Myths and truths about lichens
What are lichens?
Lichens are unique organisms. They are a symbiotic association between a fungus and an alga. More precisely the term “alga” indicates whether a cyanobacterium (Cyanobacteria) or a green alga (Chlorophyceae); the fungus is usually an Ascomycetes, although on rare occasions it may be a Basidiomycetes. The hyphae envelop the alga, giving rise to a simple structure known as a thallus. The alga provides nutrients (carbohydrates) by photosynthesis while the fungus provides water, minerals, protection from high light and desiccation, and facilitates water storage (Conti and Cecchetti, 2001; Essen and Coxson, 2015). Lichens comprising cyanobacteria must be wetted by liquid water for activation of photosynthesis while lichens composed of green algae can be activated by humid air.
Lichens exhibit extreme variability in size (from less than 1 cm in many crustose species to over 1 m in length in some epiphytic species), colour and growth form. The vegetative body (thallus) is usually classified into three main growth forms: crustose lichens form crusts tightly attached to the rocks, trees, or soils; foliose lichens are somewhat leaf-like, composed of flattened lobes, they are relatively loosely attached to their substrates, usually by means of rhizomes; fruticose lichens are erect or pendent, mostly branched, they can hang down in long strands or they can be like little shrubs growing upward (Desbenoit et al., 2004; Essen and Coxson, 2015). In nature lichens grow very slowly; as a generalization, most foliose species grow 0.5-4 mm/year, fruticose species 1.5-5 mm/year and crustose species 0.5-2 mm/year (Rankovic and Kosanic, 2015).
Lichens do not take their nutrients from the substrate, but mostly from the air and ambient water. For this reason, they could grow, potentially, on all substrates, including very nutrient-poor ones. In fact, lichens can colonize trees (epiphytes), the ground (terricolous lichens), stone (epilithic lichens) and even glass. Lichens are poor competitors and tend to favour open habitats that are mostly devoid of other vegetation (Aptroot and James, 2002; Lisci et al., 2003).
Lichens and stones: a long-time couple
Lichens were possibly one of the first life forms to occupy Earth’s land surfaces, as pioneer colonizers of fresh rock outcrops. Nowadays, an estimated 6% of the Earth’s land surface is covered by lichen-dominated vegetation. The majority of lichen species are primarily saxicolous in most parts of the world outside the tropics (Aptroot and James, 2002) and the majority of the biodiversity on rocks usually consists of lichen species. Exceptions are given for rocks permanently submerged or heavily shaded, where lichens hardly grow.
Lichens can transform stone substrates and play an important biogeochemical role in rock weathering, in the distribution of nutrients (e.g. C, N) and soil formation processes. Lichens accelerate rock weathering both with physical and chemical processes, including mechanical disruption of the substrate by hyphae of the first millimetres (0.3 to 16 mm) of stone, expansion and contraction of infiltrating biomass during wet and dry periods, secretion of organic acids (e.g. oxalic acid) which promote mineral dissolution and metal chelation (Haas and Purvis, 2006). At last, carbon dioxide, produced by the respiration of the thallus, dissolves calcareous rocks in the presence of moisture, leading to the formation of soluble bicarbonates that may be washed away or cause encrustation (Lisci et al., 2003).
Lichens and monuments: a biodiversity heritage
Lichens can grow naturally on artificial stony substrates, such as bricks, mortar, and pebbles of buildings, megalithic monuments and graveyards (Aptroot and James, 2002). The pH of the substrate performs the first selection of lichen flora; also humidity, luminosity and nitrogen supply further make the difference (Lisci et al., 2003).
A famous example is represented by the Megalithic monuments of Stonehenge, where lichens have been recorded since the 18th century. According to Powell et al. (2018), more than 100 recorded species of lichens are accepted as occurring at Stonehenge since 1973, comprising the abundant large shaggy clumps of the maritime Ramalina siliquosa. Cover of this species is especially abundant on stones that have remained relatively undisturbed during the last hundred years. The biodiversity of churchyards can be very high too: 630 lichen species have so far been recorded from churchyards in the UK, which is a third of the total British flora (Powell et al., 2018).
Lichens community can vary a lot according to the type of stone. In the surroundings of Rome, many archaeological sites have monuments made from exotic materials from distant areas of the Roman Empire. Such monuments today host an incredibly rich lichen flora, with more than 600 lichen species known (Powell et al., 2018). On the contrary, certain marbles found at ancient Ostia (Rome) are still in perfect condition and do not host lichens or other plants (Lisci et al., 2003).
The removal of lichens from tombstones, sculptures, and monuments is widely practised; nevertheless, it can damage the stone, and, in the case of extensive and repeated use of biocides, the environment too (Pinna, 2014). For these reasons, Sheppard (2007) suggested minimal intervention proposing to let the lichens contributing to the aesthetics of certain monuments.
Lichens and trees: what is the real relationship?
In forest ecosystems, lichens play many ecological roles, that scientists are now only beginning to understand. Lichens represent only a small proportion of the biomass in the forest, nonetheless, they can have a disproportionate impact on ecosystem function.
Lichens containing cyanobacteria are capable of fixing nitrogen in the air. This peculiarity is of fundamental importance for the nutrient cycle in humid forests, where the bioavailability of nitrogen is the key factor for the growth of the forest itself; as an example, in wet temperate rainforests, Lobarion lichens provide up to 16 kg of N per hectare annually (Will-Wolf et al., 2002; Essen and Coxson, 2015).
Lichens provide microhabitats and food for forest canopy invertebrates (e.g. collembola) and provide nesting material for birds and small mammals. Animals, in turn, can be important as dispersal-vectors for lichens. Herbivory is low in most lichens, probably because of their low nutrient content and defence compounds produced. Nevertheless, lichens are the dominant forage source for reindeer and caribou in subarctic and boreal forests (Aptroot and James, 2002; Essen and Coxson, 2015).
The community of epiphytic lichens (that is, lichens that grow on the surface of a plant) is controlled by a long series of factors that operate at tree, stand and landscape level. At tree level, tree species, bark chemistry (e.g. bark pH), bark structure (texture, stability, water-holding capacity), tree age, diameter, height and crown structure, are important conditions. At stand level, the communities of lichens can vary according to tree species composition, canopy structure (e.g. gaps), age distribution, microclimate (openness and humidity). At last, at landscape level other characteristics as elevation, topography and water bodies, landscape heterogeneity, should be considered (Essen and Coxson, 2015). For these reasons, lichens community can be used as an indicator of ecosystem function: some species of lichens can grow only on the trunk of old trees with rough bark, cyanolichens are sensitive to pollution, forest age and continuity, Lobaria spp. are sensitive to air quality, and so on (Will-Wolf et al., 2002).
Regarding the effect of lichens colonization on plant health, there is still a lot of confusion. Often the most luxuriant lichens are present on trees in poor condition, so many people could think that they are the main cause of this situation. Conversely, most of the species of lichens need direct light for development, and canopy openness (due for instance to the declining of a tree) could produce microhabitats with high moisture and direct light suitable for the growth of the lichens. Although lichens firmly attached to the surface of the plant, they produce their own nutrients by photosynthesis, without taking nutrients from the tree; in other words, in most cases plants are not affected by lichen growth. The question, however, cannot be solved by generalizing this assumption, as there are few reports of negative relationships for specific tree-lichen species combinations. It is the case, for instance, of the crustose Lecanora carpinea lichen and the tree species Populus tremula: Solhaug et al. (1995) found that the covering by the lichen caused shading and halved the photosynthetic rate of bark. Interestingly, P. tremula has adapted photosynthesis in that areas, neutralizing the effect of lichen cover. The corticolous lichen Evernia prunastri has long been studied as it can have a negative effect on oak health: the lichen secretes some enzymes (e.g. evernic acid) to anchor to the plant tissues and the consequent hyphal penetration has been correlated to vigour decrease of oaks induced by allelopathic processes (Favero-Longo and Piervittori, 2010). However, in the vast majority of the cases, abundant corticolous lichen colonization is a consequence and not a driving factor of defoliation.
Lichens and pollution: just look.
The use of cosmopolite organisms to assess pollution has developed notably during the last few decades (Conti and Cecchetti, 2001) and lichens are the most studied bioindicators of air quality. Lichens are sensitive to many types of environmental alterations. For instance, high pollution, particularly by sulphur dioxide, damages the lichen thallus. The number of species tends to decrease drastically from the periphery to the centre of urbanized areas (Seaward, 1976).
Lichens may be used as bioindicators and/or biomonitors in two different ways:
– by mapping the biodiversity of lichen species present in a specific area; one of the most famous methods is the elaboration of the Index of atmospheric purity (IAP); in Italy this method has been explained in detail by the National Environmental Protection Agency (ANPA, 2001) for the calculation of the Lichen biodiversity index.
– through the individual sampling of lichen species and measurement of the pollutants that accumulate in the thallus (e.g. heavy metals, fluorides, chlorides, sulphur compounds, nitrogen and phosphorous compounds, ozone, radionuclides, and other atmospheric pollutants; Conti and Cecchetti, 2001).
The influence of eutrophication on the lichen community is among the most studied. For instance, a methodology was developed in 1989 for the recognition of ammonia pollution, a major threat to vegetation, soil and drinking water in The Netherlands. Lichens were detected on selected trees species (preferably, Quercus robur, Fagus sylvatica, Pinus spp.). The recording of nitrophytes lichens (e.g. Caloplaca citrina, Lecanora muralis, Xanthoria polycarpa, …) and acidophytes lichens (e.g. Cladonia spp., Lecanora aitema, Lepraria incana, …) allowed to determine the degree of eutrophication of the air in a given area (Van Herk, 2002).
Being very sensitive to changes in microclimatic conditions and forest management activities, lichens have been used to estimate the ecological continuity of forests (ANPA, 2001). Flagship species indicating forest continuity is the leafy lichen Lobaria pulmonaria: its sensitivity to phytotoxic gases (mainly SO2 and NOx) allows to monitor the effects of atmospheric pollution.
Lichens’ usages, potentialities and conservation policies
Throughout the ages, lichens have been employed for various purposes. Lichens were used in the nutrition of many animals and humans during famine. Since Egyptians, lichens were used as dyes. Romans dyed their togas with a brown pigment obtained from Parmelia spp., Ochrolechia spp and Evernia spp, or with a purple pigment extracted by Roccella spp. In the 18th century, lichens-dyed textiles were economically important in some parts of the world as in the Canary Islands. In ancient times lichens were used also for cosmetics in general (Mitrović et al., 2011). The extracts of some species of lichens, like Evernia prunastri, are contents of perfumes and oils. Lichens were used in Ancient Egypt for embalming too: the lichen Pseudevernia furfuracea was employed in the body cavity together with sawdust, cassia and other spices, because it was high absorbent and for its antibacterial properties (Mitrovic et al., 2014).
The most important application of lichens is the one in traditional medicine for the treatment of animals and humans. In Indian spice market lichens are currently sold by name of ‘Chharila’, which consists of a mixture of two or more species of lichens. Chharila has astringent, laxative and carminative properties and is also supposed to possess aphrodisiac property. The Ayurvedic system of therapy provides extensive use of lichens. Peltigera canina was used for treating rabies (Shukla et al., 2010). Usnea species have been used in Asia, Africa and Europe for fever control and pain relief. Ramalina thrausta is used in Finland for the treatment of wounds or other skin diseases and taken to relieve sore throat and toothache (Mitrović et al., 2011). Paradoxically, over-exploitation of lichen populations for human use is a serious problem for their conservation, considering that, even if the demand is not increasing, the size and quality of many habitats hosting lichens are decreasing (Scheidegger and Werth, 2009).
Lichens are an untapped source of new bioactive molecules for pharmaceutical purposes, as antimicrobial, antioxidant and cytotoxic agents and in the development of new formulations or technologies for the benefit of human life, but also for pest management (Dayan et al., 2001; Zambare and Christopher, 2012). The lichens therefore have considerable potential applications, but due to their slow growth (with current laboratory techniques) they have not been judged suitable for commercial exploitation yet.
On the other hand, with a look to the future, it is difficult to implement conservation policies to protect endangered species, due to the limited information on taxonomy, abundance, habitat requirements and distribution of species in many ecosystems worldwide (Hunter and Webb, 2002). As an example, despite the fact that Italy is among the among the lichenologically best known areas worldwide, an exhaustive official national Red List of lichens is still lacking (Nascimbene et al., 2013). The main threats are degradation and loss of habitats, their fragmentation, overexploitation, species invasions and climate change. The primary focus in lichen conservation should therefore be the maintenance of habitats’ quality and dimension, together with their connectivity (Scheidegger and Werth, 2009).
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