Quality of coastal and estuarine essential fish habitats: estimations based on the size of juvenile common sole (Solea solea L.)

Estuarine, Coastal and Shelf Science 58 (2003) 793–803

Quality of coastal and estuarine essential fish habitats: estimations based on the size of juvenile common sole (Solea solea L.) O. Le Papea,*, J. Holleyb, D. Gue´raulta, Y. De´saunaya a IFREMER-DRV-RH-ECOHAL, rue de l’Ile d’Yeu, B.P. 21105, 44311 Nantes Cedex 03, France De´partement Halieutique, Poˆle agronomique de Rennes, 65, rue de Saint-Brieuc, CS 84215, 35042 Rennes Cedex, France

b

Received 27 March 2003; accepted 23 June 2003

Abstract Survival and growth of early fish stages are maximal in coastal and estuarine habitats where natural shallow areas serve as nurseries for a variety of widely distributed species on the continental shelf. Processes occurring in these nursery grounds during the juvenile stage affect growth and may be important in regulating the year-class strength of fishes and population size. The need, therefore, exists to protect these essential fish habitats hence to develop indicators to estimate their quality. The purpose of the present study was to use the growth of juvenile sole as a means of comparing the quality of coastal and estuarine nursery habitats in the Bay of Biscay (France). These sole nurseries were clearly identified from studies based on trawl surveys carried out during the last two decades. The size of 1-group juveniles at the end of their second summer, as estimated from these surveys, is an indicator of growth in these habitats during the juvenile phase and can be used to compare habitat quality. A model taking into account the role of seawater temperature in spatial and interannual variations of juvenile size was developed to compare growth performance in the different nursery sectors. This study shows that the size of juvenile sole after two summers of life is not density-dependent, probably because the size of the population adapts to habitat capacity after high mortality during early-juvenile stages. Size is on one hand positively related to temperature and on the other hand higher in estuarine than in non-estuarine habitats. This high growth potential of juvenile fish in estuarine areas confirms the very important role played by estuaries as nursery grounds and the essential ecological interest of these limited areas in spite of their low water quality. If a general conclusion on habitat quality is to be reached about studies based on the growth of juvenile fish, it is necessary to use not only an integrative indicator of growth, like size, representative of the intrinsic habitat quality, but also more sensitive and less integrative means, such as otolith increments or caging experiments, which better respond to anthropogenic disturbance. Moreover, it is necessary to take juvenile densities into account. Ó 2003 Elsevier Ltd. All rights reserved. Keywords: essential fish habitat; coastal nursery grounds; growth; habitat quality; estuaries; Bay of Biscay; Solea solea

1. Introduction Survival and growth of early fish stages are maximal in coastal and estuarine habitats (Miller et al., 1984, 1988) where natural shallow areas serve as nurseries for a variety of species widely distributed on the continental shelf (Lenanton and Potter, 1987), particularly flatfish (Koutsikopoulos et al., 1989a; Van der Veer et al., 2000; Riou et al., 2001). The available area and the quality of

* Corresponding author. E-mail address: [email protected] (O. Le Pape). 0272-7714/03/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0272-7714(03)00185-9

coastal and estuarine habitats have a considerable influence on recruitment level (Rijnsdorp et al., 1992; Gibson, 1994). Human pressure in the form of anthropogenic disturbances is especially high in these areas. If juveniles are confined within coastal and estuarine habitats, nutrient excess or pollution loading could limit their growth in nursery grounds (Koutsikopoulos et al., 1989b; Fonds et al., 1995; Meng et al., 2002; Phelan et al., 2000) and affect recruitment level and population size (Burke et al., 1993; Johnson et al., 1998; Peterson et al., 2000; Ferber, 2001). In other words, processes occurring locally in nursery grounds during the juvenile stage affect growth and may be important in regulating

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the year-class strength of fishes and population size (Cowan et al., 2000; Scharf, 2000). Protecting these essential fish habitat is hence very important and it is the reason why the need exists to scientifically determine optimal fish habitats and to support decision making for their management (Rubec et al., 1999). As the growth of juvenile fish can be used to estimate the quality of essential fish habitats in shallow areas (Miller et al., 1988; Able et al., 1999; Meng et al., 2002; Stunz et al., 2002), the purpose of this study was to use the size of juvenile sole at the end of their second summer of life as a growth indicator to compare the quality of different coastal and estuarine nursery habitats in the Bay of Biscay, an arm of the North Atlantic along the west coast of France (ICES Area VIIIa/b; Fig. 1). Bay of Biscay sole, considered as a stock management unit (Anon., 2003), constitute an offshore population that spawns in late winter. Postlarval stages and early juveniles reach inshore areas in spring where they

continue their growth for about two years (Koutsikopoulos et al., 1989a). The main sole nursery areas have been clearly identified in the Bay of Biscay (Koutsikopoulos et al., 1989a; Dorel and De´saunay, 1991; Le Pape et al., 2003a) from studies based on trawl surveys carried out during the last two decades (Fig. 1): three of these areas are estuarine (Vilaine, Loire and Gironde estuaries), two are non-estuarine (Bourgneuf Bay and Pertuis Breton) and one is under moderate estuarine influence (Pertuis d’Antioche). The size of 1-group juveniles at the end of their second summer, as clearly estimated from these surveys, is an integrative indicator of growth in these habitats during the juvenile phase (Miller et al., 1988) and can be used to estimate and compare habitat quality. Preliminary analyses were used to filter sample bias before a model was developed to estimate size in the different habitats. This model takes into account the role played by seawater temperature on spatial and

Fig. 1. Map of the central part of the Bay of Biscay showing the main rivers and sole nursery grounds.

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interannual variations of juvenile size (Fonds, 1975, 1979). The results were analyzed to compare habitat quality between the different nursery sectors, and especially between estuarine and non-estuarine habitats. The relevance of this indicator of nursery habitat quality is then considered with regard to alternative and/or complementary growth indicators.

2. Materials and methods 2.1. Trawl survey data From 1980 to 1997, several independent coastal trawl surveys for juvenile flatfish species (especially sole) were carried out from the end of August to the end of October in the central part of the Bay of Biscay (Le Pape et al., 2003a; Fig. 1). This period, which coincides with the distribution of juvenile flatfish during the productive stage, was suitable for their collection in nursery grounds at the end of the growth phase, when trawl surveys can provide consistent estimates for 1-group fish (Dorel et al., 1991; Hanson, 1996). Two types of gear were used during these surveys: (1) A beam trawl (2.9 m wide, 0.5 m high, with a 20mm stretched mesh net in the codend) used to obtain abundance indices, especially for flatfish. (2) A bottom otter trawl (25 m long on the headline, with a 24-mm stretched mesh net in the codend) used in the same fishing areas to complete sample collection for laboratory analysis. Dorel et al. (1991) demonstrated that the estimations of abundance obtained from the catches of 1-group sole are not significantly different between these two gears. Operating conditions were checked and standardized (Dorel et al., 1991) after the first survey. Hauls were made only in daylight and performed at 2.5 knots. All sole were counted and measured at the lowest centimeter. Age groups were established after an otolith reading for each year studied. For the size of 1-group sole, the data did not require selectivity correction within the mesh size range used (Riou et al., 2001). In this comparative study, only trawl hauls conducted in the six main nursery sectors (Fig. 1) were retained (934 trawl hauls, Table 1). On average, 301 sole were caught in each nursery sector for each survey year. For each trawl haul, the size of each 1-group sole was known, and all sizes were modified by adding 0.5 cm to correct for the bias due to measurement at the lowest centimeter. However, for the nursery sector, the date of the haul, the associated bathymetry [categorised in three classes (<5 m, 5–10 m and 10–20 m); Le Pape et al., 2003a] and the fishing gear (beam or bottom otter trawl) were also available as descriptive variables for each haul.

Table 1 Number of trawl hauls carried out in different nursery sectors during the last two decades in the Bay of Biscay (autumn surveys) Year 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1992 1993 1996 1997

Gironde Pertuis estuary d’Antioche

Pertuis Bourgneuf Breton Bay 16 13 9

33 43

51 34

33 23

37

27

Loire Vilaine estuary estuary 25 16 15 26 23 17

18

22

24 21 28 38 43 48 46 39 45 43 34 44

2.2. Statistical methods Size determinism was studied with general linear models, the size of 1-group sole at the beginning of autumn being used as a response variable. These analyses were performed on a data set in which each 1-group sole was an individual characterized by its size; hence, the number of individual in the data set is equal to the total number of 1-group fish caught. For a given sector and a given year, the size distribution of juvenile sole is supposed to be Gaussian and it is the reason why linear models based on least square estimation criteria were used. The first part of the work consisted in the verification of these application conditions. Several linear models were used in this study, first to correct the bias due to sampling strategy and then to analyze the determinism of juvenile sole growth. When several descriptors were used simultaneously, the stepwise method was used to select only the significant ones. The first order interaction effects between these factors were also systematically taken into account in these analyses. Results were discussed according to the percentage of variance estimated from these models in which each 1-group sole was an individual. When the results were significant, another database has been used: the mean size of 1-group juvenile sole has been calculated for each year for each nursery sector. These mean sizes were used to illustrate the results on figures and also in models, to determine the percentage of the variability of the size explained by the descriptors, independently from interindividual variability. 2.3. Correction of sampling bias The influence of bathymetry, gear and sample date on the size of juvenile sole was firstly analyzed in order to

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correct for any bias due to sampling strategy. The following model was used: SizeYear;Sector;Bathymetry;Gear;Date ! FactorðYear; SectorÞ þ FactorðBathymetryÞ þFactorðGearÞ þ CovariateðDateÞ þ e with the response variable SizeYear,Sector,Bathymetry,Gear, Date, the size of each individual 1-group sole, characterized by an association of gear, bathymetric class and the location and date of catch and the descriptors: Factor(Year,Sector), a single factor describing both the survey year and the sector of the catch, Factor(Bathymetry), bathymetry (<5 m, 5 to 10 m or 10 to 20 m), Factor(Gear), sampling gear, (a 2.9 m beam trawl or a 25 m bottom otter trawl), Covariate(Date), date of the catch (day number of the year after January 1). First order interaction effects were also taken into account in these analyses. Data for 1-group sole size were finally corrected for bias with this model in order to study growth determinism. 2.4. Spatiotemporal disparity in juvenile size The following model was used to study if there are some spatiotemporal differences in juvenile size: Corrected SizeYear;Sector ! FactorðYearÞ þFactorðSectorÞ þ e with the response variable Corrected SizeYear,Vilaine, i.e. the size of each juvenile sole caught, as corrected for sample bias and the descriptors Factor(Year), the year of survey and Factor(Sector), the nursery sector. Interaction effects were also taken into account in this model. 2.5. Influence of sole density in the Vilaine estuary The influence of fish density in the cohort on fish size needed to be taken into account to quantify eventual density-dependent effects. As shown in Table 1, the Vilaine estuary (Fig. 1) was the sector most investigated during the study period (covered in 12 yearly surveys). The entire nursery area was investigated with the beam trawl in each of these surveys, according to a system of stratified sampling (Koutsikopoulos et al., 1989a) and provided consistent abundance indices in this area, especially for 1-group sole (Dorel et al., 1991): Corrected SizeYear;Vilaine ! CovariateðDensityYear;Vilaine Þ þ e with the response variable Corrected SizeYear,Vilaine, i.e. the size of each juvenile sole caught in the Bay of Vilaine, as corrected for sample bias and the descriptor

Covariate(DensityYear,Vilaine), i.e. annual density of 1-group juvenile sole, calculated on the Bay of Vilaine according to Pennington and Grosslein (1978) on the stratified sampling scheme. A study of the relation between size and density was not feasible in other nursery areas because of the few survey years involved and/or of the lack of a standardized sampling scheme. 2.6. Size model according to temperature As the growth rate of juvenile sole increases with water temperature (Fonds, 1979), it is important to analyze the influence of this parameter on their size and, hence, the role played by temperature as a habitat quality factor. Moreover, if the results are significant, that part of the spatiotemporal variability of size due to temperature is filtered out, so that the other differences between nursery sectors can be estimated. Sea surface temperatures (SST) in the area were taken from a database developed by the French meteorology agency (Me´te´o France). As no reliable bottom temperature was available from any source, the SST was assumed to represent water temperatures in the water column in coastal areas. These data were obtained by in situ measurements performed from commercial ships and were interpolated for 10-day periods on a 309 (latitude and longitude) space step grid. For each nursery sector, the SST was extracted from the corresponding mesh of the grid. Postlarval sole reach coastal areas in spring, where they continue their growth (Koutsikopoulos et al., 1989a). The movements of these coastal and estuarine populations show a seasonal periodicity. Juveniles leave shallow waters in autumn and return in spring to continue their growth during the summer productive period of their second year of life (Dorel et al., 1991). The following indices, based on this life cycle of juvenile sole, were used to provide an integrative description of seawater temperature in the growth period during the first two summers of life: SST over 10-day periods were averaged from the beginning of April (the main period of larval settlement) to the end of September (the period of migration to deeper waters) for the first summer of life and from the beginning of April (the period of inverse migration to shallow waters) to the end of August (just before the sampling surveys) for the second summer. These two average SST (first and second summers of life) were used as separate descriptors of sole size, and the average of the two values was also tested. A simple model, without a ‘‘Sector’’ effect, was used initially to study the influence of temperature: Corrected SizeYear;Sector ! CovariateðTemperatureYear;Sector Þ þ e

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with the response variable Corrected SizeYear,Sector, i.e. the size of each juvenile sole caught, as corrected for sample bias and the descriptor Covariate(TemperatureYear,Sector), i.e. one of the three descriptors of sea temperature, which are: 1. SST during the last summer (first summer of life), Covariate(TemperatureFirst summer,Sector), 2. SST for the present (second summer of life) summer, Covariate(TemperatureSecond summer,Sector), 3. average SST for these two summers, CovariateðTemperatureTwo summers;Sector Þ ¼ MeanðCovariateðTemperatureFirst summer;Sector Þ; CovariateðTemperatureSecond summer;Sector ÞÞ: The same analysis was also led with two covariates describing sea temperature for the first two summers of life Corrected SizeYear;Sector ! CovariateðTemperatureFirst summer;Sector Þ þ CovariateðTemperatureSecond summer;Sector Þ þ e: These models were used first in the Vilaine estuary alone and then in the Loire estuary alone (Fig. 1), i.e. the two sectors where the number of annual surveys was sufficient to test this relation (Table 1). Then, these models were used on the whole database. Moreover, the following model was used: Corrected SizeYear;Sector ! FactorðSectorÞ þCovariateðTemperatureYear;Sector Þ þ e with the response variable Corrected SizeYear,Sector, i.e. the size of each juvenile sole caught, as corrected for sample bias and the descriptors Factor(Sector), the nursery sector, Covariate(TemperatureYear,Sector), one of the three descriptors of sea temperature described above. The same analysis was also led with two different covariates describing sea temperature for the first two summers of life. First order interaction effects between sector and temperature were also taken into account in these models. 3. Results 3.1. Preliminary tests on data distribution A first analysis of data distribution by survey year and nursery sector, based on a chi square test of goodness of fit, showed that these size data follow a Gaussian distribution without a skew to the left or right, the variance of the size being not significantly different from a sample to another. As such data are

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quite suitable for linear techniques, the conditions for the application of linear models and the use of the least square estimation criteria in the following analysis were verified without contraindication. 3.2. Bias correction Neither the bathymetry class nor the choice of sampling gear had a significant influence on the size of 1-group juvenile sole. Data collected with both the 3-m beam trawl and the 25-m bottom otter trawl could be used indifferently, so that it was unnecessary to standardize the data according to sampling bathymetry. However, the date of the catch had a significant (a < 1%) influence on the size of sampled fish. As growth was not finished at the beginning of autumn, juvenile size continued to increase after this date (estimated slope: 0.015 cm day
1). A model with an interaction effect between the ‘‘Year ! Sector’’ factor and the ‘‘Date’’ covariate was also tested. This interaction effect made a significant but very slight contribution to the model, as compared to the single effect of date. As a specific slope for each year and each sector is calculated on a limited number of fish, caught during one survey on one nursery sector, this interaction effect greatly increased the uncertainty on the slope estimate, especially when a sector is covered in a very limited number of days at sea. Consequently, the model without an interaction effect, which provides a single estimated slope for the entire database, was used in order to filter out this date effect. In the next part of the study, the size of sampled juvenile sole is corrected according to this model and standardized to a common virtual date of catch (September 1). 3.3. Spatiotemporal disparity in juvenile size For a given sector and a given year, 1-group sole showed a large size range. After correction for the ‘‘catch date effect’’, the range reached 9.2 cm on average, for a mean standard error of 1.9 cm. The interindividual variations are hence very important. However, some spatiotemporal differences were apparent despite this variability in size distribution. Fig. 2 shows mean juvenile sole size per sector for the different years studied (Table 1), as computed from standardized data after correction for the ‘‘catch date effect’’. The differences in size were large, with a range of 3.5 cm for a mean of 19.1 cm. Interannual variations of mean size were very large for the different nursery sectors. However, analysis of the temporal series of mean size per sector indicated that there was no visual or significant temporal trend in juvenile size. Linear models including both year and sector effects in the same analysis showed that both of these parameters have a significant influence on juvenile size, but that there is no significant interaction effect between

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Fig. 2. Mean sizes of 1-group juvenile sole computed after correction for the date of catch effect and standardization to September 1 (a point represents the mean size for one annual autumn survey in one nursery sector).

them. The interannual variations in sole size appear to be quite synchronous for the nursery sectors. Nevertheless, the limited overlap between years and sectors in the database (Table 1) does not allow the ‘‘sector effect’’ of this analysis to be used as a reliable descriptor for comparison of size in the different nursery grounds. 3.4. Density-dependent process in the Vilaine Bay No significant relation was found between 1-group juvenile density and size in the Vilaine estuary. Juvenile sole size at the end of their second summer of life does not appear to be density-dependent in this nursery ground. 3.5. Size-based model with temperature effect The choice of the best descriptors of sea temperature (two separate ones for the first two summers of life, or the average of these two years) was studied first. In all the models, with or without sector effect, the synthetic descriptor describing the cumulated temperature for the first two summers of growth, Covariate(TemperatureTwo summers,Sector), provides the best results in term of explained variance. As this single descriptor appeared to be the best to describe the effect of water temperature on juvenile sole size, this simple formulation was chosen for the study. Models without sector effect, which tests the relation between juvenile sole size and water temperature during

juvenile growth, indicates that high temperature was significantly favorable to the growth of juvenile sole both in the Loire (a < 1%) and Vilaine (a < 1%) estuaries (tested separately, Fig. 3). For a given nursery ground, 1-group juvenile sole are larger in autumn when their first two summers of life are warmer. Conversely, if all of the data are used, the temperature effect, masked by spatial heterogeneity, is not significant with this model. The linear model taking into account both the sector and the temperature effects, with one intercept per sector (sector effect) and a common slope (temperature effect), applied on the entire data set indicates that both the nursery sector (a < 1%) and water temperature (a < 1%) had a significant influence on juvenile sole size. This model accounts for 9% of the spatiotemporal variations when the raw data (each caught fish is an individual) are used but for 61% of spatiotemporal variations of the mean size of juvenile sole per sector and per year. An alternative model, with interaction between temperature and sectors, was also tested. This model takes a sector-specific temperature slope into account. The contribution of this interaction effect is very limited, and the positive effect of temperature does not appear to be very sector-dependent. Moreover, addition of this variable markedly increases the uncertainty of parameter estimates, as the specific slopes are calculated on a limited number of years of survey, especially for the less investigated sectors (Table 1). Consequently, the model without interaction effect was used to compare the intrinsic values of nursery

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temperature descriptor in the database. This indicator of the size of juvenile sole at the end of their second autumn of life, as obtained from the model after spatiotemporal variations due to temperature were filtered out, is higher (Fig. 4) in estuarine areas (Vilaine, Loire and Gironde estuaries) than in nursery sectors without estuarine influence (Bourgneuf Bay and Pertuis Breton). The value obtained for the Pertuis d’Antioche, a nursery sector under limited estuarine influence, appears to be intermediate to these two groups. 4. Discussion 4.1. Is 1-group sole size a good indicator of juvenile growth?

Fig. 3. Relation between the mean surface temperature during the two first summer of life and the mean size of 1-group sole, computed after correction for the date of catch effect and standardization to September 1 in the Bay of Loire (a) and the Bay of Vilaine (b).

sectors as indicators of habitat quality. To obtain a realistic representation of these sector effects, the mean sizes of 1-group juvenile sole on September 1 were computed using a model with a temperature of 16.5  C for each nursery sector, i.e. the mean value of the

Processes occurring during the juvenile stage, especially growth, may be important in regulating year-class strength (Gibson, 1994). As there appears to be no relation among the factors affecting growth in adjacent coastal areas, which are specific to individual nursery grounds (Scharf, 2000), rapid growth can be used as an indicator of habitat quality (Phelan et al., 2000). In the Bay of Biscay, winter migration to deeper waters occurs between the first two summers (Dorel et al., 1991), but the distance involved is not sufficient to cause any significant mixing of fish from different nursery grounds. Thus, juvenile sole caught in a nursery ground after their second summer of life have achieved their growth there. The Bay of Biscay is regarded as a stock management unit for the common sole (Anon., 2003), and genomic studies suggest that there are no subpopulations in this area (Exadactylos et al., 2001). As the sole population

Fig. 4. Predicted mean sizes of 1-group juvenile sole in the six nursery grounds studied, together with the associated standard error, for a temperature of 16.5  C during the productive period.

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studied in this report appears to be homogeneous, size variations may be attributed to living conditions in the different nursery grounds. For both these reasons, the size of 1-group sole appears to be a reliable integrative indicator for comparing the growth of juvenile sole between different nursery grounds, and hence to estimate the quality of nursery habitats. 4.2. Lack of long-term density-dependent regulation of growth The size of juvenile sole at the end of their second summer of life does not appear to be related to the density of the cohort. Similar results were obtained by Riou (pers. comm.) for another sole nursery on the French coast. This result is confirmed by the Gaussian distribution of these data: when density-dependent competition influences growth, distributions are skewed to the right (Lekve et al., 2002). Density-dependent process can affect spatial distribution (Swain and Morin, 1996; Riou et al., 2001; Van Der Veer et al., 2000; Le Pape et al., 2003b), mortality (Van der Veer et al., 1990; Grover et al., 2002) and growth (Rijnsdorp and Van Leeuwen, 1994; Grover et al., 2002) in nursery grounds. Considerable mortality occurs during very young stages (Wennhage and Pihl, 2001), notably after settlement when larval stocking densities are very high, leading to food dependent, and hence density-dependent, regulation (Cowan et al., 2000). Density-dependent mechanisms could be important in postlarval stages, but juveniles surviving after several months, hence after their first two summers of life, are no longer food-limited in their habitat (Van der Veer et al., 1991; Rogers, 1994; Nash et al., 1994; Amara et al., 2001). As no relation is apparent between size and density, the size of juvenile sole from different sectors in which density may differ can serve as a suitable indicator for analyzing growth variations relative to the quality of nursery habitats for juvenile fish. 4.3. The important role played by sea temperature on fish habitat quality As demonstrated by Fonds (1979) in laboratory experiments and later verified in situ (Gibson, 1994; Yamashita et al., 2001; Lekve et al., 2002), seawater temperature influences the growth of juvenile sole. According to Fonds (1975), there is a positive linear relation between seawater temperature and juvenile sole growth for the temperature range observed on the Bay of Biscay nursery grounds during the productive period (from 10 to 22  C according to the SST database). The average SST indices used in this study are, therefore, equivalent to cumulated heat (expressed in degree ! day) for a linear relation. They take into account the cumulated effect of water temperature on sole size i.e.

growth from the time of larval settlement. Hence, the positive relation between SST and sole size at the end of their second summer of life allows to confirm on an integrative time step the very important influence of sea temperature on sole growth during the juvenile phase. High temperature is one of the main factors governing nursery habitat quality; it is moreover one of the main reasons of the concentration of juvenile fish on coastal areas during the growth period (Gibson, 1994). 4.4. Quality of estuarine habitats as estimated from sole size after filtration of the temperature effect In the present study, the use of a model including both the nursery sector and temperature allows comparison of the intrinsic quality of the different nursery habitats studied filtered out of the spatiotemporal variability due to temperature, and hence of latitudinal gradients. This approach, based on the use of size as an indicator of juvenile growth, indicates that potential growth is higher in estuarine habitats than in other coastal nursery sectors. This high growth potential in estuarine areas confirms the very important role played by estuaries as nursery grounds and the essential ecological interest of these limited areas. This interest can be attributed to two main reasons: (1) Estuarine areas are more productive than other parts of the coast, notably because of nutrient and organic matter enrichment which enhances the benthic trophic chain (Grall and Chauvaud, 2002) that constitutes the food supply for juvenile fish (Salen-Picard et al., 2002). A number of fish species prey predominantly on these estuarine soft bottom invertebrate communities during their nursery phase (Peterson et al., 2000). (2) Predation pressure influences habitat choice for juvenile fish (Laegdsgaard and Johnson, 2001); if a predation refuge is available, habitat use increases independently from growth rate in this habitat (Halpin, 2000). Estuarine gradients (e.g. temperature and salinity) may produce spatial refugia for juvenile and minimise the incidence of predation (Manderson et al., 2000). Estuarine habitats offer opportunities for both higher food availability and shelter from predation compared to areas outside. Hence, estuarine habitats serve as nursery grounds, enhance the growth, ensure the continuity of the life cycle and are essential fish habitats for a number of fish species (Miller et al., 1984; Lenanton and Potter, 1987; Thiel et al., 1997), especially sole (Rijnsdorp et al., 1992; Yamashita et al., 2000; Jones et al., 2002; Le Pape et al., 2003a). On the other hand, these conclusions show that it would be very difficult to estimate a possible effect of the degradation of water quality on fish size and more generally on fish growth: in this case study on sole in the Bay of Biscay, estuarine areas are the best sectors for

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growth, but are also the most polluted ones (Claisse, 1989) and these are where eutrophication problems are most important (Chapelle et al., 1994). The observation of the fact that estuarine soft sediment habitats are essential fish habitat in spite of an important degradation of water and habitat quality appears to be common (Peterson et al., 2000; Lindegarth and Hoskin, 2001). As fishes may be relatively tolerant to water and habitat quality, estuaries may provide beneficial habitats to fish, despite environmental degradation, the favorable characteristics of estuaries outweighing some of the negative aspects of human influence (Meng et al., 2002; Whitfield and Elliot, 2002 and the present study). These conclusions underscore the importance of protecting habitats in estuaries despite significant anthropogenic impacts. 4.5. Relevance of different types of growth indicators to the assessment of habitat quality The present study based on juvenile sole size (an easily estimated indicator) shows the relevance, but also the limitations, of using this method to evaluate habitat quality. The main property of this indicator, which takes juvenile sole growth into account since birth, is integrative over a long period. This indicator is reliable for comparing growth performance between different sectors; this advantage was previously noted by Lekve et al. (2002). Nevertheless, the problem with such an indicator based on the residual population of survivors after two years of growth is its lack of sensitivity to habitat disturbance. Koutsikopoulos et al. (1989b) and Amara et al. (2000) have shown that this sensitivity is high for the youngest juvenile sole and then decreases with age. Mortality, which is very high in postlarval stages and is weight/size-dependent (Cowan et al., 2000), can lead to selection of the larger individuals (Suthers, 1998). Therefore, this indicator, though quite reliable to compare the intrinsic quality of different habitat type, is subject to a variety of regulating influences and is not sufficiently sensitive to quantify anthropogenic disturbances systematically in estuarine and coastal areas. Complementary methods are required to improve the diagnosis. (1) Recent growth in the population can be estimated according to two different methods. The first, peripheral daily increment width of otoliths, provides information on daily growth (Karakiri et al., 1989; Stunz et al., 2002). This method can be used notably to study the response of juvenile growth to short-term environmental changes (Koutsikopoulos et al., 1989b). The second method consists in estimating the growth occurring between two consecutive surveys by regressing mean length against the time when the samples were taken (Shi et al., 1995). Both these methods estimate short time growth after adaptation of population size to habitat capacity.

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(2) Other studies have used caging experiments to determine the growth of juvenile fish and thereby assess habitat quality (Able et al., 1999). These experiments were performed to determine relative habitat-specific growth in standardized conditions, without densitydependent and/or mortality-induced effects (DuffyAnderson and Able, 1999; Phelan et al., 2000; Curran and Able, 2002). As the fish used for experiments were enclosed, migration was not possible, allowing comparisons on a small spatial scale. However, growth results in enclosures need to be evaluated carefully, as these movements may have an important influence on growth (Stunz et al., 2002; Halpin, 2000). These alternative methods, though more sensitive than a fish size approach, are naturally less integrating. Therefore, it is more difficult to extrapolate the conclusions to larger spatial and temporal scales typical of coastal management requirements. In fact, a combination of several indicators is needed to obtain a reliable diagnosis of habitat quality (Suthers, 1998), density and long-term indicators of growth (such as size), to quantify both the capacity and the intrinsic quality of habitat (Curran and Able, 2002), and short-term and/or small scale (but more sensitive) indicators of habitat disturbance, such as otolith microstructure or caging. However, the resistance of fish to human degradation of habitat quality can be important, so that the effect of disturbances is difficult to estimate (Fonds et al., 1995), especially if intrinsic differences in the growth potential of nursery sectors, such as those considered between estuaries and the rest of the coast (Meng et al., 2002; Whitfield and Elliot, 2002 and the present study), can mask anthropic effects. Acknowledgements This project was supported by the French program for the coastal environment (PNEC). Special thanks are due to Pierre Beillois (IFREMER) for providing SST data. The authors are also grateful to the two anonymous reviewers and the editorial board for their fruitful suggestions. References Able, K.W., Manderson, J.P., Studholme, A.L., 1999. Habitat quality for shallow water fishes in an urban estuary: the effects of manmade structures on growth. Marine Ecology Progress Series 187, 227–235. Amara, R., Laffargue, P., Dewarumez, J.M., Maryniak, C., Lagarde`re, F., Luczac, C., 2001. Feeding ecology and growth of 0-group flatfish (sole, dab and plaice) on a nursery ground (southern Bight of the North Sea). Journal of Fish Biology 58, 788–803. Amara, R., Lagarde`re, F., De´saunay, Y., Marchand, J., 2000. Metamorphosis and estuarine colonisation in the common sole, Solea solea (L.): implications for recruitment regulation. Oceanologica Acta 23, 469–483.

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