Mesozooplankton and microzooplankton grazing during cyanobacterial blooms in the western basin of Lake Erie

Lake Erie is the most socioeconomically important and productive of the Laurentian (North American) Great Lakes. Since the mid-1990s cyanobacterial blooms dominated primarily by Microcystis have emerged to become annual, late summer events in the western basin of Lake Erie yet the effects of these blooms on food web dynamics and zooplankton grazing are unclear. From 2005 to 2007, grazing rates of cultured (Daphnia pulex) and natural assemblages of mesozooplankton and microzooplankton on five autotrophic populations were quantified during cyanobacterial blooms in western Lake Erie. While all groups of zooplankton grazed on all prey groups investigated, the grazing rates of natural and cultured mesozooplankton were inversely correlated with abundances of potentially toxic cyanobacteria (Microcystis, Anabaena, and Cylindrospermopsis; p < 0.05) while those of the in situ microzooplankton community were not. Microzooplankton grazed more rapidly and consistently on all groups of phytoplankton, including cyanobacteria, compared to both groups of mesozooplankton. Cyanobacteria displayed more rapid intrinsic cellular growth rates than other phytoplankton groups under enhanced nutrient concentrations suggesting that future nutrient loading to Lake Erie could exacerbate cyanobacterial blooms. In sum, while grazing rates of mesozooplankton are slowed by cyanobacterial blooms in the western basin of Lake Erie, microzooplankton are likely to play an important role in the top-down control of these blooms; this control could be weakened by any future increases in nutrient loads to Lake Erie.     

Epiphytic Refugium: Are Two Species of Invading Freshwater Bivalves Partitioning Spatial Resources?

Enumeration of benthic (bottom dwelling) and epiphytic (attached to plants) zebra and quagga mussels (Dreissena polymorpha and D. bugensis, respectively) at Lake Erie near-shore sites in fall of 2000 revealed an unexpected prevalence of the zebra mussel on submerged plants. Even at Buffalo, New York, USA, where benthic dreissenids have been 92–100% quagga mussel since 1996, zebra mussels constituted 30–61% of epiphytes numerically. This may reflect a partitioning of settling space consistent with interspecific competition. A seasonal epiphytic refugium might allow the zebra mussel to persist even where the benthos is almost exclusively quagga mussel. This revised version was published online in July 2006 with corrections to the Cover Date.     

Effects of invasive zebra mussels on phytoplankton,turbidity, and dissolved nutrients in reservoirs

Few experiments have quantified the effects of invasive zebra mussels (Dreissena polymorpha) on man-made reservoirs relative to other aquatic habitats. Reservoirs, however, are the dominate water body type in many of the states that are at the current front of the zebra mussel invasion into the western United States. The objective of this research, therefore, was to determine how zebra mussels affected phytoplankton, turbidity, and dissolved nutrients in water that was collected from three Kansas reservoirs that varied in trophic state (mesotrophic to hypereutrophic), but all experienced frequent cyanobacterial blooms. Laboratory mesocosm experiments were conducted to document the effects of zebra mussels on cyanobacteria and general water quality characteristics in the reservoir water. Zebra mussels significantly reduced algal biomass, and the total biovolume of cyanobacteria (communities were dominated by Anabaena) in each reservoir experiment. The effects of zebra mussels on other major algal groups (diatoms, flagellates, and green algae) and algal diversity were less consistent and varied between the three reservoir experiments. Similarly, the effects of zebra mussels on nutrient concentrations varied between experiments. Zebra mussels increased dissolved phosphorus concentrations in two of the reservoir experiments, but there was no effect of zebra mussels on dissolved phosphorus in the mesotrophic reservoir experiment. Combined, our results strongly suggest that zebra mussels have the potential to significantly impact reservoirs as they continue to expand throughout the western United States. Moreover, the magnitude of these effects may be context dependent and vary depending on the trophic state and/or resident phytoplankton communities of individual reservoirs as has similarly been reported for natural lakes.     

Invasive mussels modify the cycling,storage and distribution of nutrients and carbon in a large lake

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Testing a typology system of running waters for conservation planning in Hungary

The zebra mussel (Dreissena polymorpha) and its congener the quagga mussel (Dreissena rostriformis bugensis) are both invaders in freshwater, but have very different invasion histories, with zebra mussels attaining substantially faster rates of spread at virtually all spatial scales. However, in waterbodies where they co-occur, D. r. bugensis can displace D. polymorpha. To determine if the mechanisms for this displacement are associated with different survival and growth, we kept mussels in flow-through tanks for 289 days with two temperature regimes that mimicked the natural surface water (littoral zone) and hypolimnion conditions of Lake Erie. For the littoral zone regime, we used water directly from the surface of Lake Erie (range 4–25°C, average 11.9 ± 0.6°C). For the profundal zone treatment, Lake Erie surface water was chilled to about 6°C (range 5–8°C, average 6.2 ± 0.6°C) for the full duration of the experiment. For each of these temperature regimes, we used three replicate tanks with only zebra mussels present and three replicate tanks with only quagga mussels (150 ind./tank each), and three replicate tanks with both species (75 ind./tank of each species). Quagga mussels had higher survivorship and grew more than zebra mussels in all treatments. For both species, the size of the mussel entering the winter was critical for survivorship. Larger mussels had a higher survival over the winter in all treatments. For both species, there was a survivorship and growth tradeoff. In the warmer littoral zone treatment both species had higher growth, but lower survival than in the colder profundal zone treatment. Surprisingly, although quagga mussels outperformed zebra mussels, zebra mussel survivorship was better when they were faced with competition by quagga mussels than with just intraspecific competition. In addition, quagga mussels suffered size-specific mortality during the growing season only when facing interspecific competition with zebra mussels. Further experiments are needed to determine the possible mechanisms for these interspecific effects.     

Planktonic green algae in western Lake Erie: the importance of temporal scale in the interpretation of change

1. Total densities of planktonic Chlorophyceae collected in weekly sampling of the Kingsville (Ontario) municipal water intake in western Lake Erie were evaluated for potential effects of the recent zebra mussel ( Dreissena polymorpha ) invasion and for the longer term effects of the Lake Erie phosphorus loading control programme.
2. At a relatively small temporal scale of about 10 years, an apparent zebra mussel-related impact was clearly revealed in 1988 as an inflection point on the cumulative sum chlorophyte density curve. However, at a temporal scale of nearly three decades, this inflection point was not distinct. There was a steady decline in total Chlorophyceae throughout the 1970s which accelerated during the early 1980s; this corresponds to declining western Lake Erie phosphorus loading rates and phosphorus concentrations reported by others over the same period. In the absence of zebra mussels, average annual chlorophyte density decreased by 94% between the early 1970s and the mid-1980s.
3. The dramatic long-term decline of planktonic chlorophytes in western Lake Erie reveals the success of the phosphorus control programme, places the recent impact of the zebra mussels in its proper perspective and underscores the need for and value of long-term limnological data for management of the Laurentian Great Lakes.     

Habitat Shift in Invading Species: Zebra and Quagga Mussel Population Characteristics on Shallow Soft Substrates

Unexpected habitat innovations among invading species are illustrated by the expansion of dreissenid mussels across sedimentary environments in shallow water unlike the hard substrates where they are conventionally known. In this note, records of population characteristics of invading zebra (Dreissena polymorpha) and quagga (Dreissena bugensis) mussels from 1994 through 1998 are reported from shallow (less than 20m) sedimentary habitats in western Lake Erie. Haphazard SCUBA collections of these invading species indicated that combined densities of zebra and quagga mussels ranged from 0 to 32,500 individuals per square meter between 1994 and 1998, with D. polymorpha comprising 75–100% of the assemblages. These mixed mussel populations, which were attached by byssal threads to each other and underlying sand-grain sediments, had size–frequency distributions that were typical of colonizing populations on hard substrates. Moreover, the presence of two mussel cohorts within the 1994 samples indicated that these species began expanding onto soft substrates not later than 1992, within 4 years of their initial invasion in western Lake Erie. Such historical data provide baselines for interpreting adaptive innovations, ecological interactions and habitat shifts among the two invading dreissenid mussel species in North America.     

Preferential manganese accumulation in dreissenid byssal threads

The elemental composition of byssal threads from two freshwater mussels Dreissena polymorpha (zebra) and Dreissena bugensis (quagga) has been determined by proton-induced X-ray emission spectroscopy. Sulphur and manganese are present at 30–100-fold higher concentrations in the threads than in ambient waters of Lake Erie. Calcium, phosphorus and copper levels are also somewhat enhanced in byssus. Since dreissenid byssus is not mineralized, Mn may be organometallically complexed to the functional side chains of byssal proteins.     

太湖西北湖区2003-2012年间氮磷浓度及浮游植物主要类群变化趋势分析

基于2003-2012年太湖竺山湖和西部沿岸区水体理化指标与浮游植物丰度的逐月监测数据,分析了两个湖区氮磷营养盐状态和浮游植物丰度以及浮游植物主要类群的年际变化趋势及季节变化特征,探讨了浮游植物群落变化与水温及营养盐指标间的关系。结果表明：10年间两个湖区氮磷营养盐浓度总体呈下降趋势,以竺山湖TN、NH₃-N浓度和西部沿岸区NO₃-N浓度下降最为显著;浮游植物丰度总体呈上升趋势,蓝藻在群落结构中日益占据绝对优势;季节变化上,氮营养盐浓度表现为春冬季节高于夏秋季节,TP浓度和浮游植物丰度呈相反的变化趋势。Pearson相关分析显示,水温、NH₃-N浓度和TN/TP是影响蓝藻丰度及其在浮游植物群落中所占比例的主要因素。在温度和营养盐结构的共同作用下,10年间两个湖区蓝藻水华暴发时间逐渐提前,而消退时间逐渐滞后,水华持续时间逐年上升。在全球变暖背景下,太湖水华治理需执行更加严格的氮磷限制阈值,且在重污染的西北湖区控磷依然是关键。     

Stoichiometry of regenerated nutrients differs between native and invasive freshwater mussels with implications for algal growth

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Responses of Phytoplankton to in‐situ Nutrient Enrichment; Potential Influences on Species Dominance in a River

The Hawkesbury River at Sackville, New South Wales, Australia is fresh and vigorously mixed by tidal movement. The location has frequent blooms of Microcystis aeruginosa, which have been recorded occurring throughout the year, including winter temperatures as low as 13 °C. Nutrient enrichment tests were performed in‐situ on the natural phytoplankton population in 1997 and 1998 while Microcystis aeruginosa dominated (covering both summer and winter periods). These experiments compared population changes under the ambient nutrient regime with those after additions of ortho‐phosphate, nitrate, ammonia and various combinations of these nutrients. Under ambient conditions, the Microcystis population was able to grow significantly (P < 0.05) while most non‐cyanobacterial phytoplankton did not. Nutrient additions induced a variety of nutrient limitation responses that often varied between genera of major groups i.e. in the Chlorophyceae (Actinastrum sp. responded to phosphorus while Psephonema sp. responded to nitrogen). The possibility that shifts in population dominance from Chlorophyceae to the Cyanobacteria (M. aeruginosa) at Sackville are in response to competition for limiting nutrients is discussed.     

Feedback between zebra mussel selective feeding and algal composition affects mussel condition: did the regime changer pay a price for its success?

1. We investigated the role of algal composition on pumping, clearance, assimilation, pseudofaeces and faeces production, feeding time budgets, and condition of zebra mussels from spring to autumn at two sites in Saginaw Bay (Lake Huron) and one site in western Lake Erie. Size‐fractioned chlorophyll was used to distinguish between feeding on small (<53 μm) and large (>53 μm) size fractions, and mussel feeding behaviour was quantified by video observations. 2. Mussel pumping, clearance and assimilation rates varied among sites, particularly during summer, when phytoplankton composition varied considerably among sites. Lowest values were seen at the inner‐bay site of Saginaw Bay, low to moderate values at the outer‐bay site of Saginaw Bay, and high values at the Lake Erie site. Clearance, pumping and assimilation rates were all highly positively correlated (R² = 0.76) with per cent contribution of flagellates to total algal biomass and negatively correlated with per cent of Microcystis aeruginosa (R² = 0.63). The negative effects on pumping rate (as determined by clearance rate on the <53 μm fraction) of Microcystis, which occurred in the >53 μm fraction, could be mitigated by the presence of flagellates in the <53 μm fraction. 3. Visual observations of mussel feeding showed evidence for poor seston quality during summer negatively affecting feeding rates. High faeces production during times of low assimilation rate was suggestive of poor assimilation efficiency and/or viable gut passage of grazing resistant algae. Long periods of time not filtering by the mussels during some Microcystis blooms and lack of production of a filtering current during one experiment were suggestive of intoxication from microcystin or other secondary compounds. 4. Clearance and feeding rates of the mussels in Saginaw Bay were high during spring and autumn and very low in summer, particularly at the inner‐bay site. Condition of the mussels (mass : length ratio) was highest in spring and lowest during summer. This seasonal variation probably reflected high food assimilation rate during autumn and spring and low assimilation rate and reproduction during summer. The condition of mussels throughout the year was higher at the outer‐bay than the inner‐bay site, reflecting better feeding conditions at the former. Mussel selective feeding may have been responsible for the poor quality of food at the inner bay site; therefore, we postulate that a regime shift in phytoplankton composition promoted by the mussels fed back into lowered condition of the mussels.     

Potential effects on zooplankton from species shifts in planktivorous mussels: a field experiment in the St Lawrence River

1. Suspension feeding by bivalves exceeds that by other planktivores in many North American rivers, and food webs may be altered substantially by differences in feeding patterns between native unionid mussels and invading dreissenid mussels. 2. We conducted an experiment comparing zooplanktivory by one unionid and two dreissenid species that addressed several primary questions. Is benthic planktivory important in this river? Has this linkage been altered substantially by dreissenids? Do the two dreissenid species differ in planktivory, and is this ecologically important if quagga mussels extend their geographical range? 3. Our 12‐day experiment consisted of controls (no mussels) and treatments with unionid (Elliptio complanata), quagga (Dreissena bugensis) or zebra (D. polymorpha) mussels in 3500‐L, 80‐μm mesh enclosures placed in a slackwater area of the St Lawrence River. 4. The density of the most abundant calanoid copepod Eurytemora affinis increased in the presence of dreissenids, probably as an indirect food web response. By day 12, a cumulative effect was shown by the most overwhelmingly abundant rotifer, Polyarthra, whose density declined dramatically in dreissenid enclosures compared with control and unionid enclosures. Rotifer densities in unionid enclosures were not different from controls, nor were dreissenid treatments different from each other. The effects on rotifers were probably from predation, as Chl‐a did not vary among treatments. 5. We conclude that benthic‐pelagic coupling via planktivory is important in slackwater areas. Dreissenids have strengthened this linkage, but range extension of quaggas should not appreciably alter effects produced by a similar biomass of zebra mussels.     

Preliminary analysis to estimate the spatial distribution of benefits of P load reduction: Identifying the spatial influence of phosphorus loading from the Maumee River (USA) in western Lake Erie

Since the early 2000s, Lake Erie has been experiencing annual cyanobacterial blooms that often cover large portions of the western basin and even reach into the central basin. These blooms have affected several ecosystem services provided by Lake Erie to surrounding communities (notably drinking water quality). Several modeling efforts have identified the springtime total bioavailable phosphorus (TBP) load as a major driver of maximum cyanobacterial biomass in western Lake Erie, and on this basis, international water management bodies have set a phosphorus (P) reduction goal. This P reduction goal is intended to reduce maximum cyanobacterial biomass, but there has been very limited effort to identify the specific locations within the western basin of Lake Erie that will likely experience the most benefits. Here, we used pixel‐specific linear regression to identify where annual variation in spring TBP loads is most strongly associated with cyanobacterial abundance, as inferred from satellite imagery. Using this approach, we find that annual TBP loads are most strongly associated with cyanobacterial abundance in the central and southern areas of the western basin. At the location of the Toledo water intake, the association between TBP load and cyanobacterial abundance is moderate, and in Maumee Bay (near Toledo, Ohio), the association between TBP and cyanobacterial abundance is no better than a null model. Both of these locations are important for the delivery of specific ecosystem services, but this analysis indicates that P load reductions would not be expected to substantially improve maximum annual cyanobacterial abundance in these locations. These results are preliminary in the sense that only a limited set of models were tested in this analysis, but these results illustrate the importance of identifying whether the spatial distribution of management benefits (in this case P load reduction) matches the spatial distribution of management goals (reducing the effects of cyanobacteria on important ecosystem services).     

The role of the blue mussel Mytilus edulis in the cycling of nutrients in the Oosterschelde estuary (The Netherlands)

The fluxes of particulate and dissolved material between bivalve beds and the water column in the Oosterschelde estuary have been measured in situ with a Benthic Ecosystem Tunnel. On mussel beds uptake of POC, PON and POP was observed. POC and PON fluxes showed a significant positive correlation, and the average C:N ratio of the fluxes was 9.4. There was a high release of phosphate, nitrate, ammonium and silicate from the mussel bed into the water column. The effluxes of dissolved inorganic nitrogen and phosphate showed a significant correlation, with an average N:P ratio of 16.5. A comparison of the in situ measurements with individual nutrient excretion rates showed that excretion by the mussels contributed 31–85% to the total phosphate flux from the mussel bed. Ammonium excretion by the mussels accounted for 17–94% of the ammonium flux from the mussel bed. The mussels did not excrete silicate or nitrate. Mineralization of biodeposition on the mussel bed was probably the main source of the regenerated nutrients.From the in situ observations net budgets of N, P and Si for the mussel bed were calculated. A comparison between the uptake of particulate organic N and the release of dissolved inorganic N (ammonium + nitrate) showed that little N is retained by the mussel bed, and suggested that denitrification is a minor process in the mussel bed sediment. On average, only 2/3 of the particulate organic P, taken up by the mussel bed, was recycled as phosphate. A net Si uptake was observed during phytoplankton blooms, and a net release dominated during autumn. It is concluded that mussel beds increase the mineralization rate of phytoplankton and affect nutrient ratios in the water column. A comparison of N regeneration by mussels in the central part of the Oosterschelde estuary with model estimates of total N remineralization showed that mussels play a major role in the recycling of nitrogen.     

Suppression of microzooplankton by zebra mussels: importance of mussel size

1. The zebra mussel (Dreissena polymorpha) is amongst the most recent species to invade the Great Lakes. We explored the suppressive capabilities of mussels 6–22-mm in size on Lake St Clair microzooplankton (< 240)μm) in laboratory experiments. 2. Absolute suppression of rotifers and Dreissena veliger larvae was proportional to mussel shell length for individuals larger than 10 mm; larger zooplankton, mainly copepod nauplii and Cladocera, were not affected. Mussel clearance rates on rotifers generally exceeded those on veligers, although rates for both increased with increasing mussel size. Rotifer-based clearance rates of large (22 mm) mussels approached published values for phytoplankton food. 3. Most zooplankton taxa, particularly rotifers, declined significantly in western Lake Erie during the late 1980s concomitant with the establishment and population growth of zebra mussels in the basin. Densities of some taxa subsequently increased, although rotifers and copepod nauplii densities remained suppressed through 1993. Available evidence indicates that direct suppression by Dreissena coupled with food limitation provides the most parsimonious explanation for these patterns.     

Seston quality drives feeding,stoichiometry and excretion of zebra mussels

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Lake morphometry determines Dreissena invasion dynamics

Predicting the ecosystem effects of invasive species and the best control strategies requires understanding population dynamics and population regulation. Invasive bivalves zebra and quagga mussels (Dreissena spp.) are considered the most aggressive invaders in freshwaters and have become major drivers of ecosystem processes in the Laurentian Great Lakes. Combining all lake-wide studies of Dreissena spp. conducted in the Great Lakes, we found that invasion dynamics are largely governed by lake morphometry. Where both species are present, quagga mussels generally become dominant in 8–13 years. Thereafter, zebra mussels remain common in shallow lakes and embayments and lake-wide Dreissena density may remain similar, while in deep lakes quagga led to a near-complete displacement of zebra mussels and an ensuing dramatic increase in overall dreissenid density. In deep lakes, overall Dreissena biomass peaked later and achieved?~?threefold higher levels than in shallow lakes. Comparison with 21 waterbodies in North America and Europe colonized by both dreissenids confirmed that patterns of invasion dynamics found in the Great Lakes are very consistent with other waterbodies, and thus can be generalized to other lakes. Our biophysical model predicted that the long-term reduction in primary producers by mussel grazing may be fourfold less in deep compared to shallow lakes due to thermal stratification and a smaller proportion of the epilimnion in contact with the bottom. While this impact remains greatest in shallow areas, we show that when lakes are vertically well-mixed, dreissenid grazing impact may be greatest offshore, revealing a potentially strong offshore carbon and phosphorus sink.

     

Regulation of phosphate uptake reveals cyanobacterial bloom resilience to shifting N:P ratios

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Predator‐induced morphological defences in two invasive dreissenid mussels: implications for species replacement

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