Introduction: The Biology, Ecology, and Physiology of Zebra Mussels 1

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1 AMER. ZOOL., 36: (1996) Introduction: The Biology, Ecology, and Physiology of Zebra Mussels 1 JEFFREY L. RAM Department of Physiology, Wayne State University, Detroit, Michigan AND ROBERT F. MCMAHON Center for Biological Macrofouling Research, Department of Biology, Box 19498, The University of Texas at Arlington, Arlington, Texas The papers in this issue of American Zoologist were originally presented in a symposium entitled, "The Biology, Ecology, and Physiology of Zebra Mussels," held 5 January 1995, at the American Society of Zoologists (ASZ) Annual Meeting in St. Louis, Missouri. The zebra mussel (Dreissena polymorpha), is an endemic, freshwater, European bivalve mollusc accidentally introduced into the North American Great Lakes. Introduction was most likely by release of larvae with ship ballast water into Lake St. Clair, near Detroit, Michigan in 1986 (Hebert et al., 1989). The zebra mussel's high fecundity, passively dispersed planktonic veliger larval stage, and ability to attach by proteinaceous byssal threads to boat and barge hulls, nets, buoys, and floating debris allowed it to spread rapidly throughout the lower Great Lakes and freshwater portions of the St. Lawrence River after its initial introduction (Fig. 1). It subsequently dispersed east through the Erie Canal, into the Hudson River, overland (by unintentional human mediated vectors) into the upper Susquehana River in New York, and south and west through the Illinois River into the Mississippi River near St. Louis. After entering the Mississippi River, the zebra mussel rapidly spread downstream to New Orleans, LA, and upstream to La Crosse, WI. It is now found in the lower portions of most major Mississippi River tributaries, including the Ohio, Tennessee, Cumberland, and 1 From the Symposium Biology, Ecology and Physiology of Zebra Mussels presented at the Annual Meeting of the American Society of Zoologists, 4 8 January 1995, at St. Louis, Missouri. 239 Arkansas Rivers, but not the Missouri River (Griffiths et al, 1991; Ram et al, 1992; McMahon, 1992; O'Neill and Dextrase, 1994) (Fig. 1). By the end of 1995, the zebra mussel had invaded waters in 20 of the 38 U.S. states east of the Rocky Mountains and the Canadian provinces of Ontario and Quebec (Fig. 1). By 1994, it was also beginning to disperse, apparently by human mediated vectors, into smaller, inland bodies of water. As of January 1996, sightings of zebra mussels have been confirmed in 54 isolated inland lakes in Illinois, Indiana, Michigan, New York, Ohio, Vermont and Wisconsin (United States National Biological Service, 1995a). A second species of freshwater, dreissenid mussel, the quagga mussel, Dreissena bugensis, has also been introduced into the Great Lakes. Initially recorded in Lake Ontario, it is spreading rapidly and now occupies the eastern basin and southern shore of Lake Erie, the southern shore of Lake Ontario and the freshwater portions of the St. Lawrence River (May and Marsden, 1992; Mills et al., 1993, 1996; Zebra Mussel Information Clearinghouse, 1995). The tendency of zebra mussels to form dense aggregates on hard surfaces causes them to have great economic impact. Its planktonic veliger larvae and translocating juveniles are entrained on intake water into man-made raw water systems where they settle and attach in large numbers. Newly settled mussels reach such high densities (up to 700,000 irr 2, Griffiths et al., 1991) and have such rapid post-settlement growth rates (Nichols et al., 1990, 1996) that they rapidly form thick mats, occluding or blocking flow even in large diameter piping

2 240 J. L. RAM AND R. F. MCMAHON FIG. 1. Map showing the distribution of the zebra mussel, Dreissena polymorpha in North America as of October, Dotted lines show the borders of U.S. states and Canadian provinces and solid lines indicate major rivers and lakes. Solid circles are confirmed reports of individual zebra mussel populations while darkened areas indicate regions were mussel populations have become contiguous (data from United States National Biological Service, 1995b). (Mackie et al., 1989; McMahon, 1992; Kovalak et al., 1993; Jenner and Janssen- Mommen, 1993). Early North American experience with mussel infestations in the raw water systems of power stations, potable water treatment plants and industrial facilities on the Great Lakes suggested that their fouling developed more rapidly and was more severe than reported in Europe (Griffiths et al., 1989; LePage, 1993; Claudi and Mackie 1993). Thus, the zebra mussel invasion of North America will lead to increased macrofouling impacts, the eventual costs for repair, replacement and control estimated to be several billion dollars annually (Roberts, 1990; Office of Technology Assessment, United States Congress, 1993). The zebra mussel is also negatively impacting native North American freshwater biota. Extensive mortality or even complete extirpation of native North American unionid bivalve populations has been reported in habitats densely colonized by zebra mussels. The mussels settle on the posterior portions of unionid shells extending above the substratum surface. Massive infestations cause unionids to be dislodged from the substratum and/or experience starvation as zebra mussels filter seston food from the unionid's inhalant flow (Mackie, 1993; Schloesser et al., 1996). Suspensionfeeding by dense zebra mussel populations may also result in density reductions of phytoplankton and suspended inorganic matter (Maclsaac et al., 1992). The resulting increase in water clarity can lead to increases in the density and biomass of benthic macrophytes and animals (Hebert et al., 1991). Such diversion of energy flow by zebra mussels from pelagic into benthic food chains has been hypothesized to negatively impact pelagic fish populations while increasing demersal fish productivity (Karnaukhov and Karnaukhov, 1993). Zebra mussels also accumulate environmental contaminants; thus, predators feeding on zebra mussels can have notably elevated tissue contaminant loads and reduced reproductive success (see Maclsaac et al., 1996). Zebra mussels have already caused considerable ecological change in the lower Great Lakes and their ecological impacts are likely to extend into other drainage systems as they disperse throughout North America. While Dreissena polymorpha is likely to have negative environmental and economical impacts on North American freshwaters, North American investigators have found that this species can also be a model organism for biological, ecological and physiological investigations. The mussels are easy to collect, maintain, and culture (Nichols, this volume) making them adaptable to a wide variety of laboratory investigations, and, because they are epifaunal and sessile, they also make excellent subjects for field ecological or environmental studies. For example, the information base on zebra mussel physiology has been greatly increased by recent North American studies of ion transport (Horohov et al., 1992; Dietz et al., 1996), ciliary function (Silverman et al., 1996), physiological resistance and capacity adaptations (McMahon, et al., 1993 and McMahon, 1996), and reproductive/ developmental mechanisms (Ram et al.,

3 1993; Fong et al., 1993, 1994; Miller et al., 1994; Ram et al., 1996). Although much information has been accumulated through European studies, the zebra mussel's invasion of North America has triggered a rather extensive American/Canadian research response, sponsored by many agencies, including NSF, NOAA, the U.S. Army Corps of Engineers, the U.S. National Biological Service, power and water utilities, and Canadian and Ontario governmental research and environmental agencies. As North American data have accumulated, it has become apparent that North American and European zebra mussels are not equivalent in all aspects of their biology, ecology and physiology (Mackie and Schloesser, 1996; McMahon, 1996). Lack of congruence between European and North American data may partly result from the rapid dispersal of North American zebra mussels, their elevated growth rates and lack of natural predators, and the fact that the probable source of North American mussels was the Black Sea region of the Ukraine at the extreme southern portion of the zebra mussel's European range. 'Zebra. mussels from this area have been little studied. Instead, the majority of European studies have concentrated on northern European mussels drawn from much colder waters. Thus, North American zebra mussels appear to be more thermally tolerant (Mc- Mahon et al., 1993), to have greater growth rates (Griffiths et al., 1991) and to display greater reproductive variation (Garton and Haag, 1993) than reported for mussels from northern Europe. In addition, genetic and morphological studies on North American quagga mussels prove decisively that they are genetically distinct from zebra mussels and that their source populations are in the Dneiper River/Black Sea Region of Ukraine (Spidle et al, 1994; Rosenberg and Ludyanskiy, 1994; Marsden et al., 1996). INTRODUCTION 241 The chapters in this symposium provide a new synthesis and integration of recent biological studies on North American varieties of dreissenid mussels. Although full length papers have appeared in the published proceedings of several annual conferences on zebra mussels and other exotic species {e.g., Tsou and Mussalli, 1993; Wisconsin Sea Grant Institute, 1994; Ontario Hydro, 1995), these volumes have focused primarily on this species' macrofouling impacts and control, have been largely reports of nonzoologists, have not attempted to analyze, review, or integrate information from multiple sources, and have not been available to the general zoological research community. A more biologically oriented treatise on zebra mussels is Zebra Mussels: Biology, Impacts and Control, edited by Nalepa and Schloesser (1993), which is a collection of papers on aspects of the mussel's biology and macrofouling control. However, much of the research reported in this volume was carried out prior to 1991, before zebra mussels had dispersed little beyond Lake Erie and when most North American investigators had studied them for less than one year. Intensive study of zebra mussel biology in North America has occurred over the four years subsequent to publication of this treatise (Nalepa and Schoesser, 1993). The symposium papers in this issue of American Zoologist update the biology, ecology, and physiology of zebra mussels in North America and provide a comparison with European findings. As zebra mussels become available to an increasing number of North American investigators, this publication will provide a new and comprehensive data base supporting further research on this ecologically and economically important species. ACKNOWLEDGMENTS This symposium was sponsored by the Division of Invertebrate Zoology and cosponsored by the Division of Comparative Physiology and Biochemistry and the Division of Ecology of the American Society of Zoologists. We are grateful to the symposium participants who devoted considerable time and effort to preparing both their symposium presentations and papers. Many of the participants allocated personal or grant funds to partially support their travel expenses to the symposium. We would also like to acknowledge the experts who reviewed the papers presented in this volume. Cornelia Schlenk, Assistant Director, New York Sea Grant Institute, and Charles R. O'Neill, of the "Zebra Mussel Information

4 242 J. L. RAM AND R. F. MCMAHON Clearing House of the New York Sea Grant Institute provided invaluable assistance and advice regarding seeking of funding for presentation and publication of the symposium. Presentation and publication of the symposium was supported by grants from New York Sea Grant Institute, The Zebra Mussel Information Clearing House of the New York Sea Grant Institute and NSF Grant No. IBN REFERENCES Claudi, R. and G. L. Mackie Practical manual for zebra mussel monitoring and control. Lewis Dietz, T. H., S. J. Wilcox, R. A. Byrne, J. W. Lynn, and H. Silverman Osmotic and ionic regulation of North American zebra mussels (Dreissena polymorpha). Amer. Zool. 36: Fong, P. P., K. Kyozuka, H. Abdelghani, J. D. Hardege, and J. L. Ram In vivo and in vitro induction of germinal vesicle breakdown in a freshwater bivalve, the zebra mussel Dreissena polymorpha (Pallas). J. Exp. Zool. 269: Fong, P. P., D. M. Wall, and J. L. Ram Characterization of serotonin receptors in the regulation of spawning in the zebra mussel Dreissena polymorpha (Pallas). J. Exp. Zool. 267: Garton, D. W. and W. R. Haag Abundance and settling of zebra mussel (Dreissena polymorpha) veligers in western Lake Erie. In T. F. Nalepa, and D. W. Schloesser (eds.), Zebra mussels: Biology, impacts, and control, pp Lewis Publishers, Griffiths, R. W., W. P. Kovalak, and D. W. Schloesser The zebra mussel, Dreissena polymorpha (Pallas, 1771), in North America: Impact on raw water users. In Proceedings: EPRI service water system reliability improvement seminar, pp Electric Power Research Institute, Palo Alto, California. Griffiths, R. W., D. W. Schloesser, J. H. Leach, and W. P. Kovalak Distribution and dispersal of the zebra mussel {Dreissena polymorpha) in the Great Lakes region. Can. J. Fish. Aquat. Sci. 48: Hebert, P. D., B. W. Muncaster, and G. L. Mackie Ecological and genetic studies on Dreissena polymorpha (Pallas): A new mollusc in the Great Lakes. Can. J. Fish. Aquat. Sci. 46: Hebert, P. D., C. C. Wilson, M. H. Murdoch, and R. Lazar Demography and ecological impacts of the invading mollusc Dreissena polvmorpha. Can. J. Zool. 69: Horohov, J., H. Silverman, J. W. Lynn, and T. H. Dietz Ion transport in the freshwater zebra mussel, Dreissena polymorpha. Biol. Bull. 183: Karnaukhov, V. N. and A. V. Karnaukhov Perspectives on the ecological impacts of the zebra mussel (Dreissena polymorpha) in the former European USSR and in North America. In T. F. Nalepa and D. W. Schloesser (eds.), Zebra mussels: Biology, impacts, and control, pp Lewis Kovalak, W. P., G. D. Longton, and D. Smithee Infestation of power plant water systems by the zebra mussel (Dreissena polymorpha Pallas) In T. F. Nalepa and D. W. Schloesser (eds.). Zebra mussels: Biology, impacts, and control, pp Lewis Jenner, H. A. and J. P. M. Janssen-Mommen Monitoring and control of Dreissena polymorpha and other macrofouling bivalves in The Netherlands. In T. F. Nalepa and D. W. Schloesser (eds.), Zebra mussels: Biology, impacts, and control, pp Lewis LePage, W. L The impact of Dreissena polymorpha on waterworks operations at Monroe, Michigan: A case history. In T. F. Nalepa, and D. W. Schloesser (eds.), Zebra mussels: Biology, impacts, and control, pp Lewis Publishers, Maclsaac, H. J Potential abiotic and biotic impacts of zebra mussels on the inland waters of North America. Amer. Zool. 36: Maclsaac, H. J., W. G. Sprules, O. E. Johannsson, and J. H. Leach Filtering and impacts of larval and sessile zebra mussels in western Lake Erie. Oecologia 92: Mackie, G. L Biology of the zebra mussel (Dreissena polymorpha) and observations of mussel colonization on unionid bivalves in Lake St. Clair of the Great Lakes. In T. F. Nalepa and D. W. Schloesser (eds.). Zebra mussels: Biology, impacts, and control, pp Lewis Publishers, Mackie, G. L., W. N. Gibbons, B. W. Muncaster, and I. M. Gray The zebra mussel, Dreissena polymorpha, a synthesis of European experiences and preview for North America. ISBN: , Great Lakes Section, Water Resources Branch, Ontario Ministry of the Environment, London, Ontario. Mackie, G. L. and Don W. Schloesser Comparative biology of zebra mussels in Europe and North America: An overview. Amer. Zool. 36: Marsden, J. E., A. P. Spidle, and B. May Review of genetic studies of Dreissena spp. Amer. Zool. 36: May, B. and J. E. Marsden Genetic identification and implications of another invasive species of dreissenid mussel in the Great Lakes. Can. J. Fish, and Aquat. Sci. 49: McMahon, R. F The zebra mussel the biological basis of its macrofouling and potential for distribution in North America. In: Corrosion'92: Proceedings of the 47th Nace Annual Conference, pp National Association of Corrosion Engineers, Houston, Texas. McMahon, R. F The physiological ecology of the zebra mussel, Dreissena polymorpha, in North America and Europe. Amer. Zool. 36: McMahon, R. F., T. A. Ussery, A. C. Miller, and B. S.

5 INTRODUCTION 243 Payne Thermal tolerance in zebra mussels (Dreissena polymorpha) relative to rate of temperature increase and acclimation temperature. In J. L. Tsou and Y. G. Mussalli (eds.), Proceedings: Third international zebra mussel conference, pp EPRI TR , Electric Power Research Institute, Palo Alto, California. McMahon, R. F, M. A. Matthews, T. H. Ussery, R. Chase, and M. Clarke Further studies of heat tolerance in zebra mussels: Effects of temperature acclimation and chronic exposure to lethal temperatures. In A. H. Miller (ed.), Proceedings: Fourth international zebra mussel conference, pp Wisconsin Sea Grant Institute, Madison, Wisconsin. Miller, R. L., J. J. Mojares, J. J. Stachecki, and J. L. Ram Species specific sperm attraction in the zebra mussel, Dreissena polymorpha, and the quagga mussel, Dreissena bugensis. Can. J. Zool. 72: Mills, E. L., R. M. Dermott, E. F. Roseman, D. Dusin, E. Mellina, D. B. Conn, and A. P. Spidle Colonization, ecology, and population structure of the "quagga" mussel (Bivalvia: Dreissenidae) in the lower Great Lakes. Can. J. Fish. Aquat. Sci. 50: Mills, E. L., G. Rosenberg, A. P. Spidle, M. Ludyanskiy, Y. Pligin, and B. May A review of the biology and ecology of the quagga mussel (Dreissena bugensis), a second species of freshwater dreissenid introduced to North America. Amer. Zool. 36: Nalepa, T. F. and D. W. Schloesser (eds.) Zebra mussels: Biology, impacts, and control. Lewis Nichols, S. J Variations in the reproductive cycle of Dreissena polymorpha, in North America and Europe. Amer. Zool. 36: Nichols, S. J., A. M. Bitterman, and F. Ely Growth rates of Dreissena polymorpha in the St. Clair River and lakes St. Clair, Erie, and Ontario from June to November In Proceedings: International zebra mussel research conference, p. 11. Ohio Sea Grant College Program, Columbus, Ohio. Office of Technology Assessment, United States Congress Harmful non-indigenous species in the United States. Publication OTA-F-566, United States Congress, Washington, DC. O'Neill, C. R., Jr. and A. Dextrase The introduction and spread of the zebra mussel in North America. In A. H. Miller (ed.). Proceedings: Fourth International Zebra Mussel Conference, pp Wisconsin Sea Grant Institute, Madison, Wisconsin. Ontario Hydro Proceedings of the fifth international zebra mussel and other aquatic nuisance organisms conference The Professional Edge, Pembroke, Ontario. Ram, J. L., G. W Crawford, J. U. Walker, J. J. Mojares, N. Patel, P. P. Fong, and K. Kyozuka Spawning in the zebra mussel Dreissena polymorpha (Pallas): Activation by internal or external application of serotonin. J. Exp. Zool. 265: Ram, J. L., P. P. Fong, R. P. Croll, J. S. Nichols, and D. M. Wall The zebra mussel (Dreissena polymorpha), a new pest in North America: Reproductive mechanisms as possible targets of control strategies. Invert. Rep. Dev. 22: Ram, J. L., P. P. Fong, and D. W. Garton Physiological aspects of zebra mussel reproduction: Maturation, spawning and fertilization. Amer. Zool. 36: Roberts, L Zebra mussel invasion threatens U.S. waters. Science 249: Rosenberg, G. and M. L. Ludyanskiy A review of Russian species concepts of Dreissena, with identification of the quagga mussel as Dreissena bugensis (Bivalvia: Dreissenidae). Can. J. Fish. Aqua. Sci. 51: Schloesser, D. W, T. F. Nalepa, and G. L. Mackie Zebra Mussel infestation of unionid bivalves (Unionidae) in North America. Amer. Zool. 36: Silverman, H., J. W. Lynn, E. C. Achberger, and T. H. Dietz Gill structure in zebra mussels: Bacterial-sized particle filtration. Amer. Zool. 36: Spidle, A. T, J. E. Marsden, and B. May Identification of the great lakes quagga mussel as Dreissena bugensis from the Dneiper River, Ukraine on the basis of allozyme variation. Can. J. Fish. Aqua. Sci. 51: Tsou, J. L. and Y. G. Mussalli (eds.) Proceedings: Third international zebra mussel conference, EPRI TR , Electric Power Research Institute, Palo Alto, California. Wisconsin Sea Grant Institute Proceedings: Fourth international zebra mussel conference. Wisconsin Sea Grant Institute, Madison, Wisconsin. United States National Biological Service. 1995a. Zebra mussel distribution update as of July United States National Biological Service's Nonindigenous Aquatic Species Data Base, Southeastern Biological Science Center, Gainesville, Florida. United States National Biological Service. 1995b. Zebra mussel (Dreissena polymorpha) distribution in North America: October United Stales National Biological Service's Nonindigenous Aquatic Species Data Base, Southeastern Biological Science Center, Gainesville, Florida. Zebra Mussel Information Clearinghouse North American range of the quagga mussel as of 1 September Dreissena! 6(3):6.