Rapp. P.-v. Réun. Cons. int. Explor. Mer, 191: 287-295. 1989

Process of estuarine colonization by 0-group sole (Solea solea): hydrological conditions, behaviour, and feeding activity in the Vilaine estuary

Jocelyne Marchand and Gérard Masson

Marchand, Jocelyne and Masson, Gérard. 1989. Process of estuarine colonization by 0-group sole (Solea solea): hydrological conditions, behaviour, and feeding activity in the Vilaine estuary. - Rapp. P.-v. Réun. Cons. int. Explor. Mer, 191: 287-295.

The influence of environmental factors on the estuarine settlement and the behaviour of sole late larvae was examined by sampling which was stratified either by transects or by depth, photoperiod, and tidal conditions at one station. The initiation of inshore migration is controlled by the thermohaline conditions in the bay which depend on river flow, tidal cycle, and wind regime. Their fluctuations in abundance seem to be linked less to predator-prey relationships than to water density variations which induce spatial segregation of the sole and potential predators like ctenophora and scyphomedusae. In the estuary, late larvae exhibit a vertical migratory behaviour in relation to photoperiod with excursions up into the water column during the night. This diurnal rhythm is endogenous and is not related to feeding activity which is itself linked to tidal conditions and to predation on epi- and endo-benthic fauna.

Jocelyne Marchand and Gérard Masson: Laboratoire de Biologie Marine, Université de Nantes, 2 rue de la Houssinière, 44072 Nantes Cedex 03, France.

Introduction Methods The common sole, Solea solea, is a predominant species, In the bay and estuary of the Vilaine where the fresh­ economically and biologically, in the fish communities water flow is controlled by a barrage, 0-group sole were of the French Atlantic coast. It is especially abundant regularly sampled at 13 stations from April to June in in estuarine systems which are ideal foraging habitats for the young individuals. For some pleuronectiform species like the plaice, Pleuronectes platessa, the trans­ port mechanisms of the metamorphosing larvae from ■ESTUARY the open sea towards nursery areas have been described, in particular along the North Sea coast (Creutzberg et ’ENVINS al., 1978; Rijnsdorp et al., 1985). For the sole, little information is available on this migratory phase during which they change their morphology and their behav­ iour while they leave coastal waters to colonize estuarine areas (Lagardère, 1982; Le, 1983). This study, which is included in the National Research I le ,'"v Programme into the Determinism of Recruitment Dumet

287 TIDAL RANGE nets have a filtering area of 2.87 m^, i.e. a ratio R of 2.54 times the mouth area (Smith et al., 1968). Flow rate and hence volume filtered was measured with a centrally mounted TSK flow meter. Filtration efficiency, estimated according to Smith et al. (1968), is about 95% except when the net is clogged due to swarms of ctenophores and medusae. At each time of sampling, the glass-eel tow nets were rigged on either side of the trawler and towed °-4 ' '—I I I ' ' ' ■ |~ I 'i— i— '— r simultaneously for 10 min, first at a depth of 1 m below 20 1 10 20 1 10 20 •APRIL MAY JUNE the surface and then at a depth of 3 m. Then the bottom trawl was shot twice and towed for 500 m (thus the Figure 2. Position of sampling sessions in relation to spring- total area fished on each occasion was 1000 m 2). Abiotic neap tide cycles (1: 28-29 April; 2: 1-2 May; 3: 6-7 May; 4: 14-15 May; 5: 27-28 May ; 6: 3-4 June; 7: 9-10 June; 8: 18- parameters were recorded every 3 h; temperature and 19 June). salinity at depth intervals of 1 m and current velocity at the three sampling levels (currents will be regarded as positive when they flow downstream and negative 1987 (Fig. 1) with a small beam trawl (1 m wide by 0.3 m upstream). high, 4.1 m in length) equipped with a tickler chain and In the samples, which were fixed in 5% formalin, fitted with a 5 mm mesh at its mouth and a 1.5 mm mesh pleuronectiform fishes were identified, counted, and at its codend. measured. Their abundance was converted into num­ To study sole behaviour, one station (no. 11) was bers per 1000 m2 for the bottom samples and per 1000 m3 chosen in the main channel of the estuary and was then for the water column ones. Gut contents were analysed sampled for two months in 1986 (from late April to late with an estimation of state of fullness (empty; half-full; June) in eight different tidal conditions from spring to full) and identification of prey items. Their potential neap tides (Fig. 2). Each sampling session was 27 hours’ predators were identified, counted, and the gut contents long and included nine sets of samples taken at 3 h of the ctenophora were examined. intervals. Samples were taken from two trawlers of shallow draught which, in addition to the small beam trawl already described, were equipped with two glass- Results eel tow nets rigged on a 6 m boom to capture the sole Hydrological conditions during inshore in the water column. Each glass-eel tow net is a conical migration of sole and its biological cylinder net with a 1.2 m long anterior truncated cone characteristics of 1.2 m diameter at the mouth and 0.35 m diameter at its codend; its mesh size is 1.8 mm. The cone leads into The date of the first observation of sole late larvae in a 0.4 m long cylinder of a mesh size of 1.5 mm. These the estuary differs according to the year: they appeared

1986 1987 WIND REGIME WIND REGIME SPEED ( m. S -1) Offshore Offshore 6

3 o

3

6 Onshore Onshore

HYDROLOGICAL CONDITIONS HYDROLOGICAL CONDITIONS m-.s 01-.3 RIVER FL0M

RIVER FLO*

TIDES Figure 3. Hydroclimatic 10 15 20 conditions of the study area in APRIL APRIL April 1986 and 1987.

288 ID (as in 1986), we suppose the young sole remain in the bay, at the mouth of the outer estuary where the depth 1986 is less than 5 m: indeed, in this area, concentrations of 3 - sole were observed in early April 1987 before their penetration into the estuary. 2 - The interannual comparison of the length frequency distribution of these initial immigrants (Fig. 5) shows a significant difference in their mean size, the fish entering 1987 the estuary in April being smaller in 1986

25 20 15 (10.56 ± 1.66 mm) than in 1987 (11.21 ± 2.58 mm) (t = BAY 2.35, p < 0.05). Km from Barrage

Figure 4. Spatial variation of the water stratification index (ID) Variations of late larvae abundance in the in the Vilaine ecosystem in early April 1986 and 1987. estuary

In spring 1986, comparison of the changes in water at the end of April in 1986 and in mid-April in 1987. density with the levels of abundance of late larvae at Analysis of the hydroclimatic data can help to explain station 11 (Fig. 6) shows that the first appearance of the these differences (Fig. 3). In 1986, during the first spring tides period, although WATER DENSITY the river flow rate was low, cold freshwater (corre­ sponding to exceptional snowfall) was pushed seaward 20 - by regular offshore winds (N-NE) blowing at a speed of 3 to 7.5m s-1. In such conditions, a hydrographic front with a high density stratification occurred at the mouth of the estuary (Fig. 4) and no young sole were observed upstream. During the second spring tides, in spite of a high freshwater discharge due to heavy rainfall between 14 and 22 April, water mass exchanges were induced by regular westerly winds blowing at high speeds (4 to 9 m s-1): the first settlement of the 0-group sole occurred at the end of April. (N.IOOO m3) METAMORPHOSING SOLE (N.IOOO m2) SURF. B0TT. In early April 1987 (Fig. 3), a low river flow associated ••• MIOW. with a constant southwesterly wind (4 m s" 1) resulted in mixing in the bay and estuarine water masses and no front was detected in the area (Fig. 4). The first sole influx was observed as early as 15 April. 80- -200 When unfavourable conditions occur in the estuary -100

APRIL

CIEN0PH0RES---- PREDATORS HEDUSA— (XI000) I------(N.IOOO m3)

100 - - 2000 30 -

50 - - 1000 20 _

10 -

10 _ - 100

8 10 12 14 16 mm APRIL MAY JUNE □ 1986 m 1987 Figure 6. Variations in the abundance of sole late larvae and Figure 5. Length-frequency distribution of young sole captured their potential predators in relation to water density fluc­ in the estuary in late April 1986 and mid-April 1987. tuations in April 1986 at station no. 11.

289 larvae coincides with an increase in density. The water migration of newly settled fish does not occur in a single density (ot) reached 18.8 (at 12°C, 25 ppt salinity) which wave but can last more than one month with repetitive is closer to average marine conditions (ot; 27.2 at 9.6°C, peaks, the new immigrants mixing with the oldest ones. 35.2ppt; Camus et a i, 1987). Larval abundance The temporal changes in the abundance of the post­ decreases when the river is again in spate as on 5 May larvae and potential predators such as ctenophores when, after a week of heavy rain, o, reduced to 15.1 (at (Pleurobrachia pileus) and scyphomedusae (Aurelia 12.3°C, 20.3 ppt). Later, in early June, the new decrease aurita) (Fig. 6) show that peaks in abundance of sole of late larvae density does not correspond to unfavour­ late larvae are followed by peaks in abundance of both able water conditions but to their transformation into predator taxa. These reciprocal oscillations may be juveniles which are not considered in this analysis. From interpreted as evidence of predatory regulation of sole mid-June, there is no further influx of late larvae to the early life stages by the gelatinous predators. Such regu­ estuary and all the sole are juveniles more than 20 mm lation has been described for the larval herring popu­ in length. These variations indicate that the early stages lation in Kiel Bight (Möller, 1984) and for plaice and of sole (metamorphosing sole) are susceptible to water flounder larvae in the Wadden Sea (van der Veer, quality and move into the estuarine ecosystem in accord­ 1985) where young fish up to 12 mm were found in the ance with the water mass displacement which is mainly digestive contents of Pleurobrachia pileus. In the Vilaine governed by the river flow. ecosystem, analysis of stomach contents of these pred­ An examination of the pattern of sole late larvae ators revealed no soles but rather copepods which are distribution in relation to water density from April to the main component of the estuarine plankton. Exam­ June in the estuarine area (Fig. 7) leads to the obser­ ination of the spatial distribution of these different taxa vation that these young stages are concentrated in water in Vilaine bay and estuary in April and May 1987 (Fig. masses in which density (ot) varies between 19 and 23 9) shows that they are located in distinct water masses, and few are present in cold/euhaline (ot > 25) or warm/ the young sole being upstream and the gelatinous pred­ meso-oligohaline (a, < 17) conditions. These conditions ators downstream. Such spatial segregation was are not the same as those for the oldest sole (juveniles observed by Frank and Leggett (1985) in coastal New­ of more than 20 mm long) which in May are mainly foundland between the abundance of gelatinous pred­ concentrated in water masses where density is between ators and ichthyoplankton. 16 and 23 (with a maximum of 17), while in June, the peak of their abundance is located near the Vertical migration of postlarvae and their barrage where water density is low (ot = 11 with 630 feeding activity soles 1000 m-2). This change corresponds to their pro­ gressive adaptation to estuarine conditions. Observations of the vertical distribution of the late The length-frequency distribution of sole (Fig. 8) larvae during two of the eight sampling sessions (for from late April to mid-June indicates that inshore the six others, sole was scarce) show that they exhibit a

N 40 q I ■ Larvae 3 5 - d Juveni1 es

30

25 -

2 0 -

15

10

5 -I

JL r ~i Figure 7. Springtime distribution 11 13 17 I 1 9 21 25 27 of young sole abundance in WATER DENSITY relation to water density.

290 1986 1987 N.IOOO m3 N.IOOO m3 28-29 APRIL N E D .' SOLE APRIL

20 - -5000 30-

20-

12 - -3000

10- -2000 /\

-1000

27-28 MAY 125-

100- 40 80000 MAY 75 -

30 - 50 - •-60000

2 5 -

20 -

9-10 JUNE 10 - 50 - ■-20000

3 0 -

2 0 - Km from Barrage

1 0 - Figure 9. Spatial distribution of young sole and their potential predators in April and May 1987. MED. = medusae, CTEN. = ctenophores.

18-19 JUNE 20 - direction. The number of larvae migrating increases as current speed reduces with few or no sole late larvae to 15 - be found in the water column when the currents are strong and oriented downstream. Such adaptation to 10 - the current conditions allow young soles to remain in the estuary. In the Wadden Sea, Rijnsdorp etal. (1985) indicated that plaice larvae are more “likely pelagic -n O P i r during flood than during ebb tides and that this tendency 8 14 20 26 34 40 48 is more pronounced at night than during the day”. For LENGTH (mm) sole, no vertical migration was observed during the day, Figure 8. Length-frequency distributions observed at station even when the current conditions were favourable. Such no. 11 in spring 1986. a pattern of cyclical vertical distribution has been described for the metamorphosing English sole (Paro- phrys vetulus) in Yaquina Bay (Oregon) by Boehlert pronounced behavioural response to photoperiod: they and Mundy (1987). remain on the bottom throughout the day and migrate The diurnal pattern of migration of early life stages vertically into the water column at night (Fig. 10). of sole in the Vilaine estuary does not depend on their The hydrographic conditions in the Vilaine estuary are feeding rhythm (Fig. 11) which follows the tidal rhythm. controlled by the barrage discharge and so tidal effects Although food is continuously observed in the digestive on the vertical migration of sole larvae are minimal. contents, they seem to feed according to a semi-diurnal Nightly excursion into the water column occurs at both pattern, mainly during day and night flood tides. Their ebb and flood tides but the magnitude of migration, in prey belong to the supra-benthic meiofauna with har- terms of abundance of larvae migrating towards the pacticoid copepods as the main component of their diet. surface, seems to be linked to the current velocity and Plankton are negligible as a food resource for late

291 larvae which consume them mainly at the beginning of an estuarine recruitment which is the result of active their inshore migration (10% of the food composition behaviour adapted to the environment. According to in April) (Fig. 12). Miller (1988), “the stages in the transition from passive to active migration depend upon increased agility, Discussion and would be expected to vary among species and the particular current regime". For fish larvae, the first stage For species which spawn offshore and which have an of the migration from the open sea to the nursery areas estuarine-dependent cycle, Boehlert and Mundy (1988) has often been explained as passive transport by drift; recognize two principal phases of movement necessary such a mechanism involves planktonic larval stages of for their recruitment to estuaries: nearshore accumu­ weak swimming ability (Cushing, 1975; Miller et al., lation of the larvae which is essentially passive, then 1984; Boehlert and Mundy, 1987).

28-29 APRIL. 1986 27-28 MAY, 1986 m3.s_1 • \RIVER FLOW \RIVER FLOW 200 - 160-

150 - 120 -

100 - 80 -

50 - 40 - V *

SURFACE SURFACE

MID-WATER WATER

BOTTOMBOTTOM

ET LT FT HT ET LT FT HT ET FT HT ET LT FT HT ET LT FT

Figure 10. Vertical distribution of sole late larvae during the 28-29 April and 27-28 May sampling sessions. For each series of diagrams, on the right axis: current velocity; on the left axis: sole density (ET = ebb tide; LT = low tide; FT = flood tide; HT = high tide. Black bars indicate periods of darkness).

292 For sole which spawn in the Bay of Biscay (about 100 km offshore), the migration of early life stages STOMACH CONTENTS cannot be ascribed to a typical passive drift. Kout- sikopoulos and Herbland (1987) demonstrated impor­ tant spatial stability of the pelagic stages in the spawning 30- area with no dispersion of the egg and larvae and suggested that transport to the nursery areas is effected during late larvae stages by active behaviour, since no 20- onshore-oriented residual circulation occurred on the spawning grounds. Recent data on water circulation in the bay of Vilaine (De Nadaillac and Breton, 1986) suggest that when they enter this region, the late larvae are in a hydro- logical environment favourable to their inshore LT FT HT ET LT FT HT ET LT migration. It was demonstrated that, in the bay, tidal currents have a weak impact on water mass exchanges INTESTINE CONTENTS and residual circulation is mainly dominated by the wind 80- with bottom currents oriented landward. For meta­ morphosing larvae, this pattern of water circulation with 60- an increase of the amount of oceanic water entering the bay under wind stress (essentially onshore winds), is certainly the main feature contributing to their inshore 40- transportation. In the Marennes-Oleron region where tidal action is predominant, the role played by bottom 20- currents on the young stage transport has already been indicated by Le (1983). For sole, it is possible that the metamorphosing larvae carry out passive but selective LT FT HT ET LT FT HT ET LT horizontal movements using bottom currents to reach the mouth of the estuary where they accumulate. Such Figure 11. Occurrence of young sole with half-full (white) and a pattern of migration has previously been described full (black) gut contents during a typical tidal cycle (shaded for other pleuronectiforms like plaice in North Sea areas areas represent periods of darkness; ET = ebb tide; LT = low tide; FT = flood tide; HT = high tide). (Rijnsdorp et al., 1985; Creutzberg et al., 1978). The second stage of migration, which is estuarine penetration and settlement, is clearly an active trans­ linked to the lunar cycle: new immigrants mixing with port. For sole in the Vilaine estuary, the first incursion previously settled ones. Such pulses of fish linked to the is controlled by hydroclimatic conditions, i.e. river flow spring-neap tide cycles were observed in Parophrys and wind regime. If, as in 1986, an offshore wind is vetulus recruitment by Boehlert and Mundy (1987). At associated with a high freshwater discharge, a hydro- each abundance peak, we observed that young sole graphic front occurs at the mouth of the estuary which entered the estuary at all depths, with no size difference presents an obstacle for early life stages whose diurnal between sole collected in the water column and on the pattern of vertical migrations prevents them from pass­ ing through. As size differences were observed between soles which were trapped at the mouth of the estuary until the end of April 1986 and those which entered the estuary in early April 1987, we suggested that such differences may be attributed to lack of access to pre­ % 100 ferred feeding areas when a front occurs. This hydro- 80 graphic structure which is an uncertain phenomenon 60 controlled by the climate, can be considered as one of 40 20 the “point source” stimuli suggested by Boehlert and 0 Mundy (1988) and may have an impact on the success or failure of the estuarine settlement of sole. Settlement of metamorphosing sole extends over about 1.5 months with high abundance of meta­ Figure 12. Temporal change of food components in the diet of morphosing individuals generally occurring on spring newly-settled sole. (CR = crustacean larvae, LA = lamel- tides and low densities on the next neap tides. These libranch larvae, OS = ostracods, CO = Corophium, AN = oscillations suggest that estuarine migration may be annelids, HA = harpacticoids.)

293 bottom. This vertical distribution, which disappears in observed are similar to those described by several June, when late-larvae influxes have ceased, cor­ authors who interpreted them as predator-prey inter­ responds to a typical circadian rhythm with night excur­ actions since A . aurita and P. pileus have both been sions in the water column associated with low current confirmed as larval flatfish predators (Greve, 1972; Bai­ velocities. Champalbert et al. (1987) showed that this ley, 1984; Bailey and Batty, 1984; Purcell, 1985; van der rhythmic activity is an endogenous phenomenon which Veer, 1985). So in the present study, abrupt population persists for several days when sole late larvae are reared decrease of sole may be partly caused by these pred­ in complete darkness, light acting as a Zeitgeber. Diel ators. rhythms are known in other euryhaline species such as However, we think these predator-prey relationships plaice, flounder, or English sole with nocturnal vertical are not the main factor responsible for these oscillations. migration on flood tides (Arnold and Cook, 1984; We did not observe spatial overlap of sole and their Weinstein et al.. 1980; Creutzbergefa/., 1978; Rijnsdorp predators which were spatially segregated. Young sole etal.. 1985; Boehlert and Mundy, 1987). Although sole concentrations were located more upstream than those late larvae may be partly flushed downstream on night of A. aurita and P. pileus. The occupation of two distinct ebb tides as Rijnsdorp et al. (1985) described for the water masses by predators and their prey, which has plaice, on balance, these migrations are positive and in been observed and discussed by Frank and Leggett favour of their retention in the estuary since their period (1985), may be one possible interpretation of our data. on the bottom is longer than their occurrence in the Another argument in favour of the second hypothesis water column. concerns the size and behaviour of the metamorphosing In late larval cohorts which settled in the estuary, we larvae. Several authors demonstrated that for cruising observed a superimposition of two different rhythms: a raptorial predators like medusae, increased larval size circadian activity which favours their upstream and swimming activity results in declining vulnerability migration and their estuarine retention, and a circa- to capture, with improved detection of predators and tidal one for their feeding activity. This phenomenon better escape ability (Bailey and Houde, 1987). P. corresponds to the occurrence of the “appetitive behav­ pileus, an ambush raptorial predator drifting passively, iour” which is observed in metamorphosing larvae of feeds mainly on copepods (Fraser, 1970; Möller, 1980b). pleuronectiforms when they enter nearshore and estu­ For flatfish larvae, Bailey (1984) demonstrated that the arine areas (Boehlert and Mundy, 1988). According to escape speed of flounder increases from 26.7 mm s~1 at these authors (1987), “a suite of stimuli associated with the yolk sac stage (4 mm) to 89.7 mm s ' 1 at 7 mm feed­ tidal flux acts as a Zeitgeber to superimpose a circa-tidal ing stage. Bailey and Batty (1984) showed that capture rhythm upon the circadian rhythm which already may success by predators declines with increasing larval size, be present”. In juvenile pleuronectiform species, tidal especially for flounder and plaice larvae. We think that and circa-tidal migration patterns linked to the avail­ this phenomenon is more marked in metamorphosing ability of the intertidal feeding grounds have been stages. Furthermore A . aurita and P. pileus are plank­ described either under controlled conditions in labora­ tonic organisms and we observed that metamorphosing tory, or in their natural environments and are charac­ sole larvae spend most of the time on the bottom. teristic of their adaptation to estuarine areas (Kuipers, In the Wadden Sea, van der Veer and Bergman (1987) 1973; Le, 1983; Gibson, 1984; van der Veer and Berg­ demonstrated that a suprabenthic predator like Crangon man, 1986). In subtidal areas, Kruuk (1963), de Groot crangon causes significant mortality of 0-group plaice (1971) and Lagardère (1987) showed sole juveniles to (<30 mm). For sole, a similar pattern of predation have a daily activity rhythm with nocturnal food intake; might be expected in our study area as the brown shrimp these rhythmic activities demonstrate that the sole has population occurs in high densities. a great ability to adjust its behaviour to the charac­ So for sole, during the transition from larval to juv­ teristics of the environment. enile stage, we suggest that their increasing swimming In the Vilaine region, abrupt decreases of meta­ speed, and their vertical and horizontal distribution morphosing sole abundance from late April to early patterns in the estuarine area do not favour encounters June, correspond to outbursts of predatory cnidaria. with potential planktonic predators, but do enhance Swarms of Aurelia aurita and Pleurobrachia pileus have their vulnerability to suprabenthic predators. These often been described in nearshore and estuarine areas conditions are certainly different to those on spawning- (Fraser, 1970; Möller, 1980a; van der Veer and Sadee, grounds and should be considered in relation to larval 1984; van der Veer and Oorthuysen, 1985; Papa- mortality and to recruitment. thanassiou etal., 1987). In Scottish waters, Fraser (1970) indicated the regular appearances of P. pileus were correlated to scarcity or exclusion of other planktonic References components. This gelatinous ctenophore dominated the Arnold, G. P., and Cook, P. H. 1984. Fish migration by water over large areas. In our study, we also observed selective tidal stream transport: first results with a computer this phenomenon. The reciprocal oscillations we simulation model for the European continental shelf. In

294 Mechanisms of migration in fishes, pp. 227-261. Ed. by J. Lagardère, F. 1982. Environment péri-estuarien et biologie D. McCleave, G. P. Arnold, J. J. Dodson and W. H. Neills. des Soleidae dans le Golfe de Gascogne (Zone sud) à travers Plenum Press, New York. l’étude du céteau, Dicologoglossa cuneata (Moreau, 1881). Bailey, K. M. 1984. Comparison of laboratory rates of pre­ Thesis University of Aix-Marseille II, 303 pp. dation on five species of marine fish larvae by three plank­ Lagardère, J. P. 1987. Feeding ecology and daily food con­ tonic invertebrates: effects of larval size on vulnerability. sumption of common sole, Solea vulgaris Quensel, juveniles Mar. Biol., 79: 303-309. on the French Atlantic coast. J. Fish Biol., 30: 91-104. Bailey, K. M., and Batty, R. S. 1984. Laboratory study of Le, K. L. 1983. Les phases initiales du cycle biologique (oeufs, predation by Aurelia aurita on larvae of cod, flounder, plaice larves et jeunes) de Solea vulgaris Quensel et Solea sene- and herring: development and vulnerability to capture. Mar. galensis Kaup (Poissons, Pleuronectiformes, Soleidae); Biol., 83: 287-291. relations avec le bassin de Marennes-Oleron, écosystème Bailey, K. M., and Houde, E. D. 1987. Predators and pre­ estuarien à vocation aquicole. Thesis, University of Aix- dation as a regulatory force during the early life of fishes. In Marseille II, 136 pp. Symposium on Recruitment Processes in Marine Eco­ Miller, J. M. 1988. Physical processes and the mechanisms of systems, ICES CM 1987/Mini 2: 30 pp. coastal migrations of immature marine fishes. Am. Fish. Boehlert, G. W., and Mundy, B. C. 1987. Recruitment Soc. Symp., 3: 68-76. dynamics of metamorphosing English sole, Parophrys vet- Miller, J. M., Reed, J. P., and Pietrafesa, L. J. 1984. Patterns, ulus, to Yaquina Bay, Oregon. Estuar. Coast. Shelf Sei., 25: mechanisms and approaches to the study of migration of 261-281. estuarine-dependent fish larvae and juveniles. In Mech­ Boehlert, G. W., and Mundy, B. C. 1988. Roles of behavioral anisms of migration in fishes, pp. 209-225. Ed. by J. D. and physical factors in larval and juvenile fish recruitment McCleave, G. P. Arnold, J. J. Dodson and W. H. Neills, to estuarine nursery areas. Am. Fish. Soc. Symp., 3: 51-67. Plenum Press, New York and London. Camus, P., Arbault, S., de la Villemarque, J., Koutsikopoulos, Möller,H. 1980a. Population dynamics of Aurelia aurita Medu­ C., Morin, P., and Bourriau, P. 1987. Déterminisme du sae in Kiel Bight, Germany (FRG). Mar. Biol., 60: 123— recrutement de la sole dans le Golfe de Gascogne: Phase 128. pélagique. Campagnes SOLDET IV-V-VI. 1986. Rapport Möller, H. 1980b. Scyphomedusae as predators and food com­ IFREMER, Campagnes océanographiques françaises, 6:131 petitors of larval fish. Ber. dt. wiss. Kommn Meeresforsch., pp. 28: 90-100. Champalbert, G., Castelbon, C., Le Direach-Bourcier, L., Möller. H. 1984. Reduction of a larval herring population by and Bourdillon, A. 1987. Rythmes d’activité locomotrice jellyfish predator. Science, 224: 621-622. chez les juvéniles de soles (Solea vulgaris). C.R. Symposium Papathanassiou, E., Panayotidis, P., and Anagnostaki, K. PNDR, Nantes. 1987. Notes on the biology and ecology of the jellyfish Creutzberg, F., Eltink, A. T. G. W., and van Noort, G. J. Aurelia aurita Lam. in Elefsis Bay (Saronikos Gulf, Greece). 1978. The migration of plaice larvae Pleuronectes platessa Mar. Ecol., 8 (1): 49-58. into the western Wadden Sea. In Physiology and behaviour Purcell, J. E. 1985. Predation on fish eggs and larvae by pelagic of marine organisms, pp. 243-251. Ed. by D. S. McLusky Cnidarians and Ctenophores. Bull. Mar. Sei., 37 (2): 739- and A. J. Berry, Pergamon Press, Oxford and New York. 755. Cushing, D. H. 1975. Marine ecology and fisheries. Cambridge Rijnsdorp, A. D., van Strålen, M., and van der Veer, H. W. University Press, Cambridge, 278 pp. 1985. Selective tidal transport of North Sea plaice larvae De Nadaillac, G., and Breton, M. 1986. Les courants en baie Pleuronectes platessa in coastal nursery areas. Trans. Am. de Vilaine. Rapport IFREMER, DERO 86-02-EL, 34 pp. Fish. Soc., 114: 461-470. Frank, K. T., and Leggett, W. C. 1985. Reciprocal oscillations Smith, P. E., Counts, R. C., and Clutter, R. I. 1968. Changes in densities of larval fish and potential predators: a reflection in filtering efficiency of plankton nets due to clogging under of present or past predation? Can. J. Fish. Aquat. Sei., 42: tow. J. Cons. int. Éxplor. Mer, 32 (2): 232-248. 1841-1849. Veer, H. W. van der. 1985. Impact of coelenterate predation on Fraser, J. H. 1970. The ecology of the ctenophore Pleuro­ larval plaice Pleuronectes platessa and flounder Platichthys brachia pileus in Scottish waters. J. Cons. int. Explor. Mer, flesus stock in the western Wadden Sea. Mar. Ecol. Prog. 33: 149-168. Ser., 25: 229-238. Gibson, R. N. 1984. Hydrostatic pressure and the rhythmic Veer, H. W. van der, and Bergman, M. J. N. 1986. Devel­ behaviour of intertidal marine fishes. Trans. Am. Fish. Soc., opment of tidally related behaviour of a newly settled 0- 113: 479-483. group plaice (Pleuronectes platessa) population in the west­ Greve, W. 1972. Ökologische Untersuchungen an Pleuro­ ern Wadden Sea. Mar. Ecol. Prog. Ser., 31: 121-129. brachia pileus 2. Laboratoriumuntersuchungen. Helgol. Veer, H. W. van der, and Bergman, M. J. N. 1987. Predation Meeresunters. 23: 141-164. by crustaceans on a newly settled 0-group plaice Pleuronectes Groot, S. J. de 1971. On the interrelationships between mor­ platessa population in the western Wadden Sea. Mar. Ecol. phology of the alimentary tract, food and feeding behaviour Prog. Ser., 35: 203-215. in flatfishes (Pisces: Pleuronectiformes). Neth. J. Sea Res., Veer, H. W. van der, and Oorthuysen, W. 1985. Abundance, 5: 121-196. growth and food demand of the Scyphomedusa Aurelia Koutsikopoulos, C., and Herbland, A. 1987. The stability of aurita in the western Wadden Sea. Neth. J. Sea Res., 19 (1): the spatial distribution of the pelagic stages of sole as 38-44. explained by the trajectories of “Argos” satellite tracked Veer, H. W. van der, and Sadee, C. F. M. 1984. The seasonal buoys. In Symposium on Recruitment Processes in Marine occurrence of the Ctenophore Pleurobrachia pileus in the Ecosystems. ICES CM 1987/Mini 4: 6 pp. western Dutch Wadden Sea. Mar. Biol., 79: 219-227. Kruuk, H. 1963. Diurnal periodicity in the activity of the Weinstein, M. P., Weiss, S. L., Hodson, R. G., and Gerry, common sole, Solea vulgaris Quensel. Neth. J. Sea Res., 2: L. R. 1980. Retention of three taxa of postlarval fishes in an 1-28. intensively flushed tidal estuary, Cape Fear River, North Kuipers, B. 1973. On the tidal migration of young plaice Carolina. Fish. Bull., 78 (2): 419-436. (Pleuronectes platessa) in the Wadden Sea. Neth. J. Sea Res., 6: 376-388.

295