# Metabolism of the coastal ocean, from the local scale (Scheldt estuary, Randers Fjord and Palma bay) to the European scale

Frédéric Gazeau

► To cite this version:

Frédéric Gazeau. Metabolism of the coastal ocean, from the local scale (Scheldt estuary, Randers Fjord and Palma bay) to the European scale. Environmental Sciences. Université Pierre & Marie Curie - Paris 6; Université de Liège, 2004. English. NNT: 2004PA066130. tel-03957452

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# Métabolisme des écosystèmes côtiers :
de l'échelle locale (fjord de Randers,
baie de Palma et estuaire de l'Escaut) à
l'échelle européenne

Thèse présentée par:

Frédéric Gazeau

en vue de l'obtention
du grade de docteur en Sciences
2004

Travaux co-dirigés par
Jean-Pierre Gattuso et Michel Frankignoulle

**Jury:**

Borges A. V., Chargé de recherche au FNRS

Bouquegneau J.-M., Prof. Univ. Liège

Clavier J., Prof. Univ. Brest

Frankignoulle M., Maître de recherche au FNRS

Gattuso J.-P., Directeur de recherche au CNRS

Middelburg J. J., Chercheur au NIOO, Pays-Bas, rapporteur

Nival P., Prof. Univ. Pierre et Marie Curie

Pinay, G., Directeur de recherche au CNRS, rapporteur
<figure><img src="image_2.png" /></figure>
# Métabolisme des écosystèmes côtiers :
de l'échelle locale (fjord de Randers,
baie de Palma et estuaire de l'Escaut) à
l'échelle européenne

Thèse présentée par:

Frédéric Gazeau

en vue de l'obtention
du grade de docteur en Sciences
2004

Travaux co-dirigés par
Jean-Pierre Gattuso et Michel Frankignoulle

## Jury:

- Borges A. V., Chargé de recherche au FNRS

- Bouquegneau J.-M., Prof. Univ. Liège

- Clavier J., Prof. Univ. Brest

- Frankignoulle M., Maître de recherche au FNRS

- Gattuso J.-P., Directeur de recherche au CNRS

- Middelburg J. J., Chercheur au NIOO, Pays-Bas, rapporteur

- Nival P., Prof. Univ. Pierre et Marie Curie

- Pinay, G., Directeur de recherche au CNRS, rapporteur
Remerciements

Je tiens tout d'abord à remercier le Professeur Jean-Marie Beckers de m'avoir accueilli au sein du GHER (GeoHydrodynamics and Environment Research) ainsi que le Professeur Louis Legendre de m'avoir accueilli au sein du LOV (Laboratoire d'Océanographie de Villefranche). Je remercie tout particulièrement Jean-Pierre Gattuso et Michel Frankignoulle pour m'avoir encadré, soutenu, motivé durant ces trois années. Leur aide m'a été très précieuse et leur bonne humeur m'a permis de mener ce travail à terme dans des conditions idéales.

Merci à Alberto Borges, Bruno Delille et Laure-Sophie Schiettecatte, la dream-team Liégeoise de m'avoir supporté, aidé et fait rigoler depuis deux ans. C'était un plaisir de travailler avec vous, j'espère et je pense que notre collaboration n'en restera pas là! Un grand merci également à Emma Rochelle-Newal, Natalia Gonzales, Marie-Dominique Pizay, Osana Bonilla-Findji, Marine Fioroni, Isabelle Courtois, Olivier Calmels pour les bons moments passés à Villefranche et ailleurs.

Je tiens évidemment à remercier toutes les personnes avec qui j'ai travaillé et qui m'ont fait partager leur savoir: J. J. Middelburg, S. V. Smith, R. Wollast, J. -P. Vanderborght, C. M. Duarte, M. Loijens, L. Chou, K. Soetaert, M. Andersson, N. Brion, F. Ronday.

Un grand merci également aux équipages des différents bateaux sur lesquels j'ai effectué mes missions: le Théthys, le Mytilus, le Belgica et le Luctor.

Evidemment dans tout ça, je ne peux oublier les potes et potesses de Villefranche, de Liège ou d'ailleurs: Kosso, Caro, Bobo, les frifris, les pousses, la blondouille, les boscos, Torvick, Francis, Diane, Aurélie, les squasheurs fous d'Antibes et de Liège, Cécile l'ardennaise, Nat et Denis, Rado, Yves, François, Julia, Delphine, Matthieu, Titi, Tételle, Flo, Yann, Florent, Patrice, Dom, Agnès, Flav, Lies, Elise, Lolo, Papy etc etc....

Mes dernières pensées (pour le moment...) vont à ma famille et à mes parents en particulier qui au lieu de me dire :"Bon quand est-ce que tu vas commencer à gagner ta vie?" m'ont toujours soutenu pendant ces 7, non 8 euh, 10 années d'études. Sans votre aide, je n'y serais jamais arrivé. Mille mercis encore.
Résumé

L'océan côtier, la zone de transition entre le continent et l'océan ouvert, reçoit des apports considérables d'eau douce, de sels nutritifs ainsi que de matière organique dissoute et particulaire en provenance du continent. Ces apports font que la zone côtière est une région très active du point de vue biogéochimique. Le statut trophique de l'océan côtier, distinction entre l'autotrophie et l'hétérotrophie) est un sujet encore très discuté. L'étude présentée ici a trois objectifs: (1) de compiler et analyser une base de données bibliographique concernant la production primaire brute (GPP) et la respiration communautaire (CR) benthiques et planctoniques, mesurées par des incubations et par l'approche budgétaire Land-Ocean Interaction in the Coastal Zone (LOICZ) au niveau de la zone côtière européenne. (2) de tester différentes méthodes d'estimation du métabolisme de trois sites côtiers européens. Ces méthodes sont la méthode classique d'incubations O₂, la méthode LOICZ et d'autres méthodes en système ouvert telles que la méthode Response Surface Difference (RSD) et l'utilisation de cycles journaliers de carbone inorganique dissous et d'O₂. De plus, étant donné que l'estimation du coefficient d'échange de gaz à l'interface air-mer (k) est critique lors de l'utilisation de méthodes en système ouvert, ce paramètre et sa relation avec la vitesse du vent ont été étudiés dans deux des sites (Fjord de Randers et estuaire de l'Escaut). (3) d'étudier la relation existant entre les paramètres métaboliques tels que GPP ou CR dans les compartiments benthiques et planctoniques.

Plus de 190 publications ont été analysées dont 129 ont été intégrées à une base de données consultable sur Internet (http://www obs vlfr fr/eurotroph /index php). L'analyse de cette base de données a permis de mettre en avant un sévère manque mesures dans de nombreuses régions telles que le bassin Est de la mer Méditerranée, le nord de la Baltique et le nord de la mer du Nord. Une estimation de la production nette (NEP = GPP+ CR) de la zone côtière européenne n'a pas été possible dans cette étude. En effet, des estimations fiables de paramètres tels que la minéralisation de matière organique dans la colonne d'eau, la diminution de la production et respiration benthique avec la profondeur et la distribution des macrophytes, font cruellement défaut.

Les différentes méthodes testées ont fourni des résultats le plus souvent similaires, bien que chacune d'elles soit associée à une marge d'erreur significative qui limite son utilisation à des sites et conditions bien particuliers. La méthode LOICZ basée sur le phosphore inorganique dissous (DIP) n'a pu fournir un résultat réaliste dans l'estuaire de l'Escaut. Ceci est dû à un fort impact de processus abiotiques sur le flux non-conservatif de DIP, tels que l'adsorption/désorption sur ou à partir de particules en suspension et/ou du sédiment, dans ce système très turbide. Les méthodes en milieu ouvert souffrent de la difficulté d'estimer de façon fiable le coefficient d'échange de gaz à l'interface air-mer (O₂ ou CO₂). Bien qu'il ait été montré que la relation liant ce paramètre à la vitesse du vent dépendait du site étudié, la relation établie pour l'estuaire de l'Escaut n'a pu être validée en utilisant la méthode LOICZ appliquée au DIC en raison des fortes erreurs associées. Finalement, les différences significatives observées entre les estimations de GPP et CR à partir des incubations et des méthodes en système ouvert confirment les résultats de travaux antérieurs et mériteraient une attention particulière à l'avenir.

Les trois sites étudiés sont bien contrastés: du turbide et eutrophisé estuaire de l'Escaut à la baie oligotrophe dominée par les macrophyte (Palma). De relations significatives entre les paramètres métaboliques et les conditions environnementales ont été montrées. En effet, les plus fortes CR ont été mesurées dans l'Escaut tandis que la GPP y était très sévèrement limitée par la disponibilité en lumière. Les plus fortes GPP ont été mesurées dans le fjord de Randers où les concentrations en sels nutritifs ainsi que la stratification de la colonne d'eau et la faible turbidité permettent au phytoplancton en provenance de la rivière de continuer à produire dans la zone estuarienne. Tandis que l'estuaire de l'Escaut est clairement le site le plus hétérotrophe, il a été impossible de différencier les métabolismes de la baie de Palma et du fjord de Randers sur une échelle annuelle.
Abstract

The coastal zone, the transition area between land and the open ocean, receives considerable amounts of freshwater, nutrients as well as dissolved and particulate organic matter. These inputs make the coastal zone a very biogeochemically active area. The trophic status of the coastal zone, that is whether it is autotrophic or heterotrophic, is still a matter of debate. The present work had three main objectives: (1) to compile and analyse a bibliographic database of benthic and planktonic primary production (GPP) and community respiration (CR) measured by incubation methods and by the Land-Ocean Interaction in the Coastal Zone (LOICZ) budgeting approach in the European coastal zone, (2) to test different methods to estimate the functioning of three European coastal sites (Randers Fjord, Palma Bay and Scheldt Estuary). These methods are the classical O₂ incubation technique, the LOICZ budgeting procedure and other open-system techniques such as the Response Surface Difference (RSD) method and daily cycles of dissolved inorganic carbon (DIC) and O₂. Moreover, as the estimation of the gas exchange coefficient at the air-sea interface (k) is critical when applying open-system methods, this parameter and its relationship with wind speed were studied in two of the sites (Randers Fjord and Scheldt estuary) and (3) to study how the metabolic parameters such as GPP or CR both in the benthic and planktonic compartment are controlled by environmental conditions.

More than 190 papers have been analysed among which 129 were integrated in a database available on the Internet (http://www obs-vlfr.fr/eurotroph/index.php). The analysis of the bibliographic database allowed pinpointing a severe lack of knowledge in many areas of Europe such as the Eastern Mediterranean Sea, the Northern Baltic Sea and the Northern North Sea. An assessment of the net ecosystem production (NEP = GPP + CR) of the European coastal zone was not possible based on this study. Indeed, several confident estimates of parameters such as the mineralization of organic matter in the water column, the decrease of benthic production and respiration with depth and the distribution of macrophytes are lacking.

The different methods tested during this study generally provided consistent results although each of these is associated with significant errors and uncertainties which limit their use to specific sites and conditions. Particularly, the LOICZ procedure applied to dissolved inorganic phosphorus (DIP) failed to provide a realistic estimate of the trophic status in the Scheldt estuary. This is due to a strong impact of abiotic processes such a sorption and desorption to and from suspended matter and sediments on the non-conservative DIP flux in this highly turbid system. Open-system methods suffer from the difficulty to estimate with accuracy the gas exchange coefficient. Although the relation linking this parameter to the wind speed was shown to be site-specific, the validation of this relationship in the Scheldt estuary using the LOICZ approach applied to DIC was not possible due to strong associated errors and uncertainties. Finally, significant differences observed between GPP and CR estimated by incubation and open-system methods confirmed previous results and suggest that future works should focus on this matter.

The three sites investigated were well contrasted: from the nutrient-rich and turbid Scheldt estuary to the oligotrophic seagrass-dominated Bay of Palma. The metabolic parameters were well related to these environmental differences. Indeed, the highest CR rates were measured in the Scheldt estuary while GPP was strongly limited by light availability. The highest GPP was measured in the Randers Fjord where nutrient concentrations as well as water column stratification and a relatively low turbidity allowed the riverine phytoplankton to remain very active in the estuarine zone. While the Scheldt estuary was clearly the most heterotrophic site in this study, it was not possible to conclude whether the Randers Fjord or the Bay of Palma is the most productive ecosystem on an annual scale.
# Plan

## Remerciements

## Résumé - Abstract

<table><tr><td>Chapitre 1. Introduction</td><td>1</td></tr><tr><td>Chapitre 2. L'échelle Européenne</td><td>19</td></tr><tr><td>Chapitre 3. L'échelle locale</td><td>38</td></tr><tr><td>3.1. La baie de Palma</td><td>38</td></tr><tr><td>3.2. Coefficient d'échange dans les estuaires</td><td>90</td></tr><tr><td>3.3. Le fjord de Randers</td><td>101</td></tr><tr><td>3.4. L'estuaire de l'Escaut</td><td>142</td></tr><tr><td>Chapitre 4. Synthèse</td><td>178</td></tr><tr><td>4.1. Le statut métabolique de la zone côtière européenne</td><td>178</td></tr><tr><td>4.2. Echelle locale: comparaison des trois sites d'étude</td><td>183</td></tr><tr><td>4.3. Les méthodes d'estimation du statut trophique en zone côtière</td><td>197</td></tr><tr><td>Chapitre 5. Conclusions et perspectives</td><td>204</td></tr><tr><td>Bibliographie</td><td>206</td></tr></table>
# Chapitre 1

## Introduction
L'émission de dioxyde de carbone (CO₂) par les activités humaines (utilisation de combustibles fossiles et déforestation) est à l'heure actuelle (année 2000) de 725 Tmol C an⁻¹ (Sources: Houghton & Hackler 2002 ; Marland et al. 2003). Pour une émission de 525 Tmol C an⁻¹ dans les années 1990, l'augmentation observée de la concentration en CO₂ dans l'atmosphère n'était "que" de 270 Tmol C an⁻¹ (IPCC 2001). Cette différence est due à la capacité des autres réservoirs actifs au niveau du cycle du carbone à puiser une partie des émissions d'origine anthropique, à savoir le réservoir océanique et le réservoir terrestre.

La Terre contient environ 83 x 10⁶ Tmol C, dont 3.3 x 10³ Tmol C dans les réservoirs actifs près de sa surface et environ 0.3 x 10³ Tmol C dans les combustibles fossiles (Schlesinger 1997). Parmi ces réservoirs actifs, l'océan est de très loin le plus important site de stockage du carbone et contient environ 3.2 x 10³ Tmol C (soit environ 95% du total).

La biosphère (terrestre et océanique) possède la capacité de puiser le CO₂ pour créer de la matière organique à partir de la photosynthèse (dépendante de l'énergie lumineuse). Bien que d'autres processus de production primaire non dépendant de la lumière existent (chémoautotrophie), ceux-ci sont négligeables à l'échelle globale. Cette assimilation de CO₂ s'accompagne d'une production d'oxygène (O₂) selon la réaction simplifiée:

$$CO_2 + H_2O \rightarrow CH_2O + O_2 \quad (1)$$

Tous les organismes vivants ont besoin de matière organique d'une part pour produire leurs propres tissus et d'autre part pour satisfaire leurs besoins énergétiques (respiration) selon la réaction inverse de l'équation (1). Ce processus de reminéralisation de la matière organique s'accompagne donc de la consommation d'O₂ et de la production de CO₂.

Nous devons dans un premier temps définir quelques termes qui seront employés dans la suite du texte:

(1) la production primaire brute (gross primary production: GPP) est le taux de production de matière organique par les organismes autotrophes (i.e. capables de synthétiser par eux-mêmes les matières organiques qui les composent à partir d'éléments minéraux et d'énergie lumineuse).

(2) La production primaire nette (net primary production: NPP) est le taux de production de matière organique par les organismes autotrophes après oxydation (respiration) des composés nécessaires à combler leurs besoins énergétiques.

$$NPP = GPP + R_a$$
Où R_a est le taux de respiration des organismes autotrophes (exprimée en valeur négative). Contrairement à GPP, NPP peut être négative si |R_a| > GPP.

(3) La respiration communautaire (community respiration: CR) est la minéralisation de matière organique par tous les organismes de la communauté, qu'ils soient autotrophes ou hétérotrophes.

$$CR = R_a + R_h$$

Où R_h est le taux de respiration des organismes hétérotrophes (exprimée en valeur négative).

(4) La production communautaire nette (net community production: NCP) est le taux de production de matière organique après consommation de celle-ci par tous les organismes du système considéré (autotrophes + hétérotrophes). Un organisme hétérotrophe ne peut tirer son énergie que de la décomposition de matière organique préexistante.

$$NCP = GPP + CR$$

Le terme production nette de l'écosystème (net ecosystem production: NEP) sera souvent utilisé par la suite. Il s'agit de la somme des NCP de toutes les communautés (compartiment planctonique, microphytobenthos, macrophytes...) constituant un écosystème.

Une communauté ou un écosystème est dit autotrophe (NCP ou NEP > 0) lorsque GPP > |CR|. La production de matière organique en surplus est soit stockée, soit exportée vers les communautés ou les écosystèmes adjacents. Ce type de fonctionnement implique généralement une production nette d'O_2 et une consommation nette de CO_2. Ce processus a été appelé la pompe biologique. Ce n'est toutefois pas toujours le cas. En effet, les upwellings et les estuaires peuvent être autotrophes et pourtant des sources de CO_2 pour l'atmosphère, lorsqu'ils reçoivent des apports d'eaux riches en CO_2 (eaux profondes pour les upwellings et eaux continentales pour les estuaires). De plus, des effets strictement thermodynamiques peuvent modifier la pression partielle en CO_2 (pCO_2) tels ceux liés à des variations de température ou au mélange de masses d'eau de caractéristiques chimiques contrastées.
Une communauté ou un écosystème est dit hétérotrophe (NCP ou NEP < 0) lorsque GPP < |CR|. Ces systèmes ont besoin d'un apport externe de matière organique (matière allochtone) pour se maintenir et sont des sources de CO₂ atmosphérique avec la même remarque que ci-dessus à savoir que la direction du flux dépend de la valeur de pCO₂ initiale.

Bien que sujette à une grande incertitude, la NPP terrestre a été estimée à environ 4500-5000 Tmol C an⁻¹ à partir de mesures *in situ* (Saugier & Roy 2001 in IPCC 2001) et à partir de données de télédétection et de CO₂ atmosphérique (Ruimy *et al.* 1994 ; Knorr & Heimann 1995 in IPCC 2001 ; Field *et al.* 1998). Le réservoir terrestre serait autotrophe dans sa globalité et sa capacité à puiser le CO₂ atmosphérique a été estimée à 17 et 117 Tmol C an⁻¹ dans les années 1980 et 1990, respectivement (IPCC 2001).

La capacité des océans à puiser le CO₂ atmosphérique a été estimée à 142 ± 42 Tmol C an⁻¹ dans les années 90 (IPCC 2001), basée sur des mesures de pCO₂ (Takahashi 2002) et d'O₂ (Keeling & Shertz 1992 ; Bender *et al.* 1998), des modèles de circulation globale calibrés sur la distribution du ¹⁴C (Sarmiento *et al.* 1992 ; Murnane *et al.* 1997), des mesures isotopiques (C¹³) atmosphériques et océaniques (Quay *et al.* 1992) et des mesures atmosphériques de O₂/N (Battle *et al.* 2000). Il convient de noter que, d'une part ces méthodes prennent rarement en compte l'océan côtier et que, d'autre part les estimations faites à partir du gradient de pCO₂ entre l'air et l'eau souffrent de la difficulté d'estimer de façon fiable la vitesse d'échange de gaz entre ces deux milieux (Liss & Merlivat 1986 ; Wanninkhof 1992).

Le cas de l'océan est un peu plus complexe que celui du réservoir terrestre, car en plus de la pompe biologique décrite précédemment, la capacité de l'océan à puiser le CO₂ atmosphérique est caractérisée par deux autres processus: la pompe chimique et la pompe physique. Le carbone inorganique dissous (DIC) est présent dans l'eau sous trois formes: le bicarbonate (HCO₃⁻), le carbonate (CO₃²⁻) et le CO₂ dissous (CO₂ + H₂CO₃). Pour des valeurs de pH de 7.5 à 8.6 (gamme de variation du pH dans l'eau de mer), la majorité du DIC (91%) se trouve sous forme bicarbonate (Fig. 1). Le CO₂ atmosphérique puisé par l'océan, interagit avec le système des carbonates, pour former principalement du bicarbonate (pompe chimique). D'autre part, les eaux de surface équilibrées avec l'atmosphère peuvent être entraînées en profondeur (pompe physique) et, du fait des échelles de temps de la circulation
thermohaline, seront soustraites à tout contact atmosphérique pour des durées de l'ordre du
millier d'années.

<figure><img src="image_3.png" /></figure>

Figure 1 Variation en fonction du pH de la contribution des différentes espèces du système des carbonates à la concentration en carbone inorganique dissous.

L'efficacité de la pompe biologique océanique est difficile à quantifier à l'heure actuelle. Une des premières estimations globales de production primaire est attribuée à Riley (1939) basée sur quelques mesures avec la méthode de l'O₂ ; il s'agissait donc d'une estimation de la GPP. L'apparition de la méthode basée sur le ¹⁴C (Steemann-Nielsen 1952) a engendré une augmentation considérable des mesures *in situ* et de nombreuses estimations de la production primaire globale sont apparues par la suite (Tableau 1). Un point très important à souligner est que malgré le nombre important de mesures effectuées et la perdurance de cette méthode à l'heure actuelle, cette dernière a fait l'objet de nombreuses critiques. Premièrement, Fitzwater *et al.* (1982) ont mis en évidence que les premières estimations basées sur le ¹⁴C pouvaient être sous-estimées du fait de la contamination des stocks de ¹⁴C utilisés. Depuis 1985, les précautions nécessaires ont été prises de telle sorte que cette méthode fournit des résultats fiables (Martin *et al.* 1987 ; Knauer 1993), mais on ne sait pas exactement ce qu'estime cette méthode: GPP ou NPP (Peterson 1980) ? Selon le temps d'incubation choisit, il est possible qu'une partie du ¹⁴C incorporé à partir de la réaction de photosynthèse soit réoxydé en CO₂ par la respiration. Une incubation longue fournira donc un taux de production plus proche de NPP que de GPP. Un autre inconvénient de cette approche par rapport à la méthode basée sur l'O₂ est qu'il est impossible de quantifier la respiration. De plus, la majorité des expériences se cantonnent à mesurer uniquement la production de matière organique
particulaire (*particulate organic carbon*: POC). Il est maintenant admis qu'une part significative de la production par la photosynthèse est relarguée sous forme dissoute (*dissolved organic carbon*; DOC), particulièrement dans les régions oligotrophes (Baines & Pace 1991 ; Morán *et al.* 2002). Par exemple, Karl *et al.* (1998) ont estimé que les estimations de production primaire à l'aide du $^{14}$C à la station ALOHA (Pacifique Nord) pourraient être sous-estimées de 30 à 50% du fait de la non prise en compte de cette production dissoute. Ces possibles sous-estimations (GPP ou NPP ; production particulaire vs. production dissoute) sont également vraies pour les méthodes basée sur l'utilisation d'images satellitales calibrées sur des données acquises avec la méthode du $^{14}$C (Longhurst *et al.* 1995 ; Antoine & Morel 1996 ; Field *et al.* 1998). Il est à noter également que cette méthode se limite généralement à l'océan ouvert car (1) la turbidité qui caractérise une partie des eaux côtières fausse les estimations basées sur les images satellitales et (2) la gamme de concentration en chlorophylle *a* typiquement rencontrée en milieu côtier est le plus souvent bien au dessus de la gamme de valeurs utilisée pour le développement des algorithmes de calibration des images. Dans le Tableau 1, le terme GPP s'applique uniquement aux estimations faites à partir de l'O$_2$ alors que le terme "NPP ou GPP" correspond aux estimations basées soit directement, soit indirectement sur le $^{14}$C.

La respiration dans l'océan est très certainement le paramètre le moins bien documenté. Récemment, Robinson & Williams (sous presse) ont estimé une respiration de l'océan ouvert global de l'ordre de 9000 à 12000 Tmol C an⁻¹. Ces valeurs sont largement supérieures aux dernières estimations de production. En considérant, d'une part que les estimations basées directement ou indirectement sur la méthode du $^{14}$C fournissent des données de NPP et, d'autre part que la NPP représente 60% de la GPP (soit 40% de la GPP respirée par les organismes autotrophes), del Giorgio & Williams (sous presse) ramènent les valeurs de NPP de Longhurst *et al.* (1995), Antoine & Morel (1996) et Field *et al.* (1998) à des GPP de l'ordre de 5000-7000 Tmol C an⁻¹. Deuxièmement, del Giorgio & Williams (sous presse) ajoutent une production potentielle de DOC de l'ordre de 15% amenant les estimations de GPP à 6000-8000 Tmol C an⁻¹, toujours significativement inférieures aux estimations de respiration. L'océan ouvert serait-il hétérotrophe (Smith & Mackenzie 1987) ?
<table><caption>Tableau 1 Estimations de production primaire (GPP et "NPP ou GPP"), production nette (NEP) et exportation vers l'océan profond. Les valeurs sont exprimées en Tmol C an⁻¹.</caption><thead><tr><th>Références</th><th>GPP</th><th>"NPP ou GPP"</th><th>NEP</th><th>Export</th></tr></thead><tbody><tr><td>Riley (1939)</td><td>10500</td><td></td><td></td><td></td></tr><tr><td>Steemann-Nielsen & Jensen (1957)</td><td></td><td></td><td></td><td></td></tr><tr><td>Fleming (1957)</td><td></td><td>1670</td><td></td><td></td></tr><tr><td>Ryther (1969)</td><td></td><td>1670</td><td></td><td></td></tr><tr><td>Koblentz-Mishke (1970)</td><td></td><td>1920</td><td></td><td></td></tr><tr><td>Garrels & Mackenzie (1972)</td><td></td><td></td><td>-30</td><td></td></tr><tr><td>Platt & Subba Rao (1975)</td><td></td><td>2580</td><td></td><td></td></tr><tr><td>Eppley & Peterson (1979)</td><td></td><td>2000</td><td></td><td></td></tr><tr><td>Martin et al. (1987)</td><td></td><td>4250</td><td></td><td>500</td></tr><tr><td>Smith & Mackenzie (1987)</td><td></td><td>3750</td><td>-20</td><td>636</td></tr><tr><td>Smith & Hollibaugh (1993)</td><td></td><td>4000</td><td>-20</td><td>500</td></tr><tr><td>Longhurst et al. (1995)</td><td></td><td>4170</td><td></td><td></td></tr><tr><td>Antoine & Morel (1996)</td><td></td><td>2750</td><td></td><td></td></tr><tr><td>Field et al. (1998)</td><td></td><td>4080</td><td></td><td></td></tr><tr><td>Falkowski et al. (1998)</td><td></td><td></td><td></td><td>1330</td></tr><tr><td>Wollast (1998)</td><td></td><td>4170</td><td></td><td>350</td></tr><tr><td>Laws et al. (2000)</td><td></td><td></td><td></td><td>920</td></tr><tr><td>Schlitzer (2000)</td><td></td><td></td><td></td><td>920</td></tr><tr><td>Ducklow & McCallister (sous presse)</td><td></td><td></td><td>-200</td><td></td></tr></tbody></table>

L'idée est tentante mais malheureusement impossible à vérifier à l'heure actuelle. Cette hypothèse a été avancée par certains auteurs avec des NEP allant de -17 à -500 Tmol C an⁻¹, nettement inférieure à la différence observée plus haut. Toutefois, Karl et al. (2003), ont utilisé des mesures continues d'O₂ à la station ALOHA (Pacifique nord) pour montrer que l'autotrophie pouvait être un phénomène particulièrement épisodique et suggéré que les programmes actuels d'observation de l'océan ont une résolution temporelle trop faible, et par conséquent sous-estiment grandement la production océanique.

Un océan ouvert hétérotrophe signifierait un océan dépendant des apports de matière organique en provenance de la zone côtière, car : (1) les apports potentiels en provenance de l'atmosphère seraient beaucoup trop faibles pour supporter une hétérotrophie prononcée
(Willey *et al.* 2002) et (2) la matière organique dissoute (DOC) contenue dans l'océan profond est considérée comme principalement réfractaire (Bauer *et al.* 1992).

Il faut toutefois noter qu'un océan hétérotrophe ne signifie pas forcément une source de CO₂ pour l'atmosphère. Bien au contraire, la couche euphotique (zone de pénétration de la lumière) peut être autotrophe et ainsi un puits de CO₂, exportant de la matière organique vers l'océan profond où l'activité hétérotrophique rémineralise cette matière organique ainsi que celle en provenance de la zone côtière. C'est pourquoi certains auteurs se sont intéressés à la production d'export de la zone euphotique océanique. Falkowski *et al.* (1998) ont calculé, à partir d'estimation de production nette dérivées de mesures satellitales et d'une relation production totale vs. production d'export (Eppley & Peterson 1979) qu'environ 30% de la NPP (1330 Tmol C an⁻¹) étaient transférés et rémineralisés dans l'océan profond et ainsi échapperaient à tout contact avec l'atmosphère pendant des centaines voir des milliers d'années. Cette valeur d'export a été revue à la baisse (920 Tmol C an⁻¹) par les modèles de Laws *et al.* (2000) et de Schlitzer (2000).

Un autre processus à prendre en considération au niveau du cycle du carbone océanique est la calcification. En effet, certains organismes marins qu'ils soient benthiques ou pélagiques, animaux ou végétaux, sont capables de précipiter du carbonate de calcium (CaCO₃) selon la réaction :

$$Ca^{2+} + 2HCO_3^- \rightarrow CaCO_3 + CO_2 + H_2O \quad (2)$$

Le processus de précipitation de carbonate de calcium consomme du bicarbonate mais relargue du CO₂ dans l'eau qui, si à proximité de l'interface air-mer, pourra être dégazé vers l'atmosphère. La formation de CaCO₃ agit donc sur le CO₂ en sens inverse de la formation de matière organique. Etant donné de rôle tampon de l'eau, le quotient CO₂ produit/CaCO₃ précipité (Ψ) est, à l'heure actuelle, proche de 1 en eau douce et environ 0.6 en eau salée (Frankignoulle *et al.* 1995). Toutefois, une augmentation de la pCO₂ atmosphérique implique une diminution du pouvoir tampon de l'eau au niveau de la dynamique des carbonates. Ainsi, pour un doublement de la pCO₂ atmosphérique préindustrielle (i.e. 580 ppm), Ψ devrait augmenter et atteindre une valeur de 0.76 (Frankignoulle *et al.* 1994), agissant par conséquent comme un "feedback" positif à cette augmentation de CO₂ atmosphérique. Milliman (1993) a estimé la production globale de CaCO₃ à 60 Tmol C an⁻¹ dont 50% proviendrait de la zone côtière. Environ 40% de cette production ne s'accumule pas et est dissoute soit dans la
colonne d'eau soit au niveau du sédiment. D'après Milliman (1993), la production nette de CO₂ en surface par la calcification serait de 50 Tmol C an⁻¹.

Le budget présenté dans le Tableau 2, concernant les années 1990 (IPCC 2001) semble être balancé : annuellement, sur les 525 Tmol C émis par la combustion d'énergies fossiles, 140 Tmol C seraient puisés par les océans, 120 Tmol C seraient puisés par la biosphère terrestre et 270 Tmol C resteraient dans l'atmosphère. Toutefois, et comme nous l'avons vu plus haut, ces valeurs restent approximatives et associées à des marges d'erreur conséquentes malgré les progrès des connaissances sur le cycle de carbone et de la capacité des réservoirs actifs de la planète à puiser le CO₂ atmosphérique produit par les activités humaines. Il est à noter également que l'océan côtier n'est que rarement incorporé dans les budgets globaux de flux de carbone du fait de (1) la faible quantité de mesures de pCO₂ disponibles (2) l'hétérogénéité et la diversité des écosystèmes côtiers (3) l'intense variabilité spatiale et temporelle des processus biogéochimiques au sein d'un écosystème côtier donné et (4) la difficulté d'intégration dans des modèles de circulation générale. La capacité de l'océan à puiser le CO₂ atmosphérique dépend pourtant également de la quantité de carbone apporté dans l'océan en provenance du continent. L'océan côtier, la zone de transition entre le compartiment terrestre et océanique, ne se comporte pas comme un simple réservoir mais est le site d'intenses processus physiques et biogéochimiques qui transforment, transportent et séquestrent le carbone en provenance des rivières (Liu et al. 2000). Il est donc primordial de l'intégrer dans un budget global de carbone océanique.

<table><caption>Tableau 2 Budgets de CO₂ globaux (en Tmol C an⁻¹; IPCC 2001)</caption><thead><tr><th></th><th>Années 1980</th><th>Années 1990</th></tr></thead><tbody><tr><td>Emissions (combustibles fossiles, production de ciment)</td><td>450 ± 25</td><td>525 ± 33</td></tr><tr><td>Flux océan-atmosphère</td><td>-160 ± 50</td><td>-140 ± 50</td></tr><tr><td>Flux réservoir terrestre-atmosphère</td><td>-17 ± 60</td><td>-120 ± 70</td></tr><tr><td>Augmentation atmosphérique</td><td>275 ± 8</td><td>270 ± 8</td></tr></tbody></table>

La zone côtière, de profondeur entre 0 et 200 m, couvre une surface de 26 x 10⁶ km² et représente 7% de l'océan global. Malgré cette faible superficie, la zone côtière semble avoir un rôle considérable au niveau des cycles biogéochimiques (Gattuso et al. 1998). De plus, de par sa proximité avec le compartiment terrestre, elle est fortement influencée par les activités
humaines. L'eutrophisation a été définie par Nixon (1995) comme étant une augmentation du taux d'apport de matière organique vers un écosystème. Les activités humaines provoquent le déversement dans les rivières et les régions côtières de matière organique particulaire et dissoute ainsi que de la matière inorganique dissoute et particulaire. D'après Meybeck (1993), en plus des 31 Tmol C an⁻¹ de carbone organique (TOC: particulaire + dissous) transportés naturellement par les rivières vers la zone côtière, 8 Tmol C an⁻¹ sont ajoutés par les activités humaines. Les apports d'azote et de phosphore ont été récemment estimé à 1350 et 74 Gmol an⁻¹ respectivement (Smith *et al.* 2003). Ces apports anthropiques de sels nutritifs sont causés par l'utilisation d'engrais agricoles, le défrichage des sols, les déchets domestiques etc.. L'augmentation des apports de sels nutritifs et la modification des rapports élémentaires (par exemple, N:P:Si) ont provoqué dans certaines régions une augmentation de la production phytoplanctonique (Radach *et al.* 1990 ; Wasmund *et al.* 2001 ; Cadée & Hegeman 2002), des modifications de la composition et du fonctionnement du réseau trophique, l'apparition de floraisons toxiques, la disparition d'espèces macroalgales etc... (Ducrotoy 1999 ; Kautsky & Kautsky 2000 ; Ærtebjerg 2001). L'eutrophisation peut avoir un effet non négligeable sur le cycle du carbone au niveau de la zone côtière et ainsi sur le cycle du carbone océanique. L'augmentation de l'apport en sels nutritifs peut en effet stimuler la croissance phytoplanctonique et augmenter ainsi le pompage de CO₂ atmosphérique par ce processus. Inversement, l'augmentation de l'apport de matière organique et de particules sédimentaires peut stimuler la respiration hétérotrophe et limiter la quantité de lumière disponible pour la photosynthèse, produisant ainsi du CO₂ en excès. Par exemple, Frankignoulle *et al.* (1998) ont montré que neuf estuaires européens émettaient de 5 à 10% du CO₂ produit par les activités anthropiques en europe de l'ouest. Toutefois, l'impact de l'homme sur le cycle du carbone côtier est à l'heure actuelle difficile à quantifier car la diversité des écosystèmes rend l'extrapolation au niveau global plus difficile que dans l'océan ouvert.

Tsunogai *et al.* (1999) ont mesuré des flux de CO₂ à l'interface air-mer en mer de Chine de l'ordre de -8 mmol C m⁻² d⁻¹. Par convention, un flux négatif signifie un flux vers l'océan. Extrapolé à toute la zone côtière, cela revient à 80 Tmol C an⁻¹ puisé par l'océan côtier (contre 140 Tmol C an⁻¹ pour l'océan ouvert, voir plus haut). Ces auteurs ont avancé le terme de "continental shelf pump", à savoir la pompe du plateau continental. Depuis, Frankignoulle & Borges (2001), DeGrandpré *et al.* (2002) et Thomas *et al.* (2004) ont mesuré des valeurs légèrement inférieures mais toujours nettement significatives de l'ordre de -2 à -8 mmol C m⁻² d⁻¹ dans le Golfe de Gascogne, la côte est nord américaine (Middle Atlantic Bight) et la mer du nord, respectivement. Toutefois, ces études ne concernent que des pentes
continentales dans des régions tempérées. En effet, le récent travail de Cai *et al.* (2003) au large des côtes de la Géorgie suggère que les plateaux continentaux situés à des latitudes subtropicales seraient des sources de CO₂ vers l'atmosphère. La diversité des écosystèmes côtiers citée plus haut implique des mesures dans des systèmes variés:

- upwellings (Goyet *et al.* 1998 ; Borges & Frankignoulle 2002 ; Friederich *et al.* 2002)

- estuaires (Cai & Wang 1998 ; Frankignoulle et al. 1998 ; Raymond et al. 2000 ; Abril & Borges 2004)

- plumes de dilution (Borges & Frankignoulle 2002 ; Körtzinger 2003)

- récifs coralliens (Gattuso et al. 1993 ; Frankignoulle et al. 1996 ; Gattuso et al. 1997 ; Ohde & van Woesik 1999 ; Bates et al. 2001)

- mangroves (Borges et al. 2003)

- marais salants (Wang & Cai 2004), etc...

A l'heure actuelle, du fait du faible nombre de mesures disponibles et de la grande diversité des écosystèmes côtiers, il n'est pas possible de donner une valeur globale du flux net de CO₂ entre l'atmosphère et l'océan côtier. De plus, et comme nous l'avons mentionné précédemment, l'estimation du flux de CO₂ à l'interface air-mer requiert d'estimer le coefficient d'échange (k).

Une grande part de l'incertitude de l'estimation du flux de CO₂ est attribuée au calcul de ce coefficient. Il dépend principalement de l'état de turbulence de l'interface air-mer, et que ce soit en océan ouvert ou en zone côtière, il a été paramétrisé en fonction de la vitesse du vent considéré comme le principal générateur de turbulence à la surface. Toutefois, Raymond & Cole (2001) ont mis en évidence que cette paramétrisation du coefficient d'échange pouvait varier en fonction de la géomorphologie du site concerné (système ouvert ou fermé). Afin de fournir des estimations de flux de CO₂ fiables au niveau de la zone côtière, il devient impératif de diminuer la marge d'erreur due à l'estimation du coefficient d'échange.

De plus, pour réaliser ces budgets de CO₂, il est nécessaire de connaître la quantité de carbone inorganique dissous (DIC) transporté par les rivières et susceptible d'être dégazé au niveau de l'océan côtier (estuaires principalement, voir plus haut). Cette quantité a été estimée à 50 Tmol C an⁻¹ (Sarmiento & Sundquist 1992).

Le Tableau 3 présente les estimations de NPP, "NPP ou GPP" (basées sur le ¹⁴C), NEP et production exportée de la zone côtière. Il faut souligner que ces auteurs n'ont pas utilisé la même valeur de surface pour la zone côtière, les valeurs allant de 26 à 58 x 10⁶ km². Pour
faciliter les comparaisons, nous avons choisi ici de rapporter les valeurs obtenues par ces différentes études à une même surface, à savoir 26 x 10⁶ km² (Gattuso et al. 1998). Les estimations de NPP de Longhurst *et al.* (1995) basées sur l'analyse d'image satellitales sont d'une part nettement plus élevées que les estimations basées sur les méthodes d'incubation classiques et d'autre part contiennent une marge d'erreur très importante du fait de la difficulté d'analyser les signaux dans les régions turbides. Comme dans la section précédente (océan global), les valeurs diffèrent beaucoup en fonction des auteurs (270 – 830 Tmol C an⁻¹).

<table><caption>Tableau 3 Estimations de production primaire (GPP et "NPP ou GPP"), production nette (NEP) et production d'export au niveau de l'océan côtier. Les valeurs sont exprimées en Tmol C an⁻¹.</caption><thead><tr><th>Référence</th><th>GPP</th><th>"NPP ou GPP"</th><th>NEP</th><th>Export</th></tr></thead><tbody><tr><td>Platt & Subba Rao (1975)</td><td></td><td>270</td><td></td><td></td></tr><tr><td>Whittle (1977)</td><td></td><td>350</td><td></td><td></td></tr><tr><td>Eppley & Peterson (1979)</td><td></td><td>270</td><td></td><td></td></tr><tr><td>Wollast & Billen (1981)</td><td></td><td>475</td><td></td><td></td></tr><tr><td>Martin et al. (1987)</td><td></td><td>540</td><td></td><td></td></tr><tr><td>Smith & Mackenzie (1987)</td><td></td><td>600</td><td>-27</td><td>0</td></tr><tr><td>Walsh (1988)</td><td></td><td>275</td><td></td><td></td></tr><tr><td>Berger (1989)</td><td></td><td>390</td><td></td><td></td></tr><tr><td>Wollast (1991)</td><td></td><td>500</td><td></td><td>75</td></tr><tr><td>Walsh (1991)</td><td></td><td></td><td></td><td>83</td></tr><tr><td>Smith & Hollibaugh (1993)</td><td>500</td><td></td><td>-7</td><td>18</td></tr><tr><td>Longhurst et al. (1995)</td><td></td><td>520-830</td><td></td><td></td></tr><tr><td>Rabouille (1997)</td><td>423</td><td></td><td>12</td><td>37</td></tr><tr><td>Wollast (1998)</td><td>500</td><td></td><td>200</td><td>183</td></tr><tr><td>Gattuso et al. (1998)</td><td>790</td><td></td><td>230</td><td></td></tr><tr><td>Liu et al. (2000)</td><td></td><td>470</td><td></td><td>58</td></tr><tr><td>Rabouille et al. (2001)</td><td></td><td></td><td>13</td><td></td></tr></tbody></table>

Peu d'estimations de la production brute côtière ont été effectuées jusqu'à présent, Gattuso et al. (1998) avancent une valeur de 790 Tmol C an⁻¹, ce qui amène les auteurs à conclure que la production organique côtière représenterait 23% de la production océanique globale. Toutefois, il convient de préciser que la valeur de production de l'océan ouvert
utilisée pour ce calcul est celle de Wollast (1998), i.e. 3400 Tmol C an⁻¹ et correspondrait plus
à une valeur de NPP que de GPP (voir section précédente). Les estimations de NEP et
d'export de matière organique de la zone côtière vers l'océan ouvert (la pompe biologique
côtière) diffèrent elles aussi grandement entre les auteurs. Tandis que Smith & Hollibaugh
(1993) estiment que la zone côtière serait hétérotrophe et que l'export de matière organique
vers l'océan profond correspondrait à environ la moitié des apports organiques continentaux,
Gattuso et al. (1998) et Wollast (1998) suggèrent que l'océan côtier serait autotrophe et une
source nette de carbone organique pour l'océan ouvert. Par ailleurs, nous avons vu dans la
section précédente que la calcification pouvait avoir un rôle non négligeable au niveau du
cycle du carbone, particulièrement en zone côtière. En effet, d'après Milliman (1993), la
production et l'accumulation de CaCO₃ en zone côtière seraient de 25 et 17 Tmol C an⁻¹.
Comparées aux valeurs d'exportation de matière organique (voir Tableau 3), la production
nette de CO₂ due à l'accumulation et à l'exportation de CaCO₃ n'est pas négligeable et doit
être prise en considération dans les budgets de carbone au niveau de la zone côtière.
Cependant, du fait du faible nombre de mesures à l'échelle globale, les marges d'erreurs
associées à l'estimation de ces paramètres sont malheureusement encore trop élevées.

En conclusion, que ce soit à partir de mesures directes de pCO₂ ou d'extrapolation des
paramètres métaboliques (production/respiration, précipitation/dissolution de carbonate de
calcium) gouvernant le flux net biologique entre l'atmosphère et l'océan côtier, il est très
difficile de quantifier le rôle de la zone côtière dans le cycle global du carbone. Plusieurs
approches peuvent être utilisées pour préciser ce rôle : (1) augmenter les mesures de pCO₂
dans le domaine côtier et calculer les flux tout en affinant l'estimation du coefficient
d'échange, (2) augmenter les mesures de production/respiration de matière organique au
moyen des méthodes d'incubation classiques, (3) utiliser de nouvelles méthodes permettant
d'estimer la production nette des écosystèmes côtiers à de plus grandes échelles spatiales et
temporelles et (4) quantifier de façon plus fiable le rôle de la calcification au niveau du cycle
du carbone côtier.
L'étude présentée ici a été réalisée dans le cadre du programme européen EUROTROPH (Contrat: EVK3-CT-2000-00040 http://www.ulg.ac.be/oceanbio/eurotroph/) qui a débuté en 2001. Les objectifs étaient (1) d'étudier, par le biais d'une compilation bibliographique de mesures de paramètres métaboliques (GPP, CR et NEP), le statut trophique des écosystèmes côtiers à l'échelle européenne et (2) de quantifier le statut trophique de trois systèmes côtiers en utilisant différentes méthodes à différentes échelles de temps (échelle locale).

Les trois systèmes côtiers étudiés sont la baie de Palma, le fjord de Randers et l'estuaire de l'Escaut. Ces sites ont été choisis en fonction des différences existant au niveau des paramètres environnementaux gouvernant la balance métabolique (Fig. 2).

<figure><img src="image_4.png" /><figcaption>Figure 2 Paramètres environnementaux supposés gouverner la balance métabolique des 3 sites étudiés dans le cadre du programme EUROTROPH</figcaption></figure>

L'estuaire de l'Escaut est considéré comme l'un des estuaires les plus pollués d'europe de l'ouest en terme d'apport de sels nutritifs et de matière organique (Wollast 1988). Situé en Belgique et aux Pays-Bas (Fig. 3), il draine les eaux d'un bassin très peuplé et industrialisé. Dans cet estuaire macrotidal, la colonne d'eau est bien mélangée et la turbidité est forte dans tout l'estuaire, limitant la production phytoplanctonique (van Spaendonk et al. 1993 ; Kromkamp et al. 1995). Un temps de résidence de l'eau douce élevé (Soetaert & Herman
1995) et une activité hétérotrophe très importante (Goosen et al. 1995) sont les causes de fortes concentrations en CO₂ (Frankignoulle et al. 1998).

Le fjord de Randers est un estuaire microtidal stratifié situé sur la côte est du Danemark. Les apports en sels nutritifs et matière organique ainsi que la turbidité et le temps de résidence de l'eau douce sont nettement moins important que dans l'estuaire de l'Escaut.

Enfin, la baie de Palma située en Méditerranée occidentale (Baléares, Mallorque) est un écosystème peu turbide dominé par un herbier de phanérogames marines (*Posidonia oceanica*) qui occupe environ 30% de la surface de la baie. L'activité touristique entraîne pendant l'été une augmentation de l'apport de sels nutritifs en provenance de la ville de Palma. L'augmentation de ces apports a été identifiée comme une des causes principales de la régression de l'herbier de *posidonies* dans ce système. Une description plus détaillée de chaque site est donnée dans les chapitres correspondants.

<figure><img src="image_5.png" /><figcaption>Figure 3 Localisation des sites étudiés dans le cadre du programme EUROTROPH</figcaption></figure>

Deux campagnes dans chaque système ont été effectuées:

- avril et août 2001: fjord de Randers

- mars et juin 2002: baie de Palma

- novembre 2002 et avril 2003: estuaire de l'Escaut
De plus, l'estuaire de l'Escaut a été visité avec une fréquence mensuelle de janvier à décembre 2003.

Les méthodes utilisées dans cette étude pour déterminer le statut trophique sont:

1. la méthode d'incubation classique (mesure de la variation de la concentration en oxygène à la lumière et à l'obscurité) planctonique et benthique de façon discrète à plusieurs stations et extrapolation spatiale des résultats au moyen de cartes bathymétriques établies pour les trois sites.

2. la méthode RSD (Response Surface Difference) développée par Swaney *et al.* (1999). Cette méthode intégrative, dérivée de la méthode multistation averaging de Howarth *et al.* (1992) consiste en des profils d'oxygène à diverses stations d'un système et à différentes périodes de la journée (open-system method ou méthode en système ouvert). Cette méthode a été appliquée uniquement au fjord de Randers. Contrairement à la méthode multistation averaging, cette technique considère que dans des systèmes partiellement mélangés, la concentration en oxygène ne dépend pas que des processus biologiques et des échanges avec l'atmosphère, mais également de la profondeur et de la salinité. Il convient d'ajouter que d'autres méthodes basées sur des cycles journaliers (O₂ et DIC) ont été utilisées localement dans le fjord de Randers et la baie de Palma.

3. La méthode LOICZ (Land-Ocean Interaction in the Coastal Zone; Gordon *et al.* 1996). Il s'agit d'une procédure de budgétisation d'un système à partir des données de flux d'eau douce, de salinité et de concentration en phosphore, azote et carbone inorganiques dissous (DIP, DIN et DIC). Le volume du système est supposé constant et la salinité (paramètre conservatif) est utilisée pour estimer les flux d'échange entre les différents compartiments du système considéré ainsi qu'entre le système et l'environnement externe. La concentration des différents éléments (DIP, DIN et DIC) est elle aussi supposée constante, la déviation par rapport à la conservativité permettant d'estimer:

i. La NEP (p-r dans la terminologie LOICZ) du système en considérant que d'une part seuls les processus biologiques (production/minéralisation de matière organique, NEP) ont un effet sur la variation non-conservative du DIP et d'autre part que les flux non-conservatifs de DIC sont attribués à
la production/minéralisation de matière organique (NEP), aux échanges
de CO₂ avec l'atmosphère ainsi qu'à la précipitation/dissolution de
carbonate de calcium.

Il s'agit donc de deux estimations indépendantes de la NEP, un rapport
C:P de la matière organique particulaire permettant de convertir les flux
non conservatifs de DIP en carbone.

ii. la différence entre la fixation et la dénitrification (N<sub>fix-denit</sub> dans la terminologie LOICZ) en considérant que, outre la balance entre la production/minéralisation de matière organique (NEP), seuls ces deux processus interviennent au niveau de la variation non-conservative du DIN. Comme précédemment, un rapport (N:C)<sub>part</sub> est nécessaire pour transformer l'unité de la NEP de carbone en azote.

Cette méthode n'a pu être appliquée à la baie de Palma car elle requière, pour être fiable, une différence significative de salinité entre le système étudié et l'extérieur, ce qui n'est pas le cas pour la baie de Palma.

Comme nous l'avons vu, les méthodes open-system (RSD, cycles journaliers) ainsi que la méthode LOICZ appliquée au DIC nécessitent l'estimation du flux d'O₂ et/ou de CO₂ entre l'eau et l'atmosphère. Nous avons discuté plus haut que le coefficient d'échange (k) est un paramètre critique dans l'estimation de ces flux. Celui-ci a été étudié dans les trois sites où ces méthodes ont été appliquées.
Le manuscrit se présente selon le plan suivant:

- L'étude bibliographique permettant de faire un état des lieux de nos connaissances concernant le métabolisme de la zone côtière européenne sera présentée dans le **chapitre 2**. Ce travail a fait l'objet de la publication suivante:

Gazeau F., Gentili B., Frankignoulle M., Smith S. V. & Gattuso J.-P. *The European coastal zone: characterization and first assessment of ecosystem metabolism* (2004) *Estuarine, Coastal and Shelf Science* 60(4): 673-694.

- L'étude du métabolisme de la baie de Palma au moyen de l'intégration de données d'incubation oxygène ainsi que par l'intermédiaire de budgets DIC et O₂ sera présentée dans le **chapitre 3.1**. Ce travail fait l'objet de la publication suivante:

Gazeau F, Duarte C. M., Gattuso J.-P., Barrón C., Navarro N., Ruíz S., Prairie Y. T., Calleja M., Delille B., Frankignoulle M. and Borges A. V. *Whole system metabolism and CO₂ fluxes in the Bay of Palma (NW Mediterranean) (en preparation, soumission mi-août) Biogeosciences* issue spéciale *Coastal Biogeochemistry* co-editée par H. Thomas et A. V. Borges.

- L'étude concernant l'estimation du coefficient d'échange dans les estuaires de Randers et de l'Escaut sera présentée dans le **chapitre 3.2**. Ce travail a fait l'objet de la publication suivante:

Borges A. V., Delille B., Schiettecatte L. -S., Gazeau F., Abril G. & Frankignoulle M. *Gas transfer velocities of CO₂ in three European estuaries* (Randers Fjord, Scheldt and Thames) (sous presse) *Limnology and Oceanography* 49(5).

- L'étude du métabolisme du fjord de Randers au moyen de diverses méthodes ainsi que l'utilisation de la méthode LOICZ, à partir de données historiques acquises dans l'estuaire, sur une échelle de temps d'une dizaine d'années sera présentée dans le **chapitre 3.3**. Ce travail fait l'objet de la publication suivante:

Gazeau F., Borges A. V., Barrón C., Duarte C. M., Iversen N., Middelburg J. J., Pizay M. -D., Frankignoulle M. & Gattuso J.-P. *Net ecosystem metabolism in a micro-tidal estuary* (Randers Fjord, Denmark): *evaluation of methods and interannual variability (soumis) Marine Ecology Progress Series*.
- L'étude du métabolisme de l'estuaire de l'Escaut à partir des données de métabolisme acquises in situ pendant l'année 2002-2003, ainsi qu'à partir de la méthode LOICZ sera présentée dans le **chapitre 3.4**. Ce travail fait l'objet de la publication suivante:

Gazeau F., Gattuso J. -P., Middelburg J. J., Barrón C., Duarte C. M.,
Schiettecatte L. -S., Brion N., Pizay M. -D., Frankignoulle M. & Borges A. V. Planktonic
and whole system metabolism in a nutrient-rich estuary (The Scheldt Estuary) (soumis)
Limnology and Oceanography.

- Enfin, la synthèse sera présentée dans le **chapitre 4** et la conclusion et les perspectives dans le **chapitre 5**.
# Chapitre 2

## L'échelle
Européenne

Gazeau F., Gentili B., Frankignoulle M., Smith S. V. & Gattuso J. -P., (2004)

The European coastal zone: characterization and first assessment of ecosystem metabolism.

*Estuarine, Coastal and Shelf Science.* 60(4): 673-694.
# The European coastal zone: characterization and first assessment of ecosystem metabolism

Frédéric Gazeau<sup>a,b,*</sup>, Stephen V. Smith<sup>c</sup>, Bernard Gentili<sup>a</sup>, Michel Frankignoulle<sup>b</sup>, Jean-Pierre Gattuso<sup>a</sup>

Received 21 December 2003; accepted 10 March 2004

## Abstract

The geomorphic, oceanographic, terrestrial and anthropogenic attributes of the European coastal zone are described and published data on ecosystem function (primary production and respiration) are reviewed. Four regions are considered: the Baltic Sea, Mediterranean Sea, Black Sea and the European Atlantic coast including the North Sea. The metabolic database (194 papers) suffers from a non-homogeneous geographical coverage with no usable data for the Black Sea which was therefore excluded from this part of our study. Pelagic gross primary production in European open shelves is, by far, the most documented parameter with an estimated mean of 41 mmol C m⁻² d⁻¹, the lowest value is reported in the Mediterranean Sea (21 mmol C m⁻² d⁻¹) and the highest one in the Atlantic/North Sea area (51 mmol C m⁻² d⁻¹). Microphytobenthic primary production, mostly measured in shallow areas, is extrapolated to the entire 0–200 m depth range. Its contribution to total primary production is low in all regions (mean: 1.5 mmol C m⁻² d⁻¹). Although macrophyte beds are very productive, a regional production estimate is not provided in this study because their geographical distribution along the European coastline remains unknown. Measurements of pelagic community respiration are clearly too sparse, especially below the euphotic zone, to yield an accurate picture of the fate of organic matter produced in the water column. With a mean value of 17 mmol C m⁻² d⁻¹, benthic community respiration consumes approximately 40% of the pelagic organic matter production. Estuaries generally exhibit high metabolic rates and a large range of variation in all parameters, except microphytobenthic primary production. Finally, the problem of eutrophication in Europe is discussed and the metabolic data obtained in the framework of the Land–Ocean Interactions in the Coastal Zone (LOICZ) project are compared with available direct measurements of net ecosystem production.
© 2004 Elsevier Ltd. All rights reserved.

Keywords: ecosystems; global; metabolism; shelf; estuaries; primary production; respiration; Europe

## 1. Introduction

The coastal zone is a transition area between land and the open ocean. It receives considerable amounts of freshwater, nutrients, dissolved and particulate organic matter, sediment and contaminants. It also exchanges matter and energy with the open ocean. The coastal zone is, by definition, relatively shallow. This has two consequences: (1) light penetrates a significant portion

of the water column, even reaching the bottom in some areas; and (2) there is a strong coupling between pelagic and benthic processes. These inputs, together with its shallowness, make the coastal zone very active in terms of primary production and respiration. Coastal metabolism has been reviewed in a number of relatively recent papers (Smith and Hollibaugh, 1993; Alongi, 1998; Gattuso et al., 1998; Wollast, 1998).

The European coastal zone has geomorphic and metabolic characteristics similar to those of other coastal areas. Although these attributes have never been fully reviewed, local and thematic studies have received strong support and attention in the European research

<footnote><sup>a</sup>Laboratoire d'Océanographie de Villefranche, CNRS-Université de Paris 6, B.P. 28, F-06234 Villefranche-sur-mer Cedex, France</footnote>

<footnote><sup>b</sup>Unité d'Océanographie Chimique (B5), MARE, Université de Liège, B-4000 Sart Tilman, Belgium</footnote>

<footnote><sup>c</sup>Departamento de Ecología, Centro de Investigación Científica y de Educación Superior de Ensenada, Ensenada, Baja California, Mexico</footnote>

<footnote>* Corresponding author.</footnote>

<footnote>E-mail address: gazeau@obs-vlfr.fr (F. Gazeau).</footnote>
programs. A major reason is that the European Union (EU) has promoted inclusion of socio-economic aspects in the research projects reflecting the increasing significance of the coastal ocean in the EU and elsewhere in terms of fishing, aquaculture and recreation. The European Commission launched ELOISE (European Land–Ocean Interaction Studies) as a loose network of reasonably small coastal research projects. ELOISE is the European contribution to LOICZ (Land–Ocean Interaction in the Coastal Zone), a program element of the International Geosphere Biosphere program (IGBP).

Two of the initial goals of ELOISE (Cadée et al., 1994) were related to ecosystem function: (1) to determine the role of coastal seas in land-ocean interactions (including shelf-deep sea interactions along the shelf break) in the context of global change; and (2) to determine the regional and global consequences of human impact through pollution, eutrophication and physical disturbance on land-ocean interactions in the coastal zone.

This paper has two aims. First, to review the geomorphic, oceanographic, terrestrial and anthropogenic attributes of the EU coastal zone using global databases recently accessible. Second, to review, synthesize and analyse published data on ecosystem function, essentially primary production and respiration.

## 2. Characterization of the European coastal zone

The continental shelf, continental margin, coastal ocean and coastal zone are fuzzy concepts for which various definitions have been proposed. It is outside the scope of this paper to review these definitions. The definition of the terms as commonly used was adopted and the operational definition applied here was explicitly mentioned.

The continental shelf is the area extending from the coast to the shelf break, which is usually defined by the 200 m depth isobath. The continental margin is the transition zone between the continental crust and the oceanic crust, including the coastal plain, continental shelf, slope and rise (Kennett, 1982). The coastal ocean is the portion of the global ocean where physical, biological and biogeochemical processes are directly affected by land. It is either defined as the part of the global ocean covering the continental shelf or the continental margin. The coastal zone usually includes the coastal ocean as well as the portion of the land adjacent to the coast that influences coastal waters. It can readily be appreciated that none of these concepts has a clear operational definition. The marine portion of the coastal zone was defined as the area with a depth of 200 m or less or, when the data are gridded with a large cell size, with at least one depth sounding of 200 m or less. The land portion of the coastal zone is the land area located in the 0.5° × 0.5° cell enclosing the coastline (see below).

Two major sources of information were used: the ETOPO2 data set for the depth attributes and the LOICZ environmental database for most other attributes. The gridded ETOPO2 data set was downloaded from the Data Support Section of the National Center for Atmospheric Research (http://dss.ucar.edu/datasets/ds759.3/data/) on 9 December, 2002. It blends satellite altimetry with ocean soundings and new land data to provide a global elevation and bathymetry on a 2' × 2' grid. The UNIX version of the Generic Mapping Tool (gmt 3.4.2-3), with its full resolution coastline, was used to calculate surface area, volume, as well as median and average depths.

The international program LOICZ has compiled atmospheric, geomorphic, terrestrial, oceanic, biogeochemical and human-related variables, and produced a gridded database freely accessible (http://hercules.kgs.ukans.edu/hexacoral/envirodata/main.htm) on the World Wide Web. The grid size (0.5° or about 55 km at the equator) is coarse for coastal areas, which exhibit major gradients in their environmental and ecological attributes at scales of 1 km or less. Importantly, data for many of the variables present in the LOICZ database are simply not available on a global scale and with a better geographical resolution. The choice of the grid size was then a compromise between the existing data and the objective of using the same grid size for all variables. This database is a very powerful tool: (1) to describe the attributes of the coastal ocean at a global scale, more specifically its geomorphology, environmental setting and biogeochemical properties; and (2) to explore how the coastal zone is influenced by inputs from land and the atmosphere, as well as by human activities.

Here, four regions are examined (Fig. 1): the Baltic Sea (including the Kattegat), the Mediterranean Sea, the Black Sea (including the Sea of Azov) and the European Atlantic coast (including the English Channel, the North Sea and the Skagerrak). While the Caspian Sea is often included as an EU sea (Mamaev, 2002), this area was not considered because it is not connected to an open ocean or marginal sea. Similarly, freshwater bodies were not considered.

### 2.1. Geomorphic attributes

#### 2.1.1. Surface area and hypsometry

The European coastal zone covers 8.4% of the world coastal zone surface area (2.18 vs. $25.84 \times 10^6$ km$^2$; Table 1), with a similar median depth (60 vs. 46 m). The European Atlantic coast is the largest region (56% of the EU coastal zone) reflecting the large area of the North Sea and the extended shelf that surrounds the United Kingdom. The next largest region is the Mediterranean (21%). It has a relatively narrow shelf, except in the northern Adriatic Sea, representing only 18% of the total surface area. The coastal zones of the Baltic Sea and the
<figure><img src="image_6.png" /><figcaption>Fig. 1. Map of the European coastal zone with considered sub-regions.</figcaption></figure>

Black Sea (97% and 28% of their total surface area) represent 17% and 6% of the EU coastal zone; they are the shallowest regions (median depth of 35 and 40 m). The European Atlantic region is the deepest (median depth: 73 m). Note that part of the Baltic Sea (Gulf of Bothnia and eastern part of Gulf of Finland) has a seasonal ice cover for up to half a year; the maximum annual ice cover ranges from 12% to 100% of the surface area (Gronvall and Seina, 1999).

The hypsometric curves (Fig. 2) show that the European Atlantic region has a much steeper slope than all other regions of the European coastal zone and is steeper than the mean value for the global coastal zone. About 34% of the Baltic Sea area is shallower than 20 m, 23% of the Black Sea, 19% of the Mediterranean Sea and only 11% of the European Atlantic Ocean, compared with a mean value of 26% for the global coastal zone.

<table><caption>Table 1

Geomorphic attributes of the European coastal zone</caption><thead><tr><th>Geographical zone</th><th>Area (10<sup>6</sup> km<sup>2</sup>)</th><th>Volume (10<sup>6</sup> km<sup>3</sup>)</th><th>Mean depth ± SD (m)</th><th>Median depth (m)</th></tr></thead><tbody><tr><td>Baltic Sea</td><td>0.37</td><td>18.17</td><td>46 ± 43</td><td>35</td></tr><tr><td>Mediterranean Sea</td><td>0.45</td><td>29.07</td><td>67 ± 54</td><td>56</td></tr><tr><td>Black Sea</td><td>0.13</td><td>7.25</td><td>56 ± 49</td><td>40</td></tr><tr><td>Atlantic, European</td><td>1.23</td><td>95.59</td><td>78 ± 53</td><td>73</td></tr><tr><td>Total, mean and median depth (Europe)</td><td>2.18</td><td>150.06</td><td>69 ± 53</td><td>60</td></tr></tbody></table>

### 2.1.2. Attributes of the land adjacent to the coastal zone

Nearly 50% of total length of the European coastline (calculated at a nominal scale of 1:250 000) is in the Atlantic domain, 27% in the Baltic Sea, 20% in the Mediterranean Sea and less than 5% in the Black Sea (Table 2). The median elevation of land adjacent to the coast, that is comprised in the LOICZ coastal cells described above, is higher in the Mediterranean (194 m) than elsewhere in Europe (grand median, 112 m). The surface area of the coastal cells covered by crop land

<figure><img src="image_7.png" /><figcaption>Fig. 2. Hypsometry of the European coastal ocean.</figcaption></figure>
<table><caption>Table 2
Geomorphic attributes of the LOICZ database coastal cells</caption><thead><tr><th>Variable</th><th>Baltic Sea</th><th>Mediterranean Sea</th><th>Black Sea</th><th>European Atlantic</th><th>Whole of Europe</th></tr></thead><tbody><tr><td>Coastline length (km) [1]</td><td>77802</td><td>56650</td><td>10738</td><td>133357</td><td>278547</td></tr><tr><td>Median of mean land elevation (m) [2]</td><td>27</td><td>194</td><td>79</td><td>123</td><td>112</td></tr><tr><td>Median maximum elevation (m) [3]</td><td>68</td><td>650</td><td>227</td><td>380</td><td>331</td></tr><tr><td>Median of SD of elevation (m) [4]</td><td>14</td><td>138</td><td>46</td><td>80</td><td>68</td></tr></tbody></table>

Numbers in brackets refer to data sources listed in the appendix available at: http://www.obs-vlfr.fr/~gattuso/ECSS_app.htm.

ranges from 15% in the European Atlantic region to 42% in the Black Sea region (Fig. 3).

## 2.2. Atmospheric attributes

Some but not all atmospheric environmental parameters vary greatly depending on the zone considered. The median wind speed is higher in the European Atlantic region than in the Mediterranean region, with a difference of less than 2 m s⁻¹ (Table 3). The median air temperature is 10.5 °C for all of Europe; the median, minimum and maximum monthly air temperatures range widely from -15.4 to 31.9 °C. The median annual precipitation is similar in the Baltic, Mediterranean and Black Sea regions (range, 671–720 mm yr⁻¹) but is significantly higher in the European Atlantic region (1022 mm yr⁻¹). The largest range of mean monthly precipitation is found in the Mediterranean region (0–484 mm month⁻¹).

## 2.3. Oceanic attributes

The median mean monthly sea surface temperature (SST) varies almost 3-fold between the geographical regions (7.7 °C in the Baltic Sea and 19.5 °C in the

<figure><img src="image_8.png" /><figcaption>Fig. 3. Relative surface area (%) of cropland in the coastal cells. Data from the University of Maryland's 1 km global land cover product (Hansen et al., 2000) extracted from the LOICZ database.</figcaption></figure>

Mediterranean; Table 4). The range of mean monthly SST is >20 °C in the four regions. Sea surface salinity (SSS) is reported but some EU coastal areas are seasonally or permanently stratified. For example, according to Kautsky and Kautsky (2000) the central Baltic Proper is permanently stratified (salinities of 6–8 in the upper layer and 10–14 in the deeper layer). The median SSS differs considerably between geographical regions (6.4 in the Baltic Sea and 38.1 in the Mediterranean Sea). The median wave height is 3–4 times smaller in the Black Sea than in the other three regions; it is highest in the European Atlantic region. The median tidal range also differs largely between regions with values close to 0 m in the Baltic Sea and the Mediterranean Sea regions, and between 2 and 4 m in the European Atlantic region.

## 2.4. River basin and coastal population attributes

In Europe, 58% of the total annual runoff comes from 35 large river basins (Fig. 4); individual runoff values range from 13.1 to 329 km³ yr⁻¹. The calculated combined runoff is similar to that reported by Dai and Trenberth (2002). The European Atlantic region receives about the same total runoff as the Mediterranean Sea (Table 5), but the yield (runoff per unit of river basin area) is 3-times greater. The very large river basin area for the Mediterranean region is due to the Nile basin, which extends over 10 African countries and covers about 3×10⁶ km². As a result, the total basin population is equally large with more than 360×10⁶ inhabitants. European basins drain an area 7-times larger than the surface of the EU coastal zone (15.2 vs. 2.2×10⁶ km²). The rivers that drain Europe are small and carry little sediment (Milliman and Meade, 1983; Milliman and Syvitski, 1992). Only the Rhône, Po and Danube Rivers appear to have annual sediment discharge rates >10×10⁶ t. The Danube River, by far the largest in terms of its drainage area and water discharge volume, has a sediment discharge rate of 67×10⁶ t yr⁻¹. The total sediment discharge from Europe is 230×10⁶ t yr⁻¹. Estimates of nutrient loads, nitrogen (DIN) and phosphorus (DIP), from European drainage basins are based on the model of Smith et al. (2003). Nutrient yield from the European Atlantic river basin is about twice the average and more than 3 times the Mediterranean Sea value. The Baltic and Black Seas are each near the
<table><caption>Table 3
Atmospheric attributes of all cells with at least one depth <200 m</caption><thead><tr><th>Variable</th><th>Baltic Sea</th><th>Mediterranean Sea</th><th>Black Sea</th><th>European Atlantic</th><th>Whole of Europe</th></tr></thead><tbody><tr><td>Median wind speed (m s<sup>-1</sup>) [5]</td><td>7.4</td><td>6.5</td><td>—</td><td>8.3</td><td>7.2</td></tr><tr><td>Median of air temperature (°C) [6]</td><td>3.4</td><td>16.0</td><td>10.3</td><td>8.0</td><td>10.5</td></tr><tr><td>Minimum and maximum monthly<br>averaged air temperature (°C) [7]</td><td>-11; 21.6</td><td>-8.5; 31.9</td><td>-7.4; 24.5</td><td>-15.4; 26.6</td><td>-15.4; 31.9</td></tr><tr><td>Median CV of 12 months average air<br>temperature (°C) [8]</td><td>2.8</td><td>1.9</td><td>2.7</td><td>1.5</td><td>1.9</td></tr><tr><td>Median annual precipitation (mm yr<sup>-1</sup>) [9]</td><td>720</td><td>679</td><td>671</td><td>1022</td><td>794</td></tr><tr><td>Minimum and maximum monthly averaged<br>precipitation (mm) [10]</td><td>16; 222</td><td>0; 484</td><td>18; 277</td><td>0.1; 342</td><td>0; 484</td></tr></tbody></table>

Numbers in brackets refer data sources listed in the appendix available at: http://www.obs-vlfr.fr/~gattuso/ECSS_app.htm.

average. The human attributes of the coastal cells are shown in Table 6. The population density is the highest in the Mediterranean coastal area (58.5 inhabitants km⁻²), and minimal along the Baltic coast with a value of 13.1 inhabitants km⁻².

### 3. Metabolic performances of European coastal ecosystems

#### 3.1. Construction, content and characteristics of the database

A database was constructed using references from the Aquatic Science and Fisheries Abstracts (ASFA) database and from review papers (Charpy-Roubaud and Sournia, 1990; Smith and Hollibaugh, 1993; Heip et al., 1995; Gattuso et al., 1998; Cahoon, 1999; Cebrián, 2002; Middelburg et al., 2004). This database is available from the authors or on the World Wide Web (http://www. obs-vlfr.fr/eurotroph/). One of the striking outcomes of the literature search was that, while several hundred papers were returned for each search, a relatively small number of them could be used. Indeed, a large number

of studies focused on the metabolism of single species rather than of the community. Such data were not considered here. Although budgets of air-sea CO₂ fluxes can be a reliable estimate of the trophic status of an ecosystem (Frankignoulle et al., 1998; Thomas and Schneider, 1999; Frankignoulle and Borges, 2001), this study only focuses on measured processes and LOICZ budgets. The following information has been compiled when available: latitude and longitude of the study site, time of the year, depth of the site and of sampling, salinity, temperature, nutrient concentrations, community primary production (net or gross), community respiration and the methods used to measure these processes. The database presently comprises 194 references. The database is certainly not exhaustive, but it is regularly updated. It also has a significant bias against papers published before 1978 because the ASFA database only lists references published after that date. However, our database is believed to be a relatively unbiased sample of the literature published after 1978.

The number of studies of EU coastal ecosystem function has steadily increased during the past decades (Fig. 5). The present rate of publication is about 10–15 papers per year. However, only some of these studies

<table><caption>Table 4
Oceanic attributes of all cells with at least one depth sounding <200 m</caption><thead><tr><th>Variable</th><th>Baltic Sea</th><th>Mediterranean Sea</th><th>Black Sea</th><th>European Atlantic</th><th>Whole of Europe</th></tr></thead><tbody><tr><td>Median of monthly averaged sea surface temperature [11]</td><td>7.7</td><td>19.5</td><td>14.7</td><td>10.6</td><td>15.3</td></tr><tr><td>Minimum and maximum monthly sea surface temperature [12]</td><td>-1.8; 21</td><td>6.5; 29.3</td><td>3.6; 27.2</td><td>-1.8; 24.8</td><td>-1.8; 29.3</td></tr><tr><td>Median of monthly averaged sea surface salinity [13]</td><td>6.4</td><td>38.1</td><td>18.0</td><td>34.9</td><td>35.2</td></tr><tr><td>Minimum and maximum monthly averaged sea surface salinity [14,15]</td><td>3.3; 23.1</td><td>17.7; 39.7</td><td>15; 19.1</td><td>3.3; 37</td><td>3.3; 39.7</td></tr><tr><td>Median wave height (scaled discrete classes) [15]</td><td>3</td><td>3</td><td>1</td><td>4</td><td>3</td></tr><tr><td>Median tidal range (scaled discrete classes) [16]</td><td>0</td><td>0</td><td>1</td><td>3</td><td>1</td></tr></tbody></table>

Classes for wave height are: 0 = permanent sea ice, 1 = 0–2.5 m, 3 = 2.5–3.5 m, 4 = 3.5–4.5 m, 6 = 4.5–6.5 m, 7 = >6.5 m. Classes for tidal range are: 0 = tideless, 1 = <2 m, 3 = 2–4 m, 6 = 4–8 m, 10 = >8 m. Numbers in brackets refer data sources listed in the appendix available at: http://www.obs-vlfr.fr/~gattuso/ECSS_app.htm.
<figure><img src="image_9.png" /><figcaption>Fig. 4. Location of the 35 coastal cells that contribute most to coastal runoff.</figcaption></figure>

report yearly estimates of the processes, which limits their usefulness to derive the global properties of ecosystem function.

### 3.1.1. Methods and collection of data

The data were obtained using a wide range of techniques: change in the concentration of a tracer ($^{14}$C, CO$_2$ or O$_2$) during incubations carried out in situ or under in situ simulated conditions, or using large-scale budgeting (Gordon et al., 1996), but all are expressed in mmol C m$^{-2}$ d$^{-1}$. The metabolic process measurements originally reported in oxygen units were transformed into carbon units assuming that the photosynthetic and respiratory quotients equal 1. Although PQ seems to be higher than 1 in phytoplankton (Hedges et al., 2002), the paucity of available data and the general lack of recorded environmental conditions (including nutrient sources for photosynthesis) in the publications prevent assessment of the sensitivity of PQ in our evaluation.

Some papers report metabolic rates measured at only one depth and expressed in µmol C l$^{-1}$ d$^{-1}$. These references were excluded from our assessment that

considered only rates normalized per unit surface area, with the exception of pelagic community respiration data (see next section). A significant number of papers report hourly rates of primary production and/or respiration. Hourly pelagic and benthic respiration rates were converted into daily rates assuming constant values over 24 h. This neglects the fact that respiration can be higher in the light than in the dark in many photosynthetic organisms as reported recently for an algal-dominated reef maintained in a mesocosm (Langdon et al., 2003).

Incubations with the $^{14}$C-tracer method were generally carried out around noon; multiplying these rates by the day length averaged over an annual period (12 h) can lead to an overestimation. The procedure of Cahoon (1999) was followed and a factor of 10 was used to convert hourly to daily rates for microphytobenthic gross primary production (GPP). The same approach was used for pelagic GPP estimates.

A large proportion of the annual primary production data (90% in the pelagos and 30% in the benthos) were measured using the $^{14}$C technique during incubations ranging from 1 to 24 h. It is well recognized that the $^{14}$C

<table><caption>Table 5
River basin attributes of the European coastal zone</caption><thead><tr><th>Variable</th><th>Baltic Sea</th><th>Mediterranean Sea</th><th>Black Sea</th><th>European Atlantic</th><th>Whole of Europe</th></tr></thead><tbody><tr><td>Total river basin area (10<sup>6</sup> km<sup>2</sup>) [17]</td><td>1.86</td><td>8.68</td><td>2.49</td><td>2.19</td><td>15.22</td></tr><tr><td>Total runoff (km<sup>3</sup> yr<sup>-1</sup>) [18]</td><td>429</td><td>788</td><td>413</td><td>793</td><td>2424</td></tr><tr><td>Total river basin population (10<sup>6</sup> inhabitants) [19]</td><td>92.6</td><td>360.8</td><td>187.2</td><td>251.8</td><td>892.4</td></tr><tr><td>Median river basin population density (inhabitants km<sup>-2</sup>) [20]</td><td>19.14</td><td>45.44</td><td>42.0</td><td>34.1</td><td>34.3</td></tr><tr><td>DIN yield (10<sup>3</sup> mol m<sup>-2</sup> yr<sup>-1</sup>)</td><td>10.2</td><td>6.1</td><td>11.2</td><td>20.1</td><td>9.5</td></tr><tr><td>DIP yield (10<sup>3</sup> mol m<sup>-2</sup> yr<sup>-1</sup>)</td><td>0.5</td><td>0.3</td><td>0.6</td><td>1.1</td><td>0.5</td></tr></tbody></table>

Numbers in brackets refer data sources listed in the appendix available at: http://wwwobs-vlfr.fr/~gattuso/ECSS_app.htm.
<table><caption>Table 6
Human attributes of coastal cells</caption><thead><tr><th>Variable</th><th>Baltic Sea</th><th>Mediterranean Sea</th><th>Black Sea</th><th>European Atlantic</th><th>Whole of Europe</th></tr></thead><tbody><tr><td>Total coastal population (million inhabitants) [21]</td><td>14.9</td><td>133.0</td><td>20.5</td><td>74.7</td><td>243.1</td></tr><tr><td>Coastal population density (inhabitants per km² land area) [22]</td><td>13.1</td><td>58.5</td><td>30.9</td><td>19.4</td><td>30.0</td></tr><tr><td>Cell road density (road area divided by land area in %) [23]</td><td>0.12</td><td>0.16</td><td>0.17</td><td>0.13</td><td>0.14</td></tr></tbody></table>

Numbers in brackets refer data sources listed in the appendix available at: http://wwwobs-vlfrfr/~gattuso/ECSS_app.htm.

technique measures something between gross and net primary production (Peterson, 1980), depending on the incubation time: short incubation times are closer to GPP whereas long incubation times are closer to net primary production (NPP). Only the rates of ¹⁴C uptake measured over an incubation period ≤6 h (90% of the total number of papers reporting ¹⁴C primary production) have been considered. It was assumed that they yield rates comparable to GPP estimated by the oxygen technique.

Benthic and pelagic community respiration (CR) were mainly measured by the oxygen method. In coastal areas, and especially within sediments, the oxygen concentration is sometimes too low to allow a complete aerobic mineralization of the organic matter and alternative oxidants are used through anoxic metabolic pathways (Thamdrup and Canfield, 2000). When there is no net accumulation of reduced metabolites, i.e. when anaerobic respiration products are completely reoxidized when they reach the sediment surface, the oxygen method is a reliable estimate of total mineralization processes, both aerobic and anaerobic.

Another oxygen consuming process can occur in coastal ecosystems receiving high loads of ammonium. Nitrification, the conversion of ammonium to nitrate, is the process by which chemoautotrophic bacteria obtain their energy to fix carbon. Even though this process demands significant amounts of oxygen and may lead to suboxic conditions, especially in eutrophic estuaries, it is an inefficient autotrophic process (Heip et al., 1995) and

<figure><img src="image_10.png" /><figcaption>Fig. 5. Number of papers present in the database and year of publication.</figcaption></figure>

was not considered in our study. As oxygen consumption (OC) values reported in eutrophic estuaries often include both respiration and nitrification processes, OC therefore can overestimate CR.

Sub-annual rather than annual values of processes are reported in about 30% of the studies; these were excluded from our analysis (see Figs. 5 and 6).

<figure><img src="image_11.png" /></figure>

<figure><img src="image_12.png" /><figcaption>Fig. 6. (A) Number of papers according to ecosystem types. (B) Number of papers reporting annual or sub-annual metabolic data in the pelagos, benthos or both.</figcaption></figure>
Use of the criteria set forth above reduced the number of usable references from 194 to 129. Additional data for pelagic GPP in the North and Baltic Seas (n = 73) were obtained from MADS (Den National Database for Marine Data, National Environmental Research Institute, Denmark, http://www.dmu.dk/forside_en.asp) and BIOMAD (Database on Marine Biological Monitoring Data, Department of Systems Ecology, Stockholm University, Sweden, http://www2.ecology.su.se/dbbm/index.shtml) databases.

### 3.1.2. Geographical location of the data and systems considered

Not surprisingly, the study sites are not evenly distributed in the EU coastal zone (Fig. 7); many more measurements are available from the North Sea and the Kattegat than elsewhere. The database has relatively few data from the Mediterranean region. Most data are concentrated on specific areas, such as river plumes; there is only one site from the northern African coast and none from the Black Sea region. About the same number of data are available for the pelagos (93 references) and for the benthos (87 references; Fig. 6A), while more importantly, relatively few studies report processes from both the water column and the benthos (14 references). The study sites were distributed across different coastal ecosystems or physiographic zones, including: estuary, river plume and macrophyte-dominated ecosystems. Study sites that could not be assigned to one of these categories were grouped in a 'shelf' category which, for our analysis, also included coastal lagoons and upwelling areas. Most data were collected from the shelf (118) and estuaries (41), with few studies from other categories (3–13; Fig. 6B).

### 3.2. Coastal zone systems other than estuaries

Metabolic data for the European coastal zone were considered in three regions: the Baltic Sea, Atlantic Ocean/North Sea area and the Mediterranean Sea. Each of these regions was divided into sub-regions in order to group areas sharing similar environmental settings or metabolic properties. The Kattegat was grouped with the Baltic Sea, rather than with the North Sea as was done in Section 2, to enable comparison with previous regional estimates (Wasmund et al., 2001). The surface area of the Baltic Sea sub-regions were taken from HELCOM (1996). The Black Sea was not considered because none of the publications considered met the set of criteria described above. Estuaries are considered in a separate section because they exhibit a range of variation and a magnitude of metabolic parameters much larger than other coastal systems.

#### 3.2.1. Pelagic gross primary production

The Baltic Sea is, by far, the most documented area in term of pelagic GPP rates in our database with 83 values including 28 in published papers and 55 extracted from the MADS and BIOMAD databases. Pelagic GPP is lowest in the Belt Sea (7.9 mmol C m⁻² d⁻¹; MADS database) and highest in the plume of the Oder river (96 mmol C m⁻² d⁻¹; Wasmund et al., 2001). Following the procedure of Wasmund et al. (2001), the Baltic was divided into five sub-regions (see Table 7) and the main river plumes (Vistula, Daugava and Oder river plumes) were considered separately. Our database does not include data for the Bothnian Bay and Bothnian Sea, both of which are said to be the least productive areas of the Baltic Sea (Elmgren, 1984; Kautsky and Kautsky,

<figure><img src="image_13.png" /><figcaption>Fig. 7. Location of sites with one or more entry in the database.</figcaption></figure>
<table><caption>Table 7
Annual pelagic gross primary production (GPP) in European coastal regions</caption><thead><tr><th rowspan="2"></th><th colspan="3">Annual pelagic<br>GPP<br>(mmol C m<sup>-2</sup> d<sup>-1</sup>)</th><th rowspan="2">Area<br>(km<sup>2</sup>)</th><th rowspan="2">Ref. no.</th></tr><tr><th>Mean</th><th>SD</th><th>N</th></tr></thead><tbody><tr><td colspan="6"><strong>Baltic Sea</strong></td></tr><tr><td colspan="6"><strong>Sub-regions</strong></td></tr><tr><td>Kattegat/Belt Sea</td><td>37</td><td>14</td><td>55</td><td>42508</td><td>1–7</td></tr><tr><td>Baltic proper</td><td>43</td><td>13</td><td>15</td><td>211069</td><td>1, 8–15</td></tr><tr><td>Gulf of Finland</td><td>25</td><td>5</td><td>3</td><td>29600</td><td>16–18</td></tr><tr><td>Bothnian Sea</td><td>12</td><td>—</td><td>1</td><td>79256</td><td>14</td></tr><tr><td>Bothnian Bay</td><td>4</td><td>—</td><td>1</td><td>36260</td><td>14</td></tr><tr><td colspan="6"><strong>River plumes</strong></td></tr><tr><td>Vistula plume</td><td>64</td><td>4</td><td>4</td><td>—</td><td>14, 19–21</td></tr><tr><td>Daugava plume</td><td>68</td><td>11</td><td>3</td><td>—</td><td>14, 22</td></tr><tr><td>Oder plume</td><td>96</td><td>—</td><td>1</td><td>—</td><td>14</td></tr><tr><td>Weighted average<br>and total Baltic<br>Sea region</td><td>31</td><td>—</td><td>83</td><td>398693</td><td></td></tr><tr><td colspan="6"><strong>European Atlantic and North Sea</strong></td></tr><tr><td colspan="6"><strong>Sub-regions</strong></td></tr><tr><td>North Sea</td><td>48</td><td>13</td><td>28</td><td>454832</td><td>1, 23–30</td></tr><tr><td>English Channel</td><td>40</td><td>18</td><td>5</td><td>71175</td><td>31–34</td></tr><tr><td>Irish Sea</td><td>25</td><td>7</td><td>4</td><td>107051</td><td>35–38</td></tr><tr><td>Atlantic coast</td><td>60</td><td>12</td><td>5</td><td>594642</td><td>39–41</td></tr><tr><td colspan="6"><strong>Upwelling</strong></td></tr><tr><td>Ría of Vigo</td><td>110</td><td>6</td><td>2</td><td>—</td><td>42, 43</td></tr><tr><td>Weighted average<br>and total European<br>Atlantic and North<br>Sea regions</td><td>51</td><td>—</td><td>44</td><td>1227700</td><td></td></tr><tr><td colspan="6"><strong>Mediterranean Sea</strong></td></tr><tr><td colspan="6"><strong>Sub-regions</strong></td></tr><tr><td>Western region</td><td>20</td><td>5</td><td>8</td><td>198163</td><td>44–51</td></tr><tr><td>Northern Adriatic<br>Sea</td><td>48</td><td>—</td><td>1</td><td>72536</td><td>52</td></tr><tr><td>Eastern region</td><td>11</td><td>5</td><td>5</td><td>172871</td><td>53–57</td></tr><tr><td colspan="6"><strong>River plumes</strong></td></tr><tr><td>Rhône river plume</td><td>160</td><td>70</td><td>2</td><td>—</td><td>58, 59</td></tr><tr><td>Po river plume</td><td>134</td><td>—</td><td>1</td><td>—</td><td>52</td></tr><tr><td colspan="6"><strong>Coastal lagoons</strong></td></tr><tr><td>Gulf of Fos</td><td>150</td><td>—</td><td>1</td><td>—</td><td>60</td></tr><tr><td>Berre Lagoon</td><td>59</td><td>10</td><td>2</td><td>—</td><td>51, 61</td></tr><tr><td>Weighted average<br>and total<br>Mediterranean<br>region</td><td>21</td><td>—</td><td>20</td><td>443570</td><td></td></tr><tr><td>Weighted average<br>and total European<br>coastal zone</td><td>41</td><td>—</td><td>147</td><td>2069963</td><td></td></tr></tbody></table>

The list of references is available at http://www.obs-vlfr.fr/~gattuso/ECSS_ref.htm.

2000; Wasmund et al., 2001). Therefore, the same values as Wasmund et al. (2001) were used for the Bothnian Sea (12 mmol C m⁻² d⁻¹) and the Bothnian Bay (4 mmol C m⁻² d⁻¹). The highest values of GPP were found in river plume areas. Due to their relative small surface area, these ecosystems will not be included in our

estimation. Indeed, Wasmund et al. (2001) reported that a separate treatment of river plumes is not necessary for whole Baltic Sea primary production estimates. Pelagic GPP of the Kattegat and Belt Sea areas, based on 55 values, reaches 37 (±14) mmol C m⁻² d⁻¹, a value slightly lower than the one used by Wasmund et al. (2001) which was based on only one reference (43 mmol C m⁻² d⁻¹; Heilman et al., 1994). The mean GPP of the Baltic proper (15 values; 43±13 mmol C m⁻² d⁻¹) is higher than that of the Kattegat and Belt Sea areas and consistent with the value used by Wasmund et al. (2001) in their global estimate, and with the estimate of Shaffer (1987). The mean value found for the Gulf of Finland, based on only 3 references, is about 25 (±5) mmol C m⁻² d⁻¹. Our database does not include data from the Neva River plume entering the Gulf of Finland which was therefore excluded from our study. Considering the surface area and GPP values for each of these sub-regions, a weighted average of the whole Baltic Sea pelagic GPP of 31 mmol C m⁻² d⁻¹ is proposed Wasmund et al. (2001) proposed a pelagic GPP of 34 mmol C m⁻² d⁻¹ for the whole Baltic Sea, based on their measurements between 1993 and 1997 in the south-eastern Baltic Sea as well as data from literature. The pelagic GPP values reported by Elmgren (1984) are also consistent with our estimate.

In the Atlantic/North Sea region, 44 values were found including 18 extracted from the MADS database. The lowest value was reported for western Scotland (16 mmol C m⁻² d⁻¹; Wood et al., 1973) and the highest for Ría de Vigo, an upwelling area in north-western Spain (114 mmol C m⁻² d⁻¹; Moncoiffé et al., 2000). This region was divided in 4 areas: North Sea, English Channel, Irish Sea and Atlantic coast. The North Sea is the most documented area in this region (28 measurements) but no data were found for the northern part; its mean GPP is 48 (±13) mmol C m⁻² d⁻¹ (Table 7). The mean GPP of the English Channel is about 40 (±18) mmol C m⁻² d⁻¹ (5 values). The Irish Sea is the least productive area in north-western Europe with a mean value of 25 (±7) mmol C m⁻² d⁻¹ based on four annual measurements. Upwelling areas should be considered separately but this is not possible at this stage because of the lack of data and also the unknown surface area covered by upwellings in European waters. Data from the Ría of Vigo were therefore excluded from the analysis in order to avoid a bias. The average annual value for the Atlantic coast is about 60 (±12) mmol C m⁻² d⁻¹. A surface-weighted average pelagic GPP for the Atlantic/North Sea region of 51 mmol C m⁻² d⁻¹ was estimated. To the best of our knowledge, this is the first global estimate of pelagic GPP available for the region. In their review, Reid et al. (1990) estimated 40, 57 and 46 mmol C m⁻² d⁻¹, respectively in the northern, central and southern North Sea. Also, Joint and Pomroy (1993) gave regional estimates based on the
ICES sub-divisions of the North Sea, but their measure-
ments (from 24 h incubations) were closer to NPP than
GPP and thus, are not comparable with our estimate.

The Mediterranean Sea was divided into three basins: western (excluding the Rhône River plume), northern Adriatic Sea (excluding the Po River plume) and eastern basins. Pelagic GPP in the region is low, especially in the eastern basin which was characterized by Azov (1991) as a ‘marine desert’ resulting from phosphorus deficiency (Krom et al., 1991). The lowest value was found near the Israeli coast (4.3 mmol C m⁻²d⁻¹; Berman and Townsend, 1984) and the highest in the Cretan Sea (18 mmol C m⁻²d⁻¹; Psarra et al., 2000). The mean GPP for this area is based on 5 references and reaches a value of 11 (±5) mmol C m⁻²d⁻¹ (see Table 7). The northern Adriatic Sea is one of the most productive areas in the Mediterranean (Sournia, 1973), with a production rate of about 48 mmol C m⁻²d⁻¹. It receives the discharge from the Po River and phosphorus recycling is supposed to be very fast, decreasing the phosphorus limitation in this part of the Mediterranean Sea (Ivancic and Degobbis, 1987). The plume of the Po River has a very high production rate (134 mmol C m⁻²d⁻¹; Puddu et al., 1998). The north-western basin is the most documented in our database, with the lowest GPP reported along the Spanish coast (16 mmol C m⁻²d⁻¹; Margalef and Ballester, 1967; San Feliu and Muñoz, 1970) and the highest in the Rhône dilution plume (205 mmol C m⁻²d⁻¹; Lefèvre et al., 1997). In their recent review, Lefèvre et al. (1997) made an extensive compilation of available primary production data in the Gulf of Lions, dividing the coastal zone of this sub-region into three provinces based on hydrological features: (1) the Gulf of Marseille with a GPP of 20 mmol C m⁻²d⁻¹, (2) the Rhône River plume with very high values (70–340 mmol C m⁻²d⁻¹) and (3) the ‘Rhône River dilution zone’ with intermediate rates (26 mmol C m⁻²d⁻¹). Furthermore, these authors reported no significant increase in GPP over the last 30 years, indicating that this part of the Mediterranean Sea is less influenced by catchment-based human activities than other coastal areas of Europe. The mean GPP (excluding the Rhône River plume) estimated from our database for this area is based on eight references and reaches a value of 20 (±5) mmol C m⁻²d⁻¹ (see Table 7). Coastal lagoons in this region exhibit higher production rates, i.e. 150 and 59 mmol C m⁻²d⁻¹ for the Gulf of Fos and the Berre lagoon, respectively (Minas, 1976; Kim, 1983; Barranguet et al., 1996), and considering their small area, are not considered in our global estimate. A wider study of the metabolic performance of coastal lagoons adjacent to the Mediterranean Sea is in progress using the LOICZ approach; see the LaguNet web site at http://www.dsa.unipr.it/lagunet/. The present version of the database does not include any data from the southwestern basin. One data point was found (46 mmol C

m⁻²d⁻¹; Tellaï, 1969) but it was not included in the
database because the original paper is not available to us
and the data, obtained from a secondary source, could
not be checked. Weighing these rates according to the
surface areas represented by each sub-region, yielded
a first estimation of pelagic GPP (21 mmol C m⁻²d⁻¹)
for the coastal Mediterranean Sea, confirming its oligo-
trophic status (Nixon, 1995).

Thus, a pelagic GPP in European coastal waters of about 41 mmol C m⁻²d⁻¹ was estimated (see Table 7 and Fig. 8A for frequency distribution). Smith and Hollibaugh (1993), Wollast (1998) and Gattuso et al. (1998) estimated the global GPP of continental shelves as 37, 46 and 49 mmol C m⁻²d⁻¹ respectively. Our estimate for European open coastal waters is consistent with these global estimates.

Most of the primary production values used in this
review were estimated by the ¹⁴C-tracer method and the
difficulties for interpreting these data were discussed
above. Moreover, almost all studies dealt only with
particulate primary production. It is now well accepted
that dissolved compounds released by phytoplankton
can represent a significant portion of the produced
organic matter. Indeed, Holligan (1989), Morán et al.
(2002), Witek et al. (1999), and Larsson and Hagström
(1982) reported dissolved primary production values of
10%, 16%, 5% and 14% of the total primary pro-
duction in the North Sea, the north-western Mediterra-
nean Sea, Gulf of Gdánsk and Baltic proper, while very
high rates (up to 30%) were recorded in summer in the
Gulf of Finland (Kuparinen, 1987). Dissolved pro-
duction by phytoplankton on a global scale remains
poorly known, but Morán et al. (2002) found a signif-
icant inverse relationship between PER (percent extra-
cellular release) and total system productivity whereby
there is higher PER in oligotrophic environments, con-
firming earlier results from Fogg (1983). Data on the
relative contributions of dissolved and particulate pro-
duction to GPP are too scarce to attempt an estimation
of the importance of dissolved production in our value
of GPP. However, our estimates clearly underestimate
GPP, especially in low productivity waters, such as the
eastern Mediterranean and Baltic Seas regions.

3.2.2. *Microphytobenthic gross primary production*

Fewer annual studies of benthic GPP in coastal areas
of Europe were found in the literature compared with
pelagic GPP. The database presently comprises 40
annual measurements (both in shallow and deep areas),
but study sites are not well distributed within the region
of interest. For instance, as already reported by Cahoon
(1999), no data were found for the entire eastern Medi-
terranean Sea nor for the eastern Baltic Sea. Presumably
these two regions have low GPP values due to light
limitation in the eastern Baltic and nutrient limitation in
the eastern Mediterranean Sea. Such lack of information
<figure><img src="image_14.png" /><figcaption>Fig. 8. Frequency distribution of (A) pelagic gross primary production, (B) benthic gross primary production, and (C) community respiration in estuaries (black bars) and open shelf systems (open bars).</figcaption></figure>

of course will negatively affect upscaling. In contrast with data on pelagic GPP, most of the studies are based on the oxygen method (70%).

Calculation of depth-integrated GPP requires either data across the depth range or information on the decrease of GPP as a function of depth, the deepest

benthic production (6 mmol C m⁻² d⁻¹) being measured in the Gulf of Trieste at a depth of 22 m (Herndl et al., 1989). However, very few studies have investigated the decrease of GPP with depth although benthic GPP is assumed to occur at depths greater than 20 m (Cahoon, 1999). Data for the three major regions show different
<figure><img src="image_15.png" /><figcaption>Fig. 9. Decrease with depth of microphytobenthic gross primary production (GPP) in the Baltic Sea, based on data from Gargas (1970), Sundbäck and Jönsson (1988), and Meyercordt and Meyer-Reil (1999).</figcaption></figure>

depth ranges; 22 m in the Mediterranean Sea and 20 m in the Baltic Sea regions, but only 5 m in the Atlantic/ North Sea region. In the latter and the Baltic Sea regions, the same function for decrease of benthic GPP with depth was used. Depth-integrated (0–200 m) GPP was calculated by the relationship between GPP (% of maximal value) and depth (see Fig. 9) derived in the Baltic Sea using data from Gargas (1970), Sundbäck and Jönsson (1988), and Meyercordt and Meyer-Reil (1999): $%P_{max} = -28.894 \times LN$ (Depth) + 97.966 ($r^2 = 0.7863$, $P < 0.01$, $n = 17$; LN is the natural logarithm).

In the Mediterranean Sea, where water column turbidity is lower, GPP was estimated at three depth ranges (0–5 m, 5–10 m and 10–30 m) from published data, and the depth-integrated GPP (0–200 m) was calculated assuming that GPP is 0 below 30 m.

Benthic GPP exhibits high geographical variations in the Baltic Sea, with no production found at 3.4 m in Kirr-Bucht, Darss-Zingst Bodden, southern Baltic Sea (Meyercordt and Meyer-Reil, 1999) and the highest value reported in Faellesstrand lagoon, Denmark (34 mmol C m⁻² d⁻¹; Kristensen, 1993). Thus, the shallow (0–5 m) benthic production for this region (14±12 mmol C m⁻² d⁻¹, Table 8) must be taken with caution. Averaged over the 0–20 m zone and weighted by the surface of the coastal areas with depths <20 m, the average microphytobenthic GPP of the Baltic Sea is about 2 mmol C m⁻² d⁻¹ (Table 8), only 4% of the pelagic GPP. Our estimate is lower than that of Cahoon (1999) (4 mmol C m⁻² d⁻¹) but similar to that of Elmgren (1984) (1.2 mmol C m⁻² d⁻¹) for the whole Baltic Sea benthic compartment (including the macrophytobenthos).

The Atlantic/North Sea and Mediterranean regions are less documented than the Baltic Sea. Both regions exhibit low variation, with mean values of 22 (±5) mmol C m⁻² d⁻¹ and 16 (±6) mmol C m⁻² d⁻¹ in shallow areas of the Atlantic/North Sea and Mediterranean Sea regions (Table 8 and Fig. 8B for frequency

distribution). Using the relationship described above, a microphytobenthic GPP in the Atlantic/North Sea of about 1 mmol C m⁻² d⁻¹ (2% of the pelagic GPP) was estimated.

It must be stressed that few data are available for the Mediterranean Sea region and may not be representative of the whole area. The average benthic GPP in the Mediterranean Sea declines from 16 (±6) mmol C m⁻² d⁻¹ in the depth range 0–5 m to 5 (±1) mmol C m⁻² d⁻¹ at 10–30 m (Table 8). The depth-integrated benthic GPP is around 2.5 mmol C m⁻² d⁻¹ in the Mediterranean Sea (13% of pelagic GPP), lower than the value estimated by Cahoon (1999) (4 mmol C m⁻² d⁻¹). Cahoon (1999) and Charpy-Roubaud and

<table><caption>Table 8
Annual microphytobenthic gross primary production (GPP) in European coastal regions</caption><thead><tr><th rowspan="2"></th><th colspan="3">Annual microphytobenthic GPP (mmol C m<sup>-2</sup> d<sup>-1</sup>)</th><th rowspan="2">Area (km<sup>2</sup>)</th><th rowspan="2">Ref. no.</th></tr><tr><th>Mean</th><th>SD</th><th>N</th></tr></thead><tbody><tr><td>Baltic Sea</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>0–5 m</td><td>14</td><td>12</td><td>17</td><td>61706</td><td>2, 13, 62–68</td></tr><tr><td>0–200 m</td><td>2</td><td>—</td><td>—</td><td>398693</td><td></td></tr><tr><td>Atlantic/North Sea</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>0–5 m</td><td>22</td><td>5</td><td>8</td><td>55750</td><td>27, 69–74</td></tr><tr><td>0–200 m</td><td>1</td><td>—</td><td>—</td><td>1227700</td><td></td></tr><tr><td>Mediterranean Sea</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>0–5 m</td><td>16</td><td>6</td><td>5</td><td>35632</td><td>60, 75, 76</td></tr><tr><td>5–10 m</td><td>11</td><td>9</td><td>2</td><td>16565</td><td>60, 77</td></tr><tr><td>10–30 m</td><td>5</td><td>1</td><td>3</td><td>71625</td><td>60, 77</td></tr><tr><td>0–200 m</td><td>2.5</td><td>—</td><td>—</td><td>443570</td><td></td></tr><tr><td>Weighted average and total European coastal zone</td><td>1.5</td><td>—</td><td>—</td><td>2069963</td><td></td></tr></tbody></table>

The list of references is available at http://wwwobs-vlfr.fr/~gattuso/ECSS_ref.htm.
Sournia (1990) reported mean values of benthic primary production for worldwide temperate shallow areas (all ecosystem types included) of around 20 mmol C m⁻²d⁻¹ and 23 mmol C m⁻²d⁻¹, respectively. Our estimate (mean value for the 0–5 m depth range in European coastal waters: 17 mmol C m⁻²d⁻¹) is slightly lower, and certainly due to our separate consideration of shelves and estuaries which present higher production values (see next section).

Finally, the average microphytobenthic GPP along European coastlines (0–200 m) is about 1.5 mmol C m⁻²d⁻¹ (Table 8; 3.6% of pelagic GPP), lower than values estimated for worldwide continental shelves by Cahoon (1999) for temperate regions and Charpy-Roubaud and Sournia (1990).

### 3.2.3. Macrophytobenthic net primary production

Macrophyte (seagrass and macroalgae) beds are expected to be very productive areas. Indeed, Charpy-Roubaud and Sournia (1990) reported NPP values in temperate regions from 100 to >450 mmol C m⁻²d⁻¹, mainly from intertidal or shallow areas. They estimated a production value in the 0–50 m depth fringe of about 170 mmol C m⁻²d⁻¹ (vs. 11 mmol C m⁻²d⁻¹ for microphytobenthos), but their procedure for estimating the decrease in production with depth is not clear.

GPP by macrophytes was not uspscaled to the whole European coastal zone for three reasons: (i) very few annual studies were found in the literature for these areas (five to date), (ii) the distribution and production of macrophytes along the depth gradient is not resolved and (iii) the surface area covered by macrophytes in Europe is not yet estimated (Duarte, personal communication, 2003).

Also primary production by macrophytes seems to be relatively small in several European coastal systems. Wasmund (1986) estimated that micro- and macrophytobenthos contribute 7% of total NPP in shallow coastal lagoons of the Baltic Sea and Elmgren (1984) attributed 3% of total NPP to phytobenthos in the whole Baltic Sea. In the Wadden Sea (North Sea), where tidal flats represent approximately 50% of the surface area (Cadée and Hegeman, 1974), macroalgal production is negligible (Cadée, 1980).

The surface area potentially covered by the seagrass *Posidonia oceanica* in the Mediterranean Sea is about 0.035×10⁶ km² (Pasqualini et al., 1998), or only 8% of the surface area of the Mediterranean coastal zone. This value is similar to that of Whittaker and Likens (1975) for the global distribution of macrophytes. The depth-integrated (0–200 m) NPP (leaves plus rhizomes) for *P. oceanica* is about 1 mmol C m⁻²d⁻¹ in the coastal Mediterranean Sea, based on data for 22 sites at three different depths (Pergent-Martini et al., 1994) and for the Bay of Calvi (Corsica) at 30 m (Bay, 1984) (see Table 9 for calculation details). It is difficult to compare this

<table><caption>Table 9
Annual net primary production by *Posidonia oceanica* (leaves plus rhizomes) in the Mediterranean coastal area based on values from Pergent-Martini et al. (1994) at 5, 10 and 20 m and Bay (1984) at 30 m</caption><thead><tr><th>Depth range (m)</th><th>Measured depth (m)</th><th>Annual NPP (mmol C m<sup>-2</sup> d<sup>-1</sup>)<sup>a</sup></th><th>Area<sup>b</sup> (km<sup>2</sup>)</th></tr></thead><tbody><tr><td>0–7.5</td><td>5</td><td>73 (53–93)</td><td>3173</td></tr><tr><td>7.5–15</td><td>10</td><td>45 (35–55)</td><td>2340</td></tr><tr><td>15–25</td><td>20</td><td>20 (18–22)</td><td>2725</td></tr><tr><td>25–35</td><td>30</td><td>13.2<sup>c</sup></td><td>2318</td></tr><tr><td>Weighted average and total Mediterranean Sea region</td><td>0–200</td><td>1</td><td>445883</td></tr></tbody></table>

<sup>a</sup> Assuming a dry weight carbon content of 40% (Mateo and Romero, 1997).

<sup>b</sup> Assuming that 8% of the Mediterranean coastline is covered by *P. oceanica* (Pasqualini et al., 1998).

<sup>c</sup> Leaf blades NPP was reported (12.4 mmol C m⁻²d⁻¹). According to Pergent-Martini et al. (1994), rhizomes NPP represents 6.4% of leaf NPP.

value to the total (pelagic + benthic) net primary production in the Mediterranean Sea region but, assuming that phytoplankton and microphytobenthos respiration (R) ranges between 5 and 50% of GPP, the contribution of *P. oceanica* to the total NPP was estimated to lie between 5 and 10%. This value contrasts strongly with the 40% of total NPP estimated for worldwide continental shelves (Charpy-Roubaud and Sournia, 1990).

### 3.2.4. Pelagic community respiration

Very few measurements of depth-integrated community respiration (CR) based on the oxygen incubation method, even in the euphotic zone, were found during our compilation of data. Moreover, in contrast to primary production, planktonic CR occurs throughout the water column (Williams, 1984), and it is therefore not possible to compare rates integrated over different depth ranges. Consequently, CR is shown in volumetric units in Table 10 (µmol C l⁻¹ d⁻¹) when directly measured by the oxygen bottle method in the euphotic or aphotic zone (two references only for the latter). When only integrated values were reported, these were divided by the depth of the water column, assuming a constant rate over that depth range.

In the Baltic Sea, measurements of pelagic CR were made in the euphotic zone of the Gulf of Finland (Kuparinen, 1984; Kuparinen, 1987). These data, together with the GPP data discussed above, enable estimation of how much of GPP is remineralized in the upper water column. The euphotic CR represents 34% of the pelagic GPP integrated over the euphotic layer (10 m; GPP = 25 mmol C m⁻²d⁻¹). Therefore, net community production (NCP = GPP - CR) in the euphotic zone is 66% of pelagic GPP. Furthermore, Kuparinen et al. (1984) speculated that pelagic CR in the aphotic zone
<table><caption>Table 10
Annual pelagic community respiration (CR) in European coastal regions</caption><thead><tr><th>Region</th><th>Depth layer (m)</th><th>Annual pelagic CR (µmol C l<sup>-1</sup> d<sup>-1</sup>)</th><th>Ref. no.</th></tr></thead><tbody><tr><td colspan="4"><strong>Baltic Sea</strong></td></tr><tr><td>Gulf of Finland</td><td>Euphotic (0–10 m)</td><td>0.9</td><td>16</td></tr><tr><td>Gulf of Finland</td><td>Euphotic (0–10 m)</td><td>0.8</td><td>17</td></tr><tr><td>Gulf of Gdánsk</td><td>Euphotic (0–7 m)</td><td>14.8</td><td>78</td></tr><tr><td>Gulf of Gdánsk</td><td>Euphotic (2.5 m)</td><td>11.2</td><td>79</td></tr><tr><td>Kattegat</td><td>Aphotic (15–30 m)</td><td>1.3</td><td>80</td></tr><tr><td>Kattegat</td><td>Aphotic (15–25 m)</td><td>2.2</td><td>4</td></tr><tr><td>Pomeranian Bay</td><td>Epipelagique (0–20 m)</td><td>4.3</td><td>15</td></tr><tr><td>Gulf of Gdánsk</td><td>Water column</td><td>2.7</td><td>19</td></tr><tr><td colspan="4"><strong>Atlantic/North Sea</strong></td></tr><tr><td>North Sea</td><td>Euphotic (15 m)</td><td>2.6</td><td>81</td></tr><tr><td>North Sea</td><td>Water column (0–50 m)</td><td>2.4</td><td>82</td></tr><tr><td>Bay of Biscay</td><td>Euphotic (0–20 m)</td><td>1.8</td><td>41</td></tr><tr><td>Ría de Vigo</td><td>Euphotic (0–12 m)</td><td>4</td><td>42</td></tr><tr><td colspan="4"><strong>Mediterranean Sea</strong></td></tr><tr><td>Bay of Blanes</td><td>Euphotic (15 m)</td><td>5.2</td><td>83</td></tr><tr><td>Bay of Calvi</td><td>Euphotic (0–15 m)</td><td>6.2</td><td>84</td></tr><tr><td>Gulf of Lions</td><td>Euphotic (0–60 m)</td><td>3.5</td><td>58</td></tr></tbody></table>

The list of references is available at http://wwwobs-vlfrfr/~gattuso/ECSS_ref.htm.

(>10 m) is 50% of the euphotic NCP (30% of pelagic GPP). Thus, the amount of organic matter remineralized in the whole water column is about 70% of pelagic GPP. This result is consistent with the one found by Elmgren (1984) who used data from sediment traps in the whole Baltic Sea to estimate organic matter utilization in the whole water column of about 60% of pelagic GPP. Rydberg et al. (1990) estimated CR rates in aphotic deep waters of the south-eastern Kattegat. Based on their results and pelagic GPP estimated for this region (36 mmol C m<sup>-2</sup> d<sup>-1</sup>), the amount of organic matter remineralized in the aphotic deep-water column is estimated to 30%. In the same area, using data from Granéli (1992), a somewhat higher value of 45% of pelagic GPP was found. Based on indirect methods in the Baltic proper, Shaffer (1987), Rahm (1987), and Pers and Rahm (2000) estimated organic matter mineralization in aphotic deep-waters below the S=8 isohaline of 12, 11.5 and 10.5 mmol C m<sup>-2</sup> d<sup>-1</sup> (RQ=1). This

corresponds to about 25% of the pelagic GPP for this region and is consistent with the value found by Olesen and Lundsgaard (1995) in the Kattegat.

CR is much higher in the Gulf of Gdánsk (Witek et al., 1997; Witek et al., 1999; York et al., 2001) and the Pomeranian Bay (Witek et al., 2001), especially in surface waters. These systems receive high loads of organic matter from the Vistula and Oder rivers and CR integrated over the entire water column is higher than autochthonous production of organic matter over most of the year.

In the Atlantic/North Sea region, only four annual values were found, all measured in the euphotic zone. The lowest value was found in the Bay of Biscay (1.8 µmol C l<sup>-1</sup> d<sup>-1</sup>; Serret et al., 1999) and the highest value in the upwelling area of the Ría de Vigo (4 µmol C l<sup>-1</sup> d<sup>-1</sup>; Moncoiffé et al., 2000). CR data for the Mediterranean Sea region are high with the highest value reported for the Bay of Calvi (6.2 µmol C l<sup>-1</sup> d<sup>-1</sup>; Velimirov and Walenta-Simon, 1992). As these data were obtained in areas supporting relatively high rates of pelagic and benthic GPP, they may not be representative of the Mediterranean Sea region as a whole.

Measurements of pelagic CR in the European coastal zone are clearly too sparse to yield an accurate picture of the fate of organic matter produced in the water column. However, previous considerations of the Baltic Sea (excluding river plumes and mainly based on indirect methods) suggest that roughly 60% of pelagic GPP is consumed in the water column (30% in the euphotic and 30% in the aphotic zones). This is higher than previous estimates of coastal mineralization rates (Gattuso et al., 1998; Wollast, 1998) that indicate only 30% of the autochthonous production is consumed in the water column.

### 3.2.5. Benthic community respiration

The average benthic CR in the Atlantic/North Sea and Baltic Sea regions are 16 (±8, n = 17) and 17 mmol C m<sup>-2</sup> d<sup>-1</sup> (±8, n = 20; Table 11). Benthic CR rates from literature are not well distributed within regions, especially in the Baltic Sea where no data were found for the entire eastern Baltic Sea (Baltic proper, Gulf of Finland, Bothnian Sea and Bothnian Bay). Respiration rates are temperature-dependent but also controlled by the quality and quantity of organic matter available. Thus, lower rates should be found in these low productive regions, and our value of 17 mmol C m<sup>-2</sup> d<sup>-1</sup> may be slightly overestimated.

As with other metabolic parameters, few benthic CR measurements have been conducted in the Mediterranean Sea region (10 data points or sets were found), the most documented area being the northern Adriatic Sea (6 values) but no data were found for the most oligotrophic part (eastern basin). Thus, our estimates should be considered tentative and subject to uncertainty. The highest benthic CR rates were reported in coastal lagoons, Thau lagoon (31 mmol C m<sup>-2</sup> d<sup>-1</sup>;
<table><caption>Table 11
Annual benthic community respiration (CR) in European coastal regions</caption><thead><tr><th rowspan="2"></th><th colspan="3">Annual benthic CR (mmol C m<sup>-2</sup> d<sup>-1</sup>)</th><th rowspan="2">Area (km<sup>2</sup>)</th><th rowspan="2">Ref. no.</th></tr><tr><th>Mean</th><th>SD</th><th>N</th></tr></thead><tbody><tr><td>Baltic Sea</td><td>17</td><td>8</td><td>20</td><td>398693</td><td>4, 13, 19, 66–68, 80, 85–90</td></tr><tr><td>North Sea/Atlantic</td><td>16</td><td>8</td><td>17</td><td>1227700</td><td>28, 38, 87, 91–97</td></tr><tr><td>Mediterranean Sea</td><td>22</td><td>6</td><td>10</td><td>443570</td><td>60, 76, 77, 98–101</td></tr><tr><td>Weighted average and total European coastal zone</td><td>17</td><td></td><td></td><td>2069963</td><td></td></tr></tbody></table>

The list of references is available at http://wwwobs-vlfrfr/~gattuso/ECSS_ref.htm.

Barranguet et al., 1994) in France and Saca di Goro (55 mmol C m⁻² d⁻¹; Bartoli et al., 1996) in the northern Adriatic Sea. The benthic CR for the entire Mediterranean Sea region weighted according to surface area is 22 mmol C m⁻² d⁻¹. The weighted average of the three regions provides a benthic CR value of 17 mmol C m⁻² d⁻¹ for shelf areas in Europe (see also Fig. 8C for frequency distribution).

Based on a global benthic CR dataset, Middelburg et al. (2004) proposed a similar value for global coastal benthic CR (17 mmol C m⁻² d⁻¹). Gattuso et al. (1998) and Wollast (1998) reported benthic mineralization of about 30% of pelagic GPP. The benthic CR rate estimated in our study represents 40% of the estimated pelagic GPP (41 mmol C m⁻² d⁻¹). It should be noted that almost all the compiled data were collected in shallow areas where available organic matter and the rate of mineralization are probably higher. Since the ratio benthic: pelagic mineralization decreases with increasing depth (Jørgensen, 1983; Heip et al., 1995), a significant overestimation might be expected. On the other hand, several studies showed that the oxygen method can strongly underestimate total carbon mineralization rates in low oxygen environments because reduced metabolites cannot be completely reoxidized. For instance, Jørgensen (1982) estimated that sulfide burial resulting from net sulfate reduction can represent 10% of carbon mineralization. Overall, our estimate that benthic CR is 40% of pelagic GPP is the best present estimate of benthic mineralization in European coastal areas.

### 3.3. Estuaries

Estuaries are the main transition zone between the freshwater of the land and the salt water of the oceans (Heip et al., 1995). Receiving high amounts of nutrient,

organic matter and suspended particles, estuaries are extremely dynamic systems usually characterized by strong physico-chemical gradients, enhanced biological activity, and intense sedimentation and resuspension (Ketchum, 1983). Our database contains metabolic values from 29 papers in which benthic measurements (GPP and CR) represent almost 70% of available annual values. One of the striking outcomes (Table 12 and Fig. 8) is the strong variability in pelagic GPP compared to intertidal or shallow benthic GPP. Pelagic values range from 1.7 (Ems-Dollard estuary; Van Es, 1977) to 153.3 mmol C m⁻² d⁻¹ in the highly productive Urdaiäß estuary (Revilla et al., 2002). The smaller range of benthic GPP extends from 22.3 mmol C m⁻² d⁻¹ in the Colne River estuary (Thornton et al., 2002) to 37.8 mmol C m⁻² d⁻¹ in the western Scheldt estuary (Barranguet et al., 1998). The average benthic GPP of 31 (±5) mmol C m⁻² d⁻¹ is almost twice the benthic GPP estimated in intertidal or shallow open shelf areas (see previous section). This supports our approach of investigating and synthesizing separately the open shelves and

<table><caption>Table 12
Annual community metabolism rates in European estuaries (mmol C m⁻² d⁻¹)</caption><thead><tr><th>Site</th><th>Pelagic GPP</th><th>Benthic GPP</th><th>Pelagic CR</th><th>Benthic CR</th><th>Ref. no.</th></tr></thead><tbody><tr><td>Western Scheldt</td><td>40.4</td><td>—</td><td>—</td><td>—</td><td>102</td></tr><tr><td>Western Scheldt</td><td>—</td><td>31</td><td>—</td><td>—</td><td>103</td></tr><tr><td>Western Scheldt</td><td>52.7</td><td>—</td><td>—</td><td>—</td><td>104</td></tr><tr><td>Western Scheldt</td><td>—</td><td>37.8</td><td>—</td><td>—</td><td>105</td></tr><tr><td>Western Scheldt</td><td>—</td><td>—</td><td>—</td><td>194.2</td><td>106</td></tr><tr><td>Eastern Scheldt</td><td>75.7</td><td>—</td><td>—</td><td>—</td><td>107</td></tr><tr><td>Eastern Scheldt</td><td>—</td><td>35.6</td><td>—</td><td>—</td><td>108</td></tr><tr><td>Ems-Dollard</td><td>1.7</td><td>26.7</td><td>20.8</td><td>44.7</td><td>109</td></tr><tr><td>Ems-Dollard</td><td>—</td><td>36</td><td>—</td><td>40.5</td><td>110</td></tr><tr><td>Ems-Dollard</td><td>—</td><td>22.6</td><td>—</td><td>—</td><td>111</td></tr><tr><td>Ems-Dollard</td><td>3</td><td>—</td><td>—</td><td>—</td><td>69</td></tr><tr><td>Ems-Dollard</td><td>—</td><td>36.4</td><td>—</td><td>47.5</td><td>112</td></tr><tr><td>Norsminde Fjord</td><td>—</td><td>—</td><td>—</td><td>40.1</td><td>113</td></tr><tr><td>Norsminde Fjord</td><td>—</td><td>—</td><td>—</td><td>52</td><td>114</td></tr><tr><td>Limforden</td><td>—</td><td>—</td><td>—</td><td>34</td><td>115</td></tr><tr><td>Bristol Channel</td><td>17</td><td>—</td><td>—</td><td>—</td><td>116</td></tr><tr><td>Ythan</td><td>—</td><td>26.5</td><td>—</td><td>—</td><td>117</td></tr><tr><td>Lynher</td><td>18.5</td><td>32.6</td><td>—</td><td>—</td><td>118</td></tr><tr><td>Thames</td><td>—</td><td>—</td><td>—</td><td>64</td><td>119</td></tr><tr><td>Colne</td><td>—</td><td>22.3</td><td>—</td><td>65.1</td><td>120</td></tr><tr><td>Colne</td><td>2</td><td>—</td><td>—</td><td>—</td><td>121</td></tr><tr><td>Southampton water</td><td>40.4</td><td>—</td><td>—</td><td>—</td><td>34</td></tr><tr><td>Great Ouse</td><td>—</td><td>—</td><td>—</td><td>79.5</td><td>122</td></tr><tr><td>Great Ouse (Upper)</td><td>—</td><td>—</td><td>—</td><td>64</td><td>123</td></tr><tr><td>Urdaiäß</td><td>153.3</td><td>—</td><td>84.4</td><td>—</td><td>124</td></tr><tr><td>Douro</td><td>—</td><td>30</td><td>—</td><td>26.4</td><td>125</td></tr><tr><td>Tagus</td><td>—</td><td>35.6</td><td>—</td><td>—</td><td>126</td></tr><tr><td>Tagus</td><td>—</td><td>—</td><td>—</td><td>37.5</td><td>127</td></tr><tr><td>Elbe</td><td>—</td><td>26.4</td><td>—</td><td>—</td><td>128</td></tr><tr><td>Mean (SD)</td><td>40 (47)</td><td>31 (5)</td><td>53 (45)</td><td>61 (43)</td><td></td></tr><tr><td>n</td><td>10</td><td>13</td><td>2</td><td>13</td><td></td></tr></tbody></table>

The list of references is available at http://wwwobs-vlfrfr/~gattuso/ECSS_ref.htm.
estuaries values. Moreover, the high values and the small variation in benthic GPP between estuaries suggest that most of the systems studied were eutrophic and not nutrient limited. It is noteworthy that all measurements were made on intertidal or very shallow sediments where there was little or no light limitation. Extrapolating these rates over the whole surface area of each estuary will lead to a much greater variation in values, reflecting differences in geomorphology (e.g. relative surface area of shallow and deep water) and light availability at the seafloor. This also suggests that GPP in the pelagic compartment of estuaries is mainly driven by physical parameters such as residence time, turbidity and vertical stratification rather than by nutrient concentrations (Boynton et al., 1982; Heip et al., 1995). Moreover, the production of organic matter by chemoautotrophic bacteria such as nitrifiers, which are reported to be very active in eutrophic estuaries (Heip et al., 1995), was not taken into account. van Spaendonk et al. (1993) estimated primary production by these organisms as 32% of the total primary production in the inner Scheldt estuary. The importance of this process generally decreased seaward, becoming negligible relative to phytoplankton production (Heip et al., 1995).

With only two references of depth-integrated pelagic CR (Van Es, 1977; Revilla et al., 2002), it is difficult to provide any conclusion about its magnitude in European estuaries. In contrast to benthic GPP, benthic CR exhibits large variability between sites with minimal values in estuaries of the Portuguese coast (Cabrita and Brotas, 2000; Magalhães et al., 2002) and a very high mean annual rate in the Scheldt estuary (Middelburg et al., 1996). Intermediate values (60–80 mmol C m⁻² d⁻¹) were found in estuaries along the English coast (Colne, Great Ouse and Thames rivers). The average benthic CR in estuaries (61±43 mmol C m⁻² d⁻¹) is much higher than that on open shelves (17 mmol C m⁻² d⁻¹, see previous section). Almost all the benthic

CR data were measured in intertidal or very shallow areas. Benthic CR should decrease with increasing depth because of the absence of microphytobenthos and a decrease in available organic matter due to decomposition in the water column.

### 3.4. Metabolic balance

In this section, the metabolic balance (NCP) in both the pelagic and benthic compartments of open shelf areas and estuaries is examined, and 19 papers reporting such data in the European coastal zone were found. GPP is plotted as a function of CR in Figure 10. The data points above the 1:1 line are autotrophic with respect to carbon, whereas, those below that line are heterotrophic. Pelagic metabolic values for both open shelves and estuaries were integrated over the entire euphotic zone or the water column, if the depth was less than the euphotic zone. The database contains nine values of annual pelagic NCP for open shelf areas. Three sites had a heterotrophic euphotic zone, with minimal NCP in the Gulf of Gdansk (−37 mmol C m⁻² d⁻¹; Witek et al., 1999). The most productive area is the upwelling in the Ría de Vigo with a NCP of 65 mmol C m⁻² d⁻¹. Large variations in the GPP/CR ratio in European shelves (1.5±0.9) prevent any meaningful upscaling. Moreover, the pelagic GPP/CR ratio is certainly lower as this estimate only addresses the euphotic zone.

Only two studies of the metabolic balance in pelagic compartment of estuaries were found in the literature. The water column of the Urdaibaï estuary is autotrophic on an annual basis with a NCP of nearly 70 mmol C m⁻² d⁻¹ (Revilla et al., 2002) while Van Es (1977) reported a value of −20 mmol C m⁻² d⁻¹ in the Ems-Dollard estuary. This is clearly insufficient data from which to draw conclusions about the metabolic balance in European estuaries.

<figure><img src="image_16.png" /><figcaption>Fig. 10. Community gross primary production (GPP) as a function of community respiration (CR) in the benthos and pelagos of European estuaries and shelf environments.</figcaption></figure>
A strong variation is also observed in the benthic compartment of shallow (0–5 m) European coastal areas (GPP/CR = 0.8 ± 0.7) with a minimal NCP reported in Kirr-Bucht (Darss-Zingst Bodden), a coastal lagoon of the south-western Baltic Sea (–17 mmol C m⁻² d⁻¹; Meyercordt et al., 1999), and a maximal value in the west coast of Sweden (18 mmol C m⁻² d⁻¹; Sundbäck and Miles, 2000).

Based on our global estimations of benthic GPP and CR over the 0–200 m depth range, benthic NCP is –15 mmol C m⁻² d⁻¹ in the Baltic Sea and Atlantic/North Sea regions and –19.5 mmol C m⁻² d⁻¹ in the Mediterranean Sea. These values must be considered as preliminary, considering the uncertainty in the estimation of both benthic GPP and CR due to the relatively poor spatial distribution especially in the Mediterranean Sea. Only one estuarine benthic area was found to be net autotrophic (Douro river estuary; Magalhães et al., 2002) while all the other sites were heterotrophic, with a minimal NCP value (–43 mmol C m⁻² d⁻¹) measured in the Colne River estuary (Thornton et al., 2002). The benthic compartment in estuaries seems therefore to be heterotrophic even at shallow depths. Using the average benthic GPP and CR in estuarine shallow areas, a benthic NCP of –17 mmol C m⁻² d⁻¹ is calculated. It must be stressed that this estimate, similar to that found in Baltic Sea and Atlantic/North Sea open shelves, only concerns shallow depths (<5 m) and, then, cannot be extrapolated to the whole surface area of estuaries, due to the site-specific variation of both GPP and CR with depth. Another approach to assessing the metabolism of coastal ecosystems was developed through budgeting methods (Gordon et al., 1996). These budgets estimate net ecosystem production (NEP, expressed as p-r in the LOICZ terminology) and the balance between nitrogen fixation and nitrogen loss through denitrification (nfixndenit) from the non-conservative flux of nitrogen and phosphorus in a system. This procedure implies that the changes in dissolved inorganic phosphorus in a system depends on exchange processes with adjacent systems and on the difference between consumption by primary production and release by mineralization processes (NEP) assuming an elemental particulate organic matter C:P ratio. This procedure might be biased when applied in very turbid areas, where physico-chemical adsorption/desorption of phosphorus on or from particles is supposed to occur (Froelich, 1988).

The NEP data derived by the LOICZ method for European sites are summarized in Table 13 and show that most of sites are balanced, with net metabolism around zero. Three of the sites that depart from a balanced status are included in our database and offer the opportunity to determine consistency: the Ría of Vigo, the Gulf of Lions and the Gulf of Gdánsk. No direct measurement of ecosystem metabolism in these areas is available for comparison, although pelagic GPP

<table><caption>Table 13
Net ecosystem production of the 'preferred' LOICZ budget sites in Europe</caption><thead><tr><th>Location</th><th>NEP (mmol C m<sup>-2</sup> d<sup>-1</sup>)</th></tr></thead><tbody><tr><td><strong>Baltic Sea</strong></td><td></td></tr><tr><td>Baltic Proper</td><td>0.2</td></tr><tr><td>Belt Sea</td><td>0.0</td></tr><tr><td>Bothnian Bay</td><td>0.0</td></tr><tr><td>Bothnian Sea</td><td>0.0</td></tr><tr><td>Curonian lagoon</td><td>-1.4</td></tr><tr><td>Luleälven estuary</td><td>-10</td></tr><tr><td>Gulf of Gdánsk</td><td>17.4</td></tr><tr><td>Gulf of Riga</td><td>0.6</td></tr><tr><td>Szczecin lagoon</td><td>6.3</td></tr><tr><td>Baltic global</td><td>0.5</td></tr><tr><td>Kattegat</td><td>3.5</td></tr><tr><td><strong>Atlantic/North Sea</strong></td><td></td></tr><tr><td>Southern North Sea</td><td>0.9</td></tr><tr><td>Irish Sea</td><td>1.9</td></tr><tr><td>Ría of Vigo</td><td>12.8</td></tr><tr><td>Lough Hyne</td><td>3.4</td></tr><tr><td>Solent estuary</td><td>10.7</td></tr><tr><td><strong>Mediterranean Sea</strong></td><td></td></tr><tr><td>Sacca di Goro lagoon</td><td>-16</td></tr><tr><td>Valli di Comacchio</td><td>0</td></tr><tr><td>Gulf of Lions</td><td>16</td></tr><tr><td>Inner Thermaikos Gulf</td><td>5</td></tr><tr><td><strong>Black Sea</strong></td><td></td></tr><tr><td>Malii Adzalik</td><td>19</td></tr><tr><td>Dnieper-Bug</td><td>-21</td></tr><tr><td>Dniester</td><td>11</td></tr><tr><td>Donuzlav</td><td>0.4</td></tr></tbody></table>

Downloaded from the LOICZ environmental database on 29 April, 2003: (http://hercules.kgs.ukans.edu/hexacoral/envirodata/main.htm).

and CR values reported by Lefèvre et al. (1997) and Moncoiffé et al. (2000) in the euphotic zone of the Gulf of Lions and the Ría of Vigo suggest an autotrophic status for these areas, in agreement with the LOICZ estimate. However, Witek et al. (1997) showed that pelagic CR exceeded depth-averaged pelagic GPP in the Gulf of Gdánsk in 1993, which is counter to the NEP estimated by the LOICZ method for the same period. It was estimated above (Section 3.2.4) that the pelagic CR in the Baltic Sea represents approximately 60% of pelagic GPP. Assuming that benthic CR is 40% of pelagic GPP, NEP should be about 0 in this area, an estimate that is consistent with that obtained with the LOICZ method.

### 3.5. Coastal ecosystems and the eutrophication problem

Eutrophication refers to an increase in the rate of supply of organic matter to an ecosystem, which most commonly is related to nutrient enrichment enhancing primary production (Nixon, 1995). Several papers recently reported such phenomena in European coastal
areas. For example, inputs of nutrients to the Baltic Sea have drastically increased since the 1940s due to changes in land use, excessive use of fertilizers in agriculture, loss of wetlands, sewage outlets and emissions of nitrogen from fossil fuel burning (Larsson et al., 1985; Kautsky and Kautsky, 2000). This was also demonstrated in the North Sea (Cadée and Hegeman, 2002) although a recent decrease of nutrient loads in these areas was observed in the 1990s (Ducrotoy et al., 2000; HELCOM, 2002). The effect of these increases is a general enhancement of pelagic GPP in the Baltic (Renk et al., 1988; Richardson and Heilmann, 1995; Kaczmarek et al., 1997; Wasmund et al., 2001) and North Seas (Ducrotoy et al., 2000; Cadée and Hegeman, 2002), and intertidal microphytobenthos production increased in the Wadden Sea (Cadée, 1984). This enhanced phytoplankton production has several consequences: (1) increased water turbidity in several areas (Sandén and Hakansson, 1996; Cadée and Hegeman, 2002) decreasing light availability for benthic producers, and (2) higher sedimentation and respiration rates in deep waters leading to anoxic conditions in several places (Ducrotoy et al., 2000; Kautsky and Kautsky, 2000). Eutrophication in coastal areas has also resulted in changes in the macroalgal community, reduced biodiversity and appearance of toxic blooms (Kautsky et al., 1992; Ducrotoy, 1999; Ærtebjerg, 2001). In the Mediterranean Sea, Ærtebjerg (2001) reported a general increase of nitrogen and phosphorus loading from rivers, although only one long-term pelagic GPP study was found in the literature which concluded that no systematic eutrophication in the Gulf of Lions due to the Rhône River outflow was evident over the last 30 years (Lefèvre et al., 1997).

## 4. Conclusion

Upscaling is the process of functional generalization of data at small spatial scale (well-studied sites) to a much larger area. It has two prerequisites: (1) a classification of the area under consideration (the EU coastal zone); and (2) a relatively unbiased database of parameters (in our case, primary production and respiration) collected at study sites which are well characterized with respect to the available typology. Once this information is available, the data obtained in each category of the typology may be upscaled using a bottom-up approach: the property measured at a small scale is multiplied by the surface area of the relevant category of the typology.

This approach has both inherent limitations and limitations which are specific to its application to coastal areas. The most critical limitation is the lack of a typology for the coastal zone of the EU or for the global CZ. This goal is being actively pursued at a global scale

by LOICZ using its global environmental database and a classification tool (LOICZView; Maxwell and Buddemeier, 2002). Perhaps the major obstacle which, so far, has constrained development of a global functional typology is the lack of global datasets geo-referenced at a scale of 0.5° or less that describe biotic variables, such as the percent cover of submerged macrophytes or marine sediments. For example, the surface area of the EU coastal zone covered by, say, lagoons or macrophytes is unknown. Similarly, the proportion of vegetated vs. non-vegetated marine sediments is unknown.

Also, the community composition of the study sites cannot be considered as homogeneous both in space and time. Rather, they are mosaics of various communities, sometimes changing with time, each with distinct metabolic properties. For example, should a coastal lagoon harbouring extensive seagrass beds be classified into the lagoon or macrophytes-dominated category?

The diversity of habitats and communities in the coastal zone is very high. The classification used here, and in other recent reviews (Gattuso et al., 1998; Middelburg et al., 2004), does have a functional basis but it is sometimes too simplistic. For example, all estuaries are grouped in a single category despite having attributes, such as turbidity and residence time, that can exhibit very large differences and result in distinct metabolic properties.

This first assessment of ecosystem metabolism in the European coastal zone enables identification of geographical areas and processes which are well- or poorly-documented. Indeed, much more data were found for the Baltic Sea and Atlantic/North Sea regions than for the Mediterranean Sea region. Moreover, available data are not evenly distributed within each region. For instance, relatively few information was found for the eastern parts of the Baltic and Mediterranean Seas and the northern North Sea.

Pelagic GPP on open shelves is, by far, the better documented parameter in our database. Problems related to the use of the ¹⁴C-tracer method (net vs. gross, particulate vs. dissolved), which is the most used method to measure pelagic GPP were already discussed. Then, due to these methodological problems and to a non-perfect spatial coverage, our global estimate (41 mmol C m⁻² d⁻¹) for the European coastal zone contains some uncertainties. Anyway, this value is believed to be the most robust estimate of our study. While microphytobenthic GPP is often believed to be an important metabolic process in coastal areas, a production averaged over the entire 0–200 m depth range of <4% of pelagic GPP (1.5 mmol C m⁻² d⁻¹) is calculated. However, our procedure for estimating the decrease of production with depth is not ideal, especially in the Atlantic Ocean and the North Sea sub-regions, and adds more to the uncertainty in these first regional estimates than the limited geographical coverage of data. More
relevant data are urgently needed to allow a better
evaluation of benthic GPP on a global scale.

Macrophytes were not included in our study, mainly
because of their unknown distribution along European
coastlines. While Charpy-Roubaud and Sournia (1990)
attributed 40% of total shelf production to macro-
phytobenthos, an estimate cannot be provided at this
stage. However, many studies in European coastal areas
suggest that this value is too high and cannot be applied
to European shelves. As for benthic GPP, our estima-
tion of open shelves benthic CR (17 mmol C m⁻²d⁻¹)
suffers from some uncertainties due to the insufficient
geographical coverage, especially in the eastern Medi-
terranean and Baltic Seas regions and to the lack of data
at depths greater than 100 m. Although this estimate is
consistent with a previous one (Middelburg et al., 2004),
our value is believed to be slightly overestimated. Pelagic
CR is clearly the least-documented metabolic process in
our database, especially in the aphotic zone. Such data
are required to have a better understanding of pelagic
remineralization.

While benthic GPP in estuaries was found to be
relatively constant between sites (mean value, 31 mmol
C m⁻²d⁻¹), pelagic GPP and benthic CR exhibited
strong spatial variability. Moreover, as for open shelves,
very few pelagic CR measurements were found in the
literature.

Considering these various uncertainties, it is clearly
not possible at this stage to upscale the available data
and to obtain a meaningful metabolic balance estimate
for the EU coastal zone.

## Acknowledgements

This research was supported by the European Union
in the framework of the EUROTROPH project
(contract # EVK3-CT-2000-00040), and through a
CNRS/CGRI/FNRS cooperative agreement. It was
discussed at the ELOISE workshop ‘Demands at the
European and global levels (upscaling)’, Goes (The
Netherlands), 7–10 May, 2003. Thanks are due to the
workshop participants as well as to C.M. Duarte and
J.J. Middelburg for exciting and fruitful discussions.
The on-line environmental database used was developed
and maintained with support of the LOICZ project,
UNEP-GEF, and the U.S. National Science Foundation
grant (OCE 00-03970; Biogeography of the Hexacor-
allia) to D.G. Fautin and R.W. Buddemeier. We
gratefully acknowledge the invaluable assistance of M.
Fioroni, librarian at the Observatoire Océanologique de
Villefranche, and O. Calmels for designing the web site
of the metabolic database, as well as A.V. Borges, R.W.
Buddemeier and C.J. Crossland for useful comments on
drafts of this paper.
# Chapitre 3

## L'échelle locale
## 3.1 La baie de Palma

Gazeau F., Duarte C. M., Gattuso J. -P., Barrón C., Navarro N., Ruíz S., Prairie Y. T., Calleja M., Delille B., Frankignoulle M. & Borges A. V. (en preparation, soumission en août 2004)
Whole system metabolism and CO₂ fluxes a Mediterranean Bay dominated by seagrass beds (Palma Bay, NW Mediterranean)

Biogeosciences, issue spéciale Coastal Biogeochemistry co-éditée par H. Thomas & A. V. Borges.
**Note:** Ce chapitre est, au moment de la soumission du manuscrit de thèse, à l'état de document de travail, celui-ci n'ayant pas été corrigé et validé par l'ensemble des co-auteurs. La soumission de l'article au journal *Biogeosciences* se fera mi-août, ainsi, la version finale de ce chapitre sera intégrée à la version post-soutenance du manuscrit de thèse.

**Whole-system metabolism and CO₂ fluxes in a Mediterranean Bay dominated by seagrass beds (Palma Bay, NW Mediterranean)**

Gazeau, F.<fnref n="1" />, <fnref n="2" />, *, Duarte, C. M.<fnref n="3" />, Gattuso, J. -P.<fnref n="2" />, Barrón, C.<fnref n="1" />, Navarro, N.<fnref n="3" />, +, Ruíz, S.<fnref n="3" />, ++, Prairie, Y. T.<fnref n="4" />, Calleja, M.<fnref n="3" />, Delille, B.<fnref n="1" />, Frankignoulle, M.<fnref n="1" /> and Borges, A. V.<fnref n="1" />

<footnote n="1">¹ Unité d'Océanographie Chimique (B5), MARE, Université de Liège, B-4000 Sart Tilman - Belgium</footnote>

<footnote n="2">² Laboratoire d'Océanographie de Villefranche, CNRS-Université de Paris 6, B. P. 28, F-06234 Villefranche-sur-mer Cedex - France</footnote>

<footnote n="3">³ IMEDEA (CSIC-UIB), Grupo de Oceanografia Interdisciplinar, Instituto Mediterráneo de Estudios Avanzados, C/Miquel Marqués 21, 07190 Esporles (Islas Baleares) - Spain</footnote>

<footnote n="4">⁴ Département des sciences biologiques, Université du Québec à Montréal, Case postale 8888, succ. Centre-Ville, Montréal, H3C 3P8 - Canada</footnote>

<footnote>+ present address: Área de Biodiversidad y Conservación, ESCET, Universidad Rey Juan Carlos, C/ Tulipán s/n, Móstoles 28933, Madrid - Spain</footnote>

<footnote>++ present address: CLS Space Oceanography División, Parc technologique du Canal, 8-10 Rue Hermès, 31526 Ramonville Cedex - France</footnote>

<footnote>* corresponding author. e-mail: gazeau@obs-vlfr.fr</footnote>
The relationship between whole-system metabolism estimates based on
planktonic and benthic incubations (bare sediments and seagrass, *Posidonia oceanica*
meadows), and CO₂ fluxes across the air-sea interface were examined in the Bay of
Palma (Mallorca, Spain) during two cruises in March and June 2002. Moreover,
planktonic and benthic incubations were performed at monthly intervals from March
2001 to October 2002 in a seagrass vegetated area of the bay. From the annual study,
results showed a contrast between the planktonic compartment, which was
heterotrophic during most of the year, except for occasional bloom episodes, and the
benthic compartment, which was slightly autotrophic. Whereas the seagrass
community was autotrophic, the excess organic carbon production therein could only
balance the excess respiration of the planktonic compartment in shallow waters (< 10
m) relative to the maximum depth of the bay (55 m). This generated a horizontal
gradient from autotrophic or balanced communities in the shallow, seagrass-covered
areas of the bay, to strongly heterotrophic communities in deeper areas, consistent
with the patterns of CO₂ fields and fluxes across the bay observed during the two
extensive cruises in 2002. Finally, dissolved inorganic carbon and oxygen budgets
provided NEP estimates in fair agreement with those derived from direct metabolic
estimates based on incubated samples over the *Posidonia oceanica* meadow.
# 1. Introduction

The role of coastal ecosystems in carbon and nutrient fluxes can be conveniently summarised by their trophic status, referring to the balance between the production of organic matter, as represented by the gross primary production (GPP) of the ecosystem and its degradation through community respiration (CR; Odum 1956). Autotrophic systems, where GPP > |CR| (if CR is expressed in negative units), produce organic matter in excess and thereby act as sinks of inorganic nutrients and CO₂ from surrounding water. In contrast, heterotrophic ecosystems, where GPP < |CR|, rely on allochtonous inputs of organic matter and act as sources of inorganic nutrients and CO₂ to the surrounding water (Duarte and Prairie submitted).

The net flux of CO₂ across the air-water interface is modulated by this metabolic balance but also by external inputs of dissolved inorganic carbon (DIC; upwelling, river inputs...), calcium carbonate (CaCO₃) precipitation/dissolution, and purely thermodynamic effects related to temperature changes or mixing of water masses with different chemical characteristics.

Coastal ecosystems contain highly productive communities, such as macrophyte beds which tend to be autotrophic (Duarte and Cebrián 1996; Gattuso et al. 1998; Hemminga and Duarte 2000). As they also receive important inputs of organic matter from land, both GPP and |CR| tend to be elevated relative to open ocean waters (Duarte and Agustí 1998; Gattuso et al. 1998; Hopkinson and Smith in press).

Smith and Hollibaugh (1993) argued that coastal ecosystems are a heterotrophic compartment of the biosphere. In contrast, other authors suggested that they produce organic matter in excess relative to local demands (Duarte and Cebrián 1996; Gattuso et al. 1998; Wollast 1998) and then act as sources of organic matter for the open ocean (Wollast 1998; Liu et al. 2000; Chen et al. 2003). Duarte and Agustí (1998) and
Hopkinson and Smith (in press) concluded, on the basis of comparative analyses of coastal communities, that the metabolic balance of coastal ecosystems would be dependent on their production: e.g. autotrophic productive areas vs. heterotrophic unproductive areas.

Oligotrophic coastal systems, with unproductive planktonic communities, often support highly productive benthic components. This implies that an assessment of their metabolism requires the integration of both benthic and planktonic compartments over relevant temporal and spatial scales. Nevertheless, an examination of coastal metabolism datasets (Duarte and Agustí 1998; Gattuso et al. 1998; Hopkinson and Smith in press) reveals that most coastal communities were examined at small spatial scales (bottle incubations or benthic chambers) rather than based on research conducted at the ecosystem scale. This may be attributable to the difficulties to encompass the variability within ecosystems using discrete measurements and to extrapolate these estimates to large areas.

To overcome this problem, more integrative approaches, based on material mass balances at the ecosystem scale have been proposed (e.g. Land-Ocean Interaction in the Coastal Zone, LOICZ approach, Gordon et al. 1996). However, these methods require salinity gradients to compute water exchanges and are, therefore, best used in estuarine systems and cannot be readily used in other coastal areas.

Assessments of (oxygen) O₂ concentration and the partial pressure of CO₂ (pCO₂) may be also used to derive integrative estimates of net ecosystem production (NEP = GPP + CR). However, these estimates are not straightforward, as temperature changes, the history and residence time of water masses and other physical and biogeochemical factors may also affect O₂ concentration and pCO₂ (Frankignoulle et al. 1996; Frankignoulle et al. 2001). For instance, the computation of the CO₂ air-
water flux can be critical in the estimation of NEP based on DIC budgets (Gazeau et al. submitted), especially in coastal environments such as estuaries where simple parameterisations of the gas transfer velocity as a function of wind speed have been shown to be site specific (Borges et al. 2004).

To our knowledge, no comparison of the coherence of NEP estimates derived from the assessment of GPP and CR based on incubations and inferred from CO2 and O2 fluxes at the ecosystem scale were carried out in the past.

In this paper, the whole system metabolism of the Bay of Palma (Mallorca, NW Mediterranean) is presented and the coherence between the two approaches described above is tested. This study is carried out on the basis of (1) an annual time series of benthic and planktonic metabolism at a fixed station over a seagrass meadow and (2) extensive surveys in the bay at two contrasting periods of the annual cycle.
## 2. Methods

### 2.1 - Study site

The Bay of Palma (Mallorca, NW Mediterranean) is an oligotrophic system with a surface area of 217 km², a width of 30 km and a mean depth of 28.5 m (Fig. 1). It receives negligible freshwater inputs and, in the absence of appreciable astronomical tides, exchanges with the offshore waters are dominated by wind stress (Ramis et al. 1990). The Bay of Palma contains extensive seagrass (*Posidonia oceanica*) meadows that extend down to 34 m depth and cover more than 30% of the bay. As the water is rather clear (average ± SE extinction coefficient = 0.06 ± 0.02 m-1, Navarro et al. submitted), the sediment floor remains within the euphotic layer throughout the bay. The city of Palma de Mallorca (385,000 permanent inhabitants) supports intense tourism activities and a large harbour.

Benthic and planktonic metabolisms were estimated, using *in situ* incubations, at a fixed station from March 2001 to November 2002, and at a grid of stations during two cruises in March (EUBAL-I) and June 2002 (EUBAL-II). During these two cruises, gas fluxes and hydrography (current velocity) were also examined.

### 2.2 - Hydrography, current velocity and residence time

Five CTD (Conductivity Temperature Depth) surveys were conducted in the Bay of Palma during each of the EUBAL-I (1, 3, 7, 11 and 12/03/2002) and EUBAL-II (19, 21, 25, 26 and 27/06/2003) cruises. During the first survey of EUBAL-I, a total of 32 CTD casts were performed with an average horizontal sampling resolution of 2.8 x 2.8 km. The other surveys consisted of 11 CTD casts each, reducing the sampling resolution to 5.2 x 5.2 km. Profiles were vertically averaged every 0.5 m. Direct current measurements were obtained on four surveys during EUBAL-I (1, 3, 9
and 11/03/2002) and one survey during EUBAL-II (25/06/2002) with a ship-hull
mounted 150 kHz RD instrument ADCP (Acoustic Doppler Current Profiler). This
latter was set up to record currents from surface (10 m) to the bottom with a vertical
resolution of 4 m and a 2 min ensemble period using a firmware version 3.03
(EUBAL-I) and 3.04 (EUBAL-II) of the Transect Acquisition Software. In order to
reduce the instrumental errors, raw ADCP data were averaged to 10 min ensembles.
Absolute ADCP velocities were computed using bottom-tracking mode, which
delivers accurate estimation of the ship velocity. Post-processing of ADCP data was
carried out following the methodology described by Allen et al. (1997).
Unfortunately, the ship was not equipped with a 3D GPS (Global Positioning System)
that provides accurate heading to account for the gyrocompass error. Hence, a typical
error for a conventional gyrocompass of 2° (Griffiths 1994) is assumed in the post-
processing of ADCP data. The maximum error velocity has been estimated at about 4
cm s⁻¹.

The CTD observations were interpolated over a regular 0.5 x 0.5 km grid,
using an objective analysis based on Optimal Statistical Interpolation. The two main
parameters of this scheme are the characteristic scale and the cut-off length scale. The
first determines the influence between observations and the second gives the filtering
of scales which were not resolved by the sampling strategy. For the first CTD survey
of EUBAL-I (dense sampling), the characteristic scale was set-up to 5 km and the cut-
off scale to 10 km. For the other CTD surveys (coarse sampling), the scale derived
from statistics was 7.5 km and the cut-off length scale was set to 15 km. For further
details about this technique refer to Pedder (1993).

In order to have a qualitative view of the general circulation in the Mallorca channel,
a database of daily sea surface temperature (SST) was compiled, for the EUBAL-I
period, from remote sensing products (Instituto Espanyol de Oceanografia;
http://www.teledeteccion-oceanografica.net/).

## 2.3 - Community metabolism

The community metabolism in a *Posidonia oceanica* meadow and unvegetated sediments were studied monthly from March 2001 to October 2002 using *in situ* benthic incubation chambers at the shallow (7 m depth) Posidonia station in the Western side of the bay (Fig. 1). Benthic incubations were set up in the vegetated (4 chambers) and unvegetated (3 chambers) sediment to estimate the net community production (NCP). The benthic chambers consisted of a PVC cylinder inserted in the sediment and a gas-tight polyethylene plastic bag fitted to the cylinder with a sampling port (Hansen et al. 2000). Water samples were withdrawn with syringes at the start of the incubation and after 24 h. Samples for dissolved O₂ were transferred into Winkler bottles, fixed and measured by the Winkler technique following Carrit and Carpenter (1966) using an automated precise titration system (Mettler DL21 Auto-titrator) with potentiometric (redox electrode) end-point detection (Oudot et al. 1988). The average precision achieved in replicates was %CV = 0.29. In order to express dissolved O₂ changes per unit area, the volume of water enclosed in the benthic chambers was estimated from the dilution of a phosphate solution (0.25 mol l⁻¹) in the benthic chambers and measurements of phosphate concentrations by spectrophotometry (Hansen and Koroleff 1999) from samples collected after an equilibration period of 5 min. Dissolved O₂ changes, adjusted to 24 h, within the benthic chambers were used to calculate NCP. Further details and procedures are provided in Barrón et al. (submitted).
During both EUBAL cruises, the community metabolism of *Posidonia oceanica* meadow and unvegetated sediment communities were studied at Posidonia (7 m) and Cap Enderrocat stations (15 m) using *in situ* benthic incubations as described above. Moreover, during EUBAL-II, incubations of both communities were performed along a depth gradient at Posidonia station (4, 7, 15 and 22 m). The variation of benthic NCP with depth at this station was upscaled to the entire bay using estimates of the surface area of vegetated and unvegetated sediments based on the detailed study of Rey and Diaz del Rio (1984), using a General Information System (ArcView software package).

The planktonic metabolism was measured, at monthly intervals, from June 2001 to October 2002 at the Posidonia station. The water column was vertically mixed throughout the study, as evidenced by CTD profiles. Integrated (0 to 7 m) water samples were carefully siphoned into twelve 125 ml biological O₂ demand (BOD) bottles. Five replicates were used to determine the initial O₂ concentration and seven replicate clear bottles were suspended *in situ* at a depth of 4 m and incubated for 24 h. NCP was calculated from the difference between final and initial O₂ concentrations measured as described above and integrated to a depth of 7 m.

Planktonic GPP and CR were measured at 4 stations in the bay during each of the EUBAL cruises (Fig. 1). Samples (5 replicates) were incubated *in situ* at 4 depths for 24 h in both transparent and dark 60 ml BOD bottles. O₂ concentrations were measured before and after incubation using an automated Winkler titration technique with potentiometric end-point detection. Analyses were performed with an Orion redox electrode (9778-SC) and a custom built titrator. Reagents and standardizations were similar to those described by Knap et al. (1996). Daily planktonic CR and NCP
were estimated by regressing O₂ in the dark and transparent bottles against time, respectively. Daily GPP was estimated as the difference between NCP and CR.

At each station and incubation depth, samples were taken for chlorophyll *a*.
Water was filtered through GF/F filters that were stored frozen until extraction and
analysis by high-performance liquid chromatography (Barranguet et al. 1997). Light
penetration in the water column was measured using a LI-COR quantum LI-1935A
and a LI-1400 data-logger twice during each incubation period. During two surveys
on each cruise, vertical CTD (SeaBird SBE19) profiles of fluorescence (Chelsea and
Sea tech sensors during EUBAL-I and -II, respectively) were performed at 11 stations
in the bay (Fig. 1), and were calibrated using concomitant measurements of surface
chlorophyll *a* concentration (same method as above). Surface irradiance was
measured every 15 min during each cruise using a LI-COR cosine corrected quantum
sensor (LI-1925A) and a LI-1400 data-logger. Strong variations were observed during
the first cruise, while during the second cruise light conditions were relatively
constant (data not shown). As phytoplanktonic GPP is strongly dependent on the
available light intensity, a correction was applied to compare results obtained under
different light conditions during EUBAL-I. Relationships between daily GPP rates
normalized per unit of chlorophyll *a* and the averaged daily irradiance were
established for each station using the model of Platt et al. (1980). The resulting PI
(production vs. irradiance) curves were then used to recalculate GPP for the mean
daily surface irradiance over the whole campaign (421.5 µmol m⁻² s⁻¹).

2.4 - CO₂ / O₂ fluxes and NEP estimates

Underway parameters (seawater pCO₂, O₂, salinity and *in situ* temperature) were sampled with a frequency of 1 min from the seawater supply of the ship (pump inlet at a depth of about 2 m) during six surveys of the EUBAL-I cruise (1, 3, 7, 9, 11
and 12/03/2002) and during five surveys of the EUBAL-II cruise (19, 21, 25, 26 and 27/06/2003). Total alkalinity (TA) and O₂ were sampled from the seawater supply to cover the spatial variability during the surveys (on average 10 samples per survey).
Vertical profiles of pH, TA and O₂ were obtained at four reference stations (Fig. 1).
During the EUBAL-II cruise, vertical profiles of pCO₂ were established during 24 h cycles at three reference stations (Posidonia, Bahia and Cap Enderrocat, Fig. 1). A non-dispersive infrared gas analyser (IRGA, LI-COR, LI-6262) was used to measure pCO₂ in wet air equilibrated with seawater. The IRGA was calibrated daily using three dry gas standards: pure nitrogen (0.0 ppm; Air Liquide Belgium) and two gas mixtures with a CO₂ molar fraction of 360.5 and 773.8 ppm (National Oceanic and Atmospheric Administration). The temperature at the outlet of the equilibrator was monitored with a platinum resistance thermometer (PT100, Metrohm) with an estimated accuracy of ± 0.05°C and pCO₂ values were corrected for the temperature difference between *in-situ* seawater and water in the equilibrator using the algorithm proposed by Copin-Montégut (1988). The offset in temperature was typically 0.5°C.
The accuracy of the pCO₂ measurement by equilibration is estimated to ± 2 ppm (cumulated errors on temperature correction and instrument calibration). For further details on the equilibrator design and performance tests refer to Frankignoulle et al. (2001). A second IRGA was used to measure atmospheric pCO₂ sampled at the bow of the ship. Vertical pCO₂ profiles were established every 3.5 h with a resolution of 1 m, by pumping water from a given depth with a peristaltic field pump (ISCO 150) through a Liqui-Cel equilibrator (mini-module, 9") at a rate of about 1.5 l min⁻¹. The pCO₂ was measured using a portable IRGA (EGM-3, PPSystems) with an estimated precision of ± 2 ppm. TA was determined using the classical Gran electro-titration method, on 100 ml GF/F filtered samples with a reproducibility of ± 2 µmol kg⁻¹ and
an estimated accuracy of ± 3 µmol kg⁻¹. The measurement of pH was obtained using a combined electrode (Metrohm), calibrated on the Total Hydrogen Ion Concentration Scale (mol kg SW⁻¹), using the buffers proposed by Dickson (1993). The reproducibility of pH measurement is estimated to ± 0.004 pH units. DIC was calculated from pCO₂ and TA (underway data) and from pH and TA (vertical profile data) with the dissociation constants of carbonic acid and borate from Roy et al. (1993), the dissociation constant of boric acid from Dickson (1990) and the CO₂ solubility coefficient of Weiss (1974). The accuracy of DIC computed from the pCO₂-TA and the pH-TA couples is estimated to ± 5 and ± 10 µmol kg⁻¹, respectively. DIC was normalized to a constant salinity according to:

$$DIC_{37} = 37 \frac{DIC_{observed}}{Salinity_{observed}} \quad (1)$$

pCO₂ was normalized to a constant temperature using the algorithm proposed by Copin-Montégut (1988).

Discrete dissolved O₂ concentration was measured according to the Winkler method using a potentiometric end-point determination with an estimated accuracy of ± 2 µmol kg⁻¹. Underway O₂ concentration was measured with a polarographic electrode (Oxyguard) calibrated against the discrete O₂ samples with an estimated accuracy of ± 3 µmol kg⁻¹. Apparent oxygen utilisation (AOU) was computed using the concentration of O₂ at saturation calculated with the algorithm proposed by Benson and Krause (1984). Salinity and *in-situ* temperature were measured using a SeaBird SBE21 thermosalinograph. Vertical profile data were obtained from a 12 bottle rosette coupled to a CTD (SeaBird SBE19). The estimated errors on salinity and *in situ* temperature measurements are ± 0.05 and ± 0.01°C, respectively. Wind speed was measured at approximately 10 m height with a Batos (5 s sampling interval
during EUBAL-I) and Aanderaa (1 min sampling interval during EUBAL-II) cup anemometer.

The air-sea CO₂ flux (F; mmol C m⁻² d⁻¹) was computed from the air-sea gradient of pCO₂ (ΔpCO₂ = pCO₂ water - pCO₂ atmosphere; ppm), the gas transfer velocity (k; m d⁻¹) and the solubility coefficient of CO₂ (α; mmol m⁻³ ppm⁻¹), using equation:

$$F = \alpha k \Delta pCO_2 \quad (2)$$

As a convention, a positive flux corresponds to a source for the atmosphere. Computations were made using various algorithms of k as a function of wind speed (Liss and Merlivat 1986; Wanninkhof 1992; Wanninkhof and McGillis 1999; Nightingale et al. 2000; McGillis et al. 2001), although, we mainly discuss the values computed with the parametrization by Wanninkhof and McGillis (1999) for a consistent comparison with values from the Dyfamed station (Bégovic and Copin-Montégut 2002). For each survey, the α ΔpCO₂ data were interpolated on a grid of 0.0034°E x 0.0025°N. To account for the strong non-linearity of the k parametrizations, the flux computations were carried out using hourly bins of wind speed (assuming that the whole area is uniformly submitted to wind speed measured anywhere during the survey) and then averaged for a given survey.

NEP over the *Posidonia oceanica* meadow was computed based on a DIC budget, according to the equation:

$$NEP_{DIC} = \rho h_{pos} \frac{\left( DIC_{bay'} + t_{bay'} \frac{F_{bay'}}{\rho h_{bay'}} \right) - \left( DIC_{pos} + t_{pos} \frac{F_{pos}}{\rho h_{pos}} \right)}{t_{pos}} \quad (3)$$

where NEP<sub>DIC</sub> is expressed in mmol C m⁻² d⁻¹, ρ is the water density (kg m⁻³), DIC* is DIC<sub>37</sub> (mmol kg⁻¹), t* is the water residence time (d), h<sub>pos</sub> is the average water column height over the *Posidonia oceanica* meadow (m), h<sub>bay</sub> is the average mixed layer
depth in the Bay of Palma (excluding the *Posidonia oceanica* meadow, m), $F*$ is the air-sea CO₂ exchange computed using the Wanninkhof and McGillis (1999) *k* parametrization, subscript *pos* denotes data over the *Posidonia oceanica* meadow and subscript *bay* denotes data over the rest of the Bay of Palma (excluding the *Posidonia oceanica* meadow).

An identical equation was used to compute NEP from O₂ concentrations (NEPO₂ in mmol O₂ m⁻² d⁻¹); the flux air-sea of O₂ was computed using the Wanninkhof and McGillis (1999) *k* parametrization and the Schmidt number (Sc) formulation for seawater given by Wanninkhof (1992), assuming a *k* dependency proportional to Sc⁻⁰.⁵.

The relative water residence time over the *Posidonia oceanica* meadow and in the Bay of Palma (excluding the *Posidonia meadow*) were computed according to:

$$t_{pos} = t_{total} \frac{V_{pos}}{V_{total}} \qquad (4)$$

$$t_{bay'} = t_{total} \frac{V_{bay'}}{V_{total}} \qquad (5)$$

where $V*$ is the volume (km³), $t*$ is the water residence time (d), subscript *total* denotes data in the whole Bay of Palma, subscript *pos* denotes data over the *Posidonia oceanica* meadow and subscript *bay* denotes data over the rest of the Bay of Palma (excluding the *Posidonia oceanica* meadow).

## 3. Results and Discussion

### 3.1 - Monthly metabolism at Posidonia station

The *Posidonia oceanica* community tended to be autotrophic and the bare sediment community tended to be heterotrophic during the study (Fig. 2A). The seagrass community ranged from heterotrophy with a lowest NCP in August 2002
(-24.7 mmol O₂ m⁻² d⁻¹) to autotrophy with a highest NCP in April 2002 (88.8 mmol O₂ m⁻² d⁻¹). The unvegetated sediment community ranged from heterotrophy (-4.8 mmol O₂ m⁻² d⁻¹ in April 2001) to autotrophy (NCP = 5.0 mmol O₂ m⁻² d⁻¹ in July 2001). The benthic community metabolism at Posidonia station showed considerable variability along the study period, with the highest NCP found in spring and early summer (Fig. 2B). In contrast, the planktonic NCP showed no clear seasonality. Indeed, most monthly NCP estimates in 2001 indicated a heterotrophy while those in 2002 suggested an autotrophy. Overall, the NCP of the planktonic compartment averaged -4.6 ± 5.9 mmol O₂ m⁻² d⁻¹, indicating a metabolic balance (i.e. H₀: mean NCP = 0, P > 0.05), with a tendency towards heterotrophy whereas the benthic compartment was overall net autotrophic (16.2 ± 5.2 mmol O₂ m⁻² d⁻¹). NEP (sum of benthic and planktonic NCP) was dominated by the benthic compartment in spring and summer, and by the planktonic community in the fall and winter. At an annual scale, NEP was nearly balanced, with a tendency towards autotrophy (7.7 ± 7.7 mmol O₂ m⁻² d⁻¹).

## 3.2 - Hydrography, water currents and residence time during EUBAL-I and -II cruises

The horizontal velocity fields based on the ADCP surveys during the EUBAL-I and -II cruises differed considerably. In March, the flow pattern was initially characterised by a clear clockwise circulation with maximum velocities of 19 and 22 cm s⁻¹, on 01/03 and 09/03/2002 respectively (Fig. 3A&B). The water entered the bay on its Western side, while the water outflow is dominant on the Eastern side. The circulation changed to the opposite direction towards the end of the cruise (12/03/2002; Fig. 3C) when the flow pattern became anticlockwise and the flow intensified to reach a value of 40 cm s⁻¹. This flow reversion was consistent with a shift between the beginning and the end of the cruise, from a relatively cool, high-
salinity (37.5 to 37.6) to a warmer and less saline water mass (+ 0.5 °C; 37.2; Fig. 4).
This pattern was evident both from CTD surveys and examination of satellite SST
data (not shown).

The flow pattern during EUBAL-II was similar to the one observed at the end
of EUBAL-I, with a general anticlockwise circulation (Fig. 3D). It should be noted
that the current velocities were, on average, lower than those during EUBAL-I (6 - 7
cm s⁻¹ vs. 20 - 24 cm s⁻¹).

The water residence time in the Bay of Palma was estimated from the current velocities recorded during each survey. The average water residence time was much shorter during EUBAL-I (2.5 ± 0.2 d) than during EUBAL-II (10 d). Due to the low velocities and the consequent noise during EUBAL-II, the computed residence time is subject to a strong uncertainty.

3.3 - Ecosystem metabolism during EUBAL-I and -II cruises

Integrated chlorophyll *a* concentrations at the incubated stations were on average significantly higher in March than in June, except at Posidonia station which presented similar values during both cruises (Table 1). Minimal and maximal concentrations were found, respectively, at Cap Enderrocat station in June (1.5 mg m⁻²) and at Bahia station in March (17.3 mg m⁻²). Light attenuation coefficients (*K*) were rather low (< 0.16 m⁻¹ during both cruises) with slightly higher values in March, except for Posidonia station.

During EUBAL-I, surface planktonic GPP rates ranged from 2.8 mmol O₂ m⁻³ d⁻¹ (Posidonia) to 5.2 mmol O₂ m⁻³ d⁻¹ (Cap Enderrocat) with an average value of 3.7 ± 1.2 mmol O₂ m⁻³ d⁻¹ (Fig. 5). During EUBAL-II, surface planktonic GPP rates were slightly higher (mean: 4.7 ± 1.2 mmol O₂ m⁻³ d⁻¹) with a minimal value at Cap Enderrocat (3.3 mmol O₂ m⁻³ d⁻¹) and a maximal one at station 4 (6.3 mmol O₂ m⁻³
d⁻¹). Average water-column planktonic CR strongly increased between March and June, from 1.5 ± 0.8 mmol O₂ m⁻³ d⁻¹ to 3.4 ± 1.9 mmol O₂ m⁻³ d⁻¹, respectively. Higher vertical and horizontal gradients were found during the EUBAL-II cruise.

During EUBAL-I, maximal integrated planktonic GPP values were observed at stations Bahia and 4 (98 and 92 mmol O₂ m⁻² d⁻¹) and the minimal one at Posidonia station (36 mmol O₂ m⁻² d⁻¹, Table 2). During EUBAL-II, integrated planktonic GPP ranged from 29 mmol O₂ m⁻² d⁻¹ at Cap Enderrocat to 86 mmol O₂ m⁻² d⁻¹ at Bahia. Integrated planktonic CR showed a low spatial variability during the first cruise with a mean value of -35 ± 7.4 mmol O₂ m⁻² d⁻¹. In contrast, during the second cruise, strong geographical variations were highlighted with a minimal value measured at Posidonia (-45 mmol O₂ m⁻² d⁻¹) and a maximal one at station 4 (-107 mmol O₂ m⁻² d⁻¹). The planktonic compartment was autotrophic at all incubated stations during EUBAL-I while during EUBAL-II, two stations (Station 4 and Cap Enderrocat) presented a heterotrophic status.

Significant relationships were found between integrated planktonic GPP and integrated chlorophyll *a* concentration during both cruises (Fig. 6A). As chlorophyll *a* concentrations were estimated at 11 stations on two surveys during each cruise, these relationships were used to extrapolate GPP, integrated across the euphotic layer (34 m during EUBAL-I and 46 m during EUBAL-II) to the whole bay (Table 3). During both surveys in March, the lowest chlorophyll *a* values and consequently the lowest planktonic GPP were found at Posidonia and Cap Enderrocat stations while maximal rates were found in deep waters in the middle of the bay. During the second cruise, due to lower chlorophyll *a* concentrations, planktonic GPP were much lower and higher spatial variations were observed in comparison to March, reaching a mean
value of 33 ± 44 mmol O₂ m⁻² d⁻¹ (vs. 93 ± 43 mmol O₂ m⁻² d⁻¹ during EUBAL-I). The highest values were generally estimated over the *Posidonia oceanica* meadow.

During the first cruise, for all stations investigated during the surveys, planktonic integrated CR rates were calculated by multiplying the mean volumetric rate observed during the incubations (-1.5 ± 0.8 mmol O₂ m⁻² d⁻¹) by the depth of each station. Planktonic integrated CR was, therefore, maximal at deep stations reaching a maximal value at station 8 (60m depth; -89 mmol O₂ m⁻² d⁻¹), but was always lower than planktonic GPP except for one station during the first survey (Cap Enderrocat). Consequently, the planktonic compartment was autotrophic during EUBAL-I with an average value of 46 ± 41 mmol O₂ m⁻² d⁻¹.

Due to the strong heterogeneity in CR observed during EUBAL-II at the four incubated stations, the same procedure was not applied. During this cruise, a significant relationship was observed between GPP and CR integrated across the water column, excluding the last incubated depth (Fig. 6B). It should be mentioned that CR rates measured near the bottom and therefore near the *Posidonia oceanica* meadow do not fit with this relationship. This suggests that near the bottom, planktonic CR may be fuelled by organic matter from the *Posidonia oceanica* meadow rather than by the planktonic production. Therefore, CR rates collected at the four incubated stations were upscaled only to the area covered by the *Posidonia oceanica* meadow, while integrated CR was calculated based on the estimated GPP in the rest of the bay where chlorophyll *a* and consequent GPP rates are much lower.

On average, integrated and extrapolated planktonic CR was similar during both cruises (-47 ± 24 and -43 ± 27 mmol O₂ m⁻² d⁻¹ in March and June, respectively). Therefore, due to a higher GPP during the first cruise, the planktonic compartment
was autotrophic in March and heterotrophic in June (46 ± 41 and -10 ± 45 mmol O₂ m⁻² d⁻¹, respectively).

Seagrass communities were autotrophic at all depths during both cruises, with the highest NCP found at the shallowest station (Table 4). In contrast, bare sediment communities remained net heterotrophic during both cruises, except for the shallowest community investigated during EUBAL II (4 m). The upscaled results suggest that the NCP of the *Posidonia oceanica* meadow was marginally autotrophic during EUBAL-I (1 mmol O₂ m⁻² d⁻¹) and significantly autotrophic, with an average NCP of 26 mmol O₂ m⁻² d⁻¹, during EUBAL-II.

Combining these estimates with concurrent estimates of planktonic NCP over the *Posidonia oceanica* meadow, a NEP over the *Posidonia oceanica* meadow of 60 and 34 mmol O₂ m⁻² d⁻¹ was estimated for EUBAL-I and -II, respectively.

Considering the entire bay, where the bare sediments and the seagrass meadow cover respectively 70 and 30% of its surface, benthic NCP was estimated at -1 and 7 mmol O₂ m⁻² d⁻¹ for EUBAL-I and -II, respectively. Therefore, a whole-system NEP of 45 and -3 mmol O₂ m⁻² d⁻¹ was estimated in March and June, respectively, indicating that the Bay of Palma acted as an autrotrophic ecosystem in March and as a heterotrophic one in June.

As mentioned previously, monthly time series were obtained at one station in the bay (Posidonia). The NEP measured at this station was 40 and 4 mmol O₂ m⁻² d⁻¹ during EUBAL-I and -II, respectively while similar values (45 and -3 mmol O₂ m⁻² d⁻¹) were reported for the entire bay during the same cruises (see above). Therefore, this suggests that the annual NEP estimated at Posidonia station (7.7 mmol O₂ m⁻² d⁻¹; see above) might be a relatively confident indicator of the metabolism of the entire Bay of Palma over an annual cycle, although this extrapolation procedure could lead
to a slight overestimate especially during low planktonic GPP periods as during
EUBAL-II.

3.4 - Spatial and temporal variations of DIC, AOU and air-sea CO₂ fluxes during EUBAL-I and -II cruises

The comparison of pCO₂ among cruises required the normalization to a constant temperature of 19°C (pCO₂(19°C)), as temperature strongly affects the equilibrium constants of DIC and, in particular, the solubility coefficient of CO₂, so that pCO₂ rises of about 4% when temperature increases of 1°C. Normalization of pCO₂ values to a constant temperature allows to remove temperature effects and to focus on potential biological controls of pCO₂. The correlation between AOU and pCO₂(19°C) (Fig. 7A) strongly suggests that both variables were controlled by biological effects during the two EUBAL cruises. The pCO₂(19°C) and AOU values were on average lower during EUBAL-II than during EUBAL-I. This is related to the longer residence time of the water mass in the bay during summer (see above) that leads to an enhanced impoverishment in CO₂ and enrichment in O₂ in June despite the fact that the NEP was lower in June than in March (see above). The pCO₂(19°C) and AOU values observed were much lower than those at the Dyfamed station (located in the open waters of the Ligurian Sea, about 620 km North from the Bay of Palma) for the corresponding periods. This suggests that in the Western Mediterranean Sea, the continental shelf is more productive than the open oceanic waters.

During both EUBAL cruises, TA was well correlated to salinity (Fig. 7B)
suggesting that CaCO₃ precipitation/dissolution rates were too low and/or water
residence time too short to significantly affect surface water TA values. The linear
regression function based on data from both EUBAL cruises was very similar to that
reported by Copin-Montégut (1993) for the Alboran Sea. Based on the linear
regression function of TA as a function of salinity, DIC was computed from continuous pCO₂ measurements. DIC was normalized to a constant salinity value of 37 to remove the variations of DIC due to changes in salinity owing to mixing, evaporation or dilution.

Strong spatial gradients of pCO₂(19°C) and AOU were observed during both EUBAL cruises (Fig. 8). During the six EUBAL-I surveys, pCO₂(19°C) and AOU surface distributions exhibited variable patterns with no recurrent spatial features. This suggests either highly variable NEP in space and time and/or the advection of water masses with different pCO₂(19°C) and AOU signatures. The latter explanation is consistent with shifts in the water mass and residual current patterns observed between the start and the end of the cruise (see above). During the EUBAL-II surveys, AOU and pCO₂(19°C) minima were systematically observed near-shore, above the *Posidonia oceanica* meadow (Fig. 8 and Table 5). Also, during the EUBAL-II surveys, lower near-shore values of AOU and pCO₂(19°C) were systematically observed on the Western side of the bay in comparison to the Eastern side (Fig. 8). This is consistent with the anti-clockwise pattern of residual currents (Fig. 3), leading to an impoverishment in CO₂ and an enrichment in O₂ as the water mass is advected above the *Posidonia oceanica* meadow. Also, a higher planktonic NCP was observed on the Western side of the bay during two EUBAL-II surveys, suggesting overall higher NEP on this side of the bay (Table 2).

The variability of the flux computations related to the choice of the *k* parametrization is huge as shown in other studies (e.g. Borges and Frankignoulle 2002). The fluxes computed using the Wanninkhof and McGillis (1999) *k* parametrization were on average identical to those using the Liss and Merlivat (1986) *k* parametrization, and, corresponded to 57, 66 and 63% of those computed using,
respectively, the *k* parametrization given by Wanninkhof (1992), Nightingale et al. (2000) and McGillis et al. (2001).

The Bay of Palma was a sink for atmospheric CO₂ during EUBAL-I (on average -1.7 mmol C m⁻² d⁻¹) and a source during EUBAL-II (on average 2.7 mmol C m⁻² d⁻¹, Table 5). At the Dyfamed station, the CO₂ fluxes ranged between -2.9 and -8.7 mmol C m⁻² d⁻¹ in March 1998-99 and between 2.8 and 3.3 mmol C m⁻² d⁻¹ in June 1998-1999 (Bégovic and Copin-Montégut 2002). The stronger fluxes at Dyfamed are related to higher wind speeds since the ΔpCO₂ are more marked in the Bay of Palma: -56 ppm during EUBAL-I (-39 ppm at Dyfamed in March 1998-99) and 68 ppm during EUBAL-II (20 ppm at Dyfamed in June 1998-99).

The temperature effect on the solubility coefficient of CO₂ strongly contributes to the seasonal variability of air-sea CO₂ flux in the Bay of Palma, as also shown in open oceanic waters (Dyfamed; Bégovic and Copin-Montégut 2002) and other coastal waters (Bay of Calvi – Corsica; Frankignoulle 1988) of the Western Mediterranean Sea. Indeed, pCO₂ and ΔpCO₂ values were higher during EUBAL-II than EUBAL-I, although, pCO₂(19°C) and DIC₃₇ were actually lower during EUBAL-II (Table 5). Thus, the fact that the Bay of Palma is a source of CO₂ in June seems to be largely related to a temperature effect, since pCO₂(19°C) and AOU data were lower than in March (Fig. 7A, Fig. 8 and Table 5). At any rate, the contrasting role of the bay as a sink in March and a source in June is coherent with the positive NEP found in March and the net heterotrophy observed in June.

Our results also show that the potential impact of *Posidonia oceanica* meadows on the CO₂ air-sea flux budget in the Western Mediterranean continental shelf during summer could be small. The average CO₂ flux observed over the *Posidonia* meadow during EUBAL-II (2.54 mmol C m⁻² d⁻¹; Table 5) was only 10%
lower than that for unvegetated areas during the same cruise (2.76 mmol C m⁻² d⁻¹).

As *Posidonia oceanica* meadows are believed to cover about 25% of the shelf area (Bethoux and Copin-Montégut 1986), they can only decrease the summertime CO₂ emission from the Mediterranean continental shelf by less than 2.5%, which is a modest contribution.

3.5 - DIC- and O₂-derived NEP estimates over the *Posidonia oceanica* meadow during EUBAL-II

NEP estimates over the *Posidonia oceanica* meadow during EUBAL-II based on surface water DIC₃₇ and O₂ were highly variable and the ecosystem metabolism ranges from distinctly autotrophic status to a nearly balanced status (Table 6). The day-to-day variability of NEP seems to be mainly related to light availability, as there was a strong relationship between the NEP and surface irradiance (Fig. 9), which explained about 91 and 70% of the variance of, respectively, NEP_DIC and NEP_O₂. Based on these linear regressions and continuous surface irradiance measurements, NEP over the *Posidonia oceanica* meadow was integrated for the full duration of the EUBAL-II cruise (19-27 June): at 22 ± 12 mmol C m⁻² d⁻¹ and 10 ± 7 mmol O₂ m⁻² d⁻¹ for, respectively, NEP_DIC and NEP_O₂. The difference between NEP_DIC and NEP_O₂ could be related to net CaCO₃ production that was not included in the DIC budget. Net CaCO₃ production was measured using *in situ* benthic chambers on 20/06/2002, yielding a value of 15 mmol C m⁻² d⁻¹ for the *Posidonia oceanica* vegetated community and 1 mmol C m⁻² d⁻¹ for bare sediments of the Bay of Palma (Barrón et al. submitted). Based on the relative sea-floor coverage by these benthic communities, the integrated net CaCO₃ production between the shore and 30 m depth is 10 mmol C m⁻² d⁻¹ and corresponds to the difference between NEP_DIC and NEP_O₂.
NEP<sub>O2</sub> and NEP<sub>DIC</sub> are well correlated and the slope of the linear regression (Table 6) gives an indication on the ΔO<sub>2</sub>:ΔDIC ratios of both GPP and CR processes. The photosynthetic quotient (PQ) corresponds to the molar ratio of the release of O<sub>2</sub> to the consumption of DIC during photosynthesis while the respiratory quotient (RQ) corresponds to the molar ratio of the release of DIC to the consumption of O<sub>2</sub> during organic matter mineralization. As mentioned by Thamdrup and Canfield (2000), an important uncertainty in using O<sub>2</sub> uptake as a measure of mineralization in sediments lies in the assumption that anaerobic respiration and reoxidation of inorganic species are at steady state. Holmer et al. (2003) reported low concentrations of sulfides in seagrass sediments around Mallorca Island suggesting that the previous assumption is realistic in these sediments. Therefore, in the present study, a RQ of 1 was assumed and the NEP<sub>O2</sub> vs. NEP<sub>DIC</sub> ratio was used to compute a PQ value. This latter is slightly lower but not significantly different than 1. This would suggest that NEP over the *Posidonia oceanica* meadow is mainly related to the photosynthetic activity of the seagrass community. Indeed, one can compute a PQ of 1.06, based on the C:N:P elemental molar ratio of 956:39:1 reported by Atkinson and Smith (1983) for *Posidonia oceanica* leaves. The C:N:P elemental molar ratio of roots is 3550:61:1 (Atkinson and Smith 1983) but the below-ground production of *Posidonia oceanica* is much lower than the above-ground production (about 10%; Duarte and Chiscano 1999) and does not significantly affect the PQ estimate. Based on the C:N:P molar elemental composition of phytoplankton reported by Redfield (1963) and Hedges et al. (2002), the predicted PQ values are higher than 1, respectively, 1.30 and 1.45.

Error estimates on these NEP values (Table 6) are largely derived from the uncertainty on the water residence time. The analytical error on DIC<sub>37</sub> and O<sub>2</sub> should not significantly affect the NEP estimates, since the variables used in the
computations are averages of a large number of observations (assuming that analytical
errors are random and not systematic). The air-sea flux correction introduces a
significant uncertainty in the computations. NEP<sub>DIC</sub> computed using the air-sea CO<sub>2</sub>
fluxes calculated with Wanninkhof and McGillis (1999) *k* parametrization
corresponds on average to 99.4, 102.7, 94.7 and 95.0% of NEP<sub>DIC</sub> computed using the
*k* parametrizations given by, respectively, Liss and Merlivat (1986), Wanninkhof
(1992), Nightingale et al. (2000) and McGillis et al. (2001). NEP<sub>O<sub>2</sub></sub> computed using
the air-sea O<sub>2</sub> fluxes calculated with Wanninkhof and McGillis (1999) *k*
parametrization corresponds on average to 98.5, 96.7, 96.5 and 97.2% of NEP<sub>O<sub>2</sub></sub>
computed using the *k* parametrization given by, respectively, Liss and Merlivat
(1986), Wanninkhof (1992), Nightingale et al. (2000) and McGillis et al. (2001). The
choice of the *k* parametrization for air-sea flux correction also affects the PQ estimate,
the lowest one corresponding to the NEP computations using the Wanninkhof and
McGillis (1999) *k* parametrization (Table 6) and the highest one (1.1 ± 0.2)
corresponding to the NEP computations using the Wanninkhof (1992) *k*
parametrization. The less constrained uncertainty in the computations of NEP above
the *Posidonia oceanica* meadow during EUBAL-II probably comes from the
representativeness of the underway surface water data for the whole water column
DIC<sub>37</sub> and O<sub>2</sub>. This approach is attractive because it is based on large data sets that
adequately resolve the spatial variability, but it is based on the assumption that the
variables are homogeneous in the water column (no vertical gradients).

Examination vertical profiles of DIC₃₇ and O₂ at the four reference stations
sampled during EUBAL-II (Fig. 10) shows that these vertical gradients are more
marked for O₂ than DIC₃₇ but they remain smaller than the spatial gradients, for both
variables. We attempted to adjust the surface values of O₂ and DIC₃₇ to represent the
whole column values of these variables. Station 4 (located at the edge but outside the *Posidonia oceanica* meadow) was considered to represent the incoming water from the bay and the other three stations were considered to be representative of the *Posidonia oceanica* meadow. NEP computed from adjusted DIC₃₇ and O₂ values, assuming that surface DIC₃₇ is 1 and 4 µmol kg⁻¹ (for the entire bay and *Posidonia oceanica* meadow, respectively) lower than whole column DIC₃₇ and that surface O₂ is 9 and 4 µmol kg⁻¹ (for bay and *Posidonia oceanica* meadow, respectively) lower than whole column O₂, were much larger than NEP estimates based on surface water values, but, the PQ value remains unchanged (Table 6). NEP estimates based on the adjusted DIC₃₇ and O₂ values are also well correlated to surface irradiance (not shown), allowing the integration for the full duration of the EUBAL-II cruise (19-27 June) to yield estimates of 35 ± 8 mmol C m⁻² d⁻¹ and 48 ± 7 mmol O₂ m⁻² d⁻¹ for, respectively, NEP_DIC and NEP_O₂. In this case, net CaCO₃ production cannot explain the difference between NEP_DIC and NEP_O₂, and the difference between NEP_DIC and NEP_O₂ is probably mostly related to the error on the slope and y-intercept of the linear regressions as a function of surface irradiance that are higher for NEP_O₂. However, considering potential sources of error associated to each method, these estimates are in fair agreement with the NEP estimate based on the upscaled incubation measurements of 34 mmol O₂ m⁻² d⁻¹ over the *Posidonia oceanica* meadow during this cruise (see above).
3.6 - Daily variations of DIC during EUBAL II

The daily variations of DIC₃₇ at stations Posidonia and Cap Enderrocat follow
the daily oscillation expected from the diel alternation between photosynthesis and
respiration; DIC₃₇ decreases from dawn to dust and increases during the night (Fig.
11). However, at station Bahia, the DIC₃₇ time-course during the 24 h cycle was
erratic. This can be attributed to the fact that station Bahia is much deeper (33 m) than
stations Posidonia (13 m) and Cap Enderrocat (16 m). It is then probable that due to
the water column depth, the impact on water column DIC from metabolic activity is
much smaller at station Bahia and is not discernable from the background noise.

The difference of average DIC values from the top half of the water column
and from the bottom half of the water column (ΔDIC) provides qualitative
information on the relative importance of metabolic rates from the planktonic and
benthic compartments. During the 24 h cycle at Posidonia station, in the lower half of
the water column higher average DIC values were observed during night-time while
lower average DIC values were observed at the end of the day (Fig. 11). This suggests
higher metabolic rates in the benthic compartment than in the planktonic one, at the
Posidonia station. Indeed, the metabolic rates measured by O₂ incubations show that,
at this station, benthic CR is about 1.8 times higher than planktonic CR and that
benthic GPP is about 1.5 times higher than planktonic GPP. At station Bahia, the
reverse trend in ΔDIC is observed, suggesting higher metabolic rates in the planktonic
compartment compared to the benthic one. This conclusion is not surprising
considering that reference station Bahia is deeper than reference station Posidonia and
that benthic metabolic rates are expected to be lower due to stronger light-limitation.

Day-time net community production (NCP<sub>d</sub>) was estimated from the time
course of DIC values from dawn to dust. Considering the scatter in the data, a simple
linear regression was used. We did not attempt to estimate CR because only 3 profiles
were obtained at night. NCP<sub>d</sub> estimates were in fair agreement with those based on O<sub>2</sub>
incubations and reproduce the same spatial trend, with higher NCP<sub>d</sub> at Posidonia
station than at Cap Enderrocat station (Table 7). We can conclude that the daily DIC
time-course approach can be used with confidence to estimate metabolic rates but its
application is limited to relatively shallow waters (≤ 15 m).

4. Conclusion

The results presented in this study provided estimates of the metabolism of the Bay of Palma on the basis of multiple approaches, encompassing monthly time series at one station in the bay, extensive surveys of direct metabolic estimates and estimates indirectly derived from DIC and O₂ fields, as well as diel cycles of DIC. Our results reveal a contrasting behaviour between the benthic and planktonic compartments. The areas of the benthic compartment dominated by the seagrass *Posidonia oceanica* remained autotrophic throughout the study, whereas the unvegetated sediments are, except for the shallowest areas, a net heterotrophic component of the metabolism of the Bay of Palma ecosystem. The autotrophic nature of seagrass meadows is consistent with previous reports for these ecosystems (Duarte and Cebrián 1996; Gattuso et al. 1998; Hemminga and Duarte 2000).

The planktonic community was largely heterotrophic, although showing
episodes of autotrophy, associated to phytoplankton blooms, when planktonic GPP
increased greatly, as in March 2002 (EUBAL-I), the time of the spring bloom in the
NW Mediterranean (Duarte et al. 1999). Despite the clarity of these waters, planktonic
and benthic GPP were strongly related to the incoming irradiance, leading to an
overall relationship between NEP and surface irradiance over the *Posidonia oceanica*
meadow. Indeed, the autotrophic, seagrass-dominated benthic compartment is confined to waters reaching slightly over half of the maximum depth of the Bay of Palma, so that macrophyte-derived autotrophy only contributes to elevate NEP at the shallower waters, as reflected in the distribution of pCO₂ and O₂ in the surface waters. Despite the contribution of the seagrass community, even shallow (Posidonia station: 7 m) sites within the bay were near metabolic balance at the annual time scale, where seagrass autotrophy barely compensates the planktonic heterotrophy. Overall, the depth of the Bay of Palma (mean: 28.5 m) leads to a dominance of planktonic over benthic communities in the metabolism of the entire ecosystem. Whereas excess production by seagrass can compensate (or even create) planktonic carbon deficits in shallow areas (< 10 m), planktonic metabolism dominates in deeper waters. Moreover, the short water residence time in the bay suggests that the extended planktonic heterotrophic periods, that dominate most of the year, cannot be supported by carbon in excess accumulated during autotrophic periods. As such, the whole ecosystem might be, in general, heterotrophic, especially during summer, when the strong increase in CR, driven by the increased temperature, greatly exceeded ecosystem GPP. Instead, the heterotrophic nature of the ecosystem and the planktonic community must be supported by allochtonous organic carbon inputs, probably derived from the human populations surrounding the Bay of Palma.

During the summer cruise, the spatial variability of pCO₂ and O₂ fields and the direction of CO₂ fluxes were consistent with NEP derived from incubations. The short water residence time in the bay (2 to 10 d) renders use of pCO₂ and O₂ fields to estimate ecosystem metabolism cumbersome. However, more elaborated mass balance formulations which account for the water residence time in the bay, allowed the derivation of NEP estimates that were in fair agreement with those derived from
direct metabolic estimates from incubated samples over the *Posidonia oceanica*
meadow. Our results also provide evidence that simple day-night whole water column
DIC variations may also be useful to derive NEP estimates in shallow waters of
seagrass ecosystems.
Acknowledgements

This research was supported by the European Union in the framework of the
EUROTROPH project (contract # EVK3-CT-2000-00040), and by a
CNRS/CGRI/FNRS/CSIC cooperation. We thank the officers, crew and technical
staff of the *Téthys II* and *Mytilus* for full collaboration during the EUBAL cruises, D.
Tailliez for operating the rosette and CTD and processing the data during EUBAL-I,
C. Copin-Montégut for providing the Dyfamed data-set, R. Biondo, E. Libert, R.
Martínez, M.-D. Pizay, R. Santiago and J.-M. Théate for technical support. AVB and
MF are, respectively a post-doctoral researcher and a senior research associate at the
FNRS. CB was supported by a grant from the Balearic government, and NN was
supported by a fellowship from the Spanish Ministry of Education, Culture and
Sports.
# Tables

Table 1 Characteristics of the incubation stations during the EUBAL cruises in 2002.

Salinity and temperature values were averaged and chlorophyll *a* concentrations were integrated over the water column. *K* is the light attenuation coefficient.

<table><thead><tr><th>Station</th><th>Date</th><th>Bottom depth m</th><th>Salinity</th><th>Temperature °C</th><th>Integrated chlorophyll *a* mg m<sup>-2</sup></th><th>K m<sup>-1</sup></th></tr></thead><tbody><tr><td colspan="7"><strong>EUBAL-I</strong></td></tr><tr><td>Posidonia</td><td>04/03/2002</td><td>18</td><td>37.61</td><td>14.4</td><td>4.2</td><td>0.15</td></tr><tr><td>Bahia</td><td>06/03/2002</td><td>35</td><td>37.65</td><td>14.3</td><td>17.3</td><td>0.14</td></tr><tr><td>Station 4</td><td>08/03/2002</td><td>37</td><td>37.53</td><td>14.3</td><td>16.7</td><td>0.11</td></tr><tr><td>Cap Enderrocat</td><td>10/03/2002</td><td>20</td><td>37.62</td><td>14</td><td>11.4</td><td>0.14</td></tr><tr><td colspan="7"><strong>EUBAL-II</strong></td></tr><tr><td>Posidonia</td><td>20/06/2002</td><td>13</td><td>37.80</td><td>22.6</td><td>3.3</td><td>0.16</td></tr><tr><td>Bahia</td><td>22/06/2002</td><td>33</td><td>37.78</td><td>22.4</td><td>4.9</td><td>0.09</td></tr><tr><td>Station 4</td><td>18/06/2002</td><td>33</td><td>37.76</td><td>20.8</td><td>2.6</td><td>0.08</td></tr><tr><td>Cap Enderrocat</td><td>24/06/2002</td><td>16</td><td>37.76</td><td>23</td><td>1.5</td><td>0.09</td></tr></tbody></table>
<table><caption>Table 2 Integrated planktonic gross primary production (GPP), community respiration (CR) and net community production (NCP) at four stations during the EUBAL-I and -II cruises.</caption><thead><tr><th rowspan="2">Station</th><th rowspan="2">Bottom depth m</th><th>GPP</th><th>CR</th><th>NCP</th></tr><tr><th colspan="3">mmol O<sub>2</sub> m<sup>-2</sup> d<sup>-1</sup></th></tr></thead><tbody><tr><td colspan="5"><strong>EUBAL-I</strong></td></tr><tr><td>Posidonia</td><td>18</td><td>36</td><td>-33</td><td>3</td></tr><tr><td>Bahia</td><td>35</td><td>98</td><td>-45</td><td>53</td></tr><tr><td>Station 4</td><td>37</td><td>92</td><td>-35</td><td>57</td></tr><tr><td>Cap Enderrocat</td><td>20</td><td>73</td><td>-27</td><td>46</td></tr><tr><td colspan="5"><strong>EUBAL-II</strong></td></tr><tr><td>Posidonia</td><td>13</td><td>72</td><td>-45</td><td>27</td></tr><tr><td>Bahia</td><td>33</td><td>86</td><td>-75</td><td>11</td></tr><tr><td>Station 4</td><td>33</td><td>56</td><td>-107</td><td>-51</td></tr><tr><td>Cap Enderrocat</td><td>16</td><td>29</td><td>-59</td><td>-30</td></tr></tbody></table>