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International Coimcil C;M.1992/L:25 for the Exploration of the Sea

, .. ~. ~ •. -. 'l' ',<-. • • , :-t. • .•~ . A j\JIODEL OF ,TROpmC INTERACTIONSJN THE NORTH SEA IN 1981, THE YEAR OF THE STO:MACH*

by

•. '...... ' .VillY Christensen . . . . . International Center for Livirig Aquatic Resources Management M.C. P.G.Box 2631 .. 1266 Maka.ti, Metro Manila Philippines

This paper gives an överview of the trophic interactions in the North Sea in 1981 when 45,000 fish stomaehs were sampled. The study is based on the data base of the ICES Multispecies AssessmentWorking Group (MS .WG) and published information. A balanced, steady state model of interactions and biomasses at all trophic levels is. made usirig the II software. The model is preliminary asinfonnation was läcking for a .Ilumber of··groups.. The· results show among other . things that the food consumptiori rates used by the MS wo for three of the important gadoid species are unrealistically low.

• Resume' Cette expos6 rend compte des' intei'actions trophiques dan~ la mer du Nord OU, en 198 i, le contenu stomaciL1 de.45 000 poissoris a ete analyse. Cette ·etude a ete rea!isee a partir des informations. contenues dans .la ... base de donnees du graupe de travail sur l'evaluation plurispecifique du CIEM et dlautres ptiblications disponibles. Un modele equilibre des interactians et biomasses a tous les niveaux trophiques a ete cree al'aide du logiciel ECOPATH II..Toutefois, ce modele niest encore quill un stade preliminaire c3..r nous ne disposons pas encore de toiJtes .les informations concemant certains grotipes~ Les resultats deja obtenus .indiquent cependant que les coefficieritS de consommation. qu'utilise le. groupe de ti'avail pour trois des especes gadoides les plus importantes sant bien trop bas. .

... ICLARM Contribution No. 855.

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lritroductiöh . This contribution has cerrie about for a number of reasons. l have previciüsly worked with Noith Sea fish populations for a nuinber of years, and have followed the developmentS iri the lCEs Multigpeeies Woi-lcing Oroup (MS WG) with iriterest and the hope that their work may eventUally improve management. LOoking iri from the periphery 'Ü is however difficult to get an overview of what li actUally going on in the North Sea änd iri the MS WG. Orie reasen fo'r this is thai the MS WO's programs are basically "user hosti1e" and can be run by a handful of Propie only. Addißg is that inost emphasis nattlraiiy has been on developinent of methodoiogy, not on information and dissemination. It. is therefore of interesi te proouce a summary of the trophic interactions in the North Scii. In addition l find it of importanCe to check seme basic parameters arid assumptions in the MS WO programs where possible. Are the physiologic:al rateS re3.llstic'? An "ecöl~gical aueÜting" is approprhite noting the importance of the advice • that are ()r may be based on the MS, WG analyses. The MS WG progranls consider only the exploited, upper part of the ecosystem, igrioring the tower groups. Control of mass b3.Jance is therefore not an integcil pärt of the system, and the possibilities this affer for constritining paiärneter ranges is not corisiderecI. In ibis context the irriportance of eCosystem models serVirig as information bridges between different discipliries of fisherles arid marine scil~rice should also be emphasized. ," Of imporiance has also been ibat l arn irivolved in the development of a system for constructionof static ecosystem models" (Christe~sen ~dPauly 1992b)~ Most of the more thari 50 eCosystem models that have been made usmg this inethOdology haS been for systems where orily liriiited information is available" (ClmstenSen arid piuiy in press). A model for a weIl· stildiect area llke the Naith Sea li of interest bath for comparisoris with other eCosystems, and for sttidies related to further mOdel development. FinaIly should be mentiori@ that activities are L'l progress in iCLAF..11 towards • development "of ,a ,geneIie software system for, fishenes management inchidirig biologiCal and technicil interaction. Development of such a methooology is emphasiZed in the recent iCLARM strategie plan, and is seen to benefit from cloSe iriteractiön with the scientists mvoived iIi developmeni of ICES MS VlG programmes (iciARi-.r 1992). ' .. . Model methodology The model isconstfuctect usirig the ECOPATH ri softWäre system'äs descrlbect by Chnstensen arid Pauly (1992a). For ECOPATH models' it is asstimoo that input equals output for the time perlod considered. This assumption is modifleci here (and in the next release of ECOPATH Ii) to accept accumulatiori and depleiion of biorriasses during the time perioel modelled. ECOPATH II models are constructecI so thai there is mass balance, 1.e. Q=P+R+U (1)

2 • •

where Q is consumption, P production, R respiration; and ti uriassimilated food. Of these parameters the produdion is estimated from ... ,.' . ',' Pi = M2; + ~_f.Oi + EXi + BAi (2) where 1f2i is the predaiiori mOrtallty of group (I), MÖi is the non-predatlon rricirtality of (I), Exi is the export of (z),and BAi is the accumulated (or depletecI) of (I). Assuming the b3Jance expressed. in Eqüations (1) and (2), arid ncitllig that the predation term in EqUation (2) "linkS ,i predator and prey groups, it becomes pOssible for any group to. estimate ariy orie of the basic parnmeteis: biomass, piÖdiiction rate, consuIription rate, arid other. moi'iaiity. The. thiee other basic paiimeters arid the diet cOmpOsition rotist be gi~en (C1mstenSeiiand Pauly 199Ia,b)... , .' Orie of the basic parameters needs further explanation:' ibis is what is here termecI the ecotrophic efficiency (EE). ER scales oetween 0 arid 1, and expresses the pärt of the total producti6ii that is' uiiliZed for eith,er pi~uon, catehes. or biomass accumulation iri the system.' The complimentarj cf EE, (I-EE) corresPonds iö what is • orten ciüled "nciri-predation mcirtaliiy~ ~ , , The term "gross food conversion efficiency" is u5ed rar the ratio between total prOduction arid total foöci consumption oi any group~ , . . Iri addition to a balaricCd model of the trophic interactions a riuinber of data exploratory änalySes Can be cai'ried out using the ECOPKfH n sOftware. Noted here is the trophic äggregation arid the mixed tiophic impact routines (Christensen anct Pauly 1992b). . '", The trophic aggregation, routine aggregates the 11ows, ma system into discrete trophic levels. This ~s done by ~ disintegniti~g" the groups in the system. The routine is based on an approach suggested by UlanoWicz (in press)., . Tbc mixed trophic impact. routine is deriyed from economical input-output änaiysis as rlesciibed by Ulanowiczand Puccia (1990). This aßalysis quäntifies all the difeCt arid indiied troplrlc impacts of ail groups in tbe sysiem~ ~c! ~s~ bo~ ". , . The ECOPNm iI system' the dati ,file for the preserit mOdel are e av:ulable from the 3.uthoi I the ICLARM SoftWare Projeel. Däta soürces The key data for this model descIiption oiigin~ies {rom the ICES Multispedes Assessment Wodciiig Group data base. The core of this data base describes the 1981 ~Yeii--of-the-stomach" where moie thän 45,000 fish stomaehs were sampled arid ailaiy:ied in detail. I therefore opted to consirü6t a model of the tiophic mteractions iri the North Sea roi- that very year. . . ' Amoof the ICES MSVPA program (Sparre 199i) provided sumriiary st:iti~tlcs on the consumption in 1981 by each of the MS piedatois, Le. of cOd, whiting, saithe, macIrerel; and haddock. For the MS species(above inentioned predators plus ~erring; sprat, Norway Peut, sarideel, plaice, arid sole)' information on average stock biomass was aiso avciilable from tbe. MSVPA. For these sPecies. the ,. productlcin cotiid be estimated as stOCk size at the end of the year less stOCk size at the st3.rt cf the year phis biomass p~ated pius bionlaSs lost due to residual natuial m6rtalltY arid rishery.

3 As the MSVPA treatS allother prey than the ~fS species ciS "other fOod" more rletalled diet compositions for eod, whiting, saithe, maekerel ami haddoc~ were ob'tained from age specific information in Daan (1989) and Daan et al~ (1990). The age specific iriformätion was eori~erioo. to. stock estimates using inforrii

Tabie 1. Parameters Usedfor describing the Nonh Seafoodweb in 1981. PIB gives the productionlbiomass ratio, O/B is consumptionl biomass. Gross eH. gives the ratio betWeen production and consumption. EE, the ecouophic effficiency expresses the proportion of the production that is. used for predation,catches and biomass accumulation. For copepods only total production arid consumption is known, not B, PIB and O/B. legend: - indicates estimated values, + shows assumed values. GrÖup.Name Catches Biomass PIB O/B Gross Eff. EE t km-2 t kril-2 yearl yearl (P/O) yearl

1 Cod. 0.57 0.57 .1.11 . 3.15 0.45~ 0.76­ 2 Whiting 0.37 0.66 0.84 3.56 0.32­ 0.59~ 3 Saithe 0.21 0.65 0.58 3.29 0;19~ 0.65­ 4 Mackerel 0.11 0.46 0.29 5.79 0.04­ 0.49­ 5 Haddock 0.38 0.83 1.37 3.79 0.40­ 0.64­ 6 Herring 0.29 0.84 1.04 4.60 0.16­ 0.75­ 7 Sprat, 0.34 0.55 1.21 8.60. 0.17~. 0.51 ~ · 8 Norway pout 0.81 ',1.94 .2.48 16.53~ 0.15+ 0.69~ .9 Sandeel 1.16 2.58 2.02 13.47­ 0.15+ .0.82­ 10 Plaice 0.22 0.64 0.65 2.80. 0.31­ 0.85­ 11 Sole '0.03 0.08 0.66 4.40~ 0.15+ 0.86­ 12 Ray. . 0.00 0.53 . 0.44 2.90~ 0.15+ 0.00­ 13 Other prad.. fisl1 0.00 1.48 0.87 5.79­ 0.15+ O.OO~ 14 Other prey fish 0.00 4.35 0.48 3.50 ... 0.14­ 0.95+ ·15 Annelida " '. 0.00 ,1.60­ 3.00 20.00-' 0.15+ 0.95+ 16 Copepoda 0.00 10.00. 18.00 60.00 0.30­ 1.00~ · 17 EUfJhausiacea 0.00 9.15­ 2.43 . 16.20~ 0.15+ . 0.95+ 18 Other Crustacea 0.00 . 12.44~ 3.00 . 20.00~ 0.15+ 0.95+ 19 Echinodermata 0.00 .7.41 ~ 3.00 20.00­ 0.15+ 0.95. 20 Other inveitebrates 0.00' 36.65­ .. 3.00 20.00- 0.15+ 0.95+ 21 Phytoplankton ' 0.00 23.00 53.50 0.00. 0.76- 22 Juvenile fish 0.00 1.95- ·5.00. 25.00+ 0.20. 0.95. 23 Detritus 0.00 50.00 0.89-

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Table 2. Diet composition matrix tor the 1981 North Sea model.

Prev

Predator 1 2 5 6 7 8 9 14 15 16 17 18 19 20 21 22 23

1 Cod 0.017 0.051 0.058 0.023 0.022 0.072 0.079 0.188 0.067 0 0.050 0.320 0.009 0.044 0 0 0 2 Whiting 0.001 0.018 0.031 0.028 0.077 0.118 0.253 0.187 0.025 0 0.099 0.099 0.003 0.061 0 0 0 3 Seithe 0.001 0.003 0.056 0.008 0.008 0.465 0.05 0.029 0 0 0.358 0 0 0.022 0 0 0 4 Meckerel 0 0 0 0.021 0.019 0.031 0.188 0.012 0.005 0.214 0.365 0.031 0 0.114 0 0 0 5 Heddock 0 0 0 0 0.001 0.029 0.078 0.286 0.126 0 0.099 0.099 0.139 0.143 0 0 0 6 Herring 0 0 0 0 0 0 0 0 0 0.201 0.575 0.113 0 0 0 0.111 0 7 Spret 0 0 0 0 0 0 0 0 0 0.7 0 0.3 0 0 0 0 0 8 Norwav pout ; 0 0 0 0 0 0 0 0 0 0.335 0.515 0.075 0 0 0 0.075 0 9 Sendeel 0 0 0 0 0 0 0 0 0 0.5 0 0 0 0,49 0 0.01 0 10 P1aice 0 0 0 0 0 0 0 0 0.3 0 0 0 0.3 0.3 0 0 0.1 11 Sole 0 0 0 0 0 0 0 0 0.75 0 0 0 0.25 0 0 0 0 VI 12 Rey 0.003 0.011 0.038 0 0 0 0.189 0.125 0.092 0 0 0.542 0 0 0 0 0 13 Other pred. fish 0 0 0 0 0 0 0 0 0 0.044 0 0.244 0 0 0 0.712 0 14 Other prey fish 0 0 0 0 0 0 0 0 0.2 0 0 0 0.5 0.1 0 0 0.2 15 Annelida 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 16 Copepoda 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0.9 0 0.1 17 EuphausillclIlI 0 0 0 0 0 0 0 0 0 0.75 0 0.15 0 0.1 0 0 0 18 Other Crustac•• 0 0 0 0 0 0 0 0 0 0 0 0 0.05 0.25 0.3 0 0,4 19 Echinodermat. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0.2 0 0.8 20 Other invertebrates 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0.4 0 0.6 21 Phytoplankton 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 22 Juvenile fi6h 0 0 0 0 0 0 0 0 0 0.75 0 0.1 0 0.15 0 0 0 23 Detritus •

Group spedfic iriformation ~tS predators Inforniatiein on biomass; eonsumption and preiduetlon for the 1fS predators, Le. fcir eod (Öcidus morhua), whiting (Merlangius merianguS); Saith.e (Poilachius virens), maekerel (Scorrzber scombrus); and haddock (Melaiwgrairü1llis aeglefinUs)j is available from the M5 WO database. For these species detailed diet composiiieins' could be derived from inforriiation presented by Daan (1989) and Daan et al. (i990). The mackerei group is modelled 10 include both the North Sea mackereI and the West mackereI, oc~urring in the riorthem North Sea in the seCond ~d thiid quarters of the year. Herring (Clupea harengus). '. . . Information on bieimass and producrlon is av:iilahle from the MS WG iliiiabaSe. The consumption rate is from Pauly (1989). The diet' coinposition is based on information from LaSt (1989) äs follows. A mean cf prey weigl1tS is wreri eiver the three February. suryeys, the surveys in February, 1{ay arid August are assümed to be representätive for 5, 3, and 4 inonths respedively, and.it is assumed that ihe relative '. constimption rates in the survey i>eriOds ar6 1, 2, and 2 respectivelY. Sprat (SpraiiUS sprartui) .. Information on biomass and productiori is avaiiable freiin the MS WG ditabase. The consumption rate is based on an estlniate for Sprimus juegenSis given in Pauly (1989), which results iri a reasonable gross foOd conversion efficiency of 17%. Tbe diet eomposition is ä reiugh estimate bäSed on information in LaSt (1982; 1985). . Norway pout (Trisopterus esmarldz) Inforniation on hiomass and produdiori is aväiiable trom the MS WG dacibase. The consumption rate isestimated from an assumed gross feod conversion effidency oi 15 %; The diet corripositlon for Norway potii is baSed on iriformatlon presented by ltiiit arid Adams (1965, Fig l.B arid 2:B); Raitt arid Ad:ims preserit averiige diets based on e percent volume and ein average volurrie. per stoma~h. The.; perceni v~iume undeiestimates the impcirciriee of stömachs with large fullness of mainly fish prey, while at the same time over-representing hirge preY. due' to differential digestion time. ~erefore the'percent volume represencition iso userl äS a compromise. The overaÜ did compositicin is assurried to he. represented by the average diet composition eif juveiilles and adults.. The diet iri,feirniatlon fourid by Raitt arid' Adams (1965) is supported by stUdies of Gordon (1977). . Sandeel (Arrzmodyies spp.) . Information on biomass arid production is available {rom tbe M5 wa database. Tbe constimption rate is estimatCci from an aSsumecI gross fOOd crinverSion efficiency of 15 %. Sandeeis are predominantly zooplcmktivöious, with smali fish arid benthos cciritrlbuting iö the diet (Baden 1986). Meyer et al•. (tS)79) reports that copepods arid Sagitta eiegans contnbutes 3.round 40% (weight) each io tbe diet' of Ainerican sand lance, the rerriaining being' niainly animal remains. Tbe' actual dlet eomi>ositlon is assumed basect on these seiurces. .

6 . Plaice (P!eUrOneCleS plalessa) . '. .., IIlforrriation on oiomass arid production is available from the MS WG dataoase. Censumptiori rate is obtuned as an average ofthe eonsumptieri rates given for f6m3.Ie :arid male plaice by Palomares arid Pauly (1989);, :p'laiee feed on invertebrates, mainly polyehaetes, bivalves arid echinOderms (Bagge 1978). The diet cömPositiori is clSsuriied.

Sole (Solea solea). '.' , '. Information on biomass and production is available from the MS WG database. As no esrlmate for eorlSlimption rate was available a gross food eoriversion efficieney of 15% was assurrioo~ The diei eomposition is oased on qualitative information onIy, e.g., r.agard~re (1987).' " . Ray (Raja i"iuiiala) , The hiemass of ray is eStimated from tlle, average trawl survey abundanee as repOrted by Sparholi (199?) 'an4, re-evaluated by ,Daan et al. (1989).The fOOd eonsumption rate is esrlmated to 2.9' year1 (579,000 tannes eaten a year by 200,000 • toris of ray) ba5ed on studies hy M. Vintet, as reporied in ICES (1989). Based on tlle same souires (fables 8.4; 1 ancl 8.4.2) the diet eompOsition can beqUantified. Tbe lal~wn; möriality rate 0 (prOduetion) .of ray is not It is therefore estimaied from an ässumed gross food cOnversion 'effieieney öf 15 %.

Other precbitory fIsh 00 0 0 • 0 0 '. • 0 00 0 00 0 0 The parameters for "other piedatoIy fish were rriamty oaSed on herse riiaekerel; TnichurUS irachurus. Bioinasses for the "other" .fish species were based on average daiä (wiriter and summer trawl surveys) for 1983.;.i985 as esiiriiäted by Sparholt (i990.) In these surveys horse mackerel constltuted same 95 %of the ici.wlab1f~ biomass of "other pred3.tors". Hocse maekerel were only preseni iri noticeable quaniitles on, the' autumn ' survey. Only ineonclusive estimates of fOOd eonsumption by horse maekereI seem to be av.uIabie (Dahl and lGrkegaard i987). It was· therefore äSsum§d ihätthe "olher predators" have the same eonsumption/biomaSs ratio as maekerel. The.diet is b

o not kriciWii; therefore an ecotrophie effideney of 0.95 is aslsumCd. Creutzberg arid Dumeveld (1986) ~so gives average annual diet cOmPosiclons .for dah on mud and sand bottom~ Baden (1986) rePorts various food studies of dab indicating that echirioderms and 9ther benthos piedorriiriates in the diet. The actual diet ci>milosition is assumed baseci on these soufces.

7 Juvenile riSh .This is a heterogeneous group· intendcd to encompaSs all juvenile fish in the North Sea. Juvenile fishes are impOrtant prey for a large mimber of adult fishes, even tltough the. predation to 'some extent is iiniited duc to the generally more coaSt3.l occurience of the juveniles. Tbc preseni implemeritation includes hemng; NOrWay peut, sandeei; and other imxiatory fish (Trachurus) as predators on the juvenile fishes. Thc 11S predators are not mcluded aS predators on juveniles', perhaps mafnly because it is difficult to separate out the juveniles in tlle prey groups of the MSdata baSe: Tbc iriput data for juvenÜe fislles is m3.inly basro on qualiflea guesses, Le. 'high natUral- moftility räte ärid gross foOd coriversiori effiCiency is' asstiiried. The diet compesition is likewise baSecI on generiU knowledge of most juvenile flshes being plal'lktivorous. Co e"oda ." _.' - -' 1J P For copepoos iri the NOrtb Sea; Crisp (1975) r~rts an ariiniat'consumpticiii arid • pioductiori of 60 arid 18 g C m-2 respeetively; (conversion io gWW :; i'gC). TIus prooucrlon is within the range of more recent esHriiätes (FranSz äßd Gieskes 1984). Hannon arid roires (1989) reported a zooplankton pi"oduetion in ilie southem Nohh Sea of 15-20 gC m-2 year1• 'ihis again bt:acketS theestill1ate,of Cri.5P tlüt also shows thai his value may _be an underestima.tb as the co{iepoo prOducrlön is kriown i6 be highest in the northern North Sea• .Euphausiaceä _ Lindley (1980) gave estimates of production arid biornäss of tWo (out ofthree) doriiliiants~ies;,ThysiUiOeSia irie~~s r.~chi, ofe~phausiids I änd, T. mthe NE ,North -Sea and NW Skageriak in. 1966 _aitd 1967. BaSed on _this information a , prOduction/biomass ,ratio of 2.43 yeai-1 .,could b,e estimatecI. Lindley's estimate. of biomass could not be used (see' betow); instead it was assumed thai the gross food cönversiori efficlency of euphausüds was 0.15; 'arid thät" the ecötiOphic efficiency of the . graup is 0.95. The diet is based on qualitative intor~adcin ~nly. - - e Alzne/ida, oiher Cruitacea, Echinodennilta, and OÜter lnvertebrates ' _ Orily ver;. Ii~iied infonnationwas available on .these groups.. for ati, a prOduction rate of 3 yeai- 1, a gross foöd conversion efficiency of 15%, and an ecoti'ophic efficiency of 0.95 were aSsumccL 'Tbc diet' compositions arc aSsumed based '~n qualitative information, e.g., Taft 1975 arid various reportSfrom the ICES Benthos WG. . - .PhYtoplankton The primaiy productiori is estlrriated to armirid 200 g C iri-2 year-1baSed on .Friulsz and Gieskes (1984). "ibis corresponds to approximately 2300 gwet weight _Iti-2 year-1 (Conversion: 1 g C ..; 15 kca1; 1 g wet weight .::.:. 1.3 kC:l1; Jones 1984; leES 1989~ Fig. 9.3~). The biomaSs estimate of 3.7 gCm-2 (oi 43 gWw m-2) is tiased on infonnation given by iIanncin arid Joires (1989) for the southem Noith Sea.

-8 DetritUs Input foi detritus is not reqtiireei; An estimate cf detritus "biorriass," Le. amount of organicmatcirial is 4.3 g C m-2 (50 g WW· mm-2) reported by Hannon and loires (1989) for the.southem North Sea.

l <' '...... \.' • Results arid Discussiori

, Some cf the major results from this preliminary estimatlcn of the 1981 Ncrth Sea fOOd web stiucture are presented in Table 1. It is of interest that the system is baIancro, and thai the consumption iri the system can be accommOdatect by the primai-y produclion. This is shown by the ecotiophic eff1eieney cf phytoplCUlkion of 0.76, which iridicates that some 3/4 of the primary produetion is consürried in the system. Ta same exteilt iltis support the findings of laige scale autolysis cf phytoplanktOn repcirted by e.g. Fransi and Gieskes (1984).'1t shoüld ä!so be ncted tha.i the ecotrophic efficieney of detritus is estimated to 0.89, indicäting that 89% of the flow that enters the detritus box exit frorn it again. Thc remaining may be exportCci or dep?~ite(i.:, . . . Pre~otis. sludies of.the· Ncith. Sea have discussed how fish foOd requirements . caIi be met by the system~ Steele's (197,4) esiiriiätes cf eonsümption by fish were cither emde baSed ,on known iandings, and a.ss~med ~atunil mortallties ~ultipli,~ by)O to 3.ccO\int for fm ccnversion efficieney. The stUdies of Jones (1~82b~ 1984) were more detiilleci ineoipci~tirig sevecil.inveiteb~ie groups, yet the overalleonclusion from these studies is aS. for the present: it is Possible to eonstriICi a balailced of . the North Sea 'without grcss violations of known' relationsliips arid physiologicil , , ,. " . ~ ." processes. More speCiflc examinaiion of the roI(: of individu3.l groups and how theSe compare is possible using the present type of mOdel. This can beb of importance as a fonn for v3.lidation ofprocess oriented sttJdies cf iiophic groups~ As an exarnpie Bailey .änd KtirWik (1984) estimated for Norway po~t in tbe no~ein North Sea the mean tct3.l mortaIity rate to be 2.57 year2 far the penod 1960 to1983. This corresponds very weIl ,...... to the estimate of 2.18 year 1 obtaineci from the MS WO daci base and usea here. e SimÜar studies for other groups - also nein ~fS species - wculd be cf interest for further development of the modeL ' As an exarnple of cor1f1ictirig estimates Lindley (198(l) gave estimates of prodtictlon and biomass .of two (out of three) domiriant speCies of Euphausiacea, 11lysanoessa ineiirils and T. raschi, of Etiphausüds in the NE Noith Sea and NW Skagercik in 1966 arid 1967. Assuming a carbon/wet weight coriversion fador of 10, a mean depth öf the Northem North Sea of 100 rit, that euphausÜds' oCcur in h3.lf of the North Sea~ arid thäi the third dominant species, Jrfeganyctiphanes norvegica, adds 50% . tO the biomass, a biomass of 1.8 g m-2 ci>uld be estimated. Iri the preserit mOdei a biomass of 8.3 g m-2 is estimated, iridieating, a discrepaney that should c3.ll for iriereaSect attention to this trophieally imPortant group. . ' It may be nated that the food conversiori efficiencil~s C;Gross eff.") reported in -fable i are unreaIisiiCally high' (35, 24 and 36%) for thiee Cf the four gadoid MS species (cod, whiting, and haddock); Effidendes in the ränge of 5-15%, deperidirig on species; size, food type etc, are mtich more realistle (paloheimo and Dicide 1966, Jones 19823,).

9 r.

The conversion efficiencies are high because low consumption rates are used in .the MS WO programs. These low consumption rätes have been adoptro iri order not to overestimate the effect of prerlatiori in· the ilS WG programs (H. Gislason, pers. comm.). '. . The problem wlth the low consumption rates .far thi: gadoids is iridicative of the problem of acquiring or maintaining an overview of large, complex models. As the cast for development arid parametii~tion ofsuch modeIs are huge, effort should not be spared when it comes to ·additional data· ariälyses of the qUalliY .of the· data set, especially when it can be done withmit Iieec1 for additional däta äcquisition; Applicatlon of the present methodology is one eiample of ihis...... , For the fish SpeCies the ecötrophic efficiencies iridicate that only 49 to 86% of · the prOduction iS actu3lly used iritbe.system' (Table 1). These low efficiencies reflect thät the residu3.i mortalltY in the MSVPA ron hiS riot been fully accOunted for. Tbe MSvPAonly iriclude predatiori by theMS speeles. To c6rrect for this the MS WO aSsurnes an "other" predadori niörtaIltY (MI)and arion-pr~tlon morta.llty (110) for äll groups; These moitalitlesare paräirietrlzoo based on ver} limited Information espedallY MO, which is aSsumed to take values bi:tween. 0.1 and 0.2 year1 for the different groups ('fable 3).The MI teiin 1s not iricluded in ECOPATHmodeIS where alt predation riiortalliY is ass\lIned. t6 be acc~unt~ for. The niortallij rates are, presenied iri · Table 3 for companson; Genei'ally the M2 values are greater in the ECOPATH mädel · than in the MSVPA. This is asexpected as ECOPATH includes more predators; Yet the ECOPATH M2' is smalle.r than the summedMi arid M2 from the MSVPA irirlicatirig that not 3011 of the' ~Ü .morta1itY ean' be accotiiiioo for' in tbe ECOPAfu mOdel. This is reflected by the ~1O vaiues of ECOPATH being higher than ihe 1-.10 of · MSVPA...... Table.3. MonalitY rates (year-1) based on ECOPATH and. MSVPA analyses. Z (,,; PIS) ,is thetotal monality rate, and is assumedto eQual PIS in steady state, F is the monality, BA is the biorriass accumulation rate, M2 is predation monality, while MO is non-predation monality,. and M1 is predation by ·other fish predators· in the ., MSVPA; Fer ECOPATH Z = F + SA + MO + M2;· Fer MSVPA Z ~ F }- BA • MO } e Ml + M2. . ECOPATH MSVPA >-" '~.~ .~ • ,-~..-... . . Group Z F BA MO M2 MO Ml M2 ., .- 1. Cod 1.11 1.01 -0.23 '0.27 0.07 0.20, 0.07 0.06 2. Whiting 0.84 0.56 . -0.30· 0.34 0.24 0.20 0.17 0.21 3. Saithe 0.58 0.31 0.06 0.21 0.00 0.20· ,0.00 0.00 4. Mackerel 0.29 0.24 -0.10 0.15 0.00 0.15 0.00 0.00 5. Haddock 1.37 0.46 -0.01 0.50 0.43 0.20 0.35 0.36 6. Herring 1.04 0.35 0.21 0.26 0.22 0.10 .' 0.16 0.22 7. Sprat 1.21 0.63 -0.55 0.60 0.53 0.20 0.39 0.54 8. Norway pout 2.48 0.41 0.48 0.77 0.81 0.20 0.57 0.81 9. Sandeel 2.02 0.45 0.47· 0.37 0.73 0.20 0.28 ·0.62 10. Plaice 0.65 0.35 . 0.21 0.09 0.00 0.10 0.00 0.00 11. Sole 0.66 0.33 0.23 0.10 0.00 0.10 0.00 0.00 12. Ray .' 0.44 0.00 0.44 0.00 13. Other pred. fish 0.87 0.00 0.87 0.00 14. Other prey fish 0,48 0.00 - ,0.02 0.45

10 L100nd

~ H.",.s. --+ Otber "PO" -t- Flow 10 dettitul ~ n,spUQI~n ., 0' o • ....s....

* 1111 ~ ~ . ~I .0000 CoO •• 0: 01 ....,I I 1.0 00 ~'n L.- .... .,. •• Otw .~~ 01 01 • pr... 10 .,;L" I hOl ,.u • 0 lelJ ILI. ~ ~~~ • 0 0 I -~ --II.n ~' 00 - I"" JW1 01 '0 o. ~ ~I.U 1_~ ~.. '-- ..... W.i .,. IU." ~ 1'- '-- '7.:" 11"

~ ö : J; ~ ;!~~I~ ...... '= 00- - .. 0 ..> 1.1 --. Cl' .-. . .!! .. o • f_ I"" _ u •• ~ o. •• s. - -r;).,Fta :E I~~, -:--:-.r- .- ~'·10 .. ~ ...... , ILt o "*' .,. Uf." Otw .... lGoI) .= I ...... n.,.. Oll 11.1.1' n 00 -~ '''J 1111' I~ sn-n,.1.1 . ~.,. . ~ -- ••<• • 0 ..•

0 ~ 0 . ~ ~18 0 n . ;\• w _ . ~I . . ~1- -f~ .... llolIoUI _... D.50 '·UD

11 •• 11

Figure 1. A quantified network of trophic interactions in the North Sea in 1981. The volume of the boxes (which are assumed cubedl are proportional to the biomasses of the groups. The boxes are arranged on the Y-axis by trophic levels as estimated by ECOPATH 11. All groups are balanced so that input equals output. Flow exiting a group do so from the upper half, while flow enter on the lower half of the boxes. Flows exiting a box cannot branc~, but lan unite with flows exiting other groups. Flows are expressed in t wet welght km- year- .

11 A graphiCal representatiori of 'the quantified food web for the North Sea in 1981 . is given in Fig. 1. Here all groups are balanced so, thai input equals output. The flow chart is consinicted fOllowing some mIes of standardization aimed at enhancing visual interpreiati~~ (pauly arid Chnstensen in pr~ss). The most imporumt of the rules are given in the figure legend. It can be noticed that the boxes are arranged on the Y-riis after irophic levels. These trophic levels are fractionai and calculated based on the diet compOsitieris. ' Additional arialyses werc camoo out usirig various routines of. ECOPATH It The trophic aggregation routine prOduces the results in Table 4. The tabie shows that . the iilliX>rtant groups on tiophic levei II eire the "other invertebiates" and the cOPePOds, on level UI "other crustaceans';, juvenile fish and sandeeis, on level IV Norway Petit arid saithe.· . , , Based, on the flows it is possible to estimaie tiirisfer 'efflCiencies by trophic leveL These efficiencies .are given on ihe bottern lin~ of Table 4. The ~sfer efficiericies reflect a problem with the parametrizatiori. For tiophic level II the high efficiency (19.4%)can be attrlbuteci ,ta. the infltience of the high food conversion efficiency thai is tised for copePOds. The high efficiencies on the upper trophic levels caused bythe low ccinsumpiion r:ates of tbe piedators is not noticeablereflected in 'ihe trarisfer efficiendes because of the small contnbutlens of these groups to the overiill flow. The efficiendes compares weii witit effidendes recorded iri ether systems (Christensen 1992). . ',' '

Tab/e 4. Äbsolute fiows by discrete (I to ,VI) trophic level. The groups are soned by trophic levels (TL). The transfer efficiencies are calculated including catches. .

TL Graul) 11 11I IV V VI

4.32 Saiihe 0.1 1.4 0.7 0.03 3.95 Whiting 0.5 1.6 0.3 0.01 3.81 Other pred. fish 1.8 6.5 0.2 3.78 Cod 0.7 0.9 0.2 0.02 3.75 Herring . 1.1 2.7 0.1 ...... _ .... _ .. _1 n nn 3.70 ....."'.... CICI 1.0 1.6 0.1 v.vv 3.64 Norway pout 10.9 16.6 0.7 e 3.54 Ray 0.8 0.7 0.0 0.00 3.49 Haddock 1.7 1.4 0.1 0.00 3.09 Sprat 4.3 0.4 3.05 Euphausiacea ,128 6.0 3.03 Juvenile fish 45.7 1.4 3.01 Sandeel 32.8 0.3 ,0.0 3.00 Sole 0.4 2.90 Plaice 0.2 1.6 2.80 Other prey fish 3.0 12.2 2.30 Other Crustacea 162 69.3 2.00 Annelida 32.5 2.00 Copepoda , 600 2.00 Echinodermata 142

2.00 Other invertebrates j,~ 685 1.00 Phytoplankton 1231 1.00 Detritus 865

Total: 2096 1624 313 41.4 2.5 0.07 Transf. eff. (%): 19.9 14.0 . 9.9 11.4

12 Result from the mixed trophic impact routine anaiysis are showri in Fig. 2. This 'figure gives a very inforrriatiori nch picttire of how the different groups iri the system impact each other trophically through direct as weH as indirect interactioris. These , impacts may he cascading down the irophic web; whiting for exarnple has a negative impact on NOrWay peut due to predation; but a positive impact on Euphau.siacea, 'the mahi prey of Noeway pout ' ..... '. . ' Because of the cascading effect it is tempting to speculate: what would hapPen if orie reduced/increased the amount of whiting thfough a change in fishing pattern? The " routine is however not designed far arisweririg questions like this as it d6es not have a .time dimension and d.nnot ariiicipaie qualitative changes of the food web. '. . '. However, the mixed irophic impact routine cari be seen as a simple sensitivity analysis. It gives an idea of how important the different groups in the system are for the trophic' dyminiiCs, and therefore of where gams from improved parameter estimation' Can be expected~ . . It is noted that the model in Fig. 1 is Qrie possible represencition of the trophic interactions in the North Sea. Other assumptions would lead to somewhat, but probablY not very, different representatlons. Especially one may aSsumethat better parameter estimates for the invertf:brates would help to resti'ain the range cf possible descrlptions of the sYstem~. . The lack of accessible parameter estimates of the' rilaiil invertebrate groups of the North Sea retiectS a neecI for pr6cess orieni6d studles ahn&! a pröducing such estlrriates. Yaluable. eCological work is conducted but sttidies fcicused on prOduction aSpects arid on energy flows hetween the imPortant invertebrate groups and to their predat6rs are callect for. Fisheries biologisis have over tbe last deeade fcicused on ene!gy flow studies iri order to improve fishenes management, notably to' päriimetrize the MS ,wo progriuns. '1\, similar deveIopmeni in, invertebrate , biology could, lead to b6th increasoo _communication between the disdplines and better understanding of the eeology of the .. Norih Sea as a whole. ., . e Of importance is also that such a development will address the increasing new for rrianagement of marine ecosystems so. that the interests öf not just tbe are taken into account. (pauiy i992)~ Asstressed bY. ICES 3.Iso environmental . concern should be taken (Anon~ 1992). It is hoped thai studies such as presenied here may heipto support tbis deveIopment. . ' . .Ackno\"iedgmerit

I .. " .. .. I_ ' , • :", .1 .:.. ".. " ~.', ','" " , ;; • ,~ '.' . A major part ~f'this ,work was carriedout whilt~ p~cipating in. the ICES. 1992 . .MS Working Group. ThankS to the ,Working' Oroup, .riotably its ch:iirperlmn Steven Murawski for support arid interest. Also to Henrik Gislason for ä roll of the MSVPA, arid to Niels Oaan arid Dariiel Pauly for advice arid discussions. ThankS to Scindra GayoSa for graphical design. The support from DANIDA for the "Global comparisons of aquati~ ecosystems" project at ICLARM is appreciated.· '.

, 13 IMPACTED Gnours ..VI ~ iQ ~ .. ~ ..u ~ .Q c: ~ .. .. 0 ~ '5 ..u ~ .. t: ~ 0 -ä >- 11I § ~ .Q. .~ ~ .. C Q; .>I Q; ... .. ~ > ~ .. .!! 0 u >- Ci. Ci. ~ 0 :l Ü .5 .. VI Iii a Cl> GI '" 0 Ci. c: .. 0 ~ ~ .. 0 C -GI '0 ~ '0 .. ;; GI ~,:§ ...u ~ .\:! GI .<: ·s .. .g > ~ c:: ~ .. '0 '0 ~ - -E c: .. >- - .<: > ~ Cl> - ~>- 0 Q. Ö .. .. ö c:: % -5 :) ...... ~ u ::~ :: J: J: V1 Z V1 a: V1 a:: Ö Ö a.lI:i ö ~ 0 ~ ., a J: -. -- •" ------w. • - -•." - ---._.. • .. - • • - -• -

'h' ,,_ • •• •• • -. •• • __..--__".__.-...... -'.__1-0...··_._-'-..------~~ .-•• .'tU. q ••• ',,. ••..1__•_ ~ ~ .•-...... ------.,,'--,. I -. ----~. . - -. ... - . - •.." ...... 11I "'';'' ---JIIL.. -.;,._._LJlLJIL,.--.;.•..-- • -;.; •. ______W'-__,...J.--....--·__I.. - Ii - Other inveriebrates - .-• • ...... I W .~ Phytoplankton - __ 1-1.__-1.--.:'LI. . .' h __ ·__ _ ,,-'.W'__

Juvenile tish -• 1_=_·---....__·-,;....,;.·------• Detritus HarvllSt I······· = •• -

'. . "' ...,. , " ...... - . .-",. Figure 2. Mixed trophic impacts in the 1981 North Sea ecosystem. The bars quantifythe direct and indirect trophic impacts that the'groups on the left of the histograms have on the groups mentioned at the.top. The impacts are relative but comparable between groups. Positive impacts protrude above the baseline while negative are below.

14 Refererices Anon. 199'2. leEs to strengthen itS environmental side afterwide dlscussion. . ICES/CIEM Information 19: 1-2. . Baden; s.:? 1986. Recent changes in the Kattegat arid Skagernuc ecosystem arid their possible interdeperiderice. Nat. Swedish Environ; Protection Board Rep. 3157; 91 . p. . Bagge, O. ,1978. Kattegaiprojekt - Delrnpport. Interna! Report No. 96. Darush Institute for Fisheries arid Marine Research. 76 p~ . Bailey, R;S;,and P~A. Kunzlik. 1984. Vanation in growth arid mortalltY rates of NoriVay pout Trisopterus esmarldi (Nilssan). ICES C;M. 1984/G:70. Chrisiensen, V. 1992. Neriverk analysis of trophic iriteractions in aciuaiic ecosystems. Ph.D. thesis. Royal Danish School ofPharrriacy. 55 p. Christensen, .v~, arid ci. Pauly. 199230. A guide ~cithe ECOPATH II software system (~ersion 2~ 1). ~CLARM SoftWare 6, 72 p: International Center for Living Aquatic Resources Management (ICLARM), Manl1a~ ,. '. .

'" " ," " t ." c "":' ,.", ' . ' Chnstensen, 'v., arid D. Pauly. 1992b. ECOPATH II - A software forbäIancing steady . state models and calculating netWoi'k characteristics. ECol. Modellirig. 61: 169-185. Christensen, V., arid D. PauiY. Trophic Models of Aquatic ECosystems. ICLARM Conference Pröceedings 26, 000 p. (Iri press). . . Creutzberg, F. and G.C.A. Düineveld. 1986. The role ofthe lesser weeverTrachinus vipera .andth.e dab Liinaruia limanda.in thc berithic system of the Southern. North Sea; BIOlog1Cal Oceanography Committee, Int. Counc. Explor. Sea, Cons. Meet. C.~. 1986/L:4, 10 p. .: ,;' , " .' . .. .. Crisp, D.J~ 1975. S~ondary.pr6ductiviiyinthe sea, p. 71~89. In PiooucüvÜy of world ecosystems. National Academy of Sciences; Washington, D.C...... Daan;' N.; Editor. 1989. Däia baSe report of the stomach sampling projeet 1981 ~ leES coop. Res. Rep. No. 164j '144 p. ..' .. riaaii, N, pj._~Bromiey, J.R~G. Rislep, arid N.A. Nielsen. 199Ö. ECology of Noith Sea fish~ Netherl. J; Sea Re~. 2~(2-4): 343-386." , Dahl, K. arid E; Kirkegaard. 1987. The dil~tarid consumption of horse mactrerel . (Trachurus trachurus) in the &Stern North Sea, August 1986. ICES Counc. Meet. 1987/R:43; 23 p. .. Desilva; S.S.. 1973. Foods arid feeciirig habits of the herring dupea harengus and sprat C. sprartus in irishore waters of the west coast of Scotland. Mar. Bio!. 20: 282-290. Frarisz; li.G. anci W.W.C. Gieskes. 1984. The unbalanceof phytopiarikton and, ._ copepcids in th6 North Sea~ Rapp. P.-v. Reun~ Cons. int. EXplor. Mer 183: 218- 225. . dordo~; ~.D.M. 1977~.The fish Poptilations~n i!lshorev.:aters o~ the~est of Scotlarid. The blOlogy of the Norway pout (Trisopterus esmar/di.) 1. FlSh BIOI. 10: 417-430. Rarinon, B..and C. Jolris. 1989. A se3.sonal analysis ci the sciiithern Noi'th Sea ecosystem. Ecology 70(6): 1916-1934~.. . . ICLARM. 1992. ICLARM's Strategy For International Research on Living Aquatic Resources Management, Philippines. 79 p. + Appendix 30 p. .' '. ICES. 1989~ Rep6It oi the MuitiSj:>ecies Assessment Working Group; Copenhagenj 7:. , 16 Iurie 1989~'ICES C.M. 1989/Assess:20, 176 p. .. ICES. 1991. Report of the Multispecies Assessment Working Group, 4-13 December 1990, Woods Hole. ICES C.M~ 19911Assess:7; 246 p. '.

. 15 ) I

I •

Jarles, R. 1982a. Ecosystems, food chairis arid flsh yields; p. 195-240. in D. Pauly arid . G.t Murphy (eds.) Th~ry and)nCl!lagem~~~ of tr~pi~ fi~herie~. ICLA:.~.M~onf. Proc. 9, 360 p. Interriauonal Center for Llvmg Aquaue Resources Management;· Mariila, Philippinesand Division of Fisheries Research, Commonwealth Scientific arid Industrial Research Organisation, Cronulla, Atistralia~' . Iones, R. 19821,. Speeies interac:tions in the North seä.; p. 48-63, In M.C. Mercei (ed.) Multispecies approaches to advice. Can. Spec. Publ. Fish. Aquat. Sei. 59, 169 p. . , Iones, R. 1984. Some observations on eriergy transfer tbrough the North Sea amI Georges Bänk f60d wehs. Rapp. P.-v. Reun. Coris. int. EXplor. 1fer;183: 204-

~17:. ,q,','.'..',. , '" . " ." . Lagardere,J.P. 1987. Feeding ecology and dailyfood consumption of common sole, So/ea llu/garis Quensel, juveniles on the French Atlantie coast. I. Fish Bio!; 30: 91- 104. , . L3.St; I.M. 'i982. ne' f~ ofjuvenile sprät Spranus s[Jralius (LiMaeus 1'758) 'and .. ' herring C/upea harengus (Linnaeus 1758), in irishore waters of the Southem North Sea~ ICES Coune. Meet 1982/H: 12, 6 p. , Last, i.ir. '1985~ Further observations on the food ofO-groüp sprat Sprarrus sjJrarru.s (Linnaeus 1758) and herrlng C/upea harengus (Linnaeus 1758) from the North Sea. ICES Cmine. Meet. 1985/L:35, 6 p. , Undley, j.A~.1980. Population dynarmcs and prOduction ofEuphausüds. II. '" ThysaiweSsa inennis CÜld T. raschi in the North Sea and American coastal "vaters. Mar. Bio!. 59: 225-233. PaIomares, M.L. and D. Pauly. 1989. A multiple regressionmooel for prediciütg the food consumption of marine fish populations. Aust.- J. Mar. Freshwater Res. 40: 259-273~ Pauly, D. 1989. Food ~onsumptiori by tropical arid iemperate flsh populations: some geneializations. J. Fish. Bio!. 35(Suppl. A): 11-20.' , , Pauly, D. Assessment methodologies arid fisheries management: how to treep ritakirig sense~ PrOceedi~gs of the \Vorld Fisheries Congress, 2-8 May 1992; Athens, Greece. (In press). ., Patlly, n., ärid V. Christensen. Graphical represeriiation ofstea.dy state trophie, ecosystem mOdels, p. 000-000. In V. Christenseri arid D. Pauly (eds.) Trophic m~els of aquatie ecosyst~ms. IC~1 Conference Proceedings 26, 000 p. (In press). '., , ' Spari~, P. i9~H. Iriti-oouction to multispecies virtu31 population 'analysis. ICES mare ~Cl. Symp. 193: ;12-21., " " . " Sparholt, H. 1990. An estirriate of the total biomass of fish in the North Sea~ I. du Cons~ 46: 200-210. , .' Steele, J~H.<, 1974.•• ,..The structure• of marine, ecosystems.• '"",'BlackWell'., " ' Scientifie Publication, Oxford. 127 p. , '.. .', . . Steele; I.H., arid E.W. Hellderson~ 1977. Phinkiori patches in the ncirtheni North Sea; p. 1:..19. In J;H. Steele (ed;) Fisheries mathematics. Academic Press, London/New York., ' illanowicz, R~E. ECcisys~m' trophic fo'urirlations: Lirideman exonerata; p. 000-00o. In , B.C~ Patten arid S.E. J4>rgensen (eds~) Complex ecology. Prentice Hall; Englewood CHffs. (In press). . mariöwicz, R.E. arid C.J. puccia. 1990. Mixed trophie impacts in ecosysiems.. Coenoses 5: 7-16. .'

16