Ellie E. Prepas

Hepatotoxic Cyanobacteria: A Review of the Biological Importance of Microcystins in Freshwater Environments

Cyanobacteria possess many adaptations to develop population maxima or “blooms” in lakes and reservoirs. A potential consequence of freshwater blooms of many cyanobacterial species is the production of potent toxins, including the cyclic hepatotoxins, microcystins (MCs). Approximately 70 MC variants have been isolated. Their toxicity to humans and other animals is well studied, because of public health concerns. This review focuses instead on the production and degradation of MCs in freshwater environments and their effects on aquatic organisms. Genetic research has revealed the existence of MC-related genes, yet the expression of these genes seems to be regulated by complex mechanisms and is influenced by environmental factors. In natural water bodies, the species composition of cyanobacterial communities and the ratio of toxic to nontoxic species and strains are largely responsible for total toxin production. Cyanobacteria play vital roles in aquatic food webs, yet production, accumulation, and toxicity patterns of MCs within aquatic food webs remain obscure. R. Zurawell was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant to E. Prepas. The authors wish to thank D. G. Dixon for the inspiration to write this review and S. Pinder for assisting with figure preparation. Thorough reviews of earlier drafts by two anonymous reviewers greatly improved the content and logical development of this article.Current address for Ronald W. Zurawell is Environmental Monitoring and Evaluation Branch, Environmental Assurance Division, Alberta Environment, 10th Floor, Oxbridge Place, 9820-106 St., Edmonton, AB T5K 2J6, Canada.

Current Velocity and Its Effect on Aquatic Macrophytes in Flowing Waters

Current velocity significantly affected the biomass and shoot density of aquatic macrophytes in two slow-flowing rivers in western Canada. Studies of aquatic macrophyte communities at three sites on the Bow River, Alberta, Canada, between 1982 and 1985 showed that biomass decreased with increasing current velocity within the weed bed over the range 0.01-1 m/s; at current speeds in excess of 1 m/s, aquatic macrophytes were rare. Transplant experiments in which Potamogeton pectinatus was grown in pails containing three sediments differing in texture at three sites with different current velocities also demonstrated that biomass and shoot density were affected by both the direct effects of current velocity on plant shoots and its indirect effects on sediment nutrient concentrations. These results indicate that current velocity is an important factor regulating aquatic macrophyte biomass in flowing waters and suggest that even a relatively modest increase in current velocity within weed beds reduces the abundance of submerged aquatic plants.

VARIABILITY OF THE HEPATOTOXIN MICROCYSTIN‐LR IN HYPEREUTROPHIC DRINKING WATER LAKES1

The patterns of occurrence of the peptide hepatotoxin microcystin‐LR (MC‐LR) was studied in three hypereu‐trophic hardwater lakes (Coal, Driedmeat, and Little Beaver) in central Alberta, Canada, over three open‐water seasons. MC‐LR concentration was based on high‐performance liquid chromatography detection and expressed as μg.g−1 of total plankton biomass, ng.L−1 of lake water, and μg.g−1 of Microcystis aeruginosa Kuetz. emend. Elenkin. MC‐LR was highly variable temporally (differences up to 3 orders of magnitude) within each lake over an individual year, between years in an individual lake, and between lakes in any year. Seasonal (within‐year) changes in MC‐LR concentration (expressed in the preceding units) were positively correlated to the abundance and biomass Of the cyanobacterium M. aeruginosa (r =0.60–0.77), total and total dissolved phosphorus concentration (r =0.46–0.59), pH (r=0.38–0.58), and chlorophyll a (r=0.25–0.59). Surprisingly, there was no relationship between MC‐LR concentration and water temperature (range: 7°‐24°C, r =‐0.13 to 0.02) and a negative correlation with nitrate concentration (r =–0.27 to ‐0.34). In two synoptic surveys examining spatial variability, MC‐LR concentrations were quite variable (CV of 185 and 36% between sampling sites for Coal and Little Beaver lakes, respectively). Spatial distribution of MC‐LR on any one day was correlated with the abundance and biomass of M. aeruginosa. Over a 24‐h period, MC‐LR concentration in M. aeruginosa decreased more than 6‐fold at night relative to daytime concentrations. In general, analytical and within‐site variation of MC‐LR was relatively small (CV < 4 and 9%, respectively) but greatest both within and between years in a lake followed by diel and spatial variation.

Individual specialization and trophic adaptability of northern pike (Esox lucius): an isotope and dietary analysis

Abstract Northern pike (Esox lucius) are often considered to be specialist piscivores, but under some circumstances will continue to eat invertebrates as adults. To examine effects of fish assemblage composition on the trophic ecology of pike, we combined stable isotope analysis (SIA) of carbon and nitrogen and stomach content analysis (SCA) on pike from five lakes in northern Alberta, three of which contain only pike (“pike-only”) and two that also contain yellow perch (Perca flavescens) or white sucker (Catostomus commersoni) (“pike-other”). Fish were more important as prey and empty stomachs, which often characterize piscivores, were significantly more frequent in pike-other than in pike-only lakes. However, even though invertebrates were more important for pike in pike-only lakes, SIA and SCA indicated that invertebrates were also an important component of pike diets in pike-other lakes. SIA and SCA also revealed considerable intrapopulation variation in trophic ecology, with individuals in some populations differing by as much as two trophic levels. Comparisons of stomach contents and isotope signatures of the same fish suggested that within these variable populations, specialization on invertebrates or fish was a long-term trait of some individuals. SIA indicated that trophic position increased and diets shifted to a greater importance of littoral prey as pike grew in pike-only lakes, but not in lakes with other fish present. Trophic adaptability in northern pike is expressed at both the population level, where the trophic ecology is sensitive to differences in prey regimes, and at the organismal level, in the form of intrapopulation variation and individual specialization.

Chemical control of hepatotoxic phytoplankton blooms: Implications for human health

Chemicals used to control phytoplankton blooms induce the release of phytotoxins that increase the potential health risks in drinking water supplies. To test this hypothesis, the effects of six chemical treatments on the release of the cyanobacterial toxin, microcystin-LR (MCLR; 182–837 μg g−1 dry wt) from freshly collected phytoplankton were examined in laboratory experiments. In addition, the integrity of a chemically-treated culture of Microcystis aeruginosa was examined by both a scanning electron microscope and a transmission electron microscope. Chemicals which control cyanobacterial blooms through inhibition of cell functions (e.g. Reglone A, potassium permanganate, chlorine, and Simazine) appeared to induce cell lysis and subsequently increased dissolved MCLR concentration in the surrounding water. In contrast, both lime and alum treatment (within pH 6–10) controlled the cyanobacterial blooms mainly by cell-coagulation and sedimentation, without any (lime) or only little (alum) increase in dissolved MCLR concentration in the water. The estimated half-life of released MCLR from these dense cyanobacterial blooms ranged from 0.5 (± 0.1) to 1.6 (± 0.0) d. In contrast, × ⩾39% of the MCLR remained in decaying phytoplankton for up to 26 d, therefore it is likely that MCLR would persist and decay inside the lime or alum coagulated Microcystis cells, before being released into the surrounding water phase. For these reasons, lime or to a lesser extent alum, appears to be more suitable than either algicides or chlorine for the control of microcystin-containing cyanobacterial blooms in drinking water.

Occurrence and toxicological evaluation of cyanobacterial toxins in Alberta lakes and farm dugouts

Abstract The occurrence of neuro- and hepatotoxins produced by cyanobacteria (blue-green algae) was assessed in eight lakes and six farm dugouts, located in Alberta. Anatoxin-a, an alkaloid neurotoxin produced by Anabaena flos-aquae , was not detected in the lake blooms with gas chromatography-mass spectrometry (GC-MS). Algal blooms which contained Microcystis aeruginosa almost always had detectable concentrations of microcystin-LR, a peptide hepatotoxin, based on high performance liquid chromatography (HPLC) analyses. Bloom samples from the six farm dugouts contained no detectable quantity of either anatoxin-a or microcystin-LR. However, anatoxin-a and microcystin-LR were detected in algae isolated and subsequently cultured from two separate dugouts. Microcystin-RR was not detected in any bloom sample collected. Among three lakes studied in greater detail, the concentration of microcystin-LR present in the blooms was highly variable between lakes and temporally within each lake over the limited sampling period. Fast atom bombardment-mass spectrometry (FAB-MS) performed on a composite of several bloom samples from one lake confirmed the identity of microcystin-LR. Bioassays were performed with a subset of the bloom samples to determine acute toxicity to mice. Intraperitoneal injection of bloom extracts containing microcystin-LR resulted in a massive dose-dependent pooling of blood in the liver, shock and very rapid (as quickly as 50 min post-injection) death of injected mice.

Quantitative comparison of lake throughflow, residency, and catchment runoff using stable isotopes: modelling and results from a regional survey of Boreal lakes

An isotope-based approach for water balance assessment is presented and applied to estimate throughflow, residence time and catchment runoff to 70 headwater lakes on the Boreal plain and uplands of northern and north-central Alberta, Canada. The survey reveals a complex hydrologic regime with systematic variability in water balance due to local site characteristics. On average, runoff to lakes in wetland-dominated catchments is found to be significantly higher than runoff to upland-dominated lakes, with generally higher contributions from catchments with low bog/fen ratios. The isotope method, which relies primarily on water sampling and isotopic analysis, can be easily integrated in routine water quality surveys and is shown to be a practical alternative to conventional hydrological modelling for comparative analysis of water balance controls on hydrochemistry and aquatic ecology of lakes, particularly in low-relief wetland-rich terrain.

Hepatic and renal pathology of intraperitoneally administered microcystin-LR in rainbow trout (Oncorhynchus mykiss).

In 26 hr laboratory trials a dose of 1000 micrograms/kg microcystin-LR (MC-LR) caused 100% mortality in rainbow trout, while no mortality was observed at doses of 400 micrograms/kg or less. The liver to body mass ratio increased in fish exposed to the toxin which was likely due to water retention in the liver. In contrast to mammalian studies, hemorrhage of the liver was rare in fish. Exposure to MC-LR caused widespread hepatocellular swelling and lysis of hepatocyte plasma membranes, resulting in liquifactive necrosis (organelles floating in a milieux of cellular debris). Kidney lesions in the fish consisted of coagulative tubular necrosis with a dilation of Bowmans space. Lesions observed in the liver and kidney of fish exposed to MC-LR were considerably different than those previously reported for mammals.

POTENTIAL EFFECTS OF CLIMATE CHANGE ON AQUATIC ECOSYSTEMS OF THE GREAT PLAINS OF NORTH AMERICA

The Great Plains landscape is less topographically complex than most other regions within North America, but diverse aquatic ecosystems, such as playas, pothole lakes, ox-bow lakes, springs, groundwater aquifers, intermittent and ephemeral streams, as well as large rivers and wetlands, are highly dynamic and responsive to extreme climatic fluctuations. We review the evidence for climatic change that demonstrates the historical importance of extremes in north-south differences in summer temperatures and east-west differences in aridity across four large subregions. These physical driving forces alter density stratification, deoxygenation, decomposition and salinity. Biotic community composition and associated ecosystem processes of productivity and nutrient cycling respond rapidly to these climatically driven dynamics. Ecosystem processes also respond to cultural effects such as dams and diversions of water for irrigation, waste dilution and urban demands for drinking water and industrial uses. Distinguishing climatic from cultural effects in future models of aquatic ecosystem functioning will require more refinement in both climatic and economic forecasting. There is a need, for example, to predict how long-term climatic forecasts (based on both ENSO and global warming simulations) relate to the permanence and productivity of shallow water ecosystems. Aquatic ecologists, hydrologists, climatologists and geographers have much to discuss regarding the synthesis of available data and the design of future interdisciplinary research.

Groundwater-lake interactions: I. Accuracy of seepage meter estimates of lake seepage

Abstract The use of seepage meters to identify nearshore seepage patterns and to quantify seepage in lakes was evaluated with a Monte Carlo simulation model. The model simulated seepage flux as would be derived from seepage meter measurements along a transect extending from the shore of a hypothetical lake to 40 or 100m offshore. Along the transect, simulated seepage velocities decreased exponentially with distance from shore according to patterns measured at Narrow Lake, Alta., and Lake Sallie, MN. To determine statistical parameters needed in the model, seepage flux was measured in situ with closely spaced seepage meters at four different sites in Narrow Lake. Seepage velocities within a small area of lakebed were log-normally distributed, and the variance was positively correlated with mean seepage flux. The modeling indicated that the most sensitive parameter affecting the accuracy of seepage meter estimates of seepage patterns and average seepage flux along the transect was the variability in the spatial distribution of seepage flux within a small area of lakebed. There was little improvement in the accuracy of estimates of seepage patterns or transect flux when more than ten seepage meters were simulated along the transect, when the transect was “sampled” more than twice, or when seepage meters along the transect were simulated to follow a stratified rather than a systematic design.