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Comparative Biology of Zebra in Europe and North America: An Overview

Article in Integrative and Comparative Biology · June 1996 DOI: 10.1093/icb/36.3.244 · Source: OAI

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Comparative Biology of Zebra Mussels in Europe and North America: An Overview1

GERALD L. MACKIE Department of Zoology, University of Guelph, Guelph, Ontario NIG 2W1, Canada

AND

DON W. SCHLOESSER National Biological Service, Great Lakes Science Center, Ann Arbor, Michigan 48105

SYNOPSIS. Since the discovery of the , polymor- pha, in the Great Lakes in 1988 comparisons have been made with mussel populations in Europe and the former Soviet Union. These comparisons include: 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 on a second introduced species, the , Dreissena bugensis, have

revealed some similarities and some differences. To date it appears that Downloaded from North American populations of zebra mussels are similar to European populations in their basic biological characteristics, population growth and mortality rates, and dispersal mechanisms and rates. Relative to European populations differences have been demonstrated for: (1) individual growth icb.oxfordjournals.org rates; (2) life spans; (3) calcium and pH tolerances and requirements; (4) potential distribution limits; and (5) population densities of veligers and adults. In addition, studies on the occurrence of the two dreissenid species

in the Great Lakes are showing differences in their modes of life, depth by guest on July 8, 2011 distributions, and growth rates. As both species spread throughout North America, comparisons between species and waterbodies will enhance our ability to more effectively control these troublesome species.

INTRODUCTION objectives of this paper are to review the The zebra mussel was first discovered in results of existing biological research on ze- the Great Lakes in 1988 and is believed to bra 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 the al. (1989) reviewed the European literature classification, , general anatomy on 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- Lakes in 1989 (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- 5 at SL L UiS Missouri "* III ' ° '^ r. ,„ 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 on Ontario NIG 2W1. dispersal rates, potential distribution range, 244 ZEBRA MUSSELS IN EUROPE AND NORTH AMERICA 245 and the types of habitats that the species lack a nacre and instead are composed of will invade. This review adds the experi- aragonite with crossed-lamellar, complex ence of the North American invasion to the crossed-lamellar and pallial myostracal European literature review by Mackie et al. structures, there are distinct differences in (1989). Early invasion characteristics in the internal and external shell morpholo- North America are described in Nalepa and gies (Pathy and Mackie, 1993). The dreis- Schloesser (1993). To avoid excessive ci- senid species can be differentiated on the tations, information from these two sources basis of easily observable shell traits, as have been used liberally without specific ci- indicated below and in Table 1: tations. l(a) When viewed in cross-section, the CLASSIFICATION ventral margin is convex with a rounded ventrolateral shoulder As many as seven systems of classifica- (Fig. la) 2 tion have been described for the (Mackie et al., 1989), the most recent by l(b) When viewed in cross-section, the Nutall (1990). Nutall's (1990) classification ventral margin is flattened, arched is used because it conforms to that com- or concave, ventrolateral shoulder monly used for North American is acute (Fig. lb); freshwater, usu- {e.g., Turgeon, 1988). ally lives attached to solid sub- strates or in clumps (druses) in Downloaded from Recent research by May and Marsden mud Dreissena polymorpha (1992) on the genetics of zebra {Dreissena polymorpha) and quagga mussels {Dreis- 2(a) Internally, myophore plate is broad and well developed and sena bugensis (Rosenberg and Ludyanskiy, icb.oxfordjournals.org 1994)) show that we have two species. lacks an apophysis (Fig. lc); fresh- Readers are encouraged to refer to Rosen- water, lives attached to solid sub- burg and Ludyanskiy (1994) in their ex- strates, in clumps or as individuals haustive review of the Dreissena species, in mud Dreissena bugensis and to Spidle et al. (1994) and Marsden 2(b) Internally, myophore plate is nar- by guest on July 8, 2011 (1996) for convincing evidence that bug- row and well developed and has ensis is a distinct species. The classification an apophysis (Fig. lc); brackish of the two Dreissena species in North water leucophaeata America can be summarized as follows: Kinzelbach (1992) reviews the phyloge- CLASS BIVALVIA Linnaeus, 1758; Sub- ny and speciation of Dreissena in Europe class Neumayr, 1884; but readers should consult Spidle et al. Order VENEROIDA H. & A. Adams, (1994) and Marsden (1996) for the phylo- 1856; Suborder DREISSENACEA Gray, genetic relationships between North Amer- 1840; Superfamily ican and European Dreissena on the basis Gray, 1840; Family of allozyme characteristics. Gray, 1840; Dreissena van Beneden, 1835; Subgenus Dreissena s.l. van Bene- ANATOMY AND MORPHOLOGY den, 1835; D. polymorpha (Pallas, 1771); Mackie et al. (1989) provide references Subgenus Pontodreissena Logvinenko and that give details on different organ systems. Starobogatov, 1966; D. {P.) bugensis (An- drusov, 1897). Additional general descriptions have been provided recently by Morton (1993) and Claudi and Mackie (1994), but the most TAXONOMY significant advancement in our knowledge The taxonomy of Dreissena has re- of anatomy and morphology has been on ceived considerable attention since the dis- byssus structure. Ekroat et al. (1993), using covery of two species in the Great Lakes. scanning electron microscopy, have provid- Taxonomic keys and descriptions of Eu- ed new information on byssal structure and ropean species are numerous (Mackie et the byssal secreting process. They de- al., 1989). Although the shells of all three scribed two types of threads produced by species of North American Dreissenidae the mussels; temporary and permanent at- 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 Exterior Shape, colour Mytiliform, striped, all Mytiliform, striped, Mytiliform, some black or white light colored, white stripes, all black or in deep water dark Ventral margin Arched, flattened, acute Convex, rounded ven- Convex, rounded ven- ventro-lateral shoul- tro-lateral shoulder tro-lateral shoulder der Dorsal margin Rounded Rounded, often wing- Flattened like Umbone Pointed Pointed Rounded Posterior margin Angled ventro-posteri- Rounded ventro-poste- Rounded ventro-poste- orly riorly riorly Interior Myophore plate Broad and well devel- Broad and well devel- Narrow and well devel- oped oped oped Apophosis Absent Absent Present Position of AAMSa Both on myophore Both on myophore AAMS on myophore and ABRMS" plate plate ABRMS on apophysis Pallial line Entire, rounded Entire, rounded Indented posteriorly as pallial sinus Downloaded from * Modified from Pathy and Mackie, 1993. J Anterior adductor muscle scar. b Anterior byssal retractor muscle scar. icb.oxfordjournals.org

tachment threads. The types are differenti- MODE OF LIFE AND HABITAT ated by length, thickness, number, arrange- Mackie (1991) described the mode of life

ment and plaque morphology. Permanent of D. polymorpha in the Great Lakes as an by guest on July 8, 2011 attachment threads are formed in clumps or epifaunal one but recent research by Clax- are arranged in rows and make up the ma- ton (University of Guelph, Guelph, Ontario, jority of a byssal mass. Temporary attach- pers. comm.) indicates that D. bugensis has ment threads are few in number (1-6), ar- an ability for an epibenthic habit in deeper ranged in a tripod pattern, originate individ- waters. He collected benthic samples and ually, and are separated spatially from the settlement data from plexiglass plates at 1 main byssal mass of permanent threads. to 36.6 m and found that recruitment rates Temporary threads are secreted before or (No./m2) decreased significantly (P < 0.05) after the initial byssal mass attachment. with increasing depth, the greatest recruit- Adult mussels (2 to 2.5 mm shell length) ment occurring at 14.3 m and the least at secrete about 23 threads per mussel per 36.6 m. Benthic samples showed that the week but the rate of thread formation varies ratio of quagga to zebra mussels increased considerably, depending on size, tempera- significantly with increasing depth. Only ture and water quality. The total numbers quagga mussels were taken in Ekman grab of threads secreted can be estimated from samples at 36.6 m. Claxton (personal com- the regression, No. threads = -8.59 + munication) suggested that quagga mussels 19.26(shell length, mm) (Claudi and Mack- may be altering their shell allometry for an ie, 1994). The threads are composed of epibenthic existence; quagga mussels are DOPA (3,4-dihydroxyphenyl-alanine), a thinner and lighter in weight in soft profun- prominent amino acid present in the byssus dal sediments than on firm inshore sub- of marine mollusks, but the precursors dif- strates, whereas zebra mussels exhibit little fer considerably in sequence (Rzepecki and or no changes in shell allometry on firm or Waite, 1993). The adhesive strength of the soft substrates. zebra mussel byssal thread varies with the composition of materials on which it is at- Zebra mussels are known to inhabit es- tached (Ackerman et al., 1992). pecially large freshwater lakes and rivers ZEBRA MUSSELS IN EUROPE AND NORTH AMERICA 247 Downloaded from icb.oxfordjournals.org by guest on July 8, 2011 FIG. 1. Shell characteristics of dreissenids in North America, (a)—(d) Dreissena polymorpha: (a) schematic drawing of end view showing carinate ventro-lateral margin (arrow) and concave ventral margin; (b) outer view of right valve; (c) inner view of right valve; (d) myophore plate; (e)-(h) Dreissena bugensis: (e) schematic drawing of end view showing rounded ventro-lateral margin (arrow) and convex ventral margin; (f) outer view of right valve; (g) inner view of right valve; (h) myophore plate; (i)—(I) : (i) schematic drawing of end view showing rounded ventro-lateral margin (arrow) and convex ventral margin; (j) outer view of right valve; (k) inner view of right valve; (1) myophore plate showing apophisis (arrow).

(Strayer, 1991) but the mussels also do well incipient lethal salinity for post-veligers is in cooling ponds, quarries, and irrigation near 2 ppt and for adults (5—15 mm) it is ponds of golf courses as well. Recent re- between 2 and 4 ppt (Kilgour et al., 1994). search in North America has also demon- strated that zebra mussels are capable of PHYSIOLOGY, BIOCHEMISTRY, GENETICS living in brackish water or estuaries where Several aspects of the physiology, bio- the salinity does not exceed 8 to 12 ppt (Na- chemistry, and genetics of zebra mussels lepa and Schloesser, 1993; Kilgour et al., have been described in the European liter- 1994). Temperature, the relative amounts of ature. These include osmotic and ionic reg- sodium and potassium (Deitz et al., 1996) ulation, desiccation resistance, filtration and the rate of acclimation to salinity great- characteristics, resistance to metabolites, ly affect the tolerance of larval and adult karyotypes, polymorphic systems, DNA mussels to salinity; at higher temperatures characteristics, and protamine descriptions, (18-20°C) the optimum salinity for adult uric acid composition, anerobic fermenta- mussels is about 1 ppt but at lower temper- tion products, and carotenoid content (see atures (3-12°C) the optimum salinity for Mackie et al., 1989 for literature review). adults is 2-4 ppt (Kilgour et al., 1994). The Recent, significant advances in our knowl- 248 G. L. MACKIE AND D. W. SCHLOESSER

edge of physiology and genetics of North conclusion that freshwater ballast in trans- American dreissenids are provided else- oceanic vessels transported zebra mussels where in this symposium. Many of these from Europe to the Laurentian Great Lakes: advances have improved our abilities to (1) the common presence of veligers in bal- predict the potential distribution range of last water combined with patterns of vessel zebra mussels in North America, the poten- traffic in the Great Lakes; (2) the introduc- tial biotic and abiotic impacts of dreissenids tion of other exotics {e.g., crustaceans) on North American waters, and our under- transported in ballast water; and (3) the in- standing of the regulatory processes mech- ability to identify other probable mecha- anisms that control reproduction and re- nisms. However, desiccation studies by Us- cruitment of zebra and quagga mussels. sery and McMahon (1994) suggest that it is also possible that adult mussels may have DISPERSAL MECHANISMS attached to anchors or their chains of ves- Mackie et al. (1989) and Carlton (1993) sels in European harbors and survived the review numerous potential dispersal mech- transoceanic voyage. This is probable if the anisms of larval and adult dreissenids, anchors and chains were stored on board many of them being natural mechanisms with sufficient moisture content to allow at {e.g., water currents, birds, insects, other least some mussels to survive the voyage ) but most being human-mediated and then drop off when ships anchored in Downloaded from {e.g., artificial waterways, ships and other the Great Lakes (McMahon, personal com- vessels, fishing activities, amphibious munication). planes, and recreational equipment, to men-

tion a few). The planktonic veliger stage is GEOGRAPHIC DISTRIBUTION icb.oxfordjournals.org probably the most effective natural dispers- The range of zebra mussels before the al phase, with intracontinental dispersal oc- 19th century occurred primarily over small curring quickly via downstream movement areas of the Black, Caspian, and Azov seas of the veligers. Artificial canals enhanced

(Stanczykowska, 1977). The limited distri- by guest on July 8, 2011 the dispersal of zebra mussels in Europe, bution of zebra mussels in 1800 was a re- especially in the USSR and Britain (Kerney sult of thousands of years of natural pro- and Morton, 1970). Not all mechanisms cesses. Between 1800 and 1900, zebra mus- have been verified, especially for the plank- sels more than doubled their range in Eu- tonic stage, which are usually not the first rope (Schloesser, 1995). The doubling of life stage found in a newly established mus- the range of mussels in only 100 years is sel population (Nalepa and Schloesser, attributed to human-mediated dispersal 1993). In general, natural dispersal of zebra mechanisms (Kinzelbach, 1992; Morton, mussels is believed to occur primarily by 1993). currents carrying planktonic veligers. How- Zebra, mussels were discovered in North ever, sedentary mussels attached to floating America in June 1988 in Lake St. Clair of debris may also distribute mussels. In ad- dition, juvenile and adult mussels can pos- the Laurentian Great Lakes (Hebert et al., sibly be dispersed by extending mucous 1989). Length-frequency analysis of known threads (up to 15 mm long) from the sur- populations in 1988 and review of studies face of the water by capillary action and performed before 1988 indicate that mus- drifting with surface water currents (Martel, sels became established in Lake St. Clair 1993). Dispersal caused by turtles, crayfish, and the most western portion of Lake Erie and birds may occur but is not well docu- downstream from Lake St. Clair in 1986 mented (Carlton, 1993). (Griffiths et al, 1991) (Fig. 2). This initial founding population occurred in a range Human-mediated dispersal mechanisms about 75 km north to south (N-S) by 25 km are believed to be the most common means east to west (E-W). By 1990, zebra mussels of distributing zebra mussels, especially be- occurred primarily downstream of the tween continents and unconnected water founding population in a range extending to bodies (Table 2). Carlton (1993) describes the extreme eastern and western ends of the three lines of evidence which lead to the Great Lakes—600 km N-S by 1,400 km ZEBRA MUSSELS IN EUROPE AND NORTH AMERICA 249 Downloaded from icb.oxfordjournals.org by guest on July 8, 2011

FIG. 2. Distribution of Dreissena polymorpha in four-year intervals from 1986 (Lake St. Clair and western basin of Lake Erie = stars), to 1991 (mainly all the Great Lakes = stippled areas), and 1994 (most major tributaries of Mississippi River and many inland areas = hatched areas) as described in text. 250 G. L. MACKIE AND D. W. SCHLOESSER

E-W. Mussels were also found at several grow in waters with pH as low as 7.3 and harbors and river mouths upstream of the calcium levels between 8 and 20 mg/liter, founding mussel population. In 1991, mus- infestation levels of abundance probably sels were found outside the Great Lakes will not occur until pH exceeds 7.5-8.0 and water basin. In 1992, mussels occurred as calcium levels exceed 15—20 mg/liter. far south as Vicksburg, Mississippi, west to Minneapolis, Minnesota, and north and east HABITAT DISTRIBUTION to Quebec. By 1994 mussels were found in Mackie et al. (1989) reviewed the Euro- a range extending 1,900 km N-S by 1,700 pean literature for information on the ver- km E-W. To date most of the infested wa- tical distribution of zebra mussel veligers ters are connecting rivers of the Mississippi and the abundance of adults in relation to River such as the upper Mississippi, Ten- depth. North American research is provid- nessee, Ohio, and Arkansas, although sev- ing new information on the vertical distri- eral lakes not connected to infested rivers bution of veligers of D. polymorpha and D. are also infested. In addition, live mussels bugensis. Fraleigh et al. (1993) reported attached to trailered boats have been found that wind driven currents have a profound as far west as Los Angeles, California. Ze- effect on the vertical distribution of zebra bra mussels are also well established in mussel veligers; significant depth effects were found only at wind velocities <8 km/h

Lake Simcoe, Ontario, where-most union- Downloaded from ids have 2 to 8 zebra mussels per unionid when 5% of the population was found at 0— (Trevor Claxton, personal communication), 2 m, 30% at 2-4 m, and 64% at 4-6 m. and appear to be following the same pat- Veligers are found deeper in the water col-

terns reported for Lake St. Clair unioinids umn when NOT mixed vertically by wind. icb.oxfordjournals.org (Gillis and Mackie, 1994). Smylie (1994) examined the depth distri- The factors that will limit the distribution bution of D. polymorpha on calm days and abundance of zebra mussels appear to (waves less than 10 cm high) and found peaks in abundance between 2 and 6 m at

be temperature, pH, and calcium content. by guest on July 8, 2011 Predictions for the spread of zebra mussels sites ranging from 6 to 20 m in Hamilton in North America are currently based on an Harbour (Lake Ontario) and at 18 m at a upper thermal tolerance of 26-32°C (Stray- site deeper than 35 m in Lake Erie, but al- er, 1991), a calcium threshold for survival ways at temperatures between 16.7 and 17.8°C at all sites. of 12 mg/liter (Neary and Leach, 1991), and a pH and calcium threshold for growth Perhaps wind driven currents have less and reproduction of 7.3 and 28.3 mg/liter, effect on the vertical distribution of veligers respectively (Ramcharan, 1992a, b). These in lakes with small surface areas than in criteria are largely based on European lab- lakes with large surface areas, like Lake oratory studies which showed particularly Erie. Based on European data, Fraleigh et highly variable response levels to calcium al. (1993) showed that the maximum den- (Mackie et al., 1989). However, Hincks sities of larvae tend to decrease with in- (1994), using both laboratory and field creasing surface area and depth of lakes. studies, examined the effects of pH levels However, Lake Erie, almost twice as large less than 7.0 and calcium levels lower than as the largest reservoirs {e.g., Kuibyshev 12 mg/liter on survival, growth and repro- Reservoir and Lake Ladoga) or lake studied duction of zebra mussels and found: 100% in Europe (Lake Constance), does not fit the mortality in water with pH less than 7.1, pattern and has the largest density of larvae mortality decreasing with increasing pH in lakes reported to date (Fraleigh et al., above 7.1; positive growth at levels above 1993). pH 7.1 and 8.5 mg Ca/liter; and reproduc- Dreissena bugensis first settled in the tion in waters with calcium levels above 20 eastern basin of Lake Erie in August, 1989 mg/liter. Mackie and Kilgour (1995) found (Riessen et al, 1993). By summer, 1990 the a pH threshold limit of survival for veligers quagga mussel had been dispersed to the at 7.4-7.5. Therefore, it appears that al- mouth of the Niagara River and by Decem- though zebra mussels may survive and ber 1990 to the eastern end of Lake Ontario ZEBRA MUSSELS IN EUROPE AND NORTH AMERICA 251

(Dermott, 1993). The quagga mussel had ences in veliger abundance between inshore succeeded in occupying the entire eastern and offshore waters, but when differences and most of the central basin of Lake Erie appeared, offshore waters had greater den- and occurred at several sites along the sities of than inshore waters. Doka (1994) southern shores (U.S.) of Lake Ontario by showed that while wave height, wind ve- July, 1992 (Dermott, 1993). The species has locity, and fetch hours did not correlate displaced the zebra mussel at many sites in strongly with recruitment rates, all three Lake Erie and is the only dreissenid found were significant variables in multiple re- in waters exceeding 40 m deep (Dermott, gression models for predicting size of re- 1993). The quagga mussel has been found cruitment of Dreissena populations in Lake in depths exceeding 150 m and is reported Erie. to grow and reproduce in profundal sedi- Different patterns of distribution have ments where the temperature never exceeds been reported for adults than for larvae. For 12°C (Dermott, 1993; Mills et al., 1995). adults the depth of maximum density is In spite of these differences, many simi- highly variable among lakes and varies sea- larities in horizontal and depth distributions sonally. However, the reasons for the sea- of zebra mussels exist between European sonal shifts appear to differ between Euro- and North American lakes. For veligers, the pean and North American studies. Mackie depth of maximum abundance typically et al. (1989) reported smaller, younger varies between 3 and 7 m, but maxima at specimens migrating from shallow water in Downloaded from 11 to 12 m are common (Mackie et al., the summer to deep water in the winter. 1989). Similar depths of maximum abun- This resulted in a seasonal shift of the age

dance are described for veligers in Euro- structure in the main belt of occurrence, icb.oxfordjournals.org pean lakes (Mackie et al., 1989) but as a from an increase in the proportion of young "belt of shore waters" around the perimeter specimens during summer to a decrease in of the lake. The width of the belt depends the winter. In North American populations on the bathymetry of the lake, the widest seasonal differences tend to be attributed to belts occurring in lakes with a shallow differences in size-selected "loss rates," the by guest on July 8, 2011 slope. losses representing both mortality and Few veligers occur below the thermo- translocation. Smaller mussels translocate cline in temperate lakes (Mackie et al., at higher rates than larger mussels (Martel, 1989; Fraleigh et al, 1993; Smylie, 1994). 1993), probably because larger mussels Variations in the vertical distribution of ve- have greater numbers of byssal threads ligers can usually be attributed to wind from neighboring individuals holding them driven currents. However, there are numer- in place (Claudi and Mackie, 1994). Bishop ous other factors. Secchi depth visibility and DeGaris (1976) found that dreissenids and temperature are two factors commonly tend to occur independently of other mol- attributed to variations in maximum densi- luscan species. However, this may be be- ties (Mackie et al., 1989). Moreover, there cause dreissenids have displaced other mol- appears to be a diurnal movement of veli- lusks (Gillis and Mackie, 1994; Schloesser gers, with maximum densities occurring et al., 1996). near the surface during early morning and at 5-7 m during the day (Mackie et al., PREDATORS 1989). Larval stages of mussels appear to be Veligers are usually contagiously distrib- consumed mainly by crustacean zooplank- uted, though the factors responsible for this ton (e.g., copepods) and larval fish, but the are not yet well understood. Mackie et al. relative importance of these prey groups to (1989) describe studies that show the patch- the total mortality of larval stages is un- iness is not due to prevailing winds in Pol- known (Mackie et al., 1989). In North ish lakes, but Martel (1993) has demonstrat- America, Conn and Conn (1993) reported ed that prevailing winds plays a major role predation of larval stages by the cnidarian, in the patchiness of veliger abundance in Hydra americana. Lake Erie. Smylie (1994) found few differ- Adult zebra mussels have a very high nu- 252 G. L. MACKIE AND D. W. SCHLOESSER

tritional value of the tissues, with 60.7% they do not seem to "affect the numbers" protein, 12.0% lipid, 19.0% carbohydrate, of the zebra mussel. and 5.9% ash (Cleven and Frenzel, 1992) The survey of the European literature of and are consumed in large quantities by Mackie et al. (1989) also concluded that crayfish, fish, and waterfowl (Mackie et al, trematodes are less common parasites of ze- 1989). The nutritional value changes sea- bra mussels than protists, the greatest infes- sonally. In Europe, Mackie et al. (1989) de- tation rate observed being 10%. The most scribe several European predation studies. dangerous protists are ciliates of the family Several species of fish consume zebra mus- Ophryoglenidae which parasitize the diges- sels but the roach seems to have the most tive gland and may kill the mussel. The significant impact on mussel densities. The trematodes, Phyllodistomum folium and Bu- roach has strong pharyngeal denticles and cephalus polymorphus are also important can consume large shells. In some Polish parasites in Netherland lakes where the in- lakes, the diet of roach consists almost ex- festation prevalence is usually about 1% clusively {i.e., 95-100%) of zebra mussels, and may go as high as 10% (Nalepa and although feeding on mussels may be sea- Schloesser, 1993). Infestation apparently sonal {e.g., autumn and winter). In general, lowers the resistance of mussels to metal it appears that fish do not limit the densities accumulation, infested mussels having higher levels of Zn, Cu, Cd, and Pb than

of D. polymorpha in European lakes. Downloaded from noninfested mussels. The effects of para- In North America, zebra mussels have sites on European populations of D. poly- been found in the stomachs of walleye, yel- morpha appear to be mininimal, at least un- low perch, freshwater drum, white suckers, til high emmisions of cercariae of B. poly- and a few others. The relative contribution morphus occur (Mackie et al., 1989). Inten- icb.oxfordjournals.org of the fish species to predation of zebra sity of parasitism by P. folium was directly mussels in North America is unknown. correlated to shell size of D. polymorpha, Only the freshwater drum, Aplodinotus the maximum number recorded being 200 grunniens, has been investigated in some at a shell size of 24-28 mm. by guest on July 8, 2011 detail (Nalepa and Schloesser, 1993); pre- dation on zebra mussels increases as drum Similar results have been reported in size increases, with large drum feeding al- North America by Toews et al. (1993). most exclusively on zebra mussels. The They reported a 2.9% prevalence of pla- freshwater drum is the only species in the giorchiid metacercariae in mussels and Great Lakes that has molariform pharyn- 2.7% prevalence of adults and juvenile as- geal teeth for crushing shells of mollusks. pidogastrids in mussels from two sites in The only other significant predator of zebra Lake Erie. The ciliate, Ophryoglena, was mussels is waterfowl and Maclsaac (1996) also found, with 1.3% prevalence at a site examines the recent literature and describes in Lake St. Clair and 2.7 to 4.3% preva- the effects of predators on dreissenids in lence at two sites in Lake Erie. Toews et al. North America. (1993) concluded that although parasites do not significantly affect changes in densities of D. polymorpha, there is a great proba- PARASITES bility that mass development of zebra mus- Freshwater bivalve mollusks are com- sels may increase the infection rate in de- mon intermediate hosts of parasites, partic- finitive hosts, especially fish and waterfowl. ularly trematodes, whose definitive hosts The oligochaete, Chaetogaster limnaei, and are fish, waterfowl, and sometimes humans the chironomid Paratany'tarsus, have also (Mackie, 1976). Mackie et al. (1989) con- been reported as commensals in zebra and cluded from their European literature sur- quagga mussels (Conn et al., 1994). vey that D. polymorpha is not a common vector of parasites. Protists and digeans PRODUCTIVITY were the most common parasites found, Densities of veligers and adults in the with Nematoda observed sporadically. Great Lakes are among the highest reported Many protists are common parasites but to date. Fraleigh et al. (1993) tabulated ZEBRA MUSSELS IN EUROPE AND NORTH AMERICA 253 mean monthly densities of veligers in eight and shell and body weight follow the power European lakes and reservoirs and found function, Weight = a X Lengthb, where b that the western basin and its island region varies between 1.937 and 3.284 for Euro- averaged 126-268 individuals/liter in July pean populations, depending on lake type and August (Leach [1993] reported means and time of year. Zebra mussel populations near 400/liter), whereas European waters in the Great Lakes fall within this range; averaged about 10-lOO/liter, the Konin Nalepa and Scloesser (1993) give studies Lakes being an exception with 22—320/liter that report slope values of 2.612 for total in the same period. Mean densities (No./m2) dry weight and 2.198 for dry tissue weight of adult range from about 54,000 (Dermott (vs. shell length); Mackie (1991) reports et al, 1993) to 779,000 (Pathy, 1994) in 2.996 and 2.982, respectively for the same Lake Erie to 43,000 in Lake St. Clair (Pa- variables. Neumann and Jenner (1994) pro- thy, 1994). Average densities of adult mus- vide studies that evaluate the use of shell sels in European lakes range from about length, shell height, and shell volume for 5,000 to about 115,000/m2 (Mackie et al, accurately predicting biomass of zebra and 1989). quagga mussels. Both shell height and shell The abundance of D. polymorpha has weight are good predictors of ash free dry been related to trophic type, the largest pop- weight (AFDW) for both species; volume measurements do not provide as good an

ulations occurring in eutrophic waters Downloaded from (Mackie et al, 1989). However, Stanczy- estimate of AFDW as did shell length and kowska (1964) found no relationship be- height. tween abundance of D. polymorpha and Estimates of annual production of D. trophic status of lakes. polymorpha in European waters are uncom- icb.oxfordjournals.org Biomass of D. polymorpha in a given mon but vary between 0.1 and 29.8 g/m2/yr water body is usually related to the density dry body weight and 3.3 and 525.9 g/m2/yr but the average biomass of populations is total dry weight (Mackie et al, 1989). In highly variable among lakes (e.g., 0.13 to the Great Lakes annual production of zebra 20 kg/m2) and within lakes (e.g., 0.05-10.5 mussels is higher than most European pop- by guest on July 8, 2011 kg/m2) (Mackie et al, 1989). Some of this ulations, about 150 g/m2/yr dry body variation is due to variations in body con- weight (Dermott et al, 1993). Cleven and dition of mussels and in length-weight re- Frenzel (1992) reported annual production lationships. Several indices of condition for River Seerhein, the outlet of Lake Con- 2 have been used; length, height and/or width stance, as 138 g Corg/m , including organic or "size" of shells; wet and dry weight of shell content. In European waters the P/B whole animals, shell only and dry tissue ratio varies between 0.42 and 0.65 for dry only; length:width ratio or slenderness; body weight and 0.47 and 0.81 for total dry length:height ratio or flatness; and the ratio weight (Mackie et al, 1989). The highest of wet weight to dry weight (Mackie et al, P/B ratio recorded is 6.8 for Lake Con- 1989). Of these, slenderness, flatness, and stance (Mackie et al, 1989), but the pop- ratio of wet to dry weight showed the least ulation was still in its exponential phase of variation within and among lakes; average growth and the P/B ratio may have dropped size and weight varied considerably among when the population stabilized. Dermott et lakes but tended to vary only slightly within al. (1993) reported a P/B ratio of 4.7 for a lakes; body (tissue) weight and shell weight population in Lake Erie. tended to vary in the same manner among lakes (i.e., lakes with high shell weights LIFE HISTORY also had high body weights) (Mackie et al, The life history of D. polymorpha and its 1989). variations are well known, especially for Mackie et al. (1989) examined the Eu- European waters (Mackie et al, 1989). ropean literature and concluded that varia- Ackerman et al (1994) have reviewed the tions in length-weight relationships corre- early life history of dreissenids and have lated highly with variations in environmen- standardized the terminology with that used tal conditions. Regressions of shell length for marine mussels. Variations in life his- 254 G. L. MACKIE AND D. W. SCHLOESSER

Plantigrade _ , , \ ^N 18-90 d,158-500um 20 Pedh/eliger \^—\ Velichoncha^y/ ^ \ /

D-Shape /^^ ' um ' N\ 15 \ / 2-9 d, 70-160um Trochophore^yf o° Threshold temperature \/ ^s \ CD for reproduction 7K\2 days, 83-95um Threshold temperature \ Eggs40-96um

atu 3 /_ \ Settleme c for growth / \

Temper Gametogenesis / \^ Gametogenesis ^^ 5 / V Downloaded from n I 1 i I i i 1 1 1 1 T r i i i r in co in in in in m o m icb.oxfordjournals.org T- CM T- a o ^ J= c

Jul § cu o .5 Apr Apr i/lay i/lay —5 1 3 u. u. S Time

FIG. 3. Life cycle of Dreissena polymorpha in relation to annual temperature cycle in Great Lakes region. by guest on July 8, 2011 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 reported by Doka (1994). At least one settlement event is possible based on maximum development times but some years may have two or more, depending on durations of each stage shown in bold italics. Size ranges are for heights of shells, as reported by Ackerman et al. (1994).

tory of North American zebra mussels have summarizes the annual life cycle of zebra been described by Mackie (1991, 1993), mussels in the Great Lakes in relation to Haag and Garton (1992), Garton and Haag temperature. Additional details are provided (1993), Claudi and Mackie (1994), and Pa- by Nichols (1996). thy (1994) but the variations are somewhat Settling stages are the most sensitive different from European populations. In Eu- stages and have high mortality rates, usu- rope, adults become sexually mature in ally 90-99% (Mackie et al., 1989; Nalepa their second year of life (Mackie et al., and Schloesser, 1993). However, these mor- 1989); in North America, zebra mussels be- tality rates did not consider immigration come sexually mature in their first year of and emmigration (translocation) of young life, usally by 8 to 10 mm in shell length. stages; Maclsaac et al. (1991) suggested Zebra mussels have exceedingly high fe- that when immigration and emmigration are cundities, varying from 30,000 to 1,610,000 accounted for, mortality could be as low as eggs/female (Mackie et al., 1989; Borch- 70% in the western basin of Lake Erie. erding, 1992). Typically, gametogenesis be- They indicated that larval mortality could gins in the fall after all gametes are spent, be lower during the colonization phase and continues through winter, with intensive then increase when adults become estab- growth of oocytes and spermatozoa in lished and begin to filter their own larvae. spring when mussels attain a shell length of There is often misuse of the terms "set- 8-9 mm or larger (Pathy, 1994). Fig. 3 tlement" and "recruitment". Settlement re- ZEBRA MUSSELS IN EUROPE AND NORTH AMERICA 255 fers to the passage from a pelagic habit to shell length >4.0 cm. Populations in the a benthic one and involves not only a Great Lakes are different still, where most change in position in the water column but mussels grow quickly (1.5—2.0 cm/yr) but attachment and certain morphometric their maximum size is typically only 2.5- changes as well (Doka, 1994). Recruitment 3.0 cm (Mackie, 1991). is essentially the process of settlement com- The growth rate of D. polymorpha is de- bined with post-settlement mortality. The pendent on quality and quantity of food, process is thought to be comprised of three temperature, and body size (Mackie et al., phases; larval supply, settlement, and meta- 1989). Growth rates decrease with increas- morphosis (Doka, 1994). Newly settled ing body size and increase with increasing mussels are considered recruits if they have food concentration up to 2 mg C/liter, with survived to a size or an elapsed period of an optimum between 10 and 15°C, although time set a priori by the investigator. Doka in the Great Lakes growth and settlement (1994) found that peaks in recruitment den- rates appear to be optimum between 15 and sities occurred at similar times among her 17°C (Smylie, 1994). The temperature study sites and between years; a peak in threshold for growth usually varies between recruitment can be expected during the first 10 and 12°C (Mackie et al., 1989; Neumann three weeks in August at most sites in Lake and Jenner, 1994; Smylie, 1994); a value as Erie. However, she found variability in the

low as 6°C was reported by Bij de Vaate Downloaded from number of recruitment events between sites, (1991). The quagga mussel appears to be probably because of local hydrological con- ditions delivering larval pulses toward able to reproduce at temperatures below shore. Nevertheless, adult population dy- 8°C, in the hypolimnion of Lake Erie (Tre- namics appear to be regulated, in part at vor Claxton, University of Guelph, Guelph, icb.oxfordjournals.org least, by recruitment fluctuations as "sup- Ont., personal communication). ply-side" ecology suggests (Doka, 1994). The life span of D. polymorpha is highly variable, but it appears that North American

populations have a shorter longevity than by guest on July 8, 2011 AGE AND GROWTH European populations. The average life The growth rate of larvae in nature is span of zebra mussels is 3-5 years in most highly variable, depending mainly on tem- Polish lakes, 5 years in British waters, and perature (Mackie et al., 1989) and chloro- 6—9 years in some Russian reservoirs phyll a content (Smylie, 1994). Estimates of (Mackie et al., 1989). In North America, larval growth rates of zebra mussels are most zebra mussel populations have a life few; 1 to 4 |xm/d for larvae in two lakes in span of about 1.5 to 2 years (Mackie, 1991). Germany (Mackie et al., 1989), 6.0 to 11 Zebra mussels inhabiting heated waters u.m/d for a drifting population in the River have life spans truncated by about 1 year Rhine (Neumann and Jenner, 1994), and 2.4 compared to unheated lakes in the same to 23.7 jim/d for larvae at several sites in area (Mackie et al., 1989). Lake Erie (Smylie, 1994). Smylie (1994) also reared larvae in the laboratory and FOOD AND FEEDING achieved 4.1 to 4.5 u,m/d at 13.1°C and 6.5 to 8.7 u,m/d at 16.6°C. Food selection is performed by a variety The relationship between age and growth of cilia, including those in the mantle cavity of mussels varies considerably, much of the (gills, labial palps and foot) and in the variation being due to the method used to stomach and midgut. Cilia in the mantle age the mussels. Mackie et al. (1989) de- cavity and stomach select particles of 15— scribe two patterns of growth in European 40 (xm for food but can filter out particles populations, "slow-growing" and "fast- as small as 0.7-1.0 u.m in diameter from growing" populations. The maximum the water (see Mackie et al., 1989 for re- growth rate for the slow-growing group ap- view). Significant advancements in our pears to be less than 1 cm/yr with a maxi- knowledge of ciliary filter feeding process- mum shell size of 3.5 cm; the fast-growing es and feeding habits have been made by group exceeds 1.5 cm/yr with a maximum Silverman et al. (1996) Maclsaac (1996) 256 G. L. MACKIE AND D. W. SCHLOESSER and should be consulted for a detailed dis- mussel, pp. 677-697. In T. F. Nalepa and D. W. cussion of feeding in dreissenids. Schoesser (eds.), Zebra mussels: Biology, impacts, and control, pp. 677-698. Lewis/CRC Press, Inc., The filtration rate is affected by size, tur- Boca Raton, FL. 810 pp. bidity, temperature, and certain concentra- Claudi, R. and G. L. Mackie. 1994. Practical manual tions of specific sizes and kinds of algal for zebra mussel monitoring and control. Lewis cells (e.g., Chlamydomonas) and bacterial Publishers, Boca Raton, FL. cells (Mackie et ai, 1989; Reeders and bij Cleven, E. and P. Frenzel. 1992. Population dynamics and production of Dreissena polymorpha in the de Vaate, 1989; Reeders et al, 1993). The River Seerhein, the outlet of Lake Constance. In filtration capability of D. polymorpha in re- D. Neumann and H. A. Jenner (eds.), The zebra lation to its role as a clarifier of water in an mussel Dreissena polymorpha, pp. 45-47. Gustav entire lake, epilimnion or littoral zone has Fischer Verlag, New York, NY. been reviewed by Neumann and Jenner Conn, D. B. and D. A. Conn. 1993. Parasitism, pre- (1992); they also describe applications of dation, and other associations between dreissenid mussels and native animals in the St. Lawrence zebra mussels in water quality manage- River. Proceedings: Third International Zebra ment, particularly as water clarifiers. Al- Mussel Conference, 1993. Electric Power Re- though mussels are efficient clarifiers, the search Institute, Inc., Pleasant Hill, CA, pp. 2-25- suspended materials accumulate on the bot- 2-34. tom as faeces and pseudofaeces. The size Conn, D. B., M. A. Babapulle, and K. A. Klein. 1994. of faecal and pseudofaecal pellets varies Invading the invaders: Infestation of zebra mus-

sels by native parasites in the St. Lawrence River. Downloaded from with mussel size and the settling velocities Proceedings 4th International Zebra Mussel Con- and rate of accumulation greatly exceed ference, Madison, WI, March 1994. pp. 515-524. normal sedimentation processes (Dean, Dean, D. M. 1994. Investigations of biodeposition by 1994). Dreissena polymorpha and settling velocities of faeces and pseudofaeces. M.Sc. diss., University icb.oxfordjournals.org of Guelph, Guelph, Ontario. ACKNOWLEDGMENTS Dermott, R. M. 1993. Distribution and ecological im- Contribution Number 955, National Biolog- pact of "quagga" mussels in the lower Great Lakes. Proceedings: Third International Zebra ical Service, Great Lakes Science Center, Mussel Conference, 1993. Electric Power Re- by guest on July 8, 2011 1451 Green Road, Ann Arbor, Michigan search Institute, Inc., Pleasant Hill, CA, pp. 2-1- 48105. 2-21. Dermott, R. M., J. Mitchell, I. Murray, and E. Fear. REFERENCES 1993. Biomass and production of zebra mussels (Dreissena polymorpha) in shallow waters of Ackerman, J. D., C. R. Ethier, D. G. Allen, and J. K. northeastern Lake Erie. In T. F. Nalepa and D. W. Spelt. 1992. Investigation of zebra mussel adhe- Schoesser (eds.), Zebra mussels: Biology, impacts, sion strength using rotating discs. J. Env. Eng. and control, pp. 399-414. Lewis/CRC Press, Inc., 118:708-724. Boca Raton, FL. Ackerman, J. D., B. Sim, S. J. Nichols, and R. Claudi. Dietz, T. H., S. J. Wilcox, R. A. Byrne, J. W. Lynn, 1994. A review of the early life history of zebra and H. Silverman. 1996. Osmotic and ionic reg- mussels (Dreissena polymorpha): Comparisons ulation of North American zebra mussels (Dreis- with marine bivalves. Can. J. Zool. 72:1169- sena polymorpha). Amer. Zool. 36:326-338. 1179. Doka, S. E. 1994. Spatio-temporal dynamics and en- Bij de Vaate, A. 1991. Distribution and aspects of vironmental prediction of recruitment in industrial population dynamics of the zebra mussel, Dreis- and nearshore Dreissena populations of Lake Erie. sena polymorpha (Pallas, 1771), in the lake Ijss- elmeer area (the Netherlands). Oecologia 86:40- M.Sc. Diss., University of Guelph, Guelph, On- 50. tario. Bishop, M. J. and H. Degaris. 1976. A note on pop- Ekroat, L. E., E. C. Mastellar, J. C. Shaffer, and L. M. ulation densities of Mollusca in the River Great Steele. 1993. The byssus of the zebra mussel Ouse at Ely, Cambridgeshire. Hydrobiologia 48: (Dreissena polymorpha): Morphology, byssal 195-197. thread formation, and detachment. In T. F. Nalepa Borcherding, J. 1992. Morphometric changes in re- and D. W. Schoesser (eds.), Zebra mussels: Biol- lation to the annual reproductive cycle in Dreis- ogy, impacts, and control, pp. 239—264. Lew- sena polymorpha—a prerequisite for biomonitor- is/CRC Press, Inc., Boca Raton, FL. ing studies with zebra mussels. In D. Neumann Fraleigh, P. C, P. L. Klerks, G. Gubanich, G. Matisoff, and H. A. Jenner (eds.). The zebra mussel Dreis- and R. C. Stevenson. 1993. Abundance and set- sena polymorpha, pp. 87-99. Gustav Fischer Ver- tling of zebra mussel (Dreissena polymorpha) ve- lag. New York, NY. ligers in western and central Lake Erie. In T. F Carlton, J. T. 1993. Dispersal mechanisms of the zebra Nalepa and D. W. Schoesser (eds.), Zebra mus- ZEBRA MUSSELS IN EUROPE AND NORTH AMERICA 257

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