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The Potential Spread of Exotic Freshwater Bivalves

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The Potential Spread of Exotic Freshwater Bivalves Biol Invasions (2007) 9:161–180 DOI 10.1007/s10530-006-9013-9 ORIGINAL PAPER Changes in global economies and trade: the potential spread of exotic freshwater bivalves Alexander Y. Karatayev Æ Dianna K. Padilla Æ Dan Minchin Æ Demetrio Boltovskoy Æ Lyubov E. Burlakova Received: 7 February 2006 / Accepted: 10 April 2006 / Published online: 4 June 2006 Ó Springer Science+Business Media B.V. 2006 Abstract The globalization of economies and nalis, and Limnoperna fortunei. We suggest that trade have facilitated the spread of exotic species the spread of these exotic species has not been a including the five most important freshwater continuous process, but rather punctuated by suspension feeding invaders Dreissena polymor- periods of rapid long distance spread (jump), pha, D. bugensis, Corbicula fluminea, C. flumi- during which species greatly expanded their geo- graphic ranges. Each jump has been associated with changes in the tempo of some human activ- ity, such as the construction of shipping canals for trade, building of reservoirs for water storage and A. Y. Karatayev (&) Æ L. E. Burlakova Department of Biology, Stephen F. Austin State power production, political boundary changes or University, Box 13003, SFA Station, Nacogdoches, changes in political systems, which affected the TX 75965-3003, USA position or permeability of national borders, hu- e-mail: [email protected] man migration, changes in the mode and volume D. K. Padilla of international trade, or recent industrial prac- Department of Ecology and Evolution, Stony Brook tices and environmental laws. We hypothesize University, Stony Brook, NY 11794-5245, USA that the rate of spread of exotic species depends on the spatial scale of spread and may be accel- D. K. Padilla The National Center for Ecological Analysis and erated or slowed by various human activities. In Synthesis, 735 State Street, Suite 300, Santa Barbara, general, aquatic exotic species may quickly spread CA 93101-5504, USA along connected waterways in a new continent they invade and soon reach their maximum range D. Minchin Marine Organism Investigations, Marina Village, (continental scale). However, it will take much Ballina, Killaloe, Co Clare, Ireland longer to colonize all isolated regions (regional scale) and longer still to spread to all isolated D. Boltovskoy lakes and river systems (local scale). The differ- Department of Biological Sciences, School of Exact and Natural Sciences, University of Buenos Aires, ence in the rate of colonization across scales may C1428EHA 1428 Buenos Aires, Argentina be several orders of magnitude. D. Boltovskoy Keywords Aquatic nuisance species Æ Consejo Nacional de Investigaciones Cientificas y Tecnicas, and Museo Argentino de Ciencias Naturales Biogeography Æ Dispersal Æ Geographic spread Æ ‘‘Bernardino Rivadavia’’, Buenos Aires, Argentina Invasion Æ Globalization Æ Suspension feeders 123 162 Biol Invasions (2007) 9:161–180 Introduction power production, political boundary changes and changes in political systems, which affected the Historically, most European and American position or permeability of national borders, hu- freshwaters lacked powerful benthic suspension man migrations, changes in the mode and volume feeders that attain high densities, have high of international trade, and recent industrial growth rates, rapid recruitment, significantly alter practices and environmental laws (Table 1). the substrate (ecosystem engineers), and provide The goal of this paper is to: summarize the a direct link between benthic and pelagic com- principal factors that have facilitated the large- ponents of an ecosystem. However, such species scale spread of exotic freshwater bivalves, sum- did exist in Asia, Africa, and small regions of marize the potential or realized impacts of these south-eastern Europe, including the invasive invaders on freshwater ecosystems, compare their Dreissena polymorpha, D. bugensis, Corbicula physiological or environmental limits, and predict fluminea, C. fluminalis, and Limnoperna fortunei. their potential distribution and spread on a global Due to human activities, especially interna- and regional scale. tional trade and the globalization of economies, these species have spread far beyond their native ranges, crossed oceans and colonized large re- History of spread gions within Europe, the Americas, and Asia. Increasingly, two or sometimes three species of Dreissena polymorpha (zebra mussel) is native to exotic bivalves are found together, such as Dre- the fresh and brackish waters of the Caspian and issena and Corbicula, which have never over- Black Sea drainage basins (Mordukhai-Boltov- lapped in the past. In the future many freshwater skoi 1960; Starobogatov and Andreeva 1994). In regions around the globe may host up to five (or the late 1700s to early 1800s, D. polymorpha even more) non-native species that have large spread through canals built for commerce to ecological and economic impacts (reviewed in connect the rivers of the Black and Baltic Sea Karatayev et al. 1997, 2002, 2005a; Ricciardi 1998; basins (reviewed in Starobogatov and Andreeva McMahon 1999). 1994; Karatayev et al. 2003a). After these canals The introduction of exotic species, including were built, international trade increased consid- bivalve suspension feeders, has a long history, erably, and in 1824, D. polymorpha was found in dating back at least to the Middle Ages. For London (Kerney and Morton 1970). By the first example, the soft-shelled estuarine clam, Mya half of the 19th century there was intense ship arenaria, most likely was introduced to Northern traffic among all major European ports, and Europe from North America by Vikings in the within a few decades D. polymorpha had spread 13th century (Strasser 1999). With an increase in to many western European countries, including international trade over the 19th and especially the Netherlands (1826), Germany (1830), Bel- the 20th centuries, many more species have been gium (1833), France (1838), and Denmark (1840) introduced into different parts of the world (Mills (Kerney and Morton 1970; Kinzelbach 1992; et al. 1993a; Fofonoff et al. 2003). We contend Starobogatov and Andreeva 1994). The zebra that the spread of exotic species has not been a mussel invasion across Europe was rapid, and it continuous process, but rather punctuated by was found as far as London within ~20 years. In periods of intense activity during which some 1986 D. polymorpha was discovered in the Lau- species greatly expanded their geographic range rentian Great Lakes in North America (Hebert (jump, Reid 1899). For five important freshwater et al. 1989). Once introduced, it spread rapidly invaders, Dreissena polymorpha, D. bugensis, throughout the Great Lakes and connected Corbicula fluminea, C. fluminalis, and Limno- waterways including major rivers, and eventually perna fortunei, each jump was associated with invaded many inland lakes in both Canada and changes in the tempo of some human activity, the United States (reviewed in McMahon and such as the construction of shipping canals for Bogan 2001). Although the initial spread of zebra trade, building of reservoirs for water storage and mussels throughout most of Europe including 123 Biol Invasions (2007) 9:161–180 163 England occurred in the 1800s, D. polymorpha nalis includes France, Portugal, Spain (Araujo was not discovered in Ireland until 1997 (although et al. 1993), the Netherlands (bij de Vaate and it likely arrived in 1993/94; Minchin 2000) and Greijdanus-Klaas 1990), Germany (Haesloop Spain in 2001 (bij de Vaate et al. 2002). 1992), Belgium (Swinnen et al. 1998), Hungary A related species, Dreissena bugensis (quagga (Csanyi 1998–1999) and Ukraine (Voloshkevich mussel), has a smaller natal distribution, limited and Son 2002). In South America C. fluminea was to the Dnieper-Bug Liman (large coastal lake, reported simultaneously from Argentina (Ituarte connected to the Black Sea), and the lower 1981) and Brazil in the early 1980s (Veitenheimer- reaches of the South Bug and Ingulets rivers, Mendes 1981), and in both cases the initial invasion flowing into the liman (Andrusov 1897). Al- was estimated to be around 1970. At present its though D. bugensis colonized North America at range extends from northern Patagonia, around the same time as D. polymorpha, in the mid 1980s 39°S, to Uruguay and southern Brazil. It is very (Mills et al. 1993b), D. bugensis did not follow the likely to be present in Peru´ and Bolivia as well colonization of Europe by D. polymorpha. Al- (Darrigran 2002). though there was extensive ship traffic between Limnoperna fortunei (golden mussel) occurs areas inhabited by D. bugensis and other regions naturally in fresh and brackish waters of southern of eastern and western Europe through the mid- Asia, including China, Thailand, Korea, Laos, dle of the 20th century, D. bugensis remained Cambodia, Vietnam, and Indonesia (reviewed in restricted to the Dnieper-Bug Liman and the Ricciardi 1998). In 1965 L. fortunei colonized lower reaches of the Southern Bug River. Only by Hong Kong (Morton 1975), and in the late 1980s the 1940s D. bugensis had spread throughout the Japan (Magara et al. 2001). In the early 1990s it Dnieper River and its tributaries and eventually spread to South America (Pastorino et al. 1993), colonized the Dniester River. By the 1980s it and is presently found in Argentina, Uruguay, occurred in the River Don system (Russia) Paraguay, Bolivia and Brazil (Darrigran 2002). (Zhulidov et al. 2004), and subsequently in the In addition to the species listed above, there
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