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.     

Population genetic history of the dreissenid mussel invasions: expansion patterns across North America

This study tests population genetic patterns across the Eurasian dreissenid mussel invasions of North America—encompassing the zebra mussel Dreissena polymorpha (1986 detection) and the quagga mussel D. rostriformis bugensis (detected in 1990, which now has largely displaced the former in the Great Lakes). We evaluate their source-spread relationships and invasion genetics using 9–11 nuclear microsatellite loci for 583 zebra mussels (21 sites) and 269 quagga mussels (12 sites) from Eurasian and North American range locations, with the latter including the Great Lakes, Mississippi River basin, Atlantic coastal waterways, Colorado River system, and California reservoirs. Additionally, mtDNA cytochrome b gene sequences are used to verify species identity. Our results indicate that North American zebra mussels originate from multiple non-native northern European populations, whereas North American quagga mussels trace to native estuaries in the Southern Bug and Dnieper Rivers. Invasive populations of both species show considerable genetic diversity and structure (zebra F _ST = 0.006–0.263, quagga F _ST = 0.008–0.267), without founder effects. Most newer zebra mussel populations have appreciable genetic diversity, whereas quagga mussel populations from the Colorado River and California show some founder effects. The population genetic composition of both species changed over time at given sites; with some adding alleles from adjacent populations, some losing them, and all retaining closest similarity to their original composition. Zebra mussels from Kansas and California appear genetically similar and assign to a possible origin from the St. Lawrence River, whereas quagga mussels from Nevada and California assign to a possible origin from Lake Ontario. These assignments suggest that overland colonization pathways via recreational boats do not necessarily reflect the most proximate connections. In conclusion, our microsatellite results comprise a valuable baseline for resolving present and future dreissenid mussel invasion pathways.     

Predator‐induced morphological defences in two invasive dreissenid mussels: implications for species replacement

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Comparative Biology of Zebra Mussels in Europe and North America: An Overview

SYNOPSIS. Since the discovery of the zebra mussel, Dreissenapolymorpha, in the Great Lakes in 1988 comparisons have beenmade with mussel populations in Europe and the former SovietUnion. These comparisons include: Population dynamics, growthand mortality rates, ecological tolerances and requirements,dispersal rates and patterns, and ecological impacts. NorthAmerican studies, mostly on the zebra mussel and a few on asecond introduced species, the quagga mussel, Dreissena bugensis,have revealed some similarities and some differences. To dateit appears that North American populations of zebra musselsare similar to European populations in their basic biologicalcharacteristics, population growth and mortality rates, anddispersal mechanisms and rates. Relative to European populationsdifferences have been demonstrated for: (1) individual growthrates; (2) life spans; (3) calcium and pH tolerances and requirements;(4) potential distribution limits; and (5) population densitiesof veligers and adults. In addition, studies on the occurrenceof the two dreissenid species in the Great Lakes are showingdifferences in their modes of life, depth distributions, andgrowth rates. As both species spread throughout North America,comparisons between species and waterbodies will enhance ourability to more effectively control these troublesome 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.     

Epiphytic Refugium: Are Two Species of Invading Freshwater Bivalves Partitioning Spatial Resources?

Enumeration of benthic (bottom dwelling) and epiphytic (attached to plants) zebra and quagga mussels (Dreissena polymorpha and D. bugensis, respectively) at Lake Erie near-shore sites in fall of 2000 revealed an unexpected prevalence of the zebra mussel on submerged plants. Even at Buffalo, New York, USA, where benthic dreissenids have been 92–100% quagga mussel since 1996, zebra mussels constituted 30–61% of epiphytes numerically. This may reflect a partitioning of settling space consistent with interspecific competition. A seasonal epiphytic refugium might allow the zebra mussel to persist even where the benthos is almost exclusively quagga mussel. This revised version was published online in July 2006 with corrections to the Cover Date.     

Testing a typology system of running waters for conservation planning in Hungary

The zebra mussel (Dreissena polymorpha) and its congener the quagga mussel (Dreissena rostriformis bugensis) are both invaders in freshwater, but have very different invasion histories, with zebra mussels attaining substantially faster rates of spread at virtually all spatial scales. However, in waterbodies where they co-occur, D. r. bugensis can displace D. polymorpha. To determine if the mechanisms for this displacement are associated with different survival and growth, we kept mussels in flow-through tanks for 289 days with two temperature regimes that mimicked the natural surface water (littoral zone) and hypolimnion conditions of Lake Erie. For the littoral zone regime, we used water directly from the surface of Lake Erie (range 4–25°C, average 11.9 ± 0.6°C). For the profundal zone treatment, Lake Erie surface water was chilled to about 6°C (range 5–8°C, average 6.2 ± 0.6°C) for the full duration of the experiment. For each of these temperature regimes, we used three replicate tanks with only zebra mussels present and three replicate tanks with only quagga mussels (150 ind./tank each), and three replicate tanks with both species (75 ind./tank of each species). Quagga mussels had higher survivorship and grew more than zebra mussels in all treatments. For both species, the size of the mussel entering the winter was critical for survivorship. Larger mussels had a higher survival over the winter in all treatments. For both species, there was a survivorship and growth tradeoff. In the warmer littoral zone treatment both species had higher growth, but lower survival than in the colder profundal zone treatment. Surprisingly, although quagga mussels outperformed zebra mussels, zebra mussel survivorship was better when they were faced with competition by quagga mussels than with just intraspecific competition. In addition, quagga mussels suffered size-specific mortality during the growing season only when facing interspecific competition with zebra mussels. Further experiments are needed to determine the possible mechanisms for these interspecific effects.     

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.     

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.     

ENDOSYMBIONTS OF DREISSENA POLYMORPHA IN IRELAND: EVIDENCE FOR THE INTRODUCTION OF ADULT MUSSELS

Although zebra mussels (Dreissena polymorpha) have invaded watersacross Europe for over 200 years, they colonized Ireland onlywithin the past decade. To test the hypothesis that Irelandwas colonized by adult D. polymorpha, we examined mussels fromdifferent sites along the Lower Shannon River system in Irelandfor the presence of host specific and generalist endosymbionts.Withinthe mantle cavity and/or associated with zebra mussel tissueswe found species specific-ciliates (Conchophthirus acuminatusand Ophryoglena hemophaga) and generalist symbionts (the ciliateAncistrumina limnica, nematodes, oligochaetes and chironomids).We found a significant difference in the prevalence of symbiontsamong sites, but all mussels at all sites harboured one specialistspecies C. acuminatus, and all of the mussels at three of thefour sites also had the second specialist, O. hemophaga. Thus,with the introduction of D. polymorpha into Ireland, at leasttwo additional species, their host-specific symbionts C. acuminatusand O. hemophaga, have also been introduced. The presence ofthese symbionts in Ireland supports the hypothesis that adultzebra mussels were introduced into Ireland, rather than larvalstages. This contrasts with the introduction of zebra musselsto North America, where adult zebra mussels are devoid of host-specificsymbionts. (Received 8 June 2005; accepted 7 November 2005)     

First finding of deepwater <Emphasis Type="Italic">profunda</Emphasis> morph of quagga mussel <Emphasis Type="Italic">Dreissena bugensis</Emphasis> in the European part of its range

The deepwater profunda morph of quagga mussel Dreissena bugensis was found for the first time in the European part of its range. The mussels of this morph were found in the Cheboksary Reservoir situated in the midstream of the Volga River (Russian Federation). Traditional and geometric morphometrics confirm the similarity of studied specimens to profunda mussel described from the Great Lakes of North America. In the Cheboksary Reservoir the deepwater mussels live at depth of 26.5 m on sandy-pebbled substrate at conditions of high water velocity (>0.5 m/s), i. e. in the conditions unusual for American profunda. This fact reflects evident ecological plasticity of this morph. Discovery of the deepwater morph of quagga mussel in the European part of its range indicates that possibility of realization of the deepwater phenotype is inherent to this species. It is suggested that quagga mussel may possess two alternative developmental pathways that could be realized in appropriate conditions. Presumably, certain depth and/or water pressure may serve as signaling factors for activating the “deepwater” developmental pathway. The presence of deepwater and shallow-water morphs is very important adaptive feature for sedentary organisms such as dreissenids that are unable to select habitat actively since this feature allows for successful colonization of both deep and shallow water habitats.     

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.     

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

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

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.     

Using DNA barcoding to differentiate invasive Dreissena?species (Mollusca,Bivalvia)

The zebra mussel (Dreissena polymorpha) and the quagga mussel (Dreissena rostriformis bugensis) are considered as the most competitive invaders in freshwaters of Europe and North America. Although shell characteristics exist to differentiate both species, phenotypic plasticity in the genus Dreissena does not always allow a clear identification. Therefore, the need to find an accurate identification method is essential. DNA barcoding has been proven to be an adequate procedure to discriminate species. The cytochrome c oxidase subunit I mitochondrial gene (COI) is considered as the standard barcode for animals. We tested the use of this gene as an efficient DNA barcode and found that it allow rapid and accurate identification of adult Dreissena individuals.     

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.     

Alteration of Ecosystem Function by Zebra Mussels in Oneida Lake: Impacts on Submerged Macrophytes

Dreissenid mussels (the zebra mussel Dreissena polymorpha and the quagga mussel D. bugensis) are ecosystem engineers that modify the physical environment by increasing light penetration. Such a change is likely to affect the distribution and diversity of submerged macrophytes. Filter-feeding by these mussels has been associated with increased water clarity in many North American and European lakes. In this study, we report the increase in water clarity of Oneida Lake, New York, USA, for 1975–2002 and argue that the increase was caused by zebra mussel invasion rather than declines in nutrients. Over the study period, although mean total phosphorus decreased significantly, the main increase in water clarity occurred after the zebra mussel invasion in 1991. The average depth receiving 1% surface light increased from 6.7 m to 7.8 m after the invasion of zebra mussels, representing a 23% areal expansion. The maximum depth of macrophyte colonization, as measured by diver and hydroacoustic surveys, increased from 3.0 m before the invasion of zebra mussels to 5.1 m after their establishment. In addition, macrophyte species richness increased, the frequency of occurrence increased for most species, and the composition of the macrophyte community changed from low-light–tolerant species to those tolerating a wide range of light conditions. Comparisons with observations reported in the literature indicate that increased light penetration alone could explain these changes in macrophyte distribution and diversity. Such changes will increase the importance of benthic primary production over pelagic production in the food web, thereby representing an overall alteration of ecosystem function, a process we refer to as “benthification”.     

Origin of Spanish invasion by the zebra mussel, Dreissena polymorpha (Pallas, 1771) revealed by amplified fragment length polymorphism (AFLP) fingerprinting

The zebra mussel, Dreissena polymorpha is an aquatic nuisance invasive species originally native to the Ponto-Caspian region where it is found in lakes and delta areas of large rivers draining into the Black and Caspian seas. The dispersal of D. polymorpha began at the end of the 18th century, at a time when shipping trade become increasingly important and many canals were built for linking different navigable river systems in Europe. Over the past 200 years, zebra mussels spread to most of the lakes, rivers and waterways in Europe by a combination of natural and anthropogenic dispersal mechanisms. D. polymorpha invaded Spain around 2001, being found for the first time in the Riba-roja reservoir at the lower part of the Ebro River, North-East Spain. The relatively late invasion of Spain was most likely caused by the presence of the Pyrenees, which isolated the Iberian Peninsula from the rest of the European continent, and acted as a barrier to the dispersal of D. polymorpha. In recent studies, molecular genetic methods have successfully been used to determine phylo-geographic relationships, which may reflect invasion corridors and can help retrace source populations. Zebra mussels from populations in Great Britain, The Netherlands, Belgium, France, Germany, Spain, Italy, Romania and North America were analyzed using PCR based amplified fragment length polymorphism (AFLP)-fingerprinting to determine the source population of D. polymorpha in Spain. The phylogenetic analyses and pair-wise genetic distances revealed that the recent invasion of zebra mussels in Spain is most likely from France.     

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.     

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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