Can. J. Fish. Aquat. Sci. 55: 1140–1148 (1998). © 1998 NRC Canada

1140

Competition between larval lake herring (Coregonus artedi) and lake whitefish (Coregonus clupeaformis) for zooplankton

Bruce M. Davis and Thomas N. Todd

Abstract: Diet and growth of larval lake herring (Coregonus artedi) and lake whitefish (Coregonus clupeaformis) were compared in mesocosm experiments in a small mesotrophic lake in southeastern Michigan. Fish were sampled from single-species and mixed assemblages in 2-m3 cages for 8 weeks during April and May. Both species initially ate mostly cyclopoid copepodites and small cladocerans (Bosmina spp.). Schoener’s index of diet overlap showed considerable overlap (70–90%). Lake whitefish ate Daphnia spp. and adult copepods about 2 weeks earlier than did lake herring, perhaps related to their larger mean mouth gape. Lake whitefish were consistently larger than lake herring until the eighth week, especially in the sympatric treatments. Lake whitefish appeared to have a negative effect on the growth of lake herring, as lake herring in mixed-species treatments were smaller and weighed less than lake herring reared in single-species treatments. The diet similarities of lake whitefish and lake herring larvae could make them competitors for food in the Great Lakes. The greater initial size of lake whitefish could allow them to eat larger prey earlier and thereby limit availability of these prey to lake herring at a crucial period of development.

Résumé : Le régime et la croissance des larves de cisco (Coregonus artedi) et de grand corégone (Coregonus clupeaformis) ont été comparés dans le cadre d’expériences en mésocosmes menées dans un petit lac mésotrophe du sud-est Michigan. On a procédé pendant 8 semaines, en avril et mai, à un échantillonnage des poissons gardés dans des cages de 2 m3 contenant une seule espèce ou un mélange des espèces. Au début, les deux espèces se nourrissaient principalement de copépodites cyclopidés et de petits cladocères (Bosmina spp.). Selon l’indice de Schoener, le chevauchement des régimes alimentaires était considérable (70–90%). Le grand corégone s’est nourri de Daphnia spp. et de copépodes adultes environ 2 semaines plus tôt que le cisco, peut-être en raison de la plus grande largeur moyenne de sa bouche. Les grands corégones ont eu une taille constamment supérieure aux ciscos jusqu’à la huitième semaine, en particulier lorsqu’ils étaient soumis au mode sympatrique. Les grands corégones ont semblé exercer un effet négatif sur la croissance des ciscos, car ces derniers, lorsque les espèces étaient mélangées, avaient une taille et un poids inférieurs aux sujets des groupes monospécifiques. En raison des similarités du régime alimentaire des larves du cisco et du grand corégone, ces deux espèces pourraient entrer en compétition alimentaire dans les Grands Lacs. La taille initiale plus grande des grands corégones pourrait leur permettre de consommer plus tôt des proies plus grosses, ce qui limiterait la possibilité pour le cisco de se nourrir de ces proies à une période cruciale de son développement.[Traduit par la Rédaction]

Introduction

The coregonine fishes of the Great Lakes historically com-prised a complex group of several species differentiated pri-marily by time and place of spawning (Smith and Todd1984). Human impacts on the Great Lakes severely depletedstocks of all species, in particular, lake herring (Coregonusartedi), lake whitefish (Coregonus clupeaformis), and bloater(Coregonus hoyi), and resulted in the extinction of Coregonusalpenae, Coregonus johannae, Coregonus nigripinnis, andCoregonus reighardi (Todd and Smith 1992). Other factors

contributing to the decline included predation from alewife(Alosa pseudoharengus, on larvae), rainbow smelt (Osmerusmordax, on larvae), and sea lamprey (Petromyzon marinus,on juveniles and adults) and competition from alewife, rain-bow smelt, and other species of Coregonus (Smith 1972;Crowder et al. 1987). Recent declines in exotic fish popula-tions and favorable climatic changes have resulted in theresurgence of lake whitefish and bloater populations to recordlevels (Fleischer 1992). The resurgence of lake whitefish andbloater populations in Lakes Michigan and Huron was notaccompanied by a resurgence of lake herring populations(Fleischer 1992). The reason for the differential response isnot known, in part because the causes of the resurgence itselfare not well understood.

Factors affecting the early life history of these fishes arethought to be the most important in determining ultimate pop-ulation abundance and stability (Taylor et al. 1987; Miller etal. 1988). Small changes in the initial cohort growth rate canchange survival over the first 60 days of life 10- to 30-fold(Rice et al. 1993). Miller et al. (1990) suggested that the

Received October 21, 1996. Accepted December 19, 1997.J13709

B.M. Davis1 and T.N. Todd. Great Lakes Science Center, Biological Resources Division, 1451 Green Road, Ann Arbor, MI 48105, U.S.A.1 Author to whom all correspondence should be addressed.

e-mail: bruce_davis@USGS.GOV

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availability of appropriate sizes of zooplankton may haveprofound effects on the growth of juvenile fish and subse-quent recruitment. Food availability and the consequences ofits scarcity have affected growth and survival of both bloaterand lake whitefish larvae (Taylor and Freeberg 1984; Riceet al. 1987). Competition between lake herring, bloater, andrainbow smelt also has been suggested as a contributing fac-tor in the continuing low abundance of lake herring in LakesMichigan and Huron (Davis and Todd 1992; Todd and Davis1995). Hatch and Underhill (1988) suggested that larval mor-tality may be a reason for the continued low recruitment ofadult lake herring. Lake whitefish substantially overlap lakeherring in spawning and hatching times and locations (Cucinand Faber 1985), and lake whitefish larvae have been foundassociated with lake herring larvae (Faber 1970; Reckhan1970).

The purpose of this study was to determine the degree ofcompetition for food in larval lake herring and lake whitefishby (i) comparing their preference for particular prey species,sizes, and quantities of zooplankton and (ii) determining theextent of diet overlap between the two species.

MethodsEggs were removed from mature adults of lake herring and lakewhitefish and mechanically fertilized. Adult fecund lake herringwere taken from gill nets in the St. Mary’s River near Sault Ste.Marie, Michigan, in November 1988 and adult fecund lake whitefishwere taken from gill nets in Grand Traverse Bay near Traverse City,Michigan, in November 1988. Fertilized embryos were placed inMcDonald jars for incubation at mean temperatures of 2.4°C 6 0.05(mean 6 SE) for lake herring and 3.4°C 6 0.05 for lake whitefish.The embryos from the two species were incubated to synchronizehatching times.

On March 31, 1989, newly hatched lake herring larvae and lakewhitefish larvae were evenly distributed among twelve 2-m3 circularcages (500 per cage), 1.5 m in diameter, 1 m high, and made of 0.8-mm-mesh netting. The mesh was mainly selected to ensure retentionof the fish at their smallest size. Four cages contained only lake her-ring, four contained only lake whitefish, and four contained equalmixtures of both species (250 each). Lake herring were about11.3 mm and lake whitefish were about 14.5 mm at time of release inthe cages. The cage experiments were conducted in Pickerel Lake,Washtenaw County, Michigan, a small mesotrophic lake that sup-ports a population of native lake herring. Cages with fish larvae wererandomly distributed in four rows and four columns along with fourcages without fish (controls). We used the control cages to monitorthe difference between potentially available prey species inside andoutside the cages. This experimental setup provided five differenttreatments: single-species lake herring, single-species lake whitefish,mixed-species, no fish, and open lake.

Zooplankton and fish larvae were sampled beginning at dusk oncea week. A 4.2-L Kemmerer bottle was used to sample zooplankton.Two replicates were taken in each cage during each visit. Two repli-cates were also taken in the open lake adjacent to each control cageduring each visit. Samples were sieved through a 0.065-mm-meshbucket, rinsed into 0.5-L glass jars, and preserved in 10% formalin.During each visit, 10 fish were taken from each cage with a dip net,narcotized in 1% MS 222, and then preserved in 10% formalin. Sur-face water temperature was routinely taken with a mercury thermom-eter and routine maintenance of the cages included a thoroughscrubbing of the sides of the netting with a long-handled nylon brush2 days preceding and the day after sampling.

In the laboratory, zooplankton were identified and measured to thenearest 0.1 mm with an ocular micrometer. Five fish per species were

chosen at random from the 10 sampled from each cage on each date.All fish from the mixed-species cages were chosen. Nine to 18 fishper species on each date were selected from the remaining specimensfor use in mouth gape measurements with a gape micrometer. Fishwere weighed wet to the nearest 0.1 mg with a digital microbalanceand measured to the nearest 0.1 mm with an ocular micrometer.Stomach contents were excised and all prey were identified andcounted. Up to 20 individuals of each prey species were randomlyselected and measured to the nearest 0.1 mm. Prey items were identi-fied and prey biomass (dry weight) was estimated for each taxonfrom published length–weight regressions and values of mean dryweights (references available on request). For the few taxa for whichno dry weight value was available, weights for taxa of similar shapeand size were used. Prey species were combined into higher taxo-nomic groups for computing electivity indices for copepod nauplii,cyclopoid copepods, calanoid copepods, small cladocerans, large cla-docerans, Rotifera, and miscellaneous invertebrates. Linear preyselection indices (Strauss 1979) for these groups as prey categorieswere computed for both lake herring and lake whitefish for each visit.Strauss’ index = (ri – pi), where ri is the proportion of prey category iin the diet and pi is the proportion of prey category i in the environ-ment. Schoener’s index of diet overlap (Schoener 1970) was alsocomputed for each visit as

n

α = 1 – 0.5

^̂

x = 1|Pxi – Pyi|

!

where Pxi is the proportion of prey category i in the diet of species x,Pyi is the proportion of prey category i in the diet of species y, and nis the number of prey categories. We used analysis of variance(ANOVA) with repeated measures to (i) compare the differencesbetween the cages and the open lake for zooplankton density andsize, (ii) test differences in lengths and weights of fish, and (iii) com-pare differences between species for amount and size of eaten prey.When interactions and treatment and time effects were significant,we performed an interaction contrast analysis and used the Scheffeadjustment to calculate a critical value for the F statistic to test forcontrasts in treatment effects between the first 4 weeks and last4 weeks of the experiment (Tabachnick and Fidell 1996) because aphysical metamorphosis usually occurs between the fourth and fifthweeks of life. We also examined specific linear contrasts for varioustreatments when interaction contrasts were not significant (Tabach-nick and Fidell 1996). We used analysis of covariance (ANCOVA) toremove the effect of fish size when testing for differences in mouthgape of fish. Instantaneous growth rates were calculated weekly fol-lowing Ricker (1975) as

µ = [ln Lt2 (or Wt2

) – ln Lt1 (or Wt1

)]/(t2 – t1).

Computations were performed with the General Linear Model(GLM) procedure of SAS/STAT (SAS Institute Inc. 1989).

Results

Sixty invertebrate taxa excluding Rotifera were collectedfrom Pickerel Lake and combined into larger taxonomicgroups for analysis (Table 1). Rotifera were excluded from theanalyses because they were less than 1% of the fish diets bynumber and weight. Zooplankton density decreased in thelake and all cages except the controls throughout the study(Fig. 1). The density in the control cages peaked in week 5 andthereafter declined to values similar to the start of the study.Overall, there was a significant difference in zooplankton den-sities among treatments (F(4,15) = 84.76, P < 0.05). There was asignificant time by treatment interaction (F(28,33.87) = 3.39, P <0.05), and patterns of change in the control cages differed

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from those for the other treatments and these patterns weredifferent before and after metamorphosis (F(1,15) = 56.14, P <0.05). The slopes were significant (F(1,15) = 154.03, P < 0.05),indicating a significant linear trend in zooplankton density.

Density of the different zooplankton groups in the fishcages showed similar trends during the study. In general,cyclopoid copepod densities followed a pattern similar to totalzooplankton density (Fig. 1). There was a significant time bytreatment interaction (F(28,33.87) = 3.61, P < 0.05), and patternsof change in the control cages differed from those for the othertreatments and these patterns were different before and aftermetamorphosis (F(1,15) = 85.28, P < 0.05). Overall, there was asignificant difference in cyclopoid densities among treatments(F(4,15) = 63.56, P < 0.05). The slopes were significant(F(1,15) = 41.39, P < 0.05), indicating a significant linear trendin cyclopoid density. Copepod nauplii, the second most

abundant group, showed a significant time by treatment inter-action (F(28,33.87) = 1.94, P < 0.05), and densities appeared tobe cyclic. The variability in density of nauplii did not appearto be associated with differences in the control cages (F(1,15) =1.39, P > 0.05). The slopes were significant (F(1,15) = 343.35,P < 0.05), indicating a significant linear trend in nauplii den-sities. Both cyclopoid copepod and copepod nauplii densi-ties peaked in the fifth week. Calanoid copepod densitiesremained low throughout, although they did increase in thelake and control cages beginning in the fourth week.

Densities of large cladocerans steadily declined in most ofthe cages containing fish except for the fourth and fifth weeksin the cages with lake herring alone (Fig. 1). Densities in thelake and the control cages greatly increased before declining.There was a significant time by treatment interaction(F(28,19.45) = 2.42, P < 0.05), and there was an overall signifi-cant difference among treatments (F(4,15) = 7.04, P < 0.05).The variability in density of large cladocerans did not appearto be associated with differences in the control cages (F(1,11) =3.48, P > 0.05). The slopes were significant (F(1,11) = 27.08,P < 0.05), indicating a significant linear trend in density of

Table 1. Taxonomic groups of invertebrates occurring in Pickerel Lake in April–May 1989.

Cyclopoid copepods

Acanthocyclops robustus Diacyclops thomasiEucyclops agilis Macrocyclops albidusMesocyclops edax Microcyclops varicansTropocyclops prasinus

Calanoid copepods

Epischura lacustris Skistodiaptomus oregonensis

Copepod nauplii

Small cladocerans

Acroperus harpae Alona costataAlonella spp. Bosmina longirostrisCeriodaphnia spp. Chydorus sphaericusPleuroxus denticulatus Pleuroxus procurvusScapholeberis kingii

Large cladocerans

Daphnia galeata mendotae Daphnia pulexDiaphanosoma brachyurum Eurycercus lamellatusOphryoxus gracilis Polyphemus pediculusSimocephalus serrulatus Simocephalus vetulus

Miscellaneous invertebrates

Ceratium tripos CeratopogonidaeChaoborus punctipennis ChironomidaeCollembola EphemeropteraErgasilus spp. HarpacticoidaHyalella azteca Hydra spp.Hydracarina NematodaOdonata OligochaetaOstracoda PlecopteraTrichoptera

Fig. 1. Density of total zooplankton and major zooplankton groups in Pickerel Lake and study cages in April–May 1989. Symbols refer to cage type as follows: triangles, open lake; solid squares, control; open squares, lake whitefish; diamonds, lake herring; plus signs, mixed-species.

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Fig. 2. Mean (A) length and (B) weight of fish in cages in Pickerel Lake in April–May 1989. Symbols refer to fish type as follows: squares, single-species lake whitefish; diamonds, single-species lake herring; circles, mixed-species lake whitefish; triangles, mixed-species lake herring.

large cladocerans. Densities of small cladocerans in the fishcages declined greatly until the fifth week and then increasedwhereas in the control cages, they increased in the middleweeks before declining. There was a significant time by treat-ment interaction (F(28,33.87) = 4.13, P < 0.05), and significantdifferences were detected among treatments (F(4,15) = 30.77,P < 0.05), as patterns of change in the control cages differedfrom those for the other treatments (F(1,15) = 4.63, P < 0.05).The slopes were significant (F(1,15) = 47.68, P < 0.05), indi-cating a significant linear trend in density of small cladocer-ans. Miscellaneous invertebrates remained low until largeincreases occurred in the cages in the last 2 weeks. In mostweeks, densities of the five major groups in fish cages werehighest in the lake herring cages, lowest in the lake whitefishcages, and intermediate in the mixed-species cages.

Lake herring larvae and lake whitefish larvae grew at simi-lar rates in the first 4 weeks whether they were in mixed- orsingle-species assemblages (Fig. 2). The length–weightregression equations were lnW = –5.68 + 3.17 lnL (r2 =0.94) for single-species lake whitefish, lnW = –6.21 +3.36 lnL (r2 = 0.96) for single-species lake herring, lnW =–6.30 + 3.35 lnL (r2 = 0.98) for mixed-species lake whitefish,and lnW = –6.78 + 3.50 lnL (r2 = 0.96) for mixed-specieslake herring. In the last 4 weeks, single-species lake herringgrew faster and became as large as single-species lake white-fish. Mixed-species lake whitefish grew slightly faster thanmixed-species lake herring in the latter weeks. There was asignificant difference in mean length among treatments(F(4,15) = 4.13, P < 0.05), and the interaction contrasts showedthat the differences were between combined lake herring and

lake whitefish (F(1,12) = 112.20, P < 0.05). The slopes werehighly significant (F(1,12) = 2461.22, P < 0.05), indicating asignificant linear trend in fish growth. These differences weremore pronounced with weight. Single-species lake herringweighed as much as single-species lake whitefish in the fifthweek and were ultimately heavier by the eighth week. Mixed-species lake whitefish were much heavier than mixed-specieslake herring by the end of the study. In fact, interaction con-trasts showed mixed-species lake herring weighing signifi-cantly less than fish in the other treatments (F(1,12) = 36.59,P < 0.05). A significant time by treatment interaction wasobserved (F(21,17.78) = 5.29, P < 0.05), and patterns of changein weight of the mixed-species lake herring differed fromthose for the other treatments (F(1,12) = 11.35, P < 0.05). Theslopes were significant (F(1,12) = 544.32, P < 0.05), indicatinga significant linear trend in fish weight.

Instantaneous growth rates were generally highest early inthe study and declined as the fish became larger (Fig. 3),in particular after metamorphosis. A sharp drop in ratesoccurred in both weight and length of fish in mixed-speciescages in the fifth week that continued through the remainderof the study. This was observed after the fourth week in thesingle-species cages, especially for weight. Weight growthrate increased in all groups in the eighth week whereas lengthgrowth rate increased only in single-species lake herring.

Consumption of prey generally exhibited a significant lin-ear increase throughout the study period (F(1,12) = 133.36, P <0.05) (Fig. 4). However, prey eaten by both single-specieslake whitefish and lake herring declined sharply in the lastweek. A significant time by treatment interaction was

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observed (F(21,17.78) = 2.37, P < 0.05). Overall, the mixed-species lake whitefish ate significantly more prey (F(1,12) =15.93, P < 0.05), followed by single-species lake whitefish,mixed-species lake herring, and single-species lake herring.The variability in amount of prey eaten did not appear to beassociated with differences in the mixed-species lake white-fish treatments (F(1,12) = 0.01, P > 0.05). Throughout thestudy, the most abundant prey in fish stomachs were cyclo-poid copepods. Small cladocerans were also eaten fre-quently; fish ate Bosmina longirostris in the first 4 weeks andthen switched to Chydorus sphaericus in the last 4 weeks.Copepod nauplii were eaten by all fish for the first 3 weeks.Large cladocerans (Daphnia spp.) were eaten by both speciesin varying degrees; lake whitefish began eating Daphnia2 weeks earlier than lake herring. Single-species lake white-fish ate large cladocerans mainly from the second through thefifth week whereas they were eaten by single-species lakeherring from the third through the sixth week. Large cladocer-ans were eaten by mixed-species lake whitefish from the sec-ond through the fifth week whereas they were eaten bymixed-species lake herring in the fourth and fifth weeks. Mis-cellaneous invertebrates were mainly eaten in the sixth andseventh weeks. One lake whitefish from the mixed-speciescages had an empty stomach in the first week.

Mean lengths of eaten prey increased slightly in bothmixed- and single-species fish (Fig. 4). There was a signifi-cant treatment (F(3,12) = 48.12, P < 0.05) and time effect(F(7,84) = 19.65, P < 0.05). The single-species fish and themixed-species lake herring ate similar-sized prey, but prey of

the mixed-species lake whitefish were significantly largerthroughout the study (F(1,12) = 126.06, P < 0.05). The slopeswere significant (F(1,12) = 182.75, P < 0.05), indicating a sig-nificant quadratic trend for length of prey eaten, but were notsignificantly different across treatments (F(3,12) = 2.51, P >0.05). All fish except for lake herring in the first week ate, onaverage, prey that were larger than the size available in theirenvironment.

The mean length of zooplankton in the lake and controlcages increased slightly whereas zooplankton in the fishcages decreased in size (Fig. 4). Similar to density, meanlength of zooplankton in the mixed-species cages was inter-mediate to that in the single-species cages. There was a sig-nificant treatment effect (F(4,15) = 26.68, P < 0.05), but thetime by treatment interaction was also significant (F(28,33.87) =3.33, P < 0.05), and patterns of change in zooplankton lengthdensity in the control cages and open lake differed from thosefor the fish cages (F(1,15) = 18.83, P < 0.05). The size of zoo-plankton in the lake and the control cages was significantlylarger than in the fish cages (F(1,15) = 96.21, P < 0.05), andzooplankton in the lake herring cages were significantlylarger than in the lake whitefish cages (F(1,15) = 9.15, P <0.05) . The slopes were significant (F(1,15) = 8.50, P < 0.05),indicating a significant linear trend in mean length of zoo-plankton.

Mean weight of prey increased throughout the study simi-lar to the pattern for mean number of prey consumed (Fig. 4).However, the peak in weight was about a week later than thepeak in numbers for most fish. Overall, mixed-species lake

Fig. 3. Instantaneous growth rates in (A) length and (B) weight of fish in cages in Pickerel Lake in April–May 1989. Symbols refer to fish type as follows: squares, single-species lake whitefish; diamonds, single-species lake herring; circles, mixed-species lake whitefish; triangles, mixed-species lake herring.

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whitefish ate the most biomass followed by single-specieslake whitefish, single-species lake herring, and mixed-specieslake herring. However, except for a few instances, no signifi-cant differences were observed between treatments (F(3,12) =2.89, P > 0.05); the prey of mixed-species lake whitefishwere significantly heavier than the prey of fish in the othertreatments (F(1,12) = 5.68, P < 0.05). There was also a signifi-cant time effect (F(7,84) = 2.44, P < 0.05). The slopes were sig-nificant (F(1,12) = 23.20, P < 0.05), indicating a significantlinear trend in mean weight of prey.

The model relating mouth gape to fish length was signifi-cant (F(2,168) = 515.98, P < 0.05), and length was a significantfactor (F(1,168) = 1029.26, P < 0.05). Although mean mouthgape of lake whitefish was larger than that of lake herring inthe first 4 weeks (Table 2), mouth gape did not differ signifi-cantly between species (F(1,168) = 2.16, P > 0.05) when lengthwas considered. The larger initial size of lake whitefish prob-ably accounts for the larger mean mouth gape until metamor-phosis.

Food selection values and overall trends for both speciesand assemblages were similar throughout the study. Cyclo-poid copepods were the only prey items positively selected,and electivities remained essentially constant from week toweek (E = 0.475 6 0.02); however, great variation wasobserved among the single-species lake herring cages in thelast 2 weeks. Copepod nauplii were increasingly avoidedthroughout the study (E = –0.3276 0.02), but great variationwas observed in the lake herring cages in the fifth week. Cal-anoid copepods, large cladocerans, small cladocerans, andmiscellaneous invertebrates were randomly selected duringthe study with electivities about 0, but for small cladocerans,great variation occurred among the single-species lake her-ring cages in the last 2 weeks.

The index of diet overlap was high throughout the study.Both single-species and mixed-species assemblages had over70% overlap in the first week, peaking at over 95% in week 4.Slight decreases were observed in the last 4 weeks, althoughdiet overlap remained above 80%. The mixed-species assem-blages had a slightly higher mean overlap (89% vs. 87%), butthe differences were probably not significant.

Discussion

The high diet overlap between the species indicates potentialcompetition, especially considering the apparently high den-sities of potential prey. Index values greater than 60% suggestsignificant overlap, and overlap is usually highest amongcompeting species when food is most abundant and becomesleast when food is in short supply (Schoener 1982). However,in this study, food did not appear to be in short supply. Com-petition by definition requires that one of the competitorsshow negative effects from the interaction. Lake herring con-sumed less and grew less in the presence of lake whitefisheven when a great surplus of zooplankton appeared to occur.

Intraspecific competition among lake whitefish could existbecause lake whitefish when mixed with lake herring atemore and larger prey than lake whitefish alone. Although thedifferences were not significant, they were consistent. Thelesser number of equally large and aggressive lake whitefishcompetitors could have allowed each mixed-species treat-ment lake whitefish to eat more large-sized prey, theoreticallyeating more for less effort and with less competitive stress.

Lake whitefish could outcompete lake herring for limitedresources and thus leave them more vulnerable to predationfrom slower growth. Crowder et al. (1987) found that smallerzooplankton sizes induced reduced growth rates of larvalbloater and a prolongation of vulnerability to predation, andRice et al. (1993) demonstrated that mean growth rate andgrowth rate variation among individuals can interact stronglywith size-dependent mortality to cause significant effects onthe number, growth rates, and final sizes of survivors. Themixed lake herring showed reduced growth in length andespecially weight after the third week compared with thesingle-species lake herring. Hoagman (1974) found that ale-wife only fed on lake whitefish smaller than 17 mm. Whenour mixed lake herring reached similar lengths, the single-species lake herring were by then already 1 mm longer and10 mg heavier. However, the greatest differences in sizeoccurred several weeks later. Lake herring may even then stillbe vulnerable to alewife predation because Davis and Foltz

Fig. 4. Mean number of prey consumed per fish, mean length of prey consumed per fish, mean weight of prey consumed per fish by fish in cages, and mean length of total zooplankton in Pickerel Lake in April–May 1989. Symbols refer to fish type as follows: squares, single-species lake whitefish; diamonds, single-species lake herring; circles, mixed-species lake whitefish; triangles, mixed-species lake herring; plus signs, mixed-species.

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(1991) found land-locked blueback herring (Alosa aestivalis)eating substantial numbers of juvenile fish (mean length23.9 mm).

We raised Coregonus larvae in other years and obtainedsimilar results (Davis and Todd 1992; Todd and Davis 1995).Lake whitefish and lake herring larvae had good growth andsurvival with 500 fish per cage. However, increasing densi-ties of fish resulted in poorer growth and survival. Experi-ments in 1988 resulted in poorer growth for larvae of bothC. artedi and C. hoyi. The poorer growth in 1988 was proba-bly caused by unusually warm conditions and higher fish den-sities (1500 fish per cage) that led to excessive stress andmortality (Davis and Todd 1992). Karjalainen (1992)observed density-related responses in cage-reared vendace(Coregonus albula) and suggested that intraspecific competi-tion for food or predation disturbance on the feeding of thelarvae resulted in increased energy costs, weak growth, andultimately decreased survival of the larvae. He also noted thatvendace larvae were more dispersed in high-density situa-tions and that this deterioration of the normal schoolingbehavior might have implications for foraging efficiency.

The lake herring and lake whitefish larvae should have hadsufficient food for growth. Dabrowski (1976) reported the opti-mal feeding densities for Baltic whitefish (Coregonus lava-retus) larvae as 200–260 plankton individuals/L (199 994 –259 992/m3) (if weight is 4µg/individual). Hoagman (1974)suggested that C. clupeaformis larvae require 10–20 copepodsdaily, which all of our fish greatly exceeded. Dabrowski (1976)found C. lavaretus larvae consuming 80–97 individuals dailyat 13.5°C for the first 16 days of life. Our fish probably neededless food because temperatures averaged 7°C for the first21 days of the study; McCormick et al. (1971) found that opti-mal growth for lake herring occurred at 13–18°C.

Taylor and Freeberg (1984) and Brown and Taylor (1992)observed slower growth rates for C. clupeaformis than wefound in our fish. However, they experimentally fed their fishwith varying rations up to 100 or 110 zooplankton per fish perday in addition to deliberately starving some of them. Ourcage-raised fish generally consumed several hundred zoo-plankton daily and so obtained better growth. Our growthrates for lake whitefish were far higher than those measuredin Lake Michigan by Freeberg et al. (1990) (<29.8 mm com-pared with 17.9 mm total length after 7 weeks), but again, ourfish ate far more zooplankton.

Exact comparisons between our experimental fish and lar-val fish in the Great Lakes may not be possible because of thehigh growth rate and zooplankton densities observed in thecages. However, the relative level of response was repeated indifferent tests with varied fish and zooplankton densities in

other years of experimentation (Davis and Todd 1992; Toddand Davis 1995). Lake whitefish grew larger than lake her-ring in combined tests, but lower zooplankton densities orhigher fish densities resulted in slower growth rates thanthose reported here.

Both lake whitefish and lake herring controlled the densityand size of the zooplankton community by cropping off thelargest zooplankton. The depletion of larger zooplankton suchas daphnids and calanoids from the fish cages was also notedin 1988 and 1990 (Davis and Todd 1992; Todd and Davis1995). We inferred that they were highly preferred as preybecause they were scarce in fish cages and relatively moreabundant in the open lake and control cages. Other workershave also noted that planktivores prefer larger zooplanktonand rely on abundant cyclopoid copepods when daphnids andother cladocerans have been depleted (Bronisz 1979; Gunkel1981; Karjalainen and Viljanen 1993; Link 1996). The gapemeasurements showed that both fish species could easilyswallow most prey, providing they were eaten lengthwise.Even the largest Daphnia were no more than 1.6 mm wide,and the average lake whitefish could probably have handledthat size prey item by week 4 and lake herring that size preyitem by week 5. Cyclopoid copepods were preferred, but theywere also more available than the other large zooplankton. Ingeneral, Coregonus larvae seem to ingest the most abundantprey size without selecting the biggest ones available, even ifmechanically they were able to ingest them (Ponton andMüller 1990). John and Hasler (1956) found lake herring lar-vae preferring cyclopoids, and Reckhan (1970) and Freeberget al. (1990) found lake whitefish larvae initially feeding oncyclopoid and calanoid copepods.

Zooplankton densities were near equilibrium with theexternal environment, as most taxa appeared in similar num-bers in both the fish cages and the open lake. This may sug-gest a similar level of planktivory among the cages and thelake, or possibly that the cages provided an initial refuge forzooplankton and the high concentration of fish withindecreased the densities to open-lake levels. Most zooplanktonappeared to have flowed freely through the mesh, but passagewas probably difficult for the larger individuals of calanoidcopepods and large cladocerans. After the largest individualswere eaten, any smaller ones would also have been eaten oncethey attained similar sizes. However, as calanoids are a largeand a very elusive prey, these young fish would probably stillhave preferred cyclopoids. Miller et al. (1990) found the dietsof larval bloater dominated by copepods, and peak selectivitywas for prey 0.6–0.8 mm in fish 20–40 mm. It was not untiltheir fish were 60 mm that cladocerans were preferred andpeak selectivity was for prey 1.3–1.8 mm. Any affects on our

Table 2. Mean gape (mm 6 SE) of young lake herring and lake whitefish in Pickerel Lake in April–May 1989.

Week

1 2 3 4 5 6 7 8

Lake herring 0.5360.03 0.7260.06 0.9460.02 1.2860.07 1.7360.03 1.7260.01 1.7060.02 2.2660.09Lake whitefish 0.7160.04 0.8660.03 1.0860.05 1.6960.03 1.7360.03 1.7360.01 1.7160.01 1.8860.07

Note: Data were analyzed by ANCOVA and significance values are in the text.

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fish by the lack of availability of the largest calanoids mayhave been masked by the high abundance of other prey.

In comparing Pickerel Lake zooplankton with that of someGreat Lakes, we found major differences in abundance andspecies composition. Larval fish in our study had a veritablezooplankton soup to feed on compared with what they mightnormally encounter upon hatching in the Great Lakes. Thecages with fish had average abundances ranging from100 000 to 317 000/m3 excluding rotifers. In lake-widesurveys, Makarewicz et al. (1989) found average zooplanktonabundance from April to November in 1983–1985 to be54 689/m3 in Lake Michigan, 56 422/m3 in Lake Huron, and223 178/m3 in Lake Erie. However, these samples weretaken offshore and 40–70% of the total abundance wasattributed to rotifers. Most crustacean zooplankton species inLake Michigan are uniformly distributed in the spring (Gan-non 1975). Roth and Stewart (1973) found inshore and off-shore crustacean zooplankton (and the rotifer Asplanchna)ranging from 4000 to 32 000/m3 in southeast Lake Michiganduring April–June. Inshore densities were 10-fold higher(280 000/m3) in mid-August.

The species composition of available zooplankton preywas also quite different from what these larval fish wouldnormally encounter in the Great Lakes after hatch. However,except for certain calanoid copepods (Leptodiaptomus spp.and Limnocalanus macrurus), most of the major planktoniccopepods occurring in the Great Lakes (Robertson and Gan-non 1981) were found in Pickerel Lake. Cyclopoid copepodsand nauplii were the most abundant organisms in the cages,but there were also sizeable numbers of both large and smallcladocerans. Most studies report early spring zooplanktonbeing dominated by both calanoid and cyclopoid copepodsand nauplii (Roth and Stewart 1973; Gannon 1975; Evanset al. 1980; Makarewicz et al. 1989). Roth and Stewart (1973)reported smaller cladocerans (Bosmina) not appearing untilMay or dominating until mid-June, with larger cladoceransnot becoming significantly abundant until August. Evanset al. (1980) reported that nearshore zooplankton in southeastLake Michigan in early spring was dominated by copepodsand nauplii, and although cladocerans were present in theshallower and warmer areas of the lake, they were rare.

Because of their time of hatch in the Great Lakes, larvallake herring and lake whitefish would have less access to cla-docerans and would eat mainly cyclopoid and calanoid cope-pods. Lake herring and lake whitefish begin hatching inApril, and the larvae in Lake Huron are associated along steepshorelines with larvae of burbot (Lota lota), rainbow smelt,and deepwater sculpin (Myoxocephalus thompsoni) (Reck-han 1970); all except rainbow smelt appeared directly afterice breakup (Faber 1970). Most cladocerans do not appear inthe upper Great Lakes until after April (Balcer et al. 1984).However, we have found B. longirostris and Daphnia galeatamendotae in very low numbers from samples taken in LakeMichigan in mid-April 1993 (Great Lakes Science Center,unpublished data), and Gannon (1975) found the same spe-cies in very low numbers (<100/m3) in samples taken fromcross-lake transects in March and June.

Our study has shown that larval lake herring and lakewhitefish favor the same type of food, and these diet similari-ties could make them competitors for food in the Great Lakes.Sandlund et al. (1991) observed competition between adult

and juvenile vendace in which larger fish impacted the sur-vival of the smaller fish, and Miller et al. (1992) demon-strated that foraging ability is heavily dependent on sizedifferences. Possible competition should favor the lake white-fish whose greater initial size could allow them to eat largerprey earlier and thereby limit availability of these prey to lakeherring at a crucial period of development. Additionally,Savino and Hudson (1995) have shown that larval lake white-fish are more aggressive feeders than lake herring. The netresult of such competition would result in lake herringremaining at smaller, more vulnerable sizes for a longerperiod than lake whitefish with consequent increased mortal-ity from predation, as has also been suggested for bloater(Rice et al. 1987) and vendace (Karjalainen 1991). Size dif-ferences of only tenths of a millimetre can confer consider-able size advantages in resistance to starvation, and slight sizedifferences may have important consequences to a fish’s vul-nerability to predators (Miller et al. 1988).

Acknowledgments

We thank John LaBossiere, Michigan Department of NaturalResources, Pinckney, Michigan, for allowing our study to becarried out in Pickerel Lake and Susan Walker, biologist forGrand Traverse Bay Tribe, Grand Traverse Bay, Michigan,for obtaining lake whitefish eggs. We also thank MarcBlouin, Cynthia Kolar, John Miller, Daniel Ropek, andGentry Yearout for assistance in the field and for identifica-tion and enumeration of zooplankton samples and fishstomachs and Melissa Kostich for processing of gape mea-surements. We also thank Mary Fabrizio and Anthony Frankfor their aid in statistical analysis. We also thank JohnGannon, Jaci Savino, and Patrick Hudson for their review ofthis manuscript. Contribution 1005 of the Great LakesScience Center of the Biological Resources Division of theU.S. Geological Service.

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