Feeding Behaviour and Trophic Environment of Engraulis encrasicolus (L.) in the Bay of Biscay

Estuarine, Coastal and Shelf Science (1999) 49, 177–191 Article No. ecss.1999.0497, available online at http://www.idealibrary.com on

Feeding Behaviour and Trophic Environment of Engraulis encrasicolus (L.) in the Bay of Biscay S. Plouneveza and G. Champalbertb a

Laboratoire d’Oce´anographie et de Bioge´ochimie, Centre d’Oce´anologie de Marseille, Campus de Luminy, Case 901, 13288, Marseille Cedex, France b Institut de Recherche pour le De´veloppement, B.P. 917 Abidjan 15, Coˆte d’Ivoire Received 21 July 1998 and accepted in revised form 19 March 1999 The main environmental abiotic and biotic factors and the feeding activity of adult anchovy were analysed in the Bay of Biscay during the spawning period (spring) in neritic and oceanic areas characterized by high anchovy densities. In the neritic area located in the water plume of the Gironde estuary (‘ GIR ’) chlorophyll concentrations and zooplankton biomass, above and below the thermocline, were higher than in the oceanic area (‘ FAC ’). Copepods constituted the dominant group of zooplankton (d85%); the main species were, decreasingly: Clausocalanus sp.Paracalanus parvus, Oncea sp., Corycaeus sp., Temora longicornis and Oithona sp. in GIR and Clausocalanus sp.-P. parvus, Oithona sp., Centropages chierchiae and Acartia clausi in FAC area. Anchovy feeding activity mainly occurred during the day and was higher in the FAC area than in the GIR area. Food ingested constituted exclusively of zooplankton, in particular copepods that made up about 98%; T. longicornis, Oncea sp. and Corycaeus sp. were the main species in the ‘ GIR ’ area and C. chierchiae in the FAC area. Considering anchovy distribution and feeding characteristics, (fullness index, preponderance index especially) the results showed that, in both areas, biting (anchovy taking of prey) is the dominant or exclusive pattern of anchovy feeding behaviour. Feeding efficiency appears to be most related to zooplankton specific composition than to zooplankton abundance.  1999 Academic Press Keywords: feeding; stomach content; Engraulidae; Copepoda; spawning season; Bay of Biscay

Introduction The European anchovy, Engraulis encrasicolus lives in the NE Atlantic Ocean and in the European seas (Mediterranean Sea, Black Sea and Azov Sea). In the Bay of Biscay, as in the Mediterranean Sea, the spawning period, March to October, presents a peak between May and July (Aldebert & Tournier, 1971; Arbault & Lacroix-Boutin, 1977; Sanz & Uriarte, 1989; Lucio & Uriarte, 1990; Palomera & Sabate´s, 1990; Palomera, 1992; Motos et al., 1996). In the Bay of Biscay, as observed in many areas of the world with extensive clupeoid fisheries (see Blaxter & Hunter, 1982), the European anchovy is an important economical resource for French and Spanish fishermen (catches of 11 000 tons and 7000 tons respectively during 1997). Inter-annual variations of anchovy abundance and distribution are important but no evident relationship between their recruitment and stock size has been demonstrated (Masse´, 1996; Uriarte et al., 1996). As emphasised by Miller (1994), food supply of larvae and juveniles as well as predation are probably 0272–7714/99/080177+15 $30.00/0

the most important factors responsible of the variability of the recruitment, i.e. the number of individuals entering the fishery. Adult cannibalism can directly modify recruitment. Thus, Hunter and Kimbrell (1980) and Valde´s et al. (1987) respectively observed that 32 and 70% of the egg mortality of the Northern anchovy and the Cape anchovy is due to adult cannibalism. However, in the Catalan Sea, Tudela and Palomera (1997) found that cannibalism on anchovy eggs by adult E. encrasicolus was very low. This result was explained by the spatial and temporal mismatch between feeding activity occurring mainly during the day—while fish remain below the thermocline—and spawning occurring at night, after the diel migration above the thermocline (Aldebert & Tournier, 1971; Palomera, 1991). Recruitment can also be modified indirectly by the adult feeding activity. In the Bay of Biscay, female anchovy spawn every 3–7 days (Sanz & Uriarte, 1989; Sanz et al., 1989; Motos et al., 1991); therefore, as shown for several clupeoids (Hunter & Leong, 1981; Blaxter & Hunter, 1982; Valde´s-Szeinfeld, 1993), frequent spawnings require a high energy expenditure  1999 Academic Press

178 S. Plounevez and G. Champalbert 45°44 N

N 'Gironde' area

Great Britain

50°

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3 2 10 5 4 11 8 12

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France

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Gironde Estuary

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Hydrobiological sampling stations Location and direction of trawls

F 1. Location of hydrobiological sampling stations and trawls performed during PEGASE 97 cruise in the Bay of Biscay.

and an intake of proteins from food. Hunter and Leong (1981) observed that feeding conditions particularly affect the number of spawnings per year. The aim of the present article is to study the feeding behaviour of adult anchovy E. encrasicolus in relation to abiotic (temperature, salinity) and biotic factors (chlorophyll, zooplankton) in order to determine the impact of anchovy feeding activity on its spatial distribution during the spawning season in the Bay of Biscay.

transects and pelagic trawls to identify species in the shoals. The second part of the cruise was devoted to anchovy ecology, in particular to the study of anchovy feeding behaviour in relation to the trophic environment characteristics. Pelagic trawling, water and zooplankton sampling were performed in two areas of high anchovy densities detected by echosounding: the Gironde area (GIR) in a neritic zone, 40 m deep, near the Gironde Estuary and the Fer a` Cheval area (FAC) located offshore, with oceanic characteristics.

Materials and methods

Temperature, salinity and chlorophyll a samples

The study was carried out in the Bay of Biscay, during the PEGASE 97 cruise (PG 97: 6 May–2 June 1997) on the RV Thalassa (Figure 1). The first part of the cruise was focused on the stock assessment of the small pelagic fish from acoustic methods used along regularly spaced (10 nautical miles) inshore–offshore

In each area surveyed during the second part of the cruise (GIR and FAC), five temperature and salinity profiles were recorded (during the day or the night) along three regularly spaced transects (3 miles) with a CTD probe (Sea Bird SBE 19) (Figure 1). The CTD probe was linked to a computer by a

Feeding behaviour and trophic environment of Engraulis encrasicolus 179

transmission cable and the results observed in realtime on a monitor. Water samples were collected with a Niskin bottle at standard depths in the GIR area (0 m, 10 m, 20 m, 30 m and 40 m) and FAC area (0 m, 10 m, 20 m, 30 m, 50 m and 100 m) to measure chlorophyll a concentrations (Yentsch & Menzel, 1963). Results are expressed in ìg per litre.

the genus level (Rose, 1933). The two groups Clausocalanidae and Paracalanidae were clustered in one taxa because precise identification was time-consuming and not essential for the objectives here. The number and the relative abundance of the different taxa were calculated per m3.

Zooplankton samples

Fish samples

At each hydrological station, zooplankton was collected with a WP-2 standard net (mesh size: 200 ìm) equipped with a closing mechanism. The nets were towed vertically: from the bottom of the thermocline to the surface; from the bottom of the water column to the bottom of the thermocline in the GIR area or from 200 metres to the bottom of the thermocline in the FAC area. In the GIR area, over 30 m (stations 9, 10 and 11), a single haul was made from the bottom to the surface. On board, zooplankton samples were divided into two parts with a Motoda box; the first part was sorted in two size classes ([200–500 ìm] and >500 ìm). Each subsample was dried at 50 C for 72 h. The second part was preserved in 5% buffered formaldehyde. In the laboratory, zooplankton biomass samples were weighed on a Mettler-AT-261 Delta-Range balance (precision at 0·01 mg) and the results were sorted in dry weight per m3. In each area, zooplankton biomass samples were sorted into four groups according to the time of the day (day or night stations) and the water column layer (above or below the thermocline). A one-way analysis of variance (ANOVA), a test of homogeneity of variances (Levene test) and a comparison among a set of means (Bonferonni tests) were used to compare data obtained in the GIR area and in the FAC area. Biomass from the FAC area were transformed (square) in order to reduce the heterogeneity of variances. For each area, zooplankton samples of eight sampling stations were subsampled by the ‘ surface method ’ (Bourdillon, 1964). Zooplankton samples were poured into a circular flatbottomed receptacle of known surface. After homogenization of the sample, three subsamples delimited by a cylinder whose surface was known were picked out. Each subsample (about one thousand individuals) was decanted in a ‘ Dolfuss ’ bowl. Specimens were sorted into different taxa and identified under a stereo-microscope to group level for ostracods, molluscs, crustacean larvae, (Tregouboff & Rose, 1957a, b) and to species level for cladocerans and copepods except Clausocalanidae, Oithonidae, Oncaeidae and Corycaeidae which were identified to

Anchovies were collected using a mid-water trawl towed for about one hour at different times of the day to cover the diel cycle in each area. Twelve tows were carried out during the second part of the cruise (Figure 1). One kilogram of adult anchovy was taken at random from every haul and put immediately frozen at
40 C (cold room) to stop the digestive processes. About 4 h later, fish were preserved at
20 C to be treated in the laboratory. From each kilogram sampled, 30 to 33 adult anchovies were picked out at random to be analysed. Sex was determined and fish length was rounded down to the nearest 0·5 cm. Fish wet weight (FW, to the nearest 0·001 g), gonad wet weight (GW, to the nearest 0·001 g) and wet weight of the stomach content (SW, to the nearest 0·1 mg) were recorded. Three hundred and ninety-three fish were studied, of mean size 14·0 cmSE 1·5 cm (n=195) and 12·5 cmSE 1·0 cm (n=198) in GIR and FAC areas respectively. Out of 393 fish, 213 (16–20 fishes for each sample) were used for prey number estimates and the determination of items found in stomachs using the same criteria as those chosen for plankton samples. Anchovy feeding activity was characterized by two parameters: the stomach fullness index (F) and the index of preponderance (Ip) which is calculated from an univariate method (Marshall & Elliott, 1997). These parameters were calculated from anchovy samples in each area. Fullness Index:

where weights were expressed in g and fish whose stomachs were empty were not used. The terms of the equation are explained above. Index of preponderance:

180 S. Plounevez and G. Champalbert

where Mi is the ratio (in percent) of the weight of the prey i to the weight of all the prey and Oi is the occurrence of the ith prey. This index sorts prey items by dominance (Marshall & Elliott, 1997). It was calculated for anchovy samples from each area (0cIp=ic1 and ÓIp =1). Prey dry weights used in index calculations were measured in the laboratory for the dominant copepod species, fish larvae and crustacean larvae. Sets of Oncea sp., Corycaeus sp. Temora longicornis, Centropages chierchiae and Candacia armata were dried at 50 C for 72 h. As suggested by James (1987), a power regression of dry weight vs total length (except furca) was calculated and used to estimate the weight of other copepod species. Sets of fish larvae and crustacean larvae of each group were dried at 50 C for 72 h; their mean values were used in index calculations. For rare prey items, the relations of James (1987) were used. A two-way analysis of variance was used to test statistical significance of fullness index between the two areas and the time of trawls. In the GIR area, trawls were carried out at different times and it has been assumed that in the FAC area each trawl was performed at the same time to that of its equivalent in GIR area. Fullness indices were transformed (logarithm (n)) in order to reduce the dispersion of variances. The length and the width of five individuals of the nine dominant copepods in the field and/or the anchovy stomachs were measured. A one-way analysis of variance (ANOVA) with means comparisons (Bonferonni tests) were performed. The statistical tests were carried out with SAS software. Results Hydrological features In the GIR area, the water column was stratified into temperature and salinity (Figure 2). The thermocline and halocline were situated between 15 and 30 m. In surface waters the mean value of the temperature was about 16·5 C and in deeper waters, about 12·5 C. As a result of the direct influence of waters from the Gironde estuary, salinity was lower above the thermocline (35·10 using the Practical Salinity Scale) than below (35·45). Chlorophyll a profiles showed a clear peak (until 3·3 ìg 1
1) in the thermocline at 20 metres depth. Above the thermocline, chlorophyll a values ranged between 0·5 and 1·4 ìg 1
1, below the thermocline, the values were lower, ranging between 0·4 and 1·2 ìg 1
1.

In the FAC area, the thermocline was located between 15 and 40 metres (Figure 2). The mean temperatures above and below the thermocline were similar to those found in the GIR area. Throughout the water column salinity (about 35·60) and chlorophyll (0·3 ìg 1
1) were more homogeneous; nevertheless, slightly higher values of chlorophyll a were found at the bottom of the thermocline (30 metres depth) and below the thermocline (50 metres depth). Zooplankton Gironde area. The whole water column was rich in zooplankton (Figure 3). The highest values (P<0·05) of zooplankton biomass were observed at night above the thermocline (mean values 64 mg m
3) (Table 1). During the day, zooplankton biomass above the thermocline was not significantly different from zooplankton biomass below the thermocline (P>0·05). Moreover, zooplankton biomass above the thermocline during the day was not significantly different (P>0·05) from zooplankton biomass below the thermocline at night (mean values 33–41 mg m
3) (Table 1). The difference between day and night samples above the thermocline came from large-sized zooplankton; at night organisms >500 ìm were much more abundant than during the day time. The abundance of 200–500 ìm zooplankton was similar above and below the thermocline during day and night (about 20 mg m
3). Zooplankton-specific composition showed that copepods made up 92% above the thermocline with individual numbers ranging between 1657 and 5682 per m 3 (Table 2). The most abundant copepods were decreasingly Clausocalanus sp.-P. parvus (46%), Oncea sp. (19%), Corycaeus sp. (9%), Temora longicornis (5%) and Oithona sp. (5%). Below the thermocline, copepods made up 98% (individual number ranging between 2797 and 10 400 ind. m
3). The most abundant species were similar to those found above the thermocline, but in slightly different proportions: Clausocalanus sp.-P. parvus (44%, Oncea sp. (30%), T. longicornis (11%) Corycaeus sp. (4%), and Oithona sp. (4%). The copepods were the dominant group in the water column among which Clausocalanus sp. and P. parvus were the most abundant. Fer a` Cheval area. Zooplankton biomass did not exhibit day–night variations either above or below the thermocline (Figure 3 and Table 3). Zooplankton biomass was seven times higher above the thermocline (mean value 35 mg m
3) than below (mean value 5 mg m
3). Above the thermocline, the

GIR area Temperature (°C) 13

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Salinity

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F 2. Temperature, salinity and chlorophyll a profiles from the bottom or from 100 m to the surface in the GIR and FAC areas respectively.

Feeding behaviour and trophic environment of Engraulis encrasicolus 181

Depth (m)

12 0

Chlorophyll a (µg l–1)

Salinity

182 S. Plounevez and G. Champalbert GIR area

70

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Night

Day

Night

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Dry weight (mg m–3)

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Dry weight (mg m )

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70

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FAC area

80 Dry weight (mg m–3)

–3

Dry weight (mg m )

80

60 50 40 30 20 10 0

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60 50 40 30 20 10 0

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Day

70

F 3. Zooplankton biomass (mg m
3) by length classstandard error above (a) and below (b) the thermocline in the GIR and FAC areas. : length class >500 ìm; : 200 ìm^length class^500 ìm. T 1. Bonferroni tests on zooplankton biomass according to the time of day (day or night stations) and the water column (above or below the thermocline) in the GIR area

Zooplankton biomass

Mean (mg m
3)

T 2. Bonferroni tests on zooplankton biomass (square) according to the time of day (day or night stations) and the water column (above or below the thermocline) in the FAC area

Groupinga Zooplankton biomass

Above-day Above-night Below-day Below-night

40·7 64·3 37·2 32·9

Square (mean)

Groupinga

B A B B

Above-day Above-night Below-day Below-night

5·9 5·4 2·1 2·1

A A B B

a

Means with same letter were not significantly different (á=0·05) (ANOVA: F(3,23) =5·8 and P(F)=0·004; Levene test: F(3,23) =0·67 and (P(F)=0·57).

biomass of organisms whose size class were contained between 200 ìm and 500 ìm was slightly higher than the biomass of organisms >500 ìm. Below the thermocline, the results did not show a clear trend. Copepods were dominant in the whole water column with mean values reaching 97% above and below the thermocline (Table 4). Above the thermocline, the number of copepods ranged between 2274 and 7122 per m3 and the dominant copepods were decreasingly, Clausocalanus sp.-P. parvus (57%), Oithona sp. (17%), C. chierchiae (11%) and Acartia clausi (8%). Clausocalanus sp. and P. parvus were mainly copepodite forms (46%). Below the thermocline, copepods were 10 to 20 times less numerous

Means (mg m
3) with same letter were not significantly different (á=0·05) (ANOVA: F(3,29) =60·3 and P(F)<0·0001; Levene test: F(3,29) =1·4 and (P(F)=0·26).

a

than above the thermocline with individual numbers ranging between 85 and 825 per m3 and the same species dominated, except A. clausi which was less abundant (3%). Clausocalanus sp. and P. parvus copepodite forms were less abundant (35%) than above the thermocline.

Feeding activity of adult anchovy Gironde area. Anchovy fullness indexes, comprised between 2 and 7 during the day and in the early night but were almost equal to zero later at night (0:30 h),

T 3. Zooplankton specific composition (ind. numb. m
3) above (A) and below (B) the thermocline in the GIR area 1 Sampling station Water column

Copepoda individual number Total individual number Standard deviation

A

B

A

— — 45 24 2063 — 4 — — — 145 9 — 9 — 136 268 336 86

— — 51 9 1441 — 2 — — — 262 4 — 4 — 733 124 47 120

— — 387 29 1913 — 18 — — — 182 — — 6 — 323 927 205 —

— 18 5 9 — — —

3

7

11a

8

A

B

A

B

A

B

A

B

A

— — 184 12 2681 — 4 — — — 569 — 11 22 — 6282 268 362 6

— — 111 56 2242 — 62 — — — 242 — — — — 1889 440 217 12

— — 92 5 1381 — 3 — — — 374 — — 4 — 398 68 84 25

3 — 25 120 3010 — 201 — — — 45 — — 3 3 1697 521 47 8

— — 65 14 5602 — 2 — — — 254 6 — — — 3025 830 25 —

— — 71 18 1089 — 15 — — — 56 — — 3 — 117 129 144 15

— — 37 9 2072 — 1 — — — 516 — — 5 9 492 116 441 116

— — 200 62 1118 — 26 — — — 49 — 3 — — 472 121 85 79

— — 159 1 1396 — 9 — — — 493 8 8 25 — 4874 360 284 234

— 11 6

— 50 6

— —

— 100 3

3 10 6

15 18 8

—

—

—

— 59 6

— — —

13 14 — —

6 18 — —

—

— — —

— 19 — —

—

— 4

— 68 — 50 — 5 — — 5 23 — 18

— 13 — — — — — — — 17

— 153 — — — — — 53 12 65 6 59

3125 3324 816

2797 2860 677

3990 4424 991

2

(—: absent; aplanktonic haul throughout the water column).

B

4

6

6 — — —

—

6 — — — 22

— 56 6 — — — — 25 — 68 — 115

10 400 10 461 581

5270 5602 223

5 — — — 6 —

1 8 4 4 — —

8 — —

4 4 8

— 75 8 — — 3 — 8 22 281 3 25

2434 2470 257

5682 6220 822

4 — — — — — — —

—

8 — — —

2 — 51 6 37

— 56 — — — — — 5 3 51 — 25

9823 9962 1506

1657 1844 125

5 — — — — —

5 23 5 1

3 —

B

A

B

— — 146 27 1212 — 18 — — — 660 — — 16 5 644 271 264 111

— — 139 25 1867 — 62 — — — 359 — 31 3 3 1994 180 245 12

— — 99 12 3437 — 31 — — — 2533 — — 12 — 403 136 372 93

— 34 —

— 31 6

—

— —

— 6 6

7 13 — —

— —

— —

19 19 — —

5

— 62 7 10 — — — — 7 23 10 30

17 8 2 8 — 25 — — — 1 1 110

— 79 4 — — — — 9 14 72 2 74

— 43 — — — — — 43 12 71 — —

— 37 — — — 19 — 6 — 6 6 81

3814 3867 672

2216 2387 250

7852 8027 1324

3375 3668 506

4920 5165 637

7128 7308 1402

— — — 8 1 — — — — 2 — 3 —

2 1

13

5

6

6

Feeding behaviour and trophic environment of Engraulis encrasicolus 183

Copepoda Candacia armata Candacia sp. Acartia clausi Centropages chierchiae Clausocalanidae and Paracalanidae Euchaeta marina Calanus helgolandicus Pleuromamma gracilis Pleuromamma xiphias Anomalocera patersoni Temora longicornis Temora stylifera Clytemnestra sp. Euterpina acutifrons Microsetella sp. Oncea sp. Corycaeus sp. Oithona sp. Unidentified Copepoda Cladocera Penilia avirostris Evadne sp. Podon sp. Other Crustacea Unidentified Decapoda larvae Unidentified Euphausiacea larvae Unidentified Mysidacea larvae Amphipoda (juveniles) Miscellaneous Doliolidae Chaetognatha Appendicularia (Oı¨kopleura sp.) Siphonophora Ostracoda Mollusca Polychaeta Unidentified fish larvae Clupeiod fish larvae Anchovy eggs Unidentified fish eggs Miscellaneous

2

17 Sampling station Water column Copepoda Candacia armata Candacia sp. Acartia clausi Centropages chierchiae Clausocalanidae and Paracalanidae Euchaeta marina Calanus helgolandicus Pleuromamma gracilis Pleuromamma xiphias Anomalocera patersoni Temora longicornis Temora stylifera Clytemnestra sp. Euterpina acutifrons Microsetella sp. Oncea sp. Corycaeus sp. Oithona sp. Unidentified Copepoda Cladocera Penilia avirostris Evadne sp. Podon sp. Other Crustacea Unidentified Decapoda larvae Unidentified Euphausiacea larvae Unidentified Mysidacea larvae Amphipoda (juveniles) Miscellaneous Doliolidae Chaetognatha Appendicularia (Oı¨kopleura sp.) Siphonophora Ostracoda Mollusca Polychaeta Unidentified fish larvae Clupeiod fish larvae Anchovy eggs Unidentified fish eggs Miscellaneous Copepod individual number Total individual number Standard deviation (—: absent).

19

21

22

23

24

25

28

A

B

A

B

A

B

A

B

A

B

A

B

A

B

A

B

— — 126 358 1426 — 4 — 2 1 31 — — — 1 6 3 292 26

— — 1 4 58 1 1 — — — — — — — — — — 16 3

— — 590 525 2547 — 75 — — 4 40 — — — — — 10 273 23

2 — 30 125 330 — 7 — — — 15 — 3 — 1 — 3 88 1

— — 266 510 4738 — 21 — — — 51 — 4 — 4 — — 1526 —

— 1 9 93 271 1 6 — — — 27 — 1 — — — 2 64 5

— — 116 259 2201 — 6 — — 1 10 — 4 3 — 19 13 497 11

— — 4 19 447 1 11 — — — 6 — 1 — — — 2 42 1

— — 161 453 1557 — — — — — 43 — 6 — — 43 9 703 14

1 — 52 102 476 1 9 — — — 22 — 4 — 1 3 8 136 10

— — 686 259 1204 — 15 3 — 6 38 — — — 6 8 11 835 35

— 2 14 2 234 1 4 1 3 — 1 — — — — 1 — 44 8

— — 446 875 3941 — 86 3 — — 120 — — — — 14 6 1154 —

1 1 25 82 498 1 19 1 6 — 5 — 2 — — 1 3 54 5

— — 107 247 1986 — 3 — — — 33 — 6 — — 5 10 605 43

1 — 9 150 490 1 11 — — — 9 — 2 — — 1 5 31 4

— 14 —

— 11 —

— 86 2

— 3 —

— 103 —

— — —

— 56 3

1 2 —

— 150 —

— 8 1

— 178 6

— 3 1

— 170 6

— 3 —

— 48 2

— — —

—

— 1 — —

— 17 — —

— 1 — —

— 21 — —

— 1 — —

—

— 3 — —

— — — —

1 2 — —

— 13 — —

— 1 — —

11 8 — —

— 1 — —

—

— 3 — —

— — — — 2 — — — — — — —

— — — — — — — 10 — 6 — —

— 1 — — 1 — — — — — — —

— — — — —

— —

1 — 11 1 —

— — — — 2 — — — — — — —

— — — — — — — 20 3 28 — —

— — — — 1 — — — — — — —

— —

6 — — — 26 — —

— — — — 2 1 — — — — — —

—

1 — 29 — —

— — — — 2 — — — — — — —

— — —

— — — — — —

— — — — 3 — — — — — — —

2 — — — — — — 18 — 2

— — — — 3 — — — — — — —

85 100

4086 4207 736

604 610 159

7122 7250 1208

479 483 121

3140 3236 156

536 544 90

2990 3177 400

825 839 90

3105 3322 173

314 322 63

6644 6889 465

704 710 187

3045 3118 704

714 720 114

2 — — — — — — — — — — — 6 — — 2274 2295 286

4

6 — —

1 — — — —

6 —

4 — — — 3 —

3 — —

184 S. Plounevez and G. Champalbert

T 4. Zooplankton specific composition (ind. numb. m
3) above and below the thermocline in the FAC area

Feeding behaviour and trophic environment of Engraulis encrasicolus 185

Fullness index (g SW 1000 g–1)

30 25

GIR area Sunrise

Sunset

20 15 10 5 0 0:00 2:00 4:00 6:00 8:00 10:00 12:00 14:00 16:00 18:00 20:00 22:00 0:00 Time (h)

Fullness index (g SW 1000 g–1)

30 25

FAC area Sunrise

Sunset

20 15 10 5 0 0:00 2:00 4:00 6:00 8:00 10:00 12:00 14:00 16:00 18:00 20:00 22:00 0:00 Time (h)

F 4. Fullness index (meanstandard deviation) of anchovies vs time of day (U.T.) in the GIR and FAC areas.

suggesting that anchovy feed during the day and that feeding activity stops during the night (Figure 4). Fer a` Cheval area. The feeding activity pattern was similar to that observed in the GIR area (Figure 4). However, mean index values, ranging between 7 and 17 (except late at night), were significantly higher (P<0·001) than in the GIR area (Table 5). Diet composition of adult Engraulis encrasicolus Gironde area. The total bulk of anchovy diet was made up of zooplankton (Table 6). Copepods were the predominant stomach items in all samples (ÓIpd0·873), especially T. longicornis, Corycaeus sp. and Oncea sp. with ÓIp ranging between 0·623 and 0·954. The length and the width of these prey items ranged respectively between 0·66–1·24 mm and between 020–0·39 mm (Tables 7 and 8). In the field, Clausocalanus sp. and P. parvus were the most abun-

T 5. Two-way analysis of variance on fullness index (logarithm) between GIR and FAC areas and the time of trawls

Source Area Time class Interaction Error Total

Degrees of Sum of Mean F freedom squares squares value 1 4 4 299 308

99·9 41·2 11 67·3 219·4

99·9 10·3 2·8 0·2

444 46 12

P(F) <0·001 <0·001 <0·001

(Levene test: F(9,299) =0·97 and P(F)=0·47).

dant copepods; however, their index of preponderance in anchovy stomachs are low regardless of the sample (Ip ranged between 0·000 and 0·032). The length of these two copepod species (mean values 1·23 and 1·03 mm respectively) were higher (Table 7) than that of Corycaeus sp. (not significantly) and Oncea sp.

186 S. Plounevez and G. Champalbert T 6. Index of preponderance of prey items in anchovy stomachs of each trawl in the GIR and FAC areas Area Time (U.T.) N fish Vacuity index (%) Copepoda Candacia armata Candacia sp. Acartia clausi Centropages chierchiae Clausocalanidae and Paracalanidae Euchaeta marina Calanus helgolandicus Pleuromamma gracilis Pleuromamma xiphias Anomalocera patersoni Temora longicornis Temora stylifera Clytemnestra sp. Euterpina acutifrons Microsetella rosea Oncea sp. Corycaeus sp. Oithona sp. Unidentified Copepoda Cladocera Penilia avirostris Evadne sp. Podon sp. Other Crustacea Unidentified Decapoda larvae Unidentified Euphausiacea larvae Unidentified Mysidacea larvae Amphipoda (juveniles) Miscellaneous Doliolidaea Chaetognatha Appendicularia (Oı¨kopleura sp.) Siphonophora Ostracoda Mollusca Polychaeta Echinodermata Clupeiod fish larvae Unidentified fish larvae Anchovy eggs Unidentified fish eggs

GIR area

FAC area

03:04 07:10 12:39 15:09 16:34 21:37 03:21 08:14 14:17 16:02 16:30 21:38 16 20 16 19 18 16 18 18 18 18 18 18 50 30 0 0 0 6 100 17 0 0 0 6

0·002

0·005 0·012 0·008 0·004 0·002

0·017 0·084 0·015 0·016 0·002 0·175 0·006 0·001 0·068 0·001 0·032 0·001

0·002 0·004 0·856 0·959 0·771 0·911 0·989 0·058 0·012 0·138 0·034 0·005

0·009

0·002 0·001

0·810 0·324 0·127 0·528 0·851 0·490 0·002 0·019 0·001 0·010 0·005 0·001 0·001 0·001 0·002 0·025 0·279 0·041 0·063 0·034 0·093 0·088 0·351 0·455 0·295 0·085 0·321 0·001 0·011 0·016 0·002 0·003 0·012

0·003 0·002

0·001 0·001

0·058 0·006 0·059 0·023 0·002

0·001 0·001 0·003 0·007 0·005 0·014 0·013 0·001

0·001 0·019 0·008 0·025 0·002 0·005 0·032 0·004 0·097 0·002 0·006 0·001

0·012 0·003 0·004 0·009 0·001

0·002 0·009

0·001

(significantly); moreover they were not significantly higher (Clausocalanus sp.) or not significantly smaller (P. parvus) than the length of T. longicornis. The width of P. parvus and Clausocalanus sp. (mean values 0·33 and 0·30 respectively) were higher than the width of Corycaeus sp. and Oncea sp. and significantly smaller than the width of T. longicornis (Table 8). The length and the width of Clausocalanus sp. and P. parvus were in the size range observed for the three dominant prey items.

Regardless of sampling hour, large crustacean larvae and anchovy eggs were not important prey items, in particular in the late afternoon and early night (Table 6). Fer a` Cheval area. In all samples of the FAC area, anchovy stomach contents only consisted of zooplankton with copepods as preponderant prey items (ÓIp ranged between 0·987 and 0·998) (Table 6). Centropages chierchiae was largely dominant (Ip ranged

Feeding behaviour and trophic environment of Engraulis encrasicolus 187 T 7. Bonferroni tests on length of dominant copepods in the field and/or in anchovy stomachs Copepod Centropages chierchiae Oithona helgolandicus Clausocalanus sp. Acartia clausi Temora longicornis Paracalanus parvus Corycaeus sp. Oithona nana Oncea sp.

Mean (mm)

Groupinga

1·636 1·292 1·234 1·180 1·148 1·032 0·928 0·784 0·656

A B B C B C D C D E E F F

a

Means with same letter were not significantly different (á=0·05) (ANOVA: F(8,36) =122·57 and P(F)<0·0001; Levene test: F(8,36) =1·07 and P(F)=0·40).

T 8. Bonferroni tests on width of dominant copepods in the field and/or in anchovy stomachs Copepod Centropages chierchiae Temora longicornis Clausocalanus sp. Paracalanus parvus Acartia clausi Oithona helgolandicus Corycaeus sp. Oncea sp. Oithona nana

Mean (mm)

Groupinga

0·432 0·388 0·332 0·296 0·284 0·252 0·236 0·212 0·184

A A B B C C D C D D E E

a

Means with same letter were not significantly different (á=0·05) (ANOVA: F(8,36) =81·66 and P(F)<0·0001; Levene test: F(8,36) =1·09 and P(F)=0·39).

between 0·771 and 0·989) whereas Clausocalanus sp. and P. parvus were fairly rare (fullness index ranging between 0·005–0·138). It must be noted that the length and the width of C. chierchiae (1·64 mm and 0·43 mm respectively) were significantly higher than those of other copepods abundant in the field such as Clausocalanus sp., P. parvus, Oithona helgolandica and Oithona nana. Discussion Hydrological and trophic conditions in the Bay of Biscay In the Bay of Biscay, the main factors which induce the circulation on the continental shelf are tidal currents (up to 30 m depth), freshwater outflow from the Loire and the Gironde rivers (density gradients induce geostrophic currents in surface layers and inverse currents near the bottom) and wind (Jegou & Lazure,

1995; Koutsikopoulos & Le Cann, 1996). A weak anticyclonic circulation becoming cyclonic near the continental slope prevails in the oceanic areas and slope-water oceanic type eddies are frequent (Pingree & Le Cann, 1992; Koutsikopoulos & Le Cann, 1996). In this study, the neritic area (GIR) was located in the plume of the Gironde River whereas the oceanic area (FAC) was not located in a particular hydrological structure such as eddies. In both areas, the water column showed a classical spring-like hydrological profile with a seasonal thermocline about 10–15 m deep, surface waters about 16·5 C and deeper waters about 12·5 C. During spring, together with the lengthening of the days, the inflow of nutrient-rich waters, in particular near the Gironde River’s mouth (monthly mean of the river flow ranging between 756 and 1406 m3s
1; Castel, 1993), induces an increase of the primary production on the continental shelf (Borja et al., 1996). In accordance with these common features, the chlorophyll profiles in the GIR area showed a peak located in the thermocline (with values ranging between 1 and 3·3 ìg 1
1) whereas in the FAC area, the chlorophyll values throughout the water column remained low (between 0·03 and 1·23 ìg 1
1), which could indicate a weak primary production. Published data show that the range of variations of zooplankton biomass during spring in neritic waters of the Bay of Biscay is wide: Castel and Courties (1982) reported values ranging between 14·2 and 525·5 mg m
3. Assuming a C mg dry weight ratio of 0·4 (Champalbert et al., 1973), and a C/biovolume ratio of 0·08 (Beers et al., 1975), the transformed data of Ferna´ndez et al. (1993) and Arbault and LacroixBoutin (1970) give a mean biomass equal to 5·2 mg m
3 and to 20–100 mg m
3 respectively. Thus, the mean values, between 34 and 65 mg m
3, are ranged within mean biomass for the area and the season. Moreover, the results showed that zooplankton biomass values were similar above and below the thermocline, which differs from Ferna´ndez et al.’s (1993) findings as they observed a vertical gradient of biomass. In the Gironde area where phytoplankton was relatively abundant in the water column, trophic conditions seem favourable for zooplankton, especially for herbivorous and omnivorous copepods which are able to move vertically. This could explain the absence of a clear biomass gradient from the surface to the bottom. In oceanic waters of the Bay of Biscay, quantitative studies on zooplankton are rare. In the surface layer the transformed values of biomass (conversion factors cited above) given by Arbault and Lacroix-Boutin (1970) range between 10 and 100 mg m
3 for the

188 S. Plounevez and G. Champalbert

upper 100 m and those of Ferna´ndez et al. (1993) equal to 25·3 mg m
3 for the upper 60 m. Moreover, as in neritic waters, Ferna´ndez et al. (1993) observed a vertical gradient. Accordingly, the results showed high zooplankton biomass above the thermocline in the oceanic area with a mean value around 35 mg m
3 whereas zooplankton biomass was seven times lower (5 mg m
3) below the thermocline. Below the thermocline, in particular below 60 m, phytoplankton densities decreased and trophic conditions were less favourable than above the thermocline, explaining low mesozooplanktonic biomass between the thermocline (15–40 m) and 200 m. Considering zooplankton specific composition, the results have shown that in both areas the group of copepods was largely dominant (up to 94% in most samples) above and below the thermocline which was also observed in the Bay of Biscay during spring (Castel & Courties, 1982; D’Elbe´e & Castel, 1991; Ferna´ndez et al., 1993; Ferna´ndez de Puelles et al., 1995). The study also showed that the most abundant copepods were Clausocalanus sp.-P. parvus (mean value ranging 58 and 5602 ind. m
3) which agrees with Colebrook (1982), D’Elbe´e & Castel (1991), Ferna´ndez et al. (1993) and Ferna´ndez de Puelles et al. (1995). Besides Clausocalanus sp.-P. parvus, specific differences were observed in neritic and in oceanic areas. In neritic waters off the north coast of Spain, A. clausi and Oithona sp. were abundant (Ferna´ndez et al., 1993; Ferna´ndez de Puelles et al., 1995). Along the French coast, in the channel of Arcachon Bay, the main species were Oncea sp., Corycaeus anglicus, Euterpina acutifrons, Oithona sp. and T. longicornis (Castel & Courties, 1982). Near Arcachon Bay, D’Elbe´e and Castel (1991) found the same species except for C. anglicus. In the Gironde area, our data have shown that, besides Clausocalanus sp.-P. parvus, the most abundant copepods were Oncea sp., T. longicornis, Corycaeus sp. and Oithona sp. In oceanic waters, Oithona sp. (Ferna´ndez et al., 1993) and Acartia clausi (Colebrook, 1982) were abundant while in the FAC area it was found that Oithona sp., C. chierchiae and A. clausi were abundant. Over the continental shelf off La Corun˜a, the size of 90% of the mesozooplankton was <1·5 mm and the size range of 70% of the mesozooplankton was between 0·7 mm and 1·1 mm (Valde´s et al., 1990; Poulet, 1996). The studies of Beaudouin (1975), D’Elbe´e & Castel (1991) and Ferna´ndez et al. (1993) also showed that copepods of small and medium size (Clausocalanidae, Paracalanidae, Acartidae, Corycaeidae, etc.) were dominant. In our

study, copepods smaller than 1·5 mm were also very numerous; nevertheless, larger copepods (>1·5 mm, essentially C. chierchiae) were more abundant in the FAC area than in the GIR area.

Anchovy feeding activity Studies on the daily feeding activity of the Northern anchovy (Baxter, 1967; Loukashkin, 1970), the Cape anchovy (Valde´s-Szeinfeld, 1993) and the European anchovy (Mikhman & Tomanovich, 1977; Bulgakova, 1992; Tudela & Palomera, 1995, 1997) show that these species are mainly daytime feeders. However, James (1987) and Bulgakova (1992) observed a dominant nocturnal feeding activity respectively of Engraulis capensis and Engraulis encrasicolus. Moreover, Mikhmann and Tomanovich (1977), Tudela and Palomera (1995, 1997) evidenced a peak of feeding activity at dusk and Bulgakova (1992), irregular peaks. The results on anchovies caught in the GIR and the FAC areas have demonstrated that feeding activity was continuous during the day; this activity went on in early night and ceased later. Any peak of feeding activity at a particular time of the day was not observed. It must be pointed out that, during the day, anchovies lived below the thermocline (Masse´, 1996) and our data have shown that below the thermocline zooplankton biomass was less abundant in FAC area than in GIR area. Nevertheless, an unexpected result was observed: the anchovy feeding activity was higher in the FAC area than in the GIR area.

Diet composition and feeding behaviour of adult anchovy Studies on the diet composition of different species of anchovy have shown that phytoplankton and zooplankton were found in anchovy stomachs (Loukashkin, 1970; Longhurst, 1971; King & Macleod, 1976; Mikhman & Tomanovich, 1977; James, 1987; Konchina, 1991; Bulgakova, 1993; Chiappa-Carrara & Gallardo-Gabello, 1993). These authors except King and Macleod (1976) found that zooplankton, especially copepods and crustacean larvae, were the dominant food. In the Catalan Sea, Tudela and Palomera (1997) observed that zooplankton, essentially made of copepods was the only food of E. encrasicolus and the presence of large preys like crustacean larvae in anchovy stomachs was irregular. This result agrees with ours; in the Bay of Biscay—copepods were the predominant prey. However, crustacean larvae were rare. That suggests prey active swimming and avoidance reactions.

Feeding behaviour and trophic environment of Engraulis encrasicolus 189

Visual zooplanktivorous fish exhibit a reaction distance depending on prey size (Confer & Blades, 1975; Wright & O’Brien, 1984). The selection of the food is based ‘ on its size, abundance, and edibility and the ease with which it is caught ’ (Brooks & Dodson, 1965). Therefore, a relatively abundant species, whose size is larger than that of other species is often the dominant prey (Brooks & Dodson, 1965; O’Brien et al., 1976; O’Brien, 1979; Spencer & King, 1984; Li et al., 1985; O’Brien, 1987). In the field, such a pattern of feeding behaviour was also observed in the Northern anchovy by Loukashkin (1970), Koslow (1981) and Chiappa-Carrara and Gallardo-Gabello (1993) and also in the Cape anchovy by James (1987). Moreover, studies performed in the laboratory on the feeding behaviour of E. mordax (Leong & O’Connell, 1969) and E. capensis (James & Findlay, 1989) have shown two patterns of behaviour which were a filter feeding mechanism on small prey and a raptorial feeding mechanism on larger prey. During the filter feeding, anchovy gave five to six tail-beats and their mouths remained open until the last tail-beat; then, the anchovy glided with their mouths closed. In the raptorial feeding mechanism, the anchovy mouth remained closed during tail-beats and was opened only during the glide to swallow whole prey. The swimming speed and the length of the glide were different during filtering and biting (Leong & O’Connell, 1969; James & Findlay, 1989). Our results in the FAC area clearly illustrate that anchovy efficiently preyed on fairly large copepods such as C. chierchiae when they were relatively abundant in the field. Thus, in this oceanic area, the feeding behaviour is probably raptorial feeding. In the GIR area, it seems more difficult to define the anchovy feeding mechanisms. A strong discrepancy was observed between zooplankton composition in the field and in the anchovy stomachs, suggesting a raptorial feeding on copepods of small-medium size (0·7–1·5 mm). Nevertheless, although zooplankton was abundant in the field, feeding activity was not particularly high. The ingestion of copepods <1·5 mm could be related to the low densities of large copepods (length >1·5 mm) in the field. It seems that the high density of copepods <1·5 mm in the water column could not activate a strong feeding activity of the anchovy. Moreover, turbidity in the river plume of the Gironde estuary (Hermida et al., 1998) could reduce the anchovy perception and the efficiency of this feeding mechanism. The difference in the density of large copepods and/or in the turbidity water between the GIR area and the FAC area would explain the lower feeding activity in the GIR area than in the FAC area.

Regardless of the area, Clausocalanus sp.-P. parvus (medium-small size) were dominant in the field and rarely abundant in the stomachs; nevertheless their sizes were greater than the size of Oncea sp. and Corycaeus sp. which were relatively important prey items, which suggests that prey size is not the only criterion of selection. Considering the relationship between mesozooplankton prey and fish predators, the risk of predation depends on the swimming speed and behaviour of the prey. According to the observations of Eggers (1977) and Brewer and Coughlin (1995), the risk of being attacked increases in fastswimming prey; in the same way, Wright and O’Brien (1984) observed an increased risk to be attacked in regularly swimming prey. Predation also depends on prey shape and colour; the darkest prey (such as cladocerans with ephippia) are more readily eaten than the translucent prey such as cladocerans without ephippia (Merret & Roe, 1974; Mellors, 1975; Hobaek & Wolf, 1991). These two factors are often taken into account in prey–predator models (Eggers, 1977; Wright & O’Brien, 1984; Aksnes & Giske, 1993; Giske et al., 1994; Brewer & Coughlin, 1995). Considering the inter- and intraspecific differences observed in the swimming behaviour patterns and colours of copepods (Lowndes, 1935; Strickler, 1977; Hairston, 1980; Kerfoot et al., 1980; Hairston, 1981; Lochhead, 1962), it can be assumed that a combination of Clausocalanus sp. and P. parvus behaviour and pale colour tend to reduce their susceptibility to predation by anchovy in the Bay of Biscay.

Conclusions The present study shows that adult anchovy feed all through the day and probably in early night. Our observations also show that there is no clear relationship between anchovy level of feeding activity and zooplankton biomass but they suggest a relation between anchovy feeding activity and zooplankton composition. In oceanic areas, with low zooplankton biomass below the thermocline and a relatively high density of large copepods, feeding activity is efficient; in this area anchovy migration seems necessary to maintain feeding activity. Conversely, in neritic areas, characterized by high zooplankton biomass below the thermocline and low numbers of large copepods, the feeding activity is little and of low efficiency. The feeding activity of adults certainly plays a part in their spatial distribution in the Bay of Biscay. The dispersion of anchovy shoals at the end of the spawning season as noted in the Gironde area (Motos et al., 1996) could

190 S. Plounevez and G. Champalbert

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