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.     

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.     

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.     

The filtration rate of the zebra mussel Dreissena polymorpha used for water quality assessment in Dutch rivers

The effects of contaminated river water on the filtration rate of zebra mussels from a clean reference site were studied. After a 48-h exposure period to filtered water from the rivers Rhine, Meuse and Amstel (The Netherlands), the filtration rate was measured. It was demonstrated that water from contaminated locations inhibited the filtration rate. Inhibition was higher during low water levels in the rivers Rhine and Meuse than during high water levels, suggesting that contaminants are diluted during high water levels. It is concluded that the shortterm filtration assay with D. polymorpha can be used for assessing water quality.     

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.     

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.     

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.     

Overland transport of recreational boats as a spreading vector of zebra mussel <Emphasis Type="Italic">Dreissena polymorpha</Emphasis>

In aquatic ecosystems invasive species are among the most important threats to biodiversity worldwide. Understanding the dispersal mechanisms of aquatic invaders is very important for protection and management of vulnerable water bodies. Here we ask how recreational boats that are transported overland could contribute to the dispersal of invasive zebra mussels among lakes in Switzerland. Using a questionnaire sent to registered boat owners, we surveyed properties of transported boats and collected information on self-reported mussel fouling and transport activities of boat owners. We also sampled boat hulls at launching ramps and harbors for biofouling invertebrates. Boats that were kept seasonally or year-round in water were found to have high vector potential with mussel fouling rates of more than 40 %. However, only about 6 % of boats belonging to these groups were transported overland to other water bodies. Considering that approximately 100,000 recreational boats are registered in Switzerland, we estimated that every year around 1400 boats fouled with mussels are transported overland. Such boats pose a high risk of distributing zebra mussels between water bodies. Our results suggest that there is a considerable risk that recreational boats may spread new fouling species to all navigable water bodies within the study area. We speculate that one such species could be the quagga mussel, which has not yet invaded lakes in Switzerland. On a more positive note, our study has identified the group of high-risk boats so that possible control measures would only affect a relatively small number of boat owners.     

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.     

Predicting zebra mussel fouling on native mussels from physicochemical variables

1. Predictive models of impact are needed for the risk assessment of invasive species. One such species is the Eurasian zebra mussel ( Dreissena polymorpha ), a fouling bivalve that overgrows and kills native mussels (Unionidae) in many North American lakes and rivers. The level of mortality in a native mussel population increases with the fouling intensity – i.e. the mean number of zebra mussels attached to each native mussel.
2. We conducted a multi-site survey within the St Lawrence and Richelieu rivers (Quebec, Canada) to determine whether zebra mussel fouling intensity can be predicted from environmental variables. We found fouling intensity to be positively correlated with calcium concentration [Ca²⁺] and negatively correlated with sediment size, but not affected by local macrophyte cover.
3. A multiple regression model that includes calcium concentration and sediment size explains 86% of variation in fouling intensity across all sites.
4. Analysis of data from invaded sites in North America and Europe revealed a nonlinear relationship in which fouling intensity increases with calcium concentration up to an asymptotic threshold of 24 mg L⁻¹ Ca²⁺.
5. Our results suggest that the community-level impacts of zebra mussels are mediated by abiotic environmental variables and gradients in these variables may provide local habitat refugia for native mussels.     

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.     

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

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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.     

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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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.     

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.     

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.     

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

Summary

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

The status of the freshwater pearl mussel <Emphasis Type="Italic">Margaritifera margaritifera</Emphasis> in Scotland: extent of change since 1990s,threats and management implications

All known rivers in Scotland with recent records of freshwater pearl mussels Margaritifera margaritifera were surveyed in 2013–2015 using a standard methodology. Freshwater pearl mussel populations were classed as: (i) apparently extinct in 11 rivers, (ii) not successfully recruiting in 44 rivers, and (iii) evidence of recent successful recruitment in 71 rivers. On a regional basis, a high proportion of extant populations were located in North and West Scotland. In all regions extant populations were characterised by low pearl mussel densities, with 97 of 115 extant Scottish populations defined as ‘rare’ (0.1–0.9 mussels per 1 m ²) or ‘scarce’ (1.0–9.9 mussels per 1 m ²). Only 18 Scottish rivers now hold pearl mussel populations in densities that are considered to be ‘common’ (10–19.9 mussels per 1 m ²) or ‘abundant’ (>20 mussels per 1 m ²). Based on survey evidence, the number of apparently extinct pearl mussel populations in Scottish rivers is now 73. The decline is particularly pronounced in the West Highlands and Western Isles strongholds. The key threats are: (i) pearl fishing, (ii) low host fish densities, (iii) pollution/water quality, (iv) climate change and habitat loss, (v) hydrological management/river engineering and (vi) ‘other factors’, such as non-native invasive species. Over the last 100 years this endangered species has been lost from much of its former Holarctic range. Scotland’s extant M. margaritifera populations continue to be of international importance, but their continued decline since the first national survey in 1998 is of great concern.     

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.