A Review of the Biology and Ecology of the Quagga Mussel (Dreissena bugensis), a Second Species of Freshwater Dreissenid Introduced to North America

SYNOPSIS. North America's Great Lakes have recently been invadedby two genetically and morphologically distinct species of Dreissena.The zebra mussel (Dreissena polymorpha) became established inLake St. Clair of the Laurentian Great Lakes in 1986 and spreadthroughout eastern North America. The second dreissenid, termedthe quagga mussel, has been identified as Dreissena bugensisAndrusov, 1897. The quagga occurs in the Dnieper River drainageof Ukraine and now in the lower Great Lakes of North America.In the Dnieper River, populations of D. polymorpha have beenlargely replaced by D. bugensis; anecdotal evidence indicatesthat similar trends may be occurring in the lower LaurentianGreat Lakes. Dreissena bugensis occurs as deep as 130 m in theGreat Lakes, but in Ukraine is known from only 0–28 m.Dreissena bugensis is more abundant than D. polymorpha in deeperwaters in Dneiper River reservoirs. The conclusion that NorthAmerican quagga mussels have a lower thermal maximum than zebramussels is not supported by observations made of populationsin Ukraine. In the Dnieper River drainage, quagga mussels areless tolerant of salinity than zebra mussels, yet both dreissenidshave acclimated to salinities higher than North American populations;eventual colonization into estuarine and coastal areas of NorthAmerica cannot be ignored.     

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.     

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.     

Natural hybridization of two mussel species <Emphasis Type="Italic">Dreissena polymorpha</Emphasis> (Pallas, 1771) and <Emphasis Type="Italic">Dreissena bugensis</Emphasis> (Andrusov, 1897)

Dreissenids display a high diversity of shell morphology, and it is frequently difficult to ascribe some individuals from mixed populations to one of the two species, Dreissena polymorpha (Pallas, 1771) or D. bugensis (Andrusov, 1897). Presumably, such individuals may be interspecific hybrids. We have analyzed species-specific allozyme loci of the typical representatives of these two mussel species and putative interspecific hybrids. A natural interspecific hybrid between D. polymorpha and D. bugensis was discovered for the first time by genetic methods. It has been demonstrated that D. bugensis was a maternal parent.     

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.     

Comparative analysis of the structure and fauna of endosymbionts of communities of two dreissenid species (Mollusca,Dreissenidae) in the Upper Volga reservoirs

Investigations into the structure of communities of two dreissenid species are presented (native Dreissena polymorpha Pallas, 1771, and invasive D. bugensis Andrusov, 1897) in the Gorky and Rybinsk reservoirs (the Upper Volga basin). Significant interspecific and interpopulational differences in the main quantitative parameters and the fauna of endosymbionts are revealed between these mollusks.     

Invasion ecology of quagga mussels (<Emphasis Type="Italic">Dreissena rostriformis bugensis</Emphasis>): a review of evolutionary and phylogenetic impacts

Two invasive freshwater mussels, Dreissena rostriformis bugensis (quagga mussel) and D. polymorpha (zebra mussel), reveal differences in patterns and timing of their invasions in Europe. They belong to different clades in Dreissena phylogenetics: D. rostriformis bugensis genetically is coupled with the brackish water, lacustrine D. r. distincta and the two are believed to represent a single species. As such, the guaqqa mussel has environmental requirements that differ from the congeneric D. polymorpha. D. rostriformis bugensis invasions were confined to reservoirs of the Dnieper, Don and Dniester Rivers of the Black Sea basin. We recorded D. r. bugensis outside the Black Sea basin for the first time between 1992 and 2001, along the Volga River reservoir cascade including the Northern Caspian Sea shallows. This represents a 40-year invasion time lag since an invasion corridor through the Volgo-Don Waterway was established in 1952 (a corridor used extensively by many invertebrate species from the Black Sea region). We attribute the postponed invasion of Europe by D. r. bugensis, including peculiarities in establishment and its absence in fossil records, to its phylogenetically close relationship with D. r. distincta and its recent evolutionary origin. The relatively rapid range expansion of D. r. bugensis in eastern Europe during the past several decades was facilitated by human-mediated ecosystem transformation, notably impoundment of large eastern European rivers, that have allowed this species to utilize newly transformed ecosystems.     

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.     

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

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

Community‐level effects of co‐occurring native and exotic ecosystem engineers

1. Non‐indigenous ecosystem engineers can substantially affect native biodiversity by transforming the physical structure of habitats. In the Great Lakes–St. Lawrence River system, introduced dreissenid mussels (Dreissena polymorpha and D. bugensis) and the native benthic macroalga Cladophora act as ecosystem engineers by increasing substratum complexity and providing interstitial habitat for benthic macroinvertebrates. 2. We manipulated the topography and perimeter‐to‐area ratio of patches of dreissenid mussels in a series of colonisation experiments conducted at two sites in the St. Lawrence River. Experimental substrata were variably colonised by Cladophora, prompting us to examine (i) how the topography of Dreissena patches affects benthic macroinvertebrate diversity and (ii) the extent to which the effects of Dreissena are altered by the presence of another habitat‐modifying organism (Cladophora). 3. The results of our first experiment suggested that a patchy distribution of dreissenid mussels is an important driver of benthic diversity at small spatial scales. The results of our second and third experiments suggested that a native habitat engineer, Cladophora, modifies the impact of Dreissena on benthic macroinvertebrate communities. 4. While macroalgal blooms have been linked to the large‐scale impacts of Dreissena on light and nutrient availability, Dreissena shells inhibited Cladophora growth at our experimental scale. These findings demonstrate that the interactions between habitat‐modifying species can complicate efforts to predict the community‐level effects of an invasion.     

Soluble nitrogen and phosphorus excretion of exotic freshwater mussels (Dreissena spp.): potential impacts for nutrient remineralisation in western Lake Erie

1. Recent increases in phytoplankton biomass and the recurrence of cyanobacterial blooms in western Lake Erie, concomitant with a shift from a community dominated by zebra mussels (Dreissena polymorpha) to one dominated by quagga mussels (D. bugensis), led us to test for differences in ammonia‐nitrogen and phosphate‐phosphorus excretion rates of these two species of invasive molluscs. 2. We found significant differences in excretion rate both between size classes within a taxon and between taxa, with zebra mussels generally having greater nutrient excretion rates than quagga mussels. Combining measured excretion rates with measurements of mussel soft‐tissue dry weight and shell length, we developed nutrient excretion equations allowing estimation of nutrient excretion by dreissenids. 3. Comparing dreissenid ammonia and phosphate excretion with that of the crustacean zooplankton, we demonstrated that the mussels add to nitrogen and phosphorus remineralisation, shortening nitrogen and phosphorus turnover times, and, importantly, modify the nitrogen and phosphorus cycles in Lake Erie. The increased nutrient flux from dreissenids may facilitate phytoplankton growth and cyanobacterial blooms in well‐mixed and/or shallow areas of western Lake Erie.     

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.     

Genetic variability and phylogeographical patterns of a nonindigenous species invasion: a comparison of exotic vs. native zebra and quagga mussel populations

There have been few investigations of the number of founding sources and amount of genetic variability that lead to a successful nonindigenous species invasion, although genetic diversity is believed to play a central role. In the present study, population genetic structure, diversity and divergence patterns were analysed for the zebra mussel Dreissena polymorpha [n=280 samples and 63 putative randomly amplified polymorphic DNA (RAPDs) gene loci] and the quagga mussel D. bugensis (n=136 and 52 loci) from 10 nonindigenous North American and six Eurasian sampling sites, representing their present‐day ranges. Results showed that exotic populations of zebra and quagga mussels had surprisingly high genetic variability, similar to those in the Eurasian populations, suggesting large numbers of founding individuals and consistent with the hypothesis of multiple colonizations. Patterns of genetic relationships indicate that the North American populations of D. polymorpha likely were founded by multiple source populations from north‐western and northcentral Europe, but not from southcentral or eastern Europe. Sampling areas within North America also were significantly divergent, having levels of gene flow and migration about twice those separating long‐established Eurasian populations. Samples of D. bugensis in Lakes Erie and Ontario were significantly different, with the former being more closely related to a native population from the Dnieper River, Ukraine. No evidence for a founder effect was discerned for either species.     

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

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

Preferential manganese accumulation in dreissenid byssal threads

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

Comparison of nutrition range in <Emphasis Type="Italic">Dreissena polymorpha</Emphasis> and <Emphasis Type="Italic">Dreissena bugensis</Emphasis> mussels by biochemical markers

Based on biochemical markers, we studied the nutrition ranges of populations of Dreissena polymorpha and Dreissena bugensis mussels that inhabit the Volga reach of the Rybinsk reservoir and differ in the long-term population dynamics. Features of the nutrition ranges of mussels are regarded as the probable cause of changes in the number of mollusca.     

Assessing the effects of application time and temperature on the efficacy of hot-water sprays to mitigate fouling by Dreissena polymorpha (zebra mussels Pallas)

Dreissenid mussel (Dreissena polymorpha, Dreissena rostriformis bugensis) expansion into the Western US has renewed interest in hot-water spray mitigation of mussel fouling on boat hulls, trailers, and other equipment. However, the efficacy of hot-water sprays to mitigate dreissenid fouling has not been experimentally assessed. Emersed, adult D. polymorpha were exposed to low-pressure, hot-water sprays at 40, 50, 60, 70, and 80°C for 1, 5, or 10 s. Sprays at ≥60°C for 10 s or 80°C at ≥5 s were 100% lethal. In contrast, 1–10 s exposures did not induce 100% mortality at ≤50°C. The results indicate that mitigation of D. polymorpha fouling, especially in areas protected from the hydraulic impacts of high-pressure sprays requires spray temperatures of > 80°C applied for >5 s or no less than 60°C applied for >10 s. Thus, presently recommended spray temperatures of ≥60°C may not be 100% effective unless applied for >10 s.     

The toxicity of endod extract to the early life stages of Dreissena bugensis

Toxicity bioassays were conducted on embryos and early larvae of quagga mussels, Dreissena bugensis, using a filtered aqueous extract and a lyophilized butanol extract of the soap berry plant Phytolacca dodecandra. Developmental stages exposed to each extract were embryos to trochophores (ca 3h‐17h), trochophores to D‐hinge larvae (ca 17h‐40h) and embryos to D‐hinge (3h‐ca 40). Over the whole embryo to D‐hinge exposure period, the aqueous extract resulted in a lowest observed effective concentration (LOEC) of 5mgl^‐1 although mortality did not exceed 50%. For the butanol extract, the LOEC was 2mgl^‐1 and the LC₅₀ was 2.1 mgl^‐1. For the aqueous extract, most of the endod toxicity was seen at the embryo stage, whereas for the butanol extract the toxicity was associated with the trochophore stage. Compared with other non‐oxidizing commercial molluscicides, endod has only moderate toxicity to early dreissenid life stages.     

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.     

The influence of pre‐settlement and early post‐settlement processes on the adult distribution and relative dominance of two invasive mussel species

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