Interactions among Zebra Mussel Shells, Invertebrate Prey, and Eurasian Ruffe or Yellow Perch
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1 J. Gret Lkes Res. 28(4): Internt. Assoc. Gret Lkes Res., 2002 Interctions mong Zebr Mussel Shells, Invertebrte Prey, nd Eursin Ruffe or Yellow Perch Cynthi S. Kolr*, Aimee H. Fullerton', Kristine M. University of Notre Dme Deprtment of Biologicl Sciences P. O. Box 369 Notre Dme, Indin nd Gry A. Lmberti ABSTRACT. The exotic zebr mussel, Dreissen polymorph, is estblished in ll of the Lurentin Gret Lkes nd my ffect benthivorous fishes by incresing the complexity of benthic substrtes nd chnging energy flow ptterns within the food web. Ntive yellow perch, Perc flvescens, nd the nonindigenous Eursin ruffe, Gymnocephlus cernuus, re benthivores tht my compete for limited food resources. As ruffe spred to res with more dense zebr mussel popultions, the zone of interction mong zebr mussels, yellow perch, nd ruffe will increse nd intensify. In the lbortory, the effect of zebr mussel shells on the bility of these fishes to forge on mphipods (Gmmrus pseudolimneus) nd chironomids (Chironomus plumosus) ws exmined in light nd drkness. In 12 h, ruffe consumed more mphipods thn did similr-sized yellow perch, prticulrly in drkness on bre cobble, nd in light within zebr mussels. Amphipods decresed ctivity more in the presence of ruffe thn yellow perch. More mphipods were found in zebr mussel shells thn in bre cobble, whether or not fish were present. In drkness, when ruffe consumed more mphipods on bre cobble, mphipods becme more ssocited with zebr mussel shells. Although ruffe consumed more mphipods thn yellow perch, perch consumed more chironomids thn ruffe on bre cobble. The presence of zebr mussel shells ltered the reltive consumption of invertebrtes in some substrte-light combintions. Experiments such s these help to improve understnding of the direct nd indirect effects of predtion between nd mong ntive nd nonindigenous species tht my exert structuring forces on the nershore communities of the Gret Lkes currently or in the future. INDEX WORDS: Benthic mcroinvertebrtes, Eursin ruffe, Gmmrus, Gret Lkes, hbitt complexity, predtion, yellow perch, zebr mussels. INTRODUCTION Ecosystem engineers like zebr mussels (Dreissen polymorph) tht lter the quntity nd qulity of hbitt nd food resources vilble to other species my influence the impct of newly-estblishing exotic species in the Gret Lkes. Zebr mussels hve colonized much of the hrd substrte in the Gret Lkes (nd even some soft substrtes, Jrvis et l. 2000) nd hve lso spred to mny rivers nd inlnd lkes. Where bundnt, they hve drmticlly ltered trophic interctions nd eco- *Corresponding uthor. Present ddress: UMESC-USGS, 2630 Fnt Reed Rod, Lcrosse, WI E-mil: ckolr@usgs.gov Present Address: Ntionl Mrine Fisheries Service-EC Division, 2725 Montlke Blvd., E., Settle, WA Present Address: 962 Merrimc Circle, Nperville, IL logicl function (Nlep nd Fhnenstiel 1995). Zebr mussels hve incresed wter clrity by reducing phytoplnkton density (McIsc et l. 1991, Lech 1993) nd primry productivity (Fhnenstiel et l. 1995), ltered the community structure of benthic lge (Lowe nd Pillsbury 1995), incresed the bundnce nd depth of mcrophytes (Skubinn et l. 1995), nd ltered nutrient vilbility from their nutrient-rich feces nd pseudofeces (Stewrt et l. 1998). Chnges in the Gret Lkes ecosystem fcilitted by zebr mussels hve effectively concentrted energy flow into the benthic region from the pelgic region (McIsc et l. 1992). Severl studies hve shown drmtic increses in the density nd biomss of benthic mcroinvertebrtes, prticulrly nnelids, gstropods, mphipods, nd chironomids in 664
2 Eursin Ruffe, Yellow Perch, nd Zebr Mussels 665 nd round zebr mussel beds (Dermott et l. 1993, Stewrt nd Hynes 1994, Botts et l. 1996). Gmmrid mphipods, in prticulr, cn be limited by vilbility of interstitil hbitt (Adms et l. 1987), nd increses in this hbitt my explin observed increses in mphipods fter zebr mussel estblishment (Riccirdi et l. 1997, Stewrt et l. 1998, nd Downing 1999). If nutrients nd food resources re limited, concentrting energy in the benthos my benefit benthic fish t the expense of pelgic feeders. Yellow perch (Perc flvescens) support lrge commercil nd recretionl fisheries in the Gret Lkes nd re currently the focus of much reserch nd medi ttention becuse of severl consecutive yers of recruitment filure in Lke Michign (Shroyer nd McComish 2000). Zebr mussels nd yellow perch co-occur in the St. Louis River estury (Lke Superior) with Eursin ruffe (Gymnocephlus cernuus), nonindigenous benthivorous fish introduced into North Americ in the mid- 1980s (Prtt et l. 1992). Becuse ruffe re primrily riverine fishes in their ntive rnge (Ogle 1995), ruffe my spred not only to the other Gret Lkes (Fullerton et l. 1998), but lso to lrge river systems nd connected inlnd lkes. Any effect of zebr mussels on interctions between ruffe nd yellow perch will likely increse s the rnge in which these three species occur in symptry grows, prticulrly s ruffe spred to res with higher zebr mussel densities thn occur in Lke Superior. Becuse they both re primrily benthivorous by ge 1+ (Ogle et l. 1995) nd they prefer similr types of prey (Fullerton et l. 2000), competition between yellow perch nd ruffe hs been suggested, nd lbortory experiments hve confirmed competition for limited food resources is possible (Svino nd Kolr 1996, Fullerton et l. 2000). Adpttions of ruffe, such s well-developed lterl line system (Jnssen 1997), night-dpted vision (Ahlbert 1975), nd well-developed spines to deter piscine predtors (Ogle 1995) confer benefits of ruffe over yellow perch. Indeed, reltive to yellow perch, ruffe detected prey t further distnce (Jnssen 1997) nd hve become quite bundnt in wters where yellow perch were formerly bundnt in Lke Superior. Given their differentil feeding dpttions, however, competition between ruffe nd yellow perch my be ffected by the presence of zebr mussels. For instnce, cler wter ecosystems should benefit yellow perch since they re typiclly found in such hbitts (Wever et l. 1997), wheres turbid ecosystems should benefit ruffe (Bergmn 1987, Rosch nd Schmid 1996). Similrly, interstitilly complex substrtes should benefit yellow perch since they typiclly forge mong mcrophytes (Wever et l. 1997), wheres ruffe re often found over open mud hbitts (Ogle 1995). Becuse zebr mussels lter these two importnt fctors ffecting forging success (wter turbidity nd forging hbitt complexity), potentilly in fvor of yellow perch, the presence of zebr mussels might mitigte competition between these fishes, prticulrly if the fishes differ in their bility to locte nd consume mcroinvertebrtes ssocited with zebr mussel colonies. Although it is intuitive tht incresed bundnce nd biomss of benthic invertebrtes within zebr mussel beds would benefit benthivorous fishes, studies to dte hve not shown cler benefit (Jennings 1996, Thyer et l. 1997). These findings my be explined, in prt, by the physicl structure of zebr mussel shells. Mcroinvertebrtes such s mphipods my become very closely ssocited with zebr mussel shells, effectively reducing ctivity, remining less visible to predtors, nd deriving physicl refuge from predtion in zebr mussel beds (Stewrt et l. 1998). Such reduction in ctivity is common response of invertebrtes to the presence of fish predtors (Kolr nd Rhel 1993). Consequently, lthough more bundnt, mcroinvertebrtes might be less vilble to fish in the presence of zebr mussels or would be less profitble due to higher energetic costs. The effect of zebr mussels on benthivorous fishes would therefore depend, in prt, on the bility of ech fish species to locte nd consume mcroinvertebrtes within zebr mussel beds. In ddition to differentil bilities of fishes to remove invertebrtes from the interstices of zebr mussel shells, benthic invertebrtes my recognize potentil predtors differentilly. If indigenous nd nonindigenous benthic invertebrtes tht did not coevolve with ruffe cnnot recognize ruffe by visul or chemicl cues, then ruffe my derive more benefit thn indigenous benthivorous fishes from invertebrtes ssocited with zebr mussels. The overll gol of this project ws to determine if zebr mussels differentilly modified the consumption of invertebrtes by ruffe nd yellow perch. To ccomplish this gol, set of experiments ws conducted tht 1) exmined the behviorl responses of mcroinvertebrtes to the presence of ruffe nd yellow perch to determine if ctivity level helped explin consumption ptterns, 2) compred consumption of mcroin-
3 666 Kolr et l. vertebrtes (mphipods nd chironomids) by ruffe nd yellow perch on substrtes with nd without zebr mussels in light nd drk conditions, nd 3) quntified substrte use of mphipods in presence nd bsence of ruffe nd yellow perch. METHODS Generl Experimentl Methods Ruffe were collected from the St. Louis River estury (Duluth, Minnesot) of Lke Superior, nd yellow perch tht were rised in ponds nd hd consumed nturl prey were obtined from htchery in Michign. Fish species were held seprtely for t lest 30 dys fter collection in 240-L tnks t 17 C on 12-h light:12-h drk cycle nd were fed redworms (terrestril oligochetes). Amphipod nd chironomid species tht were redily vilble were used in experiments. Gmmrus pseudolimneus were collected from northern Indin river, nd were held in the lbortory t 17 C in erted buckets with lef debris. Typiclly considered lotic, G. pseudolimneus is found throughout the Gret Lkes region including in the Gret Lkes proper (Holsinger 1976). Individuls 8 to 12 mm were used- mngeble size for fish nd rnge encompssing sizes of G. fscitus, common in the Gret Lkes (up to 14 mm; Pennk 1978), nd Echinogmmrus ischnus, nonindigenous gmmrid found in Lkes Erie (Witt et l. 1997), Michign (Nlep et l. 2001), nd Ontrio (Dermott et l. 1998). A species with holrctic distribution, Chironomus plumosus is common throughout the Gret Lkes bsin (Cook nd Johnson 1974), nd is found in zebr mussel beds in Lke Michign (M. Berg, personl communiction). Live C. plumosus were purchsed commercilly nd were held t 8 C. Artificil cobble substrtes were creted for use in ll experiments by molding concrete into uniform hemisphericl shpes (10 cm dim). Cobbles were soked in wter for 1 week to lech out residul compounds. On hlf of them, zebr mussel shells were ttched over the entire surfce using silicone selnt. To prepre mussel shells, live zebr mussels were collected from southern Michign lke, dried, nd mussel tissue ws removed before filling shell vlves with silicone selnt. The seled shells were sorted into size ctegories: smll (10 to 15 mm shell length), medium (15 to 20 mm), nd lrge (25 to 30 mm) nd were ttched to the cobble with silicone t high (140 zebr mussels/cobble = 40 lrge, 70 medium, nd 30 smll) or low density (80 zebr mussels/cobble = 20 lrge, 40 medium, 20 smll). When three lowdensity nd three high-density cobble were plced in 40-L qurium, density of 4,400 zebr mussels/m2 ws simulted ( density found in the field, Nlep nd Fhnenstiel 1995). After ttching zebr mussels, cobbles were soked for 24 h to lech out residul compounds. To provide dditionl substrte for invertebrtes, wter-soked vermiculite (3 to 5 mm) ws dded to quri, which were then filled with well wter. Six cobble (either 6 cobbles without zebr mussels or three low density nd three high density zebr mussel cobbles) were plced on the settled vermiculite. After 24 h (to llow for wter clering nd for temperture to stbilize t 19 to 20 chironomids were dded, followed t 1-h increments by 50 mphipods nd then one fish (either yellow perch or ruffe). Ruffe ( g, mm TL; men 1 SE) nd yellow perch ( g, 82 1 mm TL) were similr in mss. At the end of n experiment, remining invertebrtes were retrieved by rinsing cobble nd vermiculite over 0.25 mm sieve. Experiments were run seprtely in the light nd drk. Seprte experiments were conducted to ssess mphipod ctivity, consumption of invertebrtes, nd zebr mussel shell use by invertebrtes. Amphipod Activity Substrte type (cobble with or without zebr mussels), predtion pressure (no fish, yellow perch, or ruffe), or light level (light or drk) were simultneously tested to determine if they influenced the swimming ctivity of mphipods (n = 3 replictes per tretment combintion). Becuse mphipod behvior ws the focus of the study, only the thret of fish predtion ws needed. Thus, observtions of mphipod movement begn immeditely fter dding the fish, before the fish ws cclimted to experimentl conditions. Anlogous experiments exmining behvior of prey with uncged predtors in the lbortory re found in the literture (Rhel nd Kolr 1990, Kolr nd Rhel 1993, McKenzie nd Greenberg 1998). In ddition, dding predtors or prey to formerly predtor-less or prey-less experimentl ren is typicl method of conducting such behviorl experiments (Wre 1972, Whl nd Stein 1988, Kolr nd Rhel 1993, Einflt nd Whl 1997). Amphipod ctivity in 1-h period ws quntified by visully scnning ech qurium every 2 min nd counting the mphipods observed moving or swimming. In drk tretments, blck light ws shone briefly bove ech qurium to quntify movement.
4 Eursin Ruffe, Yellow Perch, nd Zebr Mussels 667 Similr observtions were not possible for chironomids becuse they were well-hidden in the substrte. A 3-fctor ANOVA ws used to ssess if the proportion of mphipods moving (corrected through the observtionl period using the number of mphipods recovered nd observed predtion events) vried with substrte, light level, nd predtion pressure. Proportionl dt were rcsine squre-root trnsformed before conducting ANOVA. All sttisticl nlyses were conducted using SAS (SAS Institute 1991) fter testing for normlity, independence, equl vrince, nd linerity using the Guided Dt Anlysis option in SAS. Consumption of Invertebrtes To ssess whether consumption of chironomids nd mphipods vried with substrte type (cobble with or without zebr mussel), predtion pressure (no fish, yellow perch, or ruffe), or light level (light or drk), invertebrtes nd fish were sequentilly dded t 1-h intervls s previously described (n = 3 ech tretment combintion). After 12 h (llowing for cclimtion nd feeding), mcroinvertebrtes were recovered nd counted to determine mortlity rtes. Midwy through the experiment, mphipods were observed consuming chironomids, which ws confirmed by gut nlysis. Becuse mphipod predtion of chironomids could not be distinguished from fish predtion, nd becuse it my hve differed mong fish tretments, the number of unrecovered chironomids ws compred between tretments (without normlizing for fish mss). To determine whether chironomid consumption (combined predtion by fish nd mphipods) differed mong tretments, 3-fctor ANOVA (light, substrte, nd fish species) ws used followed by contrsts for specific tretments. It ws ssumed tht ll unrecovered chironomids from the control tretments were consumed by mphipods (bsed on complete recovery of chironomids in trils lcking mphipods fter 12 h). The 3-fctor ANOVA model bove ws used to ssess if substrte or light ffected mphipod consumption of chironomids in fishless tretments. To ssess fish consumption of mphipods, the men number of mphipods missing from fishless controls of the sme tretment combintion of light level nd substrte type ws subtrcted from the number of mphipods recovered from ech replicte. Anlysis of fish predtion on mphipods (number of mphipods consumed/g fish wet mss) ws otherwise the sme s for chironomid dt. Dt were first log lo-trnsformed to meet the ANOVA ssumption of linerity. Zebr Mussel Shell Use by Invertebrtes To ssess substrte choice by invertebrtes, vermiculite ws first dded to ech qurium, then three bre cobbles were dded to one side, nd then two high-density cobbles nd one low-density cobble with zebr mussels were dded to the other side (density of in zebr mussel portion). Chironomids, mphipods, nd fish (no fish, yellow perch, or ruffe) were dded s in prior experiments. After 1 h, quri were divided with tight-fitting Plexigls divider to seprte invertebrtes in bre cobbles from those in cobbles with zebr mussels. Ech side ws then siphoned seprtely, nd invertebrtes within ech substrte were retrieved (cobbles were rinsed s in previous experiments) nd counted (n = 5). Two-fctor ANOVAs using light level (drk or light) nd species (control, perch, or ruffe) s min effects were conducted to determine whether invertebrtes ltered their substrte type use in the presence of fish. Contrsts were used to compre specific tretments. RESULTS Amphipod Activity Prior to dding fish, mny mphipods were observed swimming or lingering on the substrte or qurium wlls. As fish were dded, these mphipods frequently scurried for cover ( behvior not induced by inserting n empty fish net into quri). After this quick djustment, mphipod ctivity remined reduced by 10 to 95% compred to tretments without fish (Fig. 1). Since fish were not cclimted to tnk conditions, they showed little interest in prey; totl of four gmmrids were observed being consumed cross ll 36 trils. Little predtion occurred, s confirmed by similr numbers of invertebrtes recovered with ( gmmrids nd chironomids) nd without fish (49.6? 0.2 gmmrids nd chironomids) (ANOVA 34 = 0.85, P = 0.36, nd = 0.26, P = 0.61, respectively). After dding fish, mphipods were seldom seen in the zebr mussel tretments, wheres they were often observed clinging to cobbles or burrowing into the vermiculite in the bre cobble tretments. Overll, mphipod ctivity ws lower in zebr mussels thn in bre cobble (Fig. 1; 3-fctor,
5 Kolr et l. W Drk Drk I > T T I I n + 6 I Species Substrte P = P = Light Light E E Bre cobble Zebr mussels FIG. 1. Swimming ctivity of mphipods in the bsence of fish, with ruffe, or yellow perch (n = 3) t different light levels (drk or light) nd on different substrte (bre cobble or cobble with zebr mussels). Significnt P-vlues from 3-fctor ANOVA re indicted. C = fishless control; P = yellow perch; R = ruffe. ANOVA, = 11.7, P = 0.002), s well s lower with ruffe thn. with yellow perch (Fig. 1; 3-fctor ANOVA; = 33.4, P < 0.001). Becuse mphipods were more ctive in the fishless tretments in zebr mussels, but were less ctive with fish in zebr mussels, there ws significnt interction between species nd substrte (3-fctor ANOVA, = 7.27, P = 0.003). Light did not ffect mphipod ctivity (3-fctor ANOVA; = 0.01, P = 0.94). Consumption of Invertebrtes Bsed on min effects in the 3-fctor ANOVA, neither fish species, nor substrte type, nor light R Bre cobble R Zebr mussels FIG. 2. Number of chironomids consumed by mphipods nd fishes in the light nd drk on substrte of either bre cobble or cobble with zebr mussels over 12 h (n = 11). Significnt differences detected within ech br grouping (light nd substrte combintion) re indicted with different letters. C = control; P = yellow perch; R = ruffe. level ffected the number of chironomids recovered from trils. However, there were significnt interction effects between light level nd species = 4.58, P = 0.01) nd between substrte type nd species = 3.62, P = 0.03). Contrsts reveled tht fish predtion effect ws detectble in the light. On bre cobble, perch predtion ws detectble (P < 0.01) nd ws higher thn tht of ruffe (P = 0.03). On zebr mussel shells (Fig. 2), pred-
6 Eursin Ruffe, Yellow Perch, nd Zebr Mussels W + T Drk sumption of mphipods. No interctions were significnt. Contrsts reveled tht in the drk on cobble, ruffe consumed more mphipods thn did yellow perch (Fig. 3; P = 0.02). Also, in light on zebr mussels, ruffe consumed more mphipods thn did yellow perch (P = 0.04). Zebr Mussel Shell Use by Invertebrtes Overll, the recovery rte of chironomids ws reltively low (15 to 75%), probbly due to predtion exerted primrily by mphipods. Chironomids hd no substrte preference = P = 1.00) in the bsence of fish (Fig. 4). When fish were T Light T Chironomids + Bre cobble Zebr mussels FIG. 3. Mss-specific consumption of mphipods by fish in the light nd drk on substrte of either bre cobble or cobble with zebr mussels over 12 h (n = 11). Significnt differences detected within ech br grouping (light nd substrte combintion) re indicted with different letters. P =yellow perch; R = ruffe. t N E b Amphipods I T by both perch (P = 0.03) nd ruffe (P 0.01) ws detectble nd similr (P = 0.23). Contrsts between fishless tretments lso showed tht mphipods consumed similr numbers of chironomids regrdless of substrte type (Fig. 2; cobble, P = 0.13; zebr mussels, P = 0.13) nd light level (Fig. 2; light, P = 0.57; drk, P = 0.59). Overll, ruffe consumed more mphipods thn did yellow perch (Fig. 3; = 8.07, P 0.01). Neither light level = 0.04, P = 0.84) nor substrte lone = 0.08, P = 0.78) ffected con- R Drk R Light FIG 4. Proportion of chironomids nd mphipods found in cobble with zebr mussels in ech tretment (C = control; P = yellow perch; R = ruffe) fter 1 h ccess to both bre cobble nd cobble with zebr mussel shells (n = 5). Asterisk indictes significntly more use of zebr mussel cobbles thn bre cobble in the presence of fish.
7 670 Kolr et l. sent, chironomids did not significntly lter their substrte use. Use of cobble with or without zebr mussels did not differ with species 24 = 0.11, P = 0.89) nor light level = 0.12, P = 0.73). More mphipods were found in zebr mussels thn in bre cobble both without fish (2-fctor ANOVA; = 9.19, P = 0.008) nd in their presence (3-fctor ANOVA; = 81.43; P < 0.001). Although the proportions of gmmrids in zebr mussels were similr between fish species (2 fctor ANOVA; = 1.10, P = 0.35) nd light level (2 fctor ANOVA; = 2.44, P = 0.13), there ws significnt interction between these two min effects. While the proportion of gmmrids found within zebr mussels without fish nd with yellow perch ws higher in light thn drk, the reverse ws true when ruffe were present (2 fctor ANOVA; = 4.13, P = 0.03). Contrsts showed tht in the drk, mphipods preferred zebr mussels to bre cobble with ruffe thn without fish (P = 0.06). No other contrsts differed between tretments (ll P > 0.13). Recovery of mphipods ws high (92 to 100% in ll replictes) nd no predtion ctivity ws observed. DISCUSSION It ws expected tht the incresed hbitt complexity provided by zebr mussel shells would reduce successful forging of both fishes. Mny studies hve shown tht predtion efficiency of fish declines in hbitts tht re structurlly complex (Svino nd Stein 1982, et l. 1989; but see nd Downing 1999 who found similr consumption rtes of yellow perch in cobble with live zebr mussels nd in bre cobble). In similr study, Myer et l. (2001) found tht in light, yellow perch consumed fewer mphipods in zebr mussels thn they did on bre sediments-lthough they ttribute differences in forging rtes more to light level thn on the structurl complexity provided by zebr mussels. Furthermore, it ws expected tht zebr mussel shells to more negtively ffect the forging rte of ruffe, which feed primrily over mud (Ogle 1995), thn yellow perch, which feed over vriety of substrtes (Dnehy nd Ringler 1991). Contrry to the predictions, the presence of zebr mussel shells did not consistently ffect consumption rtes. Overll, ruffe consumed more mphipods thn did yellow perch, but this response ws not universl. Rther, the presence of zebr mussel shells ffected predtion more subtly by ltering the reltive consumption of invertebrtes in some substrte-light combintions. In drkness, ruffe nd yellow perch consumed similr numbers of prey mong zebr mussel shells, but ruffe consumed more in bre cobble. These findings re consistent with the originl hypothesis tht ruffe would hve higher consumption rtes on simpler substrte. In ddition, ruffe hve drkdpted vision (Ahlbert 1975), sensitive lterl line system (Gry nd Best 1989), nd nocturnl feeding hbits (Jmet nd Lir 1991, Ogle et l. 1995). These dpttions my ccount for higher consumption rtes on bre cobble in drkness. In the light, however, ruffe nd yellow perch consumed similrly in bre cobble (kin to Svino nd Kolr 1996 where ruffe nd yellow perch consumed similr numbers of chironomids in simple substrte), but ruffe consumed more in zebr mussels. These findings re contrry to the hypothesis tht yellow perch would consume more prey on complex substrte. Where they re ntive, ruffe cooccur with zebr mussels, nd perhps they re dpted to forging in zebr mussels beds occsionlly (lthough these prticulr ruffe hd no previous contct with zebr mussels). Invertebrte prey often reduce ctivity in response to predtor presence (Kolr nd Rhel 1993). It is possible tht mphipods were less ctive in zebr mussels thn in bre cobble becuse of the interstitil hbitt the shells provided. It is interesting tht mphipods responded more strongly to ruffe thn to yellow perch even though G. pseudolimneus nd ruffe were not symptric. Willims nd Moore (1985) reported reduced ctivity by G. pseudolimneus fter the ddition of fish, regrdless of whether or not the fish typiclly consumed them. They suggested tht G. pseudolimresponded behviorlly to bsic fish secretion or exudte. The results support this hypothesis. Tretments in which mphipods reduced their ctivity more with ruffe thn with yellow perch (bre cobble in light nd zebr mussels in drkness) were the sme tretments in which ruffe consumed more mphipods thn yellow perch. Thus, even though mphipods cted to minimize their risk of predtion where they perceived higher predtion thret, they were still consumed more thn when perceived predtion risk ws lower. It is difficult to interpret consumption of chironomids by ruffe nd yellow perch in these experiments becuse of the unexpected predtion on chironomids by mphipods. Amphipods typiclly et periphyton nd re considered omnivorous scv-
8 Eursin Ruffe, Yellow Perch, nd Zebr Mussels 671 engers tht rrely ttck nd et live mcroscopic prey (Pennk 1978). Adults of some species cn become opportunistic predtors if sufficient prey re present (Thorp nd Covich 1991). In these experiments, mphipod predtion on chironomids ccounted for much of the chironomid consumption, since fish predtion ws not detectble in drkness. In light on bre cobble, yellow perch consumed more chironomids thn ruffe-the only time when yellow perch hd higher consumption rtes thn ruffe in these experiments. In their ntive rnge, ruffe re competitively superior to Europen perch (P fluvitilis) in consuming benthic orgnisms. When they co-occurred with high densities of ruffe, Europen perch incresed their consumption of zooplnkton (Bergmn nd Greenberg 1994). Bergmn (1990) suggested tht Europen perch were competitively sndwiched between competitively superior plnktivore (roch, Rutilus rutilus) nd benthivore (ruffe). Like Europen perch, yellow perch incresed their consumption of zooplnkton in the presence of competitively superior benthivore (pumpkinseed sunfish, Lepomis gibbosus; Hnson nd Leggett 1985). If ruffe continue to spred in North Americ nd they re ble to outcompete yellow perch for benthic orgnisms, yellow perch my become similrly sndwiched between the nonindigenous white perch (Morone mericn) nd ruffe in the lower Gret Lkes nd invded river systems. White perch lredy inhbit the lower Gret Lkes nd some inflowing rivers, hve higher consumption rtes thn yellow perch (Prrish nd Mrgrf 1990), nd et primrily zooplnkton in Lke Erie (Prrish nd Mrgrf 1990). Thus, s ruffe spred to other Gret Lkes, prticulrly to Lke Erie nd southern Lke Michign where both yellow perch nd white perch re more bundnt thn in Lke Superior, yellow perch my become competitively squeezed between better plnktivorous (white perch) nd benthivorous (ruffe) specilists. The presence of zebr mussels in the lower Gret Lkes my help to mitigte the impcts of ruffe on yellow perch or other fish species s they expnd their rnge. Ruffe re dpted to low light conditions nd re found in turbid wter where light penetrtion is low (Bergmn 1987, Rosch nd Schmid 1996). Since their estblishment, zebr mussels hve incresed wter trnsprency, nd decresed phytoplnkton bundnce nd productivity (McIsc et l. 1991, Lech 1993), llowing n increse in the bundnce nd depth occupied by mcrophytes (Skubinn et l. 1995). Combined, these effects hve ltered the Gret Lkes ecosystem where zebr mussels re bundnt to more closely resemble the preferred hbitt of yellow perch thn tht of ruffe. Currently, it is unknown whether ruffe will be ble to invde the rivers nd inlnd lkes of North Americ. Becuse they hve brod environmentl tolernces (Ogle 1995) nd re bundnt in mny lrge river systems in Eursi (Ogle 1995) with similr physio-chemicl conditions, ruffe my eventully inhbit mny rivers nd inlnd lkes in North Americ. As they become estblished in new res, ruffe will interct with ntive nd exotic species. As evidenced by the prior interctions mong se lmprey, lewife, nd rinbow smelt in the Gret Lkes, exotic species cn be powerful forces structuring qutic communities, nd such interctions will likely ply significnt role in the future. ACKNOWLEDGMENTS We thnk Dvid M. Lodge for dvice on experimentl design nd for reviewing n erlier drft of this mnuscript. We lso thnk Jci Svino nd two nonymous reviewers improving this mnuscript. Mry Blcer nd the crew of the reserch vessel from the University of Wisconsin-Superior collected ruffe, nd Alex Jurgensen ided in the lbortory. Ky Stewrt nd others of the Freimnn Life Science Center provided technicl ssistnce. This project ws funded by grnt numbers NA46RG nd NA86RG0048 dministered through the Illinois-Indin Se Grnt College Progrm. Additionl support ws provided by grdute reserch trineeship to AHF from the Ntionl Science Foundtion under Grnt No , nd from Clre Boothe Luce Memoril Fellowship to CSK. REFERENCES Adms, J., Gee, J., Greenwood, P., McKelvey, S. nd Perry, R Fctors ffecting the microdistribution of Gmmrus pulex (Amphipod): n experimentl study. Freshwt. Biol. 17: Ahlbert, I.B Orgniztion of the cone cells in the retine of some teleosts in reltion to their feeding hbits. Deprtment of Zoology, University of Stockholm, Sweden. Bergmn, E Temperture-dependent differences in forging bility of two percids, Perc fluvitilis nd Gymnocephlus cernuus. Environ. Biol. Fish. 19: Effects of roch Rutilus rutilus on two percids, Perc fluvitilis nd Gymnocephlus cernu:
9 672 Kolr et l. importnce of species interction for diet shifts. Oikos 57 : nd Greenberg, L.A Competition between plnktivore, benthivore, nd species with ontogenetic diet shifts. Ecology 75: Botts, P.S., Ptterson, B.A., nd Schloesser, D.W Zebr mussel effects on benthic invertebrtes: physicl or biotic? J. North Amer. Benthol. SOC. 15: Cook, D.G., nd Johnson, M.G Benthic mcroinvertebrtes of the St. Lwrence Gret Lkes. J. Fish. Res. Bord Cn. 31: Dnehy, R.J., nd Ringler, N.H Influence of nershore structure on growth nd diets of yellow perch (Perc flvescens) nd white perch (Morone mericn) in Mexico By, Lke Ontrio. J. Gret Lkes Res. 17: Dermott, R., Mitchell, J., Murry, I., nd Fer, E Biomss nd production of zebr mussels (Dreissen polymorph) in shllow wters of northestern Lke Erie. In Zebr mussels: biology, impcts, nd control, eds. T. Nlep nd D. Schloesser, pp Ann Arbor, MI: Lewis Publishers. Witt, J., Um, Y.M., nd Gonzlez, M Distribution of the ponto-cspin mphipod Echinogmmrus ischnus in the Gret Lkes nd replcement of ntive Gmmrus fscitus. J. Gret Lkes Res. 24: Einflt, L.M., nd Whl, D.H Prey selection by juvenile wlleye s influenced by prey morphology nd behvior. Cn. J. Fish. Aqut. Sci. 54: Fhnenstiel, G.L., Bridgemn, T.B., Lng, G.A., McCormick, M.J., nd Nlep, T.F Phytoplnkton productivity in Sginw By, Lke Huron: effects of zebr mussel (Dreissen polymorph) coloniztion. J. Gret Lkes Res. 21: Fullerton, A.H., Lmberti, G.A., Lodge, D.M., nd Berg, M.B Prey preferences of Eursin ruffe nd yellow perch: comprisons of lbortory results with composition of Gret Lkes benthos. J. Gret Lkes Res. 24: Fullerton, A.H., Lmberti, G.A., Lodge, D.M., nd Goetz, F.W Potentil for resource competition between Eursin ruffe nd yellow perch: growth nd RNA responses in lbortory experiments. Trns. Amer. Fish. SOC. 129: Gonzhlez, M.J., nd Downing, A Mechnisms underlying mphipod responses to zebr mussel (Dreissen polymorph) invsion nd implictions for fish-mphipod interctions. Cn. J. Fish. Aqut. Sci. 56: Gry, J.A.B. nd Best, A.C.G Ptterns of excittion of the lterl line of the ruffe. J. Mr. Biol. Assoc. 69: Hnson, J.M., nd Leggett, W.C Experimentl nd field evidence for inter- nd intrspecific compe- tition in two freshwter fishes. Cn. J. Fish. Aqut. Sci. 42: Holsinger, J.R The freshwter mphipod crustcens (gmmride) of North Americ. Wter Pollution Control Res. Series ELD041 (second printing) USEPA. Cincinnti, OH. Jmet, J.L., nd Lir, N An exmple of diel feeding cycle of two percids, perch (Perc fluvitilis) nd ruffe (Gymnocephlus cernuus) in eutrophic Lke Aydt (Frnce). Ann. Sci. Nt. Zool. Biol. Anim. (Pris) 12: Jnssen, J Comprison of response distnce to prey vi the lterl line in the ruffe nd yellow perch. J. Fish Biol. 51: Jrvis, P., Dow, J., Dermott, R., nd Bonnell, R Zebr (Dreissen polymorph) nd qugg mussel (Dreissen bugensis) distribution nd density in Lke Erie, Cn. Tech. Rept. Fish. Aqut. Sci. 2304: i-v; Jennings, C.A Effects of zebr mussel (Dreissen polymorph) density on the survivl nd growth of juvenile fthed minnows (Pimephles promels): implictions for North Americn river fishes. Hydrobiologi 324: Kolr, C.S., nd Rhel, F.J Interction of biotic fctor (predtor presence) nd n biotic fctor (low oxygen) s n influence on benthic invertebrte communities. Oecologi 95: Lech, J.H Impcts of the zebr mussel (Dreissen polymorph) on wter qulity nd fish spwning reefs in western Lke Erie. In Zebr mussels: biology, impcts, nd control, eds. T. Nlep nd D. Schloesser, pp Ann Arbor, MI: Lewis Publishers. Lowe, R.L., nd Pillsbury, R.W Shifts in benthic lgl community structure nd function following the ppernce of zebr mussels (Dreissen polymorph) in Sginw By, Lke Huron. J. Gret Lkes Res. 21 : McIsc, H.J., Sprules, W.J., nd Lech, J.H Ingestion of smll-bodied zooplnkton by zebr mussels (Dreissen polymorph): cn cnniblism on lrve influence popultion dynmics? Cn. J. Fish. Aqut. Sci. 48: Sprules, W.G., Johnnsson, O.E., nd Lech, J.H Filtering impcts of lrvl nd sessile zebr mussels (Dreissen polymorph) in Western Lke Erie. Oecologi 92: McKenzie, A.R. nd Greenberg, L The influence of instrem cover nd predtion risk on mcrohbitt selection of stone loch Brbtul brbtul (L.). Ecol. Freshw. Fish. 7: Myer, C.M., Rudstrm, L.G., Mills, E.L., Crdiff, S.G., nd Bloom, C.A Zebr mussels (Dreissen polymorph), hbitt ltertion, nd yellow perch (Perc flvescens) forging: system- wide effects nd
10 Eursin Ruffe, Yellow Perch, nd Zebr Mussels 673 behviourl mechnisms. Cn. J. Fish. Aqut. Sci. 58 : Nlep, T.F., nd Fhnenstiel, G.T Dreissen polymorph in the Sginw By, Lke Huron ecosystem: overview nd perspective. J. Gret Lkes Res. 21: Schloesser, D.W., Pothoven, S.A., Hondrop, D.W., Fnslow, D.L., Tuchmn, M.L., nd Fleischer, G.W First finding of the mphipod Echinogmmrus ischnus nd the mussel Dreissen bugensis in Lke Michign. J. Gret Lkes Res. 27: Ogle, D.H Ruffe (Gymnocephlus cernuus): review of published literture. Administrtive Report No. 38, Wisconsin Deprtment of Nturl Resources, Mdison, Wisconsin. Selgeby, J.H., Newmn, R.M., nd Henry, M.J Diet nd feeding periodicity of ruffe in the St. Louis River Estury, Lke Superior. Trns. Amer. Fish. Soc. 124: Prrish, D.L., nd Mrgrf, J.F Interctions between white perch (Morone mericn) nd yellow perch (Perc flvescens) in Lke Erie s determined from feeding nd growth. Cn. J. Fish. Aqut. Sci. 47: Pennk, R.W Freshwter invertebrtes of the United Sttes. Second edition. New York: John Wiley nd Sons. Prtt, D.M., Blust, W.H., nd Selgeby, J.H Ruffe, Gymnocephlus cernuus: newly introduced in North Americ. Cn. J. Fish. Aqut. Sci. 49: Rhel, F.J., nd Kolr, C.S Trde-offs in the response of myflies to low oxygen nd fish predtion. Oecologi 84: Riccirdi, A., Whoriskey, F.J., nd Rsmussen, J.B The role of the zebr mussel (Dreissen polymorph) in structuring mcroinvertebrte communities on hrd substrt. Cn. J. Fish. Aqut. Sci. 54: Rosch, R., nd Schmid, W Ruffe (Gymnocephlus cernuus L.), newly introduced into Lke Constnce: preliminry dt on popultion biology nd possible effects on whitefish (Coregonus lvretus L.). Ann. Zool. Fenn. 33: SAS Institute SAS/STAT user's guide, relese 6.04 edition. SAS Institute, Cry, North Crolin. Svino, J.F., nd Kolr, C.S Competition between nonindigenous ruffe nd ntive yellow perch in lbortory studies. Trns. Amer. Fish. SOC. 125: nd Stein, R.A Predtor-prey interction between lrgemouth bss nd bluegills s influenced by 'simulted, submersed vegettion. Trns. Amer. Fish. SOC. 111: Shroyer, S.M., nd McComish, T.S Reltionship between lewife bundnce nd yellow perch recruitment in southern Lke Michign. North Amer. J. Fish. Mnge. 20: Skubinn, J.P, Coon, T.G., nd Btterson, T.B Incresed bundnce nd depth of submersed mcrophytes in response to decresed turbidity in Sginw By, Lke Huron. J. Gret Lkes Res. 21: Stewrt, T.W., nd Hynes, J.M Benthic mcroinvertebrte communities of southwestern Lke Ontrio following invsion of Dreissen. J. Gret Lkes Res. 20: Miner, J.G., nd Lowe, R.L Quntifying mechnisms for zebr mussel effects on benthic mcroinvertebrtes: orgnic mtter production nd shell-generted hbitt. J. North Amer. Benthol. Soc. 17 : Thyer, S.A., Hs, R.C., Hunter, R.D., nd Kushler, R.H Zebr mussel (Dreissen polymorph) effects.on sediment, other zoobenthos, nd the diet nd growth of dult yellow perch (Perc flvescens) in pond enclosures. Cn. J. Fish. Aqut. Sci. 54: Thorp, J.H., nd Covich, A.P Ecology nd clssifiction of North Americn freshwter insects. Sn Diego, CA: Acdemic Press, Inc. Tonn, W.M., Pszkowski, G.A., nd Holopinen, I.J Responses of crucin crp popultions to differentil predtion pressure in mnipulted pond. Cn. J. Zool. 67: Whl, D.W., nd Stein, R.A Selective predtion by three esocids: the role of prey behvior nd morphology. Trns. Amer. Fish. SOC. 117: Wre, D.M Predtion by rinbow trout (Slmo girdneri): the influence of hunger, prey density, nd prey size. J. Fish. Res. Bord Cn. 29: Wever, M.J., Mgnuson, J.J., nd Clyton, M.K Distribution of littorl fishes in structurlly complex mcrophytes. Cn. J. Fish. Aqut. Sci. 54: Willims, D.D., nd Moore, K.A The role of semiochemicls in benthic community reltionships of the lotic mphipod Gmmrus pseudolimneus: lbortory nlysis. Oikos 44: Witt, J.D.S., Hebert, P.D.N., nd Morton, W.B Echinogmmrus ischnus: nother crustcen invder in the Lurentin Gret Lkes bsin. Cn. J. Fish. Aqut. Sci. 54: Submitted: 30 April 2001 Accepted: 11 June 2002 Editoril hndling: Thoms F. Nlep
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