Food web alterations that promote native species:the recovery of cisco (Coregonus artedi)populations through management of nativepiscivores
Damon M. Krueger and Thomas R. Hrabik
Abstract: We evaluated the effects of fisheries management on food webs in three northern Wisconsin lakes withexotic rainbow smelt (Osmerus mordax). In two of the lakes, restrictions on fishing reduced mortality rates on adultwalleye (Sander vitreus) during the study period. In these lakes, walleye populations increased concurrently with a de-cline in rainbow smelt populations. As rainbow smelt populations declined in both lakes, native cisco (Coregonusartedi) populations increased. Our analysis of walleye diets illustrated that walleye fed selectively on rainbow smelt butdid not feed on cisco during the summer months. When entered into bioenergetics simulations, this information demon-strates that walleye predation alone was enough to cause the observed rainbow smelt declines in our study lakes. Ourresults indicate that increased walleye density allows for a parallel increase in cisco density. Based on our results, fish-ery regulations to restore walleye to high densities in lakes invaded by rainbow smelt may restore native planktivoresthat have co-evolved traits.
Résumé : Nous avons examiné les effets de la gestion des pêches sur les réseaux alimentaires dans trois lacs du norddu Wisconsin contenant des éperlans arc-en-ciel (Osmerus mordax) exotiques. Dans deux des lacs, la restriction de lapêche a entraîné une réduction des taux de mortalité chez les dorés (Sander vitreus) adultes durant la période d’étude.Dans ces lacs, les populations de dorés se sont accrues parallèlement à un déclin des populations d’éperlans arc-en-ciel.Au fur et à mesure que les populations d’éperlans arc-en-ciel ont diminué dans les deux lacs, les populations indigènesde ciscos de lac (Coregonus artedi) ont augmenté. Notre analyse du régime alimentaire des dorés montre que durantles mois d’été les dorés se nourrissent préférentiellement d’éperlans arc-en-ciel, mais non de ciscos de lac. Cette infor-mation, incorporée aux simulations bioénergétiques, démontre que la seule prédation par les dorés ne suffit pas à expli-quer le déclin des populations d’éperlans arc-en-ciel observé dans nos lacs d’étude. Nos résultats indiquent que ladensité accrue de dorés permet un accroissement en parallèle de la densité des ciscos de lac. D’après ces résultats, lesrèglements de pêche qui visent la restauration des fortes densités de dorés dans les lacs envahis par l’éperlan arc-en-ciel peuvent rétablir les planctonophages indigènes qui possèdent des caractéristiques coévoluées.
[Traduit par la Rédaction]
Krueger and Hrabik 2188
Introduction
Food web manipulation offers a mechanism to manageaquatic ecosystems that have been invaded by exotic species.Within this context, predation by piscivores represents anagent that may prove useful for controlling unwanted preyfish species. However, commercial or sport fishing interestsoften exploit predator populations, decreasing their abun-dance and effects on prey species. In fact, many of theworld’s fisheries are overexploited (Myers and Worm 2003),
and decreased predator populations have caused substantialchanges in food web characteristics (Cox et al. 2002).
In some cases, decreased predator densities caused byfishing may allow less desirable fish species to dominate.For example, exotic forage fish, such as rainbow smelt(Osmerus mordax) and alewife (Alosa pseudoharengus),dominated the Lake Michigan food web after piscivore pop-ulations declined (Kitchell and Crowder 1986). This mayhave caused the decline of one or more commercially impor-tant native species (Crowder 1980).
Received 29 June 2004. Accepted 24 April 2005. Published on the NRC Research Press Web site at http://cjfas.nrc.ca on16 September 2005.J18199
D.M. Krueger1,2 and T.R. Hrabik. Department of Biology, University of Minnesota–Duluth, 211 Life Science Building, 10University Drive, Duluth, MN 55812, USA.
1Corresponding author (email: [email protected]).2Present address: Great Lakes Environmental Research Laboratories, 2205 Commonwealth Boulevard, Ann Arbor, MI 48105, USA.
Exotic rainbow smelt are rapidly colonizing small lakes inthe upper midwest and western reservoirs (Jones et al. 1994;Johnson and Goettl 1999). In many ecosystems in whichrainbow smelt became established, similar patterns of nega-tive effects were observed (Franzin et al. 1994; Hrabik et al.1998; Hrabik and Magnuson 1999). Native coregonid spe-cies, such as cisco (Coregonus artedi) and lake whitefish(Coregonus clupeaformis), show particularly rapid declinesfollowing rainbow smelt establishment in many small north-ern temperate lakes (Loftus and Hulsman 1986; Evans andLoftus 1987; Hrabik et al. 1998). Therefore the future statusof native coregonine populations in the upper midwest willlikely be related to the range expansion and success of rain-bow smelt.
Restoring or recovering native piscivore populations mayprovide a mechanism to control harmful exotic fish speciesand promote the recovery of native planktivores. In the Lau-rentian Great Lakes, decreases in predator abundance inresponse to commercial exploitation and sea lamprey preda-tion led to increases in exotic alewife and rainbow smeltpopulations (Smith 1968; Wilberg et al. 2002). However, anintensive predator stocking program increased consumptionof exotic prey fishes, which eventually led to decreased rain-bow smelt and alewife abundance in Lake Michigan (Kitchelland Crowder 1986). Furthermore, recent changes in the fishcommunity of Lake Superior suggest that increased preda-tion by lake trout is associated with rainbow smelt popula-tion declines and may have facilitated reciprocal increases innative coregonine species (Hansen 1994).
Five lakes in the Northern Highland Lakes District ofWisconsin offer the opportunity to examine the influence ofpredator density on exotic rainbow smelt populations. Twolakes support walleye (Sander vitreus) populations that haveincreased as a result of more stringent fishing regulationsand extensive stocking. A third lake contains rainbow smeltbut few predators, and represents a control system that al-lows us to assess a rainbow smelt population in a predatordepauperate environment. Data from this control lake alsodemonstrate the negative effect of rainbow smelt on nativeplanktivores. In the lakes with walleye, the smelt populationsdeclined concurrently with reciprocal increases in nativecisco populations. However, the two rainbow smelt popula-tions declined at different rates. The fourth and fifth lakescontain native piscivores and native cisco populations andallow us to determine whether cisco populations recently in-creased owing to changes in local climate. Our objective wasto determine the cause of the observed changes in the rain-bow smelt and cisco populations that occurred concomi-tantly with increased predator abundance in the lakes inwhich fishing regulations changed. The different rates of de-cline in rainbow smelt population sizes and subsequent in-creases in cisco population sizes offer insight into theinfluence of predators on rainbow smelt and cisco interac-tions. Long-term changes in prey biomass due to changes inpredation rates measure the influence of a predator on a preycommunity (Beisner et al. 2003). We therefore hypothesizedthat selective predation by walleye reduced rainbow smeltabundance and led to compensatory increases in cisco popu-lations. To evaluate this hypothesis, we used data from fieldstudies to describe fish distribution and abundance in thefive lakes from 1981 to 2002. We analyzed walleye diets and
modeled fish consumption to estimate the interactionstrength among walleye, cisco, and rainbow smelt in two ofthe lakes. We also compiled information on fishery manage-ment within the study lakes because harvest has a strong in-fluence on predator mortality (Cox and Walters 2002; Postet al. 2002). We sought to determine whether walleye fish-ery restrictions led to increased walleye predation on rain-bow smelt and allowed for cisco recovery. Therefore weexamined the following: (i) correlations among populationcharacteristics of walleye, cisco, and rainbow smelt;(ii) walleye diet composition throughout the open-water sea-son to identify whether walleye preyed selectively on rain-bow smelt; and (iii) walleye consumption rates on rainbowsmelt estimated using bioenergetics models.
Materials and methods
Study sitesWe studied five lakes in the Northern Highland Lakes Dis-
trict in Vilas County, Wisconsin (Fig. 1) from 1981 to 2002.Fence and Crawling Stone lakes are under the jurisdiction ofthe Lac Du Flambeau Band of the Lake Superior ChippewaNatural Resource Department, while Crystal, Trout, and BigMuskellunge lakes are under the jurisdiction of the Wiscon-sin Department of Natural Resources (WDNR; see Table 1for the physical characteristics of study lakes). Trout, BigMuskellunge, Fence, and Crawling Stone lakes support pop-ular sport fisheries and sustain relatively high densities ofwalleye that are augmented by annual stocking. Crystal Lakecontains few piscivorous fish and is not regularly stocked.
Prior to 1989, the Lac Du Flambeau tribal council main-tained liberal fishing regulations on Fence and CrawlingStone lakes. Both lakes had no minimum length limit, andnon-tribal anglers were allowed to harvest five walleye perday. In 1990, the WDNR implemented a statewide 15-in(1 inch = 2.5 cm) minimum length limit on walleye. Regula-tions on Fence and Crawling Stone lakes became more con-servative in 1997 when tribal fishery managers imposed an18-in minimum length limit and a bag limit of three walleyeper day. In addition to sport fishing, Fence and CrawlingStone lakes experienced unregulated spear fishing on wall-eye prior to 1997. From 1986 to 1997, spear fishers removedthousands of adult walleye each year (L. Wawronowicz,P.O. Box 67, Lac Du Flambeau, WI 54538, USA, personalcommunication). In 1997, the Lac Du Flambeau tribal coun-cil banned spear fishing (with the exception of tribal youthspearing in 2002) to allow the walleye populations in eachlake to recover and to support egg collections for localhatchery operations.
Population density and dynamics
Fish collectionWe collected walleye, cisco, and rainbow smelt using a
variety of methods in Fence and Crawling Stone lakes. Inthe spring of 2002, we set 1.5 m square mouth, 5 mm meshfyke nets to capture walleye during the spawning period atknown spawning shoals and reefs. We removed walleye fromthe nets daily for 15 consecutive days on each lake. Netswere not moved during the spawning period. After spawningactivity ended, we used a boom-style AC electrofishing boatto collect walleye at night from near-shore areas of both
lakes and to quantify the littoral zone prey fish community.We fished two 1-km transects weekly on Fence andCrawling Stone lakes from 21 May through 27 June 2002.We rotated among five sites on each lake. Following thermalstratification, we used 30 m × 3 m vertical gillnets withmesh size measuring 19, 25, 32, 38, 54, 69, 89, and 127 mmto capture pelagic fishes in Fence and Crawling Stone lakes.Nets were set monthly and biweekly throughout the sum-mers of 2001 and 2002, respectively, to measure the abun-dances and sizes of pelagic forage fishes and to recoverwalleye diets. We set gillnets at night for less than 6 h tominimize digestion of walleye stomach contents and to max-imize the number of fish caught. Using gillnet catch data,we quantified the thermal overlap among fish species (e.g.,see Schoener 1970; Hrabik et al. 1998). The Long-Term
Ecological Research – North Temperate Lakes (LTER–NTL) project sampled fish in Crystal Lake annually (seeMagnuson et al. 1984, 1994) using fyke nets, trammel nets,and a size spectrum of vertical gillnets ranging from 19 to89 mm stretch mesh.
Throughout the summer of 2002, length and weight infor-mation was continually collected on all fishes, and scaleswere collected from a subsample of each species for age es-timation. Each subsample was composed of two fish for ev-ery 5-mm increment in total length. We removed at leastthree scales from behind the left pectoral fin in all instances.
We collected supplemental catch data for cisco andwalleye in two additional LTER–NTL lakes, Trout Lake andBig Muskellunge Lake. Both lakes support sport fisheries forlarge piscivores, although neither supports rainbow smelt.
Fig. 1. Map of northern Wisconsin, USA, showing the locations of (a) Crawling Stone Lake (89°53′4 ′′ W, 45°56′25 ′′ N);(b) Fence Lake (89°50′22 ′′ W, 45°56′56 ′′ N); (c) Crystal Lake (89°36′43 ′′ W, 46°0′5 ′′ N); (d) Big Muskellunge Lake (89°37′22 ′′ W,46°0′9 ′′ N); and (e) Trout Lake (89°40′9′′ W, 46°1′9 ′′ N).
Data from these lakes allowed us to track indices of ciscobiomass in the absence of rainbow smelt predation but witha potential risk of predation. We also hoped to assesswhether regional processes were responsible for the ob-served trends in cisco abundance in Fence and CrawlingStone lakes. Data were collected online via the University ofWisconsin, Center for Limnology LTER–NTL fish database.
Mark and recaptureWe tagged and released walleye to obtain mark–recapture
population estimates in Fence and Crawling Stone lakes us-ing Chapman’s modification of Schnabel’s method (Ricker1975). Fish were captured via electrofishing and fyke netsalong the near shore areas of Fence and Crawling Stonelakes in early spring. After we marked individual walleyewith T-bar floy tags, they were released in random locations,which were generally in the pelagic area of the lake. Wemarked 340 walleye averaging 530-mm total length fromFence Lake, and 202 walleye averaging 513-mm total lengthfrom Crawling Stone Lake.
Hydroacoustic samplingHydroacoustic transects were performed following lake
stratification to obtain estimates of fish size, depth distribu-tion, and density in each study lake. The LTER–NTL pro-gram used a Simrad EY-M 70 kHz single-beam ecosounderto run yearly hydroacoustic transects on Crystal Lake (threetransects) from 1981 to 1994 and on Fence and CrawlingStone lakes (six and five transects, respectively) in 1993.HADAS postprocessing software was used to analyze thesetransects (Rudstam et al. 1993; Sanderson et al. 1999). Weused a 120-kHz BioSonics DT6000 split-beam echosounderto collect hydroacoustic data in 2001 and 2002 on Fence,Crawling Stone, and Crystal lakes. We ran five transects onFence and Crawling Stone lakes in 2001 and 2002 and threeon Crystal in 2002. We used Echoview (v.3.0) software toanalyze acoustic data for two nights in 2001 and four nightsin 2002 on Fence and Crawling Stone lakes and one night in2002 on Crystal Lake. Hydroacoustic estimates of smeltpopulation density in Crystal Lake were proportional togillnet catch rates (population estimate = 67.6 × gillnet catchper unit effort (CPUE), r2 = 0.95, p < 0.001). We used thisrelationship between gillnet catch rates and hydroacousticestimates to approximate population sizes and biomass whenno acoustic data were available (1995–2000). Hydroacousticdata for Fence and Crawling Stone lakes were not availablefor years prior to 1993. We assumed that population densi-ties of pelagic species were proportional to gillnet catch, asin Crystal Lake. We used 1993 gillnet catch and 1993 popu-lation estimates for Fence and Crawling Stone lakes to esti-mate the proportional relationships and population sizes for1982 in Fence Lake and 1986 in both lakes.
Simrad and BioSonics echosounders were calibrated bi-monthly with standard tungsten carbide spheres of knowntarget strength. We corrected 1993 fish density estimates forbias owing to differences in target strength distributions be-tween single and split-beam echosounders (e.g., Rudstam etal. 1999). We used fish species composition, depth distribu-tion, and size data from vertical gillnets to categorize indi-vidual hydroacoustic targets by species. We then estimatedtotal lake population sizes by multiplying the density of eachspecies within 1-m depth strata with the volume of water
within each stratum as in Rudstam et al. (1993) and Sander-son et al. (1999).
Analyses of body condition and fish size
Estimation of body conditionWe developed lake-specific length–weight regressions to
estimate variability in rainbow smelt body condition inFence Lake (where rainbow smelt declined) and CrystalLake (where rainbow smelt increased) between periods ofhigh and low rainbow smelt abundance. Rainbow smelt bodycondition is associated with variability in their populationdensity and offers a useful index of feeding success (Hrabiket al. 1998). We applied a linear model to log-transformedbody mass and total length data pooled across years withineach lake (Hrabik et al. 1998). A single regression fit to alllength and weight observations across all years for a lakewas used to estimate a lake-specific length–weight relation-ship. We grouped the residuals for individual fish by yearand used the mean residual in each year as an index of thebody condition of rainbow smelt in each lake. We did so toexamine whether trends in smelt body condition in FenceLake corresponded to decreases in their abundance, orwhether smelt performance in Fence Lake may have been in-fluenced by an alternative environmental variable. In addition,we sought to identify whether smelt in Crystal Lake, wherepredators were rare, exhibited indications of density depend-ence. Body condition was not calculated for Crawling StoneLake because no rainbow smelt were captured after 1993.
Analyses of fish sizeVariability in the sizes of rainbow smelt and walleye were
examined to identify any changes in size that coincided withchanges in abundance and mortality rates in each population.We examined the mean length of rainbow smelt in Crystal andFence lakes and of walleye in Fence Lake through time; datapoints represent periods with marked differences in the abun-dance and mortality of each species in each lake. We expectedthat smelt sizes would decrease in response to increases in pre-dation pressure by walleye in Fence Lake, and that the size ofwalleye would increase with decreases in their mortality.
Diet compositionWe analyzed 220 walleye stomachs collected via electro-
shocking, gillnets, and angling in Fence and Crawling Stonelakes. Following capture, stomach contents were flushedfrom live fish (Seaburg 1957) and whole stomachs were ex-cised from deceased fish caught in gillnets. We preservedstomach contents of all walleye in 95% ethanol and laterseparated and dried contents to obtain biomass proportionsfor input into bioenergetics modeling scenarios. We used nu-merical proportions of the common prey items to estimateprey selection using Chesson’s (1983) alpha. Alpha valueswere calculated for individual walleye and averaged forMay, June, July, and August.
Bioenergetics modeling
Fish growthWe examined scales to determine growth rates for 85 and
81 walleye from Fence and Crawling Stone lakes, respec-tively. We then used the proportional method (DeVries and
Frie 1996) to back calculate length at age for individual fish.The same method was used to estimate size at age andgrowth rates for rainbow smelt and cisco. Finally, wegrouped individual fish into year classes according to lengthand averaged weights for each year class. For walleye, wealso estimated the age structure of the entire population,based on the subsample of fish we aged. First, we estimateda length range for each age class. Second, we determined theproportion of sampled fish that fell into each length range.Last, we multiplied the length-at-age proportions by theacoustic population estimate to achieve a whole-lake agestructure for walleye.
TemperatureWe measured temperature profiles monthly during the
summer of 2002 in Fence and Crawling Stone lakes. TheLTER–NTL program measured temperature profiles in Crys-tal Lake biweekly from ice out to late November from 1981
to 2002. We estimated daily water temperature at depth inall three lakes using linear interpolation between water tem-perature measurement dates in each year. Temperature datawere input into bioenergetics modeling scenarios.
Estimation of prey consumptionWe used fish bioenergetics models to assess the potential
impact of walleye predation on rainbow smelt and of rain-bow smelt predation on young cisco in Fence Lake. Wequantified these effects by simulating consumption bywalleye and rainbow smelt with the Wisconsin bioenergetics3.0 software (Hanson et al. 1997). In situ weight-at-age datawere input as start and end points to estimate the energybudget for average individual walleye and rainbow smelt.We also input species- and depth-specific thermal data, aswell as diet composition (for walleye), to estimate total an-nual consumption by walleye and rainbow smelt in 1982(Fence Lake only), 1986, 1993, 2001, and 2002 in Fence and
Fig. 2. The estimated biomass of predator and prey species in each study lake from 1982 to 2002. (a) The biomass of predatory fishin Crystal Lake represented as a combined estimate of lake trout (Salvelinus namaycush) and walleye (Sander vitreus). (b) The bio-mass of rainbow smelt (Osmerus mordax; solid bars) and native perch (Perca flavescens; open bars) in Crystal Lake.(c) The biomassof walleye in Fence Lake. (d) The biomass of rainbow smelt (solid bars) and native cisco (Coregonus artedi; open bars) in FenceLake. (e) Walleye biomass through time in Crawling Stone Lake. ( f ) The biomass of rainbow smelt (solid bars) and native cisco(open bars) in Crawling Stone Lake. Note the difference in scale for the y axis between predator and prey species.
Crawling Stone lakes. To estimate total consumption, wefirst found the proportion of fish in each age class using theaforementioned methods. Then, we multiplied consumptionof the average individual in each age class by the acousticpopulation estimate for each age class to estimate total con-sumption in each study year. In addition, we compared rain-bow smelt biomass consumed by walleye with rainbow smeltbiomass available in Fence Lake to determine the proportionof the rainbow smelt population walleye consumed in eachyear of the study. We obtained the caloric densities of yel-low perch (Perca flavescens), cyprinids, and rainbow smeltused in our modeling scenarios from Bryan et al. (1996), andthe caloric density of walleye from Kitchell et al. (1977).
Results
Walleye population dynamicsIn Fence and Crawling Stone lakes, walleye population
size and mean length increased considerably from 1982 to2002. In Fence Lake, the adult walleye (total length > 300 mm)population density increased from 3.2 kg·ha–1 (1.4–5 kg·ha–1)in 1993 to 9.7 kg·ha–1 (6.2–12 kg·ha–1) in 2002 (Fig. 2).Mark–recapture estimates for walleye ranged from 3 to42 fish·ha–1 (3.9–54.6 kg·ha–1). Mean length of walleye in-creased from 361 mm in 1982 to 507 mm in 2002, indicat-ing a significant increase in size structure (Fig. 3). Stockingof fingerling walleye averaged 28 fingerlings·ha–1·year–1
(±12 fingerlings·ha–1·year–1).In Crawling Stone Lake, the biomass of walleye also in-
creased from 1986 to 2002. Initially, walleye biomass fellfrom 7.2 kg·ha–1 in 1986 to 3.1 kg·ha–1 in 1993. However,walleye biomass increased to 25.4 kg·ha–1 (15.2–35.4 kg·ha–1)by 2002 (Fig. 2). Mark–recapture population estimates aver-aged 6.3 walleye·ha–1 and ranged from 4 to 60 walleye·ha–1
(4.8–72 kg·ha–1) owing to low recapture rates. However,these estimates are comparable to hydroacoustic estimates.Walleye mean length was 495 mm in 2002, just short of theaverage in Fence Lake. Stocking of walleye fingerlings inCrawling Stone Lake was higher than in Fence Lake and av-eraged 44 fingerlings·ha–1·year–1 (±17 fingerlings·ha–1·year–1).
In Trout Lake, catch rates of adult walleye appeared torise slightly from 1981 to 2002. However, in Big Muskel-lunge Lake, there was no apparent pattern in catch rates ofadult walleye (Fig. 4).
Rainbow smelt population dynamicsWe observed the highest density of rainbow smelt in
predator-poor Crystal Lake. The biomass of rainbow smeltincreased steadily since their detection in 1986, and ap-proached 35 kg·ha–1 in 2002 (Fig. 2). As rainbow smelt bio-mass increased after 1993, their mean length distribution didnot change (Fig. 5). Rainbow smelt body condition declinedafter 1993 and the trend was consistent with density-dependent processes associated with increases in populationsize (Fig. 5). Population size of yellow perch (Percaflavescens), once the dominant planktivore in the lake, de-clined and their biomass was negatively correlated to rain-bow smelt biomass (Fig. 2).
In Fence and Crawling Stone lakes, rainbow smelt bio-mass decreased, particularly in the latter years of our study
period. In Fence Lake, rainbow smelt biomass decreasedfrom 32 kg·ha–1 in 1993 to approximately 13 kg·ha–1 in 2002(Fig. 2). Rainbow smelt average length also decreasedthrough time and coincided with increases in walleye bio-mass (Fig. 5). In contrast, the average body condition ofrainbow smelt in Fence Lake increased through time(Fig. 5). According to population age frequency data, rain-bow smelt total annual mortality was 59% in 2002 (e.g.,Ricker 1975).
In Crawling Stone Lake, rainbow smelt population densi-ties increased roughly sixfold from 1986 to 1993. However,rainbow smelt population biomass in Crawling Stone Lakedecreased substantially after 1993. Rainbow smelt biomassdeclined from approximately 12 kg·ha–1 in 1993 to undetect-able levels by 2001 (Fig. 2). Rainbow smelt were not foundin Crawling Stone Lake in 2001 or 2002, which indicates astronger decline in rainbow smelt population density thanwas observed in Fence Lake.
Cisco population dynamicsIn Fence and Crawling Stone lakes, cisco showed tremen-
dous increases in population size. In Fence Lake, cisco bio-mass increased between 1993 and 2002, and they are nowthe dominant pelagic planktivore in the system, both in num-ber and by biomass. Cisco, which were common in bothFence and Crawling Stone lakes in the 1960s (S. Gilbert,Wisconsin Department of Natural Resources, 8770 Hwy JWoodruff, WI 54568, USA, personal communication), wererare in 1993 when only one individual was caught. In 1982,1986, and 1993, no cisco younger than 4 years old were cap-tured. Cisco abundance in Fence Lake increased substan-tially between 1993 and 2002. Hydroacoustic data collectedin 2002 indicated that cisco biomass was approximately23 kg·ha–1 in Fence Lake, a 14-fold increase from 1993(Fig. 2). Furthermore, young fish dominated the cisco popu-
Fig. 3. Estimates of mean size of walleye caught in Fence Lakefrom 1982 to 2002.
lation of Fence Lake in 2002, where most fish were youngerthan 2 years.
In Crawling Stone Lake, cisco biomass increased consid-erably from 1986 to 2002. Although cisco were abundant inCrawling Stone Lake in the 1960s and 1970s, their biomassdeclined to approximately 1.2 kg·ha–1 by 1993. By 2002,however, cisco biomass increased to approximately82.5 kg·ha–1. Cisco biomass was higher in Crawling StoneLake than in Fence Lake, and fish of various ages were ob-served, including an abundant age-0 year class. Cisco inFence and Crawling Stone lakes attained a length of 200 mmin their second year, a length exceeding the gape limitationof the average adult walleye in 2002, assuming walleye con-sume prey items that are <30% of their body length(Rudstam et al. 1993). In Trout and Big Muskellunge lakes,cisco catch rates did not consistently increase after 1993(Fig. 4).
Walleye diet characteristics and consumptionConsumption by walleye increased throughout the study
in Fence and Crawling Stone lakes, which coincided with in-creases in body size and population density. In 2002, FenceLake walleye were piscivorous, and 76% of diets (n = 83 outof 110) contained fish prey. Walleye primarily consumedrainbow smelt, yellow perch, and cyprinids; other prey com-prised less than 5% of the diet. In the early summer months,walleye fed mostly on cyprinids and perch and less so on
rainbow smelt. In late summer, walleye fed selectively onrainbow smelt (Fig. 6), concomitantly with increasing spatialoverlap between rainbow smelt and walleye (Fig. 7).Walleye did not feed on the abundant cisco in Fence Lake.
Consumption by walleye on fish prey increased substan-tially in Fence Lake from 1993 to 2002 and was related toincreased walleye population density. Bioenergetics model-ing indicated that the Fence Lake walleye population con-sumed approximately 55% of rainbow smelt biomass in2002 (Fig. 8), which accounts for 93% of the total annualmortality experienced by rainbow smelt, based on populationage frequencies (e.g., Ricker 1975).
Walleye in Crawling Stone Lake were less piscivorousthan Fence Lake walleye in 2002 and a smaller proportion ofdiets contained food items (60%; n = 66 out of 110). Walleyeprimarily consumed ephemeropterans, yellow perch, andminnows throughout the summer. Despite the lack of rain-bow smelt in gillnet samples in Crawling Stone Lake, rain-bow smelt occasionally appeared in walleye diets, signifyinga relict rainbow smelt population. Walleye did not feed oncisco in Crawling Stone Lake despite the relatively highabundance of the small age-0 stages of cisco.
Prey consumption by walleye in Crawling Stone Lake in-creased substantially from 1993 to 2002. In 2002, walleyeconsumed approximately 58 kg·ha–1, which is roughly fivetimes higher than the consumption rates we observed inFence Lake (Fig. 9). We estimated that the walleye popula-
Fig. 4. Catch per unit effort (CPUE) of predator and prey species in supplemental study lakes. (a) CPUE of walleye (Sander vitreus)in Trout Lake. (b) CPUE of cisco (Coregonus artedi) in Trout Lake. (c) CPUE of walleye in Big Muskellunge Lake. (d) CPUE ofcisco in Big Muskellunge Lake. Data collected by the Long-Term Ecological Research – North Temperate Lakes (LTER–NTL) pro-gram using 24-h vertical gillnet sets and three 30-min electroshocking transects (see Magnuson et al. 1984, 1994).
tion was capable of consuming approximately 72% of theadult rainbow smelt population in 1993, when rainbow smeltwere last found in Crawling Stone Lake.
In Fence and Crawling Stone lakes, rainbow smelt popula-tion declines were concurrent with increases in prey con-sumption by walleye. Thus, there appeared to be a relationshipbetween consumption rates by predators and rainbow smeltdensity. Consumption by rainbow smelt, the factor mostlikely associated with cisco declines, was negatively associ-ated with consumption by piscivorous walleye in the studylakes (Fig. 10).
Discussion
Assessing food web structure and changes in rainbowsmelt abundance
Manipulating the density of top predators in lake ecosys-tems represents a mechanism to generate changes in lowertrophic levels through predator–prey interactions. Thesechanges may ease competition–predation effects and facili-tate recovery of a native species (Kitchell et al. 1988). Ourobservations in five northern temperate lake ecosystems thatexperienced rainbow smelt introductions indicate that ma-nipulating predator communities yields results consistentwith those observed in other lakes over the past few decades(e.g., see Kitchell and Crowder 1986; Johnson et al. 1992;Kitchell et al. 2000). In Fence and Crawling Stone lakes,where predator stocking and predator harvest regulations fa-cilitated increases in the native predator, the food web re-turned to one dominated by native species. This result was
likely the effect of selective predation on exotics by nativepredators and species-specific characteristics.
Selective predation often alters prey community composi-tion (Brooks and Dodson 1965; Carpenter and Kitchell 1988)and our results support this contention. Increased asymmet-ric predation rates in two study lakes resulted in a shift inplanktivore dominance; rainbow smelt population densitiesdeclined while cisco population densities increased. Ciscobiomass exceeded rainbow smelt biomass in both lakes in2002, yet cisco were not consumed by walleye. Cisco typi-cally represent twice the energetic benefit to a predator whencompared with rainbow smelt (Bryan et al. 1996). This iscounterintuitive to our finding that walleye selectivelypreyed upon rainbow smelt. However, our results indicatethat walleye overlapped spatially with rainbow smelt moreso than with cisco, particularly in late summer, and may ex-plain the lack of cisco in walleye diets. Differences in size atage may further explain the pattern in prey preferences ex-hibited by walleye. All rainbow smelt were vulnerable topredation by the average-sized walleye in each lake. Cisco,however, attain a size refuge relatively quickly, making themless vulnerable to walleye predation throughout most of theirlifespan. The lack of age-0 cisco in walleye diets implicatesa predator avoidance behavior that may be the result of co-adaptation over longer timescales. The high consumptionrates exhibited by walleye on rainbow smelt in later studyyears (2001 and 2002) likely allowed age-0 cisco to avoidpredation by rainbow smelt with greater success than inearly study years (1982–1993). Our results suggest that pre-dation by walleye substantially reduced rainbow smelt aver-
Fig. 5. The average length of rainbow smelt (Osmerus mordax) in (a) Crystal and (b) Fence lakes captured in gill nets and the averagebody condition of smelt in (c) Crystal and (d) Fence lakes from 1985 to 2002.
age size, rainbow smelt population density, and consumptionby the rainbow smelt populations as a whole. These declineslikely reduced competition and intraguild predation rates ofrainbow smelt on young cisco, and thereby decreased age-0
Fig. 6. Chesson’s index of prey selection for walleye (Sander vitreus) caught in Fence Lake in (a) May, (b) June, (c) July, and (d) Au-gust of 2002. Error bars indicate 95% confidence intervals; the dotted horizontal line in each box represents neutral selection.
Fig. 7. Thermal overlap between walleye (Sander vitreus) andcisco (Coregonus artedi; denoted by line with solid circles) andbetween walleye and rainbow smelt (Osmerus mordax; denotedby line with ×s) as observed in vertical gillnet catch from Juneto August 2002 in Fence Lake.
Fig. 8. Estimated consumption of smelt (Osmerus mordax) bywalleye (Sander vitreus) (open bars) and estimates of smelt bio-mass (solid bars) in Fence Lake in each study year from 1982 to2002.
cisco mortality. These results provide strong evidence thatrestoring walleye populations in small lakes will not hinderthe recovery of cisco. Instead, such management may lead topredator-mediated coexistence between cisco and rainbowsmelt.
While predation by walleye may explain the observed de-clines in rainbow smelt in two of the study systems, alterna-tive hypotheses for these declines include recruitment failureresulting from changes in regional climate, or a disease out-break in both Fence and Crawling Stone lakes. We evaluatedthe first alternative hypothesis by examining population dy-namics in Crystal Lake, which is an excellent control systemsince rainbow smelt experience very low predation rates andintraguild competition. Unlike the rainbow smelt populationsin Fence and Crawling Stone lakes, Crystal Lake rainbowsmelt biomass has continued to rise exponentially since theywere detected in 1985. If regional processes had contributedto rainbow smelt recruitment failure in Fence and CrawlingStone lakes, such recruitment variability would likely onlycause short-term fluctuations in rainbow smelt populationdensities (He and LaBar 1994) and would not explain thelonger term patterns we observed. Therefore regional cli-mate was not a likely underlying cause of the observedchanges in rainbow smelt abundances in Fence and CrawlingStone lakes. Based on the cisco catch data from Trout andBig Muskellunge lakes, we also conclude that increases incisco biomass in Fence and Crawling Stone lakes were notattributable to regional processes.
We cannot exclude the possibility that disease outbreakcontributed to the decline in rainbow smelt. However, we didnot observe any visible signs of disease in the Fence andCrawling Stone rainbow smelt populations in 2001 or 2002.In addition, rainbow smelt body condition was higher in2001 and 2002 in Fence Lake than it was prior to 1994, sug-gesting a more healthy population. Our evidence is thereforemost consistent with the hypothesis that selective predation
by walleye caused the observed declines in rainbow smeltpopulation densities in Fence and Crawling Stone lakes.
Management implicationsManaging predatory fish populations may yield several
possible outcomes, including the potential control of harmfulexotic species. Our study lakes represent three distinct sce-narios that are defined by the level of consumption by preda-tory species. Predator-rich Crawling Stone Lake showed themost striking decline in rainbow smelt density. However, theextremely high density of predators in this system, coupledwith the decrease in their prey, may lead to depressedgrowth and recruitment through density-dependent factors(Kitchell and Crowder 1986). This scenario may be accept-able if local management is focused on eliminating smelt inan effort to fully restore declining native planktivore popula-tions. However, fishery managers may be interested in main-taining quality sport fisheries while managing for native fishpopulations. The intermediate walleye density represented inFence Lake appeared to allow rainbow smelt, cisco, andwalleye to coexist and maintain a diverse forage base forwalleye. This situation may represent a balance between na-tive species restoration and high predator growth rates. Joneset al. (1994) found that walleye consumed rainbow smelt al-most exclusively in a Colorado reservoir, and growth in-creased by up to 50% in some age classes. However, therainbow smelt population was not adversely affected bywalleye predation. This was also true in Lake Champlain,where walleye and salmonid species relied heavily on rain-bow smelt, but did not cause a significant decline in the rain-bow smelt population (Kirn and LaBar 1996). However, insmaller oligotrophic lakes, such as Fence Lake, continuedpredation at current rates may further reduce rainbow smeltbiomass. In Lake Michigan, rainbow smelt encountered pre-
Fig. 9. Total consumption by walleye (Sander vitreus) in Fence(open bars) and Crawling Stone (solid bars) lakes from 1986 to2002.
Fig. 10. The apparent relationship between consumption bywalleye (Sander vitreus) and consumption by smelt (Osmerusmordax) in Fence and Crawling Stone lakes (open circles repre-sent observed values). The solid line represents the model SC =70 × e–0.16WC, where SC is consumption by smelt and WC isconsumption by walleye (p < 0.001, r2 = 0.76). The y interceptwas fixed at the estimated consumption rate observed in 2002 inCrystal Lake, where smelt existed in the virtual absence of pred-ators and where they were likely near their carrying capacity.
dation rates comparable to those in Fence Lake and subse-quently declined to very low levels (Kitchell and Crowder1986). Continued monitoring of rainbow smelt populationsis needed to fully examine the sustainability of rainbowsmelt under current predatory conditions in Fence andCrawling Stone lakes.
In Crystal Lake, rainbow smelt appear to show an expo-nential population growth pattern that has nearly eliminatedthe native yellow perch. Because predator abundance is ex-tremely low, rainbow smelt will likely increase until densitydependence and resource limitation lead to population de-clines or stabilized densities.
Our study systems represent contrasting food web config-urations and resultant population dynamics. We thereforepropose several options for fishery managers who face de-clining native fish populations caused by rainbow smelt.Management objectives should incorporate predator con-sumption rates on prey species as a factor when formulatingmanagement prescriptions. Our findings suggest thefollowing: (i) rainbow smelt populations may decline to lowlevels and cisco may recover when walleye consume58 kg·ha–1·year–1 of prey; (ii) walleye consumption rates atapproximately 12 kg·ha–1·year–1 may promote a diverse for-age base but allow native cisco to recover; and (iii) un-checked rainbow smelt populations will likely growexponentially and cause native species to decline (Hrabik etal. 2001). Our results are likely specific to situations inwhich walleye depend on rainbow smelt for a substantialpart of their diet, and the attributes of the lakes are similar tothose observed in this study. Although walleye can be signif-icant predators on rainbow smelt and alewife (Porath et al.2003), they may not be as effective at controlling all exoticforage fishes. Ogle et al. (1996) showed that walleye did notprey upon ruffe (Gymnocephalus cernuus) at high enoughrates to control their abundances in the western arm of LakeSuperior. Changes in the food web of Fence and CrawlingStone lakes indicate that walleye predation can indirectly al-low cisco populations to recover. As a result of widespreadstocking of walleye by management agencies in the upperGreat Lakes region, the applicability of such strategies repre-sents a mechanism to prevent rainbow smelt establishmentand restore threatened populations of cisco in their southernranges. Fishery managers will need to identify the food webconfiguration and predator consumption regime that bestsuits the objectives for the ecosystems within their jurisdic-tion.
Acknowledgements
This study was performed at the University of Wisconsin,Center for Limnology, Trout Lake Research Station. Numer-ous individuals and entities contributed assistance through-out this study. We thank the Great Lakes Indian Fish andWildlife Commission, the Lac Du Flambeau tribal hatchery,John Pastor at the University of Minnesota, Duluth, GregSass and Brian Roth at the University of Wisconsin, Madi-son, Tim Kratz, Pam Faschingbauer and John Vehrs at theTrout Lake Research Station, Steve Gilbert at the Woodruff,Wisconsin DNR, and Bill Swenson at the University of Wis-consin, Superior. Funding for this project was provided bythe Sand County Foundation, Bradley Fund for the Environ-
ment, the North Temperate Lakes Long-Term EcologicalResearch Program (funded by grant DEB 0217533) and theUniversity of Minnesota Duluth Graduate School.
References
Beisner, B.E. Ives, A.R., and Carpenter, S.R. 2003. The effects ofan exotic fish invasion on the prey communities of two lakes. J.Anim. Ecol. 72: 331–342.
Brooks, J.L., and Dodson, S.I. 1965. The effect of a marineplanktivore on lake plankton illustrates theory of size, competi-tion, and predation. Science (Wash., D.C.), 150: 707–714.
Bryan, S.D., Soupir, C.A., Duffy, W.G., and Freiburger, C.E. 1996.Caloric densities of three predatory fishes and their prey in LakeOahe, South Dakota. J. Freshw. Ecol. 11: 153–161.
Carpenter, S., and Kitchell, J.F. 1988. Consumer control of lakeproductivity — large-scale experimental manipulations revealcomplex interactions among lake organisms. BioScience, 38:764–769.
Chesson, J. 1983. The estimation and analysis of preference and itsrelationship to foraging models. Ecology, 64: 1297–1304.
Cox, S.P., and Walters, C.J. 2002. Modeling exploitation in recre-ational fisheries and implications for effort management on Brit-ish Columbia rainbow trout lakes. N. Am. J. Fish. Manag. 22:21–34.
Cox, S.P., Martell, S.J.D., Walters, C.J., Essington, T.E., Kitchell,J.F., Boggs, C., and Kaplan, I. 2002. Reconstructing ecosystemdynamics in the central Pacific Ocean, 1952–1998. I. Estimatingpopulation biomass and recruitment of tunas and billfishes. Can.J. Fish. Aquat. Sci. 59: 1724–1735.
Crowder, L.B. 1980. Alewife, rainbow smelt and native fishes inLake Michigan: competition or predation? Environ. Biol. Fishes,5: 225–233.
DeVries, D.R., and Frie, R.V. 1996. Determination of age andgrowth. In Fisheries techniques. Edited by B.R. Murphy andD.W. Willis. American Fisheries Society, Bethesda, Md.pp. 483–512.
Evans, D.O., and Loftus, E.H. 1987. Colonization of inland lakesin the Great Lakes region by rainbow smelt, Osmerus mordax:their freshwater niche and effects on indigenous fishes. Can. J.Fish. Aquat. Sci. 44(Suppl. 2): 249–266.
Franzin, W.G., Barton, B.A., Remnant, R.A., Wain, D.B., andPagel, S.J. 1994. Range extension, present and potential distri-bution, and possible effects of rainbow smelt in Hudson Baydrainage waters of Northwestern Ontario, Manitoba and Minne-sota. N. Am. J. Fish. Manag. 14: 65–76.
Hansen, M.J. 1994. The state of Lake Superior in 1992. Gt. LakesFish. Comm. Spec. Publ. No. 94-1.
Hanson, P.C., Johnson, T.B., Schindler, D.E., and Kitchell, J.F.1997. Fish bioenergetics 3.0. University of Wisconsin Sea GrantInstitute, Madison, Wisc. Tech. Rep. WISCU-T-97-001.
He, X., and LaBar, G.W. 1994. Interactive effects of cannibalism,recruitment, and predation on rainbow smelt in Lake Champlain.A modeling synthesis. J. Gt. Lakes Res. 20: 289–298.
Hrabik, T.R., and Magnuson, J.J. 1999. Simulated dispersal of ex-otic rainbow smelt (Osmerus mordax) in a northern Wisconsinlake district and implications for management. Can. J. Fish.Aquat. Sci. 56(Suppl. 1): 35–42.
Hrabik, T.R., Magnuson, J.J., and McLain, A.S. 1998. Predictingthe effects of rainbow smelt on native fishes in small lakes: evi-dence from long-term research on two lakes. Can. J. Fish.Aquat. Sci. 55: 1364–1371.
Hrabik, T.R., Carey, M.P., and Webster, M.S. 2001. Interactions be-tween young-of-the-year exotic rainbow smelt and native yellow
perch in a northern temperate lake. Trans. Am. Fish. Soc. 130:568–582.
Johnson, B., and Goettl, J.P. 1999. Food web changes over fourteenyears following introduction of rainbow smelt into a ColoradoReservoir. N. Am. J. Fish. Manag. 19: 629–642.
Johnson, B., Luecke, C., Stewart, S., Staggs, M., Gilbert, S., andKitchell, J.F. 1992. Forecasting effects of harvest regulationsand stocking of walleyes on prey fish communities in LakeMendota, Wisconsin. N. Am. J. Fish. Manag. 12: 797–807.
Jones, M.S., Goettl, J.P., and Flickinger, S.A. 1994. Changes inwalleye food habits and growth following a rainbow smelt intro-duction. N. Am. J. Fish. Manag. 14: 409–414.
Kirn, R.A., and LaBar, G.W. 1996. Growth and survival of rainbowsmelt, and their role as prey for stocked salmonids in LakeChamplain. Trans. Am. Fish. Soc. 125: 87–96.
Kitchell, J.F., and Crowder, L.B. 1986. Predator–prey interactionsin Lake Michigan: model predictions and recent dynamics. En-viron. Biol. Fishes, 16: 205–211.
Kitchell, J.F., Stewart, D.F., and Weininger, D. 1977. Applicationsof a bioenergetics model to yellow perch (Perca flavescens) andwalleye (Stizostedion vitreum). J. Fish. Res. Board Can. 34:1922–1935.
Kitchell, J.F., Evans, M.S., Scavia, D., and Crowder, L.B. 1988.Food web regulation of water quality in Lake Michigan: reportof a workshop. J. Gt. Lakes Res. 14: 109–114.
Kitchell, J.F., Cox, S.P., Harvey, C.J., Johnson, T.B., Mason, D.M.,Schoen, K.K., Aydin, K., Bronte, C., Ebener, M., Hansen, M.,Hoff, M., Schram, S., Schreiner, D., and Walters, C.J. 2000.Sustainability of the Lake Superior fish community: interactionsin a food web context. Ecosystems, 3: 545–560.
Loftus, D.H., and Hulsman, P.R. 1986. Predation on larval lakewhitefish (Coregonus clupeaformis) and lake herring(Coregonus artedi) by adult rainbow smelt (Osmerus mordax).Can. J. Fish. Aquat. Sci. 43: 812–818.
Magnuson, J.J., Bowser, C.J., and Kratz, T.K. 1984. Long-TermEcological Research (LTER) on Northern Temperate Lakes inthe United States. Verh. Int. Verein. Limnol. 22: 533–535.
Magnuson, J.J., Benson, B.J., and McLain, A.S. 1994. Insights onspecies richness and turnover from long-term ecological re-search: fishes in north temperate lakes. Am. Zool. 34: 347–351.
Myers, R.A., and Worm, B. 2003. Rapid worldwide depletion ofpredatory fish communities. Nature (Lond.), 423: 290–283.
Ogle, D.H., Selgeby, J.H., Savino, J.F., Newman, R.M., and Henry,M.G. 1996. Predation on ruffe by native fishes of the St. LouisRiver estuary, Lake Superior, 1989–1991. N. Am. J. Fish.Manag. 16: 115–123.
Porath, M.T., Peters, E.J., and Eichner, D.L. 2003. Impact of ale-wife introduction on walleye and white bass condition in LakeMcConaughy, Nebraska, 1980–1995. N. Am. J. Fish. Manag.23: 1050–1055.
Post, J.R., Sullivan, M., Cox, S.P., Lester, N.P., Walters, C.J., Par-kinson, E.A., Paul, A.J., Jackson, L, and Shuter, B.J. 2002. Can-ada’s recreational fishery: the inevitable collapse? Fisheries, 27:6–17.
Ricker, W.E. 1975. Estimation of survival rate and mortality ratefrom age composition. In Computation and interpretation of bio-logical statistics of fish populations. Can. J. Fish. Aquat. Sci.Bull. No. 191. pp. 29–73.
Rudstam, L.G., Lathrop, R.C., and Carpenter, S.R. 1993. The riseand fall of a dominant planktivore: direct and indirect effects onzooplankton. Ecology, 74: 303–319.
Rudstam, L.G., Hansson, S., Lindem, T., and Einhouse, D.W.1999. Comparison of target strength distributions and fish densi-ties obtained with split and single beam echo sounders. Fish.Res. 42: 207–214.
Sanderson, B., Hrabik, T.R., Magnuson, J.J., and Post, D.M. 1999.Cyclic dynamics of a yellow perch (Perca flavescens) popula-tion in an oligotrophic lake: evidence for the role of intraspecificinteractions. Can. J. Fish. Aquat. Sci. 56: 1534–1542.
