The influence of environmental conditions on settlement, distribution and growth of 0-group sole (Solea solea (L.)) in a macrotidal estuary (Vilaine, France)

307

Netherlands Journal of Sea Research 27 (3/4): 307-316 (1991)

THE INFLUENCE OF ENVIRONMENTAL CONDITIONS ON SETTLEMENT, DISTRIBUTION AND GROWTH OF 0-GROUP SOLE (SOLEA SOLEA (L.)) IN A MACROTIDAL ESTUARY (VILAINE, FRANCE) JOCELYNE MARCHAND Laboratoire de Biologie Marine, Universite de Nantes, 2 rue de la Houssiniere, 44072-Nantes Cedex 03, France

ABSTRACT In the Vilaine estuary, the environmental conditions at the onset of the settlement of metamorphosing sole have been surveyed for 5 years. The inshore migration occurs either in early or in late April depending on the hydroclimatic conditions: sole are observed in the estuary when bottom water salinity varies between 25 and 30 S and water temperature is up to 11°C. During spring, their distribution pattern is similar in all years: first, accumulation at the entrance of the estuary, then concentration in the upper parts and finally, colonization of the whole estuarine area by juveniles. Interannual variations in growth rates were observed during their first estuarine phase, in particular when the estuary is transformed into a 'ria' with high water temperature and salinity. These biological features are discussed according to ontogenic changes occurring during these early life stages. From field and experimental data and from literature information on sole and other pleuronectiform species, a conceptual model on relationships between environmental parameters and metamorphosis processes in estuarine areas is proposed. 1. INTRODUCTION Estuarine nursery areas are used by juveniles of many euryhaline fish species. In these areas growth occurs under favourable conditions, i.e. with large food resources and few predators (MILLER et al., 1985; DAY et al., 1989). Only few studies discuss the interannual variability of larval recruitment in relation to environmental parameters (ALLEN & BARKER, 1990). ROGERS (1989) presented a review of the literature concerning the ecology of the juvenile sole Solea solea (L.), which is a typically estuarine-dependent species. Although much information is available on the egg, larval and juvenil e stages (distribution, patterns of migration, diets), the mechanisms involved in metamorphosis and settlement of soles into the nurs-

ery areas are not well understood. In the Bay of Biscay, which is bordered by many shallow-water bays and estuaries, sole is one of the most important commercial species. Spawning and larval development occur in offshore stable waters (KOUTSIKOPOULOS & HERBLAND,, 1987; KOUTSIKOPOULOS et al., 1988), and metamorphosing soles are observed in the many bays and estuaries with different environmental conditions (LAGARD#__RE, 1982; LE, 1983; MARCHAND & MASSON, 1989). The hydrological structure of these coastal areas depends directly on the meteorological conditions. Therefore the timing of larval immigration into the nursery and distribution on the feeding grounds is supposed to be controlled by these abiotic parameters. This study examines the interannual variability of the larval immigration to and settlement of sole in one of its nursery areas, as well as the growth rate of the newly settled individuals. The link between these biological data and the environmental conditions will be discussed and a conceptual model on relationships between environment and metamorphosis processes will be proposed. Acknowledgements.--This work, which was supported by grants from the CNRS and the IFREMER, is part of the French Programme on the 'Determinism of Recruitment'. The author is grateful to J.P. Bourse for his assistance in the field work. 2. MATERIALS AND METHODS The Vilaine ecosystem (bay and estuary) is located in southern Brittany. For surveys of juvenile sole the nursery ground (110 km 2) was divided into 5 areas defined according to depth and sediment (DOREL et al., 1989; KOUTSIKOPOULOSet al., 1989) (Fig. 1). The present study concerned only areas 0, 1 and 2. In the estuary (9 km long; area 0=3 km 2 with mud substrates), hydrological conditions depend on the river discharge, which is controlled by a barrage, and on the semidiurnal tides, which range from 1.8 m at neap tides to 5.8 m at spring tides. When there is no river discharge, bottom and surface current speeds

308

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vey). Sampling was conducted from a 10-m commercial trawler. From 1987 to 1989, stations were sampled with a small beam trawl (1 m width; 1.5 mm mesh size) as described in MARCHAND & MASSON (1989). In 1990 sampling was done with an epibenthic sledge. The sledge consisted of a rectangular frame (1 m width, 0.7 m height) mounted on a chassis with skates, which allowed the sampler to be towed across the bottom without digging into the sediment. Nevertheless, in most cases the lower edge of the 1.5-mm mesh size net was working less than 10 cm above the bottom (occurrence of benthic fauna like mollucs, annelids and starfish). As the aim of this work was to study the distribution of sole and not their abundance, gear efficiencies were not compared. At each station, gears were towed for 10 to 15 minutes, at a mean boat speed of 2.6 knots so that haul distance, estimated by a Korel Radar System, was always about the same (900 m) irrespective of the hydrological conditions. In the estuary, towing was done in the channel against the current around

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Fig. 1. Above, map of the Vilaine bay and estuary (divided into 5 strata) with position of the transect prospected from 1987 to 1990 and location of the station (,) studied in 1986 (diel cycles). Below, profile of the prospected transect with depth and sediment nature.

I. . . . . . . . . .

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vary between 0.3 to 0.7 m.s -1 at ebb tide and 0.5 to 1 m.s-1 at flood tide. When the river is in spate, both surface and bottom current speeds are reduced at flood tide (0.1 to 0.4 re.s-l). At ebb tide, surface current speeds increase (0.6 to 1.25 m.s-1), whereas bottom speeds are slightly reduced (0.3 to 0.5 m.s -1) (LE HIR et al., 1986; MARCHAND & MASSON, 1987). In the bay, the offshore limits of area 1 (27 km 2 with muddy sand) and area 2 (41 km 2 with sandy mud) correspond to the 5- and the 10-m-depth strata, respectively. In these areas, the hydrological conditions are mainly linked to the wind regime, tides having a weak impact on water circulation with current speeds of 0.3 m-s -1 (DE NADAILLAC & BRETON, 1986; SALOMON & LAZURE, 1988). The residual circulation is mainly driven by the wind and can reverse in different meteorological situations. According to the wind direction, surface and bottom currents may be either in the same direction or opposite. From 1987 to 1990, surveys of metamorphosing and juvenile soles were conducted from April to June along a 18-km-long transect (15 to 20 stations by sur-

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Fig. 2. Hydroclimatic conditions in the Vilaine ecosystem from 1986 to 1990. a. evolution of the monthly hydraulic coefficient from April to September; b. characteristics of wind regime and speed calculated by fortnightly periods from April to June.

SETTLEMENT, DISTRIBUTION AND GROWTH OF 0-GROUP SOLE IN ESTUARY IN FRANCE

309

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low tide when mudflats were emerged (due to the topography of estuarine banks, there are few pools on mud flats at low tide where young fish may concentrate). Every spring at each station, hydrological data (temperature and salinity) were recorded on vertical profiles with a 5005 ABB Kent salinity and temperature bridge. Hydroclimatic conditions were provided by the Central Hydrological Service for river discharge values from a station located 16 km upriver from the barrage and by the National Meteorological Office for wind regime from the Belle-lie weather station located in the Bay of Vilaine, 60 km off the barrage. From the river flow values recorded during the study period and the average values calculated over a 6-year period (1980-1985), the 'hydraulic coefficient' (H.C.) of the Vilaine was estimated for each month. When H.C. is up to 1, the freshwater budget is considered in excess; when it is lower than 1, it is in deficit. According to the compass card, offshore wind (360 ° to 80 ° ) was considered positive values, onshore wind (180° to 280 ° ) negative values. In addition to these surveys, data collected in 1986 surveys (diel cycles at one estuarine station, Fig. 1) will be also taken in consideration (MARCHAND & MASSON, 1989). The growth of young sole during their first estuarine phase was studied by conducting surveys in September with a 3-m beam trawl (20-mm stretched inside mesh net without tickler chains) described in KOUTSIKOPOULOS et al. (1989). For each sample all soles were sorted, measured (total length) and counted. Abundance and size composition were corrected according to the gear selectivity (DOREL et al., 1989). From these measurements, mean size was calculated with standard deviation either in the whole or in each subarea and growth rate was estimated from increases in mean lengths over time. The larval stages were determined according to the criteria defined by RYLAND (1966) for plaice and revised by Lagardere (unpublished data) for sole: metamorphosis occurs during stages 4 and 5, which are divided into substages. Sole are considered juvenile when scales appear on the head and when pigmentation pattern is similar to that of the adults. 3. RESULTS 3.1. HYDROCLIMATIC AND HYDROLOGICAL CONDITIONS The hydroclimatic conditions High interannual variability river flow (Fig. 2a) was observed. In 1986, deviations of the river flow were considerable in April, July and September with exceptional wet spells due to snow melting in April and intermittent rainfalls in summer. In 1987 and 1988,

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Fig. 3. Estuarine hydrological conditions (presented by fortnightly periods) during spring from 1986 to 1990: above, bottom water temperature; below, bottom water salinity. Periods of first occurrence of sole are indicated by vertical arrows. values were close to average except in May, August and September 1987, when dry periods occurred. In 1989 and 1990, the river flow values highly diverged from average with an exceptionally dry spell from April to September. The main wind directions were north-northeast (offshore) and west-southwest or northwest (onshore) (Fig. 2b). In 1986, after a period of offshore wind (first 2 weeks of April) the wind regime remained stable with onshore winds. The period of offshore winds may be longer, as observed in 1988 (1.5 months). In 1987, 1989 and 1990, onshore winds occurred in early April and then alternated more or less regularly with offshore winds. When long periods (1 month) of stability occurred with onshore winds, like in late AprilMay 1986, the residual circulation in the bay is strongly orientated to the estuarine areas (surface and bottom) (KERDREUX et al., 1986; SALOMON & LAZURE, 1988). Ten to fifteen day-long periods with offshore winds (like in April 1986 and 1988) induce a surface water drift in a west-northwestern direction (parallel to the shore line) and an orientation of the bottom water layer to the estuary. The wind influence may be modified by the level of river discharge. Temperature and salinity data were recorded in the

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bottom water layer (0.5 m above the substrate) at a station located in the estuary, 7 km downstream the barrage. These parameters, means per 2 weeks periods, followed the same pattern from April to June in 1987, 1988, 1989 and 1990 (Fig. 3). Temperature increased progressively from 12°C in early April to 20-22°C in June and salinity varied between 25 and 30 S except in 1990, when no freshwater influx occurred (31 to 34 S). In early spring 1986, conditions were different: cold (8°C) and mesohaline water (7 S) during the first 2 weeks of April, normal conditions in late April (14°C and 27 S) and again mesohaline (14 S) and colder (12°C) waters in early May. These variations were linked to snow melting and considerable rainfall, which occurred in April and May, respectively. The hydroclimatic conditions during spring can be summarized as cold and wet weather in 1986; warm and dry weather in 1987; warm and wet weather in 1988; hot and very dry weather in 1989 and 1990. 3.2. IMMIGRATION AND SETTLING OF SOLES The first young soles always arrived in the first part of April. Only in 1986 during cold and wet weather did they start immigration in the second part of April (Fig. 3). In all cases, river flow was less than 100 m3 and water temperature was up to 11°C. Immigration of metamorphosing soles occurred for 30 to 45 days and ended in early June in 1986 and in May the other years (Fig. 4). Evaluation of the metamorphosing soles caught showed that April was the main demersal settlement period except in spring 1986, when intensive larval immigration took place up to early June. In all years of study, the first soles collected on the nursery grounds were either metamorphosing (1986, 1987, 1989, 1990) or newly metamorphosed (1988) •

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3.3. DISTRIBUTION OF NEWLY SETTLED SOLES Interannual comparisons of newly settled soles from April to June in the study area showed that distribution patterns were similar in all years (Fig. 5). In April, the distribution was mainly limited to the estuary entrance in high density water areas (23 to 25) characterized by muddy sand sediments. In May, they migrated upstream colonizing the muddy estuarine area, and in some cases concentrations were observed at the bottom of the barrage (1987-1989). Abundance peaks mainly occurred in areas with the lowest water density. In June, the distribution was either limited to the estuary when the water density was different in both parts of the estuary (1987) or more or less extended to the bay when hydrological conditions were homogeneous all along the transect (1988, 1989, 1990). The onset period of estuarine settlement was studied during 2 periods in April 1990 (Fig. 6). On 2 April, the metamorphosing soles (substages 5a-c) were mainly concentrated in the bay in high-density waters (25). On 18 April, one peak was present at the same location in the bay (water density=25); and the second was found in the estuary (water density=22.5). In the bay there were no significant differences (o~=5%) between size and stage distribution on the two dates (t=0.07; df=235). In the estuary soles were clearly larger and older when they settled there in mid-April (substage 5c and juveniles with a 12.07 mm mean size) (t=11.5; df=568).

1

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stages with sizes of 7 to 15 mm total length (Fig. 4). Comparisons of size distributions of metamorphosing soles at stations where they were the most abundant showed significant differences (o~=5%) between April and May with smaller ones in April, except for 1986 and 1988. Interannual comparisons showed that soles collected in April 1988 were larger and older (newly metamorphosed) than those sampled the other years. However, no significant differences were found from soles collected in May 1987 and May 1989. Likewise, no significant differences were observed between metamorphosing soles collected throughout spring 1986 and those sampled in April 1987 and April 1989. Such variations among years suggest that timing of migration and sole characteristics are linked to the hydrological conditions of the nursery grounds: the association river flood-offshore wind is clearly unfavourable to the estuarine penetration of metamorphosing soles (1986). When the hydraulic coefficient of the river is low, the wind influence is less obvious and whatever its orientation, marine waters enter the estuarine area (mainly by the bottom) and allow the settlement of young soles.

10

20

JUNE

Fig. 4. Variations of the mean total length (with standard deviations) of the settling soles in the Vilaine ecosystem during spring from 1986 to 1990.

SETTLEMENT, DISTRIBUTION AND GROWTH OF 0-GROUP SOLE IN ESTUARY IN FRANCE

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Considering the distribution of young soles (mean sizes at abundance peaks) according to bottom water density, we noticed that whereas metamorphosing soles were always concentrated in high water density areas (20 to 25), juveniles were found in a wider and lower range of water density (10 to 25) (Fig. 7). This suggests that as 0-group sole grow, their ability to tolerate various haline conditions improves.

3.4. GROWTH VARIATIONS OF JUVENILE SOLE Two successive growth periods were considered: April to June (spring) and June to September (summer). Interannual comparisons of daily growth rates showed that during spring high variations were observed from 0.49 mm.d-1 in 1989 to 0.74 ram.d-1 in

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Fig 6. Comparisons of distribution, size and stage composition of the metamorphosing soles at settlement in April 1990. 1988 and that during summer growth rates were rather similar (0.6 mm.d -1 except for 1990). Interannual comparisons of mean sizes showed that significant differences were observed in June except for 1986 compared with 1989 and 1987 compared with 1990, when there were also no significant

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differences between mean sizes of metamorphosing soles in April (Fig. 8). The strongest deviations were observed for soles collected in September 1988 and 1990 (Fig. 9). In 1988, soles which were completely metamorphosed at their entry into the estuary in April reached a large mean size in September (122.05

SETTLEMENT, DISTRIBUTION AND GROWTH OF 0-GROUP SOLE IN ESTUARY IN FRANCE

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Total length (mm) Fig. 7. Distribution of metamorphosing sole according to estuarine conditions. Relation between their mean total length and water density from April to June (5 year data cumulated). mm). This difference was linked to the particularly high spring growth rate (0.7 mm.d -1) in 1988. The small mean sizes in September 1990 (84.06 mm) may be mainly related to the low summer growth rate 0.4 mm.d -1 instead of 0.6 mm.d -1. These data indicated that interannual growth rates vary mainly during the spring, which generally has unstable hydroclimatic conditions; in summer, the growth rate is more regular and the only disturbance observed was linked to an exceptional heatwave associated with a complete lack of freshwater discharge in 1990. 4. DISCUSSION Most of the fish species, spawning offshore and being estuarine-dependent, recruit to estuaries at late larval stages, near or after metamorphosis (BOEHLERT & MUNDY, 1988). Recruitment, migration and utilization of estuarine nurseries have been •

1986

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313

described and discussed in terms of distribution, behaviour and metabolic processes in relation to physical factors (temperature, currents, salinity, oxygen, etc.) (ARNOLD, 1981; MILLER etal., 1984, 1985; BOEHLERT & MUNDY, 1987). AS the estuarine environment is typically unstable, effects of variations in abiotic conditions may be expected on the immigration processes of metamorphosing larvae (timing, size, stages), which undergo important changes (behaviour, physiology, metabolism, nervous system, olfactive tractus, etc.) and then, on the distribution and growth of juveniles. For sole, we observed that the first cohort which entered the bay consisted only of metamorphosing larvae. Some weeks later, another cohort with an identical size structure was collected in the same area. At the same time, in the estuary, older larvae and juveniles were present. We assume that for most sole, metamorphosis occurs during their transport from the spawning grounds to the nursery areas and that the bay corresponds to the 'channel' or 'mouth' described by BOEHLERT & MUNDY (1988) as the area under estuarine influence. In this area, metamorphosing larvae migrate by pulses to the estuary with a remarkable stability in location of their catch peaks. This zone may play the role of an 'accumulation' area (BOEHLERT & MUNDY, 1988) particularly when the estuarine conditions are unfavourable as in 1986. When an offshore wind is associated with river floods, accumulation of metamorphosing soles out of the estuary, which remains an oligo-/mesohaline area may be prolonged for 2 or 3 weeks and slackening of metamorphosis processes may be observed. Such a delayed estuarine settlement of sole consists of several pulses, each pulse corresponding to the improvement of estuarine conditions (MARCHAND & MASSON, 1989). An early settlement may be observed in the estuary when the hydrological condi-

1990

% 50

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30/1

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Fig. 8. Interannual variations of mean sizes (with standard deviations) of 0-group sole from April to June (1986 to 1990) in the estuarine ecosystem.

10

60

70

80

90

100

110

120

130

140

150

Total length (mm)

Fig. 9. Comparisons of size distribution of 0-group sole in September 1988, 1989 and 1990 in the Vilaine ecosystem.

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J. MARCHAND

tions are favourable. When the river flow is weak, the influence of tide cycles on mixing of marine and estuarine waters is prevailing. If wind conditions are favourable (onshore winds), this process may be speed up by the shoreward displacement of the whole water column (KERDREUX et al., 1986; SALOMON & LAZURE, 1988). In this case, the bay is only a 'transit' area and when they settle on the nursery grounds, the young soles are nearly or completely metamorphosed. Such a situation was observed in 1987, 1988, ]989 and 1990, and then immigration is accomplished more quickly, mainly in April. Temperature is one of the main parameters controlling larval development (FOND& 1979; RAMOS, 1986; LAGARDI~RE, 1989). Experimentally, RAMOS (1986) observed that whereas at 14°C, metamorphosis occurs when larvae are 21 days old, it occurs in 12 days when the water temperature is 18°C. Moreover, this author showed that with increasing temperatures, growth rates increased (0.2 mm.d -~ at 14°C; 0.47 mm.d -1 at 21°C). Otolith reading carried out on sole larvae collected in sea for ageing showed that in 1987, metamorphosis occurred at 9.5 mm when the larvae were more than 30 days old; in 1988, larvae metamorphosed at 9-mm length when 30 days old (Lagardere, pers. comm.). Such differences in age and size at metamorphosis may explain deviations of sole characteristics observed as they settle on the nursery grounds: young soles may be either newly metamorphosed as in 1988 or in metamorphosis as in 1987, depending on the hydrological conditions they encountered during their early larval stages on the spawning grounds and during their transport in the bay. To understand mechanisms involved in settlement processes, we propose a conceptual model (Fig. 10) based on field and experimental observations and on literature information on sole and other fish species (mainly pleuronectiforms). In the bay, an area of estuarine influence, young fish ready to settle are subjected to a complex assemblage of 'cues' from the estuarine environment: temperature, salinity, food, etc. (BOEHLERT & MUNDY, 1988). The physiological changes occurring during metamorphosis of sole larvae are controlled by the endocrine system, which depends on photoperiod and temperature seasonal variations (HOAR, 1957). Our observations on the distribution of metamorphosing soles according to salinity conditions suggest that in the area of estuarine influence (bay), the increasing temperature stimulates the activity of the endocrine system. Hormonal secretions by the pituitary gland or the thyroid induce a progressive improvement of the osmotic ability, which furthers their upstream migration to areas of decreasing salinity. In the Vilaine estuary, this hypothesis is even more likely since other environmental parameters such as the nature of sediment

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VIRONMENTAL PARAMETERSJ

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(upstreammigration) (feedingadivity) Fig. 10. Scheme summarizing hypotheses on relationships between environmental parameters and sole ontogenic processes during metamorphosis in an estuarine ecosystem. (mud) and food resources, which are similar in the whole settlement area (from the mouth to the barrage) cannot be considered as keyfactors. Likewise, the immigration of sole in the area under estuarine influence may be favourable to the speeding up of their ontogenic transformation by stimulation of output of thyroid hormones, which control metamorphosis (thyroxine) (TANAKA et al., 1989; INUI & MIWA, 1985). These hypotheses will have to be considered in future research on sole metamorphosis processes. HOAR (1957) indicated that thyroid activity influences swimming activity. BERGHAHN (1983) observed that newly metamorphosed soles are able to swim against the ebb-tide currents and exhibit a positive rheotaxis behaviour, which allows them to remain in the puddles and drainage gullies on tidal flats at low tide. MACQUART-MOULIN et al. (1989) demonstrated experimentally that a circatidal behaviour of sole larvae and juveniles was induced by pressure variations like waves or tides increasing their swimming activity at ebb tides. The progressive upstream migration we observed in the nursery grounds may be interpreted as a manifestation of this behaviour, whereby the newly metamorphosed soles are progressively losing the nychthemeral rhythm of vertical migrations observed during metamorphosis (MARCHAND & MASSON, 1989; CHAMPALBERT et al., 1989).

SETTLEMENT, DISTRIBUTION AND GROWTH OF 0-GROUP SOLE IN ESTUARY IN FRANCE

The feeding behaviour of sole is well known (DE GROOT, 1971; KRUUK, 1963; LAGARD#:RE,1987). Feeding activity is nocturnal and sole is mainly an olfactive-feeder. The chemosensory organs are elaborated during larval development and the definitive olfactive apparatus is completed at the end of metamorphosis (APPELBAUM et al., 1983). MACKIE et al. (1980) showed that 'detection and selection of food by captive Dover sole (Solea solea (L.)) are mediated by specific chemicals that diffuse from the food pellet into the water and react with chemosensory cells'. A chemical which attracts juvenile sole is glycine-betaine, which is a component of animals, like polychaetes, mollucs and crustacea, consumed by them (KONOSU et al., 1966; KONOSU & HAYASHI, 1975). For plaice, CREUTZBERG et al. (1978) demonstrated experimentally that feeding conditions act upon the swimming activity of larvae: when larvae do not find adequate benthic food, starvation induces pelagic swimming. When they are subjected to offshore water movements carrying olfactory substances from inshore areas, a benthic behaviour is induced. MARCHAND & MASSON (1987, 1989) observed that as metamorphosis occurs, sole behaviour evolves progressively from a nychthemeral rhythm of vertical migrations to a benthic activity and that digestive tracts of most sole collected in the water column were empty. These data suggest that the role of olfaction in the orientation and behaviour of metamorphosing sole is important and deserves further study. For sole, the 'water odour' could be one of the estuarine 'attractive cues'. BERGHAHN (1987) showed that growth of 0-group plaice during their first estuarine phase may be affected by tidal migrations between channels and mudflats and that an insufficient food supply may induce a slow increase in length. For the sole we observed that in September variability in size may be high. An explanation may be the hydroclimatic conditions, which act upon the hydrological structure (temperature and salinity) of the nursery grounds. Growth rate may be low in a hot and dry years (1989-1990), and high in hot and wet year (1988). When the river flow is regular throughout spring, barrage gates are regularly opened and a freshwater discharge occurs in the estuary. Then the estuary is a true brackish water area with typical benthic communities. This was the case in 1986, 1987 and 1988 with a high haline gradient in the estuary. When the river flow is too low, barrage gates remain closed and as no river discharge occurs, the estuary becomes a 'riM' with warm and euhaline waters with no salinity gradient between its upstream and downstream limits. As the estuarine benthic communities are affected by these conditions (species composition and abundance) we assume that they are not able to constitute large amounts of adequate food for the whole predatory

315

community. In this case, interspecific competition for food may occur between sole and other predators as BERGHAHN (1987) observed for plaice in Wadden Sea. Moreover, as water exchange between the bay and the estuary is weak (only tides), anoxia may occur and fish, which avoid this area are obliged to consume more oxygen for their movements or their food seeking. MILLER et al. (1985) indicated that swimming costs may be three times higher than tolerance costs for estuarine fish when estuarine conditions are too stressful. Then less energy is invested in growth process and thus, maximal sizes may be reduced. The success of settlement of 0-group sole (and certain other estuarine-dependent species) on estuarine nursery grounds depends on to the agreement or the gap, which may occur between the different stimuli characterizing the estuarine waters and the physiological features of fish. This hypothesis would have to be considered in further studies. 5. REFERENCES ALLEN, D.M. & D.L. BARKER, 1990. Interannual variations in

larval fish recruitment to estuarine epibenthic habitats.--Mar. Ecol. Prog. Ser. 63: 113-125. APPELBAUM,S., J.W. ADRON, S.G. GEORGE,A.M. MACKIE& B.J.S. PIRIE, 1983. On the development of the olfactory and the gustatory organs of the Dover sole, Solea solea, during metamorphosis.--& mar. biol. Ass. U.K. 83: 97-108. ARNOLD, G.R, 1981. Movements of fish in relation to water currents.I In: D.J. AIDLEY. Animal migration. Cambridge University Press, New York: 55-77. BERGHAHN, R., 1983. Untersuchungen an Plattfischen und Nordseegarnele (Crangon crangon) im Eulittoral des Wattenmeeres nach dem Ubergang zum Bodenleben.--Helgol~.nder Meeresunters. 36: 163-181. ----, 1987. Effects of tidal migration on growth of 0-group plaice (Pleuronectes platessa L.) in the North Frisian Wadden Sea.--Ber. dt. wiss. Kommn Meeresforsch. 31" 209-226. BOEHLERT,G.W. & B.C. MUNDY,1987. Recruitment dynamics of metamorphosing English sole, Parophrys vetulus, to Yaquina Bay, Oregon.--Estuar. coast. Shelf Sci. 25: 261-281. ----, 1988. Roles of behavioral and physical factors in larval and juvenile recruitment to estuarine nursery areas.Am. Fish. Soc. Symp. 3: 51-67. CHAMPALBERT, G., A. BOURDILLON, C. CASTELBON, D. CNIKHI, L. LE DIREACH-BOURSlER, C. MACQUART-MOULIN & G. PATRITI, 1989. Determinisme des migrations des

larves et juveniles de soles.--Oceanis 15: 171-180. CREUTZBERG, F., A.TH.G.W. ELKING & G.J. VAN NOORT, 1978.

The migration of plaice larvae Pleuronectes platessa into the Western Wadden Sea. In: D.S. MCLUSKY& A.J. BERRY. Physiology and behaviour of marine organisms: 243-251. DAY, J.W., C.A.S. HALL, W.M. KEMP 8 A. YA~ez-Arancibia, 1989. Estuarine ecology. Wiley & Sons: 1-558.

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J. M A R C H A N D

DOREL, D., Y. DESAUNAY & J. MARCHAND, 1989. Prise en compte des migrations saisonnieres des soles juveniles pour I'estimation d'abondance des prerecrues sur une nourricerie (Golfe de Gascogne, France).--ICES C.M. 1989/G:30 (mimeo). FONDS, M., 1979. Laboratory observations on the influence of temperature and salinity on development of the eggs and growth of the larvae of Solea solea (Pisces).--Mar. Ecol. Prog. Ser. 1: 91-99. GROOT, S.J. DE, 1971. On the interrelationships between morphology of the alimentary tract, food and feeding behaviour in flatfishes (Pisces: Pleuronectiformes).-Neth. J. Sea Res. 5: 121-196. HOAR, W.S., 1957. Endocrine organs. In: ME. BROWN. The physiology of fishes 1: 246-285. INUl, Y. & S. MtWA, 1985. Thyroid hormone induces metamorphosis of flounder larvae.--Gen, compar. Endocr. 60: 450-454. KERDREUX M., M. MERCERON, R LE HIR, & M. BRETON, 1986. Suivi de flotteurs dans la zone Loire-Vilaine.-Rapport IFREMER DERO-86-30: 1-29. KONOSU, S. & T. HAYASHI, 1975. Determination of a-alanine betaine and glycine betaine in some marine invertebrates.--Bull. Jap. Soc. scient. Fish. 41: 743-746. KONOSU, S., Y.N. CHEN, & Y. HASHIMOTO, 1966. Constituents of the extracts of a marine worm, Perinereis brevicirrus.--Bull. Jap. Soc. scient. Fish. 32: 881-886. KOUTSIKOPOULOS, C. & A. HERBLAND, 1987. The stability of the spatial distribution of the pelagic stages of sole as explained by the trajectories of 'Argos' satellite tracked buoys.--Mini Symposium on Recruitment processes in Marine Ecosystems, ICES C.M. 1987/Mini no. 4. KOUTSIKOPOULOS, C., I~ PETITGAS, S. ARBAULT, P. BOURRIAU, P. CAMUS, J. VILLEMAROUE & C. ROUXEL, 1988. Environmental features governing the spatial distribution of the early stages of sole (Solea vulgaris Quensel) in the Bay of Biscay.--ICES C.M. 1988/L: 18 (mimeo). KOUTSIKOPOULOS, C., Y. DESAUNAY, D. DOREL & J. MARCHAND, 1989. The role of coastal areas in the life history of sole (Solea solea L.) in the Bay of Biscay. In: J.D. ROS. Topics in Marine Biology.--Scient. Mar. 53: 567-575. KRUUK, H., 1963. Diurnal periodicity in the activity of the common sole, Solea vulgaris Quensel.--Neth. J. Sea Res. 2: 1-28. LAGARDI~RE, E, 1982. Environnement peri-estuarien et biologie des Soleidae dans le Golfe de Gascogne (Zone Sud) a travers I'etude du Ceteau, Dicologoglossa cuneata (Moreau, 1881). Thesis University of AixMarseille I1: 1-303. - - - - , 1989. Influence of feeding conditions and temperature on the growth rate and otolith-increment deposition of larval Dover sole (Solea solea (L.).--Rapp. R-v. Reun. Cons. perT. int. Explor. Mer 191: 390-399. LAGARD#RE, J.F~, 1987. Feeding ecology and daily food consumption of common sole, Solea vulgaris Quensel, juveniles on the French Atlantic coast.--J. Fish Biol. 30: 91-104. LE, K.L., 1983. Les phases initiales du cycle biologique (oeufs, larves et jeunes) de Solea vulgaris Quensel et

Solea senegalensis Kaup (Poissons, Pleuronectiformes, Soleidae); relations avec le bassin de Marennes-Oleron, ecosysteme estuarien a vocation aquicole. Thesis, University of Aix-Marseille II: 1-136. LE HIR, P., C. DUCHENE, A. MEREL, G. DE NADAILLAC, M. MERCERON & M. BRETON, 1986. Impact du regime du barrage d'Arzal sur la stratification a rembouchure de la Vilaine. Etude par modelisation numerique.-Rapport IFREMER DERO-86-36-EL: 1-35. MACQUART-MOULIN, C., C. CASTELBON, G. CHAMPALBERT, g. CHIKHI, L. LE DIREACH-BOuRSIER & R PATRITI, 1989. The role of barosensitivity in the control of migrations of larval and juvenile sole (Solea solea (L.): influence of pressure variations on swimming activity and orientation.--Rapp. P.-v. Reun. Cons. perT. int. Explor. Mer 191: 400-408. MACKIE, A.M., J.W. ADRON & P.m.GRANT, 1980. Chemical nature of feeding stimulants for the juvenile Dover sole, Solea solea (L.).--J. Fish. Biol. 16: 701-708. MARCHAND, J. & G. MASSON, 1987.--Strategie de migration en milieu estuarien des post-larves de sole (Solea solea) au cours de leur metamorphose: impact des conditions hydrologiques sur leur dispersion et leur comportement sur les zones de nourriceries.--Rapp. IFREMER/CNRS: 1-44. - - - - , 1989. Process of estuarine colonization by 0-group sole (Solea solea): hydrological conditions, behaviour, and feeding activity in the Vilaine estuary.--Rapp. R-v. Reun. Cons. p e r t int. Explor. Mer 191: 287-295. MILLER, J.M., J.P. REED & L.J. PIETRAFESA, 1984. Patterns, mechanisms and approaches to the study of migration of estuarine-dependent fish larvae and juveniles. In: J.D. MCCLEAVE, G.P ARNOLD, J.J. DODSON & W.H NEILLS. Mechanisms of migration in fishes. Plenum Press, New York and London: 209-225. MILLER, J.M., L.B. CROWDER & M.L. MOSER, 1985. Migration and utilization of estuarine nurseries by juvenile fishes: an evolutionary perspective.--Contr. Mar. Sci. 27 (suppl.): 338-352. NADAILLAC, G. DE & M. BRETON, 1986. Les courants en bale de Vilaine.--Rapp. IFREMER, DERO 86-02-EL, 1-34. RAMOS, J., 1986. Crecimiento larvario del lenguado (Solea solea L.) a diferentes temperaturas y fotoperiodos.-Bol. Inst. Esp. Oceanogr. 3: 5-10. ROGERS, S.l., 1989. The ecology of juvenile Dover sole Solea solea L.: a review of the literature.--Prog Underw. Sci. 14: 53-66. RYLAND, J.S., 1966. Observations on the development of larvae of the plaice, Pleuronectes platessa L., in aquaria.--J. Cons. perT. int. Explor. Mer 30: 177-195. SALOMON, J.C. & IR LAZURE, 1988. Etude par modele mathematique de quelques aspects de la circulation marine entre Quiberon et Noirmoutier.--Rapp. IFREMER DERO-88-26-EL: 1-104. TANAKA, M., J.B. TANANGONAN, M. TAGAWA & m. HIRANO, 1989. Ontogenetic changes in thyroid hormone concentrations related to morphological and ecological events during the early life history of fish (Abstract).-Rapp. R-v. Reun. Cons. perT. int. Explor. Mer 191: 490.