Catchment land use and trophic state impacts on phytoplankton composition: a case study from the Rotorua lakes’ district, New Zealand

Trophic state of lakes has been related to catchment land use, but direct links between phytoplankton taxa and land use are limited. Phytoplankton composition, represented by relative cell abundance of phyla, was measured over a period of 4 years in 11 lakes in the Rotorua region, New Zealand. The lakes differed in morphometry, trophic state and land use (as percentage catchment area). We tested whether relative proportion of land uses, indirectly representing relative nutrient loading, was the overarching driver of phytoplankton composition. Trophic state was correlated negatively with native forest and positively with pasture and urban area. Cyanoprokaryota were correlated negatively with native forest and positively with pasture and trophic state, Chlorophyta were correlated positively with native forest and urban land use and negatively with pasture and trophic state, and Bacillariophyta were positively correlated with dissolved reactive silica to dissolved inorganic nitrogen (Si:DIN) and Si to dissolved reactive phosphorus (Si:DRP) ratios. Lakes with higher nutrient loads had higher trophic state and Cyanoprokaryota dominance. Chlorophyta were negatively correlated with Cyanoprokaryota and Bacillariophyta, suggesting competition amongst these groups. Our results apply to lakes potentially subject to changes in catchment land use, which may have implications for trophic state, phytoplankton composition and Cyanoprokaryota blooms.     

Use of marker pigments and functional groups for assessing the status of phytoplankton assemblages in lakes

Phytoplankton is a key biological quality element for the establishment of the Water Framework Directive (WFD) ecological status in reservoirs and lakes. In freshwaters, inverted microscope examination is the traditional standard method for estimating phytoplankton and assessing taxonomic composition. Based on the enumeration of algal units and measurements for biovolume calculation, this technique is cumbersome and time-consuming. In large monitoring programmes, such as the application of the WFD in lakes and reservoirs, chemotaxonomy (HPLC pigment analysis and CHEMTAX treatment) is ideally suited as an alternative method because it allows the rapid processing of large numbers of samples from numerous locations and depths, thereby providing ideal temporal and spatial resolution. The low taxonomical detail obtained by HPLC and CHEMTAX (phytoplankton classes or phyla) can easily be overcome by a rapid inverted microscope screening with identification of the dominant species. Combining HPLC and microscopy provides a useful method for monitoring phytoplankton assemblages, which can be used to implement the WFD with respect to phytoplankton. Here, we present the application of a method combining marker pigments and microscopy to phytoplankton samples from 12 Belgian reservoirs. This method substantially reduced the workload and enabled us to assess the status of the phytoplankton assemblage in these lakes. The method complies with the WFD, as it takes into account taxonomic composition, assesses abundance and biomass of the phytoplankton taxa, and easily detects blooms. Additionally, a set of templates of probability of occurrence of phytoplankton functional groups at the maximal ecological potential for reservoirs from the Central/Baltic region is presented, based on reference conditions defined for natural lakes from other regions.     

Planktonic indices in the evaluation of the ecological status and the trophic state of the longest lake in Poland

Due to the intensive mixing polymictic lakes should be homogenous. However, morphometric diversity and high water dynamics contribute to the differentiation of many parameters in various areas of the lakes. This study analyzes both phytoplankton and zooplankton to assess differences in water quality along the north–south axis of the longest lake in Poland. New phytoplankton indicators were applied for determining the lake's ecological status: the Q index based on functional groups and the PMPL (Phytoplankton Metric for Polish Lakes) index based on phytoplankton biomass. TSI_ROT index (Rotifer Trophic State Index), which comprises the percentage of species indicating a high trophic state in the indicatory group and the percentage of bacteriovorus in the Rotifera population, was used for zooplankton analysis.TP content was different at different sites – we observed its gradual increase from the south to the north. Spatial variation of phosphorus did not considerably affect plankton diversity. The phytoplankton was dominated by Oscillatoriales, typical of shallow, well-mixed eutrophic lakes. The ecological status of the lake based on the EQR (Ecological Quality Ratio) was poor or moderate. The zooplankton was dominated by rotifers (at almost all sites), which indicates a eutrophic state of the lake. The values of phytoplankton indices at the studied sites did not differ considerably; the differences resulted more from local conditions such as the contaminant inflow and the macrophyte development than water dynamics.We have demonstrated that in the lake dominated by filamentous Cyanobacteria the ecological status should be determined according to the PMPL index or other indices dependent on the dominant Cyanobacteria species. Since the Q index does not include the functional group S1, the results can lead to the false conclusion that water quality improves with an increased amount of phytoplankton. The high abundance of Cyanobacteria in the lake may have contributed to the poor growth of rotifers.     

Cyanobacteria dominance influences resource use efficiency and community turnover in phytoplankton and zooplankton communities

Freshwater biodiversity loss potentially disrupts ecosystem services related to water quality and may negatively impact ecosystem functioning and temporal community turnover. We analysed a data set containing phytoplankton and zooplankton community data from 131 lakes through 9 years in an agricultural region to test predictions that plankton communities with low biodiversity are less efficient in their use of limiting resources and display greater community turnover (measured as community dissimilarity). Phytoplankton resource use efficiency (RUE = biomass per unit resource) was negatively related to phytoplankton evenness (measured as Pielou's evenness), whereas zooplankton RUE was positively related to phytoplankton evenness. Phytoplankton and zooplankton RUE were high and low, respectively, when Cyanobacteria, especially Microcystis sp., dominated. Phytoplankton communities displayed slower community turnover rates when dominated by few genera. Our findings, which counter findings of many terrestrial studies, suggest that Cyanobacteria dominance may play important roles in ecosystem functioning and community turnover in nutrient‐enriched lakes.     

A multiomics approach to study the microbiome response to phytoplankton blooms

Phytoplankton blooms are predictable features of marine and freshwater habitats. Despite a good knowledge base of the environmental factors controlling blooms, complex interactions between the bacterial and archaeal communities and phytoplankton bloom taxa are only now emerging. Here, the current research on bacterial community’s structural and functional response to phytoplankton blooms is reviewed and discussed and further research is proposed. More attention should be paid on structure and function of autotrophic bacteria and archaea during phytoplankton blooms. A multiomics integration approach is needed to investigate bacterial and archaeal communities’ diversity, metabolic diversity, and biogeochemical functions of microbial interactions during phytoplankton blooms.     

Distinct successional patterns and processes of free-living and particle-attached bacterial communities throughout a phytoplankton bloom

1. Understanding the successional patterns of microbial communities during a phytoplankton bloom is crucial for predicting the compositional and functional stability of lake ecosystems in response to the disturbance of a bloom. Previous studies on bacterial communities associated with blooms have rarely studied the dynamics of these communities. The successional patterns of bacterial communities within different micro-habitats (i.e. water column versus particles) and mechanisms that shape these communities that differ in composition and structure remain unclear.
2. We selected a eutrophic urban lake to investigate the succession of bacterial communities during a bloom. We divided the bacterial communities into free-living (FL) and particle-attached (PA) groups based on their different lifestyles. The amplicon-based 16S rRNA gene high-throughput sequencing technology was used to obtain bacterial community composition and phylogenetic structure.
3. Our study showed distinct successional patterns between FL and PA bacterial communities, and the two bacterial lifestyles showed different responses and resilience to the bloom, in terms of diversity and relative abundance of bacterial taxa. Alpha-diversity of the PA bacterial community decreased during the bloom, whereas that of the FL bacterial community increased. More taxa in the FL bacterial community showed resilience after the disturbance than in the PA bacterial community.
4. The influence of phytoplankton blooms on the assembly of the bacterial community can be viewed as niche selection that led to the decrease in the relative importance of stochastic processes in shaping both FL and PA bacterial communities. This study shows the ecological significance of the bacterial community response to bloom events in lakes. It also shows that assembly processes differ for bacterial communities that have different lifestyles in lake ecosystems disturbed by phytoplankton blooms.

     

Seasonal succession of cladocerans and phytoplankton and their interactions in a shallow eutrophic lake (Lake Vela,Portugal)

Lake Vela is a polymictic shallow lake exhibiting some characteristics typical of an advanced trophic state, namely, the permanently turbid water, the reduction in biodiversity, and the recurrent occurrence of Cyanobacteria blooms, which occasionally lead to large fish kills. This study was carried out in order to understand the seasonal variation of Lake Vela’s phytoplankton and cladoceran communities and their interactions under advanced eutrophic conditions. When comparing our results with general models of plankton succession observed in other temperate and tropical lakes we found some coherence between several seasonal events. Our results suggest that phytoplankton is mainly regulated by nutrients (“bottom-up” effect). However, the warm mediterranean temperatures had an important role in the phytoplankton succession, being responsible for the rapid and intense Cyanobacteria development in spring and summer. Our work also demonstrated that phytoplankton is one of the main factors responsible for the seasonal structure of the community of cladocerans, which are well related to changes in algae diversity and abundance, being the Cyanobacteria having major impact. Moreover, the occurrence of a massive Cyanobacteria bloom during the study, which induced anoxia and consequent fish kill, enhanced the structuring role that fish have on the cladoceran seasonal succession and the effects of this episode in the normal seasonal succession of plankton.     

Water-blooming and toxin-producing cyanobacteria in Swedish fresh and bracish waters, 1981–1995

During the period 1981–1995 331 phytoplankton samples from 153stations in different parts of Sweden were analysed regardingspecies composition and possible toxicity. Toxins were indicated in156 samples which gives a percentage of 47. The toxicity wasconfirmed by mouse bioassay. All samples were collected fromwater-blooming lakes, mainly containing taxa belonging to thecyanobacterial genera Anabaena, Aphanizomenon, Microcystis and Planktothrix. In addition to informationabout occurrence of neuro- or hepatotoxins, knowledge about thedistribution of water-blooming lakes in the country was obtained aswell as about their predominating taxa. Microcystisaeruginosa, Anabaena flos-aquae and Aphanizomenonflos-aquae were the most frequently occurring taxa in the lakes.Among the taxa observed, nine different cyanobacterial species withcertainty produce toxins. Microcystis spp. most frequentlyproduced toxic blooms (only hepatotoxins). Anabaena spp.,however, caused the majority of waterblooms. The Anabaenaflos-aquae-group produced neurotoxins [incl. anatoxin-a(s)],neurotoxins + hepatotoxins or only hepatotoxins. Aphanizomenon flos-aquae was only recorded as toxin-producing inthree Swedish lakes, which may be compared with the conditions inFinland, where it was toxic in 36 bloom samples. Aspects are givenon toxicity versus lake acidification and trophic conditions, aswell as on health effects on animals and humanbeings.     

Autumn phytoplankton assemblages in temperate lakes of different eutrophication level in the middle part of Sweden

Phytoplankton assemblages were studied during autumn 1998 in oligo-, meso- and eutrophic lakes in central Sweden (62°54'N). Differences in phytoplankton assemblages have been detected both in space and time. In eutrophic lakes coccoid Chlorophyceae dominated quantitatively during September and October. Diatoms were the most diverse group in all types of lakes in September and in meso- and oligotrophic lakes in October. In November Cryptophyceae became the most abundant group in all lakes. The total richness of species decreased in the meso- and oligotrophic environments in November compared to September and October, whilst in the eutrophic environment it remained almost unchanged. Cluster analyses, using both presence-absence and presence-absence in combination with abundance matrices, showed similar results and a good resolution between the lakes of different eutrophication conditions. We conclude that the phytoplankton assemblages of the lakes studied depended on the trophic conditions and thus they can be used for resolution between different eutrophication levels.     

Abundance and diversity of eukaryotic rather than bacterial community relate closely to the trophic level of urban lakes

Scientific understanding of biotic effects on the water trophic level is lacking for urban lakes during algal bloom development stage. Based on the Illumina MiSeq sequencing, quantitative polymerase chain reaction (PCR), and multiple statistical analyses, we estimated distribution patterns and ecological roles of planktonic bacteria and eukaryotes in urban lakes during algal bloom development stage (i.e., April, May, and June). Cyanobacteria and Chlorophyta mainly dominated algal blooms. Bacteria exhibited significantly higher absolute abundance and community diversity than eukaryotes, whereas abundance and diversity of eukaryotic rather than bacterial community relate closely to the water trophic level. Multinutrient cycling (MNC) index was significantly correlated with eukaryotic diversity rather than bacterial diversity. Stronger species replacement, broader environmental breadth, and stronger phylogenetic signal were found for eukaryotic community than for bacterial community. In contrast, bacterial community displayed stronger community stability and environmental constraint than eukaryotic community. Stochastic and differentiating processes contributed more to community assemblies of bacteria and eukaryotes. Our results emphasized that a strong linkage between planktonic diversity and MNC ensured a close relationship between planktonic diversity and the water trophic level of urban lakes. Our findings could be useful to guide the formulation and implementation of environmental lake protection measures.     

Macrophytes moderate the taxonomic and functional composition of phytoplankton assemblages during a nutrient loading experiment

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Increased risk of cyanobacterial blooms in northern high‐latitude lakes through climate warming and phosphorus enrichment

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Feeding dynamics of the copepod Diacyclops thomasi before, during and following filamentous cyanobacteria blooms in a large, shallow temperate lake

Cyanobacteria blooms are an increasing problem in temperate freshwater lakes, leading to reduced water quality and in some cases harmful effects from toxic cyanobacteria species. To better understand the role of zooplankton in modulating cyanobacteria blooms, from 2008 to 2010 we measured water quality and plankton abundance, and measured feeding rates and prey selectivity of the copepod Diacyclops thomasi before, during and following summertime cyanobacteria blooms in a shallow, eutrophic lake (Vancouver Lake, Washington, USA). We used a combined field and experimental approach to specifically test the hypothesis that copepod grazing was a significant factor in establishing the timing of cyanobacteria bloom initiation and eventual decline in Vancouver Lake. There was a consistent annual succession of zooplankton taxa, with cyclopoid copepods (D. thomasi) dominant in spring, followed by small cladocerans (Eubosmina sp.). Before each cyanobacteria bloom, large cladocerans (Daphnia retrocurva, Daphnia laevis) peaked in abundance but quickly disappeared, followed by brief increases in rotifers. During the cyanobacteria blooms, D. thomasi was again dominant, with small cladocerans abundant in autumn. Before the cyanobacteria blooms, D. thomasi substantially consumed ciliates and dinoflagellates (up to 100% of prey biomass per day), which likely allowed diatoms to flourish. A shift in copepod grazing toward diatoms before the blooms may have then helped to facilitate the rapid increase in cyanobacteria. Copepod grazing impact was the highest during the cyanobacteria blooms both years, but focused on non-cyanobacteria prey; copepod grazing was minimal as the cyanobacteria blooms waned. We conclude that cyclopoid copepods may have an indirect role (via trophic cascades) in modulating cyanobacteria bloom initiation, but do not directly contribute to cyanobacteria bloom decline.     

Phytoplankton distribution patterns in the northwestern Sargasso Sea revealed by small subunit rRNA genes from plastids

Phytoplankton species vary in their physiological properties, and are expected to respond differently to seasonal changes in water column conditions. To assess these varying distribution patterns, we used 412 samples collected monthly over 12 years (1991–2004) at the Bermuda Atlantic Time-Series Study site, located in the northwestern Sargasso Sea. We measured plastid 16S ribosomal RNA gene abundances with a terminal restriction fragment length polymorphism approach and identified distribution patterns for members of the Prymnesiophyceae, Pelagophyceae, Chrysophyceae, Cryptophyceae, Bacillariophyceae and Prasinophyceae. The analysis revealed dynamic bloom patterns by these phytoplankton taxa that begin early in the year, when the mixed layer is deep. Previously, unreported open-ocean prasinophyte blooms dominated the plastid gene signal during convective mixing events. Quantitative PCR confirmed the blooms and transitions of Bathycoccus, Micromonas and Ostreococcus populations. In contrast, taxa belonging to the pelagophytes and chrysophytes, as well as cryptophytes, reached annual peaks during mixed layer shoaling, while Bacillariophyceae (diatoms) were observed only episodically in the 12-year record. Prymnesiophytes dominated the integrated plastid gene signal. They were abundant throughout the water column before mixing events, but persisted in the deep chlorophyll maximum during stratified conditions. Various models have been used to describe mechanisms that drive vernal phytoplankton blooms in temperate seas. The range of taxon-specific bloom patterns observed here indicates that different ‘spring bloom'' models can aptly describe the behavior of different phytoplankton taxa at a single geographical location. These findings provide insight into the subdivision of niche space by phytoplankton and may lead to improved predictions of phytoplankton responses to changes in ocean conditions.     

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.     

Equilibrium/steady-state concept in phytoplankton ecology

This paper summarises the outcomes of the 13^th Workshop of the International Association of Phytoplankton Taxonomy and Ecology (IAP). The authors mostly addressed their contributions on the following topics: the effect of trophic state on the attainment of a steady-state; the establishment of equilibria in deep and shallow lakes; the role of spatial heterogeneity, disturbance, and stress in the establishment of equilibrium assemblages; the mechanisms leading to the steady state; the frequency and longevity of equilibrium phases, and the role of morphological and physiological plasticity of phytoplankton in maintaining the (apparently) same populations under different environmental conditions. The composition of steady-state assemblages is compared to that of phytoplankton functional groups (coda). Those functional associations recognised as steady-state assemblages appear to be strongly K-determined in many instances.     

Extracellular phosphatases produced by phytoplankton and other sources in shallow eutrophic lakes (Wuhan, China): taxon-specific versus bulk activity

Extracellular phosphatases are an important part of the phosphorus cycle in aquatic environments. Phosphatase activity (PA) in plankton was studied in seven subtropical shallow lakes of different exploitation management and trophic status in the urban area of Wuhan City. Bulk PA was rather high (range 1.1–11 μmol l⁻¹ h⁻¹), although concentrations of soluble reactive phosphorus (SRP) were also high (range 27 μg P l⁻¹ to ~1.5 mg P l⁻¹) in all lakes. Cell-associated extracellular PA in phytoplankton was detected using the fluorescence-labelled enzyme activity technique. Phytoplankton species partly contributed to the bulk PA. We found explicit differences in the presence of cell-associated phosphatase within the main phytoplankton groups; species belonging to Chlorophyta and Dinophyta were regularly phosphatase-positive, while Cyanophyta and Bacillariophyceae were phosphatase-negative in all but one case. Furthermore, there is a certain potential of extracellular phosphatases produced by heterotrophic nanoflagellates in most of the lakes. This new finding compromises the ‘traditional’ interpretation of bulk phosphatase data as being due to overall phytoplankton or bacterial P regeneration.     

The composition and abundance of phytoplankton in Lake Bukoni,western Uganda

Lake Bukoni is one of the crater lakes in western Uganda. Investigations into this lake is limited compared to other African lakes. Data on phytoplankton ecology in the lake are lacking. Phytoplankton consists of a community of photosynthetic, microscopic plants adapted to suspension in water. They constitute ‘hidden flora’ which make an important contribution to the primary productivity of a water mass. Some phytoplankton taxa, among them species belonging to Cyanophyta, are known to influence ecological transformations and to cause health hazards in water bodies that are used by humans. From July 2004 to December 2005, phytoplankton was collected from two sites (inshore and offshore) in Lake Bukoni. An inverted microscope, Sedgwick counting chamber and multiple tally denominator were used to quantify the phytoplankton. Phytoplankton was dominated by nonheterocystous cyanoprokaryotes especially Lyllgbya limnetica followed by the diatoms Synedra ulna and Fragillaria mutabilis. The inshore site had more phytoplankton species. Differences in phytoplankton diversity and density were mainly attributed to mixing and presence of macrophytes. The occurrence of large numbers of cyanoprokaryotes poses a potential health hazard to the local people who utilize the water from Lake Bukoni. The dominance of cyanoprokaryotes might result in ecological transformations like loss of biodiversity.     

Nutrient limitation and algal blooms in urbanizing tidal creeks

Tidal creeks are commonly found in low energy systems on the East and Gulf Coasts of the United States, and are often subject to intense watershed human development. Many of these creeks are receiving urban and suburban runoff containing nutrients, among other pollutants. During the period 1993-2001, we studied three tidal creeks located in southeastern North Carolina, a rapidly urbanizing area. All three creeks received anthropogenic nutrient loading. Oligohaline to mesohaline stations in upper tidal creek regions had much higher nutrient (especially nitrate-N) concentrations than lower creek areas, and hosted spring and summer phytoplankton blooms that at times exceeded 200 μg chlorophyll a l⁻¹. Phytoplankton biomass during winter was low at all stations in all three creeks. Spring and summer nutrient addition bioassay experiments were conducted to characterize the nutrients limiting phytoplankton growth. Water from high salinity stations in all three creeks always showed significant positive responses to nitrate-N inputs, even at concentrations as low as 50 μg N l⁻¹. Low salinity stations in upper creek areas often showed significant responses to nitrate-N inputs, but on occasion showed sensitivity to phosphorus inputs as well, indicating the influence of anthropogenic nitrate loading. During several experiments, one of the upper stations showed no positive response to nutrient inputs, indicating that these stretches were nutrient replete, and further phytoplankton growth appeared to be light-limited either by phytoplankton self-shading or turbidity. Water from upper creek areas yielded much higher chlorophyll a concentrations in bioassay experiments than did lower creek water. In general, these urbanizing tidal creeks were shown to be very sensitive to nitrogen loading, and provide a physical environment conducive to phytoplankton bloom formation in nutrient-enriched areas. Tidal creeks are important ecological resources in that they are considered to be nursery areas for many species of fish and shellfish. To protect the ecological function of these small, but very abundant estuarine systems, management efforts should recognize their susceptibility to algal blooms and focus on control of nonpoint source nutrient inputs, especially nitrogen.     

Increased nutrient loading and rapid changes in phytoplankton expected with climate change in stratified South European lakes: sensitivity of lakes with different trophic state and catchment properties

We hypothesised that increasing winter affluence and summer temperatures, anticipated in southern Europe with climate change, will deteriorate the ecological status of lakes, especially in those with shorter retention time. We tested these hypotheses analysing weekly phytoplankton and chemistry data collected over 2 years of contrasting weather from two adjacent stratified lakes in North Italy, differing from each other by trophic state and water retention time. Dissolved oxygen concentrations were higher in colder hypolimnia of both lakes in the second year following the cold winter, despite the second summer was warmer and the lakes more strongly stratified. Higher loading during the rainy winter and spring increased nutrient (N, P, Si) concentrations, and a phytoplankton based trophic state index, whilst the N/P ratio decreased in both lakes. The weakened Si limitation in the second year enabled an increase of diatom biovolumes in spring in both lakes. Chlorophyll a concentration increased in the oligo-mesotrophic lake, but dropped markedly in the eutrophic lake where the series of commonly occurring cyanobacteria blooms was interrupted. The projected increase of winter precipitation in southern Europe is likely to increase the nutrient loadings to lakes and contribute to their eutrophication. The impact is proportional to the runoff/in-lake concentration ratio of nutrients rather than to the retention time, and is more pronounced in lakes with lower trophy.