Lichen biota from gypsum soils: a comprehensive approach

Abstract

Gypsum soils are considered “extreme habitats”, as the presence of this mineral produces a series of physico-chemical restrictions that limit the establishment and distribution of different organisms. Despite these constraints, gypsum substrate fosters a complex biological community, the biological soil crust or biocrust, composed of lichens, bryophytes, fungi, algae, or cyanobacteria. Lichens which are well-adapted to this substrate, being occasionally dominant, play a key ecosystemic role in providing various ecosystem services, such as participating in water and nutrient cycles, influencing plant germination, reducing soil erosion, or providing shelter and food to invertebrates. However, lichens are not able to actively regulate their water content (poikilohydric) or temperature (poikilotermic). Thus, they are considered environmental bioindicators, as this condition makes them highly sensitive indicators of environmental changes. In recent years, the importance of lichens in gypsum soils has been remarked, mainly due to a significant number of studies. However, some aspects concerning their distribution and ecology have not been deeply treated. Despite several regional studies listing lichen species growing on gypsum ecosystems, there are no studies at a global scale compiling the species present in gypsum soils. Furthermore, the species composition of several regions is still unknown. It is known that the presence of gypsum highly influences the composition of lichen communities. However, the relationship between lichens and gypsum is scarcely treated, including the affinity for this substrate, which is unknown in numerous species, and the mechanisms allowing lichens to cope with gypsum presence. Furthermore, ecological studies focused on these communities are centered on the taxonomic diversity (TD, mainly richness), neglecting other dimensions such as functional (FD) and phylogenetic (PD) diversities. A single diversity dimension may not capture the response of communities to environmental changes, and the integration of different diversity dimensions may help to understand better the response of communities to environmental changes.

Objectives The general objective of this thesis focuses on deepening the knowledge concerning the species composition and distribution of gypsum lichen communities on a global scale, the ecology, and the response of these communities to environmental variables. The specific objectives of this thesis are: 1) To study the lichen composition in gypsum ecosystems at a global scale by constructing a comprehensive checklist from literature and in Spain, by sampling along a latitudinal gradient (Chapters 1 and 3); 2) To evaluate the affinity of main lichen species for gypsum substrates (Chapter 2); 3) To analyze the environmental variables influencing different diversity dimensions (TD, PD, and FD) (Chapter 4); 4) To assess the response of gypsum lichen communities to environmental changes through their functional traits (Chapter 4).

Methodology This study analyses lichen communities from gypsum soils along a latitudinal gradient covering the main gypsum areas in Spain. Thirty-five plots of 30 × 30 meters were surveyed, and ten quadrats of 50 × 50 centimeters were placed within each plot: four at the corners of the plot, and the remaining six randomly distributed. Lichen cover (%) was estimated from the species included in each quadrat. Functional traits of identified lichen species were assessed. Eight qualitative traits (growth form, type of photobiont, type of attachment structures, presence of pruina, thallus color, thallus continuity, reproduction strategy, and secondary metabolites), were based on bibliographical data, and eleven quantitative traits related to water use strategy (water holding capacity, WHC and specific thallus mass, STM)), photosynthetic activity (chlorophyll a, b, and carotenoids), and nutrient acquisition strategy (carbon, nitrogen and sulfur content and their isotopes) were measured. A combined phylogenetic analysis comprising all the species found in the study was constructed, using six gene regions (nuITS, nuLSU, nuSSU , mtSSU, RPB1, and RPB2). Sequencing of the nuITS region was carried out to identify doubtful species by comparing them against GenBank data base or by performing phylogenetic analyses. Different taxonomic (richness, inverse Simpson, Pielou), functional (CWM and RAO), and phylogenetic (RAO) indices were calculated. Furthermore, different statistical approaches (e.g., generalized linear models, partitioning analysis, NMDS) were employed to analyze how environmental variables influenced the diversity dimensions, functional traits, and species composition based in presence of species and cover. The information to elaborate the global data set of gypsum lichen species was extracted from the literature included in different repositories, including Web of Science (WOS), Mattick's Literature Index, Hamburg University’s Worldwide Checklist, and several national checklists. Finally, to assess gypsum affinity, species occurrence information was downloaded from GBIF and from literature. The retrieved information was intersected with two different gypsum soil maps: one based on lithology (geological map) and the other constructed from the distribution of four strict gypsophile plant species (biological map). To test the accuracy of both methods, the results were compared with the literature review.

Results Chapter 1 provides a data set comprising 6114 specimen records, belonging to 336 lichen species growing on gypsum soils from 26 countries, extracted from a total of 321 studies. The results showed large differences in the number of recorded species among countries, caused by an unequal sampling effort. Both, Spain and Germany hosted the highest number of recorded species (160 and 114 species, respectively). On the other hand, Southern Hemisphere countries (i.e. Australia, Chile, Namibia, and South Africa) hosted a low number of studies from gypsum lands.

Chapter 2 yielded valuable information concerning lichen gypsum affinity and methodology. After comparing both maps with the literature review, the results showed that the biological map was more accurate. The results for the most abundant lichen species growing in gypsum soils in Spain probed the existence of gypsophile lichens. Of the 50 taxa analyzed, 20 lichen species were considered gypsophiles, including 7 strict and 13 preferential (ca. 40% of analyzed taxa), and 30 gypsovag species. Increases in species records improve ecological analyses have been positively demonstrated when comparing GBIF data with data extracted from the literature.

Results obtained in Chapter 3 revealed new records and new species from gypsum habitats in Spain. In total, 72 lichen species were found, including four species recorded for the first time in Spain, and 37 new provincial records. Furthermore, four new species from the genera Gyalolechia, Squamarina, Thalloidima and Xanthoria, were found. Differences in species composition are present, whether in plots from the same region or different, being caused by climatic variables and gypsum content.

Chapter 4 showed that the responses of lichen diversity dimensions to environmental variables were not equal, as richness (taxonomic diversity) and functional diversity were more related to environmental variables than phylogenetic diversity. The partition of quantitative FD and qualitative FD revealed a higher response of quantitative trait diversity to the environmental variables studied, whereas qualitative diversity was mostly related to the phylogenetic diversity. The minimum temperature of the coldest month emerged as the most influential variable. Thus, a higher minimum temperature promoted richer communities, with more functional and phylogenetic diversity. Precipitation, temperature, and gypsum content influenced certain traits, acting as environmental filters. Thus, lower precipitation, lower minimum temperature, and high gypsum content promoted a water-conservative strategy where lichens have high values of WHC and STM. On the other hand, a higher minimum temperature and higher precipitation are linked to lichens with faster and shorter metabolic activity periods, where species have lower values of STM. Intraspecific trait variability explains trait variability in photosynthetic activity and nutrient uptake traits, whereas water use traits (WHC and STM) are mostly explained by species turnover.

Conclusions The outcome of this thesis expands the knowledge concerning the composition, distribution, ecology, and diversity of gypsum lichen communities. New data about the distribution of lichen species at a global scale are provided. Furthermore, the results highlighted the differences in the number of studies between countries caused by unequal sampling efforts, pinpointing which are the most understudied areas. New data are also provided for Spain regarding new records and species. Furthermore, the distribution area of certain species has been expanded, remarking that even in well-studied areas, there are still gaps to be filled. The surveys along the gradient and the analyses of the gypsum affinity of the most abundant species have demonstrated that these communities are composed of stresstolerant species also present in calcareous soils (gypsovags, ca. 60%), and some specialist species (gypsophiles ca. 40%). Lichen communities in gypsum soils responded to environmental changes differently through their diversity dimensions. The minimum temperature of the coldest month emerged as the most influential variable, as its increase is linked to more species, phylogenetically distant, and with different functional traits. Additionally, precipitation and gypsum content, selected specific functional traits, and filtering those species that are not adapted to certain environmental conditions. The high trait variability contribution provided by ITV indicates high plasticity of lichens in most of the traits. However, in the case of the water use traits this plasticity is not enough, being the species replaced by other better adapted. All in all, this study emphasizes the importance of quantitative functional traits and trait-by-trait analysis to understand how lichen communities in gypsum soils respond to environmental change.