Discovery of Dreissena rostriformis bugensis (Andrusov 1897) in Western Europe

Live individuals of Dreissena rostriformis bugensis were found in a trawlnet sample taken in April 2006 near Willemstad in the Hollands Diep, part of the main distributary in the Rhine delta in The Netherlands. This represented the first record of this species in Western Europe and a major westward range extension for this Ponto-Caspian species. Density was very low, with the ratio of Dreissena polymorpha to D. rostriformis bugensis in the order of 100:1. Mean length (n = 5) was 22.5 mm (range 20.4–24.6 mm), suggesting that they were at least two years old and that the original introduction into the Hollands Diep had occurred in 2004 or earlier. Species identity was confirmed by morphological and molecular methods. We speculate that the invasion occurred through the Main-Danube Canal – a pathway that is becoming increasingly recognized as a southern corridor for the potential movement of non-indigenous aquatic species between Eastern and Western Europe.     

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.     

Susceptibility of quagga mussels (Dreissena rostriformis bugensis) to hot-water sprays as a means of watercraft decontamination

The recent spread of dreissenid mussels to various bodies of water in the western US has sparked interest by many state and federal agencies to develop protocols to stop further expansion. Quagga mussels (Dreissena rostriformis bugensis) are of particular importance as they are currently the most widespread dreissenid species in the region. This project examined the susceptibility of quagga mussels to hot-water sprays at different temperatures and durations of spray contact at Lake Mead (Nevada-Arizona, USA). Emersed adult quagga mussels were exposed to hot-water sprays at 20, 40, 50, 54, 60, 70, and 80°C for 1, 2, 5, 10, 20, 40, 80, and 160 s. Sprays at ≥60°C for 5 s were shown to be 100% lethal. Sprays of 54°C for 10 s, 50°C for 20 s, and 40°C for 40 s also resulted in 100% mortality. A spray temperature of 60°C for 5 s is recommended for mitigating fouling by quagga mussels.     

Susceptibility of quagga mussels (Dreissena rostriformis bugensis) to hot-water sprays as a means of watercraft decontamination

The recent spread of dreissenid mussels to various bodies of water in the western US has sparked interest by many state and federal agencies to develop protocols to stop further expansion. Quagga mussels (Dreissena rostriformis bugensis) are of particular importance as they are currently the most widespread dreissenid species in the region. This project examined the susceptibility of quagga mussels to hot-water sprays at different temperatures and durations of spray contact at Lake Mead (Nevada-Arizona, USA). Emersed adult quagga mussels were exposed to hot-water sprays at 20, 40, 50, 54, 60, 70, and 80°C for 1, 2, 5, 10, 20, 40, 80, and 160?s. Sprays at ≥60°C for 5?s were shown to be 100% lethal. Sprays of 54°C for 10?s, 50°C for 20?s, and 40°C for 40?s also resulted in 100% mortality. A spray temperature of 60°C for 5?s is recommended for mitigating fouling by quagga mussels.     

Range expansion of quagga mussels Dreissena rostriformis bugensis in the Volga River and Caspian Sea basin

In 1992, we discovered populations of the nonindigenous quagga mussel Dreissena rostriformis bugensis in the middle reaches of the Volga River. The same species was found in samples collected between 1994 and 1997 in the Volga delta and in shallow areas of the Northern Caspian Sea. D. r. bugensis always co-occurred with its more widespread congener, the zebra mussel D. polymorpha (Pallas 1771). The quagga mussel's contribution to total Dreissena abundance increased over time in the middle Volga reservoirs and Volga River delta. D. r. bugensis was common in the Volga portion of Rybinsk Reservoir during 1997 and, by 2000, it was in Uglich, Rybinsk and Gorky Reservoirs on the Upper Volga River. D. r. bugensis was neither found in Ivankov Reservoir, nor in terminal sections of the Volga-Baltic corridor including the eastern Gulf of Finland. Presently, all but the northern-most regions of the Volga River have been colonized by D. r. bugensis. We hypothesize that its introduction into the Volga River and Caspian basin occurred no later than the late 1980s via commercial shipping that utilized the Volga-Don waterway to navigate between the source Black-Azov Sea region and recipient areas on the Volga River. Larval drift likely contributed to establishment of populations at downstream sites, while human-mediated vectors may be responsible for introductions to upstream locations on the Volga River. We anticipate continued northward dispersal in conjunction with shipping activities.     

Transformation of the offshore benthic community in Lake Michigan: recent shift from the native amphipod Diporeia spp. to the invasive mussel Dreissena rostriformis bugensis

1. The native amphipod Diporeia spp. was once the dominant benthic organism in Lake Michigan and served as an important pathway of energy flow from lower to upper trophic levels. Lake‐wide surveys were conducted in 1994/1995, 2000 and 2005, and abundances of Diporeia and the invasive bivalves Dreissena polymorpha (zebra mussel) and Dreissena rostriformis bugensis (quagga mussel) were assessed. In addition, more frequent surveys were conducted in the southern region of the lake between 1980 and 2007 to augment trend interpretation. 2. Between 1994/1995 and 2005, lake‐wide density of Diporeia declined from 5365 to 329 m⁻², and biomass (dry weight, DW) declined from 3.9 to 0.4 g DW m⁻². The percentage of all sites with no Diporeia increased over time: 1.1% in 1994/1995, 21.7% in 2000 and 66.9% in 2005. On the other hand, total dreissenid density increased from 173 to 8816 m⁻², and total biomass increased from 0.4 to 28.6 g DW m⁻². Over this 10‐year time period, D. r. bugensis displaced D. polymorpha as the dominant dreissenid, comprising 97.7% of the total population in 2005. In 2007, Diporeia was rarely found at depths shallower than 90 m and continued to decline at greater depths, whereas densities of D. r. bugensis continued to increase at depths greater than 50 m. 3. The decline in Diporeia occurred progressively from shallow to deep regions, and was temporally coincident with the expansion of D. polymorpha in nearshore waters followed by the expansion of D. r. bugensis in offshore waters. In addition, Diporeia density was negatively related to dreissenid density within and across depth intervals; the latter result indicated that dreissenids in shallow waters remotely influenced Diporeia in deep waters. 4. With the loss of Diporeia and increase in D. r. bugensis, the benthic community has become a major energy sink rather that a pathway to upper trophic levels. With this replacement of dominant taxa, we estimate that the relative benthic energy pool increased from 17 to 109 kcal m⁻² between 1994/1995 and 2005, and to 342 kcal m⁻² by 2007. We project that previously observed impacts on fish populations will continue and become more pronounced as the D. r. bugensis population continues to expand in deeper waters.     

Distribution and invasion genetics of the quagga mussel (<Emphasis Type="Italic">Dreissena rostriformis bugensis</Emphasis>) in German rivers

The quagga mussel Dreissena rostriformis bugensis, native to the Dnieper and the northern Black Sea, has become a major invasive species in both the Volga River and the North American Great Lakes since the early 1990s. Findings in the Netherlands (2006) and Germany (2007) mark the start of its establishment in Western Europe. We investigated the current distribution, time of first arrival and population structure of D. rostriformis bugensis from the rivers Rhine, Main and in the Main-Danube canal in Germany. Two putative sources of the German populations were analysed by genetically comparing these populations to older invasive populations from North America and the southeast Danube. Dreissena rostriformis bugensis was abundant in the Main and in three Rhine harbours, but rare in the actual Rhine river and absent south of the Main-Danube canal. Mussels found in the Rhine harbours were significantly smaller than in the Main. Population genetic analyses found no sign of founder effects and minimal differentiation between German, North American and southeast Danube populations. The genetic data suggest that these invasive populations derive from a common and rapidly expanding source. Based on the non-continuous distribution and shell size differences of Rhine harbour and Main populations, our results indicate that expansion in Germany involved at least two independent settling events, one of which happened before 2005, and most likely was caused by jump dispersal.     

Invasion history, distribution, and relative abundances of Dreissena bugensis in the old world: a synthesis of data

We examined trends in expansion patterns and relative abundances of Dreissena bugensis in reservoirs and major river systems in eastern Europe. Based on our own data and data from the literature, it is apparent that trends were variable across river basins and not easily related to environmental conditions. In some cases these did not conform to the patterns typically found for dreissenids. In the early period of expansion beyond its native range in the Dnieper-Bug delta and estuary, D. bugensis rapidly replaced Dreissena polymorpha in the upper Dnieper River system, but increased only gradually and over time became less abundant relative to D. polymorpha in the Don-Manych River system. Contrary to the Dnieper and Don River systems, in the Volga River system considerable spatial variability in relative abundances was apparent, particularly in northern reservoirs. Moreover, even though D. bugensis usually displaces D. polymorpha as the dominant dreissenid, the latter can remain dominant in certain types of habitats where conditions are less favourable for the former. Suggested factors that may be responsible for differences in invasion patterns in the river systems may include differential responses to temperature, or to some other factor(s) associated with geographical latitude, the level of water mineralization, and selective predation by molluscivorous fish. In particular, the northward expansion of D. bugensis seems to be limited by temperature. The lack of long-term data on appropriate scales precludes linking these differences to specific features within the environment, but our comparisons indicate that the expansion of D. bugensis relative to D. polymorpha is more complex than previously believed.     

Fouling of European freshwater bivalves (Unionidae) by the invasive zebra mussel (Dreissena polymorpha)

1. The zebra mussel (Dreissena polymorpha) is well known for its invasive success and its ecological and economic impacts. Of particular concern has been the regional extinction of North American freshwater mussels (Order Unionoida) on whose exposed shells the zebra mussels settle. Surprisingly, relatively little attention has been given to the fouling of European unionoids. 2. We investigated interspecific patterns in fouling at six United Kingdom localities between 1998 and 2008. To quantify the effect on two pan‐European unionoids (Anodonta anatina and Unio pictorum), we used two measures of physiological status: tissue mass : shell mass and tissue glycogen content. 3. The proportion of fouled mussels increased between 1998 and 2008, reflecting the recent, rapid increase in zebra mussels in the U.K. Anodonta anatina was consistently more heavily fouled than U. pictorum and had a greater surface area of shell exposed in the water column. 4. Fouled mussels had a lower physiological condition than unfouled mussels. Unlike tissue mass : shell mass ratio, tissue glycogen content was independent of mussel size, making it a particularly useful measure of condition. Unio pictorum showed a stronger decline in glycogen with increasing zebra mussel load, but had a broadly higher condition than A. anatina at the time of study (July). 5. Given the high conservation status and important ecological roles of unionoids, the increased spatial distribution and fouling rates by D. polymorpha in Europe should receive more attention.     

Targeted and passive environmental DNA approaches outperform established methods for detection of quagga mussels,Dreissena rostriformis bugensis in flowing water

1. The early detection of invasive non‐native species (INNS) is important for informing management actions. Established monitoring methods require the collection or observation of specimens, which is unlikely at the beginning of an invasion when densities are likely to be low. Environmental DNA (eDNA) analysis is a highly promising technique for the detection of INNS—particularly during the early stages of an invasion.
2. Here, we compared the use of traditional kick‐net sampling with two eDNA approaches (targeted detection using both conventional and quantitative PCR and passive detection via metabarcoding with conserved primers) for detection of quagga mussel, Dreissena rostriformis bugensis, a high priority INNS, along a density gradient on the River Wraysbury, UK.
3. All three molecular tools outperformed traditional sampling in terms of detection. Conventional PCR and qPCR both had 100% detection rate in all samples and outperformed metabarcoding when the target species was at low densities. Additionally, quagga mussel DNA copy number (qPCR) and relative read count (metabarcoding) were significantly influenced by both mussel density and distance from source population, with distance being the most significant predictor.
4. Synthesis and application. All three molecular approaches were more sensitive than traditional kick‐net sampling for the detection of the quagga mussel in flowing water, and both qPCR and metabarcoding enabled estimates of relative abundance. Targeted approaches were more sensitive than metabarcoding, but metabarcoding has the advantage of providing information on the wider community and consequently the impacts of INNS.

     

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.     

Long-term demography of a zebra mussel (Dreissena polymorpha) population

1. We used long‐term data and a simulation model to investigate temporal fluctuations in zebra mussel populations, which govern the ecological and economic impacts of this pest species. 2. The size of the zebra mussel (Dreissena polymorpha) population in the Hudson River estuary fluctuated approximately 11‐fold across a 13‐year period, following a cycle with a 2–4 year period. 3. This cycling was caused by low recruitment during years of high adult population size, rapid somatic growth of settled animals, and adult survivorship of 50% per year. 4. Adult growth and body condition were weakly correlated with phytoplankton biomass. 5. The habitat distribution of the Hudson's population changed over the 13‐year period, with an increasing proportion of the population spreading onto soft sediments over time. The character of soft‐sediment habitats in the Hudson changed because of large amounts (mean = 34 g DM m^?2) of empty zebra mussel shells now in the sediments. 6. Simulation models show that zebra mussel populations can show a range of long‐term trajectories, depending on the balance between adult space limitation, larval food limitation, and disturbance. 7. Effective understanding and management of the effects of zebra mussels and other alien species depend on understanding of their long‐term demography, which may vary across ecosystems.     

Impending extinctions of North American freshwater mussels (Unionoida) following the zebra mussel (Dreissena polymorpha) invasion

1. Freshwater mussels (Order Unionoida) are the most imperiled faunal group in North America; 60% of described species are considered endangered or threatened, and 12% are presumed extinct. Widespread habitat degradation (including pollution, siltation, river channelization and impoundment) has been the primary cause of extinction during this century, but a new stress was added in the last decade by the introduction of the Eurasian zebra mussel, Dreissena polymorpha , a biofouling organism that smothers the shells of other molluscs and competes with other suspension feeders for food. Since the early 1990s, it has been spreading throughout the Mississippi River basin, which contains the largest number of endemic freshwater mussels in the world. In this report, we use an exponential decay model based on data from other invaded habitats to predict the long-term impact of D. polymorpha on mussel species richness in the basin.
2. In North American lakes and rivers that support high densities (>3000 m⁻²) of D. polymorpha , native mussel populations are extirpated within 4–8 years following invasion. Significant local declines in native mussel populations in the Illinois and Ohio rivers, concomitant with the establishment of dense populations of D. polymorpha , suggest that induced mortality is occurring in the Mississippi River basin.
3. A comparison of species loss at various sites before and after invasion indicates that D. polymorpha has accelerated regional extinction rates of North American freshwater mussels by 10-fold. If this trend persists, the regional extinction rate for Mississippi basin species will be 12% per decade. Over 60 endemic mussels in the Mississippi River basin are threatened with global extinction by the combined impacts of the D. polymorpha invasion and environmental degradation.     

Journey into the past: using cryogenically stored samples to reconstruct the invasion history of the quagga mussel (Dreissena rostriformis) in German river systems

Knowledge about the spatial–temporal dynamics of biological invasions often remains incomplete, because precise information about the invaders’ arrival dates is rare. This applies to the quagga mussel, which has become one of the most successful invasive species in Western European freshwaters. We here used cryogenically stored Dreissena samples from the German Environmental Specimen Bank to reconstruct the colonization history of the quagga mussel in German river systems. Our retrospective genetic analysis significantly improved upon previous findings of when the quagga mussel arrived in Germany and can be used as chronological landmarks to reconstruct its range expansion. The discovery of Dreissena rostriformis in 2004 in the Rhine River near Koblenz presented the first record of this species not only in Germany, but also in Western Europe. Our results show that the quagga mussel had already invaded not only large parts of the Rhine and the Danube, but also the Elbe River. This demonstrates the value of cryobanked biological samples for the retrospective analysis of biological ‘pollution’ through alien invasive species.     

Shell biofilm nitrification and gut denitrification contribute to emission of nitrous oxide by the invasive freshwater mussel Dreissena polymorpha (zebra mussel)

Nitrification in shell biofilms and denitrification in the gut of the animal accounted for N(2)O emission by Dreissena polymorpha (Bivalvia), as shown by gas chromatography and gene expression analysis. The mussel's ammonium excretion was sufficient to sustain N(2)O production and thus potentially uncouples invertebrate N(2)O production from environmental N concentrations.     

Disentangling the genetic origin of Heracleum persicum (Apiaceae) in Europe: multiple introductions from multiple source populations

Biological Invasions - Unraveling the origin and colonization history of invasive plants is a long-standing challenge in evolutionary and conservation biology. The knowledge of the origin of the...     

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.     

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.