Potential Abioti anc d Biotic Impact os f Zebra Mussel os ...freshwater communities based on European and North American studies. Taxa benefiting from Dreissena in-vasion are indicated

AMER. ZOOL., 36:287-299 (1996)

Potential Abiotic and Biotic Impacts of Zebra Mussels on theInland Waters of North America1

HUGH J. MACISAAC

Department of Biological Sciences andGreat Lakes Institute for Environmental Research,

University of Windsor, Windsor, Ontario N9B 3P4, Canada

SYNOPSIS. The expansion of zebra mussel distribution into inland wa-terways of North America portends significant abiotic and biotic changesmediated either directly or indirectly by Dreissena. Dreissena fouls awide array of submerged substrates including rock surfaces, macrophytes,native molluscs, canal and dock walls, and watercraft and motor out-drives. Fouling of water intake pipes and associated installations can se-verely impair water delivery to hydroelectric, municipal and industrialusers, necessitating proactive or reactive control measures. Mussels in-crease water clarity by removing suspended clay, silt, bacteria, phyto-plankton, and small zooplankton. Clear water phases associated withDreissena grazing may exceed in magnitude and duration those generatedby zooplankton grazing. Enhanced water clarity increases light transmit-tance and growth of benthic plants. Some benthic invertebrates {e.g.,unionid molluscs) are adversely affected by Dreissena, whereas others,including amphipod crustaceans, exploit structure associated with orwastes generated by zebra mussels. Dreissena is exploited by a host ofpredators, most notably waterfowl, fish and crayfish. Waterfowl predatorsthat consume contaminated Dreissena have elevated concentrations oforganic pesticides and polychlorinated biphenyl compounds. Invasion ofshallow lakes and ponds by Dreissena may divert production and biomassfrom pelagic to benthic foodwebs, shifting ecosystems to an alternativestate.

When new species arrive and spread, munity composition or structure (Mills eteven if they do not have the appearance al., 1993). However, significant economicof the explosive invader, they may herald and ecological problems have been record-the onset of future changes in the balance ed in a diverse array of ecosystems invadedof populations by exotic species {e.g., see McCoid, 1991).

—Charles Elton, 1958 In addition to affecting community com-position and species diversity, exotic spe-

INTRODUCTION c j e s m a v ai{e r nutrient cycling and energyCharles Elton's (1958) classic work illus- flow in ecosystems {e.g., Walker and Vitou-

trated the extent to which human activities sek, 1991).have deliberately or unwittingly facilitated At least 36 mollusc species have been in-the global movement and interchange of traduced to Atlantic, Pacific and Gulf coastsspecies. The introduction of species to new of North America, including some that haveecosystems often results in little conspicu- caused significant economic and ecologicalous change in native species diversity, com- problems (Carlton, 1992). For example, the

Asian clam Corbicula fluminea has causedsevere fouling of water works installations

' From the Symposium The Biology Ecology and t h r o u g h o u t t h e southern United States (Me-Physiology of Zebra Mussels presented at the Annual . , ^ « - , ^ » , . •Meeting of the American Society of Zoologists, 4-8 Mahon, 1983). More recently, dramatic re-January 1995, at St. Louis, Missouri. ductions in phytoplankton and zooplankton

287

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288 HUGH J. MACISAAC

Piscivorous> fishes

Zooplankton - - - - - • • Planktivorousf k fishes

p'hytoplankton Molluscivorous* fishes

DivingWaterfowl

Feces,Pseudofeces

Suspended U n i o J i dmussels

BenthicInvertebrates

FIG. 1. Schematic of observed (solid line) and potential (dotted line) impacts of Dreissena polymorpha infreshwater communities based on European and North American studies. Taxa benefiting from Dreissena in-vasion are indicated with a (+) symbol on the arrowhead, those adversely affected by a (-) symbol. Stronginteractions are denoted by thicker arrows. Only interactions in which Dreissena directly or indirectly affectsother taxa are included. Dreissena may indirectly impact planktivorous and piscivorous fish by altering foodsupply or habitat quality. Refer to text for specific examples of each interaction.

biomass and displacement of the softshellclam Mya arenaria in San Francisco Bayhave been ascribed to the clam Potamocor-bula amurensis, a 1986 invader of the baycommunity (Nichols et al., 1990; Kimmereret al, 1994).

While these introductions had pro-nounced effects on recipient communities,the 1986 invasion of the North AmericanGreat Lakes by the zebra mussel Dreissenapolymorpha provides one of the most in-structive examples to date of ecologicalmodifications and economic damage asso-ciated with human-mediated species intro-ductions (Hebert et al., 1989). Despite itsbrief history in North America, the zebramussel has already had dramatic effects oninvaded systems. These impacts are bothabiotic and biotic, direct and indirect. In thefollowing sections, I review realized and

potential effects of Dreissena on inlandlakes and rivers of North America based onEuropean and Great Lakes' precedents.Forecasting specific impacts in a particularsystem is a tenuous practice, though evi-dence gleaned from previous Dreissena in-vasions permits some generalizations re-garding anticipated impacts in newly invad-ed systems (Fig. 1).

IMPACTS ON WATER USERS

Perhaps the greatest abiotic effect ex-pected of zebra mussels in newly invadedlakes, reservoirs, streams, navigation chan-nels and locks will be problems associatedwith mussel biofouling. In the Great Lakes,Dreissena fouling is generally limited tostructures submerged below 1.2-m depth(Claudi and Mackie, 1994). Permanent ma-rine structures including pilings, bridges

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ZEBRA MUSSEL IMPACTS IN NORTH AMERICA 289

and docks are particularly vulnerable tofouling. Temporary marine structures in-cluding buoys and other navigational aids,and fishing nets, may also be fouled de-pending on availability of competent lar-vae, resuspended postmetamorphic juve-niles, and mobile adults (Martel, 1993).Fouling of recreational and commercial wa-tercraft has contributed to the export ofDreissena from the Great Lakes (Carlton,1993).

Water intake structures for municipal, in-dustrial and hydroelectric plants are highlyvulnerable to fouling if they draw from wa-terbodies contaminated with adult or larvalDreissena. Power plant components thatmay become fouled include crib structures,trash bars, screenhouses, steam condensers,heat exchangers, penstocks, service watersystems and water level gauges (Kovalak etal, 1993; Claudi and Mackie, 1994). Verylong or narrow pipelines are particularlyvulnerable to fouling and severely impededflow (Claudi and Mackie, 1994). Kovalaket al. (1993) reported mussel densities ashigh as 750,000 ind.m-2 at the Monroepower plant in western Lake Erie. Thesevalues far exceeded densities (<5000ind.m"2) on adjacent lakebed at that time,and at a nearby (Fermi) nuclear power plantthat utilized ~30 times less water than theMonroe facility (Kovalak et al., 1993). Ex-traordinary mussel densities can beachieved in raw water intakes because ofthe enormous number of potential colonistsentrained in the intake current, constant re-plenishment of food resources and removalof mussel wastes, and the absence of pred-ators.

The intensity of mussel fouling dependscritically on substrate type (Table 1). Kil-gour and Mackie (1993) reported coloni-zation differences greater than four ordersof magnitude on substrates ranging fromcopper to stainless steel. Many materialsused to construct dams, retaining walls,piers and pipelines {e.g., concrete, galva-nized iron, PVC) are suitable colonizationsubstrates for Dreissena (Walz, 1975; Kil-gour and Mackie, 1993). Mussel foulingalso depends on current velocity. Flow ve-locities exceeding 1.5 m-sec"1 minimizemussel settlement in raw water intakes

TABLE 1. Colonization of select substrates by D.polymorpha.'

Settling substratecomposition

CopperGalvanized IronAluminumPVCTeflonPressure-treated

woodPolypropyleneStainless SteelCharaceaeD. polymorpha

coloniesStonesSandMud

PolyvinylchloridePolypropylenePolyolefine

Mussels-sub-

strate"1

0548

2,3247,4718,593

15,25517,55421,812

1,727

455611313

241817

Reference

Kilgour and Mackie,1993

Lewandowski, 1982

Walz, 19752

1 Methodological differences among studies limitcomparisons to substrates within studies.

2 Based on exposure of colonization plates for 93days.

(Claudi and Mackie, 1994). The raw waterintake for the city of Windsor, Ontario, hasa flow velocity ~2.5 msec"1 and has notbeen fouled internally by zebra mussels (P.McQuarrie, personal communication).

ABIOTIC EFFECTS

A prominent and important abiotic effectof Dreissena in invaded ecosystems is en-hanced water clarity. In contrast to the gen-erally negative attitude held of Dreissenaby most North Americans, the species hasbeen intentionally stocked in lakes in theNetherlands as a "biomanipulation" tool toremedy poor water quality (see Reeders andBij de Vaate, 1990; Noordhuis et al., 1992).Water clarity, measured as Secchi disktransparency, is inversely related to the con-centration of suspended sediments, detritusand plankton (Preisendorfer, 1986). Zebramussels possess unique attributes that ren-der them suitable water quality manage-ment "tools." First, because zebra musselsare present year-round, filtering impacts aremuch less ephemeral than those of zoo-plankton (see Maclsaac et al., 1992; Nich-olls and Hopkins, 1993). Second, Dreissena

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may achieve population biomasses fargreater than those of herbivorous zooplank-ton. For example, dry mussel biomass val-ues >150 mg-cm~2 rock surface area wereobserved in western Lake Erie (MacIsaac,1996). Third, unlike most zooplankton thatconsume only a narrow size spectrum offoods, usually between 2 and 25 |i,m (Stern-er, 1989), zebra mussels filter a muchbroader suite of particles. Ten Winkel andDavids (1982) described positive selectionby Dreissena of particles between 15 and40 |xm, though particles up to 750 u,m wereingested. Dreissena also appears capable ofingesting particles finer than those con-sumed by most zooplankton. Sprung andRose (1988) observed that Dreissena in-gested particles as small as 0.7 |xm, thoughat low efficiency. More recent work has es-tablished that ~l-u,m bacteria are efficient-ly cleared from suspension (see Silvermanet al., 1996). Roditi et al. (1995) reportedthat Dreissena removed particles between0.4 and >40 |xm with approximately equalefficiency. These findings support those ofCotner et al. (1995), who observed thatDreissena cleared 0.36 and 0.91 u,m mi-crospheres from suspension at nearlyequivalent rates, and suggested that thelower limit for particle removal is in therange of 0.22—0.36 u,m. Ingestion of sub-micron particles by Dreissena greatly ex-pands the range and quantity of suitableresources.

Dreissena-induced improvements in wa-ter clarity need not result from ingestion ofsuspended particles. As with many marinebivalves, Dreissena selects particles for in-gestion on the basis of size, and possiblytaste (Morton, 1971; Ten Winkel and Da-vids, 1982; Sprung and Rose, 1988). Sus-pended clays, silts, and large phytoplanktoncells (e.g., Asterionella formosd) entrainedin the inhalant current are sorted on the la-bial palps, enveloped in mucus, and ex-pelled as pseudofeces via the inhalant si-phon (Walz, 1978; Ten Winkel and Davids,1982). Dreissena increased feces and pseu-dofeces production when exposed to 25-250 mgliter"1 suspensions of l-p-m illite-smectite clay (MacIsaac and Rocha, 1995).Field patterns generally support the viewthat biodeposition of feces and pseudofeces

associated with mussel filtering activitiescan improve water clarity. Griffiths (1993)reported that Secchi disk transparency inLake St. Clair increased from 0.5 to 1.5 mprior to Dreissena invasion to between 1.8and 2.8 m in 1990. Water transparency in-creased by 100% in the southern portion ofthe west basin of Lake Erie between 1990and 1992 relative to 1984 and 1986 (Hol-land, 1993). Transparency also increased inthe north section of the west basin, as wellas in the west-central and eastern (LongPoint Bay) basins of the lake following es-tablishment of large Dreissena populations(Leach, 1993; R. Knapton, personal com-munication). This pattern has been repeatedin inner Saginaw Bay, Lake Huron. Meanturbidity declined from 9.2 NTU in 1991,one year following initial observations ofDreissena in the bay, to 8.3 NTU in 1992when maximum mussel density was almostfive times higher; turbidity declined furtherin 1993 to 3.7 NTU (Skubinna et al., 1995).A clear demonstration of D. polymorpha'sability to clarify natural systems was pro-vided following the introduction of mus-sels, at a density of 540 ind.m"2, into oneof two adjacent, hypertrophic ponds in theNetherlands (Reeders et al., 1993). Secchidisk transparency was consistently higher inthe treated pond relative to the referencesystem.

It is interesting to note that Dreissena-mediated changes in water transparencyhave generally occurred in shallow, well-mixed lakes, ponds and embayments. Theeffects of Dreissena on water quality in lo-tic environments are less clear. A review ofEuropean studies revealed that mussels areconfined largely to rivers >30 m wide(Strayer, 1991). Minimum nephelometricturbidity of Detroit River water declinedsignificantly (33% overall) following Dreis-sena invasion of Lake St. Clair, the river'ssource (t = 3.96, df = 12, P = 0.0019)(Fig. 2). Dreissena colonized the HudsonRiver, New York, in 1991 and experienceda large population increase in 1992 (M.Pace, personal communication). The musselis attributed with massive (—90%) reduc-tions in algal and microzooplankton bio-mass but only a 7% increase in water trans-parency, perhaps owing to resuspension of

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8 l

6 -

•o

S 4 -3

1980 1985 1990 1994Year

FIG. 2. Variation (mean ± 1 SE) in water turbidity inthe Detroit River for the June 1-Sept. 30 period between1981 and 1994. Means are based on 10-day minimumvalues for each month. The solid line separates yearsprior and subsequent to development of large Dreissenapopulations at upstream sites in Lake St. Clair (see He-bert et al., 1991); the dotted line indicates the putativeinvasion date (Hebert el ai, 1989). Mean turbidity leveldeclined significantly following Dreissena establish-ment in the lake (Maclsaac and Rocha, 1995).

feces and pseudofeces (M. Pace and N. Car-aco, personal communications). Althoughempirical evidence is lacking, water trans-parency changes may be more apparent inslow-flowing rivers that mix less thorough-ly than tide-influenced systems like theHudson River. Thus, a continuum may existfrom non-stratified lakes and rivers withpoor to moderate mixing to stratified lakesand well mixed rivers, wherein respectiveDreissena effects on turbidity and transpar-ency decline from pronounced to almostnonapparent.

One factor that could reduce the impactof Dreissena on water quality is the pres-ence of high concentrations of suspendedinorganic particles. Alexander et al. (1994)observed significant but unexplained de-creases in Dreissena respiration when ani-mals were exposed to a moderate (31mgliter"1) concentration of bentonite clay.Dreissena stopped filtering during sedimentresuspension in Lake Druzno, Poland, andresumed only when small particles re-mained suspended (Wisniewski, 1990). De-spite this sensitivity, overall ingestion rate(mg seston consumedind"'hr"') of musselsexposed to suspended sediment was equalto or greater than those of individuals in

treatments lacking sediment (Wisniewski,1990). Maclsaac and Rocha (1995) ob-served that the proportion of time spentwith valves closed was <3% even in thepresence of high concentrations of illite-smectite clay. Mussels chronically exposedto high concentrations of suspended sedi-ments may increase the palp to gill surfacearea ratio to effect efficient sorting of foodand non-food particles (Payne et al., 1995).Thus, both behavioral and anatomical re-sponses permit Dreissena to tolerate turbidwater conditions characteristic of many riv-er systems. It is unclear, however, whetherDreissena will demonstrably impact waterquality in turbid systems like the southernMississippi River, considering that addi-tional stressors {e.g., temperature) may af-fect mussels at these localities.

One possible physical change yet to beexplored in lakes and reservoirs invaded byDreissena is alteration of mixing depth. Be-cause Secchi disk depth is positively cor-related with mixing depth (Mazumder etal., 1990), any Dreissena-induced reductionin concentrations of suspended inorganic ororganic particles that results in greater in-cident solar radiation penetration could alsoincrease epilimnion depth. Such a changecould alter, among other things, the ratiobetween and respective volumes of the epi-limnion and hypolimnion, as well as the hy-polimnetic oxygen depletion rate. An in-crease in the latter parameter would be ofparticular importance in basins vulnerableto seasonal anoxia (e.g., central Lake Erie).

BIOTIC EFFECTS

Some European and North Americanfreshwater communities have experiencedprofound ecological changes subsequent toinvasion by D. polymorpha. Biota impactedby Dreissena encompass most categories oflife in freshwater ecosystems.

One of the most predictable effects ofDreissena invasions of lakes and rivers isgreatly diminished phytoplankton biomass.By ingesting or enveloping phytoplanktoncells in negatively buoyant pseudofecal pel-lets, mussels can greatly reduce phyto-plankton standing biomass, particularly inwell mixed systems in which refiltration ofwater is reduced. For example, Reeders et

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al. (1993) reported a pronounced decline(~46%) in phytoplankton biovolume in apond stocked with Dreissena relative to areference pond lacking mussels. Phyto-plankton biomass, as estimated by chloro-phyll a concentration, also declined dra-matically (~60%) in the western and west-central basins of Lake Erie between 1988and 1991, and in Saginaw Bay (59%) sub-sequent to establishment of large Dreissenapopulations (Leach, 1993; Fahnenstiel etal, 1995). Depletion of phytoplankton inwestern Lake Erie was most severe directlyover mussel beds (MacIsaac et al., 1992),and in the southeastern section of the basin(82-91% reduction) (Holland, 1993). Phy-toplankton depletion has also been ob-served in inland lakes and rivers. Chloro-phyll a concentration declined sharply be-tween 1990 and 1993 in Oneida Lake, andbetween 1991 and 1992 in the Hudson Riv-er (90% decline) commensurate with dra-matic growth of Dreissena populations (E.L. Mills, M. Pace, personal communica-tions). Nicholls and Hopkins (1993) statedthat the decline in phytoplankton density inLake Erie was incompatible with predic-tions based on phosphorus concentration,but was consistent with that expected byDreissena feeding.

It is not clear whether vulnerability tomussel ingestion varies among phytoplank-ton taxa, nor whether Dreissena filtering ac-tivities promote changes in phytoplanktoncommunity composition. In western LakeErie, all major phytoplankton taxa {e.g., Ba-cillariophyceae, Cyanophyceae, Cryptophy-ceae), including large colonial forms, ex-perienced abundance declines following in-vasion of the basin by Dreissena (Nichollsand Hopkins, 1993). Similarly, Dreissenaingested spherical algal colonies (>l-mm)and filaments (>3-mm length) from OneidaLake (E. L. Mills, personal communica-tion). These studies corroborate earlierwork that established broad feeding capa-bilities of Dreissena (Ten Winkel and Da-vids, 1982), but contradict results from amesocosm grazing experiment in SaginawBay in which the standing crops of diatomsand chlorophytes were differentially sup-pressed relative to those of colonial cyano-bacteria (Microcystis) and large chryso-

phytes (Synura) when exposed to Dreissena(Heath et al., 1995). Thus, despite the abil-ity to consume a wide size range of phy-toplankton cells, Dreissena may feed pref-erentially on particles between <1- and<50-u,m (Ten Winkel and Davids, 1982;Cotner et al, 1995; Roditi et al, 1996; Sil-verman et al, 1996). Results from differentstudies may be reconciled if feeding selec-tivity is hunger-dependent; Ten Winkel andDavids (1982) observed that mussels tem-porarily deprived of food fed indiscrimi-nately on natural seston that included cellsas large as 750-|xm, whereas well-nourishedindividuals fed selectively on a much nar-rower range of particles. Non-selectivefeeding could be important in systems sup-porting high mussel densities but low phy-toplankton biomass.

Cyanobacteria blooms have been report-ed in basins supporting large mussel pop-ulations, including western Lake Erie (J. H.Leach, unpublished data), Saginaw Bay(Heath et al, 1995) and Oneida Lake (E.L. Mills, personal communication). Con-versely, cyanobacteria (Anabaena, Oscilla-toria and Aphanizomenori) blooms devel-oped in a reference pond lacking Dreissena,but not in a pond stocked with mussels(Reeders et al, 1993). Possible factors thatmay account for enhanced cyanobacteriaabundance in systems with Dreissena in-clude a reduction in the N:P ratio, enhancedlight penetration, greater buoyancy of cy-anobacteria filaments, or chemical or me-chanical inhibition of mussel filtering bycyanobacteria. D. polymorpha and D. bug-ensis (quagga mussel) did not open theirvalves or feed, and experienced between 30and 100% mortality, when exposed to 10-25 g-liter'1 Mycrocystis aeruginosa (Birgeret al, 1978). Mussel filtering activity wasalso diminished in Saginaw Bay during acyanobacteria bloom (Heath et al 1995).Mechanical interference by large, armoredCeratium cells was attributed with seasonaldeclines in Dreissena filtering rate in LakeMikolajskie, Poland (Stanczykowska et al,1976).

Three important factors that can influ-ence Dreissena filtering impact in lakes andrivers are ambient temperature, seston con-centration and mussel size frequency distri-

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bution. Reeders and Bij de Vaate (1990)proposed that filtering rate (ml fil-teredmussel^'hr"1) was maximal between5 and 20°C, but declined sharply at eitherlower or higher temperatures. By contrast,Morton (1971) reported progressive in-creases in filtering rate up to a maximal val-ue at 30°C; beyond this temperature, two ofthree mussels died. Walz (1978) observedthat Dreissena ingestion rate (u,g ingest-ed-mussel~1-hr~1) could be modeled by abell curve, with an optimal value at 12.5°C.Despite these divergent results, temperaturecould be a very important factor limitingactivity or distribution of mussels in south-ern U.S.A. rivers, lakes and reservoirs if themussels' thermal preference or tolerancelimits are exceeded.

Seston concentration has a profound ef-fect on assimilation efficiency of Dreissena.Ingestion rate increases linearly with foodconcentration until an asymptote is reachedat the incipient limiting level (Walz, 1978;Sprung and Rose, 1988). Filtering rate,which is constant and maximal below theincipient limiting level, declines exponen-tially above it (Sprung and Rose, 1988).Walz (1978) estimated the incipient limitinglevel at ~2 u,g C-ml~', and the onset ofpseudofeces production at approximatelyone tenth this value. The proportion of foodexpelled as pseudofeces increased rapidly atfood levels above 0.2 u.g Cml~' (Walz,1978).

Zooplankton populations may be ad-versely impacted either indirectly or direct-ly by Dreissena. Populations of small zoo-plankton, particularly rotifers and Dreis-sena veligers, were suppressed when incu-bated with Dreissena >10-mm (Maclsaacet ai, 1991, 1995). Small zooplankton (e.g.,Keratella, Polyarthra) entrained in the in-halant stream of feeding mussels fail toelicit a rejection response by Dreissena, areincapable of escaping from the current, andare ingested (Maclsaac et al, 1991). Largezooplankton can either evade mussel feed-ing currents or are expelled from the inha-lant siphon area following contact with, andirritation of, siphonal tentacles. In westernLake Erie, rotifer abundance declined by74% between 1988 and the 1989-1993 pe-riod; this change occurred coincident with

establishment of enormous Dreissena pop-ulations (up to 342,000 ind.m"2) beginningin 1989 (Leach, 1993; Maclsaac et al,1995). Cladoceran density has not changedappreciably, though total copepod abun-dance (mainly nauplii) declined between39% and 69% between 1988 and 1993. Itis difficult to discriminate between suppres-sion of zooplankton resulting from directingestion by Dreissena and that causedfood limitation. However, the direct sup-pression hypothesis is supported by resultsfrom San Francisco Bay, where the exoticclam Potamocorbula is attributed with in-gestion and strong suppression of copepodnauplii (Kimmerer et al., 1994). Moreover,recruitment of settling Dreissena on tiles inSaginaw Bay was inversely related to adultdensity, indicating possible direct ingestionof larvae (Nalepa et al., 1995). Rotifers andprotozoans were strongly suppressed in theHudson River subsequent to developmentof a large Dreissena population in 1992,possibly owing to food limitation (M. Pace,personal communication).

Suppression of small zooplankton mayreduce food availability to fishes that areplanktivorous at some developmental stage.Yellow perch (Perca flavescens) recruit-ment and commercial harvest declined dra-matically in western Lake Erie concomitantwith the zebra mussel invasion, though oth-er factors, notably an expanding whiteperch (Morone americand) population, maypartially account for observed changes(OMNR, 1994). Spawning success of wall-eye (Stizostedion vitreum) in western LakeErie was poor between 1987 and 1989, in-creased in 1990 and 1991, but declinedagain in 1992 (OMNR, 1994). Commercialwalleye quotas have been met in the basindespite the presence of Dreissena (OMNR,1994). A factor of greater concern with re-spect to walleye is alteration of habitat as-sociated with increased light transmittance.Rod-hour sport landings and net-based fish-eries assessment catches declined by ~50%in Lake St. Clair subsequent to establish-ment of Dreissena (OMNR, 1995). In ad-dition, adult walleye are now found pri-marily in the shipping channel, the deepestand most turbid portion of the lake (D.MacLennan, personal communication).

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Changes in fish abundance do not appearrelated to recruitment as both spawning andhatching success were good in the ThamesRiver, a major contributor to fish popula-tions in the lake (OMNR, 1995). It is quitelikely that young walleye were consumedby smallmouth bass (Micropterus dolo-mieu), largemouth bass (M. salmoides),northern pike (Esox lucius), and muskel-lunge (E. masquinongy), all of which haveincreased in abundance in recent years(OMNR, 1995).

In contrast to hypothesized, adverse in-direct effects on walleye, zebra musselsrepresent an abundant food source for manyfish species (Fig. 1). French (1993) reportedthat fishes with upper and lower pharyngealteeth or lower pharyngeal teeth and chew-ing pads were likely consumers of zebramussels in North America. Fishes known orexpected to exploit Dreissena include fresh-water drum (Aplodinotus grunniens), redearsunfish (Lepomis microlophus), pumpkin-seed (L. gibbosus), copper (Moxostomahubbsi) and river (M. carinatum) redhorseand common carp {Cyprinus carpio)(French, 1993). Zebra mussels have beenreported in digestive tracts of other fishesin the Great Lakes including yellow perch,white perch, walleye, white bass (Moronechrysops), lake whitefish {Coregonus clu-peaformis), lake sturgeon (Acipenserfulves-cens) and the round goby (Neogobius me-lanostomus) (French, 1993).

Positive feedback may exist between pro-duction of macrophytes and Dreissena inshallow, light-limited systems (Figs. 1, 2).Mussel production may promote enhancedwater clarity, which in turn facilitates in-creased macrophyte production and in-creased settling substrate for Dreissena. Eu-ropean workers described high settlementrates of competent Dreissena on macro-phytes (Table 1; Lewandowski, 1982).

The increase in abundance of northernpike, muskellunge and bass in Lake St.Clair may relate to increased production ofmacrophytes in conjunction with enhancedwater clarity and increased euphotic depth.The euphotic zone in Lake St. Clair has ex-panded to encompass most of the benthicsurface area. Large regions of the lake nowsupport macrophyte growth (Griffiths,

1993). During spring and summer 1994,enormous volumes of decaying Elodea can-adensis and, to a lesser extent, Myriophyl-lum spicatum, Vallisneria americana, Najasflexilis and Potamogeton spp., washedashore on both Canadian and Americanshorelines causing severe water qualityproblems and beach fouling. MetropolitanBeach, southwest of the Clinton River, MI,was closed owing to high bacterial countsand macrophyte stranding. Front-end load-ers were employed to remove macrophytesfouling the beach. Stranding resulted fromunusual wind patterns that trapped macro-phytes along shorelines rather than flushingthe material into the Detroit River. Never-theless, the current nutrient status of LakeSt. Clair coupled with enhanced solar ra-diation penetration indicates that prolificgrowth of macrophytes may become thenorm. Production of shade-sensitive watercelery {Vallisneria) also increased in LongPoint Bay in eastern Lake Erie concomitantwith establishment of Dreissena (R. Knap-ton, personal communication).

Dreissena invasion and the attendantshift in energy from planktonic to benthicfoodwebs may profoundly affect benthic in-vertebrate communities (Fig. 1). Unionidmolluscs are among the taxa most affected,and may be extirpated from systems sup-porting large Dreissena populations (seeSchloesser et al., this volume). By contrast,many other invertebrates may benefit fromstructure associated with Dreissena colo-nies or from enhanced food supply. Stewartand Haynes (1994) assessed macroinverte-brate communities in southwestern LakeOntario before (1983) and after (1991-1992) invasion of D. polymorpha and D.bugensis. Dreissena dominated invertebratecommunities numerically (79-93%) in1991 and 1992, though all taxa increased inabundance following Dreissena establish-ment. Total non-Dreissena invertebrateabundance increased between 1,316 and4,595 ind.m 2 following establishment ofDreissena. Taxa showing the greatest in-creases included annelids (Manayunkia spe-ciosa, Spirosperma ferox and unidentifiedtubificids), gastropods (Helisoma anceps,Physa heterostropha, Stagnicola catasco-pium, Valvata tricarinata, Goniobasis liv-

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escens and Amnicola limosa), amphipods{Gammarus fasciatus), and crayfish (Orco-nectes propinquus) (Stewart and Haynes,1994). These patterns strongly parallel re-sults for eastern Lake Erie (Dermott et al.,1993) and Lake St. Clair (Griffiths, 1993).Increased abundances of amphipods, leech-es, triclads, snails, mayflies, caddis flies andtrue flies were attributed to enhanced hab-itat structure, whereas annelid worms andcrayfish may have increased owing to en-hanced food supply (Dermott et al., 1993;Griffiths, 1993; Stewart and Haynes, 1994;Maclsaac, 1994; Martin and Corkum,1994). Griffiths (1993) argued that benthicinvertebrate communities in southeasternLake St. Clair shifted toward those char-acteristic of more oligotrophic systems.

Benthic invertebrate diversity may alsobenefit from Dreissena invasion. Total in-vertebrate diversity increased from <22species to between 27 and 32 taxa at a cob-ble site, and from <15 species to between19 and 26 taxa at an artificial reef site inLake Ontario following Dreissena invasion(Stewart and Haynes, 1994). This resultshould be interpreted with caution, howev-er, because Griffiths (1993) observed in-creased macroinvertebrate diversity be-tween 1980 and 1990 at sites in Lake St.Clair both with and without Dreissena.

Diving waterfowl are important predatorsof Dreissena in Europe (Stempniewicz,1974; Stariczykowska et al., 1990; Bij deVaate, 1991; Cleven and Frenzel, 1993) andNorth America (Wormington and Leach,1992; Hamilton et al., 1994; Mazak, 1995).Wormington and Leach (1992) reportedgreater waterfowl flock size and staging du-ration in the Point Pelee, Ontario area sub-sequent to development of Dreissena pop-ulations in Lake Erie. Numerical responseswere greatest for greater scaup (Aythyamarila), lesser scaup (A a/finis) and com-mon goldeneye (Bucephala clangula). Eachof these species, as well as bufflehead (B.albeola), feed extensively on zebra musselsin western Lake Erie (Wormington andLeach, 1992; Hamilton et al., 1994; Mazak,1995). Ducks consumed 57% of autumnmussel biomass in western Lake Erie, buthad little impact on mussel biomass the fol-lowing spring because of growth of small

individuals (Hamilton et al., 1994). Duckslikewise consumed 90% of standing bio-mass in River Seerhein (Lake Constance)during winter months, but had little impacton the population owing to recruitment andimmigration of new individuals (Clevenand Frenzel, 1993). Regulation of Dreis-sena biomass and abundance by waterfowlis unlikely in central North America be-cause predation is limited to ice-off periods(Hamilton et al., 1994). Regulation of mus-sel populations is more likely at southernlocalities in the U.S.A. where waterfowlcould prey on mussels for protracted peri-ods of time.

Zebra mussels, by virtue of their abilityto biomagnify metal and organochlorinecontaminants, may serve as an effectiveconduit for transfer of contaminants to hightrophic levels {e.g., see Mersch and Pihan,1993; Bruner et al., 1994). For example,lesser and greater scaup in western LakeErie that consumed Dreissena contained el-evated concentrations of a broad spectrumof organic contaminants relative to conspe-cifics from the lower Detroit River that con-sumed mainly macrophytes (Mazak, 1995).Biomagnification of organochlorine con-taminants in ducks that consumed musselsdepended on the chemicals' octanol-waterpartition coefficient (K^,) (Fig. 3). Bio-magnification factors are higher for highlyhydrophobic chemicals (high Kow) than forless hydrophobic ones (Fig. 3). Previouswork demonstrated that tufted ducks (A. fu-ligula) fed a diet of highly contaminatedDreissena experienced a host of reproduc-tive problems ranging from smaller clutchand egg size, to higher embryo mortalityand higher incidence of nest abandonment(de Kock and Bowmer, 1993). To date,however, reproductive problems associatedwith organic contaminants have not beenidentified for Lake Erie waterfowl that uti-lize Dreissena.

Alternate ecosystem states?Scheffer et al. (1993) proposed that shal-

low lakes may have two alternative equilib-ria: a clear state dominated by macrophytes,and a turbid state supporting high algal bio-mass. The transition between clear and tur-bid states is believed to be governed by

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ooCOu.

ion

reo

"E

oma

1 2 -

8 -

4 -

o-

• Greater Scaup• Lesser Scaup

44m_^ 52 101

195

203

138

£0 5.75 5.84 6.38 6.83 7.53 7.65Log Kow

FIG. 3. Biomagnification factors ([duck]/[Dreissenaprey]) of greater and lesser scaup from western LakeErie in relation to octanol-water partition coefficients(K^) of six polychlorinated biphenyls (PCBs). IUPACcongener number is provided above each bar for eachPCB. Duck diets consisted of >95% Dreissena bymass. Data courtesy of Ed Mazak.

feedback relationships between macro-phytes and turbidity. Because the lowerdepth limit of macrophytes is positivelycorrelated with Secchi disk transparency(Scheffer et al, 1993), turbid systems havea limited ability to support benthic vegeta-tion. By stripping suspended sediments andalgae from the water column, DreissenaAn-duced increases in transparency may facil-itate the growth of macrophytes in shallowlakes. The presence of macrophytes andDreissena feces and pseudofeces providehabitat and food to many benthic inverte-brates and fishes. Thus, it is possible thatshallow systems invaded by Dreissena mayexperience dramatic shifts in energy andbiomass from pelagic to benthic foodwebs.In this regard, water quality effects exertedby Dreissena resemble, but may be strongerthan, those associated with "biomanipula-tion" programs in which piscivorous fishesare stocked to reduce algal biomass and en-hance water transparency.

SUMMARY

Invasion of inland waterways by Dreis-sena may result in dramatic physical andbiological changes, particularly in shallowor well-mixed systems. Based on Europeanand Great Lakes precedents, users of rawwater from invaded systems may incur sig-nificant biofouling mitigation expenses.Mussel filtering activities often result in re-

duced concentrations of suspended solidsand phytoplankton, with attendant increasesin light transmittance and macrophyte pro-duction. Zooplankton may be suppressedowing to food limitation or, for small taxa,direct ingestion by Dreissena. Habitatstructure associated with, and waste prod-ucts generated by, colonies of Dreissenaenhance production of many benthic inver-tebrates. Invertebrate {e.g., crayfish) andvertebrate (fishes, waterfowl) predators mayexperience numerical responses in habitatssupporting high Dreissena densities. Pred-ators of contaminated Dreissena biomag-nify organochlorine compounds, thereby al-tering contaminant cycling.

ACKNOWLEDGMENTS

I thank the symposium organizers Drs. J.Ram and R. McMahon for the opportunityto participate in the conference. J. Fraserand P. McQuarrie of the Windsor UtilitiesCommission furnished Detroit River turbid-ity data. E. Mazak provided contaminantdata for Lake Erie waterfowl. This manu-script benefited from discussions with J.Leach, T. Dietz, H. Silverman, R. Griffiths,E. Mills, M. Pace, N. Caraco, R. Knapton,E. Mazak, D. MacLennan, T. Nalepa, J. Fra-ser and P. McQuarrie, and the comments ofanonymous reviewers. My Dreissena re-search has been generously supported bygrants from NSERC, Ontario Ministries ofNatural Resources and Environment andEnergy, Great Lakes University ResearchFund, Canadian Wildlife Service, Depart-ment of Fisheries and Oceans, and the Uni-versity of Windsor Research Board.

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Documents

Potential Abioti anc d Biotic Impact os f Zebra Mussel os ...freshwater communities based on European and North American studies. Taxa benefiting from Dreissena in-vasion are indicated