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ComparativeBiologyofZebraMusselsinEuropeandNorthAmerica:AnOverview

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AMER. ZOOL., 36:244-258 (1996)

Comparative Biology of Zebra Mussels in Europe andNorth America: An Overview1

GERALD L. MACKIE

Department of Zoology, University of Guelph, Guelph, Ontario NIG 2W1, Canada

AND

D O N W. SCHLOESSER

National Biological Service, Great Lakes Science Center, Ann Arbor, Michigan 48105

SYNOPSIS. Since the discovery of the zebra mussel, Dreissena polymor-pha, in the Great Lakes in 1988 comparisons have been made with musselpopulations in Europe and the former Soviet Union. These comparisonsinclude: Population dynamics, growth and mortality rates, ecological tol-erances and requirements, dispersal rates and patterns, and ecological im-pacts. North American studies, mostly on the zebra mussel and a few ona second introduced species, the quagga mussel, Dreissena bugensis, haverevealed some similarities and some differences. To date it appears thatNorth American populations of zebra mussels are similar to Europeanpopulations in their basic biological characteristics, population growth andmortality rates, and dispersal mechanisms and rates. Relative to Europeanpopulations differences have been demonstrated for: (1) individual growthrates; (2) life spans; (3) calcium and pH tolerances and requirements; (4)potential distribution limits; and (5) population densities of veligers andadults. In addition, studies on the occurrence of the two dreissenid speciesin the Great Lakes are showing differences in their modes of life, depthdistributions, and growth rates. As both species spread throughout NorthAmerica, comparisons between species and waterbodies will enhance ourability to more effectively control these troublesome species.

INTRODUCTION objectives of this paper are to review theThe zebra mussel was first discovered in results of existing biological research on ze-

the Great Lakes in 1988 and is believed to b r a mussels in North America and to corn-have been introduced in 1985/86 (Hebert et pare them to the European experiences.al., 1989; Griffiths et al., 1991). Mackie et This paper examines recent advances in theal. (1989) reviewed the European literature classification, taxonomy, general anatomyon the biology, impact, and control of the and morphology, mode of life and habitat,zebra mussel to try to predict the conse- physiology, biochemistry, genetics, dispers-quences of its introduction into North al mechanisms, geographic and habitat dis-American waters. Since that review, nu- tribution, predators, parasites, productivity,merous studies have been performed on life history, age and growth, and feeding,several North American populations. The Recent research on a second dreissenid,

Dreissena bugensis, discovered in the Great• From the Symposium Biology, Ecology and Phys- L a k e s i n 1 9 8 9 (Dermott, 1993), has shown

iology of Zebra Mussels presented at the Annual Meet- differences in many biological traits COIT1-ing of the American Society of Zoologists, 4-8 Janu- pared to the zebra mussel. Many of the re-

" * III5' a t SL L ° U i S ' ^ M i s s o u r ir . ,„ f X/I „. „ search findings for both species have re-

2 Address correspondence to: Gerald L. Mackie De- & . .partment of Zoology University of Guelph Guelph, suited in modifications ot predictions onOntario NIG 2W1. dispersal rates, potential distribution range,

244

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ZEBRA MUSSELS IN EUROPE AND NORTH AMERICA 245

and the types of habitats that the specieswill invade. This review adds the experi-ence of the North American invasion to theEuropean literature review by Mackie et al.(1989). Early invasion characteristics inNorth America are described in Nalepa andSchloesser (1993). To avoid excessive ci-tations, information from these two sourceshave been used liberally without specific ci-tations.

CLASSIFICATION

As many as seven systems of classifica-tion have been described for the Mollusca(Mackie et al., 1989), the most recent byNutall (1990). Nutall's (1990) classificationis used because it conforms to that com-monly used for North American Bivalvia{e.g., Turgeon, 1988).

Recent research by May and Marsden(1992) on the genetics of zebra {Dreissenapolymorpha) and quagga mussels {Dreis-sena bugensis (Rosenberg and Ludyanskiy,1994)) show that we have two species.Readers are encouraged to refer to Rosen-burg and Ludyanskiy (1994) in their ex-haustive review of the Dreissena species,and to Spidle et al. (1994) and Marsden(1996) for convincing evidence that bug-ensis is a distinct species. The classificationof the two Dreissena species in NorthAmerica can be summarized as follows:CLASS BIVALVIA Linnaeus, 1758; Sub-class HETERODONTA Neumayr, 1884;Order VENEROIDA H. & A. Adams,1856; Suborder DREISSENACEA Gray,1840; Superfamily DREISSENOIDEAGray, 1840; Family DREISSENIDAEGray, 1840; Genus Dreissena van Beneden,1835; Subgenus Dreissena s.l. van Bene-den, 1835; D. polymorpha (Pallas, 1771);Subgenus Pontodreissena Logvinenko andStarobogatov, 1966; D. {P.) bugensis (An-drusov, 1897).

TAXONOMY

The taxonomy of Dreissena has re-ceived considerable attention since the dis-covery of two species in the Great Lakes.Taxonomic keys and descriptions of Eu-ropean species are numerous (Mackie etal., 1989). Although the shells of all threespecies of North American Dreissenidae

lack a nacre and instead are composed ofaragonite with crossed-lamellar, complexcrossed-lamellar and pallial myostracalstructures, there are distinct differences inthe internal and external shell morpholo-gies (Pathy and Mackie, 1993). The dreis-senid species can be differentiated on thebasis of easily observable shell traits, asindicated below and in Table 1:

l(a) When viewed in cross-section, theventral margin is convex with arounded ventrolateral shoulder(Fig. la) 2

l(b) When viewed in cross-section, theventral margin is flattened, archedor concave, ventrolateral shoulderis acute (Fig. lb); freshwater, usu-ally lives attached to solid sub-strates or in clumps (druses) inmud Dreissena polymorpha

2(a) Internally, myophore plate isbroad and well developed andlacks an apophysis (Fig. lc); fresh-water, lives attached to solid sub-strates, in clumps or as individualsin mud Dreissena bugensis

2(b) Internally, myophore plate is nar-row and well developed and hasan apophysis (Fig. lc); brackishwater Mytilopsis leucophaeata

Kinzelbach (1992) reviews the phyloge-ny and speciation of Dreissena in Europebut readers should consult Spidle et al.(1994) and Marsden (1996) for the phylo-genetic relationships between North Amer-ican and European Dreissena on the basisof allozyme characteristics.

ANATOMY AND MORPHOLOGY

Mackie et al. (1989) provide referencesthat give details on different organ systems.Additional general descriptions have beenprovided recently by Morton (1993) andClaudi and Mackie (1994), but the mostsignificant advancement in our knowledgeof anatomy and morphology has been onbyssus structure. Ekroat et al. (1993), usingscanning electron microscopy, have provid-ed new information on byssal structure andthe byssal secreting process. They de-scribed two types of threads produced bythe mussels; temporary and permanent at-

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246 G. L. MACKIE AND D. W. SCHLOESSER

TABLE 1. Summary of diagnostic shell features of North American dreissenids. *

Shell features Dreissena poh'tnorpha Dreissena bugensis Mylilopsis leucophaeala

ExteriorShape, colour

Ventral margin

Dorsal margin

UmbonePosterior margin

InteriorMyophore plate

ApophosisPosition of AAMSa

and ABRMS"Pallial line

Mytiliform, striped, allblack or white

Arched, flattened, acuteventro-lateral shoul-der

Rounded

PointedAngled ventro-posteri-

orly

Broad and well devel-oped

AbsentBoth on myophore

plateEntire, rounded

Mytiliform, striped,light colored, whitein deep water

Convex, rounded ven-tro-lateral shoulder

Rounded, often wing-like

PointedRounded ventro-poste-

riorly

Broad and well devel-oped

AbsentBoth on myophore

plateEntire, rounded

Mytiliform, somestripes, all black ordark

Convex, rounded ven-tro-lateral shoulder

Flattened

RoundedRounded ventro-poste-

riorly

Narrow and well devel-oped

PresentAAMS on myophoreABRMS on apophysisIndented posteriorly as

pallial sinus

* Modified from Pathy and Mackie, 1993.J Anterior adductor muscle scar.b Anterior byssal retractor muscle scar.

tachment threads. The types are differenti-ated by length, thickness, number, arrange-ment and plaque morphology. Permanentattachment threads are formed in clumps orare arranged in rows and make up the ma-jority of a byssal mass. Temporary attach-ment threads are few in number (1-6), ar-ranged in a tripod pattern, originate individ-ually, and are separated spatially from themain byssal mass of permanent threads.Temporary threads are secreted before orafter the initial byssal mass attachment.Adult mussels (2 to 2.5 mm shell length)secrete about 23 threads per mussel perweek but the rate of thread formation variesconsiderably, depending on size, tempera-ture and water quality. The total numbersof threads secreted can be estimated fromthe regression, No. threads = -8.59 +19.26(shell length, mm) (Claudi and Mack-ie, 1994). The threads are composed ofDOPA (3,4-dihydroxyphenyl-alanine), aprominent amino acid present in the byssusof marine mollusks, but the precursors dif-fer considerably in sequence (Rzepecki andWaite, 1993). The adhesive strength of thezebra mussel byssal thread varies with thecomposition of materials on which it is at-tached (Ackerman et al., 1992).

MODE OF LIFE AND HABITAT

Mackie (1991) described the mode of lifeof D. polymorpha in the Great Lakes as anepifaunal one but recent research by Clax-ton (University of Guelph, Guelph, Ontario,pers. comm.) indicates that D. bugensis hasan ability for an epibenthic habit in deeperwaters. He collected benthic samples andsettlement data from plexiglass plates at 1to 36.6 m and found that recruitment rates(No./m2) decreased significantly (P < 0.05)with increasing depth, the greatest recruit-ment occurring at 14.3 m and the least at36.6 m. Benthic samples showed that theratio of quagga to zebra mussels increasedsignificantly with increasing depth. Onlyquagga mussels were taken in Ekman grabsamples at 36.6 m. Claxton (personal com-munication) suggested that quagga musselsmay be altering their shell allometry for anepibenthic existence; quagga mussels arethinner and lighter in weight in soft profun-dal sediments than on firm inshore sub-strates, whereas zebra mussels exhibit littleor no changes in shell allometry on firm orsoft substrates.

Zebra mussels are known to inhabit es-pecially large freshwater lakes and rivers

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ZEBRA MUSSELS IN EUROPE AND NORTH AMERICA 247

FIG. 1. Shell characteristics of dreissenids in North America, (a)—(d) Dreissena polymorpha: (a) schematicdrawing of end view showing carinate ventro-lateral margin (arrow) and concave ventral margin; (b) outer viewof right valve; (c) inner view of right valve; (d) myophore plate; (e)-(h) Dreissena bugensis: (e) schematicdrawing of end view showing rounded ventro-lateral margin (arrow) and convex ventral margin; (f) outer viewof right valve; (g) inner view of right valve; (h) myophore plate; (i)—(I) Mytilopsis leucophaeata: (i) schematicdrawing of end view showing rounded ventro-lateral margin (arrow) and convex ventral margin; (j) outer viewof right valve; (k) inner view of right valve; (1) myophore plate showing apophisis (arrow).

(Strayer, 1991) but the mussels also do wellin cooling ponds, quarries, and irrigationponds of golf courses as well. Recent re-search in North America has also demon-strated that zebra mussels are capable ofliving in brackish water or estuaries wherethe salinity does not exceed 8 to 12 ppt (Na-lepa and Schloesser, 1993; Kilgour et al.,1994). Temperature, the relative amounts ofsodium and potassium (Deitz et al., 1996)and the rate of acclimation to salinity great-ly affect the tolerance of larval and adultmussels to salinity; at higher temperatures(18-20°C) the optimum salinity for adultmussels is about 1 ppt but at lower temper-atures (3-12°C) the optimum salinity foradults is 2-4 ppt (Kilgour et al., 1994). The

incipient lethal salinity for post-veligers isnear 2 ppt and for adults (5—15 mm) it isbetween 2 and 4 ppt (Kilgour et al., 1994).

PHYSIOLOGY, BIOCHEMISTRY, GENETICS

Several aspects of the physiology, bio-chemistry, and genetics of zebra musselshave been described in the European liter-ature. These include osmotic and ionic reg-ulation, desiccation resistance, filtrationcharacteristics, resistance to metabolites,karyotypes, polymorphic systems, DNAcharacteristics, and protamine descriptions,uric acid composition, anerobic fermenta-tion products, and carotenoid content (seeMackie et al., 1989 for literature review).Recent, significant advances in our knowl-

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248 G. L. MACKIE AND D. W. SCHLOESSER

edge of physiology and genetics of NorthAmerican dreissenids are provided else-where in this symposium. Many of theseadvances have improved our abilities topredict the potential distribution range ofzebra mussels in North America, the poten-tial biotic and abiotic impacts of dreissenidson North American waters, and our under-standing of the regulatory processes mech-anisms that control reproduction and re-cruitment of zebra and quagga mussels.

DISPERSAL MECHANISMS

Mackie et al. (1989) and Carlton (1993)review numerous potential dispersal mech-anisms of larval and adult dreissenids,many of them being natural mechanisms{e.g., water currents, birds, insects, otheranimals) but most being human-mediated{e.g., artificial waterways, ships and othervessels, fishing activities, amphibiousplanes, and recreational equipment, to men-tion a few). The planktonic veliger stage isprobably the most effective natural dispers-al phase, with intracontinental dispersal oc-curring quickly via downstream movementof the veligers. Artificial canals enhancedthe dispersal of zebra mussels in Europe,especially in the USSR and Britain (Kerneyand Morton, 1970). Not all mechanismshave been verified, especially for the plank-tonic stage, which are usually not the firstlife stage found in a newly established mus-sel population (Nalepa and Schloesser,1993). In general, natural dispersal of zebramussels is believed to occur primarily bycurrents carrying planktonic veligers. How-ever, sedentary mussels attached to floatingdebris may also distribute mussels. In ad-dition, juvenile and adult mussels can pos-sibly be dispersed by extending mucousthreads (up to 15 mm long) from the sur-face of the water by capillary action anddrifting with surface water currents (Martel,1993). Dispersal caused by turtles, crayfish,and birds may occur but is not well docu-mented (Carlton, 1993).

Human-mediated dispersal mechanismsare believed to be the most common meansof distributing zebra mussels, especially be-tween continents and unconnected waterbodies (Table 2). Carlton (1993) describesthree lines of evidence which lead to the

conclusion that freshwater ballast in trans-oceanic vessels transported zebra musselsfrom Europe to the Laurentian Great Lakes:(1) the common presence of veligers in bal-last water combined with patterns of vesseltraffic in the Great Lakes; (2) the introduc-tion of other exotics {e.g., crustaceans)transported in ballast water; and (3) the in-ability to identify other probable mecha-nisms. However, desiccation studies by Us-sery and McMahon (1994) suggest that it isalso possible that adult mussels may haveattached to anchors or their chains of ves-sels in European harbors and survived thetransoceanic voyage. This is probable if theanchors and chains were stored on boardwith sufficient moisture content to allow atleast some mussels to survive the voyageand then drop off when ships anchored inthe Great Lakes (McMahon, personal com-munication).

GEOGRAPHIC DISTRIBUTION

The range of zebra mussels before the19th century occurred primarily over smallareas of the Black, Caspian, and Azov seas(Stanczykowska, 1977). The limited distri-bution of zebra mussels in 1800 was a re-sult of thousands of years of natural pro-cesses. Between 1800 and 1900, zebra mus-sels more than doubled their range in Eu-rope (Schloesser, 1995). The doubling ofthe range of mussels in only 100 years isattributed to human-mediated dispersalmechanisms (Kinzelbach, 1992; Morton,1993).

Zebra, mussels were discovered in NorthAmerica in June 1988 in Lake St. Clair ofthe Laurentian Great Lakes (Hebert et al.,1989). Length-frequency analysis of knownpopulations in 1988 and review of studiesperformed before 1988 indicate that mus-sels became established in Lake St. Clairand the most western portion of Lake Eriedownstream from Lake St. Clair in 1986(Griffiths et al, 1991) (Fig. 2). This initialfounding population occurred in a rangeabout 75 km north to south (N-S) by 25 kmeast to west (E-W). By 1990, zebra musselsoccurred primarily downstream of thefounding population in a range extending tothe extreme eastern and western ends of theGreat Lakes—600 km N-S by 1,400 km

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ZEBRA MUSSELS IN EUROPE AND NORTH AMERICA 249

FIG. 2. Distribution of Dreissena polymorpha in four-year intervals from 1986 (Lake St. Clair and westernbasin of Lake Erie = stars), to 1991 (mainly all the Great Lakes = stippled areas), and 1994 (most majortributaries of Mississippi River and many inland areas = hatched areas) as described in text.

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250 G. L. MACKIE AND D. W. SCHLOESSER

E-W. Mussels were also found at severalharbors and river mouths upstream of thefounding mussel population. In 1991, mus-sels were found outside the Great Lakeswater basin. In 1992, mussels occurred asfar south as Vicksburg, Mississippi, west toMinneapolis, Minnesota, and north and eastto Quebec. By 1994 mussels were found ina range extending 1,900 km N-S by 1,700km E-W. To date most of the infested wa-ters are connecting rivers of the MississippiRiver such as the upper Mississippi, Ten-nessee, Ohio, and Arkansas, although sev-eral lakes not connected to infested riversare also infested. In addition, live musselsattached to trailered boats have been foundas far west as Los Angeles, California. Ze-bra mussels are also well established inLake Simcoe, Ontario, where-most union-ids have 2 to 8 zebra mussels per unionid(Trevor Claxton, personal communication),and appear to be following the same pat-terns reported for Lake St. Clair unioinids(Gillis and Mackie, 1994).

The factors that will limit the distributionand abundance of zebra mussels appear tobe temperature, pH, and calcium content.Predictions for the spread of zebra musselsin North America are currently based on anupper thermal tolerance of 26-32°C (Stray-er, 1991), a calcium threshold for survivalof 12 mg/liter (Neary and Leach, 1991),and a pH and calcium threshold for growthand reproduction of 7.3 and 28.3 mg/liter,respectively (Ramcharan, 1992a, b). Thesecriteria are largely based on European lab-oratory studies which showed particularlyhighly variable response levels to calcium(Mackie et al., 1989). However, Hincks(1994), using both laboratory and fieldstudies, examined the effects of pH levelsless than 7.0 and calcium levels lower than12 mg/liter on survival, growth and repro-duction of zebra mussels and found: 100%mortality in water with pH less than 7.1,mortality decreasing with increasing pHabove 7.1; positive growth at levels abovepH 7.1 and 8.5 mg Ca/liter; and reproduc-tion in waters with calcium levels above 20mg/liter. Mackie and Kilgour (1995) founda pH threshold limit of survival for veligersat 7.4-7.5. Therefore, it appears that al-though zebra mussels may survive and

grow in waters with pH as low as 7.3 andcalcium levels between 8 and 20 mg/liter,infestation levels of abundance probablywill not occur until pH exceeds 7.5-8.0 andcalcium levels exceed 15—20 mg/liter.

HABITAT DISTRIBUTION

Mackie et al. (1989) reviewed the Euro-pean literature for information on the ver-tical distribution of zebra mussel veligersand the abundance of adults in relation todepth. North American research is provid-ing new information on the vertical distri-bution of veligers of D. polymorpha and D.bugensis. Fraleigh et al. (1993) reportedthat wind driven currents have a profoundeffect on the vertical distribution of zebramussel veligers; significant depth effectswere found only at wind velocities <8 km/hwhen 5% of the population was found at 0—2 m, 30% at 2-4 m, and 64% at 4-6 m.Veligers are found deeper in the water col-umn when NOT mixed vertically by wind.Smylie (1994) examined the depth distri-bution of D. polymorpha on calm days(waves less than 10 cm high) and foundpeaks in abundance between 2 and 6 m atsites ranging from 6 to 20 m in HamiltonHarbour (Lake Ontario) and at 18 m at asite deeper than 35 m in Lake Erie, but al-ways at temperatures between 16.7 and17.8°C at all sites.

Perhaps wind driven currents have lesseffect on the vertical distribution of veligersin lakes with small surface areas than inlakes with large surface areas, like LakeErie. Based on European data, Fraleigh etal. (1993) showed that the maximum den-sities of larvae tend to decrease with in-creasing surface area and depth of lakes.However, Lake Erie, almost twice as largeas the largest reservoirs {e.g., KuibyshevReservoir and Lake Ladoga) or lake studiedin Europe (Lake Constance), does not fit thepattern and has the largest density of larvaein lakes reported to date (Fraleigh et al.,1993).

Dreissena bugensis first settled in theeastern basin of Lake Erie in August, 1989(Riessen et al, 1993). By summer, 1990 thequagga mussel had been dispersed to themouth of the Niagara River and by Decem-ber 1990 to the eastern end of Lake Ontario

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ZEBRA MUSSELS IN EUROPE AND NORTH AMERICA 251

(Dermott, 1993). The quagga mussel hadsucceeded in occupying the entire easternand most of the central basin of Lake Erieand occurred at several sites along thesouthern shores (U.S.) of Lake Ontario byJuly, 1992 (Dermott, 1993). The species hasdisplaced the zebra mussel at many sites inLake Erie and is the only dreissenid foundin waters exceeding 40 m deep (Dermott,1993). The quagga mussel has been foundin depths exceeding 150 m and is reportedto grow and reproduce in profundal sedi-ments where the temperature never exceeds12°C (Dermott, 1993; Mills et al., 1995).

In spite of these differences, many simi-larities in horizontal and depth distributionsof zebra mussels exist between Europeanand North American lakes. For veligers, thedepth of maximum abundance typicallyvaries between 3 and 7 m, but maxima at11 to 12 m are common (Mackie et al.,1989). Similar depths of maximum abun-dance are described for veligers in Euro-pean lakes (Mackie et al., 1989) but as a"belt of shore waters" around the perimeterof the lake. The width of the belt dependson the bathymetry of the lake, the widestbelts occurring in lakes with a shallowslope.

Few veligers occur below the thermo-cline in temperate lakes (Mackie et al.,1989; Fraleigh et al, 1993; Smylie, 1994).Variations in the vertical distribution of ve-ligers can usually be attributed to winddriven currents. However, there are numer-ous other factors. Secchi depth visibilityand temperature are two factors commonlyattributed to variations in maximum densi-ties (Mackie et al., 1989). Moreover, thereappears to be a diurnal movement of veli-gers, with maximum densities occurringnear the surface during early morning andat 5-7 m during the day (Mackie et al.,1989).

Veligers are usually contagiously distrib-uted, though the factors responsible for thisare not yet well understood. Mackie et al.(1989) describe studies that show the patch-iness is not due to prevailing winds in Pol-ish lakes, but Martel (1993) has demonstrat-ed that prevailing winds plays a major rolein the patchiness of veliger abundance inLake Erie. Smylie (1994) found few differ-

ences in veliger abundance between inshoreand offshore waters, but when differencesappeared, offshore waters had greater den-sities of than inshore waters. Doka (1994)showed that while wave height, wind ve-locity, and fetch hours did not correlatestrongly with recruitment rates, all threewere significant variables in multiple re-gression models for predicting size of re-cruitment of Dreissena populations in LakeErie.

Different patterns of distribution havebeen reported for adults than for larvae. Foradults the depth of maximum density ishighly variable among lakes and varies sea-sonally. However, the reasons for the sea-sonal shifts appear to differ between Euro-pean and North American studies. Mackieet al. (1989) reported smaller, youngerspecimens migrating from shallow water inthe summer to deep water in the winter.This resulted in a seasonal shift of the agestructure in the main belt of occurrence,from an increase in the proportion of youngspecimens during summer to a decrease inthe winter. In North American populationsseasonal differences tend to be attributed todifferences in size-selected "loss rates," thelosses representing both mortality andtranslocation. Smaller mussels translocateat higher rates than larger mussels (Martel,1993), probably because larger musselshave greater numbers of byssal threadsfrom neighboring individuals holding themin place (Claudi and Mackie, 1994). Bishopand DeGaris (1976) found that dreissenidstend to occur independently of other mol-luscan species. However, this may be be-cause dreissenids have displaced other mol-lusks (Gillis and Mackie, 1994; Schloesseret al., 1996).

PREDATORS

Larval stages of mussels appear to beconsumed mainly by crustacean zooplank-ton (e.g., copepods) and larval fish, but therelative importance of these prey groups tothe total mortality of larval stages is un-known (Mackie et al., 1989). In NorthAmerica, Conn and Conn (1993) reportedpredation of larval stages by the cnidarian,Hydra americana.

Adult zebra mussels have a very high nu-

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252 G. L. MACKIE AND D. W. SCHLOESSER

tritional value of the tissues, with 60.7%protein, 12.0% lipid, 19.0% carbohydrate,and 5.9% ash (Cleven and Frenzel, 1992)and are consumed in large quantities bycrayfish, fish, and waterfowl (Mackie et al,1989). The nutritional value changes sea-sonally. In Europe, Mackie et al. (1989) de-scribe several European predation studies.Several species of fish consume zebra mus-sels but the roach seems to have the mostsignificant impact on mussel densities. Theroach has strong pharyngeal denticles andcan consume large shells. In some Polishlakes, the diet of roach consists almost ex-clusively {i.e., 95-100%) of zebra mussels,although feeding on mussels may be sea-sonal {e.g., autumn and winter). In general,it appears that fish do not limit the densitiesof D. polymorpha in European lakes.

In North America, zebra mussels havebeen found in the stomachs of walleye, yel-low perch, freshwater drum, white suckers,and a few others. The relative contributionof the fish species to predation of zebramussels in North America is unknown.Only the freshwater drum, Aplodinotusgrunniens, has been investigated in somedetail (Nalepa and Schloesser, 1993); pre-dation on zebra mussels increases as drumsize increases, with large drum feeding al-most exclusively on zebra mussels. Thefreshwater drum is the only species in theGreat Lakes that has molariform pharyn-geal teeth for crushing shells of mollusks.The only other significant predator of zebramussels is waterfowl and Maclsaac (1996)examines the recent literature and describesthe effects of predators on dreissenids inNorth America.

PARASITES

Freshwater bivalve mollusks are com-mon intermediate hosts of parasites, partic-ularly trematodes, whose definitive hostsare fish, waterfowl, and sometimes humans(Mackie, 1976). Mackie et al. (1989) con-cluded from their European literature sur-vey that D. polymorpha is not a commonvector of parasites. Protists and digeanswere the most common parasites found,with Nematoda observed sporadically.Many protists are common parasites but

they do not seem to "affect the numbers"of the zebra mussel.

The survey of the European literature ofMackie et al. (1989) also concluded thattrematodes are less common parasites of ze-bra mussels than protists, the greatest infes-tation rate observed being 10%. The mostdangerous protists are ciliates of the familyOphryoglenidae which parasitize the diges-tive gland and may kill the mussel. Thetrematodes, Phyllodistomum folium and Bu-cephalus polymorphus are also importantparasites in Netherland lakes where the in-festation prevalence is usually about 1%and may go as high as 10% (Nalepa andSchloesser, 1993). Infestation apparentlylowers the resistance of mussels to metalaccumulation, infested mussels havinghigher levels of Zn, Cu, Cd, and Pb thannoninfested mussels. The effects of para-sites on European populations of D. poly-morpha appear to be mininimal, at least un-til high emmisions of cercariae of B. poly-morphus occur (Mackie et al., 1989). Inten-sity of parasitism by P. folium was directlycorrelated to shell size of D. polymorpha,the maximum number recorded being 200at a shell size of 24-28 mm.

Similar results have been reported inNorth America by Toews et al. (1993).They reported a 2.9% prevalence of pla-giorchiid metacercariae in mussels and2.7% prevalence of adults and juvenile as-pidogastrids in mussels from two sites inLake Erie. The ciliate, Ophryoglena, wasalso found, with 1.3% prevalence at a sitein Lake St. Clair and 2.7 to 4.3% preva-lence at two sites in Lake Erie. Toews et al.(1993) concluded that although parasites donot significantly affect changes in densitiesof D. polymorpha, there is a great proba-bility that mass development of zebra mus-sels may increase the infection rate in de-finitive hosts, especially fish and waterfowl.The oligochaete, Chaetogaster limnaei, andthe chironomid Paratany'tarsus, have alsobeen reported as commensals in zebra andquagga mussels (Conn et al., 1994).

PRODUCTIVITY

Densities of veligers and adults in theGreat Lakes are among the highest reportedto date. Fraleigh et al. (1993) tabulated

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mean monthly densities of veligers in eightEuropean lakes and reservoirs and foundthat the western basin and its island regionaveraged 126-268 individuals/liter in Julyand August (Leach [1993] reported meansnear 400/liter), whereas European watersaveraged about 10-lOO/liter, the KoninLakes being an exception with 22—320/literin the same period. Mean densities (No./m2)of adult range from about 54,000 (Dermottet al, 1993) to 779,000 (Pathy, 1994) inLake Erie to 43,000 in Lake St. Clair (Pa-thy, 1994). Average densities of adult mus-sels in European lakes range from about5,000 to about 115,000/m2 (Mackie et al,1989).

The abundance of D. polymorpha hasbeen related to trophic type, the largest pop-ulations occurring in eutrophic waters(Mackie et al, 1989). However, Stanczy-kowska (1964) found no relationship be-tween abundance of D. polymorpha andtrophic status of lakes.

Biomass of D. polymorpha in a givenwater body is usually related to the densitybut the average biomass of populations ishighly variable among lakes (e.g., 0.13 to20 kg/m2) and within lakes (e.g., 0.05-10.5kg/m2) (Mackie et al, 1989). Some of thisvariation is due to variations in body con-dition of mussels and in length-weight re-lationships. Several indices of conditionhave been used; length, height and/or widthor "size" of shells; wet and dry weight ofwhole animals, shell only and dry tissueonly; length:width ratio or slenderness;length:height ratio or flatness; and the ratioof wet weight to dry weight (Mackie et al,1989). Of these, slenderness, flatness, andratio of wet to dry weight showed the leastvariation within and among lakes; averagesize and weight varied considerably amonglakes but tended to vary only slightly withinlakes; body (tissue) weight and shell weighttended to vary in the same manner amonglakes (i.e., lakes with high shell weightsalso had high body weights) (Mackie et al,1989).

Mackie et al. (1989) examined the Eu-ropean literature and concluded that varia-tions in length-weight relationships corre-lated highly with variations in environmen-tal conditions. Regressions of shell length

and shell and body weight follow the powerfunction, Weight = a X Lengthb, where bvaries between 1.937 and 3.284 for Euro-pean populations, depending on lake typeand time of year. Zebra mussel populationsin the Great Lakes fall within this range;Nalepa and Scloesser (1993) give studiesthat report slope values of 2.612 for totaldry weight and 2.198 for dry tissue weight(vs. shell length); Mackie (1991) reports2.996 and 2.982, respectively for the samevariables. Neumann and Jenner (1994) pro-vide studies that evaluate the use of shelllength, shell height, and shell volume foraccurately predicting biomass of zebra andquagga mussels. Both shell height and shellweight are good predictors of ash free dryweight (AFDW) for both species; volumemeasurements do not provide as good anestimate of AFDW as did shell length andheight.

Estimates of annual production of D.polymorpha in European waters are uncom-mon but vary between 0.1 and 29.8 g/m2/yrdry body weight and 3.3 and 525.9 g/m2/yrtotal dry weight (Mackie et al, 1989). Inthe Great Lakes annual production of zebramussels is higher than most European pop-ulations, about 150 g/m2/yr dry bodyweight (Dermott et al, 1993). Cleven andFrenzel (1992) reported annual productionfor River Seerhein, the outlet of Lake Con-stance, as 138 g Corg/m

2, including organicshell content. In European waters the P/Bratio varies between 0.42 and 0.65 for drybody weight and 0.47 and 0.81 for total dryweight (Mackie et al, 1989). The highestP/B ratio recorded is 6.8 for Lake Con-stance (Mackie et al, 1989), but the pop-ulation was still in its exponential phase ofgrowth and the P/B ratio may have droppedwhen the population stabilized. Dermott etal. (1993) reported a P/B ratio of 4.7 for apopulation in Lake Erie.

LIFE HISTORY

The life history of D. polymorpha and itsvariations are well known, especially forEuropean waters (Mackie et al, 1989).Ackerman et al (1994) have reviewed theearly life history of dreissenids and havestandardized the terminology with that usedfor marine mussels. Variations in life his-

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254 G. L. MACKIE AND D. W. SCHLOESSER

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TimeFIG. 3. Life cycle of Dreissena polymorpha in relation to annual temperature cycle in Great Lakes region.Threshold temperatures for growth and reproduction are also shown. Life cycle is based on maximum devel-opment times reported by Ackerman et al. (1994) in relation to typical settlement periods in Great Lakes reportedby Doka (1994). At least one settlement event is possible based on maximum development times but some yearsmay have two or more, depending on durations of each stage shown in bold italics. Size ranges are for heightsof shells, as reported by Ackerman et al. (1994).

tory of North American zebra mussels havebeen described by Mackie (1991, 1993),Haag and Garton (1992), Garton and Haag(1993), Claudi and Mackie (1994), and Pa-thy (1994) but the variations are somewhatdifferent from European populations. In Eu-rope, adults become sexually mature intheir second year of life (Mackie et al.,1989); in North America, zebra mussels be-come sexually mature in their first year oflife, usally by 8 to 10 mm in shell length.Zebra mussels have exceedingly high fe-cundities, varying from 30,000 to 1,610,000eggs/female (Mackie et al., 1989; Borch-erding, 1992). Typically, gametogenesis be-gins in the fall after all gametes are spent,continues through winter, with intensivegrowth of oocytes and spermatozoa inspring when mussels attain a shell length of8-9 mm or larger (Pathy, 1994). Fig. 3

summarizes the annual life cycle of zebramussels in the Great Lakes in relation totemperature. Additional details are providedby Nichols (1996).

Settling stages are the most sensitivestages and have high mortality rates, usu-ally 90-99% (Mackie et al., 1989; Nalepaand Schloesser, 1993). However, these mor-tality rates did not consider immigrationand emmigration (translocation) of youngstages; Maclsaac et al. (1991) suggestedthat when immigration and emmigration areaccounted for, mortality could be as low as70% in the western basin of Lake Erie.They indicated that larval mortality couldbe lower during the colonization phase andthen increase when adults become estab-lished and begin to filter their own larvae.

There is often misuse of the terms "set-tlement" and "recruitment". Settlement re-

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ZEBRA MUSSELS IN EUROPE AND NORTH AMERICA 255

fers to the passage from a pelagic habit toa benthic one and involves not only achange in position in the water column butattachment and certain morphometricchanges as well (Doka, 1994). Recruitmentis essentially the process of settlement com-bined with post-settlement mortality. Theprocess is thought to be comprised of threephases; larval supply, settlement, and meta-morphosis (Doka, 1994). Newly settledmussels are considered recruits if they havesurvived to a size or an elapsed period oftime set a priori by the investigator. Doka(1994) found that peaks in recruitment den-sities occurred at similar times among herstudy sites and between years; a peak inrecruitment can be expected during the firstthree weeks in August at most sites in LakeErie. However, she found variability in thenumber of recruitment events between sites,probably because of local hydrological con-ditions delivering larval pulses towardshore. Nevertheless, adult population dy-namics appear to be regulated, in part atleast, by recruitment fluctuations as "sup-ply-side" ecology suggests (Doka, 1994).

AGE AND GROWTH

The growth rate of larvae in nature ishighly variable, depending mainly on tem-perature (Mackie et al., 1989) and chloro-phyll a content (Smylie, 1994). Estimates oflarval growth rates of zebra mussels arefew; 1 to 4 |xm/d for larvae in two lakes inGermany (Mackie et al., 1989), 6.0 to 11u.m/d for a drifting population in the RiverRhine (Neumann and Jenner, 1994), and 2.4to 23.7 jim/d for larvae at several sites inLake Erie (Smylie, 1994). Smylie (1994)also reared larvae in the laboratory andachieved 4.1 to 4.5 u,m/d at 13.1°C and 6.5to 8.7 u,m/d at 16.6°C.

The relationship between age and growthof mussels varies considerably, much of thevariation being due to the method used toage the mussels. Mackie et al. (1989) de-scribe two patterns of growth in Europeanpopulations, "slow-growing" and "fast-growing" populations. The maximumgrowth rate for the slow-growing group ap-pears to be less than 1 cm/yr with a maxi-mum shell size of 3.5 cm; the fast-growinggroup exceeds 1.5 cm/yr with a maximum

shell length >4.0 cm. Populations in theGreat Lakes are different still, where mostmussels grow quickly (1.5—2.0 cm/yr) buttheir maximum size is typically only 2.5-3.0 cm (Mackie, 1991).

The growth rate of D. polymorpha is de-pendent on quality and quantity of food,temperature, and body size (Mackie et al.,1989). Growth rates decrease with increas-ing body size and increase with increasingfood concentration up to 2 mg C/liter, withan optimum between 10 and 15°C, althoughin the Great Lakes growth and settlementrates appear to be optimum between 15 and17°C (Smylie, 1994). The temperaturethreshold for growth usually varies between10 and 12°C (Mackie et al., 1989; Neumannand Jenner, 1994; Smylie, 1994); a value aslow as 6°C was reported by Bij de Vaate(1991). The quagga mussel appears to beable to reproduce at temperatures below8°C, in the hypolimnion of Lake Erie (Tre-vor Claxton, University of Guelph, Guelph,Ont., personal communication).

The life span of D. polymorpha is highlyvariable, but it appears that North Americanpopulations have a shorter longevity thanEuropean populations. The average lifespan of zebra mussels is 3-5 years in mostPolish lakes, 5 years in British waters, and6—9 years in some Russian reservoirs(Mackie et al., 1989). In North America,most zebra mussel populations have a lifespan of about 1.5 to 2 years (Mackie, 1991).Zebra mussels inhabiting heated watershave life spans truncated by about 1 yearcompared to unheated lakes in the samearea (Mackie et al., 1989).

FOOD AND FEEDING

Food selection is performed by a varietyof cilia, including those in the mantle cavity(gills, labial palps and foot) and in thestomach and midgut. Cilia in the mantlecavity and stomach select particles of 15—40 (xm for food but can filter out particlesas small as 0.7-1.0 u.m in diameter fromthe water (see Mackie et al., 1989 for re-view). Significant advancements in ourknowledge of ciliary filter feeding process-es and feeding habits have been made bySilverman et al. (1996) Maclsaac (1996)

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256 G. L. MACKIE AND D. W. SCHLOESSER

and should be consulted for a detailed dis-cussion of feeding in dreissenids.

The filtration rate is affected by size, tur-bidity, temperature, and certain concentra-tions of specific sizes and kinds of algalcells (e.g., Chlamydomonas) and bacterialcells (Mackie et ai, 1989; Reeders and bijde Vaate, 1989; Reeders et al, 1993). Thefiltration capability of D. polymorpha in re-lation to its role as a clarifier of water in anentire lake, epilimnion or littoral zone hasbeen reviewed by Neumann and Jenner(1992); they also describe applications ofzebra mussels in water quality manage-ment, particularly as water clarifiers. Al-though mussels are efficient clarifiers, thesuspended materials accumulate on the bot-tom as faeces and pseudofaeces. The sizeof faecal and pseudofaecal pellets varieswith mussel size and the settling velocitiesand rate of accumulation greatly exceednormal sedimentation processes (Dean,1994).

ACKNOWLEDGMENTS

Contribution Number 955, National Biolog-ical Service, Great Lakes Science Center,1451 Green Road, Ann Arbor, Michigan48105.

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