Community Analysis Reveals Close Affinities Between Endophytic and Endolichenic Fungi in Mosses and Lichens

Endolichenic fungi live in close association with algal photobionts inside asymptomatic lichen thalli and resemble fungal endophytes of plants in terms of taxonomy, diversity, transmission mode, and evolutionary history. This similarity has led to uncertainty regarding the distinctiveness of endolichenic fungi compared with endophytes. Here, we evaluate whether these fungi represent distinct ecological guilds or a single guild of flexible symbiotrophs capable of colonizing plants or lichens indiscriminately. Culturable fungi were sampled exhaustively from replicate sets of phylogenetically diverse plants and lichens in three microsites in a montane forest in southeastern Arizona (USA). Intensive sampling combined with a small spatial scale permitted us to decouple spatial heterogeneity from host association and to sample communities from living leaves, dead leaves, and lichen thalli to statistical completion. Characterization using data from the nuclear ribosomal internal transcribed spacer and partial large subunit (ITS-LSU rDNA) provided a first estimation of host and substrate use for 960 isolates representing five classes and approximately 16 orders, 32 families, and 65 genera of Pezizomycotina. We found that fungal communities differ at a broad taxonomic level as a function of the phylogenetic placement of their plant or lichen hosts. Endolichenic fungal assemblages differed as a function of lichen taxonomy, rather than substrate, growth form, or photobiont. In plants, fungal communities were structured more by plant lineage than by the living vs. senescent status of the leaf. We found no evidence that endolichenic fungi are saprotrophic fungi that have been “entrapped” by lichen thalli. Instead, our study reveals the distinctiveness of endolichenic communities relative to those in living and dead plant tissues, with one notable exception: we identify, for the first time, an ecologically flexible group of symbionts that occurs both as endolichenic fungi and as endophytes of mosses.     

ITS1 metabarcoding highlights low specificity of lichen mycobiomes at a local scale

As self‐supporting and long‐living symbiotic structures, lichens provide a habitat for many other organisms beside the traditionally considered lichen symbionts—the myco‐ and the photobionts. The lichen‐inhabiting fungi either develop diagnostic phenotypes or occur asymptomatically. Because the degree of specificity towards the lichen host is poorly known, we studied the diversity of these fungi among neighbouring lichens on rocks in an alpine habitat. Using a sequencing metabarcoding approach, we show that lichen mycobiomes clearly reflect the overlap of multiple ecological sets of taxa, which differ in their trophic association with lichen thalli. The lack of specificity to the lichen mycobiome is further supported by the lack of community structure observed using clustering and ordination methods. The communities encountered across samples largely result from the subsampling of a shared species pool, in which we identify three major ecological components: (i) a generalist environmental pool, (ii) a lichenicolous/endolichenic pool and (iii) a pool of transient species. These taxa majorly belong to the fungal classes Dothideomycetes, Eurotiomycetes and Tremellomycetes with close relatives in adjacent ecological niches. We found no significant evidence that the phenotypically recognized lichenicolous fungi influence the occurrence of the other asymptomatic fungi in the host thalli. We claim that lichens work as suboptimal habitats or as a complex spore and mycelium bank, which modulate and allow the regeneration of local fungal communities. By performing an approach that minimizes ambiguities in the taxonomic assignments of fungi, we present how lichen mycobiomes are also suitable targets for improving bioinformatic analyses of fungal metabarcoding.     

Diversity and distribution of cultured endolichenic fungi in the Ny-Ålesund Region,Svalbard (High Arctic)

Endolichenic fungi within 17 lichen species in the area near Ny-Ålesund (Svalbard, High Arctic) were studied by a culture-based method. The 247 fungal isolates were obtained from 2712 lichen thallus segments. The colonization rate of endolichenic fungi ranged from 1.6 to 26.5 %, respectively. These isolates were identified to 40 fungal taxa, including 35 Ascomycota (10 orders), 4 Basidiomycota (3 orders), and 1 unidentified fungus. Thelebolales was the most abundant order, while Sordariales were the most diverse order. The common fungal taxa shared by more than 3 lichen species were Thelebolus microsporus (93 isolates), Coniochaeta hoffmannii (7 isolates), Sarocladium kiliense (33 isolates), Coniochaeta sp. 1 (5 isolates), Coniochaeta sp. 4 (28 isolates), and Coniochaeta sp. 2 (5 isolates). Low Sorenson’s similarity coefficients were observed among different lichen species, indicating that host-related factor may shape the endolichenic fungal communities in this region. In addition, no endolichenic fungal taxa were previously found in the Antarctica and Austrian Alps, suggesting endolichenic fungal communities in this region might be also shaped by the Arctic climate. The results demonstrate the existence of specific cultured endolichenic fungal species, which may be suitable objects for further study of their possible functional roles in the lichen thalli.     

Phorophyte specificity and environmental parameters versus stochasticity as determinants for species composition of corticolous crustose lichen communities in the Atlantic rain forest of northeastern Brazil

A transect of 47 mature trees was studied within an Atlantic rain-forest plot in northeastern Brazil to determinate effects of phorophyte specificity and environmental parameters vs. stochasticity on the structure of corticolous, crustose microlichen communities. A total of 150 lichen species was found, most being rare to extremely rare. Multivariate analysis of sample plots indicated subtle phorophyte preferences among certain lichen species, corresponding to differences in bark pH, degree of bark shedding, density and size of bark lenticels, and presence of milk sap. Individual and multiple regressions revealed correlations between lichen species richness; respectively, area cover and bark pH (negative); density and size of bark lenticels (negative); degree of bark shedding (negative); presence of milk sap (positive); and diffuse site factor (positive). No strongly delimited lichen communities were detected, but cluster analysis revealed three main groups and six subgroups with slightly different lichen species composition, each one with characteristic indicator species but with highly variable overall species composition. Beta diversity was high among samples and lacked spatial structure. However, beta diversity was significantly lower among samples belonging to the same tree species, independent of their spatial arrangement. It was concluded that community formation in tropical rain-forest understory lichens subtly correlates with two main environmental factor complexes—phorophyte bark characteristics and microclimate—but is to a large extent determined by the stochastic effects of species dispersal, especially of rare species.     

ITS2 metabarcoding analysis complements lichen mycobiome diversity data

Lichen thalli harbor complex fungal communities (mycobiomes) of species with divergent trophic and ecological strategies. The complexity and diversity of lichen mycobiomes are still largely unknown, despite surveys combining culture-based methods and high-throughput sequencing (HTS). The results of such surveys are strongly influenced by the barcode locus chosen, its sensitivity in discriminating taxa, and the depth to which public sequence repositories cover the phylogenetic spectrum of fungi. Here, we use HTS of the internal transcribed spacer 2 (ITS2) to assess the taxonomic composition and diversity of a well-characterized, alpine rock lichen community that includes thalli symptomatically infected by lichenicolous fungi as well as asymptomatic thalli. Taxa belonging to the order Chaetothyriales are the major components of the observed lichen mycobiomes. We predict sequences representative of lichenicolous fungi characterized morphologically and assess their asymptomatic presence in lichen thalli. We demonstrated the limitations of metabarcoding in fungi and show how the estimation of species diversity widely differs when ITS1 or ITS2 are used as barcode, and particularly biases the detection of Basidiomycota. The complementary analysis of both ITS1 and ITS2 loci is therefore required to reliably estimate the diversity of lichen mycobiomes.     

Environmental filtering structures fungal endophyte communities in tree bark

The factors that control the assembly and composition of endophyte communities across plant hosts remains poorly understood. This is especially true for endophyte communities inhabiting inner tree bark, one of the least studied components of the plant microbiome. Here, we test the hypothesis that bark of different tree species acts as an environmental filter structuring endophyte communities, as well as the alternative hypothesis, that bark acts as a passive reservoir that accumulates a diverse assemblage of spores and latent fungal life stages. We develop a means of extracting high‐quality DNA from surface sterilized tree bark to compile the first culture‐independent study of inner bark fungal communities. We sampled a total of 120 trees, spanning five dominant overstorey species across multiple sites in a mixed temperate hardwood forest. We find that each of the five tree species harbour unique assemblages of inner bark fungi and that angiosperm and gymnosperm hosts harbour significantly different fungal communities. Chemical components of tree bark (pH, total phenolic content) structure some of the differences detected among fungal communities residing in particular tree species. Inner bark fungal communities were highly diverse (mean of 117–171 operational taxonomic units per tree) and dominated by a range of Ascomycete fungi living asymptomatically as putative endophytes. Together, our evidence supports the hypothesis that tree bark acts as an environmental filter structuring inner bark fungal communities. The role of these potentially ubiquitous and plant‐specific fungal communities remains uncertain and merits further study.     

New Lineages of Elaphocordyceps Harboring in Lichen Thalli

All species of Elaphocordyceps parasitize the fungal genus Elaphomyces, except for three species growing on scarabid beetle larvae or cicada nymphs. During our study on the diversity of culturable endolichenic fungi, some Elaphocordyceps species are found widely harboring in lichen thalli. A total of 64 fungal strains belonging to Elaphocordyceps were isolated from 42 lichen samples respectively collected from 5 provinces of China and the Antarctic. Phylogenetic analysis based on ITS nrDNA shows that these endolichenic fungi are possibly heterospecific. The endophytic fungi of plant often provide benefits to their hosts. However, the endolichenic fungi may be parasites or nutrient competitors of the mycobiont, because they have to obtain nutrient components from mycobionts or photobionts. Our study partly proves this hypothesis, since most known species of Elaphocordyceps are parasites of fungi.     

Corticolous lichens as potential bioindicators of fire history: a study in the cerrado of the Distrito Federal, central Brazil

Abstract. The aim of this study was to investigate the potential use of epiphytic corticolous lichens as indicators of fire history in the cerrado (savannas) of central Brazil. Work was carried out at the Reserva Ecológica do IBGE and the Jardim Botânico de Brasilia, 33 km outside Brasilia D.F., in ten plots of cerrado denso within the ‘Fire Project’ area. Each plot was subjected to a specific prescribed burning regime, with study sites varying from a plot protected from fire for over 20 years to a plot burned every 2 years. Research was carried out in two stages: (1) a preliminary survey of plots with different fire histories, measuring variables about the lichen habitat and the lichen communities present in the habitats; (2) lichen sampling in plots with different fire histories, where collection and identification of lichen species took place. Field techniques used included plotless sampling, and identification of lichens was carried out using taxonomic keys, both in the field and in the laboratory. The results show that fire is a major determinant of epiphytic corticolous lichen communities in cerrado denso vegetation. The abundance, distribution and recolonization of lichen communities can clearly be correlated with the frequency and behaviour, in terms of homogeneity and flame heights, of the fires that have occurred in each of the plots surveyed. Particular lichen species also show differential sensitivities to fire frequency and behaviour. This study shows that responses of corticolous lichens, at both the community and species level, can be used as bioindicators of fire history in areas of cerrado denso vegetation in central Brazil.     

Population dynamics of the lichen genus Bulbothrix Hale as potential bioindicators of 'time-since-last-fire' in the cerrado of the Distrito Federal, central Brazil

This paper investigates the potential use of the corticolous lichen genus Bulbothrix Hale as a bioindicator of ‘time-since-last-fire’ in the cerrado (savannas) of central Brazil. Work was carried out at the Reserva Ecológica do IBGE and the Jardim Botãnico de Brasilia, 33 km outside Brasilia D.F., in plots of cerrado denso with known fire histories within the ‘Fire Project’ area. Measurements of abundance and thallus size were taken of all Bulbothrix individuals encountered up to 2 m on the trunks of three phorophyte species. The results show that abundances and thalli sizes of the Bulbothrix populations can be correlated with the ‘time-since-last-fire’ that had occurred in each of the plots. This study shows that is is possible to use characteristics of specific lichen populations as bioindicators of fire history.     

乌鲁木齐南部山区森林生态系统树生地衣群落结构

为了探明乌鲁木齐南部山区树生地衣种类及其群落结构特征,应用多元分析中的主成分分析及聚类分析方法,对分布在乌鲁木齐南部山区森林生态系统中的树生地衣植物群落进行数量分类,并对其群落结构的物种多样性、相似性和均匀度等群落参数进行了比较系统的研究。结果表明,分布在乌鲁木齐南部山区的树生地衣共有39种,隶属于5目13科26属。根据多元分析结果,将该地区的树生地衣划分为3种类型：（1）小茶渍（Lecanorahageni（Ach．）Ach．）＋蜈蚣衣（肋归ciastellaris（L．）Nyl．）＋柳茶渍（￡-。saligna（Schrad．）Zahlbr．）群落;（2）斑面蜈蚣衣（Physciaaipolia（Humb．）Furm．）＋对开蜈蚣衣（Ph．dimidiata（Arn．）Nyl．）＋喇叭石蕊（Cladoniapyxidata（L．）Hoffm．）群落：（3）拟石黄衣（Xanthoria fallax（Hepp）Arnold．）＋丽石黄衣（xelegans（Link．）Th．Fr．）群落。群落3的多样性指数最大,为1．509,其次为群落2,其多样性指数为1．109,群落1的多样性指数最低,为1．088。同时,研究发现海拔高度和树种是影响乌鲁木齐南部山区森林生态系统树生地衣结构的两个重要因素。     

The Lichen Connections of Black Fungi

Many black meristematic fungi persist on rock surfaces—hostile and exposed habitats where high doses of radiation and periods of desiccation alternate with rain and temperature extremes. To cope with these extremes, rock-inhabiting black fungi show phenotypic plasticity and produce melanin as cell wall pigments. The rather slow growth rate seems to be an additional prerequisite to oligotrophic conditions. At least some of these fungi can undergo facultative, lichen-like associations with photoautotrophs. Certain genera presenting different lifestyles are phylogenetic related among the superclass Dothideomyceta. In this paper, we focus on the genus Lichenothelia, which includes border-line lichens, that is, associations of melanised fungi with algae without forming proper lichen thalli. We provide a first phylogenetic hypothesis to show that Lichenothelia belongs to the superclass Dothideomyceta. Further, culture experiments revealed the presence of co-occurring fungi in Lichenothelia thalli. These fungi are related to plant pathogenic fungi (Mycosphaerellaceae) and to other rock-inhabiting lineages (Teratosphaeriaceae). The Lichenothelia thallus-forming fungi represent therefore consortia of different black fungal strains. Our results suggest a common link between rock-inhabiting meristematic and lichen-forming lifestyles of ascomycetous fungi.     

Functional response of lignicolous fungal guilds to bark beetle deforestation

Conifer-dominated forests in the northern hemisphere are prone to large-scale natural disturbances, yet our understanding of their effects beyond changes in species diversity is limited. Bark beetle disturbances provide dead wood for lignicolous fungal guilds and increase insolation but also desiccation. We investigated whether species richness of these guilds increases and functional diversity decreases after bark beetle disturbance, which would promote through habitat filtering the coexistence of species adapted to harsh conditions, i.e. light stress for lichens and substrate desiccation for wood-inhabiting fungi.We sampled epixylic and epiphytic lichens (primary producers) and wood-inhabiting fungi (mainly wood decomposers, some form ectomycorrhizas) in the Bohemian Forest (Long Term Ecological Research – LTER – Site Bavarian Forest National Park), an area in Central Europe most heavily affected by the bark beetle Ips typographus, on undisturbed plots and disturbed plots with spruce (Picea abies) dieback 8 years ago. We analysed species diversity, functional diversity (optimized by phylogeny), and functional compositions.Species richness of lichens but not that of wood-inhabiting fungi was higher on disturbed plots than on undisturbed plots. Community compositions of both guilds differed considerably on disturbed and undisturbed plots. On both types of plots, lichen communities were clustered according to functional diversity, which indicated habitat filtering, and fungal communities were overdispersed, which indicated competition. Disturbance increased the strength of these two patterns only slightly and was significant only for fungi. Single-trait analysis revealed changes in the functional composition; on disturbed plots, lichenous species with larger and more complex growth forms and fungi with large, perennial fruit bodies were favoured. Although the forest canopy changed tremendously because of the bark beetle disturbance, the most important driver of lichen and fungal diversity and mean trait assemblages seemed to be the enrichment of dead wood. The changes in insolation and moisture did not act as habitat filters for either guild. This indicated that the assembly patterns of lichen and fungal communities in coniferous forests are not affected by stand-replacing disturbances in contrast to the predictions for other disturbance regimes.     

The yeast lichenosphere: high diversity of basidiomycetes from the lichens Tephromela atra and Rhizoplaca melanophthalma

Lichens are well-known examples of complex symbiotic associations between organisms from different Kingdoms. Microfungi in particular, establish diverse associations with the hosting lichen thallus, as species-specific parasites or transient co-inhabitants. The whole community of lichen-associated fungi constitute the ‘lichen mycobiome’ comprising both ascomycetes and basidiomycetes, including filamentous and yeast taxa. Metabarcoding results and microscopy analyses show that in some thalli, basidiomycetes are frequent lichen-associated fungi but still only a few species could be axenically isolated and morphologically characterized. Within a broad project aiming at characterizing the mycobiome diversity by culture-dependent and independent approaches in two lichen species selected as reference models – Rhizoplaca melanophthalma and Tephromela atra, we succeed in isolating and culturing 76 new strains of basidiomycetous yeasts. The lichen thalli were collected in different mountain regions worldwide and at relatively high elevation. The yeast strains were isolated on different growth media and were studied for their morphological and genetic diversity. Nuclear internal transcribed spacer (ITS) and ribosomal large subunit (LSU) sequence analyses identified them to belong to ten families within the orders Agaricostilbomycetes, Cystobasidiomycetes, Microbotryomycetes, Tremellomycetes and Ustilaginomycetes. The yeasts here detected showed patterns of host-preference in a few cases and they are potentially related to the ecological conditions.     

乌鲁木齐南部山区森林生态系统树生地衣群落结构

为了探明乌鲁木齐南部山区树生地衣种类及其群落结构特征, 应用多元分析中的主成分分析及聚类分析方法, 对分布在乌鲁木齐南部山区森林生态系统中的树生地衣植物群落进行数量分类, 并对其群落结构的物种多样性、相似性和均匀度等群落参数进行了比较系统的研究。结果表明, 分布在乌鲁木齐南部山区的树生地衣共有39种, 隶属于5目13科26属。根据多元分析结果, 将该地区的树生地衣划分为3种类型: (1) 小茶渍(Lecanora hageni (Ach.) Ach.) + 蜈蚣衣(Physcia stellaris (L.) Nyl.) + 柳茶渍(L. saligna (Schrad.) Zahlbr.)群落; (2) 斑面蜈蚣衣(Physcia aipolia (Humb.) Furm.) + 对开蜈蚣衣(Ph. dimidiata (Arn.) Nyl.) + 喇叭石蕊(Cladonia pyxidata (L.) Hoffm.)群落; (3) 拟石黄衣(Xanthoria fallax (Hepp) Arnold.) + 丽石黄衣(X. elegans (Link.) Th. Fr.)群落。群落3的多样性指数最大, 为1.509, 其次为群落2, 其多样性指数为1.109, 群落1的多样性指数最低, 为1.088。同时, 研究发现海拔高度和树种是影响乌鲁木齐南部山区森林生态系统树生地衣结构的两个重要因素。     

Composition and diversity of endolichenic microfungal communities from saxicolous lichens at Nahal Boker,the central Negev Desert,Israel

We studied the endolichenic fungal communities from saxicolous lichens occupying the cobbles at Nahal Boker, the central Negev Desert, Israel. Overall, 101 species belonging to 64 genera were isolated from 12 lichen species collected in three seasons from the south-facing slope (SFS) and north-facing slope (NFS) of the wadi. The endolichenic communities possessed a set of traits, which helped them to cope with harsh internal and external conditions. It included a prevalence of melanin-containing fungi with thick-walled and multicellular spores and a comparatively high contribution of thermotolerant species and species with meiospore-producing life cycle stage at the more microclimatically severe SFS. Species richness and isolate density of endolichenic communities was the highest in fruticose lichens with thick and wrinkled thalli, and the lowest in endolithic species possessing thin and smooth thalli. The communities from lichens formed a more diverse group than those from surrounding cobbles probably due to the influence of various species of lichens belonging to different growth forms.     

天山森林生态系统树生地衣植物群落数量分类及其物种多样性的研究

地衣是由低等植物中的藻类与菌类中的真菌和兰细菌共生而成的一群特殊的植物。由于耐寒耐旱对生活中的养分要求不高,在养纷贫瘠、环境恶劣的高山寒漠、平原、戈壁和沙漠中地衣都能生长,因而广泛地分布和生长在不同的生态环境中。有关新疆地衣方面的研究报道集中在物种分类水平上,对于地衣群落结构方面的研究比较少。因此,我们应用多元分析中的主分量分析及聚类分析方法对分布在天山森林生态系统中树生地衣植物群落进行数量分类并对群落结构物种多样性、相似性和均匀度等群落参数进行了比较系统的研究。结果表明, 在西部天山不同森林生态系统中树生地衣群落的分布与海拔高度和树种有密切的关系, 不同海拔的不同类型的森林生态系统中分布着不同种类的树生地衣植物。 根据多元分析结果和生境的综合特征,该地区的树生地衣可划分为4种类型: 1) 茎口果粉衣+金黄茶衣群丛Chaenotheca stemonea+Candellaria aurella Association; 2)叉小孢衣+裸扁枝衣+粉唇蜈蚣衣群丛Bryoria furcellata+Evernia esorediosa+Physcia tribacoides Association; 3)亚广开梅衣+槽梅衣+疑小梅衣群丛Parmelia fertilis+Parmelia sulcata+Parmeliopsis ambigua Association; 4)睫毛黑蜈蚣衣+黑蜈蚣衣群丛Phaeophyscia ciliata+Phaeophyscia nigricans Association。其群落多样性指数以亚广开梅衣+槽梅衣+疑小梅衣群丛为最高 (1.920), 叉小孢衣+裸扁枝衣+粉唇蜈蚣衣群丛为最低 (1.562)。     

Fungal community composition shifts along a leaf degradation gradient in a European beech forest

Aims

The fungal communities in living and decomposed leaves of European Beech (Fagus sylvatica) were compared to identify the phyllosphere fungi involved in litter decomposition at a site in Bavaria, Germany.

Methods

New primers were designed to cover a broad range of fungal ribosomal DNA sequence diversity. Following ‘environmental PCR’, clone libraries from each of five samples of living leaves (surface-sterilized and untreated), freshly fallen, initially and highly decomposed leaves, were screened using RFLP fingerprinting.

Results

Statistical analysis (ANOSIM) revealed that the fungal communities colonizing living (a) and initially decomposed leaves (c) significantly differed between each other and from freshly fallen (b) and highly decomposed leaves (d). Fungal assemblages of a and d were statistically indistinguishable from each other and from the endophyllous fungal community in living leaves.

Conclusions

The results showed that endophyllous fungi play a role throughout the whole decomposition process of beech leaf litter. Therefore, clarification of the life cycle of certain endophytic and/or soil fungi may only be achieved by considering both phyllosphere and soil habitats.     

新疆天山西部山脉森林生态系统地衣群落结构的初步研究

 根据多年的研究资料并采用聚类分析方法对分布在天山西部山脉的地衣群落结构进行了研究。结果表明,分布在该地区的地衣种类形成了6种群落:1) 土星猫耳衣（Leptogium saturninum)＋矮石蕊(Cladonia humilis)＋兰灰蜈蚣衣（Physcia caesia）群落;2）黑穗石蕊（Cladonia amaurocr     

Photobiont selectivity leads to ecological tolerance and evolutionary divergence in a polymorphic complex of lichenized fungi

Background and Aims

The integrity and evolution of lichen symbioses depend on a fine-tuned combination of algal and fungal genotypes. Geographically widespread species complexes of lichenized fungi can occur in habitats with slightly varying ecological conditions, and it remains unclear how this variation correlates with symbiont selectivity patterns in lichens. In an attempt to address this question, >300 samples were taken of the globally distributed and ecologically variable lichen-forming species complex Tephromela atra, together with closely allied species, in order to study genetic diversity and the selectivity patterns of their photobionts.

Methods

Lichen thalli of T. atra and of closely related species T. grumosa, T. nashii and T. atrocaesia were collected from six continents, across 24 countries and 62 localities representing a wide range of habitats. Analyses of genetic diversity and phylogenetic relationships were carried out both for photobionts amplified directly from the lichen thalli and from those isolated in axenic cultures. Morphological and anatomical traits were studied with light and transmission electron microscopy in the isolated algal strains.

Key Results

Tephromela fungal species were found to associate with 12 lineages of Trebouxia. Five new clades demonstrate the still-unrecognized genetic diversity of lichen algae. Culturable, undescribed lineages were also characterized by phenotypic traits. Strong selectivity of the mycobionts for the photobionts was observed in six monophyletic Tephromela clades. Seven Trebouxia lineages were detected in the poorly resolved lineage T. atra sensu lato, where co-occurrence of multiple photobiont lineages in single thalli was repeatedly observed.

Conclusions

Low selectivity apparently allows widespread lichen-forming fungi to establish successful symbioses with locally adapted photobionts in a broader range of habitats. This flexibility might correlate with both lower phylogenetic resolution and evolutionary divergence in species complexes of crustose lichen-forming fungi.     

ECOLOGY OF FOLIICOLOUS LICHENS AT THE ‘ BOTARRAMA ’ TRAIL (COSTA RICA), A NEOTROPICAL RAINFOREST. IV. SPECIES ASSOCIATIONS,THEIR SALIENT FEATURES AND THEIR DEPENDENCE ON ENVIRONMENTAL VARIABLES

A community ecology approach using an association of species test and a principal component analysis resulted in the recognition of two major and two minor foliicolous lichen communities in a neotropical rainforest. The major communities are governed by microclimatic factors, one characteristic of the shady understorey and the other confined to light gaps. The minor communities are due to subtle phorophyte preferences towards palm and dicot leaves. The shady understorey community is dominated by the families Arthoniaceae , Opegraphaceae , Trichotheliaceae and Pilocarpaceae , which predominantly have Phycopeltis as their phycobiont, thin thalli, abundant sexual reproduction, small ascospores produced in high numbers, and pycnidial conidiomata. The light-gap community is mainly composed of the families Gomphillaceae and Ectolechiaceae , with Trebouxia as their phycobiont, thickly crystalline or whitish, dispersed thalli, frequent asexual reproduction, large ascospores produced in low numbers, and specialized campylidia and hyphophores as conidiomata. Phycobiont, thallus structure, and the mode of reproduction are considered as adaptations to different microsites, whereas the shape and size of ascospores and conidia seem to be of less importance. The foliicolous lichen communities reflect the spatial and temporal structure of the forest, in particular the continuity of the shady understorey in comparison to the discontinuity of the light gaps. While the formation of the shady understorey community follows more deterministic patterns, the light-gap community exhibits high stochasticity.