Fishing down then up the food web of an invaded lakeErin S. Dunlopa,1, Daisuke Gotob,2, and Donald A. Jacksonb

aAquatic Research and Monitoring Section, Ontario Ministry of Natural Resources and Forestry, Peterborough, ON K0L 2G0, Canada; and bDepartment ofEcology and Evolutionary Biology, University of Toronto, Toronto, ON M5S 3B2, Canada

Edited by Alan Hastings, University of California, Davis, CA, and approved August 16, 2019 (received for review May 13, 2019)

Analysis of commercial catches reveals a serial depletion of someoceanic fish stocks over time, resulting in fisheries focusing onincreasingly smaller species closer to the base of the food chain.This effect, described as fishing down the marine food web, isobserved when the trophic level of the catch declines over time,raising concerns about the ecosystem impacts of fishing. Fresh-water systems also experience harvest, yet do not appear tocommonly show the same fishing down response perhaps becausetime series are too short to witness early depletions, fishing isoften recreational, or other factors like stocking and invasivespecies influence patterns. Here we make use of extensive catchrecords from Lake Simcoe dating back to the 1860s, to examine iffishing down effects are observed in this highly exploited Canadianinland lake. We measured 2 commonly used indicators from catchdata, mean trophic level (MTL) and fishing-in-balance (FiB), andcompared trends between a historical period dominated by com-mercial fishing and a contemporary period when commercial fishingceased and recreational fishing effort increased. We found a strik-ing difference between the 2 time periods, with MTL (and to someextent FiB) declining during commercial fishing but increasingduring recreational fishing. However, indicators either increased ordecreased due to invasive species and increased due to stocking. Weshow that while declining MTL can occur in a freshwater lake, thetrajectory can be altered by a switch to recreational fishing, as wellas stocking and invasive species.

Great Lakes | angling | lake trout | Bythotrephes | dreissenid mussels

Humans have been harvesting aquatic resources for centuries,with historical records showing a long history of associated

ecosystem impacts (1, 2). Although most ecological studies onlydate back a decade or 2 at most, historical records of fisherieslandings can span half a century or more and provide valuableinsights that can be used to inform conservation and manage-ment efforts (3, 4). In this manner, analysis of select fishery catchdata has revealed a serial depletion of some oceanic fish stocksover time, resulting in fisheries focusing on increasingly smallerspecies closer to the base of the food web (5). This effect, de-scribed as fishing down the marine food web, arises if the biomassof long-lived, large, and piscivorous species declines more rapidlythan smaller species with higher natural mortality (5). Over time,catches can switch from being dominated by top predators to anincreased prevalence of planktivorous fish or invertebrates. De-clining trophic levels of fisheries catches have been observed inseveral marine systems, where it has become apparent that in-dustrial fishing can impact ecosystems in ways that underminelong-term sustainability of fisheries resources (6, 7).Freshwater fish populations can also experience high rates of

harvest pressure, yet it is unclear whether the same successionalpatterns in species catches are expected as we see in some ma-rine environments. Commercial fishing occurs in freshwaters, forexample, in the Laurentian and African Great Lakes (8, 9) andseveral inland lakes in Europe (10), but recreational fishing is thepredominant form of harvest in many inland systems world-wide (11). Indigenous and sustenance fishing are widespread infreshwater systems but are typically smaller in scale (8). Harvestpressure from recreational fishing can be high and unsustain-able, resulting in stock depletion just as is the case for commercial

exploitation (12). Many anglers prefer to catch larger piscivorespecies, leading to the potential for depletions of these higher-trophic level species over time. However, gear, regulations, andpractices can differ between commercial and recreational fisheries,potentially leading to different impacts and dynamics over time.Despite high exploitation pressure of some freshwater fisher-

ies, fishing down the food web does not appear to be occurring aswidely in these systems. For example, 5 shallow eutrophic fresh-water lakes in China, known to be heavily polluted and impactedby habitat alteration, showed no significant trends in mean trophiclevel of fisheries catch over a 60-y period (13). In a study by Paulyet al. (14) of aquatic ecosystems in Canada, freshwater fisheriesdid not show the declining trophic level in landings that wereobserved in marine fisheries on the west and east coast. Potentialreasons given by Pauly et al. (14) for this different response werethe prevalence of fish stocking in many inland lakes and that timeseries in inland systems might not date back far enough to captureearly fisheries’ impacts. Owing to their smaller size and increasedaccessibility, many freshwater systems might have experiencedstock depletion long ago (e.g., with European settlement in NorthAmerica), whereas emerging technology has only more recentlypermitted fishing fleets to exploit remote marine habitats. An-other factor might be that many recreational anglers harvestspecies with smaller body sizes (e.g., panfish); these smaller spe-cies are often more common, are easy to catch, and have superiortaste or lower contaminant loads. It could also be that recreationalfishing in inland systems is self-regulating, with anglers switchingto fishing different lakes or rivers when catch rates decline, pos-sibly obscuring depletions (12). Finally, catch-and-release, often oflarge piscivores, is common in many recreational fisheries (15),

Significance

Fishing down the food web occurs in oceans when the meantrophic level (MTL) of the fisheries’ catch declines over time.Such a trend arises if fisheries successively deplete higher-trophic level species like top predators, moving on to harvestspecies closer to the base of the food web such as small fishand invertebrates. Freshwater fisheries have not shown thesetrends. We analyzed 148 y of catch records for an exploitedlake, revealing that MTL declined during years dominated bycommercial fishing but increased during the contemporaryphase of recreational fishing. Recently, MTL was altered byinvasive species and stocking. Thus, while MTL declined his-torically in this lake, the switch to recreational fishing andother factors altered the trajectory.

Author contributions: E.S.D. and D.A.J. designed research; E.S.D. and D.G. performedresearch; E.S.D. and D.G. analyzed data; and E.S.D., D.G., and D.A.J. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

Published under the PNAS license.1To whom correspondence may be addressed. Email: erin.dunlop@ontario.ca.2Present address: Demersal Fish Research Group, Institute of Marine Research, 5005Bergen, Norway.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1908272116/-/DCSupplemental.

First published September 16, 2019.

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thus potentially changing harvest patterns relative to commercialfisheries.In addition to harvest, freshwater systems experience pressure

from many other stressors such as species invasions and habitatalteration. These stressors impact marine fisheries as well (16)but could have more potent or visible effects in freshwater sys-tems owing to the smaller size, proximity to human development,and accessibility of lakes and rivers. This makes detecting rec-reational fishing impacts challenging, explaining why collapses infreshwater systems may be invisible (17). The effects of otherstressors might play a more prominent role in shaping freshwaterfish communities and therefore lead to different cumulativechanges over time in catches than would be observed in marinesystems. Invasive species can disrupt food web structure andcause trophic level changes of species within lake ecosystems (18,19). However, no previous study we are aware of has consideredthe effect that invasive species could have on trends in catch-based indicators.Here we use a 148-y time series of an intensively harvested

inland lake to examine whether catch indicators show a patternconsistent with fishing down the food web. We estimated 2commonly used indicators, the mean trophic level (MTL) andfishing-in-balance (FiB) metric (20) from catch records datingback to the 1860s. MTL is derived from species-specific catch dataand diet information. FiB measures total harvest offset againstMTL, relative to a baseline. FiB is meant to account for increasesin catch that might occur when fisheries shift to catching lowertrophic level, typically more productive species. FiB values below0 are interpreted as a fishery being out of balance (20).The study system, Lake Simcoe, is a large (744 km2) inland

lake near Toronto, Canada, and has experienced 2 distinct har-vesting phases: a historical period of commercial fishing and acontemporary period when commercial fishing ceased and rec-reational fishing pressure rose (21). The lake has also experiencedpressures from land use change (22) and invasive species (23–25)and has been stocked as part of management efforts to restoresport fish populations. The primary objective of our study is todetermine if indicator trends differ among the commercial andrecreational fishing periods. Our prediction is that the com-mercial fishing period will show signs of fishing down the foodweb given that our time series dates back far enough to captureearly depletions of large piscivores. In contrast, we predict thatthe recreational fishing period will not show this downward trendin MTL; this is because Lake Simcoe would have already expe-rienced depletions from the previous era of commercial fishingand because recreational fishing pressure is expected to poten-tially differ (as described above) from commercial fishing,making trend detection difficult. The second objective is to ex-amine the potential for species invasions and the stocking offish to affect indicator trends. For this objective, we focused oncontemporary (i.e., post-1980) species invasions and stockinglevels due to data availability. We predict species invasions willchange indicator values by altering the food web and consumerdiets, but the direction of change is unclear because it might de-pend on the invasive species in question. We furthermore predictstocking to increase indicator values because it allows the stockedspecies biomass to remain artificially high in the lake and providesanglers an opportunity to catch more high-trophic level fishes.Historical fishery landings data for Lake Simcoe were collected

from the Ontario government (21) and used to calculate the MTLand FiB indicators (26) for 1868 to 1952. For the recreationalfishing data, catch estimates were based on standardized creelsurveys conducted on the lake since 1961 by the Ontario Ministryof Natural Resources and Forestry (MNRF) (27). For our recre-ational fishery indicator values, we used catch data from the winterice fishery, which accounts for, on average, 76% of the effort and75% of the catch (based on 1981 to 2011 creel surveys) for the

lake. The winter creel survey is a lake-wide, extensive roving an-gler survey conducted near annually.To examine the contribution of contemporary species inva-

sions and stocking, we used detailed, time-varying stomachcontent data collected by the MNRF in 1981 to 2015. For in-vasive species, recreational fishing indicators were separated into3 time periods: 1) pre-1991; 2) 1992 to 2003, when spiny waterflea (Bythotrephes longimanus) and zebra mussels (Dreissenapolymorpha) became established; and 3) 2004 to 2015, whenquagga mussels (Dreissena bugensis) and round goby (Neogobiusmelanostomus) became established. We then recalculated theindicators using diet data from pre-1991 and compared them tothe values calculated using the actual (i.e., invaded), time-varyingdiet information. For stocking, the indicators were reestimatedby removing stocked lake trout (Salvelinus namaycush) and lakewhitefish (Coregonus clupeaformis) from the fishery catches(distinguishable by fin clips).We also estimated indicators from fishery-independent data

available from 2003 to 2015. Fishery-independent survey datacan provide a more accurate reflection of trends in the under-lying fish community (28), rather than focusing on how fisherycatches change over time. The fishery-independent data werefrom an annual index gill netting survey conducted by MNRF.

ResultsThere were distinct trends through time in both commercialfishery landings and indicator values. Commercial landings showed2 distinct periods, 1868 to 1902 and 1911 to 1952, separated by lowreported landings during 1903 to 1910 (Fig. 1A). Patterns in totalcatch were as follows: 1) an initial increase for the first 40 to 50 y;2) a low landings period in early 1900s; 3) a rapid increase inlandings to a peak in 1910 to 1920s; and 4) declining catches overthe course of about 25 y, with very low levels by the 1950s. In thefirst phase of commercial fishing, landings were more species di-verse and consisted of many large piscivores including lake stur-geon (Acipenser fulvescens), muskellunge (Esox masquinongy),smallmouth bass (Micropterus dolomieu), walleye (Sander vitreus), andlake trout. The second phase was dominated by fewer species,and those tended to be lower-trophic level species (i.e., benthivoresand herbivores) such as white sucker (Catostomus commersonii) andnonnative common carp (Cyprinus carpio). Some large, apex pred-ators such as lake sturgeon and muskellunge virtually disappearedfrom the landings by the beginning of the 1900s.Recreational fishing catches showed distinct changes through

time (Fig. 1B). Total catches sharply rose at the beginning of thetime series, declined, and then rose again, reaching a peak in thelater 20 y, exceeding total harvest experienced under commercialfishing. Lake whitefish dominated catches for the first 2 decadesbut then declined as smaller prey fish (yellow perch [Perca flavescens],cisco [Coregonus artedi], and rainbow smelt [Osmerus mordax])increased. During the 1990s, lake whitefish and lake trout catchesincreased, whereas cisco catch declined to record low levels (notethe cisco fishery was closed in 2001 because of population collapse).One of the most obvious trends is that over the course of the timeseries, yellow perch increased and is now the most prevalent speciesin the catch.MTL of the commercial fishery declined over the course of

our time series, culminating in a total drop of over 1 trophic level(Fig. 2). The commercial fishing FiB indicator was more stable,fluctuating around 0 before declining toward the end of the timeseries. For the recreational catches, MTL showed a gradual in-creasing trend but overall changed by only a fraction of a trophiclevel. There was a slight drop in 2003 for the recreational MTL,that is more obvious when examining trends on a different scale(Fig. 3). The recreational fishing FiB was close to 0 for about 10 y,before gradually increasing and then showing a slight declinein 2003 similar to the MTL. Statistical analysis of the trends(described in SI Appendix) supports our observations, detecting a

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significant decline in MTL and an initially stable but then sig-nificant decline in FiB during commercial fishing. A significantincreasing trend was detected between the 1970s and 2002 and inthe late 1980s for MTL and FiB, respectively (SI Appendix).Removing several recent invasive species had an obvious effect

on indicator values (Fig. 3). Removing invasives caused a lowerMTL and FiB for 1992 to 2002 but an increase in MTL and FiBvalues after 2012. Removing stocked fish from catches also hadan effect, lowering both the MTL and FiB indicators (Fig. 3).MTL measured from the fishery-independent data revealed

little trend through time, varying between 2.4 and 2.9 during2003 to 2015 (SI Appendix, Fig. S1). Values were within a verysimilar range to the recreational fishing-based indicators and theeffect of removing invasive species from MTL values (SI Ap-pendix, Fig. S1) was in the same direction as that observed withthe recreational fisheries data (Fig. 3).

DiscussionThe 148-y time series of Lake Simcoe fisheries revealed distinctdifferences in the trajectory of indicators between commercialand recreational fishing eras. Between 1860 and the end of most

commercial harvest in the 1950s, the MTL of the catch declinedby over 1 trophic level, averaging about a 0.12 drop per decade.This decline is slightly faster than the range published for Ca-nadian marine fisheries (0.03 to 0.1 per decade), which wasreported as being similar to global trends (14). Our results showthat an inland lake can undergo declines in MTL at a similar oreven greater rate to those reported in marine systems, a patternconsistent with the effects of fishing down the food web (5–7).The FiB indicator from commercial landings was more stable

initially than MTL, until notable declines occurred between the1940s and 1960s. A stable FiB might occur if increasing catchescompensate for declining trophic level, an observation in somecommercial marine fisheries (20). However, the shift to a decliningFiB in the 1940s to 1950s could signal that commercial fishing wasno longer in balance (20), and stocks were declining as trophiclevel of the catch continued to decrease.The trajectory of the 2 indicators reversed as the Lake Simcoe

fishery transitioned from a commercial fishery to one dominatedby recreational fishing. The increase was more subtle, however,with MTL changing by about 0.3 trophic levels over the 54-yperiod of recreational fishing. Thus, the rate of decline in trophic

Fig. 1. (A) Commercial fisheries landings and (B) recreational fishing catches for Lake Simcoe.

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level during commercial fishing was about twice the rate of in-crease during recreational fishing. Increasing MTL and FiB inother fisheries have been described as being consistent withan expanding fishery (29). Such a trend might also occur if theoverall harvest pressure declined, different species were tar-geted, or harvest practices changed in other ways when the shiftoccurred from commercial to recreational fishing, allowing somerecovery of MTL between the 1960s and 2000s. The switch froma more substantial and rapid decline to an increase in trophiclevel implies potential higher sustainability of the recreationalfishery compared to the commercial fishery. Although we lackdirect estimates of harvest rates, harvest pressure was likelyhigher during the commercial fishing period, most notably at thebeginning of the time series when fishing was conducted with fewrestrictions. Commercial fishing used gear such as gill netting,night spear fishing, and baited hooks and was often conductedduring seasons when fish were most vulnerable to harvest, suchas during spawning (30); these practices meant that a high bio-mass of fish could be removed. When recreational fishing effortbegan to increase, management agencies had realized the im-portance of implementing regulations to ensure the sustainabilityof the fishery (30). The contrasting pattern between commercialand recreational fishing trends offers one explanation for whyCanadian inland lakes, dominated by recreational fishing, didnot show the same declining MTL observed in marine fisheriesexperiencing commercial fishing (14).A closer look at species composition of the harvest provides

information that aids interpretation of the indicator trends.During the initial stages of the commercial fishing time series,harvest focused on native predators such as lake trout, lakewhitefish, and smallmouth bass, as well as several species not

commonly observed today such as muskellunge and walleye. Inthis initial phase, harvest was spread out among a greater di-versity of species, compared with the second phase of commer-cial harvest. The pronounced shift, from a higher diversity of toppredators to an increased dominance by fewer species (includingsucker and carp which feed on more invertebrates and plants),would contribute to the lowering of MTL. When recreationalfishing took over, harvest was mainly dominated by lake white-fish, followed by a subsequent shift to harvest spread more evenlyamong more species including a top predator, lake trout. Althoughthese trends reflect changes in underlying species abundances tosome extent, various other extrinsic and intrinsic factors wouldhave contributed. Changes in regulations, angler preferences andbehavior, technology and gear, fuel costs, and environmentaleffects will affect the fishery catch composition.MTL of the catch is influenced not only by the species com-

position of the catch but also by the diet, and thus the trophiclevel, of the consumers that make up the catch. In Lake Simcoe,changes in trophic level were influenced by both of these factors.Large shifts in species composition of the catch occurred, asdescribed above, but there have also been shifts in diet andtrophic level (SI Appendix, Table S2) of various fish species overtime. Invasive species, in particular, affected both catch com-position and diets. Most obviously, the introduction of commoncarp led the way to the establishment of a commercial fishery forthe species in the early 1900s which dominated catches for manydecades. Rainbow smelt, a small pelagic planktivore, was firstobserved in the lake in 1962 and quickly appeared in the dietof top predators such as lake trout, potentially displacing cisco.Rainbow smelt also became a component of both commercialand recreational catches. More recently, a successive series of

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Fig. 2. Trends in catch-based indicators, (A and B) MTL and (C and D) FiB, for commercial and recreational fishing periods on Lake Simcoe. Red horizontal lineindicates FiB = 0.

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invasions further impacted the lake’s food web, including es-tablishment of spiny water flea, dreissenid mussels, and roundgoby (24, 30)—these species are not fished, so their impactswould occur by changing diets or more indirectly by affectingabundances of fished species.Interestingly, different phases of the recent species invasions

were associated with opposing trends in the MTL. In the early1990s when spiny water flea and zebra mussels invaded, the MTLcalculated with invasive species was overall higher than withoutinvasive species (Fig. 3). The higher MTL we detected with thisset of invaders was caused by shifts in diet that changed trophiclevels of the consumers making up the catch. Spiny water flea(a predatory cladoceran) was observed to elevate trophic positionof zooplankton communities and cisco in lakes (31), which couldexplain the pattern we found. Elevated trophic position of zoo-plankton and cisco in Bythotrephes-invaded lakes is attributed toshifts in the zooplankton community from herbivorous cladoc-erans to omnivorous or predatory copepods (31).The species invasions occurring in the 2000s had the opposite

effect to those in the preceding decade and appeared to con-tribute to a lowering of MTL. After round goby and quaggamussels became established in Lake Simcoe post-2004, MTLdeclined as diets shifted. For both the fishery-independent andfishery-dependent data, the MTL measured with invasive speciesswitched to being lower after 2004 than the MTL measuredwithout invasive species. A declining MTL might be in part dueto increasing dreissenids in the diet of Lake Simcoe fishes. Forexample, dreissenids began appearing in the diet of Lake Simcoelake trout in the 2000s (32), and a prominent shift to dreissenidconsumption occurred for lake whitefish in nearby Lake Huron(33). In Lake Simcoe, delta N15, a measure of trophic level,showed a general decline in various fishes and invertebrates

between the 1980s and 2009, although only a few species showeda statistically significant change (23). It is not possible to elimi-nate all effects of the species invasions on the food web of LakeSimcoe by simply removing them from the diet. However, ourresults do offer an explanation of why the indicators were trendinghigher toward the end of the 1990s and then shifted lower in the2000s—i.e., invasive species might have changed the trajectorybecause of impacts to the diet of fished species. In the immediatefuture, we predict a reversal toward higher MTLs if lake whitefishswitch to consuming round goby as they have in Lake Huron (34),which is expected to increase their trophic position relative towhen they were eating more dreissenids.Pauly et al. (14) suggested that stocking of inland lakes might

explain why fishing down the food web was not observed in thosesystems. We found evidence that stocking of lake trout and lakewhitefish contributed to higher MTL and FiB in the catch.Stocking of various species has occurred in Lake Simcoe forspecies rehabilitation or to create fishing opportunities (21).Lake trout and lake whitefish have been the most intensivelystocked and are the only stocked fish that are routinely capturedin the recreational fishery, while other species have been stockedmore infrequently or in much fewer numbers (SI Appendix, TableS1). When we removed stocked lake trout and lake whitefishfrom the recreational catches, the resultant MTL was lower thanthe observed harvest with both wild and stocked fish present.Stocking allows trophic levels to remain artificially high becausethe stocked species (which are generally higher in trophic level)are added to the system annually, whereas the numbers of wildfish of those same species would have been lower. The higherMTL would only have come about through the appearance ofstocked fish in the catch, rather than by changes in diet.

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Another reason cited for the lack of a fishing down effect inCanadian lakes is that the time series in those systems did notdate back far enough to include initial depletions arising withEuropean settlement and expanding development (14). Our timeseries, capturing 148 y of commercial and recreational harvest,shows the long history of exploitation experienced by an inlandlake. By the time recreational fishing became prominent on LakeSimcoe in the past 50 y, species such as muskellunge and lakesturgeon had become rare. Although datasets are few, manyother lakes around the world have long histories of exploitationof at least a century or more (10, 16, 35), including lakes in NorthAmerica that have similar timelines of European settlement andfishery stock depletions (8, 36). These stock depletions have in-cluded reductions in abundances of large, native predators (37).Our study shows how far back changes in fishery catch compo-sition can occur in lakes and that commercial and recreationalfishing spanning decades are associated with vastly differentindicator trends.Biases associated with interpreting fishery landings data can be

present and lead to discrepancies between MTL of the catch andthe underlying status of species in the ecosystem (28, 38, 39). ForLake Simcoe, limitations in the data are most likely for thecommercial fishing time series. The commercial catch data werefrom reported landings and do not include illegal and unlicensedcatches (21). We lacked diet data for the commercial time seriesand instead used FishBase to provide estimates of trophic posi-tion. Some recreational fishing occurred prior to the 1960s whenour winter creel time series began (21). Finally, the recreationalfishing data used to estimate indicators were catches (i.e., withsome fish released) and are not entirely comparable to thelandings data used for the commercial fishing period. With thoselimitations in mind, the tapering of commercial fishing in the1940s and the 4-fold increase in angler effort between the 1960sand present (SI Appendix, Fig. S2) still represent a stark contrastbetween time periods and show the drastically shifting fisheriesin Lake Simcoe. Furthermore, many of the above biases are atleast consistent within each time series.Indicators measured from fishery-independent data (e.g., us-

ing standardized monitoring programs) do not suffer from someof the biases associated with interpreting recreational and com-mercial catch data and may provide a better understanding ofunderlying trends in the ecosystem or true species abundances(28). On Lake Simcoe, a lake-wide, depth-stratified gill-nettingsurvey began in 2003 to monitor fish populations in the lake,allowing us to estimate MTL using fishery-independent data.MTL values were in a similar range to those estimated from therecreational fishing data, and removal of invasive species fromthe analysis caused the same direction of change (SI Appendix,Fig. S1). However, the short time series of fishery-independentdata does not permit a more complete comparison. As such, ourfisheries-derived indicators do not show how fishing alone hasimpacted fish populations and the food web. Indeed, the lake hasbeen impacted by many stressors, including land use change andpoor water quality, that have affected fish populations (40). In-stead, the fishery-based indicators represent the combined ef-fects of a number of factors on fisheries catch, revealing adeclining MTL in an inland lake similar to that observed inmarine systems and a switch in direction of indicators when ex-ploitation changes from a commercial to a recreational fishery.Our long time series, capturing a shift from commercial to

recreational fishing, offers insights that can be applied to manyother freshwater and marine systems. First, our study confirmsthat commercial fishing is associated with similar fishing downtrends across systems. There is nothing unique to Lake Simcoebeing an inland lake that prevents the types of depletions ob-served in marine commercial fisheries. Second, our study showsthat fishing down trends are not always expected if harvestpressure comes predominately from recreational fishing. Many

inland lakes around the world are presently only harvested viarecreational fishing and, thus, might not show declining MTL asin commercially fished systems. Third, our analysis shows howother factors—in this case invasive species and stocking—can af-fect trends in catch-based indicators, warranting caution in otherstudies when attributing trends solely to the effects of fishing.Stocking to enhance recreational fishing or for stock rehabilita-tion occurs globally (41), while the introduction of nonnativespecies continues to be among the top threats to freshwater bio-diversity (42). Finally, in cases where commercial fishing ceases,our study suggests that recovery of MTL from past fishery de-pletions may be possible even while recreational fishing expands.If this recovery occurred in Lake Simcoe, an intensively fished lakein close proximity to large urban populations, it is likely possibleelsewhere.

Materials and MethodsFollowing Pauly et al. (26), mean trophic level �Ty of fishery landings in yeary is given by

�Ty =

Pni=1Ti,y ·Hi,yPn

i=1Hi,y,

where Ti,y and Hi,y are trophic level and catch, respectively, of speciesi in year y. Fishing-in-balance FiBy of fishery landings in year y is given by

FiBy = logHy ·�1E

��Ty

− log

"H0 ·

�1E

��T0#,

where Hy is total catch of all species considered in year y and H0 and �T0 aretotal catch of all species considered and mean trophic level, respectively, inthe first year of the time series (here 1868). Trophic efficiency E betweentrophic levels in lakes varies from 5 to 15%; we assume E is 10% followingother studies (43).

Commercial Fishing Period (1868 to 1952). Annual commercial landings recordsfor licensed commercial fishers on Lake Simcoe were compiled from archivesof the MNRF (also reported in ref. 21). Commercial catch indicators werecalculated from reported landings for the following species: lake trout, lakewhitefish, cisco, lake sturgeon, white sucker, muskellunge, yellow perch,smallmouth bass, walleye, common carp, and channel catfish (Ictaluruspunctatus). Trophic level Ti,y of exploited fishes was obtained from FishBase(www.fishbase.ca/) for the commercial fishing time series because no dietdata were available for Lake Simcoe prior to 1975 (SI Appendix, Table S2).

Recreational Fishing Period (1961 to 2015). Winter recreational catch datawere obtained from annual lake-wide, roving creel surveys conducted since1961 by the MNRF (27). The creel survey has a random stratified samplingdesign and is conducted by agency staff that visit and interview anglersfishing on the ice. Catch data and biological samples are collected. Special-ized agency software, FISHNET (44), was used to estimate annual species-specific catch, standardized to a 50-d survey period to account for variabilityin ice cover duration. For indicator catch estimates, we used the 5 mostcommon species captured, accounting for >99% of the catch: lake trout,lake whitefish, cisco, rainbow smelt, and yellow perch. We estimated annualcatches in biomass by multiplying annual catches in numbers for each ageclass and species by the annual age-specific mean mass of that species caughtby anglers. For each species, total catch in biomass (Hi,y) was estimated bysumming across age classes. In some years, body mass was not collected forindividual fish, and we estimated mean fish mass by linear interpolationamong adjacent years with data. Catch estimates (both killed and releasedfish) were used to estimate recreational indicators because killed fish werenot separately recorded before the 1980s.

Trophic level of each fish species Ti,yfor the recreational time series (SIAppendix, Table S2) was calculated from diet composition data collectedfrom Lake Simcoe by the MNRF during specific survey years (1975, 1983,1991, 1999, 2001, 2002, 2005, 2008, 2009, 2013, 2014, and 2015). Diet datawere then pooled for 3 periods, chosen to coincide with prominent speciesinvasions that likely altered diets: 1) 1961 to 1991, 2) 1992 to 2003 (invasionby spiny water flea and zebra mussels), and 3) 2004 to 2015 (invasion byquagga mussels and round goby). Diet items were recorded in various tax-onomic resolutions, and thus, we aggregated diet items to higher taxonomiclevels (e.g., genera) per survey year, except for fish prey and invasive species,

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which were kept at the species level. We then computed the trophic levelTi,yof each fish species per survey year (7),

Ti,y = 1+Xnj=1

�pj,i,y * Tj,y

�,

where Tj,yis the trophic level of prey item j and pj,i,y is the proportion (bymass or volume) of prey item j in the diet composition. Trophic positions ofinvertebrates and some small fish prey items were obtained from the liter-ature (SI Appendix, Table S3).

Role of Invasive Species and Stocking. We examined how invasive speciesappearing within the diet of harvested fish might affect indicators. Recre-ational indicators were recalculated using diet data from the preinvasionperiod (1961 to 1991), but fishery catches were left unchanged because theinvasive species did not contribute to recreational catches. These reestimatedindicators were then compared to the indicators derived using the appro-priate diet data for the 2 invasion time periods (1992 to 2003 and 2004 to2015). We did not examine earlier invasions (i.e., carp and smelt) because welacked detailed stomach content records for earlier time periods.

To examine the contribution of stocking, indicators were reestimated byremoving 2 species of stocked fish from recreational catches. Stocked fish arereadily identified with a fin clip and recorded in the catch records.We focused

on lake whitefish and lake trout, which continue being stocked for man-agement purposes in Lake Simcoe. For this analysis, catch estimates wereadjusted, but trophic levels remained unchanged because stocked and wildfish cannot be delineated in stomach contents. The recreational creel surveydata only differentiate between stocked and wild fish after 1980, and thus,our analysis of stocking effects was for 1980 to 2015.

Fishery-Independent Indicators. We also derived indicator values using datafrom an annual index gill netting survey conducted by the MNRF in 2003 to2014. Thesemonitoring surveys had a random stratified sampling design withspatial and depth strata; in each survey year, ∼30 samples of species, catch-per-unit-effort, and mass of fish were collected with multimesh monofilamentgill nets (45). We estimated mean total biomass-per-unit-effort (metric tonper hour) by multiplying numbers-per-unit-effort by mean mass of fishcaught. The same 5 species were used as for the recreational catches, whichare also the most abundant species caught in the gill nets. Data reported inthis paper can be found in Datasets S1 and S2.

ACKNOWLEDGMENTS. We thank Justin Trumpickas for compiling data andthe Lake Simcoe Fisheries Assessment Unit for collecting the long-termmonitoring data used in this study. Funding was provided by the Lake SimcoeProtection Plan, through the Ontario Ministry of the Environment, Conserva-tion, and Parks.

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