Development of a quantitative PCR method to explore the historical occurrence of a nuisance microalga under expansion

A number of marine and freshwater harmful algal bloom (HAB) species have colonized new areas and expanded their habitat range in recent years. Nevertheless it is notoriously difficult to establish when colonization first occurred, what the dispersal routes are, and to separate recent invasion from increases in existent but small populations. The freshwater raphidophyte Gonyostomum semen is a nuisance species that has expanded its habitat range and increased in abundance in northern Europe during the past decades. To evaluate to what extent sediments can be used for determining historic occurrence of G. semen, a quantitative real-time PCR method for detecting cysts of this algae was developed. This paper presents a qPCR protocol with a set of primers that are specific to Gonyostomum and with PCR conditions optimized for sediment samples from humic lakes, which are the common habitat of G. semen. With this sensitive method as few as 1.6 cysts per PCR reaction could be reliably quantified, corresponding to 320 cysts per g wet weight sediment. Cysts were present in sediments with ages ranging from years to decades and their persistence allows detection of historic populations up to at least 50 years old. With this qPCR assay it will be possible to trace the presence of G. semen in environments prior to the onset of algae-specific monitoring programs as well as for quantification in water column samples.     

Factors affecting occurrence and bloom formation of the nuisance flagellate Gonyostomum semen in boreal lakes

We examined changes in G. semen occurrence and bloom incidence in 146 boreal lakes in Sweden sampled at least once between 1992 and 2010, and used a time-by-space model to assess the environmental variables that best explain patterns in G. semen distribution and bloom formation.We showed that G. semen has become more common, although there were no significant shifts in its geographical distribution during the study period. In particular, G. semen was spreading into new lakes in the Central Plains ecoregion (southern Sweden), whereas its occurrence and biomass usually remained low in the Borealic Upland and Fennoscandian Shield ecoregions.G. semen biomass and the incidence of blooms did not increase significantly during the study period, but fluctuated among years and reached a maximum in 2003. The occurrence of G. semen was mainly explained by temperature and the length of the growing season, whilst local-scale variables, such as pH and water color, were the best predictors of blooms.Analysis of bloom formation at three different levels of G. semen dominance: G. semen >50%, >75%, and >90% of total phytoplankton biomass revealed a wide range of responses to environmental variation. For example, pH, water color and to a lesser extent temperature explained bloom formation at the 50% level, whereas lake morphometry was important at the 90% level.These results suggest that with ongoing brownification and climate warming boreal systems will likely become more susceptible to invasions of G. semen.     

Phenotypic plasticity and differentiation in an invasive freshwater microalga

Recent studies show that both marine and limnic microalgal species often consist of several genetically distinct populations. This is also valid for the nuisance freshwater algae Gonyostomum semen, which originates from acidic, brown water swamp lakes, but can nowadays also be found in clearer lakes with close to neutral pH. We hypothesized that the observed genetic differentiation among G. semen lake populations, reported in earlier studies, is connected to adaptation to local environmental conditions. In the present study we performed controlled laboratory experiments to test whether 12 strains originating from five lakes varied in their response to five to six different pHs, light intensities and DOC concentrations. Overall, growth (0.01–0.37 day⁻¹) was observed over a wide range of light intensities and pHs, demonstrating high potential for photoacclimation and extensive plasticity of individual strains. Moreover, we found similar growth rates and consistent growth optima for specific pHs by strains from the same lake, suggesting genetic differentiation of populations into distinct phenotypes. However, observed strain specific preferences did not always reflect environmental conditions in the lakes of origin and provided limited evidence for the hypothesized local adaptation. Instead, the observed phenotypic differentiation may indicate resilient effects of founder events. We suggest that the wide phenotypic plasticity in this species enables it to thrive in fluctuating and variable environments, and may play a role in its ability to colonize new habitats.     

Light and nutrient control phytoplankton biomass responses to global change in northern lakes

Global change affects terrestrial loadings of colored dissolved organic carbon (DOC) and nutrients to northern lakes. Still, little is known about how phytoplankton respond to changes in light and nutrient availability across gradients in lake DOC. In this study, we used results from whole‐lake studies in northern Sweden to show that annual mean phytoplankton biomass expressed unimodal curved relationships across lake DOC gradients, peaking at threshold DOC levels of around 11 mg/L. Whole‐lake single nutrient enrichment in selected lakes caused elevated biomass, with most pronounced effect at the threshold DOC level. These patterns give support to the suggested dual control by DOC on phytoplankton via nutrient (positively) and light (negatively) availability and imply that the lakes' location along the DOC axis is critical in determining to what extent phytoplankton respond to changes in DOC and/or nutrient loadings. By using data from the large Swedish Lake Monitoring Survey, we further estimated that 80% of northern Swedish lakes are below the DOC threshold, potentially experiencing increased phytoplankton biomass with browning alone, and/or combined with nutrient enrichment. The results support the previous model results on effects of browning and eutrophication on lake phytoplankton, and provide important understanding of how northern lakes may respond to future global changes.     

Dominance patterns of planktonic algae in Swedish forest lakes

Dominance patterns of phytoplankton during a late phase (August) in the seasonal sequence of species are presented from 15 Swedish forest lakes with little or no local anthropogenic impact. The main question to elucidate is if predominance of a small number of species (1–3) occurs during a mature phase of the annual succession i.e. if there is an evident competitive exclusion of species in favour of a few dominants. Ten August months per lake are used to illustrate interannual variations caused mainly by differences in weather conditions. In general, 1–3 dominant taxa do not reach more than 60% of the total phytoplankton volume. Only lakes exposed to some stress factors exhibit a more pronounced dominance pattern with 1–3 species occupying >80% of the phytoplankton biomass. Stress factors are harsh climate (arctic lake), light deficiency (very brown water), acidification and occurrence of the invasive raphidophycean species Gonyostomum semen. The variation in phytoplankton assemblages in relation to environmental variables and years was tested by classification and ordination methods (TWINSPAN, CCA). The consistency of the species/lake groupings and the set of explanatory environmental variables was checked in a discriminant function analysis. Species associations during investigated years and environmental variables show a very good consistency and 75% of the lakes was classified in the same species group irrespective of year, indicating stable species assemblages from summer to summer.     

Changes in phytoplankton,benthic invertebrate and fish assemblages of boreal lakes following invasion by Gonyostomum semen

1. During recent decades, Gonyostomum semen populations have spread in northern temperate regions forming dense blooms that may dominate the phytoplankton assemblage for extended periods. In this study, we investigate the effects of G. semen blooms in boreal brown water lakes with special emphasis on phytoplankton, fish and benthic invertebrate assemblages using data from 10 boreal lakes sampled annually over a 10‐year period. 2. Significant differences in phytoplankton and benthic invertebrate assemblages were found between lakes with high (3.01 mm³ L^?1; >80% phytoplankton biomass) and lakes with low G. semen biomass (0.03 mm³ L^?1; <5% phytoplankton biomass). In particular, high G. semen lakes had lower biomass of smaller, edible phytoplankton and a higher abundance and biomass of benthic invertebrates, especially Chaoborus flavicans, and perch than low G. semen lakes. 3. The length distribution of fish also suggested a tendency towards large and older fish and a lower recruitment success in high G. semen lakes, as denoted by lower abundances of fish shorter than 10 cm and higher biomass and abundance of fish longer than 15 cm in high G. semen lakes. 4. This study shows that high G. semen lakes are characterised by less edible phytoplankton, dominance by a few species and enhanced benthic secondary and fish production. Hence, the conjecture that high biomasses of G. semen create a bottleneck in the energy transfer to higher trophic levels seems less likely in boreal lakes.     

Lake responses to long‐term disturbances and management practices

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Mass development of the flagellate Gonyostomum semen (Raphidophyta) in Swedish forest lakes - an effect of acidification?

During the last 20–30 years the flagellate Gonyostomum semen has become more abundant in lakes, especially small humic lakes, in Scandinavia. Mass development of the alga has been reported from areas affected by anthropogenic acid deposition, and reports from bathers of health problems are becoming frequent. Although there is an apparent connection between the appearance of Gonyostomum and acidification, it seems not to be the low pH per se that is the cause, but rather interlinked factors. The present tendency towards a wider distribution of the alga in non-humic lakes, emphasizes the importance of a better understanding of small humic lakes.     

Effects of humic stress on the zooplankton from clear and DOC‐rich lakes

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Freshwater protists do not go with the flow: population structure in Gonyostomum semen independent of connectivity among lakes

Many recent studies have found genetically differentiated populations in microorganisms despite potentially high dispersal. We designed a study to specifically examine the importance of physical dispersal barriers, i.e. geographic distance and lack of hydrological connectivity, in restricting gene flow and enhancing divergence in limnic microorganisms. We focused on the nuisance microalga Gonyostomum semen, which has recently expanded in Northern Europe and differentiated into genetically distinct populations. G. semen was sampled from six lakes distributed in two adjacent watersheds, which thereby comprised, both connected and non‐connected lakes. The individual isolates were genotyped by amplified fragment length polymorphism. Several lake populations were differentiated from each other, but connectivity within watersheds could not explain the observed population genetic pattern. However, isolation by distance was moderate and might limit the gene flow among distant populations. In addition, we found low, but significant linkage disequilibrium, which indicates regular sexual recombination in this species, despite its high degree of asexual reproduction. Therefore, we conclude that the genetic properties of microalgae with occasional sexual reproduction essentially mirror regularly recombining species. Furthermore, the data indicated bottlenecks supporting the hypothesized recent range expansion of this species.     

Waterfowl grazing effects on submerged macrophytes in a shallow mediterranean lake

Waterfowl exclusion cages were set up in Sentiz Lake, an eutrophic shallow lake in León (NW of Spain) in order to determine the role of waterfowl herbivory on macrophyte biomass and species composition. Total macrophyte biomass was high during the study (250 g DW m⁻² in summer). The macrophyte community was mainly formed by Myriophyllum alterniflorum (95% cover), Ceratophyllum demersum (5%) and Potamogeton gramineus (<0.5%). High densities of co-occurring coots (Fulica atra; 24 ind/ha) and ducks (Anas penelope, A. strepera and A. platyrhynchos; 18 ind/ha) did not have a significant effect on macrophyte biomass in the lake. There were no statistical differences between total biomass inside and outside the exclosures, although plant biomass reached a higher value inside the cages than in the lake. Biomass species composition was significantly different inside and outside exclosures; C. demersum was more abundant in the cages than in the lake. P. gramineus, almost absent in the lake, became co-dominant with M. alterniflorum in some exclosures. The detailed study of M. alterniflorum flower buds in summer showed significant herbivory by coots. Flower bud abundance was lower in the lake (35% lower in June; 85% lower in July) than under waterfowl exclusion. The effect of waterfowl on macrophyte biomass in Mediterranean wetlands seems to be negligible as compared to effects identified in northern European lakes. Apart from an important role in dispersal, waterfowl in Mediterranean areas have a strong qualitative effect on the structure of plant communities by selecting most palatable species or their reproductive structures.     

Browning reduces the availability—but not the transfer—of essential fatty acids in temperate lakes

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Population Genetic Structure of a Microalgal Species under Expansion

Biological invasions often cause major perturbations in the environment and are well studied among macroorganisms. Less is known about invasion by free-living microbes. Gonyostomum semen (Raphidophyceae) is a freshwater phytoplankton species that has increased in abundance in Northern Europe since the 1980''s and has expanded its habitat range. In this study, we aimed to determine the genetic population structure of G. semen in Northern Europe and to what extent it reflects the species'' recent expansion. We sampled lakes from 12 locations (11 lakes) in Norway, Sweden and Finland. Multiple strains from each location were genotyped using Amplified Fragment Length Polymorphism (AFLP). We found low differentiation between locations, and low gene diversity within each location. Moreover, there was an absence of genetic isolation with distance (Mantel test, p = 0.50). According to a Bayesian clustering method all the isolates belonged to the same genetic population. Together our data suggest the presence of one metapopulation and an overall low diversity, which is coherent with a recent expansion of G. semen.     

The past and future of phytoplankton in the UK's largest lake,Lough Neagh

Lough Neagh is the largest lake in the UK and has been extensively monitored since 1974. It has suffered from considerable eutrophication and toxic algal blooms. The lake continues to endure many of the symptoms of nutrient enrichment despite improvements in nutrient management throughout the catchment, in particular a permanently dominant crop of the cyanobacterium Planktothrix agardhii. This study examines the historical changes in the Lough, and uses the PROTECH lake model to predict how the phytoplankton community may adapt in response to potential future changes in air temperature and nutrient load. PROTECH was calibrated against 2008 observations, with a restriction on the maximum simulated mixed depth to reflect the shallow nature of the lake and the addition of sediment released phosphorus throughout the mixed water column between 1 May and 1 October (with an equivalent in-lake concentration of 2.0 mg m⁻³). The historical analysis showed that phytoplankton biomass (total chlorophyll a) experienced a steady decline since the mid-1990s. During the same period the key nutrients for phytoplankton growth in the lake have shown contrasting trends, with increases in phosphorus concentrations and declines in nitrate concentrations. The modelled future scenarios which simulated a temperature increase of up to 3 °C showed a continuation of those trends, i.e. total chlorophyll a and nitrate concentrations declined in the surface water, while phosphorus concentrations increased and P. agardhii dominated. However, scenarios which simulated a 4 °C increase in air temperature showed a switch in dominance to the cyanobacteria, Dolichospermum spp. (formerly Anabaena spp.). This change was caused by a temperature related increase in growth driving nutrient consumption to a point where nitrate was limiting, allowing the nitrogen-fixing Dolichospermum spp. to gain sufficient advantage. These results suggest that in the long term, one nuisance cyanobacteria bloom may only be replaced by another unless the in-lake phosphorus concentration can be greatly reduced.     

Clustering and canonical correspondence analysis of phytoplankton and environmental variables in Swedish lakes

Phytoplankton data consisting of 145 species from a limnological study of lakes from relatively undisturbed areas throughout Sweden were analysed in relation to 11 physical and chemical environmental variables. Three multivariate methods were applied: WPGMA clustering and TWINSPAN for classification, and detrended canonical correspondence analysis (DCCA), a recent technique which extracts ordination axes that can be related directly to variation in the environment. Three types of lakes were recognized consistently: acid humic lakes with Gonyostomum semen as the dominant species, very acid impoverished lakes with rather few, stress-tolerant species, and subarctic lakes with low total biomass but with a varied phytoplankton flora. DCCA allowed a straightforward display of the locations of lakes and species along environmental gradients (including the acidification gradient) reflected in phytoplankton composition. It is suggested that such analyses may be a useful tool for the early detection of environmental change.     

The functional quality of decomposing litter outputs from an Arctic plant community is affected by long-term exposure to enhanced UV-B

Plant exposure to enhanced UV-B radiation typically induces changes in leaf secondary metabolite profiles which will be inherited in litter, affecting litter breakdown and the carbon (C) dynamics of sensitive plant communities. A key enzyme in the decomposition process is phenol oxidase which is influenced by litter quality and, hence, a decomposition bioindicator. Here we investigated dwarf shrub litter decomposition following experimental community exposure to enhanced UV-B over two decades in the Swedish sub-Arctic. We examined the hypothesis that foliar UV-B exposure would alter litter quality to elevate phenol oxidase activity. This was tested in the field by measuring phenol oxidase activity in freshly collected mixed-community litter from under our experimental vegetation. A laboratory mesocosm was next used in a decomposition assay to investigate individual species responses over eight weeks, with an emphasis on the quality of leachate outputs from decomposing litter (from Empetrum hermaphroditum, Vaccinium vitis-idaea, Vaccinium uliginosum). In the assay bi-weekly collections of leachate were analysed for phenol oxidase activity, together with total phenolics and dissolved organic C (DOC). At the end of the assay litter mass loss and respired C were also determined. The initial assessment on field mixed-community litter found no enhanced UV-B treatment (henceforth: ‘UV-B treatment’) effect on phenol oxidase activity. However, in the controlled laboratory mesocosm assay, significant species-specific effects of the UV-B treatment were evident, with increased phenol oxidase activity in V. vitis-idaea leachate (P < 0.001) and a significant reduction (P = 0.05) in respired C. Leachate DOC release from the UV-B treatment was greater in both Vaccinium species and the effect on V. uliginosum was significant (P < 0.05). The UV-B treatment had no effect on the total phenolic concentration of litter or leachates for any species, but there were significant differences in leachate total phenolics, both over time and between species. Also the initial phenolic concentration in leachates from the decomposing litter of E. hermaphroditum was greater than both Vaccinum species. Results suggest a species specific role for UV-B in influencing enzyme function and decomposition, dependent on individual traits. This has implications for decomposition dynamics in this system and more widely. Our study highlights the value of using a laboratory assay to gain a mechanistic understanding the species level impacts of a global change factor (UV-B) on decomposition, which are otherwise obscured by community-level responses and difficult to determine under field conditions.     

The effect of lake morphology on aquatic vegetation development and changes under the influence of eutrophication

Data on aquatic and emergent vegetation, morphology and water quality from 274 Polish lowland lakes surveyed in the years 1996–2009 were used to validate the preliminary typology of Polish lakes based on macrophytes and to indicate the environmental parameters which most significantly determine the vegetation patterns in lakes under various morphological conditions. In highly alkaline lowland lakes representing non-disturbed conditions the key determinants influencing the vegetation patterns were mean depth and the shape of the littoral. Three morphological lake types were distinguished: shallow (<3.5 m), deep, and additionally, within the latter, deep ribbon-shaped, with a clearly elongated base and steep bed slopes. The lake types varied in their vegetation patterns developed under non-disturbed conditions. In the shallow lakes, the share of the phytolittoral in the total lake area (%phytol) was the highest (40–100%, 72.3% on average) and the maximum colonisation depth (C_max) the lowest (3.2 m as the maximum) compared to the lakes from both deep types. In the ribbon-shaped deep lakes, %phytol and the plant coverage (%cover) were the lowest, the proportion of submerged vegetation was extraordinarily high (over 90%) and the emergent vegetation was extremely sparsely developed (<6%) compared to the lakes of the two other types.The alterations of aquatic vegetation resulting from the eutrophication process in distinguished morphological lake types were explored. Within the macrophyte variables tested, three groups of indicators were distinguished: (a) metrics performing best in selected lake types, i.e. the type-specific indicators (abundance metrics, %Pota), (b) metrics performing equally well in all the lake types, considered as the universal indicators (e.g. S_Chara, %Subm and %Emerg) and (c) metrics performing poorly in all the lake types, with generally limited applicability (most of the metrics on syntaxonomic richness). In the shallow lakes, %cover and %phytol performed notably better than in deep lakes, whereas C_max worked best in deep lakes and showed the strongest response in the deep regular-shaped lakes. Moreover, in deep regular-shaped lakes the number of communities of stoneworts and submerged plants (S_Chara and S_Subm), and in deep ribbon-shaped lakes the proportion of area inhabited by vascular plant communities (%Pota) performed exceptionally better than in the other two lake types. The most universal metrics, performing equally well in all the lake types, were the proportions of submerged (%Subm) and emergent (%Emerg) vegetation in the total phytolittoral area.     

In-Lake Processes Offset Increased Terrestrial Inputs of Dissolved Organic Carbon and Color to Lakes

Increased color in surface waters, or browning, can alter lake ecological function, lake thermal stratification and pose difficulties for drinking water treatment. Mechanisms suggested to cause browning include increased dissolved organic carbon (DOC) and iron concentrations, as well as a shift to more colored DOC. While browning of surface waters is widespread and well documented, little is known about why some lakes resist it. Here, we present a comprehensive study of Mälaren, the third largest lake in Sweden. In Mälaren, the vast majority of water and DOC enters a western lake basin, and after approximately 2.8 years, drains from an eastern basin. Despite 40 years of increased terrestrial inputs of colored substances to western lake basins, the eastern basin has resisted browning over this time period. Here we find the half-life of iron was far shorter (0.6 years) than colored organic matter (A₄₂₀ ; 1.7 years) and DOC as a whole (6.1 years). We found changes in filtered iron concentrations relate strongly to the observed loss of color in the western basins. In addition, we observed a substantial shift from colored DOC of terrestrial origin, to less colored autochthonous sources, with a substantial decrease in aromaticity (-17%) across the lake. We suggest that rapid losses of iron and colored DOC caused the limited browning observed in eastern lake basins. Across a wider dataset of 69 Swedish lakes, we observed greatest browning in acidic lakes with shorter retention times (< 1.5 years). These findings suggest that water residence time, along with iron, pH and colored DOC may be of central importance when modeling and projecting changes in brownification on broader spatial scales.     

Changes in physicochemical and biological factors during regime shifts in a restoration demonstration of macrophytes in a small hypereutrophic Chinese lake

Shallow, eutrophic lakes are usually characterized by a turbid state devoid of submerged vegetation subject to human-induced eutrophication. In most cases, it is rather hard to restore a vegetated clear state due to reduced resilience caused by a blend of complicated factors. In this study, we successfully reestablished a plant community in a small hypereutrophic lake over a certain period. In winter and spring with transparency of >55 cm and temperature of <20 °C, a submerged stands bed formed gradually under strong human interventions. The reestablished plant bed displayed obvious seasonal succession and prolonged the clear-water stage until July 2005, when it collapsed. The regime shift to a turbid state was mainly attributed to the decreasing biomass of stands bed and mechanical damage brought about by the elimination of Spirodela polyrhiza, increasing water temperature, P concentration as well as periphyton biomass, etc. The reestablishment also changed the aquatic ecosystem greatly. A ‘clear-water’ stage was characterized by higher NO₃^?–N, NH₄⁺–N, electrical conductivity, transparency and TN/TP level and more cladocerans (mainly Daphnia pulex), while the turbid state was characterized by higher temperature, chlorophyll a and TP level and more abundant rotifers. It is thus viable to restore submerged macrophytes in such lakes in winter and spring, when transparency is relatively high while temperature and water level are low. Nevertheless, to obtain a long-term, vegetated clear state, control of internal nutrient loading by means of obstruction, purification, dredging or solidification, is extremely necessary since nutrients play an important role in regime shifts as evidenced by the present case, too.     

Nitrogen effects on the pelagic food web are modified by dissolved organic carbon

Global environmental change has altered the nitrogen (N) cycle and enhanced terrestrial dissolved organic carbon (DOC) loadings to northern boreal lakes. However, it is still unclear how enhanced N availability affects pelagic food web efficiency (FWE) and crustacean zooplankton growth in N limited boreal lakes. Here, we performed in situ mesocosm experiments in six unproductive boreal Swedish lakes, paired across a DOC gradient, with one lake in each pair fertilized with N (2011: reference year; 2012, 2013: impact years). We assessed how zooplankton growth and FWE were affected by changes in pelagic energy mobilization (PEM), food chain length (phytoplankton versus bacterial production based food chain, i.e. PP:BP), and food quality (seston stoichiometry) in response to N fertilization. Although PP, PEM and PP:BP increased in low and medium DOC lakes after N fertilization, consumer growth and FWE were reduced, especially at low DOC—potentially due to reduced phytoplankton food quality [increased C: phosphorus (P); N:P]. At high DOC, N fertilization caused modest increases in PP and PEM, with marginal changes in PP:BP and phytoplankton food quality, which, combined, led to a slight increase in zooplankton growth and FWE. Consequently, at low DOC (<12 mg L^?1), increased N availability lowers FWE due to mismatches in food quality demand and supply, whereas at high DOC this mismatch does not occur, and zooplankton production and FWE may increase. We conclude that the lake DOC level is critical for predicting the effects of enhanced inorganic N availability on pelagic productivity in boreal lakes.