Temporal variation in zebra mussel (Dreissena polymorpha) density structure the benthic food web and community composition on hard substrates in Lake Constance, Germany

Invasive species often influence existing biocenoses by altering their environment or facilitating the ecology of other species. Here we combined stable isotope analysis with quantitative benthic community sampling to investigate temporal variation in the influence of biodeposition of organic material (biodeposits) by the zebra mussel (Dreissena polymorpha) on the benthic food web in hard substrate habitats of Lake Constance, Germany. The accumulation of organic material excreted by zebra mussels (faeces and pseudofaeces) is hypothesised to implement a biodeposition based food web. By means of stable isotope analyses, we found that the feeding strategy of amphipods was dependent on the availability of zebra mussel biodeposits. The proportion of pelagic resources contributing to the diet (by ??¹³C) and trophic position (by ??¹⁵N) of amphipods were significantly and positively correlated to the production of zebra mussel biodeposits. Also, the benthic community in Lower Lake Constance showed a shift towards higher densities of the mayfly Caenis spp., Chironominae, and the caddisfly Ecnomus tenellus, which might act as links to higher trophic levels when more zebra mussel biodeposits were available. These results demonstrate that temporal variation in zebra mussel density, and thus in organic biodeposition, have a strong impact on the benthic communities and food web structure associated with hard substrates to the extent that there may be dependence on zebra mussel occurrence in such habitats in Lake Constance.     

Specific amplification of the 18S rRNA gene as a method to detect zebra mussel (Dreissena polymorpha) larvae in plankton samples

An important issue in the management of zebra mussel (Dreissena polymorpha) populations is early, rapid, and accurate detection of the planktonic larvae (veliger) of the zebra mussel. The goal of this study was to explore the feasibility of developing a molecular approach for the detection of zebra mussel larvae in diverse environments. In this study a Dreissena polymorpha-specific 18S ribosomal RNA gene targeted oligonucleotide primer (ZEB-715a) and Polymerase Chain Reaction (PCR) assay was developed and compared with cross-polarized microscopy as a means to detect zebra mussel veligers in plankton samples. The design of the zebra mussel-specific primer was facilitated by sequencing nearly the complete 18S rRNA gene from the zebra mussel and three other closely related freshwater Veneroids including the quagga mussel (D. bugensis), the dark false mussel (Mytilopsis leucophaeata), and the Asian freshwater clam (Corbicula fluminea). The specificity of the primer for the zebra mussel was empirically tested by using the primer as a direct probe in a blot hybridization format. A single veliger in a plankton sample could be detected by PCR using this approach. Veliger detection sensitivity using the PCR approach was estimated to be over 300 times more sensitive than cross-polarized light microscopy based techniques. Cross-polarized light microscopy and the PCR technique were used to identify the presence of zebra mussel larvae in plankton samples that were collected from a variety of natural and industrial water sources. Detection results (presence or absence) were generally consistent between the two methods. Although additional studies will be required before routine application of molecular based veliger detection technology is available, a long-term goal of this work is the application of molecular technology to the development of a field device for the routine detection and quantification of zebra mussel veligers.     

Putative identification of expressed genes associated with attachment of the zebra mussel (Dreissena polymorpha)

Because of its aggressive growth and firm attachment to substrata, the zebra mussel (Dreissena polymorpha) has caused severe economic and ecological problems since its invasion into North America. The nature and details of attachment of this nuisance mollusc remains largely unexplored. Byssus, a special glandular apparatus located at the root of the foot of the mussel produces threads and plates through which firm attachment of the mollusc to underwater objects takes place. In an attempt to better understand the adhesion mechanism of the zebra mussel, the suppression subtractive hybridization (SSH) assay was employed to produce a cDNA library with genes unique to the foot of the mussel. Analysis of the SSH cDNA library revealed the presence of 750 new expressed sequence tags (ESTs) including 304 contigs and 446 singlets. Using BLAST search, 365 zebra mussel ESTs showed homology to other gene sequences with putative functions. The putative functions of the homologues included proteins involved in byssal thread formation in zebra and blue mussels, exocrine gland secretion, host defence, and house keeping. The generated data provide, for the first time, some useful insights into the foot structure of the zebra mussel and its underwater adhesion.     

Putative identification of expressed genes associated with attachment of the zebra mussel (Dreissena polymorpha)

Because of its aggressive growth and firm attachment to substrata, the zebra mussel (Dreissena polymorpha) has caused severe economic and ecological problems since its invasion into North America. The nature and details of attachment of this nuisance mollusc remains largely unexplored. Byssus, a special glandular apparatus located at the root of the foot of the mussel produces threads and plates through which firm attachment of the mollusc to underwater objects takes place. In an attempt to better understand the adhesion mechanism of the zebra mussel, the suppression subtractive hybridization (SSH) assay was employed to produce a cDNA library with genes unique to the foot of the mussel. Analysis of the SSH cDNA library revealed the presence of 750 new expressed sequence tags (ESTs) including 304 contigs and 446 singlets. Using BLAST search, 365 zebra mussel ESTs showed homology to other gene sequences with putative functions. The putative functions of the homologues included proteins involved in byssal thread formation in zebra and blue mussels, exocrine gland secretion, host defence, and house keeping. The generated data provide, for the first time, some useful insights into the foot structure of the zebra mussel and its underwater adhesion.     

Space as a limiting resource in freshwater systems: competition between zebra mussels (Dreissena polymorpha) and freshwater sponges (Porifera)

Species interactions between two types of sessile benthic invertebrates, the zebra mussel (Dreissena polymorpha) and freshwater sponges (Porifera), were evaluated in Michigan City IN Harbor in southern Lake Michigan during 1996. The study objective was to define whether competition plays a role in structuring benthic communities using experimental techniques commonly employed in marine systems. Sponges were uninhibited by zebra mussel presence and overgrew zebra mussel shells on hard vertical substrata. In contrast, zebra mussels did not overgrow sponge colonies, but did show an ability to re-capture hard substrata if relinquished by the sponge. The negative affect of sponges on zebra mussels through overgrowth and recruitment suggests interactions that could eventually displace zebra mussels from these benthic communities. However, seasonal reduction of sponge biomass from autumn through winter appears to allow the zebra mussel a periodic respite from overgrowth, preventing exclusion of zebra mussels from the community and allowing these two taxa to co-exist.     

Current and modeled potential distribution of the zebra mussel (Dreissena polymorpha) in Sweden

In this study, we report the results from a recently performed survey of zebra mussel in Sweden and present a risk model for the potential distribution of the species. The zebra mussel was found in 11 of the 30 surveyed lakes and rivers. Most of the observations were made in the north-eastern parts of Lake M?laren, i.e., in the basins Ekoln, Skarven, and G?rv?ln. Hierarchical partitioning and stepwise selection of water chemistry variables in a multiple logistic model identified pH and magnesium concentrations as the best predictors for zebra mussel occurrence. We conjecture that magnesium is an important predictor due to its crucial role in mussel physiology. The logistic model was applied on 2,781 lakes and in total 109 lakes (3.9%), most of them situated in specific areas in central Sweden, in the very south and on the island of Gotland, were predicted to be potentially at risk for zebra mussel invasions. The lakes potentially at risk for zebra mussel invasions are separated by the soft-water boreal lakes that constitute the vast majority of lakes on the Fennoscandian peninsula, thus forming barriers for further dispersal.     

Zebra mussel adhesion: structure of the byssal adhesive apparatus in the freshwater mussel, Dreissena polymorpha

The freshwater zebra mussel (Dreissena polymorpha) owes a large part of its success as an invasive species to its ability to attach to a wide variety of substrates. As in marine mussels, this attachment is achieved by a proteinaceous byssus, a series of threads joined at a stem that connect the mussel to adhesive plaques secreted onto the substrate. Although the zebra mussel byssus is superficially similar to marine mussels, significant structural and compositional differences suggest that further investigation of the adhesion mechanisms in this freshwater species is warranted. Here we present an ultrastructural examination of the zebra mussel byssus, with emphasis on interfaces that are critical to its adhesive function. By examining the attached plaques, we show that adhesion is mediated by a uniform electron dense layer on the underside of the plaque. This layer is only 10-20 nm thick and makes direct and continuous contact with the substrate. The plaque itself is fibrous, and curiously can exhibit either a dense or porous morphology. In zebra mussels, a graded interface between the animal and the substrate mussels is achieved by interdigitation of uniform threads with the stem, in contrast to marine mussels, where the threads themselves are non-uniform. Our observations of several novel aspects of zebra mussel byssal ultrastructure may have important implications not only for preventing biofouling by the zebra mussel, but for the development of new bioadhesives as well.     

Zebra mussel colonisation of soft sediments facilitates invertebrate communities

1. We examined the effect of zebra mussel colonisation on invertebrate communities inhabiting soft sediments in two bays along the Vermont shoreline of Lake Champlain, U.S.A. 2. In summer 2001, we conducted manipulative experiments (addition and removal of zebra mussel colonies) with respective controls to assess the effect of colonies on invertebrate abundance, richness, and position within sediments (within colony versus underlying colony) and compared these data to comparative studies of natural communities in summer 2002. 3. Split core samples were taken two months after the manipulation and the following year so that we could quantify individuals and species inhabiting zebra mussel colonies separately from those in sediments underlying zebra mussel colonies and adjacent sediments lacking zebra mussels. 4. Zebra mussel‐covered sediments supported more abundant and richer invertebrate communities than adjacent sediments lacking zebra mussels. 5. Abundance and richness patterns in zebra mussel‐addition and removal treatments closely paralleled those in natural communities. 6. Despite severe oxygen depletion at the interface of underlying sediments and overlying zebra mussel colonies, most infaunal invertebrates responded positively to zebra mussel colonisation either by remaining in sediments underlying zebra mussel colonies or by migrating into zebra mussel colonies.     

Zebra mussels (Dreissena polymorpha) in Ireland, AFLP-fingerprinting and boat traffic both indicate an origin from Britain

1. The zebra mussel (Dreissena polymorpha) is an aquatic nuisance species that invaded Ireland around 1994. We studied the invasion of the zebra mussel combining field surveys and genetic studies, to determine the origin of invasion and the vector of introduction. 2. Field surveys showed that live zebra mussels, attached to the hulls of pleasure boats, were transported from Britain to Ireland. These boats were lifted from British waters onto trailers, transported to Ireland by ferry and lifted into Irish waters within a day. Length‐frequency distributions of dead and living mussels on one vessel imported 3 months earlier revealed a traumatic occurrence caused by the overland, air‐exposed transportation. Results show that a large number of individuals survived after re‐immersion in Irish waters and continued to grow. 3. Zebra mussels from populations in Ireland, Great Britain, the Netherlands, France and North America, were analysed using amplified fragment length polymorphisms (AFLP)‐fingerprinting to determine the origin of the Irish invasion. Phylogenetic analysis revealed that Irish and British mussels clustered closely together, suggesting an introduction from Britain. 4. Ireland remained un‐invaded by the zebra mussel for more than 150 year. The introduction of the zebra mussel to Ireland occurred following the abolition of value added tax in January 1993 on imported second‐hand boats from the European Union (UK and continental Europe). This, together with a favourable monetary exchange rate at that time, may have increased the risk of invasion of the zebra mussel.     

The effect of seasonal variation in selective feeding by zebra mussels (Dreissena polymorpha) on phytoplankton community composition

1. To investigate the impact of zebra mussels ( Dreissena polymorpha ) on phytoplankton community composition, temporal variability in selective feeding by the mussels was determined from April to November 2005 in a natural lake using Delayed Fluorescence (DF) excitation spectroscopy.
2. Selective grazing by zebra mussels varied in relation to seasonal phytoplankton dynamics; mussels showed a consistent preference for cryptophytes and avoidance of chlorophytes and cyanobacteria. Diatoms, chrysophytes and dinoflagellates responded differentially to zebra mussel grazing depending on their size. Analysis of excreted products of the zebra mussels revealed that in addition to chlorophytes and cyanobacteria, phytoplankton >50  μ m and very small phytoplankton (≤7  μ m) were largely expelled in pseudofaeces.
3. The zebra mussel is a selective filter-feeder that alters its feeding behaviour in relation to phytoplankton composition to capture and ingest high quality phytoplankton, especially when phytoplankton occur in preferred size ranges. Flexibility of zebra mussel feeding behaviour and variation in susceptibility among phytoplankton groups to mussel ingestion indicate that invading zebra mussels could alter phytoplankton community composition of lakes and have important ecosystem consequences.     

Habitat engineering by the invasive zebra mussel <Emphasis Type="Italic">Dreissena polymorpha</Emphasis> (Pallas) in a boreal coastal lagoon: impact on biodiversity

Habitat engineering role of the invasive zebra mussel Dreissena polymorpha (Pallas) was studied in the Curonian lagoon, a shallow water body in the SE Baltic. Impacts of live zebra mussel clumps and its shell deposits on benthic biodiversity were differentiated and referred to unmodified (bare) sediments. Zebra mussel bed was distinguished from other habitat types by higher benthic invertebrate biomass, abundance, and species richness. The impact of live mussels on biodiversity was more pronounced than the effect of shell deposits. The structure of macrofaunal community in the habitats with >10³ g/m² of shell deposits devoid of live mussels was similar to that found within the zebra mussel bed. There was a continuous shift in species composition and abundance along the gradient ‘bare sediments—shell deposits—zebra mussel bed’. The engineering impact of zebra mussel on the benthic community became apparent both in individual patches and landscape-level analyses.     

Horizontal and Vertical Distribution of the Zebra Mussel (Dreissena polymorpha,Pallas) Larvae in the Modrac Reservoir,Bosnia and Herzegovina

In the Modrac Reservoir, loaded with coal separation suspended material, rapid development of the zebra mussel (Dreissena polymorpha) took place from at least 1987. It is probably the first distinguished “infection” for this part of Balkan Peninsula, caused by this organism. Horizontal and vertical distribution of this mussel, at 15 different reservoir profiles, had been investigated.     

Zebra mussel (<Emphasis Type="Italic">Dreissena polymorpha</Emphasis>) affects the feeding ecology of early stage striped bass (<Emphasis Type="Italic">Morone saxatilis</Emphasis>) in the Hudson River estuary

Variability in the feeding ecology of young fishes over short and long time scales in estuaries is likely to affect population dynamics. We studied 14 years of early stage Striped Bass feeding ecology in the Hudson River Estuary over a 25-year time span, including years in which invasive zebra mussels markedly altered energy flow within the estuary. We predicted that feeding success would be low and that diet composition would be altered during years of high zebra mussel impact, particularly in upriver locations where mussels occur. Feeding success in the short term was indicated by volume of gut contents and in the long term by dry mass at length, i.e. condition; these measures were positively intercorrelated and varied significantly year to year. We tested for associations between condition and multiple biotic and abiotic environmental variables. There was a strong negative effect of zebra mussel grazing rate on condition in upriver locations and a weak positive effect in downriver locations. In upriver locations, condition was 33% higher when local salinity was high and zebra mussel grazing rates were low, whereas in downriver locations, condition was 35% higher when zebra mussel grazing rates and copepod abundance were high and local dissolved oxygen was low. Copepods, amphipods, mysids, and Leptodora constituted the highest prey-specific index of relative importance throughout the estuary. There was no evident effect of the zebra mussel invasion on diet composition. This long-term study corroborates the inferences of earlier studies that zebra mussels reduced early-stage striped bass growth rate.     

Characterization of zebra mussel (Dreissena polymorpha) sperm motility: duration of movement, effects of cations, pH and gossypol

We have examined effects of time after activation, pH, sodium and potassium, and gossypol concentrations on sperm motility of zebra mussel (Dreissena polymorpha). Zebra mussel spermatozoa appeared to have remarkable viability in the fresh water in comparison with freshwater fish sperm. Duration of sperm motility in fresh water is possibly one of the longest among freshwater animals, since it was not significantly changed 3 h after incubation at room temperature (20 °C) or 24 h of incubation at ±0 °C. High osmotic pressure suppresses sperm motility and effects of sodium and potassium are similar. Spermatozoa were inactive at acid pH and became gradually motile when exposed to pH 6.0–9.0. Gossypol appeared to be a very potent spermicidal agent and inhibited motility. This compound also inhibited fertilization. We observed some differences in gossypol effects on spermatozoa between North American and European zebra mussels. These data on zebra mussel sperm biology may be useful for better handling of gametes under laboratory conditions.     

Predation on invasive zebra mussel, Dreissena polymorpha, by pumpkinseed sunfish, rusty crayfish, and round goby

The enemy release hypothesis states that invasive species are successful in their new environment because native species are not adapted to utilize the invasive. If true for predators, native predators should have lower feeding rates on the invasive species than a predator from the native range of the invasive species. We tested this hypothesis for zebra mussel (Dreissena polymorpha) by comparing handling time and predation rate on zebra mussels in the laboratory by two North American species (pumpkinseed, Lepomis gibbosus, and rusty crayfish, Orconectes rusticus) and one predator with a long evolutionary history with zebra mussels (round goby, Neogobius melanostomus). Handling time per mussel (7 mm shell length) ranged from 25 to >70 s for the three predator species. Feeding rates on attached zebra mussels were higher for round goby than the two native predators. Medium and large gobies consumed 50–67 zebra mussels attached to stones in 24 h, whereas pumpkinseed and rusty crayfish consumed <11. This supports the hypothesis that the rapid spread of zebra mussels in North America was facilitated by low predation rates from the existing native predators. At these predation rates and realistic goby abundance estimates, round goby could affect zebra mussel abundance in some lakes.     

An indirect effect of biological invasions: the effect of zebra mussel fouling on parasitisation of unionid mussels by bitterling fish

Invasive species represent a major threat with both direct and indirect effects on natural ecosystems, including effects on established and coevolved relationships. In a series of experiments, we examined how the interaction between two native species, a unionid mussel (Unio pictorum) and the European bitterling (Rhodeus amarus), a fish that parasitises unionids, was affected by the non-native zebra mussel (Dreissena polymorpha). The zebra mussel fouls hard substrates, including shells of living unionids, and its presence is often associated with a decrease in population density of native unionid mussels. Bitterling lay their eggs into live unionids and the embryos develop inside their gills. Using a range of zebra mussel densities, we demonstrated that zebra mussel fouling had a negative effect on the number of bitterling eggs inside the mussel host, with abundances of 5–10 zebra mussels (shell size 15–25 mm) per unionid critical for bitterling ability to utilise the host. In a further experiment, we found that bitterling did not discriminate between unfouled unionids and those fouled with five zebra mussels. Most ovipositions into fouled hosts, however, were unsuccessful as eggs failed to reach the unionid gills. We discuss implications of such unsuccessful ovipositions for bitterling recruitment and population dynamics.     

Development of a molecular diagnostic system to discriminate Dreissena polymorpha (zebra mussel) and Dreissena bugensis (quagga mussel)

A 3-primer PCR system was developed to discriminate invasive zebra (Dreissena polymorpha) and quagga (Dreissena bugensis) mussel. The system is based on: 1) universal primers that amplifies a region of the nuclear 28s rDNA gene from both species and 2) a species-specific primer complementary to either zebra or quagga mussel. The species-specific primers bind to sequences between the binding sites for the universal primers resulting in the amplification of two products from the target species and one product from the nontarget species. Therefore, nontarget products are positive amplification controls. The 3-primer system accurately discriminated zebra and quagga mussels from seven geographically distinct populations.     

Phosphorus recycling by zebra mussels in relation to density and food resource availability

Using flow-through microcosms, we examined phosphorus (P) recycling by zebra mussels under conditions of nearly constant food resource supply and varying zebra mussel population densities (600–5200 ind./m²). At all density levels, zebra mussels filtered substantial algae, measured as chlorophyll biomass. Because chlorophyll biomass inputs were low throughout the study, zebra mussel biomass-specific rates of chlorophyll filtration declined with increasing density, suggesting food resource limitation at the higher densities. We observed net total P export and high zebra mussel biomass-specific rates of P recycling over time in microcosms at high zebra mussel densities. In systems with a low zebra mussel density, net total P export did not occur over time. Our results suggest the occurrence of P remineralization by zebra mussels and net loss associated with emaciation during periods of temporary starvation. These findings have implications for P dynamics since zebra mussels can be subjected to periods of starvation over seasonal and annual time scales.     

Field and laboratory studies of Ophryoglena sp. (Ciliata: Ophryoglenidae) infection in zebra mussels,Dreissena polymorpha (Bivalvia: Dreissenidae)

This study, conducted in the Dnieper-Bug Canal in Belarus, is the first to monitor the seasonal (June-November) dynamics of infection with the parasitic ciliate Ophryoglena sp. in a zebra mussel (Dreissena polymorpha) population. Mean population prevalence and intensity of infection varied, respectively, from 11 to 62% and from 0.9 to 24.1 ciliates/mussel. Mean prevalence was highly correlated with mussel length in mussels <20 mm (R(2)=0.97) and was lower in larger mussels. Mean infection intensity in mussels 1-25 mm long was similarly correlated with their size (R=0.98), reached a maximum in the 20-25 mm size-class, and then sharply decreased, thus providing evidence, albeit limited, that high intensity of infection might be lethal. Transinfection of zebra mussels by Ophryoglena sp. was achieved in the laboratory-a first for a protozoan parasite of D. polymorpha; from an initial complete lack of infection, mean prevalence and intensity rose, respectively, to 86.7% and 8.3 ciliates/mussel.