare and endangered lichens, potentially high conservation value should always be attributed to this element of local landscapes in low pollution areas.
... It is widely recognized that disturbance plays a major role in determining species diversity, distributions, and functions (Hutchinson 1953;Connell 1978;Johst and Huth 2005). Approaches to understanding the impacts of disturbance have included examining effects of variables across trophic levels (Wootton 1998), spatial scales (Witman et al. 2008;Limberger and Wickham 2012), and temporal scales (Svensson et al. 2007;Zemanová et al. 2017). Others have explored how disturbance affects functional diversity and ecosystem services (Biswas and Mallik 2010;Thom and Seidl 2016), whether choice of diversity measure matters (Mackey and Currie 2001;Johst and Huth 2005;Svensson et al. 2007), and how species traits such as dispersal respond to disturbance (Johansson et al. 2013). ...
... In contrast, few studies have incorporated data derived from total lichen diversity, with most studies completely excluding microlichens that can comprise more than half the total diversity in an area (e.g., Tripp 2015;Lendemer et al. 2016). Second, research to date has emphasized responses to catastrophic disturbances (Mistry 1998;McMullin et al. 2008;O'Bryan et al. 2009;Ellis and Coppins 2010;Lundström et al. 2013;Bartels and Chen 2015), land management practices (Zemanová et al. 2017;Ray et al. 2015), and pollution (McCune et al. 1997;Ellis and Coppins 2010;Shrestha and St. Clair 2011). In contrast, much less is known about the impacts of milder to moderate forms of disturbance such as patchiness, extent and quality of native habitat, and forest maturity (but see Johansson et al. 2012;Pastore et al. 2014). ...
... There is extensive evidence documenting that lichen diversity declines with increasing disturbance (Lücking 1995;Ellis and Coppins 2010;Benítez et al. 2012;Nylén and Luoto 2015;Ardelean et al. 2015;Tarasova et al. 2017;Zemanová et al. 2017). However, while this connection is wellestablished, prior studies have almost exclusively focused on subsets of total lichen diversity (e.g., macrolichens or epiphytes) and treated disturbance either qualitatively by assigning broadly defined classes (Lücking 1995;Rivas Plata et al. 2008;Benítez et al. 2012) or utilized time since disturbance as a proxy for degree of disturbance (Hestmark et al. 2007;O'Bryan et al. 2009;Ellis and Coppins 2010;Chen 2014, 2015;Nelson et al. 2015;Arsenault Fig. 5 Sexual lichen diversity increases linearly with decreasing disturbance as in previous analyses, although two additional variables, precipitation (x-axis), and rock cover (columns) modulate this relationship Tarasova et al. 2017;Zemanová et al. 2017). ...
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The impacts of disturbance on biodiversity and distributions have been studied in many systems. Yet, comparatively less is known about how lichens–obligate symbiotic organisms–respond to disturbance. Successful establishment and development of lichens require a minimum of two compatible yet usually unrelated species to be present in an environment, suggesting disturbance might be particularly detrimental. To address this gap, we focused on lichens, which are obligate symbiotic organisms that function as hubs of trophic interactions. Our investigation was conducted in the southern Appalachian Mountains, USA. We conducted complete biodiversity inventories of lichens (all growth forms, reproductive modes, substrates) across 47, 1-ha plots to test classic models of responses to disturbance (e.g., linear, unimodal). Disturbance was quantified in each plot using a standardized suite of habitat quality variables. We additionally quantified woody plant diversity, forest density, rock density, as well as environmental factors (elevation, temperature, precipitation, net primary productivity, slope, aspect) and analyzed their impacts on lichen biodiversity. Our analyses recovered a strong, positive, linear relationship between lichen biodiversity and habitat quality: lower levels of disturbance correlate to higher species diversity. With few exceptions, additional variables failed to significantly explain variation in diversity among plots for the 509 total lichen species, but we caution that total variation in some of these variables was limited in our study area. Strong, detrimental impacts of disturbance on lichen biodiversity raises concerns about conservation and land management practices that fail to incorporate complete estimates of biodiversity, especially from ecologically important organisms such as lichens.
... Intact forests are important repositories of precious irreplaceable and often endangered biodiversity, and they provide a wide range of valuable ecosystem services [1]. The reasons behind the increasing interest in studying intact forests are four-fold: (1) the need to improve the management of second-growth forests [2][3][4][5][6]; (2) the sheer scientific curiosity in studying the most complex natural terrestrial ecosystems still at hand in many geographical regions of the Earth [7,8]; (3) the need to protect fragile habitats, many of them hosted by intact forests [9,10]; and (4) the issue of forest carbon pool [11,12]. ...
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The study zone includes one of the largest montane old-growth forests in Europe (Slatioara UNESCO site), and understanding the structure and functioning of sill intact forests in Europe is essential for grounding management strategies for secondary forests. For this reason, we set out to analyze the dependencies between aboveground biomass (AgB), tree species and size diversity and terrain morphology, as well as the relationship between biomass and diversity, since neither of these issues have been sufficiently explored. We found that tree species diversity decreases with increased solar radiation and elevation. Tree size heterogeneity reaches its highest mean values at elevations between 1001 and 1100 m, on slopes between 50 and 60 degrees. AgB is differentiated with elevation; the highest mean AgB (293 tonnes per hectare) is recorded at elevations between 801 and 900 m, while it decreases to 79 tonnes per hectare at more than 1500 m a.s.l. It is also influenced by tree species diversity and tree size heterogeneity, with the highest AgB reached in the most complex forest ecosystems in terms of structural diversity. We showed that intact temperate montane forests develop maximum biomass for optimum species diversity and highest size heterogeneity; all three are modulated mainly by elevation.
... Sun-exposed live trees, another disturbance legacy, also provide an important habitat for many lichen species (Ellis, 2012). Therefore, it is not only deadwood quantity and quality, but also the proportion of legacy trees post disturbance that may play a crucial role in maintaining the diversity and resilience of forest communities (Zemanová et al., 2017). In addition, biological legacies often serve as the starting point for community reorganisation after passing ecological bottlenecks (Lõhmus et al., 2017). ...
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Aim Natural disturbances influence forest structure, successional dynamics, and, consequently, the distribution of species through time and space. We quantified the long-term impacts of natural disturbances on lichen species richness and composition in primary mountain forests, with a particular focus on the occurrence of endangered species. Location Ten primary mountain spruce forest stands across five mountain chains of the Western Carpathians, a European hotspot of biodiversity. Methods Living trees, snags, and downed logs were surveyed for epiphytic and epixylic lichens in 57 plots. Using reconstructed disturbance history, we tested how lichen species richness and composition was affected by the current forest structure and disturbance regimes in the past 250 years. We also examined differences in community composition among discrete microhabitats. Results Dead standing trees as biological legacies of natural disturbances promoted lichen species richness and occurrence of threatened species at the plot scale, suggesting improved growing conditions for rare and common lichens during the early stages of recovery post-disturbance. However, high-severity disturbances compromised plot scale species richness. Both species richness and the number of old-growth specialists increased with time since disturbance (i.e. long-term uninterrupted succession). No lichen species was strictly dependent on live trees as a habitat, but numerous species showed specificity to logs, standing objects, or admixture of tree species. Main conclusions Lichen species richness was lower in regenerating, young, and uniform plots compared to overmature and recently disturbed areas. Natural forest dynamics and its legacies are critical to the diversity and species composition of lichens. Spatiotemporal consequences of natural dynamics require a sufficient area of protected forests for provisioning continual habitat variability at the landscape scale. Ongoing climatic changes may further accentuate this necessity. Hence, we highlighted the need to protect the last remaining primary forests to ensure the survival of regionally unique species pools of lichens.
... The spatial continuity of suitable habitats is undoubtedly the factor that determines these results (Figure 1a), and justifies the (admittedly small) differences with the observed situation between NOG sites (Figure 1c). In addition, our old-growth forest sites are characterized by a high number of old and uneven trees ( Table 1) that may represent suitable intermediate substrates (micro-refugia) for the low-range dispersal diaspores [42]. This structural complexity may contribute to this trend of vegetative species. ...
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1) Research Highlights: The work studied the beta diversity patterns of epiphytic lichens as a function of their reproductive strategies in old-growth and non-old growth forests from the Mediterranean area. (2) Background and Objectives: The reproductive strategies of lichens can drive the dispersal and distribution of species assemblages in forest ecosystems. To further investigate this issue, we analyzed data on epiphytic lichen diversity collected from old-growth and non-old growth forest sites (36 plots) located in Cilento National Park (South Italy). Our working hypothesis was that the dispersal abilities due to the different reproductive strategies drove species beta diversity depending on forest age and continuity. We expected a high turnover for sexually reproducing species and high nestedness for vegetative ones. We also considered the relationship between forest continuity and beta diversity in terms of species rarity. (3) Materials and Methods: we used the Bray-Curtis index of dissimilarity to partition lichen diversity into two components of beta diversity for different subsets (type of forest, reproductive strategy, and species rarity). (4) Results: The two forest types shared most of the common species and did not show significant differences in alpha and gamma diversity. The turnover of specific abundance was the main component of beta diversity , and was significantly greater for sexually reproducing species as compared to vegetative ones. These latter species had also the least turnover and greater nestedness in old-growth forests. Rare species showed higher turnover than common ones. (5) Conclusions: Our results suggest that sexually reproducing lichen species always have high turnover, while vegetative species tend to form nested assemblages, especially in old-growth forests. The rarity level contributes to the species turnover in lichen communities. Contrary to what one might expect, the differences between old-growth and non-old growth forests are not strong.
... Preventing natural disturbances and conducting salvage logging can cause habitat loss for many forest specialist species, and it has a detrimental effect on a broad array of forest communities, including birds, saproxylic beetles, springtails, wood-inhabiting fungi, and epixylic lichens Mikoláš et al., 2017b). Some forest specialist species are dependent on the continuous presence of primary forest habitat features, such as old trees, high amounts and diversity of deadwood, and natural dynamics often result in open to semi-open structure of the forest canopy (Miklin and Cizek, 2014;Zemanová et al., 2017). For these species, conservation of primary forests is critical. ...
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Book
A comprehensive, up-to-date review of lichens as biomonitors of air pollution (bioindication, metal and radionuclide accumulation, biomarkers), and as monitors of environmental change (including global climate change and biodiversity loss) in a wide array of terrestrial habitats. Several methods for using lichens as biomonitors are described in a special section of the book.
Article
Abundant canopy lichen communities characterize wet-temperate rainforests on the windward slopes of interior mountain ranges in north-central British Columbia, Canada. Historically, these forests have regenerated through gap-dynamics; however, our knowledge of lichen colonization within gaps is limited. We have now compared lichen biomass on regenerating trees in naturally occurring 1-3 ha gap-disturbances (these gaps presumed to have originated from insect out-breaks in the late 1800's) with those on regenerating trees of similar age growing in the understory of the surrounding old growth forest. Only small differences were seen in total lichen biomass on regenerating trees between the two settings, however, analysis of the individual lichen groups (Alectoria, Bryoria, Foliose, and Cyanolichen) revealed striking differences. The Bryoria group was 35% more abundant on gap trees (632 g/tree) and was distributed vertically through a larger proportion of the tree crown. The Cyanolichen functional group was largely absent from gap trees, despite high levels of biomass loading (1,332 kg/ha) in the surrounding old-growth stand. Alectoria and Foliose functional groups did not differ significantly in biomass or distribution between regenerating trees of the two types. Tree size positively affected lichen loading. Total lichen biomass was 38% greater on the larger size class (31-44 cm dbh) regenerating trees, with the Alectoria functional group alone having 45% greater biomass on larger trees. Presence or absence of leaves on branch substrate had no effect on lichen loading. Stand-level projections indicate that the old growth forest had 19% more arboreal lichen biomass (2,684 kg/ha) and contained greater lichen species diversity than did the "second-growth" regenerating forest patches. The low cyanolichen biomass in naturally occurring gap openings poses concern for the proposed utility of "new-forestry" type harvesting practices to retain canopy biodiversity using current harvest rotation intervals.
Article
Old trees have declined in Europe due to agricultural intensification and forestry. For shade-intolerant epiphytic species occurring on old trees in semi-open landscapes, host tree numbers have further decreased because of shading by developing secondary woodland. Moreover, in this habitat, regeneration that could replace the extant old trees is low. This suggests that epiphytic species associated with old trees are declining. However, for species with low extinction rates, the decline may be slow and hard to elucidate.We investigated the persistence of five old-oak-associated epiphytic lichens with different traits by simulating metapopulation dynamics using Bayesian incidence function models for dynamic landscapes. With an oak-rich landscape as a reference, we investigated effects of (i) drastic habitat decline, (ii) conservation actions such as clearing around trees or increased regeneration rate, (iii) low tree regeneration and (iv) clearing and increased regeneration after 100 years of low regeneration.After drastic habitat decline, the number of occupied trees continued to decrease, displaying long time-lags before reaching new metapopulation equilibriums. Lichen extinction risks increased with decreasing habitat and were highest for species that only colonise very old trees or have large dispersal propagules. In landscapes with low tree densities, conservation actions had only minor effects on lichen extinction risks.Low tree regeneration rates increased lichen extinction risks, but species declines were slow. Conservation actions that increased regeneration after 100 years of low regeneration decreased the extinction risks to very low levels.Synthesis and applications. Due to low rates of local extinction, epiphytes display long time-lags to reach new equilibriums after habitat loss. Thus, we should expect ongoing declines in epiphyte metapopulations in landscapes where old trees have recently declined. Slow extinction gives an opportunity to improve persistence by conservation actions, but the success depends on species traits and the current density of old trees. In landscapes with many old but few young trees, epiphytes may persist if conservation actions quickly address the need to increase tree regeneration rates. The best conservation approach for long-term persistence of epiphytic lichens is to ensure regular tree regeneration in landscapes with a current high density of old trees.