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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 America1

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 M A Y

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 bytwo genetically and morphologically distinct species of Dreissena. Thezebra mussel {Dreissena polymorpha) became established in Lake St.Clair of the Laurentian Great Lakes in 1986 and spread throughout easternNorth America. The second dreissenid, termed the quagga mussel, hasbeen identified as Dreissena bugensis Andrusov, 1897. The quagga occursin the Dnieper River drainage of Ukraine and now in the lower GreatLakes of North America. In the Dnieper River, populations of D. poly-morpha have been largely replaced by D. bugensis; anecdotal evidenceindicates that similar trends may be occurring in the lower LaurentianGreat Lakes. Dreissena bugensis occurs as deep as 130 m in the GreatLakes, but in Ukraine is known from only 0-28 m. Dreissena bugensisis more abundant than D. polymorpha in deeper waters in Dneiper Riverreservoirs. The conclusion that North American quagga mussels have alower 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 bothdreissenids have acclimated to salinities higher than North American pop-ulations; eventual colonization into estuarine and coastal areas of NorthAmerica cannot be ignored.

1 From the Symposium Biology, Ecology and Physiology of Zebra Mussels presented at the Annual Meetingof the American Society of Zoologists, 4-8 January 1995, at St. Louis, Missouri.

271

272 E. L. MILLS ET AL.

INTRODUCTION

North America's Great Lakes have re-cently been invaded by two species ofDreissena (Rosenberg and Ludyanskiy,1994; Spidle et al, 1994). The zebra mussel(Dreissena polymorpha) became estab-lished in Lake St. Clair of the LaurentianGreat Lakes by 1986 (Hebert et al, 1989)and has spread rapidly from the GreatLakes eastward through the Mohawk andHudson River systems and southwardthrough the Mississippi River drainage. InAugust of 1991, specimens of a morpho-logically and genetically distinct Dreissena,termed the quagga mussel, were discoveredin the Erie Canal and Lake Ontario wherethey coexisted with more numerous D.polymorpha (May and Marsden, 1992). Thequagga mussel, identified as Dreissena bug-ensis Andrusov, 1897 (Rosenberg and Lu-dyanskiy, 1994; Spidle et al, 1994), has adistinctive shell with convex ventral marginand lacks the carina between the ventral andlateral shell surfaces resulting in a roundedcross-section. Dreissena polymorpha has aflat or concave ventral margin and pro-nounced carina so that the ventral edge ofthe shell is perpendicular to the lateral, al-lowing the zebra mussel to remain uprightwhen placed on a flat surface. Although D.polymorpha is presently the prevailing spe-cies in North America, D. bugensis haslargely replaced D. polymorpha in theDnieper River drainage system in Ukraine(Pligin, 1979). In North America, the quag-ga mussel is primarily restricted to LakeErie, Lake Ontario and the St. LawrenceRiver although one sighting of D. bugensishas been confirmed outside the Great Lakesbasin in the Mississippi River near St. Lou-is, MO (O'Neill, 1995).

This paper summarizes current informa-tion about the taxonomy, geographic distri-bution, genetics, physiology, and ecologyof the quagga mussel (£>. bugensis) and re-lates this information to other dreissenids inNorth America and Ukraine when possible.

IDENTIFICATION OF THE QUAGGA MUSSEL ASDREISSENA BUGENSIS

At the time of the discovery of the quag-ga mussel in North America, the systemat-

ics of Dreissena were poorly understood,with no clear consensus as to the numberof species in the genus nor their distribu-tions. As a result, biologists were not im-mediately able to determine the taxonomicidentity of the quagga mussel. The quaggamussel was known to have originated in theOld World, because variation at proteincoding loci matched that of tissue samplesfrom the Dnieper River, where only twodreissenid species are present: Dreissenapolymorpha and D. bugensis (Zhadin,1952). Rosenberg and Ludyanskiy (1994)reviewed the systematic literature on Dreis-sena and examined type material in the Pa-leontological Institute in Moscow. Theyfound that the quagga mussel correspondsto the original description and type speci-mens of D. bugensis Andrusov, 1897. Thus,genetic analysis and examination of the pri-mary systematic literature firmly estab-lished the identity of the North Americanquagga mussel as D. bugensis (see reviewby Marsden of genetics for Dreissena inthis volume).

Russian classifications have treated D.bugensis as a full species or as a subspeciesof D. rostriformis Deshayes, 1838. Accord-ing to Rosenberg and Ludyanskiy (1994),living specimens of Dreissena bugensis canbe distinguished from D. rostriformis bytheir larger size (reaching 38 mm comparedto 23 mm), more pronounced byssalgroove, generally less compressed shell,and a distinct color pattern. Dreissena bug-ensis typically occurs in freshwater in Rus-sia in salinities up to 1 ppt (Nevesskaya,1965) while D. rostriformis does not occurin freshwater and is restricted to the middleand southern Caspian Sea, in salinities upto 12.7 ppt (Zhadin, 1952). While Marelli(1991) recently suggested that D. bugensisand D. polymorpha are synonymous, mostrecent authors consider them to belong todifferent subgenera, and their fossil recordsclearly indicate different lineages (Taktak-ishvili, 1973; Babak, 1983; Nuttall, 1990).

The creation of putative zebra X quaggamussel hybrids in the laboratory by poolinggametes collected after exposing adults toserotonin has recently been reported, indi-cating that interspecies fertilization eventsmay be possible (Nichols and Black, 1994).

BIOLOGY AND ECOLOGY OF QUAGGA MUSSELS 273

These putative hybrid larvae have not beensuccessfully reared, however, indicatingthat their (1) viability may be limited or (2)that these were single species haploid lar-vae. Evidence for species-specific sperm at-tractants exists (Miller, 1994) suggestingthat interspecific fertilization events may berare in nature. Further, electrophoretic sur-veys of loci diagnostic between zebra andquagga mussels have failed to find evidenceof adult hybrids in natural populations inLake Ontario and Lake Erie (Spidle et al.,1995), suggesting that if interspecific fertil-ization does occur, and if offspring of thosefertilization events survive to adulthood,such hybrid individuals do not constitute ameasurable proportion of the dreissenidcommunity.

GEOGRAPHIC DISTRIBUTION

Two populations of D. bugensis areknown to exist in the world today, in theUkraine and the Laurentian Great Lakes. Inthe Dnieper River drainage of the Ukraine(Fig. 1), D. bugensis was first discovered inthe Bug portion of the Dnieper-Bug Estuarynear Nikolaev by Andrusov (1890), whonamed the species in 1897. Since the 1940s,the quagga mussel has spread into the Dnie-per River drainage to regions that earlierhad only D. polymorpha. Fig. 1 illustratesthe range expansion of D. bugensis in theDnieper and Bug River systems during theperiods of 1950-53, 1970-73, and 1990-1992. Until the 1940s, D. bugensis wasfound only in the South Bug River and thelower Ingulets River (Andrusov, 1890,1897; Zhadin, 1952; Zhuravel', 1951); itwas absent from both the Dnieper portionof the Dnieper-Bug estuary and the lowerDnieper River (Markovskiy, 1954; Olivari,1971; Moroz; 1993). In 1941, D. bugensiswas found in the Zaporozh'ye Reservoir,the first reservoir built on the Dnieper River(Fig. 1A). As reservoirs such as the Kak-hovka (Markovskiy, 1954), Dneprodzer-zhinsk, Kiev, and Kanev (Pligin, 1984,1985) were built in the 1950s and 1960s,D. polymorpha invaded first and D. bug-ensis appeared later (Fig. 1 B). By 1990-92, D. bugensis had spread to the Pripyat'River delta which is currently its northern-most range (Fig. 1 C). Between 1964 and

1989, D. bugensis spread approximately500 km northward, as well as east and souththrough canals; it now occurs in almost alllarge and medium Dnieper reservoirs in theeastern and southern regions of Ukraine andthe deltas of Dnieper River tributaries. Lessinformation is available on the presence ofD. bugensis in Dnieper River tributaries,but it dominates the macrobenthos of smallreservoirs on the Ros' River, 200 km fromits confluence with the Dnieper River.Dreissena bugensis is absent from the del-tas of small rivers and estuaries on theBlack Sea to the west of the Dnieper-Bugestuary (Moroz, 1993). The quagga hasbeen reported in the Dniester River basin(Shevtsova, personal communication, 1994)but is absent in the Danube River and itscanals (Grossu, 1993).

The first sightings of the quagga musselin the Laurentian Great Lakes were in Sep-tember 1989, when one quagga was foundnear Port Colborne, Lake Erie (Fig. 2)(Mills et al., 1993), although the recogni-tion of the quagga type as a distinct speciesdid not occur until 1991 (May and Mars-den, 1992). By the spring of 1993, the dis-tribution of D. bugensis in the LaurentianGreat Lakes was from the central basin ofLake Erie to the St. Lawrence River at Que-bec City. In 1992, quagga mussels were ab-sent in Lake St. Clair, the Detroit River,western Lake Erie, the Erie-Barge Canal,Oneida Lake, the Mohawk River, the Hud-son River, and Cayuga and Seneca Lakes ofNew York's Finger Lakes although thesewater bodies all contained D. polymorpha(Mills et al., 1993; Dermott and Munawar,1993). In the fall of 1994, however, the firstquaggas were sighted on intake structuresof electric power generating stations in Ca-yuga and Seneca Lakes (R. Tuttle, NewYork State Gas & Electric, Binghamton,NY, personal communication). The firstconfirmation of quaggas outside the GreatLakes basin was made in the MississippiRiver between St. Louis, MO and Alton, IIin 1995 (O'Neill, 1995).

ENVIRONMENTAL LIMITS

The presence of two genetically distinctspecies of Dreissena in the LaurentianGreat Lakes and in the Ukraine raises the


A t


'Albany

FIG. 2. Locations of quagga (Q) (Dreissena bugensis) and zebra (Z) (Dreissena polymorpha) in the lower GreatLakes and inland waterways of New York State during 1992. • = quagga and zebra mussel absent; O = quaggaand/or zebra mussel present. Adapted after Mills et ai, 1993.

possibility that they have different habitatpreferences and environmental limits lead-ing to differential range expansion. Infor-mation about the distribution of both spe-cies in North America and Eurasia providescircumstantial evidence that D. polymorphaand D. bugensis may have different toler-ances to salinity and temperature.

Salinity toleranceThe range of salinity levels inferred to

limit D. polymorpha in Eurasia is quitewide, from 2 to 12 ppt in inland seas, butonly 0.5 ppt in estuaries on the Atlanticcoast of the Netherlands (see review inStrayer and Smith, 1993). Exposure to 1.6ppt NaCl for a week was observed to befatal to zebra mussels in one set of labora-tory experiments (Horohov et al., 1992),while other tests have shown perturbationsin respiration of D. polymorpha, but nomortality, resulting from increasing salinityto 10 ppt (Karpevich, 1947). If either Dreis-

sena species exhibits tolerance to salinitythey could colonize estuarine and coastalareas. Side by side comparisons of salinitytolerance in North American populations ofD. polymorpha and D. bugensis showedthat neither species could survive salinitylevels greater than 5 ppt (Spidle, 1994). Nointerspecific difference in survival timewhen exposed to salinity was shown (Spi-dle, 1994). The negative effect of salinityon survival is enhanced at warmer temper-atures (5°C to 20°C), with mussels of bothspecies having a much shorter survival timeat all salinity levels (Spidle, 1994) com-pared to Eurasian populations. For NorthAmerican quagga, there is no evidence thatthe salinity tolerance of the quagga musselis any greater than that of the zebra mussel.

The main factor controlling Dreissenadistribution in the Dnieper-Bug estuary iswater salinity (Grigoryev, 1968, Alexenko,1991, Moroz, 1993). In the lower DnieperRiver, salinity is typically about 0.3 ppt,

FIG. 1. Range expansion of Dreissena bugensis (stripe pattern) in the Dnieper River drainage between 1950and 1992. Panel A: 1950-53; Panel B: 1970-73; Panel C: 1990-92. Numbers identify location of reservoirs: 1= Kiev; 2 = Kanev; 3 = Kremenchug; 4 = Dneprodzerzhinsk; 5 = Zaporozh'ye; 6 = Kakhovka; and 7 =Dnieper-Bug Liman.


whereas in the Dnieper-Bug estuary, de-pending on the flow of the Dnieper River,it varies from 0.5 to 10 ppt. Dreissena poly-morpha is more tolerant of increases in sa-linity than is D. bugensis (Alexenko, 1991;Moroz, 1993; Antonov and Shkorbatov,1990; and Orlova, 1987).

Dreissena polymorpha in the lowerDnieper was found to have maximumgrowth at salinities of 1-1.5 ppt, whereasin the Dnieper-Bug estuary maximumgrowth occurs at 1-3 ppt (Markovskiy,1954). The maximum salinity in which D.polymorpha was found in the early 1950swas 8 ppt. In the lower Dnieper River andthe Dnieper-Bug estuary, more than 50% ofthe mussel population was D. polymorphaat salinities ranging between 0.0-1 ppt asCl~, whereas D. bugensis dominated at sa-linities between 0.00-0.02 ppt (Aleksenko,1991). The maximum total salinities atwhich each species was found were 7.6 and4.0 ppt, respectively. These findings con-trast with Strayer and Smith (1993) whopredicted that the North American distri-bution of D. polymorpha would be limitedto a maximum salinity (marine ion com-position) of 2 ppt. Apparently populationsof Dreissena in Ukraine, which have ex-perienced more generations, show greateracclimation to salinity extremes than morerecently colonized dreissenids in NorthAmerica.

Distribution of D. bugensis and D. poly-morpha in the Dneiper-Bug estuary de-pends on Dnieper River run-off and salinity(Alexsenko, 1991; Moroz, 1993). Thesetwo parameters are strongly related: whenthe annual run-off is high, the estuary be-comes less saline; when annual runoff islow, saline water from the Black Sea in-trudes freshwater areas, killing off Dreis-sena. Dreissena polymorpha increases inabundance relative to D. bugensis as salin-ity increases. For example, in the low pre-cipitation year of 1984, with high salinitylevels, no D. bugensis were observed, whilein the high precipitation year of 1981, whensalinity was low, living D. bugensis pre-dominated over D. polymorpha. The re-verse situation was recorded in 1986-1987.

Laboratory experiments using UkrainianDreissena show that both species can ac-

climate to higher salinities; at 7-15°C andover a 40-day period, D. bugensis accli-mated to a salinity of 5 ppt (survival 68%),and D. polymorpha to 8 ppt (survival 70%)(Aleksenko, 1991). At the same tempera-ture over a 10-day period, mortality wasmore than 90% beginning from a salinity of8 ppt for D. bugensis and 11 ppt for D.polymorpha. For mussels exposed to tem-peratures of 18-21°C for over a 40 day pe-riod, D. bugensis and D. polymorpha accli-mated to salinities of 4 ppt (survival 91%)and 6 ppt (survival 100%), respectively.Subsequent salinities of 5 ppt and 8 pptwere lethal within 10 days to both species.

Salinity tolerances for D. polymorphafrom the lower Dnieper River and thosefrom the estuary have been shown to bedifferent (Aleksenko, 1991). These studiesconcluded that estuarine D. polymorpha cansurvive higher salinities than riverine D.polymorpha, apparently because they accli-mated to increased salinities in the estuaryduring years of low flow of the DnieperRiver, when the salinity of the estuary wasusually 1-3 ppt higher. Similar data wererecorded for D. polymorpha and D. bug-ensis inhabiting the main flow of the LowerDnieper River and the Dnieper-Bug estuary(Table 1), concluding that D. polymorphawas the more salinity tolerant of the twospecies (Antonov and Shkorbatov, 1990).

The acclimation of D. polymorpha to lo-cal ecological conditions has been shown inthe Volga River in Russia (Antonov andShkorbatov, 1983). Here, the effects of tem-perature and salinity on whole animals andciliated gill epithelium of D. polymorphataken from six river populations indicated1) the population most tolerant to salinityand temperature changes was the southern-most, nearest to the Caspian Sea; and 2) theleast resistant population was the northern-most, farthest from the sea.

Temperature toleranceNorth American populations.—The up-

per thermal limit of the North Americanquagga mussel is lower than that of the ze-bra mussel. Three estimates of temperaturetolerance have shown that increasing accli-mation temperature will increase the tem-perature tolerance of individual mussels.


TABLE 1. Salinity tolerance of Dreissena bugensis and D. polymorpha when acclimated to freshwater and 4ppt salinity and tested at four different salinities (after Antonov and Shkorbatov, 1990).

conditions

Freshwater

4 ppt salinity

Dreissenid species

River D. polymorphaEstuarine D. polymorphaD. bugensis

River D. polymorphaEstuarine D. polymorphaD. bugensis

4

606835

798763

Salinity (ppt)

6

Percent active

233713

637323

8

272913

747720

The three test techniques included introduc-ing mussels directly into heated water(Domm et al, 1993), comparing survivaltime at constant elevated temperature fol-lowing a gradual increase of temperaturefrom ambient (Spidle, 1994), and experi-mental determination of upper lethal tem-perature by increasing temperature fromambient at varying rates to a lethal temper-ature (Spidle, 1994). Results of these ex-periments indicate that some of the ob-served depth stratification in the lowerGreat Lakes between the species may bedue to thermal stress in the quagga musselabove certain depths.

The quagga mussel has been shown tohave a greater instantaneous mortality ratethan the zebra mussel across acclimationtemperatures that were eventually lethal toboth species (Domm et al, 1993). The ze-bra mussel has been demonstrated to sur-vive indefinitely at 30°C (McMahon et al,1994; Spidle, 1994). Conversely, the quag-ga mussel shows rapid mortality at 30°C(Fig. 3; Spidle, 1994).

In the Great Lakes, an important concernis the susceptibility of the quagga mussel tomechanisms that have been found to suc-cessfully control zebra mussels in water in-takes. Recirculating hot water through theintake pipe has been shown to be effectivein reducing zebra mussel colonization of in-take pipes. Models have been generated topredict the effect of different rates of tem-perature increase on instantaneous mortalityrate of zebra mussels for given acclimationtemperatures (McMahon et al, 1993). Sim-ilar tests conducted with quagga musselshave demonstrated that the LT50 (instanta-neous temperature required to cause 50%

mortality) of D. bugensis is from 2-5°Clower than that of D. polymorpha (Table 2).In spite of the difference in LT50, theLT100 (instantaneous temperature requiredto cause 100% mortality) predicted from alogistic regression model is not statisticallydifferent between the species. The lack ofdifference in LT100 indicates that eventhough most quaggas die at lower temper-atures than will kill zebra mussels, a fewexceptional quagga mussels may be as tol-erant of elevated temperature as is the zebramussel (Fig. 4).

Evolutionary studies suggest that the op-timal temperature of an organism will co-evolve with its thermal maximum, and inthe same direction (Huey et al, 1991; Mar-tins and Garland, 1991). Because the NorthAmerican quagga mussel clearly has a low-er thermal maximum than the zebra mussel,it is possible to assume that the quaggamussel has a lower optimal temperature forfeeding and reproduction than does the ze-bra mussel, which may explain the depthstratification observed to partially separateD. bugensis and D. polymorpha in LakesErie and Ontario. A lower thermal optimumfor the quagga mussel would explain theobservation that D. bugensis has not beenfound in large numbers outside of the GreatLakes nor was it observed in the Erie Canalin repeated surveys in 1992 (Mills et al,1993).

Information is not yet available on therelative response of quagga mussels and ze-bra mussels to extreme low temperatureconditions. Recent theory in the evolutionof stress response points out that the criticalthermal maximum and minimum appear toevolve independently rather than together


mm

Surv

ive

co

Per

100 j

9 0 - •

8 0 -

70-

60 - -

50 -

4 0 -

30-

20 -

1 0 -

0 •

• - 5C: ao - 5C: b•—15C: ao— 15C:b»—20C: a

*>—20C: b

Time (Days)FIG. 3. Percent survival of quagga mussels (Dreissena bugensis) through time in replicated trials (a & b) whenexposed to water temperatures of 30°C. The numbers 5, 15, and 20 indicate prior acclimation temperature in

(Huey and Kingsolver, 1989; Hoffmann andParsons, 1991; Huey and Kingsolver,1993). Even though the zebra mussel ismore tolerant of warm water than the quag-ga mussel, the response of the two speciesto cold water must be determined in labo-ratory experiments which test both the crit-ical minimum temperature and the mini-mum temperature for essential activitiessuch as feeding and reproduction for eachspecies of Dreissena.

Ukrainian populations.—The distribu-tion of D. bugensis along the Dneiper Riveris reflective of a north to south gradientwith the warmest temperatures occuring inthe southern reaches of the basin. The max-imum summer temperature in the Dnieper-Bug estuary is usually 24-25°C offshoreand 30-32°C in the littoral zone (Zhurav-leva, 1988). In the Dnieper reservoirs, themaximum summer temperatures are lower:23.5°C in Kahovhka Reservoir (the south-ernmost) and 21°C in Kiev Reservoir (thenorthernmost) (Shevchenko, 1989). Ac-cording to Shevtsova (1968), increasing

water temperatures from north to south cor-relates with the quagga's more southerly oc-currence in the Dneiper River basin. Thisfinding contrasts with earlier suggestions inthis paper that the North American D. bug-ensis may be a cold deep-water form (Der-mott and Munawar, 1993; Mills et al.,1993).

The effects of elevated temperatures onDreissena in Ukraine populations haveshown the onset of mortality to be 27-27.3°C for D. polymorpha and 28.TC forD. bugensis (Antonov and Shkorbatov1990). Fifty percent mortality was recordedat 28.2-28.4°C and 29.3°C for each species,respectively (Antonov and Shkorbatov1990). As the water temperature increased,the first D. polymorpha with fully openedshells were observed at 28.6°C, whereas thefirst D. bugensis with fully open shells wereobserved at 29.7°C. Antonov and Shkor-batov (1990) reported the upper lethal tem-perature for Dreissena as 32-35°C, but didnot give separate lethal ranges for each spe-cies.


In contrast to the results of Antonov andShkorbatov (1990), the results of Domm etal., (1993) showed that North American D.polymorpha's upper temperature limit wassignificantly higher than that of D. bugen-sis. The average survival time of D. poly-morpha at a constant, eventually lethal,temperature was also significantly longer.Differences in thermal resistance in D.polymorpha are commonly reported in theliterature; the results depend strongly onlength of thermal acclimation and it is dif-ficult to compare temperature resistancedata obtained from mussels collected in dif-ferent geographic locations (McMahon etal, 1994).

ECOLOGY

Depth

The depths at which quagga mussels andzebra mussels have been observed in LakeOntario are among the deepest (>100 m)ever recorded for the genus Dreissena(Mills et al., 1993). In Polish lakes, zebramussels generally reach maximum densitiesbetween 2 and 4 m depth and are sparse atdepths >8 m (Stanczykowska, 1977; Stan-czykowska et al., 1983; Stanczykowska andLewandowski, 1993). Similar patterns havebeen noted for European lakes (Wesenberg-Lund, 1939; Dunn, 1954) although Walz(1973) found adult zebra mussels at a depthof 55 m and zebra mussel larvae at depthsbetween 120 and 140 m. In Lake Ontario,both quagga and zebra mussels coexist atdepths of 8-110 m, with only D. bugensisfound at depths of 130 m. In the easternbasin of Lake Erie, Dermott and Munawar(1993) found D. bugensis outnumbered ze-bra mussels by 14 to 1 in the deeper off-shore waters and colonized soft substratabeyond depths of 40 m. In both Lakes On-tario and Erie, the proportion of D. bugensisincreased with depth and declined as watertemperature increased, suggesting that thisdreissenid is possibly a cold water form.The dominance by quagga mussel in pro-fundal areas of North American lakes in-dicates that the impacts on food webs bydreissenids is not limited to shallow nearshore regions of lakes.

Dreissena bugensis is much more abun-

TABLE 2. LT50 and LT100 estimated from logit mod-els, and SM100 observed for each treatment in theacute temperature stress experiment.*

Species

qzqzqzqzqzqzqzqzqzqzqzqz

Rate

606060606060303030303030151515151515555555

Acclima-tion

ature

55

15152020

55

15152020

55

15152020

55

15152020

LT50

30.86935.00334.05635.66935.06336.20133.05736.01434.81536.09935.479*36.444*34.09936.30634.94937.19234.63437.08533.49137.00136.10237.20336.442X

SM100

35373537363836383737373837383939373838393939NANA

LT100

39.16639.82234.33538.75535.33240.27639.45139.71736.93138.94036.961**42.276**38.86941.00539.41039.34839.79337.65242.76739.26140.22340.48945.195X

* Species is coded as q = quagga and z = zebra;rate is given as minutes per °C increase; x indicates nomortality occurred within the range of observation. NAindicates 100% mortality was not reached. Quagga andzebra mussels have different predicted LT50 values (p< 0.05) except where indicated by * and similar pre-dicted LT100 values (p > 0.05) except where indicatedby ** (From Spidle, 1994).

dant in deep waters in the Dnieper reser-voirs than D. polymorpha (Zhuravel,1967a) which is consistent with observa-tions in North America. Pligin (1989) con-firmed this for the Dneiper River system,showing that D. bugensis comprised 99—100% of the mollusks in the deepest areasof reservoirs, while in littoral zones D.polymorpha comprised 15—20%. Further,the first sightings of D. bugensis in the newDnieper River reservoirs (Kremenchug,Kiev, and Kanev) in the 1950s to the 1970swere made in the deeper downstream por-tions near the dams, and only later did ex-pansion occur upstream through the reser-voirs (Pligin, 1989).

An analysis of Dreissena depth distri-bution in Dnieper reservoirs indicates thatD. bugensis inhabits a wider range of


30 31 32 33

Test Temperature (C)FIG. 4. Percent survival in zebra and quagga mussels in tests of tolerance to acute temperature stress (averagedacross four rates of temperature increase). The key indicates species and acclimation temperature for each test.(Q: 5C represents the treatments of quagga mussels acclimated to 5°C).

depths than D. polymorpha (Table 3). Themaximum abundance of both species wasfrom 4 to 10 m. Below 12 m, reductions inmussel abundance might be explained by adeficit of favorable substrata due to the sil-tiness of the deeper sections of the reser-voirs, as well as by reduced oxygen con-centrations. However, exact data on

TABLE 3. Mean abundance o/D. polymorpha and D.bugensis by depth in Kremenchug and Kakhovka Res-ervoirs, 1985-1992 (Pligin, unpublished).

Depth(m)

0.0-2.02.1-4.04.1-6.06.1-8.08.1-10.0

10.1-12.012.1-14.014.1-16.016.1-18.018.1-20.0>20.1

(+ denotes

Number ofsamples

14652494153271913595

few).

Densities (number per m2)

D. polymorpha

29727088093541813132++00

D. bugensis

743656

2,1402,5622,7911,200

1798+++

changes in oxygen concentration with depthin Dnieper reservoirs is not available. Thedeepest record of D. bugensis was at 28 min Kakhovka reservoir, which has a maxi-mum depth of 35 m.

Displacement of D. polymorpha by D.bugensis

In the 1960s and 1970s, D. bugensis al-most entirely displaced D. polymorpha inZaporozh'ye reservoir and had become thedominant form in the Kakhovka Reservoirand other water basins of the Dneiper River(Zhuravel', 1965; Birger et al., 1968; Dygaand Zolotareva, 1976; Lubyanov and Zo-lotareva, 1976). Dreissena bugensis repre-sented 80-90% of the Dreissena populationin canals and reservoirs, sometimes com-pletely displacing it in deeper waters ofsome reservoirs (Zhuravel' 19676). In hy-dropower plant intake structures on theDnieper River, D. bugensis steadily gainedin dominance over D. polymorpha (Dyga etal., 1975). In 1964, D. bugensis constitutedonly 7% of the Dreissena in fouling intake


structures, in 1966, 15% and by 1973, 98%(Dyga et al, 1975).

Pligin (unpublished) has compiled dataon the occurrence of the two dreissenid spe-cies in the Kremenchug and Kiev Reser-voirs. He found that D. polymorpha com-prised 43-45% of the benthos in the Kre-menchug Reservoir soon after it was cre-ated in 1961. The first specimens of D.bugensis were found in the lower portionnear the dam of this reservoir in 1967, andfrom 1971 to 1975, D. bugensis expandedinto D. polymorpha habitat. Dreissena bug-ensis was found in the littoral zone only asrecently as 1974. In the first two years afterthe filling of the Kiev Reservoir, D. poly-morpha comprised 44% and 90% of thebenthos (Olivari, 1972). There were no con-tinuous field studies in this reservoir for thenext nine years, but the first specimen of D.bugensis was found there near the dam in1971, after which the population of thisspecies expanded. As D. bugensis expand-ed, the ratio of D. bugensis to D. polymor-pha shifted in favor of D. bugensis by 1979.In the main flow of the lower Dnieper Rivernear Kherson, D. bugensis displaced D.polymorpha in four years (Moroz, 1980). In1975 both species were abundant, with bio-masses of 4,952 and 2,797 g/m2 for D. bug-ensis and D. polymorpha, respectively. In1976-77 D. bugensis (biomass = 9,330g/m2) began to displace D. polymorpha(biomass = 59 g/m2) and in 1978 this dis-placement was almost complete {Dreissenabugensis = 10,900 g/m2 and D. polymorpha= 18 g/m2).

Recent field work by Rosenberg and Lu-dyanskiy (1994) verifies the predominanceof D. bugensis in the Dnieper River basin(Fig. 5). Samples were collected at depthsnot greater than one meter, except for grabsamples which were collected at 2-3 m inthe Dnieper Bug estuary. For all sites ex-cept the site in the Samara River (#5), thebiomass of D. bugensis was at least 3.3times greater than D. polymorpha. At theSamara River site, water flow may not havebeen suitable for D. bugensis settlementsince it was the highest compared to theother sites. The biomass of D. bugensis rel-ative to D. polymorpha increased fromnorth to south at low-flow stations (1 and

ChtmobyV

FIG. 5. Ratio of the biomass in grams of Dreissenabugensis to D. polymorpha (underlined numbers) atfour sites in the Dnieper River during August 1993.Letters identify location of sites: A = Desna Riverdelta; B = Dnieper River at Kiev; C = Dnieper Riverat Dnepropetrovsk; and D = Dnieper River at Kher-son.

4) along the Dnieper River. At the DnieperRiver sites, specimens of D. bugensis weremuch larger on average than those of D.polymorpha.

In the lower Great Lakes, where popu-lations of D. bugensis have had less time todevelop than in the Ukraine, there is onlyanecdotal evidence that quaggas may be ex-panding into habitats once dominated by D.polymorpha. In Lake Erie, for example,quaggas are expanding westward into areasknown to be dominated by D. polymorpha(Culligan, personal communication NYS-DEC, Dunkirk, NY). Similar observationswere made in Lake Ontario during the sum-mer of 1994 (R. Owens, personal commu-nication National Biological Survey, GreatLakes Center, Oswego, NY) where D. bug-ensis appeared to dominate at depths>25 m.

SubstratumIn the lower Dnieper River and its estu-

aries, substratum availability may be more


important than water salinity for determin-ing the distribution of Dreissena (Aleksen-ko, 1991). Aleksenko (1991) found Dreis-sena preferred solid substrata but ques-tioned the assumption that they do not liveon sand substrata (Mordukhai-Boltovskoi,1960). In shallow waters where sands wereaffected by the hydrodynamic activity ofwaves, Dreissena lived only on hard sub-strata such as unionid bivalves, stones andpieces of wood. However, as turbulence de-creased with increasing depth, Dreissenacolonized sand substrata. In the Dnieper-Bug estuary, Dreissena were abundant onsands and silty sands, D. polymorpha beingmore abundant on sands than D. bugensisand D. bugensis being more abundant onsilty sands than D. polymorpha (Aleksenko,1991). Pligin (unpublished) collected simi-lar data in Ukrainian reservoirs, showing D.polymorpha dominant on sand and siltysand, and D. bugensis dominant on varioussilty substrata.

In the Great Lakes, Dreissena specieshave been found on all types of hard sub-strata (Domm et al., 1993). Dreissena bug-ensis colonizes soft substratum in waterdepths exceeding 40 m and sand and sandysilt between 10 and 30 m (Dermott and Mu-nawar, 1993). By 1992, at least 80% ofLake Erie's bottom substrata were invadedby Dreissena and only areas where periodicanoxia occurred were devoid of the genus(Dermott and Munawar, 1993). For LakeErie and other North American lakes whereD. bugensis and D. polymorpha coexist, itis now clear that both dreissenids will im-pact not only the littoral shoals but the pro-fundal areas of lakes as well.

DISCUSSION

Historically, Dreissena evolved by neo-tenous retention of the byssus from now ex-tinct infaunal forms such as Congeria andDreissenomya (Morton, 1993). Dreissenapolymorpha is highly derived, havingevolved the keeled shape that allows it toanchor tightly to hard substrata. Dreissenabugensis lacks this keel, and does not attachas firmly; however, it retains the primitiveability to colonize soft substrata. The abilityof dreissenids to colonize both hard rockynearshore substrata and soft sediments of

lakes (soft substratum often dominates thebottom lake area of lakes) means that theseorganisms through their filtering activitywill impact the ecology of both littoralshoals and the profundal zone. In Lake Eriewhere quagga mussels occupy the soft sub-stratum (80% of the lake bottom is soft sub-stratum), competition for space and food byD. bugensis already has shown signs ofnegative impact on profundal organismslike the burrowing amphipod Diporeia(Dermott and Munawar, 1993).

The finding that quagga mussels occupydeeper, colder waters in the Great Lakescontrasts sharply with observations in theDnieper River drainage and raises newquestions about the optimal depth of thisspecies. No point in the Dneiper Riverdrainage is deeper than 35 m and D. bug-ensis is most abundant in the Dneiper res-ervoirs between 4 and 10 m, with a maxi-mum recorded depth of 28 m. In Lake On-tario, D. bugensis have been found at 110m (Mills et al, 1993) and in Lake Erie theycolonize soft substrata beyond 40 m (Der-mott and Munawar, 1993). In the DneiperRiver basin, D. bugensis initially inhabitedthe deeper areas of newly colonized watersand appeared later in shallow littoral habi-tats. As a result, patterns of colonization byUkrainian quagga mussel populationswould suggest that D. bugensis is not lim-ited to deep water habitats but could inhabita wider range of depths in North Americanwaters than once thought. In addition,Ukrainian populations once dominated byD. polymorpha have been largely replacedby D. bugensis. For the Great Lakes, thereis anecdotal evidence that D. bugensis isexpanding into shallower depths, lendingsupport to the notion that the quagga musselmay be able to occupy a wide range ofdepths here as well.

The conclusion that North Americanquagga mussels have a lower thermal max-imum than zebra mussels is not supportedby observations made on populations in theUkraine. Laboratory studies have shownthat the North American quagga mussel hasa higher mortality rate than the zebra mus-sel across acclimation temperatures thatwere eventually lethal to both species(Domm et al, 1993). Quagga mussels ex-


hibit high mortality at 30°C (Spidle, 1994)whereas the zebra mussel can survive in-definitely at the same temperature (McMa-hon et at, 1994; Spidle, 1994). However,Dnieper River populations of D. bugensisspawn at higher temperatures than D. poly-morpha (Shevtsova, 1968) and laboratorystudies indicate that D. bugensis exhibitedlower mortality at elevated temperaturescompared to D. polymorpha (Antonov andShorbatov, 1990). While experience fromthe lower Laurentian Great Lakes suggeststhat the quagga is a cold deep water form,findings from the Ukraine suggest other-wise and will need to be taken into accountwhen extrapolating the potential thermalrange of the quagga mussel in North Amer-ica. Furthermore, species closely related to,if not conspecific with, Dreissena polymor-pha occur in Greece and Asia Minor (Ro-senberg and Ludyanskiy, 1994), regionsthat are much warmer than Ukraine andRussia, so the potential thermal range ofthat species might also be higher than re-cent experiments indicate.

The genus Dreissena which is highlypolymorphic and produces millions of lar-vae has a high potential for rapid adapta-tion. In a few generations, rare alleles mightincrease greatly in frequency. This wouldallow new allelic heterozygote types to beformed, and creation of new alleles by re-combination. Consequently, Dreissenacould adapt to new environmental condi-tions after several generations. Strayer andSmith's (1993) prediction of a salinity limitof 2 ppt for North American Dreissena maysomeday be too low in light of the Ukrain-ian data. Distribution of Dreissena in theDnieper-Bug estuary is controlled by salin-ity and D. bugensis has been shown to sur-vive salinities twice that predicted for NorthAmerica. While North American quaggapopulations apparently cannot acclimate tosalinities to which Ukrainian populationshave, eventual colonization into estuarineand coastal areas of North America cannotbe ruled out. Evidence for this possibilitycomes from D. rostriformis grimmi, a closerelative of D. bugensis, which which isknown to inhabit the Caspian Sea at salin-ities up to 12.7 ppt (Rosenberg and Lu-dyanskiy, 1994).

Dreissena has colonized North Americanwaters for less than a decade and acclima-tion studies to date have been on a muchshorter time scale than seasonal changes orthan the 3—5 year life span of Dreissena. Inthe Ukraine, on the other hand, the responseof Dreissena to changing environmentalconditions has had a much longer time scaleto evolve. The potential for rapid adaptationto extreme environments by a highly poly-morphic and fecund species such as D.polymorpha is high. A highly polymorphic,fecund species like D. polymorpha has highpotential for adaptation to extreme environ-ments via rapid evolution of allelic fre-quencies and combinations. Dreissena bug-ensis has evolved as a more saline and ther-mal tolerant riverine and reservoir speciesin the Ukraine compared to North Ameri-can populations. Although we can speculateabout the eventual range expansion ofDreissena in North America and whetherDreissena bugensis will dominate over D.polymorpha, we know that colonization bythese dreissenids in freshwater and possiblyestuaries will have significant long-term im-pacts on North American waters.

ACKNOWLEDGMENTS

We are grateful to V. S. Polishchuk, T. L.Aleksenko, and T. G. Moroz from Kherson,Ukraine who shared with us their informa-tion on the ecology of D. polymorpha andD. bugensis in the lower Dnieper River andits delta. We also thank the National Sci-ence Foundation for providing travel sup-port funds and both Robert McMahon andJeffrey Ram for organizing a symposium onDreissena at the January 1995 Meeting ofthe American Society of Zoologists in St.Louis, Missouri. Special thanks to FredHenson and Jana Chrisman for drafting thegraphics. Research on Ukrainian dreissenidswas supported by National Oceanic and At-mospheric Administration NA26RG0403-01, the National Sea Grant Program. Con-tribution number 172 of the Cornell Bio-logical Field Station.

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