Benthic Diatoms from the Hypersaline Mar Menor coastal lagoonTaxonomy, phylogeny and responses to environmental changes

Abstract

Introduction and objectives Diatoms are the most abundant group within benthic microalgae that form biofilms in aquatic systems. These communities play a key role in the functioning of shallow coastal systems, such as lagoons and estuaries, at the primary production level and in biogeochemical cycles, and are considered the basis of the food chain. They also constitute one of the first compartments that react to any environmental variation or type of impact. In the marine environment, information on distribution, ecology and taxonomy, and the use of benthic diatoms as biological indicators of environmental changes, are scarce. The present assay was carried out in the coastal Mar Menor lagoon (SE Spain), where previous floristic information practically cannot be found. The lagoon is subject to multiple anthropogenic impacts, including contributions of metals and nutrients loads. Populations may be strongly affected by the increase in temperature associated with global climate change. Therefore, it is an ideal study area to investigate the relationships of species and communities with environmental gradients, and it may help to understand the biotic and abiotic factors that structure benthic diatom communities. The general objective of this thesis is to improve knowledge about the ecology and taxonomy of the benthic diatom communities in the coastal Mar Menor lagoon and to evaluate their potential as biological indicators of the multiple stressors that affect and threaten the lagoon. Any work conducted on bioindicators is based on good floristic knowledge, but this information is lacking in Mar Menor. For this reason, the following specific objectives were identified: i) to morphologically, ecologically and phylogenetically study the genus Hyalosynedra; ii) investigate the composition and abundance of the species of the genus Licmophora in the lagoon, and its phylogenetic relationships; iii) evaluate the combined effect of temperature and the stoichiometric N:P ratio of water on populations of the stalked marine diatom Licmophora colosalis, and to test whether overproduction of stalks could serve as an indicator of nutrient contamination; iv) study the composition, structure and biological traits of the species of two benthic diatom communities influenced differently by the chronic contamination of metals and nutrients, and investigate their responses to the sporadic exposure of both factors. These objectives aim to evaluate the suitability of these communities as a tool to environmentally monitor the lagoon. Methodology Floristic works include morphological descriptions obtained by optical microscopy and scanning electron microscopy, and by molecular analyses using cell cultures, extraction of genetic material, sequencing and phylogenetic analyses of sequences. Laboratory bioassays consist of applying different temperatures and nutrient treatments to evaluate the effect on population dynamics (growth measures, cell size, mortality), stalks production (by image analyses) and carbohydrates (chemical analyses) of Licmophroa colosalis. The field experiment involves applying different treatments of metals and nutrients individually and combined. The community response was analysed at different levels: structural (biological indices and species abundance) and biological traits (growth form types). Biofilm characterisation was done by a biomass analysis, accumulated metal, chlorophyll a and carbohydrates content. Results and Conclusions Our results show that benthic diatom communities can serve as biological indicators of anthropogenic impacts on the coastal Mar Menor lagoon. The composition and abundance of species, as well as concentration of accumulated metals, can show the existence of discharges of metals and nutrients of only 1 hour for 4 days, which is a similar pattern to the torrential rains in the area. The results reveal that sporadic discharges of nutrients can amplify the impact of metals on the benthic communities in the Mar Menor, which was observed at all the studied levels: community composition and structure, metal accumulation, chlorophyll a concentration, and the 3-dimensional biofilm structure. At the structural level, metal inputs favour the colonisation of tolerant species, and when they act together with nutrients, they seem to favour mainly those with specific growth forms. Thus the communities affected by both stressors are characterised by tolerant species, such as Berkeleya fennica, which forms mucilage tubes, and Neosynedra provincialis, which forms zig-zag-like colonies, as reflected by the increased complexity of the 3-dimensional biofilm. O. krumbeinii, however, was negatively affected by all the treatments, and is proposed as a potentially sensitive species. These data suggest that the approach based on biological species traits can provide additional information on the species' ecology, which can rapidly reveal environmental changes and can be useful for monitoring these environments. The 47 taxa found in the works of this thesis are new cites for the Mar Menor lagoon, and two new species were described for science: Hyalosynedra lanceolata and Licmophora colosalis. The phylogenetic analysis was crucial to identify them, and changes in some closely related taxa are also proposed. The need to perform more molecular studies with a larger number of species to clarify the phylogenetic relationship among closely related taxonomic groups was evidenced; for example, Hyalosynedra species and S. toxoneides. In the global climate change context, an increase in temperature up to 36°C, which falls within the prediction limits for lagoon waters, would be lethal to L. colosalis. The optimal growth temperature is around 26°C, with a stoichiometric range of N:P = 16. Hence their populations would be able to better face the increase in temperature if the N: P range remains balanced. With Mar Menor, and current contributions of nitrates, the N:P ratio value is above 16. Our results indicate that, in this situation, if the temperature increases up to 31ºC, which was reached in August 2017), it can lead to high mortality and the massive production of mucilaginous stalks. This indicates that an unbalanced N:P (e.g., N: P> 16) stoichiometric range, along with thermal stress, can cause changes in the population dynamics of L. colosalis. It also suggests that production of stalks, which gives rise to arbuscular macroscopic colonies in a natural environment, can be used to detect nutrient contamination.