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AMER. ZOOL., 36:271-286 (1996) A Review of the Biology and Ecology of the Quagga Mussel (Dreissena bugensis), a Second Species of Freshwater Dreissenid Introduced to North America’ EDWARD L. MILLS Department of Natural Resources, Cornell Biological Field Station, 900 Shackelton Point Road, Bridgeport, New York 13030 GARY ROSENBERG The Academy of Natural Sciences, 1900 Benjamin Franklin Parkway, Philadelphia, Pennsylvania 19103 ADRIAN P. SPIDLE School of Fisheries HF-10, University of Washington, Seattle, Washington 98195 MICHAEL LUDYANSKIY Lonaz Inc., Research and Development, P.O. Box 993, Annandale, New Jersey 08801 YURI PLIGIN Institute of Hydrobiology, Kiev, Ukraine AND BERNIE MAY Genome Variation Analysis Facility, Department of Natural Resources, Fernow Hall, Cornell University, Ithaca, New York 14853 SYNOPSIS. North America’s Great Lakes have recently been invaded by two genetically and morphologically distinct species of Dreissena. The zebra mussel (Dreissena polymorpha) became established in Lake St. Clair of the Laurentian Great Lakes in 1986 and spread throughout eastern North America. The second dreissenid, termed the quagga mussel, has been identified as Dreissena bugensis Andrusov, 1897. The quagga occurs in the Dnieper River drainage of Ukraine and now in the lower Great Lakes of North America. In the Dnieper River, populations of D. poly- morpha have been largely replaced by D. bugensis; anecdotal evidence indicates that similar trends may be occurring in the lower Laurentian Great Lakes. Dreissena bugensis occurs as deep as 130 m in the Great Lakes, but in Ukraine is known from only 0-28 m. Dreissena bugensis is more abundant than D. polymorpha in deeper waters in Dneiper River reservoirs. The conclusion that North American quagga mussels have a lower thermal maximum than zebra mussels is not supported by obser- vations made of populations in Ukraine. In the Dnieper River drainage, quagga mussels are less tolerant of salinity than zebra mussels, yet both dreissenids have acclimated to salinities higher than North American pop- ulations; eventual colonization into estuarine and coastal areas of North America cannot be ignored. 1 From the Symposium Biology, Ecology and Physiology of Zebra Mussels presented at the Annual Meeting of the American Society of Zoologists, 4-g January 1995, at St. Louis, Missouri. 271 272 E. L. MILLS ET AL. INTRODUCTION ics of Dreissena were poorly understood, with no clear consensus as to the number North America’s Great Lakes have re- of species in the genus nor their distribu- cently been invaded by two species of tions. As a result, biologists were not im- Dreissena (Rosenberg and Ludyanskiy, mediately able to determine the taxonomic 1994; Spidle et al., 1994). The zebra mussel identity of the quagga mussel. The quagga (Dreissena polymorpha) became estab- mussel was known to have originated in the lished in Lake St. Clair of the Laurentian Great Lakes by 1986 (Hebert et al., 1989) Old World, because variation at protein coding loci matched that of tissue samples and has spread rapidly from the Great from the Dnieper River, where only two Lakes eastward through the Mohawk and dreissenid species are present: Dreissena Hudson River systems and southward polymorpha and D. bugensis (Zhadin, through the Mississippi River drainage. In 1952). Rosenberg and Ludyanskiy (1994) August of 1991, specimens of a morpho- logically and genetically distinct Dreissena, reviewed the systematic literature on Dreis- sena and examined type material in the Pa- termed the quagga mussel, were discovered leontological Institute in Moscow. They in the Erie Canal and Lake Ontario where found that the quagga mussel corresponds they coexisted with more numerous D. to the original description and type speci- polymorpha (May and Marsden, 1992). The mens of D. bugensis Andrusov, 1897. Thus, quagga mussel, identified as Dreissena bug- genetic analysis and examination of the pri- ensis Andrusov, 1897 (Rosenberg and Lu- mary systematic literature firmly estab- dyanskiy, 1994; Spidle et al., 1994) has a lished the identity of the North American distinctive shell with convex ventral margin quagga mussel as D. bugensis (see review and lacks the carina between the ventral and by Marsden of genetics for Dreissena in lateral shell surfaces resulting in a rounded this volume). cross-section. Dreissena polymorpha has a Russian classifications have treated D. flat or concave ventral margin and pro- bugensis as a full species or as a subspecies nounced carina so that the ventral edge of of D. rostriformis Deshayes, 1838. Accord- the shell is perpendicular to the lateral, al- ing to Rosenberg and Ludyanskiy (1994) lowing the zebra mussel to remain upright living specimens of Dreissena bugensis can when placed on a flat surface. Although D. be distinguished from D. rostriformis by polymorpha is presently the prevailing spe- their larger size (reaching 38 mm compared cies in North America, D. bugensis has to 23 mm), more pronounced byssal largely replaced D. polymorpha in the groove, generally less compressed shell, Dnieper River drainage system in Ukraine and a distinct color pattern. Dreissena bug- (Pligin, 1979). In North America, the quag- ensis typically occurs in freshwater in Rus- ga mussel is primarily restricted to Lake sia in salinities up to 1 ppt (Nevesskaya, Erie, Lake Ontario and the St. Lawrence 1965) while D. rostriformis does not occur River although one sighting of D. bugensis in freshwater and is restricted to the middle has been confirmed outside the Great Lakes and southern Caspian Sea, in salinities up basin in the Mississippi River near St. Lou- to 12.7 ppt (Zhadin, 1952). While Marelli is, MO (O’Neill, 1995). (1991) recently suggested that D. bugensis This paper summarizes current informa- and D. polymorpha are synonymous, most tion about the taxonomy, geographic distri- recent authors consider them to belong to bution, genetics, physiology, and ecology different subgenera, and their fossil records of the quagga mussel (D. bugensis) and re- clearly indicate different lineages (Taktak- lates this information to other dreissenids in ishvili, 1973; Babak, 1983; Nuttall, 1990). North America and Ukraine when possible. The creation of putative zebra X quagga mussel hybrids in the laboratory by pooling IDENTIFICATION OF THE QUAGGA MUSSEL AS gametes collected after exposing adults to DREISSENA BUGENSIS serotonin has recently been reported, indi- At the time of the discovery of the quag- cating that interspecies fertilization events ga mussel in North America, the systemat- may be possible (Nichols and Black, 1994). BIOLOGY AND ECOLOGY OF QUAGGA MUSSELS 273 These putative hybrid larvae have not been 1989, D. bugensis spread approximately successfully reared, however, indicating 500 km northward, as well as east and south that their (1) viability may be limited or (2) through canals; it now occurs in almost all that these were single species haploid lar- large and medium Dnieper reservoirs in the vae. Evidence for species-specific sperm at- eastern and southern regions of Ukraine and tractants exists (Miller, 1994) suggesting the deltas of Dnieper River tributaries. Less that interspecific fertilization events may be information is available on the presence of rare in nature. Further, electrophoretic sur- D. bugensis in Dnieper River tributaries, veys of loci diagnostic between zebra and but it dominates the macrobenthos of small quagga mussels have failed to find evidence reservoirs on the Ros’ River, 200 km from of adult hybrids in natural populations in its confluence with the Dnieper River. Lake Ontario and Lake Erie (Spidle et al., Dreissena bugensis is absent from the del- 1995) suggesting that if interspecific fertil- tas of small rivers and estuaries on the ization does occur, and if offspring of those Black Sea to the west of the Dnieper-Bug fertilization events survive to adulthood, estuary (Moroz, 1993). The quagga has such hybrid individuals do not constitute a been reported in the Dniester River basin measurable proportion of the dreissenid (Shevtsova, personal communication, 1994) community. but is absent in the Danube River and its canals (Grossu, 1993). GEOGRAPHIC DISTRIBUTION The first sightings of the quagga mussel Two populations of D. bugensis are in the Laurentian Great Lakes were in Sep- known to exist in the world today, in the tember 1989, when one quagga was found Ukraine and the Laurentian Great Lakes. In near Port Colborne, Lake Erie (Fig. 2) the Dnieper River drainage of the Ukraine (Mills et al., 1993), although the recogni- (Fig. 1), D. bugensis was first discovered in tion of the quagga type as a distinct species the Bug portion of the Dnieper-Bug Estuary did not occur until 1991 (May and Mars- near Nikolaev by Andrusov (1890), who den, 1992). By the spring of 1993, the dis- named the species in 1897. Since the 1940s tribution of D. bugensis in the Laurentian the quagga mussel has spread into the Dnie- Great Lakes was from the central basin of per River drainage to regions that earlier Lake Erie to the St. Lawrence River at Que- had only D. polymorpha. Fig. 1 illustrates bec City. In 1992, quagga mussels were ab- the range expansion of D. bugensis in the sent in Lake St. Clair, the Detroit River, Dnieper and Bug River systems during the western Lake Erie, the Erie-Barge Canal, periods of 1950-53, 1970-73, and .1990- Oneida Lake, the Mohawk River, the Hud- 1992. Until the 1940s D. bugensis was son River, and Cayuga and Seneca Lakes of found only in the South Bug River and the New York’s Finger Lakes although these lower Ingulets River (Andrusov, 1890, water bodies all contained D. polymorpha 1897; Zhadin, 1952; Zhuravel’, 1951); it (Mills et al., 1993; Dermott and Munawar, was absent from both the Dnieper portion 1993). In the fall of 1994, however, the first of the Dnieper-Bug estuary and the lower quaggas were sighted on intake structures Dnieper River (Markovskiy, 1954; Olivari, of electric power generating stations in Ca- 1971; Moroz; 1993).

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