Coping with warmer, large rivers: a field experiment on potential range expansion of northern quagga mussels (Dreissena bugensis)

SUMMARY 1. Zebra mussels ( Dreissena polymorpha ) have established a much greater range in North America and Europe than quagga mussels ( D. bugensis ), which occupy a very similar niche.
2. We hypothesised that quaggas are physiologically capable of sustaining populations in warmer rivers currently occupied only by zebra mussels and that unidentified, non-physiological factors account for their more limited distribution.
3. Growth and survival of individually tagged mussels (976 D. bugensis from Lake Erie; 2625 D. polymorpha from Lake Erie and the Ohio River) were recorded monthly for up to 15 months in an outdoor stream mesocosm receiving unfiltered water from the Ohio River.
4. Extreme temperatures stressed both species; but in contrast to several previous laboratory studies, quaggas survived high temperatures better than zebra mussels. We suspect this was the result of species-specific differences in their ability to obtain, assimilate and/or catabolise food at high, sublethal temperatures.
5. A unimodal growth pattern was observed in both species, with the highest growth rates from late spring to early autumn.
6. Our survival and growth data suggest that quaggas are not physiologically limited from expanding southward.
7. While lacking definitive proof that dreissenid populations in rivers are ecologically sustainable without upstream lentic ecosystems and/or unintended human intervention, we suggest that complex river currents and upstream retentive and highly productive slackwater habitats in rivers may help sustain downstream populations of these meroplanktonic, dreissenid mussels.     

Aspects of ecology and conservation of sympatric,prosobranch snails in a large river

We examined factors influencing distribution of prosobranch snails with field surveys, lab substrate-choice and movement experiments, and outdoor artificial stream experiments manipulating current, substrate and temperature. Restriction of Lithasia obovata to shallow, isolated rock patches and the more continuous distribution of Pleurocera canaliculatum on diverse substrates (shallow to deep water) seem related to food availability, predator vulnerability, wave resistance and dispersal abilities. Shallow, rocky habitats favored by the relatively fragile-shelled Lithasia maximize the more nutritious, epilithic microalgal food while minimizing wave displacement (firmer substrate) and exposure to molluscivorous fish inhabiting deeper waters. The broader distribution of the heavily-armored Pleurocera is attributed mostly to greater dispersal abilities (e.g. via deep water, gravel pathways), prevalence in more substrate types, and resistance to fish predators, but their relatively small foot may account for low densities in very shallow, wave-swept habitats. Lithasia is vulnerable because of its restriction to isolated, shallow rocky habitats, inability to reach deeper gravel dispersal pathways, and greater susceptibility to cold temperatures (slowing colonization of other habitats). Impoundments increase this threat by blocking inter-reach dispersal and hindering intra-reach dispersal through siltation. Pleurocera's survival is threatened by biofouling from zebra mussels which are more prevalent in depths inhabited by this species.     

Relative Distributions of Dreissena bugensis and Dreissena polymorpha in the Lower Don River System,Russia

A survey was conducted in the lower Don River system in Russia to confirm the presence of Dreissena bugensis, and to compare its distribution relative to that of Dreissena polymorpha. In 1999 and 2001–2002, dreissenid mussels were collected at 15 sites in the main river, in connecting reservoirs, and in a major tributary, the Manych River. Collections were made near stations where long‐term monitoring data on total mineral (sum of principal ions) and calcium content were available. Both dreissenid species were found at all sites, with D. bugensis comprising 4–75% of all dreissenids at individual sites. D. bugensis was relatively more abundant than D. polymorpha in the Manych River where total mineral and calcium content was significantly higher than in the Don River, suggesting the two species may have different calcium requirements. Examination of archived samples indicated that D. bugensis was present in the Don River system as early as the 1980s, presenting the unresolved enigma of why D. bugensis has not displaced D. polymorpha as the dominant species as typically found over shorter time periods in other water bodies. (© 2004 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

Impacts of Dreissena invasions on benthic macroinvertebrate communities: a meta-analysis

Dreissenid mussels (the zebra mussel Dreissena polymorpha and the quagga mussel Dreissena bugensis ) have invaded lakes and rivers throughout North America and Europe, where they have been linked to dramatic changes in benthic invertebrate community diversity and abundance. Through a meta-analysis of published data from 47 sites, we developed statistical models of Dreissena impact on benthic macroinvertebrates across a broad range of habitats and environmental conditions. The introduction of Dreissena was generally associated with increased benthic macroinvertebrate density and taxonomic richness, and with decreased community evenness (of taxa excluding Dreissena ). However, the strength of these effects varied with sediment particle size across sites. The effects of Dreissena differed among taxonomic and functional groups of macroinvertebrates, with positive effects on the densities of scrapers and predators, particularly leeches (Hirudinea), flatworms (Turbellaria), and mayflies (Ephemeroptera). Gastropod densities increased in the presence of Dreissena , but large-bodied snail taxa tended to decline. Dreissena was associated with declines in the densities sphaeriid clams and other large filter-feeding taxa, as well as burrowing amphipods ( Diporeia spp.), but had strong positive effects on gammarid amphipods. These patterns are robust to variation in the methodology of primary studies. The effects of Dreissena are remarkably concordant with those of ecologically similar species, suggesting universality in the interactions between introduced byssally attached mussels and other macroinvertebrates.     

Patterns of Spread of the Zebra Mussel (Dreissena polymorpha (Pallas)): the Continuing Invasion of Belarussian Lakes

The invasion of the freshwaters of Belarus by the zebra mussel, Dreissena polymorpha (Pallas), began at least 200 years ago by the opening of shipping canals linking the Black Sea and Baltic Sea drainage basins. However, zebra mussels have invaded only 93 (16.8%) of 553 studied lakes; at least 20 of these lakes were invaded within in the past 30 years. Zebra mussels were found disproportionately in lakes that were mesotrophic, larger, and had some commercial fishing. Although larger lakes have more intensive fisheries with larger catches, the intensity of the fishery and average catch did not affect the probability of zebra mussel invasion. Zebra mussels were not found in dystrophic lakes (10% of the lakes studied), probably due to their low pH and calcium content. Zebra mussels became locally extinct in one lake due to anthropogenic eutrophication and pollution. Many ecologically suitable lakes have yet to be invaded, which suggests that natural vectors of overland dispersal, e.g., waterfowl, have been ineffective in Belarus. Thus, future spread of this species will continue to depend on human activities such as commercial fishing.     

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.

     

Effects of Artificial Filamentous Substrate on Zebra Mussel (Dreissena polymorpha) Settlement

Though a great deal of research focuses on the range expansion and presence of adult zebra mussels, there is still a need to understand the processes of larval settlement and how that relates to adult populations. There is evidence that marine bivalves preferentially settle on filamentous substrates such as hydroid colonies and algae; however, similar studies are rare in freshwater systems. We examined the importance of filamentous substrate for the settlement of the zebra mussel (Dreissena polymorpha) larvae by deploying PVC settlement plates with and without polypropylene filaments in the Bark River for a 6-week period. Larval supply was monitored weekly. Our results suggest that artificial filaments facilitated recruitment, primarily by increasing surface area available for attachment. Mussels on artificial filaments were significantly smaller in size than mussels attached to filamentous or control plate surfaces, providing some evidence that mussels may detach from filamentous substrate after initial settlement. This study adds to our general understanding about the role of filamentous substrates in the process of larval settlement and suggests that substrates colonized by filamentous epibionts may face increased risk of fouling by zebra mussels. An erratum to this article is available at .     

Filtering Impacts of an Introduced Bivalve (Dreissena polymorpha) in a Shallow Lake: Application of a Hydrodynamic Model

Nonindigenous species may exert strong effects on ecosystem structure and function. The zebra mussel (Dreissena polymorpha) has been attributed with profound changes in invaded ecosystems across eastern North America. We explored vertical profiles of water flow velocity and chlorophyll a concentration in western Lake Erie, over rocky substrates encrusted with Dreissena, to assess the extent to which mussels influence coupling between benthic and pelagic regions of the lake. Flow velocity was always low at surveyed sites (less than or equal to 2.9 cm s^-1) and declined in direct proximity to the lakebed. Mean chlorophyll a concentration was also low (less than 5μg L^-1) at all sites and depths. Chlorophyll a concentration was positively correlated with distance above lakebed and was lowest (0.3μg L^-1) directly adjacent to the lakebed. Spatial patterns of zooplankton grazers could not explain observed vertical gradients in chlorophyll concentration. Hydrodynamic modeling revealed that filtering effects of Dreissena in a nonstratified, shallow basin depend mainly on upstream chlorophyll concentration, intensity of turbulent diffusion, feeding efficiency of the mussel colony, and the distance downstream from the leading edge of the mussel colony. In contrast to widespread perceptions that molluscs reduce phytoplankton concentration only adjacent to the lakebed, modeling scenarios indicated that depletion occurs throughout the water column. Depletion was, however, inversely proportional to distance above the lakebed. Simulation results are consistent with field-based observations made in shallow water habitats populated by large Dreissena populations in the Great Lakes and elsewhere. Results from this study indicate that zebra mussels strongly enhance coupling between pelagic and benthic regions in shallow lakes. Enhanced coupling between these regions explains, in part, high population densities of Dreissena and of many benthic invertebrates in ecosystems invaded by zebra mussels. Received 14 July 1998; accepted 25 March 1999.     

Zebra mussel (Dreissena polymorpha) seasonal colonization patterns in a sub-tropical floodplain river

Zebra mussel (Dreissena polymorpha) seasonal colonization patterns, growth and habitat preferences were determined in a sub-tropical floodplain river at the southern edge of its distribution in North America during 1995–96 (Atchafalaya River Basin, Louisiana). Zebra mussel movement into subtropical areas represents a major frontier for this species worldwide. The onset of adult zebra mussel colonies occurred when the minimum daily temperature dropped below 31 °C and dissolved oxygen levels rose above 6.5 mg l^-1 in the fall. By mid-winter, mussel populations were established at lateral distances >10 km from the main river channel. Mussel growth occurred throughout the winter with an increase in growth in April and May. Adult mortality occurred during May–August as dissolved oxygen levels declined and minimum daily temperature warmed above 29 °C in the floodplain and 32.5 °C in riverine sites. Limiting factors responsible for the seasonal pattern include temperature and dissolved oxygen tolerances experienced during summer months in the ARB. Summer water conditions apparently preclude establishment of resident zebra mussel populations in the Atchafalaya floodplain. Naturally occurring seasonal patterns in temperature and dissolved oxygen in floodplain rivers may have implications for the expansion of this exotic mollusk in warmwater systems with source colonies restricted to mainstem rivers and seasonal sinks in floodplain regions. This revised version was published online in July 2006 with corrections to the Cover Date.     

Serotonergic mechanisms mediating spawning and oocyte maturation in the zebra mussel,Dreissena polymorpha

Summary

The zebra mussel, Dreissena polymorpha, is a freshwater biofouling bivalve unintentionally introduced in the 1980s into North America from Europe. Oocyte maturation (germinal vesicle breakdown, GVBD) and spawning of the zebra mussel can be triggered with serotonin (5-hydroxytryptamine, 5-HT). In pharmacological experiments to characterize the receptor mediating spawning, the serotonin receptor agonists 8-OH-DPAT, TFMPP, and 1-(1-naphthyl)piperazine were effective at stimulating spawning; whereas, 2-methylserotonin and alpha-methylserotonin had no effect. In experiments with antagonists of serotonin receptors ketanserin and propranolol had no effect; mianserin, NAN-190, and cyproheptadine had partial inhibitory effects; and methiothepin was a very effective antagonist. Metergoline had mixed agonist/antagonist properties. Ergotamine was the most effective activator of spawning in females. Compared to serotonergic receptors in other organisms, the receptors that activate spawning in zebra mussels resemble 5HTlym, 5HTdro2 and human 5HT1Dβ, which are receptors that may act both by inhibiting adenylyl cyclase and by activating phospholipase C. In zebra mussels, 5-HT and 8-OH-DPAT activate GVBD in gonad fragments, a process also initiated by manual dissection of gonad fragments. GVBD can be inhibited by pre-treatment of ovaries with forskolin and theophylline, suggesting an inhibitory role for cyclic AMP. The Ca²⁺ ionophore A23187 can trigger GVBD and polar body formation. Thus, oocyte maturation in zebra mussels may be initiated via serotonergic receptors simultaneously inhibiting adenylyl cyclase and activating Ca²⁺ mechanisms.     

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.     

Modelling the impact of benthic filter-feeders on the composition and biomass of river plankton

SUMMARY 1. The POTAMON model [Everbecq E. et al . (2001) Water Research , 35 , 901] has been used to simulate the effect of benthic bivalves (mainly Dreissena polymorpha ) on the phytoplankton and zooplankton in a lowland Western European river (the Moselle). Here we use a modified version of the POTAMON model with five categories of phytoplankton ( Stephanodiscus , Cyclotella -like, large diatoms, Skeletonema and non-siliceous algae) to model filter-feeding effects of benthic bivalves in the Moselle. Zooplankton has been represented in the model by two categories, Brachionus -like and Keratella -like rotifers.
2. According to density estimates from field surveys (Bachmann V. et al . (1995) Hydroécologie Appliquée , 7 , 185, Bachmann V. & Usseglio-Polatera P. (1999) Hydrobiologia , 410 , 39), zebra mussel density varied among river stretches, and increased through the year to a maximum in summer. Dreissena filtration rates from the literature were used, and mussels have been assumed to feed on different phytoplankton categories (but less on large and filamentous diatoms) as well as on rotifers.
3. The simulations suggest a significant impact of benthic filter-feeders on potamoplankton and water quality in those stretches where the mussels are abundant, their impact being maximal in summer. Consequently, different plankton groups were not affected to the same extent, depending on their period of development and on indirect effects, such as predation by mussels on herbivorous zooplankton.
4. A daily carbon balance for a typical summer shows the effect of benthic filter-feeders on planktonic and benthic processes: the flux of organic matter to the bottom is greatly enhanced at high mussel density; conversely, production and breakdown of organic carbon in the water column are reduced. Mussel removal would drive the carbon balance of the river toward autotrophy only in the downstream stretches.     

Connectivity and complexity of floodplain habitats govern zooplankton dynamics in a large temperate river system

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Northern map turtles (Graptemys geographica) derive energy from the pelagic pathway through predation on zebra mussels (Dreissena polymorpha)

1. Zebra mussels ( Dreissena polymorpha ) derive their energy from the pelagic energy pathway by filtering plankton. Because zebra mussels occur in high densities in littoral habitats, they potentially constitute an important trophic link between littoral consumers and pelagic energy sources. Northern map turtles ( Graptemys geographica ) are widespread in North America and consume zebra mussels.
2. We used stable isotopes analyses to quantify the flow of energy from the pelagic pathway to northern map turtles and to infer the contribution of zebra mussels to map turtle biomass. We then built a bioenergetic model to estimate the annual intake of zebra mussels by northern map turtles in Lake Opinicon, Ontario, Canada.
3. Stable isotopes analyses indicated that zebra mussels constitute between 0% and 14% of the diet of males and between 4% and 36% of the diet of females. Assuming that zebra mussels account for all of the pelagic contribution, we estimated that map turtles consume 3200 kg of zebra mussels annually. Because female map turtles are much larger than males and consume more zebra mussels, they are responsible for 95% of the zebra mussel biomass ingested annually.
4. The pelagic pathway supports an important part of the standing crop biomass of map turtles in Lake Opinicon. We highlight the importance of freshwater turtles in lake ecosystems. Unravelling the trophic interactions mediated by freshwater turtles will lead to a more integrated picture of lake ecosystems.     

Flow rate and vertical position influence ingestion rates of colonial zebra mussels (Dreissena polymorpha)

1. Zebra mussels aggregate to form dense colonies where, depending on the flow rate, individuals in different vertical locations within the colony may experience restricted food availability. 2. Using ³²P‐labelled Chlamydomonas angulosa, we found ingestion rates of individual mussels located at the surface to exceed those in the bottom of a 6 cm thick colony by up to 75%. 3. Higher velocities (10 and 20 cm s^?1) increased algal delivery to the colony's middle layer (2–4 cm depth), subsequently increasing ingestion rates to equal those in the surface layer, while increasing ingestion only for the smallest mussels in the bottom (4–6 cm). 4. At all vertical locations within the colonies, smaller mussels showed higher ingestion rates per unit mass than larger mussels, particularly at higher flow rates.     

Bioaccumulation and Partitioning of Cadmium within the Freshwater Mussel Dreissena polymorpha Pallas

Kinetics of uptake, partitioning and elimination of cadmium were investigated in experimental studies with the freshwater mussel, Dreissena polymorpha. The radioactive cadmium isotopes ¹⁰⁹Cd and ¹¹⁵Cd were used as tracers. Shells, soft parts and body fluid of the mussel exhibited considerable differences in accumulation and elimination. Accumulation factors up to more than 70,000 were calculated for the periostracum, whereas accumulation factors for the whole mussels ranging up to 3,000 were calculated. The shells bound a great deal of cadmium, but only loosely, and the metal could be readily eliminated after transfer to uncontaminated water. In contrast, no significant amounts of the cadmium incorporated in the soft parts were eliminated. The results indicate that the major portion of cadmium in the soft parts is strongly bound and cannot be eliminated by exchange processes.     

Impact of Bythotrephes longimanus on zooplankton assemblages of Harp Lake, Canada: an assessment based on predator consumption and prey production

1. Following the 1993 invasion of Harp Lake by Bythotrephes longimanus a number of small-bodied zooplankton declined dramatically compared to pre-invasion densities, and some larger species increased. 2. To test whether these changes were caused by Bythotrephes, we measured its consumption of zooplankton in 1995 and compared this to production by the prey species with which it overlapped spatially and temporally. 3. On a seasonal basis Bythotrephes consumption was 199 mg dry mass (DM) m⁻², or 25% of zooplankton production which was 783 mg DW m⁻². However, for some species, such as the small copepod Tropocyclops extensus , consumption greatly exceeded production—this was one of the species noted to decline in Harp Lake following the appearance of Bythotrephes . By contrast, for the larger cladocerans Daphnia galeata mendotae and Holopedium gibberum , consumption was much less than production—these species were observed to increase following the invasion. 4. Our results thus support the hypothesis that zooplankton changes in Harp Lake were caused by Bythotrephes . We speculate that lower quality prey remaining in Harp Lake may lead to reduced densities of Bythotrephes , or impose strong selective forces that lead to new adaptations by this predator.     

Variation in growth rates of the zebra mussel, Dreissena polymorpha, within Lake Wawasee

1. Field experiments conducted in Lake Wawasee in 1995 and 1996 measured the response of shell growth of Dreissena polymorpha to environmental gradients.
2. Shell growth decreased with initial shell length in four mussel size classes ranging between 8 and 22 mm, and decreased with depth, with mussels in shallow water (<4 m) having growth rates nearly twice those of mussels in deeper water (4–7 m).
3. Growth occurred early in the spring–summer period (May–June) with relatively little shell added later in the summer (July–September), and varied significantly among sites within Lake Wawasee, but not between the 2 years of this study.
4. Rank order of sites was consistent for both years implying that environmental conditions responsible for variation in shell growth were stable within Lake Wawasee.
5. Cage design did not have a significant effect on mussel shell growth nor did the distance of growth cages above the bottom (0.5–0.75 m above the bottom versus directly on the bottom).
6. This study demonstrates the sensitivity of adult mussel growth to subtle variation in environmental conditions occurring within and among lakes, with potential consequences for mussel population dynamics and community structure and function.     

Vertical, lateral and longitudinal movement of zooplankton in a large river

1. The spatial distribution and movement patterns of zooplankton in large rivers are little known compared with those in lake environments. We conducted a series of studies in the Ohio River (U.S.A.) during the low flow period to assess diel vertical (DVM), longitudinal and lateral movement of crustacean zooplankton. 2. The dominant large zooplankter, the copepod Eurytemora affinis, showed a consistent vertical migration pattern of daytime ascent and night‐time descent during all sampling periods – the reverse of the most common migratory pattern of zooplankton in lakes. The cladoceran Bosmina migrated in a similar way in two of the three sampling periods. Surveys taken longitudinally in the river showed similar trends for both taxa. 3. During the lateral surveys, E. affinis was significantly more abundant in the shallow littoral zone during the night than in the daytime. The combination of vertical and lateral movement patterns along with the diel distribution of zooplanktivorous fish suggest that these movements are a predator‐avoidance mechanism. 4. Sampling programmes in large rivers should consider that larger zooplankton such as E. affinis may not be randomly distributed in the river channel and behaviours such as diel vertical migration may be just as evident in river habitats as in lakes.     

Trinucleotide microsatellite loci for the zebra mussel Dreissena polymorpha,an invasive species in Europe and North America

The high mutation rate at microsatellite loci can supply important demographic information on founder events and range expansion in an invasive species such as the zebra mussel Dreissena polymorpha, following its initial introduction. In order to facilitate studies into the colonization patterns of this species in new habitats in Europe and North America, five trinucleotide microsatellite loci were isolated from a partial DNA library. Allelic diversity at all described loci was high, ranging from 20 to 35 alleles per locus. Homologous loci were not amplified in a second related invasive species, Dreisenna bugensis, using the primers developed here.