© 2004 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
Contrasting years in the Gironde estuary (Bay of Biscay, NE Atlantic) springtime outflow and consequences for zooplankton pyruvate kinase activity and the nutritional condition of anchovy larvae: an early view
Laboratoire Ecologie Halieutique, Direction des Ressources Vivantes, IFREMER, Centre de Nantes BP 21105, F-44311 Nantes Cedex 03, France
*Correspondence to J-P. Bergeron: tel: 33 2 40374162; fax: 33 2 40374075. e-mail: jean.Pierre.Bergeron{at}ifremer.fr.
A major spawning ground of the European anchovy (Engraulis encrasicolus) population in the Bay of Biscay is located near the mouth of the Gironde estuary. Variations in the river discharge affect the supply of nutrients to the coastal marine area encompassing anchovy spawning grounds. Two "Pegase" cruises (May–June 1997 and 1998) observed two contrasting situations: with and without a superficial layer of less saline water. Two new nutritional indices were used to assess potential effects (1) on carbohydrate assimilation rates by zooplankton estimated via pyruvate kinase (PK) activity measurements and (2) on nutritional condition of the anchovy larvae measured with the DNA/C index. Both indices indicated a much poorer situation in 1997 compared to 1998. Results of this study implicate river outflow rate as a potential factor influencing larval anchovy condition and perhaps to some extent recruitment variability.
Keywords: anchovy larvae, Bay of Biscay, DNA/C index, pyruvate kinase, river outflow
Received 30 May 2003; accepted 15 June 2004.
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Introduction |
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Unlike other species of anchovy living in different parts of the world's oceans, the population dynamics of the European anchovy (Engraulis encrasicolus) do not appear to be controlled predominantly by a major physical process, such as the strength and extent of upwelling along western coasts of continents (E. mordax in California, E. ringens in Peru, E. encrasicolus, previously known as E. capensis, in Namibia and South Africa). The spawning region of the stock exploited in the Bay of Biscay (NE Atlantic) by the French and Spanish fleets is subject to many extrinsic drivers. It is a patchwork of different systems including: (1) coastal systems influenced either by river plumes or local upwellings caused by special wind regimes and (2) "oceanic" systems along the shelf break where deep water may be upwelled or large eddies may form. Run-off from large rivers such as the Gironde (Figure 1) may particularly influence the supply of nutrients to these coastal and oceanic systems. Moreover, large interannual fluctuations occur in the discharge rates.
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In 1997 and 1998, two Pegase ("Pélagiques Gascogne") cruises were carried out between May and June on the RV "Thalassa". These cruises coincided with a period of low (1997) and high (1998) river discharge. During these cruises, estimates of carbohydrate (essentially synthesized by primary producers) assimilation rates by mesozooplankton were obtained via pyruvate kinase (PK) activity analysis (Bergeron and Herbland, 2001) and estimates of individual larval anchovy nutritional condition were made using the DNA/C index (Bergeron et al., 1991, 1997). Results of an early field application were recently presented by Bergeron (2000). This paper examines if the potential effects of different rates of river discharge could be assessed using these two new nutritional indices.
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Material and methods |
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Portions of the Pegase 97 (24–26 May) and 98 (10–13 June) cruises were devoted to sampling sites near the mouth of the Gironde in the estuarine plume (Figure 1).
At each fixed station
- – temperature and salinity vertical variations were recorded with a CTD (Sea Bird SBE 19);
- – water samples were collected with five Niskin bottles at standard depths (0, 10, 20, 30 and 40 m) in order to estimate nutrient concentrations: immediately frozen at –30°C, these samples were thereafter entrusted to collaborators (see "Acknowledgements" section) for later analysis in laboratory, following the methods of Strickland and Parsons (1972);
- – a mesozooplankton sample was collected by a 1-knot vertical tow of a WP2 net (200-µm mesh size) from bottom to surface, following two similar (or, at least, centred on the same geographic point, i.e. 45°30'N and 1°30'W) grids of stations (15 in 1997, 10 in 1998; cf. Figure 1).
- – water samples were collected with five Niskin bottles at standard depths (0, 10, 20, 30 and 40 m) in order to estimate nutrient concentrations: immediately frozen at –30°C, these samples were thereafter entrusted to collaborators (see "Acknowledgements" section) for later analysis in laboratory, following the methods of Strickland and Parsons (1972);
Sieving the samples through 5-mm mesh eliminated macrozooplankton. The samples were ground in iced distilled water with a Polytron and immediately frozen in liquid nitrogen; they were thereafter stored at –90°C until analysis in the laboratory. After thawing, the crude extract was homogenized with a Potter-Elvehjem and centrifuged (10 min at 4000 rev min–1, 3°C). An aliquot of 200 µl of the supernatant fluid was used for enzyme assay or protein determination. Pyruvate kinase (PK) activity was estimated according to the method of Bucher and Pfleiderer (1955), under the conditions specified by Bergeron and Herbland (2001). Protein (for determination of specific activities) was estimated by the method of Lowry et al. (1951) with bovine serum albumin as standard.
Between fixed stations, anchovy larvae were collected using double oblique, 2-knot tows between bottom and surface with a "carré net" (1-m2 mouth opening; 380-µm mesh size). Collected larvae had to be shared for different purposes, especially otolith-based age and growth rate determination. Larvae for DNA/C estimates were taken from three samples in 1997, from four samples in 1998 and, owing to their greater sensitivity to environmental trophic conditions (Bergeron, 2000), only individuals (4.9–9.7 mm long) at development stages earlier than the notochord flexion one were selected. They were quickly sorted, frozen at –40°C, and subsequently stored at –30°C. In the laboratory, larvae were thawed and individually ground in varying volumes (0.8–2.4 ml according to size) of cold distilled water (4°C) with a Potter-Elvehjem homogenizer. An aliquot was rapidly placed in a tin capsule for carbon analysis and the remaining sample was immediately processed for DNA determination by a fluorimetric method (Le Pecq and Paoletti, 1966) modified according to Karsten and Wollenberger (1972, 1977). Type I DNA (Sigma) from calf thymus was used as the standard. The sample for carbon determination was dried (60°C) in an oven and then processed in a Perkin–Elmer CHNS/O 2400 analyzer. It must be remembered that a low DNA/C index characterizes a good nutritional state (Bergeron et al., 1991, 1997) and vice versa: Bergeron (2000) defined 60 µg DNA mg C–1 as the upper value of the threshold at which anchovy larvae are in good condition.
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Results |
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The seasonal variations of Gironde flow rates show strong interannual differences (Figure 2). The general pattern observed in 1997 was classical for temperate regions: after winter peaks, a long decreasing trend characterized the springtime period. However, in 1998, the pattern was different and high flow rates were measured in late April and May (Figure 2). As a consequence, the vertical hydrological structure of the study area showed very different aspects from one year to the other (Figure 3). Quite unlike 1997, when the lowest surface salinities were >34.9, the 1998 surface salinities implied an intrusion of less saline water. This less saline water contained elevated concentrations of NO3 (from 1 to 4 µM) compared to more saline surface waters in 1997 (NO3 = "undetected" to 0.1 µM). Nutritional indices for zooplankton (PK specific activity) and larval anchovy (DNA/C) were greatly enhanced in 1998 compared to 1997 (Table 1). In the latter year, these indices were quite poorer (differences are highly significant: t-test indicates p < 0.001 for PK specific activity mean values and even below for DNA/C index values).
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Discussion |
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Nutritional condition of larval fish is considered an important factor affecting recruitment fluctuations of the population, either directly by inducing mortality or indirectly by lengthening the duration of larval life and exposure to predators. In a previous study (Bergeron, 2000), larval anchovy DNA/C index in the Bay of Biscay indicated that good nutritional condition was only detected along the shelf break or in the river plume (ERAG 93 cruise, June 1993). In 1993, the Gironde run-off was not characterized by peaks of the same magnitude as in 1998, but a brief peak occurred at the beginning of May (over 3 x 103 m3 s–1) proceeded by rates which were 2x greater than normal (oscillating around 103 m3 s–1). During this period in 1993, larval nutritional condition was also better (mean DNA/C = 54; s.d. = 6).
The anchovy population in the Bay of Biscay spawns in two main areas, one located near the shelf break and one in the Gironde plume (Motos et al., 1996). The enrichment of the shelf break environment is controlled by large scale oceanic physical processes (New and Pingree, 1990; Laborde et al., 1999): tidally induced internal waves are very energetic in the Bay of Biscay; it is particularly manifested near the Armorican shelf in the North (e.g. around 47°–48°N according to Langlois et al., 1990) and they are still strong enough in the more southern part of the region (around 45°N), where spawning of anchovies occurs, to induce notable enrichment in nutrients (Pichon and Correard, in press). Moreover, the superficial fertilization of this area is reinforced by strong instabilities of the poleward slope current linked to bathymetric anomalies such as canyons, notably in the present case the "canyon du Cap Ferret" (X. Carton, Laboratoire de Physique des Oceans, IFREMER, Brest, pers. comm.). It is obvious that these physical processes are potentially less interannually variable than rates of the Gironde run-off. The latter is dependent on variable climate conditions, which may be from year to year notably different for a given season, over the southwestern part of the French territory, while the former is driven by larger-scale, more stable and reproducible physical processes. Therefore it may be hypothesized that a considerable fraction of the anchovy population spawns in an environment which is sometimes unfavourable for larval feeding and survival (e.g. 1997). The early stages of larval life of fishes are recognized to be especially delicate (Hewit et al., 1985; Heath, 1992) and their survival is still considered by many authors as a strong determinant of the annual recruitment level. Consequently, variation in the rate of Gironde outflow might be likely to play a role in the recruitment variability of anchovy. This, if confirmed by future studies, should be taken into account for forecasts of this fishery, possibly being incorporated into predictive models such as those in course of development (Allain et al., 2001).
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Acknowledgements |
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I am greatly indebted to several colleagues: P. Bourriau, P. Grellier, D. Halgand for field sampling and larvae sorting; N. Schreiber for biochemical analyses; C. Dejouy for drawing figures; B. Planque for hydrological data processing and carrying out salinity sections. Nutrient data were kind communications from P. Morin (Université de Bretagne Occidentale, Brest) and C. Labry (Université du Littoral de Côte d'Opale, Wimereux; new and present address: IFREMER, Centre de Brest) for 1997 and 1998, respectively. Thanks are also due to J. Massé, Manager of the IFREMER Project "Ecologie des Petits Pélagiques" and to Captain, officers and crew of the RV "Thalassa". Constructive comments and criticisms of two anonymous reviewers were much appreciated for the improvement of an early version of the manuscript. This study was carried out within the framework of the "Programme National sur le Déterminisme du Recrutement", a French contribution to the GLOBEC International Programme.
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References |
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TopIntroductionMaterial and methodsResultsDiscussionReferences |
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Allain G., Petitgas P., Lazure P. (2001) The influence of mesoscale ocean processes on anchovy (Engraulis encrasicolus) recruitment in the Bay of Biscay estimated with a three-dimensional hydrodynamic model. Fisheries Oceanography 10:151–163.[CrossRef][Web of Science]
Bergeron J.P. (2000) Effect of strong winds on the nutritional condition of anchovy (Engraulis encrasicolus L.) larvae in the Bay of Biscay, Northeast Atlantic, as inferred from an early application of the DNA/C index. ICES Journal of Marine Science 57:249–255.
Bergeron J.P., Boulhic M., Galois R. (1991) Effet de la privation de nourriture sur la teneur en ADN de la larve de sole (Solea solea L.). ICES Journal of Marine Science 48:127–134.
Bergeron J.P. and Herbland A. (2001) Pyruvate kinase activity as index of carbohydrate assimilation by mesozooplankton: an early field implementation in the Bay of Biscay, NE Atlantic. Journal of Plankton Research 23:157–163.
Bergeron J.P., Person-Le Ruyet J., Koutsikopoulos C. (1997) Use of carbon rather than dry weight to assess the DNA content and nutritional condition index of sole larvae. ICES Journal of Marine Science 54:148–151.
Bucher T. and Pfleiderer G. (1955) Pyruvate kinase from muscle. In Colowick S.P. and Kaplan N.O. (Eds.). Methods in Enzymology(Academic Press, London) vol. 1: pp. 435–440.[CrossRef][Web of Science]
Heath M.R. (1992) Field investigations of the early life stages of marine fish. Advances in Marine Biology 28:2–174.
Hewit R.P., Theilacker G.H., Lo N.C.H. (1985) Causes of mortality in young jack mackerel. Marine Ecology Progress Series 26:1–10.[Web of Science]
Karsten U. and Wollenberger A. (1972) Determination of DNA and RNA in homogenized cells and tissues by surface fluorometry. Analytical Biochemistry 46:135–148.[CrossRef][Web of Science][Medline]
Karsten U. and Wollenberger A. (1977) Improvements in the ethidium bromide method for direct fluorometric estimation of DNA and RNA in cell and tissue homogenates. Analytical Biochemistry 77:464–470.[CrossRef][Web of Science][Medline]
Laborde P., Urrutia J., Valencia V. (1999) Seasonal variability of primary production in the Cap-Ferret Canyon area (Bay of Biscay) during the ECOFER cruises. Deep-Sea Research II 46:2057–2079.[CrossRef]
Langlois G., Gohin F., Serpette A. (1990) Refroidissements locaux aux abords du talus continental Armoricain. Oceanologica Acta 13:159–169.[Web of Science]
Le Pecq J.B. and Paoletti C. (1966) A new fluorometric method for RNA and DNA determination. Analytical Biochemistry 17:100–107.[CrossRef][Web of Science][Medline]
Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. (1951) Protein measurement with Folin-phenol reagent. Journal of Biological Chemistry 193:265–275.
Motos L., Uriarte A., Valencia V. (1996) The spawning environment of the Bay of Biscay anchovy (Engraulis encrasicolus L.). Scientia Marina 60:Supplement 2, 117–140.
New A.L. and Pingree R.D. (1990) Evidence for internal tidal mixing near the shelf break in the Bay of Biscay. Deep-Sea Research 37:1783–1803.
Pichon A. and Correard S. M. (2004) Internal tides modelling in the Bay of Biscay. Comparisons with observations. Oceanologica Acta, in press.
Schlitzer R. (2001) Ocean Data View http://www.awi-bremerhaven.de/GEO/ODV.
Strickland J.D.H. and Parsons T.R. (1972) A Practical Handbook of Seawater Analysis. Bulletin of the Fisheries Research Board of Canada 2nd edn 167: 310 pp.
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