New insights into POC dynamics in the subtropical northeast Atlantic Ocean

1 D..Juan Luis Gómez Pinchetti...SECRETARIO DEL DEPARTAMENTO DE .....Biología.... DE LA UNIVERSIDAD DE LAS PALMAS DE GRAN CANARIA CERTIFICA, Que el Consejo de Doctores del Departamento en sesión extraordinaria tomó el acuerdo de dar el consentimiento para su tramitación, a la tesis doctoral titulada "New insights into POC dynamics in the subtropical northeast Atlantic Ocean" presentada por el/la doctorando D. Iván Julio Alonso González y dirigida por el Dr. Javier Arístegui Ruiz y el Dr. Antoni Calafat Frau. Y para que así conste, y a efectos de lo previsto en el Art◦73.2 del Reglamento de Estudios de Doctorado de esta Universidad, firmo la presente en Las Palmas de Gran Canaria, a Octubre de 2010. 3 UNIVERSIDAD DE LAS PALMAS DE GRAN CANARIA Departamento: Biología Programa de Doctorado: Oceanografía. Bienio 2005-2007. Con Mención de Calidad de la ANECA. Título de la Tesis: "New insights into POC dynamics in the subtropical northeast Atlantic Ocean" Tesis Doctoral presentada por D. Iván Julio Alonso González Dirigida por: Javier Arístegui Ruiz - ULPGC Antoni Calafat Frau - Universitat Barcelona El Director El Codirector El Doctorando Las Palmas de Gran Canaria, Diciembre de 2010 A mis padres y Verónica... Acknowledgments/ Agradecimientos "... dejé esa roca llorando. Es que dejaba en ella raíces en la roca y raíces de roca". Miguel de Unamuno, Fuerteventura, 1924 Alo largo de la vida, y aunque ha sido duro, he ido cosechando triunfos y fracasos que me han moldeado como persona. Sin embargo, rápidamente te das cuenta de que nada valen si no tienes a quién agradecércelo. Bueno, pues ha llegado la hora de agradecer a toda las personas la ayuda que me han brindado durante el camino hacia este "triunfo personal". Empezaré, con el permiso de la ciencia, por lo que considero más importante, la familia. Mis padres, Antonio y Ángela, dos majoreros de los que están en peligro de extinción, y de los que habría que hacer una tesis doctoral sobre ellos. Digo esto, porque siendo seis hermanos y estando la situación económica familiar "justita" permiten y apoyan a un hijo, el cual les sale rana, que dice "quiero estudiar". A eso le llamo yo sabiduría y valor!, no de lo que alardeamos los "universitarios". Dicho esto, y teniendo en cuenta que ni siquiera sabían que era eso de las Ciencias del Mar, ya sólo me queda agraderles y dedicarles al completo esta tesis doctoral. A mis hermanos, Sandra, Raúl, Toño, Neli y Ayoze, gracias por el apoyo económico prestado durante la carrera y sobre todo por hacerme desconectar cuando volvía a casa, motivo por el cual me era muy difícil volver. Gracias también por esos apodos que me pusisteis: "inspector mejillón", "cientísico" (por mi color amarillo fluorescente de laboratorio), "el universitario",....qué burleteros que sois! Ahora, me gustaría agradecer de una manera muy especial a Verónica la ayuda, apoyo, cariño y la fuerza dada, pero sobre todo por ser la razón de todas las cosas. Creo que sin ti, no sólo hubiera sido más difícil sino que hubiese abandonado. Siempre has sido la que en los momentos difíciles tomabas las riendas de los ánimos y empujabas con valentía. Gracias por hacer sacrificios Contents 1 INTRODUCTION 1 1.1 GENERAL INTRODUCTION .................. 1 1.1.1 Organic matter in the ocean ................ 1 1.1.2 Balance between synthesis and destruction of particulate organic carbon in the epipelagic waters .......... 3 1.1.3 Carbon balance in the mesopelagic waters ........ 5 1.1.4 Impact of mesoscale eddies on organic carbon fluxes . . 6 1.2 THESIS OBJETIVES AND ORGANIZATION ......... 13 I Particle settling velocity spectrum 17 2 Role of slowly settling particles in the ocean carbon cycle 19 2.1 Introduction ............................. 22 2.2 Methods ............................... 23 2.2.1 Sampling .......................... 23 2.2.2 POC and Biomarker Analysis ............... 24 2.2.3 Integrated Mass Flux Density Calculation ........ 24 2.3 Results ................................ 24 2.3.1 Fluxes and Current Velocity Variability ......... 24 2.3.2 Particle Settling Velocity Spectrum ............ 25 2.4 Discussion .............................. 28 2.4.1 Effect of Current Velocity on POC Fluxes ........ 28 2.4.2 Particle Settling Velocity Spectra ............. 29 2.4.3 Implications of Slowly Settling Particles Dominating the Size Spectrum ........................ 30 2.5 References .............................. 34 2.6 Appendix I ............................. 39 2.6.1 Chlorophyll concentration and mixed layer depth seasonality ............................. 39 2.6.2 Principal components analysis ............... 41 x Contents II Suspended and slowly-sinking particulate organic carbon 45 3 Lateral POC transport and consumption in surface and deep waters of the Canary Current region: a box model study 47 3.1 Introduction ............................. 50 3.2 Data and Methods ......................... 52 3.3 Results ................................ 54 3.3.1 POM Concentrations .................... 54 3.3.2 POC Transport ....................... 57 3.4 Discussion .............................. 60 3.4.1 Coastal Ocean Gradients in Suspended POM ...... 60 3.4.2 Offshore Suspended Organic Carbon Pumping to the Interior of the North Atlantic Ocean ............ 62 3.4.3 Carbon Budget and Mesopelagic Respiration ...... 66 3.5 References .............................. 72 4 Spatio-temporal variability of water column respiration in the Canary Basin: the role of suspended particulate organic carbon 81 4.1 Introduction ............................. 84 4.2 Data and Methods ......................... 85 4.2.1 Data sources ........................ 85 4.2.2 Respiratory Electron Transport System (ETS) activity . 86 4.2.3 POM analysis ........................ 87 4.3 Results ................................ 87 4.3.1 Hydrographic structure .................. 87 4.3.2 Suspended particulate organic matter distribution . . . 90 4.3.3 Spatial variability in respiratory activity ......... 91 4.3.4 Temporal and depth variability in respiratory activity . 93 4.4 Discussion .............................. 96 4.4.1 Epipelagic respiration ................... 96 4.4.2 Mesopelagic respiration .................. 97 4.4.3 Contribution of POCsusp to water column respiration . . 99 Contents xi 4.5 Conclusions ............................. 101 4.6 References .............................. 103 III Sinking particulate organic carbon: role of mesoscale eddies 109 5 Regional and temporal variability of sinking organic matter in the subtropical northeast Atlantic Ocean: a biomarker diagnosis 111 5.1 Introduction ............................. 114 5.2 Methods ............................... 116 5.2.1 Locating mesoscale eddies ................. 116 5.2.2 Sample collection ...................... 116 5.2.3 POM analysis ........................ 117 5.2.4 Pigment analysis ...................... 118 5.2.5 Amino acid analysis .................... 119 5.2.6 Statistical analyses (PCA) ................. 120 5.3 Results ................................ 120 5.3.1 Oceanographic settings ................... 120 5.3.2 Sinking POM fluxes .................... 121 5.3.3 Pigment fluxes and composition .............. 125 5.3.4 Total hydrolyzable amino acid (THAA) fluxes and composition ........................... 128 5.4 Discussion .............................. 130 5.4.1 Eddy-field influence on organic matter fluxes ...... 130 5.4.2 Cyclonic vs. anticyclonic eddies .............. 135 5.4.3 Regional variability in organic matter composition and flux137 5.5 Conclusions ............................. 139 5.6 References .............................. 142 6 Increased carbon sequestration by mesoscale eddies in the northeast Atlantic Ocean 153 6.1 Introduction ............................. 156 6.2 Methods ............................... 157 xii Contents 6.2.1 Studied area and sampling ................. 157 6.2.2 POC and biomarkers analysis ............... 158 6.2.3 Principal components analysis (PCA) .......... 158 6.3 Results and Discussion ....................... 159 6.3.1 Impact of cyclonic eddies and zooplankton activity on organic matter fluxes and composition .......... 159 6.3.2 Annual influence of cyclonic eddies on carbon sequestration167 6.3.3 Role of cyclonic eddies and migrant zooplankton on the mesopelagic carbon imbalance ............... 168 6.4 Conclusions ............................. 169 6.5 References .............................. 172 6.6 Appendix II ............................. 177 6.6.1 Climatological ROMS (Regional Ocean Modeling System) numerical model configuration of the Canary Basin 177 7 GENERAL DISCUSSION 181 7.1 Role of suspended and slowly-sinking POC in the water column biogeochemistry ........................... 181 7.2 Significance of mesoscale eddies to POC dynamic in the subtropical northeast Atlantic ....................... 186 7.3 Conceptual model of POC flow and decomposition in the Canary Basin ................................. 189 8 CONCLUSIONS 197 9 Spanish summary/ Resumen en español 201 9.1 INTRODUCCIÓN GENERAL .................. 201 9.1.1 La materia orgánica en el océano ............. 201 9.1.2 Balance entre síntesis y destrucción de carbono orgánico particulado en la aguas epipelágicas ........... 205 9.1.3 Balance de carbono en las aguas mesopelágicas . . . . . 207 9.1.4 Impacto de los remolinos mesoescalares en los flujos de carbono orgánico ...................... 210 9.2 Objetivos de la tesis y organización ................ 221 Contents xiii 9.3 METODOLOGÍA ......................... 225 9.4 RESULTADOS Y DISCUSIÓN GENERAL ........... 230 9.4.1 Papel del carbono suspendido y de baja tasa de sedimentación en la biogeoquímica de la columna de agua . 230 9.4.2 Importancia de los remolinos mesoescalares en la dinámica del POC en el Atlántico Noreste subtropical . 235 9.4.3 Modelo conceptual de flujos y descomposición de POC en la Cuenca Canaria ................... 240 9.5 CONCLUSIONES ......................... 252 List of Figures 2.1 Seasonal variability of variables measured with IRSC sediment traps. Mass flux (grey squares); POC fluxes (grey bars); mol% glycine (grey dots); current velocity measured with current meters at 275 m depth (black dots). (a) Period I: from June 2005 to December 2005. (b) Period II: from December 2005 to June 2006. (c) Period III: from June 2006 to December 2006. (d) POC flux versus current velocity for periods I and II. ...... 26 2.2 Settling velocity groups. Time-integrated mass flux density (IMFD) versus particle settling velocity for (a) period I, (b) period II, and (c) period III. Black lines correspond to each of the SV traps (SV1 and SV2), grey bars stand for the average of SV1 and SV2 and grey lines stand for the relative contribution (in %) of each of the velocity-classes of particles to the total POC flux. See Figure 3.1 for period dates. (d) Mass flux density normalized to total mass flux, for the RODA, Medflux and VERTIGO deployments. ............................ 27 2.3 Seasonal variability of surface Chl-a concentration, mixed layer and euphotic zone depth (MLD and Ze, respectively). Empty spaces in the Chl-a time evolution are due to the presence of clouds. ................................ 40 2.4 Principal component analysis (PCA) of the different particle velocity groups. PCA was conducted on amino acid and pigment composition data in material collected using IRSC sediment traps. Samples are divided into two categories: slowly settling particles (crosses) and fast settling particles (circles). This separation highlights the different compositions of these two classes of particles. ....................... 43 xvi List of Figures 3.1 Hydrographic box: black dots indicate the position of CTD stations. Locations of biogeochemical stations are circled. The full box was sampled between 7 and 29 September 2003. ...... 52 3.2 POC concentrations and C/N ratios along each section according to neutral density layers: (a) north, (b) south, (c) west, and (d) east transects. Locations and depths of sampling for POC are shown with black dots. ....................... 56 3.3 Integrated mass as a function of density layer for the north (black dash-dotted line), south (gray dashed line), west (gray dashdotted line), and east (black dashed line) transects with their net transport (black solid line). For each transect, positive and negative values mean outputs and inputs, respectively. The sign of the net transport is positive (negative) for divergence (convergence) flow out of (into) the box. ................. 58 3.4 POC fluxes (108mol C d−1) as a function of neutral density layers at each transect. Negative values for POC transport indicate inputs, and positive values indicate outputs. The y axes are labeled on the left by the neutral density and on the right by the average depth of the interfaces of each layer. ........... 59 3.5 Offshore suspended organic carbon fluxes (108mol C d−1) in the different water masses. The values were obtained by subtracting the open ocean baseline POC concentration calculated from the Bermuda Atlantic Time series Study (BATS). Note that the highest POC fluxes are in central waters of the more coastal section. ............................... 64 3.6 Comparison of the average POC profile measured during this study (CORICA) with the baselines used in the sensitive analysis to compute lateral POC fluxes. The BATS baseline was generated by fitting a power law equation to the average BATS POC profiles (black line). A fake baseline (dashed line) was derived by applying the same equation observed at BATS to higher surface POC values (see text for details). ............. 65 List of Figures xvii 4.1 Map indicating the stations location along two sections extending from the NW African coast to the open ocean. Black dots indicate the position of CTD stations. Locations of biogeochemical stations are circled. Position of the European Station for Time Series in the Oceans, Canary Islands, (ESTOC) is also showed. ............................... 86 4.2 Mean θ/S curves for 21◦N September 2002 (COCA I) and June 2003 (COCA II) and for 26◦N September 2002 (COCA I) and June 2003 (COCA II). σθisolines are also indicated. ...... 88 4.3 Vertical distribution (0-1000 m) of temperature (◦C) and salinity (psu) during COCA I cruise (September 2002). ......... 89 4.4 Vertical distribution (0-1000 m) of temperature (◦C) and salinity (psu) during COCA II cruise (June 2003). ............ 90 4.5 Vertical distribution (0-1000 m) of respiratory electron transport system (ETS) activity (µmol O2m−3h−1) for each cruise and section. Dots represent depths sampled at each station. ..... 92 4.6 Vertical distribution of average (both sections) ETS and POCsusp: (a) COCA I cruise (September 2002). (b) COCA II cruise (June 2003). (c) COCA I-COCA II average of POCsusp and ETS activity and ETS activity from the ESTOC station. (d) Regression lines for the relationship between ETS activity and POCsusp concentration during COCA I, COCA II and the COCA average cruises. Notice the deep peaks in POCsusp coinciding with the mesopelagic ETS maximums. The dashed lines stand for the interface between epipelagic and mesopelagic waters. 95 5.1 Map showing the location of the free-drifting sediment trap deployments carried out during August 2006 and February 2007. 4far-field, ⊗anticyclonic eddy, cyclonic eddy and + S stations.117 5.2 Vertical distribution of potential temperature across eddies CE1, CE2, AE1 and AE2. Ticks on the top axis represent XBT stations. Dashed lines indicated stations where sediment traps were deployed, coinciding with the location of the eddy core. . . . . . 122 List of Tables 1.1 Integrated daily rates (mmol O2m−2d−1) of gross primary production (GPP), net community production (NCP) and community respiration (R) from the August cruise (RODA I). Depth of integration, 120 m. POC flux (mmol C m−2d−1) at the base of the euphotic zone (150 m). ..................... 4 2.1 Average (±1SD) fluxes and contribution (%) of POC and PON to the total mass for each period. I, June 2005 to December 2005; II, December 2005 to June 2006; III, June 2006 to December 2006. 25 2.2 Pigment and amino acid biomarkers used to evaluate the degradation state of the two different settling velocity groups (>326 and 0.7-11 m d−1). See Table 2.1 for period dates. Dash indicates not determined; GABA, -aminobutyric acid; ND, not detected. 28 3.1 POC Fluxes in the Different Water Masses for the North, South, West, and East Transectsa..................... 60 3.2 Estimates of Vertical and Lateral POC Fluxes in the Different Water Massesa........................... 65 4.1 Mean suspended POC concentrations and C/N ratios (±standard deviation) in the epipelagic and mesopelagic waters during the two periods of study (September 2002 and June 2003). "Coastal": average value of coastal stations (stations 1 and 2 at 26◦N, stations 9 and 10 at 21◦N); "Oceanic": average value of oceanic stations (stations 3, 4 and 5 at 26◦N, stations 6, 7 and 8 at 21◦N). .................... 91 4.2 Mean volumetric values (±standard deviation) of plankton ETS activities in the epipelagic and mesopelagic waters during the two periods of study (September 2002 and June 2003). For "coastal", "oceanic" criteria see Table 4.1 caption. ............. 93 xxvi List of Tables 4.3 Integrated (epipelagic 0-200 m; mesopelagic 200-1000 m) values of plankton ETS activity from stations in the two sections during September 2002 and June 2003. For "coastal", "oceanic" criteria see Table 4.1 caption. ....................... 94 5.1 RODA drifting traps characteristics: type and station locations and depths of deployment. Time of sediment trap deployment was 24 h for both cruises. AE: anticyclonic eddy; CE: cyclonic eddy; FF: Far-field station. .................... 118 5.2 Chloropigment fluxes and compositions at 150 m in sediment trap samples from far-field (FF) and eddy-field stations during August 2006. chl: chlorophyll-a; pptn: pheophytin-a; ppb: pheophorbide-a; pyro: Pyropheophorbide-a: fuco: fucoxanthin. NDnot detected. .......................... 125 5.3 Diagnostic table of amino acid and pigment biomarkers used to examine variation in organic composition of sinking particles collected during the RODA project. ................ 126 5.4 Chloropigment fluxes and compositions at 200 m depth obtained from sediment trap samples during February 2007. chl: chlorophyll-a; pptn: pheophytin-a; ppb: pheophorbide-a; pyro: Pyropheophorbide-a: fuco: fucoxanthin. ND Ð not detected. . . 127 5.5 Amino acid fluxes and compositions at 150 m in sediment trap samples from far-field and eddy-field stations during August 2006. AA-C/POC is the contribution of amino acids to the total POC flux. ND -not detected. ................... 128 5.6 Amino acid fluxes and compositions at 200 m depth obtained from sediment trap samples during February 2007. AA-C/POC is the contribution of amino acids to the total POC flux. S8 amino acid sample was lost during analysis. See names for amino acids in Table 5.5. ND - not detected. .............. 129 5.7 Prokaryotic abundance (PA) determined by flow cytometry in water samples from surface to 200 m during August 2006 and February 2007. S2, S3, S4 and S5 correspond with ‘coastal’ stations while S6 and S7 stand for oceanic stations. ....... 132 List of Tables xxvii 6.1 Influence of eddies on POC fluxes. Average (±1 SD) fluxes (mg m−2d−1) of POC for eddy and non-eddy conditions. Teff = mesopelagic transfer efficiency defined as 500/290m and 1000/500m POC flux. R eddy/non-eddy = POC flux ratio between eddy and non-eddy conditions. Average eddy-induced carbon flux increase at 1000 m calculated as POC fluxes during eddy conditions minus POC fluxes during non-eddy conditions (9.9+21.3)/2 - (2.1+4.1)/2) = 12.5 mg C m−2d−1. I: June 2005-December 2005; II: December 2005-June 2006; III: June 2006-December 2006. * Anomalous values mediated by vertically migrating zooplankton (see text and Figure 6.3 for explanation). 161 9.1 Tasas integradas diarias (mmol O2m−2d−1) de producción primaria bruta (GPP), producción neta comunitaria (NCP) y respiración comunitaria (R) de la campaña de agosto (RODA I). Profundidad de integración, 120 m. Flujo de POC (mmol C m−2d−1) en la base de la capa fótica (150 m). ......... 207 Chapter 1 INTRODUCTION 1.1 GENERAL INTRODUCTION 1.1.1 Organic matter in the ocean Primary Production (PP) by phytoplankton cells is considered the main source of organic matter in the ocean [Mopper and Degens, 1979]. These microscopic flora play a key role in the ocean carbon cycle by converting inorganic carbon into organic matter through photosynthesis. Other minor, but locally important inputs of organic matter, in addition to primary production by marine plankton and macrophytes, include terrestrial inputs by rivers, atmosphere deposition, resuspension of organic matter from marine sediments, hydrothermal emissions, chemoautotrophy, and direct oil spills. On the contrary, ocean respiration (R) is the process whereby heterotrophic organisms obtain energy through oxidation of organic matter and converted back it into its inorganic constituents. Since organic matter cycling rely on the balance of these two processes, PP and R are widely accepted as critical factors controlling the carbon cycle in the ocean [Arístegui et al. 2005]. However, the mechanisms controlling the distribution of organic matter in the water column have received less attention presumably because of their difficulty in quantifying such processes in situ. Understanding how these mechanisms of transport operate is crucial for quantitative prediction of organic matter fluxes and pathways in different environments. An essential aspect to try understand the mechanisms involved in the carbon transport is to identify the different carbon pools presented in the water column. Traditionally, organic matter in the ocean has been operationally divided into two different pools according to filtration techniques. Organic 2 Chapter 1. INTRODUCTION matter passing through glass-fiber filters with an effective pore size of about 0.2-0.7 µm is assumed to be dissolved organic matter (DOM), while material retained is considered particulate organic matter (POM). Another key issue affecting carbon dynamics in the water column is the organic matter composition. DOM in surface waters consists of a mixture of very old, refractory DOM and a smaller fraction of young, labile DOM [Benner, 2002] produced in situ by plankton communities. In tropical and subtropical areas, most of the bioavailable DOM fraction is mineralized at surface and upper mesopelagic waters contributing little to deep-water prokaryotic metabolism or carbon storage in the dark ocean. Indeed, DOC exported with the overturning circulation accounts for only 10-20% of the global apparent oxygen utilization in the dark ocean [Arístegui et al. 2002; Hansell and Carlson, 20xx]. This supports the current view that microbial life in the deep ocean is mainly driven by the organic particulate pool [Honjo 1996; Bendtsen et al. 2002; Arístegui et al. 2009]. Regarding to the particulate pool, organic composition of POM is dominated by phytoplankton derived compounds [Lee et al. 2004]. However, during its travel to deeper levels, organic matter undergoes alteration of its original composition due to heterotrophic activity. Such alteration of the original signature is particle size-dependent, thus the interest of determine the different size classes of particles. Particles carrying organic carbon in the ocean are part of a size continuum [Verdugo et al. 2004], however, they are operationally divided by oceanographers into two distinct classes attending to its properties: i) suspended particulate organic carbon (POCsusp), and ii) sinking particulate organic carbon (POCsink). The differentiation between these fractions is essential since each of them present a different behavior in the water column. POCsusp is assumed to comprise particles ranging from 0.7 to 50 µm while POCsink those generally larger than about 50 µm [McCave, 1975; 1984]. POCsusp dominates the standing stock of particulate matter in the ocean [McCave, 1975; Kepkay 2000], although, surprisingly, our knowledge of its biogeochemical significance is scarce. This lack of information has been due to the fact that researchers have traditionally focused on sinking particulate organic carbon [Suess, 1980; 1.1. GENERAL INTRODUCTION 3 Boyd and Trull, 2007]. On the contrary, the transfer of organic carbon produced in surface waters to the deep ocean via POCsink is critical, on a large scale, to the removal of climatically active elements, such as carbon dioxide from the atmosphere. Recent evidence suggest that the behavior of particles in the water column is not only dependent of particle size, but also of the difference between its average density and that of the surrounding water [Burd and Jackson, 2009]. Thus, particle settling velocity is thought to be the key issue influencing vertical fluxes and carbon remineralization, although little is known about its spatio-temporal variability. Particle settling velocity determines whether organic carbon undergoes lateral or vertical transport, travelling within or across water masses, respectively. Therefore, an interesting question arises: What is the regional and temporal variability in the shape of the particle settling velocity spectrum? 1.1.2 Balance between synthesis and destruction of particulate organic carbon in the epipelagic waters In the global ocean and in steady state, the amount of photosynthetically fixed organic matter by autotrophic organisms has to be balanced by the organic matter consumption by heterotrophic organisms. Nevertheless, regional studies on plankton metabolism suggest a regional variability in the metabolic balance between autotrophic and heterotrophic processess. Indeed, several experiments on plankton metabolism conducted in the subtropical Northeast Atlantic Ocean have reported that this is a net heterotrophic ecosystem [Duarte et al. 2001; González et al. 2001; Serret et al. 2002]. A possible explanation to this imbalance is that gross primary production could be underestimated due to methodological issues [Robinson and Williams, 2005]. Duarte et al. [2001] suggest that the organic carbon needed to support this imbalance must be supplied by external inputs (e.g., lateral transport and atmospheric deposition). Another possibility reported by other authors is that these rates may be biased by its different time scale as well as its different spatio-temporal 4 Chapter 1. INTRODUCTION variability, especially PP [del Giorgio et al. 1997; Arístegui and Harrison, 2002; Karl et al. 2003; Williams et al. 2004]. South of the Canary Islands, Arístegui et al. [2003] suggest that the high respiration rates measured in the Canaries are fueled by mesoscale eddies and external inputs of organic matter. Despite the apparently consistency of this anomaly, an heterotrophic metabolic imbalance (P<R) can hardly be explained when particles are collected below the euphotic zone, if we take into account only the carbon production and export from the surface ocean. As an example, Table 9.1 shows the results of a study conducted in the subtropical northeast Atlantic (unpublished data) where we looked at mesoscale and regional trends in both plankton metabolism and POCsink fluxes obtained from in vitro changes in dissolved oxygen and free floating sediment trap deployments, respectively. Table 1.1: Integrated daily rates (mmol O2m−2d−1) of gross primary production (GPP), net community production (NCP) and community respiration (R) from the August cruise (RODA I). Depth of integration, 120 m. POC flux (mmol C m−2d−1) at the base of the euphotic zone (150 m). Station Lat. N Long. W GPP NCP R P/R POC flux 1 29.42 20.02 58.8 -47.3 106.5 0.55 5.53 2 28.75 18.27 112.2 -7.2 119.2 0.94 6.06 3 27.59 17.33 89.2 -16.4 105.5 0.85 13.09 4 27.58 15.60 113.5 -7.7 121.0 0.94 6.38 5 27.71 16.00 73.0 -11.6 84.7 0.86 9.63 As can be observed, NCP rates were always negative during RODA I cruise (August, 2006). Therefore, we might expect that the POC export from the euphotic zone is negligible. Nevertheless, these stations presented considerable POC export rates ranging from 5.5 to 13 mmol C m−2d−1rising the question of the origin of the organic matter below the euphotic zone. This conundrum leads us to the second question we would like to answer in our study: Are we correctly interpreting carbon balances in surface waters by just looking at the 1.1. GENERAL INTRODUCTION 5 in situ production rates? 1.1.3 Carbon balance in the mesopelagic waters Over the last two decades several evidences indicate that mesopelagic prokaryotes represent a major metabolic component of the ocean [see review by Arístegui et al. 2009]. According to the classical view of the biological pump, prokaryotic assemblages in the mesopelagic waters are supplied with particulate organic matter largely formed in the surface waters and transported down into the ocean via sinking particles. This is corroborated by the finding that dissolved organic carbon (DOC) contributes only 10-20%, at a global scale, to the remineralization rates in the dark ocean [Arístegui et al. 2002]. Nevertheless, sinking POC collected with current sediment traps does not explain the remaining 80-90% of oxygen utilization rates in the dark ocean [Reinthaler et al. 2006; Steinberg et al. 2008; Baltar et al. 2009]. This apparent imbalance is one of the most exciting unresolved paradoxes in the ocean carbon cycle and indicates either the existence of alternative mechanisms to fulfill the high carbon demand of the mesopelagic waters or that metabolic activity in the dark ocean is being over-estimated. The calculation of the conversion factors used to estimate metabolic rates in the deep waters present several uncertainties [Burd et al. 2010], so over-estimation of the metabolic rates would be possible. However, estimates of bacterial metabolic activity in deep NW Mediterranean waters are suggested to be greater at in situ pressures compared with those made under decompressed conditions [Tamburini et al. 2003], indicating that unaccounted carbon sources must exist [see Burd et al. 2010 for more details]. One of these unaccounted carbon sources could be the presence of low-sinking or suspended organic carbon (POCsusp) udersampled with current sediment traps. The majority of particulate organic matter in the water column is formed by suspended, neutrally buoyant particles [Kepkay 2000; Verdugo et al. 2004], although, paradoxically, the mechanisms of advective transport and remineralization of POCsusp are barely known [Bauer and Druffel, 1998], in contrast to sinking POC [see review in Boyd and Trull 2007]. Recently, Baltar 12 Chapter 1. INTRODUCTION Steinberg, D. K, et al. (2008), Microbial vs. zooplankton control of sinking particle flux in the ocean’s twilight zone, Limnol. Oceanogr., 53, 1327-1338. Suess, E., (1980), Particulate organic carbon flux in the oceans-surface productivity and oxygen utilization, Nature, 288, 260-263. Sweeney, E. N., D.J. McGillicuddy, and K.O. Buesseler (2003), Biogeochemical impacts due to mesoscale eddy activity in the Sargasso Sea as measured at the Bermuda Atlantic Time Series Study (BATS), Deep-Sea Res., II 50, 3017-3039. Tamburini, C., J. Garcin, A. Bianchi (2003), Role of deep-sea bacteria inorganic matter mineralization and adaptation to hydrostatic pressure conditions in the NW Mediterranean Sea. Aquatic Microbial Ecology 32, 209-218. Verdugo, P., A. L. Alldredge, F. Azam, D. L. Kirchman, U. Passow, and P. H. Santschi (2004), The oceanic gel phase: A bridge in the DOM-POM continuum, Mar. Chem., 92, 67-85. 1.2. THESIS OBJETIVES AND ORGANIZATION 13 1.2 THESIS OBJETIVES AND ORGANIZATION The general aim of this thesis was to deepen our understanding of the particulate organic carbon (POC) dynamic in the subtropical northeast Atlantic ocean, as well as to determine the biogeochemical significance of the two fractions accounting for total POC (non-sinking and sinking POC). To achieve this goal, several specific objectives were tackled. Basically, we tried to respond to the questions raised in the general introduction: - 1. What is the regional and temporal variability in the shape of the settling velocity spectrum? - 2. What is the contribution of suspended POC to the carbon demand in the dark ocean? Is there any mechanism able to supply enough POCsusp to fulfill the metabolic carbon demand in the mesopelagic waters? - 3. What is the degree of coupling between suspended POC and respiration? - 4. Can we elucidate what are the factors controlling carbon export within eddies using biomarkers? - 5. Can eddies change the composition of the exported organic matter? - 6. Can eddies enhance carbon sequestration in the deep ocean? ∗To address the first question, we deployed a mooring in the Canary Current region over a 1.5-year period. This mooring accommodated Indented Rotating Sphere Carousel (IRSC) sediment traps [Peterson et al., 2005] at 260 m, with the capacity of separating particles into discrete classes as a function of their sinking velocity. In order to know the potential biogeochemical role of each settling velocity fraction, we performed analysis of amino acid and chloropigment fluxes and compositions. (Chapter 2) This work has resulted in the following publication: 14 Chapter 1. INTRODUCTION -"Role of slowly settling particles in the ocean carbon cycle" published in Geophysical Research Letters (GRL). ∗To try to resolve the apparent carbon imbalance in surface and mesopelagic waters (questions 2 and 3), two chapters are presented. In the first study, to answer question 2, we estimated the horizontal transport and consumption, from surface to 3000 m depth, of suspended particulate organic carbon (POC) collected with oceanographic bottles. The analysis was performed through a box model approach, with physical boundaries extending from 20◦to 29◦10’N and 20◦35’ to 26◦W (1000 x 600 Km) in the Canary Current region. (Chapter 3) ∗In the second study, to answer question 3, the spatio-temporal variability in the epipelagic and mesopelagic respiration through the enzymatic activity of the electron transport system (ETS) in microplankton was analyzed. This study was conducted along two zonal sections (21◦N and 26◦N) extending from the northwest African costal upwelling to the open ocean waters of the subtropical North Atlantic. (Chapter 4) These works have resulted in the following publications: -"Lateral POC transport and consumption in surface and deep waters of the Canary Current region: A box model study" published in Global Biogechemical Cycles (GBC). -"Spatio-temporal variability of water column respiration in the Canary Basin: the role of suspended particulate organic carbon" submitted to Journal of Marine Systems (JMS) ∗In order to elucidate the factors controlling carbon export within eddies we report, together with total POC/PON fluxes, mesoscale and regional trends in amino acid (THAA) and chloropigment compositions and fluxes obtained 1.2. THESIS OBJETIVES AND ORGANIZATION 15 from free floating sediment trap deployments in the northeast Atlantic Ocean. (Chapter 5) This work has resulted in the following publication: -"Regional and temporal variability of sinking organic matter in the subtropical northeast Atlantic Ocean: a biomarker diagnosis" published in Biogeosciences (BG). ∗To address the specific objectives number 5 and 6, we measured POC, amino acid and chloropigment fluxes and compositions in samples collected from a mooring deployed in the area of generation of cyclonic eddies south of the Canary Islands over a 1.5-year period. The effects of the presence of an eddy were investigated from surface down to 1000 m.(Chapter 6) This work has resulted in the following publication: -"Increased carbon sequestration by mesoscale eddies in the northeast Atlantic Ocean" submitted to Proceedings of the National Academy of Sciences, (PNAS). Part I Particle settling velocity spectrum Chapter 2 Role of slowly settling particles in the ocean carbon cycle Iván Alonso-González1, Javier Arístegui1, Cindy Lee2, Anna SánchezVidal3, Antoni Calafat3,Joan Fabrés4,Pablo Sangrá1, Pere Masqué5, Alonso Hernández-Guerra1and Verónica Benítez-Barrios.1 1Facultad de Ciencias del Mar, Universidad de Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, 35017, Spain 2School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY 11794-5000, USA 3GRC Geocincies Marines, Dep. de Estratigrafia i Paleontologia, Universitat de Barcelona, Barcelona, 08028, Spain 4UNEP Shelf Programme Facility, UNEP/GRID-Arendal, Arendal, Norway. 5Institut de Ciéncia i Tecnologia Ambientals, Departament de Física, Universitat Autónoma de Barcelona, Bellaterra, Spain. Geophysical Research Letters, 37, L13608, doi:10.1029/2010GL043827, 2010 Abstract Here we present results from sediment traps that separate particles as a function of their settling velocity, which were moored in the Canary Current region over a 1.5-year period. This study represents the longest time series using "in situ" particle settling velocity traps to date and are unique in providing year-round estimates. We find that, at least during half of the year in subtropical waters 20 Chapter 2. Role of slowly settling particles in the ocean carbon cycle (the largest ocean domain), more than 60% of total particulate organic carbon is contained in slowly settling particles (0.7-11 m d−1). Analyses of organic biomarkers reveal that these particles have the same degradation state, or are even fresher than rapidly sinking particles. Thus, if slowly settling particles dominate the exportable carbon pool, most organic matter would be respired in surface waters, acting as a biological source of CO2susceptible to exchange with the atmosphere. In the context of climate change, if the predicted changes in phytoplankton community structure occur, slowly settling particles would be favored, affecting the strength of the biological pump in the ocean. KEYWORDS: Particle settling velocity, Lateral transport, carbon balance 21 Contents 2.1 Introduction ......................... 22 2.2 Methods ............................ 23 2.2.1 Sampling ........................... 23 2.2.2 POC and Biomarker Analysis ................ 24 2.2.3 Integrated Mass Flux Density Calculation ......... 24 2.3 Results ............................. 24 2.3.1 Fluxes and Current Velocity Variability .......... 24 2.3.2 Particle Settling Velocity Spectrum ............. 25 2.4 Discussion ........................... 28 2.4.1 Effect of Current Velocity on POC Fluxes ......... 28 2.4.2 Particle Settling Velocity Spectra .............. 29 2.4.3 Implications of Slowly Settling Particles Dominating the Size Spectrum ........................ 30 2.5 References ........................... 34 2.6 Appendix I .......................... 39 2.6.1 Chlorophyll concentration and mixed layer depth seasonality .............................. 39 2.6.2 Principal components analysis ............... 41 28 Chapter 2. Role of slowly settling particles in the ocean carbon cycle To evaluate the degradation state of these two different classes of settling particles we selected four biomarkers: chlorophyll-a, pheophytin-a, pheophorbide-a and -aminobutyric acid (Table 2.2). During Period I, biomarkers indicated that the dominant slowly settling particles were fresher than the rapidly settling particles (the latter enriched in pheophytin and Gaba mole%), whereas the opposite pattern was found during Period II. Additionally, glycine, a diatom indicator, was used to evaluate the contribution of this phytoplankton group to the carbon fluxes. During period II, mole% glycine and POC flux follow a similar behavior characterized by a directly proportional relationship (r2= 0.84; p < 0.05). Table 2.2: Pigment and amino acid biomarkers used to evaluate the degradation state of the two different settling velocity groups (>326 and 0.7-11 m d−1). See Table 2.1 for period dates. Dash indicates not determined; GABA, -aminobutyric acid; ND, not detected. 2.4 Discussion 2.4.1 Effect of Current Velocity on POC Fluxes Previous laboratory and field analysis regarding the effects of flow velocity on the collection efficiency of sediment traps have shown conflicting results (see reviews by Gardner [2000] and Buesseler et al. [2007b]). Here we report new results that fuel this controversy, but may represent a step forward in understanding the complex mechanisms that control sediment trap collection efficiency. Our observed correlations between flow velocity and POC flux also show contradictory results (Figure 2.1d). Period I shows a decrease in POC flux with increased flow velocity (Pearson’s r = -0.64, p < 0.05), while 2.4. Discussion 29 during Period II no statistically difference was found. This change in the flux-flow velocity relationship could be explained by the modifications that the ecosystem undergoes with time. Period I is dominated by slow sinking particles which are susceptible to lateral advection, while Period II is dominated by fast sinking particles that are presumably less affected by current velocity. According to these results, particle-settling velocity is a key factor controlling the hydrodynamic biases affecting sediment traps, in agreement with Gust and Kozerski [2000]. 2.4.2 Particle Settling Velocity Spectra The analysis of the temporal evolution of near-surface Chl-a and depth of the mixed layer (MLD) and euphotic zone (Ze) reveal that the depth interval between the bottom of the MLD and the depth of the sediment trap is higher during Periods I and III (when slow sinking particles dominate), suggesting that these particles were passively collected, rather than mixed down from surface to the trap depth (see Appendix 2.5). A comparison of the sinking rate spectra observed here with those obtained using IRSC traps at approximately the same depth (∼300 m) in the subarctic K2, subtropical ALOHA (North Pacific) and DYFAMED (Mediterranean) stations reveals important findings (Figure 2.2d). The DYFAMED station showed particle-sinking spectra similar to our Period II, characterized by a Gaussian portion of fast settling particles, which dominate sinking fluxes, and a tail of slowly settling particles [Armstrong et al., 2009]. More interesting is the fact that these studies were carried out in the same season as our Period II. This suggests that a large fraction of the surface primary production generated during the late-winter bloom (Figure 2.3) is rapidly (∼1 month) exported to the dark ocean via fast-settling particles. This phenomenon is induced by a higher contribution of large phytoplankton cells and zooplankton fecal pellets to the sinking flux as indicated by the contributions of glycine (Figure 2.1b) and pheophorbide to the organic matter (Table 2.2). 30 Chapter 2. Role of slowly settling particles in the ocean carbon cycle On the other hand, the SV spectra at both Pacific stations, determined in the same season that our Periods I and III (ALOHA, June 2004 and K2, July 2005) showed a contribution of slowly settling particles (2-13 m d−1) to the total POC flux ranging from 15 to 50% [Trull et al., 2008]. In addition to this significant contribution, the authors indicated that the addition of brine solution into the cups could have affected the entry of slowly settling particles. In our case, we used HgCl2diffusers within the cups, thus avoiding such problems [Peterson et al., 2005]. Moreover, the short rotation cycle of the IRSC valve (6 hours) used at the Pacific stations limited the minimum-settling rate that can be resolved to 2 m d−1(versus 0.68 m d−1with the 24 h cycle used in our study). Taking into account all these factors, it is reasonable to think that slowly settling particles could be a major fraction of the mass flux in those stations. Overall, these studies suggest that particle settling velocities in the ocean vary seasonally and with location, with profound implications for carbon sequestration in the deep ocean. 2.4.3 Implications of Slowly Settling Particles Dominating the Size Spectrum Our results give evidence that slowly settling particles dominated the carbon flux in our study during summer and autumn. In such a situation, sediment traps may miss a fraction of the exported POC in the smallest particles. Thus, if vertical carbon fluxes derived from sediment traps are used to construct budgets for different biogeochemical processes, strong imbalances may arise. Indeed, recent studies have reported important discrepancies between the mesopelagic metabolic carbon demand (MCD) of planktonic communities and the vertical carbon supply [Steinberg et al., 2008; Baltar et al., 2009]. We suggest that this "apparent" mismatch between MCD and vertical POC fluxes would presumably be less noticeable when fast-sinking particles dominate the flux and/or current velocities are low, as lateral transport would be relatively less important. The consumption of the undersampled slowly settling carbon pool could be therefore an additional mechanism buffering this imbalance by uncoupling MCD from vertical fluxes. However, considering the slow sinking 2.4. Discussion 31 rate of these particles, the effect of this undersampled carbon pool would be restricted to the upper mesopelagic waters (the place where the MCD is higher and the major decrease in molecularly-characterized material occurs) [Baltar et al., 2009; Lee et al., 2004]. Biomarkers indicate that the slowly settling particles have the same degradation state, or are even fresher, than the rapidly settling particles during the summer-autumn (Table 2.2). This observation raises the questions of how can a carbon pool that sinks at 1-10 m d−1be very labile? Could it be that slow sinking particles are in fact broken parts of larger particles, which were formed during rotation of the IRS ball? To test if the signal of fresh particles in a slow velocity class reflects these biases in the SV trap, we performed a principal components analysis (PCA) to quantitatively assess variation in the organic composition of the different settling particle classes. PCA indicates that the two velocity groups (slowly and fast sinking particles) differ in organic matter composition, giving evidence against this hypothesis (See Appendix 2.5). Other studies [Goutx et al., 2007; Wakeham et al., 2009] reached the same conclusion after analyzing the composition of particles collected at 200 m in the Mediterranean Sea and separated by settling velocity. Samples from the Pacific Ocean also showed that material collected by in situ filtration, assumed to be suspended or with low settling rates, contained a remarkable abundance of labile organic compounds [Lee et al., 2000; Sheridan et al., 2002]. Therefore, the high bioavailability of slowly settling particles seems likely to be a general feature rather than an isolated case. Small "suspended" particles may result from sinking particles disaggregated by physical forces [Burd and Jackson, 2009] or the activity of microbes and zooplankton [Sheridan et al., 2002], but also by self-assembly of dissolved organic material yielding porous microgels [Chin et al., 1998]. In all cases these small particles seem to be a suitable nutrient-rich habitat to be colonized by microorganisms. Indeed, recent studies have demonstrated a strong association between suspended particles and dark-ocean prokaryotic metabolism, 32 Chapter 2. Role of slowly settling particles in the ocean carbon cycle supporting the view that microbial life is mainly dependent on small buoyant particles [e.g., Baltar et al., 2009]. The high microbial activity reported during summer and autumn in the mesopelagic zone of the Canary region [Arístegui et al., 2005], would support our observations of a greater contribution of slowly sinking particles during these periods. In terms of carbon sequestration, the depth of organic matter decomposition determines whether respired CO2may be exchanged quickly with the atmosphere or rather be sequestered over long periods of time [Armstrong et al., 2001]. Thus, if slowly settling particles dominate the exportable carbon pool, most organic matter would be respired in the epipelagic and upper mesopelagic zones, acting as a biological source of CO2susceptible to exchange with the atmosphere. On the contrary, if fast-sinking particles contribute largely to the carbon flux, the carbon transfer efficiency to the mesopelagic waters increases, resulting in an enhanced carbon sequestration in the deep ocean. The implications of this work for understanding regional and global ocean carbon balances are profound if slowly settling particles are a significant portion of the exportable carbon pool. This phenomenon may explain several unresolved issues of the ocean carbon cycle. In the context of climate change, if the predicted changes in phytoplankton community structure occur, slowly settling particles would be favored, modifying the strength of the biological pump in the ocean. Our results also highlight the urgent need to extend our regional database of the sinking particle velocity spectrum, as well as to develop new technologies to measure and collect the total spectrum of sinking particles in the ocean. Acknowledgments This work has been funded through the Spanish "Plan Nacional de I+D" under the RODA (CTM2004-06842C03-03/MAR) project. We thank the captain and crew of the R/V García del Cid for their support at sea. Special thanks goes to Joan Puigdefábregas for his valuable help with the mooring design and 2.4. Discussion 33 handling and to Michael Peterson, who help with the IRSC traps. Thanks to Mercator Océan team members who made their model results readily available. P.M. was supported through the prize ICREA Academia funded by the Generalitat de Catalunya. We also thank two anonymous reviewers for their comments to improve the manuscript. 34 Chapter 2. Role of slowly settling particles in the ocean carbon cycle 2.5 References Arístegui, J., et al. (2002), Dissolved organic carbon support of respiration in the dark ocean, Science, 298, 1967, doi:10.1126/science.1076746. Arístegui, J., C. M. Duarte, J. M. Gasol, and L. Alonso-Sáez (2005), Active mesopelagic prokaryotes support high respiration in the subtropical northeast Atlantic Ocean, Geophys. Res. Lett., 32, L03608, doi:10.1029/2004GL021863. Armstrong, R. A., C. Lee, J. I. Hedges, S. Honjo, and S. G. Wakeham (2001), A new mechanistic model for organic carbon fluxes in the ocean: based on the quantitative association of POC with ballast minerals, Deep Sea Res., Part II, 49, 219-236, doi:10.1016/S0967-0645(01)00101-1. Armstrong, R. A., M. L. Peterson, C. Lee, and S. G. Wakeham (2009), Settling velocity spectra and the ballast ratio hypothesis, Deep Sea Res., Part II, 56, 1470-1478, doi:10.1016/j.dsr2.2008.11.032. Baltar, F., J. Arístegui, J. M. Gasol, E. Sintes, and G. J. Herndl (2009), Evidence of prokaryotic metabolism on suspended particulate organic matter in the dark waters of the subtropical North Atlantic, Limnol. Oceanogr., 54, 182-193. Bopp, L., O. Aumont, P. Cadule, S. Alvain, and M. Gehlen (2005), Response of diatoms distribution to global warming and potential implications: A global model study, Geophys. Res. Lett., 32, L19606, doi:10.1029/2005GL023653. Boyd, P., and P. Newton (1995), Evidence of the potential influence of planktonic community structure on the interannual variability of particulate organic-carbon flux, Deep Sea Res., Part I, 42, 619-639, doi:10.1016/09670637(95)00017-Z. Buesseler, K. O., et al. (2007a), Revisiting carbon flux through the ocean’s twilight zone, Science, 316, 567-570, doi:10.1126/science.1137959. 2.5. References 35 Buesseler, K. O., et al. (2007b), An assessment of the use of sediment traps for estimating upper ocean particle fluxes, J. Mar. Res., 65, 345-416. Burd, A. B., and G. A. Jackson (2009), Particle aggregation, Annu. Rev. Mar., Sci., 1, 65-90. Chin, W.C., M. V. Orellana, and P. Verdugo (1998), Spontaneous assembly of marine dissolved organic matter into polymer gels, Nature, 391, 568-572, doi:10.1038/35345. Gardner, W. D. (2000), Sediment trap technology and sampling in surface waters, in The Changing Ocean Carbon Cycle: A Midterm Synthesis of the Joint Global Ocean Flux Study, edited by R. B. Hanson et al., p. 240-281, Cambridge Univ. Press, New York. Goutx, M., et al. (2007), Composition and degradation of marine particles with different settling velocities in the northwest Mediterranean Sea, Limnol. Oceanogr., 52, 1645-1664. Guidi, L., et al. (2009), Effects of phytoplankton community on production, size, and export of large aggregates: A world-ocean analysis, Limnol. Oceanogr., 54, 1951-1963. Gust, G., and H.P. Kozerski (2000), In situ sinking-particle flux from collection rates of cylindrical traps, Mar. Ecol. Prog. Ser., 208, 93-106, doi:10.3354/meps208093. Lee, C., S. G. Wakeham, and J. I. Hedges (2000), Composition and flux of particulate amino acids and chloropigments in equatorial Pacific seawater and sediments, Deep Sea Res., Part I, 47, 1535-1568, doi:10.1016/S09670637(99)00116-8. 36 Chapter 2. Role of slowly settling particles in the ocean carbon cycle Lee, C., S. Wakeham, and C. Arnosti (2004), Particulate organic matter in the sea: The composition conundrum, Ambio, 33, 565-575. Lee, C., M. L. Peterson, S. G. Wakeham, R. A. Armstrong, J. K. Cochran, J. C. Miquel, S. W. Fowler, D. Hirschberg, A. Beck, and J. Xue (2009), Particulate organic matter and ballast fluxes measured using time-series and settling velocity sediment traps in the northwestern Mediterranean Sea, Deep Sea Res., Part II, 56, 1420-1436, doi:10.1016/j.dsr2.2008.11.029. Peterson, M. L., S. G. Wakeham, C. Lee, M. A. Askea, and J. C. Miquel (2005), Novel techniques for collection of sinking particles in the ocean and determining their settling rates, Limnol. Oceanogr. Methods, 3, 520-532. Ploug, H., M. Iversen, and G. Fischer (2008), Ballast, sinking velocity, and apparent diffusivity within marine snow and zooplankton fecal pellets: Implication for substrate turnover by attached bacteria, Limnol. Oceanogr., 53, 1878-1886. Sheridan, C. C., C. Lee, S. G. Wakeham, and J. K. B. Bishop (2002), Suspended particle organic composition and cycling in surface and midwaters of the equatorial Pacific Ocean, Deep Sea Res., Part I, 49, 1983-2008, doi:10.1016/S0967-0637(02)00118-8. Steinberg, D. K., et al. (2008), Microbial vs. zooplankton control of sinking particle flux in the ocean’s twilight zone, Limnol. Oceanogr., 53, 1327-1338. Trull, T. W., et al. (2008), In-situ measurement of mesopelagic particle sinking rates and the control of carbon transfer to the ocean interior during the Vertical Flux in the Global Ocean (VERTIGO) voyages in the North Pacific, Deep Sea Res., Part II, 55, 1684-1695, doi:10.1016/j. dsr2.2008.04.021. Wakeham, S. G., et al. (2009), Organic biomarkers in the twilight zone: Time series and settling velocity sediment traps during MEDFLUX, Deep Sea 2.5. References 37 Res., Part II, doi:10.1016/j.dsr2.2008.11.030. Part II Suspended and slowly-sinking particulate organic carbon Chapter 3 Lateral POC transport and consumption in surface and deep waters of the Canary Current region: a box model study Iván Alonso-González1, Javier Arístegui1, Juan Carlos Vilas1and Alonso Hernández-Guerra.1 1Facultad de Ciencias del Mar, Universidad de Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, 35017, Spain Global Biogeochemical Cycles, 23, GB2007, doi:10.1029/2008GB003185, 2009 Abstract We have estimated the lateral transport and consumption, from surface to 3000 m, of suspended particulate organic carbon (POC), through a box model approach, in the Canary Current region (subtropical northeast Atlantic). Our results show that lateral POC fluxes are up to 3 orders of magnitude higher than vertical fluxes. In the mesopelagic ocean, the central waters (100-700 m) presented a net carbon consumption of 8.51 x 108mol C d−1with the highest POC entering through the more coastal section. This lateral flux accounted for 28-59% of the total mesopelagic respiration (R), on the basis of lower and upper case scenarios of vertical POC inputs and dissolved organic carbon contribution 48 Chapter 3. Lateral POC transport and consumption to R. We suggest that boundary currents may support higher lateral export of coastally produced POC than previously assumed. A large fraction of this POC would, however, be remineralized in the upper 1000 m instead of being transported to the ocean interior. KEYWORDS: Lateral transport, suspended POC, remineralization 49 Contents 3.1 Introduction ......................... 50 3.2 Data and Methods ...................... 52 3.3 Results ............................. 54 3.3.1 POM Concentrations ..................... 54 3.3.2 POC Transport ........................ 57 3.4 Discussion ........................... 60 3.4.1 Coastal Ocean Gradients in Suspended POM ....... 60 3.4.2 Offshore Suspended Organic Carbon Pumping to the Interior of the North Atlantic Ocean ............. 62 3.4.3 Carbon Budget and Mesopelagic Respiration ....... 66 3.5 References ........................... 72 50 Chapter 3. Lateral POC transport and consumption 3.1 Introduction One of the interests of boundary currents in the global ocean context is the role they may play in the transport and remineralization of organic matter produced in coastal waters of continental margins. Several studies have suggested that margins may export significant amounts of organic matter to the ocean interior, which are not considered in global ocean biogeochemical models [e.g., Walsh, 199; Falkowski et al., 1994; Santschi et al., 1999; Liu et al., 2000; Wollast and Chou, 2001; Arístegui et al., 2005a; Ducklow and McCallister, 2005; Inthorn et al., 2006]. However, the overall exchange rate of organic matter between the coast and the open ocean remains a matter of speculation since the lateral transport of organic matter, rather than being directly measured, has being estimated by mass balance approaches, frequently solely on the basis of sinking particles [Walsh, 1991; Liu et al., 2000; Wollast and Chou, 2001; Ducklow and McCallister, 2005]. Bauer and Druffel [1998], comparing the natural radiocarbon abundance in two coastal and open ocean profiles in the water column, found that continental slope and rise waters of the North American coasts contained both dissolved (DOC) and suspended particulate (POCsusp) organic carbon concurrently older and in higher concentrations that in the adjacent subtropical gyres of the Atlantic and Pacific Oceans. These results led the authors to conclude from their study that the POCsusp inputs from ocean margins to the ocean interior could be more than an order of magnitude greater than inputs of recently produced organic carbon derived from the surface ocean. In spite of their observations, and the general knowledge that the suspended POM pool is quantitatively far larger than the sinking pool [McCave, 1984; Kepkay, 2000; Verdugo et al., 2004], the construction of ocean carbon budgets is still largely based on vertical fluxes of sinking POM (POMsink) collected with sediment traps. However, according to the abundance of suspended material, one would expect that a significant amount of excess suspended or low-sinking-rate particles, not remineralized on the continental margins, could be exported to the open ocean. Indeed, the analysis of POMsink collected with sediment traps deployed across the path of the Canary Current, revealed that most of the particulate material collected in the deeper traps proceeded from the NW Africa coastal upwelling system 3.1. Introduction 51 [Neuer et al., 2002a; Abrantes et al., 2002]. These particles traveled as far as 700 km off the coast, where the furthermost trap was deployed, suggesting a significant lateral transport of particles with low sinking rates from the continental margin to the open ocean. The exchange of material between margins and the open ocean would presumably be particularly intense along eastern boundary currents, because of the high productivity of the upwelling regions and the high mesoscale variability of their coastal transition zones (CTZ), which help enhance the exchange of shelf waters with the open ocean. During the past two decades intense effort has been focused on complex multidisciplinary programs along the CTZ of eastern boundary regions, like the California Current [Brink and Cowles, 1991] and the Canary Current [Barton et al., 1998; Barton and Arístegui, 2004] in the northern hemisphere. However, most of this research was restricted to the near-surface waters, looking at fluxes [e.g., Álvarez-Salgado et al., 2007] and variability [e.g., Basterretxea and Arístegui, 2000; Arístegui et al., 2005a] at the mesoscale level, but ignoring the deep-water transport of organic matter to the ocean interior. In this study we have estimated the horizontal transport and consumption, from surface to 3000 m depth, of particulate organic carbon (POC) collected with oceanographic bottles, assumed to be suspended in the water column or having very low sedimentation rates. We aimed to evaluate if the Canary Current and its underlying intermediate and deep waters act as links or sinks of organic matter transported from the NW African coast to the subtropical Gyre. The analysis was performed through a box model approach, with physical boundaries extending from 20◦to 29◦10’N and 20◦35’ to 26◦W (1000 x 600 Km) in the Canary Current region (subtropical northeast Atlantic Ocean), during a low productivity period in the year. To our knowledge this is the first effort to directly estimate the lateral transport of POMsusp across an eastern boundary current toward the ocean interior. 52 Chapter 3. Lateral POC transport and consumption 3.2 Data and Methods In September 2003, the R/V Thalassa carried out a high-density hydrographic survey along the path of the Canary Current (CORICA cruise). It consisted of four sections shaping a box with a total of 51 hydrographic (30 of them biogeochemical) stations (Figure 3.1). Conductivity, temperature and depth were recorded with a SeaBird 911 + CTD. The temperature and pressure sensors were calibrated at the SeaBird factory before the cruise. Salinity calibrations were carried out on board with a Guildline AUTOSAL model 8400 B salinometer (see Hernández-Guerra et al. [2005] for further details). Longitude Latitude CORICA Cruise −200 −1000 −2000 −3000 −4000 −5000 2425262728293031 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 6566 77 78 79 80 81 82 83 84 28oW 24oW 20oW 16oW 12oW 18oN 21oN 24oN 27oN 30oN Canary Islands Africa Figure 3.1: Hydrographic box: black dots indicate the position of CTD stations. Locations of biogeochemical stations are circled. The full box was sampled between 7 and 29 September 2003. At the biogeochemical stations (Figure 3.1), discrete samples for particulate 3.2. Data and Methods 53 organic matter (POM) were obtained at selected depths from surface to 3000 m (5, 150, 300, 500, 700, 1000, 1200, 1500, 2000, 2500 and 3000 m), by means of a rosette sampler equipped with 24 10 L Niskin bottles. Water samples (2-6 L) for particulate organic carbon and nitrogen (POC and PON, respectively) were collected and filtered onto precombusted (450 ◦C, 12 h) 25 mm Whatman GF/F filters. The filters were wrapped in precombusted aluminum foil and frozen at - 20 ◦C until processed. In the laboratory, the filters were thawed and dried overnight at 55 ◦C, then placed overnight in a desiccator saturated with HCl fumes, dried again with silica gel and packed in nickel sleeves. The carbon analyses were performed with a PerkinElmer 2400 CHN elemental analyzer [UNESCO, 1994]. The DOC adsorption onto GF/F filters was subtracted from samples to avoid the overestimation of POC [Turnewitsch et al., 2007]. DOC adsorption onto the filters ranged from 0.6 to 2 mmol C per 25 mm diameter GF/F filter (about 3.2 cm2of exposed filter), being similar to the blanks reported by Moran et al. [1999] and Turnewitsch et al. [2007]. In order to quantify the transport of organic matter to the open ocean, and to investigate the relative importance of the remineralization processes versus the overall transport in the Canary Current, we used a box model approach. For this purpose we selected a grid box across the path of the Canary Current, which was spaced from the continental shelf about 250-450 miles at its eastern section. The reason for this distancing was to avoid the large mesoscale variability, in the form of eddies and filaments close to the upwelling jet, which would impede to estimate with accuracy the mass transport fluxes. Hence we assume that a large fraction of organic matter exported from the coast could be already remineralized before entering in our box. The geostrophic velocities were obtained integrating the thermal wind equations, considering the neutral density level γn= 28.072 kg m−3as the reference level of no motion. This level generally occurs at the 3000 m isobath, along the interface separating Middle North Atlantic Deep Water (MNADW) and Lower North Atlantic Deep Water (LNADW). The choice of the reference level of no motion at γn= 28.072 kg m−3follows the study of 60 Chapter 3. Lateral POC transport and consumption Mass balance calculations in the upper surface water layer (above the neutral surface of 26.44) and the central waters (26.44-27.38) resulted in negative balances of 5.09x108mol C d−1and 8.51x108mol C d−1, respectively (Table 3.1), with the maximum transport concentrated through the more coastal section (20◦W). Intermediate waters (27.38-27.922) presented lower transports, except in the north transect. The overall balance at this depth layer yielded a positive carbon export of 3.38 x 108mol C d−1, with most of the transport channeled through the north section. Interestingly, the exported carbon is not transported from the south, where POC values at intermediate layers are low. Rather it seems to be transported from the east, and particularly from the Cape Blanc and Canary Islands regions, as suggested by the high POC values observed at these latitudes along the eastern transect. Finally, in the deep waters (27.922-28.072), the suspended POC transport was almost negligible. Table 3.1: POC Fluxes in the Different Water Masses for the North, South, West, and East Transectsa 3.4 Discussion 3.4.1 Coastal Ocean Gradients in Suspended POM Particles in the ocean exist in a continuum of sizes, but two classes are frequently recognized: suspended and sinking matter. They are distinguished operationally by the sampling method used to collect them: suspended matter with oceanographic bottles or large-volume in situ pumps [e.g., Turnewitsch et al., 2007], and sinking matter with sediment traps. Nevertheless, bottles may also trap particles with moderate to fast sedimentation rates [Gardner, 1977], whose contribution to the overall POM will depend on the relative 3.4. Discussion 61 importance of the sinking pool versus the suspended pool. The majority of POM in the water column is thought, however, to be formed by fine suspended material or particles with almost negligible sedimentation rates compared with horizontal fluxes [McCave, 1984; Kepkay, 2000; Verdugo et al., 2004]. These particles, referred to here as POCsusp, would be characterized by a conservative behavior in the water column undergoing lateral transport [Brun-Cottan, 1976]. In this study we have assumed that all POM collected with bottles represents suspended material or particles with very low sedimentation rates, susceptible of being transported horizontally. Strong evidence supports this hypothesis. Recent studies south of the Canary Islands, based on particle settling velocities using IRSC (Indented Rotating Sphere Carousel) traps [Peterson et al., 1993] during a 6 month period (summer to autumn 2005), indicate that about 60% of the POM collected in the traps have low sinking rates (<5 m d−1), allowing particles to be laterally transported [AlonsoGonzález et al., 2010]. Comparatively, the average POC sinking velocity recorded using the same sediment traps at the DYFAMED station in the Mediterranean Sea, is of 350 m d−1[Peterson et al., 2005; Armstrong et al., 2009]. The reason for the low sedimentation rates in the Canary region is still a matter of debate [e.g., Arístegui et al., 2003], but would explain the low export ratio with respect to the f ratio, reported by Neuer et al. [2002b] at the ESTOC station, north of the Canary Islands, compared to the Bermuda Time Series Station (BATS). Paradoxically, the POM concentrations collected with bottles in the water column are much higher in the Canary region. Indeed, POC at the BATS [Steinberg et al., 2001], like in other open ocean regions [e.g., Menzel and Goering, 1966], decrease exponentially with depth, reaching values typically <1 mmol L−1at depths >200 m. In our study, POC concentrations in the deep ocean (down to 3000 m) were >2 mmol L−1in the eastern sector of the box, decreasing toward the open ocean. An intermediate situation (range 1-3 mmol L−1POC at depths >200 m) is found in the Azores region [Vezzulli et al., 2002], a transition zone between the Canary Current and the central waters of the North Atlantic subtropical Gyre (NASG). 62 Chapter 3. Lateral POC transport and consumption Our results agree with the autumn values reported by Neuer et al. [2007] for the 200-1000 m layer at the ESTOC, which were the lowest recorded during the annual cycle. The highest average POM values in the upper 1000 m (as high as 8 mmol L−1) were reported for the spring months. No measurements were, however, carried out during summer [Neuer et al., 2007], when the upwelling activity, and hence the potential offshore export, is higher. Indeed, POC concentrations measured between the Canary Islands (28◦N) and Cape Blanc (21◦N), along four cruises carried out during spring (2003) and summer (2002), reached typical average concentrations of about 6 mmol L−1down to at least 2000 m (J. C. Vilas, personal communication, 2007), without any indication of an exponential decrease with depth. Thus, lateral transport of organic matter generated over the NW-Africa continental shelf may largely contribute to the POMsusp observed in the Canary Current region. The transport would be more pronounced during the periods of higher upwelling intensity, decreasing the concentrations toward the open ocean because of remineralization processes. Vilas et al. [2009] reached the same conclusion after studying the distribution of POM around Seine, a seamount placed east of Madeira Island, in the Canary Current. These authors observed peaks of POC in the 200-1000 m layer at the stations closer to the continental shelf and coinciding with the highest activity of the upwelling system. 3.4.2 Offshore Suspended Organic Carbon Pumping to the Interior of the North Atlantic Ocean To estimate the net lateral flux of POCsusp in the mesopelagic and bathypelagic waters, we first subtracted the open ocean ‘baseline’ POC concentration, obtained from averaging the monthly POC profiles in each depth layer at the Bermuda Atlantic Time-series (BATS) station, from the POC concentrations at the east and west transects. The BATS station, placed at the center of the NASG, presented a typical exponential decrease of POC with depth, reaching values <1µM below 200 m. In a comparative study of three subtropical time series stations (BATS, HOT and ESTOC), Neuer et al. [2002b] concluded that the annually integrated net primary production was similar at all three 3.4. Discussion 63 sites, with slightly lower values at ESTOC. However, the POC sinking flux (measured with drifting traps at about 150-200 m) was approximately 2-3 mmol C m−2d−1at BATS (Bermuda) and HOT (north of Hawaii), while at ESTOC (north of the Canary Islands) was only about 20% of these values (0.55 mmol C m−2d−1). Recent results (J. Arístegui, unpublished data, 2007; Alonso-González, unpublished data, 2007) of sinking POC, collected with similar traps at 150-200 m, from 30◦N to 21◦N, outside the influence of the intense eddy field, indicate that the POC flux varies on average from 0.7 to 2 mmol C m−2d−1from spring to autumn, increasing to 3-4 mmol Cm−2d−1 during the late winter bloom. Since sinking fluxes in our region of study are not higher than in BATS, we consider that the BATS POC would characterize the typical POC profile in the western Canary region, assuming only vertical flux of POC. Lateral fluxes were particularly intense along the east and west transects. Thus, we focused our analysis on the net balance considering the fluxes through these two transects. We calculated a lateral flux of suspended POC at the central and intermediate waters (100-1700 m depth layer) of 8.77 x 108mol C d−1and 4.8 x 108mol C d−1for the east and west transects respectively, extending along 1.01 x 106m in length (Figure 3.5). In any case, a simple sensitivity analysis was added to assess the effect of baseline subtraction to the magnitude of the lateral POC fluxes. First, the BATS POC data were fitted to a power law function, and then a "fake baseline" was generated by applying the same equation observed at BATS to higher surface POC values (Figure 3.6). Subtracting the fake baseline from the POC concentrations at the east and west transects, the lateral fluxes of suspended POC at Central and intermediate waters were 5.78 and 4.26 x 108 mol C d−1for the east and west transects respectively. The POC increase over the BATS baseline (1.5 times higher) results in a decrease in the lateral POC fluxes of 34% for the east transect and 11% for the west transect. 64 Chapter 3. Lateral POC transport and consumption Figure 3.5: Offshore suspended organic carbon fluxes (108mol C d−1) in the different water masses. The values were obtained by subtracting the open ocean baseline POC concentration calculated from the Bermuda Atlantic Time series Study (BATS). Note that the highest POC fluxes are in central waters of the more coastal section. Table 3.2 compares the vertical and lateral POC transport in the Canary region. The lateral fluxes correspond to this study, whereas the vertical fluxes were obtained from surface-tethered and deep-moored traps [Neuer et al., 1997, 2002b, 2007; Arístegui et al., unpublished data, 2003]. As observed, the lateral POC fluxes are 2 or 3 orders of magnitude higher than vertical fluxes depending on water masses, confirming our hypothesis of a more relevant horizontal versus vertical flux of POM per unit area. This conclusion is partly in agreement with the work of Bauer and Druffel [1998] who suggested that suspended POC inputs from ocean margins to the open ocean interior might be more than an order of magnitude greater than inputs of recently produced organic carbon derived from the surface ocean. However, we should keep in mind that the overall differential effect of the POC transport will depend on the aerial extension of the vertical versus lateral fluxes under consideration. 3.4. Discussion 65 ! Figure 3.6: Comparison of the average POC profile measured during this study (CORICA) with the baselines used in the sensitive analysis to compute lateral POC fluxes. The BATS baseline was generated by fitting a power law equation to the average BATS POC profiles (black line). A fake baseline (dashed line) was derived by applying the same equation observed at BATS to higher surface POC values (see text for details). Table 3.2: Estimates of Vertical and Lateral POC Fluxes in the Different Water Massesa 66 Chapter 3. Lateral POC transport and consumption 3.4.3 Carbon Budget and Mesopelagic Respiration The surface waters (0-100 m) inside the box received an overall higher external input (17.48 x 108mol C d−1; sum of north and east transects) of POCsusp than exported (12.39 x 108mol C d−1; sum of south and west transects) outside the box (Table 3.1). The resultant balance is 5.09 x 108mol C d−1 (0.85 mmol C m−2d−1). This value is in the range of the sinking POC flux reported above for the region of study, but somewhat higher than that estimated by Neuer et al. [2007] for the ESTOC (European Station for Time series in the Ocean, Canary Islands) north of the Canaries (Table 3.2). Sedimentation rates measured downstream the Canary Islands are however 2-4 times higher [Arístegui et al., 2004], because of the enhanced production and eddy filament exchange processes along the intense mesoscale field [Arístegui et al., 1994, 1997; Barton et al., 1998, 2004]. Island eddies are known to increase productivity leading to positive net community production [e.g., Arístegui and Montero, 2005]. A fraction of this excess production not sunk down may be laterally advected to the open ocean, contributing to the surface carbon budget inside our box. Assuming nonsignificant atmospheric inputs, the amount of carbon sedimented into the dark ocean (see above) would match the external inputs into the box, leading to a carbon balance in the surface waters. Nevertheless, Dachs et al. [2005] have reported high average net gaseous diffusive air water fluxes of organic carbon (25-30 mmol C m−2d−1) in the subtropical northeast Atlantic, which in case they occur during our study, would shift the balance toward a strong heterotrophy. Independently of whether the surface waters were or not in metabolic balance (see discussions by Duarte et al. [2001], Dachs et al. [2005], and Neuer et al. [2007]), the vertical export flux of POC to the dark ocean, which is the flux in which we are interested in our study, seems to be quite constant from spring to autumn, as derived from the sediment traps records. In order to calculate the respiration rate that could support the total carbon supply below the surface waters, we considered all the carbon fluxes inside the box. Sinking POC collected with surface-tethered traps range from 0.55 to 2 mmol C m−2d−1(see the above section). Drifting sediment traps 3.4. Discussion 67 have been frequently reported to underestimate the export flux [Michaels et al., 1994; Buesseler, 1998; Buesseler et al., 2000; Neuer et al., 2007]. However, results comparing POC flux in BATS, both derived from surface-tethered traps and 234Th [Buesseler, 1998], show that during low productivity (PP) periods (average PP from March to October: 36 mmol C m−2d−1) the traps and 234Th estimates reasonably agree, yielding average POC sedimentation rates of 2.6 mmol C m−2d−1, which corresponded to an export/ production ratio (e ratio) of 5-10%. At the ESTOC station (which is closer to the upwelling region than our sampling area), the average annual PP is about 30 mmol Cm−2d−1, with the lowest values (<10 mmol C m−2d−1) recorded during autumn [Neuer et al., 2007]. Similarly, low PP was measured by Basterretxea and Arístegui [2000] in an offshore station west of the Canary Islands, during summer. An e ratio of 5-10% would therefore lead to a POC flux of 0.5-1 mmol Cm−2d−1 at PP = 10 mmol C m−2d−1, and 1.5-3 mmol C m−2d−1at PP = 30 mmol C m−2d−1. These calculations provide confidence to the measured range in sedimentation rates with drifting traps (0.55-2 mmol C m−2d−1), which would represent a reasonable lower/upper scenario for passive sinking of POC in our region of study. Diel migrating zooplankton contributes also to the vertical flux of POC (the so-called ‘active flux’) by feeding in surface during the night and defecating unassimilated POC at depth during the day. Hernández-León et al. [2001] estimated an active flux of 0.22 mmol C m−2d−1in the eddy field downstream the Canaries, similar to the average value (0.17 mmol C m−2d−1) reported by Steinberg et al. [2000] for BATS. These fluxes represented 25% and 8% of the passive POC fluxes in their respective regions. If we assume that the active flux represents at best a 20% of the passive flux, the vertical POC flux (passive + active) in our box would range from 0.7 to 2.4 mmol C m−2d−1. Multiplying these values by the box area (6 x 1011 m2) yield a total POC supply of 4.2-14.4 x 108mol C d−1. The central waters (approximately 100-700 m; hereafter named mesopelagic zone) inside our box received a net lateral POC supply of 8.5 x 108mol C d−1 68 Chapter 3. Lateral POC transport and consumption (Table 3.1). If we assume that about 90% of the vertical POC flux is respired in the mesopelagic zone [Arístegui et al., 2005b], and adding the net lateral carbon supply we obtained a total mesopelagic POC reservoir (POCmeso) of 12.3-21.5 x 108mol C d−1. How this POC flux compares with the DOC flux? The relative contribution of dissolved organic carbon (DOC) to total mesopelagic respiration (R) was estimated by Arístegui et al. [2003], in a section spanning the coastal transition zone (CTZ) in the Canary Current. In their study, DOC contributed 30% to the total mesopelagic oxygen consumption, a value 2 times higher than the average (15%) calculated by Arístegui et al. [2002] for the global ocean. Unlike the eastern Canaries-CTZ our region of study was characterized by a stable surface thermocline, and was outside the influence of the eddy field region, which might enhance vertical mixing. Thus, we would expect to have a lower contribution of DOC to total mesopelagic R. In a best case scenario of a 30% contribution of DOC, the total carbon fluxes (lateral and vertical fluxes of DOC and POC) would support an integrated (100-700 m) mesopelagic respiration rate of 2.9-5.1 mmol C m−2d−1(computed by dividing POCmeso by both the box area and 0.7). If DOC contributed 15% (a more reasonable contribution) the total R would be 2.4-4.2 mmol C m−2d−1(POCmeso/box areax0.85). From these calculations we can infer that the lateral POC would account for 28-49% of total mesopelagic R in the 30% DOC scenario, and 34-59% in the 15% DOC scenario. Total R is about an order of magnitude lower than that estimated by Arístegui et al. [2005a] for the Canary Current region, during summer time, combining actual oxygen consumption measurements and enzymatic activities (ETS activity). The discrepancy in the magnitude of the rates may be explained by the fact that, during the summer sampling, the POCsusp concentrations were about 4-6 times higher in the water column than during this study (not shown) and that the summer rates were averaged including near coastal stations downward the Canary Islands region, where vertical POC flux is several times higher. 3.4. Discussion 69 Our calculated R estimates are also about half of the mesopelagic oxygen consumption rates (9 mmol C m−2d−1) reported by Jenkins and Goldman [1985] for the NASG, inferred from changes in the apparent oxygen utilization (AOU) and the use of tracers to calculate the apparent age of the water mass. A similar twofold imbalance was observed in BATS between the AOU/tracers approach when compared with estimations of POC and DOC 1-D fluxes in the mesopelagic zone [Carlson et al., 1994; Michaels et al., 1994]. Although there are known pitfalls in the accurate determination of carbon fluxes [e.g., Buesseler, 1998; Hansell, 2002; Arístegui et al., 2005b], we must not exclude the uncertainty associated with the inference of mesopelagic respiration from changes in the oxygen field, because of eddy diffusivity [Jenkins and Wallace, 1992]. The sources of the lateral mesopelagic carbon fluxes to our region of study may be variable. Upwelling filaments have been identified as playing a key role in coastal ocean export of organic matter [Álvarez-Salgado et al., 2001]. According to Barth et al. [2002], the exported organic matter from filaments may be forced downward along sloping density surface through conservation of potential vorticity along the meandering jet path. These authors found a mesopelagic chlorophyll maximum in the California Current System over 300 Km offshore and between 150 and 250 m, reporting a carbon injection into the adjacent deep ocean of 2.4 x 106Kg C per event. 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Fabiano (2002), The distribution and biochemical composition of biogenic particles across the subtropical Front 80 Chapter 3. Lateral POC transport and consumption in June 1993 (Azores-Madeira region, Northeast Atlantic), Sci. Mar., 66(3), 205-214. Vilas, J. C., J. Arístegui, K. Kiriakoulakis, G. A. Wolff, M. Espino, I. Polo, M. F. Montero, and A. Mendonça (2008), Seamounts and organic matteris there an effect? The case of Sedlo and Seine Seamounts; Part 1. Distributions of dissolved and particulate organic matter, Deep Sea Res., Part II, in press. Walsh, J. J. (1991), Importance of continental margins in the marine biogeochemical cycling of carbon and nitrogen, Nature, 350(6313), 53-55. Wollast, R., and L. Chou (2001), The carbon cycle at the ocean margin in the northern Gulf of Biscay, Deep Sea Res., Part II, 48(14-15), 3265-3293. Chapter 4 Spatio-temporal variability of water column respiration in the Canary Basin: the role of suspended particulate organic carbon Iván Alonso-González1, Javier Arístegui1, Juan Carlos Vilas1, María Fernanda Montero1, and Minerva Espino1 1Facultad de Ciencias del Mar, Universidad de Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, 35017, Spain Submitted to Journal of Marine Systems Abstract Here, we have studied the spatio-temporal variability in the epipelagic (0-200 m) and mesopelagic (200-1000 m) respiration through the enzymatic activity of the electron transport system (ETS) in microplankton. The study was conducted along two zonal sections (21◦N and 26◦N) extending from the northwest African costal upwelling to the open ocean waters of the North Atlantic subtropical gyre at 26◦W, during autumn (September 2002) and late spring (June 2003). 82 Chapter 4. Variability of water column respiration The EST activity in the epipelagic waters exhibited contrasting zonal patterns of distribution. At 21◦N, ETS was higher at the coastal stations associated with the Cape Blanc filament, decreasing towards the open ocean, while at 26◦N the open-ocean waters presented higher ETS than near the African shelf.When averaging the values from each section, the highest ETS activities were found along 21◦N, yielding to an important meridional variability. No significant temporal variability in the epepelagic ETS activity was observed. The ETS activity in the mesopelagic waters did not display clear patterns of either zonal or meridional distributions, except at 26◦N, where ETS activity was clearly lower at the most coastal stations. The mesopelagic waters showed however a significant temporal variability, being the ETS activity 30% higher in autumn (202±19.3 mmol O2m−2d−1) than in late spring (150±13.9 mmol O2m−2d−1). The average integrated ETS activity in the mesopelagic zone (176±10.1 mmol O2m−2d−1) was high with respect to other oceanic regions, and comparable in magnitude to the epipelagic ETS (189±40.8 mmol O2m−2d−1). Based on significant correlations between average POCsusp concentrations and ETS activities from surface to 1000 m and previous results, we conclude that plankton respiration was mainly (65-74%) supported by seasonal fluctuations in the laterally advected suspended organic matter, highlighting a low contribution of sinking POC (<20%) to the water column respiration. This finding could help to explain the apparent imbalance between the carbon sources and the oxygen utilization rates in the mesopelagic waters when accounting only for the vertical sinking POC collected with sediment traps. KEYWORDS: ETS activity; suspended organic carbon; ocean respiration; carbon imbalance; Canary Basin 83 Contents 4.1 Introduction ......................... 84 4.2 Data and Methods ...................... 85 4.2.1 Data sources ......................... 85 4.2.2 Respiratory Electron Transport System (ETS) activity . . 86 4.2.3 POM analysis ......................... 87 4.3 Results ............................. 87 4.3.1 Hydrographic structure ................... 87 4.3.2 Suspended particulate organic matter distribution . . . . 90 4.3.3 Spatial variability in respiratory activity .......... 91 4.3.4 Temporal and depth variability in respiratory activity . . 93 4.4 Discussion ........................... 96 4.4.1 Epipelagic respiration .................... 96 4.4.2 Mesopelagic respiration ................... 97 4.4.3 Contribution of POCsusp to water column respiration . . 99 4.5 Conclusions .......................... 101 4.6 References ........................... 103 84 Chapter 4. Variability of water column respiration 4.1 Introduction Primary production, respiration and the organic matter transport mechanisms are the main factors controlling the ocean carbon cycle. The classical view of the biological pump consider that the organic matter synthesized in the ocean is mostly respired within surface waters, being the non-oxidized matter transported vertically into the dark ocean. However, some studies have shown that lateral particulate organic carbon (POC) inputs from ocean margins to the ocean interior could be more than an order of magnitude greater than inputs of vertically transported organic carbon derived from the surface (Bauer and Druffel, 1998; Alonso-González et al. 2009). Supporting this idea, Barth et al. 2002, concluded that the off-shelf flux of carbon from coastal margins to the ocean interior must be considered when computing oceanic carbon budgets. These lateral inputs of organic matter would be particularly intense along eastern boundary currents, because of the high productivity of the nearby upwelling regions. Recent studies in the coastal transition zone of the Canary Current region indicates that upwelling filaments may transport offshore up to 50% of coastal upwelling primary production, accounting for 2.5 to 4.5 times the offshore carbon export driven by Ekman transport. Nevertheless, most of this surface-export carbon takes place in dissolved form (see review in Álvarez-Salgado et al., 2007). A more plausible mechanism of shelf-offshore carbon transport is through suspended particles along density gradients in the dark ocean (e.g. Vilas et al., 2009). Indeed, Alonso-González et al. 2009 estimated, through a box-model approach, that suspended POC in the mesopelagic zone of the Canary Current could account for up to 60% of the total mesopelagic respiration. They suggested that a large fraction of this POC could be originated in the nearby coastal upwelling region, being respired in the upper 1000 m of the Canary basin, instead of being transported to the ocean interior. To test the hypothesis of the correlation between suspended POC and respiration we have looked at regional gradients and temporal variability in water column respiration and suspended particulate organic material. 4.2. Data and Methods 85 Here, we report results from two cruises that took place in the Canary Current region in September 2002 (COCA I) and June 2003 (COCA II). We measured suspended particulate organic matter and the microbial respiratory activity at 10 stations placed along two sections expanding from the African coast to the open ocean. The aim of the work was to characterize and quantify the spatio-temporal variability of surface and mesopelagic respiration in the Canary region, and to show whether this variability responds to fluctuations in suspended organic matter supply, which presumably could be largely originated in the continental margin. 4.2 Data and Methods 4.2.1 Data sources The study was conducted along two zonal sections (21◦N and 26◦N) extending from the costal upwelling to the open ocean at 26◦W (Figure 4.1). The cruises consisted of a total of 31 hydrological stations and 10 biogeochemical stations, half of them along each section, which were roughly equidistant. At each station, conductivity, temperature and depth were determined by means of a 911+ CTD and fluorescence with a Seapoint sensor. Bottle casts were made down to 1000 m and seawater samples were collected at fixed depths every 50 m from surface to 1000 m for respiratory electron transport system (ETS) activity and suspended particulate organic carbon (POCsusp) analyses. As a control system, we used measurements of ETS and POCsusp at the European Station for Time Series in the Oceans, Canary Islands, (ESTOC), located 100 Km north of the Canary Islands. The ESTOC is not under the influence of the high mesoscale activity generated south of the Canary Islands. ETS measurements at ESTOC were carried out during 2002, while POCsusp data was obtained from Neuer et al. 2007. 92 Chapter 4. Variability of water column respiration cruises (Table 4.2). The highest ETS activities were found along the 21◦N section (39.3 ±5.3 µmol O2m−3h−1, average value of both cruises), coinciding with the Cape Blanc region, while much lower values were observed at 26◦N (22.9 ±14.5 µmol O2m−3h−1). The epipelagic integrated ETS activities also show this contrasting zonal pattern between sections (Table 4.3). At 21◦N, the integrated epipelagic ETS was higher on the coastal stations (10.34 mmol O2 m−2h−1), decreasing toward the open ocean, while at 26◦N the surface openocean waters presented higher integrated ETS than near the African shelf (8.31 and 1.93 mmol O2m−2h−1, respectively). ! Figure 4.5: Vertical distribution (0-1000 m) of respiratory electron transport system (ETS) activity (µmol O2m−3h−1) for each cruise and section. Dots represent depths sampled at each station. The ETS activity in the mesopelagic zone (200-1000 m) did not display a clear meridional trend, like in the epipelagic, except at coastal stations during June 2003 (Table 4.2). However, a significant zonal gradient with higher (p<0.05) ETS at the open ocean was clearly apparent at 26◦N (Table 4.2, Figure 4.5). Integrated ETS rates for the mesopelagic waters also showed im- 4.3. Results 93 portant zonal variations, with a minimum at the coastal stations (mean 7.21 and 6.25 mmol O2m−2h−1for 21◦and 26◦N, respectively) and a maximum at open ocean stations (mean 9.72 and 9.36 mmol O2m−2h−1) during September, following the same pattern during June (Table 4.3). Table 4.2: Mean volumetric values (±standard deviation) of plankton ETS activities in the epipelagic and mesopelagic waters during the two periods of study (September 2002 and June 2003). For "coastal", "oceanic" criteria see Table 4.1 caption. 4.3.4 Temporal and depth variability in respiratory activity The epipelagic ETS activity did not show a significant temporal variability (p>0.05), being the mean values, 40.41±5.5 and 38.2±7.5 µmol O2m−3h−1 for 21◦N and 22.4±21.0 and 23.5±17.5 µmol O2m−3h−1for 26◦N, during COCA I and II, respectively. However, there was an important difference in the mesopelagic ETS activity between the two periods. On average, the ETS activity in the mesopelagic waters was 9.8±1.8 µmol O2m−3h−1(202 mmol O2m−2d−1) during September while in June the mean ETS activity in the mesopelagic zone was a ∼30% lower (6.9±2.5 µmol O2m−3h−1; 150 mmol O2 m−2d−1). 94 Chapter 4. Variability of water column respiration Table 4.3: Integrated (epipelagic 0-200 m; mesopelagic 200-1000 m) values of plankton ETS activity from stations in the two sections during September 2002 and June 2003. For "coastal", "oceanic" criteria see Table 4.1 caption. The depth distribution of the average ETS activity and suspended organic carbon concentrations for each cruise, and the average of both cruises are shown in Figure 4.6. Average ETS activity shows high values in the epipelagic waters (33.47 and 31.19 µmol O2m−3h−1for COCA I and COCA II, respectively), but also large deep maximums (values exceeding 10 µmol O2 m−3h−1) between 200 and 400 m and between 700 and 800 m. Remarkably, the depth distribution of average POCsusp follow exactly the same pattern as the ETS activity independently of the season, suggesting that this pool of organic matter is the main substrate supporting ETS activity (Figures 4.6a and 4.6b). Figure 4.6c displays the depth distribution of the average (COCA I and II) ETS activity and POCsusp concentrations and compare it with the control station ESTOC. ETS activity within the epipelagic waters at ESTOC station showed similar ETS values than COCA cruises. However, mesopelagic waters presented a clear lower ETS activity, with little variation between depth levels. POC concentrations at ESTOC station were apparently constant and lower than 4 µM, although the sampling depths resolution is much lower than 4.3. Results 95 in our study (Neuer et al. 2007). Figure 4.6: Vertical distribution of average (both sections) ETS and POCsusp: (a) COCA I cruise (September 2002). (b) COCA II cruise (June 2003). (c) COCA I-COCA II average of POCsusp and ETS activity and ETS activity from the ESTOC station. (d) Regression lines for the relationship between ETS activity and POCsusp concentration during COCA I, COCA II and the COCA average cruises. Notice the deep peaks in POCsusp coinciding with the mesopelagic ETS maximums. The dashed lines stand for the interface between epipelagic and mesopelagic waters. Regression lines were calculated to describe the dependence of respiratory ETS activity on suspended POC concentration. Figure 4.6d shows the relationship between the average POCsusp concentrations and ETS activity from surface to 1000 m. We found that respiratory ETS activity was correlated 96 Chapter 4. Variability of water column respiration with POCsusp in both seasons (September and June). The correlation was stronger in September (R2= 0.74) than in June (R2= 0.65). Again, this strong correlation suggests that respiration was directly or indirectly based on suspended particulate organic carbon. 4.4 Discussion 4.4.1 Epipelagic respiration Respiratory ETS activity was in general high (> 0.7 mmol O2m−3d−1) in the whole epipelagic waters. Overall, the ETS values reported here are higher than those previously reported from open ocean waters of the north Atlantic (Arístegui and Harrison, 2002) and the Canary region (Arístegui et al., 2003). The high epipelagic ETS activities coincide also with high POC concentrations. Indeed, the mean values of POCsusp along the study sections (Table 4.1) were significantly higher than values observed in previous studies in this area (Arístegui et al., 2003; Alonso-González et al., 2009). POCsusp inputs to the epipelagic zone can be due to local primary production, lateral advection from the coast or atmospheric carbon inputs. Unfortunately, we do not have enough data to discriminate the contribution of these different inputs to the POCsusp pool in the epipelagic zone. Nevertheless, since a large metabolic deficit in the balance between plankton primary production and respiration has been routinely observed in this area (Duarte et al. 2001; Robinson et al. 2002), it seems reasonable to think that the high respiratory activity is fuelled by external organic matter inputs. The meridional variability in ETS activity in the epipelagic waters is related to differences in the POCsusp concentrations (Table 4.1). The presence of the giant filament off Cape Blanc seems to cause the high POC concentrations values and hence the increase in ETS near the coast. Several studies have reported the influence of NW African filaments on biogeochemical properties, metabolism and plankton community structure (Gabric et al., 1993; Head et al., 1996; Olli et al., 2001, Arístegui et al., 2004). However, the observed zonal 4.4. Discussion 97 variability at the 26◦N section cannot be explained only by the distribution of the suspended organic matter. As observed in Table 4.1, the highest ETS activity at 26◦N values are closely related to the lower C/N ratios of the suspended organic matter (dashed lines), suggesting that the total amount of POC is not the only factor controlling the magnitude of the ETS activity. Another factor affecting the ETS activity may be the temperature of the water. Temperatures during September 2002 were generally higher than 21 ◦C at open ocean stations, decreasing to 18 ◦C toward the African coast. Temperature-dependence studies have shown that ETS activity increase with temperature (Ramírez et al. 2006). Therefore, the high ETS activity reported for the surface waters of open ocean stations could be associated both with less refractory material (lower C/N ratios) and higher temperatures. 4.4.2 Mesopelagic respiration The mesopelagic waters are thought to be a zone of intense organic matter remineralization. Indeed, the major decrease in molecular-characterized material occurs in the mesopelagic zone, even though the larger relative decrease in flux is in the euphotic zone (Lee et al. 2004). The substantial decrease in the amount of organic matter that may be easily identified at the molecular level is indicative of a high bacterial and zooplankton activity. In spite of the key role of the mesopelagic waters as the site where the bulk of the exported matter from the epipelagic zone is remineralizated, to our knowledge there are no studies that tackle both the spatial and temporal respiration variability in the mesopelagic zone. In this work, we first provide a regional description of the mesopelagic respiratory variability, and then correlate it with the organic matter supply, its labiliy and the hydrological conditions. The mesopelagic waters did not present a clear meridional ETS variability. As can be observed in Table 4.1, there are no large mesopelagic differences in POCsusp concentrations between the two sections, like in the epipelagic zone. This opposite trend with respect to the epipelagic waters could be a consequence of the different organic matter sources between both depth 98 Chapter 4. Variability of water column respiration levels. The major source of POCsusp in the epipelagic waters is via primary production, which is highly variable with latitude and affected by mesoscale features. However, the potential sources of POCsusp to the mesopelagic waters are disaggregation of particles sinking from the epipelagic zone and lateral advection of suspended material at density gradients. Contrary to the epipelagic zone, the mesopelagic waters presented a marked zonal variability in ETS with the highest values in the open-ocean rather than near the coast. Surprisingly, POCsusp concentrations in the mesopelagic zone did not show important differences between coastal and oceanic stations. However, the C/N ratios in the mesopelagic waters were lower at open-ocean than coastal stations (Table 4.1). These results suggest that the source of the POCsusp at open ocean stations is not mainly related to the continental margin. Suspended particles at open ocean stations may result from sinking particles disaggregated by physical forces (Burd and Jackson, 2009) or by lateral transport of organic matter biosynthesized within the eddy-field generated upstream (south of the Canaries). According to this, a recent study focused on the organic matter composition indicated that the open ocean stations (approximately same stations) were more associated with chlorophyll-a and fresh cytoplasm components, while coastal station presented an strong heterotrophic signature (Alonso-González et al. 2010). Alternatively, the "freshness" of the POCsusp at open ocean stations may be related to the self-assembly of dissolved organic material yielding porous microgels (Chin et al. 1998), although we do not have any data supporting this hypothesis. In all cases these suspended particles seem to be a suitable nutrient-rich habitat to be colonized by microorganisms. Thus, the zonal variability in the mesopelagic ETS activity is found to be controlled by the degradation state of the suspended organic matter. On the other hand, the mesopelagic waters showed an important temporal variability, being the ETS 30% higher in autumn than in late spring. Since mesoscale activity is higher during autumn than spring (Pacheco and Hernández-Guerra, 1999), we hypothesize that the temporal variability in the mesopelagic respiration was mainly controlled by fluctuations in the suspended organic matter supply from mesoscale activity, rather than from vertical sinking of particles from the euphotic zone after the late-winter/spring 4.4. Discussion 99 bloom. Several evidences supported this hypothesis: (i) the lack of a clear depth gradient in ETS activity suggest that its substrate is not related to the sinking particles, (ii) deep peaks in ETS activity were observed through the mesopelagic zone associated to POCsusp peaks, (iii) low export fluxes recorded with drifting sediment traps during the same study (unpublished), and (iv) a control station (ESTOC station, north of the Canary Islands), not affected by mesoscale activity, showed a clear lower ETS activity in the mesopelagic zone. 4.4.3 Contribution of POCsusp to water column respiration The correlation between the particulate fraction of the organic matter pool and the ETS activity of planktonic communities could be expected a priori taking into account that the ETS activity represent also a living biomass (enzyme) measurement . However, total prokaryote abundances in the sampled mesopelagic waters represented only a small fraction of total POC. Prokaryote abundances ranged from 1 to 3 x 105cells ml−1(Gasol et al. 2009). Assuming an average (coastal and open ocean stations) carbon conversion factor of 20 fg cell−1(Fukuda et al. 1998) the maximum prokaryote abundance (3 x 105 cells ml−1) yields a prokaryotic carbon content of 0.5 µmol C L−1. This value represents less than 12% of total POCsusp and suggests that the correlation between ETS activity and POCsusp is not biomass dependent. The regression between ETS and POCsusp in the whole water column (0-1000 m) suggests that respiratory activity is mainly supported by suspended particulate organic carbon. The correlation analysis reveals that POCsusp supports between 65% and 74% of the respiration in the water column. These results are in agreement with a recent box-model study in the Canary Current region, which provides evidence that POCsusp may account up to 60% of the total mesopelagic oxygen consumption (Alonso-González et al. 2009). Assuming that dissolved organic carbon contributes only 10% to 25% to total respiration in the mesopelagic zone (Arístegui et al. 2002; Arístegui et al. 2003), the contribution of the sinking POC would be lower than 25%. These estimations would explain the metabolic imbalance observed between sources 100 Chapter 4. Variability of water column respiration and sinks in the dark waters of the North Atlantic when accounting only for the vertical sinking POC, collected with sediment traps (Reinthaler et al. 2006; Baltar et al. 2009; 2010). In order to calculate the total sinking POC flux necessary to support the "oceanic" ETS activity found in this study, we transformed the average integrated (200-1000 m) ETS respiratory activity to actual respiration rates (R) in carbon units. R was calculated using a respiratory quotient of 1 and a R:ETS conversion factor ranging from 0.2 to 0.6 (see Baltar et al. 2010 for discussion). The average integrated "oceanic" ETS activity during this study was 8.3 mmol O2m−2h−1(Table 4.3). Applying the above conversion factors yield an average mesopelagic respiration rate of 40 to 120 mmol C m−2 d−1. The measured sinking POC rates, which would represent a reasonable lower/upper scenario for passive sinking of POC in our oceanic stations range from 1 to 8 mmol C m−2d−1(Neuer et al. 2007; Alonso-González et al. 2010), which would account for 1 to 20% of R. On the other hand, another simple evidence that supports the idea that the suspended POC is the principal substrate for respiration is the presence of intermediate depth peaks (400 to 800 m) of POC associated with ETS peaks, suggesting hot-spots of POC remineralization which might be laterally transported. Some of these deep POC maximums coincide with the depth of the Deep Scattering Layer (DSL), probably due to the disaggregation of fresh daily fecal pellets onto suspended particulate matter because of zooplankton swimming activity. In a previous work, Arístegui et al. 2003 reported the presence of mesopelagic ETS peaks associated with the relative maxima of DOC at the DSL. Recently, Baltar et al. 2009, also found significant correlations between POM and ETS in the bathypelagic waters (1000 m to 3000 m) of the subtropical North Atlantic. These findings, together with our results, indicate that microbial metabolism in the mesopelagic waters is mainly fuelled by suspended POC. Why suspended particles show enhanced microbial activity vs. sinking particles? A possible explanation for the greater contribution of suspended matter to respiration is that these particles have longer residence times in 4.5. Conclusions 101 the water column compared with the faster sinking particles. Therefore, they would be relatively more "accessible" than the faster particles, and hence more efficiently colonized by heterotrophic organism. Supporting this idea, Goutx et al. (2007) concluded that the faster settling particles (with indicators of ‘fresh material’) contain less bioavailable organic matter, whereas slower settling particles (with "reworked material" indicators) were more bioavailable. Biomarker compositions of samples from the Pacific Ocean also showed that material collected by in situ filtration, assumed to be suspended or with low settling rates, presents a remarkable abundance of labile organic compounds (Wakeham et al. 1988; Lee et al. 2000). 4.5 Conclusions Epipelagic waters showed a clear meridional variability with highest ETS activities along the 21◦N section, while no temporal variability was observed. On the contrary, mesopelagic waters, mainly at 26◦N, presented an opposite zonal variability with higher ETS activities in open-ocean stations, coinciding with lower C/N ratios in the organic material. Temporal variability was also observed in the mesopelagic, being the ETS activity 30% higher in autumn than in late spring. The spatio-temporal variability in the mesopelagic waters was found to be related to the availability of suspended POC from mesoscale activity and its degradation state. The estimated integrated mesopelagic respiratory activities are comparable in magnitude to the epipelagic zone. This gives evidence of the importance of the dark waters of this coastal transition zone (CTZ) as a sink of carbon in the northeast Atlantic Ocean. Our results also indicate that R in this area is likely controlled by seasonal fluctuations in the lateral advection of suspended particulate organic carbon rather than by sinking particles from the euphotic zone. This finding could explain the apparent imbalance between the carbon sources and sinks in the mesopelagic waters when accounting only for the vertical sinking POC collected with sediment traps. This study underlines the fact that respiration changes in the deep ocean do not occur uniformly over time and space. Hence, the urgent need to expand our database on regional and large scales to gain a better Part III Sinking particulate organic carbon: role of mesoscale eddies Chapter 5 Regional and temporal variability of sinking organic matter in the subtropical northeast Atlantic Ocean: a biomarker diagnosis Iván Alonso-González1, Javier Arístegui1, Cindy Lee2and Antoni Calafat3 1Facultad de Ciencias del Mar, Universidad de Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, 35017, Spain 2School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY 11794-5000, USA 3GRC Geocincies Marines, Dep. de Estratigrafia i Paleontologia, Universitat de Barcelona, Barcelona, 08028, Spain Biogeosciences, 7, 2101-2115, 2010. Abstract Sinking particles through the pelagic ocean have been traditionally considered the most important vehicle by which the biological pump sequesters carbon in the ocean interior. Nevertheless, regional scale variability in particle flux is a major outstanding issue in oceanography. Here, we have studied the regional and temporal variability of total particulate organic matter fluxes, as well as 112 Chapter 5. Variability of sinking organic matter fluxes chloropigment and total hydrolyzed amino acid (THAA) compositions and fluxes in the Canary Current region, between 20-30◦N, during two contrasting periods: August 2006, characterized by warm and stratified waters, but also intense winds which enhanced eddy development south of the Canary Islands, and February 2007, characterized by colder waters, less stratification and higher productivity. We found that the eddy-field generated south of the Canary Islands enhanced by >2 times particulate organic carbon (POC) export with respect to stations (FF; far-field) outside the eddy-field influence. We also observed flux increases of one order of magnitude in chloropigment and 2 times in THAA in the eddy-field relative to FF stations. Principal Components Analysis (PCA) was performed to assess changes in particulate organic matter composition between stations. At eddy-field stations, higher chlorophyll enrichment reflected "fresher" material, while at FF stations a higher proportion of pheophytin indicated greater degradation due to microbes and microzooplankton. PCA also suggests that phytoplankton community structure, particularly the dominance of diatoms versus carbonate-rich plankton, is the major factor influencing the POC export within the eddy field. In February, POC export fluxes were the highest ever reported for this area, reaching values of ∼15 mmol C m−2d−1 at 200 m depth. Compositional changes in pigments and THAA indicate that the source of sinking particles varies zonally and meridionally and suggest that sinking particles were more degraded at near-coastal stations relative to open ocean stations. KEYWORDS: sinking organic matter, eddies, biomarkers 113 Contents 5.1 Introduction ......................... 114 5.2 Methods ............................ 116 5.2.1 Locating mesoscale eddies ..................116 5.2.2 Sample collection .......................116 5.2.3 POM analysis .........................117 5.2.4 Pigment analysis .......................118 5.2.5 Amino acid analysis .....................119 5.2.6 Statistical analyses (PCA) ..................120 5.3 Results ............................. 120 5.3.1 Oceanographic settings ...................120 5.3.2 Sinking POM fluxes .....................121 5.3.3 Pigment fluxes and composition ...............125 5.3.4 Total hydrolyzable amino acid (THAA) fluxes and composition ............................128 5.4 Discussion ........................... 130 5.4.1 Eddy-field influence on organic matter fluxes .......130 5.4.2 Cyclonic vs. anticyclonic eddies ...............135 5.4.3 Regional variability in organic matter composition and flux137 5.5 Conclusions .......................... 139 5.6 References ........................... 142 114 Chapter 5. Variability of sinking organic matter fluxes 5.1 Introduction Export of organic matter via particles settling out of the euphotic zone is one of the main mechanisms by which atmospheric CO2can be transported to the deep ocean. Organic matter production and its subsequent cycling by zooplankton and microbes are key processes in carbon export. Several studies suggest that mesoscale features may have a major impact on upper ocean biogeochemistry by enhancing biological activity (Falkowski et al., 1991; Sweeney, 2001; Bidigare et al., 2003; Benitez-Nelson et al., 2007; McGillicuddy et al., 2007). Recently, intense effort has been focused on complex multidisciplinary mesoscale programs, like E-Flux (North Pacific) and EDDIES (EDdy Dynamics, mixing, Export, and Species composition, North Atlantic) to address the role of mesoscale eddies in downward export flux. Surprisingly, both programs concluded that eddies did not enhance carbon flux, although they might increase the flux of biogenic silica (Benitez-Nelson and McGillicuddy, 2008). Moreover, these programs revealed our lack of knowledge about the complex mechanisms that control organic matter export from the euphotic zone within eddies. Most sediment trap studies have measured bulk properties of the fluxes, such as total carbon and nitrogen, while individual organic compounds have received much less attention. Although total carbon and nitrogen values are useful, knowledge of the specific compounds provides more precise information on lability, interaction with other elements, and mechanisms of degradation (Lee et al., 2000; Sheridan et al., 2002; Ingalls et al., 2006). Unfortunately, there are only a limited number of studies, mainly focused on pigment composition determined in suspended material, that have documented changes in the organic matter composition within mesoscale features (Jeffrey and Hallegraeff, 1980; Olaizola et al., 1993; Rodríguez et al., 2003). More recently, some studies have highlighted the important role of frontal structures on organic matter fluxes by using sediment trap biomarkers in the Alborán Sea (Sánchez-Vidal et al., 2004; Tolosa et al., 2004, 2005) and in the northeast Atlantic Ocean (Goutx et al., 2005). 5.1. Introduction 115 In this work we report, together with total POC/PON fluxes, mesoscale and regional trends in amino acid (THAA) and chloropigment compositions and fluxes obtained from free floating sediment trap deployments in the northeast Atlantic Ocean. Both THAA and chloropigments are useful indicators of decomposition, source and transport in the water column (e.g., Wakeham et al., 1997; Dauwe and Middelburg, 1998; Lee et al., 2000). Amino acids are structural components of proteins, making up a major fraction of characterized carbon in marine particulate matter (Lee et al., 2004). Since inorganic nitrogen can control the biological pump through its role as a limiting nutrient, the decomposition and remineralization of organic nitrogen as amino acids are of particular importance. Chloropigments are key indicators of organic matter diagenesis, since their origin stems from surface water communities. By following chlorophyll degradation as particles fall from the surface through the water column we can determine the ‘freshness’ of organic matter during its transport to deeper layers. Our study was conducted during two different periods of the year: (i) August 2006 (cruise RODA I), characterized by warm and stratified waters, but also intense winds which enhanced eddy development south of the islands, and (ii) February 2007 (cruise RODA II), characterized by colder waters and less stratification. RODA I was planned to evaluate the role of the Canary eddy field in the enhancement of organic matter fluxes. RODA II was designed to look at the spatial variability in the Canary Current region, between 20-30◦N, during the time of the year when primary production is highest (Arístegui et al., 2001; Hernández-León et al., 2007). We hypothesized (1) that organic matter fluxes would be more intense during the most productive season (February), increasing towards the upwelling region, and (2) that eddies south of the Canary Islands would induce changes in organic matter composition, as well as the enhancement of fluxes, compared with waters outside the eddy field. 116 Chapter 5. Variability of sinking organic matter fluxes 5.2 Methods 5.2.1 Locating mesoscale eddies Before the sediment traps were deployed, eddy features in the Canary Current region were identified by satellite sea-surface temperature (AVHRR) images. Once the approximate location was obtained, high-resolution expendable bathythermograph (XBT) transects were carried out to determine the thermal gradients of the mesoscale eddy field. Four eddies were selected for this study: two anticyclonic (AE1 and AE2) and one cyclonic, (CE1) during RODA I and one cyclonic (CE2) during RODA II (Figure 5.1, Table 5.1). Hydrographic sections across the selected eddies were performed to determine the exact location of the eddy core. Conductivity, temperature and depth were recorded with a SeaBird 911+CTD; temperature and pressure sensors were calibrated by the manufacturer just before the cruise. The fluorescence signal of in vivo chlorophyll a (chl-a) was measured with a Seapoint sensor. 5.2.2 Sample collection Sinking particles were collected from 150 m depth at three eddy and two far-field (FF; outside eddy-field influence) stations during RODA I and from 200 m depth at CE2 and 8 non-eddy stations (S1-S8) southwestward of the eddy field, during RODA II (Table 5.1, Figure 5.1). We used a free-drifting multi-trap array holding 8 cylinders (9 cm diameter: 50 cm length and 0.005 m2collection area), similar to the model described by Knauer et al. (1979). NaCl (∼45 g L−1; analytical reagent-grade) was added to increase the salinity inside the traps. No poisons were used to retard bacterial decomposition during the deployment. Upon recovery (24 h after deployment), samples were visually checked and all fluid from each cylinder filtered onto pre-combusted (450 ◦C, 12 h) 25 mm Whatman GF/F filters. Swimmers were rarely present, but if so were processed in the laboratory according to the procedure described by Heussner et al. (1990). Large swimming organisms were removed by wet sieving through a 1 mm nylon mesh, while organisms <1 mm were handpicked under a microscope with fine-tweezers. The filters were wrapped 5.2. Methods 117 −200 −1000 −2000 −3000 −4000 −5000 FF1 FF2 AE1 AE2 CE1 CE2 S1 S2 S3 S4 S5 S6 S7 S8 28oW 24oW 20oW 16oW 12oW 20oN 22oN 24oN 26oN 28oN 30oN Longitude Latitude Africa Canary Islands Figure 5.1: Map showing the location of the free-drifting sediment trap deployments carried out during August 2006 and February 2007. 4 far-field, ⊗anticyclonic eddy, cyclonic eddy and + S stations. in pre-combusted aluminum foil and frozen at -20 ◦C until processing. One filter (corresponding to the filtration of 1 or 2 cylinders) was analyzed for POC/PON and one for chloropigments and amino acids in all samples except for CE2. 5.2.3 POM analysis In the laboratory, filters for particulate organic carbon (POC) and nitrogen (PON) analysis were thawed and dried overnight at 60 ◦C, then placed overnight in a desiccator saturated with HCl fumes, dried again for 24 h in a second desiccator with silica gel and packed in ultra clean nickel sleeves. The carbon analyses were carried out on a Perkin-Elmer 2400 CHN elemental analyzer (UNESCO, 1994). The DOC adsorption onto GF/F filters 220 Chapter 9. Spanish summary/ Resumen en español 9.2. Objetivos de la tesis y organización 221 9.2 Objetivos de la tesis y organización El objetivo general de esta tesis fue profundizar en el conocimiento de la dinámica del carbono orgánico particulado (POC) en el Océano Atlántico Noreste Subtropical, así como determinar la importancia biogeoquímica de las dos fracciones que conforman el total del POC (el POC que no se hunde y el que se hunde). Para la consecusión de este objetivo general, numerosos objetivos específicos fueron abordados. Básicamente, tratamos de responder a las preguntas planteadas en la introducción general: - 1. Cuál es la variabilidad regional y temporal en la forma del espectro de velocidades de sedimentación de las partículas? - 2. ál es la contribución del carbono orgánico suspendido a la demanda de carbono en el océano profundo? Existe algún mecanismo capaz de suministrar suficiente POCsusp para satisfacer la demanda metabólica de carbono en las aguas mesopelágicas? - 3. Cuál es el grado de acoplamiento entre el POC suspendido y la respiración? - 4. Podemos dilucidar cuáles son los factores que controlan la exportación de carbono en los remolinos usando biomarcadores? 222 Chapter 9. Spanish summary/ Resumen en español - 5. Pueden los remolinos cambiar la composición de la materia orgánica exportada? - 6. Pueden los remolinos aumentar el secuestro de carbono hacia el océano profundo? ∗Para abordar la primera pregunta, desplegamos un fondeo en la región de la Corriente de Canarias durante un periodo de un año y medio. Este fondeo estaba compuesto de trampas de sedimento (IRSC) [Peterson et al., 2005] ancladas a 260 m de profundidada. Estas trampas poseen la capacidad de separar las partículas en clases discretas en función de su velocidad de sedimentación. Para conocer el papel biogeoquímico potencial de cada una de las fracciones de velocidad, llevamos a cabo análisis de flujos y composición de aminoácidos y cloropigmentos. (Capítulo 2) Este trabajo resultó en la siguiente publicación: -"El papel de las partículas de sedimentación lenta en el ciclo del carbono oceánico" publicado en Geophysical Research Letters (GRL). ∗Para intentar resolver el aparente desbalance de carbono en aguas 9.2. Objetivos de la tesis y organización 223 superficiales y mesopelágicas (preguntas 2 y 3), se presentan dos capítulos. En el primer estudio, para responder a la pregunta 2, estimamos el transporte y consumo horizontal, desde la superficie hasta 3000 m de profundidad, de carbono orgánico suspendido recogido con botellas oceanográficas. El análisis fue realizado usando una aproximacin de modelo de caja, con fronteras físicas que se extienden desde 20◦a 29◦10’N y 20◦35’ a 26◦W (1000 x 600 Km) en la región de la Corriente de Canarias. (Capítulo 3) ∗En el segundo estudio, para responder a la pregunta 3, la variabilidad espacio-temporal de la respiración del microplancton en aguas epipelágicas y mesopelágicas fue analizada a través de la actividad enzimática del sistema de transporte de electrones (ETS). este estudio fue llevado a cabo a lo largo de dos secciones zonales (21◦N y 26◦N) que se extendían desde el afloramiento costero del noroeste de África hasta las aguas de océano abierto del Atlántico noreste subtropical. (Capítulo 4) Estos trabajos resultaron en las siguientes publicaciones: -"Transporte lateral y consumo de POC en aguas superficiales y profundas de la región de la Corriente de Canarias: un estudio de modelo de caja" publicado en Global Biogechemical Cycles (GBC). 224 Chapter 9. Spanish summary/ Resumen en español -"Variabilidad espacio-temporal de la respiración de la columna de agua en la Cuenca Canaria: el papel del carbono orgánico suspendido" sometido a Journal of Marine Systems (JMS) ∗Para delucidar los factores que controlan la exportación de carbono en los remolinos reportamos, junto con los flujos de POC y PON, patrones regionales y mesoescalares de la composición y flujos de aminoácidos y cloropigmentos obtenidos a partir de trampas de sedimento a la deriva y fijas en el Océano Atlántico noreste. (Capítulo 5) Este trabajo resultó en la siguiente publicación: -"Variabilidad regional y temporal de los flujos de materia orgánica en el Océano Atlántico noreste subtropical: un diagnóstico por biomarcadores" publicado en Biogeosciences (BG). ∗Para abordar los objetivos específicos número 5 y 6, medimos flujos y composición de POC, aminoácidos y cloropigmentos en muestras recogidas en un fondeo anclado en el área de generación de los remolinos ciclónicos que se generan al sur de Las Islas Canarias durante un periodo de 1.5 años. Los efectos de la presencia de los remolinos fueron investigados desde la superficie hasta los 1000 m. 9.3. METODOLOGÍA 225 (Capítulo 6) Este trabajo resultó en la siguiente publicación: -"Secuestro de carbono incrementado por los remolinos mesoescalares en el Océano Atlántico noreste" sometido a Proceedings of the National Academy of Sciences, (PNAS). 9.3 METODOLOGÍA Cálculo del flujo exportado de materia orgánica particulada (POM): se estima a partir del material recolectado en trampas de sedimento flotantes. Se desplegaron dos trampas situadas a 100 y 200 m de profundidad. Estas trampas se dejan a la deriva durante 14-15 horas en las diferentes estaciones de 16 h. El material recolectado en las trampas, situadas justo por debajo de la zona eufótica, representa (teóricamente) la producción exportada particulada. La MOP se concentró en filtros de fibra de vidrio mediante filtración, y se congelaron hasta su análisis. Se analiza la composición de C y N en los filtros mediante combustión a alta temperatura en un analizador elemental (CHN, Perkin Elmer). Cálculo del balance metabólico (P/R): se cuantificó el balance 226 Chapter 9. Spanish summary/ Resumen en español metabólico (producción bruta vs. respiración comunitaria) en aguas superficiales (0-90 m) de las siguientes estaciones: R2, T1, T2, T5, T6, T9, T11, T14, T15, T18 y T21. Para ello se desarrolla un sistema de incubación de muestras en la oscuridad y en la luz que reproduce las condiciones ambientales. De esta manera se eliminan posibles errores de irradiancia y temperatura de incubación. El procedimiento de muestreo fue el siguiente: en el CTD de recogida del agua para las incubaciones se determinaban las temperaturas de las cinco profundidades (5, 15, 30, 60, y 90 m) y se ajustaban los baños termostáticos a las mismas. Se llenaban todas las botellas de incubación (iniciales, claras y oscuras) con el agua de sus respectivas profundidades, previamente homogeneizada. Posteriormente las claras eran ubicadas en su respectivo sistema de incubación, las oscuras en los baños termostáticos correspondientes y las iniciales fijadas para la determinación del oxígeno inicial. Transcurridas 24 horas se fijaban las claras y las oscuras y el oxígeno se determinaba por valoraciones Winkler, con un sistema automatizado de gran precisión con punto final colorimétrico (microwinkler) (Arístegui Harrison 2002). Distribución y concentración de materia orgánica particulada (POM): se realizaron perfiles para obtener la distribución y las concentraciones de materia orgánica particulada (POC y PON). En estos perfiles se recolectaron muestras cada 50 m, desde la 9.3. METODOLOGÍA 227 superficie hasta 1000 m de profundidad. Dichas muestras (entre 3 y 4 litros de agua) se concentraron en filtros de fibra de vidrio GF/F y se congelaron a -80◦C hasta que sean analizadas en el laboratorio de la Facultad de Ciencias del Mar. En cada estación, y a diferentes profundidades, se ponía un doble filtro GF/F baja el primero, para medir la adsorción de carbono orgánico disuelto (DOC) y restárselo al valor total del POC. Se ha visto que el carbono debido a la adsorcin de DOC por el filtro puede llegar a ser >1uM. Por otro lado, las concentraciones de materia orgánica particulada, estiamadas a partir de muestras recogidas con botellas oceanográficas, se compararán con concentraciones obtenidas a partir de muestras recogidas con bombas de filtracin in situ (SAPs). Cuantificación de la respiración del microplancton (R) en la columna de agua: se estima a partir de la actividad enzimática respiratoria del sistema de transferencia de electrones (actividad ETS; Packard, 1985). Se utilizan índices R/ETS calculados durante esta campaña para transformar la respiración potencial (ETS) en respiración real (R). Con el fin de obtener perfiles verticales con la resolución necesaria para ver la contribución de las comunidades mesopelágicas a la respiración se recolectaron muestras cada 50 m, desde la superficie hasta 1000 m de profundidad. Las muestras (entre 4 y 5 litros de agua) se concentran en filtros de fibra de vidrio y se congelan en nitrógeno líquido hasta que 228 Chapter 9. Spanish summary/ Resumen en español sean analizadas en el laboratorio de la Facultad de Ciencias del Mar. Clorofila a, feofitina a, feofórbido a, y pirofeofórbido a fueron determinados mediante Cromatografía Líquida de Alta Resolución en fase inversa (HPLC) [Lee et al., 2000; Wakeham et al., 2009]. Los aminoácidos fueron medidos por HPLC en los mismos filtros analizados para pigmentos, usando una precolumna y derivatización con o?pthaldialdehyde (OPA) después de la hidrólisis [Lee et al., 2000; Wakeham et al., 2009]. Los Análisis Principales de Componentes son comúnmente utilizados en el análisis de complejas bases de datos orgánicas [Goñi et al., 2000; Ingalls et al., 2006; Goutx et al., 2007]. Es un análisis de regresión multivariante que reduce un largo número de variables a unos pocos componentes. El PCA fue usado en esta tesis para calcular cuantitativamente variaciones en la composición de las partículas que se hunden. El PCA fue aplicado a los datos de composición de pigmentos y amioácidos. Antes de realizar el PCA, los datos de abundancia en mol% de cada muestra son estandarizadas restando la media de todos los valores y dividiendo por la desviación estándar de todos los valores [Dauwe and Middelburg, 1998; Dauwe et al., 1999; Sheridan et al., 2002]. El primer componente principal del PCA es el eje de máxima variación del conjunto de datos, mientras que el segundo es equivalente a el eje de máxima variación residual. 9.3. METODOLOGÍA 229 Todos los PCA fueron realizados en Sirius en Windows (versión 7.0). 236 Chapter 9. Spanish summary/ Resumen en español remolinos ciclónicos y anticiclónicos, de una manera similar a las calles de von Karman y los cuales representan la mayor fuente de variabilidad mesoescalar al sur del archipiélago [ver Sangrá et al. 2005]. Estas estructuras, acomodan un diverso conjunto de interacciones físicas, químicas, y biológicas las cuales influencian la biogeoquímica marina en un amplio rango de escalas temporales [Benítez-Nelson and McGillicuddy, 2008]. Aumento de la producción primaria, inducida por un bombeo de nutrientes en la zona fótica por parte de los remolinos ciclónicos ha sido reportado [Arístegui et al. 1997; Oschlies and Garçon, 1998]. Sin embargo, los cambios asociados a la presencia de los remolinos en en la estructura del plankton, interacciones tróficas, impacto sobre la exportación de materia orgánica e importancia biogeoquímica en esta área son escasamente conocidos. El objetivo principal de los capítulos 5 y 6 fue completar el hueco en nuestro conocimiento acerca de la importancia de los remolinos en la dinámica del carbono. Para abarcar este objetivo medimos, junto con los flujos totales de POC, patrones mesoescalares en la composición y flujos de aminoácidos (THAA) y cloropigmentos obtenidos por fondeos de trampas de sedimentos a la deriva y fijas en el Océano Atlántico Noreste. Ambos, THAA y cloropigmentos son prácticos indicadores de descomposición, fuentes y transporte en la columna de agua [e.g., Wakeham et al., 1997; 9.4. RESULTADOS Y DISCUSIÓN GENERAL 237 Dauwe and Middelburg, 1998; Lee et al., 2000]. Como el nitrógeno inorgánico puede controlar la bomba biológica a través de su papel de nutriente limitante, la descomposición y remineralización del nitrógeno orgánico a aminoácidos son de particular importancia. Los cloropigmentos son indicadores clave de la diagénesis de la materia orgánica, puesto que su origen está en las comunidades de aguas superficiales. Entonces, siguiendo la degradación de la clorofila a medida que las partículas caen desde la superficie a través de la columna de agua podemos determinar la "frescura" de la meria orgánica durante su transporte hacia capas más profundas. Bajo condiciones de estado estacionario, el aumento en los flujos de nutrientes inducidos por los remolinos tiene que ser compensado por una estimulación de la tasa de crecimiento del fitoplancton marino, y como consecuencia, un aumento de la exportación de POC desde la zona fótica para balancear el aporte de nutrientes entrante. Sin embargo, este balance entre inyección de nutrientes, producción y exportación no siempre es alcanzado, debido a que la respuesta de la comunidad a la entrada de nutrientes es compleja [Buesseler et al. 2008]. De hecho, dos programas mesoescalares recientes (E-Flux, Pacífico Norte y EDDIES, Atlántico Norte), centrados en el papel de los remolinos mesoescalares en el flujo exportado de materia, concluyeron que los remolinos no aumentan el flujo de carbono, aunque si incrementaron el flujo de sílice biogénica [Benitez-Nelson 238 Chapter 9. Spanish summary/ Resumen en español and McGillicuddy, 2008]. Estos resultados plantean un cuestión de primer orden: Cuáles son los factores que controlan la exportación de carbono en los remolinos? En base a los análisis de biomarcadores (capítulos 5 y 6), nosotros sugerimos que la estructura de la comunidad del fitoplancton, particularmente el predominio de organismos de carbonato cálcico sobre diatomeas, un "lastrado" eficiente y una consecuente menor actividad de pastaje por parte del zooplancton son los mayores factores que influencian la exportación de materia orgánica en los remolinos. Numerosos trabajos han indicado que un fracción importante de la materia orgánica producida en aguas superficiales es transportada a profundidad asociada con minerales de "lastre" [Armstrong et al. 2002; Francois et al. 2002], especialmente con los carbonatos [Klaas and Archer, 2002]. Por tanto, el aumento del flujo de POC observado en los remolinos generados al sur de Las Islas Canarias puede ser debido a un aumento de la velocidad de sedimentación de las partículas en un sistema altamente lastrado por carbonatos en comparación con esos sistemas lastrados por ópalo (como Hawaii). Además, nuestro capítulo 6 y un estudio previo [Ingalls et al. 2006] sugieren que, en áreas ricas en diatomeas, la presión de pastaje por parte del zooplancton es mayor que en áreas ricas en organismos de CaCO3, teniendo estas últimas una mayor exportación de agregados en lugar de empaquetados fecales. 9.4. RESULTADOS Y DISCUSIÓN GENERAL 239 Entonces, nuestros resultados son consistentes con la hipótesis propuesta por los programas mencionados anteriormente de el pastaje del zooplancton como un mecanismo para reducir la exportación de POC en los remolinos. En los remolinos enriquecidos en ópalo, se encontr que la biomasa producida es procesada por el microzooplancton, los cuales a su vez son predados por ciliados grandes y dinoflagelados liberando materia orgánica suspendida y disuelta en lugar de producir empaquetados fecales [Landry et al. 2008; Maiti et al 2008]. Nuestros resultados (capítulo 6) también sugieren que una importante fracción del carbono generado durante los periodos de mezcla y enriquecidos en ópalo (como nuestro bloom estacional o los remolinos de Hawaii) es mediada por el zooplancton migrador vertical. Estos organismos se alimentan en superficie y zona mesopelágica superior y defecan por debajo de 500 m, por ello podrían potencialmente contribuir de manera significativa a el flujo vertical de carbono por debajo de la zona mesopelágica [Hernández-León et al. 2010]. Sin embargo, nuestros resultados muestran que la eficiencia de transferencia de POC entre 290 y 1000 m durante estos periodos fue sólo del 8%, mientras que fue del 27 al 73% asociada a los remolinos durante el periodo de estratificación. Por tanto, nosotros sugerimos que un transporte activo importante por parte de los migradores verticales facilita el 240 Chapter 9. Spanish summary/ Resumen en español reciclado del carbono orgánico particulado en la zona mesopelágica, por lo que resulta en un debilitamiento de la bomba biológica. Por el contrario, los resultados presentados arriba indican que los remolinos ciclónicos en esta área son más efectivos transportando POC al océano profundo que las aguas ambientales (incluyendo el bloom estacional), poniendo de manifiesto el importante papel que tienen estas estructuras en la biogeoquímica regional. No obstante, el aparente desbalance metabólico en las aguas mesopelágicas no puede ser satisfecho por aportes verticales de POC que se hunde derivados de los remolinos, reforzando la visión actual de que la vida microbiana en el océano profundo es más dependiente de las partículas de sedimentación lenta y suspendidas que del POC que se hunde (capítulos 2, 3 y 4). 9.4.3 Modelo conceptual de flujos y descomposición de POC en la Cuenca Canaria Un foco principal de las ciencias marinas durante las 3 últimas décadas ha sido la identificación de los factores que controlan la exportación de las partículas biogénicas hacia el océano profundo, la conocida "bomba biológica" [Boyd and Trull, 2007]. La mayor parte de nuestro conocimiento actual de los procesos biogeoquímicos oceánicos que afectan a la materia particulada es derivado de datos de trampas de sedimento [Buesseler et al. 2000], sin embargo, 9.4. RESULTADOS Y DISCUSIÓN GENERAL 241 numerosos aspectos sin resolver acerca de la efectividad de las trampas de sedimentos prevalecen hoy en dia [ver Gardner, 2000]. Se piensa que las trampas de sedimento submuestrean las partículas de sedimentación lenta, las cuales pueden sufrir advección lateral durante largas distancias (capítulo 3) así como resuspensión en el interior de las trampas de sedimento [Gust and Kozerski, 2000]. Como consecuencia, la construcción de los ciclos biogeoquímicos globales, balances de carbono oceánicos, interacciones tróficas, y mecanismos de transporte han sido ampliamente guiados por la simplificación introducida por las trampas de sedimento, las cuales dan una visión en una dimensión del "panorama" total.Esta tesis, además de los flujos verticales de POC, trata de proveer información acerca del transporte lateral de POC a través de aproximaciones de balances de masa y biomarcadores orgánicos. Figura 9.3 ilustra el modelo conceptual de flujo de POC propuesto para la Cuenca Canaria después de esta tesis de investigación. Este modelo está básicamente dividido en dos escenarios de acuerdo a la estacionalidad, condiciones hidrográficas y estructura de la comunidad del plancton. El panel de la izquierda muestra las condiciones de verano-otoño, dónde la columna de agua está estratificada, dominan los organismos fitoplanctónicos de carbonato cálcico y los remolinos ciclónicos son más intensos. Por el contrario, el panel de la derecha muestra las condiciones de invierno-primavera, dónde 242 Chapter 9. Spanish summary/ Resumen en español las aguas superficiales están mezcladas y ocurre un eriquecimiento relativo de diatomeas. Estas dos situaciones diferentes fuerzan a la dinámica del POC a una dependencia temporal que no había sido préviamente establecida. Condiciones de Verano-Otoño Durante este periodo de tiempo la ruta del flujo de POC es principalmente via partículas de sedimentación lenta y suspendidas las cuales sufren transporte lateral (capítulo 3). Esta situación da lugar a una ditribución de POC en capas con máximos localizados en las interfaces de las masas de agua y microgradientes de densidad debido a la acumulación de este pool orgánico con características de flotabilidad casi neutra. Adicionalmente, esta distribución en capas es alimentada por carbono suspendido lateralmente exportado desde margen continental del Noroeste de África. De acuerdo con esta distribución, estas partículas tienen tiempos de residencia mayores en la columna de agua en comparación con las partículas de sedimentación rápida. Por tanto, es razonable pensar que la respiración pueda igualar o superar las tasas de producción primaria como ha sido frecuentemente reportado para esta área [Duarte et al. 2001; González et al. 2001; Marañón et al. 2007]. Sin embargo, la exepción a esta distribución se encuentra en los remolinos, donde la mezcla vertical es más pronunciada y el flujo de POC es más vertical y eficiente. Teniendo los remolinos en cuenta, nuestros 9.4. RESULTADOS Y DISCUSIÓN GENERAL 243 resultados muestran un flujo importante de POC a 1000 m de profundidad durante este periodo (Figura 6.1), indicando que, si el sistema es evaluado como un todo, el balance entre la producción y la respiración tiene que ser positivo. Estos descubrimientos también sugieren que un déficit de carbono durante en verano-otoño debiera existir en ausencia de remolinos, resaltando el importante papel de estas estructuras. La estructura de la comunidad del fitoplancton en los remolinos está principalmente dominada por organismos de carbonato cálcico, resultando en una baja presión de pastaje por parte del zooplancton y también en un bajo transporte activo por el mesozooplancton migrador. Condiciones de Invierno-Primavera Durante el periodo de invierno-primavera la estructura trófica y rutas del POC biogénico están determinadas por el grado de mezcla vertical de las aguas superficiales. Nuestros resultados sugieren un enriquecimiento superficial en silice debido a la mezcla invernal (ver capa de mezcla más profunda, MLD; Figura 6.1a), aumento relativo de diatomeas y consiguiente incremento en la exportación de POC en la base de la capa fótica. Estas condiciones son favorables para la producción de partículas de mayor tamaño y con mayores tasas de sedimentación (como fue reportado en el capítulo 2), por ello uno esperaría que estas partículas pudieran potencialmente 244 Chapter 9. Spanish summary/ Resumen en español contribuir al flujo vertical por debajo de la zona mesopelágica. Sin embargo, en comparación con el periodo de verano-otoño, encontramos una baja eficiencia de transferencia de POC entre 290 y 1000 m, lo que sugiere que el POC biosintetizado durante el bloom tardío de invierno tiene otro destino que la exportación en forma de partículas. En base a los flujos de POC y biomarcadores, concluimos que el POC que se hunde es rápidamente procesado por la comunidad microbiana, baipaseada a la capa de reflecxión profunda (DSL) por los organismos migradores y transformada en POC que no se hunde, lo que está de acuerdo con la baja eficiencia de transferencia de POC registrada a 1000 m. Esto también puede explicar la paradoja de que la materia orgánica en estaciones ricas en diatomeas es eliminada por mecanismos que no resultan en la aparicón de marcadores de degradación en la materia que se hunde [Ingalls et al. 2006]. En conjunto, estos descubrimientos indican que que el destino del material generado durante el bloom estacional es ser reciclado en la zona mesopelágica en lugar de ser transportado hacia el océano profundo. Entonces, la importancia de los migradores verticales diários en este área está más ligada al suministro de carbono orgánico para la respiración mesopelágica, que al secuestro de carbono hacia el océano profundo. En términos de la asociación de la materia orgánica que se hunde con los minerales "lastre" (carbonato cálcico y ópalo) nuestros datos coinciden con Armstrong et al. [2002] y Klaas and Archer [2002] en que los flujos de carbono orgánico que se hunde se 9.4. RESULTADOS Y DISCUSIÓN GENERAL 245 correlacionan más con el carbonato cálcico que con el ópalo. Ellos argumentan que la mayoría del flujo de carbono orgánico hacia el océano profundo es llevado a cabo por el carbonato cálcico, debido a que es más denso que el ópalo y más abundante que el material terrígeno. Nosotros sugerimos también que la materia orgánica asociada con ópalo es más biodisponible que la materia orgánica asociada al carbonato cálcico. Una posible explicación para esto es que aproximadamente el 50% del ópalo se disuelve en los primeros 100 m de la columna de agua, mientras que para el carbonato cálcico este porcentaje es mucho menor [Tréguer et al. 1995]. Como consecuencia, la exportación neta de carbonato cálcico y materia orgánica asociada desde la superficie del océano es mayor que los flujos correspondientes de materia orgánica asociada con ópalo. 252 Chapter 9. Spanish summary/ Resumen en español 9.5 CONCLUSIONES "Es débil porque no ha dudado bastante y ha querido llegar a conclusiones" Miguel de Unamuno, 1864-1936 Las principales conclusiones que surgen de esta tesis son: (a) La forma del espectro de velocidades de sedimentación de las partículas en nuestra región esta dominada por las partículas de sedimentación lenta (0.7-11 m d−1) durante el verano y el otoño y por partículas de sedimentación rápida durante invierno y primavera. Esta descubrimiento tiene profundas implicaciones para la dinámica del carbono: i. Durante el verano y el otoño, las trampas de sedimento pueden perder una fracción del POC exportado en las partículas de sedimentación lenta. Entonces, si los flujos verticales de carbono derivados de trampas de sedimento son usados para construir balances para diferentes procesos biogeoquímicos, fuertes desbalances pueden surgir. ii. Cuando las partículas de sedimentación lenta dominan el pool de carbono exportable, la mayoría de la materia 9.5. CONCLUSIONES 253 orgánica sería respirada en la zona epipelágica y mesopelágica superior, actuando como una fuente biológica de CO2 susceptible de ser intercambiada con la atmósfera. Por el contrario, si las partículas de sedimentación rápida contribuyen mayoritariamente al flujo de carbono, la eficiencia de transferencia de carbono a la zona mesopelágica incrementa, resultando en un aumento del secuestro de carbono hacia el océano profundo. (b) Una fracción significativa del balance de carbono mesopelágico en la región oeste de la Corriente de Canarias es alimentada por advección lateral de carbono suspendido desde el márgen continental o de la actividad a mesoescla en la región de frontera este. Sin embargo, una gran parte de este carbono mesopelágico podría ser remineralizado en los primeros 1000 m en lugar de ser transportado hacia océano abierto. i. Los flujos laterales de POC son 2 o 3 órdenes de magnitud superiores a los flujos verticales dependiendo de las masas de agua, confirmando la hipótesis de que el flujo horizontal de materia orgánica particulada es más relevante por unidad de área que el vertical. ii. La influencia del carbono orgánico particulado advectado horizontalmente desde la costa Noroeste de África hacia la región del giro subtropical puede llegar a más de 1000 Km de distancia. 254 Chapter 9. Spanish summary/ Resumen en español iii. Este flujo lateral de POC soporta entre un 28 y un 59% de la respiración total mesopelágica, en base a una baja o alta contribución de los flujos verticales de POC y del carbono orgánico disuelto a la repiración. (c) La respiración del plancton es principalmente (65-74%) soportada por las fluctuaciones de la materia orgánica suspendida advectada lateralmente, resaltando una baja contribución del POC que se hunde (<20%) a la respiración de la columna de agua. Este conclusión podría ayudar a explicar el aparente desbalance entre las fuentes de carbono y las tasas de utilización de oxígenoen las aguas mesopelágicas cuando sólo se tienen en cuenta los flujos verticales de POC que se hunde recogido con trampas de sedimento. (d) El campo de remolinos generados al sur de Las Islas Canarias aumenta entre 2 y 4 veces el flujo de POC con respecto a las aguas ambientales. Incrementos de entre 2 y 10 veces en los flujos de cloropigmentos y aminoácidos son observados en el campo de remolinos con respecto a condiciones de no remolino. (e) La estructura de la comunidad del fitoplancton, particularmente, el predominio de organismos enriquecidos en CaCO3sobre diatomeas, el "lastrado" más eficiente por parte del CaCO3, y por tanto la menor presión por parte del zooplancton son sugeridos como los mayores factores de control sobre la exportación de materia orgánica en los remolinos. 9.5. CONCLUSIONES 255 (f) Los análisis de biomarcadores orgánicos revela que la materia orgánica exportada durante condiciones de remolino tiene un estado de degradación menor con respecto a las condiciones de no remolino. (g) Durante el bloom de fitoplancton tardío de invierno, un cambio importante en la dinámica del POC que se hunde, presumiblemente mediado por el zooplancton migrador vertical resulta en una menor eficiencia de transferencia de POC hacia el océano profundo (>1000 m), respecto a el efecto debido a los remolinos ciclónicos. (h) El material transferido durante el bloom tardío de invierno es principalmente reciclado en la zona mesopelágica, mientras que los remolinos ciclónicos durante el periodo de estratificación aumentan el secuestro de carbono, resaltando así la importancia de estas estructuras en la biogeoquímica de la columna de agua a nivel regional. (i) El aparente desbalance metabólico en las aguas mesopelágicas no puede ser satisfecho por aportes verticales de POC que se hunde derivados de los remolinos, reforzando la visión actual de que la vida microbiana en el océano profundo es más dependiente de las partículas de sedimentación lenta y suspendidas que del POC que se hunde. 256 Chapter 9. Spanish summary/ Resumen en español Figure 9.1: Modelo conceptual dependiente de la velocidad de la dinámica de las partículas. (a) En un sistema donde las partículas de sedimentación rápida dominan, la remineralización epipelágica y mesopelágica del POC que se hunde debe ser mínima; (b) En un sistema donde las partículas de sedimentación lenta dominan, una importante fración del POC sufrirá advección lateral y puede escapar de las trampas de sedimentos, dando lugar a un desacoplamiento entre el flujo de POC y la demanda de POC procariota. Flechas contínuas negras = velocidad de las partículas. Flechas discontínuas negras = trajectorias del carbono. Líneas contínuas grises ilustran la distancia horizontal teórica alcanzada por las partículas de sedimentación lenta durante dos periodos diferentes de tiempo (10 y 100 dias). Las distancias fueron estimadas usando una velocidad zonal de la corriente de 10 cm s−1y5cms−1 para las zonas epipelágica y mesopelágicas, respectivamente. Los círculos representan partículas con el mismo "punto de partida" (Z = 0 m) pero con diferentes características dinámicas. Después de 10 dias, la mayor parte del POC permanece en la zona fótica (∼50 m) en (b), pero alcanza 3000 m en (a). Las líneas discontínuas grisesindican la cantidad de POC potencialmente recolectable por las trampas de sedimento (asumiendo la misma PP) en cada escenario. 9.5. CONCLUSIONES 257 Figure 9.2: Modelo conceptual de la contribución de las diferentes fuentes de carbono orgánico a la respiración mesopelágica. Los paneles de abajo ilustran las diferentes fuentes de carbono en función del tamaño de partícula, mientras que los paneles superiores muestran el mecanismo de transporte dominante de cada una de ellas. 258 Chapter 9. Spanish summary/ Resumen en español Bathypelagic zone Mesopelagic zone Epipelagic zone A) Carbonated stratificated and eddy periods B) Opal enriched mixed period (Seasonal bloom) CO2 CO2 Low POC Teff High POC Teff x 2-4 CO2 CO2 CO2 CO2 * CO2 CO2 Atmosphere POCsink POCsink POCsink R R R DSL POCsusp POCsusp POCsusp POCsink POCsink R DOC POCsusp Zoopl. POCsusp PP PP R x 2-4 Alonso-González, 2010 DSL Eddy PP Figure 9.3: Modelo conceptual de la evolución temporal del flujo y descomposición de POC para la Cuenca Canaria. El modelo comprende cuatro capas básicas: atmósfera, zona epipelágica, zona mesopelágica y zona batipelágica. Los flujos de carbono orgánico (POC) son ilustrados por líneas contínuas negras, mientras que los flujos de carbono inorgánico (CO2) son mostrados por líneas discontínuas negras. Las líneas negras a puntos representan el intercambio entre el POC que se hunde y el suspendido. Durante verano-otoño (panel A)) el POC presenta una distribucón en capas, excepto en los remolinos, dónde la mezcla vertical es más pronunciada. La entrada externa de carbono suspendido es representada por tres flechas negras contínuas localizadas en la izquierda. *CO2representa una entrada neta de CO2desde la atmósfera a el océano inducida por la presencia de los remolinos ciclónicos. La línea negra vertical discontínua indica un bajo baipas de POC por parte del zooplancton. Durante invierno-primavera (panel B)) el POC presenta una distribución parcheada con la mayor parte de las partículas viajando verticalmente. El mesozooplancton migrador realiza un baipas de una importante fracción del POC epipelágico liberándolo como materia orgánica disuelta o suspendida cerca del fondo de la zona mesopelágica. Esto resulta en una menor eficiencia de transferencia de POC (Teff ) hacia la zona batipelágica comparado con el panel A).