'YBiological Invasions 5z 213-221, 2003.O 2003 Kluwer Academic Publishers. Printed in the Netherlands.

Patterns of spread of the zebra mussel (Dreissena polymorphs (Pallas)):the continuing invasion of Belarussian Lakes

Alexander Y. Karatayevr, Lyubov E. Burlakoval, Dianna K. padilla2'* &Ladd E. Johnson3I Biology Department, Stephen E Austin State (Jniversity, Nacogdoches, TX 75962-3002, USA;2Department of Ecology and Evolution, State University of New York at Stony Brook, Stony Brook,NY I 1794-5245, USA; 3 Ddpartement de Biotogie and Qudbec-Ocdan, Universitd Laval, Qudbec, QC, Gl K 7p4,Canada;*Authorfor corcespondence (e-mail: padilla@lfe.bio.sunysb.edu; fax: +I-631-632-7626)

Received l8 May 2001; accepted in revised form 20 May 2003

Key words.' aquatic nuisance species, biogeography, dispersal, geographic spread, invasion, lakes, zebramussels

Abstract

The invasion of the freshwaters of Belarus by the zebra mussel, Dreissena polymorpha (Pallas), began at least200 years ago by the opening of shipping canals linking the Black Sea and Baltic Sea drainage basins. However,zebra mussels have invaded only 93 (16.87o) of 553 studied lakes; at least 20 of these lakes were invaded withinin the past 30 years. Zebra mussels were found disproportionately in lakes that were mesotrophic, larger, and hadsome commercial fishing. Although larger lakes have more intensive fisheries with larger catches, the intensityof the fishery and average catch did not affect the probability of zebra mussel invasion. Zebra mussels were notfound in dystrophic lakes (l\Vo of the lakes studied), probably due to their low pH and calcium content. Zebramussels became locally extinct in one lake due to anthropogenic eutrophication and pollution. Many ecologicallysuitable lakes have yet to be invaded, which suggests that natural vectors of overland dispersal, e.g., waterfowl,have been ineffective in Belarus. Thus, future spread of this species will continue to depend on human activitiessuch as commercial fishins.

Introduction

The invasion of North America by the zebra mussel(Dreissena polymorpha) has focused attention on eco-nomic and environmental problems associated withexotic species. As with many exotic species, the spreadof zebramussels has been tightly linked to human activ-ities. Carlton (1993) identified over2}potential ways inwhich zebramussels can be dispersed and made impor-tant contrasts between (l) the dispersal of larvae andadults, (2) natural and human-mediated dispersal, and(3) dispersal overland between bodies of water and dis-persal within a body of water. A planktonic larval stage(veliger) makes zebra mussels well suited to spreadnaturally within lakes and reservoirs or downstreamwithin a watershed. However, this life history appears

to prevent the establishment of populations in streamsor rivers that do not have a source population in aheadwater lake (Horvath et al.1996). The ability of theadult stage to attach to submerged objects (e.g.,wood,macrophytes) can also aid in downstream dispersal(Horvath and Lamberli l99l). Obviously, any humanactivity that moves either water (e.g., fish stocking) orobjects (e.g., boats) within or between waterbodies hasthe potential to disperse this species. Unfortunately, weare only beginning to understand the relative impor-tance of different potential vectors of spread (Johnsonand Carlton 1996; Johnson et al. 2001).

Studies in eastern and western Europe have pro-vided useful information on a variety of aspects ofzebra mussel biology (Morton 1969; Stanczykowska1977; Lvova 1980; Karatayev 1988), ecology

214

(Stanczykowska l9l1; Stanczykowska andLewandowski 1993; Karatayev et al. 1994, 1997,1998), and distribution (Kinzelbach 1992;Starobogatov and Andreeva 1994). The spatial andtemporal dynamics of the invasion of this and otherexotic species has been difficult to address, espe-cially at the regional level (Johnson and Padilla 1996;Buchan and Padill a 1999). However, studies of the geo-graphic pattern and rate of spread of zebra mussels areextremely helpful if we are to predict, slow or stop thespread of zebra mussels and other exotics to new fresh-water bodies, as well as identify important vectors forspread (Buchan and Padilla 1999; Bossenbroek et al.2O0l; Kraft et a1.2002).

Because the initial invasion of zebra mussels acrosseastern and western Europe occurred largely duringthe 1800s (Andrusov l89l; Skorikov 1903; Deksbakh1935; Kinzelbach 1992; Ludyanskiy et al. 1993),detailed quantitative information on the spread of zebramussels in Europe is generally lacking. Zebra mus-sels were originally found in the fresh and brack-ish waters of the Caspian and Black Sea drainagebasins including large tributary rivers (Andrusov1897 ; Mordukhai-Boltovskoi 1960; Starobogatov andAndreeva 1994). Because shipping was restricted tothe largest rivers, canal systems were built in the late1700s-early 1800s, through what is now Belarus, toconnect these large rivers and the Black, Caspian andBaltic Seas for commerce (Andrusov 1891; Zhadin1946; Kinzelbach 1992; Starobogatov and Andreeva1994). After these canals were built and commer-cial ships traveled regularly through them, zebra mus-sels appeared throughout eastern and western Europe(Zhadin 1946; Kinzelbach 1992; Starobogatov andAndreeva 1994). They appeared in England in 1824,the Netherlands in 1826, Germany in 1830, Denmarkin 1840, and in France shortly thereafter (Kerney andMorton 1970; Kinzelbach 1992; Starobogatov andAndreeva 1994). Zebra mussels continue to spread tonew lakes and areas across Europe, and have recentlyinvaded Ireland (Minchin 1998). Although there issome information about the spread of zebra musselsthrough major rivers and canal systems, there is verylittle information available on the spread of zebramussels from these river and canal systems to otherwaterbodies, especially those not directly connected torivers.

Systematic searching of waterbodies across a regionis required to adequately study the pattern and timingof spread of any invading species, and it is equally

important to know where they are and are not found(Johnson and Padilla 1996; Kraft and Johnson 2000).Although such information is rare, ithas been collectedin the Republic of Belarus over the past 200 years. Toassess the historic and present spread of zebra musselsacross Belarus, we reviewed the literature on the historyof the spread of zebra mussels across Belarus. We alsoused a unique data set for 553 lakes of a wide rangeof sizes and trophic types assembled during the past25 years as part of a comprehensive limnological study,to address questions about the spread and invasion ofzebra mussels. We tested whether zebra mussels weremore likely to be found in lakes with different trophicstatus, different sizes, with or without fishing, withdifferent degrees of fishery activity, and in differentdrainage basins.

Materials and methods

There are 1072 lakes with surface area greater than0. I km2 in Belarus (Kurlovich and Serafimovich 198 I ).Most of these lakes were formed during the last glacia-tion and are found in northern Belarus (BelarussianLakeland), especially the Zapadnaya Dvina Riverdrainage basin (Figure 1; Table 1). Due to intensiveagriculture, all Belarussian lakes suffer from anthro-pogenic eutrophication. Therefore, no lakes are oligo-trophic, few are meso-oligotrophic or mesotrophic andmost are eutrophic. Some Belarussian lakes are dys-trophic. Although there are many flood-plain lakes inBelarus, they are usually very small, and were notconsidered in our study.

To determine the current distribution and recentspread of zebra mussels in Belarus, we examined datacollected from 553 glacial lakes between l97l and1996. As part of a larger survey of Belarussian lakes,a variety of chemical, geological, physical, biological,and socioeconomic data were systematically collectedfor each of these lakes fl-akes Research Laboratory ofthe Belarussian State University (LRL)1.

The data we used for this paper were: lake surfacearea, trophic status, presence of commercial fishingduring a 15 year period, the average fishery catch overthat same 15 years, and presence or absence of zebramussels. Although the availability of substrate for theattachment of zebra mussels can limit their distributionin some lakes, all of the lakes in our data set had atleast some substrate adequate for zebra mussel attach-ment, therefore, this factor was not considered in our

215

Table 1. The presence of zebra mussels in Belarussian lakes withsurface area >0. 1km2. The locations of river basins can be foundin Figure l. The total number of lakes in each river basin is fromKurlovich and Serafimovich (1981).

River basin Total Number Number ofnumber of lakes studied lakesof lakes studied (7o) with zebra

mussels (7o)

Figure /. Map of the Republic of Belarus. (A) The first studies ofthe invasion of zebra mussels were conducted when Belarus wassplit between Poland and the USSR (dashed line indicates border),and only the USSR portion was surveyed. The filled circles (lakes)and open triangles (rivers) indicate the known populations of zebramussels before our study. (B) The drainage basins of theZapadnaya

474 (62.6) 86 (18.1)11 (9.4) 3 (27.3)33 (36.3) 3 (e .1)20 (23.3) 0e (6e.2) l (1 l . l )6 (7s.0) 0

553 (s1.6) 93 (16.8)

analyses. Lake surface areas were estimated from maps(1 :25,000 scale). Trophic status (oligotrophic, meso-oligotrophic, mesotrophic, eutrophic, dystrophic) wasassigned by the LRL staff, and was determined usingchemical (total ion content, organic content, phos-phorous content), physical (transparency, color), andbiological (phytoplankton density, biomass, speciescomposition) data (Winberg 1960; Yakushko l97lRossolimo l9l1). Karatayev and Burlakova (1995)examined a similar data set; however, the data set weused in this study was revised and updated in 1995and 1996. The re-evaluation of trophic status of theselakes included more emphasis on the biological data,and included the summer biomass of phytoplankton,zooplankton and benthos, and the taxonomic structureof planktonic and benthic communities. In many cases,a re-examination of the data by both hydrochemists andbiologists resulted in reassignment of lake trophic sta-tus from the data set used by Karatayev and Burlakova(199s) .

The intensity of the commercial fishery was esti-mated from 196l to 1916 wrth records from theFish Conservation Committee of the State Committeeof Ecology and Conservation of Natural Resources,Republic of Belarus. We chose this 15 year period forseveral reasons. To test if fisheries have been importantvectors for the spread of zebta mussels, we neededto use fisheries data that were collected prior to the

Dvina (ZD), Dnieper (D), Neman (N), Pripyat (P), Zapadnyi Bug(ZB), and Lovat (L) rivers. (C) Circles (lakes) and open triangles(rivers) indicate all known populations of zebra mussels in Belarus.Filled circles indicate lakes and reservoirs where we know theapproximate date of zebra mussel invasion.

Zapadnaya Dvina (ZD)

Dnieper (D)

Neman (N)

Pripyat (P)

Zapadnyi Bug (ZB)

Lovat (L)

Total

157n 79 l861 38

t072

- - t t - * a a

ZB

2 1 6

sampling dates for the majority of the lakes in ourdataset. For this l5 year period we have good annualdata on fisheries. The commercial fisheries in Belaruswere relatively stable from the early 1960s through theearly 1990s, but then collapsed when the Soviet Unionwas dissolved. We used the number of years during that15 year period as an estimate of fishery intensity, andthe average annual catch as an estimate of the size ofthe fishery.

The presence or absence of zebta mussels was deter-mined from 6 to25 benthic samples (depending on thesize of the lake such that sampling effort was as similaras possible across lakes) collected from sites system-atically distributed across the lake (Mitropolsky andMordukhai-Boltovskoi 1975). Benthic samples werecollected with an Ekman or Petersen grab (sampling

area -- 0.025 m2) and washed through a 550 pm mesh.After sampling, all macroinvertebrates were trans-ferred to containers with l07o neutral buffered formalinand labeled. All macroinvertebrates were identified tothe genus or species level, counted and weighed to thenearest 0.0001 g after being blotted dry on absorbentpaper. Because this technique is not appropriate for anaccurate estimate of zebra mussels density (Karatayev

et al. 1990), here we considered only presence/absenceof Dreissena in studied lakes. The sampling regimewas designed to maximize the coverage of the lake bot-tom and to include all major microhabitats. In addi-tion, benthic species composition along a 100-150mstretch of the littoral zone (down to 1.5 m depth) and6-25 plankton samples (for veligers) were examined.The densities of zebramussel populations in Europeanlakes have been recorded to fluctuate greatly (reviewed

in Ramcharan et al. 1992b). Although this samplingregime might not detect azebramussel population thatwas either very localized or very small, it did stan-dardize the search effort among lakes. Because of thescale of this project, different lakes were examined indifferent years, and most lakes were only examinedonce. However, over 100 lakes of various sizes weresampled more than once, and more than 50lakes werestudied >2 times.

Differences in frequencies in the presence andabsence of zebra mussels in different categories oflakes where tested using multi-way G-tests. These testsare a log-linear estimator of goodness of fit and arerecommended when expected values within cells arelow (below 30) and when some cell values are zero(Fienberg 1910).

Results

Zebra mussels were found in 93 (16.8%o) of the 553lakes examined (Table 1). At least 20 of the lakeswere invaded between 1971 and 1996 (as determinedby repeated sampling of the same lake during thattime period). Using a 3-way G-test, we found thatzebra mussels were found more often in larger lakes(0 .01trophic status (Pbe expected by random chance. Zebra mussels werefound disproportionately more often in mesotrophiclakes (39.2Vo), and they were completely absent from

dystrophic lakes (Table 3). With respect to lake size,zebra mussels were found over four times more oftenin the largest lakes (> 15 k*2) than in the smallest lakes(0.1-0.25km2; Table 2). Overall, larger lakes tendedto have a higher trophic status than would be expectedby random (0.05 > P > 0.025,3-way G-test). All

of these results were the same when dystrophic lakeswere eliminated from the analysis.

Using a 3-way G-test including lake size and fish-

ery intensity, we found that zebra mussels weremore common in larse lakes than small lakes

Table 2. Occurrence of zebra mussels in lakes of different size. The

total number of lakes in Belarus is from Kurlovich and Serafimovich( l 9 8 1 ) .

Number Number of

of lakes studied lakes

studied (7o) with zebra

mussels (7o)

Lake area(km2)

Total

number

of lakes

0.1 l-0.250.26-0.500.51-1.00l .0 l -5 .005.01-15.0t5.t-79.6

Total

5453301972t '7441 8

to12

r22 (22.4)l3s (40.9)tt4 (s7.9)143 (6s.9)27 (61.4)12 (66.7)

l1 (e .0)r s ( l l . r )t9 (16.7)33 (23.1)r0 (37.0)s (4r.7)

Titble 3. Occurrence of zebra mussels in lakes of different

trophic type.

Trophic type With zebra mussels

Number Percent

of lakes of lakes

Total number

of lakes

studied

Meso-oligotrophicMesotrophic

Eutrophic

Dystrophic

Total

265 l

42155

553

520680

93

t9.239.216.20

16.8

(0.025 > P > 0.0001), and more common in lakeswith fisheries than those without (P < 0.001). Largerlakes were much more likely to have an intensivefishery than small lakes (Pconsidered the size of the lake fisheries (average annualcatch), we again found that large lakes were morelikely to have large fishery catches (P < 0.0001).Greater fish catches were not associated with zebramussel invasion, when lake size was taken into account( Ppower could account for this lack of statistical sig-nificance. When we eliminated lakes without a fish-ery from the analysis, we found that large lakes weremore likely to have intensive and large catch fish-eries (Plikely to have zebra mussels (0.01However, lakes with more years of fishing or higherfish catches were not more likely to have zebramussels( 0 . 5 0 > P > 0 . 2 5 ) .

Lake colonization by zebra mussels was not equallylikely among drainage basins (0.025G-test; Table l). Lakes in the Zapadnaya DvinaRiver basin were more likely to have zebra mussels(86 lakes), and in the Dnieper River basin, zebramussels were present in a disproportionate number oflakes, occurring in 3 of 11 lakes. No zebra musselswere found in glacial lakes in the Pripyat or Lovatdrainage basins. In addition, zebra mussels were foundin 85 of 356 lakes studied on the southern bank of theZapadnaya Dvina River but only 1 of 118 lakes stud-ied on the northern bank was found to contain zebramussels.

Discussion

Zebra mussels have been invading the freshwaters ofeastern Europe for over 200 years, but not all lakesin Belarus have been invaded. Although the spreadof zebra mussels along shipping canals and the riversthey connect may have occuned quickly, the subse-quent spread to unconnected waters has occurred muchmore slowly. Another dreissenid mussel, D. bugensis,is abundant in the Ukraine, however, only thezebra mussel, D. polymorpha, has invaded Belarus.D. polymorpha has been the most important invaderacross Europe, and, at present, it is not known whythese two species seem to differ in their ability to invadenew lakes and rivers.

2 l l

Historic spread of zebra mussels

The spread of zebra mussels to lakes and rivers inBelarus (former USSR) began over 200 years ago andwas probably associated with shipping activities, espe-cially through canals (Ovchinnikov 1933; Lyakhnovichet al. 1984; Starobogatov and Andreeva 1994). Threecanals connecting the Dnieper and Zapadnyi BugRivers (1715), the Dnieper and Neman Rivers (1804)and Dnieper and Zapadnaya Dvina Rivers ( 1805), wereconstructed in Russia (what is now Belarus) to connectshipping routes between the Black Sea and Baltic Seabasins (Figure l). Not only did these canals increasetraffic along these rivers, they also established con-nections to river basins that previously had no navi-gable or hydrological links to the Black Sea basin, inparticular, the lake-rich basin of the Zapadnaya DvinaRiver.

The first study of the distribution of zebra mus-sels in what is now Belarus was by Ovchinnikov in1929. At that time, present day Belarus was dividedbetween the USSR and Poland, and he was only able tostudy the eastern (Soviet) part. Although his expeditionsurveyed many lakes, he only reported those wherehe found zebra mussels. He found zebra mussels inthree glacial lakes, three large rivers (Dnieper, Pripyat,and Berezina), and several small rivers (Ovchinnikov1933). From 1948 to 1953 zebramussels were reportedfrom five additional lakes in the Zapadnaya DvinaRiver basin and in Palik Lake which is connected tothe Berezina River (Drako 1953; Drako and Gavrilovl9l2). Lyakhnovich et al. (1984) reported that zebramussels had invaded the Drut River (ChigirinskoeReservoir), the Sozh River (near Gomel), the NemanRiver (near Grodno), and the Mukhovets River. Thus,before 1910, zebra mussels were known to haveinvaded at least nine glacial and two flood-plain lakes,six large and four small rivers and one reservoir inBelarus (Figure 1).

Present distribution

Zebra mussels were found in only 93 (16.87o) of553 lakes studied. Because of repeated sampling forsome of the lakes, we know that at least 20 (2l.5%o)of those lakes have been invaded during the past30 years. Although some of the lakes that have not beeninvaded are unsuitable for zebra mussels due to lowpH or low calcium, most are suitable for zebra mussels

218

based on the properties of invaded lakes and predic-tions from other European lakes (Ramcharan et al.1992a).

Lakes do not appear to have been invaded in arandom geographic pattern. At a large spatial scale,the percentage of lakes invaded by zebra mussels isgreatest in the Dnieper (27Vo) and Zapadnaya Dvina(l\Va) drainage basins which were connected by theDnieperZapadnaya Dvina canal in 1805. This canaland the rivers it connects run through the BelarussianLakeland in northeastern Belarus which contains morethan 62%b of the lakes in Belarus (Figure 1, Table l).Although this canal system has clearly been most influ-ential in the spread of zebra mussels within Belarus,two other canals, the Dnieprovsko-Bugskyi and theDnieprovsko-Nemanskyi, were considered the primaryroutes for the spread of zebra mussels to the rest ofEurope (Kinzelbach 1992; Starobogatov and Andreeva1994).

Different attributes of lakes also affected their prob-ability of being invaded by zebra mussels. Largerlakes, lakes with commercial fisheries, and lakes withlower trophic status were more likely to be invadedthan expected by random chance alone. The pres-ence of zebra mussels enhances the production ofbottom feeding fish, such as roach, white bream, andbream (Karatayev 1983; Lyankhnovich et al. 1988) andin some cases, doubled the size of a lake's fishery(Karatayev 1992; Karatayev and Burlakova 1995).Therefore, it is unclear whether the association betweenzebra mussel invasion and fisheries is because zebramussels enhance fish production, stimulating commer-cial fishing, or because fishing activities directly affectzebra mussel invasion, or both. Similarly, we do notknow if zebra mussels invade more often or survivebetter in lakes with lower trophic status, or if they arefound in lakes with lower trophic status because theyreduce the trophic status of lakes they invade, or both.The presence of zebramussels can shift the trophic sta-tus of a lake to a lower level by reducing phytoplanktonabundance (Karatayev and Burlakova 1995; Karatayevet al. 1991).

Zebra mussels were more common in large lakes,and large lakes were much more likely to have moreintensive fisheries with higher fish catches. Althoughlakes with fisheries were more likely to have zebramussels, zebra mussels were not more common as afunction of fishing intensity or the size of fishery catch.Again, it is difficult to separate the relative impor-tance of lake size and the presence of a fishery on the

likelihood of zebra mussel invasion because these twofactors are completely confounded.

The slow spread of zebra mussels from the majorrivers and canals to the lakes of Belarus appears tobe due to dispersal limitations. Early during the initialinvasion, zebra mussels were able to invade those fewlakes directly connected to rivers and their interbasincanals (Ovchinnikov 1933). However, most lakes inBelarus are not connected by navigable waterways, andthus the subsequent spread of zebra mussels has hadto depend on overland dispersal. In North America,recreational boating and fishing are thought to be theprimary overland vectors for the dispersal of zebramussels (Johnson and Carlton 1996; Padilla et al.1996; Schneider et al. 1998; Buchan and Padilla 1999;Johnson et al. 2001), but in Belarus, recreational motorboats are quite rare, and boats of any kind are seldomtransported between bodies of water. Although manyother potential dispersal mechanisms exist (Carlton1993), commercial fishing is most likely responsiblefor transporting mussels between the lakes in Belarus.Not only are zebra mussels associated with the pres-ence of fisheries, direct observations of fishing activ-ity indicate that they are capable of transporting zebramussels among lakes. Sweep-nets, used by fishermen,can harbor hundreds of zebramussel druses in an indi-vidual net (Karatayev 1983). Such fishing equipment isoften used in multiple lakes, and because zebra musselscan survive up to several weeks in wet nets (Deksbakh1935), zebramussels can be easily spread to other lakesin this manner. The government commercial fisheryfrom the 1960s to 1990s was very intensive. Severalfishery groups harvested fish from more than 400lakes.Although some lakes were harvested only annually,some were fished almost daily (Karatayev et al. 1999).

Waterfowl have been suggested to be a possiblevector for transporting zebra mussels as adults or aslarvae among unconnected waterbodies (CharlemagneI9l4; Reichholf and Windsperger 1972). Johnson andCarlton (1996) have experimentally shown that thismechanism is unlikely to spread zebramussels, and ourstudy supports their conclusion. Waterfowl are abun-dant and diverse in all of the lakes in Belarus. however.only a small fraction of these lakes have been invadedby zebra mussels during the past 200 years. Therefore,we do not expect waterfowl to be important vectors forthe transport of zebramussels to uninfected lakes.

Although the majority of the spread of zebramusselsdepends on overland dispersal vectors, not all inva-sions are independent events. While transport to an

individual isolated lake may be a stochastic and rareevent (Buchan 1997; Buchan and Padilla 1999), oncea lake is invaded, zebra mussels can easily spread todownstream lakes through the dispersal of their lar-vae which spend up to several weeks drifting in theplankton. For example, a group of l1 hydrologicallyconnected lakes in the Zapadnaya Dvina River basin(northwestern Belarus) were colonized between themid-1960s and the early 1980s. The invasion began in1964-1966 when zebra mussels appeared in DrivyatyLake, the largest lake in this group, and then spreaddownstream to the other 10 lakes (Lyakhnovich et al.1984). This could explain why zebra mussels werefound disproportionately on the southern bank com-pared to the northern bank of the Zapadnaya DvinaRiver. In Belarus, zebra mussels spread from southto north - downstream in the Zapadnaya Dvina Riverbasin. They were less likely to spread upstream andcolonize lakes on the right bank of the river. Similarly,in the Narochanskie Lake system in the Neman Riverbasin, zebra mussels were first detected in MyastroLake in 1984 (Ostapenya et al. 1994) and then spreaddownstream (<1km) into Naroch Lake where theywere found in 1989 (Ostapenya et al. 1993). However,we also found zebra mussels in lakes Myadel andVolchin which, although near the other lakes (2 andl2km, respectively), are a part of another drainagebasin. The mechanisms of these latter invasions arenot obvious.

As we have no historic information on the presenceor absence of zebra mussels for the majority of lakesstudied, it is difficult to estimate when zebra mus-sels colontzed each waterbody. However; data frommultiple surveys of individual lakes can give insightsinto the timing of an invasion. For example, zebramussels were not found in 1968-1969 in LukomskoeLake but were detected in a subsequent survey in 1972(Lyakhnovich et al. 1982; Karatayev 1983). Based onsimilar data, the colonization of 20 lakes, 7 reservoirs,and 3 rivers in Belarus has been documented since theend ofthe 1960s.

Once zebra mussels invade a waterbody, they gen-erally do not go extinct, except in areas suffering frompollution or high levels of anthropogenic eutrophi-cation. According to Kinzelbach (1992), zebra mus-sels were commonly found in the Middle Elbe Riverafter 1827 , but then disappeared due to water pol-lution. Anthropogenic eutrophication also appearsto have caused the extinction of zebra mussels insix Masurian lakes (Poland) between 1959 and 1988

2t9

(Stanczykowska and Lewandowski 1993). We foundonly one case where zebra mussels went extinct for anyperiod of time. Between l9l2 and 1986, zebra musselscolonized Boloiso Lake in the Zapadnaya Dvina Riverdrainage basin. At that time, it was a well-oxygenated,mesotrophic lake with good water quality and summertransparency >3m. Since the mid-1980s Boloiso hasbeen heavily polluted by metropolitan waste from thecity of Braslav (Karatayev et al. 1995) and has beentransformed into a hyper-eutrophic lake. Phosphateconcentrations have increased from 0.05mgl-l inl972to 0.25 mgl-l in 1986 and to 0.50 mg l-r in 1996;summer transparency has now decreased to 0.6 m. Inthe early 1990s zebra mussels were no longer foundin this lake. No other populations of zebra musselsin over 50 other lakes that have been sampled afterzebra mussels were first detected are known to havedisappeared.

Zebra mussels have proven to be very effectiveinvaders worldwide when transported by human activ-ities. Without the construction of canals and humanshipping activity, the spread of zebra mussels beyondtheir native waters would have been much slowerand more restricted. Much like an earlier invasionby Corbicula fluminea, another freshwater bivalve(McMahon 1982), the rapid spread of the zebramusselin North America over the past decade appears largelydue to downstream dispersal of larvae and the move-ment of commercial ships and barges within the hydro-logically connected lakes, rivers, and canals of thedrainage basins of the Mississippi and St. LawrenceRivers and the Laurentian Great Lakes (Johnson andCarlton 1996). The overland spread of zebra musselsis much slower (Johnson and Carlton 1996; Padillaet al. 1996; Buchan and Padilla 1999). Kraft andJohnson estimated that between 3Vo and 8%a of theinland lakes surrounding the Laurentian Great Lakesare being invaded each year although this rate is highlyvariable (0-20Va) among different regions (Kraft andJohnson 2000). Our study of Belarussian lakes andrivers provides much the same picture but over a muchlonger time scale, i.e., centuries rather than decades.Obviously, there are many differences between thesetwo systems, especially in terms of the relative impor-tance of different human-mediated dispersal mecha-nisms. However, this study offers rare information ofthe dispersal patterns of an invading aquatic species ata spatial scale for which we know very little (Johnsonand Padilla 1996). The rapid increase of the rangeof geographic extent of zebra mussels across Europe

220

during the past two centuries and across eastern NorthAmerica during the past decade has lead to its repu-tation of being a highly invasive species (Ludyanskiyetal. 1993). However, our data from Belarus, one of thecountries closest to the native range of the zebramussel,indicates that the invasion of European waters withinthat total range is slow, and far from over. More exten-sive examination of the geographic spread of zebramussels across the rest of Europe will greatly enhanceour understanding of how this and other aquatic exoticspecies spread.

Acknowledgements

This research was supported by grants from theUniversity of Wisconsin Sea Grant Institute undergrants from the National Sea Grant College program,National Oceanic and Atmospheric Administration,US Department of Commerce, and from the State ofWisconsin. Federal Grant NA90AA-D-SG469, andgrant number R/LR65. In the Republic of Belarus theresearch was supported by a grant from the Ministryof Education and Science Republic of Belarus, grantnumber 651/65.

References

Andrusov NI ( 1897) Fossil and recent Dreissenidae of Eurasia. TrudyS.-Petersburgskago Obshchestva Estesrvoispytatelei 25: l-6g3 [inRussianl

Bossenbroek JM, Kraft CE and Nekola JC (2001) pre{iction of long-distance dispersal using gravity models: zebra mussel invasion ofinland lakes. Ecological Applications I l: 1778-178g

Buchan LAJ (1997) Predicting Invasion patterns of NonindigenousAquatic Species. PhD thesis. Department of Zoology, Universityof Wisconsin-Madison, Madison, Wisconsin

Buchan LAJ and Padilla DK (1999) Estimaring the probabilityof long-distance overland dispersal of invading aquatic species.Ecological Applications 9: 254-265

Carlton JT (1993) Dispersal mechanisms of the zebra musselDreissena polymorpha. In: Nalepa TF and Schloesser DW (eds)Zebra Mussels: Biology, Impacts, and Control, pp 677-697.Lewis Publishers, Ann Arbor, Michigan

Charlemagne EV ( 1914) To the question of rhe role of birds in dis-persal of bivalve mussels. Works of the Dnieprovskaya BiologicalStation l:49-51 [in Russian]

Deksbakh NK (1935) Spread of Dreissena polymorpha pallas(Mollusca) in the European part of the USSR and the factorsresponsible for their spread. Byulleten Moskovskogo ObschestvaIspytatelej Prirody, Ordelenie Biologii 44: 153-163 [in Russian]

Drako MM (1953) Species composition quanritarive and foddermeaning of bottom fauna (benthos) of fishine lakes of BSSR.

Candidate Dissertation, Department of Invertebrate Zoology,Belarussian State University, Minsk, Belarus, 259 pp [in Russian]

Drako MM and Gavrilov SI (1972) Species composition quantirativeand fodder meaning of bottom fauna in Ushachskaya lakes sys-tem. Animal Kingdom of Belarussian Lakeland, Minsk. Issue 2:97-108 [in Russian]

Fienberg SE (1970) The analysis of multidimensional contingencytables. Ecology 51: 419433

Horvath TG and Lamberti GA (1997) Drifting macrophytes as amechanism for zebra mussel (Dreissena polymorpha) invasion oflake-outlet streams. American Midland Naturalist 138: 29-36

Horvath TG, Lamberti GA, Lodge DM and peny WL (1996) Zebramussel dispersal in lake-stream systems: source-sink dynam-ics? Journal of the North American Benthological Society 15:564-575

Johnson LE and Carlton JT (1996) Post-establishment spread inlarge-scale invasions: dispersal mechanisms of the zebra musselDreissena polymorpha. Ecology 7l: 1686-1690

Johnson LE and Padilla DK (1996) Geographic spread of exoticspecies: ecological lessons and opportunities from the invasion ofthe zebra mu ssel Dreissena polymorpha. Biological Conservation18:23-33

Johnson LE, Ricciardi A and Carlton JT (2001) Overland disper-sal of aquatic invasive species: a risk assessment of transientrecreational boating. Ecological Applications I l: 1789-1799

Karatayev AY (1983) Ecology of Dreissena polymorpha pallas andits effects on macrozoobenthos of the thermal power plant'scooling reservoir. Candidate Dissertation, Zoology Institute ofAcademy of Science Belorussian SSR, Minsk, 153 pp [in Russian]

Karatayev AY (1988) Ecology of Macroinverrebrates of CoolingReservoirs of Belarus (paper 875-888 Dep). VINITI press,

Minsk, 178 pp [in Russian]Karatayev AY (1992) The structure and function of benthic and

periphyton communities in cooling water reservoirs. DoctoralDissertation,Zoology Institute of Academy of Science RepublicBelarus, Minsk, 331 pp [in Russian]

Karatayev AY and Burlakova LE (1995) The role of Dreissena inlake ecosystems. Russian Journal of Ecology 26:207-2ll

Karatayev Al Lyakhnovich VP and Reznichenko OG 0990)Quantitative study of the density, biomass and abundancedynamic. In: Shkorbatov GL and Starobogarov yI (eds) Methodsfor Study of Bivalvian Molluscs, Yol219, pp 172-178. TrudyZoologicheskogo Instituta [in Russian]

Karatayev Al Lyakhnovich VP, Afanasiev SA, Burlakova LE,Zakutsky VP, Lyakhov SM, Miroshnichenko Mp, Moroz TG,Nekrasova MY Skalskaya IA, Kharchenko TG and protasov AA(1994) The place of species in ecosystems. In: Starobogatov JI(ed) Freshwater Zebra Mussel Dreissena polymorpha (pall.)(Bivalvia, Dreissenidae). Systematics, Ecology, practical

Meaning, pp 180-195. Nauka Press, Moscow [in Russian]Karatayev AY, Samoilenko VM, Burlakova LE, Kartashevich ZK

and Rachevsky AN (1995) Recommendations for Restorationof Lakes with High Anthropogenic Influence. Belarussian StateUniversity Press, Minsk,73 pp [in Russian]

Karatayev Al Burlakova LE and Padilla DK (1997) The effects ofDreissena polymorpha (Pallas) invasion on aquatic communitiesin Eastern Europe. Journal of Shellfish Research 16: l8j-203

Karatayev AY, Burlakova LE and Padilla DK (1998) physical factorsthat limit the distribution and abundan ce of Dreissena polymorpha(Pall.). Journal of Shellfish Research t7: l2t9-1235

T

Karatayev AY, Rudakovskiy IA, Prischepov PG and Burlakova LE( 1999) The fish productivity of Belarussian lakes. The Present Sta-tus and Perspectives of Developmentof Aquaculture. Proceedingsof the International Conference (Gorky, Belarus), pp 22-23 [inRussianl

Kerney MP and Morton BS (1970) The distribution of Dreissenapolymorpha (Pallas) in Britain. Journal of Conchology 27:97-100

Kinzelbach R (1992) The main features of the phylogeny and disper-sal of the zebra mussel Dreissena polymorpha. In: Neumann Dand Jenner HA (eds) The Zebra Mussel Dreissena polymorpha:Ecology, Biological Monitoring and First Applications in theWater Quality Management, pp 5-17. Gustav Fisher, Stuttgart

Kraft CE and Johnson LE (2000) Regional differences in rates andpatterns of North American inland lake invasions by zebra mus-sels. Canadian Journal of Fisheries and Aquatic Sciences 57:993-1001

Kraft CE, Sullivan PJ, Karatayev AY, Burlakova LE, Nekola JC,Johnson LE and Padilla DK (2002) Landscape pattern of anaquatic invader, Dreissena polymorpha: assessing dispersalextent from spatial distribution. Ecological Applications 12:149-759

Kurlovich NN and Serafimovich AA (1981) Lakes resources ofBelarus. Vestnik Belarusskoso Universiteta. Seriva 2. 1: 68-72

[in Russian]Ludyanskiy ML, McDonald D and MacNeill D (1993) Impact of the

zebra mussel, a bivalve invader. BioScience 43: 533-544Lvova AA (1980) Ecology of Dreissena (Dreissena polymorpha

po lymo rp ha (Pall.)). Trudy Vsesoyuznogo GidrobiologicheskogoObschestva 23: l0l-l l9 [in Russian]

Lyakhnovich VP, Gavrilov SI, Karatayev Al Karatayeva IV andNekhaeva TI (1982) Long-term changes in macrozoobenthosof Lukomskoe Lake. Vestsi Akademii Navuk Belarusi. SeriyaBiyologichnikh Navuk l: 9l-93 [in Belorussian]

Lyakhnovich VP, Karatayev AY and Tischikov GM (1984)Distribution of Dreissena polymorpha Pallas in Belarus. Proceed-ings of the All Union Conference on Model Species of AquaticInvertebrates, pp l6-20. VINITI Press, Vilnius [in Russian]

Lyakhnovich VP, Karatayev AY, Mitrakhovich PA, Guryanova LVand Vezhnovets GG ( 1988) Productivity and prospects for utiliz-ing the ecosystem of Lake Lukoml, thermoelectric station coolingreservoir. Soviet Journal of Ecology 18:255-259

McMahon RF (1982) The occurrence and spread of the introducedAsiatic freshwater clam, Corbicula fluminea (Muller), in NorthAmerica. Nautilus 96: 134-145

Minchin D (1998) Distribution of the zebra mussel Dreissenapolymorpha (Pallas) in Ireland, 1997. Irish Naturalists'Journal26:3842

Mitropolsky VI and Mordukhai-Boltovskoi FD (1975) Zoobenthos.In: Methods for Study Ecosystems of Inland Reservoirs,pp 158-170. Nauka Press, Moscow [in Russian]

Mordukhai-Boltovskoi FD (1960) Caspian Fauna in the Azov andBlack Sea Basins. Academia Nauk Press, Moscow, 288 pp [inRussianl

Morton B (1969) Studies on the biology of Dreissena polymorphaPall.4. Habits, habitats, distribution and control. WaterTreatmentand Examination 18: 233-240

Ostapenya AP, Kovalev AA, Zhukova TV Mikheeva TM,Kryuchkova NM, Babitsky VA, Kovalevskaya RZ,

22r

Kostyukevich SB, Inkina GA, Makarevich TA, Zhukov EP,Ikonnikov VF, Samusenko AM, Orlovsky AF, Rachevsky ANand Jakushko OF (1993) Ecological Passport of Naroch Lake.Ekomir Press, Minsk, 95 pp lin Russian]

Ostapenya AP, Kovalev AA, Mikheeva TM, Babitsky VA,Zhukova TV Kryuchkova NM, Kovalevskaya RZ,Kostyukevich SB, Inkina GA, Makarevich TA, Zhukov EP,Ikonnikov VF, Samusenko AM, Orlovsky AF, Rachevsky ANand Jakushko OF (1994) Ecological Passport of Myastro Lake.Ekomir Press, Minsk, 45 pp [in Russian]

Ovchinnikov IF (1933) Contemporary spread of Dreissenupolymorpha Pallas (Mollusca) in the BSSR - zoogeographicalessay. Trudy Instituta Zoologii Akademii Nauk SSSR I :365-373

[in Russian]Padilla DK, Chotkowski MA and Buchan LAJ (1996) Predicting

the spread of zebra mussels (Dreissena polymorpha) to inlandwaters using boater movement patterns. Global Ecology andBiogeography Letters 5: 353-359

Ramcharan CW Padilla DK and Dodson SI (1992a) Models topredict potential occurrence and density of the zebra mussel,Dreissena polymorpha. Canadian Journal of Fisheries andAquatic Sciences 49: 26ll-2620

Ramcharan CW, Padilla DK and Dodson SI (1992b) A multivari-ate model for predicting population fluctuations of Dreissenapolymorpha in North American lakes. Canadian Journal ofFisheries and Aquatic Sciences 49: 150-158

Reichholf J and Windsperger W (1972) Erste Funde derWandermuschel (Dreissena polymorpha) am Unteren Inn.Anzeiger der Ornithologischen Gesellschaft in Bayernl l : 3 2 3

Rossolimo LL (1911) Change in Limnetic Ecosystems underAntropogenic Impact. Nauka Press, Moscow, 144 pp

[in Russian]Schneider DW Ellis CD and Cummings KS (1998) A trans-

portation model assessment of the risk to native mussel com-munities from zebra mussel spread. Conservation Biology l2:788-800

Skorikov AS (1903) Recent distribution of Dreissena polymorphaPallas in Russia. Ezhegodnik Volzhskoi Biologicheskoi Stantsii4:205-250 [in Russian]

Stanczykowska A (197'7) Ecology of Dreissena polymoryha(Pall.) (Bivalvia) in lakes. Polskie Archiwum Hydrobiologii 24:46 l -530

Stanczykowska A and Lewandowski K (1993) Thirty years of stud-ies of Dreissene polymorpha ecology in Mazurian Lakes ofNortheastern Poland. In: Nalepa TF and Schloesser DW (eds)

Zebra Mussels: Biology, Impacts, and Control, pp 3-33. LewisPublishers, Ann Arbor, Michigan

Starobogatov JI and Andreeva SI (1994) Distribution and history.In: Starobogatov JI (ed) Freshwater Zebra Mussel Dreissenapolymorpha (Pall.) (Bivalvia, Dreissenidae). Systematics,Ecology, Practical Meaning, pp 47-55. Nauka Press, Moscow

[in Russian]Winberg GG ( I 960) Primary Production of Waterbodies. Academiya

Nauk BSSR Press, Minsk,329 pp [in Russian]Yakushko OF (1971) Belarussian Lakeland. Visheishaya Shkola

Press, Minsk, 335 pp [in Russian]Zhadin VI ( 1946) The traveling shellfish Dre issena. Priroda 5:29-3'7

[in Russian]