The impact of trophic changes over 45 years on the Eurasian perch, Perca fluviatilis, population of Lake Geneva

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1 Aqut. Living Resour. 21, (28) c EDP Sciences, IFREMER, IRD 28 DOI: 1.151/lr: Aqutic Living Resources The impct of trophic chnges over 45 yers on the Eursin perch, Perc fluvitilis, popultion of Lke Genev Jen-Pul Dubois 1,, Christin Gillet 1, Ndine Hilgert 2 nd Gérrd Blvy 1 1 INRA, UMR CARRTEL, Centre Alpin de Recherche sur les Réseux Trophiques des Ecosystèmes Limniques, 75 venue de Corzent, BP 511, 7423 Thonon-les-Bins Cedex, Frnce 2 UMR Anlyse des Systèmes et Biométrie, ENSAM INRA, 2 plce Pierre Vil, 346 Montpellier Cedex 1, Frnce Received 11 December 27; Accepted 12 September 28 Abstrct The chnge in ctches nd men size of one-yer-old perch (Perc fluvitilis) in Lke Genev ws studied between 1957 nd 25, nd relted to trophic chnges nd verge temperture. The sttus of Lke Genev, ssessed on the bsis of totl phosphorus concentrtions, switched from being oligotrophic before 196 to eutrophic, with totl phosphorus concentrtion reching nerly 9 µg L 1 in In response to mngement mesures, the trophic sttus then returned to mesotrophy in the erly 2s. Zooplnkton is the min food consumed by young perch, nd quntities present (nnul biovolumes of zooplnkton) were recorded throughout the study period. The lke wter temperture ws lso recorded. Dt obtined from perch ctches nd perch spwns enbled eleven strong cohorts of perch to be identified. Strong cohorts dominted the stock for three yers, until they were mssively cught by fishermen. Yields hve fluctuted widely, incresing rpidly until 1975, nd subsequently decresing, with n exceptionl decline between 1976 nd During the period , unfvourble climtic conditions in spring were probbly the min cuse of this fll in perch yields. For the other periods, perch yields nd the men size of one-yer-old perch were significntly correlted with trophic prmeters, totl phosphorus concentrtion nd zooplnkton biovolume. Correltions re higher if only strong cohorts re tken into ccount. As result of the re-oligotrophiction process, perch growth hs been progressively reduced, ge t first mturity delyed nd strong cohorts become less frequent; the men size of + individuls in strong cohorts is significntly smller thn in the other cohorts, suggesting popultion density effect in the context of limited supply of zooplnkton. During the study period, trophic chnges in Lke Genev hve hd more impct on perch growth nd yield thn hs temperture, since no significnt correltion could be detected between wter temperture nd perch growth. Key words: Pre-Alpine lke / Fishing yields / Growth Eutrophiction Phosphorus Zooplnkton Perc fluvitilis Résumé Impct des chngements trophiques sur les popultions de perche, Perc fluvitilis, dulclémn, durnt 45 ns. Entre 196 et 25, l évolution des cptures totles et celle de l tille moyenne des perches (Perc fluvitilis) âgées d un n du lc Lémn ont été étudiées en reltion vec l évolution trophique et l tempérture moyenne du milieu. Le sttut trophique du lc, estimé à prtir des concentrtions en phosphore totl, évolué de l oligotrophie vnt 196 jusqu à l eutrophie, le phosphore totl tteignnt près de 9 µg L 1 en Suite ux mesures d ssinissement, le lc est redevenu mésotrophe dès 21. Les quntités de zooplncton, principle nourriture des jeunes perches, ont été mesurées (biovolume nnuel de zooplncton). L tempérture églement été mesurée. En se bsnt sur les nlyses fites sur les cptures et sur les études menées lors de l reproduction, onze fortes cohortes de perches ont été identifiées. D une mnière générle, les fortes cohortes constituent l essentiel du stock de perches pendnt trois ns, jusqu à ce que les pêcheurs les ient décimées. Les cptures présentent d importntes vritions inter-nnuelles ; les quntités pêchées ont ugmenté rpidement jusqu en 1975 et diminuent depuis, vec une chute exceptionnelle entre 1976 et De 1977 à 1981, une succession de muvises conditions climtiques printnières explique probblement cette chute des cptures. Pour les utres périodes, les quntités de perches cpturées et l tille moyenne des perches à 1 n sont corrélées ux prmètres trophiques (concentrtion en phosphore totl et biovolume de zooplncton). Les corréltions sont plus élevées si seules les fortes cohortes Corresponding uthor: dubois@thonon.inr.fr Article published by EDP Sciences

2 42 J.-P. Dubois et l.: Aqut. Living Resour. 21, (28) sont prises en compte. Avec le processus de ré-oligotrophistion, l croissnce des perches diminue, l âge de l mturité sexuelle est retrdé et les fortes cohortes sont plus espcées ; l tille moyenne des individus + des fortes cohortes est significtivement plus petite que celle des utres cohortes, trduisnt un effet mrqué de densité-dépendnce vis-à-vis de l ressource limitée de zooplncton. Durnt l période étudiée, les chngements trophiques du lc Lémn ont eu un effet plus mrqué que l tempérture sur l croissnce et les cptures de perches, puisque ucune corréltion positive n pu être mise en évidence entre l tempérture de l eu et l croissnce ou les rendements de l pêche des perches. 1 Introduction Lke Genev, pre-lpine lke in Western Europe, underwent eutrophiction during the 196s nd 197s. In the erly 198s, restortion progrm led to reduction in phosphorus inputs, nd resulted in progressive reduction in the phosphorus concentrtion: process known s re-oligotrophiction. The yerly men totl phosphorus concentrtion (totl P) in the lke wter rose from 15 µg L 1 in 196 to 89.5 µg L 1 in 1979, nd then fell to 29.4 µg L 1 in 25 (dt from the Interntionl Committee for the Protection of Lke Genev: Commission Interntionle pour l Protection des Eux du lc Lémn, CIPEL). The rise nd fll in totl P hveledtoprofound chnges in the biocenosis nd food web structures of the lke. Previous studies hve described the response of phytoplnkton ssemblges (Anneville et l. 22), nd plnktonic rotifer (Molinero et l. 26), cldocern, nd copepod communities (Anneville et l. 27). The effects of eutrophiction nd re-oligotrophiction on fish popultions in Lke Genev hve been studied minly in slmonid species, Arctic chrr (Slvelinus lpinus) (Chmpigneulle nd Gerdeux 1995) nd whitefish (Coregonus lvretus) (Gerdeux 24). Eursin perch (Perc fluvitilis Linneus) hve received less ttention until now, despite the importnce of this species for the fisheries of Lke Genev, nd the drop in lnded ctches recorded over severl yers (Gerdeux et l. 26). Perch re found in lkes with wide rnge of trophic conditions (Jeppesen 2), nd their recruitment seems little ffected (Mssol et l. 27). Long-term surveys hve reveled tht chnges in trophic levels nd food resources cn hve considerble impct on the growth nd survivl of perch popultions. Perch hve been seen to grow fster during eutrophiction in mny lkes, including Lke Erie (Nepzy 1977), Lke Constnce (Hrtmnn 1975), nd Lkes Hjlmren nd Mlren (Rundberg 1977). In Lke Constnce, the increse in professionl fishing ctch during eutrophiction ws due to stronger yer-clsses, better growth rtes nd reduction in cnniblism (Eckmnn et l. 26). Perch growth is lso ffected by fish density (Mehner et l. 1998; O Gormn nd Burnett 21); perch in lrgepopultionsusullygrow slowly, nd ny reduction in their number results in improved individul growth, s observed in Lke Windermere (Le Cren 1958). Lke re-oligotrophiction is recent phenomenon, nd its effects on fish communities hve been less mply documented thn those of eutrophiction (Gerdeux et l. 26). To dte, the effects of re-oligotrophiction on perch biology nd popultion dynmics hve only been described in Lke Constnce (Eckmnn et l. 26). As fctor driving biologicl ctivity, wter temperture cn influence the growth of perch (Le Cren et l. 1977; Mehneretl.1998; Pxtonetl.24). However, one could sk wht the reltive importnce of temperture is with regrd to chnges in the performnce of perch popultions subjected to mjor trophic chnges. The present study investigtes the effects of eutrophiction nd re-oligotrophiction on chnges in perch popultion: nnul ctches by fishermen, nd the growth of + perch in Lke Genev. Long-term series of dt re vilble covering the periods of eutrophiction nd re-oligotrophiction. These dt include wter physicochemistry, phytoplnkton nd zooplnkton communities (dt from CIPEL), nd fish yields (dt published ech yer by the relevnt French nd Swiss Government deprtments). We ssessed the reltive importnce of chnges in trophic fctors (phosphorus nd the mount of zooplnkton, min food source for young perch; Romre 2), nd temperture fluctutions on the chnges in perch growth nd yields. 2 Mterils nd methods 2.1 Study site, phosphorus nd zooplnkton surveys, temperture recording Lke Genev (46N, 6E), locted on the border between Frnce nd Switzerlnd in Western Europe, is the lrgest lke in the pre-lpine region, with n re of 582 km 2, nd volume of m 3. The qulity of its wter (nutrient concentrtions, plnkton quntity nd composition) hs been regulrly nlysed since 1959 by CIPEL: Dt on physico-chemistry, productivity nd the bundnce of phyto- nd zooplnkton in the lke re determined in its centrl re, between Evin nd Lusnne where the lke is deepest (39 m). CIPEL smpling cmpigns re crried out every month; twice month during the growing seson (My to October), nd once month for the rest of the yer (November to April). Vlues of the different prmeters re then clculted on yerly bsis. Totl phosphorus concentrtion (totl P), expressed s the men P concentrtion (µg L 1 ) of the lke, is the men vlue of ll the P mesurements recorded t 2 different depths through the wter column over the yer (CIPEL protocol). Surfce wter temperture ws continuously recorded from 1991 to 25 by probe connected to n utomted wether sttion (type Enerco 411, Cimel Electronique, Pris, Frnce). Prior to 1991, temperture ws recorded by mechnicl temperture recorder (Jules Richrd Instruments, Argenteuil, Frnce). The nnul sum of degree-dys bove 14 C ws lso clculted. This prmeter ws shown to be positively correlted with perch recruitment in Lke Windermere (Le Cren et l. 1977). A 2-µm mesh size plnkton net huled verticlly from 5 m to the surfce, thus tking in the trophogenic zone, ws used to collect the zooplnkton present. The plnkton biovolume ws then mesured bck t the lbortory in decnttion funnel; ny lge present floted bove the zooplnkton, nd were removed. The nnul bundnce, which is the cumultive

3 J.-P. Dubois et l.: Aqut. Living Resour. 21, (28) 43 mount of zooplnkton, is expressed s the settled biovolume of zooplnkton per unit re (ml m 2 yer 1 )(CIPEL protocol). 2.2 Fish study Since 195, professionl fishermen hve reported the volume of their ctches of commercil fish species to the uthorities. Dt re reported nnully in Frnce nd Switzerlnd. Perch re cught with bottom nets, seines nd trps. The minimum uthorized mesh size is 23 mm, nd the minimum legl size bove which perch cn be lnded is 15 mm TL (totl length). Scientific smples were lso tken with fishnets nd trps of different mesh sizes, rnging from 1 to 3 mm. Totl length ws mesured to the nerest mm on fresh fish. Sex nd mturity were recorded, nd the ge ws determined from the operculr bones; fish size t one yer ws determined by bck clcultion (Le Cren 1947). The regression (r) between perch size nd operculr rdius ws clculted from 3161 fish from Lke Genev cught between 1966 nd 25. TL = 15. X S (1) r 2 =.93, with 58 mm < TL < 373 mm nd 3.5 mm < X S < 23.9mm where TL (mm) is the length of fish when cught, nd X S is the operculr bone rdius (mm) when cught. Smples were vilble for 31 different yers. The length of one-yer-old perch (TL 1, mm) ws estimted using the following eqution: TL 1 = TL(15. X S )/(15. X S ) (2) where X S1 is the operculr rdius (mm) t the first nnulus. Of the fish nlysed, 71 nd 22 percent were 1+ nd 2+, respectively. When 1+ nd 2+ groups of perch of the sme cohort were nlysed, the differences observed between the clculted men size t one yer, nd those clculted from ech group never exceeded 5%, except in 1992 (8%). 2.3 Identifiction of strong perch cohorts by studying the fluctutions of spwner popultions Perch eggs re grouped in egg-strnds or ribbons. Ech femle lys one egg-ribbon (Thorpe 1977), nd this mkes it possible to ssess the number of mture femles by counting the number of egg-ribbons. This is esier thn trying to count the mobile dults (Lng 1987). The length nd width of ech eggribbon is correlted with the size of the corresponding mture femle nd histogrms displying the width of egg-ribbons cn be used to ssess the size structure nd ge of the breeding femles (Lng 1987; Gillet et l. 1995; Dubois et l. 1996;Lng 1999). To mke it esier to observe perch egg-ribbons, spwners cn be ttrcted to rtificil spwning substrtes (Gillet nd Dubois 1995). Artificil spwning substrtes, consisting of conifer brnches (spruce, Pice bies nd yew, Txus bcct), tied onto wire netting (length 2 m, height 1 m), were plced in Lke Genev from 1984 to 26 (Gillet nd Dubois 27). The spwning substrtes were lid t three different depths: 4, % of egg-ribbons Number of egg-ribbons b Yer Fig. 1. Perch spwns (egg ribbons) collected on rtificil substrtes, from 1984 to 26, in Lke Genev. () Size distribution: htched re: egg ribbon width up to 2 mm, blnk re: egg ribbon width 21 4 mm, drk re: egg ribbon width over 4 mm; 15 nd 21 mm perch correspond to 2 nd 4 mm spwns, respectively. (b) Number of egg ribbons per spwning substrte. 8 nd 12 m. From 1984 to 1989, severl spwning substrtes were lid t 4 m nd 8 m. From 199, only one spwning substrte ws lid t ech of the three depths. Artificil spwning substrtes were thus used to ssess the size distribution nd spwning intensity of mture femles ech yer (number of egg-ribbons per spwning substrte). The yerly vritions in the number of perch egg-ribbons cn be relted to the yerly fluctutions of perch yields, nd to the mortlity of perch popultions (Lng 1987). It ws possible to ssess the birth yer of strong perch cohorts in Lke Genev by combining dt on the number of egg-ribbons, the width distribution of egg-ribbons, nd the ge of femles t their first spwning. A lrge number of egg-ribbons with the smllest width would therefore indicte tht femles belonging to strong cohort hd just reched mturity. This phenomenon ws observed in 1984 (Lng 1987; Gillet et l. 1995;Lng1999), s mny 1+ perch reched their first mturity, nd so it ws deduced tht strong cohort hd been born in In order to detect the occurrence of strong perch cohorts during the period of re-oligotrophiction, observtions of the egg-ribbons were crried on until 26. AccordingtoLng(1987), when strong cohort perch reched the size for fishing, ctches incresed considerbly, nd the cohort ws lmost completely fished within three yers. For exmple the strong cohort of 1982 produced n increse of perch yields in 1983, 1984 nd 1985, with pek vlue in Pek vlues in the perch yield time series lso reflect the occurrence of strong cohorts in the fish stock. The percentge of mture femles of 2, 3 or 4 yers were ssessed from dt of the Vud county fisheries gency for the period , nd from direct observtions of fish cught by professionl fishermen from 1991 to Sttisticl nlyses Sttisticl nlyses consisted minly of identifying ny significnt links between vribles, nd in detecting chnges in

4 44 J.-P. Dubois et l.: Aqut. Living Resour. 21, (28) the progression of ech time series. Mens were compred using the Wilcoxon rnk test. Person correltion coefficients, denoted s r, were clculted between totl P, zooplnkton biovolume, wter temperture, perch yields nd the size of one-yer-old perch. Chnge ws detected by model selection method developed by Lvielle (25), which hs lredy been tested (e.g. Picrd et l. 25). This is stochstic optimiztion procedure, known s Detection of Chnges using Penlized Contrsts (DCPC), bsed on n dptive choice of the penlty function for utomticlly estimting the number of chnge points. The time series re ssumed to be piecewise sttionry, i.e. tht some of their chrcteristics chnge bruptly t some unknown instnts. These chnges cn ffect the probbility distribution of the series. The number of chnges is lso unknown. In this cse, chnge detection consists in estimting the timing nd number of men chnges. Most of the sttisticl nlyses were performed using S-plus softwre (S-plus 2). The DCPC procedure ws crried out with the Mtlb DCPC pckge, vilble t lvielle/progrms. 3 Results 3.1 Determintion of strong cohorts by studying the spwner popultion from 1984 to 25 nd the perch ctches from 196 to 25 The mesurements of the width of perch egg-ribbons in the spwning res from 1984 to 25 reveled succession of five peks when smll egg-ribbons (width up to 2 mm) occurred (Fig. 1). In 1984, smll egg-ribbons ccounted for high percentge of spwns; they were lid by 2-yer-old spwners belonging to the strong cohort of 1982 (Lng 1987; Gillet et l. 1995). Ech pek of smll egg-ribbons ws followed by pek of egg-ribbons of intermedite size (width in the 21 4 mm rnge), which in turn ws followed by pek of lrge egg-ribbons (width over 4 mm). Five peks were lso observed in the number of egg-ribbons per spwning substrte (Fig. 1b). The first two peks were synchronous with the smll egg ribbon peks, nd ech of the lst three peks ppered one yer lter. The ge when femle perch mtured in Lke Genev hd progressively incresed from 1+ to 2+ during the reoligotrophiction period (Tble 1). The pek of smll eggribbons observed in 1987 hd been spwned by strong cohort born in 1985 (ccording to Tble 1, Fig.1). From 1988, most of the femles were mture t 2+ nd, by deduction, the smll egg-ribbon peks observed in 1995 nd 1996, preceded by slight increse in 1994, were spwned by two strong cohorts born in 1992 nd 1993 respectively. At the end of study series, the pek of smll egg-ribbons observed in 22 ws spwned by strong cohort born in Strong perch cohorts were born in 1982, 1985, 1988, 1992, 1993 nd The highest pek of egg-ribbon per spwning substrte ws observed in It ws preceded by pek of smll egg-ribbons in The 1999 pek probbly corresponded to the spwning of 3- yer-old femles, born in 1996; Lng (1999) observed tht strong perch cohort ws born in Four peks of ctches occurred between 196 nd 1976, corresponding to four strong Perch yield (t) Totl P (µg L -1 ) Yer Zooplnkton biovolume (ml m -2 ) Fig. 2. Trends in totl phosphorus concentrtion (totl P, inµg L 1 ), nnul biovolume of settled zooplnkton (ml m 2 ) nd perch yield (t) in Lke Genev. Perch yield (t) r = Totl P (µg L -1 ) b r = Zooplnkton biovolume (ml m -2 ) Fig. 3. () Correltions between totl P nd perch yields; nd (b) between zooplnkton biovolume nd perch yields. Dt correspond to the mens of 3 yers of fishing of strong cohorts. cohorts tht ppered in 1963, 1966, 197 nd 1973 respectively (Fig. 2). Overthe wholeobservtionperiod,pek vlues occurred t three- or four-yer intervls, except between 1976 nd From 1977 to 1981, unusully cold growing sesons occurred tht were chrcterized by sums of degree-dys bove 14 C of less thn 5 (rnge ). Yers of birth of strong cohorts corresponded to higher sums of degree-dys: 676 in 1982, 624 in 1985, 688 in Chnges in perch yields during the eutrophiction nd re-oligotrophiction of Lke Genev; effect of climte chnges During the period of eutrophiction ( ), perch yields incresed from 1957 to 1975, nd decresed shrply therefter. The decrese continued up to 1981, when the period of re-oligotrophiction begn. Perch yields then first rose from

5 J.-P. Dubois et l.: Aqut. Living Resour. 21, (28) 45 Tble 1. Chnge in the % of sexully mture femle perch in Lke Genev nd totl phosphorus concentrtion. The numbers of fishes nlysed re given in brckets. Period Age of fish t spwning Totl P (µgl 1 ) (*) 58 (?) 73 (?) 1 (?) (*) 84 (232) 1 (16) (*) 4 (135) <1 (148) (present study) 43 (13) 77 (15) >9 (71) (present study) 4 (45) 61 (15) 1 (33) 32 4 (*) Swiss Fisheries Agency to 1984, but subsequently fluctuted widely (Fig. 2). During the whole study period, no significnt correltion could be detected between totl P level nd perch yield (r = +.14, df = 47, p >.5). The correltion ws however significnt if the yers from 1976 to 1983, corresponding to shrp decrese of perch yields, were excluded from the clcultion (r =+.44, df = 39, p <.1). The coefficient of correltion ws even higher if only ctches corresponding to the strong cohorts were tken into ccount, i.e. the sums of perch yields during the pek periods (sum of ctches during pek vlue yer, the yer preceding it, nd the one following it) (r =+.66, df = 8, p <.5, Fig. 3). Only one chnge in the men perch yield hs been detected by the DCPC procedure since 1957 (p =.8). This chnge ws estimted to hve occurred between 1977 nd 1978 (Fig. 4), when the trophic level of Lke Genev ws t its highest. Men perch yield ws bout 683 ± 64 t (11.7 ± 1.1 kgh 1 ) before 1977, nd 289 ± 32 t (5. ±.5kgh 1 ) fterwrds (p <.1, Wilcoxon rnk test, n = 49). From 1959 to 25, the overll zooplnkton biovolume ws positively correlted with the totl P level (r = +.75, df = 45, p <.1). After 1983 however, during reoligotrophiction, despite inter-nnul fluctutions, it never exhibited ny consistent upwrd or downwrd trend (p >.5, Mnn-Kendll test). Using the DCPC procedure, two chnges re thought to hve occurred in the time series of zooplnkton biovolume: between 1969 nd 197, nd between 1983 nd 1984 (p <.1) (Fig. 4). The yerly men ws high from 197 to 1983 (198 ± 8mlm 2 ). From 1984 to 25, the yerly men ws firly similr to tht clculted before 1969 (129 ± 5 nd 123 ± 11 ml m 2 respectively) nd ws significntly lower thn from 197 to 1983, when the trophic level of Lke Genev ws t its highest, bsed on the concentrtion of totl P (Wilcoxon rnk test, n = 47, p <.1). The coefficient of multiple determintion between zooplnkton biovolume nd totl P in combintion with wter temperture nd perch yield ws not very different from the coefficient of determintion between zooplnkton biovolume nd totl P lone:.6 vs..57. No significnt correltion could be detected between zooplnkton biovolume nd perch yield since 1959 (r =+.25, df = 45, p >.5). However the correltion ws significnt if the yers from 1976 to 1983 were excluded (r = +.6, df = 37, p <.1), nd ws even more mrked if only the strong cohorts were tken into ccount (r =+.9, df = 8, p <.1) (Fig. 3). The coefficient of multiple determintion between perch yield nd zooplnkton biovolume in combintion with totl P nd wter temperture Zooplnkton biovolume (ml m -2 ) 1-yer-old perch men size (mm) Yer b Yer Fig. 4. () Trends inperchyield (t) (fine unbroken line) nd zooplnkton biovolume (ml m 2 yer 1 ) (bold unbroken line); nd (b) men size (with stndrd error) of one-yer-old perch in Lke Genev (unbroken lines). Men levels nd chnges detected by the DCPC procedure re indicted by dotted lines. ws not very different from the coefficient of determintion between perch yield nd zooplnkton biovolume lone:.4 vs..36. Yerly mens of surfce wter temperture fluctuted widely. Severl consecutive wrm yers were often preceded nd followed by severl cold yers. Using the DCPC procedure, one chnge is thought to hve occurred in the time series of surfce wter temperture from 1957: this chnge ws estimted to hve occurred between 1987 nd The temperture men ws ±.1 C before 1988, nd 12.5 ±.1 C fterwrds (p <.1, Wilcoxon Rnk Test, n = 51 Fig. 5). During the whole study period, surfce temperture ws negtively correlted with totl perch yield, zooplnkton biovolume nd totl P (Tble 2,Fig.5). 6 2 Perch yield (t)

6 46 J.-P. Dubois et l.: Aqut. Living Resour. 21, (28) Tble 2. Coefficients of correltion r 2 between the different prmeters; in the correltions with perch yield, dt from the period hve been excluded. *: p <.5, **: p <.1, ***: p <.1. Phosphorus Zooplnkton Temperture Perch yield Perch size Phosphorus 1 Zooplnkton.57 *** 1 Temperture.9*.1* 1 Perch yield.19**.36***.13* 1 Perch size.29*.46*** Yerly men temperture ( C) Yerly yield (t) 1-yer-old perch men size (mm) Yer b c r = r = Wter temperture ( C) Fig. 5. Annul men temperture ( C) of the surfce wter of Lke Genev. () Temperture trend (unbroken line) with men levels nd chnge detected by the DCPC procedure (dotted line). (b) Correltions between temperture nd nnul perch yield (t); nd (c) temperture nd men size (TLmm) of one-yer-old perch. 3.3 Comprison of juvenile perch growth during eutrophiction nd re-oligotrophiction; influence of wter temperture The size of perch juveniles t the end of their first growing seson ws significntly higher during the period of high trophic level ( : yerly men TL: 113 ± 2 mm), when totl P level nd zooplnkton biovolume were t their highest vlues, thn it ws from 1985 to 25, nd before 197 (yerly men TL: 97 ± 2 mm), when totl P ws below 75 µg L 1 nd zooplnkton biovolume below 15 ml m 2 (Wilcoxon rnk test, n = 31, p <.1). A chnge in the men size of oneyer-old perch, clculted by the DCPC procedure (p <.1) 14 (Fig. 4b), occurred between 1982 nd It is not possible to be more precise bout exctly when this chnge occurred, becuse perch born in 1983 nd 1984 were very scrce nd smples insufficient to estimte their men size. Over the whole study period, the men size of + perch ws significntly relted to the totl P level (r = +.54, df = 29, p <.1), nd to the zooplnkton biovolume (r =+.67, df = 29, p <.1). The correltions re higher if only strong cohorts re tken into ccount (men size nd zooplnkton: r =+.92, df = 8, p <.1, men size nd totl P: r =+.72, df = 8, p <.5, Fig. 6). During the period of re-oligotrophiction, from 1985 to 25, the men + size of strong cohorts (s defined in the previous prgrph: 1985, 1988, 1992, 1993, 1996 nd 1999) ws significntly smller thn tht of the other cohorts born in other yers during the sme period (Wilcoxon rnk test, n = 19, p <.1). No significnt correltion could be detected between lke wter temperture nd perch size (Tble 2, Fig.5). The coefficient of multiple determintion between perch size nd zooplnkton biovolume in combintion with totl P nd wter temperture ws not very different from the coefficient of determintion between perch size nd zooplnkton biovolume lone:.49 vs Discussion 4.1 Succession of strong nd wek cohorts Strong cohorts of perch were generlly seprted by intervls of three or four yers, s hs lso been reported for perch ctches in Lke Genev during the periods nd (Lng nd Büttiker 1985; Lng1987), nd spwner popultions during the period (Gillet et l. 1995). Wide internnul fluctutions in the strength of the yer clsses hve been reported for Lke Windermere (Crig et l. 1979), in Crystl Lke for yellow perch (P. flvescens) (Snderson et l. 1999), in Lke Abborrtjrn (Persson et l. 2), in Lke Neuchâtel from 1961 to 1977 (dt of the Neuchâtel county fisheries gency), nd in Lke Constnce (Eckmnn et l. 26). Predtion exerted by perch on the following yer-clss (cnniblism) is n importnt cuse of inter-nnul fluctutions (Thorpe 1977). Persson et l. (2) showed tht the emergence nd development of new yerclss cn only occur in yers when the older yer-clss perch hve been strongly reduced. In the oligotrophic Crystl Lke, + yellow perch were eliminted for four successive yers s result of competition nd cnniblism by older perch (Snderson et l. 1999); three dominnt cohorts were observed

7 J.-P. Dubois et l.: Aqut. Living Resour. 21, (28) 47 1-yer-old perch men size (mm) r = Totl P (µg L -1 ) b r = Zooplnkton biovolume (ml m -2 ) Fig. 6. () Correltions between totl P nd men size (TL mm) of one-yer-old perch; nd (b) between zooplnkton biovolume nd men size of one-yer-old perch. Dt correspond to the strong cohorts only. during the 16-yer study period. In Lke Genev, the predtion exerted by strong cohorts on their offspring during the following 2 or 3 yers my hve gretly contributed to the cyclic fluctutions observed in perch bundnce. Perch were not fished until they reched 15 mm, the protective size limit, but then they were soon removed by fishermen (Lng 1987). Perch of strong cohorts dominted the perch popultion for severl yers, s reflected in the professionl ctches. Individuls born in 1988 constituted the mjority of the perch cught in 199, 1991 nd 1992 (dt of the Vud county fisheries gency; Dubois, unpubl. dt). The reduction of strong cohort by fishing then llowed new strong cohort to emerge. It is possible tht cnniblistic pressure hs incresed during re-oligotrophiction in Lke Genev, s hs been observed in Lke Constnce becuse of the reduction of zooplnkton nd of submerged mcrophytes tht constitute nturl shelters for young fish (Eckmnn et l. 26). Climtic conditions cn interfere with the settlement of strong cohorts. In Lke Genev, during the period , unusully cold conditions during spring nd summer (Anneville, pers. comm.) probbly strongly reduced perch recruitment, resulting in low perch ctches until Unfvourble climtic conditions re known to interfere with perch recruitment (Alto nd Newsome 1993). In Lke Neuchâtel (dt from the cntonl Swiss fisheries gency) nd Lke Constnce (Eckmnn et l. 26), which re situted in the vicinity of Lke Genev nd therefore experienced the sme climtic conditions, the sme collpse of perch ctches ws observed from 1977 to In ll three lkes, the perch stock recovered fter the wrm spring of In 1992 nd 1993, two consecutive lrge cohorts were born in Lke Genev. Although cool tempertures in spring cused prtil reduction of the recruitment in 1992, wrm spring tempertures in 1993 (Anneville, pers. comm.) enhnced recruitment in spite of the cnniblism nd competition exerted by the preceding cohort. 4.2 Effect of trophic chnges on zooplnkton biovolume; consequences for on perch yields Like mny other lpine lkes (Gerdeux et l. 26; Eckmnn et l. 26), Lke Genev hs undergone two mjor trophic chnges over the lst 5 yers. The concentrtion of P incresed 6-fold between the erly 196s nd the erly 198s during the eutrophiction process, nd the biovolume of zooplnkton incresed mrkedly (Blvy 1998). As result of the re-oligotrophictionprocess, totl P returned to pproximtely 3 µg L 1 in the erly 2s. Throughout the period studied, zooplnkton production ws positively correlted with totl P. The shrp decrese observed from 1981 to 1985, nd detected by the DCPC nlysis, ws probbly due to combintion of decrese in totl P level nd n increse in grzing pressure, becuse of the birth of strong perch cohort in 1982 following prolonged period of wek recruitment. Moreover, strong roch cohort ws lso born in 1982 (Ponton pers. comm). Throughout the re-oligotrophiction process, the continuous expnsion of the whitefish popultion (Coregonus lvretus) (Gerdeux et l. 26) probbly contributed to controlling zooplnkton popultions. It is importnt to note tht chnges in the reltive proportions of zooplnkton species during the growing seson hve lso occurred in Lke Genev. For exmple, now tht re-oligotrophiction is occurring in Lke Genev, clnids re incresing, while other copepods nd herbivorous cldocerns re showing decline (Anneville et l. 27). Lng nd Lng (1983) found close reltionship between totl P nd perch yields in the Swiss prt of Lke Genev, during the eutrophiction period of 1964 to 1975 (r =.69; n = 12; p <.5). An increse in perch yields hs lso been reported during eutrophiction in Lke Constnce (Eckmnn et l. 26), nd in Lke Neuchâtel (dt from the cntonl Swiss fisheries gency). Gerdeux et l. (26) described chnges in fish ctches in 11 peri-lpine lkes during eutrophiction nd re-oligotrophiction. These studies reveled tht the highest percid yields occurred when totl P levels were between 7 nd 8 µg L 1 (eutrophic stge); bove this level, nd prticulrly with totl P > 9 µg L 1, cyprinids becme the dominnt species, nd percid yields decresed. The sme pttern occurred in the hypertrophic shllow lkes of northern Europe (Jeppesen et l. 2). Yerly men perch yields during the re-oligotrophiction period were only hlf those obtined before 1977, probbly linked to decrese in the food vilble for perch. This chnge in perch yields is found by the DCPC procedure in the period when perch ctches slumped; suggesting tht the dte clculted for the chnge is debtble. Yields vry considerbly from yer to yer, nd it is difficult to detect ny reltionship between the trophic sttus (totl P or zooplnkton biovolume) nd perch yields, such s the positive correltion proposed by Lng nd Lng (1983). However, if only the three yers of fishing ssocited with ech of the successive strong cohorts re tken into ccount in clculting the correltion, then perch yields

8 48 J.-P. Dubois et l.: Aqut. Living Resour. 21, (28) nd zooplnkton biovolume pper to be strongly correlted for the period Clcultions mde over three-yer periods cn blur considerble differences in the vlues of the trophic prmeters. It is possible to hypothesize tht within strong cohorts intrspecific competition for food ws more severe, nd this ment tht trophic chnges hd mrked effect on perch production nd yield. During the pst 45 yers, the number of fishermen nd the level of fishing ctivity hve not chnged gret del (Mtthey 1975; Gerdeux et l. 26), so the reltionships found between nnul fish yields nd trophic prmeters in Lke Genev (Lng nd Lng 1983; this work) led us to think tht nnul yields cn be used s indictors of the stock of perch. Other observtions lso confirm this. In Lke Oneid between 1957 nd 1974, Forney (1977) recorded prllel chnges in the stock of mture femles of wlleye (Stizostedion vitreum vitreum), percid fish evluted by mrking nd recpture, nd in the trp-net ctches mde during the breeding seson. Additionlly, Lng (1987) suggested tht the bundnce (density) of perch femles could be resonbly ccurtely estimted from the bundnce of egg-ribbons (see lso Thorpe 1977), nd in Lke Genev, the density of eggribbons nd nnul perch yields were lso positively correlted (r =+.7; period ) (Lng 1999). 4.3 Effect of trophic nd zooplnkton chnges on + perch growth The effect of totl P on + perch growth is not s direct s tht on zooplnkton, which could explin why correltions were lwys greter for zooplnkton biovolume thn for totl P. The size of one-yer-old perch ws positively correlted with the trophic sttus, on verge 16 mm greter during the period of highest trophic level thn during the reoligotrophiction period, slightly more thn tht observed in Lke Constnce (1 cm; Eckmnn et l. 26). The 16 mm increse ws equivlent to 1.6 fold increse in weight (Dubois, unpub. dt), which is comprble to the increse in the zooplnkton biovolume estimted from the DCPC procedure. Severl uthors hve lredy described n improvement of perch growth in lkes undergoing eutrophiction. Under oligotrophic conditions, the totl P is still n influentil vrible (O Gormn nd Burnett 21), but hs reltively little impct compred to competition for food nd cnniblism (Snderson et l. 1999). Zooplnkton is the essentil diet of + perch, nd this hs led to considerble qulittive nd quntittive investigtions (e.g., Mehner et l. 1998; Snderson et l. 1999; Romre 2). In Lke Constnce, the bundnce of zooplnkton during eutrophiction llowed even dult perch to feed minly on such prey (Hrtmnn 1975); s result of re-oligotrophiction, food becme limited nd inter yer-clss competition incresed (Eckmnn et l. 26). The nlysis of perch popultions by cohorts provides useful informtion bout the impct of the trophic level on + perch growth. Higher correltions were obtined for the strong cohorts thn for ll the cohorts combined, indicting tht the strong cohorts were prticulrly sensitive to trophic sttus, nd especilly to the mount of zooplnkton vilble. Under reoligotrophiction conditions, strong cohorts hd lower men individul + growth thn wek cohorts, s result of competition for zooplnkton. O Gormn nd Burnett (21) observed tht the growth of + perch ws fster when ge clsses were smll. Mehner et l. (1998) reported tht the strength of yer-clsses ws not relted to the mount of zooplnkton in Lke Butzen, but tht the size of the + fish t the end of the yer ws inversely relted to the yer-clss strength. During eutrophiction, zooplnkton ws bundnt, nd predtion reduced, s observed by Hrtmnn (1975) nd Lng nd Lng (1983). As result of re-oligotrophiction, the zooplnkton food source ws less bundnt, nd this ffected the growth of + perch, prticulrly in the strong cohorts. As perch grow slowly once mesotrophic conditions hve been restored, they tke longer to rech exploitble size nd ttin mturity; nd s result the intervls between two successive strong cohorts increse. Moreover, with reoligotrophiction, perch re subject to prsitism, s hs been reported in Lke Constnce (Brinker nd Hmers 27), nd slower growing + perch re probbly more vulnerble to predtion (Eckmnn et l. 26). The combintion of ll these fctors hs probbly contributed to the lowering of the perch yield in Lke Genev. 4.4 Interction between climte wrming nd trophic chnges in Lke Genev In context of climte wrming, surfce wter temperture of Lke Genev incresed by pproximtely 1 C during the study period, with significnt shift between 1987 nd 1988 s hs been observed in the western Alps (Beniston 25). After 1988, the nnul men wter temperture remined over 12 C t time when the trophic level ws dropping continuously. It seems tht the impct of the trophic level fr exceeded tht of the rising temperture on perch growth nd perch yields. Moreover, the combintion of temperture with zooplnkton biovolume nd/or totl P never gretly modified the vlue of correltion coefficients between perch yield nd zooplnkton, zooplnkton nd totl P or perch growth nd zooplnkton. In Lke Windermere, temperture hs been shown to be mjor fctor in controlling perch growth or recruitment (Le Cren et l. 1977;Pxtonetl.24). The lck of ny mesurble impct of temperture on perch growth or yield in Lke Genev, nd more generlly in peri-lpine lkes (Mssol et l. 27), could be t lest prtly explined by the fct tht this lke is wrmer thn Lke Windermere. In Lke Windermere, the sum of degree-dys bove 14 C only exceeded 4 during wrm summers, wheres in Lke Genev, it ws lwys bove 4 degree-dys (with mximum 983 degree-dys in 23). However, surfce wter temperture of Lke Genev never exceeded 24 C, the optimum for perch growth (Melrd et l. 1996). The mount of vilble food is therefore probbly more importnt thn wter temperture for the growth nd yield of perch in Lke Genev. 5 Conclusion Perch growth nd yields in Lke Genev re relted to totl P, nd especilly dependent on the vilbility of

9 J.-P. Dubois et l.: Aqut. Living Resour. 21, (28) 49 zooplnktonic food, prticulrly in the cse of strong cohorts. The influence of re-oligotrophiction fr outweighed the effects of rising temperture on perch growth nd yields. If the totl P level continues to decline, perch performnce could be more seriously ffected. Acknowledgements. This study is bsed in prt on dt collected by the CIPEL, by the French nd Swiss fisheries dministrtions, nd by the professionl fishermen of Lke Genev. We re grteful to Orlne Anneville, Clude Lng nd Alexis Chmpigneulle for their helpful suggestions while we were writing this rticle. References Alto S.K., Newsome G.E., 1993, Winds nd the demic structure of popultion of yellow perch, Perc flvescens. Cn. J. Fish. Aqut. Sci. 5, Anneville O., Ginot V., Drurt J.C., Angeli N., 22, Long-term study ( ) of sesonl chnges in the phytoplnkton in Lke Genev: multi-tble pproch. J. Plnkton Res. 24, Anneville O., Molinero J.C., Souissi S., Blvy G., Gerdeux D., 27, Long-term chnges in the copepod community of Lke Genev. J. Plnkton Res. 29, Blvy G., 1998, Le zooplncton du Lémn comprtiment incontournble du réseu trophique. Arch. Sci. Genève 51, Beniston M., 25, Mountin climtes nd climtic chnge: n overview of processes focusing on the Europen Alps Pure Appl. Geophys. 162, Brinker A., Hmers R., 27, Evidence for negtive impct of plerocercoid infection of Trienophorus nodulosus on Perc fluvitilis L. stock in Upper Lke Constnce, wter body undergoing rpid reoligotrophiction. J. Fish Biol. 71, Chmpigneulle A., Gerdeux D., 1995, Survey, mngement nd recent rehbilittion of the Arctic chr (Slvelinus lpinus) fishery in the French Swiss Lke Lemn. Nord. J. Freshw. Res. 71, Crig J.F., Kipling C., Le Cren E.D., McCormck J.C., 1979, Estimtes of the numbers, biomss nd yer-clss strengths of perch (Perc fluvitilis L.) in Windermere from 1967 to 1977 nd some comprisons with erlier yers. 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10 41 J.-P. Dubois et l.: Aqut. Living Resour. 21, (28) perch (Perc fluvitilis) in Windermere, U.K.J. Fish Biol. 65, Persson L., Byström P., Whlström E., 2, Cnniblism nd competition in Eursin perch: popultion dynmics of n ontogenetic omnivore. Ecology 81, Picrd F., Robin S., Lvielle M., Visse C., Dudin J.J., 25, A sttisticl pproch for rry CGH dt nlysis. BMC Bioinformtics 6, Romre P., 2, Growth of lrvl nd juvenile perch: the importnce of diet nd fish density. J. Fish Biol. 56, Rundberg, H. 1977, Trends in hrvest of pikeperch (Stizostedion lucioperc), Eursin perch (Perc fluvitilis), nd northern pike (Esox lucius) nd ssocited environmentl chnges in lkes Mälren nd Hjälmren, J. Fish. Res. Bord Cn. 34, Snderson B.L., Hrbik T.R., Mgnuson J.J., Post D.M., 1999, Cyclic dynmics of yellow perch (Perc flvescens) popultion in n oligotrophic lke: evidence for the role of intrspecific interctions. Cn. J. Fish. Aqut. Sci. 56, Thorpe J.E., 1977, Synopsis of biologicl dt on the perch Perc fluvitilis Linneus, 1758 nd Perc flvescens Mitchill, FAO (Food nd Agriculture Orgniztion of the United Ntions) Fisheries Synopsis 113.