Bioprocessing of polluted suspended matter from the water column by the zebra mussel (Dreissena polymorpha Pallas)

Measurements of pseudofaeces production of Dreissena polymorpha were carried out with the aim of developing a biological filter at the freshwater inlet of Lake Volkerak-Zoommeer, the Netherlands. Bioprocessing of polluted suspended matter by suspended cultures of D. polymorpha occurs by filtration and sedimentation of the suspended matter as pseudofaeces. The measurements were conducted under semi-natural conditions.Pseudofaeces production was mainly determined by the dry matter content of the water; the relation is linear. Temperature was of much less importance. This agrees with earlier investigations of the filtration rate of D. polymorpha. Even at the lowest temperature measured during the experiments (6.4 °C) no large decrease in activity was observed. The relation of pseudofaeces production with shell length was sigmoid in shape, in accordance with measurements of the filtration rate.The pseudofaeces produced was slightly more polluted than suspended matter, partly due to a finer grainsize. D. polymorpha from Lake IJsselmeer exposed for 217 days at the intended location of the filter showed bioaccumulation of toxicants, especially organic pollutants and Polycyclic Aromatic Hydrocarbons (up to 10-fold accumulation). The required number of D. polymorpha in the biological filter to treat the waterflow of 14 m³ s^–1 entering Lake Volkerak-Zoommeer is 1.24 * 10⁹. The purification efficiency of the filter, the reduction of the amount of toxicants, partly depends on the binding properties of the toxicants and is highest for those strongly bound to suspended matter.     

Estimating the effective clearance rate and refiltration by zebra mussels, Dreissena polymorpha, in a stratified reservoir

1. The grazing impact of zebra mussels, Dreissena polymorpha Pallas, is often evaluated by applying the individual filtration rate measured in the laboratory to the field abundance and then by comparing the total volume of water filtered with the whole lake volume. Since this approach overlooks refiltration, it overestimates the grazing impact of zebra mussels. To deal with this problem, the present authors developed an in situ method for collecting faeces and pseudofaeces to measure the actual volume of water that is cleared of suspended particles by Dreissena in a unit time under a given set of environmental conditions. This is termed the effective clearance rate (ECR). 2. The experiment was conducted in Hargus Lake, OH, U.S.A., a small thermally stratified reservoir, to test the effects of spatial aggregation, mussel density and the concentration of particulate inorganic matter (PIM) on the effective clearance rate of Dreissena. 3. Over 40 measurements, the ECR values ranged from 15.3 to 68.6 mL ind^??1 h^??1. Much of the variation can be explained by colony form, mussel density and seston concentration. The effects of these variables were all statistically significant. The average ECR for isolated individuals was higher than that for those in clumps (40.4 versus 32.8 mL ind^??1 h^??1), which is attributed to increased refiltration in the cores of the clumps. The ECR decreased with increased zebra mussel density because of intensified competition for food particles within the group. The ECR increased with increased PIM concentration in the lake water, which may be interpreted as a result of enhanced water mixing which ultimately caused increases in both sediment resuspension and particle delivery to the mussels. 4. Taking the filtration rates for a 20-mm mussel to be between 116 and 234 mL ind^??1 h^??1, based on data from the literature, the clumped mussels under the present experimental conditions would have a refiltration ratio between 3.4 and 6.9. 5. The present authors developed an areal clearance model which predicts that seston removal by the Dreissena population is limited by the particle delivery from the ambient water to the mussel bed and will reach a maximum value beyond which no further increase will occur with increased population density. 6. It is concluded that the direct grazing impact of zebra mussel on phytoplankton in thermally stratified lakes is much less effective than predicted from simple filtration rate estimation.     

Distribution and aspects of population dynamics of the zebra mussel,Dreissena polymorpha (Pallas, 1771), in the lake IJsselmeer area (The Netherlands)

Summary The distribution, settling and growth of the zebra mussel, Dreissena polymorpha Pallas, in Lake IJsselmeer and Lake Markermeer in The Netherlands were studied from 1980 to 1985. In these lakes D. polymorpha is the most important food source for wintering diving ducks. The study was part of an investigation into the carrying capacity of the lakes for these birds.     

Indigenous microflora and opportunistic pathogens of the freshwater zebra mussel, Dreissena polymorpha

Freshwater fouling invertebrate zebra mussels (Dreissena polymorpha) harbor a diverse population of microorganisms in the Great Lakes of North America. Among the indigenous microorganisms, selective species are opportunistic pathogens to zebra mussels. Pathogenicity to zebra mussels by opportunistic bacteria isolated from the mussels was investigated in this study. Among the more than 30 bacteria isolated from temperature-stressed mussels, Aeromonas media, A. veronii, A. salmonicida subsp. salmonicida, and Shewanella putrefaciens are virulent pathogens to juvenile zebra mussels. Inoculation of a bacterial concentration of A. media, A. salmonicida subsp. salmonicida and S. putrefaciens at 10⁷ cells per zebra mussel resulted in 100% mortality within 5 days, and only 64.9% for A. veronii. In contrast, mortality was less than 12.3% following inoculation of a sterile phosphate buffer solution as a control. In addition, mortality was dependent on the size of the pathogen population used in inoculation and the incubation temperature, indicating the close relationship between the bacterial population and subsequent death. On the mussel tissue, a dense microbial population was evident from the moribund mussels viewed with Scanning Electron Microscope (SEM). Opportunistic bacteria invaded and destroyed the D. polymorpha tissue after 7 days of incubation when the bacterial inoculation was larger than 10⁵ per zebra mussel. Our results suggest that mussels are reservoirs of opportunistic pathogenic microorganisms to aquatic organisms and humans and a better understanding of the microbial ecology of the mussels will provide insights to the possible health hazards from these microorganisms.     

Long-term changes in a population of an invasive bivalve and its effects

Although the ecological and economic effects of non-native species probably often change through time, few studies have documented such effects. The zebra mussel (Dreissena polymorpha) is an important invader that has had large ecological and economic effects on the ecosystems it has invaded in North America and western Europe. Our 20-year study of the Hudson River, New York, showed that the characteristics of a zebra mussel population and its effects on other benthic animals both changed substantially through time. Over the period of study, annual survivorship of adult zebra mussels fell >100-fold, which caused the aggregate filtration rate of the population to fall by 82%. Population size and body size of zebra mussels may also have fallen. In the early years of the invasion, densities of nearly all benthic animals in deepwater sites fell steeply (by 80–99%). After about 8 years of decline, these populations began to recover, and are approaching pre-invasion densities. The littoral zoobenthos showed neither the initial decline nor the subsequent recovery. Although the mechanisms behind these changes are not fully clear, our study shows that the effects of an invader may change considerably over time.     

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.     

Strong impact of wintering waterbirds on zebra mussel (Dreissena polymorpha) populations at Lake Constance, Germany

1. Since zebra mussel invaded Lake Constance in the 1960s the number of wintering waterbirds increased fourfold. We studied the impact of predation by waterbirds (tufted duck Aythya fuligula, pochard Aythya ferina and coot Fulica atra) on the population of Dreissena polymorpha in winter 2001/2002. These three species, with monthly peak numbers of approximately 230 000 individuals, currently comprise up to 80% of the waterbird population wintering at Lake Constance. 2. Four different study sites and four depths, that represent typical and characteristic habitats of mussels in Upper Lake Constance, were chosen. 3. Zebra mussels were sampled before, during and after predation by waterbirds. Their biomass in shallow areas decreased by >90%; the biomass reduction in deeper areas was highly variable and dependent on the substratum. With one exception, no changes could be detected at the greatest depth (11 m). 4. Concurrent exclosure studies revealed that the decrease in zebra mussels was caused by waterbird predation. A GIS‐based approximation revealed that in an area of 1 km² a total of approximately 750 t mussel fresh mass was removed by birds, which is equivalent to 1390 g mussels per bird per day. 5. Wintering waterbirds have a strong structural impact on the littoral community of Lake Constance and could be the key predator of zebra mussels.     

Effects of increasing temperatures on population dynamics of the zebra mussel <Emphasis Type="Italic">Dreissena polymorpha</Emphasis>: implications from an individual-based model

Zebra mussels (Dreissena polymorpha, Pallas, 1771) have had unprecedented success in colonizing European and North American waters under strongly differing temperature regimes. Thus, the mussel is an excellent model of a species which is able to cope with increasing water temperatures expected under global change. We study three principle scenarios for successful survival of the mussel under rising temperatures: (1) no adaptation to future thermal conditions is needed, existing performance is great enough; (2) a shift (adaptation) towards higher temperatures is required; or (3) a broadening of the range of tolerated temperatures (adaptation) is needed. We developed a stochastic individual-based model which describes the demographic growth of D. polymorpha to determine which of the alternative scenarios might enable future survival. It is a day-degree model which is determined by ambient water temperature. Daily temperatures are generated based on long-term data of the River Rhine. Predictions under temperature conditions as recently observed for this river that are made for the phenology of reproduction, the age distribution and the shell length distribution conform with field observations. Our simulations show that temporal patterns in the life cycle of the mussel will be altered under rising temperatures. In all scenarios spawning started earlier in the year and the total reproductive output of a population was dominated by the events later in the spawning period. For maximum temperatures between 20 and 26°C no thermal adaptation of the mussel is required. No extinctions and stable age distributions over generations were observed in scenario 2 for all maximum temperatures studied. In contrast, no population with a fixed range of tolerated temperatures survived in scenario 3 with high maximum temperatures (28, 30, 32°C). Age distributions showed an excess of 0+ individuals which resulted in an extinction of the population for several thermal ranges investigated. Priority programme of the German Research Foundation—contribution 14.     

Effect of filtering activity of Dreissena polymorpha (Pall.) on the nutrient budget of the littoral of Lake Mikołajskie

The effect of filtering activity of D. polymorpha on nutrient dynamics in Lake Mikoajskie depended mostly on population density: D. polymorpha was important in N and P cycling in periods when its population density was medium or high. The amounts of N and P accumulated in mussel populations at medium density may be similar to those in emergent and submerged macrophytes. However, mussels remove nutrients from cycling matter for a much longer time than do macrophytes. The amounts of nutrients accumulated in a mussel population are several times lower than the quantities which flow through it.     

Changes in the distribution and abundance of Dreissena polymorpha within lakes through time

Dreissena polymorpha population densities and biomass were followed in three Belarusian lakes with different trophic status over a 12-year period subsequent to initial colonization. In all three lakes zebra mussel population densities did not change once they reached a maximum. Application of the Ramcharan et al. [1992. Canadian Journal of Fisheries and Aquatic Sciences 49: 2611–2620] model for predicting population dynamics of zebra mussels was accurate for two of the three lakes studied. Population density appears to depend on the time since initial colonization, relative abundance of substrate available for colonization, lake morphometry and trophic type. Zebra mussel distribution within lakes was highly patchy, but the degree of dispersion decreased over time after initial colonization, which may be a result of saturation of suitable substrates by zebra mussels as populations increase and reach carrying capacity. In lakes where submerged macrophytes are the dominant substrate for zebra mussel attachment, populations may be less stable than in lakes with a variety of substrates, which will have a more balanced age distribution, and be less impacted by year to year variation in recruitment. Dreissena polymorpha usually reach maximum population density 7–12 years after initial introduction. However, the timing of initial introduction is often very difficult to determine. Both European and North American data suggest that zebra mussels reach maximum density in about 2–3 years after populations are large enough to be detected.     

Filtering impacts of larval and sessile zebra mussels (Dreissena polymorpha) in western Lake Erie

Summary We assessed the feeding biology of veliger larvae of the introduced zebra mussel (Dreissena polymorpha Pallas) in laboratory experiments using inert microspheres as food analogues. Mean clearance rate on 2.87-m beads ranged between 247 and 420 L veliger^–1 day^–1. Clearance rate was unrelated to bead concentration up to 100 beads L^–1, but was positively correlated with veliger shell length. Clearance rates of Dreissena veligers are within the range of those reported for marine bivalve veligers of similar size and for herbivorous Great Lakes microzooplankton, but are orders of magnitude lower than those of settled, conspecific adults. The impact of settled zebra mussel grazing activities on phytoplankton stocks may be up to 1162 times greater than that exerted by veliger populations in western Lake Erie. Based on 1990 size-frequency distributions and associated literature-derived clearance rates, reef-associated Dreissena populations in western Lake Erie (mean depth 7 m) possess a tremendous potential to filter the water column (up to 132 m³ m^–2 day^–1) and redirect energy from pelagic to benthic foodwebs. Preliminary analyses indicate that chlorophyll a concentration is strongly depleted (<1 g L^–1) above Dreissena beds in western Lake Erie.     

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.     

Invasive zebra mussel (Dreissena polymorpha) threatens an exceptionally large population of the depressed river mussel (Pseudanodonta complanata) in a postglacial lake

1. Freshwater mussels are in decline worldwide, with the depressed river mussel Pseudanodonta complanata being one of the rarest and most endangered species in Europe. Invasive mussels are suspected to be an important factor of decline, but there is little information on their interaction with native species.
2. This study analyzed densities, depth distribution, and individual sizes and weights in one of the largest known populations of P. complanata in Europe in relation to the co‐occurring invasive zebra mussel Dreissena polymorpha and other mussel species, using a systematic transect analysis.
3. Pseudanodonta complanata was the dominant unionid species in Lake Siecino reaching densities of up to 26 ind/m², with half of the specimens found at a water depth of 2.0–4.0 m. Densities were highest on sandy substrates in areas of underwater currents. In contrast, 67% of native Unio tumidus were found at depths < 1 m, indicating different habitat preference.
4. In the study area, 91% of P. complanata, 92% of U. tumidus, and all Anodonta individuals were fouled by D. polymorpha. The dreissenid:unionid mass ratio (mean ± SD; maximum) was 0.43 ± 0.56; 4.22 and 0.86 ± 1.87; 8.76 in P. complanata and U. tumidus, respectively. Pseudanodonta complanata fouled with D. polymorpha were impaired in their anchoring capability and had shell deformations potentially affecting shell closing and filtration activity. Fouling intensity was negatively correlated with unionid density, potentially leading to accelerated population declines.
5. The observed adverse effects of invasive zebra mussels on the depressed river mussel and the difficulties in eradicating established populations of invasive mussels suggest that D. polymorpha should be considered a serious threat to P. complanata. Therefore, the further spread of zebra mussels into habitats with native unionids needs to be avoided by all means.

     

Quantitative trends of zebra mussels in Lake Balaton (Hungary) in 2003–2005 at different water levels

During the extremely dry period between 2000 and 2003, the water level of Lake Balaton decreased by 82 cm and 80% of the stony littoral, an important habitat for the zebra mussel (Dreissena polymorpha), became dry. A recovery period started in 2004 due to intense precipitation, which increased water levels in the lake. Seasonal and spatial variations of the relative abundance, population density, population structure and biomass of the zebra mussel and the relative abundance of the amphipod Chelicorophium curvispinum were monitored in the period of 2003–2005 at four different shoreline sections and in two different portions (on the bottom and near the surface portion of the rip-rap) of Lake Balaton. Along with these studies, a quantitative survey of mussel larvae found in the plankton and of the abundance of mussel feeding diving ducks were made. As a consequence of the water level fall, on the dried part of the stony littoral, numerous zebra mussel druses perished. Following the dry period in early 2004, the relative abundance of the mussel on the bottom stones was smaller than in 2003 and the bottom community was dominated by C. curvispinum. By the end of 2004 and during 2005, the water level returned to normal and the surfaces of the reinundated stones were conducive to the successful colonization of zebra mussels. Hence, they returned as the dominant fauna in 2005. The stones near the surface might provide a new substrate for the recruitment of zebra mussels, probably offering more suitable substrata for the settlement in 2005 than in 2003. Therefore, the new substrata available in 2005 may have encouraged better and more rapid zebra mussel colonization than before. Zebra mussels may be better competitors for new space than C. curvispinum. A minor change of water-level fluctuation in 2005 and the reduction in population size of the mussel feeding waterfowl could have contributed to the intensive spread of zebra mussel by 2005.     

Size‐structured vulnerability of the colonial cyanobacterium,Microcystis aeruginosa,to grazing by zebra mussels (Dreissena polymorpha)

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Gill Structure in Zebra Mussels: Bacterial-Sized Particle Filtration

SYNOPSIS. The filtration mechanics of the gill of the zebramussel, Dreissena polymorpha, allow this organism to captureparticles less than 1 µm. The organization of gill cirriand the architecture of the cirri appear to be important inproviding the organism with the ability to filter small particles.Bacteria may provide a useful nutrient source for these animalsas bacterial proteins can be digested and assimilated into musselproteins. Laboratory experiments indicate that D. polymorphais capable of filtering and assimilating a wide range of bacteriaranging in size from 1–4 µm. Unionid species appearto be at least an order of magnitude less efficient at filteringbacteria than D. polymorpha. Because of its relatively smallergill size, C. fluminea also filters bacteria less efficientlythan D. polymorpha. We suggest that bacterial utilization byfreshwater mussel species has important population and evolutionaryimplications.     

Biology of the exotic zebra mussel,Dreissena polymorpha,in relation to native bivalves and its potential impact in Lake St. Clair

The zebra mussel, Dreissena polymorpha, is a new exotic species that was introduced into the Great Lakes as early as the fall of 1985. It differs markedly from native species of bivalves in its: (i) shell form; (ii) mode of life; (iii) reproductive potential; (iv) larval life cycle; (v) population dynamics; (vi) distribution, (vii) dispersal mechanisms; (viii) physiology; (ix) potential impact on the ecosystem; and (x) impact on society and the economy. In body form, it has an anterior umbone, a flat ventral surface with permanent aperature for the byssal apparatus and a shape that together make the animal well adapted for life on a hard surface. The shell has a zebra-stripe pattern, a heteromyarian muscle condition and lacks hinge teeth which make it easily identifiable from native bivalves. The zebra mussel is strongly byssate and has an epifaunal mode of life not seen in native bivalves. The species is dioecious and has external fertilization, the eggs developing into pelagic veligers which remains planktonic for approximately 4 weeks. Gametogenesis begins in late winter to early spring, veligers appear in the water column in late May to early June and disappear in mid to late October in Lake St. Clair. Adults live for about 2 years and have very rapid growth rates. Maximum shell lengths average 2.3 to 2.5 cm. Standing crops as high as 200 000 m^-2 are present in the 1-m depths of the Ontario shores. Infestations may be interfering with the normal metabolism of native unionid clams and there is potential of the unionid clam populations being reduced or even eliminated from Lake St. Clair.     

Susceptibility of larval dragonflies to zebra mussel colonization and its effect on larval movement and survivorship

Colonization by the zebra mussel, Dreissena polymorpha, was quantified for five dragonfly species that differed in size and larval habits in a Michigan lake. Both larger size and a non-burrowing habit independently increased susceptibility to colonization. In 2005, over 50% of the final instars of the sprawlers Didymops transversa and Hagenius brevistylus were colonized, as well as younger instars. Rarely colonized were Progomphus obscurus and Dromogomphus spinosus, whose larvae burrow under sand, and the sprawler Epitheca princeps, whose final instars were lightly covered with sand. Hagenius larvae that had been preyed upon carried more mussels than those dying of other causes. More generally, mussel attachment decreased the probability that sprawlers left the water to emerge, the distance that some species traveled before emerging, and the ability of an overturned sprawler to right itself. On average, final instars of Didymops and Hagenius remaining in the water carried three times as many mussels as individuals known to emerge. Compared to uncolonized individuals, Epitheca and Progomphus with mussels emerged closer to the water line. Among colonized Didymops, the distance traveled on land before emerging decreased with increasing mussel load. Of the colonized Didymops that could right themselves, righting time increased with mussel load. Because the two common species of sprawlers were disproportionately colonized, and mussel attachment decreased their chances of emerging, our results suggest that D. polymorpha has the potential to affect the community structure of this guild of aquatic and terrestrial predators. Handling editor: R. Bailey     

Invasive mussels induce community changes by increasing habitat complexity

Habitat complexity is among the most important factors affecting the diversity, structure, and density of natural communities. The invasive byssate bivalves zebra mussel (Dreissena polymorpha (Pallas, 1771)) and golden mussel (Limnoperna fortunei (Dunker, 1857)) are sessile suspension feeders that form aggregations (druses), physically changing sediments and increasing habitat complexity, and providing shelter and food for other benthic organisms. In this study, we explored the impact of the change in habitat complexity on benthic community created by druses of L. fortunei and D. polymorpha, formed on various sediments. D. polymorpha was studied in Europe (Naroch Lake, Belarus) and in North America (Glen Lake and Lower Nashotah Lake, USA), and L. fortunei was studied in South America (Río Tercero Reservoir, Argentina). Druses of D. polymorpha or L. fortunei and samples of bare nearby sediment (without druses of exotic mussels) were collected at each sampling site. We found significant changes in species richness, density, biomass, taxonomic, and trophic structure of communities formed in druses compared to the nearby bare sediments. Community taxonomic richness increased threefold, and density increased sevenfold with increasing complexity of habitat from sand to druse. The feeding functional group approach indicated that the impact of increased complexity was reinforced by an increase in food supply in D. polymorpha and L. fortunei druses. Along with increasing species richness and densities, byssate bivalves homogenized benthic communities.     

The annual reproductive cycle of the freshwater mussel Dreissena polymorpha Pallas in lakes

Summary The annual development of the gonads of Dreissena polymorpha was studied at three sampling sites in two lakes over 3 and 1 1/2 years, respectively. A resting stage occurred after the last spawning in summer/autumn. Oogenesis (accompanied by multiplying segmentation of the oogonia and early growth processes of its oocytes) restarted in specimens at least 1 year old at low temperatures (below 10° C) during winter and early spring. At one location (Fühlinger See) the onset of the spawning season was correlated with an increase of water temperatures above 12° C. At 2 m depth, two main spawning periods in May and August were normally recognized, the first at temperatures of 12–16° C, the second at 16–21° C. It was clearly demonstrated for the first time in Dreissena polymorpha that the oocytes became mature in successive cohorts within one gonad. A female mussel may spawn several times during the reproductive season. At 9 m depth, the onset of spawning also started at about 12° C; this occurred in late summer, with two spawning periods within 1 month at a temperature range of 12–16° C. At another location (Heider Bergsee) the size of the gonads and the oocytes was reduced during April of both years studied, when food supply was low simultaneously with rapidly rising water temperatures in this shallow lake. There was no spawning period during spring. The major spawning period was delayed until July (temperatures 19–22°C). This shows (1) the synchronizing influence of low winter temperatures on the annual reproductive cycle and (2) a temperature threshold of at least 12° C for the start of the spawning processes. The results are discussed with regard to the geographical limits of further spread of Dreissena polymorpha.