Recent Patterns in Lake Erie Phosphorus and Chlorophyll a Concentrations in Response to Changing Loads.

Despite the initial success of extensive efforts to reduce phosphorus (P) loading to Lake Erie as a part of the Great Lakes Water Quality Agreement, Lake Erie appears to be undergoing a re-eutrophication and it is plagued by harmful algal blooms. To offer insights into potential lake responses under differing Maumee River loads and reveal recent changes with time, we explored patterns in phosphorus and chlorophyll a data from 2008 to 2018 collected in western Lake Erie near the mouth of the Maumee River. We found high, but relatively stable Maumee River and lake concentrations of total P (TP) and soluble reactive P (SRP) with no discernable annual or seasonal patterns. Maumee spring TP load was not strongly related to lake TP, and lake SRP concentrations were positively but weakly related to SRP loads. Lake TP was a strong predictor of chlorophyll a, but the relationship was weaker at sites closer to the Maumee. These results highlight spatial differences both in P concentration and the relationship between TP and chlorophyll a, and these indicate that spring phosphorus loads are a weak algal biomass predictor in the portion of the western basin of Lake Erie represented by these sampling stations.

Cyanobacterial harmful algal blooms are a biological disturbance to Western Lake Erie bacterial communities.

Human activities are causing a global proliferation of cyanobacterial harmful algal blooms (CHABs), yet we have limited understanding of how these events affect freshwater bacterial communities. Using weekly data from western Lake Erie in 2014, we investigated how the cyanobacterial community varied over space and time, and whether the bloom affected non-cyanobacterial (nc-bacterial) diversity and composition. Cyanobacterial community composition fluctuated dynamically during the bloom, but was dominated by Microcystis and Synechococcus OTUs. The bloom's progression revealed potential impacts to nc-bacterial diversity. Nc-bacterial evenness displayed linear, unimodal, or no response to algal pigment levels, depending on the taxonomic group. In addition, the bloom coincided with a large shift in nc-bacterial community composition. These shifts could be partitioned into components predicted by pH, chlorophyll a, temperature, and water mass movements. Actinobacteria OTUs showed particularly strong correlations to bloom dynamics. AcI-C OTUs became more abundant, while acI-A and acI-B OTUs declined during the bloom, providing evidence of niche partitioning at the sub-clade level. Thus, our observations in western Lake Erie support a link between CHABs and disturbances to bacterial community diversity and composition. Additionally, the short recovery of many taxa after the bloom indicates that bacterial communities may exhibit resilience to CHABs.

Ecophysiological Examination of the Lake Erie Microcystis Bloom in 2014: Linkages between Biology and the Water Supply Shutdown of Toledo, OH.

Annual cyanobacterial blooms dominated by Microcystis have occurred in western Lake Erie (U.S./Canada) during summer months since 1995. The production of toxins by bloom-forming cyanobacteria can lead to drinking water crises, such as the one experienced by the city of Toledo in August of 2014, when the city was rendered without drinking water for >2 days. It is important to understand the conditions and environmental cues that were driving this specific bloom to provide a scientific framework for management of future bloom events. To this end, samples were collected and metatranscriptomes generated coincident with the collection of environmental metrics for eight sites located in the western basin of Lake Erie, including a station proximal to the water intake for the city of Toledo. These data were used to generate a basin-wide ecophysiological fingerprint of Lake Erie Microcystis populations in August 2014 for comparison to previous bloom communities. Our observations and analyses indicate that, at the time of sample collection, Microcystis populations were under dual nitrogen (N) and phosphorus (P) stress, as genes involved in scavenging of these nutrients were being actively transcribed. Targeted analysis of urea transport and hydrolysis suggests a potentially important role for exogenous urea as a nitrogen source during the 2014 event. Finally, simulation data suggest a wind event caused microcystin-rich water from Maumee Bay to be transported east along the southern shoreline past the Toledo water intake. Coupled with a significant cyanophage infection, these results reveal that a combination of biological and environmental factors led to the disruption of the Toledo water supply. This scenario was not atypical of reoccurring Lake Erie blooms and thus may reoccur in the future.

A kinetic study of accumulation and elimination of microcystin-LR in yellow perch (Perca flavescens) tissue and implications for human fish consumption.

Fish consumption is a potential route of human exposure to the hepatotoxic microcystins, especially in lakes and reservoirs that routinely experience significant toxic Microcystis blooms. Understanding the rates of uptake and elimination for microcystins as well as the transfer efficiency into tissues of consumers are important for determining the potential for microcystins to be transferred up the food web and for predicting potential human health impacts. The main objective of this work was to conduct laboratory experiments to investigate the kinetics of toxin accumulation in fish tissue. An oral route of exposure was employed in this study, in which juvenile yellow perch (Perca flavescens) were given a single oral dose of 5 or 20 µg of microcystin-LR (MC-LR) via food and accumulation in the muscle, liver, and tank water were measured over 24 h. Peak concentrations of the water soluble fraction of microcystin were generally observed 8-10 h after dosing in the liver and after 12-16 h in the muscle, with a rapid decline in both tissues by 24 h. Up to 99% of the total recoverable (i.e., unbound) microcystin was measured in the tank water by 16 h after exposure. The relatively rapid uptake and elimination of the unbound fraction of microcystin in the liver and muscle of juvenile yellow perch within 24 h of exposure indicates that fish consumption may not be a major route of human exposure to microcystin, particularly in the Great Lakes.

Reduced forms of nitrogen are a driver of non-nitrogen-fixing harmful cyanobacterial blooms and toxicity in Lake Erie.

Western Lake Erie (WLE) experiences anthropogenic eutrophication and annual, toxic cyanobacterial blooms of non-nitrogen (N) fixing Microcystis. Numerous studies have shown that bloom biomass is correlated with an increased proportion of soluble reactive phosphorus loading from the Maumee River. Long term monitoring shows that the proportion of the annual Maumee River N load of non-nitrate N, or total Kjeldahl nitrogen (TKN), has also increased significantly (Spearman's ρ = 0.68, p = 0.001) over the last few decades and is also significantly correlated to cyanobacterial bloom biomass (Spearman's ρ = 0.64, p = 0.003). The ratio of chemically reduced N to oxidized N (TKN:NO3) concentrations was also compared to extracted chlorophyll and phycocyanin concentrations from all weekly sampling stations within WLE from 2009 to 2015. Both chlorophyll (Spearman's ρ = 0.657, p < 0.0001) and phycocyanin (Spearman's ρ = 0.714, p < 0.0001) were significantly correlated with TKN:NO3. This correlation between the increasing fraction of chemically reduced N from the Maumee River and increasing bloom biomass demonstrates the urgent need to control N loading, in addition to current P load reductions, to WLE and similar systems impacted by non-N-fixing, toxin-producing cyanobacteria.

Challenges for mapping cyanotoxin patterns from remote sensing of cyanobacteria.

Using satellite imagery to quantify the spatial patterns of cyanobacterial toxins has several challenges. These challenges include the need for surrogate pigments - since cyanotoxins cannot be directly detected by remote sensing, the variability in the relationship between the pigments and cyanotoxins - especially microcystins (MC), and the lack of standardization of the various measurement methods. A dual-model strategy can provide an approach to address these challenges. One model uses either chlorophyll-a (Chl-a) or phycocyanin (PC) collected in situ as a surrogate to estimate the MC concentration. The other uses a remote sensing algorithm to estimate the concentration of the surrogate pigment. Where blooms are mixtures of cyanobacteria and eukaryotic algae, PC should be the preferred surrogate to Chl-a. Where cyanobacteria dominate, Chl-a is a better surrogate than PC for remote sensing. Phycocyanin is less sensitive to detection by optical remote sensing, it is less frequently measured, PC laboratory methods are still not standardized, and PC has greater intracellular variability. Either pigment should not be presumed to have a fixed relationship with MC for any water body. The MC-pigment relationship can be valid over weeks, but have considerable intra- and inter-annual variability due to changes in the amount of MC produced relative to cyanobacterial biomass. To detect pigments by satellite, three classes of algorithms (analytic, semi-analytic, and derivative) have been used. Analytical and semi-analytical algorithms are more sensitive but less robust than derivatives because they depend on accurate atmospheric correction; as a result derivatives are more commonly used. Derivatives can estimate Chl-a concentration, and research suggests they can detect and possibly quantify PC. Derivative algorithms, however, need to be standardized in order to evaluate the reproducibility of parameterizations between lakes. A strategy for producing useful estimates of microcystins from cyanobacterial biomass is described, provided cyanotoxin variability is addressed.

The contrasting roles of sedimentary plant-derived carbon and black carbon on sediment-spiked hydrophobic organic contaminant bioavailability to Diporeia species and Lumbriculus variegatus.

In bioavailability studies, the biota sediment accumulation factor (BSAF) is invoked to describe the thermodynamic partitioning of a hydrophobic organic contaminant (HOC) between the organism lipid and the organic carbon fraction of the sedimentary matrix and accounts for differences in bioavailability among sediments. Bioaccumulation experiments were performed with Lumbriculus variegatus and Diporeia species exposed in seven sediments dosed with 2,4,5,2',4',5'-hexachlorobiphenyl (HCBP) and benzo[a]pyrene (BaP) or pyrene (PY) and 3,4,3',4'-tetrachlorobiphenyl (TCBP). The BSAF values for the nonplanar HCBP were consistent with equilibrium partitioning theory (EQP) and averaged 2.87 for L. variegatus and 1.45 for Diporeia, while the BSAF values for the planar compounds (BaP, PY, TCBP) were generally lower than estimated from EQP (<1). Correcting the BSAF values of the planar compounds for enhanced sorption due to black carbon improved the BSAF values for L. variegatus, generally resulting in values consistent with EQP, but substantial variation remained for Diporeia. The BSAF values for the planar compounds showed significant positive correlations with plant-derived carbon in sediments (lignin and pigments) but were more consistent for L. variegatus than for Diporeia. These correlations imply that compounds sorbed to plant-derived carbon are more bioavailable since this material is more likely ingested providing a second exposure route.

Time-dependent toxicity of dichlorodiphenyldichloroethylene to Hyalella azteca.

Temporal effects on body residues of dichlorodiphenyldichloroethylene (DDE) associated with mortality in the freshwater amphipod Hyalella azteca were evaluated. Toxicokinetics and body residues were determined from water-only exposures that varied from 4 to 28 d, and DDE concentrations ranging from 0.0013 to 0.045 micromol L(-1). Uptake and elimination parameters were not affected significantly by the various temporal and concentration treatments. Uptake rate coefficients ranged from 134.3 to 586.7 ml g(-1) h(-1), and elimination rate coefficients ranged from 0.0011 to 0.0249 h(-1). Toxicity metric values included body residue for 50% mortality at a fixed sample time (LR50) and mean lethal residue to produce 50% mortality from individual exposure concentrations (MLR50) for live organisms and dead organisms. A twofold increase occurred in the MLR50 values calculated using live organisms compared to MLR50 values using dead organisms. Toxicity and kinetic data were fit to a damage assessment model that allows for the time course for toxicokinetics and damage repair, demonstrating the time-dependence of body residues to toxicity. The DDE appeared to act through a nonpolar narcosis mode of action for both acute and chronic mortality in H. azteca. Furthermore, the temporal trend in the toxic response using body residue as the dose metric is steep and found to be similar to another chlorinated hydrocarbon, pentachlorobenzene, but was more potent than that found for polycyclic aromatic hydrocarbons (PAHs).

Bioaccumulation and critical body residue of PAHs in the amphipod, Diporeia spp: additional evidence to support toxicity additivity for PAH mixtures.

Polycyclic aromatic hydrocarbons (PAHs) are considered to act additively when exposed as congener mixtures. Additive internal concentrations at the site of toxic action is the basis for recent efforts to establish a sum PAH guideline for sediment-associated PAH toxicity. This study determined the toxicity of several PAH congeners on a body residue basis in Diporeia spp. These values were compared to the previously established LR(50) value for a PAH mixture based on the molar sum of PAH congeners and demonstrated similar LR(50) values for individual PAH. These results support the contention that the PAH act at the same molar concentration whether present as individual compounds or in mixture. Aqueous exposures were conducted for 28 d, and the water was exchanged daily to maintain the exposure concentration. The concentration in the exposures declined by an average of 22% between water exchanges across all compounds, and ranged from 11% to 32%. The toxicokinetics were determined using both time-weighted-average (TWA) and time-variable water concentrations and were not statistically different between the two source functions. Toxicity was determined for both mortality and immobility (failure to swim on prodding) and on both a TWA water concentration and a body residue basis. The LC(50) values ranged from 1757 microg l(-1) for naphthalene after 10 d exposure to 79.1 microg l(-1) for pyrene after 28 d exposure, and the EC(50) ranged from 1587 microg l(-1) for naphthalene after 10 d exposure to 38.2 microg l(-1) for pyrene after 28 d exposure. The LR(50) values for all congeners at all lengths of exposure were essentially constant and averaged 7.5+/-2.6 micromol g(-1), while the ER(50) for immobility averaged 2.6+/-0.6 micromol g(-1). The bioconcentration factor declined with increasing exposure concentration and was driven primarily by a lower uptake rate with increasing dose, while the elimination remained essentially constant for each compound.

The role of desorption for describing the bioavailability of select polycyclic aromatic hydrocarbon and polychlorinated biphenyl congeners for seven laboratory-spiked sediments.

Lumbriculus variegatus and Diporeia spp. were exposed to two contaminant pairs 3H-benzo[a]pyrene (BaP) and 14C-2,4,5,2'4',5'-hexachlorobiphenyl (HCBP), and 3H-pyrene (PY) and 14C-3,4,3',4'-tetrachlorobiphenyl (TCBP) sorbed to each of seven field-collected sediments of varying composition. Toxicokinetic coefficients, bioaccumulation factors (BAF), and biota-sediment accumulation factors ([BSAF], BAF normalized to the organism lipid content and sediment organic carbon content) were determined. The contaminant desorption rates from sediments were measured with a Tenax resin extraction technique. The desorption rate constants for rapid, slow, and very slow contaminant compartments and the fractions of contaminant in each compartment were compared with the toxicokinetic coefficients, BAF, and BSAF to describe contaminant behavior across sediments, among compounds, and between species. The best description of the bioavailability was the log BSAF regressed against the fraction rapidly desorbed (F(rapid)) across all sediments and compounds for both species, r2 = 0.67 and 0.66 for L. variegatus and Diporeia, respectively. Use of a calculated fraction desorbed in 6 h or 24 h, which has been suggested as a surrogate for F(rapid,) did not produce as predictive a regression because of uneven desorption in a fixed duration for each compound among the sediments. Thus, F(rapid)provided a good surrogate for the bioavailability of the sediment-sorbed contaminant as represented by BSAF across seven sediments and four compounds with predictions within a factor of approximately two of the measured value.

Time-dependent lethal body residues for the toxicity of pentachlorobenzene to Hyalella azteca.

The study examined the temporal response of Hyalella azteca to pentachlorobenzene (PCBZ) in water-only exposures. Toxicity was evaluated by calculating the body residue of PCBZ associated with survival. The concentration of PCBZ in the tissues of H. azteca associated with 50% mortality decreased from 3 to 0.5 micromol/g over the temporal range of 1 to 28 d, respectively. No significant difference was observed in the body residue calculated for 50% mortality when the value was determined using live or dead organisms. Metabolism of PCBZ was not responsible for the temporal response because no detectable PCBZ biotransformation occurred over an exposure period of 10 d. A damage assessment model was used to evaluate the impact and repair of damage by PCBZ on H. azteca. The toxicokinetics were determined so that the temporal toxicity data could be fit to a damage assessment model. The half-life calculated for the elimination of PCBZ averaged approximately 49 h, while the value determined for the half-life of damage repair from the damage assessment model was 33 h.

Investigating the role of desorption on the bioavailability of sediment-associated 3,4,3',4'-tetrachlorobiphenyl in benthic invertebrates.

Only a fraction of all sediment-associated hydrophobic organic contaminants are bioavailable, and a simple Tenax extraction procedure may estimate this fraction. Bioavailability is assumed to coincide with the rapidly and, possibly, slowly desorbing sediment-associated contaminant. River sediment was spiked with radiolabeled (14C) and nonradiolabeled (12C) 3,4,3',4'-tetrachlorobiphenyl (TCBP), and desorption kinetics using Tenax extraction were obtained at 10 degrees C and 22 degrees C. Bioaccumulation was measured in Lumbriculus variegatus, Chironomus tentans, and Hyalella azteca. Desorption of TCBP was triphasic at 22 degrees C and slowed at 10 degrees C to show only biphasic kinetics. The rapidly desorbing fractions decreased with increasing TCBP sediment concentration. The biota sediment accumulation factors, biota accumulation factors, and sediment clearance coefficients (ks) also decreased with increasing sediment TCBP concentration. The rapidly plus slowly desorbing fractions and the total TCBP desorbed when 99.9% of the rapidly desorbing fraction had desorbed were used to estimate bioavailable TCBP. These Tenax-based fractions did not explain the decreasing bioavailability with increasing TCBP load. Several factors, such as animal behavior and TCBP water solubility limitations, were evaluated to explain the concentration effect, but the most likely cause was severe diffusion limitations in whole sediment that were not predicted by the fully mixed Tenax extraction. Therefore, desorbing fractions determined by Tenax extraction overestimated the bioavailable fractions in sediments.

Effect of 3,4,3',4'-tetrachlorobiphenyl on the reworking behavior of Lumbriculus variegatus exposed to contaminated sediment.

The reworking response (bioturbation) of the oligochaete Lumbriculus variegatus was measured by following the burial rate and spread of a 137Cs marker layer translating worm activity into a biological burial rate (Wb) and a biological diffusion rate constant (Db) for surficial sediment mixing. Reworking was measured at 10 and 22 degrees C in two sediments: a reference site sediment dosed with 3,4,3',4'-tetrachlorobiphenyl (TCBP) and a field-collected sediment from a polychlorinated biphenyl (PCB)-contaminated site in Dicks Creek (DCC, Middletown, OH, USA). The body residue associated with response to TCBP also was determined. Reduction in the temperature from 22 to 10 degrees C reduced both Wb and Db by a factor of approximately two. The internal TCBP concentration to reduce the Wb by 50% was 96 nmol/g (95% CI 45-225 nmol/g) and 124 nmol/g (40-547 nmol/g) (28 and 36 microg/g) wet weight at 22 and 10 degrees C, respectively, and was independent of temperature. The Wb for the DCC sediment was lower than observed for the highest TCBP treatment. The internal body residue for total PCB for worms exposed to DCC sediment was 20-fold lower than TCBP in worms exposed to the lowest TCBP treatment on a molar basis. Comparing body residues of total PCB to TCBP assumes that the PCB congeners act additively on a molar basis. The DCC site contained a higher proportion of coarse material and a lower organic carbon concentration. The difference in sediment characteristics was assumed to be responsible for differences in the Wb.

Comparing behavioral and chronic endpoints to evaluate the response of Lumbriculus variegatus to 3,4,3',4'-tetrachlorobiphenyl sediment exposures.

The response of Lumbriculus variegatus to 3,4,3',4'-tetrachlorobiphenyl (TCBP) was examined with feeding behavior and changes in carbon assimilation by using stable carbon isotopes at 22 and 10 degrees C. The classical measure of feeding behavior determined on a subset of sediment for which the biological burial rate was determined in a companion study allowed direct method comparison. This comparison helped address relationships between biological burial rate, feeding rate, and bioaccumulation. The change in stable isotope composition reflects the total metabolic activity by measuring carbon assimilation rate and was compared to feeding rate, biological burial rate (as determined in the companion study), and reproduction. Decreasing the temperature from 22 to 10 degrees C resulted in a twofold reduction in feeding rate and carbon assimilation. The fractional decline in feeding rate relative to the control mimicked the decline in the biological burial rate with increasing TCBP concentration that was found in the companion study. The bioaccumulation factor declined with increasing TCBP sediment concentration, tracking the feeding rate decline. Stable isotope measures showed differences in metabolic rates between the exposure temperatures but did not distinguish a metabolic rate change at 22 degrees C among TCBP treatments. Likewise, reproduction declined from 22 to 10 degrees C, with no reproduction at 10 degrees C. Like the stable isotope measure, no dose response was found among TCBP treatments at 22 degrees C. The reduction in carbon assimilation rate tracked the reduction in reproduction with lower temperature.

Predicting bioavailability of sediment-associated organic contaminants for Diporeia spp. and oligochaetes.

Biota-sediment accumulation factors (BSAF) were calculated for Diporeia spp. and oligochaete worms exposed to polychlorinated biphenyls (PCBs) and polycyclic aromatic hydrocarbons (PAHs) from field-collected sediment. These data were compared to the contaminant fraction extracted from sediment with Tenax resin using a 24 h extraction. A previous laboratory study suggested a linear relationship between log BSAF and the contaminant fraction rapidly desorbed from sediment. However, the BSAF data in our study did not fit this relationship. Better predictive regressions for both PCBs and PAHs were found when the log of the lipid-normalized organism contaminant concentrations were plotted against the log of the Tenax-extracted organic carbon-normalized sediment contaminant concentration. Regression lines for the two species had the same slope, but the Diporeia intercept was 2.3 times larger. When adjusted for a 6 h Tenax extraction, based on a regression between 6 and 24 h Tenax extractions, data from this study and two other studies that included multiple oligochaete species fit a single predictive regression. The exception included some PAHs that fell below the regression line. Thus, a single relationship generally predicted bioaccumulation across sediments, compound classes, oligochaete species, and among laboratories.