Spatial and temporal distribution of European hake, Merluccius merluccius (L.), eggs and larvae in relation to hydrographical conditions in the Bay of Biscay

Fisheries Research 50 (2001) 111±128

Spatial and temporal distribution of European hake, Merluccius merluccius (L.), eggs and larvae in relation to hydrographical conditions in the Bay of Biscay Paula Alvarez*, Lorenzo Motos, Adolfo Uriarte, Joseba EganÄa AZTI, Technological Institute for Fisheries and Food, Av. SatruÂstegui 8, 20008 Donostia-San SebastiaÂn, Basque Country, Spain

Abstract The distribution patterns for hake eggs and larvae were determined by analysing samples collected on 12 cruises in the Bay of Biscay from February to June both in 1983 and 1995. The majority of the eggs and larvae were found in late winter and early spring. The expected northern displacement of both hake eggs and larvae as the season progresses was observed only in the case of larvae. A particular spatial pattern of larval distribution was found. Small larvae (2±4 mm) were found close to the spawning grounds at the shelf break. Mid-size larvae (4±8 mm) showed a more widespread distribution from the continental shelf and to areas well beyond the shelf break. Finally, the biggest larvae sampled (>8 mm) were recorded only on the continental shelf. This pattern seems to be a consequence of the combined action of different mechanisms. Wind-induced transport in the Ekman layer favoured an onshore transfer in 1983, whereas prevalent wind and geostrophic circulation favoured a northern, onshore transfer in 1995. # 2001 Elsevier Science B.V. All rights reserved. Keywords: Hake eggs; Hake larvae; Distribution; Hydrography; Advection

1. Introduction The European hake, Merluccius merluccius (L.), is the main commercial demersal species in the Bay of Biscay, being exploited by several Spanish and French ¯eets, with an annual average catch of 61 500 t in the period 1978±1990. These catches are worth an average of 319 million ECU at ®rst sale (Casey and Pereiro, 1995). Despite its economic importance, studies on the early life history of hake are few. The spawning area of the European hake population in Atlantic waters extends all along the western margin of Europe from Portugal to north Scotland. Spawning *

Corresponding author. Tel.: ‡34-43214124; fax: ‡34-43212162. E-mail address: [email protected] (P. Alvarez).

has also been recorded in Norwegian Fjords and in the Skagerrak and Kattegat. The peak spawning time of hake is earlier in southern waters, being later as the latitude increases (Casey and Pereiro, 1995). In this way, peak spawning is closer to winter months (February±March) in the Portuguese coast. It ranges from January to May in Galician waters (PeÂrez and Pereiro, 1985), Cantabrian sea (Alcazar et al., 1983) and Bay of Biscay (Sarano, 1983; Martin, 1991). In the Celtic Sea (ICES subarea VII) peak spawning takes place from April to June (Clark, 1920; Coombs and Mitchell, 1982; Horstman, 1988; Fives et al. this issue). In western Ireland, spawning occurs from April to July and from May to August for sea areas west of Scotland (Hickling, 1930; O'Brien, 1986). Ripening hake has been also recorded in the West Coast of Norway in August (Kvenseth et al., 1996).

0165-7836/01/$ ± see front matter # 2001 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 5 - 7 8 3 6 ( 0 0 ) 0 0 2 4 5 - 9

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ICES (1980) presented the results of the 1977 triennial survey for hake larvae. Larvae were mainly distributed along the shelf edge from south Biscay to south Ireland, and displaced to the north as the season progresses. This latitudinal variation in peak spawning time is common to other ®sh species. In the case of hake, it can be explained by a migration of spawners from south to north, or alternatively, by a spawning wave going from south to north as local population components reach maturity and spawn, or it can be a combination of both. The phenomenon seems to be related to changes in environmental factors such as temperature and the consequent changes in biological features of the spawning habitat. Hake eggs show a temperature preference in the range of 10.5±128C (Arbault and Lacroix-Boutin, 1969; Coombs and Mitchell, 1982). The ®nal spatio-temporal distribution pattern of eggs and larvae will depend on the initial position of the spawning, and after the release of eggs by the parental stock, on the hydrographical features acting upon this initial distribution. Authors have expressed a variety of interpretations to explain the cross-shelf distribution of eggs and larvae. Arbault and LacroixBoutin (1969) concluded that the spawning in the Bay of Biscay is initiated close to the coast and it spreads towards deeper waters as the season progress. In more northern latitudes, Horstman (1988) and Fives et al. (this issue) suggested the contrary, i.e. spawning starts along the shelf edge (200 m depth contour) and spreads onto the shelf afterwards. The in¯uence of the hydrographical features on the dispersion of eggs and larvae is of increasing interest. Several species spawn, as hake does, in areas far away from the coast but, at the same time, have coastal nursery areas where the young individuals are recruited. The European hake occupy different nursery areas, all of them located in coastal, relatively shallow waters such as the muddy bottoms of the northern Bay of Biscay known as the ``Grand VasieÂreÁ'' (Bez et al., 1995). Consistent mechanisms of retention over the shelf, and furthermore, transport towards the coast should occur in the area to ensure the maintenance of the population in the long term (Heath, 1992; Koutsikopoulos et al., 1991; Koutsikopoulos and Lacroix, 1992). Oceanographic events that contribute to the dispersion of ELH stages towards open ocean waters can cause high larval mortality and

substantially decrease successful recruitment (Laevastu and Hayes, 1981; Hollowed and Bailey, 1989). Several studies have described the main hydrographical features in the Bay of Biscay. The general circulation is weak and the presence of cyclonic and anticyclonic eddies is frequent (Koutsikopoulos and Le Cann, 1996). A consistent poleward seeking slope current is apparent but it shows marked seasonal changes (Pingree and Le Cann, 1990). The residual currents over the shelf are principally governed by the wind, the tide in the northern part and the water density. The meteorological conditions show marked spatial and temporal heterogeneity which can have a notable in¯uence in ®sh populations (Koutsikopoulos and Le Cann, 1996; Borja et al., 1996; SaÂnchez, 1994). This paper describes the spatio-temporal pattern of distribution of hake eggs and larvae in the Bay of Biscay during the main spawning period for the years 1983 and 1995. Based on the distribution pattern found, a mechanism to ensure the retention or transportation of eggs and larvae towards the putative nursery areas where juveniles are recruited is suggested. The spatio-temporal distribution pattern is analysed in the light of the available data on concurrent oceanographic features. The in¯uence of the environmental conditions where hake eggs and larvae develop is assessed by comparing the events described in the study to the eventual hake recruitment levels achieved in the year of study (ICES, 1996). 2. Material and methods Table 1 summarises the cruises analysed in this study. Hake eggs and larvae were sorted from the samples collected in a series of cruises carried out within the frame of the ICES triennial egg survey, both in 1983 and in 1995. Additionally, two cruises were carried out to speci®cally collect hake eggs and larvae in February and March 1995. For comparison purposes, the cruises were grouped by month. Results were available for 3 months in 1983, i.e. March, May and June, and for 5 months in 1995, i.e. February, March, April, May and June. During the surveys, a set of single oblique plankton tows were made using a BONGO net, 60 cm mouth diameter (Mcgowan and Brown, 1966) in a grid of stations arranged in transects perpendicular to the

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Table 1 Summary of the main characteristics of the surveys carried out Cruise

Survey dates

Bay of Biscay

Period

Gear

Year 1983 Cirolana 4 Scotia 5 Tridens 5 Scotia 6 Tridens 6

18 March±9 April 4±18 May 4±31 May 8±28 June 31 May±7 June

18 March±9 April 8±12 May 4±31 May 18±22 June 31 May±7 June

March May May June June

GULF GULF GULF GULF GULF

Year 1995 Lebal 2 Lebal 3 Walter Herwig III 4 Cirolana 4a Scotia 5 Tridens 5 Tridens 6

15±24 February 22 March±1 April 26 March±12 April 22 April±17 May 23 April±12 May 18±31 May 13±26 June

15±24 February 22 March±1 April 2±9 April 15±17 May 1±7 May 22±31 May 13±21 June

February March April May May May June

BONGO-60 BONGO-60 GULF III GULF III GULF III GULF III GULF III

shelf edge contour. The sampling methodology used in the cruises followed standard procedures. Temperature and depth pro®les were recorded at each haul by means of a MINILOG probe. Ancillary hydrographical data, namely temperature, salinity and chlorophyll ``a'' were recorded during the cruises using a SEABIRD 25 CTD. The standard plankton net used in the ICES triennial egg surveys is the GULF III. The procedures used in these surveys are described in detail elsewhere (ICES, 1994). Double oblique tows were carried out in a grid of stations located at the mid-point of 0:5  0:5 rectangles along the whole mackerel and horse mackerel spawning area. Only samples collected south of 488, i.e. within the Bay of Biscay, were processed in this work. Ancillary hydrographical data were also collected during the ICES cruises. On completion of the hauls, plankton was preserved in a 4% buffered formaldehyde solution. Hake eggs and larvae were sorted from the samples collected in the speci®c hake cruises. ICES samples were re-sorted for hake eggs and larvae at AZTI, after separating the eggs and larvae of the cruise-speci®c target species, i.e. mackerel and horse mackerel, in the laboratory of origin. All hake eggs sorted were classi®ed by developmental stage and hake larvae were measured to the nearest lower 0.1 mm. In this study no correction was made to allow for shrinkage of larvae due to ®xation procedures. Bailey (1982) gave a shrinkage ®gure of

Samples III III III III III

53 35 70 35 45 40 62 40 17 28 58 60

9±22% for small Paci®c hake larvae (<4 mm) ®xed 5± 10 min after collection, and he assumed smaller shrinkage rates for bigger larvae. Egg and larval abundance in both BONGO and GULF III sampler hauls were converted to numbers per 10 m2 following standard procedures (Smith and Richardson, 1977; ICES, 1994). The distribution of hake eggs and larvae were mapped to show the spatio-temporal pattern of distribution. Furthermore, this pattern was summarised by mapping the centroids of distribution and their variance (Hollowed, 1992). The centroids were estimated as the mean position (latitude and longitude) of the positive stations for hake eggs or larvae weighted by the abundance of eggs or larvae found at each station. An ellipse shows the centre and the orientation of the animal's distribution in space and the amount of dispersion about the centre (Kendall and Picquelle, 1989). The secondary axis is at right angles to the principal (Sokal and Rholf, 1980; Kendall and Picquelle, 1989; Hollowed, 1992). The ellipse is the twodimensional analogue of mean and standard error bars (Kendall and Picquelle, 1989). The major and minor axes are each two standard deviations long. The centroids of the station grid covered in each survey were also calculated to compare them with the respective centroids of hake egg and larval distribution and to test if the gravity centre of the sampling area could confound the comparison.

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Wind data for the area and period of study was supplied by NOAA as obtained from FNMOC (Fleet Numerical Oceanographic Center). Geostrophic wind data is derived from surface pressure ®elds measured every 6 h. To approximate geostrophic wind to real wind data, the magnitude has to be reduced by 30% and the wind vector has to be turned 158 anticlockwise (Bakun, 1973). The data used in 1983 were obtained at position 458N, 58W. We assumed that the wind does not change substantially between two points, if the distance between them is less than 38 of latitude or longitude. This is a good approximation to reality (Bakun, 1973). The data used in 1995 were obtained at 458N, 28W since wind data at 458N, 58W were not available. Both positions were approximately centred in the survey area. Drift vectors were calculated by using Ekman's theory (Pond and Pickard, 1983) to depict windinduced drift on hake eggs and larvae. Results were produced for the reproductive periods of 1983 and 1995 at 15 and 100 m water depth. All the six hourly drift vectors were added to produced one monthly vector. This vector indicates the potential displacement of eggs and larvae during that period assuming that the displacement of hake eggs and larvae only depends on this factor. The wind-induced current velocity decreases exponentially with water depth as shown by Ekman's theory:    t p p   ea…ÿz† cos az ‡ (1) uˆ 4 Aa 2    t p p ea…ÿz† sin az ‡ (2) vˆ 4 Aa 2 r rf (3) aˆ 2A where z is the water depth, t the wind stress, A the eddy viscosity, r the water density, f the Coriolis parameter. The variation of tide-induced current velocity with water depth has been described by Postma (1988):  z 0:2 (4) V z ˆ v0 h where v0 is the surface current velocity, h the water depth, z the depth at which velocity is calculated.

3. Results 3.1. Distribution of eggs The distribution of hake eggs by month/year is shown in Fig. 1, together with the distribution centroids. In February 1995, a low abundance of hake eggs was noted but widely distributed throughout the study area. A relative abundance maximum (500 eggs/10 m2) occurred close to the shelf edge at around 478450 N latitude. Eggs were also found in the southeastern corner of the Bay of Biscay, although in very low abundance. In March, eggs were more abundant and widespread than in February. Peak abundance (700 eggs/10 m2) was located close to the shelf break between 458450 N and 478450 N. No eggs were found south of 448N in that month. Egg abundance continued to be relatively high in April. Eggs occurred very close to the shelf edge in most of the sampling area covered (45±488N) and were absent in inner shelf stations (Fig. 1). Abundance peaks were located close to the shelf break from 468 to 478450 N (282 eggs/ 10 m2). Egg abundance was lower later, both in May and June. They occurred over the outer continental shelf of northern Biscay. Hake eggs in the shelf break area are almost absent in those months, although an unusual presence was identi®ed in oceanic waters off the shelf at 478450 N latitude. The cruises covered only 3 months in 1983, March, May and June. In general, the seasonal pattern of egg distribution found that year was similar to that in 1995. Abundance peaks were located in March. Peak abundance in this month (1000 eggs/10 m2) were located around and close to the shelf break, but eggs were widespread from near the shelf edge to the inner shelf stations. They were also found in southern waters of the Bay of Biscay (Cantabrian Sea) although in very low abundance. Hake eggs appeared in lower quantities both in May and in June 1983. The peak abundance was 10 times lower in May (158 eggs/10 m2) than it was in March and was located over the external part of the continental shelf at a latitude of 478250 N. Low abundance egg patches were also observed at latitudes of 448250 N and at 468750 N in June 1983. The distribution centroids of hake eggs summarise the displacements along the season (Table 2 and Fig. 2). In 1983, the egg distribution centroids occur at 46.728N, 4.128W in March and at 47.048N, 5.868W

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Fig. 1. Proportional representation of egg densities of hake, M. merluccius, in the Bay of Biscay in 1983 and in 1995. Dot size indicates the abundance (numbers/10 m2) of eggs relative to the maximum observed in that year (1156 eggs/10 m2 in 1983 and 700 eggs/10 m2 in 1995). Crosses indicate station where hake eggs were not observed. Distribution ellipses are also plotted.

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Table 2 Summary of the position of the centroids calculated for both egg and larvae distribution Period

1983

1995

Survey

Eggs

Larvae

Survey

Eggs

Larvae

Latitude Longitude Latitude Longitude Latitude Longitude Latitude Longitude Latitude Longitude Latitude Longitude February ± March 46.05 April ± May 46.48 June 46.14

± ÿ4.29 ± ÿ5.21 ÿ4.58

± 46.72 ± 47.04 45.45

± ÿ4.12 ± ÿ5.86 ÿ2.99

± 47.09 ± 47.45 45.86

± ÿ4.24 ± ÿ4.51 ÿ3.06

in May, ending with a location more southerly and onshore in June (45.458N, 2.998W). In 1995, the egg centroid is located at 46.138N, 3.658W in February and it remains in a similar position in March (46.018N, 3.798W). The centroid goes up and outwards in April (46.628N, 4.998W), and May (46.618N, 5.058W), and ®nally it continues northwards in June (47.228N, 4.238W), but with a remarkably onshore movement. Most observations of hake eggs in May 1995 were placed well inside the continental shelf. However, the corresponding distribution ellipse was clearly in¯uenced by an offshore presence (Fig. 1). Comparing the displacement of the distribution centroids of the stations sampled in each survey, the displacements observed in the egg centroids show something different. The northern displacement shows in most cases a similar magnitude for both egg distribution and station distribution centroids. A southern movement was observed only in June 1983. Regarding the onshore/offshore movements, however, the evolution in 1983 was to go out from March to May and to go back to the continental shelf in June. In 1995, the centroids stayed similarly placed in longitude from February to April but showed a clear onshore displacement in May and June (Fig. 2). So, no net movement to the north can be unequivocally inferred from the data gathered in this study, but it shows a clear coastward movement in May (only in 1995) and June (both years). The orientation of the principal axis of the egg distribution ellipses is in a direction similar to that of the shelf break in the area, i.e. NW±SE, along the whole sampling period. The sizes of the ellipses increased somewhat from February to May in both directions (N±S and W±E).

45.50 45.70 46.67 46.55 46.76

ÿ3.21 ÿ3.51 ÿ4.88 ÿ5.40 ÿ6.94

46.13 46.01 46.62 46.61 47.22

ÿ3.65 ÿ3.79 ÿ4.99 ÿ5.05 ÿ4.23

45.40 46.66 47.23 47.42 ±

ÿ3.16 ÿ4.42 ÿ5.5 ÿ5.25 ±

3.2. Distribution of larvae Hake larvae occurred in low abundance in February 1995 (Fig. 3). An hot spot (30 individuals/10 m2) was found in the southern corner of the sampling area that month. Hake larvae were much more abundant in March 1995 and occurred more northerly. Abundance peaks (50 individuals/10 m2) occurred over the shelf break between 468450 N and 478450 N. Hake larvae also occurred in the south-eastern corner of the Bay of Biscay during this period but in a smaller numbers (four individuals/10 m2) than in February 1995. A similar distribution pattern was found in the April 1995 cruise, although hake larvae occurred in lower abundance than in March 1995. In May 1995, hake larvae were restricted to the area north of 468300 N. Hake larval abundance decreased in May 1995 with relation to March±April 1995, although an abundance peak (70 larvae/10 m2) appeared in shelf waters and a patch of lower abundance occurred close to the shelf break. Larvae were absent in June. The highest larval abundance in 1983 were found in March (Fig. 3), when a peak of abundance was located in shelf waters off Brest (52 larvae/10 m2) in the northern corner of the Bay of Biscay. No larvae appeared south of 468N in that cruise. The distribution pattern was roughly similar in May 1983, when a relative abundance peak (44 larvae/10 m2) was situated off Brest. Hake larvae were still present in June 1983, although in very low abundance and centred more southerly. The centroids of hake larval distribution showed perceptible monthly changes (Figs. 3 and 4, Table 2). Again, the movements of the cruise station distribution masked the apparent movements of the larval

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Fig. 2. Centroids and associated ellipses of hake eggs, M. merluccius, in the Bay of Biscay in (a) 1983 and (b) 1995. Centroids of distribution (months within blank square) are placed in the mid-point of the associated ellipse. The centroids of the sampling stations covered each cruise (months within black squares) are also represented for comparative purposes.

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Fig. 3. Proportional representation of larvae densities of hake, M. merluccius, in the Bay of Biscay in 1983 and in 1995. Dot size indicates the abundance (numbers/10 m2) of larvae to maximum observed both years (70 eggs/10 m2).

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Fig. 4. Centroids and associated ellipses of hake larvae, M. merluccius, in the Bay of Biscay in (a) 1983 and (b) 1995. Centroids of distribution (months within blank square) are placed in the mid-point of the associated ellipse. The centroids of the sampling stations covered each cruise (months within black squares) are also represented for comparative purposes.

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Fig. 5. Distribution of mean length of hake larvae, M. merluccius, in the Bay of Biscay in 1995 and 1983. Bar size indicates the mean length (mm) of larvae relative to the maximum observed in that year (11.4 mm in 1983 and 9 mm in 1995). Crosses indicate station where hake larvae were not observed.

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distribution centroids. However, a close comparison between both distributions permits a distinction between the northern movement recorded between February and March 1995, which was still noticeable from April to May (Fig. 4b) and the onshore movement which was noticeable from May to June 1983 (Fig. 4a) and from April to May 1995 (Fig. 4b). During the ®rst survey period (February) of 1995, the centroid of larval distribution was in front of the Gironde Estuary, the most southerly location of the centroids of either eggs or larvae found in this study. Afterwards, they moved from 458400 N in February 1995 to 478420 N in May 1995, with a main contribution from February to March (160 km in the northern direction). At the same time, the larval distribution centroid moved onshore from April to May, after having remained in a similar position with relation to the shelf break from February to April. Concerning the relative position of larval distribution centroid in relation to the egg distribution centroid, the former are generally located more to the north and to the east (coastward) than the latter (Figs. 1±4). This feature is clearer in 1983 than in

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1995. The only remarkable exception to this rule is the situation observed in February 1995, when the larval distribution was much more southerly than in any of the eggs and larval distribution observed in the remainder of the cruises. The distribution of larval mean length per station is shown in Fig. 5. There was no apparent pattern in the spatial distribution of this parameter in February. However, during the remainder of the cruises there was a consistent pattern, with the largest larvae generally occurring closer to the coast than the smaller. When all the observations are pooled, the spatial distribution of larvae by size shows a particular pattern (Fig. 6). Small larvae (2±4 mm total length, 40% of the larvae observed) occurred close to the spawning grounds over the shelf break. Mid-sized larvae (4± 8 mm, 54% of the larvae observed) show a more widespread distribution over the continental shelf, shelf break and even beyond it. Finally, the biggest larvae (>8 mm, 6% of the larvae observed) were recorded only over the continental shelf. Furthermore, the largest larvae were mostly recorded over the inner part of the continental shelf.

Fig. 6. Summary of the hake larvae length spatial distribution derived from the results obtained in this study. All the observations of hake larvae in both years 1983 and 1995 are pooled together and the distribution shown by size groups: <4 mm (circles), 4±8 mm (diamonds) and >8 mm (squares).

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Fig. 7. Progressive vectors of wind-induced Ekman drift for the 1983 and 1995 spawning season of hake. Wind data were obtained every 6 h from 1 April to 31 May (60 days) at 458N, 58W in 1983 and at 458N, 28W in 1995. The magnitudes of the vectors are calculated following Eqs. (1)±(3) in the text. They are applied in a daily basis to the egg distribution centroids estimated in late March 1983 (left panel) and 1995 (right panel). The resultant potential drift is shown both for surface waters (15 m) and for a deeper depth layer (100 m). The latter is negligible.

Fig. 8. Histograms of egg and larval abundance by 0.58C temperature class. Temperature as recorded at 20 m water depth.

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Data on vertical distribution of hake eggs and larvae (Coombs and Mitchell, 1982; Motos et al., 2000) indicate that both eggs and larvae occur in the upper 150 m of the water column. Furthermore, Motos et al. (2000) found that egg and larval distribution was substantially deeper in February 1995 than in March 1995. In the former, hake eggs occurred at a mean depth of 120 m (not enough data were gathered for hake larvae). In March 1995, hake eggs occurred in the 0±50 m water depth range, whereas hake larvae were found mostly in the 50±100 m water depth range. Based on these previous ®ndings, 15 and 100 m were chosen as the range of water depths potentially relevant for egg and larval transport during the 1983 and 1995 reproductive season (Fig. 7). We applied the wind-induced drift vector at 15 m depth to the egg distribution centroid of March during 60 days (from late March to late May). This resulted in a displacement of about 200 km in the SE direction (mean current velocity of about 5 cm sÿ1) in 1983 and 52 km in the NW direction in 1995 (mean current velocity of about 2.5 cm sÿ1). Wind-induced drift in the 100 m depth layer was one order of magnitude weaker than in the 15 m depth layer, in both years, showing very little potential for wind-induced advection at that layer. Fig. 8 shows the frequency distribution of egg and larval abundance by 0.58C temperature classes (20 m depth temperature). Most eggs and larvae occurred in the 10.5±138C temperature range. This range is very similar to the optimum temperature range for hake spawning stated in the literature, i.e. 10±12.58C (Arbault and Lacroix-Boutin, 1969; Dicenta, 1979; Coombs and Mitchell, 1982; Valencia et al., 1989). 4. Discussion Ideally, all the putative spawning season and areas of the European hake population have to be covered for a comprehensive study of the patterns of egg and larval distribution. This study was restricted to the Bay of Biscay, a main area of hake spawning but only a part of the geographical range of spawning of the European hake, and no information was available on hake egg and larval distribution in other hake spawning areas. Within the Bay of Biscay, the main spawning season of hake is assumed to extend from February to May

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(Martin, 1991). Since the data used in this study, came from cruises directed to other target species they provided an incomplete spatio-temporal coverage. In 1983, there was no cruise in February and the data from the April cruise were not available for further processing, giving an uneven temporal coverage in that year. However, the spatial coverage of the 1983 cruises was satisfactory and they covered the areas of the Bay of Biscay where the putative hake spawning ®elds are located. In 1995, the temporal coverage was satisfactory, with cruises all along the main spawning season of hake in the Bay of Biscay, but the spatial coverage was not full. Both in February and in March, the northern part of the area, namely the shelf edge north of 478150 N, was not covered, and in February bad weather conditions further impeded the completion of transects in the northern area (Motos et al., 2000). However, these two surveys were speci®cally directed to hake and the sampling methodology used, namely the high volumes ®ltered by the 60 cm BONGO nets, aimed at getting a more representative picture of the distribution of hake eggs and larvae in these cruises than in the other cruises where GULF III samplers were used. However, the de®cits in the spatio-temporal sampling pattern do not reduce the value of the data set. It constitutes a valuable illustration of hake eggs and larval distribution patterns in the Bay of Biscay along the reproductive season in 2 years, 1983 and 1995. The seasonal variation of hake egg distribution in the Bay of Biscay shows a similar sequence in both years 1983 and 1995. Peak egg abundance occurred in March and decreased both in density and in the proportion of positive hauls as the reproductive season progressed. Although the temporal coverage is not uniform between years, these results indicate that the peak spawning period of hake in the Bay of Biscay is centred in March. This general pattern of distribution is consistent with previous data on hake spawning periodicity in the area. Several authors reported that the presence of hake eggs, and hence spawning, is particularly intense during the ®rst quarter of the year (late winter and early spring months) in the Bay of Biscay (Anon., 1980; Arbault and Lacroix-Boutin, 1969; Dicenta, 1979; Sola and Franco, 1985; Valencia et al., 1989; Martin, 1991; Motos et al., 2000). However, some spawning still remains in the Bay of Biscay throughout the ®rst half of the year (PeÂrez and Pereiro,

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1985; Martin, 1991) as con®rmed by the presence of hake eggs in June both in 1983 and in 1995, although in very low abundance. In quantitative terms and regarding the maximum abundance period (March), our results show that hake eggs in 1983 were about twice as abundant as in 1995 (Motos et al., 1997). This decrease in egg abundance is consistent with the general decline in hake population abundance recorded in the same period (ICES, 1996). Concerning the spatial distribution of spawning, the differences in spatial coverage in the different sampling periods should be taken into consideration. However, two aspects can be highlighted. First, the platform close to the shelf edge appears as a preferential region for spawning in the months of peak spawning, i.e. maximum egg abundance occur in stations close to the 200 m isobath. Second, the shelf break seems to represent a natural barrier for the spawning of this species, since eggs are almost absent in stations located outside the continental shelf. The seasonal evolution of the distribution of egg and larval centroids (Table 2 and Figs. 2 and 4), give some insights about the spatio-temporal pattern of hake spawning in the Bay of Biscay. An initial, northward movement is followed by a coastward and eventually southward movement at the end of the study period. This pattern can be better demonstrated in 1995, the year with a better coverage. This pattern is also consistent with the current knowledge of hake spawning along the North Atlantic coast concerning the northern displacement of the spawning as the season progresses (Coombs and Mitchell, 1982; Casey and Pereiro, 1995; O'Brien and Fives, 1996; Horstman and Fives, 1994; Fives et al., this issue). Either a northward migration of the spawners or a maturation wave going northwards as the season advances can explain this fact. On the other hand, the observed movement of the distribution centroids towards the coast in May and/or June is consistent with the description of a spawning starting near the shelf break and extending later in the season towards the continental shelf (Horstman, 1988; Fives et al., this issue). However, as mentioned in Section 1, it contradicts the observations of Arbault and Lacroix-Boutin (1969) about hake spawning starting close to the coast and spreading towards deeper waters later in the season. Spawning time is the result of an adaptive evolutionary process leading to the population sustaining

itself in the long term (Heath, 1992). The northward movement of spawning shown in this study should be related to particular hydrographical conditions favouring maturation and spawning. Temperature appears to be a determinant factor driving the timing Ð both beginning and duration Ð of the spawning season (Hoar and Randall, 1988). In the case of hake, this paper con®rms that the optimum temperature range for spawning lies between 10 and 12.58C (Fig. 8). This temperature range is common in Bay of Biscay waters in the depth range of the hake habitat along the reproductive season of this species, i.e. from January to June (Koutsikopoulos and Le Cann, 1996). Therefore, the observed displacement of the spawning areas, although within the temperature range mentioned above, has to be related to other factors (Valencia et al., 1989). These authors suggested that vertical homogeneity and the winter peak of the phytoplankton cycle were environmental factors related to hake spawning. In more northern latitudes the spawning period of hake is located in late spring, early summer months (O'Brien and Fives, 1996; Horstman and Fives, 1994), coinciding with water temperature Ð or related hydrological conditions Ð close to the optimum range. For both eggs and larvae the position of the distribution centroids in the highest abundance month, i.e. March, indicated that in 1983 the spawning centres were displaced to the north earlier than in 1995 (78 km for eggs, and 48 km for larvae) (Fig. 3). Horstman and Fives (1994), observed an earlier spawning of hake and other species in the Celtic Sea and West Irish waters in 1983 and suggested an earlier warming up of sea water that year as the factor giving rise to early spawning. The distribution of larvae was similar in both years. It was widespread all along the study area during the two ®rst period intervals (February and March) and concentrated in the north-eastern corner of the Bay of Biscay in April and May, giving evidences of a northeasterly movement of larvae as indicated above. The spatial distribution of average length of hake larvae (Fig. 5) shows a size gradient in the east±west direction. With some exceptions, the largest larvae appear generally in those stations closer to the coast. Again, this suggests a coastward displacement of the larvae from the main spawning areas close to the shelf break, which is consistent with general residual

P. Alvarez et al. / Fisheries Research 50 (2001) 111±128

current maps presented by Castaing et al. (1993) and Koutsikopoulos and Le Cann (1996) for the Bay of Biscay. Nevertheless, the distribution of mean length of hake larvae in the northern-most part of the study area in March 1995 showed a different pattern, with bigger larvae both in the offshore and the coastal part of the northernmost transects and smaller larvae in the mid-part. There, the geostrophic ¯ow ®elds show the presence of a cyclonic eddy placed outside the shelf break (Motos et al., 2000). This gyre could be trapping part of the larvae coming from the shelf break spawning area and could be responsible of the retention and offshore drift of the trapped larvae. However, the pattern explained above would be similar in the rest of the transect, where eggs and larvae would be advected onto the shelf, giving rise to the observed increasing gradient of larval sizes from the shelf break to the coast. The occurrence of the largest sized larvae (<8 mm) exclusively over the continental shelf (Fig. 6) suggest that larvae advected offshore would be trapped in a unfavourable environment and will eventually die as already pointed out by Hollowed and Bailey (1989) for Merluccius productus. Our results suggest that if hake larvae are not transported onto the continental shelf before they reach 8 mm, it is likely that they will eventually die. The oceanographic conditions prevailing during the ELH stages will be of primary importance concerning the transport of eggs and larvae onto the shelf, in order to ensure survival success for the egg and larval cohorts, and hence, recruitment success. The present paper and data elsewhere (Anon., 1980; Arbault and Lacroix-Boutin, 1968, 1969; Motos et al., 2000) show that there is usually a high abundance of hake eggs and larvae pears in the northern part of the Bay of Biscay, i.e. in waters off southern Brittany (Bretagne). The European hake has several documented juvenile nursery areas (ICES, 1996). In the Bay of Biscay, a main nursery area is indeed located in the northern part, where hake juveniles (0 group) concentrate from 120 m depth-line to the coastline from late spring to the autumn (Bez et al., 1995). However, the main spawning centre of hake in this area is well offshore, mainly over the shelf edge, as described in this paper. Eggs and larvae must therefore be transported towards the coast over the shelf into the nursery areas. We have also show that hake larvae tend to be

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localised more north-easterly than hake eggs at the same season of the year. Prevalent residual currents in the area (Castaing et al., 1993; Koutsikopoulos and Le Cann, 1996; Barscht et al., 1996; Motos et al., 2000) and passive diffusion (Koutsikopoulos et al., 1991) processes will determine whether the eggs and larvae move towards the coast, remain in the spawning areas or are dispersed offshore. Any further analysing of net transport of hake eggs and larvae, would have to consider tidal currents, wind-induced currents and geostrophic currents. The most relevant forcing factor in the upper water (15 m) is generally the wind, which can induce currents on the order of 5±10 cm sÿ1. Net transport due to tides is negligible at the shelf break, although, it increases coastwards. The wind-induced current velocity decreases exponentially with water depth according to Ekman's theory. Therefore, the wind-induced current velocity at 100 m water depth is of the order of between 0.05 and 0.1 cm sÿ1. The variation of tide-induced current velocity with water depth (Postma, 1988) shows that the current velocity decreases slowly at the surface layers and then decreases rapidly towards the bottom. In the Bay of Biscay, the average tidal range is of about 4.6 m and tide-induced currents are larger in shallow waters than in the open sea. Nevertheless, tide-induced transport can be considered negligible at any depth. The magnitudes of geostrophic currents (0±100 m) in the Bay of Biscay analysed in this study has been derived from CTD pro®les, and are in the range 2±3 cm sÿ1 (Motos et al., 2000). Some exceptions can be found in some eddies, were velocities can be in excess of 10 cm sÿ1. Therefore, in the upper layers of the water column, the net dominant current is the one induced by the wind. On the other hand, at 100 m water depth, the dominant net ¯ow is determined by geostrophy. Nevertheless, in order to get a good approximation of the magnitude of the currents in the area, the three forcing factor components (wind, tide and geostrophy) should be added. The wind-induced drift data shown here for 1983 favoured an onshore transport (SE) toward coastal nurseries (Fig. 7). Data from studies carried out in the Bay of Biscay in 1983 (Castaing et al., 1993) pointed out that residual currents moved in a northeasterly direction during mid-winter to spring that

126

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year. The distribution pattern of hake larvae found that year appears to be coherent with the hydrographical processes observed during the study period. The geostrophic ¯ow observed during the March 1995 cruise showed clear ¯uxes in the north-eastern direction (Motos et al., 2000). Wind-induced drift was much weaker in 1995 than in 1983 and possibly had a very low contribution to the net ¯ow. During 1995, hake eggs and larvae were advected from the spawning areas at the shelf edge, towards the north and towards the inner shelf by the dominant geostrophic ¯uxes, leading eventually to the spatial distribution of larvae found in March. This advection pattern was also con®rmed by a three-dimensional physical model of the southern European shelf area (Barscht et al., 1996). Finally, meso-scale events such as gyres or ®laments can trap slope water where hake eggs and larvae inhabit and advect them offshore (Barscht et al., 1996; Motos et al., 2000). As already stated above, larvae advected offshore are removed from the population suggesting that the in¯uence of slope water ®laments and gyres can be detrimental to recruitment success. Another known nursery area usually appears in the south-eastern corner of the Bay of Biscay (28W) (SaÂnchez, 1994). The highest abundance of hake larvae in this area was found during the February cruise in 1995. In addition, the larval distribution found there in March 1995, although low, seems to

suggest that eggs spawned in February were retained and developed into large larvae by the end of March (Barscht et al., 1996). Alternatively, the occurrence of large larvae can result from the accumulation of material coming from the coastal areas of the Cantabrian Sea. The general circulation in the area shows an eastward transport (Barscht et al., 1996) which can result in accumulation of material in the eastern Cantabrian Sea (SaÂnchez, 1994; Cabanas, 1994), where the direction pattern of the currents is not clear and the intensity slackens. Based on the patterns of distribution described here, several issues are worth emphasising. By comparing distribution of eggs and larvae, we inferred dispersion (advection plus diffusion) in the north and northeast directions. These drift patterns were similar for both years and are consistent with the available data on the physical oceanography of the area. The pattern of oceanographical processes in the peak season of hake egg production in the Bay of Biscay leads to the maintenance of the integrity of the population by linking the main spawning areas located in the shelf break with the known nursery areas located in shelf waters closer to the coast. These kinds of processes have been postulated as one important regulatory mechanism of recruitment, and hence, population sustainability (Sinclair, 1988). The average current patterns on the spatio-temporal window of hake peak spawning in the study area may have resulted in the

Table 3 Summary of recruitment variation for several fish populations Species

Population

na

CVb (%)

Hake

M. merluccius

Cod

M. productus M. capensis M. bilinearis M. gayi M. gayi G. morhua

Haddock

M. aeglefinus

Anchovy Mackerel Horse mackerel

E. encrasicholus S. scombrus T. trachurus

ICES northern ICES southern North Pacific South Africa 1.6 NAFO 4VWX Peru Chile NAFO 2J3KL NE Arctic NAFO 3NO NE Arctic Bay of Biscay NE Atlantic NE Atlantic

14 9 32 20 20 10 14 31 43 25 42 15 19 9

22 60 138 34 54 57 29 57 72 185 129 103 50 226

a b

Number of recruitment estimates available for a given species. Coefficient of variation of the mean recruitment. The data is taken from Myers et al. (1995).

P. Alvarez et al. / Fisheries Research 50 (2001) 111±128

evolution of reproductive patterns such that hake spawn in winter and early spring months when onshore transport prevails in northern Biscay waters. Hake recruitment shows rather low variability when compared with other ®sh species. Table 3 shows the coef®cients of variation (CV) of recruitment for a series of populations (Myers et al., 1995). The CV of hake recruitment of the northern population unit in the ICES area, was 20%, one of the lowest in ®sh populations. This suggests that the pattern of hake recruitment described above is consistent year after year and leads to a relatively low variation in recruitment success in the long term. Based on the pattern of egg and larval distribution described here, we inferred advection processes in particular directions. The drift patterns were compatible with the physical oceanography of the area. These results re-inforce the need for a good knowledge of the fundamental physical processes so as to understand better the complex physical/biological interactions in¯uencing recruitment of marine populations (Sinclair, 1988; Kendall and Picquelle, 1989; Francis et al., 1989; Heath, 1992; Koutsikopoulos and Le Cann, 1996; Motos et al., 2000; ValdeÂs et al., 1996). Acknowledgements The results presented in this study were obtained within the European Union SEFOS project (contract AIR2-CT93-1105). SEFOS is the acronym for Shelf Edge Fisheries and Oceanography Studies. The authors very much appreciate the bene®ts of the contrast of opinions with the various colleagues involved in the SEFOS project. Ichthyoplankton samples were provided by MAFF Fisheries Laboratory (Lowestof, UK) SOAFD Marine Laboratory (Aberdeen, Scoland) and RIVO-DLO (Ijmuiden, the Netherlands). Inmaculada MartõÂn and InÄaki Rico (AZTI) carried out the sample sorting work. References Alcazar, J., Carrasco, J., Llera, E., Menendez, M., Ortega, J., Vizcaino, A., 1983. BiologõÂa dinaÂmica y pesca de la merluza en Asturias. Recursos Pesqueros de Asturias 3.

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