Some advances in the study of lichens since the time of E. M. Holmes

Some of the principal advances in our knowledge of lichens made since the time of E. M. Holmes are briefly reviewed. Floristic studies on British lichens have continued and distribution maps of particular species are now being produced. These studies have shown that many species have disappeared from areas affected by air pollution by sulphur dioxide. Lichen taxonomy has seen the acceptance of chemical characters as valid taxonomic criteria, and the realization that ascus types, ascocarp structure and ascocarp ontogeny are more important at the generic level than ascospore characters alone. Lichens are not now thought of as a single taxonomic group but as fungi related to various orders of non-lichenized Ascomycotina, united only in their common method of nutrition (symbiosis with algae); some lichenized and non-lichenized species with identical types of ascocarps are consequently being treated as members of the same genus. Considerable progress has been made in describing lichen communities characteristic of particular substrates and situations and in understanding the factors which may affect the occurrence of particular species. Lichens have proved to be particularly valuable indicators of mean air pollution levels and scales for the estimation of these levels based solely on the lichen vegetation have been devised. Physiological and ultrastructural studies on lichens have progressed rapidly in the last decade. Carbohydrates have been demonstrated to move from the algal to the fungal component and the mobile carbohydrates found to differ in lichens with different genera of algae. The algal and fungal partners have been isolated and studied in pure culture. Most attempts to synthesize lichens have met with little success but in 1970 a thallus was formed from its components in culture. It is now possible to grow some lichens under controlled conditions in the laboratory and these techniques, together with transplant experiments, will clearly assume considerable importance in the investigation of taxonomic and ecological problems in the future. Little progress has been made in the study of lichen cytology or the factors affecting the establishment of lichen thalli. Lichens constitute an important part of some ecosystems and their decline due to anthropogenic influences is consequently a matter of concern for all biologists.     

Ecological and biotechnological aspects of lichens

Lichens and the partners from three different kingdoms are both taxonomically and physiologically a very diverse group, which makes them interesting from both ecological and biotechnological points of view. A lichen is a mutual ecophysiological innovation in many extreme environments in which symbiosis seems to protect the partners. Lichen’s ability to grow in harsh environments can be advantageous, resulting in important ecological niches, or disadvantageous when lichens occupy and cause biodeterioration of cultural monuments. Recently, new candidate compounds for drugs, UVB protection, and antifreeze proteins for frozen foods were discovered. Lichens were also found to have potential in bioplastic degradation and prevention of desertification. Nevertheless, there is still large potential for further industrial screening and research on lichen products. Due to improved culture techniques of isolated symbionts, increased knowledge of their secondary metabolism and improved methods for solubilizing lichen metabolites, the screening and activity tests can be implemented more easily today than in the past.     

The association of oribatid mites with lichens

Oribatei (Acari, Cryptostigmata) are found in a variety of terrestrial habitats, and many are associated with lichens; the relationship ranges from casual to highly dependent. Eighty-three species associated with lichens have been surveyed, and a tentative classification, based on their ecological requirements, is presented: Group A consists of species restricted to lichens as a biotope, though occasionally occurring as accidentals in other habitats; Group B consists of species which while preferring lichens as a habitat and feeding source are also adapted to existence on other plants (though in some cases their immatures may be lichen-restricted); Group C consists of species which, though frequently found on lichens, are equally common in other biotopes, particularly mosses, and must be regarded as much more generalized in their feeding habits. Certain aspects of oribatid-lichen specificity are discussed. The importance of oribatid-lichen associations from the point of view of soil fertility and energetics is emphasized.     

A comprehensive catalogue of polyketide synthase gene clusters in lichenizing fungi

Lichens are fungi that form symbiotic partnerships with algae. Although lichens produce diverse polyketides, difficulties in establishing and maintaining lichen cultures have prohibited detailed studies of their biosynthetic pathways. Creative, albeit non-definitive, methods have been developed to assign function to biosynthetic gene clusters in lieu of techniques such as gene knockout and heterologous expressions that are commonly applied to easily cultivatable organisms. We review a total of 81 completely sequenced polyketide synthase (PKS) genes from lichenizing fungi, comprising to our best efforts all complete and reported PKS genes in lichenizing fungi to date. This review provides an overview of the approaches used to locate and sequence PKS genes in lichen genomes, current approaches to assign function to lichen PKS gene clusters, and what polyketides are proposed to be biosynthesized by these PKS. We conclude with remarks on prospects for genomics-based natural products discovery in lichens. We hope that this review will serve as a guide to ongoing research efforts on polyketide biosynthesis in lichenizing fungi.     

Lichens as material for Lepidoptera's housing: A molecular approach to a widespread and highly selective interaction

Interactions between lichens and invertebrates are widespread and have evolved independently in several orders of invertebrates. Lichens participate as food, shelter, background for mimicry, or as camouflage for animals to wear. For this study, we discovered caterpillars of the moth family Psychidae living inside bags made from silk and lichens. We used molecular techniques to identify the lichens present and analyzed caterpillar selectivity for lichen species. We selected 13 bags and recovered the ITS genetic marker for every visually different lichen fragment. Obtained sequences were compared against a newly created ITS database from lichens of the study area. Caterpillars only used eight out of the 300 lichen species present showing a strong selection tendency for microfoliose lichens containing sekikaic acid. Our results suggest that caterpillars select lichen species at a higher rate than what is expected based on their local abundances. We provide an accessible way to study these widespread interactions in future projects.     

Water relations and photosynthetic characteristics in different functional groups of epiphytic lichens in montane forest of Ailaoshan

Aims There are abundant epiphytic lichens in the tropical and subtropical montane forest ecosystems, which are important components of forest canopy and play a vital role in biodiversity conservation, environmental monitoring and nutrient cycling. In accordance with photobiont type, growth form and reproductive strategy, the epiphytic lichens can be divided into different functional groups, with different distribution patterns. In this study we aim to explain this phenomenon from the perspective of physiological ecology. Methods The maximum water content, water loss curves, photosynthetic water and light response curves were determined in four epiphytic lichen functional groups, including cyanolichens, fruticose lichens, broadly lobed foliose lichens and narrowly lobed foliose lichens. Important findings The functional characteristics of epiphytic lichens influence their maximum water-holding capacity and rate of water loss. The cyanolichens have higher maximum water content, while the fruticose lichens have a faster water loss. The cyanolichens that are widely distributed in the moist habitats require particularly high moisture for their photosynthetic activities; their optimal water content for photosynthesis is higher in comparison with other groups. They also have a low light compensation point and a high light saturation point, which explain the wide range of light intensity of the habitat. The fruticose lichens, widely distributed in the relatively arid habitats with high irradiance, have high light compensation point and light saturation point, and low optimum water content for photosynthesis. The broadly lobed foliose lichens and the narrowly lobed foliose lichens have a high light compensation point and light saturation point; they preferably occur in habitats with strong light.     

哀牢山山地森林不同附生地衣功能群的水分关系和光合生理特征

附生地衣是热带和亚热带山地森林生态系统中重要的结构性组分, 在生物多样性保护、环境监测、养分循环中发挥着重要作用。附生地衣按共生藻、生活型和繁殖策略的不同可划分为不同的功能群, 不同附生地衣功能群的分布格局存在较大的差异, 然而其生理生态机制仍不清楚。该研究以我国西南地区哀牢山亚热带山地森林中的附生地衣优势类群为研究对象, 对该地区蓝藻地衣、阔叶地衣、狭叶地衣及枝状地衣4种功能群的8种附生地衣的水分关系、光合生理特征等进行了测定分析, 结果显示: 不同功能群附生地衣的持水力和失水速率均存在差异, 其中蓝藻地衣具有较高的最大水分含量, 而枝状地衣的失水速率较快; 过高和过低的水分含量都会抑制附生地衣的光合作用, 但抑制程度有所差异; 蓝藻地衣的光合作用最适水分含量比较高, 表明它们的光合生理活动对水分条件要求较高, 所以它们偏好潮湿的生境, 同时蓝藻地衣的光补偿点比较低但光饱和点却不低, 反映出它们具有较宽的光强适应范围, 所以蓝藻地衣能够同时分布于强光和弱光生境中; 枝状地衣的光合最适水分含量较低, 表明它们的光合生理活动对水分条件要求不是很高, 能够适应较为干旱的环境, 同时枝状地衣的光补偿点和光饱和点都很高, 说明它们的光合生理活动对光照条件要求比较高, 所以它们广泛分布于强光生境中; 阔叶和狭叶地衣的光补偿点比较高, 说明它们更适应有充足光照条件的生境。     

Hydration-dependent photosynthetic production of lichens: what do laboratory studies tell us about field performance?

Extensive investigations made in the past two decades on lichen photosynthesis in relation to water content have shown two features of particular interest: first, the depression of net photosynthesis at high water contents, suprasaturation (i.e. the lichen contains more water than necessary to saturate photosynthesis), and, second, the ability of green algal lichens to regain photosynthetic activity by uptake of water from humid air. Evidence from several investigators is presented to confirm that both phenomena are now well substantiated through laboratory investigations. It has been questioned whether these features do actually occur in nature and, if they do, to what extent. Recent work is summarized that demonstrates that for many of the lichens studied suprasaturation is of major importance and can result in depressed photosynthesis for around a third of the time that the lichens are photosynthetically active. Reactivation of photosynthesis of green algal lichens by high humidity is also, apparently, very common in some environments, for example, humid temperate rainforests, occurring almost every night. It is possible that the dominance of green algal lichens, rather than cyanobacterial species, in these habitats is a result of their ability to utilize water vapour. If so, then the phenomenon must have major ecological importance for lichen productivity. In general, laboratory studies seem to be able to predict extremely well the behaviour of lichens in their natural habitat.     

Major clades of parmelioid lichens (Parmeliaceae, Ascomycota) and the evolution of their morphological and chemical diversity

Parmelioid lichens comprise about 1500 species and have a worldwide distribution. Numerous species are widely distributed and well known, including important bioindicators for atmospheric pollution. The phylogeny and classification of parmelioid lichens has been a matter of debate for several decades. Previous studies using molecular data have helped to establish hypotheses of the phylogeny of certain clades within this group. In this study, we infer the phylogeny of major clades of parmelioid lichens using DNA sequence data from two nuclear loci and one mitochondrial locus from 145 specimens (117 species) that represent the morphological and chemical diversity in these taxa. Parmelioid lichens are not monophyletic; however, a core group is strongly supported as monophyletic, excluding Arctoparmelia and Melanelia s. str., and including Parmeliopsis and Parmelaria. Within this group, seven well-supported clades are found, but the relationships among them remain unresolved. Stochastic mapping on a MC/MCMC tree sampling was employed to infer the evolution of two morphological and two chemical traits believed to be important for the evolutionary success of these lichens, and have also been used as major characters for classification. The results suggest that these characters have been gained and lost multiple times during the diversification of parmelioid lichens.     

Endolithic growth of two Lecidea lichens in granite from continental Antarctica detected by molecular and microscopy techniques

Through the combined use of molecular and microscopy techniques, the endolithic lichens Lecidea cancriformis and Lecidea sp. were identified, even in the absence of fruiting bodies, and positioned under epilithic lichens. Cells of both algal and fungal symbionts were observed in fissures and cracks of the lithic substrate with no clear heteromerous structure. At the ultrastructural level, the two lichens differed in terms of their algal-fungal relationships. Only one genotype of Trebouxia ITS sequence was identified from specimens of Lecidea sp., Umbilicaria aprina and Buellia frigida from the same zone, which could be mainly determined by low availability of alga in these extreme environments. These lichens showed features typical of both chasmoendolithic and euendolithic microorganisms. Signs of biogeophysical and biogeochemical action on the substrate were detected close to fungal cells. This action seemed to be mainly conditioned by the local physico-chemical features of the substrate. Evidence for the biomobilization of elements by these endolithic lichens was found. L. cancriformis was observed to accumulate substantial amounts of calcium-rich biominerals. The combined approach proposed is useful for mapping the distribution of endolithic lichens and analysing the processes that occur in their microscopic environment.     

How lichens impact on terrestrial community and ecosystem properties

Lichens occur in most terrestrial ecosystems; they are often present as minor contributors, but in some forests, drylands and tundras they can make up most of the ground layer biomass. As such, lichens dominate approximately 8% of the Earth's land surface. Despite their potential importance in driving ecosystem biogeochemistry, the influence of lichens on community processes and ecosystem functioning have attracted relatively little attention. Here, we review the role of lichens in terrestrial ecosystems and draw attention to the important, but often overlooked role of lichens as determinants of ecological processes. We start by assessing characteristics that vary among lichens and that may be important in determining their ecological role; these include their growth form, the types of photobionts that they contain, their key functional traits, their water‐holding capacity, their colour, and the levels of secondary compounds in their thalli. We then assess how these differences among lichens influence their impacts on ecosystem and community processes. As such, we consider the consequences of these differences for determining the impacts of lichens on ecosystem nutrient inputs and fluxes, on the loss of mass and nutrients during lichen thallus decomposition, and on the role of lichenivorous invertebrates in moderating decomposition. We then consider how differences among lichens impact on their interactions with consumer organisms that utilize lichen thalli, and that range in size from microfauna (for which the primary role of lichens is habitat provision) to large mammals (for which lichens are primarily a food source). We then address how differences among lichens impact on plants, through for example increasing nutrient inputs and availability during primary succession, and serving as a filter for plant seedling establishment. Finally we identify areas in need of further work for better understanding the role of lichens in terrestrial ecosystems. These include understanding how the high intraspecific trait variation that characterizes many lichens impacts on community assembly processes and ecosystem functioning, how multiple species mixtures of lichens affect the key community‐ and ecosystem‐level processes that they drive, the extent to which lichens in early succession influence vascular plant succession and ecosystem development in the longer term, and how global change drivers may impact on ecosystem functioning through altering the functional composition of lichen communities.     

Lichen palatability depends on investments in herbivore defence

Lichens are well-suited organisms for experimental herbivory studies because their secondary compounds, assumed to deter grazing, can be non-destructively extracted. Thalli of 17 lichen species from various habitats were cut in two equal parts; compounds were extracted from one part by acetone, the other served as a control. These two pieces were offered as a paired choice to the generalist herbivore snail Cepaea hortensis. Control thalli of all lichens were consumed at a low rate regardless of their investments in acetone-extractable lichen compounds; naturally compound-deficient lichen species were not preferred compared to those with high contents. However, for extracted thalli, there was a highly significant positive correlation between rate of consumption and the extracted compound contents. These data imply that herbivore defence has evolved in different directions in different lichens. Studied members of Parmeliaceae, common in oligotrophic habitats, have high contents of carbon-rich acetone-soluble compounds; these lichens became highly palatable to snails subsequent to acetone rinsing. Extracted lichen compounds were applied to pieces of filter paper and fed to snails. Extracts from members of the Parmeliaceae significantly deterred feeding on paper. Such data suggest that generalist herbivores may have shaped evolution in the widespread and highly diverse Parmeliaceae towards high investments in lichen compounds. On the other hand, lichens belonging to the Physciaceae and Teloschistales, common in nutrient-enriched habitats, are deficient in, or have low concentrations of, lichen compounds. Such lichens did not become more palatable after acetone rinsing. The orange anthraquinone compound parietin, restricted to the Teloschistales, and which has previously been found to protect against excess light, did not deter grazing.     

A method for the direct detection of airborne dispersal in lichens

This study sets out a novel method to determine dispersal distances in lichens. Direct measurement of dispersal often remains difficult for lichens and other small inconspicuous species because of the need to track microscopic reproductive propagules, which even if they can be captured, cannot be identified using traditional morphological approaches. A low‐cost device (<£200) was developed to trap the reproductive propagules of lichens, capable of sampling around 0.1 m³ of air per minute. In parallel, molecular techniques were developed to enable species‐specific detection of propagules caught by the devices, with identification using novel species‐specific primers and optimization of a standard DNA extraction and nested PCR protocol. The methods were tested for both their sensitivity and specificity against a suite of lichen epiphytes, differing in their reproductive mechanisms, dispersal structures and rarity. Sensitivity tests showed that the molecular techniques could detect a single asexual propagule (soredium or isidium), or as few as 10 sexual spores. As proof of concept, propagule traps were deployed into a wooded landscape where the target epiphytes were present. Extractions from deployed propagule traps were sequenced, showing that the method was able to detect the presence of the target species in the atmosphere. As far as we are aware, this is the first attempt to use mechanized propagule traps in combination with DNA diagnostics to detect dispersal of lichens. The tests carried out here point the way for future dispersal studies of lichen epiphytes and other passively dispersed microscopic organisms including fungi or bryophytes.     

Slowest to fastest: Extreme range in lichen growth rates supports their use as an indicator of climate change in Antarctica

Global temperature rise is suggested to be greater and more rapid in polar regions. There has been a clear temperature rise of 0.056 °C y⁻¹ in the Antarctic Peninsula and this has led to changes in higher plant extent and range. In the more extreme environments of the main continent the vegetation is scattered and composed of lichens and mosses. There is interest in the possible effects of global climate change on these communities acting through changes in temperature and precipitation. Lichens have been extensively used to date the substrates on which they are growing using the techniques of lichenometry. The slow growth and longevity of lichens particularly suites them for this use. We present evidence that there appears to be a substantial (two orders of magnitude) cline in lichen growth rate from the warmer, wetter and more productive Peninsula to the cold Dry Valleys at 77°S latitude. The differences in growth rate reflect the precipitation and temperature regimes at the different sites. The large range in growth rates coupled with the simplicity of measuring lichen growth using modern techniques suggests that this could be an excellent tool for the detection of climate change in continental Antarctica.     

Lichen translocation with reference to species conservation and habitat restoration

Lichen translocation techniques that may be of value in the salvage of endangered lichen species, or in the latter stages of habitat restoration, are reviewed. Successful translocation is defined here as the transfer of a target organism from a donor site to a receptor site to establish a new self-maintaining colony; for lichens, this may or may not include co-transfer of the thallus-supporting substrate. In a time of global environmental change many species are under threat and the need for effective translocation methods is clear. Indeed, some lichens are already amenable to translocation from one substrate to another. Global conservation requires the restoration of degraded ecosystems and translocation technology offers a tool for habitat replenishment. The re-introduction of lichenised fungi into sites from which they have been lost is an integral part of the restoration of complex habitats. Successful translocation creates in turn niches for other organisms which inhabit, or feed upon, them.     

Assessment of vegetation cover by lichen-indication methods (by the example of the north of Central Siberia)

The vegetation cover in the north of Central Siberia has been assessed from lichenological data. The approaches and methods of lichen-based indication of the state of vegetation cover have been developed with the application of the data on diversity of lichens and lichen synusias, their projective cover and morphological deviations. The species of lichens and synusias that can be used for indication purposes have been defined. The changes in the characteristics of the lichen component in vegetation cover under the increasing chemical air pollution caused by industrial plants have been examined. The early deviations are indicated by morphological changes of lichen thalli, species depletion, and diversity of lichen synusias. Practical recommendations on lichen indication of the vegetation cover in the north of Siberia have been given.     

Climate change impacts on endemic,high-elevation lichens in a biodiversity hotspot

Previous studies of the impacts of climate change on lichens and fungi have focused largely on alpine and subalpine habitats, and have not investigated the potential impact on narrowly endemic species. Here, we estimate the impacts of climate change on high-elevation, endemic lichens in the southern Appalachians, a global diversity hotspot for many groups of organisms, including lichens. We conducted extensive field surveys in the high elevations of the region to accurately document the current distributions of eight narrowly endemic lichen species. Species distribution modeling was used to predict how much climatically suitable area will remain within, and north of, the current range of the target species under multiple climate change scenarios at two time points in the future. Our field work showed that target species ranged from extreme rarity to locally abundant. Models predicted over 93 % distributional loss for all species investigated and very little potentially suitable area north of their current distribution in the coming century. Our results indicate that climate change poses a significant threat to high-elevation lichens, and provide a case study in the application of current modeling techniques for rare, montane species.     

Discoveries and identification methods of metal oxalates in lichens and their mineral associations: A review of past studies and analytical options for lichenologists

Lichens are generally acknowledged as the main agents of the initial bioweathering of rock substrates. The most direct evidence of a chemical interaction between lichens and their mineral substrata is the production of oxalic acid, of which interaction with ions present in a close lichen environment occasionally results in the precipitation of metal oxalates. In the past, only a few studies revealed the presence of metal oxalates in lichens, and currently, almost no new discoveries are arriving. Therefore, the main goal of this review is to bring the focus back to this phenomenon. To date, only Mg oxalate dihydrate, Mn oxalate dihydrate, Cu oxalate hemihydrate, Zn oxalate dihydrate, and anhydrous Pb oxalate have been detected in lichens. The most reliable diagnostic methods of metal oxalates in lichens are powder X-ray diffraction (pXRD), infrared spectroscopy (IR), extended X-ray absorption fine structure (EXAFS) spectroscopy, and Raman spectroscopy. Prospective lichen specimens for investigations may be found in anthropogenically-polluted environment or naturally metal-rich rock substrata. This review acts as an initial guide that provides analytical options for field lichenologists, offers a few suggestions for further research on this matter, and encourages to new biomineral discoveries in the scope of mineralogy. Survival in the metal-toxic environment, ability to produce oxygen, and extremophile nature, are the reasons why lichens are good subjects for research within the context of currently expanding astrobiology sciences, as well.     

Pharmaceutically relevant metabolites from lichens

Lichen metabolites exert a wide variety of biological actions including antibiotic, antimycobacterial, antiviral, antiinflammatory, analgesic, antipyretic, antiproliferative and cytotoxic effects. Even though these manifold activities of lichen metabolites have now been recognized, their therapeutic potential has not yet been fully explored and thus remains pharmaceutically unexploited. In this mini-review, particular attention is paid to the most common classes of small-molecule constituents of lichens, from both the chemical viewpoint and with regard to possible therapeutic implications. In particular, aliphatic acids, pulvinic acid derivatives, depsides and depsidones, dibenzofuans, anthraquinones, naphthoquinones as well as epidithiopiperazinediones are described. An improved access to these lichen substances in drug discovery high-throughput screening programs will provide impetus for identifying novel lead-compounds with therapeutic potential and poses new challenges for medicinal chemistry.     

Lichens as rapid bioindicators of pollution and habitat disturbances in the tropics

Lichens have value as bioindicators of environmental pollution, climate change, and ecological continuity. Extensive work has been undertaken in temperate areas, but in only few cases have the techniques been applied in the tropics. Most tropical studies to date are in relation to air pollution and forest disturbance, but these are scattered geographically and remain to be undertaken in most tropical regions. The potential of lichens as rapid bioindicators in the tropics can start to be realized even where the species described are not fully identified as they are perennial and separable by eye or hand lens, and a lack of training is identified as the main constraint. An extensive bibliography is included.