Eutrophication: A new wine in an old bottle?

According to the Intergovernmental Panel on Climate Change report released in September 2014, unprecedented changes in temperature and precipitation patterns have been recorded globally in recent decades and further change is predicted to occur in the near future, mainly as the result of human activity. In particular, projections show that the Mediterranean climate zone will be markedly affected with significant implications for lake water levels and salinity. This may be exacerbated by increased demands for irrigation water. Based on long-term data from seven lakes and reservoirs covering a geographical gradient of 52° of latitudes and a literature review, we discuss how changes in water level and salinity related to climate change and water abstraction affect the ecosystem structure, function, biodiversity and ecological state of lakes and reservoirs. We discuss mitigation measures to counteract the negative effects on ecological status that are likely to result from changes in climate and water abstraction practices. Finally, we highlight research required to improve knowledge of the impacts of anthropogenically induced changes on lake water level and consequent changes in salinity.

Ecological impacts of global warming and water abstraction on lakes and reservoirs due to changes in water level and related changes in salinity

1. Different components of the climate system have been shown to affect temporal dynamics in natural plankton communities on scales varying from days to years. The seasonal dynamics in temperate lake plankton communities, with emphasis on both physical and biological forcing factors, were captured in the 1980s in a conceptual framework, the Plankton Ecology Group (PEG) model.

2. Taking the PEG model as our starting point, we discuss anticipated changes in seasonal and long-term plankton dynamics and extend this model to other climate regions, particularly polar and tropical latitudes. Based on our improved post-PEG understanding of plankton dynamics, we also evaluate the role of microbial plankton, parasites and fish in governing plankton dynamics and distribution.

3. In polar lakes, there is usually just a single peak in plankton biomass in summer. Lengthening of the growing season under warmer conditions may lead to higher and more prolonged phytoplankton productivity. Climate-induced increases in nutrient loading in these oligotrophic waters may contribute to higher phytoplankton biomass and subsequent higher zooplankton and fish productivity.

4. In temperate lakes, a seasonal pattern with two plankton biomass peaks – in spring and summer – can shift to one with a single but longer and larger biomass peak as nutrient loading increases, with associated higher populations of zooplanktivorous fish. Climate change will exacerbate these trends by increasing nutrient loading through increased internal nutrient inputs (due to warming) and increased catchment inputs (in the case of more precipitation).

5. In tropical systems, temporal variability in precipitation can be an important driver of the seasonal development of plankton. Increases in precipitation intensity may reset the seasonal dynamics of plankton communities and favour species adapted to highly variable environments. The existing intense predation by fish on larger zooplankters may increase further, resulting in a perennially low zooplankton biomass.

6. Bacteria were not included in the original PEG model. Seasonally, bacteria vary less than the phytoplankton but often follow its patterns, particularly in colder lakes. In warmer lakes, and with future warming, a greater influx of allochthonous carbon may obscure this pattern.

7. Our analyses indicate that the consequences of climate change for plankton dynamics are, to a large extent, system specific, depending on characteristics such as food-web structure and nutrient loading. Indirect effects through nutrient loading may be more important than direct effects of temperature increase, especially for phytoplankton. However, with warming a general picture emerges of increases in bacterivory, greater cyanobacterial dominance and smaller-bodied zooplankton that are more heavily impacted by fish predation.

http://elserlab.asu.edu/pdf/Domis_2012.pdf

Plankton dynamics under different climatic conditions in space and time

The monocyclic heptapeptides microcystins (MCs), are a group of hepatotoxins, produced worldwide by some bloom-forming cyanobacterial species/strains both in marine and freshwater ecosystems. MCs are synthesized non-ribosomally by large multi-enzyme complexes consisting of different modules including polyketide synthases and non-ribosomal peptide synthetases, as well as several tailoring enzymes. More than 85 different variants of MCs have been reported to exist in nature. These are chemically stable, but undergo bio-degradation in natural water reservoirs. Direct or indirect intake of MCs through the food web is assumed to be a highly exposed route in risk assessment of cyanotoxins. MCs are the most commonly found cyanobacterial toxins that cause a major challenge for the production of safe drinking water and pose a serious threat to global public health as well as fundamental ecological processes due to their potential carcinogenicity. Here, we emphasize recent updates on different modes of action of their possible carcinogenicity. Besides the harmful effects on human and animals, MC producing cyanobacteria can also present a harmful effect on growth and development of agriculturally important plants. Overall, this review emphasizes the current understanding of MCs with their occurrence, geographical distribution, accumulation in the aquatic as well as terrestrial ecosystems, biosynthesis, climate-driven changes in their synthesis, stability and current aspects on its degradation, analysis, mode of action and their ecotoxicological effects.

The cyanotoxin-microcystins: current overview

Morphological evolution from a unicellular to multicellular state provides greater opportunities for organisms to attain larger and more complex living forms. As the most common freshwater cyanobacterial genus, Microcystis is a unicellular microorganism, with high phenotypic plasticity, which forms colonies and blooms in lakes and reservoirs worldwide. We conducted a systematic review of field studies from the 1990s to 2017 where Microcystis was dominant. Microcystis was detected as the dominant genus in waterbodies from temperate to subtropical and tropical zones. Unicellular Microcystis spp. can be induced to form colonies by adjusting biotic and abiotic factors in laboratory. Colony formation by cell division has been induced by zooplankton filtrate, high Pb2+ concentration, the presence of another cyanobacterium (Cylindrospermopsis raciborskii), heterotrophic bacteria, and by low temperature and light intensity. Colony formation by cell adhesion can be induced by zooplankton grazing, high Ca2+ concentration, and microcystins. We hypothesise that single cells of all Microcystis morphospecies initially form colonies with a similar morphology to those found in the early spring. These colonies gradually change their morphology to that of M. ichthyoblabe, M. wesenbergii and M. aeruginosa with changing environmental conditions. Colony formation provides Microcystis with many ecological advantages, including adaption to varying light, sustained growth under poor nutrient supply, protection from chemical stressors and protection from grazing. These benefits represent passive tactics responding to environmental stress. Microcystis colonies form at the cost of decreased specific growth rates compared with a unicellular habit. Large colony size allows Microcystis to attain rapid floating velocities (maximum recorded for a single colony, ∼ 10.08 m h-1 ) that enable them to develop and maintain a large biomass near the surface of eutrophic lakes, where they may shade and inhibit the growth of less-buoyant species in deeper layers. Over time, accompanying species may fail to maintain viable populations, allowing Microcystis to dominate. Microcystis blooms can be controlled by artificial mixing. Microcystis colonies and non-buoyant phytoplankton will be exposed to identical light conditions if they are evenly distributed over the water column. In that case, green algae and diatoms, which generally have a higher growth rate than Microcystis, will be more successful. Under such mixing conditions, other phytoplankton taxa could recover and the dominance of Microcystis would be reduced. This review advances our understanding of the factors and mechanisms affecting Microcystis colony formation and size in the field and laboratory through synthesis of current knowledge. The main transition pathways of morphological changes in Microcystis provide an example of the phenotypic plasticity of organisms during morphological evolution from a unicellular to multicellular state. We emphasise that the mechanisms and factors influencing competition among various close morphospecies are sometimes paradoxical because these morphospecies are potentially a single species. Further work is required to clarify the colony-forming process in different Microcystis morphospecies and the seasonal variation in this process. This will allow researchers to grow laboratory cultures that more closely reflect field morphologies and to optimise artificial mixing to manage blooms more effectively.

Colony formation in the cyanobacterium Microcystis

SUMMARY 1. Climate change affects aquatic ecosystems differently depending on local conditions. In the Mediterranean region, predicted drier seasons could especially affect lake water residence time and in consequence cyanobacteria and cyanotoxin dynamics. 2. We carried out a 3-year study of a shallow, Mediterranean lake (Lake Albufera, Spain), to study the effects of water residence time and other drivers on the dynamics of harmful cyanobacteria and microcystin concentrations (MCYST). 3. Longer water residence time in dry years and dry seasons increased total cyanobacteria biomass, Microcystis aeruginosa populations and MCYST concentrations in the lake water and seston. Droughts increased water retention time by about 45%, and M. aeruginosa populations and MCYST were 1–2 orders of magnitude higher. 4. All samples analysed contained MCYST, and among them 70% had values above the recommended guidelines. Flows lower than 10 m 3 s )1 raised toxicological risk from low to moderate-high according to international standards. Mean MCYST concentrations bound in the cells were one order of magnitude higher than in the water (11 ± 2.9 and 1.2 ± 0.3 l gL )1 , respectively). 5. The microcystin content per unit biovolume of M. aeruginosa was generally higher at the start of population growth (April–May) than at the population maximum (July–October). This was related to increase in water residence time, total phosphorus concentration and mean colony size within the edible range (<50 lm). The maximum MCYST content corresponded with average populations of 10 3 colonies L )1 and 2 mm 3 L )1 , which could additionally be used to evaluate toxicological risks in the lake. 6. Microcystis aeruginosa colonies were larger with increasing water residence time and more closely related to the lake hydrology and water column stagnation than to MCYST colony content. 7. Feasible measures for restoration and conservation of shallow Mediterranean lakes in a future climate scenario are discussed.

Water residence time and the dynamics of toxic cyanobacteria

Cyanobacteria dominance and cyanotoxin production can become major threats to humans and aquatic life, especially in warm shallow lakes, which are often dominated by cyanobacteria. This study investigates the occurrence and distribution of microcystins (MCYST) in water, cell-bound and in the tissues of the commercial mugilid Liza sp. in the largest, coastal, Spanish Mediterranean lake (Albufera of Valencia). This is the first report concerning microcystin accumulation in tissues of mugilid fish species. Considerable amounts of microcystins were found in the water and seston, which correlated with development of Microcystis aeruginosa populations in the lake. The MCYST concentrations found in Lake Albufera (mean 1.7 and 17 μg/L and maximum 16 and 120 μg/L in water and seston, respectively) exceeded by one to two orders of magnitude the guideline levels proposed by the World Health Organization and were higher than that reported in other lakes of the Mediterranean zone. The presence of MCYST was found in all the fishes studied and accumulated differently among tissues of the commercial species Liza sp. Toxin accumulation in fish tissues showed that although the target organ for MCYST was the liver, high concentrations of microcystins were also found in other analysed tissues (liver>intestine>gills>muscle). Human tolerable daily intake for microcystins is assessed relative to the WHO guidelines, and potential toxicological risks for humans, wildlife and related ecosystems of the lake are discussed.

Francisca Fernández

Papers

Water residence time and the dynamics of toxic cyanobacteria

Assessment of microcystins in lake water and fish (Mugilidae, Liza sp.) in the largest Spanish coastal lake.