The Ponto-Caspian Quagga Mussel, Dreissena Rostriformis Bugensis (Andrusov, 1897), Invades Great Britain

Aquatic Invasions (2014) Volume 9, Issue 4: 529–535 doi: http://dx.doi.org/10.3391/ai.2014.9.4.11 Open Access

Research Article

The Ponto-Caspian quagga mussel, Dreissena rostriformis bugensis (Andrusov, 1897), invades Great Britain

David C. Aldridge1*, Samantha Ho2 and Elsa Froufe3 1Aquatic Ecology Group, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EK, UK 2Environment Agency, Apollo Court, 2 Bishops Square Business Park, Hatfield A110 9EX, UK 3Aquatic Ecology and Evolution Group, CIMAR/CIIMAR, University of Porto, 4050-123 Porto, Portugal E-mail: [email protected] (DCA), [email protected] (SH), [email protected] (EF) *Corresponding author

Received: 28 October 2014 / Accepted: 19 November 2014 / Published online: 26 November 2014 Handling editor: Frances Lucy

Abstract

Great Britain has been subject to an increasing rate of invasion from freshwater species of Ponto-Caspian origin. A recent horizon-scan of potential invaders into Great Britain named the Ponto Caspian quagga mussel, Dreissena rostriformis bugensis (Andrusov, 1897), as the non-native species least wanted. On 29th September 2014 quagga mussels were discovered in the Wraysbury River, Surrey, during a routine kick sample collected by the Environment Agency. Identity was confirmed using genetic markers (Cytochrome Oxidase I - COI) on five individuals encompassing a broad morphological variation. The absence of very large individuals (max. length 16 mm), absence of shells and absence of quagga mussels in samples collected during March 2014 point toward a recent invasion. The quagga mussels were found attached to submerged rocks, vegetation, bridge walls and shells of zebra mussels, Dreissena polymorpha (Pallas, 1771). The collection site is a small (<5m wide), shallow (<50cm deep) stream that is not navigable or regularly fished. This suggests that the species is more widely distributed than the current location, because such a system is unlikely to be the point of introduction. The shallow depth (30cm) in open water at which quagga mussels were abundant is surprising given that zebra mussels have failed to establish in such habitats, despite being present in the catchment for over 100 years. Previously published models predict quagga mussels will establish widely across England, western and southern Wales and central Scotland. The high abundance and inter-connectivity of waterways adjacent to the Wraysbury River suggest further spread is likely. Containment through national biosecurity measures (e.g. ‘Check, Clean, Dry’ of boats and equipment, as promoted by the UK Environment Agency) is recommended, although ultimately it can be assumed that quagga mussels will cause similar widespread ecological and economic harm in Britain as has been experienced in invaded regions of Western Europe and North America. Key words: dreissenind, invasive, zebra mussel, Wraysbury, alien, non-native, first record

Introduction Recent studies suggest that The Netherlands contains over 20 Ponto-Caspian freshwater In recent years, there has been a dramatic spread species that have yet to be found in Great Britain of Ponto-Caspian species into Western Europe. (Gallardo and Aldridge 2013a). One of the species This spread has been facilitated by the construction of greatest concern to Britain’s freshwaters is the of canals which have linked different river quagga mussel, Dreissena rostriformis bugensis systems. Canal construction has not only provided (Andrusov, 1897), which was identified as the improved trade routes but has also created a species that posed the greatest risk to Britain’s number of invasion corridors from east to west biodiversity in a recent multi-taxon, multi- (Bij de Vaate et al. 2002). Many of these new ecosystem horizon scan (Roy et al. 2014). Until species have driven major ecological changes the early twenty-first century the quagga mussel and caused considerable economic harm. The was a slower invader than the congeneric Ponto- predominance of facilitative and commensal Caspian zebra mussel Dreissena polymorpha interactions between Ponto-Caspian species (Pallas, 1771), a species that already costs Britain heightens their invasive potential and threatens approximately £5 million per year (Oreska and to drive an ‘invasional meltdown’ (Gallardo and Aldridge 2011) and threatens native biota (Aldridge Aldridge 2014). et al. 2004; Sousa et al. 2010; Sousa et al. 2011).

529 D.C. Aldridge et al.

The original native range of the quagga mussel is fast flow, and areas with macrophyte substrate the Lower Dnieper River and Southern Bug onto which zebra mussels preferentially attach River (Son 2007). However, over the last few (Diggins et al. 2004). In Western Europe, quagga decades the quagga mussel has considerably mussels have been found to displace zebra extended its range, establishing widely in Russia, mussels at a rate of 26 to 36 % per year (Heiler North America and Western Europe (Van der et al 2012, 2013). In Russia, the lag for quagga Velde et al. 2007) and is now spreading at a rate mussels to replace zebra mussels is estimated to in Western Europe that far exceeds that of the be 5–10 years (Orlova et al. 2004). zebra mussel (Matthews et al. 2014). The possession of a bysuss means that quagga Quagga mussels will affect invaded ecosystems mussels also represent a considerable biofouling in a number of ways. Clearer waters resulting risk. By attaching to one-another quagga mussels from massive filtration capacity (Cross et al. 2010) can block raw water pipes in irrigation systems, will lead to changes in algal diversity and power plants and water treatment facilities. In abundance. Selective removal of green algae by North America, Connelly et al. (2007) estimated dreissenids can reduce cyanobacteria from the combined economic cost of quagga and zebra competition and lead to toxic blooms (MacIsaac mussels to the water and power industries to be et al. 1996). Grazing of algae by quagga mussels $US 161 – 467 million between 1989 and 2004. was estimated to match that of zooplankton in On 29th September 2014 a routine macro- Lake Erie, USA (Zhang et al. 2011) and may invertebrate sample (three minute kick sample) explain the significant declines in biomass of collected by the Environment Agency found cyclopoid copepods in Lake Ontario following specimens of a dreissenid in the Wraysbury mussel invasion (Bowen et al. 2011). The abundance River, Surrey, UK (51˚26.55′N, 00˚31.25′W). of ciliates, Daphnia and rotifers reduced by 39, Similar sampling conducted at the same site in 40 and 45 % respectively in Lake Michigan March 2014 did not record the presence of following dreissenid invasion (Kissman et al. dreissenids. This paper reports the results of 2010). preliminary investigations into the identity, Nalepa et al. (2009) found that offshore benthic population structure, origins and potential spread communities in Lake Michigan experienced a of this dreissenid. major shift following the invasion of quagga mussels, with the replacement of native amphipods with the new mussel. A meta-analysis Materials and methods of benthic macroinvertebrate communities following Dreissena invasions (Ward and Riciardi 2007) Study site suggests that following invasion, there is an increase The Wraysbury River is a small (<5 m width), in benthic density and taxonomic richness, but a shallow (<50 cm depth), slow-flowing stream reduced evenness. There were positive effects on with a benthos dominated by gravel. Monthly densities of scrapers and predators (especially records collected by the Environment Agency for leeches, flatworms and mayflies), but reductions 2013 give mean water chemistry parameters of in large snails, sphaeriid clams, unionid mussels pH 8.10, Conductivity 845.5 µS/cm, Dissolved and burrowing amphipods. Gammarid amphipods Oxygen 10.49 mg/l, Temperature 11.58 ˚C, Total showed a positive response, and this may reflect Oxidised Nitrogen 8.24 N mg/l, Alkalinity their tendency to gain shelter from the mussels’ 229.63 mg/l CaCO3. The river forms part of the shells (Madgwick and Aldridge 2011). A decline in River Colne system, and is surrounded by a unionid mussels through quagga mussel fouling complex network of canals and ditches that has been reported by Schloesser et al. (2006). ultimately feed into the River Thames. The adjacent Throughout its invaded range, quagga mussels landscape contains water storage reservoirs and have been seen to replace zebra mussels in most numerous flooded gravel pits which house dive habitats (Wilson et al. 2006; Van der Velde et al. centres, sailing clubs and angling clubs. 2010). This has been attributed to the quagga mussel’s lower respiration rates, greater shell Morphology growth, greater shell mass, faster filtration rates and greater assimilation efficiency (Diggins 2001; Specimens collected from the Wraysbury River Baldwin et al. 2002; Stoeckmann 2003). Zebra at the point of first discovery were identified mussels appear to find refugia from quagga using external and internal shell characteristics mussels in certain habitats, including those with by reference to Mackie and Claudi (2009).

530 Quagga mussels in Great Britain

DNA extraction, amplification and sequencing In order to confirm the species identification using genetic markers, five animals were collected from the Wraysbury River at the point of first discovery and fixed in 96% ethanol in the field. Whole genomic DNA from each mussel was isolated using the Jetquick tissue DNA Spin Kit (Genomed) following the manufacturer’s protocol. A fragment of the cytochrome oxidase c subunit I gene (COI) was amplified by PCR using universal primer modified versions, i.e., LCO22me2 and HCO700dy2 (Walker et al. 2006, 2007). The PCR conditions (25 µL reactions) were as follows: each reaction contained 2.5 µL 10x Figure 1. External shell morphology of a typical quagga mussel Invitrogen PCR Buffer, 0.5 µL 10mM of each specimen from Wraysbury River. a) Ventral view showing waved primer, 1.5 µL 50mM MgCl2, 0.5 µL 10mM valve margin and small byssal groove; b) Right lateral view dNTP’s, 0.1 µL Invitrogen Taq DNA Polymerase showing rounded posterior margin and banding rather than the and approximately 1 µL DNA template. The zig-zag pattern seen in zebra mussels; c) Anterior view showing deep, rounded keel rather than the shallow, angular keel found in cycle parameters were: initial denaturation at zebra mussels. Photographs by David Aldridge. 94ºC for 3 min, denaturation at 94ºC (30 s), annealing at 50ºC (40 s) and extension at 72ºC (60 s) repeated for 38 cycles and a final extension at 72ºC of 10 min. Amplified DNA templates were purified and sequenced (forward and reverse) by a commercial company, Macrogen, using the same primers.

Habitat and population structure A 100m stretch of the Wraysbury River at the point of first discovery was surveyed on 30th September 2014. To assess population structure all mussels encountered were collected during a ten minute hand sample whilst wading within the channel. All available habitat (e.g. bridge supports, Figure 2. Size-frequency distribution of quagga mussels in the gravel, boulders, submerged vegetation, plastic Wraysbury River. ‘Length’ is maximum length (mm) from debris) was sampled in proportion to its relative anterior to posterior shell margin, measured with vernier callipers. Mussels were collected by hand from all available substrates in abundance. Each collected mussel was measured proportion to their abundance in the river channel. Inset shows a along its longest axis using Vernier Callipers. growth series of quagga mussels from the survey site.

Results Morphology Dreissena rostriformis bugensis sequences from GenBank were downloaded and the final The species was identified as the quagga mussel, alignment revealed that the new sequences from D. rostriformis bugensis, based on key external this study are indeed Dreissena rostriformis and internal shell characteristics (Mackie and bugensis (GenBank accession number KP057252). Claudi 2009; Figure 1) Habitat and population structure Genetic verification Live quagga mussels were small in size, but Both forward and reverse sequences from the ranged in length from 3 to 16 mm, with a modal five specimens were aligned, and no indels and length of 13mm (Figure 2). Live mussels were no stop codons were observed, after translating found attached to bridge walls, boulders, plastic all sequences to amino acids. All available debris, submerged wood, and the shells of other

531 D.C. Aldridge et al.

Figure 3. Habitat within the Wraysbury River. a) Shallow, narrow stream channel with shallow depth (30cm) and bottom- rooting macrophytes such as Sparganium and Ranunculus; b) Quagga mussels attached to surface of a boulder; c) Quagga mussel attached to a submerged tree branch; d) Quagga mussel attached to the empty shell of a zebra mussel. Photographs by David Aldridge.

bivalves (Figure 3). Even in open water, live from UV light and so this could explain their specimens could be found on the underside of persistence in the river once the river returned to cobbles at water depths of 20–30 cm. No empty typical depth conditions of ca. 30 cm. shells were found, except above the water line where shells still attached to walls and boulders Date of arrival had apparently been stranded during falling water levels. The small size of the quagga mussels in the Wraysbury River (16mm maximum length), combined with the absence of empty shells and Discussion the lack of records during the Environment Agency’s March 2014 survey suggests that the Habitat mussels entered the river during late 2013 or early 2014. This is further supported by data It is surprising that the Wraysbury River has from Lake Mead, USA, where the annual growth been colonised by quagga mussels; zebra mussels rate of juvenile quagga mussels is between 13 have been present in the region for over 200 and 19 mm (Wong et al. 2012). Well-established years (Aldridge 2010) and yet have not established quagga mussel populations show a maximum in the river. Dreissenid veliger larvae are highly length of 35mm in North American systems sensitive to UV radiation (Wright 1998), and this (Mills et al. 1999). Maximum lengths reported typically precludes them from establishing in for Western Europe are typically smaller, with shallow waters such as those found at the 27 mm reported for the Meuse River (Matthews Wraysbury River. It is possible that the quagga et al. 2012). mussel veligers entered the system and established during the unprecedented floods of the Wraysbury Origins River during winter/spring 2013/14, during which the water was especially turbid and had a The current distribution and origin of the quagga recorded maximum depth of 70 cm (Environment mussels in the Wraysbury River remains unclear. Agency, Wraysbury River Gauging Station). Once The river is very small, has limited public access, dreissenid mussels have settled and formed their is not routinely fished and is not navigable. It is shell valves they become relatively protected therefore likely that the mussels entered the

532 Quagga mussels in Great Britain system from elsewhere, and that the population Options for management and control is not localised to the Wraysbury River. The Given the potential ecological and economic Wraysbury River forms part of a highly inter- impacts that quagga mussels could have in connected system of streams, rivers and canals, Britain’s freshwaters, it is desirable to consider including the River Thames and River Colne. whether tools are available for containment. If The immediate area is also occupied by a number the population is localised, eradication from the of large, inter-linked water storage reservoirs and Wraysbury River may be possible through isolation flooded gravel pits that house sailing clubs and and draining (Ricciardi et al.1995) or by dosing diving clubs. Further surveys are required to the water column with degradable control agents, better understand the distribution of the mussel. such as BioBullets (Aldridge et al. 2006) or Molecular analyses of this population and others Zequanox® (Meehan et al. 2014). Whilst any are needed to help identify the possible origins of control strategy is likely to have consequential this invasion event. deleterious impacts on non-target biota, this might be a short-term consequence worth embracing. Potential spread and impacts However, decision on any control strategy requires The large number of adjacent waterways may not the ecological and economic costs and benefits only provide a possible source for the mussel, it to be balanced against the potential for re-invasion also provides a considerable risk for future (Caffrey et al. 2014). On a more practical level, spread. This is exacerbated by the potential of there is certainly a place for increased biosecurity the Wraysbury River to flood into nearby rivers measures to limit spread into other waterbodies. and gravel pits. Perhaps of greatest concern is Transmission upon waders, boats and fishing the River Thames, into which the Wraysbury flows. gear can be reduced through the standardised The Thames has been identified as a hotspot for check, clean, dry procedures already promoted in freshwater invaders (Gallardo and Aldridge Britain’s freshwaters (http://www.nonnativespecies. 2013a, b; Jackson and Grey 2013), including many org/checkcleandry/). Additional protection can be Ponto-Caspian species, and this further increases offered by exposing equipment to water at 50 ˚C the potential for invasional meltdown (Gallardo for 20 seconds (Comeau et al. 2011). and Aldridge 2014). The River Thames also serves as a major corridor for transport into the wider Acknowledgements British river and canal network (Aldridge 2010). A number of industries draw raw water from the Financial support for the genetic analyses and publication costs River Thames, including water treatment works was provided by the Environment Agency, UK. Additional and power plants, and these have already support for genetic analyses came from the Portuguese Foundation for Science and Technology (FCT) project experienced high levels of costly biofouling from PTDC/AAC-AMB/117688/2010. We are grateful to Colette Sales zebra mussels (Elliott et al. 2005; Oreska and and Trevor Renals, Environment Agency, for their provision of Aldridge 2010). data and helpful comments on the manuscript. Two anonymous Bioclimatic models suggest there is wide referees and Frances Lucy provided helpful comments which strengthened the manuscript. habitat suitability within Great Britain for quagga mussels to establish (Gallardo and Aldridge 2013a). It can be assumed that the widespread References distribution of zebra mussels in Britain will be similarly matched by quagga mussels, which will Aldridge DC (2010) The zebra mussel in Britain: history of spread and impacts. In: Van der Velde G, Rajagopal S, Bij de replace the zebra mussels in many sites. Distribution Vaate A (eds), The Zebra Mussel in Europe. Backhuys is likely to include much of England, western Publishers, Leiden, pp 79–93 and southern Wales and central Scotland. Quagga Aldridge DC, Elliott P, Moggridge GD (2006) Microencapsulated mussels favour lentic systems, such as reservoirs BioBullets for the control of biofouling zebra mussels. Environmental Science and Technology 40: 975–979, and lakes. They are not found in fast flowing http://dx.doi.org/10.1021/es050614+ rivers, but canals provide ideal habitats. British Aldridge DC, Elliott P, Moggridge GD (2004) The recent and freshwaters provide a wealth of suitable hard rapid spread of the zebra mussel (Dreissena polymorpha) in substrates which have already been seen to support Great Britain. Biological Conservation 119: 253–261 Baldwin BS, Mayer MS, Dayton J (2002) Comparative growth the widespread establishment of zebra mussels. and feeding in zebra and quagga mussels (Dreissena As populations establish, shell material enables polymorpha and Dreissena bugensis): implications for North expansion into muddy substrates (Bially and American lakes. Canadian Journal of Fisheries and Aquatic MacIsaac 2000). Sciences 59: 680–694, http://dx.doi.org/10.1139/f02-043

533 D.C. Aldridge et al.

Bially A, MacIsaac HJ (2000) Fouling mussels (Dreissena spp.) Heiler KCM, Brandt S, Albrecht C, Hauffe T, Wilke T (2012) A colonize soft sediments in Lake Erie and facilitate benthic new approach for dating introduction events of the quagga invertebrates. Freshwater Biology 43: 85–97, http://dx.doi.org/ mussel (Dreissena rostriformis bugensis). Biological Inva- 10.1046/j.1365-2427.2000.00526.x sions 14: 1311–1316, http://dx.doi.org/10.1007/s10530-011-0161-1 Bij de Vaate A, Jazdzewski K, Ketelaars HAM, Gollasch S, Van Jackson MC, Grey J (2013) Accelerating rates of freshwater der Velde G (2002) Geographical patterns of range extension invasions in the catchment of the River Thames. Biological of Ponto-Caspian macroinvertebrate species in Europe. Invasions 15: 945–951, http://dx.doi.org/10.1007/s10530-012-0343-5 Canadian Journal of Fisheries and Aquatic Sciences 59: Kissman CEH, Knoll LB, Sarnelle O (2010) Dreissenid mussels 1159–1174 (Dreissena polymorpha and Dreissena bugensis) reduce Bowen KL, Johannsson OE (2011) Changes in zooplankton microzooplankton and macrozooplankton biomass in biomass in the Bay of Quinte with the arrival of the mussels, thermally stratified lakes. Limnology and Oceanography 55: Dreissena polymorpha and Dreissena rostiformis bugensis, 1851–1859, http://dx.doi.org/10.4319/lo.2010.55.5.1851 and the predatory cladoceran, Cercopagis pengoi: 1975 to MacIsaac HJ (1996) Potential abiotic and biotic impacts of Zebra 2008. Aquatic Ecosystem Health and Management 14: 44– mussels on the inland waters of North America. American 55, http://dx.doi.org/10.1080/14634988.2011.550528 Zoologist 36: 287–299 Caffrey JM, Baars J-R, Barbour JH, Boets P, Boon P, Davenport Mackie GL, Claudi R (eds) (2009) Monitoring and control of K, Dick JTA, Early J, Edsman L, Gallagher C, Gross J, macrofouling mollusks in fresh water systems, Second Heinimaa P, Horrill C, Hudin S, Hulme PE, Hynes S, Edition. CRC Press, Boca Raton, FL, 508 pp, http://dx.doi.org/ MacIsaac HJ, McLoone P, Millane M, Moen TL, Moore N, 10.1201/9781439804414 Newman J, O’Conchuir R, O’Farrell M, O’Flynn C, Madgwick G, Aldridge DC (2011) Killer shrimps in Britain: hype Oidtmann B, Renals T, Ricciardi T, Roy H, Shaw R, van or horror? British Wildlife 22: 402–412 Valkenburg JLCH, Weyl O, Williams F, Lucy FE (2014) Matthews J, Van der Velde G, Bij de Vaate A, Collas FPL, Tackling Invasive Alien Species in Europe: the Top 20 Koopman KR, Leuven RSEW (2014) Rapid range expansion Issues. Management of Biological Invasions 5: 1–20, of the invasive quagga mussel in relation to zebra mussel http://dx.doi.org/10.3391/mbi.2014.5.1.01 presence in The Netherlands and Western Europe. Biological Comeau S, Rainville S, Baldwin W, Austin E, Gerstenberger S, Invasions 16: 23–42, http://dx.doi.org/10.1007/s10530-013-0498-8 Cross C, Wong H (2011) Susceptibility of quagga mussels Matthews J, Van der Velde G, Bij de Vaate A, Leuven RSEW (Dreissena rostriformis bugensis) to hot-water sprays as a (2012) Key factors for spread, impact and management of means of watercraft decontamination. Biofouling 27: 267– quagga mussels in The Netherlands. Reports Environmental 274, http://dx.doi.org/10.1080/08927014.2011.564275 Science 404. Radboud University, Nijmegen, 120 pp Connelly NA, O’Neill CR, Knuth BA, Brown TL (2007) Meehan S, Gruber B, Lucy FE (2014) Zebra mussel control using Economic impacts of zebra mussels on drinking water Zequanox® in an Irish waterway. Management of Biological treatment and electric power generation facilities Invasions 5: 279–286, http://dx.doi.org/10.3391/mbi.2014.5.3.11 Environmental Management 40: 105–112, http://dx.doi.org/ Mills EL, Chrisman JR, Baldwin B, Owens RW, O’Gorman R, 10.1007/s00267-006-0296-5 Howell T, Roseman EF, Raths MK (1999) Changes in the Cross CL, Wong WH, Che TD (2010) Estimating carrying Dreissenid Community in the Lower Great Lakes with capacity of quagga mussels (Dreissena rostriformis bugensis) Emphasis on Southern Lake Ontario. Journal of Great Lakes in a natural system: A case study of the Boulder Basin of Research 25: 187–197, http://dx.doi.org/10.1016/S0380-1330(99) Lake. Aquatic Invasions 6: 141–147, http://dx.doi.org/10.3391/ 70727-6 ai.2011.6.2.03 Nalepa TF, Fanslow DL, Lang GA (2009) Transformation of the Diggins TP (2001) A seasonal comparison of suspended sediment offshore benthic community in Lake Michigan: recent shift filtration by quagga (Dreissena bugensis) and zebra (D. from the native amphipod Diporeia spp. to the invasive polymorpha) mussels. Journal of Great Lakes Research 27: mussel Dreissena rostriformis bugensis. Freshwater Biology 457–466, http://dx.doi.org/10.1016/S0380-1330(01)70660-0 54: 466–479, http://dx.doi.org/10.1111/j.1365-2427.2008.02123.x Diggins TP, Weimer M, Stewart KM, Baier RE, Meyer AE, Oreska MP, Aldridge DC (2010) Estimating the financial costs of Forsberg RF, Goehle MA (2004) Epiphytic refugium: are two freshwater invasive species in Great Britain: a standardized species of invading freshwater bivalves partitioning spatial approach to invasive species costing Biological Invasions resources? Biological Invasions 6: 83–88, http://dx.doi.org/ 13: 305–319, http://dx.doi.org/10.1007/s10530-010-9807-7 10.1023/B:BINV.0000010124.00582.d3 Orlova MI, Muirhead JR, Antonov PI, Scherbina GK, Elliott P, Aldridge DC, Moggridge GD, Chipps M (2005) The Starobogatov YI, Biochino GI, Therriault TW, MacIsaac HJ increasing effects of zebra mussels on water installations in (2004) Range expansion of quagga mussels Dreissena England. Water and Environment Journal 19: 367–375 rostriformis bugensis in the Volga River and Caspian Sea Gallardo B, Aldridge DC (2013a) Priority setting for invasive basin. Aquatic Ecology 38: 561–573, http://dx.doi.org/10.1007/ species management: risk assessment of Ponto-Caspian s10452-004-0311-y invasive species into Great Britain. Ecological Applications Ricciardi A, Serrouya R, Whoriskey FG (1995) Aerial exposure 23: 352–364, http://dx.doi.org/10.1890/12-1018.1 tolerance of zebra and quagga mussels (Bivalvia, Gallardo B, Aldridge DC (2013b) The ‘dirty dozen’: socio- Dreissenidae) – implications for overland dispersal. economic factors amplify the invasion potential of high risk Canadian Journal of Fisheries and Aquatic Sciences 52: aquatic invasive species in Great Britain and Ireland. Journal 470–477, http://dx.doi.org/10.1139/f95-048 of Applied Ecology 50: 757–766, http://dx.doi.org/10.1111/1365- Roy HE, Peyton J, Aldridge DC et al. (2014) Horizon scanning 2664.12079 for invasive alien species with the potential to threaten Gallardo B, Aldridge DC (2014) Is Great Britain heading for a biodiversity in Great Britain. Global Change Biology 20: Ponto-Caspian Invasional Meltdown? Journal of Applied 3859–3871, http://dx.doi.org/10.1111/gcb.12603 Ecology, http://dx.doi.org/10.1111/1365-2664.12348 Schloesser DW, Metcalfe-Smith JL, Kovalak WP, Longton GD, Heiler KCM, Bij de Vaate A, Ekschmitt K, von Oheimb PV, Smithee RD (2006) Extirpation of freshwater mussels Albrecht C, Wilke T (2013) Reconstruction of teh early (Bivalvia: Unionidae) following the invasion of dreissenid invasion history of the quagga mussel (Dreissena rostriformis mussels in an interconnecting river of the Laurentian Great bugensis) in Western Europe. Aquatic Invasions 8: 53–57, Lakes. American Midland Naturalist 155: 307–320, http://dx.doi.org/10.3391/ai.2013.8.1.06 http://dx.doi.org/10.1674/0003-0031(2006)155[307:EOFMBU]2.0.CO;2

534 Quagga mussels in Great Britain

Son M (2007) Native range of zebra mussel and quagga mussel Walker JM, Bogan AE, Bonfiglio EA, Campbell DC, Christian and new data on their invasions within the Pontocaspian AD, Curole JP, Harris JL, Wojtecki RJ, Hoeh WR (2007) region. Aquatic Invasions 3: 174–184, http://dx.doi.org/10.3391/ Primers for amplifying the hypervariable, male-transmitted ai.2007.2.3.4 COII-COI junction region in amblemine freshwater mussels Sousa R, Gutierrez JL, Aldridge DC (2010) Non-indigenous (Bivalvia: Unionoidea: Ambleminae). Molecular Ecology invasive bivalves as ecosystem engineers Biological Notes 7: 489–491, http://dx.doi.org/10.1111/j.1471-8286.2006. Invasions 11: 2367–2385, http://dx.doi.org/10.1007/s10530-009- 01630.x 9422-7 Ward JM, Ricciardi A (2007) Impacts of Dreissena invasions on Sousa R, Pilotto F, Aldridge DC (2011) Fouling of European benthic macroinvertebrate communities: a meta-analysis freshwater bivalves (Unionidae) by the invasive zebra mussel Diversity and Distributions 13: 155–165, http://dx.doi.org/10. (Dreissena polymorpha). Freshwater Biology 56: 867–876, 1111/j.1472-4642.2007.00336.x http://dx.doi.org/10.1111/j.1365-2427.2010.02532.x Wilson KA, Howell ET, Jackson DA (2006) Replacement of Stoeckmann A (2003) Physiological energetics of Lake Erie zebra mussels by quagga mussels in the Canadian nearshore dreissenid mussels: a basis for the displacement of Dreissena of Lake Ontario: the importance of substrate, round goby polymorpha by Dreissena bugensis. Canadian Journal of abundance, and upwelling frequency. Journal of Great Lakes Fisheries and Aquatic Sciences 60: 126–134, http://dx.doi.org/ Research 32: 11–28, http://dx.doi.org/10.3394/0380-1330(2006) 10.1139/f03-005 32[11:ROZMBQ]2.0.CO;2 Van der Velde G, Platvoet D (2007) Quagga mussels Dreissena Wong WH, Gerstenberger S, Baldwin W, Moore B (2012) rostriformis bugensis (Andrusov, 1897) in the Main river Settlement and growth of quagga mussels (Dreissena (Germany). Aquatic Invasions 2: 261–264, http://dx.doi.org/ rostriformis bugensis Andrusov, 1897) in Lake Mead, 10.3391/ai.2007.2.3.11 Nevada-Arizona, USA. Aquatic Invasions 7: 7–19, Van der Velde G, Rajagopal S, Bij de Vaate A (2010) From zebra http://dx.doi.org/10.3391/ai.2012.7.1.002 mussel to quagga mussels: an introduction to the Wright DA (1998) The use of high energy monochromatic UV Dreissenidae. Chapter 1. In: Van der Velde G, Rajagopal S, light to kill dreissenid larvae: In Proceedings of the Sixth Bij de Vaate A (eds), The Zebra Mussel in Europe. Backhuys International Zebra Mussel and Other Aquatic Nuisance Publishers, Leiden, pp 1–10 Species Conference, Dearborn, USA, pp 467–476 Walker JM, Curole JP, Wade DE, Chapman EG, Bogan AE, Zhang H, Culver DA, Boegman L (2011) Dreissenids in Lake Watters GT, Hoeh WR (2006) Taxonomic distribution and Erie: an algal filter or a fertilizer? Aquatic Invasions 6: 175– phylogenetic utility of gender-associated mitochondrial 194, http://dx.doi.org/10.3391/ai.2011.6.2.07 genomes in the Unionoida (Bivalvia). Malacologia 48: 265– 282

535