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Netherlands; Austria; The Laxenburg, Amsterdam, A-2361 XH 1098 Amsterdam, of University a fish Soudijn H. piscivorous Floor large of collapses fishing-induced population prevent can fish forage Harvesting PNAS clgclDnmc ru,Wgnne aieRsac,17 PImie,TeNetherlands; The IJmuiden, CP 1976 Research, Marine Wageningen Group, Dynamics Ecological eateto vltoaySuiso isses h rdaeUiest o dacdSuis(oedi,Hym,Kngw 4-13 aa;and Japan; 240-0193, Kanagawa Hayama, (Sokendai), Studies 87501 Advanced NM for Fe, University Santa Graduate Institute, The Fe Biosystems, Santa of Studies Evolutionary of Department h motneo neoytmbsd utseisapproach multispecies ecosystem-based, an of importance The cd olc,ec)adtnsadsalpakioosfish gadids planktivorous small as tunas—and fish—such and piscivorous etc.) pollock, large (cod, both target isheries 01Vl 1 o e1917079118 6 No. 118 Vol. 2021 | e rdtrpe dynamics predator–prey eateto ilgclSine,Uiest fBre,50 egn Norway; Bergen, 5006 Bergen, of University Sciences, Biological of Department a,b,c,1 | bioenergetics d etefrOenLf,TcnclUiest fDnakAu,TcnclUiest fDnak 80KnesLyngby, Kongens 2800 Denmark, of University Technical Aqua, Denmark of University Technical Life, Ocean for Centre .Dani P. , | utpetohclevels trophic multiple lvnDenderen van el ¨ % fgoa fish- global of | d ik Heino Mikko , c vlto n clg rga,ItrainlIsiuefrApidSsesAnalysis, Systems Applied for Institute International Program, Ecology and Evolution doi:10.1073/pnas.1917079118/-/DCSupplemental at online information supporting contains article This 1 ndmntaigta avsigfrg s osntalways not can does fishing such fish agree Instead, negatively. forage analyses populations harvesting piscivore model affect that and statistical fish demonstrating and forage in dynamic on pressures Our fishing patterns piscivores. and historical Using rela- biomasses evaluate piscivore (13). statistically Assessment is in Stock then herring) pis- Legacy we web and (RAM) both (14), Myers food (sprat Database include A. fish its Ransom species global forage fish We because the and piscivores. exploited Sea (cod) and the Baltic civores fish and the forage simple are both on explore tively food system for we focus their the model, fishing first on this of throughout Using effect effects energy consistently. the direct of for a flows accounted thus has the addi- fish and In incor- sources, by budgets. model energy consumption The feed- individual-level tion, 12). and size-dependent interactions, (10, populations, ing fish communities size-structured fish community this porates Sea on do Baltic effects We fisheries investigate central to fish. of designed the specifically piscivorous was of that (12) the model dynamics published predators, a their using on fish age 11). communities, (10, harvesting and and predation populations size-selective 3) fish the and through of accounting flows are: consistent communities 2) bioenergetic fish structure, of size models fish-population in 1) essential considered are that ulse eray2 2021. 2, February Published See the under Published Submission.y Direct PNAS a is article This interest.y competing no declare authors The and model community-dynamics U.D., provided analysis.y M.H., A.M.d.R. P.D.v.D., and and F.H.S. construction F.H.S., and data; paper; the analyzed F.H.S. wrote P.D.v.D. research; A.M.d.R. and designed F.H.S. A.M.d.R. research; and U.D., performed M.H., P.D.v.D., F.H.S., contributions: Author owo orsodnemyb drse.Eal [email protected] Email: addressed. be may correspondence whom To n h rtcino icvru s stocks. fish fisheries piscivorous of forage-fish protection of the management and the regarding pol- advice for icy implications have findings Our population. when forage-fish the in occurs dependence density effect releases fish beneficial forage of The harvesting the fish. forage their har- by of reduced are vesting mortality piscivorous fishing low hand, to other exposed the stocks fish On fish. from forage benefit their mortality of fishing harvesting high to exposed piscivo- stocks belief, held fish widely rous this to contrary that, resilience. show and we Here, neg- abundance fish population forage piscivore of affects harvesting atively that thought forage generally as fish, is known fish, It predatory prey fish. their target as well fisheries as piscivores, as ecosystems, known marine many In Significance c,e,f nti td,w netgt h fet ffihn o for- for fishing of effects the investigate we study, this In online l Dieckmann Ulf , o eae otn uha Commentaries. y as such content related for f nttt fMrn eerh 05Bre,Norway; Bergen, 5005 Research, Marine of Institute b NSlicense.y PNAS nttt o idvriyadEoytmDynamics, Ecosystem and Biodiversity for Institute https://doi.org/10.1073/pnas.1917079118 c,g n Andr and , . y https://www.pnas.org/lookup/suppl/ .d Roos de M. e ´ b,h | f8 of 1

ECOLOGY protect large-piscivore populations from fishing-induced col- Community-Dynamics Model of the Baltic Sea. To analyze the effects of mul- lapses. These results challenge the generally accepted idea that tispecies fishing, we used the stage-structured bioenergetics model of the large piscivores always benefit from less fishing of their forage central Baltic Sea introduced by van Leeuwen et al. (12). The model includes fish (6, 15). the key ecological interactions between predatory and forage fish and their resources; it is aimed to qualitatively reproduce the dynamics of this sys- Materials and Methods tem. We improve on the model by van Leeuwen et al. (12) by implementing Below, we present the models used for our analyses in general terms. reproduction as a seasonal process, following Soudijn and de Roos (16). The Details are described in SI Appendix, in Appendix A for the community- model structure and size-based, stage-specific parameterization are derived dynamics model and in Appendix B for the statistical model. Analysis of from individual-level data of Baltic cod, sprat, and herring (SI Appendix, the community-dynamics model was carried out by using publicly avail- Appendix A). Fig. 1A shows the interactions between fish populations in able C-based simulation programs. The statistical model analysis is based the model. Sprat and herring, the prey fish of cod, are assumed to have a on publicly available data. similar ecological role. Hence, they are modeled as a clupeid population that

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0.06 0.001

0.03 Adult clupeid biomass (kg/m Clupeid resource 0.000

0.00 net-production rate (d 0 102030 Low High Time (years) Clupeid fishing mortality

Fig. 1. Interactions between cod and clupeids in the community-dynamics model of the Baltic Sea. (A) Trophic interactions among fisheries (narrow gray arrows), cod and clupeid stages, and their resources (black arrows; see SI Appendix, Table S4 for the foraging preferences of the cod stages). Individual fish grow through stages from left to right (broad gray arrows). (B) Time series of adult cod biomass (Top) and adult clupeid biomass (Middle), both including −1 −1 reproductive storages; and biomass of the clupeid resource (Bottom) for low (black lines; FS = 0.2 year ) and high (red lines; FS = 0.5 year ) clupeid fishing −1 mortality. The cod fishing mortality is high, FC = 0.75 year . The time series start from equilibrium biomasses for low cod and clupeid fishing mortalities −1 −1 (FC = 0.5 year , FS = 0.2 year ). (C) Averages over years 0–10 of the biomass of annual clupeid reproduction (Top), clupeid juvenile biomass (Middle), and −1 −1 the mass-specific net-biomass-production rate of adult clupeids (Bottom) for low (left bars: FS = 0.2 year ) and high (right bars: FS = 0.5 year ) clupeid fishing mortality. Fishing mortality is here measured by the instantaneous fishing mortality rate. All other parameters are set to default values (SI Appendix, Tables S2–S4).

2 of 8 | PNAS Soudijn et al. https://doi.org/10.1073/pnas.1917079118 Harvesting forage fish can prevent fishing-induced population collapses of large piscivorous fish Downloaded by guest on September 30, 2021 Downloaded by guest on September 30, 2021 avsigfrg s a rvn sigidcdpplto olpe flrepsioosfish piscivorous large of collapses population fishing-induced prevent can fish forage Harvesting al. et Soudijn S4 Fig. included. In Appendix , (SI S6). of combinations Table stock robustness of these the and of importance tested exclusion the the We to of persistence. results indicator piscivore our for an forage-fish stock as forage-fish rates, function the turnover easily stock cannot biomass forage-fish rates. stock these biomass-depletion of knowledge forage-fish Without and the by biomass-production determined jointly pis- is forage-fish the biomass sug- support stock might singly forage-fish to However, This sufficient stock. ). S4 not civore Fig. was Appendix, biomass forage-fish (SI the stock that piscivore gest the of that than lower analysis. the for used were (SI time through increased only that Appendix, stocks two and distance Cook’s on based overlaps in spatial shown with is 50% combinations stocks Stock than inclusion. less their of to 50 of results overlaps of spatial ness found we 95% combinations, stock to other three in For overlap ically. spatial a 95% found with of stocks We piscivore excess (19). and areas forage-fish fisheries-assessment of their combinations 23 of coordinates regions geographical bounding the the on of based stock piscivore and stock decline forage-fish the of beginning the the as at measured and maximum end was the a decline period. at and biomasses piscivore-biomass years piscivore 5 The of of years. ratio duration 15 minimum of a and on duration S8–S10 based Tables results could that show Appendix, periods we the (SI of durations selected years) be 19 piscivore to thus (8 in maximum and decline years) 14 greatest to of periods Appendix , (SI derive biomass to used methods We S2). different and S1 three Figs. Appendix , (SI areas fisheries-assessment considered in changes on mortalities expected fishing pisci- is piscivore protect and biomass. interaction forage-fish piscivore can an of fish effects (Results), the forage collapses Appendix, in of (SI fishing-induced to harvesting mortalities from data intermediate fishing vores survey If and and biomasses B). catch stock Appendix of cur- of syntheses Database Assessment estimates available Stock derive best Legacy the RAM represent the rently in (ref. and assessments Database stock biomasses Assessment at The accessible Stock stock publicly Legacy 3.0; of RAM version patterns 14; the from historical mortalities using fishing in ecosystems Fish across Forage their alize World. and the Piscivores around between ingestion Ecosystems Interactions through of Model decline Statistical and foraging of semichemo- absence follow the fish. hence, by and, in rate growth have turnover to stat assumed reproductive and are each productivity model of thus constant the reproductive start in are a the the resources and unstructured in at three biomass Biomass body The juvenile adults. season. adult to the the converted as is of processes storages to same part allocated the sea- are by energy reproductive storages affected the stages, reproductive until fish storages The pro- adult reproductive son. and net-energy in all stored on stage For is depend small-adult (16). reproduction stage the mortality large-adult to and the juvenile duction to the reproduc- small-adult from in the and energy rates growth from all somatic transition invest to The adults energy Large tion. their reproduction. somatic to of for remainder part production the allocate net-energy and adults all small-adult, Small use juvenile, growth. a Juveniles of (12). and/or consist stage growth clupeids large-adult in and invested cod is is energy Both biomass If reproduction. costs, 17). maintenance If (12, covering occurs costs. after reproduction or left star- maintenance to growth due no cover lost and is mortality, to their biomass vation energy, used assimilated Following the first (18). exceed costs is Innes maintenance energy and Yodzis assimilated by approach, introduced originally approach dynamics. lpisi h oe.Uigtemdl eass h fet fteinstanta- the (F of cod effects for the rates the assess mortality we and fishing model, neous cod the juvenile Using Accord- between model. juvenile the 1A). competition in (Fig. resource while clupeids maturation direct fish upon no fish is small larger there and ingly, and benthos zooplankton to on switches piscivore and forages the community, Cod, life. this its throughout in (zooplankton) resource same the uses o orsokcmiain,teboaso h oaefihsokwas stock forage-fish the of biomass the combinations, stock four For of combination each for overlap spatial of degree the determined We the in biomass piscivore of decline strong a with periods time selected We bioenergetics the on based is (17) model biomass stage-structured The eicue hs tcsi h nlss u eie h robust- the verified but analysis, the in stocks these included We . .I oa,2 tc combinations stock 23 total, In S7). 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The a low the from at on system present depends the low invade not is cannot or mortality present fishing is cod alternative when 3A; two dynamics (Fig. exhibit stable can system of cod–clupeid patterns The 3). dynam- (Fig. population diet cod–clupeid ics the their in bistability in with mortalities clupeids juvenile on 1C). strongly 1A cod, (Fig. (Fig. benefits depend clupeids cod clupeids juvenile of since juvenile production higher of the Finally, production higher a and consequently, net- and, higher reproduction a clupeids enables adult This by of 1B). production (Fig. density energy clupeids the the increasing of resource and the food reducing for thereby competition biomass, clupeid intraspecific adult in the reduces increase biomass clupeids 1C ing clupeid (Figs. This mortality clu- fishing juvenile 3). higher clupeid with Surprisingly, at increases and mortalities. pronounced B, 2 fishing less 1B, becomes peid pressure (Figs. biomass predation clupeid lessened the adult is as increases cod biomass from clupeid fishing decreases, adult population cod cod the the When of distribution. size level clupeid the any for about extinct beyond goes mortality. and population mortalities mor- fishing withstand, cod fishing of the can range clupeid cod the high decrease that a harvesting clupeid to the of about on up than fishing of remains clupeids clupeid tality of cod the effect of of higher positive resilience The harvesting much har- 2A). can tolerates high are (Fig. cod cod without with clupeids general, Yet, mortalities when In 1B). fishing mortality intensely. 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Fig. 2. Effects of fishing on biomasses and yields in the community-dynamics model of the Baltic Sea. Biomass of adult cod (A) and adult clupeids (B), both including reproductive storages, and annual yield of cod (C) and clupeids (D) as a function of cod (FC; horizontal axes) and clupeid (FS; vertical axes) fishing mortalities. All other parameters are set to default values (SI Appendix, Tables S2–S4). Fishing mortality is here measured by the instanta- neous fishing mortality rate. Yield is measured by the annual catch of, for cod, adults only and, for clupeids, adults and juveniles together (SI Appendix, Appendix A).

means that the conditions under which cod is able to (re)colonize where the cod yield is very low or zero, close to or beyond where the system become more permissive with intensive clupeid cod goes extinct. harvesting (Fig. 3). At low cod fishing mortalities, however, fishing for clupeids Fishing for Forage Fish Can Protect Piscivores in Ecosystems around decreases cod biomass (Fig. 2A). This happens because when the World. Investigating historical piscivore-biomass declines, cod is present at high density, cod predation keeps the clupeid we find that the statistical model best explaining the declines population at a low level (Figs. 1 B and C and 3). Consequently, includes fishing mortalities of both piscivores and forage fish, as competition for food in the clupeid population is weak, even well as their interaction (Table 1, Fig. 4). The interaction is posi- without clupeid harvesting. tive, implying that for high piscivore fishing mortalities, piscivore Fishing for clupeids decreases the maximum yield that can be declines are smaller when the fishing mortalities of forage fish harvested from the cod population. The highest maximum yield are higher. For low piscivore fishing mortalities, the interaction of cod is found for a low clupeid fishing mortality of FS = 0.0 implies the opposite. This finding, based on piscivore stocks and to 0.05 year−1, where the clupeid yield is low or zero (Fig. 2 C forage-fish stocks in a wide range of marine ecosystems, corrob- and D). In addition, with intensifying clupeid harvesting, obtain- orates the predictions of the community-dynamics model of the ing the maximum cod yield requires an increasingly high fishing Baltic Sea. mortality (Fig. 2C). On the other hand, the maximum clupeid We considered several alternative definitions for the periods yield increases with increasing cod fishing mortality (Fig. 2 C and of largest decline in piscivore biomasses (SI Appendix, Appendix D). The highest maximum yield of the clupeids occurs at values B). For all methods considered, the best model was either a

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u ttsia eut r outt hne nteminimum the in changes to robust are results statistical Our Clupeid adult Clupeid juvenile Cod adult biomass (kg/ m3 ) biomass (kg/ m3 ) biomass (kg/ m3 ) 0.000 0.005 0.010 0.015 0.020 0.025 0.030 fet ffihn ntebsaiiyo o ouaindnmc in dynamics population cod of bistability the on fishing of Effects 0.10 0.15 0.20 0.25 0.30 0.35 0.00 0.01 0.02 0.03 0.04 ftevrac (adjusted variance the of ...... 1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0 and Cod fishingmortality epciey nldn erdciestor- reproductive including respectively, Bottom, F S . year 0.2 = r −1 2 B al and 1 Table ; ...... 1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0 n ih(B; high and ) F C year ( r  1 F 2 S IAppendix, SI ) . year 0.5 = ≤ 0.07; −1 SI ) ln(B ln(B scaatrzn oeswt usatal essupport. less substantially AIC with models the characterizing is as AIC score. coefficients, AIC regression minimal the and intercept and score, the of error terms dard model the respectively, M of, and coefficients piscivores rate analysis. regression of the exploitation the for 5 combinations the used 23 between by were of vary fish measured total to forage here A allowed is biomass). is catch/stock mortality period (annual Fishing decline years. the 15 of and Methods duration and The (Materials S1). period Fig. decline the of beginning B mortality ing mortality fishing piscivore average the ln(B Model world the piscivore in around of declines ecosystems effects piscivore-biomass the on of fishing models forage-fish statistical and the Alternative in 1. food Table of for increase competition an to and due biomass reduced shrinks, forage-fish is population fish (adult) piscivore forage small the of when to production community- due the the growth, model, In piscivore (23–25). dynamics for constraints avail- crucial body-size the is piscivore’s piscivory, items the of prey onset small fishing the of the diet during ability from piscivore Especially benefit the prey. can of their fish. piscivores of part the forage essential Therefore, juvenile an for- 1A). up small (Fig. make community- harvesting of fish production low, may small the the These is fish in increases abundance fish forage When, age piscivore harvesting piscivores. model, fishing, large dynamics of through affect that, effect positively shown have secondary we this Here, (20–22). recognized widely large benefit can fish forage sup- for nevertheless fishing piscivores. but that methods, hypothesis statistical the robust the port piscivore- completely of of not details are magnitude some results to the latter on These fish declines. biomass forage of their mortalities and fishing statistical between piscivores our interaction positive predictions, a theoretical shows model these with mortality. fishing accordance piscivore In high pre- at what clupeids collapses to of population cod harvesting contrary vents intermediate Yet, har- suggests, mortality. clupeid paradigm fishing increasing the with piscivore with low line biomass at In cod vesting of 15). Sea Baltic decrease (6, the a of piscivores predicts forage model large community-dynamics of our for fishing paradigm, harmful this the always that is paradigm fish the challenge findings Our higher has Discussion still term Neverthe- interaction S7). the Table power. similar including explanatory Appendix, being model (SI models the support three less, in empirical resulting their stock, in influential an of pi pi p p p p p p h he oesdsrb h oaihi decline logarithmic the describe models three The is fish of distributions size alter to fishing of potential The 13.4 M smaue ytertoo icvr imse tteedada the at and end the at biomasses piscivore of ratio the by measured is 1 2 1 3 2 1 pi pi pi 0.29 = 0.54 = 0.37 = 0.009 = 0.009 = 0.005 = ff ) ) ) . = = = M r 2 −1.0 −0.8 1.2 ff I stedfeec nACsoerltv otemdlwt the with model the to relative score AIC in difference the is 4AIC stecefiin fdtriain(adjusted determination of coefficient the is + − M 51.1 − − 9.6 ff 1. 1.0 uigtedciepro.Tepsioeboasdecline piscivore-biomass The period. decline the during M M I ausi xeso w r tnadyrecognized standardly are two of excess in values 4AIC M M pi pi M pi pi − ff −1.5 M ff https://doi.org/10.1073/pnas.1917079118 M p 17.5 . .14. 5.0 48.0 0.01 0.3 1.1 0.5 4.6 3.1 . .64. 0 43.0 0.26 0.8 1.0 2.5 SE 1 pi , p n h vrg oaefihfish- forage-fish average the and 2 and , 24. 6.6 49.6 −0.02 p r 2 3 ln(B hwthe show r pi 2 and safnto of function a as ) ,S stestan- the is SE ), AIC PNAS M IAppendix, SI P pi , ausfor values M | ff 4AIC f8 of 5 and ,

ECOLOGY 0.4 ular, accounting for costs of maintenance), 2) the size structure 0.25 0.15

ff of fish populations, and 3) feedbacks between trophic levels are

0.3 indispensable for the effects of fishing mortality on the pro- duction of juvenile forage fish to become amenable to analysis Biomass 0.2 (10, 17, 37). 0.20 decline 1.00 Previous studies have ascribed reduced growth of piscivore

0.3 0.75 populations after a decline in their population to cultivation-

0.50 depensation mechanisms (40–42). After a piscivore decline, 0.15 increased forage-fish biomass may, for example, lead to 0.4 0.25 0.2 increased competition between juvenile piscivores and forage fish and/or predation of forage fish on eggs and larvae of pi- scivores (40, 41). These mechanisms could lead to the same Forage−fish fishing mortality M Forage−fish 0.10 0.6 0.15 net positive effect of harvesting forage fish on piscivore persis- tence as biomass overcompensation, the mechanism explained 0.1 0.2 0.3 0.4 above. To determine the importance of the different mech- Piscivore fishing mortality Mpi anisms, detailed data on the interaction between forage fish Fig. 4. Effects of fishing on piscivore-biomass declines in the statistical and piscivores are required. Such data are not generally avail- model of piscivore fish stocks and forage-fish stocks in ecosystems around able. For the central Baltic Sea, detailed analyses of available the world. The decline is shown as a function of the average piscivore fish- data have shown that biomass overcompensation could explain ing mortality (horizontal axis) and the average forage-fish fishing mortality the lack of recovery of cod in this ecosystem (43), while no (vertical axis). The piscivore-biomass decline is measured by the ratio of pi- sufficient data are available to test whether predatory cultiva- scivore biomasses at the end and at the beginning of the decline period tion depensation could explain the lack of cod recovery. For (Materials and Methods and SI Appendix, Fig. S1). Fishing mortality is here this reason, we did not include cultivation-depensation mech- measured by the exploitation rate (annual catch/stock biomass). The dots anisms in our community-dynamics model. The inclusion of represent the 23 combinations of piscivores and forage-fish stocks used for these mechanisms in the model would likely strengthen the the analysis. The estimated model shows that piscivore biomasses decline more strongly for higher piscivore and forage-fish fishing mortalities, with observed effect. a positive interaction. The global RAM Legacy Stock Assessment Database (14), which we have used for our data analysis, is currently the most extensive source of fish-stock assessment data. While the forage-fish population. An increase of forage-fish population findings from our statistical model support those from our biomass has often been documented in relation to declines of community-dynamics model, caution is needed, as the for- piscivores (26–28). Signs of competition, such as a reduced mer analysis is based on a relatively small number of cases. growth and body condition, have been observed in forage-fish In addition, the statistical analysis may have biases hindering populations after the declines of cod in the Northwest Atlantic the detection of effects. For example, no established method and the Baltic Sea (12, 29, 30). In addition, the estimated total is available for choosing the duration of periods of declining reproductive output of clupeids in the Baltic Sea shows a steep piscivore biomass. Furthermore, variability in primary produc- decline during the years leading up to the collapse of cod (12). tion among the considered fisheries-assessment areas implies These examples show that population biomass and competition that absolute fishing mortalities may not be directly comparable. for food can both increase in forage-fish populations after or Moreover, we inferred trophic interactions between forage-fish during declines of their piscivorous predators. Moreover, pisci- and piscivorous-fish stocks based on spatial overlap and trophic vores in the Northwest Atlantic and the Baltic Sea appear to level. This does not necessarily reflect the trophic interactions suffer from a reduced body condition since their collapse, which that occur in the ecosystems. Finally, a global analysis will always may be indicative of a persistent shortage of food (31–34). While remain correlative, rather than establish causation. In-depth the high biomass of forage fish in these ecosystems seems to studies of prey size distributions in the stomach contents of pisci- imply a high food abundance for the piscivores, the signs of vores could provide more direct evidence of effects of forage- food shortage suggest that prey of the right size may, in fact, fish fisheries on the feeding conditions of the corresponding be scarce. piscivores. A positive effect of forage-fish harvesting on piscivores has The RAM Legacy Stock Assessment Database is widely used not been reported in previous model-based studies (e.g., refs. 15 as the authoritative source of stock-abundance data for fish- and 35). However, it has recently been argued that multispecies eries analyses (e.g., ref. 44). The estimates of stock biomass in fisheries models do not incorporate all relevant biological pro- the database result from single-species stock-assessment mod- cesses (10, 11). For example, multispecies fisheries models do not els, which typically assume natural mortality to be constant always consider size-selective predation and harvesting, as well as over time. The assumption of constant natural mortality poten- the size structures of piscivore and forage-fish populations (10, tially leads to confounding effects of declining predator biomass 11). Moreover, the energy budget of fish is often not accounted on the estimates of forage-fish fishing mortality (45). Yet, the for in a consistent way (10), as somatic growth is assumed to forage-fish fishing mortalities used in our analysis seem to fluc- be independent of food availability, or costs of maintenance tuate randomly during the periods of piscivore biomass decline and/or costs and food dependence of reproduction are ignored (SI Appendix, Fig. S2). The assessment methodology may also (10). These factors are all included in the community-dynamics raise questions about the representativeness of the resultant model we have used for the present study. Our model predicts estimates. Preferably, validation of a hypothesis is based on mul- a positive effect of clupeid fishing mortality on juvenile clupeid tiple lines of evidence. A combination of commercial-landings biomass—a phenomenon known as biomass overcompensation, data and biomass estimates is needed to allow for the analy- which has been described in both theoretical and experimental sis of trends in biomasses and fishing mortalities. To the best studies (17, 36, 37). Crucially, biomass overcompensation does of our knowledge, there are not sufficient trawl-survey-based not occur when the size structure of populations is ignored (17, biomass estimates available to repeat our analysis with alterna- 38). It also does not occur when energy losses through main- tive data sources (SI Appendix, Figs. S5 and S6 and Appendix tenance costs are not explicitly considered (39). Therefore, a B). While trawl-survey data may be available for longer peri- consistent treatment of 1) individual energy budgets (in partic- ods than shown in the figures, there are no recordings of

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(SI Appendix, closely relatively estimates find stock-assessment-based did calcula- the we are follow that estimates the estimates biomass biomass for which trawl-survey-based The on needed based. effort, catch-per-unit are the of which tion available, area trawl-swept avsigfrg s a rvn sigidcdpplto olpe flrepsioosfish piscivorous large of collapses population fishing-induced prevent can fish forage Harvesting al. et Soudijn .C .Suasi .A etPe .E ut .A rnh .Hlon xmnn com- Examining Hilborn, Cury R. P. Branch, A. 9. T. Punt, E. A. Vert-Pre, A. K. Szuwalski, S. for C. test-bed 8. The species: forage Lynam on P. fisheries C. of 7. Management Duplisea, D. Rice, J. 6. Pikitch K. E. 5. global Increasing Pikitch food: K. E. for 4. fishing or feed Engelhard for H. G. Fishing 3. Metian, M. Tacon, G. A. sustainable 2. the 2018—meeting aquaculture and fisheries world of state “The FAO, 1. h rae ato oaefihcthsi sda edin feed as used is catches forage-fish of part greater The the for webs food many in link essential an form fish Forage inmdlwt esnlrpouto yasaesrcue ims model. biomass stage-structured a by Ecol. reproduction seasonal with model tion ecosystems. pcfi ims hnmraiyicess h nuneo auainversus maturation of (1992). 1175 influence The increases: mortality regulation. reproduction when biomass specific Assessment Stock Legacy RAM the with species Database. marine exploited commercially of tus of Exploration the 2014). for Denmark, Council Copenhagen, Sea, International the 2014/SSGRSP:08, Rep. SGSPATIAL (ICES (2008). 89–104 birds. for dynamics recruitment of meta-analysis fisheries. 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Changes protected Ricker, E. marine W. of 20. benefits Global Heal, G. Rising, J. 19. 5 .Gsao,Snl n utseisrfrnepit o atcfihstocks. fish Baltic for points reference multispecies and Single Gislason, H. 35. The feeding? poor Eero by limited M. cod northern 34. of recovery Is Rose, A. G. Mullowney, R. D. 33. Eero M. 32. morhua ) (Gadus cod Atlantic of reserves energy and Condition Dutil, D. J. Lambert, Y. Trunca- 31. rule: Bergmann’s Breaking Leggett, Casini C. M. W. 30. Frank, T. K. Fisher, D. A. J. 29. Casini M. by 28. cod- triggered formerly cascades Trophic a Mihneva, V. in Rodionov, cascades S. Grishin, Trophic N. Leggett, A. Daskalov, C. W. M. G. Choi, S. 27. J. Petrie, B. size Frank, relative T. How K. Hall, E. 26. J. Rice, A. C. Greene, M. C. Beckman, R. B. Chamberlin, W. in J. fishes” piscivorous 25. of conse- ecology ecological “Feeding its Scharf, S. and F. Buckel, piscivory A. of J. Juanes, ontogeny F. The 24. Persson, L. Mittelbach, G. ontogenetic- G. an drives 23. Exploitation Boyce, G. D. Leggett, C. W. Petrie, B. Frank, populations: T. K. harvested in 22. changes Adaptive Heino, M. Dieckmann, U. Ernande, B. 21. eedvlpdfo olbrtv okb h aeatosicue in included authors paper same the F.H.S. the of of by thesis Portions work PhD Arkel 1A. the collaborative Fig. van from in Jan developed displayed institute. were illustration the the the and support Villum designed IIASA Project that by (IBED) the Council supported Organizations by were Research Member U.D. supported Life, National Norwegian and M.H., excellence Ocean by F.H.S., (255530). for supported of MESSAGE Center was center the M.H. Rasmussen (COFUND- within Foundation. Kann (Marie 609405 work Villum Program Grant the a Agency People conducted Executive the and Research PostdocDTU) by under supported Dutch Actions) the was by Curie Analysis P.D.v.D. financed Systems was Council. program Applied the for Research in F.H.S. Institute of International participation standardizing the the and (IIASA); at processing, YSSP inspira- the cleaning, and in during for used Scientists discussions data Maureaud Young trawl-survey helpful A. 2014 the thank for all We participants and tion. Leeuwen, (YSSP) van Program A. Summer Amsterdam, of University 3.0; ACKNOWLEDGMENTS. analy- version model 14; statistical (ref. the accessible for database/). have publicly used is model Database sis statistical Assessment the Stock Legacy of https://zenodo.org/ at analysis deposited been and be model not community-dynamics obviously Availability. Data should increases fishes fish forage forage overfished. on resilience, pressure argue fishing we piscivore While intermediate them. an cause on depend even that that may piscivores fishes the cases, forage of some of collapses In mortality conse- exploited. fishing heavily negative the are decreasing unwanted fishing that have lowering piscivores for- may for drastically quences fishes of good that forage management imply with on results the is pressures our in It Yet, (4). caution fish. fisheries urge age of scientists value that economic reason contri- the indirect their to and butions functioning ecosystem for fishes forage aesw98.Acse etme 2019. September 1 Accessed papers/w19982. Sci. assessment. stock revisited. hypothesis capelin fish. forage of depletion local avoid (2012). and predators of ery stock. Lawrence St. of Gulf Northern the Sci. of collapse the during international extensive an using evidence sizes. 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