The so-called functional traits are the features of a living organism that play a role in driving its responses to the environmental factors interacting with it (Koch et al. 2019). Substantially, its biological, anatomical and morphological features.
When using them for applied studies, functional traits can be described with quantitative values or just at a qualitative level. Traits of vascular plants are generally quantitative (stem lenght, seed viability, thickness of chlorophyll parenchyma, to name some of them), whereas traits of lichens are generally categorical. The second scenario allows to unite different species in the so-called functional groups, i.e. groups of species which have in common a certain trait. For example, in lichens functional groups are based on traits like thallus growth form (crustose, squamulose, foliose, fruticose, composite), photobiont type (chlorococcoid green alga, trentepohlioid green alga, cyanobacterium), reproduction type, etc. etc.
What is the difference between studying lichen communities’ traits and studying richness or composition, two parameters which have been more used until now?
Functional traits can give us different information. Species are unique, whereas traits can group more than one species; and traits can differ between taxonomically or ecologically similar species. Therefore, studying traits can be important to understand why phylogenetically close species can behave in very different ways, or, vice versa, why phylogenetically distant species can show similar responses to the same environmental or disturbance factor(s).
Between the 1990s and the 2010s, applied lichenological research used to investigate the effects of pollutants with the assessment of richness and composition of lichen communities, but the environmental emergencies currently acting on our planet – among which striking are the climate change and the loss/fragmentation/transformation of natural habitats – suggest that a more effective method to understand their impacts on lichen communities could be precisely to investigate their functional diversity, i.e. the diversity of their traits.
Investigating traits can be particularly revelatory when we deal with communities in which taxonomic diversity is low, but trait diversity is high.
An exemplary case is represented by terricolous lichen communities in acidic dry grasslands of the western Po Plain: here, Cladonia is the only genus, sometimes with a high number of species, but anyway the belonging of all the species to a single genus somehow trivializes taxonomic diversity. But not the same is for functional diversity: in fact, Cladonia is a very diversified genus in terms of morphology (podetia can have very different shapes, and also primary squamules are variable), reproductive strategies and compounds produced by the secondary metabolism. And such variability had never been explored at the best of its potential, to date.
This situation – lichen communities built-up by a single genus with a huge unexplored potential – took me to conceive a research that I developed together with some colleagues and that has been recently published on Microorganisms (Gheza et al. 2021).
Study area and study sites: acidic dry grasslands of the western Po Plain (Northern Italy) (from Gheza et al. 2021).
The focus of this research is on a very particular habitat: acidic dry grasslands, which are characterized by a precariousness due chiefly to vegetation dynamics, which leads to their disappearance. In fact, the typical composition of such grasslands includes pioneer plants, along with lichens and bryophytes, that can be found mainly in pioneer stages; when soil develops a layer of organic matter, vegetation evolves and the encroachment by more competitive plants causes the disappearance of pioneer ones…and of lichens and mosses! This would be a natural dynamics, that is however accelerated by the occurrence of some invasive plants which are very competitive and produce high amounts of organic matter, e.g. black locust (Robinia pseudoacacia). Vegetation dynamics is the main reason causing the need of an active managament of dry grasslands: management aims at maintaining pioneer conditions, in order to save the habitat requirements for pioneer plants and cryptogams.
For this reason, the main environmental features considered in our research described the vegetation dynamics, to better elucidate how it influences functional traits of Cladonia. To do this, we used the vascular plants life forms [1], assuming that, in a grassland habitat, therophytes are the first colonizers and are dominant in pioneer stages, whereas hemicryptophytes and geophytes are dominant in intermediate-mature stages, and woody species – chamaephytes and phanerophytes – occur in mature stages and increase at increasing vegetation and soil maturity, sometimes also indicating ecotone situations.
The other environmental features considered included local ones – soil pH, occurrence of disturbance by trampling and by an invasive Lagomorph that proved to be detrimental to lichens in this habitat (Gheza et al. 2018) – and climatic ones, i.e. mean annual temperature and annual rainfall.
Such variables were put in relation, by means of statistical analyses, with three groups of functional traits purposely redefined with the explicit intention of highlighting the functional variability typical of genus Cladonia.
The main group of traits was the thallus growth form.
Cladonia has a unique feature in the world of lichens: it has a composite thallus, built-up by the union of the so-called “primary thallus” and “secondary thallus”. The primary thallus is the basal part, made of little scales called squamules. The secondary thallus is the most morphologically variable part, made by structures called podetia, whose aim is to produce the apothecia. Podetia can have very different sizes and shapes across the species.
In spite of this variability, previous literature assigned to Cladonia just two (foliose, fruticose) or three (foliose, fruticose with simple podetia, fruticose with branched podetia) growth forms. Considering the possible combinations between the two parts of the thallus and the morphological types of podetia, we introduced the use of six growth forms.
The six growth forms considered in this study, represented in scale; it can be easily noticed that also the average sizes of each form, aside of morphology, are very different.
The second group of traits was the reproduction strategy.
Previous literature considered only if reproduction is mainly sexual (by means of apothecia in Cladonia) or asexual by some vegetative propagule (soredia are the most common in Cladonia).
But the peculiar morphology of Cladonia allowed a further possibility, in addition: due to the composite thallus, in Cladonia pycnidia can occur either on primary squamules or on podetia, depending on the species. Therefore, the other element we took in account to describe the reproductive strategy was the position of pycnidia on the thallus. It could be assumed that species which produce pycnidia on primary squamules can do it faster than species which produce them on podetia, since squamules develop first; and therefore species with pycnidia on squamules could be faster and more effective colonizers of pioneer substrates/habitats.
The two descriptors of reproductive strategy: apothecia vs soredia (above) and pycnidia on squamules vs pycnidia on podetia (below).
The third group of traits included the secondary metabolites.
Lichen compounds, which are produced exclusively by lichens, are widely studied due to their interesting pharmaceutical potential [2], but still largely unexplored under the standpoint of their ecological roles. And obviously the latter is far more intriguing to explore, for the ecologists.
Among the most common metabolites in Cladonia we find atranorin, zeorin, and fumarprotocetraric, homosekikaic, rangiformic and usnic acids.
Surprisingly, the statistical analysis revealed more correlations than expected between the traits of Cladonia and the selected environmental variables. Furthermore, some of these correlations were very interesting and allowed to formulate some hypotheses that can help improving our understanding of trait-mediated interactions between lichens and the surrounding environment.
Significant correlations (coloured squares) between Cladonia functional traits and the considered environmental variables; positive correlations in cold colours, negative correlations in warm colours (from Gheza et al. 2021).
Many correlations were related to descriptors of vegetation dynamics, which revealed that species with small simple podetia and pycnidia on the primary squamules are positively related to pioneer stages and negatively to intermediate-mature stages, whereas an opposite pattern was evident for species with branched podetia, that were related to mature stages.
Interesting were also correlations disclosed between some metabolites and some environmental features, even more if considering that previous literature that investigated similar correlations is very scarce (one of the best is the detailed work by Zraik et al. 2018). Striking was the case of two metabolites with opposite correlations to what we can call a “canopy”, i.e. the cover of the vascular plants which produce a thicker cover (chamaephytes and phanerophytes, that can really be compared to what is for us a forest canopy, if seen from the perspective of organisms tall only few centimetres like lichens): usnic acid correlated negatively, whereas atranorin correlated positively. Previous literature suggested a photoprotection function for usnic acid (Farkas et al. 2020), which is therefore appropriate to find in species growing in exposed sites, and a role in facilitating the exploitation of low light intensities for atranorin (Rao & LeBlanc 1965), which is therefore appropriate to find in species that can grow under a moderate shading. In this case, our findings support interesting ecological roles already hypothesized by previous research.
I got also a valuable hint to deepen a question that has been in my mind for long: how is it possible that three species which differ so much in size, morphology and reproductive strategy, i.e. Cladonia cariosa, Cladonia rei and Cladonia rangiformis, have in common the fact of being widespread and often abundant also in disturbed and prohibitive habitats, and generally dominant in the lichen communities they occur within? The answer may lie within their metabolites: in fact, these three species contain homosekikaic and/or rangiformic acids, both of which correlated positively with all the dynamic stages of vegetation – pioneer and intermediate-mature. This suggests that the trait that drives such a wide distribution and ecological amplitude could well be the occurrence of one (or both) of these two metabolites. A better understanding of the ecological role of these two substances could perhaps help us to better understand the success of the species that produce them: a promising starting point for future research.
C. cariosa (left), C. rei (centre) and C. rangiformis (right) are the most successful species in this habitat, which often dominate the lichen vegetation in which they occur.
Finally, also climatic features correlated to some traits, and some of these correlations can be an alarm bell towards climate change. Most of these correlations gave a negative signal, but the most striking one is surprisingly positive. In fact, atranorin correlated positively with temperature and negatively with precipitation, suggesting that the modifications induced by global warming could foster species that produce such metabolite.
I am very satisfied for this study, not only because it allowed to deepen the diversity of Cladonia traits in a way that they really deserved, but also because it gave several interesting hints.
The next step shall be to follow and deepen some of these hints…
References
Farkas E., Biró B., Szabó K., Veres K., Csintalan Z., Engel R. 2020. The amount of lichen secondary metabolites in Cladonia foliacea (Cladoniaceae, lichenised Ascomycota). Acta Botanica Hungarica 62: 33-48.
Gheza G., Assini S., Marini L., Nascimbene J. 2018. Impact of an invasive herbivore and human trampling on lichen-rich dry grasslands: soil-dependent response of multiple taxa. Science of the Total Environment 639: 633-639.
Koch N.M., Matos P., Branquinho C., Pinho P., Lucheta F., de Azevedo Martins S.M., Ferrao Vargas V.M. 2019. Selecting lichen functional traits as ecological indicators of the effects of urban environment. Science of the Total Environment 654: 705-713.
Rao D.N., LeBlanc F. 1965. A possible role of atranorin in the lichen thallus. The Bryologist 68: 284-289.
Zraik M., Booth T., Piercey-Normore M.D. 2018. Relationship between lichen species composition, secondary metabolites and soil pH, organic matter, and grain characteristics in Manitoba. Botany 96: 267-279.
Notes
[1] Plant life forms were introduced by the Danish botanist Christen Raunkiaer, and are therefore known also as “Raunkiaer System”. Life forms classify vascular plants by the mode in which they overcome the adverse season, considering as the main feature the position of the wintering buds. Hereinafter the definitions of the life forms mentioned in our research.
Therophytes: annual herbs that survive the adverse season in the form of seed.
Hemicryptophytes: biennial or perennial herbs and forbs with wintering buds at or near the soil surface.
Geophytes: perennial herbs and forbs with subterranean resting buds within rhizomes or bulbs.
Chamaephytes: perennial plants with a woody base with perennating buds close to the soil surface (between 5 and 25 cm from soil).
Phanerophytes: perennial woody plants with perennating buds above 25 cm from the soil surface.
[2] Among the ecological roles attested for some of these metabolites, striking is the biocidal action, that can be directed towards different fronts: to control the proliferation of photobiont cells within the thallus, to fight competitors in the surrounding environment by means of allelopathy, to discourage herbivores to feed on thalli that contain them. Due to this activities, some of these metabolites are widely studied to exploit their antimicrobial, antifungal and even anticancer potential.
Cladoniarium 