______,Ea-

Numerical ecology Coastal nursery Fish community Spatio-temporal variability Ecological guild Pleuronectiform juveniles Écologie numérique in the structure Nourricerie littorale Peuplement ichthyologique Guilde écologique of a nectobenthic fish nursery: Pleuronectiformes juvéniles a descriptive study

Patrick SAFRAN Laboratoire d'Écologie Numérique-SN3, Station Marine de Wimereux, Université des Sciences et Techniques de , 59655 Villeneuve-d' Ascq Cedex, . Present address: Department of Fishery Sciences, Laboratory of Marine Living Resources, faculty of Agriculture, Tohoku University, 1-1 Tsutsumidori Amamiyama­ chi, Sendai 981, Japan.

Received 16/ll/88, in revised form 717/89, accepted 13/7/89.

ABSTRACT When the by-catch of an artisanal brown shrimp fishery in the Canche bay demonstra­ ted the existence of an important nursery of nectobenthic fishes, a survey of this nursery was performed along the coast of the Pas-de-Calais (Eastern Manche) from January 1985 to June 1986. Tne samples were obtained from 210 hauls of an exper­ imental trawl containing 51 600 juveniles of 37 species. Complementary multivariate statistical methods, such as diversity index, rank-frequency diagrams, particularly the smoothed rank-frequency diagram have proved to be powerful tools in assessing the relationships between the populations of different species in a community. Qualitative and quantitative similarity, cluster analysis and correspondence analysis showed that: 1) the fish community in this area was qualitatively, quantitatively and structurally homogeneous; 2) this single, "multispecific" community was maintained by a seasonal flow of individuals, which passed through the nursery and induced a turnover of the dominant populations, without any modification to the general faunistical pattern (structure); 3) Dab (Limanda limanda, L.) constituted the predominant population. Three other important populations were: dragonet (Callionymus lyra, L.); sand goby (Pomatoschistus minutus, P.); and plaice (Pleuronectes platessa, L.). Less important species were: sole (Solea so/ea, L.); sprat (Sprattus sprattus, L.); hook-nose (Agonus cataphractus, L.); and poor cod (Trisopterus minutus, L.); 4) The three pleuronecti­ forms, dab, plaice and sole, formed a structural guild, referred to here as the LPS guild (L. for Limanda, P. for Pleuronectes and S. for Solea), within the nursery community. Within the LPS guild, seasonal succession showed autumnal and hibernal dab populations (1986); hibernal (1985) and coastal estival plaice; and a printempal sole. Their various growth-rates (plaice > dab >sole) induced the cohabitation of indivi­ duals of various size classes, without obvious exclusion of any of the three species. The distribution of individuals in space and time, which was the result of a regular flow of individuals passing into the nursery, replenishing the stocks with juveniles, maintained this cohabitation. Oceano/ogica Acta, 1990. 13, 1, 97-106.

RÉSUMÉ Variabilité spatio-temporelle de la structure d'une nourncene de pois­ sons nectobenthiques: une étude descriptive Suite à une étude de la pêche accessoire dans la pêcherie artisanale de crevettes grises en baie de Canche, qui a démontré l'existence d'une importante nourricerie littorale de poissons nectobenthiques, une étude écologique de cette dernière a été effectuée de janvier 1985 à juin 1986 à partir d'un échantillonnage comprenant 210 traits de chalut, répartis le long du Pas-de-Calais, et qui ont permis la collecte d'environ 51600 individus juvéniles de 37 espèces. Des méthodes statistiques multivariables complémen­ taires les unes des autres : diversité spécifique, diagramme rang-fréquence, similarités qualitatives et quantitatives, analyses factorielles des correspondances et classifications

0399-1784/90/01 97 10/$ 3.00/© Gauthier-Villars 97

.., P. SAFRAN

numériques représentées par des dendrogrammes, ont permis de démontrer: 1) une homogénéité faunistique qualitative, quantitative et structurelle dans cette zone; 2) l'existence d'un peuplement unique, réparti sur l'ensemble de la zone d'étude, soumis à un flux saisonnier d'individus qui traversait en permanence la nourricerie et entraînait le renouvellement des populations structurantes, sans modification de la composition faunistique générale; 3) La limande (Limanda limanda, L.) représentait la population dominante de ce peuplement. Trois autres populations étaient structurantes : celles du callionyme (Callionymus lyra, L.), du gobie (Pomatoschistus minutus, P.) et de la plie (Pleuronectes platessa, L.), accompagnées par celles de la sole (Solea solea, L.), du sprat (Sprattus sprattus, L.), de la souris (Agonus cataphractus, L.) et du petit tacaud (Trisopterus minutus, L.). Parmi ces espèces, les Pleuronectiformes (Limande, Plie et Sole) representaient une guilde structurante (nommée ci-après guilde LPS) du peuplement; 4) Au sein de la guilde LPS, les remplacements saisonniers successifs faisaient apparaître une limande automnale et hivernale (1986), une plie hivernale (1985) et estivale collectée principalement à la côte, et une sole printanière, Leurs vitesses de croissance différentes (plie>limande>sole) semblaient induire une cohabit­ ation d'individus de toutes tailles sans entraîner d'exclusion. Oceanologica Acta, 1990. 13, 1, 97-106.

INTRODUCTION

It has been established that the coastal zone is an area of reproduction, egg-laying, growth and nursery target-species without taking into consideration the grounds for many species of offshore fishes (Peres, fluctuations of the others. This reflects the realization 1972; 1976; Bou gis et al., 1976; Margalef, 1977; 1983; that single-species population dynamic models are Ross, 1977; Lackey and Nielsen, 1980). The factors insufficient for fisheries management purposes; multi­ influencing migrations and temporary concentrations species interactions must be considered, as well as the have yet to be determined. Fishery studies tend to focus impact on stocks caused by fishing, etc. on commercial adult populations, and knowledge of The work presented here documents, for the first time factors that influence the juvenile populations is often in this area, the fish community of a coastal multispe­ poor (Weinstein, 1982; Alderdice, 1985). Recruitement cific nursery, and concludes that there is one single to adult stocks depends on the events occuring during community. Multivariate statistical methods are used the juvenile growth period. Nurseries ensure the perma­ to analyse the multispecific samples obtained by this nence of populations, but at the same time, owing to survey. their geographical localization, their limited area and Moreover, special attention is given to dab, plaice and the possible competition between species, they consti­ sole. These three flatfish populations are studied here tute a limitation, and most probably a regulatory mech­ in more depth for two main reasons. Firstly, they anism for stocks. are of primary economie importance, constituting pre­ Only a few ecological studies are performed on recruitment stages of stocks exploited by an artisanal nurseries; these are generally focused on commercial fishery (off Boulogne-sur-mer and Etaples, Pas-de­ species, as for example, herring ( Clupea harengus L. : Calais, France). Secondly, they are the most numerous Hodgson, 1957; Burd, 1962; Cushing, 1968), plaice species in this survey. Dab is the main species and (Pleuronectes platessa L.: Gross, 1947; Beverton and plaice is a dominant one of the single coastal nursery Holt, 1957; Dawson and Grimm, 1980), or managed community sampled along the Pas-de-Calais. Another in restricted areas such as , hays and lagoons important species is sole, which constitutes an escort (Marchand et al., 1983; Labourg et al., 1985). The population, while dab and plaice are structural (in study area in the present work is located in the open terms of data analysis). These three species belong to sea, along the coastal zone of the Pas-de-Calais in the the same family Pleuronectidae. They may have similar Eastern Manche (), a zone harvested ecological requirements and foraging strategies (Barrett by an artisanal brown shrimp (Crangon crangon, L.) and Yonge, 1958; Wheeler, 1978; Bauchot and Pras, fishery. The study of the bycatch of this shrimp fishery 1980; Muus and Dahlstrom, 1981; Quero, 1984), and in Canche Bay demonstrates the existence of an import­ so fit the definition of an ecological guild (Lincoln et ant nursery of exploited flatfishes (Safran, 1984; 1985; al., 1982; Barbault, 1983), which is referred to here as 1987 a) including plaice, dab (Limanda limanda, L.) and the LPS guild (L. for Limanda, P. for Pleuronectes and sole (Solea solea, L.). Many other species, whether S. for Solea; in decreasing order of importance). exploited or not, occur together with these flatfishes: Concentration on the three structural species of the the area is a multispecific nursery. lt is therefore clear gui1d provides a rouch better understanding of the that spatio-temporal variations, abundance fluctu­ general results, and specifies cohort succession and ations, and cohort successions of sampled populations growth during the period the fishes spend in the "foster inside this coastal stretch cannot be analysed for one mother" zone.

98 VARIABILITY AND STRUCTURE IN A FISH NURSERY

MATERIALS AND METHODS

Study area The sampling area was located along the French "Opal Coast" (Pas-de-Calais, Eastern Manche), between the southern mouth of Canche Bay and the northern end of Boulogne-sur-mer (Fig. 1). A preliminary study of the nursery from commercial trawl samples (Safran, 1987 a) allowed the demarcation of a coastal zone with a sandjsand-mud bottom, and a depth varying tidally t from 3 to 6 m. -N­ I Sampling An experimental beam-trawl was designed for this study, and adapted to the oceanographie vessel "Sepia II' (Station marine de Wimereux, CNRS), a ship similar Hardelot in its technical characteristics to small professional fish­ ing boats. It is 12.5 m in length and is powered by a 112 horsepower engine (Safran, 1987 b). The trawl length was about 8. 20 rn, with a pole stretching a span of 2.80 m and skates which were 0.40 m in height. The Figure 1 pocket included two sectors, the first formed by a Study area: a) general Stells 14 mm mesh-side and the second one by a 10 mm localization; and b) sc hematie 50'30'N localization of the 13 experimental mesh-size. In front of this net, a chain-pad was pre­ trawling sites. ceded by a chain used to hoist the fish. Each trawling Zone d'étude: a) localisation operation was carried out at a speed of about générale; et (b) localisation sché­ matique des 13 traits expérimen­ 1 . 5 knots, for 15 minutes, against the tidal current, taux. parallel to the coast. From January 1985 to June 1986, 13 experimental trawls per month were carried out Specifie diversity was estimated by the Shannon index (Fig. 1 b), in north-south and shore-offshore directions corresponding to initial working hypotheses based on (Shannon and Weaver, 1963), white evenness was esti­ the existence of faunistica1 gradients according to those mated by the Pielou index (Pielou, 1975). Multivariate two directions. analysis was performed by factorial analysis of corre­ spondence (FAC), which is one of the most frequent! y used analyses for multivariate data tables in ecological Data analysis studies (Legendre and Legendre, 1984); by numerical 176 experimental trawls were performed, producing a classification using cluster analysis, which was obtained total of sorne 38 000 individuals belonging to 37 species. by the quantitative similarity index of Gower based on The nomenclature follows the Check-List of Fishes of the abundance of species (Gower, 1971); and by the the North Atlantic and Mediterranean (Hureau and qualitative similarity index of Ochiai based on the Monod, 1973). Catch composition was variable, so the presence-absence of species (Ochiai, 1957). Dendro­ following multivariate statistical methods were used to grams were obtained by the flexible clustering method show the similarities and differences between the sam­ of Lance and Williams (Lance and Williams, 1967). pies. Rank-frequency diagram methods (Frontier, Following Blondel (1979), Barbault (1981) and Lincoln 1976; 1985) provide good descriptions of the specifie et al. (1982), a population is defined as a group of diversity of a sample by representing the distribution individuals of the same species, present in the same of individuals among species. A rank-frequency curve zone; and a "multispecific" community in a given zone is obtained by placing the log of the rank on the as the communities (or populations) of different species abscissa vs. the log of the frequency on the ordinate. present. For one sample, the shape of the curve is generally In order to follow changes in the mutual proportions irregular. A regular, smoothed shape is obtained when of dab, plaice and sole, without considering the other the numbers of individuals are cumulated following two species simultaneously sampled, their variations were methods (Safran, 1987 a): 1) a "cumulative" diversity is presented on triangular diagrams (Calot, 1973). This obtained, higher than the mean diversity of the samples, corresponds to the simplex representation in factorial when the number of individuals of different species are analysis (Benzecri et al., 1982; 1984). It should be cumulated. The rank-frequency diagram, or "RFD", noted that Factorial Analysis of Correspondence is an is more convex and extended on the right, as the ordination in the simplex, but in the simplex of ali the number of species increased; 2) when the number of variables. The study of the guild was restricted to on1y individuals are cumulated by rank, independent of the three variables: abundance of dad, plaice and sole. species in the ranks which fluctuate from one sample Analysis of spatio-temporal variations of mutual per­ to another, a smoothed "average RFD" is obtained. centages (relative abundances of species) for these three

99 P. SAFRAN

2 18.75% Figure 2 Winter (February 27, 1985). Correspondence Ana/y­ Tm sis shows projections in the plane of axes 1 and 2 of "station" vectors (code numbers are the sampling m Ac Hardelot. Canche stations in time and in space throughout the survey. " They are grouped according to the samp/ing loca­ J .•. tions given in Figure lb; see also Safran, 1987b) and "species" vectors (see species abreviations in Appendix). Hiver (27 février 1985) : Analyse Factorielle des 1 Correspondances : projections dans le plan facto­ riel ( 1, 2) des vecteurs « stations » (les numéros 5G.39% Boulogne représentent les stations d'échantillonnage dans le temps et dans l'espace durant cette étude, et sont Pp groupés selon les lieux d'échantillonnage donnés figure 1 b; voir aussi Safran, 1987 b), et des vec­ teurs « espéces » (les abréviations des espéces sont données en Annexe). species according to the study area by the triangular diagram method, which showed the succession of domi­ sole, were dominant in spring and in summer. Popula­ nant populations, and biometrical study using size­ tions of dab and dragonet were dominating the summer frequency distributions to establish an arrival-departure and autumn communities. calendar of cohorts, residence time and growth rates, Sampling zones were used to analyse the guild. The size-frequency distribution histograms are not presented in this paper. Sampling zones were analysed to show a possible shore­ only the main results are given. offshore faunistical gradient, and to specify those faun-

RESULTS

The fish community Sa The general data matrix, with full reference to spatio­ s 1 temporal sampling stations, species names and numbers 9 of individuals caught per sampling trawl, is presented in Safran (1987 b).

The faunistical composition of the samples showed .... ~ 50 qualitative homogeneity and high quantitative hetero­ geneity. To determine whether the homogeneity was {={ ::~~-______J due to a space-time division into sub-communities, identifiable by multivariate analysis, attention was shore{:: ~----__J---l focused on seasonal variations and sampling zones. 70~------~ The aim of these investigations was to determine a possible underlying coherence based on the observed offshore) :: ~==:::::;------, heterogeneity. ..f9 Seasona/ variations .. Wimereux ., The predominant winter species were sprat (Sprattus l Ochiai Index too% 50 sprattus, L.), encountered principally in the south, and n~======~,-~--~--~----~--~ harbour plaice. They were accompanied by dab, sand 68 goby (Pomatoschistus minutus, P.), flounder (Platich­ 71 South 70 thys flesus, L.) and herring. Following those, in order •• of numerical importance, were hook-nose (Agonus .. cataphractus, L.), unarmoured sea robin (Eutrigla gur­ nardus, L.) and poor cod (Trisopterus minutus, L.) •• (Fig. 2). Sole appeared in the summer of 1985 in the North ) :: t==:J------, harbour zone, together with plaice. Sole replaced plaice 13 as a dominant species of the community in the winter 10 11 of 1985-1986. The main summer species were dab, Figure 3 offshore, and coastal dragonet (Cal/ionymus lyra, L.), Summer (July 2, 1985). (a) Correspondence Analysis shows projections associated with sand goby (Fig. 3 a, where the grouping in the plane of axes 1 and 3 of "station" vectors and "species" tJectors. in the plane of axes 1 and 3 were more obvious than (b) and (c) show flexible c/ustering methods: dendrograms obtained by (b) quantitative similarity (Gower index), and by (c) qualitative similar­ in the plane of axes 1 and 2). No fundamental differen­ ity (Ochiai index). ces were found among the faunistical compositions of Été (2 juillet 1985). (a) Analyse Factorielle des Correspondances : the different zones. The winter species (sprat, dab, projection dans le plan factoriel (1, 3) des vecteurs «stations» et «espèces». (b) et (c) :méthode de groupements agglomératifs à liens plaice) were progressively replaced by dragonet, poor flexibles : dendrogrammes obtenus par (b) similarité quantitative cod, hook-nose and sole; those four species, especially (indice de Gower), et par (c) similarité qualitative (indice d'Ochiai).

100 VARIABILITY AND STRUCTURE IN A FISH NURSERY

1 oo Frequency% Figure 4 always verified. In fact, each sampling station resem­ Boulogne-sur-Mer. Rankjrequen­ bled a micro-zone within an identical zone (which we station 3 cy diagram by smoothing method. can call daughter-zone), which itself belonged to the Cumulative rank-frequency curves station 4 for stations 3 and 4. whole "foster mother": the nursery. There was a certain Boulogne-sur-Mer. Diagrammes qualitative, quantitative and structural coherence rangs-fréquences globaux obtenus within each "daughter-zone" and also within the par lissage pour les stations 3 10 et 4. coastal nursery, in spite of light fluctuations due to seasonal flows of populations (flows inherent to the species' bio-ethology), which carried sorne variations in the faunistical compositions, in the specifie diversity and in the structure of the sampled community. Only the distribution of numbers of individuals among lead­ ing species varied according to the "daughter-zone" without modification of the general faunistical compo­ sition or of the structure of the sampled fish commu­ nity. r---~2~16~.1~2v------~a=

0.1

21.30%

0.01 L__....._....._....__. _ __._...... 1 3 4 5 10 15 20 25 Rank istical compositions with the smoothed RFD method, white F AC and numerical classification of the sampling dates were used to check the existence, or non-exist­ ence, of a north-south faunistical gradient. Throughout the study cycle, the harbour zone (stations 3 and 4, Boulogne-sur-Mer; Fig. 1) differed from the

others. Whatever the season, this zone took on indivi­ 68 dual characteristics. This was probably due to its shel­ tered position, with extensive man-made piers offering protection against heavy hydrodynamic and sedimen­ 1 tary perturbations. The principal species of this multi­ 24 specific nursery community were plaice (dominant), sole, dab, goby, dragonet and book nose, accompanied by sprat and poor cod during cold seasons (Fig. 4). For each sampling date, there was obvious association between harbour stations 3 and 4 and the coastal station 8 (Fig. 3 a), and close qualitative and Station9 quantitative similarities (Fig. 3 b). Nevertheless, 2 although the fish community was made up of the same group of species, the flatfishes seemed less dominant here. The seasonal flow of populations was more 173 distinct. Winter sprat (accompanied by herring) was progressively replaced by summer pleuronectiforms 25 (sole, plaice and dab): a conspicuous phenomenon in 1985. Dragonet, also, appeared during the summer of 1986. A north-south faunistical gradient was most noticeable during the winter of 1984-1985 and summer of 1985 (Fig. 3 c). From the autumn of 1985 it diminished progressively: the north stations (1 and 2: Wimereux) showed the same qualitative and quantitative character­ Station10 istics as the south stations. This homogeneization was Figure 5 conspicuous in the summer of 1985 (Fig. 3 a), in the Canche estuary. Correspondence Analysis shows project(ons in the autumn of 1985, in the winter of 1985-1986 and in the plane of axes l and 2 of "species" vectors, and of "station" vectors summer of 1986. These results came from a numerical for stations 8, 9 and lO: (a), (b) and (c), respective/y. Embouchure de la Canche. Analyse factorielle des Correspondances: classification of samples, based on faunistical outlines. projections dans le plan factoriel ( 1, 2) des vecteurs « espèces » et Generally speaking, this north-south gradient was not « stations » pour les stations 8 (a), 9 (b) et 10 (c).

101 P. SAFRAN

The presence of a shore-offshore faunistical gradient Spatio-temporal variability was confirmed for short distances of Jess than half A study of spatio-temporal variability in mutual per­ a nautical mile. From the summer of 1985, it was centages of the three species of the LPS guild high­ conspicuous for the sampled stations. opposite the lighted the following points. Firstly, there was near­ Canche estuary and Stella. From the autumn of 1985, shore-offshore · faunistica1 gradient, with plaice in the the gradient was clear: coastal samplings showed a dominant position for stations 1 (Wimereux), 5 (Harde­ qualitative and quantitative homogeneity which distin­ lot, Fig. 7 a) and 8 (Canche estuary exit); and dab for guished them from deeper samples. This depth gradient the offshore stations 6 and 7 (Hardelot, Fig. 7 band c), was conspicuous among stations 8, 9 and 10 (Canche and 9 and 10 (opposite the Canche estuary). This estuary). Station 8 took on individual characteristics gradient was not visible for stations 11, 12 and 13 compared with stations 9 and 10 during the winter of (Stella), where dab was also dominant ali along the 1985-1986, the spring of 1986 and the summer of 1986 study cycle. Secondly, harbour stations 3 and 4 (Fig. 8) (Fig. 5). Concerning this depth-related gradient (one presented almost the same seasonal evolution profiles of the working hypotheses), except for the demarcation among themselves. The plaice of the winter 1984-1985 between coastal and offshore sampled stations opposite was replaced by spring sole. Dab appeared as dominant Canche and Stella, there was a good homogeneity, population in the autumn of 1985 and in the winter characteristic of each sampling area. Analysis of the 1985-1986. These results showed that, in the coastal curve shape obtained by a smoothed RFD (Fig. 6) for nursery located along the Pas-de-Calais, dab, plaice ali of the coastal samplings (micro-zones 1, 3, 5, 8 and and sole were mutually replaced, as follows: Il), and for ali of the offshore samplings (micro-zones 2, 4, 6, 9 and 12), confirmed the existence of this plaice sole plaice dab dab sole homogeneity: the curve shapes of average RFD winter spring summer autumn winter spring (Fig. 6a) and cumulative RFD (Fig. 6b) were similar 1985 1986 and superimposable, and showed that the depth-related gradient was not really obvious in this study area. Dab was confirmed as the dominant population of the A detailed analysis of the curve obtained by a smoothed LPS guild, and consequently of the community of RFD for the whole system involving micro-zones, sampled juveniles in this coastal nursery. Plaice had a "daughter-zones", and "foster mother" provided an preferential affinity for the near coast. The inshore­ overview of the structural homogeneity and the faunist­ offshore gradient was weil pronounced for the sampled ical composition of the community. Dab was the domi­ stations opposite Hardelot and the Canche estuary. The nant species of this coastal nursery and the fish com­ munity, sampled along the Pas-de-Calais, was also 1 o o Frequency % 1o o Frequency % made up of populations of dragonet, goby, plaice, sole, hook nose, sprat and poor cod (in decreasing order of shore importance). Analysis of ali the RFDs produced the offshore leading species faunistical list, which constituted a description of the ichthyological community of the Pp Cl coastal multispecific nursery: the four dominant (or Prif···... Sv structural) species (in decreasing order of importance) 10 Pp···· ... Ac 10 ·-\ss were dab, dragonet, goby and plaice; and the four sv accompanying species were sole, sprat, hook nose and s \ poor cod.

The LPS guild Dab, plaice and sole were the most numerous species in this survey: 17540 individuals were caught, account­ ing for 43% of ali the sampledjuvenile fish (dab: 22%, plaice: 12% and sole: 9 %).

0.1 0.1

Figure 6 The nursery: a) average rank-frequency diagrams; and b) average R.F.D. cumulative R.F.D. cumulative rank-frequency diagrarns for ali coastal and offshore samples. 0.01 ,___...... _~...... _ _ __._---~o_.....~ La nourricerie. a) diagrammes rangs-fréquences moyens; 1 3 4 5 10 20 % 3 4 5 10 20 et b) globaux, obtenus pour l'ensemble des traits de côte Rank Rank et pour l'ensemble des traits du large.

102 VARIABILITY AND STRUCTURE IN A FISH NURSERY

Figure 7 Hardelot individualization of station 8 compared with stations 9 Hardelot: seasonal -1115 0 and 10 was confirmed, marked on the one hand by a Station 5 change in relative ahun­ ···--· 1118 dance for dab, plaice and 1ow frequency of plaice collected at stations 9 and 10, sole, on a triangular and on the other hand by large quantitative differences diagram for stations 5 among these three stations. (a), 6 (b) and 7 (c). Hardelot-plage. Évolu• The guild tion saisonnière des abondances relatives en The movement of individuals regularly crossing the limande, plie et sole, représentées par un nursery did not permit a study of growth parameters. diagramme triangulaire Nevertheless, an analysis of size-frequency distribution pour les stations 5 (a), 6 50 Dab histograms for each species of the LPS guild was per­ (b) et 7 (c). formed to improve upon previous observations and to G draw uPthe nursery's arrival-departure calendar. The Station 6 follow-up of cohorts was not always obvious, and most of the time one principal mode was observed. Indeed, the nursery was only a temporary stopping-place where cohort followed cohort, each remaining in the nursery from its recruitment size to its departure size. An arriv­ a1-departure calendar for the· nursery could be formu­ lated from the biometrical analysis. Table 1 shows the ~ successive arrivai and departure waves during the study ~~------~----~~~~ 50 period: dab and plaice arrived at the same time (Febru­ Dab ary), followed by sole (March). A cohort of plaice was 0 the first to leave the zone (July), as a second wave, Station 7 composed of plaice and sole arrived (July), soon fol­ lowed by dab (August). The first cohort of dab and sole left the nursery around the same time (October), followed subsequently by the second cohort of sole departed (January), and finally plaice and dab (Febru­ ary). The growth rates of each species, calculated from the ~ recruitment dates, were almost similar for the two ~~------~~----~~~ growth periods (Tab. 2). Growth of plaice was faster than that of dab, which was faster than that of sole.

Figure 8 Boulogne-sur-mer ® @ Boulogne-sur-Mer: seasonal change in relative Station 3 abundance for dab, plaice and sole, on a triangular --- 1985 diagram for stations 3 (a) and 4 (b). ------1988 Boulogne-sur-Mer. Évolutions saisonnières des abondances relatives en limande, plie et sole, représentées par un diagramme triangulaire pour les stations 3 (a) et 4 (b).

50 50 Dab Dab

Table 1 Schematical calendar of arrivai and departure in the nursery for dab, plaice and sole (numbers are the mean length in centimeters). Calendrier schématique des arrivées et des départs dans la nourricerie pour la limande, la plie et la sole (les chiffres indiquent les tailles en centimètres). 1985 1986 J F M A M J J A s 0 N D J F Mon th

Dab 5 19 Plaice 5 22 Sole 7 17 Sole 2 14 Plaice 3 25 Dab 5 20

103 P. SAFRAN

Table 2 Table 3 Mean growth rates for dab, plaice and sole (according to recruitment Size-classes used in Factorial Analysis of Correspondence (deduced date). from size-frequency distribution histogram studies published in Safran, Vitesses de croissance calculées pour la limande, la plie et la sole, en 1987b). fonction des dates de recrutement. Classes de tailles utilisées pour les Analyses Factorielles. Species Mon th of arrivai Growth rate (cm/month) Size (cm) Dab February 1.75 Class min. max. August-September 2.14 1 Plaice February 2.83 A 4 July 2.75 B 5 6 Sole March 1.43 c 7 8 July 1.71 D 9 10 E Il 12 .F 13 15 G 16 30

Although these three species followed each other in time, periods of coexistence were observed. Moreover, DISCUSSION since the growth rates were different and the size­ frequency distribution histograms could be superimpo­ The results as a whole demonstrated: 1) an identical sed, there were periods of cohabitation of different qualitative composition: wherever it was situated in sizes of juveniles. In order to confirm this cohabitation, the nursery, nearly the same species composition was and to follow the simultaneous growth of the three recorded ali through the study cycle; 2) the same species, Factorial Analysis of Correspondence was per­ smoothed RFD: curve shape obtained was almost simi­ formed on the size classes, as deduced from size-fre­ lar and superimposable; 3) that only the ranks of quency distribution histogram studies and presented in species were permuted according to the seasons, the Table 3. The factorial analysis (Fig. 9 a and b) executed spatial gradients or at random. on the data matrix crossing 14 sampling-station 3 by Insufficient definition concerning discernible states 20 size classes, showed that 32.50 % of the total inertia exists to conclude that there was one single "multispe­ was absorbed by the first axis, which described the cific" community or that there were two or more. increasing size for dab, and contrasted E and F classes Creating models of groups of interacting species, Ker­ (structural classes of this axis) with the B class. Axis 2 ner (1957; 1959) establishes that, in a system including (21.60 % of the inertia) described the parallel evolution a large number of interacting species, the species fluctu­ of size for plaice and sole (Fig. 9 a), and contrasted A, ate with dephased oscillations while keeping the same B and C classes of sole and A and B of plaice with C distribution of individuals among species ("quantitative and D classes of plaice. The representation obtained structure"). The species can be permuted among them­ in the plane of axes 1 and 3 was interesting (Fig. 9 b). selves within this distribution. Maynard Smith (1975) Additional information appeared along axis 3 (16.60% contests this multispecific model and recalls that, in of the inertia), which described the increasing size for reality, an identified multispecific community always plaice and sole, and contrasted the D, E and F classes has the same rare species and the same abundant spe­ of sole with the D and E classes of plaice. These results cies. This reasoning is circular (Frontier, 1986): insofar showed that, for the small (3 to 6 cm) plaice and as a multispecific community is defined by the perma­ sole (the summer recruitment), the seasonal evolution nence of proportions, then Kerner's model is pertinent profiles of growth were parallel, with sorne variations and seems to be true for any group of species which of these profiles for the medium-sized (7 to 12 cm) are in competition for space and food, as appeared to individuals. The small-sized dab contrasted with the be the case in this coastal multispecific nursery. Analys­ small-sized plaice and sole, while the medium-sized dab ing ali the results by considering spatio-temporal varia­ presented a different seasonal evolution of growth from bility, Safran ( 1987 b) came to the conclusion that one plaice and sole. The large individuals (13 to 30 cm) of single community existed in this multispecific nursery, the three species, however, evolved together. made up of populations of juveniles, which presented temporal and spatial fluctuations, determined or alea-

Figure 9 2 21.8% 1 316.6% LPS guild: Correspondence Analysis shows projec­ Dab iAf-:-. A 4! :' tions of the "size-classes" vectors and "sampling­ Plaice :' :, : ' station 3" vectors in the plane of axes 1 and 2 (a), 1. Sole R"E. and in the plane of axes 1 and 3 (b). The letters ~I f t are the size classes defined in Table 3. Sum:r1er" ··~'-·~"···o / 1 ··c s La guilde LPS. Analyse Factorielle des Summer , Correspondances : projections des vecteurs tl,! Spring ; « classes de tailles » et « prélèvement-station 3 » lé 1 dans les plans factoriels (a) : 1, 2; et (b) : 1, 3. Les qi ~o~Dec.J o''lt: c 32.5% lettres représentent les classes de tailles données 't ~ \ ' tableau 3. t: . - - G\\• Wmter_,,'''Fe bJ C" \, WintidFeb.J t----E•D WÎnteTF_.., _1·~ _6: 1 32 5 (Dec.J.__c~~~Autu,;.m".(t.s:rg · 7o " \E--6 ® ~. @ ··c ~:

104 VARIABILITY AND STRUCTURE IN A FISH NURSERY

~ .. N tory, in the dominance of species. These populations 0 . ::;· :g 0 :;; l:! ~ .0 100 - ,.; ..; were not necessarily interconnected; but they might .,; ..; :~ .,; ::: have been in the past or might become so in the future. The sampling step permitted description of the seasonal fluctuations in the local faunistical compositions (there­ fore describing the specifie diversity and structure of the sampled community according to the zone), without modification of the general faunistical composition or 10 of the structure of the ichthyological community. The follow-up of temporal evolution for the individual RFD in station 3 of Boulogne-sur-mer (Fig. 10 a), for example, explicitly showed the faunistical fluctuations caused by successive replacements of the leading species in the first ranks. These seasonal flows of populations seemed to indicate a kind of "turnover" phenomenon at the structurallevel for the first ranks, albeit without modifying the general faunistical composition: i.e. the same species were always present. The four first ranks temporal evolution of the RFD-station 3 were occupied successively by .. populations of plaice, dab sole, accompanied by those Ss of goby, dragonet and sprat (Fig. 10a). The same distribution was obtained by smoothing, as represented by the cumulative RFD in Figure 4. These populations were apparently unconnected. Principal Component Analysis, a comp1ementary numerica1 method, executed on the the contingency table crossing 26 species by 15 samplings (Fig. 10 b), confirmed that seasonal flows were made up of small groups of individuals. Popula­ tions of the rare species were weak1y interconnected (0. 65 > r > 0.50), but no significant correlation was found among the dominant (structural, in terms of factorial analysis) species of this community.

The smoothed RFD methods (Safran, 1987 a) used Figure 10 here, particularly cumulative RFD, have proved useful Boulogne-sur-Mer (station 3): a) temporal evolution of individual rank­ frequency diagrams; and b) Principal Component Analysis: projections in clarifying the structure and faunistical composition in the plane of axes l and 2 of "species" vector [*=the flve flrst ranks of a sampled community. For a few selective environ­ of the RFD; correlation of species in the groups is 0.65 > r > 0.50]. ment, the RFDs are convex when there is a random Boulogne-sur-Mer (station 3). a) évolution temporelle des dia­ grammes rangs-fréquences individuels; et b) Analyse en Composantes permutation of the leading species in the samples Principales : projections dans le plan factoriel (1, 2) des vecteurs (Frontier, 1985). RFDs would be linear or concave, «espèces» (les espèces des 5 premiers rangs des DRF sont with a predominance of one or a few species, if the marquées*; les groupes correspondent à des espèces moyennement corrélées entre celles : 0,65 > r > 0,50). environment was highly selective (e.g. through seasonal turnover, pollution, etc.), and with the dominant few species likely to be distributed in the same order. Con­ sequently, the permutability of species might be, like the curve shape of the RFD, a characteristic of only undisturbed systems.

The complementary results obtained in the detailed study of dab, plaice and sole permitted acceptance of the existence of an LPS guild where, in the same Acknowledgements locality, ail sizes of individuals, belonging to three taxonomically related species and having similar ecol­ ogical resource requirements and foraging strategies, The author is grateful to Serge Frontier for advice shared space and time without obvious exclusion of and helpful suggestions during this work, and to lan any of the three species. The distribution of individuals Gleadall for constructive criticism of this text. He in space and time, which was a consequence of a thanks Elizabeth Harley for correcting the English regular flow of individuals passing through the nursery draft. The comments of anonymous reviewers were · and feeding the stocks with juveniles, allowed the main­ appreciated. This paper is adapted from part of the tenance of this cohabitation. It would be interesting, author's doctoral dissertation at the University of Lille in a complementary survey, to verify whether these (France), and was completed white at the Tohoku Uni­ juveniles of ail sizes are, or are not, confronted with versity (Sendai, Japan) under the support of a Monbu­ inter- and/or intra-specific competition phenomena. sho Fellowship from the Japanese Government.

105 P. SAFRAN

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