sign in sign up
<<
Home , Atlantic Ocean, Sargasso Sea

Oceanography of the Sargasso : Overview of Scientific Studies M.W. Lomas, N.R. Bates, K.N. Buck, and A.H. Knap

Number 5 Alliance Science Report Series When referenced this report should be referred to as: Lomas, M.W., Bates, N.R., Buck, K.N. and A.H. Knap. (eds) 2011a. of the Sargasso Sea: Overview of Scientific Studies. Sargasso Sea Alliance Science Report Series, No 5, 64 pp. ISBN 978-0-9847520-7-2 The Sargasso Sea Alliance is led by the Government and aims to promote international awareness of the importance of the Sargasso Sea and to mobilise support from a wide variety of national and international organisations, governments, donors and users for protection measures for the Sargasso Sea.

Further details: Dr David Freestone, Executive Director, Sargasso Sea Alliance, Suite 300, 1630 Connecticut Avenue NW, Washington D.C., 20009, USA. Email: [email protected] Kate K. Morrison, Deputy Director, at the same address Email: [email protected] The Secretariat of the Sargasso Sea Alliance is hosted by the Washington D.C. Office of the International Union for the Conservation of (IUCN). Website is www.sargassoalliance.org This case is being produced with generous support of donors to the Sargasso Sea Alliance: Ricardo Cisneros, Erik H. Gordon, JM Kaplan Fund, Richard Rockefeller, David E. Shaw, and the Waitt Foundation. Additional support provided by: WWF and the Pew Environment Group.

Cover photo: Taking water samples at Hydrostation S., Tiffany Wardman. ISBN 978-0-9847520-7-2 Oceanography of the Sargasso Sea: Overview of Scientific Studies

M.W. Lomas, N.R. Bates, K.N. Buck, and A.H. Knap

Bermuda Institute of Sciences (BIOS), Inc. Founded in 1903 as the Bermuda Biological Station 17 Biological Station, St. George’s, Bermuda Foreword

etween 2010 and 2012 a large number of authors from seven different countries and B 26 separate organisations developed a scientific case to establish the global importance of the Sargasso Sea. A summary of this international study was published in 2012 as the “Summary science and Supporting Evidence Case.” Nine reasons why the Sargasso Sea is important are identified in the summary. Compiling the science and evidence for this case was a significant undertaking and during that process a number of reports were specially commissioned by the Sargasso Sea Alliance to summarise our knowledge of various aspects of the Sargasso Sea. This report is one of these commissioned reports. These are now being made available in the Sargasso Sea Alliance Science Series to provide further details of the research and evidence used in the compilation of the summary case. A full list of the reports in this series can be found in the inside back cover of this report. All of them can be downloaded from www.sargassoalliance.org.

Professor Howard Roe Professor Dan Laffoley Science Advisory Committee Chair Science Coordinator Sargasso Sea Alliance Sargasso Sea Alliance

2 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Table of Contents Chapter 1: Overview of the Importance of the Sargasso Sea and this report . . . . . 5

Chapter 2: Physical Characteristics of the Sargasso Sea...... 6 2.1: Meteorology and Seasonal Cycling of the Upper Ocean...... 7 2.2: Subtropical Mode Water (STMW)...... 8 2.3: Influence of the North Atlantic Oscillation on Sargasso Sea Variability. . . . .10 2.4: Dynamics and Implications for Short and Long Term Variability. . . . . 10 2.5: Deep Water masses in the Sargasso Sea ...... 12 References ...... 13

Chapter 3: Chemical Characteristics of the Sargasso Sea ...... 14 3.1: Nutrients in the Sargasso Sea ...... 14 3.2: Trace elements in the Sargasso Sea...... 16 3.3: Organic Contaminants in the Sargasso Sea...... 17 References ...... 19

Chapter 4: Biological Food Webs/BATS...... 23 4.1: Food Web Overview ...... 23 4.2: Research ...... 23 4.3: Zooplankton Research ...... 24 4.4: Microbial ...... 26 4.5: Sediment Traps and Carbon Export ...... 27 4.6: Ocean Optics and Remote Sensing...... 29 References ...... 30

Chapter 5: Biogeochemical Cycles in the Sargasso Sea ...... 33 5.1: Marine biogeochemical cycles in the Sargasso Sea...... 33 5.2: The Global Ocean Carbon Cycle and Observations in the Sargasso Sea . . . . 35 5.3: Calcium Carbonate Production ...... 36 References ...... 37

Chapter 6: Air-sea Interactions ...... 39 6.1: Variability, NAO/ENSO Influences on the Subtropical Gyre...... 39 6.2 : Atmospheric Deposition and Acid ...... 40

6.3: Air-sea Gas Exchange, CO2 and DMS...... 41 References ...... 42

Chapter 7: and ...... 44 7.1 : Climate Change ...... 44 7.2: Ocean Acidification ...... 44 References ...... 46

Appendix 1: Contact Information for Contributing Authors...... 47 Appendix 2: Glossary of Important Terms...... 48 Appendix 3: Compilation, by year through June 2011, of peer-reviewed publications arising from work at or near the Bermuda Atlantic Time-series Study (BATS) site.. . . 49 Acknowledgements

The authors of this report are grateful to all the support staff, without whom, this achievement would not have been possible. There are far too many people to mention each by name, but these individuals were crucial in collecting and compiling the necessary data. The authors are also grateful to the USA funding agencies whose support over the past 58 years have made this work possible. In particular, the USA National Science Foundation (NSF) for providing critical financial support of the Panulirus Hydrographic Stations and Bermuda Atlantic Time-series Study (BATS), the Microbial Observatory and the Ocean Flux Program. NSF has consistently shown a commitment to the scientific work conducted at BIOS as well as the institution’s research vessels Panulirus II, Weatherbird I, Weatherbird II and Atlantic Explorer. Historical grants are too numerous to mention; current grants are listed below.

Award Number / Award Title 1012444 2010 Shipboard Scientific Support Equipment for R/V Atlantic Explorer­­. 1119773 2011 Oceanographic Instrumentation: R/V Atlantic Explorer. 1044934 Collaborative Research: Isotopic and Compositional Investigation of the Sources and Interactions of Reactive Nitrogen in the Marine Atmosphere at Bermuda. 0752161 Collaborative Research: Combining Flow Cytometry and Stable Isotope Techniques: A Method to Measure Phytoplankton- and Bacteria-specific Nitrogen and Carbon Uptake. 1030149 Collaborative Research: Community Composition and Trophic Interactions as Modifiers of Carbon Export in the Sargasso Sea. 0918422 Shipboard Scientific Support Equipment for R/V Atlantic Explorer. 0927567 Collaborative Research: Prochlorococcus and its contribution to new production in the Sargasso Sea. 0928406 BEACON: BErmuda ocean Acidification and iNvestigation. 1045966 Dimensions: Collaborative Research: Biological Controls on the Ocean C:N:P ratios. 0752366 The Bermuda Atlantic Time-series Study (BATS): Year 21-25. 0549750 Collaborative Research: Development of the Automated Dissolved Inorganic Carbon Analyzer (AMICA) for Seawater DIC Analyses. 0825701 Operation of a Community Marine-Atmospheric Sampling Facility at Tudor Hill, Bermuda. 0927453 USA GEOTRACES North Atlantic Section: The chemical speciation of dissolved iron and copper. 0648016 The Panulirus Hydrographic Stations: Years 54-59. 0927098 Time Series Particle Flux Measurements in the Sargasso Sea. 0936341 Oceanographic Technical Services, 2009-2011: R/V Atlantic Explorer. 0505888 Operations Weatherbird II.

4 Sargasso Sea Alliance – Oceanography of the Sargasso Sea chapter 1 Overview of the Importance of the Sargasso Sea and this Report A.H. Knap

he Sargasso Sea is an anticyclonic gyre in the central these two stations has afforded scientists with a unique TNorth . Noted as oligotrophic, understanding of the Atlantic Ocean over time and acts the Sargasso Sea (also known as the North Atlantic as a barometer for changing climate. Subtropical Gyre) has low nutrient levels and is considered From research conducted at the Bermuda Institute to be representative of most oceanic gyres. Gyres like this of Ocean Sciences (BIOS Inc.), as part of BATS, we one cover 60 percent of the ocean surface or roughly know that, over the past several decades, portions of 40 percent of the globe. Traditionally the boundaries of the western , namely the Sargasso the Sargasso Sea were defined by the presence of the Sea, have warmed ~0.3-0.5ºC, and that carbon dioxide free-floating pelagic plant . Now, however, the content has increased 10 percent. What we do not know Sargasso Sea is defined in terms of physical boundaries— is how widespread these changes are within the North the Gulf to the west, the Atlantic Gyre as a whole, or how other oceanographic to the north, the Canaries Current to the east, and the and parameters may have changed as a result, to the south. The only landmass so further study is extremely important. in the Sargasso Sea is the of Bermuda, making it an Within the boundaries of the Sargasso Sea, the ideal place for research. major surface biological life, Sargassum seaweed, can The waters around Bermuda are home to two of the be found anywhere. While it may be more consistently longest running time-series measurement sites in the . copious in certain sectors, abundance at any single In 1954, the late Henry Stommel started a time-series location is quite unpredictable. The floating Sargassum of ocean measurements in the Sargasso Sea at Station ‘S’ is home to more than 60 species of organisms, with the (32°10’N, 64°30’W) The data collected at Station ‘S’ has ecosystem housing everything from small plant species to provided invaluable insight into the changing conditions juvenile and adult fish. Generally the area is relatively free of the deep ocean. In 1988, a more complex measurement of pollution, though tar and can amalgamate with program called the Bermuda Atlantic Time-series Study the Sargassum community. (BATS) was started 80 kilometers southeast of Bermuda. While the floating Sargassum is an important With funding from the US National Science Foundation ecosystem, the majority of the Sargasso Sea life is pelagic, as well as other US agencies, the data collected at mid and deep-water organisms of the Atlantic Ocean.

Figure 1. Ocean map showing the location, extent and circulation pattern of the five ocean gyres. Credit: NOAA

5 Sargasso Sea Alliance – Oceanography of the Sargasso Sea This is due to the Sargasso Sea’s abyssal depths of 4000 The Bermuda are located about half way or more meters. Dr. described many of the between the major western North Atlantic humpback organisms in his record bathyscape dives off Bermuda in whale breeding areas in the and the northern 1932 (These dives actually resulted in the first live radio feeding grounds extending from the New broadcasts from the deep ocean). While there are far too coast to . Therefore they provide an excellent many organisms to name in this article, there are some place for observation of this species. Adult whales species of specific interest to the scientific community. The reach up to 30 tons and range from 12 – 19 meters Sargassum community, the yearly eel migration/spawning in length. The flippers are unique, they measure activity and the migration of marine are all of up to one-third of the body weight and are used as special interest, and there are many species of migrating cooling planes through which a whale loses heat. This fish that provide for sport fishery in Bermuda. cooling allows the humpbacks to live closer to the One of the interesting mysteries of this part of warmer equatorial waters than other whales. They the ocean is the spawning of the American eel (Anguilla also use these large fins to defend themselves against rostrata) and the (Anguilla anguilla). Various killer whales as well as for feeding, to sweep into sized larvae of both species were captured and studied to their mouths. Although there are many reports of the infer that adults of these species migrate to the Sargasso sighting of whales off Bermuda going back to the early Sea and and die, but surprisingly, the routes and settlers, it was not until Verril in 1902 where there was mechanisms of the adult migration is still largely unknown. more of a description of their seasonality. The whales Anguilla occupy fresh water , , brackish waters arrived off Bermuda in late February or early March and the open ocean in various stages in their life cycle. They and left around the first of June, most accompanied by apparently spawn in the Sargasso Sea and ocean currents suckling cubs. did exist in Bermuda for a time, transport the developing larvae northward until the young beginning in 1911, but it was banned in 1942. Various metamorphose into juveniles and then move upstream studies have been carried out using acoustic studies of along the . There is apparently no difference in humpbacks and from 1967 to 1972 at least 10 whales the vertical distribution of the two species in the Sargasso were observed off Bermuda per day with up to 25 Sea, as the larval (leptocephali) of both species were found in a single day. These whales also produce “songs” in equal abundance between 0 and 350 meters. Developing which last on average 15 minutes but can extend to 30 eels remain in fresh or brackish water for about 10 years minutes. There is some suggestion that the humpback before they return to the sea to spawn. Although larvae of whale population off Bermuda has decreased since the both species have been positively identified, no adult eels 17th, 18th, and but this may be due to the have been found and therefore where and what depth the better food availability in other areas. mature eels occupy is still largely unknown.

chapter 2 Physical Characteristics of the Sargasso Sea R.J. Johnson

Over the past several decades our understanding of the into the temporal (diurnal to decadal) and spatial (finescale relevant physics of the Sargasso Sea (more commonly of < 10km to mesoscale <100km) variability of this region. known as the North Atlantic Subtropical Gyre) has benefited For this geographical province, the prevailing from extensive field programs of this (e.g., MODE, wind patterns of easterly trades in the tropics and mid- POLYMODE, FASINEX, GEOSECS, BIOWATT, TTO, WOCE, latitude westerlies cause surface ocean flows to converge CLIMODE, ARGO, JGOFS, BATS and Hydrostation ‘S’). towards the center of the gyre resulting in a net vertical These programs have mostly succeeded in defining the large for the subtropical gyre interior. The need scale gradients and dominant seasonal cycles of the physical to conserve potential vorticity following this interior parameters and importantly have provided valuable insight downwelling creates a southward Sverdrup transport

6 Sargasso Sea Alliance – Oceanography of the Sargasso Sea that ultimately is balanced by an intense current along predominately through latent heat flux (Michaels et al., the western edge of the ocean basin. These dynamics 1994). In the region becomes dominated by the essentially define the Sargasso Sea domain where it is large Bermuda- high leading to generally stable bounded to the west and north by the , to conditions with light winds and high humidity. the south by the North Equatorial current and to the east Tropical cyclones can abruptly alter these conditions by the weak gyre recirculation flows (Fig. 2.1). with a marked impact on upper ocean inventories of

Climate change concerns over the past two heat, and TCO2 (Bates et al., 1998; Nelson 1998) decades have intensified, leading to more emphasis on and single have been observed to reduce SST by detecting and understanding emerging patterns of long ~ 2.5ºC (Dickey et al., 1998). term change in the heat and salinity budgets of the upper Seasonal cycling in the upper ocean of the ocean. For the Sargasso Sea, the monthly Bermuda Atlantic Sargasso Sea is predominately a direct response to the Time-series Study (BATS) and biweekly Hydrostation ‘S’ local atmospheric conditioning that dictates the surface programs play a pivotal role in this challenge to better flux of heat, freshwater and momentum and ultimately understand long term change and serve as an important drives convective mixing in the upper ocean. At the BTS reference framework for larger scale field and modeling a relatively strong seasonal cycle of vertical mixing is studies due to their relatively long temporal span observed characterized by variable deep winter mixing (Fig. 2.1). The locations of the BIOS operated Bermuda (150 to 400m, Fig 2.2) and shallow warm mixed layers in Time-series Sites (BTS) are 31º 40’N, 64 10’W (BATS) and the summer months (Menzel and Ryther, 1961; Michaels 32º 10’N, 64º 30’W (Hydrostation ‘S’) which positions et al., 1994; Steinberg et al., 2001). The transition from net them northwest of the center of the Sargasso Sea (Fig. 2.1). warming to net cooling, during September and October, initiates convective entrainment of the shallow summer- 2.1. Meteorology and Seasonal Cycling time that increases through the winter months of the Upper Ocean ending with the erosion of the seasonal and During winter, the northern Sargasso Sea is conditioned formation of a deep mixed layer. Stabilization of the water by the passage of low-pressure atmospheric systems column begins in late March in response to the net heat originating from at near weekly intervals. flux turning positive (i.e. heat gain by the ocean) and as Air masses associated with these storms are typically the warming cycle continues the upper ocean at the BTS cold and dry which combined with high wind speed returns to a highly stratified state with a shallow diurnal results in a large rapid heat loss of the upper ocean mixed layer trapped above the seasonal thermocline.

Figure 2.1. Satellite image of the Sargasso Sea showing sea surface height and derived geostrophic velocity, illustrating typical mesoscale variability. The long-term mean circulation of the warm waters (>17ºC) of the subtropical gyre is shown as thick black arrows where the numbers indicate transport in Sverdrup (Worthington 1976). Satellite data courtesy of University of Colorado and image adapted from Steinberg et al., 2001.

7 Sargasso Sea Alliance – Oceanography of the Sargasso Sea This summer time mixed layer rarely extends below 20m 2.2. Subtropical Mode Water (STMW) allowing for rapid increases in SST (maximum ~28ºC) and An important of the Sargasso Sea is Subtropical episodic development of shallow warm fresh layers in Mode Water (STMW) or more classically referred to as response to low wind high precipitation events (Michaels ‘18 degree water’ which forms in the northern Sargasso et al., 1993). Sea typically north of 33ºN (Worthington, 1976). As to the north of the BTS experience more discussed above, intense cooling of the surface layers in intense winter storms due to the closer proximity to the winter months of the northern Sargasso Sea causes the central low pressure and thus heat loss increases deep mixed layers which extend to depths of ~400m, northwards from the BTS towards the Gulf Stream forcing with mixed layer temperatures of ~18ºC (Worthington, deeper mixing and greater seasonality. In contrast, mixing 1976). Thermohaline properties of this STMW tend to be to the south of the BTS and particularly south of the relatively stable over time that is likely a consequence of subtropical convergence zone (near 28ºN) is relatively the strong air-sea surface fluxes (Talley and Raymer, 1982). weak leading to a permanently stratified water column. During the onset of spring, the STMW becomes capped Hence, a feature of the BTS locale is strong seasonal from the air-sea interface by the seasonal thermocline and meridional gradients implying observations at the BTS are subsequently subducts to the south through isopycnal likely sensitive to interannual variations in the atmospheric transport thereby carrying surface properties (physical forcing of the gyre and further can exhibit upper ocean and biogeochemical) to the interior of the Sargasso Sea. properties similar to both northern and southern At the BTS previously formed STMW is typically (Siegel et al., 1990). observed between 150 and 400m as a near homogeneous The BTS programs provide an invaluable 57 years lens readily identifiable by a minimum in the potential of repeat observations for understanding variability in vorticity (Talley and Raymer, 1982; Ebbesmeyer and the seasonal cycling of the upper ocean with linkages Lindstrom, 1986). Understanding the dynamics and to climate change. As such, these data have been used properties of STMW at the BTS is a key element for extensively in climatological studies of the North Atlantic assessing inter-annual variability since mixed layer to identify inter-annual, decadal and centennial variability entrainment during the winter months extends into the (e.g., Dickson et al., 1996; Houghton 1996; Levitus et al., underlying STMW which then becomes mixed with the 1996; Marsh and New, 1996; Talley, 1996; Molinari et al., local surface waters. Analyses of the Hydrostation ‘S’ 1997; Joyce, 2000; Bates 2001; Goodkin 2008). time-series reveal the depth of STMW core is remarkably

Figure 2.2. Contour plots of temperature and salinity for the upper 500m at Hydrostation ‘S’ for years 1955 to 2010. Mixed layer depth is overlaid as a solid black line.

8 Sargasso Sea Alliance – Oceanography of the Sargasso Sea variable over both short (monthly) and long (annual) highlight the value of the Hydrostation ‘S’ observations as a timescales with a mean core temperature of 18.1 ± 0.4 ºC reference metric for change in the Sargasso Sea. (Johnson, 2003). The most striking feature of the 57 year A number of process-oriented cruises have been record of STMW is the dramatic upward displacement of established to better define the properties and extent this lens during 1969-1973 followed by a steady relaxation of STMW formation in the northern Sargasso Sea (e.g., through 1975 (Fig.2.3). During this pentad of uplifted MODE, POLYMODE, CLIMODE) although there are no STMW, Hydrostation ‘S’ observed the coldest SST’s on continuous time-series observations in this region. The record (Fig 2.3) for this location even though the mixed Argo float program (Roemmich et al., 2009) helps fill this layer depths were not overly deep for this period. This void with a hundred or so autonomous profiling floats strongly argues that the change in SST was largely due in this region but since they are free drifting, temporal to the positioning of the STMW and hence, evolution of analyses are difficult. In addition to the core measurements the surface waters at the BTS is conditioned by properties at the BTS a number of ancillary programs using chemical of STMW formed in previous years (Bates et al., 2002; tracers such as 3H (tritium, for anthropogenic inputs) and Johnson, 2003). This upward displacement of the STMW 7Be (berylium 7 as tracers of cosmic produced radioisotope during the 1969-1973 pentad was not isolated to the BTS deposited to the ocean surface ocean during precipitation region and was found to be prevalent through much of events) have proven effective for determining the age of the subtropical gyre (Levitus, 1989) being attributed to STMW at the BTS. The 7Be is useful for periods of weeks the westward propagation of a Rossby wave (Ezer, 1999). to several months and has identified the rapid arrival In contrast to the Rossby wave theory, Marsh and New (2 to 4 months) of recently formed STMW to the BTS (1996) using a modeling approach were able to reproduce (Kadko, 2009) whereas the 3H studies have shown the the STMW variability at Hydrostation ‘S’ during 1969-1973 age of STMW at the BTS to be variable ranging from one concluding that the variability was due to anomalous forcing to several years (Jenkins, 1994). The integration of these events associated with frequent outbreaks of cold dry air other programs with observations from the BTS remain a over the Gulf Stream. Such findings demonstrate the need robust framework for interpreting variability in STMW and to understand processes at many scales in order to asses assessing the significance of this water mass as a repository inter-annual variability of the upper ocean and further, of heat and carbon (Bates et al., 2002).

Figure 2.3. Time-series plots of temperature and salinity anomaly at 300m (STMW) for Hydrostation ‘S’ 1955-2011. Anomaly computed by subtracting long- term mean for this depth. Red line shows a 1-year central running mean and the observed data is shown as blue dots. Long- term trends for temperature and salinity are determined as 0.009 °C year-1 (p < 0.01) and 0.002 year-1 (p < 0.01) respectively.

9 Sargasso Sea Alliance – Oceanography of the Sargasso Sea 2.3. Influence of the North Atlantic Oscillation et al., 2010) and data from the BTS remain a key element on Sargasso Sea Variability for assessing this important ocean-atmosphere linkage The dominant long-term mode of meteorological (Bates et al., 2001). More recently, emphasis has been variability in the North Atlantic is associated with the with trying to establish the significance of the NAO North Atlantic Oscillation (NAO) that is typically induced physical variability on biogeochemical cycles referenced by the NAO index defined as the difference of the upper ocean and it seems that some previously in the normalized sea level pressures between , thought paradigms for carbon export may need and Stykkisholmur, Iceland (Hurrell, 1995). alteration (Lomas et al., 2010). Atmospheric dynamics during a positive NAO phase 2.4. Eddy Dynamics and Implications lead to anomalously high pressures across the subtropical for Short and Long Term Variability Atlantic, whereas for negative phases the Icelandic low- pressure system shifts to the south driving more intense In the vicinity of the BTS, the long term flows are winter storms across the Sargasso Sea. Although the NAO characterized by low (< 5cm s-1) south westerly geostrophic has shown considerable variability over the past several currents (Worthington, 1976) with net Ekman downwelling decades it has mostly been negative for years 1950 to rates of ~4cm day -1 (McClain and Firestone, 1993). Given 1970 and since this period has switched to a positive state these low velocities, the BTS are presumed appropriate with short aperiodic reversals to a negative phase (e.g., locations for time-series studies since advective processes Talley 1996, Hurrell 1995). should be small compared to those forced by local Changes in the atmospheric dynamics of the North conditions (Michaels, 1994). However, in contrast to Atlantic associated with the NAO undoubtedly influence these long-term mean flows much of the interior of the variability in the upper ocean of the Sargasso Sea (Rogers Sargasso Sea is continually subjected to the presence of 1990). At the BTS the principal influence of the NAO mesoscale eddies resulting in complex rotational flows on the upper ocean hydrography is the depth of winter with typical instantaneous speeds ranging between 10 to mixing and subsequent SST. Given the greater storminess 50 cms-1 (Siegel and Deuser 1997; Fig. 2.1). Mesoscale during negative NAO years winter mixing tends to be eddy phenomena in the Sargasso Sea include cold core deeper with colder SST’s whereas relatively shallow warm rings (Richardson, 1978) and mid-ocean mesoscale eddies winter mixed layers are more normal for positive phases (McGillicuddy and Robinson 1997). The core of these two (Bates et al., 2001). Since the depth of this deep winter types of eddies are quite different in that the ‘cold-core’ mixing is a key factor for deducing heat storage and contains water from north of the Gulf Stream and thus , the NAO state plays an intimate transport foreign waters to the northern Sargasso Sea. role in modulating the ocean’s climate change response. Due to the closed recirculation flow in this region these This becomes further complicated on consideration that cold core eddies tend to remain in the northwest sector the STMW underlying the surface waters at the BTS of the gyre (Cornillion et al., 1986) although have been has been pre-conditioned in previous years. This was infrequently observed near the BTS (Siegel et al., 1999). highlighted by Talley (1996) using data from the BTS In contrast, mid-ocean eddies are presumed to originate who showed that variations in the STMW properties are within the Sargasso Sea such that the temperature-salinity directly related to the NAO. In particular, Talley (1996) profile through the permanent thermocline of these eddies concludes that heavier STMW is formed as result of is consistent with gyre water types. increased convective activity plus increased transport of Advancements in satellite altimetry in the early relatively saline waters to the western subtropical gyre. 90’s helped reveal the extent and ubiquitous nature In addition to changes in direct local convective activity, of mid-ocean mesoscale eddies in the Sargasso Sea the intensity of the North Atlantic gyre circulation has (Fig 2.1) that was first hypothesized in the MODE and been linked with NAO variability (Curry and McCartney POLYMODE programs. From satellite data these features 2001). Although the association is not directly covariant can be recognized by changes in sea level height. While Curry and McCartney (2001) suggest that consideration from oceanographic observations, eddies are readily of time integration of the ocean signal due to mixed layer identified by displacements of the density surfaces in memory and Rossby wave propagation gives a first order the upper ocean. Mid-ocean mesoscale eddies can be agreement with the NAO. broadly categorized into three types: (i) cyclonic- density Evidence for the NAO accounting for a significant surfaces elevated resulting in anomalously cold water fraction of the variance in the hydrography of the upper and a depressed sea level at its center (ii) anticyclonic ocean of the Sargasso Sea continues to emerge (Lozier —density surfaces depressed resulting in anomalously

10 Sargasso Sea Alliance – Oceanography of the Sargasso Sea warm water and an elevated sea level at its center and program) often identify anomalous water masses at (iii) mode water or lens eddy—formed when a lens of the core of the eddy. Thus contrary to earlier genesis near uniform water resides between two density surfaces theories, mid-ocean eddies may permit a pathway for causing density surfaces to be elevated and depressed foreign waters into the Sargasso Sea (Li et al., 2008). for depths above and below the lens, respectively. In Analysis of the depth of specific isopycnal the case of a lens eddy, the density surface perturbation surfaces in the upper ocean at the BTS reveal substantial tends to be greater in the deeper layers and thus in displacements over short (biweekly to monthly) timescales terms of sea level height resemble a weak anticyclone which are coherent with satellite derived estimates of sea (McGillicuddy and Robinson, 1997; McGillicuddy et al., level height associated with the passage of mesoscale 1999). Mid-ocean eddies have diameters of <100km, eddies (Siegel et al., 1999). Additionally, data from BATS lifetimes of months to years with propagation speeds Spatial Validation cruises (BVAL) highlight the spatial of 3 to 5 km day-1, predominately track on a westerly heterogeneity of parameters (e.g., temperature, salinity to north westerly course and their signal is apparent and nutrients) at fixed depth horizons that is found to through the base of the permanent thermocline be statistically consistent with the temporal variability (~1000m) (McGillicuddy et al., 1999). Mesoscale eddies observed at the BTS (McGillicuddy et al., 1999). Hence, represent an important mode of transport for physical the passage of mesoscale eddies through the BATS is and chemical properties, however, understanding their the dominant mode of variability for depths below the full impact through a specific region is difficult since surface mixed layer. their passage alters upper ocean inventories through Impact of mesoscale eddies in the upper 100m both horizontal and vertical mechanisms (Woods 1988). is more complicated since other processes, principally Furthermore, it is still unclear whether mesoscale eddies convective mixing, interact with eddy dynamics. are turbulent self-contained features or are the result of Modeling studies of the upper ocean heat and salinity linear planetary wave propagation (Siegel et al., 1999) budgets at the BTS have been performed to assess although recent field surveys off Bermuda (EDDIES eddy influence on the mixed layer (Doney 1996; Project) suggest the former (Benitez-Nelson and Johnson 2003). Results from these modeling exercises McGillicuddy, 2008). show significant imbalances in the heat and salinity In addition to modulating upper ocean physics, budgets from that which can be accounted for by local mesoscale eddies also impact biogeochemical processes atmospheric forcing in a 1-dimensional sense. This in the upper ocean by simply lifting or depressing the imbalance implies the need for advection to balance nutricline into the euphotic zone. Assessment of this the system and appears to be a direct consequence of process is important for understanding the role of mesoscale eddies (Glover et al., 2002). eddies in the oceanic biological pump (Volk and Hoffert The spatial and temporal evidence from the BTS 1985) and field campaigns off Bermuda (EDDIES programs strongly imply that the upper ocean in this region Project) have been instrumental for investigating is intimately modulated by mesoscale eddies which in turn pertinent dynamics (Benitez-Nelson and McGillicuddy, has consequences for understanding system processes at 2008). It is clear that eddies in the Sargasso Sea drive the BTS. This is also supported by continuous measurements significant spatial variability in the physics and biology of velocity and temperature from the Bermuda Testbed over a wide range of length scales (10’s to 100’s Mooring (BTM) which suggest a de-correlation time scale km). Further, mixing and subsequent nutrient supply of ~20 days, which is similar to the sampling frequency at the to the euphotic zone differs for each eddy type and BTS (Dickey et al., 1998). However over longer time scales importantly, eddy/wind interactions dictate the new (years to decades) the eddy-induced variability appears to production potential of an eddy (McGillicuddy et al., be balanced such that the 1-dimensional approximation is 2007). Observations from the EDDIES project reveal able to account for a significant fraction of the variance in wind interactions with mode water eddies amplify the the heat and salinity budgets of the upper ocean (Johnson eddy-induced upwelling that can result in significantly 2003). Time- series analysis of data from the BTS reveals large biological blooms whereas for cyclones the significant long-term trends in the temperature and salinity eddy/wind interaction reduces the upwelling signal of the upper ocean above the short-term eddy variability (McGillicuddy et al., 2007). Although mid-ocean (Fig. 2.3) (Johnson et al., 2008). For the upper 400m, eddies are presumed to consist of water local to the temperature and salinity are increasing by ~ 0.01ºC year-1 Sargasso Sea, intensive surveys of these features and 0.002 year-1, respectively. The significance level of this (EDDIES project and on-going work through the BATS trend rises with depth reaching a maximum near 300m

11 Sargasso Sea Alliance – Oceanography of the Sargasso Sea that is approximately the long-term mean depth of STMW at the BTS with an inferred 6-year transit time. At the BTS, at the BTS (Fig.2.3). Sea water is observed at ~2000m and analysis of the Hydrostation ‘S’ data reveal significant trends for 2.5. Deep Water masses in the Sargasso Sea this water mass (Whitefield et al., 2008). For years 1985 The previous discussion has mostly focused on properties –2004, a dramatic decrease in temperature (~0.012 ºC of the upper ocean, however assessment of the deep year -1) and salinity (~ 0.002 year -1) is observed which has water masses of the Sargasso Sea is important for since reversed with temperature and salinity increasing understanding variability of the Atlantic Meridional for the past pentad (Fig.2.4). Interestingly, the analyses Overturning Circulation (AMOC) and ultimately climate by Curry et al., (1998) predicted continued cooling into change. Over the past decade there has been concern that the next decade which has since been proved correct at the AMOC could significantly weaken during this century Hydrostation ‘S’. thus reducing the northward transport of heat to the New research activities continue to investigate the North Atlantic (Houghton et al., 2001). Schematically, the physical processes of the Sargasso Sea with the time-series zonally averaged components of the AMOC comprise of programs operated at BIOS central to this observational a northward flow in the upper 1300m, a southward return network for assessing climate processes and ocean flow of North Atlantic Deep Water (NADW) between response. The BATS program has recently expanded its 1300 and 4000m, and a northward flow of spatial strategy to help deduce eddy transport and also (AABW) below 4000m. Given the location continues to run annual transects from 35ºN to 19ºN to of the formation sites of these water masses, observations determine meridional changes in the water masses of the of these deep-water masses at the BTS provide a unique Sargasso Sea. A new array of deep moorings (DYNAMITE, framework for assessing coordinated climate change in lead PI Ruth Curry – WHOI) has recently been deployed the Atlantic basin. Direct linkages with climate conditions off Bermuda with the most northern mooring situated at deep-water formation sites with observations at the between the BTS. The aim of DYNAMITE is to measure BTS have been established. For example, Curry et al., abyssal flows along the Bermuda Rise in order to (1998) show that ‘imprinted’ properties of surface waters understand interior circulation of the gyre and is likely to in the sub-polar Labrador basin appear in upper NADW be complimentary to the existing time-series programs.

Figure 2.4. Time-series plots of temperature and salinity anomaly at 2000m ( water) for Hydrostation ‘S’ 1970-2011. Anomaly computed by subtracting long- term mean for this depth. Note significant (p < 0.01) decline in temperature (-0.010 °C year-1) and salinity (-0.0018 year-1) for 1985 -2010. Red line shows a 1-year running central mean and the observed data is represented by the blue dots.

12 Sargasso Sea Alliance – Oceanography of the Sargasso Sea References for Chapter 2

Bates, N.R., 2001. Interannual Ebbesmeyer, C.C. and Joyce, T.M., Deser, C., and Spall, McGillicuddy, D.J., Johnson, variability of oceanic CO2 and Lindstrom, E.J., 1986. Structure M.A., 2000. The relation between R.J., Siegel, D.A., Michaels, A.F., biogeochemical properties in of the 18ºC water observed decadal variability of subtropical Bates, N.R. and Knap, A.H., the Western North Atlantic during the POLYMODE local mode water and the North 1999. Mesoscale variations of subtropical gyre. Deep-Sea Research dynamics experiment. Journal Atlantic Oscillation. Journal of biogeochemical properties in the II, 48, 1507–1528. , 16, Climate, 13(14), 2550–2569. Sargasso Sea. Journal of Geophysical 443–453. Research, 104, 13381–13394. Bates, N.R., Pequignet, C., Kadko, D., 2009. Rapid Johnson, R.J. and Gruber, N., Ezer, T., 1999. Decadal oxygen utilization in the ocean McGillicuddy D.J., Anderson, 2002. A short-term sink for variabilities of the upper layers of twilight zone assessed with the L.R., Bates, N.R., Bibby, T., 7 atmospheric CO2 in subtropical the subtropical North Atlantic: cosmogenic isotope Be. Global Buesseler, K.O., Carlson, C.A., mode water of the North Atlantic an ocean model study. Journal Biogeocehmical Cycles, 23, GB4010. Davis, C.S., Ewart, C., Falkowski, Ocean. Nature, 420, 489–493. of Physical Oceanography, 29, P.G., Goldthwait, S.A., Hansell, 3111–3124. Levitus, S., 1989. Interpentadal D.A., Jenkins, W.J., Johnson, Benitez-Nelson, C.R. variability of temperature and R.J., Kosnyrev, V.K., Ledwell, and McGillicuddy, D.J., Glover, D.M., Doney, S.C., salinity at intermediate depths of J.R., Li, Q.P., Siegel, D.A., 2008. Mesoscale physical— Mariano, A.J., Evans, R.H. and the North Atlantic Ocean, 1970– Steinberg, D.K., 2007. Eddy/ biological—biogeochemical McCue, S.J., 2002. Mesoscale 1974 versus 1955–1959. Journal of wind interactions stimulate linkages in the open ocean: An variability in time series data: Marine Research, 36, 311–322. extraordinary mid-ocean plankton introduction to the results of the Satellite based estimates for blooms. Science, 316:1021–1026. E-Flux and EDDIES programs— the USA JGOFS Bermuda Levitus, S., Antonov, J., Zhou, Preface. Deep-Sea Research II, 55, Atlantic Time-series Study X., Dooley, H., Selemenov, Menzel, D.W. and Ryther, J.H., 1133–1138. (BATS) site. Journal of Geophysical K. and Tereschenkov, V., 1961. Annual variations in primary Research, 107, C8, 3092, doi: 1996. Decadal-scale variability production of the Sargasso Sea Cornillion, P.D., Evans, D. and 10.1029/2000JC000589. of the North Atlantic Ocean. off Bermuda. Deep-Sea Research, 7, Large, W., 1986. Warm outbreaks Eds. D.G. Martinson, K. Bryan, 282–367. of the Gulf Stream into the Goodkin, N.F., Hughen, K.A., M. Ghil, M.M. Hall, T.M. Karl, E.S. Sargasso Sea. Journal of Geophysical Curry, W.B., Doney, S.C. and Sarachik, S. Sorooshian and L.D. Michaels, A.F., Knap, A.H., Research, 91, 6853–6596. Ostermann, D.R., 2008. Sea Talley. Natural Climate Variability Dow, R.L., Gundersen, K., surface temperature and salinity on decade-to-century time scales. Johnson, R.J., Sorensen, Curry, R.G., McCartney, M.S. variability at Bermuda during National Academy of Science Press, J., Close, A., Knauer, G.A., and Joyce, T.M., 1998. Ocean the end of the . 318–324. Lohrenz, S.E., Asper, V.A., transport of subpolar climate Paleoceanography, 23, PA3203. Tuel, M.A. and Bidigare, R.R., signals to mid-depth subtropical Li, Q.P., McGillicuddy, D.J., 1994. Seasonal patterns of ocean waters. Nature, 391, 575–577. Houghton, R.W.,1996. Subsurface Hansell, D.A., Bates, N.R., and biogeochemistry at the USA quasi-decadal fluctuations in the Johnson, R.J., 2008. Uncertainty JGOFS Bermuda Atlantic Time- Curry, R.G. and McCartney, North Atlantic. Journal of Climate, in the biogeochemical M.S., 2001. series Study Site. Deep-Sea Research 9:1363–1373. impact of a cyclonic eddy in I, 41, 1013–1038. circulation changes associated the Sargasso Sea. Journal of with the North Atlantic Houghton, J.T., Ding, Y., Griggs, Geophysical Research, 113, C10006, Michaels, A.F., Siegel, D.A., Oscillation. Journal of Geophysical D.J., Noguer, M., Van der doi:10.1029/2008JC004840. Johnson, R.J., Knap, A.H. and Research, 31, 3374–3400. Linden, P.J., Dai, X., Maskell, K. Galloway, J.N., 1993. Episodic and Johnson, C.A., Eds., (2001) Lomas, M.W., Steinberg, D.K, inputs of atmospheric nitrogen to Dickey, T.D., Frye, D., Jannasch, Climate Change 2001: The Scientific Dickey, T., Carlson, C.A., Nelson, H., Boyle, E.A., Manov, D., the Sargasso Sea: Contributions Basis. Cambridge University Press, N.B., Condon, R.H. and Bates, to new production and Sigurdson, D., McNeil, J., 881pp. N.R., 2010. Increased ocean Stramska, M., Michaels, A.F., phytoplankton blooms. Global carbon export in the Sargasso Biogeochemical Cycles, 7, 339–351. Nelson, N.B., Siegel, D.A., Hurrell, J.W., 1995. Decadal Sea linked to climate variability Chung, G., Wu, J. and Knap, trends in the North Atlantic is countered by its enhanced Molinari, R.L., Mayer, D., Festa, A.H., 1998. Initial results from Oscillation: regional temperatures mesopelagic attenuation. J. and Bezdek, H., 1997. Multi- the Bermuda Testbed Mooring and precipitation. Science, 269, Biogeosciences, 7, 57–70. Year Variability in the Near Program. Deep-Sea Research, 45, 676–679. Surface Temperature Structure 771–794. Lozier, M.S., Roussenov, V., of the Midlatitude Western Jenkins, W.J. (1994) A time Reed, M.S.C. and Williams, R.G., 3 North Atlantic Ocean. Journal Dickson, R., Lazier, J., Meincke, series of tritium and He in the 2009. Opposing decadal changes J., Rhines, P. and Swift, J., Sargasso Sea. Journal of Geophysical of Geophysical Research, 102, for the North Atlantic meridional 3267–3278. 1996. Long-Term Coordinated Research, 103, 15,817–15,831. overturning circulation. Nature Changes in the Convective Geoscience, 3, October 2010. Nelson, N.B., 1998. Spatial and Activity of the North Atlantic. Johnson, R.J., 2003. Climatic and mesoscale modulation of temporal extent of sea surface Progress in Oceanography, 38, Marsh, R. and New, A.L. temperature modifications by 241–295. the upper ocean at the Bermuda (1996) Modelling 18 degree time-series sites. Ph.D thesis, hurricanes in the Sargasso Sea water variability. Journal of Physical during the 1995 season. Monthly Doney, S.C., 1996. A synoptic University of Southampton, U.K. Oceanography, 26, 1059–1080. atmospheric surface forcing data Weather Review, 126, 1364–1368. set and physical upper ocean Johnson, R.J., Knap, A.H., McClain, C.R. and Firestone, J., Bates, N.R., Whitefield, J.D, Richardson, P.L., Cheney, R.E. model for the USA JGOFS 1993. An investigation of Ekman and Worthington, L.V., 1978. A Bermuda Atlantic Time-series Site. Kadko D. and Lomas, M.W., upwelling in the North Atlantic. 2008. Coordinated change in the census of Gulf Stream rings, Journal of Geophysical Research, 101, Journal of Geophysical Research, 98, spring 1975. Journal of Geophysical 25, 615–26, 634. heat, salinity and CO2 budgets 12237–12339. of the mesopelagic zone at the Research, 83, 6136–6144. Bermuda time-series sites. Ocean McGillicuddy, D.J. and Sciences meeting, Orlando 2008 Robinson, A.R., 1997. Eddy (oral presentation). induced nutrient supply and new production in the Sargasso Sea. Deep-Sea Research, 44, 1427–1450.

13 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Roemmich, D., Johnson, G.C., Siegel, D.A. and Deuser, W.G., Talley, L.D. and Raymer, M.E., Whitefield, J.D., Johnson, R.J. Riser, S., Davis, R., Gilson, J., 1997. Trajectories of sinking 1982. Eighteen Degree Water and Knap A.H., 2008. Deep Owens, W.B., Garzoli, S.L., particles in the Sargasso Sea: Variability. Journal of Marine water­ variability at the Bermuda Schmid, C. and Ignaszewski, Modelling of “statistical funnels” Research, 40:757–775. Timeseries Sites. Ocean Sciences M., 2009. The Argo program above deep ocean sediment traps. meeting, Orlando 2008 (poster observing the global ocean with Deep-Sea Research I, 44, 1519–1541. Talley, L.D. (1996) North presentation). profiling floats. Oceanography, 22, Atlantic Circulation and 34–43. Siegel, D.A., McGillicuddy, D.J. Variability, Reviewed for the Worthington, L.V. (1976) On and Fields, E.A (1999) Mesoscale CNLS conference Physica D. 98, the North Atlantic circulation. The Rogers, J.C. (1990) Patterns of eddies, satellite altimetry and new 625–646. John Hopkins Oceanography Studies, low-frequency monthly sea level production in the Sargasso Sea. 6, 1–110. pressure variability (1899–1986) Journal of Geophysical Research, 104, Volk, T. and Hoffert, M.I., and associated wave cyclone 13,359–3,379. 1985. Ocean carbon pumps: frequencies. Journal of Climate, 3, analysis of relative strengths 1364–1379. Steinberg, D.K., Carlson, C.A., and efficiencies in ocean-driven Bates, N.R., Johnson, R.J., atmospheric CO2 changes. In The Siegel, D.A., Iturriga, R., Bidigare, Michaels, A.F. and Knap, A.H., Carbon Cycle and Atmosphere R.R., Smith, R.C., Pak, H., Dickey, 2001. Overview of the USA CO2: Natural variations Archeaan T.D., Marra, J. and Baker, K.S., JGOFS Bermuda Atlantic Time- to Present (Sundquist, E.T. and 1990. Meridional variations of series Study (BATS): A decade- Broecker, W.S., Eds.) American the springtime phytoplankton scale look at ocean biology and Geophysical Union, Geophysical community in the Sargasso Sea. biogeochemistry. Deep-Sea Research Monograph, 32, Washington D.C., Journal of Marine Research, 48, Part II, 48, 1405–1447. 99–110. 379–412.

chapter 3 Chemical Characteristics of the Sargasso Sea

3.1. Nutrients in the Sargasso Sea The primary source of inorganic macronutrients K.N. Buck to the euphotic zone, and associated phytoplankton Located within the North Atlantic Gyre, the Sargasso Sea communities, of open ocean regions like the Sargasso Sea, is “oligotrophic,” characterized by low macronutrient is from mixing with enriched waters from deeper in the concentrations (Siegel et al., 1990; Michaels and Knap water column. This mixing typically occurs during winter 1996; Cavender-Bares et al., 2001; Lipschultz 2001; when temperatures cool sufficiently to break down the Steinberg et al., 2001; Babiker et al., 2004; Kamykowski thermocline and allow overturn of the upper hundreds 2008). Phytoplankton require the macronutrient elements of meters of the water column. Year to year variability in nitrogen (N), phosphorus (P) and silica (Si) to grow and nutrient budgets and resulting and reproduce. Carbon is also a vital macronutrient, but one particle export from the surface ocean at the Bermuda not generally considered to be limiting, and is discussed Atlantic Time-series Study (BATS) are related to the separately (“Biogeochemical cycles in the Sargasso Sea” variability in winter convective mixing in this region of the and “Ocean acidification”). Sargasso Sea (Talley and Raymer 1982; Michaels and Knap The distributions of macronutrient elements in 1996; Steinberg et al., 2001). The BATS area is located in a the reflect the assimilation of dissolved inorganic transition boundary between the northern and southern N (DIN), P (DIP) and Si (silicate) by phytoplankton into Sargasso Sea (Nelson et al., 2004), with the region south new organic matter in the sunlit upper water column, or of BATS exhibiting less mixing and corresponding lower euphotic zone. When phytoplankton cells die, they sink surface macronutrients year round (Siegel et al., 1990; as particles out of the euphotic zone into deeper waters, Michaels and Knap 1996; Lipschultz 2001). where that organic matter is re-mineralized and dissolved In the northern Sargasso Sea, winter convection inorganic pools restored over time and depth in the water is complemented as a nutrient source by additional column. In the Sargasso Sea, strong summer stratification entrainment of macronutrients from mixing during isolates surface waters from the relatively enriched strong events (Lomas et al., 2009 a, b) and eddy waters below, exacerbating depletion and resulting in activity (Lipshultz et al., 2002; Jenkins and Doney undetectable macronutrient concentrations at the surface 2003; Bibby and Moore 2011). Mesoscale eddies in (Siegel et al., 1990; Michaels and Knap 1996; Lipschultz particular have been shown to be a substantial source 2001; Steinberg et al., 2001). of macronutrients fueling primary production in surface

14 Sargasso Sea Alliance – Oceanography of the Sargasso Sea waters of the Sargasso Sea in the region of BATS 2011; Mather et al., 2008). The dominant phytoplankton (McGillicuddy Jr. et al., 2003; Sweeney et al., 2003; groups increase DOP uptake at low DIP concentrations Cianca et al., 2007; Ledwell et al., 2008; Li et al., 2008; such that total P assimilation, as a for growth Krause et al., 2010). Nitrogen fixation, the conversion of rate, remains essentially constant (Casey et al., 2009). In

N2 gas to DIN by phytoplankton, is another source of addition, phytoplankton growing in oligotrophic waters DIN to surface waters of the Sargasso Sea (Sarmiento like the Sargasso Sea can also reduce their P requirements and Gruber 1997; Hood et al., 2001), though it may be a by substituting with N and sulfur-based lipids (Van Mooy relatively minor contributor to the N budget in the BATS et al., 2006, 2009). This is an advantageous adaptation region (Hansell et al., 2004; Knapp et al., 2005). for this region, where dissolved organic forms of N and In the southern Sargasso Sea, on the other hand, P (DON and DOP, respectively) are typically at least 90% winter temperatures do not consistently cool enough of the total N and P pools (Cavender-Bares et al., 2001). to result in overturn, and there is little eddy kinetic Unlike N and P, which are incorporated by energy, leading to a stratified water column and nearly phytoplankton into organic matter (soft parts), Si is undetectable surface DIN and DIP throughout the year predominantly used by one group of phytoplankton, (Siegel et al., 1990; Michaels and Knap 1996; Lipschultz diatoms, to create external biogenic Si (bSi) tests (hard 2001; Lipschultz et al., 2002; Nelson et al., 2004). In parts). In models of nutrient cycling in the North Atlantic the absence of regular vertical mixing, nitrogen fixation (Lima and Doney 2004), demonstrate that temporal and atmospheric deposition of DIN are larger sources variability in diatom blooms at BATS are related to of DIN to surface waters (Hastings et al., 2003; Hansell variations in southward transport of Si and seed diatom et al., 2004). Summer rain originating over the southern populations. Mode water eddies, which mix up high Sargasso Sea is particularly high in DIN, presumably due macronutrient and particularly high Si (Bibby and to lightning activity in the region (Hastings et al., 2003). Moore 2011), have been shown to produce ~6x higher The ratio of N:P is a particularly useful tool in bSi concomitant with higher diatom abundances than oceanography for predicting nutrient limitation. The reported at BATS in the absence of eddy activity (Krause canonical , an N:P of 16:1, is traditionally et al., 2010). Unlike eddies, passage of winter storms applied to the global ocean, and deviations from this result in enhanced primary production and a very rapid ratio may indicate potential N limitation (N:P<16) or P diatom growth response (order of several days; Lomas et limitation (>16). In the Sargasso Sea at BATS, the ratio of al., 2009a, b) that does not accumulate but rather sinks N:P in surface waters typically exceeds the Redfield ratio on the same time scale and can account for nearly all the of 16 (Michaels et al., 1994; Michaels and Knap 1996; particulate organic carbon flux (Krause et al., 2009a). Steinberg et al., 2001), and averaged ~40 between 1989 Overall, though, BATS data from 1989 to 2003 indicate a and 1998 (Babiker et al., 2004) More recently, Cavender- year-over-year linear decrease in Si supply to this region, Bares et al., (2001), using high sensitivity methods for due in part to decreasing winter mixing, but also to both DIN and DIP detection, found relatively constant different nutrient gradients between DIN and Si that favor N:P ratios of ~40-50 in surface waters between 31 and relatively higher DIN inputs. This decrease in Si supply is 37ºN, consistent with the BATS dataset. Phytoplankton associated with a roughly 40% decline in biogenic silica in this area have been found to display physiological (bSi) production in the upper 120 m of the water column characteristics consistent with DIP limitation (Lomas et here (Krause et al., 2009b). This data record suggests a al., 2004), as have heterotrophic bacteria (Obernosterer reducing role of the productive diatom populations as a et al., 2003). In the southern Sargasso Sea, N:P ratios likely result of climate change at BATS. are much lower (<16:1; Cavender-Bares et al., 2001), a Intra- and inter-decadal-scale natural variations in condition that geochemically would favor either nitrogen climate like the North Atlantic Oscillation (NAO) and fixing phytoplankton or phytoplankton growing at near El Niño Southern Oscillation (ENSO) have been shown physiological maximum growth rates (Klausmeier et al., to introduce substantial variability in winter convection, 2004; Mills and Arrigo, 2010) . eddy activity, nutrient budgets and ensuing productivity While DIP is the favored form of P for phytoplankton at BATS (e.g., Steinberg et al., 2001; Bates and Hansell and heterotrophic bacteria in the Sargasso Sea 2004; Cianca et al., 2007). Anthropogenically-forced (Michelou et al., 2011), recent studies indicate that these warming of the surface ocean may be expected to present phytoplankton adapt to very low DIP concentrations by similar, though potentially irreversible, trends toward using organic forms of P (DOP) to acquire the needed P increasing stratification and reduced nutrient budgets (Dhyrman et al., 2006; Lomas et al., 2010; Michelou et al., in the Sargasso Sea. Additionally, recent research based

15 Sargasso Sea Alliance – Oceanography of the Sargasso Sea in part at BATS (Beman et al., 2011) indicates that DIN Iron (Fe) is arguably considered the most significant supply to the surface ocean from depth is likely to further micronutrient, regulating phytoplankton processes in a decrease as a result of increasing ocean acidification on number of oceanic settings (de Baar et al., 2005; Boyd the biochemical processes involved in N remineralization. and Ellwood 2010). At the Bermuda Atlantic Time- On the other hand, atmospheric sources of nitrogen, series Study (BATS) site, Sedwick et al., (2007) measured and nitrogen fixation, may be expected to increase as especially low dissolved Fe concentrations in the summer a result of anthropogenic activity (Bates and Hansell deep chlorophyll maximum (100-150 m) and suggested 2004; Duce et al., 2008; Krishnamurthy et al., 2009). the phytoplankton community in this region of the water Given the considerable research conducted to date column may be Fe limited seasonally. Cyclonic eddies in at BATS indicating that this system is highly sensitive the Sargasso Sea that have low dissolved Fe (Sedwick et to nutrient inputs, which are in turn intimately tied to al., 2007) and high macronutrients (Bibby and Moore climate variability, anthropogenic impacts to this region 2011) may also be Fe-limiting to phytoplankton growth. of the Sargasso Sea are likely to increasingly influence In surface waters, there is evidence for Fe stimulation macronutrient cycling and phytoplankton growth here. of new production from nitrogen fixation at the surface following a summer rain event (Kim and Church 2001), 3.2. Trace Elements in the Sargasso Sea supporting previous suggestions that Fe deposition here K.N. Buck may alleviate N stress (Michaels and Knap 1996; Gruber Beyond macronutrients, phytoplankton growth in the and Sarmiento 1997; Capone et al., 1997). marine environment is also heavily influenced by trace In general, though, the Sargasso Sea is an elements. Trace elements, by definition, are present at oligotrophic system, primarily limited by low inorganic very low concentrations, on the order of parts per trillion, N and P concentrations. Under these conditions, in open ocean regions like the Sargasso Sea. The low phytoplankton may use enzymes like urease and alkaline concentrations of these elements in the ocean, and their phosphatase in an attempt to access the organic pools of predominance on land, requires painstaking efforts be N and P, respectively. As these enzymes require the trace taken in sampling and analysis to avoid contamination. As a elements Ni (urease) and Co or Zn (alkaline phosphatase) result, trace element data published before the 1980’s are as metal cofactors to function, these elements are considered largely inaccurate due to likely overwhelming suspected to play a particularly important role in this contamination. There are several references for trace ecosystem. Indeed, Co and Zn concentrations are heavily elements in the Sargasso Sea that are not considered depleted in surface waters of the Sargasso Sea (Bruland here (Menzel and Ryther 1961; Menzel and Spaeth 1962; and Franks 1983; Saito and Moffett 2001, 2002; Jakuba et Spencer and Brewer 1969; Brewer et al., 1972; Bender and al., 2008; Milne et al., 2010), particularly when inorganic Gagner 1976) because of these concerns. P is less than 10 nM (Jakuba et al., 2008). There is much In the Sargasso Sea, nutrient-type profiles are less data available on Ni in this region, although surface typically reported for the trace elements iron (Fe: Wu depletion is apparent in depth profiles (Bruland and and Luther 1994, 1996; Wu et al., 2001; Wu and Boyle Franks 1983; Milne et al., 2010) and Twining et al., (2010) 2002; Sedwick et al., 2007; Cullen et al., 2006; Milne et found that Synechococcus cells have higher Ni and Zn al., 2010; Lee et al., 2011), copper (Cu: Bruland and Franks when collected from anticyclone eddies that are stressed 1983; Hanson et al., 1988; Jickells and Burton 1988; by low inorganic N and P, reflecting the heightened need Moffett et al., 1990; Moffett 1995; Milne et al., 2010; for these trace elements to acquire alternate forms of Lee et al., 2011), cobalt (Co: Jickells and Burton 1988; N and P. Cells collected from surface waters overall also Saito and Moffett 2001, 2002; Milne et al., 2010), nickel had much higher Ni than cells collected from the deep (Ni: Bruland and Franks 1983; Jickells and Burton 1988; chlorophyll maximum, reflecting the additional role of Ni Milne et al., 2010), cadmium (Cd: Bruland and Franks in oxidative defense (Twining et al., 2010). Furthermore, 1983; Milne et al., 2010; Lee et al., 2011) and zinc (Zn: the trace elements Co, Cd and Zn are also used in the Milne et al., 2010; Lee et al., 2011), with depletion in the enzyme carbonic anhydrase to acquire and concentrate upper water column reflecting uptake by phytoplankton. cellular CO2. Cyanobacteria, like Prochlorococcus and These nutrient-type trace elements, typically referred Synechococcus have an associated obligate Co requirement to as “micronutrients,” are used by phytoplankton in a (Saito et al., 2002), while some eukaryotic species can variety of enzymes and proteins to accomplish numerous circumvent this issue by interchanging Zn or Cd when one physiological tasks, including macronutrient (N, P, C) of these micronutrients is depleted (Sunda and Huntsman acquisition, oxidative defense, and photosynthesis itself. 1995; Saito and Goepfert 2008). As the phytoplankton

16 Sargasso Sea Alliance – Oceanography of the Sargasso Sea community of the Sargasso Sea is dominated by fluxes in the upper water column lead to short residence Prochlorococcus and Synechococcus, Co is particularly times of Fe in the surface, on the order of days to weeks important here (Saito 2001; Saito and Moffett 2001). (Jickells 1999; Sarthou et al., 2003; Croot et al., 2004; Copper (Cu) in the Sargasso Sea, on the other Weber et al., 2007). Anthropogenic aerosols from North hand, continues to be associated with concern for America contribute trace elements with higher fractional toxicity. The depth profile of Cu at BATS is generally solubility than their counterparts (Sedwick nutrient-type (Bruland and Franks 1983; Hanson et al., et al., 2007; Krishnamurthy et al., 2009; Sholkovitz et al., 1988; Jickells and Burton 1988; Moffett 1995; Milne 2009, 2010). In the case of Fe, recent studies estimate et al., 2010; Lee et al., 2011), with upper water column that anthropogenic dust contributes ~70% of the soluble depletion reflecting the micronutrient role of Cu in Fe deposited to the surface Sargasso Sea near Bermuda oxidative defense and electron transport (Sandmann (Sholkovitz et al., 2009). Anthropogenic sources of Cu et al., 1983; Peers and Price 2006), as well as expected in rain are higher than marine sources (Kieber et al., photochemical processes in superoxide production and 2004), and anthropogenic aerosols have higher fractional Fe cycling (Weber et al., 2005). However, several early solubility of Cu than Saharan dust (Sholkovitz et al., 2010). studies of Cu at BATS have shown that the bioavailable Anthropogenic dust also contributes a significant amount Cu2+ concentrations below the euphotic zone are high of Zn and contaminant elements like vanadium (V), (Hanson et al., 1988; Moffett 1995), exceeding toxicity selenium (Se), chromium (Cr), lead (Pb) and antimony thresholds of phytoplankton (Brand et al., 1986), and (Sb) to the surface Sargasso Sea (Duce and Hoffman may result in toxic levels of Cu2+ in surface waters after 1976; Settle et al., 1982; Chen and Duce 1983; Schaule storm-induced mixing (Moffett 1995). More recently, and Patterson 1983; Boyle et al., 1986; Veron et al., 1994; Mann et al., (2002) found a negative correlation between Wu and Boyle 1997; Arimoto et al., 2003; Connelly et [Cu2+] and Prochlorococcus cell densities in vertical profiles al., 2006; Sedwick et al., 2007; Milne et al., 2010; Lee et at BATS, indicating that variations in [Cu2+] with depth at al., 2011). Atmospheric inputs of mercury to this region BATS have a direct effect on phytoplankton community from anthropogenic environments are significant as structure in the Sargasso Sea. well (Mason et al., 1994, 1998, 2001). As such, metal The primary source of trace elements to the budgets in this region of the North Atlantic Ocean Sargasso Sea is atmospheric, whether in the form of wet have clearly been affected by human activities on the (rain) or dry (dust) deposition. Small surface maxima in surrounding continents. concentrations of Fe, Ni, Co, Zn and manganese (Mn) 3.3. Organic Contaminants in the Sargasso Sea indicate that these micronutrient elements have an atmospheric source (Milne et al., 2010; Lee et al., 2011). A.J. Peters Wet deposition of Fe and Cu are significant inputs of the There have been few studies of organic contaminants in bioavailable forms of these elements to the surface Atlantic seawater or marine biota from the Sargasso Sea. Some (Kim and Church 2001; Kieber et al., 2003, 2004; Willey initial studies in the 1970’s focused on the occurrence of et al., 2004; Witt and Jickells 2005). The bioavailability of petroleum products in the surface ocean, particularly “tar these elements in rain is dependent on peroxide (Willey balls”, which at that time were fairly common owing to et al., 2004) and superoxide (e.g., Weber et al., 2005) the prevailing practices in oil tanker operations (National cycling, which can be highly seasonal (Kieber et al., 2001; Academy of Sciences, 1975). Knap et al., (1980) compared Brooks Avery Jr. et al., 2005). Dry atmospheric aerosols in the quantity of tar balls on beaches in Bermuda during the Sargasso Sea largely originate from Saharan in 1978-79 with that from 1971-72. There was no significant summer and fall, and from urban North America in winter change in the amount during this period, despite a and spring (Duce and Hoffman 1976; Chen and Duce reported decrease in operational discharges from oil 1983; Arimoto et al., 1995, 2003; Moody et al., 1995; tankers over the same period. Huang et al., 1999; Chen and Siefert 2004; Sedwick et al., However, by 1985, Smith and Knap (1985) reported 2007). The distinction between these two aerosol sources a significant decrease in the amount of tar balls washed is important. African dust is higher in bulk Fe with low Fe up on beaches in Bermuda compared with the earlier solubility (Sedwick et al., 2007; Sholkovitz et al., 2009). studies. This decline was attributed to the introduction of The highest bulk dust deposition falls on the Sargasso Sea legislation to reduce discharges of petroleum products by in summer, originating from Saharan Africa (Arimoto et (MARPOL Convention). al., 1995, 2003; Jickells 1999; Moore et al., 2002, 2004; Joyce (1998) reported on floating tar in the Western Prospero et al., 2002), and the resulting high particle North Atlantic and Sea, including the Sargasso

17 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Sea region. The data were derived from 2786 neuston tows appeared to be the same order of magnitude as the input conducted between 1982 and 1996, during which time the of petroleum residues at that time, and the incorporation amount of tar detected was shown to significantly decrease of particulate hydrocarbons into zooplankton faecal over the whole area, though significant amounts were pellets could provide a mechanism for rapid sedimentation still present in the Sargasso Sea in 1996. The decrease in of hydrocarbons through the water column. amount of tar was attributed to “legal and economic forces Requejo and Boehm (1985) characterized hydro- that limit the amount of oil introduced into the ocean”. carbons in a subsurface (c. 250 m) oil-rich layer in the Butler et al., (1998) demonstrated a general correlation Sargasso Sea (centered on 20°N, 55°W). They detected of the occurrence of beach tar in Bermuda with estimated a suite of hydrocarbons with a lower average molecular inputs of petroleum to the North Atlantic Ocean over a mass than that reported for pelagic or stranded tar, and similar time period, 1971-1996. the molecular and isotopic composition consistent with Butler et al., (1998) furthermore suggested that a seep of a fossil hydrocarbon source somewhere on the the quantity of tar washing up on beaches in Bermuda Venezuelan shelf. was time-dependent, and primarily governed by the The contamination of the marine environment mesoscale circulation of the Sargasso Sea. This produces by macro-, micro- and nano-particles of plastic is an alternating periods of upwelling, clean water and area of recent focus. These particles can be ingested by convergences containing floating detritus, including tar, marine organisms and thus displace food in the gut or which is deposited on and removed from beaches on a they can physically the gut, leading to starvation tidal cycle, with resulting residence times of 6 h to a few (Derraik, 2002) and they can also concentrate organic days (Iliffe and Knap, 1979). contaminants in seawater by adsorption to the particle Sleeter and Butler (1982) sampled zooplankton and surface (Teuten et al., 2007), leading to enhanced uptake their faecal pellets from Hydrostation S in the Sargasso of contaminants when the particles are ingested. Moret- Sea in 1979 and determined that the rate of zooplankton Ferguson et al., (2010) analyzed neuston tows from 11 grazing of particulate hydrocarbons in surface waters cruises between , USA and the Caribbean

Figure 3. Sampling locations for plastic particles between 1991–1995 and 2004– 2007 (Moret-Ferguson et al., 2010).

18 Sargasso Sea Alliance – Oceanography of the Sargasso Sea which traversed the Sargasso Sea in the period 1991- the organochlorine pesticide trans-nonachlor; 4-4’-DDE 2007 (Fig. 3). They found significant amounts of particles (a degradation product of the insecticide DDT), and two which were mostly fragments less than 10 mm in size and polychlorinated biphenyl congeners, PCB 138 and PCB less than 0.05 g mass. The particles exhibited signs of 180. Although estimated blood concentrations of these significant mechanical and photochemical degradation, chemicals in the test animals from the vicinity of Bermuda with the mean particle size in samples decreasing from were low, significant oestrogenic activity in their blubber the 1990’s to the 2000’s. was detected, suggesting that they may have been There have been a small number of studies exposed to POP contaminants at biologically relevant undertaken of synthetic organic chemicals and persistent concentrations. Knap and Jickells (1983) reported organic pollutants (POPs) in the Sargasso Sea area. concentrations of PCB’s and trace metals in goose-beaked Knap et al., (1986) measured the flux to the deep whales that stranded and died on Bermuda beaches. ocean of polychlorinated biphenyls (PCBs) and some Other studies have considered the occurrence and organochlorine pesticides as well as studies over the potential effects of contaminants on migratory species that Sargasso Sea by aircraft (Knap and Binkley, 1991). Three are resident in the Sargasso Sea on a seasonal basis and/or studies have determined the levels and significance of for certain life-stages. Larsson et al., (1991) examined the POPs in marine mammals from the Sargasso Sea. Houde uptake of POPs such as DDT and PCBs in the European at al. (2006) measured the levels of PCBs and their eel (Anguilla anguilla) and determined that significant body bio-transformation products, hydroxylated-PCBs (OH- burdens could be accumulated during the eel’s freshwater PCBs) in plasma from two Bottlenose Dolphins from life-stage that would be subsequently depleted during the Bermuda. Levels of both PCBs and OH-PCBs were lower single lifetime occurrence of migration to and spawning in the dolphins from Bermuda than in dolphins from the in the Sargasso Sea. Dickhut et al., (2009) showed that coastal USA, suggesting lower levels of exposure in the differences in the ratios of POPs in Bluefin Tuna (Thunnus open ocean environment. Yordy et al., (2010) used an thynnus) tissue may be used to distinguish between and endocrine screening test to look for oestrogenic activity illustrate mixing of tuna stocks from the North West in dolphin blubber arising from exposure to four POPs: Atlantic and the .

References for Chapter 3

Arimoto, R., Duce, R.A., Ray, Beman, J.M., Chow, C.E., King, Boyle, E. A., Chapnick, S. D., Bruland, K. W., and Franks, R. B.J., Ellis Jr., W.G., Cullen, J.D., A.L., Feng, Y., Fuhrman, J.A., Shen, G. T., and Bacon, M. P., P., 1983. Mn, Ni, Cu, Zn and Cd and Merrill, J.T., 1995. Trace Andersson, A., Bates, N.R., 1986. Temporal variability of lead in the western North Atlantic, p. elements in the atmosphere Popp, B.N., and Hutchins, in the western North-Atlantic. 395–414. In C. S. Wong, E. Boyle, over the North Atlantic. Journal D. A., 2011. Global declines Journal of Geophysical Research— K. W. Bruland, J. D. Burton and E. of Geophysical Research, 100: in oceanic nitrification rates Oceans, 91: 8573–8593. D. Goldberg [eds.], Trace metals in 1199–1213. as a consequence of ocean seawater. Plenum Press. acidification. Proceedings of the Brand, L. E., Sunda, W. Arimoto, R., Duce, R.A., Ray, National Academy of Sciences, 108: G., and Guillard, R. R. L., Butler, J.N., Wells, P.G., Johnson, B.J., and Tomza, U., 2003. Dry 208–213. 1986. Reduction of marine S. and Manock, J.J., 1998. deposition of trace elements phytoplankton reproduction rates Beach tar on Bermuda: Recent to the western North Atlantic. Bender, M. L., and Gagner, C., by copper and cadmium. Journal observations and implications for Global Biogeochemical Cycles, 17: 1976. Dissolved copper, nickel, of Experimental Marine Biology and global monitoring. 10.1029/2001GB001406. and cadmium in Sargasso Sea. Ecology, 96: 225–250. Bulletin, 36, 458–463. Journal of Marine Research 34: Babiker, I.S., Mohamed, M.A.A., 327–339. Brewer, P. G., Spencer, D. W., Capone, D.G., Zehr, J.P., Komaki, K., Ohta, K., and Kato, and Robertson, D. E., 1972. Trace Paerl, H.W., Bergman, K., 2004. Temporal variations in Bibby, T. S., and Moore, C. M., element profiles from GEOSECS- B., and Carpenter, E.J., the dissolved nutrient stocks in 2011. Silicate:nitrate ratios of II test station in Sargasso Sea. 1997. Trichodesmium, a the surface water of the western upwelled waters control the and Planetary Scienc­e Letters, globally significant marine North Atlantic Ocean. Journal of phytoplankton community 16: 111–116. cyanobacterium. Science, 276: Oceanography 60: 553–562. sustained by mesoscale eddies in 1221–1229. sub-tropical North Atlantic and Brooks Avery Jr., G., Cooper, Bates, N.R., and Hansell, D.A., Pacific. Biogeosciences, 8: 657–666. W. J., Kieber, R. J., and Willey, 2004. Temporal variability of J., 2005. Hydrogen peroxide at excess nitrate in the subtropical Boyd, P. W., and Ellwood, M. the Bermuda Atlantic Time-series mode water of the North Atlantic J., 2010. The biogeochemical Station: Temporal variability of Ocean. Marine Chemistry, 84: cycle of iron in the ocean. Nature seawater hydrogen peroxide. 225–241. Geoscience, 3: 675–682. Marine Chemistry, 97: 236–244.

19 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Casey, J., Lomas, M.W., de Baar, H. J. W., Boyd, P. W., Hansell, D. A., Bates, N. R., and Kamykowski, D., 2008. Michelou, V., Orchard, E.D., Coale, K. H., Landry, M. R., Olson, D. B., 2004 Excess nitrate Estimating upper ocean Dyhrman, S.T., Ammerman, Tsuda, A., Assmy, P., Bakker, and nitrogen fixation in the North phosphate concentrations J.W., and Sylvan, J., 2009. D. C. E., Bozec, Y., Barber, R. T., Atlantic Ocean. Marine Chemistry, using ARGO float temperature Phytoplankton taxon-specific Brzezinski, M. A., Buesseler, 84: 243–265. profiles. Deep-Sea Research I, 55: orthophosphate (Pi) and ATP K. O., Boye, M., Croot, P. L., 1580–1589. uptake in the northwestern Gervais, F., Gorbunov, M. Y., Hanson, A.K., Sakamoto- Atlantic subtropical gyre. Aquatic Harrison, P. J., Hiscock, W. T., Arnold, C.M., Huizenga, D.L., Kieber, R. J., Cooper, W. J., Microbial Ecology, 58: 31–44. Laan, P., Lancelot, C., Law, C. S., and Kester, D.R., 1988. Copper Willey, J. D., and Brooks Levasseur, M., Marchetti, A., complexation in Sargasso Sea Avery Jr, G., 2001. Hydrogen Cavender-Bares, K.K., Karl, Millero, F. J. Nishioka, J., Nojiri, and Gulf stream warm-core ring peroxide at the Bermuda D.M., and Chisholm, S.W., Y., Van Oijen, T., Riebesell, U., waters. Marine Chemistry, 23: Atlantic Time series Station. 2001. Nutrient gradients in Rijkenberg, M. J. A., Saito, H., 181–203. Part 1: Temporal variability of the western North Atlantic Takeda, S., Timmermans, K. R., atmospheric hydrogen peroxide Ocean: Relationship to microbial Hastings, M. G., Sigman, D. M., and its influence on seawater Veldhuis, M. J. W., Waite, A. M., and Lipschultz, F., 2003. Isotopic community structure and and Wong, C. S., 2005. Synthesis concentrations. Journal of comparison to patterns in the evidence for source changes of Atmospheric Chemistry, 39: 1–13. of experiments: nitrate in rain at Bermuda. Journal . Deep-Sea Research I, From the Iron Age in the age 48: 2373–2395. of Geophysical Research, 108: Kieber, R. J., Skrabal, S. A., of enlightenment. Journal of ACH4790. Smith, C., and Willey, J. D., Chen, L., and Siefert, R. L., 2004. Geophysical Research—Oceans, 110: 2004. Redox speciation of copper Seasonal and spatial distribution Art. No. C09S16. Hood, R. R., Bates, N. R., in rainwater: Temporal variability and dry deposition fluxes of Capone, D. G., and Olson, D. and atmospheric deposition. Derraik, J.G.B., 2002. The B., 2001. Modeling the effect of atmospheric total and labile iron pollution of the marine Environmental Science & Technology, over the tropical and subtropical nitrogen fixation on carbon and 38: 3587–3594. environment by plastic debris: A nitrogen fluxes at BATS. Deep-Sea North Atlantic Ocean. Journal of review. Marine Pollution Bulletin, 44, Geophysical Research, 109: D09305. Research II, 48: 1609–1648. Kieber, R. J., Willey, J. D., 842–852. and Brooks Avery Jr, G., Huang, S., Rahn, K. A., Arimoto, Chen, L., and Duce., R.A. Dickhut, R.M., Deshpande, 2003. Temporal variability of 1983. The sources of sulfate, R., Graustein, W. C., and rainwater iron speciation at the A.D., Cincinelli, A., Cochran, Turekian, K. K., 1999. Semiannual vanadium and mineral matter in M.A., Corsolini, S., Brill, R.W., Bermuda Atlantic Time Series aerosol particles over Bermuda. cycles of pollution at Bermuda. Station. Journal of Geophysical Secor, D.H. and Graves, J.E., Journal of Geophysical Research, 104: Atmospheric Environment, 17: 2009. Atlantic Bluefin Tuna Research, 108: 3277–3283. 2055–2064. 30309–30318. (Thunnus thynnus) population Kim, G., and Church, T. M., Cianca, A., Helmke, P., Mouriño, dynamics delineated by Houde, M., Pacepavicius, G., 2001. Seasonal biogeochemical B., Rueda, M. J., Llinás, O., organochlorine tracers. Wells, R.S., Fair, P.A., Letcher, fluxes of 234Th and 210Po in the and Neuer, S., 2007. Decadal Environmental Science and R.J., Alaee, M., Bossart, G.D., upper Sargasso Sea: Influence analysis of hydrography and Technology, 43, 8522–8527. Hohn, A.A., Sweeney, J., from atmospheric iron deposition. Solomon, K.R. and Muir, D.C.G., in situ nutrient budgets in the Duce, R. A., and Hoffman, Global Biogeochemical Cycles, 15: western and eastern North 2006. Polychlorinated biphenyls 651–661. G. L., 1976. Atmospheric and hydroxylated polychlorinated Atlantic subtropical gyre. Journal of vanadium transport to the ocean. Geophysical Research, 112: C07025. biphenyls in plasma of Bottlenose Klausmeier, C.A., Litchman, Atmospheric Environment, 10: Dolphins (Tursiops truncatus) from E., Daufresne, T., and Levin, Connelly, D. P., Statham, P. J., 989–996. the Western Atlantic and the Gulf S.A., 2004. Optimal nitrogen- and Knap, A. H., 2006. Seasonal Duce, R. A., Laroche, J., Altieri, of . Environmental Science to-phosphorus stoichiometry changes in speciation of dissolved K., Arrigo, K. R., Baker, A. and Technology, 40, 5860–5866. of phytoplankton. Nature, 429, chromium in the surface Sargasso 171–174. R., Capone, D. G., Cornell, Iliffe, T.M. and Knap, A.H., Sea. Deep-Sea Research I, 53: S., Dentener, F., Galloway, J., 1975–1988. 1979. The fate of stranded pelagic Knap, A.H., Iliffe, T.M. and Ganeshram, R. S., Geider, R. tar on a Bermuda beach. Marine Butler, J.N., 1980. Has the Croot, P. L., Streu, P., and Baker, J., Jickells, T., Kuypers, M. M., Pollution Bulletin, 10:203–205. amount of tar on the open ocean A. R., 2004. Short residence Langlois, R., Liss, P. S., Liu, S. changed in the past decade? time for iron in surface seawater M., Middelburg, J. J., Moore, Jakuba, R. W., Moffett, J. Marine Pollution Bulletin, 11, impacted by atmospheric dry C. M., Nickovic, S., Oschlies, W., and Dyhrman, S. T., 161–164. deposition from Saharan dust A., Pedersen, T., Prospero, 2008. Evidence for the linked events. Geophysical Research Letters, J., Schlitzer, R., Seitzinger, S., biogeochemical cycling of zinc, Knap, A.H., Binkley, K.S. and 31: L23S08. Sorensen, L. L., Uematsu, M., cobalt, and phosphorous in the Deuser, W.G., 1986. Synthetic Ulloa, O., Voss, M., Ward, B., western North Atlantic Ocean. organic chemicals in the deep Cullen, J. T., Bergquist, and Zamora, L., 2008. Impacts Global Biogeochemical Cycles, 22: Sargasso Sea. Nature, 319 572 574. B. A., and Moffett, J. W., of anthropogenic nitrogen on GB4012. 2006. Thermodynamic the open ocean. Science, 320: Knap, A.H. and Binkley, K.S. characterization of the 893–897. Jenkins, W. J., and Doney, S. C., 1991. The occurrence of organic partitioning of iron between 2003. The subtropical nutrient contaminants in the troposphere soluble and colloidal species in the Dyhrman, S. T., Chappell, P. spiral. Global Biogeochemical Cycles, over the North Alantic Ocean as Atlantic Ocean. Marine Chemistry, D., Haley, S. T., Moffett, J. W., 17: 1110. measured by aircraft. Atmospheric 98: 295–303. Orchard, E. D., Waterbury, Environment, 25A (8):1507–1516. J. B., and Webb, E. A., Jickells, T. D., and Burton, J. D., 2006. Phosphonate utilization 1988. Cobalt, copper, manganese Knapp, A. N., Sigman, D. M., by the globally important marine and nickel in the Sargasso Sea. and Lipschultz, F., 2005. N diazotroph Trichodesmium. Nature, Marine Chemistry, 23: 131–144. isotopic composition of dissolved 439: 68–71. organic nitrogen and nitrate at Joyce, P., 1998. Floating tar the Bermuda Atlantic Time-series Gruber, N., and Sarmiento, in the Western North Atlantic Study site. Global Biogeochemical J.L., 1997. Global patterns and , 1982– Cycles, 19: GB1018. of marine nitrogen fixation 1996. Marine Pollution Bulletin, 36, and denitrification. Global 167–171. Biogeochemical Cycles, 11: 235–266.

20 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Krause, J. W., Lomas, M. W., and Lipschultz, F., Bates, N.R., Mcgillicuddy Jr., D. J., Anderson, Moore, J. K., Doney, S. C., Nelson, D. M., 2009a. Biogenic Carlson, C. A., and Hansell, D.A., L. A., Doney, S. C., and Maltrud, Glover, D. M., and Fung, I. Y., silica at the Bermuda Atlantic 2002. New production in the M. E.. 2003. Eddy-driven sources 2002. Iron cycling and nutrient- Time-series Study site in the Sargasso Sea: History and current and sinks of nutrients in the limitation patterns in surface Sargasso Sea: Temporal changes status. Global Biogeochemical Cycles, upper ocean: Results from a 0.1º waters of the World Ocean. Deep- and their inferred controls based 16: 1001. resolution model of the Research II, 49: 463–507. on a 15-year record. Global Atlantic. Global Biogeochemical Biogeochemical Cycles, 23: GB3004. Lomas, M.W., Burke, A.L., Cycles, 17: 1035. Moore, J. K., Doney, S. C., Lomas, D. A., Bell, D.W., and Lindsay, K., 2004. Upper Krause, J., Nelson, D.M., Lomas, Shen, C., Dyhrman, S.T., and Menzel, D. W., and Ryther, J. ocean ecosystem dynamics and M.W., 2009b. Ammerman, J.W., 2010. Sargasso H., 1961. Nutrients limiting the iron cycling in a global three- Biogeochemical responses to Sea phosphorus biogeochemistry: production of phytoplankton in dimensional model. Global late-winter storms in the Sargasso an important role for dissolved the Sargasso Sea, with special Biogeochemical Cycles, 18: GB4028. Sea. II. Increased production organic phosphorus (DOP). reference to iron. Deep-Sea and export of biogenic silica. Biogeosciences, 7: 695–710. Research, 7: 276–281. Morét-Ferguson, S., Law, K.L., Deep-Sea Research I, doi:10.1016/j. Proskurowski, G., Murphy, dsr.2009.1001.1002. Lomas, M.W., Lipschultz, F., Menzel, D. W., and Spaeth, J. E.K., Peacock E.E. and Reddy, Nelson, D. M., Krause, J.W., P., 1962. Occurrence of iron in C.M., 2010. The size, mass, and Krause, J. W., Nelson, D. M., and and Bates, N. R., 2009a. the Sargasso Sea off Bermuda. composition of plastic debris Lomas, M. W., 2010. Production, Biogeochemical responses to Limnology and Oceanography, 7: in the western North Atlantic dissolution, accumulation, and late-winter storms in the Sargasso 155–158. Ocean. Marine Pollution Bulletin, potential export of biogenic silica Sea, I—Pulses of primary and new 60, 1973–1878. in a Sargasso Sea mode-water production. Deep-Sea Research I, Michaels, A. F., and Knap, A. eddy. Liminology and Oceanography 56: 843–860. H., 1996. Overview of the USA National Academy of Sciences 55: 569–579. JGOFS Bermuda Atlantic Time- (1975) Petroleum in the Marine Lomas, M.W., Roberts, N.L., series Study and the Hydrostation Environment, Washington, DC, Krishnamurthy, A., Moore, Lipschultz, F., Krause, J., S program. Deep-Sea Research II, 106 pp. J. K., Mahowald, N., Luo, C., Nelson, D.M., Bates, N.R., 43: 157–198. Doney, S. C., Lindsay, K., and 2009b. Biogeochemical responses Nelson, N. B., Siegel, D. A., and Zender, C. S., 2009. Impacts of to late-winter storms in the Michaels, A. F., Knap, A. H., Yoder, J. A., 2004. The spring increasing anthropogenic soluble Sargasso Sea. IV. Rapid succession Dow, R. L., Gundersen, K., bloom in the northwestern iron and nitrogen deposition on of major phytoplankton groups. Johnson, R. J., Sorensen, Sargasso Sea: spatial extent and ocean biogeochemistry. Global Deep-Sea Research I, 56, 892–908. J., Close, A., Knauer, G. A., relationship with winter mixing. Biogeochemical Cycles 23: GB3016. Lohrenz, S. E., Asper, V. A., Deep-Sea Research II, 51: 987–1000. Lomas, M.W., Swain, A., Tuel, M., and Bidigare, R. R., Larsson, P., Hamrin, S. and Okla, Shelton, R., and Ammerman, 1994. Seasonal patterns of ocean Obernosterer, I., Kawasaki, N., L., 1991. Factors determining the J.W., 2004. Taxonomic variability biogeochemistry at the USA and Benner, R., 2003. P-lim­­ uptake of persistent pollutants in of phosphorus stress in Sargasso JGOFS Bermuda Atlantic Time- itation of respiration in the eel populations (Anguilla anguilla Sea phytoplankton. Limnology and series Study site. Deep-Sea Research Sargasso Sea and uncoupling of L.) Environmental Pollution 69, Oceanography 49: 2303–2310. II, 41: 1013–1038. bacteria from P-regeneration in 39–50. size-fractionation experiments. Mann, E.L., Ahlgren, N., Michelou, V. K., Lomas, M. Aquatic Microbial Ecology, 32: Ledwell, J.R., Mcgillicuddy Moffett, J.W., and Chisholm, W., and Kirchman, D. L., 229–237. Jr., D.J., and Anderson, L.A., S.W., 2002. Copper toxicity 2011. Phosphate and adenosine- 2008. Nutrient flux into an and cyanobacteria ecology in 5’-triphosphate uptake by Peers, G., and Price, N. M., intense deep chlorophyll layer the Sargasso Sea. Limnology and cyanobacteria and heterotrophic 2006. Copper-containing in a mode-water eddy. Deep-Sea Oceanography, 47: 976–988. bacteria in the Sargasso Sea. plastocyanin used for electron Research II, 55: 1139–1160. Limnology and Oceanography, 56: transport by an oceanic diatom. Mason, R. P., Fitzgerald, 323–332. Nature, 441: 341–344. Lee, J.-M., Boyle, E. A., W. F., and Morel, F. M. M., Echegoyen-Sanz, Y., 1994. The biogeochemical Milne, A., Landing, W., Bizimis, Prospero, J. M., Ginoux P., Fitzsimmons, J. N., Zhang, R., cycling of elemental mercury: M. and Morton, P., 2010. Torres, O., Nicholson, S., and and Kayser, R. A., 2011. Analysis Anthropogenic influences. Determination of Mn, Fe, Co, Ni, Gill, T. E., 2002. Environmental of trace metals (Cu, Cd, Pb, Geochimica et Cosmochimica Acta, Cu, Zn, Cd and Pb in seawater characterization of global sources and Fe) in seawater using single 58: 3191–3198. using high resolution magnetic of atmospheric soil dust identified batch nitrilotriacetate resin sector inductively coupled plasma with the NIMBUS 7 Total Ozone extraction and isotope dilution Mason, R. P., Lawson, N. M., mass spectrometry (HR-ICP- Mapping Spectrometer (TOMS) inductively coupled plasma mass and Sheu, G.R., 2001. Mercury MS). Analytica Chimica Acta, 665: absorbing aerosol product. Reviews spectrometry. Analytica Chimica in the Atlantic Ocean: Factors 200–207. of , 40: 1002. Acta, 686: 93–101. controlling air-sea exchange of mercury and its distribution in the Moffett, J. W., 1995. Temporal Requejo, A.G. and Boehm, Li, Q. P., Hansell, D.A., upper waters. Deep-Sea Research II, and spatial variability of copper P.D. (1985) Characterization of Mcgillicuddy Jr., D.J., Bates, 48: 2829–2853. complexation by strong chelators hydrocarbons in a subsurface N.R., and Johnson, R J., in the Sargasso Sea. Deep-Sea oil-rich layer in the Sargasso Sea. 2008. Tracer-bases assessment Mason, R. P., Rolfhus, K. R., and Research I, 42: 1273–1295. Marine Environmental Research, 17, of the origin and biogeochemical Fitzgerald, W. F., 1998. Mercury 45–64. transformation of a cyclonic eddy in the North Atlantic. Marine Moffett, J. W., Brand, L. E., and Chemistry 61: 37–53. Zika, R. G., 1990. Distribution Saito, M. A., 2001. The in the Sargasso Sea. Journal of Biogeography of Cobalt in the Geophysical Research, 113: C10006. and potential sources and sinks of Mather, R., Reynolds, S., Wolff, copper chelators in the Sargasso Sargasso Sea. PhD. MIT/WHOI Lima, I. D., and Doney, S.C., G., Williams, R.G., Torres- Sea. Deep-Sea Research, 37: 27–36. Joint Program. 2004. A three-dimensional, Valdes, S., Woodward, E.M.S., Landolfi, A., Pan, X., Sanders, Moody, J. L., Oltsman, S. J., Saito, M. A., and Goepfert, T. J., multinutrient, and size-structured 2008. Zinc-cobalt colimitation in ecosystem model for the North R.W., and Achterberg, E., Levy, H., and Merrill, J. T.. 2008. Phosphorus cycling in 1995. Transport climatology of Phaeocystis . Limnology and Atlantic. Global Biogeochemical Oceanography, 53: 266–275. Cycles, 18: GB3019. the North and South Atlantic tropospheric ozone: Bermuda, Ocean subtropical gyres. Nature 1988–1991. Journal of Geophysical Lipschultz, F. 2001. A time-series Geosciences 1, 439–443. Research, 100: 7179–7194. assessment of the nitrogen cycle at BATS. Deep-Sea Research II, 48: 1897–1924.

21 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Saito, M. A., and Moffett, J. W., Sholkovitz, E. R., Sedwick, Twining, B. S., Nuñez-Milland, Wu, J., and Boyle, E., 2002. Iron 2001. Complexation of cobalt P. N., and Church, T. M., D., Vogt, S., Johnson, R. J., and in the Sargasso Sea: Implications by natural organic ligands in 2009. Influence of anthropogenic Sedwick, P. N., 2010. Variations for the processes controlling the Sargasso Sea as determined combustion emissions on the in Synechococcus cell quotas of dissolved Fe distribution in the by a new high-sensitivity deposition of soluble aerosol phosphorus, sulfur, manganese, ocean. Global Biogeochemical Cycles, electrochemical cobalt speciation iron to the ocean: Empirical iron, nickel, and zinc within 16: 1086–1093. method suitable for open ocean estimates for island sites in the mesoscale eddies in the Sargasso work. Marine Chemistry, 75: 49–68. North Atlantic. Geochimica et Sea. Limnology and Oceanography, Wu, J., Boyle, E., Sunda, W., and Cosmochimica Acta, 73: 3981– 55: 492–506. Wen, L.S., 2001. Soluble and Saito, M. A., and Moffett, J. 4003. colloidal iron in the oligotrophic W., 2002. Temporal and spatial Van Mooy, B. A. S., Fredricks, North Atlantic and North Pacific. variability of cobalt in the Atlantic Sholkovitz, E. R., Sedwick, P. H. F., Pedler, B. E., Dyhrman, Science, 293: 847–849. Ocean. Geochimica et Cosmochimica N., and Church, T. M., 2010. On S. T., Karl, D. M., Koblizek, Acta, 66: 1943–1953. the fractional solubility of copper M., Lomas, M. W., Mincer, T. Wu, J. F., and Luther III, G. W., in marine aerosols: Toxicity J., Moore, L. R., Moutin, T., 1994. Size-fractionated iron Saito, M. A., Moffett, J. W., of aeolian copper revisited. Rappé, M. S., and Webb, E. A., concentrations in the water Chisholm, S. W., and Waterbury, Geophysical Research Letters, 37: 2009. Phytoplankton in the ocean column of the western North- J. B., 2002. Cobalt limitation and L20601. use non-phosphorus lipids in Atlantic Ocean. Limnology and uptake in Prochlorococcus. Limnology response to phosphorus scarcity. Oceanography, 39: 1119–1129. and Oceanography, 47: 1629–1636. Siegel, D. A., Itturiaga, R., Nature, 458: 69–72. Bidigare, R. R., Smith, R. C., Pak, Wu, J., and Luther III, G. W., Sandmann, G., Reck, H., Kessler, H., Dickey, T. D., Marra, J., and Van Mooy, B. A. S., Rocap, G., 1995. Complexation of Fe (III) E. and Boger, P., 1983. Baker, K. S., 1990. Meridional Fredricks, H. F., Evans, C. T., and by natural organic ligands in the Distribution of plastocyanin and variations of the spring-time Devol, A. H., 2006. Sulfolipids Northwest Atlantic Ocean by a soluble plastidic cytochrome-c in phytoplankton community in the dramatically decrease phosphorus competitive ligand equilibration various classes of algae. Archives of Sargasso Sea. Journal of Marine demand by picocyanobacteria method and a kinetic approach. Microbiology, 134: 23–27. Research, 48: 379–412. in oligotrophic marine Marine Chemistry 50: 159–177. environments. Proceedings of the Sarmiento, J. L., and Gruber, Smith, S.R. and Knap, A.H., Wu, J., and Luther III, G. W., N., 1997. Global patterns National Academy of Sciences, 103: 1996. Spatial and temporal 1985. Significant decrease in 8607–8612. of marine nitrogen fixation the amount of tar stranding on distribution of iron in the surface and denitrification. Global Bermuda. Marine Pollution Bulletin, Véron, A. J., Church, T. M., water of the northwestern Biogeochemical Cycles, 11: 235–266. 16, 19–21. Patterson, C. C., and Flegal, Atlantic Ocean. Geochimica et Cosmochimica Acta, 60: 2729–2741. Sarthou, G., Baker, A. R., A. R., 1994. Use of stable lead Spencer, D. W., and Brewer, P. isotopes to characterize the Blain, S., Achterberg, E. P., G., 1969. Distribution of copper, Wu, J. F., and Boyle, E. A., Boye, M., Bowie A. R., Croot, sources of anthropogenic lead 1997. Lead in the western North zinc and nickel in sea water of in North Atlantic surface waters. P., Laan, P., De Baar, H. J. W., Gulf of and Sargasso Sea. Atlantic Ocean: Completed Jickells, T. D., and Worsfold, Geochimica et Cosmochimica Acta, response to leaded gasoline Geochimica et Cosmochimica Acta, 58: 3199–3206. P. J., 2003. Atmospheric iron 33: 325–339. phaseout. Geochimica et deposition and sea-surface Weber, L., Völker, C., Oschlies, Cosmochimica Acta, 61: 3279–3283. dissolved iron concentrations in Steinberg, D. K., Carlson, C. A., and Burchard, H., 2007. Iron Wu, J. F., and Luther III, G. W., the eastern Atlantic Ocean. Deep- A., Bates, N. R., Johnson, R. J., profiles and speciation of the Sea Research I, 50: 1339–1352. Michaels, A. F., and Knap, A. 1994. Size-fractionated iron upper water column at the concentrations in the water H.. 2001. Overview of the US Bermuda Atlantic Time-series Schaule, B. K., and Patterson, JGOFS Bermuda Atlantic Time- column of the western North- C. C., 1983. Perturbations of the Study site: a model based Atlantic Ocean. Limnology and series Study (BATS): a decade- sensitivity study. Biogeosciences, 4: natural lead depth profile inthe scale look at ocean biology Oceanography, 39: 1119–1129. Sargasso Sea by industrial lead, p. 689–706. and biogeochemistry. Deep-Sea Yordy, J.E., Mollenhauer, M.A.M, 487–503. In C. S. Wong, E. Boyle, Research II, 48: 1405–1447. Weber, L., Völker, C., Schartau, K. W. Bruland, J. D. Burton and E. Wilson, R.M., Wells, R.S., Hohn, M., and Wolf-Gladrow D. A., A., Sweeney, J., Schwacke, D. Goldberg [eds.], Trace metals in Sunda, W. G., and Huntsman, 2005. Modeling the speciation seawater. Plenum Press. S. A., 1995. Cobalt and zinc L.H., Rowles, T.K., Kucklick, and biogeochemistry of iron at J.R. and Peden-Adams, M.M., interreplacement in marine the Bermuda Atlantic Time-series Sedwick, P. N., Sholkovitz, E. R., phytoplankton: Biological and 2010. Complex contaminant and Church, T. M., 2007. Study site. Global Biogeochemical exposure in cetaceans: A geochemical implications. Cycles, 19: GB1019. Impact of anthropogenic Limnology and Oceanography, 40: comparative E-Screen analysis of combustion emissions on the 1404–1407. Willey, J. D., Kieber, R. J., blubber and fractional solubility of aerosol and Brooks Avery Jr, G., mixtures of four persistent organic iron: Evidence from the Sargasso Sweeney, E. N., Mcgillicuddy 2004. Effects of rainwater iron pollutants. Environmental Toxicology Sea. Geochemistry Geophysics Jr., D. J., and Buesseler, K. O., and hydrogen peroxide on iron and Chemistry, 29, 2143–2153. Geosystems, 8: Q10Q06. 2003. Biogeochemical impacts speciation and phytoplankton due to mesoscale eddy activity in growth in seawater near Bermuda. Settle, D. M., Patterson, the Sargasso Sea as measured at C. C., Turekian, K. K., and Journal of Atmospheric Chemistry, the Bermuda Atlantic Time-series 47: 209–222. Cochran, J. K., 1982. Lead Study (BATS). Deep-Sea Research II, precipitation fluxes at tropical 50: 3017–3039. Williams, R. G., Roussenov, oceanic sites determined from V., and Follows, M. J., 210Pb measurements. Journal of Talley, L. and Raymer, M. E., 2006: Nutrient streams and Geophysical Research, 87: 1239– 1982. Eighteen degree water their induction into the mixed 1245. variability. Journal of Marine layer. Global Biogeochemical Research 40: 757–775. Shaw, G.E., 1983. Bio-controlled Cycles, 20, GB1016, thermostasis involving the sulfur Teuten, E.L., Rowland, S.J., doi:10.1029/2005GB002586. cycle. Climatic Change, 5: 297–303. Galloway, T.S., and Thompson, Witt, M., and Jickells, T. R.C., 2007. Potential for 2005. Copper complexation in to transport hydrophobic marine and terrestrial rain water. contaminants. Environmental Atmospheric Environment, 39: Science and Technology, 41, 7759– 7657–7666. 7764.

22 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Chapter 4 Biological Food Webs/BATS

4.1. Oceanic Food Web Overview crustacean grazers (e.g., ciliates), and primary production M.W. Lomas and N.R. Bates is largely recycled through dissolved organic matter and The marine ecosystem is characterized by a number bacteria back to phytoplankton (Pomeroy 1974, Azam of trophic (i.e., nutritional) levels starting with the et al., 1983) with very little carbon sinking into the deep photosynthetic plants, macroalgae and phytoplankton, ocean. In both types of food webs, producer/consumer the animals that graze upon them, zooplankton, and then relationships govern both the composition and fate of multiple higher trophic levels ranging from small schooling particles and the magnitude of the energy and carbon flow. fish such as anchovies on up to apex predators. The More recent research has shown that interactions number and specific members of each trophic level varies both within and between the classical and microbial food with location in the global ocean, but in general there are webs are more complex than originally thought. This fewer trophic levels in highly productive coastal regions research has emphasized the need to consider phenomena and more in the open ocean. In addition, there are fewer like selective grazing by zooplankton, dissolved organic species overall within a given trophic level in cold polar carbon (DOC) production and consumption, and “active than in the warm such as the Sargasso carbon transport” by diel migrators in quantifying Sea. The complex array of processes and pathways that pathways of carbon flow (e.g., Carlson et al., 1994; Dam describe the flow of energy and carbon within and et al., 1995; Lomas et al., 2002; Richardson and Jackson, between these trophic levels in the marine environment 2007; Rivkin et al., 1996; Serret et al., 2001; Steinberg et al., is called a food web. Because of the importance of near- 2000). In addition, satellite observations, in combination shore fisheries as a food source to coastal communities, with directed field work, are being used to shed light on research on how marine food webs function, specifically the temporal and spatial variability of marine what controls their yield, has been conducted from the (Yoder et al., 2010). These new findings continue to late 19th century. The study of the structure and function keep marine food webs an area of active research of open ocean food webs, however is a much younger especially in light of the ecosystem level ‘experiments’ field of study with some of the most exciting advances that are happening associated with ocean warming and in our understanding coming in the past 20 or 30 years. acidification (see section 7 by Bates). These topics and Traditionally, planktonic (i.e., free floating) food others will be discussed in the following sections. web structure has been roughly defined by organism 4.2. Phytoplankton Research in the Sargasso Sea size (Legendre and Lefevre, 1995; Michaels and Silver, 1988) which has led to the paradigm of two distinct M.W. Lomas and N.R. Bates food web types, the classical or “herbivorous” food web Studies on the distribution and abundances of marine and the microbial food web. In the classical food web, phytoplankton have been conducted in the Sargasso Sea large phytoplankton such as diatoms and dinoflagellates from at least the late 1950’s (Hulbert, 1962; Hulbert et dominate photosynthesis (also called primary production al., 1960; Marshall, 1967). These early studies focussed as it is the mechanism by which the majority of organic on what were likely the most abundant groups of micro- matter enters marine food webs), are consumed directly by phytoplankton (micro- meaning 20-200 µm in size) large crustacean zooplankton, which are in turn consumed at that time, namely the diatoms, dinoflagellates and by fish (Steele and Frost, 1977). Some fraction of primary coccolithophorids. These groups were abundant during production is not channeled to fish, but rather sinks into this period of the late 1950’s and early 1960’s in large the deep ocean; this sinking carbon, relative to primary part due to winter nutrient concentrations in the surface production, is termed the biological carbon pump. These ocean that were much higher than has been observed ecosystems are generally highly productive at all trophic over the past two decades. While not known at the levels and tend to occur near to shore or on the continental time, one possible explanation for the elevated nutrient shelf where nutrient inputs are greater. In the microbial concentrations was that the 1960’s were characterized by food web, primary producers are dominated by much a negative phase of the North Atlantic Oscillation (NAO), smaller phytoplankton that are consumed by small non- a dominant climate mode now linked to variability in

23 Sargasso Sea Alliance – Oceanography of the Sargasso Sea phytoplankton and primary production (Bates, 2001; models, phytoplankton biomass and productivity has Lomas et al., 2010a; Lomas and Bates, 2004). During actually increased, not decreased, by ~50% over the past the negative phase of the NAO, winter storms track two decades in the Sargasso Sea due the preferential closer to Bermuda and perhaps with greater frequency growth and accumulation of these small cyanobacteria (Worthington, 1976), resulting in deeper convective over that of microplankton (Lomas et al., 2010a, Fig.4.1). mixing and a greater nutrient flux to the surface ocean. This shift in the dominant groups of phytoplankton Another possible explanation is mesoscale eddies, has had profound implications for the Sargasso Sea food which depending upon the type can increase the flux of web. For example, increasing abundance of cyanobacteria, nutrients to the surface ocean, resulting in the accumulation if anything, should have resulted in a decrease in the of diatom biomass (McGillicuddy et al., 2007) due to oceans ability to sequester carbon in the deep ocean as enhancement of physiological capacity (Krause et al., these cells are not thought to contribute in a meaningful 2010). However, from the 1970’s through the 1990’s the way to the biological carbon pump. However, the strength NAO has trended to a positive phase, which ultimately of the biological carbon pump has actually increased by would reduce nutrient inputs due to convection. Perhaps nearly 50% over the past two decades. This increase in the not unexpectedly, diatom abundance has decreased strength of the biological carbon pump could be related significantly from the late 1980’s through the 1990’s as the to the increase in zooplankton biomass, supported by the result of reduced nutrients overall and suboptimal silica to increased phytoplankton biomass, which has resulted in nitrate ratios in the dissolved nutrient pool (Krause et al., an increase in the zooplankton mediated fluxes of carbon 2009). Data on the other two groups of microplankton are (Steinberg et al., in review). An alternate explanation is that much less common but suggest that absolute abundance these small cyanobacteria can form amorphous organic of dinoflagellates is increasing (Best et al., 2011, Lomas aggregates increasing their effective size and gravitational et al., unpubl. data) while the abundance of coccolithophores settling rates and enhancing their contribution to carbon is largely unchanged (Lomas et al., 2010a). export (Lomas and Moran, 2011). Interestingly, research The importance of microplankton in the 1960’s has shown that some phytoplankton over-produce and was also an artifact of technology; the technology to exude polysaccharide-rich dissolved organic compounds visualize pico-plankton (pico- meaning <2 µm in size) under conditions of ocean acidification (Engel et al., was not common in oceanography at the time. In fact, 2002, Engel 2004), which is currently happening in the the most numerically abundant phytoplankton species on Sargasso Sea (see section 7 below). Regardless, these earth was discovered in the Sargasso Sea only in the mid findings, which are expanded upon in sections below, 1980’s (Chisholm et al., 1988). This species, Prochlorococcus highlight a disconnect between theory and practice marinus, is a photosynthetic marine bacterium that is requiring additional research to understand. ~1 µm in size and was only discovered through the use 4.3. Zooplankton Research in the Sargasso Sea of a state-of-the-art optical instrument called a flow cytometer. Since its discovery, Prochlorococcus, along with D.K. Steinberg another photosynthetic marine bacteria Synechococcus, Zooplankton (mostly small, drifting animals) occupy a is now known to dominate the phytoplankton biomass key position in pelagic food webs, forming a direct link in the nutrient depleted tropical and subtropical oceans between primary producers (phytoplankton) and higher around the globe (e.g., DuRand et al., 2001; Partensky et trophic levels such as fishes, sea birds, and some marine al., 1999). Flow cytometry, when coupled with molecular mammals. Zooplankton grazing plays a key role in the techniques, has also identified a group of similarly sized recycling of all biogenic elements, and export of these organisms called picoeukaryotes which have a very high elements from the upper water column. The zooplankton level of genetic diversity, and hypothesized biogeochemical contain representatives of nearly every animal phyla, and function (Not et al., 2007). Due to their small size, the the abundance of particular taxa can dramatically affect picoplankton are more efficient than their larger relatives cycling and export of nutrients and organic matter. at competing for low nutrient concentrations, however, Zooplankton are food for commercially important fish; because they dominate in low nutrient environments, they for example, in the genus Calanus are the are tightly controlled by small non-crustacean grazers that primary food source for larval and juvenile , one of the rapidly recycle these nutrients through the microbial food most important commercial species in the North Atlantic web with little biomass buildup and sinking of carbon to (Kane, 1984), and zooplankton in subtropical and tropical the ocean interior (see section 4.4. Microbial ecology). environments such as the Sargasso Sea form an important Counter to expectations arrived from these conceptual link to and thus to larger commercial species.

24 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Figure 4.1. Contours of picoplankton abundance (cells ml-1) in the Sargasso Sea from 2004 through 2010 (upper three panels) and their relative contributions to autotrophic organic carbon (bottom panel). The contour plots show the temporal (both seasonal and year-over-year) and spatial (depth) variability of Prochlorococcus, Synechococcus and picoeukaryotes. The two cyanobacterial groups have alternating niches with Prochlorococcus dominating at depth in the summer and Synechococcus competing with the picoeukaryotes to dominate in the surface waters during the winter/spring period. Over time, the combined cyanobacterial carbon biomass has increased significantly at the expense of the picoeukaryotes.

25 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Studies of zooplankton species composition and eddies compared to outside eddies, as was carbon export seasonal dynamics in the Sargasso Sea near Bermuda date both by diel vertical migration and flux of zooplankton back over 60 years (Moore 1949, 1950; Sutcliff 1960; fecal pellets (Goldthwait and Steinberg 2008). Factors Menzel and Ryther, 1961; Beers, 1966; Deevey, 1971; affecting small-scale spatial distribution of zooplankton Deevey and Brooks, 1971; Deevey and Brooks, 1977; in the Sargasso Sea have also been explored, such as the von Bodungen et al., 1982, Wen-tseng and Biggs, 1996, association of small zooplankton with millimeter-size Madin et al., 1996). More recent studies focused on diel colonial phytoplankton (Trichodesmium) (Sheridan et al., or seasonal changes in biomass or community structure 2002), analogous to the associations of shrimp, fish, and and the effects of zooplankton on biogeochemical other organisms with the larger Sargassum seaweed. cycling (Dam et al., 1995; Roman et al., 1993, 1995, Future effort in zooplankton research in the 2002; Steinberg et al., 2000, 2002; Madin et al., 2001; Sargasso Sea should be placed in better characterizing Schnetzer and Steinberg 2002a, b; Steinberg et al., 2004; changes in individual zooplankton species in both the Jiang et al., 2007; Goldthwait and Steinberg 2008, Eden surface/epipelagic community, and establishing a baseline et al., 2009). Changes in zooplankton communities are for deep-sea zooplankton biomass and taxonomic important indicators of the effects of climate change structure (for which we have very little information) to on pelagic ecosystems (Hays et al., 2005; Richardson, which future studies can be compared. A multi-species 2008), and regular sampling for zooplankton biomass and inventory of zooplankton at BATS (established by D. species composition at the Bermuda Atlantic Time-series Steinberg and L. Madin) is available as part of the Census Study (BATS) has been a part of the program from the of Marine Life’s (CoML) Oceanographic Biogeographic beginning (Madin et al., 2001; Steinberg et al., 2001). Information system (OBIS), a repository for global marine The most comprehensive time-series studies species data (http://www.iobis.org/). Analysis of these of seasonal and interannual variation in zooplankton species data has resulted in some significant findings, in the Sargasso Sea is described in Madin et al., (2001) including discovery of seven new species of copepods and recently in Steinberg et al., (submitted in review). (small crustaceans) that have never been recorded in the The latter examines long-term changes in zooplankton Sargasso Sea. Coupled with process studies examining biomass at BATS, and explores possible mechanisms zooplankton grazing and metabolic rates, our ability to driving these changes. During a 16-year period (1994- predict how changing zooplankton community structure 2009) zooplankton biomass increased in surface waters affects nutrient cycling and food webs in the Sargasso Sea by 50% (Steinberg et al., in review). Zooplankton biomass will be enhanced. was positively correlated with sea-surface temperature 4.4. Microbial Ecology in the Sargasso Sea and water column stratification, and was significantly correlated with multi-decadal climate indices—the North S.J. Giovannoni and C.A. Carlson Atlantic Oscillation plus three different Pacific Ocean In the late 1980’s, when molecular biology was first climate indices, indicating tele-connections between conceived of as a solution to understanding how vast climate forcing in the two oceans and ecosystem response. populations of unknown microorganisms function in Resultant changes in biogeochemical cycling included an global cycles, pioneering work began from the deck of increase in carbon export both by diel vertical migration the Weatherbird I in the Sargasso Sea. The Sargasso Sea and flux of zooplankton fecal pellets. The most likely was selected for these early studies because BIOS offered mechanism driving the zooplankton biomass increase is access to one of the largest ecosystems on this planet and a parallel increase in phytoplankton, translating up the an excellent long-term scientific monitoring program. food web into zooplankton. Decreases in zooplankton In 1990, with a homemade Polymerase Chain predators in the Sargasso Sea or displacement of tropical Reaction (PCR) machine, genes were cloned from species northward as a result of ocean warming may also Sargasso Sea environmental DNA that revealed the play a role. existence of the bacterium SAR11, which is widely Other recent efforts have also focused on physical believed to be the most abundant organism on our planet processes that affect spatial distribution of zooplankton in (Giovannoni et al., 1990). SAR11 is now called Pelagibacter. the Sargasso Sea. Mesoscale eddies, on the order of 100- Today we know that this organism is a major player in the 150 km in diameter, significantly affected zooplankton global carbon cycle (Morris et al., 2002). The discovery biomass, community structure, and nutrient cycling of Pelagibacter was followed up with a series of papers (Goldthwait and Steinberg 2008, Eden et al., 2009). that used genetic markers to define many other key Zooplankton biomass was enhanced in certain types of microbial groups that have cosmopolitan distributions in

26 Sargasso Sea Alliance – Oceanography of the Sargasso Sea marine ecosystems (SAR202, SAR86, SAR116, SAR406) continued to reconstruct the “operational priorities” of (Giovannoni et al., 1996, Gordon and Giovannoni 1996, the ocean microbial community by applying advanced Mullins et al., 1995). Worldwide, most marine bacteria mass spectrometry technology to identify important today, particularly elusive, uncultured species that are proteins (Sowell et al., 2009). Also, the tedious task highly abundant, are named and identified using the of reconstructing metabolic pathways from gene lists “SAR” series nomenclature system that emerged from began to fill in details of community function (Tripp et early work at Hydrostation S, southeast of Bermuda. al., 2008). Also in the early 1990’s, Giovannoni’s research The Ocean Microbial Observatory is actively team began to define major patterns in ocean pursuing this research today. Some of its major microbial community structure by merging molecular activities were conceived of by studying genomes and analysis methods with the BATS program. This work microbial communities and using this data to predict showed that ocean microbial communities were highly novel mechanisms of DOC oxidation. This research is stratified between the euphotic zone and dimly lit increasingly becoming interdisciplinary as chemistry upper mesopelagic (“twilight zone”) just beneath it techniques are incorporated into the long-term study to (Giovannoni, et al., 1996; Gordon and Giovannoni, understand the interplay between microbial communities 1996; Mullins, et al., 1995; Wright, et al., 1997). During and the ocean carbon cycle. this period Giovannoni and Carlson, who was studying 4.5. Sediment Traps and Carbon Export the carbon cycle at BATS, began working together and founded the Ocean Microbial Observatory with support M.H. Conte from the National Science Foundation. This long- The Bermuda Time-Series Site, located in the northern term ecological study of bacterioplankton population Sargasso Sea, is one of the most extensively studied dynamics published papers about previously unreported regions in the open ocean and is the site of several seasonal and spatial patterns in bacterioplankton ongoing, complementary time-series measurement distributions and tied them to the carbon cycle. Details programs: the Hydrostation S time-series (1954-present, emerged about the microbial carbon pump, which leads 32°10’N, 64°30’W) of 0-4200m hydrographic properties to the long-term storage of carbon in the ocean interior. (Michaels and Knap, 1996 and references therein); the For example, of DOC accumulating annually at the ocean Oceanic Flux Program (OFP) time-series (1978 to present, surface was found to oxidize when winter storms mixed 31050’N, 64010’W) of deep ocean particle flux (Conte et surface water into the upper mesopelagic (Carlson et al., al., 2001 and references therein); the Bermuda Atlantic 2004). The composition of DOC was shown to change Time-Series Study (BATS) time-series of upper ocean with depth, correlating with shifts in community structure biogeochemical parameters (1989-present, Steinberg (Goldberg et al., 2009, Morris et al., 2005, Treusch et et al., 2001 and references therein); and the Bermuda al., 2009) (Fig. 4.2). The ocean came to be viewed as Testbed Mooring (BTM) time-series of meteorological, a structured microbial ecosystem in which a few dozen physical and optical properties in the 0-650 m water important microbial groups form dynamically changing column (1994-2007, Dickey et al., 2001). Together with communities that catalyze major reactions in geochemical remote sensing products, these time-series are providing a cycles. Studies began of viruses, an important source of uniquely detailed view of the complex interactions among microbial mortality (Angly et al., 2006). Importantly, the the physics, chemistry and biology of the oligotrophic Ocean Microbial Observatory provided the first insights North Atlantic gyre. into how microbial communities would change when Since 1978 the Oceanic Flux Program (OFP) time- global warming caused increasing ocean stratification— series, headed by BIOS faculty member Maureen Conte, has organisms adapted to the extremely low nutrients found continuously measured particle fluxes in the deep Sargasso at the surface in the Sargasso Sea in the summer would Sea. The particle flux, i.e. the transfer of materials from increase their range (Treusch et al., 2009). the surface ocean to the sediments, is a primary process Because of the history of research in the Sargasso controlling the global cycling of elements, the removal of Sea, it was selected by Craig Venter to become the site carbon dioxide from the atmosphere, the food supply that of the world’s first major meta-genomic study (Venter et fuels life in the deep ocean, and the efficiency of cleansing al., 2004). Meta-genomics began providing information the ocean of contaminants. The residual flux material that about how the unknown microbial groups of the “SAR” is preserved in the layers of underlying ocean sediments series function. But, meta-genomics filled in only part further provide a rich record of past ocean conditions that of the story. The BIOS Ocean Microbial Observatory enables us to reconstruct ocean history.

27 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Figure 4.2 Contours of SAR11 ecotype cell densities in the surface 300 m from 2003 through 2005. These contour plots reveal the temporal and spatial (depth) patterns of various ecotypes SAR11 including Ia (a), Ib (b) and II (c). White dashed line represents mixed layer dept and is used to examine distribution patterns in the context of mixing and stratification. Ecotype Ia and Ib are most pronounced in the surface 80m during periods of water column stratification. Ecotype II is most pronounced within the upper mesopelagic zone (140–250m) during or shortly after deep convective mixing. The response of SAR11 Ecotype II at depth is presumably in response to the delivery of surface derived DOM upon deep mixing. Figure adapted from (Carlson et al., 2009).

28 Sargasso Sea Alliance – Oceanography of the Sargasso Sea At more than 33 years duration, the OFP is the with remote sensing data to produce insightful analysis of longest particle time-series of its kind and has produced an processes in the Sargasso Sea. unparalleled record of temporal variability in the deep ocean Studies of ocean optics and the use of remote particle flux on time-scales ranging from weeks to decades. sensing to address science issues in the Sargasso Sea have The OFP has elucidated many of the complex processes been part of the time-series oceanographic research controlling particle flux magnitude and composition and effort since near the beginning of the BATS program. The by virtue of its length, is one of the few programs that can Bermuda Bio-Optics Project (BBOP), started by Dave assess how the particle flux is affected by changes in basin- Siegel (UCSB) and Tony Michaels (BIOS) in 1992, and scale climatic patterns (e.g. ENSO and the North Atlantic now headed by Norm Nelson (UCSB, formerly BIOS), has Oscillation) and ocean chemistry (e.g. ocean acidification). compiled a continuing record of ocean optics properties At the heart of the OFP time-series is a four km that is unprecedented, by piggybacking on BATS cruises. long subsurface mooring fitted with three sediment traps Our researchers and colleagues used optics instruments (500m, 1500m, 3200m depth) to collect settling particles on the Bermuda Testbed Mooring project to study ocean and a current meter/sensor package to monitor deep- processes at one point on the seconds-to-seasons time water currents and physical and chemical properties. scale. In addition to the field campaigns researchers have Samples collected by the OFP sediment traps are studied used remote sensing data, including ocean color, infrared by Conte and collaborators from around the world. Current imagery, and radar altimetry to study processes in the research focuses includes studies of the coupling between region. Selected results of the program are detailed here. deep flux patterns and near surface ocean mesoscale BBOP was started in 1992 with the goal of variability, assessment of the influence of increasing ocean understanding processes controlling light propagation acidification on the deep flux, the influence of hurricane- in the ocean and its interactions with the biological and induced transport of sediment plumes on the deep ocean physical environment (Siegel et al., 1995, Garver and chemistry, investigations on how changing composition Siegel 1997, Morrison and Nelson 2004). Initial results of the particle flux affects deep water ecosystems, and were startling, indicating that a hitherto unstudied development of “proxy” indicators of ocean properties in fraction of chromophoric dissolved organic matter (called support of paleoceanographic research. CDOM) was responsible for much of the variability of The invaluable insights on ocean processes that the underwater light availability (Siegel and Michaels, have resulted from the OFP time-series could not have 1996; Nelson et al., 1998). This discovery led to a broad been realized without the record length and continuity, area of inquiry, including the development of methods and the value of this time-series increases with each new for detecting CDOM from space-borne instruments observation. Advances in ocean and analytical technologies (Siegel et al., 2002), a revolution in understanding the are providing greater context for the flux observations biological control of ocean color (Siegel et al., 2005), and ever more detailed information that is embedded and connections between ocean circulation, CDOM, in the chemistry of the recovered sample material. The and climate (Nelson et al., 2007). The concentration of numerous unresolved questions and hypotheses we have CDOM in the upper water column also mediates the rate regarding the controls on particle flux and how the deep of photochemical reactions, so these results stimulated ocean will change due to anthropogenic forcing can only studies of photochemistry that relates to the cycles of be tested by extending the time-series and protecting the climate relevant gases such as DMS (a climate moderator, region from deleterious activities that could undermine Toole et al., 2008) and greenhouse gases such as carbon the integrity of the Bermuda Time-series site. monoxide (Zafiriou et al., 2008). Remote sensing studies specifically focused on 4.6. Ocean Optics and Remote Sensing of the the Sargasso Sea conducted by our group have included Sargasso Sea a wide range of topics. Remote sensing at BIOS was N.B. Nelson and D.A. Siegel stimulated by the presence of an HRPT satellite receiving Environmental optics, using remote sensing by satellite station (1994-2000) which enabled us to obtain high- or in situ measurements, is an important technique for resolution imagery from old-technology spacecraft understanding the physical, biological, and chemical that could not store global high-res data on board. environment of the ocean using time and space scales We also conducted several projects (some ongoing) that are not accessible using conventional techniques. At to develop and validate new products from remote Bermuda we have pioneered the integration of in situ data sensing data. Data from NOAA’s AVHRR and NASA’s collected as part of the BATS project or related studies SeaWiFS sensor collected at BIOS were used to study

29 Sargasso Sea Alliance – Oceanography of the Sargasso Sea the impact of hurricanes on the Sargasso Sea (Nelson observations made at the BATS site, and the importance 2008, see also Dickey et al., 2008, Nelson 1996), large- of a broad, high quality in situ data set for validating and scale spatial gradients in carbon cycling (Nelson et al., interpreting remote sensing data. 2001) and primary productivity (Nelson et al., 2004). Research on ocean optics carried out in the The importance of mesoscale eddies to productivity and Sargasso Sea is important not only for local but also for carbon cycling was also identified at BATS (Sorenson global oceanographic research. Discoveries at Bermuda and Siegel 2001, Siegel et al., 1999) and has resulted in have stimulated novel oceanographic research not only major research efforts in the Sargasso Sea (Siegel et al., in the Sargasso Sea, but all over the world. Continued 2008) using ocean color, infrared, and radar altimeter research support in the form of collaboration with the remote sensing. Overall the results of remote sensing BATS program will allow us to continue to validate remote investigations of the Sargasso Sea have highlighted sensing data and address new known and unknown the importance of spatial data in terms of interpreting science problems.

References for Chapter 4

Angly, F.E., Felts, B., Breitbart, Carlson, C.A., Giovannoni, Dam, H.G., Roman, M.R. Dickey, T. D., Frye, J., McNeil, M., Salamon, P., Edwards, R.A., S.J., Hansell, D.A., Goldberg, and Youngbluth, M.J., J., Manov, D., Nelson, N., Carlson, C., Chan, A.M., Haynes, S.J., Parsons, R., Vergin, K., 1995. Downward export of Sigurdson, D., Jannasch, H., M., Kelley, S., Liu, H., Mahaffy, 2004. Interactions among respiratory carbon and dissolved Siegel, D., Michaels, A. and J.M., Mueller, J.E., Nulton, J., dissolved organic carbon, microbial inorganic nitrogen by diel-migrant Johnson, R., 1998. Upper Olson, R., Parsons, R., Rayhawk, processes, and community mesozooplankton at the JGOFS ocean temperature response to S., Suttle, C.A., and Rohwer, F., structure in the mesopelagic zone Bermuda time-series station. Deep- as measured by 2006. The marine viromes of four of the northwestern Sargasso Sea. Sea Research, 42, 1187–1197. the Bermuda Testbed Mooring. oceanic regions. Plos Biology 4, (11), Limnology and Oceanography, 49 (4), Monthly Weather Review, 126,1195– 2121–2131. 1073–1083. Deevey, G.B., 1971. The annual 1201. cycle in quantity and composition Azam, F., Fenchel, T., Field, Carlson, C., Ducklow, H., and of the zooplankton of the Sargasso DuRand, M., Olson, R., and J.G., Gray, J.S., Meyer-Reil, Michaels, A., 1994. Annual Sea off Bermuda. I. The upper 500 Chisholm, S., 2001. Phytoplankton L.A., Thingstad, F., 1983. The flux of dissolved organic carbon m. Limnology and Oceanography, 16, population dynamics at the ecological role of water column from the euphotic zone in the 219–240. Bermuda Atlantic Time-series microbes in the sea. Marine Ecology, northwestern Sargasso Sea. Nature, Study station in the Sargasso Sea. 10, 257–263. 371, 405–408. Deevey, G.B. and Brooks, Deep-Sea Research Part II, 48 (8–9), A.L., 1971. The annual cycle in 1983–2003. Bates, N.R., 2001. Interannual Carlson, C. A., Morris, R., quantity and composition of variability of oceanic CO2 and Parsons, R., Treusch, A. H., the zooplankton of the Sargasso Eden, B. R., Steinberg, biogeochemical properties in the Giovannoni, S. J. and K. Vergin Sea off Bermuda. 2. The surface D. K., Goldthwait, S. A., Western North Atlantic subtropical 2009. Seasonal dynamics of to 2000 m. Limnology and and McGillicuddy, D.J., gyre. Deep-Sea Research Part II, 48: SAR 11 populations in the Oceanography, 16, 927–943. 2009. Zooplankton community 1507–1528. euphotic and mesopelagic zones structure in a cyclonic and mode— of the northwestern Sargasso Sea. Deevey, G.B. and Brooks, A.L., water eddy in the Sargasso Sea. Bates, N.R., 2001. Regional ISME Journal, 3:283-295. 1977. Copepods of the Sargasso Deep-Sea Research I, 56: 1757–1776. testbeds: Interannual variability Sea off Bermuda: Species of the oceanic carbon cycle at the Chisholm, S.W., Olson, composition, and vertical and Engel, A., 2004. Distribution USA JGOFS Bermuda Atlantic R.J., Zettler, E.R., Goericke, seasonal distribution between the of transparent exopolymer Time-series Study (BATS) site. R., Waterbury, J.B., and surface and 2000 m. Bulletin of particles (TEP) in the northeast In WOCE International Project Office, Welschmeyer, N.A., 1988. Marine Science, 27, 256–291. Atlantic Ocean and their potential Report of the WOCE/JGOFS A novel free-living Prochlorophyte significance for aggregation Ocean Transport Workshop, abundant in the oceanic euphotic Dickey, T., Zedler, S., Frye, processes. Deep-Sea Research I, 51, WOCE Report No. 174/2001, zone. Nature, 334 (6180), 340– D., Jannasch, H., Manov, D., 83–92. pp. 43–46. 343. Sigurdson, D., McNeil, J. D., Dobeck, L., Yu, X., Gilboy, T., Engel, A., Goldthwait, S., Passow, Beers, J. R., 1966. Studies on Conte, M., Ralph, N., and Ross, Bravo, C, Doney, C.S., Siegel, D.A. U., Alldredge, A., 2002. Temporal the chemical composition of the E., 2001. Seasonal and interannal and Nelson, N. 2001: Physical and decoupling of carbon and nitrogen major zooplankton groups in variability in the deep ocean biogeochemical variability from dynamics in a mesocosm diatom the Sargasso Sea off Bermuda. particle fluxes at the Oceanic hours to years at the Bermuda bloom. Limnology and Oceanography, Limnology and Oceanography, 11, Flux Program (OFP)/Bermuda Testbed Mooring: June 1994– 47, 753–761. 520–528. Atlantic Time-series (BATS) site March 1998. Deep-Sea Research, II in the western Sargasso Sea near 48, 2105–2140. Best, C., Purdie, D., and Lomas, Bermuda. Deep-Sea Research II, 48, M.W., 2011. Temporal dynamics of 1471–1506. microplankton in the Sargasso Sea. American Society of Limnology and Oceanograpy 2011 Meeting, San Juan , Puerto Rico.

30 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Galloway J.N., Townsend A.R., Kane, J., 1984.­­ The feeding habits Mather, R., Reynolds, S., Wolff, Nelson, N.B., Bates, N.R., Erisman J.W., Bekunda M., Cai of co-occuring cod and G., Williams, R.G., Torres-Valdes, Siegel, D.A., and Michaels, A.F., Z.C., Freney J.R., Martinelli, larvae from . Marine S., Woodward, E.M.S., Landolfi, 2001: Spatial variability of the CO2 Seitzinger S.P., and Sutton Ecology Progress Series, 16, 9–20. A., Pan, X., Sanders, R.W., and sink in the Sargasso Sea. Deep-Sea M.A. Transformation of the Achterberg, E., 2008. Phosphorus Research II, 48, 1801–1821. nitrogen cycle: Recent trends, Krause, J., Lomas, M., and cycling in the North and South questions, and potential solutions. Nelson, D., 2009. Biogenic Atlantic Ocean subtropical gyres. Nelson, N.B., D.A. Siegel, and Science, 320 Issue: 5878 Pages: silica at the Bermuda Atlantic Nature Geosciences 1, 439–443. A.F. Michaels, 1998: Seasonal 889–892. Time-series Study site in the dynamics of colored dissolved Sargasso Sea: Temporal changes McGillicuddy, D.J., Anderson, L., material in the Sargasso Sea. Deep- Garver, S.A., and Siegel, D.A., and their inferred controls based Bates, N.R., Bibby, T., Buesseler, Sea Research I, 45, 931–957. 1997: Inherent optical property on a 15-year record. Global K.O., Carlson, C., Davis, C.S., inversion of ocean color Biogeochemical Cycles, 23, GB3004, Ewart, C., Falkowski, P.G., Nelson, N.B., 1998: Spatial and spectra and its biogeochemical doi:3010.1029/2008GB003236. Goldthwait, S.A., Hansell, D., temporal extent of sea surface interpretation: I. Time series Jenkins, W.J., Johnson, R., temperature modifications by from the Sargasso Sea. Journal of Krause, J., Nelson, D., and Kosnyrev, V.K., Ledwell, J., Li, Q., hurricanes in the Sargasso Sea Geophysical Research, 102, 18,607– Lomas, M., 2010. Production, Siegel, D., and Steinberg, D.K., during the 1995 season. Monthly 18,625. dissolution and potential export 2007. Eddy/Wind interactions Weather Review, 126:1364–1368. of biogenic silica in a Sargasso Sea stimulate extraordinary mid-ocean Giovannoni, S., Rappe, mode-water eddy. Limnology and Nelson, N.B., 1996: The wake of plankton blooms. Science, 316, Hurricane Felix. International Journal M., Vergin, K., and Adair, Oceanography, 55, 569–579. 1021–1025. N., 1996. 16S rRNA genes of Remote Sensing. 17: 2893–2895. Legendre, L. and Lefevre, J., reveal stratified open ocean Menzel, D.W. and Ryther, J.H., Nelson, N.B., D.A. Siegel, bacterioplankton populations 1995. Microbial food webs and 1961. Zooplankton in the Sargasso the export of biogenic carbon in C.A. Carlson and C.M. related to the green non-sulfur Sea off Bermuda, and its relation Swan, 2010: Tracing global bacteria phylum. Proceedings of the oceans. Aquatic Microbial Ecology, to organic production. Journal 9, 69–77. biogeochemical cycles and National Academy of Sciences, 93, du Conseil Permanent International meridional overturning circulation 7979–7984. Lomas, M., Bates, N., Knap, pour l’Exploration de la Mer, 26, using chromophoric dissolved 250–258. Goldberg, S., Carlson, C., A., Karl, D., Lukas, R., Landry, organic matter, Geophysical Hansell, D., Nelson, N., and M., Bidigare, R., Steinberg, D., Michaels, A.F., and Silver, M.W., Research Letters, 37, L03610, Siegel, D., 2009. Temporal and Carlson, C., 2002. Refining 1988. Primary production, sinking doi:10.1029/2009GL042325. dynamics of dissolved combined our understanding of ocean fluxes, and the microbial food web. biogeochemistry and ecosystem Nelson, N.B., Siegel, D.A., neutral sugars and the quality of Deep-Sea Research, 35, 473–490. Carlson, C.A., Swan, C., Smethie dissolved organic matter in the functioning. EOS, 83, 559–561. Mills, M.M., and Arrigo, K.R. Jr., W.M., and Khatiwala, Northwestern Sargasso Sea. Deep- Lomas, M., Steinberg, D., S., 2007: Hydrography of Sea Research I, 56, 672–685. 2010. Magnitude of oceanic Dickey, T., Carlson, C., Nelson, nitrogen fixation influenced chromophoric dissolved organic Goldthwait, S. A., and Steinberg, N., Condon, R., and Bates, N., by the nutrient uptake ratio of matter in the North Atlantic. D.K., 2008. Elevated Biomass of 2010a. Increased ocean carbon phytoplankton. Nature Geoscience, Deep-Sea Research, 54, 710–731. Mesozooplankton and Enhanced export in the Sargasso Sea is 3, 412–416. countered by its enhanced Nelson, N.B., Siegel, D.A., and Fecal Pellet Flux in Cold-Core and Yoder, J.A., 2004: The spring Mode-Water Eddies in the Sargasso mesopelagic attenuation. Moore, H.B., 1949. The Biogeosciences, 7, 57–70. zooplankton of the upper waters bloom in the northwestern Sea. Deep-Sea Research II, 55 (10– Sargasso Sea: Spatial extent and 13): 1360–1377. of the Bermuda area of the North Lomas, M.W., and Bates, N.R., Atlantic. Bulletin of the Bingham relationship with winter mixing. Gordon, D., and Giovannoni, 2004. Potential controls on Oceanographic Collection, 12 (2), Deep-Sea Research, 51, 987–1000. S., 1996. Stratified microbial interannual partitioning of organic 97 pp. carbon during the winter/spring Nelson, N.B., Carlson, C.A., populations related to Chlorobium and Steinberg, D.K., 2004: and Fibrobacter detected in the phytoplankton bloom at the Moore, H.B., 1950. The relation Bermuda Atlantic Time-series between the scattering layer and Production of chromophoric Atlantic and Pacific oceans. Applied dissolved organic matter by and Environmental Microbiology, 62, Study (BATS) site. Deep-Sea the Euphausiacea. Biological Bulletin, Research Part I, 51 (11), 1619–1636. Woods Hole, 99, 181–212. Sargasso Sea microbes. Marine 1171–1177. Chemistry, 89, 273–287. Hays, G. C., Richardson, A. J. Lomas, M.W., and Moran, S.B., Morris, R.M., Vergin, K.L., 2011. Evidence for aggregation and Cho, J.C., Rappe, M.S., Carlson, Not, F., Gausling, R., Azam, F., and Robinson, C., 2005. Climate Heidelberg, J., and Worden, change and marine plankton, export of cyanobacteria and nano- C.A., and Giovannoni, S.J., eukaryotes from the Sargasso Sea 2005. Temporal and spatial A.Z., 2007. Vertical distribution Trends in Ecology and Evolution, of picoeukaryotic diversity in 20(6), 337–344. euphotic zone. Biogeosciences, 8, response of bacterioplankton 203–216. lineages to annual convective the Sargasso Sea. Environmental Hulbert, E., 1962. Phytoplankton overturn at the Bermuda Atlantic Microbiology, 9, 1233–1252. Madin, L.P., P. Kremer and S. in the southwestern Sargasso Sea Time-series Study site. Limnology Partensky, F., Hess, W., and Hacker (1996) Distribution and Oceanography, 50 (5), and north equatorial current, Vaulot, D., 1999. Prochlorococcus, a and vertical migrations of salps 1687–1696. February, 1961. Limnology and marine photosynthetic prokaryote Oceanography, 7, 307–315. (Tunicata, Thaliacea) near Bermuda. Journal of Plankton Morrison, J.R., and Nelson, of global significance. Microbiology Hulbert, E., Ryther, J., and Research, 18, 747–755. N.B., 2004: Seasonal cycle of and Molecular Biology Reviews, 63, Guillard, R., 1960. The phytoplankton UV absorption 106–127. Madin, L. P., E. F. Horgan, and D. at the Bermuda Atlantic Time- phytoplankton of the Sargasso Pomeroy, L., 1974. The ocean’s K. Steinberg (2001), Zooplankton series Study site. Limnology and Sea of Bermuda. Journal du Conseil food web, a changing paradigm. at the Bermuda Atlantic Time- Oceanography, 49, 215–224. Permanent International pour BioScience 24, 499–504. l’Exploration de la Mer, 25, 115–128. series Study (BATS) station: Mullins, T., Britschgi, T., diel, seasonal and interannual Richardson, T., and Jackson, G., Krest, R., and Giovannoni, S., Jiang, S., Dickey, T. D., variation in biomass, 1994–1998, 2007. Small phytoplankton and 1995. Genetic comparisons Steinberg, D. K., and Madin, L. Deep-Sea Research Part II, 48(8–9), carbon export from the surface reveal the same unknown P., 2007. Temporal variability of 2063–2082. ocean. Science 315, 838–840. zooplankton biomass from ADCP lineages in Atlantic and Pacific backscatter time series data at the Marshall, H., 1967. bacterioplankton communities. Richardson, A. J., 2008. In hot Bermuda Testbed Mooring site. Coccolithophores in the northwest Limnology and Oceanography, 40, water: zooplankton and climate Deep-Sea Research I, 54: 608–636. Sargasso Sea. Limnology and 148–158. change, ICES Journal of Marine Oceanography, 370–376. Science, 65 (3), 279–295.

31 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Rivkin, R.B., Legendre, L., Deibel, Siegel, D.A., Maritorena, S., Sowell, S., Wilhelm, L., Treusch, A.H., Vergin, K., Finlay, D., Tremblay, J.E., Klein, B., Nelson, N.B., Behrenfeld, M.J. Norbeck, A., Lipton, M., L., Donatz, M., Burton, R., Crocker, K.M., Roy, S., Silverberg, and McClain, C.R., 2005: Colored Nicora, C., Barofsky, D., Carlson, C., and Giovannoni, N., Lovejoy, C., Mesple, F., dissolved organic matter and Carlson, C., Smith, R., and S., 2009. Seasonality and vertical Romero, N., Anderson, M., its influence on the satellite- Giovanonni, S., 2009. Transport structure of microbial communities Matthews, P., Savenkoff, C., and based characterization of the functions dominate the SAR11 in an ocean gyre. Isme Journal, 3, Grant Ingram, R., 1996. Vertical ocean biosphere. Geophysical metaproteome at low-nutrient 1148–1163. flux of biogenic carbon in the Research Letters, 32, L20605, extremes in the Sargasso Sea. Isme ocean: Is there food web control? doi:10.1029/2005GL024310. Journal, 3, 93–105. Tripp, H., Kitner, J., Schwalbach, Science, 272, 1163–1166. M.S., Dacey, J.W.H., Wilhelm, L., Siegel, D.A., Maritorena, S., Steele, J., Frost, B., 1977. The and Giovannoni, S., 2008. SAR11 Roman, M.R., Dam, H.G., Nelson, N.B., Hansell, D.A., structure of plankton communities. marine bacteria require exogenous Gauzens, A.L. and Napp, J.M Lorenzi-Kayser, M., 2002. Global Philosophical Transactions of the reduced sulphur for growth. (1993) Zooplankton biomass and distribution and dynamics of Royal Society of London Series B— Nature, 452, 741–744. grazing at the JGOFS Sargasso colored dissolved and detrital Biological Sciences, 280, 485–534. Sea time series station. Deep-Sea organic materials. Journal of Venter, J.C., Remington, K., Research, 40, 883–901. Geophysical Research, 107, 3228, Steinberg, D., Lomas, M., and Heidelberg, J.F., Halpern, A.L., doi:10.1029/2001JC000965. Cope, J., 2012. Long-term increase Rusch, D., Eisen, J.A., Wu, D.Y., Roman, M.R., Caron, D.A., in mesozooplankton biomass Paulsen, I., Nelson, K.E., Nelson, Kremer, P., Lessard, E.J., Madin, Siegel, D.A., Doney, S.C. and in the Sargasso Sea: Linkage to W., Fouts, D.E., Levy, S., Knap, L.P., Malone, T.C., Napp, J.M, Yoder, J.A., 2002: The spring climate and implications for food A.H., Lomas, M.W., Nealson, K., Peele, E.R., and Youngbluth, bloom of phytoplankton in web dynamics and biogeochemical White, O., Peterson, J., Hoffman, M.J., 1995. Spatial and temporal the North Atlantic Ocean cycling. Global Biogeochemical Cycles, J., Parsons, R., Baden-Tillson, changes in the partitioning of and Sverdrup’s critical depth 26, GB 1004, doi:10.1029/2010 H., Pfannkoch, C., Rogers, Y.H., organic carbon in the plankton hypothesis. Science, 296, 730–733. GB 004026. Smith, H.O., 2004. Environmental community of the Sargasso Sea genome shotgun sequencing of off Bermuda. Deep-Sea Research, 42, Siegel, D.A., Nelson, N.B., Steinberg, D.K., Nelson, N.B., the Sargasso Sea. Science, 304 973–992. O’Brien, M.C., Westberry, T.K., Carlson, C.A., and Prusak, (5667), 66–74. and others, 2001 The Bermuda A.C., 2004: Production of Roman, M.R., Adolf, H.A., BioOptics Project: Bio-optical chromophoric dissolved organic Von Bodungen, B., Jickells, Landry, M.R., Madin, L.P., modeling of primary production matter (CDOM) in the open ocean T., Smith, S., Ward, J., Hillier, Steinberg, D.K., and Zhang, from space-sensible variables. by zooplankton and the colonial G., 1982. The Bermuda Marine X. 2002. Estimates of oceanic Deep-Sea Research II 48, 1865– cyanobacterium Trichodesmium. Environment Volume III. Bermuda mesozooplankton production: A 1896. Marine Ecology Progress Series, 267, Biological Station for Research, comparison using the Bermuda 45–56 Inc., St. George’s, p. 123. and Hawaii time-series data. Deep- Siegel, D.A., Fields, E. and Sea Research II, 49: 175–192. McGillicuddy Jr., D.J., Steinberg, D. K., Carlson, C. Wen-tseng, L. and Biggs, D. 1999. Mesoscale motions, satellite A., Bates, N. R., Johnson, R. J., C., 1996. Temporal variability Schnetzer, A., and Steinberg, altimetry and new production Michaels, A. F., and Knap, A. in the night-time distribution of D. K., 2002a. Natural diets of in the Sargasso Sea. Journal of H., 2001. Overview of the US epipelagic siphonophores in the vertically migrating zooplankton Geophysical Research, 104, 13359– JGOFS Bermuda Atlantic Time- North Atlantic Ocean at Bermuda. in the Sargasso Sea, Marine Biology, 13379. series Study (BATS): a decade- Journal of Plankton Research, 18, 141(1), 89–99. scale look at ocean biology and 923–939. Siegel, D.A., and Michaels, biogeochemistry, Deep-Sea Research Schnetzer, A., and Steinberg, A.F., 1996. Quantification of Part II, 48(8–9), 1405–1447. Worthington, L.V., 1976. On the D. K., 2002b. Active transport of non-algal light attenuation in North Atlantic circulation. The John particulate organic carbon and the Sargasso Sea: Implications Steinberg, D.K., Goldthwait, Hopkins Oceanography Studies, 6, nitrogen by vertically migrating for biogeochemistry and remote S.A., and Hansell, D.A., 1–110. zooplankton in the Sargasso Sea, sensing. Deep-Sea Research II, 43, 2002. Zooplankton vertical Marine Ecology-Progress Series, 234, 321–345. migration and the active transport Wright, T., Vergin, K., Boyd, P., 71–84. of dissolved organic and inorganic and Giovannoni, S., 1997. A novel Siegel, D.A., Michaels, A.F., nitrogen in the Sargasso Sea. Deep- delta-subdivision proteobacterial Serret, P., Fernandez, R., Anadon, Sorensen, J., O’Brien, M.C., and Sea Research I, 49: 1445–1461. lineage from the lower ocean R., and Varela, M., 2001. Trophic Hammer, M.A., 1995. Seasonal surface layer. Applied and control of biogenic carbon export variability of light availability and Sutcliffe, W. H. J., 1960. On Environmental Microbiology, 63, in Bransfield and Gerlache Straits, its utilization in the Sargasso Sea. the diversity of the 1441–1448. Antarctica. Journal of Plankton Journal of Geophysical Research, 100, population in the Sargasso Sea of Research, 23, 1345–1360. 8695–8713. Bermuda. Ecology, 42, 585–587. Yoder, J., Doney, S., Siegel, D., Wilson, C., 2010. Study of marine Sheridan, C.C., Steinberg, D.K., Sorensen, J.C., and D.A. Siegel, Toole, D.A., and Siegel, D.A., ecosystems and biogeochemistry and Kling, G.W. 2002. The 2001: Variability and models of 2004: Light-driven cycling now and in the future: examples microbial and metazoan the effective quantum yield of of dimethylsulfide (DMS) of the unique contributions from community associated with carbon assimilation in the Sargasso in the Sargasso Sea: closing space. Oceanography, 23, 104–117. colonies of Trichodesmium spp.: Sea, Deep-Sea Research II, 48, the loop. Geophysical Research a quantitative survey. Journal of 2005–2035. Letters, 31, L09308, DOI: Zafiriou, O.C., Xie, H., Nelson, Plankton Research, 24(9): 913–922. 10.1029/2004GL019581. N.B., Najjar, R.G., and Wang, Steinberg, D.K., Carlson, C. W., 2008. Diel Siegel, D.A., Court, D.B., A., Bates, N.R., Goldthwait, Toole, D.A., Kieber, D.J., Kiene, cycling in the upper Sargasso Menzies, D.W., Peterson, P., S.A, Madin, L.P., and Michaels, R.P., Siegel, D.A. and Nelson, Sea near Bermuda at the onset Maritorena, S. and Nelson, A.F., 2000. Zooplankton vertical N.B. 2003: Photolysis and the of spring and in midsummer. N.B., 2008: Satellite and in situ migration and the active transport dimethylsulfide (DMS) summer Limnology and Oceanography, 53, observations of the bio-optical of dissolved organic and inorganic paradox in the Sargasso Sea. 835–850. signatures of two mesoscale eddies carbon in the Sargasso Sea. Deep- Limnology and Oceanography, 48, in the Sargasso Sea. Deep-Sea Sea Research I, 47, 137–158. 1088–1100. Research Part II, 55, 1218–1230.

32 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Chapter 5 Biogeochemical cycles in the Sargasso Sea

5.1. Marine Biogeochemical Cycles in the (a reduction in the potential for vertical exchange). Sargasso Sea Over the past 57 years, observations at Hydrostation N.R. Bates and M.W. Lomas S have shown significant warming of the surface ocean (~0.1ºC decade-1) and reorganization of the global The global ocean is responding to environmental hydrological cycle as evidenced by an increase in ocean change that includes warming, changes in the water salinity (~0.02 decade-1) in the upper ~300 m. Although (or hydrological) cycle and ocean nutrient availability the warming and increase in salinity may seem small, (e.g., Boyce et al., 2010) that controls the growth and they have large impacts on the Sargasso Sea as a whole, accumulation of phytoplankton which in turn form the with complex feedbacks and interactions thus making base of the . The response of marine it more difficult in the long term to entrain nutrients ecosystems and the biogeochemistry of important from depth. elements such as carbon and oxygen, and nutrient The global ocean nutrient cycles that support compounds to environmental changes demands detailed the marine food web also appear to be impacted by observations and improvements in understanding of the human activities, climate-related physical processes, and important physical, chemical and biological processes a very dynamic marine nitrogen and phosphorus cycle. that control them. A critical component for investigating For example, the inputs of anthropogenic nutrients to change in marine ecosystems and biogeochemistry is the the coastal ocean (e.g., Galloway et al., 2008) and fixed network of time-series observations in the global ocean. nitrogen to the open ocean (via atmospheric deposition) In the open-ocean, time-series observations in the are expected to increase (e.g., Duce et al., 2008; Seitzinger subtropical North Atlantic Ocean off Bermuda (i.e., the et al., 2010). Ocean warming appears to be increasing Sargasso Sea) and in the North Pacific Ocean off Hawaii stratification of the surface ocean potentially reducing comprise the two longest running studies of marine nutrient supply and the rates of phytoplankton primary biogeochemistry and the responses of the ocean to production globally (Boyce et al., 2010). However, there environmental changes. In the Sargasso Sea, the ocean are complex and counteracting processes that control the time-series, Hydrostation ‘S’ (1954 to present) and the physical supply nutrients to the surface ocean thereby Bermuda Atlantic Time-series Study (BATS; 1988 to influencing the global ocean nutrient cycles (e.g., Williams present), provide critically needed data on the time- et al., 2006; Cianca et al., 2007; Wong et al., 2007; Di varying fluxes and sequestration of carbon and nutrients Lorenzo et al., 2009; Steinhoff et al., 2010; Canfield et al., over the last few decades and more importantly the 2010). The marine nitrogen cycle is very dynamic, with controls on marine biogeochemistry. One measure of for example, complex linkages between eutrophication, the impact of the BATS program is the strong publication nutrients and carbon (e.g., Chen and Borges, 2009; record resulting from this research. The cumulative Borges and Gypens, 2010). Recent studies in the Sargasso publications and technical references for these programs Sea indicate that the potential rate of nitrification of since 1988, now exceed 500 articles, with an average of ammonia is declining with ocean acidification (Beman et ~20 publications per year since BATS sampling started in al., 2011), while the significance of global oceanic nitrogen 1988 (Fig. 5; Appendix III). fixation, especially in the Sargasso Sea, is highly debated The basic hydrographic properties of seawater, (e.g., Michaels et al., 1996; Gruber and Sarmiento, 1997; temperature and salinity, control the density of seawater Hansell et al., 2004; Bates and Hansell 2004; Hansell and ultimately vertical exchange processes in the global et al., 2008; Gruber, 2008). Many of these processes ocean. This control of vertical exchange has important impact one nutrient biogeochemical cycle, nitrogen or implications for the Sargasso Sea, as it is the deeper phosphorus, more than the other, resulting in potentially ocean waters that contain the nutrients required to large deviations from the canonical Redfield Ratio, which support the surface sunlit ocean ecosystem. Over the defines not only the relative concentrations of inorganic last twenty years, temperature and salinity in the upper nitrate and phosphate in the deep ocean, but also which ocean layers of the subtropical gyre at BATS has increased nutrient limits primary production. The Sargasso Sea is significantly with concurrent increases in stratification already characterized by a ratio of inorganic nitrate and

33 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Figure 5. Statistics of scientific publications arising from research conducted in the Sargasso Sea from 1978 to present. (A) Cumulative number of publications (red line), and the number of different first authors (dark blue circles) and institutions (light blue circles) in each year. (B) Publications within each year divided into the seven ‘disciplinary’ categories listed in the legend. Statistics are current through June 2011.

34 Sargasso Sea Alliance – Oceanography of the Sargasso Sea phosphate that is much higher than the canonical Redfield plants that allow them to rapidly adapt to a changing Ratio, but the response of phytoplankton and their environment. A critical question is just how adaptable control over this ratio of available nutrients is currently are these phytoplankton, and if they cannot adapt to being challenged (e.g., Mills and Arrigo, 2010). a changing ocean, will they be lost from the ocean’s As mentioned above, primary production has been genomic library as the ocean climate changes. Datasets increasing in the Sargasso Sea over the past decade or like those generated at BATS are forcing oceanographers more. While this may seem at odds with the lack of increase to rethink our understanding of natural processes in the in nutrient inputs, a likely explanation is the utilization global ocean and how this information is assimilated into of different nutrient forms, namely dissolved organic attempts to predict the future state of the ocean. nutrients. Specifically, it is dissolved organic phosphorus 5.2. The Global Ocean Carbon Cycle and (DOP) that has been hypothesized to support over 50% Observations in the Sargasso Sea of primary production in both the western and eastern North Atlantic Ocean (Lomas et al., 2010b; Mather et N.R. Bates al., 2008; Torres-Valdes et al., 2009), although the source On societally relevant timescales (e.g., decades to centuries), regions for DOP, and the complex processes which lead the global ocean sequesters large quantities of carbon to its net production, appear to be different between the dioxide (CO2) from the atmosphere. Photosynthetic western and eastern North Atlantic Ocean. In addition fixation of CO2 into particulate matter and production to the use of DOP to support primary production, the of calcium carbonate (CaCO3) by calcifying marine particulate nutrient ratio, nitrogen:phosphorus, has phytoplankton, coupled with the subsequent downward steadily increased relative to the Redfield Ratio over transfer via settling of particles and biologically mediated the past ~7 years. This is consistent with the increasing processes represents an important export of carbon. importance of marine cyanobacteria (see section 4.2 These processes are collectively termed the ocean Phytoplankton research) which are known to have ratios biological carbon pump and it sequesters carbon into the greater than Redfield, as well as the observation that deep ocean on the timescale of the global overturning ocean acidification conditions results in a still further circulation (hundreds to thousands of years) e.g., Broecker increase in the particulate nitrogen:phosphorus ratio and Peng, 1982; Gruber and Sarmiento, 2002. The in marine cyanobacteria (e.g., Fu et al., 2007). These reservoir of carbon in the global ocean is approximately observations might also explain the increased carbon 60-70 times greater than that of the atmosphere. As such, flux associated with the increase in cyanobacteria in the even a small change in the ocean reservoir of carbon has Sargasso Sea via the COP/SS hypothesis (Carbon Over a significant impact on the atmospheric concentration of

Production/Species Shift hypothesis; Lomas, Andersson CO2 and the response of the climate system to the release and Bates, unpubl. data). This combination of DOP of anthropogenic (i.e., human produced) CO2. utilization and changes in elemental stoichiometry in At present, the global ocean sequesters about response to changes in species and/or ocean acidification 25% of anthropogenic CO2 in the atmosphere, with would comprise a negative feedback loop on increasing the total amount of anthropogenic carbon sequestered carbon dioxide in the upper ocean. in the ocean estimated at ~120-140 Pg (Pg = 1015 g) All of these changes in the Sargasso Sea, while of carbon (e.g., Sabine et al., 2004; Khatiwala et al., presented individually, are inextricably interconnected 2009). The global ocean uptake of CO2 is estimated at within the ecosystem (a field of scientific study called ~1.4 to 2.5 Pg C per year (e.g., Takahashi et al., 2002, ocean biogeochemistry) and often lead to non-intuitive 2009; Manning and Keeling, 2006), with the ocean results. One such outcome is the increase in biological uptake increasing with time (e.g., Le Quéré et al., 2009) fixation of CO2 by single cell plants (phytoplankton) as the amount of anthropogenic CO2 released to the and the associated increases in their abundance. As atmosphere has increased (Friedlingstein et al., 2010). mentioned earlier, the Sargasso Sea is warming and it is Thus, the sequestration of CO2 into the global ocean becoming more difficult—on longer timescales—to bring is one of the primary mechanisms that controls the critical nutrients from the deep ocean to the surface that concentrations of CO2 in the lower atmosphere and the phytoplankton require to grow, and thus it is puzzling impact of human produced CO2 on the climate system that ocean phytoplankton been able to become more (IPCC, 1990, 2001, 2007). abundant. In part, it is due to shifts in the large diversity Understanding the time-varying magnitude and and relative abundances of these phytoplankton, but it is controlling dynamics underlying the sequestration also due to substantial changes in the physiology of these of carbon requires a detailed study of the biological,

35 Sargasso Sea Alliance – Oceanography of the Sargasso Sea geological and chemical processes that control the vertical and horizontal mixing, biological production, transfer of carbon across the air-sea interface and into the diurnal warming/cooling, and storm events (e.g., Bates et deep ocean. Superimposed on long-term decadal trends al., 2002; Gruber et al., 2002; Dore et al., 2003; Keeling in ocean sequestration of CO2 are large regional, seasonal et al., 2004; Brix et al., 2004). Interpretation of oceanic and inter-annual variations in CO2 uptake that reflects CO2 time-series data is further complicated by variability changes in temperature, ocean primary production, imparted by spatial heterogeneity in the ocean as a ocean and atmosphere circulation that respond to result of mesoscale and sub-mesoscale phenomena (e.g., natural and human induced climate variability such as the McGillicuddy et al., 2007), and meridional and zonal El Niño-Southern Oscillation (ENSO), Pacific-Decadal physical gradients. Oscillation Antarctic Annular Oscillation and North Long-term observations at the BATS site also Atlantic Oscillation (e.g., Gruber et al., 2002; Bates et indicate that the salinity normalized DIC (nDIC) of al., 2002; Feely et al., 2006, Bates, 2007, Le Quéré et al., surface and deeper water layers have increased at 2009; section 7.1). A critical component for investigating divergent rates over time since water-column sampling the present and future role of CO2 on the climate system began in 1988 (Bates et al., 2002; Gruber et al., 2002). is the network of time-series observations in the global In deeper subtropical mode waters (STMW), the mean ocean, with observations collected in the Sargasso Sea rate of change of nDIC (1988-2001) was significantly constituting the longest record. higher than surface waters, increasing at a rate of 2.2 ± Although quite a few open-ocean and coastal 0.26 µmoles kg-1 year-1 (Bates et al., 2002). The STMW ocean CO2 time-series have been initiated, only four of the North Atlantic Ocean is formed each winter by time-series sites are of sufficient length to evaluate cooling and convective mixing at the northern edges of longer-term inter-annual trends globally. These are: (1) the subtropical gyre south of the Gulf Stream (Klein and BATS (Bermuda Atlantic Time-series Study), located Hogg, 1996; Hazeleger and Drijfhout, 1998). The shallow near Bermuda (32°10’N, 64°30’W) in the NW Atlantic depths of the subtropical gyre (~250-400m deep) are Ocean (2) Hydrostation S, (32°50’N, 64°10’W) located ventilated during STMW formation and the STMW layer near Bermuda in the NW Atlantic Ocean, (3) ALOHA (A is found throughout the subtropical gyre. This water mass Long-term Oligotrophic Habitat Assessment) or HOT is classically defined by temperatures ranging from 17.8° site, located near Hawaii (22°45’N, 158°W) in the North to 18.4°C, by a salinity of ~36.5 ± 0.05, and by a minimum Pacific Ocean; and; (4) ESTOC (European Station for in the vertical gradient of potential density (or isopycnic Time-series in the Ocean (ESTOC), located potential vorticity) (Klein and Hogg, 1996; Jenkins, 1998; near in the NE Atlantic Ocean. Hanawa and Talley, 2001; Alfutis and Cornillon, 2001). The

These long-term observations at several ocean non-conservative increase of CO2 does not result from time-series show upward trends of dissolved inorganic remineralization of organic matter or density variability, carbon (DIC) and seawater pCO2 due to the uptake of but rather, weak wintertime mixing and lack of STMW anthropogenic CO2 (e.g., Bates, 2001; Bates et al., 2002; re-ventilation, which appear associated with an NAO Dore et al., 2003; Keeling et al., 2004; Brix et al., 2004; positive phase (Bates et al., 2002; Gruber et al., 2002).

Bates, 2007; Santana-Casiano et al., 2007; Dore et al., Since 1988, ~0.6-2.8 Pg (1015 g) of CO2 has accumulated 2009; Gonzalez-Davila et al., 2010). The anticipated rate within the gyre STMW, representing a long-term oceanic of change in surface ocean CO2 due to the accumulation sink of CO2 (>10 years). The accumulation of CO2 in of anthropogenic CO2 in the atmosphere and the STMW should continue until winters with stronger mixing surface ocean buffer factor (assuming that near-surface (associated with a NAO negative phase) entrain STMW waters in the subtropical gyres have residence times long CO2 into surface waters, ultimately releasing CO2 to the enough to equilibrate entirely with the anthropogenic atmosphere. Inter-annual variability in the uptake of CO2 perturbation in atmospheric CO2) can be theoretically into STMW thus provides another factor and feedback calculated. An equilibrium rate of dissolved inorganic controlling the global ocean uptake of CO2. carbon (DIC) increase due to anthropogenic CO2 of +0.9 5.3. Calcium Carbonate Production µmoles kg-1 yr-1 was calculated for the subtropical gyres including the Sargasso Sea (Bates et al., 2002; Gruber and N.R. Bates

Sarmiento, 2002). Any assessment of long-term trends in Production of calcium carbonate (CaCO3) by calcifying oceanic CO2 is complicated by large seasonal variability marine phytoplankton such as coccolithophores, pteropods of the inorganic carbon cycle due to processes such as and foraminfera also contributes substantively to carbon seasonal temperature, salinity, and density changes, export to the deep ocean. Extensive coccolithophore

36 Sargasso Sea Alliance – Oceanography of the Sargasso Sea blooms in other regions of the global ocean (e.g., Bering classes of phytoplankton, coccolithophores can increase

Sea, , off Iceland) can significantly impact the seawater pCO2 content and thus contribute to a negative ocean carbon cycle (e.g., Robertson et al., 1994; Bates et al., coccolithophore-CO2 feedback (Riebesall et al., 2000; 1996a; Murata and Takizawa, 2002; Murata, 2006; Harley Zondervan et al., 2001; Ridgewell et al., 2007) that et al., 2010). In the Sargasso Sea, episodic coccolithophore has potentially important implications for the role of blooms have been observed (Brown and Yoder, 1994) the global ocean in the uptake of anthropogenic CO2, accompanied by significant decreases in ocean alkalinity modulation of atmospheric CO2 and climate responses observed (Bates et al., 1996b). Unlike other taxonomic over the next few centuries.

References for Chapter 5

Alfutis., M.A., and Cornillon Bates, N.R., and Peters, A.J., Brix, H., Gruber, N., Keeling, C.D., Doney, S.C., 2006. The dangers P., 2001. Annual and interannual 2007. The contribution of Bates, N.R., Le Quéré, C., and of ocean acidification. Scientific changes in the North Atlantic atmospheric acid deposition McKinley, G., 2004. Interannual American, March 2006, 58–65. STMW layer properties. Journal to ocean acidification in the variability and trends in the of Physical Oceanography, 31, subtropical North Atlantic Ocean. oceanic carbon cycle: From HOT Doney, S.C., Mahowald, N., Lima, 2066–2086. Marine Chemistry, 107, 547–558. and BATS to the Subtropical Gyre. I., Feely, R.A., Mackenzie, F.T., AGU Ocean Science Meeting, Lamarque, J.-F., Rasch, P.J., 2007. Bates, N.R., 2001. Interannual Bates, N.R., Michaels, A.F., and February 2004. The impact of anthropogenic changes of oceanic CO2 and Knap, A.H., 1996a. Seasonal atmospheric nitrogen and sulfur biogeochemical properties in the and interannual variability of the Broecker, W.S., and Peng, T-H., deposition on ocean acidification Western North Atlantic subtropical oceanic carbon dioxide system at 1982. Tracers in the Sea. Eldigio and the inorganic carbon system. gyre. Deep-Sea Research II, 48(8–9), the USA JGOFS Bermuda Atlantic Press Palisades , 690 pp. Proceedings of the National Academy 1507–1528. Time-series Site. Deep-Sea Research of Sciences, 104 (37), 14580–14585. II, 43(2–3), 347–383. Brown, C.W., and Yoder, J.A., Bates, N.R., 2002. Interannual 1994. Coccolithophorid blooms Dore, J.E., Lukas, R. Sadler, D.W. variability in the global ocean Bates, N.R., Michaels, A.F., and in the global ocean. Journal of and Karl, D.M., 2003. Climate- uptake of CO2. Geophysical Research Knap, A.H., 1996b. Alkalinity Geophysical Research, 99, 7467– driven changes to the atmospheric Letters. changes in the Sargasso Sea: 7482. CO2 sink in the subtropical North Geochemical evidence of Pacific Ocean. Nature, 424, Bates, N.R., 2002. Seasonal calcification? Marine Chemistry, 51 Canfield, D.E., Glazer, A.N., 754–757. variability of the effect of coral (4), 347–358, doi:10.1016/0304– and Falkowski, P.G., 2010. The reefs on seawater CO2 and air- 4203(95)00068–2. evolution and ’s Dore, J.E., Lukas, R., Sadler, D.W., sea CO2 exchange. Limnology and nitrogen cycle. Science, 330, Church, M.J., and Karl, D.M., Oceanography, 47 (1), 43–52. Bates, N.R., Pequignet, A.C., 192–196. 2009. Physical and biogeochemical Johnson, R.J., and Gruber, N. modulation of ocean acidification Bates, N.R., 2007. Interannual 2002. A short-term sink for Chen, C.T.A., and Borges, A.V., in the central North Pacific. variability of the oceanic CO2 2009. Reconciling opposing views atmospheric CO2 in subtropical Proceedings of the National Academy sink in the subtropical gyre of mode water of the North Atlantic on carbon cycling in the coastal of Sciences, 106, 12235–12240, the North Atlantic Ocean over Ocean Nature, 420 (6915), 489– ocean: continental shelves as sinks doi:10.1073/pnas.0906044106. the last two decades. Journal of 493, doi:10.1038/nature01253. and near-shore ecosystems as Geophysical Research (Oceans), sources of atmospheric CO2. Deep- Duce, R.A., LaRoche, J., Altieri, doi:10.1029/2006JC003759. Beman, J.M., Chow, C.-E., King, Sea Research II, 56, 578–590. K., Arrigo, K.R., Baker, A.R., A.L., Feng, Y., Fuhrman, J.A., Capone, D.G., Cornell, S., Bates, N.R., and Hansell, D.A., Andersson, A., Bates, N.R., Cianca, A., Helmke, P., Mourino, Dentener, F., Galloway, J., 1999. A high resolution study Popp, B.N., and Hutchins, D.A., B., Rueda, M.J., Llinás, O., and Ganeshram, R.S., Geider, R.J., of surface layer hydrographic 2011. Global declines in oceanic Neuer, S., 2007. Decadal analysis Jickells, T., Kuypers, M.M., and biogeochemical properties nitrification rates as a consequence of hydrography and in situ nutrient Langlois, R., Liss, P.S., Liu, between and of ocean acidification. Proceedings budgets in the western and eastern S.M., Middelburg, J.J., Moore, Bermuda. Marine Chemistry, of the National Academy of Sciences, North Atlantic subtropical gyre. C.M., Nickovic, S., oschlies, 67, 1–16, doi:10.1016/S0304– 108(1), 208–213, doi: 10.1073/ Journal of Geophysical Research, 112, A., Pedersen, T., Prospero, 4203(99)00045–6. pnas.1011053108. doi:10.1029/2006JC003788. J., Schlitzer, R., Seitzinger, S., Bates, N.R., and Hansell, D.A., Di Lorenzo, E., Cobb, K.M., Sorensen L.L., Uematsu, M., Borges, A.V. and Gypens, M., Ulloa, O., Voss, M., Ward, B., 2004. Temporal variability of 2010: Carbonate chemistry in Furtado, J.C., Schneider, excess nitrate in the Subtropical N., Anderson, B.T., Bracco, and SAmora, L., 2008, Impacts the coastal zone responds more of atmospheric anthropogenic Mode Water of the North Atlantic strongly to eutrophication than A., Alexander, M.A., and Ocean. Marine Chemistry, 84, Vimont, D.J., 2009: Nutrient nitrogen on the open ocean. ocean acidification. Limnology Science, 320: 893–897. doi: 225–241. Oceanography, 55, 346–353. and salinity decadal variations in the central and eastern 10.1126/science.1150369. Boyce, D.G., Lewis, M.R., North Pacific. Geophysical and Worm, B., 2010. Global Research Letters, 36, L14601, phytoplankton decline over the doi:10.1029/2009GL038261. past century. Nature, 466 591–596.

37 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Feely, R.A., Takahashi, T., Hanawa, K., and Talley, L.D., Jenkins, W.J., 1998, Studying McGillicuddy, D.J., Anderson, L., Wanninkhof, R., McPhaden, 2001. Mode waters. In Ocean subtropical thermocline ventilation Bates, N.R., Bibby, T., Buesseler, M.J., Cosca, C.E., Sutherland, Circulation and Climate (G. Siedler, and circulation using tritium and K.O., Carlson, C., Davis, C.S., S.G., and Carr, M.E., 2006. J. Church and J. Gould, Editors), 3He. Journal of Geophysical Research, Ewart, C., Falkowski, P.G., Decadal variability of the air- Academic Press, San Diego, 103, 15817–15831. Goldthwait, S.A., Hansell, D., sea CO2 fluxes in the equatorial International Geophysics Series, Jenkins, W.J., Johnson, R., Pacific Ocean. Journal of volume 77, pp. 373–386. Keeling, C.D., Brix, H., and Kosnyrev, V.K., Ledwell, J., Li, Q., Geophysical Research—Oceans Gruber, N., 2004. Seasonal and Siegel, D., and Steinberg, D.K., 111 (C08), C08S90, doi: Hansell, D.A., Bates, N.R., and Long-term dynamics of the upper 2007. Eddy/Wind interactions 10.1029/2005JC003129. Olson, D.B., 2004. Excess nitrate ocean carbon cycle at Station stimulate extraordinary mid-ocean and nitrogen fixation in the North ALOHA near Hawaii. Global plankton blooms. Science, 316, Friedlingstein, P., Houghton, Atlantic Ocean. Marine Chemistry, Biogeochemical Cycles, 18, GB4006, 1021–1025. R.A., Marland, G., Hackler, 84 (3–4), 243–265, doi:10.1016/ doi:10.1029/ 2004GB002227. J., Boden, T.A., Conway, T.J., j.marchem.2003.08.004. Michaels, A.F., Olson, D., Canadell, J.G., Raupach, M.R., Khatiwala, S., Primeau, F, and Sarmiento, J.L., Ammerman, Ciais, P., and Le Quere, C., Hansell, D.A., Olson, D.B., Hall, T., 2009. Reconstruction J.W., Fanning, K., Jahnke, R., Dentener, F., and Zamora, L.M., of the history of anthropogenic 2010. Update on CO2 emissions. Knap, A.H., Lipschultz, F., and Nature Geoscience, 3, 811–812. 2008. Assessment of excess nitrate CO2 concentrations in the ocean. Prospero, J.M., 1996. Inputs, development in the subtropical Nature, 462: 346–349. losses and transformations of Fu, F., Warner, M.E., Zhang, North Atlantic. Marine Chemistry, Klein, B., and Hogg N., 1996. On nitrogen and phosphorus in the Y., Feng, Y., and Hutchins, 106, 562–579. pelagic North Atlantic Ocean. D.A., 2007. Effects of increased the interannual variability of Harley, J., Borges, A.V., Van Der 18 Degree Water formation Biogeochemistry, 35, 181–226. temperature and CO2 on photosynthesis, growth, and Zee, C., Delille, B., Godi, R.H.M., as observed from moored Mills, M.M., and Arrigo, K.R. elemental ratios in marine Schiettecatte, L.-S., Roevros, instruments at 55°W. Deep-Sea 2010. Magnitude of oceanic Synechococcus and Prochlorococcus N., Aerts, K., Plapernat, P.-E., Research, 43, 1777–1806. nitrogen fixation influenced (Cyanobacteria). Journal of Rebreanu, L., Groom, S., Daro, by the nutrient uptake ratio of M.-H., Van Grieken, R., and Le Quéré, C., Raupach, M.R., Phycology, 43, 485–496. Canadell, J.G., Marland, G., et phytoplankton. Nature Geoscience, Chou, L., 2010. Biogeochemical 3, 412–416. Galloway, J.N., Townsend, A.R., study of coccolithophore bloom al., 2009. Trends in the sources Erisman, J.W., Bekunda, M., in the northern and sinks of carbon dioxide. Nature Murata A, and Takizawa Cai, Z.C., Freney, F.R., Martinelli, (NE Atlantic Ocean) in June Geosciences, 2, 831–836. T., 2002. Impact of a L.A., Sietzinger, S.P., and Sutton, 2004. Progress in Oceanography, Lomas, M.W., Burke, A., Lomas, coccolithophorid bloom on the M.A., 2008: Transformation of 86, 317–336, doi: 10.1016/j. D., Shen, C., Bell, D., Dyhrman, CO2 system in surface waters the nitrogen cycle: Recent trends, pocean.23010.04.029. S.T., and Ammerman, J.W., of the eastern shelf. questions, and potential solutions. Geophysical Research Letters, 29 (11), Hazeleger, W., and Drifjhout, 2010b. Sargasso Sea phosphorus Science, 320, 889–892, doi: biogeochemistry: an important Art. No. 1547. 10.1126/science.1136674. S.S., 1998. Mode water variability in a model of the subtropical gyre: role for dissolved organic Murata A, 2006. Increased phosphorus (DOP). Biogeosciences González-Dávila M., Santana- response to atmospheric forcing. surface seawater pCO2 in the Casiano, J.M., and Gonzalez- Journal of Physical Oceanography, 28, 7, 695–710. eastern Bering Sea shelf: an effect Davila, E.F., 2007. Interannual 266–288. Lomas, M.W., and Moran, S.B., of blooms of coccolithophorid variability of the upper ocean 2011. Evidence for aggregation and Emiliania huxleyi. Global carbon cycle in the northeast IPCC, 1996. Climate Change Biogeochemical Cycles, GB4006, doi: 1995: The science of climate change, export of cyanobacteria and nano- Atlantic Ocean. Geophysical eukaryotes from the Sargasso Sea 10.1029/2005GB002615. Research Letters, 34, L07608, Contribution of working group I to the Second Assessment Report of the euphotic zone. Biogeosciences, 8, Quay, P., 2002. Ups and downs of doi:10.1029/2006GL028145. 203–216. intergovernmental Panel on Climate CO2 uptake. Science, 298, 2344. González-Dávila, M., Santana- Change. Houghton, J. T., Meiro McGillicuddy, D.J., Anderson, L., Casiano, J.M., Rueda, M.J., Filho, L. G., Callander, B. A., Harris, Ridgwell, A., Zondervan, I., Bates, N.R., Bibby, T., Buesseler, Hargreaves, J.C., Bijma, J., and and Llinás, O., 2010. The N., Kattenberg, A., and Maskell, K., K.O., Carlson, C., Davis, C.S., water column distribution of eds, Cambridge University Press, Lenton T.M., 2007. Assessing Ewart, C., Falkowski, P.G., the potential Long-term increase carbonate system variables at Cambridge, 572 p. Goldthwait, S.A., Hansell, D., the ESTOC site from 1995 to of oceanic fossil fuel CO2 uptake IPCC, 2001. Climate change Jenkins, W.J., Johnson, R., due to CO -calcification feedback. 2004. Biogeosciences, 7, 3067–3081, Kosnyrev, V.K., Ledwell, J., Li, Q., 2 doi:10.5194/bg–7–3067–2010. 2001: The scientific basis, Biogeosciences 4(4), 381–492. Contribution of Working Group Siegel, D., and Steinberg, D.K., Gruber, N. 2008. The marine I to the Third Assessment Report 2007. Eddy/Wind interactions Riebesell, U., I. Zondervan, B. nitrogen cycle: overview and of the Intergovernmental Panel on stimulate extraordinary mid-ocean Rost, P.D. Tortell, P.D., Zeebe, challenges. In Nitrogen in the Climate Change. Houghton, J. T., plankton blooms. Science, 316, R.E., and Morel, F.M.M., Marine Environment, (Capone, D.G., Ding, Y., Griggs, D. J., Noguer, 1021–1025. 2000. Reduced calcification of marine plankton in response D.A. Bronk, M.R. Mulholland, M., van der Linden, P. J., Dai, X., Manning, A.C., and Keeling,. E.J. Carpenter, eds.) Academic, Maskell, K., and Johnson, C. A., to increased atmospheric CO2. R.F., 2006. Global oceanic and Nature, 407, 364–367. Burlington, MA pp. 1–50. eds., Cambridge University Press, land biota sinks from the Scripps Cambridge, 881 p. Gruber, N., and Sarmiento, J.L., atmospheric oxygen flask sampling Robertson, J.E.,Turner, D.R., 2002. Biogeochemical Physical IPCC, 2007. Climate Change network, Tellus, 58B, 95–116. Holligan, P., Watson, A.J., Boyd, P., Fernandez, E., and Interactions in Elemental Cycles, 2007: The Physical Science Basis. Mather, R., Reynolds, S., Wolff, in The Sea: Biological-Physical Contribution of Working Group I to Finch, M., 1994. The impact G., Williams, R.G., Torres-Valdes, of a coccolithophore bloom on Interactions in the Ocean, edited the Fourth Assessment Report of the S., Woodward, E.M.S., Landolfi, by A. R. Robinson, J. J. McCarthy, Intergovernmental Panel on Climate oceanic carbon uptake in the A., Pan, X., Sanders, R.W., and Northeast Atlantic during summer & B.J. Rothschild, John Wiley Change. Solomon, S., D. Qin, M. Achterberg, E., 2008. Phosphorus and Sons, New York, Volume 12, Manning, Z. Chen, M. Marquis, 1991. Deep-Sea Research I, 41, cycling in the North and South 297–315. 337–399. K.B. Avery, M. Tignor and H.L. Atlantic Ocean subtropical gyres. Miller (eds.), Cambridge University Nature Geosciences 1, 439–443. Gruber, N., Bates, N.R., and Press, Cambridge, Keeling, C.D., 2002. Long-term and New York, NY, USA, 996 p. observations of interannual variability in the North Atlantic carbon sink. Science, 298, 2374– 2378.

38 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Sabine, C.L., Feely, R.A., Gruber, Spokes, L.J., and Jickells, T.D., Takahashi, T., Sutherland, S.C., Williams, R. G., V. Roussenov, N., Key, R.M., Lee, K., Bullister, 2005. Is the atmosphere really Wanninkhof, R., Sweeney, C., and M. J. Follows, 2006: Nutrient J.L., Wanninkhof, R., Wong, an important source of reactive Feely, R.A., Chipman, D.W., streams and their induction C.S., Wallace, D.W.R., Tilbrook, nitrogen to coastal waters? Hales, B., Friederich, G.E., into the mixed layer. Global B., Millero, F.J., Peng, T.-H., Research 25 (16), Chavez, F.P., Watson, A.J., Biogeochemical Cycles, 20, GB1016, Kozyr, A., Ono, T., and A.F. Rios, 2022–2035. Bakker, D.C.E., Schuster, U., doi:10.1029/2005GB002586. A.F., 2004. The oceanic sink for Metzl, N., Yoshikawa-Inoue, Steinhoff, T, Friedrich, T., Wong, C.S., L. Xie, Hsieh, anthropogenic CO2. Science, 305, H., Olafsson, J., Arnarson, T.S., 367–371. Hartman, S.E., Oschlies, A., Tilbrook, B., Johannessen, T., W.W., 2007. Variations in Wallace, D.W.R., and Kortzinger, Olsen, A., Bellerby, R.J., de nutrients, carbon and and other Santana-Casiano, J.M., A., 2010: Estimating mixed layer Baar, H.J.W., Nojiri, Y., Wong, hydrographic parameters related Gonzalez-Davila, M., Rueda, nitrate in the North Atlantic C.S., Delille, B., and Bates, N.R., to the 1976/77 and 1988/89 M.-J., Llinas, O., and Gonzalez- Ocean. Biogeosciences, 7, 795–807 2009. Climatological mean and regime shifts in the sub- Davila, E.-F., 2007. The doi:10.5194/bg–7–795–2010. decadal change in surface ocean Northeast Pacific, Progress in interannual variability of Oceanography, 75, 326–342. pCO2, and net sea-air CO2 flux oceanic CO parameters in the Takahashi, T., Sutherland, S.G., 2 Sweeney, C., Poisson, A.P., Metzl, over the global oceans. Deep-Sea Zondervan, I., Zeebe, R. E., Rost, western Atlantic subtropical Research II, (in press). gyre at the ESTOC site. Global N., Tilbrook, B., Bates, N.R., B, and Riebesell, U., 2001. Biogeochemical Cycles, 21, GB1015, Wanninkhof, R.H., Feely, R.A., Torres-Valdes, S., Rousseau, Decreasing marine biogenic doi:10.1029/2006GB002788. Sabine, C.L., and Olafsson, J., V., Sanders, R.W., Reynolds, S., calcification: a negative feedback 2002. Biological and temperature Pan, X., Mather, R., Landolfi, A., on rising atmospheric pCO2. Global Seitzinger S. P., Mayorga, E., effects on seasonal changes of Wolff, G., Achterberg, E., and Biogeochemical Cycles, 15, 507–516. Bouwman, A.F., Kroeze, C., pCO2 in global ocean surface Williams, R., 2009. Distribution Beusen, A.H.W., Billen, G., Van waters. Deep-Sea Research II, 49, of dissolved organic nutrients and Drecht, G., Dumont, E., Fekete, 1601–1622. their effect on export production B.M., Garnier, J., and Harrison, over the Atlantic Ocean. Global J.A., 2010: Global nutrient Biogeochemical Cycles 23, GB4019, export: A scenario analysis of doi:4010.1029/2008GB003389. past and future trends. Global Biogeochemical Cycles, 24, GB0A08 doi:10.1029/2009GB003587.

CHapter 6 Air-Sea Interactions

6.1. Climate variability, NAO/ENSO Influences which is a tripolar oscillation between the North Pacific and on the Subtropical Gyre North Atlantic, centered over the Arctic region (Visbeck et N.R. Bates al., 2001). The NAO has significant effects on climate and Variability in the marine carbon cycle and ocean carbon atmospheric variability. Strong eastward airflow between sources and sinks has been studied most thoroughly in the Iceland Low and carries storms towards the tropical Pacific Ocean in connection with the El Niño western from North America. If the NAO index Southern Oscillation (ENSO). El Niño-La Niña changes is negative, storm tracks are thought to shift southward, have profound impacts on weather and climate globally. cooling surface waters, enhancing 18°C mode water By contrast, little is known about the contribution of formation and deepening winter mixed layers (Rodwell the subtropical and subpolar gyres to atmospheric et al., 1999). In , for example, there is an

CO2 variations, despite the fact that these gyres cover increase in winter storms and precipitation during these more than half of the world’s ocean. Natural climate periods. During positive NAO winters, westerlies that phenomena, such as the North Atlantic Oscillation usually prevail in the region between and (NAO) and the Arctic Oscillation (AO) also have strong Hatteras (west of the Azores High) weaken. Reduced wind regional (particularly in Europe) and global impacts on stress and heat exchange leads to the development of weather and climate. warm temperature anomalies in the subtropical gyre (e.g., The dominant mode of atmospheric and climate Cayan, 1992a,b) with a magnitude of ~0.2 to 0.4°C (e.g., variability in the North Atlantic Ocean region is the NAO, Davies et al., 1997; Kapala et al., 1998). which is a dipole meridional oscillation in atmospheric Although the NAO is the dominant mode of pressure between the Iceland Low and Azores High mid-latitude atmospheric variation, dynamical relations (Hurrell, 1995; Hurrell and Van , 1997; Hurrell et al., between El Ninõ and Atlantic climate have long been 2002). The NAO is linked to the Arctic Oscillation (AO), documented (e.g., Enfield and Mayer, 1997; see references

39 Sargasso Sea Alliance – Oceanography of the Sargasso Sea in Penland and Matrosova, 1998). For example, the Gulf research facility. The results of the AEROCE program were Stream position shifts northwards after El Niño events summarized by Prospero (2001). Some of the key findings and during NAO positive phases with a lag of ~2 years relevant to the Sargasso Sea include: (e.g., Taylor et al, 1998; Taylor and Stephens, 1998). Within 4-12 months of El Niño warming in the Pacific 1. Seasonal cycles in aerosol pollutants in Bermuda Ocean, warming is observed in the tropical North are determined more by the speed and duration of Atlantic, Caribbean Sea and the SE subtropical gyre (e.g., atmospheric transport than by strength of source 1996; Bojariu, 1997; Penland and Matrosova, 1998). The emissions (e.g. Moody et al., 1995). mechanism for this apparently relates to a reduction in 2. Anthropogenic sources contribute a significant cloud cover in the drier, more stable Atlantic atmosphere amount to the atmospheric loadings of sulphur and (e.g., Davies et al., 1997; Jones and Thorncroft, 1998). nitrogen species (e.g. Savoie, et al., 1992).

6.2. Atmospheric deposition and Acid 3. Sea-salt aersosol is a major reaction medium and Precipitation sink for sulphur and nitrogen species over the North Atlantic Ocean (e.g. Keene et al., 1998). N.R. Bates and A.J. Peters 4. Records of deposition of African dust to the Sargasso Human modification of the global biogeochemical cycles Sea were consistent with loadings of atmospheric of nitrogen and sulphur has led to acidic deposition from dust observed at Bermuda, and annual variations the atmosphere, which has affected sensitive terrestrial and in sediment trap fluxes were linked to changes in ocean ecosystems (e.g., Farrell, 1995; Rodhe et al., 2002; atmospheric transport rather than source strength Bouwman et al., 2003; Holland et al., 2005; Lamarque et al., (Jickells et al., 1998). 2005; Dentener et al., 2006; Doney et al., 2007). In those regions with acid deposition, industrial emissions of sulphur 5. is the dominant light scattering aerosol and nitrogen compounds (e.g., North America, Europe and over a large part of the tropical and subtropical North East ) or intensive agricultural practices contribute Atlantic Ocean (e.g. Maring et al., 2000). to the acidity of rainwater with pH typically ranging from about 4 to 6 (e.g., Rodhe et al., 2002). Atmospheric deposition of nitrogen species also The Sargasso Sea is downwind of pollution sources can support ocean primary production although it varies from the North American and consequently widely by ocean region (e.g., Paerl, 1997; de Leeuw et al., experiences acid deposition with rainfall pH levels 2003; Hastings et al., 2003; Spokes and Jickells, 2005; typically ranging from about 4.4 to 5.6 (Jickells et al., 1982; Boulart et al., 2006; Jickells, 2006). Annual rates of primary Bates and Peters, 2007). Early studies of atmospheric production at BATS are typically ~150 g C m-2 year-1 deposition of nitrogen or sulphur were focused on the (Steinberg et al., 2001), and the amount supported by contributions from H2SO4, HNO3, CaCO3, organic acids, atmospheric nitrogen deposition is typically insignificant soil dust and reduced and oxidized sulphur and nitrogen (0.2–0.5%) except potentially for rare high rainfall compounds to the acidity of wet deposition (e.g., Keene events (e.g., Knap et al., 1986; Fanning, 1989; Owens et and Galloway, 1988; Whelpdale et al., 1996). The pH and al., 1992; Michaels et al., 1993). However, future changes chemical composition of rainwater has been monitored in atmospheric nitrogen deposition (e.g., Duce et al., on the island of Bermuda since the early 1980’s (Jickells 2008), coupled with the long term reductions in nutrient et al., 1982; Galloway et al., 1993), initially as part of supply from below might enhance this mechanism the Western Atlantic-Ocean Experiment (WATOX; supporting oceanic primary production. Perhaps more Galloway et al., 1987 and Atmosphere-Ocean Chemistry important than atmospheric nitrogen deposition, in Experiments (AEROCE; Huang et al., 1996) projects). terms of supporting primary production, are atmospheric AEROCE was a multi-disciplinary collaborative iron inputs which keep the Sargasso Sea replete with a program focused on linked atmospheric and marine biologically important trace metal (Sedwick et al., 2007; chemical processes in the North Atlantic Ocean region. see also section 3). Under this initiative a number of atmospheric research Some studies of synthetic organic chemicals in the towers were constructed at key sites in the North Atlantic remote marine atmosphere have been conducted in the Ocean region, including a 23m tower constructed in 1988 Sargasso Sea region. Concentrations of polychlorinated at Tudor Hill, Bermuda. This facility was used for daily biphenyls (PCBs) and organochlorine pesticides (OCPs) sampling of gases, aerosol and precipitation for over a have been detected in the atmosphere of the North decade and continues to be maintained and used as a Atlantic Ocean at levels similar to those from other

40 Sargasso Sea Alliance – Oceanography of the Sargasso Sea remote locations (Bidleman et al., 1981; Whelpdale et oxidized to sulphate and methane sulphonate aerosols al., 1990) and these compounds have been shown to be (Shaw, 1983), which act as cloud condensation nuclei. well mixed in the troposphere up to an altitude of 10,000 Variability in oceanic DMS production and ventilation feet, with concentrations over the western North Atlantic to the atmosphere has the potential to alter aerosol Ocean generally lower than those over the continental abundance, cloud coverage, and cloud properties, which USAA. (Knap and Binkley, 1991). A long term study in turn affects the atmospheric radiative balance and of PCBs in the oceanic atmosphere undertaken at the climate (Charlson et al., 1987). former AEROCE facility in Bermuda in 1992-93 showed There is a need to quantitatively understand biogenic little change in PCB levels over the previous 20 years, sulphur dynamics in the oceans and the role of DMS in and an atmospheric half-life of greater than 23 years structuring past, as well as future, global climates. In was estimated for these compounds (Panshin and Hites, order to accomplish this, a better understanding of the 1994). PCB concentrations were significantly higher in air fates of the DMS and dimethylsulphoniopropionate masses arriving at Bermuda from Africa and the eastern (dissolved and particulate DMSP) pools in the ocean Atlantic region. More recent work has demonstrated the is required. The task is difficult because the biological presence polyfluorinated chemicals (PFCs), a relatively and chemical processes involved in the cycling of new class of industrial chemicals, in this region (Shoeib biogenic sulphur are broad and complex. Short term at al., 2010). Further long-term investigation of organic (UV inhibition, nutrient pulses) as well as long-term contaminants in the atmosphere of the Sargasso Sea (light regime, nutrient regime, temperature) stressors region has continued at the Tudor Hill facility as part of impact the biogeochemical cycling processes of the the Global Atmospheric Passive Sampling (GAPS) study oceanic sulphur pool. Because the oceans account for (Harner et al., 2006; Pozo at al., 2006; Pozo at al., 2009). > 50% of the global source of reduced sulphur to the atmosphere, it is critical to understand the various 6.3. Air-sea gas exchange, CO and DMS 2 reservoirs and cycling processes. In the Sargasso Sea, N.R. Bates early measurements of oceanic DMS and DMSP have

Carbon Dioxide (CO2). The atmosphere-ocean exchanges provided the only long-term time series for DMS in the of CO2 in the Sargasso Sea are discussed in section 3 and deep ocean (Dacey et al., 1998; Toole et al., 2008). The 5.2. However, the Sargasso Sea is an important region for observed decoupling of DMS concentration from any uptake of CO2 from the atmosphere with distinct seasonal measure of its precursors (i.e., DSMP) embodies the variability in uptake and release of CO2 (Bates et al., 1996; DMS “summer paradox” hypothesis (Simó and Pedrós- Bates et al., 1998a,b; Bates and Hansell, 1999; Nelson et Alió, 1999). More recent studies off Bermuda (Dacey, al., 2001; Bates, 2001, 2002; Takahashi et al., 2002; Bates, Toole, Bates, unpublished data) have suggested that the 2007; Takahashi et al., 2009). The annual net ocean uptake DMS ‘summer paradox’ is a reoccurring phenomenon of CO2 in the subtropical gyre of the North Atlantic off in this area of the ocean. The continuing development Bermuda appears to be increasing in contrast to other parts of more precise and accurate measurement techniques of the North Atlantic Ocean (especially in the subpolar is also imperative as demonstrated by the significant gyre; Watson et al., 2009; Schuster et al., 2009). reduction in DMSPd concentrations. Time-series data Dimethylsulphide (DMS): Dimethylsulphide (DMS) such as these are important for understanding present is produced through biogeochemical processes in the global and also for modeling and surface ocean food web. DMS is the primary source predicting future fluctuations in physical, chemical, and of natural sulphur to the atmosphere, where the gas is biological processes.

41 Sargasso Sea Alliance – Oceanography of the Sargasso Sea References for Chapter 6

Bates, N.R., 2001. Interannual Bojariu, R., 1997. Climate Dentener, F., Drevet, J., Lamarque, Galloway, J.N., Savoie, D.L., changes of oceanic CO2 and variability modes due to ocean- J.F., Bey, I., Eickhout, B., Fiore, Keene, W.C., and Wilson, biogeochemical properties in the atmosphere interaction in the A.M., Hauglustaine, D., Horowitz, P.A., 1993. The temporal and Western North Atlantic subtropical central Atlantic. Tellus, 49A, L.W., Krol, M., Kulshrestha, U.C., spatial variability of scavenging gyre. Deep-Sea Research II, 48(8–9), 362–370. Lawrence, M., Galy-Lacaux, C., ratios for NSS sulphate, nitrate, 1507–1528. Rast, S., Shindell, D., Stevenson, methanesulfonate and sodium in Boulart, C., Flament, P., D., Van Noije, T., Atherton, C., the atmosphere over the North- Bates, N.R., 2002. Interannual Gentilhomme, V., Deboudt, Bell, N., Bergman, D., Butler, T., Atlantic Ocean. Atmospheric variability in the global ocean K., Migon, C., Lizon, F., Cofala, J., Collins, B., Doherty, Environment Part A— General Topics, uptake of CO2. Geophysical Research Schapira, M., and Lefebvre, A., R., Ellingsen, K.K., Galloway, 27 (2), 235–250. Letters, 29 (5), 1059–1064, 2006. Atmospherically-promoted J., Gauss, M., Montanaro, V., doi:10.1029/2001GL013571. photosynthetic activity in a well- Muller, J.F., Pitari, G., Rodriguez, Galloway, J.N., Townsend, A.R., mixed ecosystem: significance of J., Sanderson, M., Solmon, F., Erisman, J.W., Bekunda, M., Bates, N.R., 2007. Interannual wet deposition events of nitrogen Cai, Z.C., Freney, F.R.,Martinelli, variability of the oceanic CO Strahan, S., Schultz, M., Sudo, K., 2 compounds. Estuarine, Coastal and Szopa, S., Wild, O., 2006. Nitrogen L.A., Sietzinger, S.P., and Sutton, sink in the subtropical gyre of the Shelf Science, 69 (3–4), 449–458. M.A., 2008. Transformation of North Atlantic Ocean over the last and sulfur deposition on regional and global scales: a multimodel the nitrogen cycle: Recent trends, two decades. Journal of Geophysical Bouwman, A.F., Van Vuuren, questions, and potential solutions. Research, (Oceans 112 (C9), C09013, D.P., Derwent, R.G., and Posch, evaluation. Global Biogeochemical Cycles, 20 (4), GB4003. Science, 320, 889–892, doi: doi:2006JC003759, May 4, 2007. M., 2003. A global analysis of 10.1126/science.1136674. acidification and eutrophication doi:10.1029/2005GB002672. Bates, N.R., and Hansell, D.A., of terrestrial ecosystems. Water, Doney, S.C., Mahowald, N., Harner, T., Pozo-Gallardo, K., 1999. A high resolution study Air and Soil Pollution 141 (1–4), Gouin, T., Macdonald, A.M., of surface layer hydrographic Lima, I., Feely, R.A., Mackenzie, 349–382. F.T., Lamarque, J.-F., Rasch, Hung, H., Cainey, J. and Peters, and biogeochemical properties A. (2006) Global pilot study between Chesapeake Bay and Cayan, D.R., 1992a. Latent and P.J., 2007. The impact of anthropogenic atmospheric for persistent organic pollutants Bermuda. Marine Chemistry, sensible heat flux anomalies (POPs) using PUF disk passive air 67, 1–16, doi:10.1016/S0304– over the Northern Oceans: nitrogen and sulfur deposition on ocean acidification and samplers. Environmental Pollution, 4203(99)00045–6. the connection to monthly 144:445–452. . Journal of the inorganic carbon system. Bates, N.R., and Peters, A.J., Climate, 5, 354–369. Proceedings of the National Academy Hastings, M.G., Sigman, D.M., 2007. The contribution of of Sciences, 104 (37), 14580–14585. and Lipschultz, F., 2003. Isotopic atmospheric acid deposition Cayan, D.R., 1992b. Latent and Duce, R.A., LaRoche, J., Altieri, evidence for source changes to ocean acidification in the sensible heat flux anomalies over of nitrate in rain at Bermuda. subtropical North Atlantic Ocean. the Northern Oceans: driving the K., Arrigo, K.R., Baker, A.R., Capone, D.G., Cornell, S., Journal of Geophysical Research Marine Chemistry, 107, 547–558. sea surface temperature. Journal of [Atmospheres], 108 (D24) (Art. No. Physical Oceanography, 22, 859–881. Dentener, F., Galloway, J., Bates, N.R., Michaels, A.F., and Ganeshram, R.S., Geider, R.J., 4790). Knap, A.H., 1996. Seasonal and Charlson, R.J., Lovelock, J.E., Jickells, T., Kuypers, M.M., Holland, E.A., Braswell, B.H., interannual variability of the Andreae M.O., and Warren S.G., Langlois, R., Liss, P.S., Liu, Sulzman, J., and Lamarque, J.F., oceanic carbon dioxide system at 1987. Oceanic phytoplankton, S.M., Middelburg, J.J., Moore, 2005. Nitrogen deposition onto the USA JGOFS Bermuda Atlantic atmospheric sulfur, cloud albedo C.M., Nickovic, S., oschlies, the and Western Time-series Site. Deep-Sea Research and climate. Nature, 326, 655–661. A., Pedersen, T., Prospero, Europe: synthesis of observations II, 43(2–3), 347–383. J., Schlitzer, R., Seitzinger, S., Dacey, J.W., Howse, F.A., and models. Ecological Applications, Sorensen L.L., Uematsu, M., 15 (1), 38–57. Bates, N.R., Pequignet, A.C., Michaels, A.F., and Wakeham, Ulloa, O., Voss, M., Ward, B., Johnson, R.J., and Gruber, N. S.G., 1998. Temporal variability and SAmora, L., 2008, Impacts Huang, S.L., Arimoto, R., and 2002. A short-term sink for of dimethylsulfide and of atmospheric anthropogenic Rahn, K.A., 1996. Changes in atmospheric CO2 in subtropical dimethylsulfoniopropionate in the nitrogen on the open ocean. atmospheric lead and other mode water of the North Atlantic Sargasso Sea. Deep-Sea Research I, Science, 320: 893–897. doi: pollution elements at Bermuda. Ocean. Nature, 420 (6915), 489– 45, 2085–2099. 10.1126/science.1150369. Journal of Geophysical Research 493, doi:10.1038/nature01253. Davies, J.R., Rowell, D.P., and [Atmospheres], 101 (D15), 21033– Enfield, D.B., and Mayer, D.A., 21040. Bates, N.R., Takahashi, T., Folland, C.K., 1997. North 1997. sea surface Chipman, D.W., and Knap, A.H., Atlantic and European seasonal temperature variability and its Hurrell, J.W., 1995. Decadal 1998. Variability of pCO2 on diel predictability using an ensemble of relation to El Niño-Southern trends in the North Atlantic to seasonal timescales in the multidecadal atmospheric GCM Oscillation. Journal of Geophysical Oscillation: regional temperatures Sargasso Sea near Bermuda. Journal simulations. International Journal of Research, 102, 929–945. and precipitation. Science, 269, of Geophysical Research, 103 (C8), Climate, 17, 1263–1284. 676–679. 15,567–15,585. Fanning, K.A., 1989. Influence of de Leeuw, G., Spokes, L., Jickells, atmospheric pollution on nutrient Hurrell, J.W., and Van Loon, H., Bates, N.R., Knap, A.H., and T., Skjoth, C.A., Hertel, O., limitation in the Ocean. Nature 1997. Decadal variations in climate Michaels, A.F., 1998. Contribution Vignati, E., Tamm, S., Schulz, 339 (6224), 460–463. associated with the North Atlantic of hurricanes to local and global M., Sorensen, L.L., Pedersen, B., Oscillation. Climatic Change, 36, estimates of air-sea exchange Klein, L., and Schlunzen, K.H., Farrell, E.P., 1995. Atmospheric 301–326. of CO2. Nature, 395, 58–61, 2003. Atmospheric nitrogen deposition in maritime doi:10.1038/25703. inputs into the North Sea: effect environments and its impact on Hurrell, J.W., Kushnir, Y., and on productivity. Continental Shelf terrestrial ecosystems. Water, Air Visbeck, M., 2002. The North Bidleman, T.F., Christensen, E.J., Research, 23 (17–19), 1743–1755. and Soil Pollution, 85 (1), 123–130. Atlantic Oscillation. Science, 291, Billings, W.N. and Leonard, R., 603–606. 1981. Atmospheric transport of Galloway, J.N., Church, T.M., organochlorines in the North Knap, A.H., Whelpdale, D.M., Jickells, T., 2006. The role of Atlantic gyre. Journal of Marine and Miller, J.M., 1987. The air-sea exchange in the marine Research, 39, 443–464. Western Atlantic-Ocean nitrogen cycle. Biogeosciences 3, Experiment. ACS Symposium Series, 271–280. 349, 39–55.

42 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Jickells, T., Knap, A., Church, Michaels, A.F., Siegel, D.A., Rodwell, M.J., Rowell, D.P., and Takahashi, T., Sutherland, S.C., T., Galloway, J., and Miller, J., Johnson, R.J., Knap, A.H., and Folland, C.K., 1999 Oceanic Wanninkhof, R., Sweeney, C., 1982. Acid-rain on Bermuda. Galloway, J.N., 1993. Episodic forcing of the wintertime North Feely, R.A., Chipman, D.W., Nature, 297 (5861), 55–57. inputs of atmospheric nitrogen to Atlantic Oscillation and European Hales, B., Friederich, G.E., the Sargasso Sea—contributions climate. Nature, 398, 320–323. Chavez, F.P., Watson, A.J., Jickells, T.D., Dorling, S., Deuser, to new production and Bakker, D.C.E., Schuster, U., W.G., Church, T.M., Arimoto, R. phytoplankton blooms. Global Rodhe, H., Dentener, F., and Metzl, N., Yoshikawa-Inoue, and Prospero, J. 1998. Airborne Biogeochemical Cycles ,7 (2), Schulz, M., 2002 The global H., Olafsson, J., Arnarson, T.S., dust fluxes to a deep water 339–351. distribution of acidifying wet Tilbrook, B., Johannessen, T., sediment trap in the Sargasso Sea. deposition. Environmental Science Olsen, A., Bellerby, R.J., de Global Biogeochemical Cycles, 12, Moody, J. L., Oltmans, S.J., and Technology 36, 4382–4388. Baar, H.J.W., Nojiri, Y., Wong, 311–320. Levy II, H. and Merrill J.T., Savoie, D.L., Prospero, J.M. C.S., Delille, B., and Bates, N.R., 1995. Transport climatology of 2009. Climatological mean and Jones, C.G., and Thorncroft, tropospheric ozone: Bermuda, Oltmans, S.L., Graustein, W.C. C.D., 1998. The role of El Niño in Turekian, K.K., Merrill, J.T. and decadal change in surface ocean 1988–1991, Journal of Geophysical pCO , and net sea-air CO flux Atlantic activity. Research, 100, 7179–7194. Levy II, H., 1992. Source of nitrate 2 2 Weather, 53, 324–336. and ozone in the marine boundary over the global oceans. Deep-Sea Nelson, N.B., Bates, N.R., layer of the North Atlantic, Research II, 56 (8–10), 554–577, Kapala, A., Maechel, H., and Siegel, D.A., and Michaels, A.F., Journal of Geophysical Research, 97, doi:10.1016/j.dsr2.2008.12.009. Flohn, H., 1998. Behaviour of 2001. Spatial variability of the 11575–11589. the centres of action above Toole, D.A., Siegel, D.A., and CO2 sink in the Sargasso Sea. Doney, S.C., 2008. A light-driven, the Atlantic since 1881. Part II Deep-Sea Research II, 48 (8–9), Shaw, G.E., 1983. Bio-controlled Associations with regional climate thermostasis involving the sulfur one-dimensional dimethylsulfide 1801–1821, doi:10.1016/S0967– biogeochemical cycling model anomalies. International Journal of 0645(00)00162–4. cycle. Climatic Change, 5: 297–303. Climatology, 18, 23–36. for the Sargasso Sea. Journal of Owens, N.J.P., Galloway, J.N., Shoeib, M., Vlahos, P., Harner, Geophysical Research—Biogeosciences, Keene, W.C., and Galloway, J.N., and Duce, R.A., 1992. Episodic T., Peters, A., Graustein, M. 113, G02009. 1988. The biogeochemical cycling atmospheric nitrogen deposition and Narayan, J., 2010. Survey of formic and acetic acids through of polyfluorinated chemicals Watson, A.J, Schuster, U., to oligotrophic oceans. Nature, Bakker, D.C.E., Bates, N.R., the troposphere:an overview of 357 (6377), 397–399. (PFCs) in the atmosphere over current understanding. Tellus 40B, the northeast Atlantic Ocean— Corbiere, A., Gonzalez-Davila, 322–334. Paerl, H.W., 1997. Coastal Bermuda, Sable Island and coastal M., Friedrich, T., Hauck, J., eutrophication and harmful USA. Atmospheric Environment , Heinze, C., Johannessen, Keene, W.C., Sander, R., Pszenny, algal blooms: importance of 44:2887–2893. T., Körtzinger, A., Metzl, A.A.P., Vogt, R., Crutzen, P.J. and atmospheric deposition and N., Olafsson, J., Olsen, A., Galloway, J.N., 1998. Aerosol pH in groundwater as “‘new”‘ nitrogen Simo, R., and Pedros-Alio, C., Oschlies, A., Padin, X.A., Pfiel, the marine boundary layer: A review and other nutrient sources. 1999. Short-term variability in B., Santana-Casiano, M., and model evaluation. Journal of Limnology and Oceanography, 42 the open ocean dimethylsulphide. Steinhoff, T., Telszewski, M., Aerosol Science, 29, 339–356. (5), 1154–1165. Global Biogeochemical Cycles, 13, Rios, A.F., Wallace, D.W.R., and 1173–1181. Wanninkhof, R., 2009. Accurately Knap, A.H. and Binkley, K.S., Panshin, S.Y. and Hites, R.A., tracking the variation in the North 1991. Chlorinated organic Spokes, L.J., and Jickells, T.D., 1994. Atmospheric concentrations Atlantic sink for atmospheric CO2. compounds in the troposphere of polychlorinated biphenyls in 2005. Is the atmosphere really Science, 326, 1391–1393. over the western North Atlantic Bermuda. Environmental Science and an important source of reactive Ocean measured by aircraft. Technology, 28, 2001–2007. nitrogen to coastal waters? Taylor, A.H., and Stephens, Atmospheric Environment, 25A, Continental Shelf Research, 25 (16), J.A., 1998. The North Atlantic 1507–1516. Penland, C., and Matrosova, 2022–2035. Oscillation and the latitude of the L., 1998. SST anomaly in the El Gulf Stream. Tellus, 50A, 134–142. Knap, A.H., Jickells, T., Nino region is a strong 6 month Schuster, U., Watson, A.J., Bates, Pszenny, A., Binkley, K.S., predictor of SST anomaly in the N.R., Corbiere, A., Gonzalez- Taylor, A.H., Jordan, M.B., and 1986 Significance of atmospheric- north Tropical Atlantic. Journal of Davila, M., Metzl, N., Pierrot, Stephens, J.A., 1998. Gulf Stream derived fixed nitrogen on Climate, 11, 483–490. D., and Santana-Casiano, M., shifts following ENSO events. productivity of the Sargasso Sea. 2009. Trends in North Atlantic Nature, 393, 638. Nature, 320 (6058), 158–160. Pozo, K., Harner, T., Wania, F., sea-surface fCO2 from 1990 Muir, D.C.G., Jones, K.C. and to 2006. Deep-Sea Research II, Visbeck, M., Hurrell, J.W., Lamarque, J.-F., Kiehl, J.T., Barrie, L.A., 2006. Toward a 56, 620–629, doi:10.1016/j. Polvani, L., and Cullen, H.M., Brasseur, G.P., Butler, T., global network for persistent dsr2.2008.12.011. 2001. The North Atlantic Cameron-Smith, P., Collins, organic pollutants in air: Oscillation: Past, present, and W.D., Collins, W.J., Granier, C., Results from the GAPS study. Steinberg, D.K., Carlson, C.A., future. Proceedings National Hauglustaine, D., Hess, P.G., Environmental Science and Technology Bates, N.R., Johnson, R.J., Academy of Sciences, 98, 12876– Holland, E.A., Horowitz, L., 40, 4867–4873. Michaels, A.F., and Knap., 12877. Lawrence, M.G., McKenna, D., A.H., 2001. Overview of the US Merilees, P., Prather, M.J., Rasch, Pozo, K., Harner, T., Lee, S.C., JGOFS Bermuda Atlantic Time- Whelpdale, D.M., , P.J., Rotman, D., Shindell, D., Wania, F., Muir, D.C.G. and series Study (BATS): a decade- P.W., Sanhueza, E., Artz, R.A., Thornton, P., 2005. Assessing Jones, K.C., 2009. Seasonally scale look at ocean biology Ayers, G., Delmas, R.J., Dovland, future nitrogen deposition and resolved concentrations of and biogeochemistry. Deep-Sea H., Galloway, J.N., Gillewtt, R., carbon cycle feedback using a persistent organic pollutants Research Part II, 48, 1405–1447. Hara, H., Lacaux, J.-P., Luke, W., multimodel approach: analysis in the global atmosphere from Pedersen, U., Ryaboshapko, of nitrogen deposition. Journal of the first year of the GAPS Takahashi, T., Sutherland, A., 1996. A global overview of Geophysical Research, 110, D19303. study. Environmental Science and S.G., Sweeney, C., Poisson, acid deposition. In: Whelpdale, doi:10.1029/2005JD005825. Technology, 43, 796–803. A.P., Metzl, N., Tilbrook, B., D.W., Kaiser, D.M. (Eds.), World Bates, N.R., Wanninkhof, R.H., Meteorological Organization/Global Maring H., Savoie, D.L., Prospero, J.M., 2001. The Feely, R.A., Sabine, C.L., and Atmospheric Watch Report, 106. Izaguirre, M.A., McCormick, Atmosphere-Ocean Chemistry Olafsson, J., 2002. Biological and WMO/GAW Report 106. C., Arimoto, R., Prospero, J.M. Experiment (AEROCE): temperature effects on seasonal and Pilinis, C., 2000. Aerosol Background and major changes of pCO2 in global ocean physical and optical properties accomplishments. IGAC Newsletter, surface waters. Deep-Sea Research II, and their relationship to 24, 3–5. 49, 1601–1622. aerosol composition in the free troposphere at Izaña, Tenerife, Canary Islands during July 1995, Journal of Geophysical Research, 105,14,677–14,700.

43 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Chapter 7 Climate change and ocean acidification

7.1 Climate Change on Climate Change (IPCC; Prentice et al., 2007) model

N.R. Bates projections of future anthropogenic CO2 emissions and

The NAO, like El Niño, also has profound impacts on subsequent ocean absorption of anthropogenic CO2 ocean biogeochemical dynamics and the fate of CO2. indicate that surface ocean pH will decrease by 0.3-0.5 In the North Atlantic, the NAO plays a large role in units over the next century and beyond (Caldeira and determining the exchange of CO2 between the ocean Wickett, 2003; 2005). The effects of ocean acidification and atmosphere (Bates, 2001; Bates et al., 2002; Gruber are potentially far-reaching in the global ocean, et al., 2002). It appears likely that there is a coordinated particularly for organisms that secrete calcium carbonate basinwide response in the North Atlantic Ocean to (CaCO3) skeletons, tests or shells (Buddemeier et al., climate phenomena such as NAO (Gruber et al., 2002; 2004; Royal Society, 2005; Orr et al., 2005; Doney, Levine et al., 2011). 2006; Fabry et al., 2008) including hermatypic corals There is also increasing evidence that shows a that are the framework for coral reef ecosystems. strong linkage between NAO and atmospheric dust Ocean acidification is an emerging environmental issue transport variability which consequently control the but one that appears to have impacts on many marine variability of ecosystem structure and functioning in the ecosystems, for example even the apparently healthy North Atlantic subtropical gyre (Bates and Hansell, 2004; coral reef ecosystems of Bermuda (Bates et al., 2001; Lomas and Bates, 2004). In the tropical and subtropical Bates, 2002; Bates et al., 2010). ocean, it has also been hypothesized that tropical Increasing seawater pCO2 and ocean acidification cyclones (i.e., hurricanes and typhoons) play a significant also results in a decrease in the surface seawater carbonate 2- role in determining the exchange of CO2 between ocean ion concentration [CO3 ] and the saturation state ( ) and atmosphere (Bates et al., 1998a,b; Bates and Merlivat, with respect to calcium carbonate (CaCO3) minerals 2001; Bates, 2002). such as calcite and aragonite. This has profound negative implications for marine organisms in both high and low 7.2 Ocean Acidification latitude oceans that produce tests, shells or skeletons N.R. Bates made of carbonate minerals, such as corals, coralline Over the last several centuries, human activities have algae, pelagic pteropods and coccolithophorids, mollusks, released large quantities of carbon dioxide (CO2) into echinoderms, and foraminifera (Buddemeier et al., 2004; the atmosphere (IPCC, 1996, 2001, 2007; Sarmiento and Royal Society, 2005; Orr et al., 2005; Doney, 2006; Fabry Wofsy, 1999; Wofsy and Harris, 2001). Anthropogenic et al., 2008). It is also well known that dissolution of

CO2, emitted primarily from fossil fuel use, cement carbonate minerals will increase as a result of decreasing manufacture, and land use changes (Houghton and seawater CaCO3 saturation state (Andersson et al., 2003; Hackler, 2002) has not only accumulated in the 2005, 2007; Kuffner et al., 2008). atmosphere (Prentice et al., 2001), but it has also been The responses of coccolithophores, carbonate taken up by the terrestrial biosphere and global oceans mineral-bearing phytoplankton, to climate change and (Quay, 2002; Sabine et al., 2004). anthropogenic induced ocean acidification, plus the

As a consequence of the direct uptake of feedbacks to atmospheric CO2 and climate, are, without anthropogenic CO2, surface seawater dissolved inorganic doubt, complex, uncertain and subject to intense carbon (DIC) concentration and partial pressures of scientific debate. Calcification and production of biogenic

CO2 (pCO2) have increased while the pH has decreased CaCO3 by marine calcifiers is associated with the uptake 2- - (Figure 7; Bates et al., 1996; Winn et al., 1998; Bates, of [CO3 ] or [HCO3 ], which, in turn, acts to increase

2007; Bates and Peters, 2007; Santana-Casiano et al., CO2. Associated uptake of total alkalinity (TA) and 2007; Takahashi et al., 2009). This gradual process, dissolved inorganic carbon (DIC) in the ratio of 2:1, shifts termed ocean acidification has long been recognized by the equilibrium of the carbonate system towards CO2 2+ 2- 2+ - chemical oceanographers (Broecker and Takahashi, (i.e., [Ca ] + [CO3 ] = CaCO3 [1], or: [Ca ] + 2[HCO3

1966; Broecker et al., 1971; Bacastow and Keeling, ] = CaCO3 + [H2O] + [CO2] [2]) (Dickson et al., 2007).

1973). Estimates based on the Intergovernmental Panel For coccolithophores, [HCO3] uptake, for example, is

44 Sargasso Sea Alliance – Oceanography of the Sargasso Sea a potential source of CO2 for photosynthesis. However, classes of phytoplankton blooms, coccolithophores can whether coccolithophore calcification is a source of CO2 increase seawater pCO2 content and thus contribute to to the ocean depends on the balance of CaCO3 production a negative coccolithophore-CO2 feedback (Riebesall et to organic carbon production (e.g., CO2 production occurs al., 2000; Zondervan et al., 2001; Ridgewell et al., 2007) when CaCO3 production > organic carbon production). In that has potentially important implications for the role the field, a few studies have shown increases in seawater of the global ocean in the uptake of anthropogenic CO2, pCO2 in response to coccolithophore calcification in modulation of atmospheric CO2 and climate responses the North Atlantic Ocean. Thus unlike other taxonomic over the next few centuries.

Figure 7. Time-series of atmospheric and ocean carbon dioxide, pH and aragonite saturation states. a. Timeseries of atmospheric carbon dioxide (in parts per million) from Mauna Loa, Hawaii (red line), and Bermuda (pink symbol), and surface ocean seawater carbon dioxide (μatm) at the Bermuda Atlantic Time-series Study (BATS) site off -Bermuda. Observed (grey) and seasonally detrended (blue line) surface ocean seawater carbon dioxide levels are shown. Earlier seawater data from the GEOSECS and TTO expeditions in the North Atlantic Ocean are also shown in this and following panels. b. time-series of surface ocean seawater pH at the BATS site off Bermuda. Observed (grey) and seasonally detrended (green line) seawater pH are shown. c. time-series of surface ocean aragonite saturation state (W) for calcium carbonate at the BATS site off Bermuda. Observed (purple) and seasonally detrended (purple line) seawater aragonite saturation state (Ω) are shown. Statistical and seasonal detrending methods follow Bates (2007), Bates and Peters (2007), and Bindoff et al., (2007).

45 Sargasso Sea Alliance – Oceanography of the Sargasso Sea References for Chapter 7

Andersson, AJ, Mackenzie, FT, Bates, N.R., and Hansell, D.A., Buddemeier, R.W., Kleypas, J.A., Houghton, R.A., and Hackler, and Ver, L.M., 2003. Solution 2004. Temporal variability of and Aronson, R.B., 2004. Coral J.L., 2002. in Trends: A Compendium of shallow-water carbonates: An excess nitrate in the Subtropical Reefs and Global Climate Change: of Data on Global Change (Carbon insignificant buffer against rising Mode Water of the North Atlantic Potential Contributions of Climate Dioxide Information Analysis atmospheric CO2. , 31, Ocean. Marine Chemistry, 84, Change to Stresses on Coral Reef Center, Oak Ridge National 513– 516. 225–241. Ecosystems, p. 44, (download Laboratory, TN, 2002), http:// report at http://www.pewclimate. cdiac.esd.ornl.gov/ trends/ Andersson, AJ, Mackenzie, F.T., Bates, N.R., and Peters, A.J., org/globalwarmingindepth/all_ landuse/ Houghton/houghton. and Lerman, A., 2005. Coastal 2007. The contribution of reports/coral_reefs/index.cfm). html. ocean and carbonate systems atmospheric acid deposition Pew Center on Climate Change. in the high CO2 world of the to ocean acidification in the IPCC, 1996. Climate Change Anthropocene. American Journal of subtropical North Atlantic Ocean. Caldeira, K., and Wickett, M.E., 1995: The science of climate change, Science, 305, 875–918. Marine Chemistry, 107, 547–558. 2003. Anthropogenic carbon and Contribution of working group I to ocean pH, Nature, 425 (6956), the Second Assessment Report of the Andersson, A.J., Mackenzie, F.T., Bates, N.R., Michaels, A.F., and 365–365. intergovernmental Panel on Climate and Lerman A., 2006. Coastal Knap, A.H., 1996. Seasonal and Change. Houghton, J. T., Meiro ocean CO2-carbonic acid- interannual variability of the Caldeira, K., and Wickett, Filho, L. G., Callander, B. A., Harris, carbonate sediment system oceanic carbon dioxide system at M.E., 2005. Ocean model N., Kattenberg, A., and Maskell, K., of the Anthropocene. Global the USA JGOFS Bermuda Atlantic predictions of chemistry changes eds, Cambridge University Press, Biogeochemical Cycles, 20, GB1S92, Time-series Site. Deep-Sea Research from carbon dioxide emissions Cambridge, 572 p. doi:10.1029/2005GB002506. II, 43(2–3), 347–383. to the atmosphere and ocean. Journal of Geophysical Research, IPCC, 2001. Climate change Andersson, A.J., Bates, N.R., and Bates, N.R., Michaels, A.F., and Oceans, 110, (C9), C09S04, doi 2001: The scientific basis, Mackenzie, F.T., 2007. Dissolution Knap, A.H., 1996. Alkalinity 10.1029/2004JC002671. Contribution of Working Group of carbonate sediments changes in the Sargasso Sea: I to the Third Assessment Report under rising pCO2 and ocean Geochemical evidence of Dickson, A.G., Sabine, C.L., of the Intergovernmental Panel on acidification: Observations from calcification? Marine Chemistry, 51 and Christian, J.R., 2007. Guide Climate Change. Houghton, J. T., Devil’s Hole, Bermuda. Aquatic (4), 347–358, doi:10.1016/0304– to best practices for ocean CO2 Ding, Y., Griggs, D. J., Noguer, Geochemistry, 13 (3), 237–264, doi 4203(95)00068–2 measurements. Sidney, British M., van der Linden, P. J., Dai, X., 10.1007/s10498–007–9018–8. Columbia, North Pacific Marine Maskell, K., and Johnson, C. A., Bates, N.R., Takahashi, T., Science Organization, PICES Bacastow, R.D., and Keeling, Chipman, D.W., and Knap, A.H., eds., Cambridge University Press, Special Publication 3. Cambridge, 881 p. C.D., 1973. Atmospheric carbon 1998a. Variability of pCO2 on dioxide and radiocarbon in the diel to seasonal timescales in the Doney, S.C., 2006. The dangers IPCC, 2007. Climate Change natural carbon cycle: II. Changes Sargasso Sea. Journal of Geophysical of ocean acidification. Scientific 2007: The Physical Science Basis. from A.D. 1700 to 2070 as Research, 103, 15,567–15,585. American, March 2006, 58–65. Contribution of Working Group I to deduced from a geochemical Bates, N.R., Knap, A.H., and Doney, S.C., Mahowald, N., the Fourth Assessment Report of the model. In: Woodwell, G.M., and Intergovernmental Panel on Climate Pecan, E.V. (editors) Carbon and Michaels, A.F., 1998b. The effect Lima, I., Feely, R.A., Mackenzie, of hurricanes on the local to global F.T., Lamarque, J.-F., Rasch, Change. Solomon, S., D. Qin, M. the biosphere. USA Atomic Energy Manning, Z. Chen, M. Marquis, Commission, pp. 86–135. air-sea exchange of CO2. Nature, P.J., 2007. The impact of 395, 58–61. anthropogenic atmospheric K.B. Avery, M. Tignor and H.L. Bates, N.R., 2001. Interannual nitrogen and sulfur deposition Miller (eds.), Cambridge University Bates, N.R., Amat, A., and Press, Cambridge, United Kingdom changes of oceanic CO2 and on ocean acidification and biogeochemical properties in the Andersson, A.J., 2010. The the inorganic carbon system. and New York, NY, USA, 996 p. Western North Atlantic subtropical interaction of carbonate chemistry Proceedings of the National Academy and coral reef calcification: the Kuffner, I.B., Andersson, A.J., gyre. Deep-Sea Research II, 48(8–9), of Sciences of the United States of Jokiel, P.L., Rodgers, K.S., and 1507–1528. carbonate chemistry coral reef America, 104 (37), 14580–14585. ecosystem feedback (CREF) Mackenzie, F.T., 2008. Decreased Bates, N.R., 2002a. Interannual hypothesis. Biogeosciences, 7 (5), Fabry, V.J., Seibel, B.A., Feely, abundance of crustose coralline variability in the global ocean 2509–2530, doi:10.5194/bg–7– R.A., and Orr, J.C. 2008. Impacts algae due to ocean acidification. Nature Geoscience, 1, 114–117. uptake of CO2. Geophysical Research 2509–2010. of ocean acidification on marine Letters, 29 (5), 1059–1064, fauna and ecosystem processes. Broecker, W.S., and Takahashi, Levine, N.M., Doney, S.C., Lima doi:10.1029/2001GL013571. ICES Journal of Marine Science, 65, I., Wanninkhof, R., Sabine, C.L., T., 1966. Calcium carbonate 414–432. Bates, N.R., 2002b. Seasonal precipitation on the . Feely, R.A., and Bates, N.R., variability of the effect of coral Journal of Geophysical Research, 71, Gruber, N., Bates, N.R., and 2011. The impact of interannual reefs on seawater CO and air- 1575–1602. Keeling, C.D., 2002. Long-term variability on the uptake and 2 accumulation of anthropogenic sea CO2 exchange. Limnology and observations of interannual Oceanography, 47 (1), 43–52. Broecker, W.S., Li, Y-H., Peng, variability in the North Atlantic CO2 in the North Atlantic. Global T-H., 1971. Carbon dioxide—man’s carbon sink. Science, 298, 2374– Biogeochemical Cycles. Bates, N.R., 2007. Interannual unseen artifact. In: Hood, D.W. 2378. Lomas, M.W., and Bates, N.R., variability of the oceanic CO2 (editor) Impingement of man on the sink in the subtropical gyre of oceans. John Wiley and Sons, Inc, Hansell, D.A., Bates, N.R., and 2004. Potential controls on the North Atlantic Ocean over pp 287–324. Olson, D.B., 2004. Excess nitrate interannual partitioning of organic the last two decades. Journal of and nitrogen fixation in the North carbon during the winter/spring Geophysical Research (Oceans), 112 Brown, C.W., and Yoder, J.A., Atlantic Ocean. Marine Chemistry, phytoplankton bloom at the (C9), C09013, doi:2006JC003759, 1994. Coccolithophorid blooms 84 (3–4), 243–265, doi:10.1016/ Bermuda Atlantic Time-series May 4, 2007. in the global ocean. Journal of j.marchem.2003.08.004. Study (BATS) site. Deep-Sea Geophysical Research, 99, 7467– Research Part I, 51 (11), 1619–1636. Bates, N.R., and Merlivat, L., 7482. Hansell, D.A., Olson, D.B., 2001. The influence of short-term Dentener, F., and Zamora, L.M., wind variability on air-sea CO2 2008. Assessment of excess nitrate exchange. Geophysical Research development in the subtropical Letters, 28 (17), 3281–3284. North Atlantic. Marine Chemistry, 106, 562–579.

46 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Orr, J.C., Fabry, V.J., Aumont, Riebesell, U., I. Zondervan, B. Steinhoff, T, Friedrich, T., Winn, C.D., Li, Y.-H., Mackenzie, O., Bopp, L., Doney, S.C., Rost, P.D. Tortell, P.D., Zeebe, Hartman, S.E., Oschlies, A., F.T., and Karl, D.M. 1998. Rising Feely, R.A., Gnanadesikan, A., R.E., and Morel, F.M.M., Wallace, D.W.R., and Kortzinger, surface ocean dissolved inorganic Gruber, N., Ishida, A., Joos, F., 2000. Reduced calcification of A., 2010: Estimating mixed layer carbon at the Hawaii Ocean Time- Key, R.M., Lindsay, K., Maier- marine plankton in response nitrate in the North Atlantic series site. Marine Chemistry, 60, Reimer, E., Matear, R., Monfray, to increased atmospheric CO2. Ocean. Biogeosciences, 7, 795–807 33–47. P., Mouchet, A., Najjar, R.G., Nature, 407, 364–367. doi:10.5194/bg–7–795–2010. Plattner, G. K., Rodgers, K.B., Wofsy, S.C., and Harriss, R.C., Sabine, C.L., Sarmiento, J.L., Royal Society, 2005. Ocean Takahashi, T., Sutherland, S.G., 2001. The North American Carbon Schlitzer, R., Slater, R D., acidification due to increasing Sweeney, C., Poisson, A.P., Metzl, Program Plan (NACP). A Report of Totterdell, I.J., Weirig, M.F., atmospheric carbon dioxide. The N., Tilbrook, B., Bates, N.R., the Committee of the USA Carbon Yamanaka, Y., and Yool, A., Clyvedon Press, Ltd, . Wanninkhof, R.H., Feely, R.A., Cycle Science Steering Group. Sabine, C.L., and Olafsson, J., 2005. Anthropogenic ocean Sabine, C.L., Feely, R.A., Gruber, Wong, C.S., L. Xie, Hsieh, acidification over the twenty- 2002. Biological and temperature N., Key, R.M., Lee, K., Bullister, effects on seasonal changes of W.W., 2007. Variations in first century and its impacts on J.L., Wanninkhof, R., Wong, nutrients, carbon and and other pCO2 in global ocean surface calcifying organisms. Nature, 437, C.S., Wallace, D.W.R., Tilbrook, hydrographic parameters related 681–686. waters. Deep-Sea Research II, 49, B., Millero, F.J., Peng, T.-H., 1601–1622. to the 1976/77 and 1988/89 Prentice, C., et al., 2001. in Kozyr, A., Ono, T., and A.F. Rios, regime shifts in the sub-arctic Climate Change 2001: The Scientific A.F., 2004. The oceanic sink for Takahashi, T., Sutherland, S.C., Northeast Pacific. Progress in Basis. Contribution of Working Group anthropogenic CO2. Science, 305, Wanninkhof, R., Sweeney, C., Oceanography, 75. 326–342. I to the Third Assessment Report of the 367–371. Feely, R.A., Chipman, D.W., Hales, B., Friederich, G.E., Zondervan, I., Zeebe, R. E., Intergovernmental Panel on Climate Santana-Casiano, J.M., Rost, B, and Riebesell, U., Change, J.T. Houghton et al., Eds. Chavez, F.P., Watson, A.J., Gonzalex-Davila, M., Rueda, Bakker, D.C.E., Schuster, U., 2001. Decreasing marine biogenic (Cambridge Univ. Press, New York, M.J., Llinas, O., and Gonzalez– calcification: a negative feedback 2001), pp. 183–237. Metzl, N., Yoshikawa-Inoue, Davila, E.F., 2007. The interannual H., Olafsson, J., Arnarson, T.S., on rising atmospheric pCO2. Global Quay, P., 2002. Ups and downs of variability of oceanic CO2 Tilbrook, B., Johannessen, T., Biogeochemical Cycles, 15, 507–516. parameters in the northeast CO2 uptake. Science, 298, 2344. Olsen, A., Bellerby, R.J., de Atlantic subtropical gyre at the Baar, H.J.W., Nojiri, Y., Wong, Ridgwell, A., Zondervan, I., ESTOC site. Global Biogeochemical C.S., Delille, B., and Bates, N.R., Hargreaves, J.C., Bijma, J., and Cycles, 21: GB1015. 2009. Climatological mean and Lenton T.M., 2007. Assessing decadal change in surface ocean the potential Long-term increase Sarmiento, J.L. and Wofsy, S.C., 1999. A USA Carbon cycle pCO2, and net sea-air CO2 flux of oceanic fossil fuel CO2 uptake science plan. A report of the over the global oceans. Deep-Sea due to CO2-calcification feedback. Research II (in press). Biogeosciences, 4(4), 381–492. carbon and climate working group. Washington, D.C., USA Global Change Research Program.

Appendix I Contact information for contributing authors

Nicholas R. Bates, Senior Maureen Conte, Associate Anthony H. Knap, President and F. Gerald Plumley, Deputy Scientist and Associate Director Scientist, Bermuda Institute of Director, Senior Scientist, Bermuda Director, Senior Scientist, Bermuda for Research, Bermuda Institute Ocean Sciences, 17 Biological Institute of Ocean Sciences, 17 Institute of Ocean Sciences, 17 of Ocean Sciences, 17 Biological Station, St. George’s GE01, Biological Station, St. George’s Biological Station, St. George’s Station, St. George’s GE01, Bermuda, email: (p) 508– GE01, Bermuda, (p) 441–297–1880 GE01, Bermuda, (p) 441–297– Bermuda, (p) 441–297–1880 289–7744, (f) 508–457–1548, x 244, (f) 441–2970–8143, email: 1880 x240, (f) 441–2970–8143, x209, (f) 441–2970–8143, email: [email protected]. [email protected]. email: [email protected]. [email protected]. Adjunct Associate Scientist (resident), The Ecosystems Center, Michael W. Lomas, Senior David A. Siegel, Professor, Kristen N. Buck, Assistant Marine Biological Lab, 7 MBL Scientist, Bermuda Institute of Director Earth Research Institute, Scientist, Bermuda Institute of Street, Woods Hole, MA 02543 Ocean Sciences, 17 Biological Earth Research Institute, University Ocean Sciences, 17 Biological Station, St. George’s GE01, of California, Santa Barbara, CA Station, St. George’s GE01, Stephen J. Giovannoni, Dept. Bermuda, (p) 441–297–1880 93106–3060, USA, (p) 805–893– Bermuda, (p) 441–297–1880 x711, of Microbiology, 220 Nash Hall, x703 , (f) 441–2970–8143, email: 4547, email: [email protected]. (f) 441–2970–8143, email: Kristen. Oregon State University, Corvallis, [email protected]. [email protected] OR 97331, USA. (p) 541–737– Deborah K. Steinberg, Professor 1835, (f) 541–737–0496, email: Norman M. Nelson, Researcher, in Marine Science, Craig A. Carlson, Professor and steve.giovannoni@oregonstate. Earth Research Institute, Earth Institute of Marine Science, The Vice Chair, Department of Ecology, edu. Research Institute, University College of William and Mary, Evolution, and Marine Biology, of California, Santa Barbara, CA Gloucester Point, VA 23062, University of California, Santa Rodney J. Johnson, Assistant 93106–3060, USA, (p) email: USA. (p) 804–684–7838, email: Barbara, Santa Barbara, CA 93106– Scientist, Bermuda Institute of [email protected]. [email protected]. 9620, USA. (p) 805–893–2541 (f) Ocean Sciences, 17 Biological 805–893–8062, email: carlson@ Station, St. George’s GE01, Andrew Peters, Associate lifesci.ucsb.edu. Bermuda, (p) 441–297–1880 Scientist, Bermuda Institute of x700, (f) 441–2970–8143, email: Ocean Sciences, 17 Biological [email protected]. Station, St. George’s GE01, Bermuda, (p) 441–297–1880 x240, (f) 441–2970–8143, email: [email protected].

47 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Appendix II

Glossary of important terms

Aerosol – solid or liquid Eddy – a drift or tendency North Atlantic Oscillation – Sargasso Sea – a region in the particles dispersed and that is counter to or separate dominant long-term mode middle of the North Atlantic suspended in air. from a main current. of meteorological variability Ocean surrounded by ocean in the North Atlantic. currents. It is bounded on the Atlantic Meridional El Niño-La Niña (ENSO) – west by the Gulf Stream; on Overturning Circulation The irregular cyclic swing of Ocean acidification – the north, by the North Atlantic – the part of the large-scale warm and cold phases in the term describing the process Current; on the east, by the ocean circulation in the eastern tropical Pacific. by which carbon dioxide ; and on the North Atlantic that is driven accumulates in the surface Euphotic zone – the shallow south, by the North Atlantic by global density gradients ocean thus lowering the Equatorial Current. created by surface heat and waters of the surface ocean ocean’s pH. freshwater fluxes. where there is sufficient Subtropical mode water light for primary production, Oligotrophic – characterized (STMW) – also known as Anthropogenic – meaning quantitatively defined as the by very low, nanomolar ‘18 degree water’, it is a derived from human activities, 1% light depth. level, inorganic nutrient water mass that sits below as opposed to those occurring concentrations. Food web – term describing the seasonal thermocline in in biophysical environments the western North Atlantic without human influence. the complex interactions Organic – relating to, between multiple trophic or denoting chemical subtropical gyre. Biogeochemistry – is the levels of producers and compounds containing carbon Trace elements – nutrients, scientific discipline that consumers in the marine (other than simple binary commonly metals, that are involves the study of the environment. compounds such as CO2 and required by phytoplankton chemical, physical, geological, some carbon containing salts) usually for enzymes that are and biological processes and Gyre – any large system and chiefly or ultimately of of rotating ocean currents, required in ultra low levels reactions that govern the biological origin. (10-3 nanomolar). composition of the natural particularly those involved environment. with large wind movements. PCR – abbreviation for Troposphere – the lowest ‘polymerase chain reaction’, Macronutrient – chemicals region of the atmosphere, Biological carbon pump – a technique for rapidly extending from the earth’s term describing the export of that an organism needs in producing many copies greatest supply to live and surface to a height of about biologically derived particulate of a fragment of DNA 6–10 km. carbon from the euphotic grow, most commonly used for diagnostic or research zone where it is produced to in reference to carbon, purposes. Zooplankton – ‘animal the mesopelagic where it is nitrogen and phosphorus. plankton’ that are the primary Phytoplankton – oceanic remineralized. Mesopelagic – a term grazers of phytoplankton in single cell plants responsible the open ocean. CDOM – is the optically to describe the zone or for primary production measurable component of organisms inhabiting the the dissolved organic matter intermediate depths of the Primary Production in water. It is also known as ocean between approximately – fixation of carbon by chromophoric dissolved organic 100 and 1000 meters and marine plants, the primary matter, yellow substance, below the euphotic zone. mechanism by which carbon and gelbstoff. (and energy) enters marine Microbial food web – a food webs. DOC – dissolved organic specific type of foodweb carbon, major pool of that includes bacteria and exchangeable carbon in their role in producing the ocean. and consuming dissolved organic matter.

48 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Appendix III Compilation, by year through June 2011, of peer-reviewed publications arising from work at or near the Bermuda Atlantic Time-series Study (BATS) site

2011 Sparks, T.H., Butchart, S.H.M., *Krause, J.W., Nelson, D.M., , V., Friedrichs, M.A.M., Balmford, A., Bennun, L., Lomas, M.W. 2010. Production, Carr, M-E., Antoine, D., Beman, J.M., Chow, C.–E., Stanwell-Smith, D., Walpole, M., dissolution and potential export Armstrong, R., Asanuma, King, A.L., Feng, Y., Fuhrman, Bates, N.R., Bombard, B., Bruno, of biogenic silica in a Sargasso Sea I., Aumont,O., Bates, N.R., J.A., Andersson, A., Bates, J., Buchanan, G., Chenery, A.M., mode-water eddy. Limnology and Behrenfeld, M., Bennington, N.R., Popp, B.N., and Hutchins, Collen, B., Csirke, J., Diaz, R.J., Oceanography, 55: 569–579. V., Bopp, L., Bruggemann, J., D.A., 2011. Global declines Dulvey, N.K., Fitzgerald, C., Buitenhuis, E.T., Ciotti, A., in oceanic nitrification rates Kapos, V., Mayaux, P., Selig, Lomas, M.W., Burke, A., Doney, S.C., Dowell, M., Dunne, as a consequence of ocean E., Tierney, M., Waycott, M., Lomas, D.A., Bell, D.W., Shen, J., Dutkiewicz, S., Gregg, W., acidification. Proceedings of the Wood, L., and Green, R.E., in C., Ammerman, J.W., and Hoepffner, N., Hyde, K.J.W., National Academy of Sciences. press. Linked indicator sets for Dyhrman, S.T. 2010. Sargasso Ishizaka, I., Kameda, J., Lima, 108(1), 208–213, doi: 10.1073/ addressing biodiversity loss. Sea phosphorus biogeochemistry: I., Lomas, M.W., Marra, J., pnas.1011053108. Oryx—The International Journal An important role for dissolved McKinley, G.A., Melin, F., organic phosphorus (DOP). Bibby T.S., Moore C.M. of Conservation. 1–9, Oryx– Moore, J.K., Morel, A., O’Reilly, Biogeosciences, 7: 695–710. J., Salihoglu, B., Scardi, M., 2011. Silicate: nitrate ratios of 10–A–0228.RI, doi:10.1017/ Smyth, T.J., Tang, S., Tjiputra, upwelled waters control the S003060531100024X. Lomas, M.W., Steinberg, D.K., J., Uitz, J., Vichi, M., Waters, phytoplankton community Dickey, T., Carlson, C.A., Nelson, Stewart, G., Moran, S.B., Lomas, K., Westbury, T.K., and Yool, sustained by mesoscale eddies in N.B., Condon, R.H. and Bates, M.W., Kelly, R.O. 2011. Applying A. 2010. The challenges of sub-tropical North Atlantic and 210 234 N.R., 2010. Increased carbon both Po and Th as POC flux modeling depth-integrated Pacific. Biogeosciences, 8: 657–666. tracers at the Bermuda Atlantic export is countered by increased mesopelagic attenuation in the marine primary productivity Kadko, D., Prospero, J. Time Series Site. Journal of over multiple decades: A case Environmental Radioactivity, in press. Sargasso Sea. Biogeosciences, 7: 2010. Deposition of Be–7 to 57–70. study at BATS and HOT. Global Bermuda and the regional ocean: Thrash J.C., Cho J.C., Bertagnolli Biogeochemical Cycles, 24: GB3020, Environmental factors affecting A.D., Ferriera S., Johnson J., Longnecker, K., Lomas, doi:10.1029/2009GB003655. estimates of atmospheric flux to M.W., and Van Mooy, B.A.S., Vergin K.L., Giovannoni, S.J., Stewart, G., Moran, S.B., and the ocean. Journal of Geophysical 2010. Characterizing the 2011. Genome Sequence of Lomas, M.W. 2010. Deficit of Research,—Oceans, 116: C02013. the Marine Janibacter Sp Strain abundance and diversity of heterotrophic bacterial cells polonium-210 predicts particulate Lee J.M., Boyle E.A., Echegoyen- HTCC2649. Journal of Bacteriology, organic carbon flux from winter 193: 584–585. assimilating phosphate in the sub- Sanz Y., Fitzsimmons J.N., tropical North Atlantic Ocean. through spring at the Bermuda Zhang R.F., Kayser R.A. Tucker K.P., Parsons R., Environmental Microbiology, in press. Atlantic Time Series (BATS) site. 2011. Analysis of trace metals (Cu, Symonds E.M., Breitbart, M. Deep-Sea Research I, 57: 113–124. Cd, Pb, and Fe) in seawater using Malmstrom, R.R., Coe, A., 2011. Diversity and distribution Stramska, M., 2010. The diffusive single batch nitrilotriacetate resin of single-stranded DNA phages in Kettler, G.C., Martiny, A.C., extraction and isotope dilution Frias-Lopez, J., Zinser, E.R., component of particulate organic the North Atlantic Ocean. ISME carbon export in the North inductively coupled plasma mass Journal, 5: 822–830. Chisholm, S.W. 2010. Temporal spectrometry. Analytica Chimica Dynamics of Prochlorococcus Atlantic estimated from SeaWiFS Acta, 686: 93–101. Ecotypes in the Atlantic and ocean color. Deep-Sea Research I, 2010 Pacific Oceans. ISME Journal, 4: 57: 284–96. Levine, N.M., Doney, S.C., Lima Bates, N.R., Amat, A., and 1252–1264. I., Wanninkhof, R., Sabine, C.L., Twining, B., Nunez-Milland, Andersson, A.J., 2010. The D., Vogt, S., Johnson, R., and Feely, R.A., and Bates,N.R., in Mattern, J., Dowd, M., and interaction of carbonate chemistry Sedwick P., 2010. press. The impact of interannual Fennel, K., 2010. Sequential data Variations and coral reef calcification: the in Synechococcus cell quotas of variability on the uptake and carbonate chemistry coral reef assimilation applied to a physical- accumulation of anthropogenic biological model for the Bermuda phosphorus, sulfur, manganese, ecosystem feedback (CREF) iron, nickel, and zinc within CO in the North Atlantic. Global Atlantic time series station Journal 2 hypothesis. Biogeosciences, 7 (5), mesoscale eddies in the Sargasso Biogeochemical Cycles. of Marine Systems, 79: 144–156. 2509–2530, doi:10.5194/bg–7– Sea. Limnology and Oceanography, Lomas, M.W., and Moran, S.B.. 2509–2010. Orchard, E.D., Benitez-Nelson, 55: 492–506. 2011. Evidence for aggregation C.R., Pellechia, P.J., Lomas, Fouilland, E., Mostajir, B. Vila-Costa M., Rinta-Kanto and export of cyanobacteria M.W., Dyhrman, S.T. 2010. 2010. Revisited phytoplanktonic J.M., Sun S.L., Sharma, and nano-eukaryotes from the Polyphosphate in Trichodesmium carbon dependency of S., Poretsky, R., Moran, Sargasso Sea euphotic zone. from the low phosphorus heterotrophic bacteria in M.A. 2010. Transcriptomic Biogeosciences, 8, 203–216. freshwaters, transitional, coastal Sargasso Sea. Limnology & Oceanography, 55: 2161–2169. analysis of a marine bacterial Michelou, V.K., Lomas, M.W., and oceanic waters. FEMS. community enriched with Kirchman, D.L. 2011. Phosphate Microbial Ecology, 73(3):419-429. Orchard, E.D., Ammerman, J.W., dimethylsulfoniopropionate. ISME Journal, 4: 1410–1420. and ATP uptake by cyanobacteria Helmke, P., Lomas, M.W., Lomas, M.W., and Dyhrman, and heterotrophic bacteria in S.T., 2010. Dissolved inorganic Conte, M., Köster, J., and Neuer, While, J., Haines, K. 2010. A the Sargasso Sea. Limnology and and organic phosphorus uptake S. What determines the variability comparison of the variability Oceanography, 56:323–332. in Trichodesmium and the microbial of organic carbon export and flux of biological nutrients against attenuation in the subtropical community: The importance of Popendorf, K., Van Mooy, B.J., phosphorus ester in the Sargasso depth and potential density. Lomas, M.W. 2011. Microbial North Atlantic gyre? Deep-Sea Biogeosciences, 7: 1263–1269. Research I, 57: 213–227. Sea. Limnology and Oceanography, Sources of Intact Polar Membrane 55: 1390–1399. Lipids in the North Atlantic Knapp, A.N., Hastings, M.G., Ocean. Organic Geochemistry, Sigman, D.M., Lipschultz, F., in press. Galloway, J.N. 2010. The flux and isotopic composition of reduced and total nitrogen in Bermuda rain. Marine Chemistry, 120: 83–89.

49 Sargasso Sea Alliance – Oceanography of the Sargasso Sea 2009 Ducklow, H., Doney, Mourino-Carballido, B., Ullmann, D., McKinley, G., S., and Steinberg, D., 2009. Eddy-driven pulses of Bennington, V., and Dutkiewicz, Bates, N.R., Amat, A., and 2009. Contributions of Long- respiration in the Sargasso Sea. S., 2009. Trends in the North Andersson, A.J., 2009. The term Research and Time-series Deep-Sea Research I, 56: 1242– Atlantic carbon sink: 1992– interaction of carbonate chemistry Observations to Marine Ecology 1250. 2006. Global Biogeochemical Cycles, and coral reef calcification: the and Biogeochemistry. Annual 23: GB4011. carbonate chemistry coral reef Review of Marine Science 1: Mourino-Carballido, B., ecosystem feedback (CREF) 279–302. and Anderson L., 2009. Net Van Mooy, B.A.S., Fredricks, hypothesis. Biogeosciences— community production of oxygen H.F., Pedler, B.F., Dyhrman, Discussion, 6 (5), 6727–7672, Eden, B., Steinberg derived from in vitro and in situ S.T., Karl, D.M., Koblížek, M., manuscript bg–2009–171). D., Goldthwait, S.A., 1-D modeling techniques in a Lomas, M.W., Moore, L.R., and McGillicuddy, D., cyclonic mesoscale eddy in the Moutin, T., Rappé, M.S., and Birdsey, R., Bates, N.R., 2009. Zooplankton community Sargasso Sea. Biogeosciences, 6: Webb, E.A., 2009. Phytoplankton Behrenfield, M., Davis, K., structure in a cyclonic and mode- 1799–1810. in the oligotrophic ocean Doney, S.C., Feely, R.A., Hansell, water eddy in the Sargasso Sea. use non-phosphorus lipids in D.A., Heath, L.S., Kasischke, E., Deep-Sea Research I, 56: 1757–75. Reid, P.C., Fischer, A., Lewis- response to phosphorus scarcity. Law, B.E., Lee, C., McGuire, D., Brown, E., Meredith, M., Nature Geosciences, doi:10.1038/ Raymond, P., and Tucker, C.J., Goldberg, S.J., Carlson, C.A., Sparrow, M., Andersson, nature07659. 2009. Carbon cycle observations: Hansell, D.A., Nelson, N.B. and A.J., Antia, A., Bates, N.R., Gaps threaten climate mitigation Siegel, D.A. 2009. Temporal Bathmann, U., Beaugrand, G., Watson, A.J, Schuster, U., policies. EOS, Transactions, dynamics of dissolved combined Brix, H., Dye, S., Edwards, M., Bakker, D.C.E., Bates, N.R., American Geophysical Union, 90 neutral sugars and the quality of Furevik, T., Gangstø, R., Hátún, Corbiere, A., Gonzalez-Davila, (34), 292–293, 25 August 2009, dissolved organic matter in the H., Hopcroft, R.R., Kendall, M., M., Friedrich, T., Hauck, J., Paper 2009ES002647. Northwestern Sargasso Sea. Deep- Kasten, S., Keeling, R., Corinne Heinze, C., Johannessen, Sea Research I, 56: 672–685. Le Quéré, C., Mackenzie, T., Körtzinger, A., Metzl, Brew, H.S., Moran, S.B., Lomas, F.T., Malin, G., Mauritzen, C., N., Olafsson, J., Olsen, A., M.W., Burd, A.B., and Kelly, R.P. Huang, S, and Conte, M., Ólafsson, J., Paull, C., Rignot, Oschlies, A., Padin, X.A., 2009. Pico-plankton control of 2009. Source/process E., Shimada, K., Vogt, M., Pfiel, B., Santana-Casiano, particulate organic carbon and apportionment of major and trace Wallace, C., Wang, Z., and M., Steinhoff, T., Telszewski, thorium size distributions in the elements in sinking particles in Washington R., 2009. Impacts M., Rios, A.F., Wallace, Sargasso Sea: Implications for the Sargasso Sea. Geochimica et of the oceans on climate change. D.W.R., and Wanninkhof, R., carbon export. Journal of Marine Cosmochimica Acta, 73: 65–90. Advances In Marine Biology, 56, 2009. Accurately tracking the Research, 67: 845–868. Kaiser, K., and Benner, R., 1–150, doi: 10.1016/S0065– variation in the North Atlantic Carlson, C.A., Morris, R., 2009. Biochemical composition 2881(09)56001–4. sink for atmospheric CO2. Science, 326, 1391–1393. Parsons, R., Treusch, A.H., and size distribution of organic Schuster, U., Watson, A.J., Bates, Giovannoni, S.J., Vergin, matter at the Pacific and Atlantic N.R., Corbiere, A., Gonzalez- K. 2009. Seasonal dynamics Time-series stations. Marine Davila, M., Metzl, N., Pierrot, 2008 of SAR11 populations in the Chemistry, 113: 63–77. D., and Santana-Casiano, M., Bibby, T.S., Gorbunov, M.Y., euphotic and mesopelagic zones 2009. Trends in North Atlantic of the northwestern Sargasso Sea. Krause, J.W., Lomas, Wyman, K.W., Falkowski, sea-surface fCO from 1990 ISME Journal, 3: 283–295. M.W., and Nelson, D.M. 2 P.G. 2008. Photosynthetic 2009. Biogenic silica in the to 2006. Deep-Sea Research II, community responses to Casey, J., Lomas, M.W., Sargasso Sea: Hypothesized 56, 620–629, doi:10.1016/j. upwelling in mesoscale eddies in Michelou, V., Orchard, E.D., controls on temporal variability dsr2.2008.12.011. the subtropical North Atlantic and Dyhrman, S.T., Ammerman, Pacific Oceans. Deep-Sea Research based on a 15–year record Sowell S, Wilhelm L, Norbeck J.W., and Sylvan, J., II, 55:1310–1320. at the BATS site. Global A, Lipton M, Nicora C, 2009. Phytoplankton taxon- Biogeochemical Cycles, 23: GB3004, et al., 2009. Transport specific orthophosphate (Pi) and Black, W.J. and Dickey, T.D. doi:10.1029/2008GB003236. functions dominate the SAR11 ATP uptake in the northwestern 2008. Observations and analyses metaproteome at low-nutrient Atlantic subtropical gyre. Aquatic Krause, J.W., Nelson, of upper ocean responses to extremes in the Sargasso Sea. Isme Microbial Ecology, 58: 31–44. D.M., and Lomas, M.W. tropical storms and hurricanes in 2009. Biogeochemical responses Journal, 3: 93–105. the vicinity of Bermuda. Journal of The CLIMODE Group* Geophysical Research—Oceans 113: to late-winter storms in the Stanley, R., Jenkins, W., Lott, D., 2009. (Marshall, J., Andersson, 10.1029/2007JC004358. Sargasso Sea. II. Increased rates and Doney S.C., 2009. Noble A., Bates, N., Dewar, W., Doney, of biogenic silica production and gas constraints on air-sea gas S., Edson, J., Ferrari, R., Fratantoni, Buesseler, K.O., Lamborg, C., export. Deep-Sea Research I, 56: exchange and bubble fluxes. D., Gregg, M., Joyce, T., Kelly, K., Cai, P., Escoube, R., Johnson, 861–874. Journal of Geophysical Research— Lozier, S., Lumpkin, R., Samuelson, R., Pike, S., Masque, P., Oceans, 114: C11020. R., Skyllingstad, E., Straneo, F., Lomas, M.W., Lipschultz, F., McGillicuddy, D., Verdeny, E. Talley, L., Toole, J., and Weller, Nelson, D.M., and Bates, N.R., 2008. Particle fluxes associated Takahashi, T., Sutherland, S.C., with mesoscale eddies in the R.). Observing the cycle of 2009. Biogeochemical responses Wanninkhof, R., Sweeney, convection and restratification to late-winter storms in the Sargasso Sea. Deep-Sea Research II, C., Feely, R.A., Chipman, 55:1426–1444. over the Gulf Stream system Sargasso Sea. I. Pulses of new and D.W., Hales, B., Friederich, G., and the subtropical gyre of the primary production. Deep-Sea Chavez, F., Watson, A., Bakker, Ewart, C.S., Meyers, M.K., North Atlantic Ocean: preliminary Research I, 56: 843–860. D.C.E., Schuster, U., Metzl, Wallner, E.R., McGillicuddy, D.J., results from the CLIMODE Lomas, M.W., Roberts, N., N., Yoshikawa-Inoue, H., Ishii, Carlson, C.A. 2008. Microbial field campaign. Bulletin of the Lipschultz, F., Krause, J.W., M., Midorikawa, Nojiri, Y., dynamics in cyclonic and American Meteorological Society, Nelson, D.M., and Bates, N.R., Kortzinger, A., Steinhoff, T., anticyclonic mode-water eddies September, 2009, 1337–1350, 2009. Hoppema, M., Olafsson, J., in the northwestern Sargasso doi:10.1175/2009BAMS2706.1. Biogeochemical responses to late-winter storms in the Arnarson, T.S., Tilbrook, B., Sea. Deep-Sea Research II, 55: Johannessen, T., Olsen, A., Dickey, T.D., Bates, N.R., Byrne, Sargasso Sea. IV. Rapid succession 1334–1347. Bellerby, R., Wong, C.S., Delille, R.H., Chang, G., Chavez, F.P., of major phytoplankton groups. B., Bates, N.R., and de Baar, Goldthwait, S.A., Steinberg, Feely, R.H., Hansen, A., Karl, D., Deep-Sea Research I, 56: 892–908. H.J.W., 2009. Climatological D.K. 2008. Elevated biomass of Moore, C., Wanninkhof, R., and Luz, B., and Barkan, E., mean and decadal change in mesozooplankton and enhanced Sabine C.L., 2009. The NOPP 2009. surface ocean pCO , and net fecal pellet flux in cyclonic O-SCOPE and MOSEAN Projects: Net and gross oxygen 2 sea-air CO flux over the global and mode-water eddies in the Advanced sensing for ocean production from O-2/Ar, 2 oceans. Deep-Sea Research II, 56 Sargasso Sea. Deep-Sea Research II, observing systems. Oceanography, O-17/O-16 and O-18/O-16 (8–10), 554–577, doi:10.1016/j. 55: 1360–1377. 22(2): 168–181, June 2009. ratios. Aquatic Microbial Ecology, 56: 133–145. dsr2.2008.12.009.

50 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Goodkin, N.F., Hughen, K.A., 2007 LeQuere, C. et al., (including 2006 Curry, W.B., Doney, S.C. and N.R. Bates) 2007. Chapter 5. Andersson, A.J., Bates, N.R. and Angly, F.E., B. Felts, M. Breitbart, Ostermann, D.R. 2008. Sea Intergovernmental Panel on Climate Mackenzie, F.T. 2007. Dissolution P. Salamon, R. A. Edwards, C. surface temperature and Change (IPCC) 4th Assessment. of carbonate sediments Carlson, A. M. Chan, M. Haynes, salinity variability at Bermuda under rising pCO and ocean S. Kelly, H. Liu, J. M. Mahaffy, J. during the end of the Little 2 McGillicuddy, D.J., L.R. acidification: Observations from E. Mueller, J. Nulton, R. Olson, R. Ice Age. Paleooceanography 23: Anderson, N.R. Bates, T. Bibby, Devil’s Hole, Bermuda. Aquatic Parsons, S. Rayhawk, C. A. Suttle, 10.1029/2007PA001532. K.O. Buesseler, C.A., Carlson, C.S. Geochemistry 13: 237–264. Davis, C. Ewart, P.G. Falkowski, and F. Rohwer. 2006. The marine Gordon, A.L., Giulivi, C.F. S.A. Goldthwait, D.A. Hansell, viromes of four oceanic regions. Bates, N.R., 2007. Interannual 2008. Sea surface salinity W.J. Jenkins, R.J. Johnson, V.K. Plos Biology, 4: 2121–2131. variability of the oceanic CO trends over fifty years within 2 Kosnyrev, J.R. Ledwell, Q.P. LI, sink in the subtropical gyre of Brix, H., N. Gruber, D. Karl, and the subtropical North Atlantic. D.A. Siegel, D.K., Steinberg, the North Atlantic Ocean over N.R. Bates. 2006. Interannual Oceanography, 21:20–29. 2007. Eddy/wind interactions the last two decades. Journal variability of the relationship stimulate extraordinary mid- of Geophysical Research 112: between primary, net community Jackson, G.A. and Kiorboe, T. ocean plankton blooms. Science, doi:10.1029/2006JC003759. and export production in the 2008. Maximum phytoplankton 316:1021–1026. concentrations in the sea. subtropical gyres. Deep-Sea Research Bates, N.R.. and A.J. Peters. Limnology and Oceanography 53: Mulholland, M.R., M.W. Lomas, II, 53:698–717 2007. The contribution of acid 395–399. 2007. Nitrogen uptake and deposition to ocean acidification Connelly, D., P. Statham, and assimilation. In: Nitrogen in in the subtropical North Atlantic A.H. Knap. 2006. Seasonal Kamykowski, D. Estimating upper the Marine Environment, 2nd Ocean. Marine Chemistry, 107: changes in speciation of dissolved ocean phosphate concentrations Ed. (eds.) D.G. Capone, M.R. 547–558. chromium in the surface Sargasso using ARGO float temperature Mulholland, D.A. Bronk, E.J. profiles. Deep-Sea Research I, 55: Sea. Deep-Sea Research I, 53: Casey, J.R., M.W. Lomas, J. Carpenter. 1580–1589. 1975–1988. Mandecki, and D.E. Walker. Phillips, H.E. and Joyce, T.M. 2007. Prochlorococcus Contributes Davis, C. S., and D. McGillicuddy. Ledwell, J.R., McGillicuddy, D.J., 2007. Bermuda’s tale of two Time- to New Production in the 2006. Transatlantic abundance Anderson, L.A. 2008. Nutrient series: Hydrostation S and BATS. Sargasso Sea Deep Chlorophyll of the N -fixing colonial flux into an intense deep Journal of Physical Oceanography, 37, 2 Maximum. Geophysical Research cyanobacterium Trichodesmium. chlorophyll layer in a mode-water 554–571. eddy. Deep-Sea Research II, 55: Letters, Vol. 34, L10604, Science, 312: 1517–1521. 1139–1160. doi:10.1029/2006GL028725. Qian, J.T., D.J. McGillicuddy, D.A. Hansell, D.A., N.R. Bates, and Haines, K. and others Choi, D., J. Cho, B. L, S. 2006. Li, Q.P., Hansell, D.A., W.J. Jenkins, 2007. Uncertainty Salinity assiilation using Giovanonni, and B. Cho. McGillicuddy, D.J., Bates, N.R., in the biogeochemical impact of S(T): Covariance relationships. 2007. Maribius salinus gen. nov., Monthly Weather Review, Johnson, R.J. 2008. Tracer- a cyclonic eddy in the Sargasso 134: sp nov., isolated from a solar based assessment of the Sea. Journal of Geophysical Research 759–771. origin and biogeochemical saltern and Maribius pelagius sp (submitted). Henry-Edwards, A., and M. transformation of a cyclonic eddy nov., cultured from the Sargasso Tomczak. 2006. Detecting in the Sargasso Sea. Journal of Sea, belonging to the Roseobacter Salihoglu, B., V. Garcon, A. changes in Labrador Sea water Geophysical Research—Oceans, 113: clade. International Journal of Oschilies, and M.W. Lomas. through a water mass analysis of 10.1029/2008JC004840. Systematic and Evolutionary Influence of nutrient utilization Microbiology, 57: 270–275. and remineralization stoichiometry BATS data. Ocean Science, 2: 19–25. Sunda, W.G., Hardison, D.R. on phytoplankton species and Hernes, P.J., and R. Benner. 2008. Contrasting seasonal Cianca, A., Helmke, P., Mourino, carbon export: a modeling study 2006. Terrigenous organic matter patterns in dimethylsulfide, B., Rueda, M.J., Llinas, O. at BATS. Deep-Sea Research I, sources and reactivity in the North dimethylsulfoniopropionate, and and Neuer, S. 2007. Decadal 55:73–105. Atlantic Ocean and a comparison chlorophyll a in a shallow North analysis of hydrography and to the Arctic and Pacific oceans. Carolina estuary and the Sargasso in situ nutrient budgets in the Santana-Casiano, J.M., M. Marine Chemistry, 100: 66–79. Sea. Aquatic Microbial Ecology, western and eastern North Gonzalez-Davila, M.J. Rueda, O. 53:281–294. Atlantic subtropical gyre. Journal of Llinas, and E. F. Gonzalez-Davila. Hood, R.R. E.A. Laws, R.A. Geophysical Research—Oceans, 112: 2007. The interannual variability Armstrong, N.R. Bates, C.W. Tchernov, D. and Lipschultz, 10.1029/2006JC003788. of oceanic CO2 parameters in the Brown, C.A. Carlson, F. Chai, F. 2008. Carbon isotopic northeast Atlantic subtropical S.C. Doney, P.G., Falkowski, R.A. composition of Trichodesmium spp. Del Valle, D., D. Kieber, and R. gyre at the ESTOC site. Global Feely, M.A.M. Freidrichs, M.R. colonies off Bermuda: effects of Kiene. 2007. Depth-dependent Biogeochemical Cycles, 21: GB1015. Landry, J.K. Moore, D.M. Nelson, colony mass and season. Journal of fate of biologically-consumed T.L. Richardson, B. Salihoglu, M. Plankton Research 30:21–31. dimethylsulfide in the Sargasso Sedwick, P.N., Sholkovitz, E.R. Schartau, D.A. Toole, and J.D. Sea. Marine Chemistry, 103: and Church, T.M. 2007. Impact Wiggert, 2006. Functional Group Toole, D.A., Siegel, D.A. and 197–208. of anthropogenic combustion Modeling: progress, challenges and Doney, S.C. 2008. A light-driven, emissions on the fractional Hewson, I., P. Moisander, prospects. Deep-Sea Research II, 53: one-dimensional dimethylsulfide solubility of aerosol iron: K.M. Achilles, C.A. Carlson, 459–512. biogeochemical cycling model Evidence from the Sargasso Sea. for the Sargasso Sea. Journal of B.D. Jenkins, E. Mondragon, Geochemistry, Geophysics, Geosystems, Koeve W.C., 2006. C:N Geophysical Research—Biogeosciences A. Morrison, and J.P. Zehr. 8: 10.1029/2007GC001586. stoichiometry of the biological 113: 10.1029/2007JG000426. 2007. Characteristics of pump in the North Atlantic: diazotrophs in surface to Weber, L., Volker, C., Oschlies, Constraints from climatological Zafiriou, O.C., Xie, H.X., Nelson, abyssopelagic waters of the A. and Burchard, H. 2007. Iron data. Global Biogeochemical Cycles, N.B., Najjar, R.G. and Wang, Sargasso Sea. Aquatic Microbial profiles and speciation of the 20 (3): Art. No. GB3018 SEP 7 W. 2008. Diel carbon monoxide Ecology, 46: 15–30. upper water column at the 2006. cycling in the upper Sargasso Bermuda Atlantic Time-series Sea near Bermuda at the onset Jiang, S.N., Dickey, T.D., Study site: a model based Lomas, M. W., and F. Lipschultz. of spring and in midsummer. Steinberg, D.K. and Madin, L.P. sensitivity study. Biogeosciences ,4: 2006. The primary nitrite Limnology and Oceanography, 53: 2007. Temporal variability of 689–706. maximum: Phytoplankton 835–850. zooplankton biomass from ADCP backscatter time series data at the or nitrifiers? Limnology and Bermuda Testbed Mooring site. Oceanography: Reviews, 51.2453– Deep-Sea Research I, 54: 608–636. 2467.

51 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Martin, A.P., and P. Pondaven. Colman, A., R. Blake, D. Karl, Mackenzie, T.D.B., J.M. Johnson, Sedwick, P.N. and others 2006. New primary production M. Fogel, and K. Turekian. A.M. Cockshutt, R.A. Burns, 2005. Iron in the Sargasso and nitrification in the western 2005. Marine phosphate oxygen and D.A. Campbell. 2005. Large Sea (Bermuda Atlantic Time- subtropical North Atlantic: isotopes and organic matter reallocations of carbon, nitrogen, series Study region) during A modeling study, Global remineralization in the oceans. and photosynthetic reductant summer: Eolian imprint, Biogeochemical Cycles. 20: GB4014, Proceedings of the National Academy among phycobilisomes, spatiotemporal variability, doi10.1029/2005GB002608. of Sciences of the United States of photosystems, and Rubisco during and ecological implications. America, 102: 13023–13028. light acclimation in Synechococcus Global Biogeochemical Cycles, Mourino-Carballido, B., and D.J. elongatus strain PCC7942 are 19,doi:10.1029/2004GB002445. McGillicuddy. 2006. Mesoscale Hays, G., A. Richardson, and constrained in cells under low variability in the metabolic balance C. Robinson. 2005. Climate environmental inorganic carbon. Tolli, J., and C. Taylor. of the Sargasso Sea. Limnology and change and marine plankton. Archives of Microbiology, 183: 2005. Biological CO oxidation in Oceanography, 51: 2675–2689. Trends in Ecology and Evolution, 20: 190–202. the Sargasso Sea and in Vineyard doi:10.1016/j.tree.2005.1003.1004. , . Limnology Sholkovitz, E.R., and P.N. Maranon, E. 2005. Phytoplankton and Oceanography, 50: 1205–1212. Sedwick. 2006. Open-ocean Henry-Edwards, A., and M. growth rates in the Atlantic deployment of a buoy-mounted Tomczak. 2005. Remote subtropical gyres. Limnology and Ueyama, R., and B.C. Monger. aerosol sampler on the Bermuda detection of water property Oceanography, 50: 299–310. 2005. Wind-induced modulation Testbed Mooring: Aerosol iron changes from a Time-series of of seasonal phytoplankton blooms and sea salt over the Sargasso Sea. oceanographic data. Ocean Science Moore, L.R., M. Ostrowski, in the North Atlantic derived from Deep-Sea Research, 53: 547–560. Discussions, 2: 399–415. D. J. Scanlan, K. Feren, and satellite observations. Limnology T. Sweetsir. 2005. Ecotypic and Oceanography, 50: 1820–1829. Stanley, R., W.J. Jenkins, and Jiao, N. Z. and others variation in phosphorus acquisition S.C. Doney. 2006. Quantifying 2005. Dynamics of autotrophic mechanisms within marine Veldhuis, M.J.W., K.R. seasonal air-sea gas exchange picoplankton and heterotrophic picocyanobacteria. Aquatic Timmermans, P. Croot, processes using noble gas Time- bacteria in the . Microbial Ecology, 39: 257–269. and B. Van Der Wagt. series: A design experiment. Journal Continental Shelf Research, 25: 2005. Picophytoplankton; a of Marine Research, 64: 267–295. 1265–1279. Morris, R. M., K.L. Vergin, comparative study of their J.C. Cho, M.S. Rappe, C.A. biochemical composition and Toole, D., D. Slezak, R. Kiene, Keigwin, L., M. Bice, and N. Carlson, and S.J. Giovannoni. photosynthetic properties. Journal D. Kieber, and D. Siegel. Copley. 2005. Seasonality and 2005. Temporal and spatial of Sea Research, 53: 7–24. 2006. Effects of solar radiation stable isotopes in planktonic response of bacterioplankton on dimethylsulfide cycling in the foraminifera off , lineages to annual convective Weber, L., C. Volker, M. western Atlantic Ocean. Deep-Sea Massachusetts. Paleoceanography, overturn at the Bermuda Atlantic Schartau, and D.A. Wolf- Research I, 53: 136–153. 20.PA4011,doi:10.1029/2005 Time-series Study site. Limnology Gladrow. 2005. Modeling the PA001150. and Oceanography, 50: 1687–1696. speciation and biogeochemistry Tress, M., D. Cozzetto, A. of iron at the Bermuda Tramontano, and A. Valencia. Kettle, A.J. 2005. Comparison Mourino, B., E. Fernandez, R. Atlantic Time-series Study site. 2006. An analysis of the of the nonlocal transport Pingree, B. Sinha, J. Escanez, and Global Biogeochemical Cycles, Sargasso Sea resource and the characteristics of a series of one- D. DE Armas. 2005. Constraining 19,doi:10.1029/2004GB002340. consequences for database dimensional oceanic boundary effect of mesoscale features on composition. BMC Bioinformatics, layer models. Ocean Modelling, 8: carbon budget of photic layer in 2004 7: Art.213. 301–336. the NE subtropical Atlantic. Marine Ecology—Progress Series, 287: 45–52. Agusti, S. 2004. Viability and Van Mooy, B., G. Rocap, Kettle, A.J. 2005. Diurnal cycling niche segregation of Prochlorococcus H. Fredricks, C. Evans, and of carbon monoxide (CO) in the Nelson, C., and C.A. Carlson. and Synechococcus cells across the A.H. Devol. 2006. Sulfolipids upper ocean near Bermuda. Ocean 2005. A nonradioactive assay of Central Atlantic Ocean. Aquatic dramatically decrease phosphorus Modelling, 8: 337–367. bacterial productivity optimized Microbial Ecology, 36: 53–59. demand by picocyanobacteria in for oligotrophic pelagic oligotrophic marine environments. Knapp, A. N., D.M. Sigman, and Babiker, I.S., M.A.A. Mohamed, F. Lipschultz. 2005. N isotopic environments. Limnology and Proceedings of the Academy of Oceanography: Methods, 3: 211–220. K. Komaki, K. Ohta, and K. Kato. Natural Sciences of Philadelphia, 103: composition of dissolved organic 2004. Temporal variations in 8607–8612. nitrogen and nitrate at the Palter, J., M. Lozier, and R. the dissolved nutrient stocks in Bermuda Atlantic Time-series Barber. 2005. The effect of the surface water of the western Zinser, E. and others study site. Global Biogeochemical advection on the nutrient reservoir North Atlantic Ocean. Journal of 2006. Prochlorococcus ecotype Cycles, 19,GB1018,doi:10.1029/200 in the North Atlantic subtropical Oceanography, 60: 553–562. abundances in the North Atlantic 4GB002320. gyre. Nature, 437: 687–692. Ocean as revealed by an improved Babin, S.M., J.A. Carton, T.D. quantitative PCR method. Applied Kuhnert, H., T. Cruger, and J. Quinn, P., M. Cortes, and J. Dickey, and J.D. Wiggert. and Environmental Microbiology, 72: Patzold. 2005. NAO signature Bollmann. 2005. Morphological 2004. Satellite evidence of 723–732. in a Bermuda coral Sr/Ca record. variation in the deep ocean- hurricane-induced phytoplankton Geochemistry Geophysics Geosystems, dwelling coccolithophore blooms in an oceanic desert. 6,doi:10.1029/2004GC00786. 2005 Florisphaera profunda (Haptophyta). Journal of Geophysical Research— Levy, M., Y. Lehahn, J.M. Andre, European Journal of Phycology, 40: Oceans, 109. Anderson, T.R. 2005. Plankton 123–133. functional type modelling: running L. Memery, H. Loisel, and E. Bates, N.R., and D.A. Hansell. before we can walk? Journal of Heifetz. 2005. Production Rossby, T., C.N. Flagg, and K. 2004. Temporal variability of Plankton Research, 27: 1073–1081. regimes in the northeast Atlantic: Donohue. 2005. Interannual excess nitrate in the subtropical A study based on Sea-viewing variations in upper-ocean transport mode water of the North Atlantic Avery, G.B., W.J. Cooper, Wide Field-of-view Sensor by the Gulf Stream and adjacent Ocean. Marine Chemistry, 84: R.J. Kieber, and J.D. Willey. (SeaWiFS) chlorophyll and ocean waters between New 225–241. 2005. Hydrogen peroxide at the general circulation model mixed and Bermuda. Journal of Marine Bermuda Atlantic Time Series layer depth. Journal of Geophysical Research, 63: 203–226. Brix, H., N. Gruber, and C.D. Station: Temporal variability of Research—Oceans, 110. Keeling. 2004. Interannual seawater hydrogen peroxide. variability of the upper Marine Chemistry, 97: 236–244. Loncaric, N., G.J. Brummer, and ocean carbon cycle at D. Kroon. 2005. Lunar cycles and station ALOHA near Hawaii. Boushaba, K., and M. Pascual. seasonal variations in deposition Global Biogeochemical Cycles, 2005. Dynamics of the ‘echo’ fluxes of planktic foraminiferal 18,doi:1029/2004GB002245. effect in a phytoplankton system shell carbonate to the deep South with nitrogen fixation. Bulletin of Atlantic (central ). Mathematical Biology, 67: 487–507. Deep-Sea Research, 52: 1178–1188.

52 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Carlson, C.A., S.J. Giovannoni, Lefevre, N., A. Watson, A. Morrison, J.R., and N.B. Willey, J.D., R. J. Kieber, and G. B. D.A. Hansell, S.J. Goldberg, Olsen, A. Rios, F. Perez, and T. Nelson. 2004. Seasonal cycle of Avery. 2004. Effects of rainwater R. Parsons, and K. Vergin. Johannessen. 2004. A decrease phytoplankton UV absorption at iron and hydrogen peroxide on 2004. Interactions among in the sink for atmospheric the Bermuda Atlantic Time-series iron speciation and phytoplankton dissolved organic carbon, microbial CO2 in the North Atlantic. Study (BATS) site. Limnology and growth in seawater near Bermuda. processes, and community Geophysical Research Letters, 31: Oceanography, 49: 215–224. Journal of Atmospheric Chemistry, 47: structure in the mesopelagic zone doi:10.1029/2003GL018957. 209–222. of the northwestern Sargasso Sea. Nelson, N.B., D.A. Siegal, and Leffanue, H., and M. Tomczak. J.A. Yoder. 2004. The spring Limnology and Oceanography, 49: 2003 1073–1083. 2004. Using OMP analysis to bloom in the northwestern observe temporal variability in Sargasso Sea: spatial extent and Anderson, T. R., and P. Pondaven. Cho, J.C., and S.J. Giovannoni. water mass distribution. Journal of relationship with winter mixing. 2003. Non-redfield carbon and 2004. Oceanicola granulosus Marine Systems, 48: 3–14. Deep-Sea Research, 51: 987–1000. nitrogen cycling in the Sargasso gen. nov., sp nov and Oceanicola Sea: pelagic imbalances and batsensis sp nov., poly-beta- Lima, I.D., and S.C. Doney. Nelson, N.B., C.A. Carlson, and export flux. Deep-Sea Research, 50: hydroxybutyrate-producing 2004. A three-dimensional, D.K. Steinberg. 2004. Production 573–591. marine bacteria in the order multinutrient, and size- of chromophoric dissolved organic ‘Rhodobacterales’. International structured ecosystem model matter by Sargasso Sea microbes. Arimoto, R., R. A. Duce, B. J. Journal of Systematic and Evolutionary for the North Atlantic. Marine Chemistry, 89: 273-287. Ray, and U. Tomza. 2003. Dry Microbiology, 54: 1129–1136. Global Biogeochemical Cycles, deposition of trace elements 18,doi:1029/2003GB002146. Schollaert, S.E., T. Rossby, and to the western North Atlantic. Church, M.J., H.W. Ducklow, J. A. Yoder. 2004. Gulf Stream Global Biogeochemical Cycles and D.A. Karl. 2004. Light Liu, H.B., M. DaggG, L. cross-frontal exchange: possible 17,doi:1029/2001GB001046. dependence of H-3 leucine Campbell, and J. Urban-Rich. mechanisms to explain interannual incorporation in the oligotrophic 2004. Picophytoplankton and variations in phytoplankton Bertilsson, S., O. Berglund, D. North Pacific Ocean. Applied and bacterioplankton in the Mississippi chlorophyll in the Slope Sea during M. Karl, and S. W. Chisholm. Environmental Microbiology, 70: River plume and its adjacent the SeaWiFS years. Deep-Sea 2003. Elemental composition 4079–4087. waters. Estuaries, 27: 147–156. Research, Part II, 51: 173-188. of marine Prochlorococcus and Synechococcus: Implications for the Cropp, R.A., J. Norbury, A.J. Lomas, M.W., A. Swain, R. Stanley, R.H.R., K.O. Buesseler, ecological stoichiometry of the sea. Gabric, and R.D. Braddock. Shelton, and J. W. Ammerman. S.J. Manganini, D.K. Steinberg, Limnology and Oceanography, 48: 2004. Modeling dimethylsulphide 2004. Taxonomic variability of and J.R. Valdes. 2004. A 1721–1731. production in the upper ocean. phosphorus stress in Sargasso comparison of major and minor Global Biogeochemical Cycles, Sea phytoplankton. Limnology and elemental fluxes collected in Bird, C., and M. Wyman. 18,doi:10.1029/2003GB002126. Oceanography, 49: 2303–2310. neutrally buoyant and surface- 2003. Nitrate/nitrite tethered sediment traps. Deep-Sea assimilation system of the marine Garcia-Fernandez, J.M., Lomas, M.W., and N.R. Bates. Research, 51: 1387-1395. picoplanktonic cyanobacterium and J. Diez. 2004. Adaptive 2004. Potential controls on Synechococcus sp strain WH 8103: mechanisms of nitrogen and interannual partitioning of organic Steinberg, D.K., N. Nelson, Effect of nitrogen source and carbon assimilatory pathways carbon during the winter/spring C.A. Carlson, and A. availability on gene expression. in the marine cyanobacteria phytoplankton bloom at the Prusak. 2004. Production of Applied and Environmental Prochlorococcus. Research in Bermuda Atlantic Time-series chromophoric dissolved organic Microbiology, 69: 7009–7018. Microbiology, 155: 795–802. Study (BATS) site. Deep-Sea matter (CDOM) in the open ocean Research I, 51: 1619–1636. by zooplankton and the colonial Brzezinski, M. A., J. L. Jones, K. Hansell, D.A., N.R. Bates, and cyanobacterium Trichodesmium spp. D. Bidle, and F. Azam. 2003. The D.B. Olson. 2004. Excess nitrate Losa, S.N., G.A. Kivman, and Marine Ecology—Progress Series, 267: balance between silica production and nitrogen fixation in the North V.A. Ryabchenko. 2004. Weak 45–56. and silica dissolution in the Atlantic Ocean. Marine Chemistry, constraint parameter estimation sea: Insights from Monterey 84: 243–265. for a simple ocean ecosystem Toole, D.A., and D.A. Siegel. Bay, California, applied to the model: what can we learn about 2004. Light-driven cycling of global data set. Limnology and Hansell, D.A., H.W. Ducklow, A. the model and data? Journal of dimethylsulfide (DMS) in the Oceanography, 48: 1846–1854. MacDonald, and M. Baringer. Marine Systems, 45: 1–20. Sargasso Sea: Closing the loop. 2004. Metabolic poise in the Geophysical Research Letters, 31. Cho, J. C., and S. J. Giovannoni. North Atlantic Ocean diagnosed Mazard, S.L., N.J. Fuller, K.M. 2003. Croceibacter atlanticus from organic matter transport. Orcutt, O. Bridle, and D.J. Tositti, L., S. Hubener, gen. nov., sp nov., a novel Limnology and Oceanography, 49: Scanlan. 2004. PCR analysis of H.J. Kanter, W. Ringer, S. marine bacterium in the family 1084–1094. the distribution of unicellular Sandrini, and L. Tobler. Flavobacteriaceae. Systematic and cyanobacterial diazotrophs in 2004. Intercomparison of Applied Microbiology, 26: 76–83. Keeling, C.D., H. Brix, and N. the . Applied and sampling and measurement of Gruber. 2004. Seasonal and Environmental Microbiology, 70: Be–7 in air at four high-altitude Cho, J.C., and S.J. Giovannoni. Long-term dynamics of the 7355–7364. locations in Europe. Applied 2003. Parvularcula bermudensis gen. upper ocean carbon cycle at Radiation and Isotopes, 61: 1497– nov., sp nov., a marine bacterium Station ALOHA near Hawaii. Mckinley, G., M. Follows, and 1502. that forms a deep branch in the Global Biogeochemical Cycles, J. Marshall. 2004. Mechanisms alpha-Proteobacteria. International 18,doi:1029/2004GB002227. of air-sea CO2 flux variability Venter J.C., K. Remington, J.F. Journal of Systematic and Evolutionary in the equatorial Pacific and Heidelberg, A.L. Halpern, D. Microbiology, 53: 1031–1036. Keigwin, L.D. 2004. Radiocarbon the North Atlantic. Global Rusch, J.A. Eisen, D.Y. Wu, I. and stable isotope constraints Biogeochemical Cycles, 18: Paulsen, K.E. Nelson, W. Nelson, Conte, M. H., T.D. Dickey, J.C. on and doi:10.1029/2003GB002179. D.E. Fouts, S. Levy, A.H. Knap, Weber, R.J. Johnson, and A.H. ventilation M.W. Lomas, K. Nealson, O. Knap. 2003. Transient physical in the western North Morris, R.M., M.S. Rappe, E. White, J. Peterson, J. Hoffman, forcing of pulsed export of Atlantic. Paleoceanography, Urbach, S.A. Connon, and S. J. R. Parsons, H. Baden-Tillson, bioreactive material to the deep 19,doi:10.1029?2004PA001029. Giovannoni. 2004. Prevalence C. Pfannkoch, Y.H. Rogers, and Sargasso Sea. Deep-Sea Research, 50: of the Chloroflexi-related H.O. Smith. 2004. Environmental 1157–1187. Le Clainche, Y., M. Levasseur, SAR202 bacterioplankton cluster genome shotgun sequencing of A. Vezina, J.W.H. Dacey, and throughout the mesopelagic the Sargasso Sea. Science, 304: Dickson, R.R., R. Curry, and I. F. Saucier. 2004. Behaviour of zone and deep ocean. Applied and 66–74. Yashayaev. 2003. Recent changes the ocean DMS(P) pools in the Environmental Microbiology, 70: in the North Atlantic. Philosophical Sargasso Sea viewed in a coupled 2836–2842. Transactions of the Royal Society physical-biogeochemical ocean of London Series a—Mathematical model. Canadian Journal of Fisheries Physical and Engineering Sciences, and Aquatic Sciences, 61: 788–803. 361: 1917–1933.

53 Sargasso Sea Alliance – Oceanography of the Sargasso Sea El Alaoui, S., J. Diez, F. Karl, D.M., N.R. Bates, S. Mishonov, A.V., W.D. Vaillancourt, R.D., J. Marra, Toribio, G. Gomez-Baena, A. Emerson, P.J. Harrison, C. Gardner, and M.J. Richardson. M.P. Seki, M.L. Parsons, and Dufresne, and J. M. Garcia- Jeandal, K.K. Liu, J.-C. Marty, 2003. Remote sensing and surface R.R. Bidigare. 2003. Impact of a Fernandez. 2003. Glutamine A.F. Michaels, J.C. Miquel, S. POC concentration in the South cyclonic eddy on phytoplankton synthetase from the marine Neuer, Y. Nojiri, and C.S. Wong, Atlantic. Deep-Sea Research II, 50: community structure and cyanobacteria Prochlorococcus spp.: 2003. Temporal studies of 2997-3015. photosynthetic competency in characterization, phylogeny and biogeochemical processes in the the subtropical North Pacific response to nutrient limitation. world’s oceans during the JGOFS Mongin, M., D.M. Nelson, P. Ocean. Deep-Sea Research Part I, 50: Environmental Microbiology, 5: era. In Ocean Biogeochemistry: Pondaven, M.A. Brzezinski, and 829–847. 412–423. The Role of the ocean Carbon Cycle P. Treguer. 2003. Simulation of in Global Climate Change. (M.R. upper-ocean biogeochemistry Westberry, T.K., and D.A. Siegel. Eshel, G. 2003. North Atlantic FASHAM, ed.), Springer, pp. with a flexible-composition 2003. Phytoplankton natural thermal persistence and 239–265. phytoplankton model: C, N and fluorescence variability in the coherent evolution. Journal of Si cycling in the western Sargasso Sargasso Sea. Deep-Sea Research I, Geophysical Research—Oceans, Katz, R.W., M.B. Parlange, and Sea. Deep-Sea Research Part I, 50: 50: 417–434. 108,doi:10.1029/2001JC001180. C. Tebaldi. 2003. Stochastic 1445-1480. modeling of the effects of large- Worden, A.Z., and B.J. Binder. Fasham, M.J.R. 2003. JGOFS: scale circulation on daily weather Obernosterer, I., N. Kawasaki, 2003. Application of dilution a retrospective view. In Ocean in the southeastern US. Climatic and R. Benner. 2003. P-limitation experiments for measuring Biogeochemistry: The Role of the Change, 60: 189-216. of respiration in the Sargasso growth and mortality rates among ocean Carbon Cycle in Global Climate Sea and uncoupling of bacteria Prochlorococcus and Synechococcus Change. (M.R. FASHAM, ed.), Latif, M. 2003. Tropical Pacific from P-regeneration in size- populations in oligotrophic Springer, pp. 270–277. influences on the North Atlantic fractionation experiments. Aquatic environments. Aquatic Microbial . Annals of Microbial Ecology, 32: 229–237. Ecology, 30: 159–174. Friis, K., A. Kortzinger, and Geophysics, 46: 99-107. D. Wallace. 2003. The salinity Paffenhofer, G.A., and M.G. normalization of marine Kieber, R.J., J.D. Willey, and Mazzocchi. 2003. Vertical 2002 inorganic carbon chemistry data. G.B. Avery. 2003. Temporal distribution of subtropical Bates, N.R. 2002. Seasonal Geophysical Research Letters, 30: variability of rainwater iron epiplanktonic copepods. Journal of variability of the effect of coral doi:10.1029/2002GL015898. speciation at the Bermuda Plankton Research, 25: 1139–1156. reefs on seawater CO2 and air- Atlantic time series station. Journal sea CO exchange. Limnology and Rocap, G. and others 2 Goldman, J.C., and D.J. of Geophysical Research-Oceans, Oceanography, 47: 43–52. McGillicuddy. 2003. Effect of 108,doi:10.1029/2001JC001031. 2003. Genome divergence in two large marine diatoms growing Prochlorococcus ecotypes reflects Bates, N.R. 2002. Interannual at low light on episodic new Kim, G., N. Hussain, and T.M. oceanic niche differentiation. variability in the global ocean production. Limnology and Church. 2003. Tracing the Nature, 424: 1042–1047. uptake of CO2. Geophysical Research Oceanography, 48: 1176–1182. advection of organic carbon into Letters, 29(5): Art. No. 1059 MAR Schartau, M., and A. Oschilies. the subsurface Sargasso Sea using a 1 2002. Gonzalez-Davila, M., J.M. Ra-228/Ra-226 tracer. Geophysical 2003. Simultaneous data-based Santana-Casiano, M.J. Rueda, Research Letters, 30. optimization of a 1D-ecosystem Bates, N.R. A.C. Pequignet, R.J. O. Llinas, and E. F. Gonzalez- model at three locations in the Johnson, and N. Gruber, 2002. Davila. 2003. Seasonal and Lefevre, N., A.H. Taylor, F.J. North Atlantic: Part II—Standing A short-term sink for atmospheric interannual variability of sea- Gilbert, and R.J. Geider. stocks and nitrogen fluxes. Journal CO2 in Subtropical Mode Water of surface carbon dioxide species at 2003. Modeling carbon to of Marine Research, 61: 795–821. the North Atlantic Ocean Nature, the European Station for Time nitrogen and carbon to chlorophyll 420, 389–393. Series in the Ocean at the Canary a ratios in the ocean at low Sullivan, M., J. Waterbury, and Islands (ESTOC) between 1996 latitudes: Evaluation of the role of S. Chisholm. 2003. Cyanophages Carlson, C.A. 2002. Production and 2000. Global Biogeochemical physiological plasticity. Limnology infecting the oceanic and Removal Processes. In: Cycles, 17. and Oceanography, 48: 1796-1807. cyanobacterium Prochlorococcus. Biogeochemistry of Marine Dissolved Nature, 424: 1047–1050. Organic Matter (eds. D.A. Hansell, Hastings, M.G., D.M. Losa, S.N., G.A. Kivman, J. C.A. Carlson). Academic Press, Sweeney, E.N., D.J. McGillicuddy, Sigman, and F. Lipschultz. Schroter, and M. Wenzel. Amsterdam, pp. 91–152. 2003. Isotopic evidence for 2003. Sequential weak constraint and K.O. Buesseler. source changes of nitrate in parameter estimation in an 2003. Biogeochemical impacts Carlson, C.A. and others rain at Bermuda. Journal of ecosystem model. Journal of Marine due to mesoscale eddy activity in 2002. Effect of nutrient Geophysical Research—Atmospheres, Systems, 43: 31-49. the Sargasso Sea as measured at amendments on bacterioplankton 108,doi.10.1029/2003JD003789. the Bermuda Atlantic Time-series production, community structure, Maranon, E., M. Behrenfeld, Study (BATS). Deep-Sea Research and DOC utilization in the Heldal, M., D. J. Scanlan, S. N. Gonzalez, B. Mourina, Part II, 50: 3017–3039. northwestern Sargasso Sea. Aquatic Norland, F. Thingstad, and and M. Zubkov. 2003. High Microbial Ecology, 30: 19–36. N. H. Mann. 2003. Elemental variability of primary production Tanaka, T., Y. W. Watanabe, composition of single cells in the oligotrophic waters of the S. Watanabe, S. Noriki, N. Christian, J.R. and T.R. of various strains of marine Atlantic Ocean: uncoupling from Tsurushima, and Y. Nojiri. Anderson. 2002. Modeling Prochlorococcus and Synechococcus phytoplankton biomass and size 2003. Oceanic Suess effect of DOM biogeochemistry. In: using X-ray microanalysis. Limnology structure. Marine Ecology-Progress delta C-13 in subpolar region: The Biogeochemistry of Marine Dissolved and Oceanography, 48: 1732–1743. Series, 257: 1-11. North Pacific. Geophysical Research Organic Matter (eds. D.A. Hansell, Letters, 30. C.A. Carlson). Academic Press, Jenkins, W.J., and S.C. Doney. Martin, A.P., and P. Pondaven. Amsterdam, Toole, D.A., D. Kieber, R. 2003. The subtropical nutrient 2003. On estimates for the pp. 717–756. spiral. Global Biogeochemical Cycles, vertical nitrate flux due to Kiene, D.A. Siegel, and N.B. 17,doi:10.1229/2003GB002085. eddy pumping. Journal of Nelson. 2003. Photolysis and the Conte, M.H., and J.C. Weber. Geophysical Research-Oceans, dimethylsulfide (DMS) summer 2002. Long-range atmospheric Juranek, L.W., A.D. Russell, and 108,doi:10.1029/2003JC001841. paradox in the Sargasso Sea. transport of terrestrial biomarkers H.J. Spero. 2003. Seasonal oxygen Limnology and Oceanography, 48: to the western North Atlantic. and carbon isotope variability McGillicuddy, D.J., L.A. 1088–1100. Global Biogeochemical Cycles, in euthecosomatous pteropods Anderson, S.C. Doney, and 16,doi:10.1029/2002GB001922. from the Sargasso Sea. Deep-Sea M. Maltrud. 2003. Eddy- Usbeck, R., R. Schlitzer, Research, 50: 231–245. driven sources and sinks of G. Fischer, and G. Wefer. Diekmann, R., and U. Piatkowski. nutrients in the upper ocean: 2003. Particle fluxes in the ocean: 2002. Early life stages of Results from a 0.1o resolution comparison of sediment trap cephalopods in the Sargasso Sea: model of the North Atlantic. data with results from inverse distribution and diversity relative Global Biogeochemical Cycles, 17: modelling. Journal of Marine to hydrographic conditions. Marine doi:10.1029/2002GB001987. Systems, 39: 167–183. Biology, 141: 123–130.

54 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Glover, D.M., S.C. Doney, A.J. Landry, M. R. 2002. Integrating Orcutt, K.M., Rasmussen, U., Takahashi, T., Sutherland, S.G., Mariano, R.H. Evans, and classical and microbial food web Webb, E.A., Waterbury, J.B., Sweeney, C., Poisson, A.P., Metzl, S.J. McCue. 2002. Mesoscale concepts: evolving views from Gundersen, K., and Bergman, N., Tilbrook, B., Bates, N.R., variability in time series data: the open-ocean tropical Pacific. B. 2002. Characterization of Wanninkhof, R.H., Feely, R.A., Satellite-based estimates for the Hydrobiologia, 480: 29–39. Trichodesmium spp. by genetic Sabine, C.L., and Olafsson, J. US JGOFS Bermuda Atlantic Time- techniques. Applied and 2002. Biological and temperature series Study (BATS) site. Journal Lee, K., D. M. Karl, R. Environmental Microbiology, 68: effects on seasonal changes of Wanninkhof, and J. Z. Zhang. of Geophysical Research—Oceans, 2236–2245. pCO2 in global ocean surface 107,doi:10.1029/2000JC000589. 2002. Global estimates of waters. Deep-Sea Research II, 49, net carbon production in the Oschilies, A. 2002. Can eddies 1601–1622. Gruber, N., C.D. Keeling, and nitrate-depleted tropical make ocean deserts bloom? N.R. Bates. 2002. Interannual and subtropical oceans. Global Biogeochemical Cycles, Witter, A.E. and Luther, G.W. variability in the North Atlantic Geophysical Research Letters, 16,doi:10.1029/2001GB001830. 2002. Spectrophotometric Ocean carbon sink. Science, 298: 29,doi:10.1029/2001GLO14198. measurement of seawater 2374–2378. Paffenhofer, G.A., and carbohydrate concentrations in Lefevre, M., Vezina, A., Mazzocchi, M.G. 2002. On neritic and oceanic waters from Grutzner, J. and others Levasseur, M., and Dacey, J.H.W. some aspects of the behaviour them US Middle Atlantic Bight 2002. Astronomical age models 2002. A model of dimethylsulfide of Oithona plumifera (Copepoda: and the Estuary. Marine for drift sediments dynamics for the subtropical North Cyclopoida). Journal of Plankton Chemistry, 77: 143–156. from the western North Atlantic Atlantic. Deep-Sea Research, 49: Research, 24: 129–135. (ODP Sites 1055–1063). Marine 2221–2239. Zedler, S.E., Dickey, T.D., Doney, Geology, 189: 5–23. Palinska, K.A. and others S.C., Price, J.F., Yu, X., and Lindell, D. and others 2002. The signal transducer P-II Mellor, G.L. 2002. Analyses and Gundersen, K., M. Heldal, S. 2002. Nitrogen stress response and bicarbonate acquisition in simulations of the upper ocean’s Norland, D. A. Purdie, and A.H. of Prochlorococcus strain PCC 9511 Prochlorococcus marinus PCC 9511, a response to Hurricane Felix at the Knap. 2002. Elemental C, N, and (Oxyphotobacteria) involves marine cyanobacterium naturally Bermuda Testbed Mooring site: P cell content of individual bacteria contrasting regulation of ntca deficient in nitrate and nitrite 13–23 August 1995. Journal of collected at the Bermuda Atlantic and amt1. Journal of Phycology 38: assimilation. Microbiology-Sgm, 148: Geophysical Research—Oceans, 107. Time-series Study (BATS) site. 1113–1124. 2405–2412. Limnology and Oceanography, 47: Zheng, X.B., Dickey, T., and 1525–1530. Lupschultz, F.J., Bates, N.R., Ragueneau, O., Dittert, N., Chang, G. 2002. Variability of the Carlson, C.A., and Hansell, D.A. Pondaven, P., Treguer, P., and downwelling diffuse attenuation Hansell, D.A. 2002. DOC in the 2002. New production in the Corrin, L. 2002. Si/C decoupling coefficient with consideration of global ocean carbon cycle. In: Sargasso Sea: history and current in the world ocean: is the Southern inelastic scattering. Applied Optics, Biogeochemistry of Marine Dissolved status. Global Biogeochemical Cycles, Ocean different? Deep-Sea Research, 41: 6477–6488. Organic Matter (eds. D.A. Hansell, 16,doi:10.1029/2000GB001319. 49: 3127–3154. C.A. Carlson). Academic Press, Amsterdam, pp. 685–716. Lomas, M.W., Bates, N.R., Roman, M.R., Adolf, H.A., 2001 Knap, A.H., Karl, D.M., Lukas, Landry, M.R., Madin, L.P., Bates, N.R. 2001. Interannual Jiao, N. Z., Y. H. Yang, H. R., Bidigare, R.R., Landry, M., Steinberg, and Zhang, X. variability of oceanic CO2 and Koshikawa, and M. Watanabe. Steinberg, D.K., and Carlson, 2002. Estimates of oceanic biogeochemical properties in the 2002. Influence of hydrographic C.A. 2002. Towards a revised mesozooplankton production: a Western North Atlantic subtropical conditions on picoplankton understanding of oceanic comparison using the Bermuda gyre. Deep-Sea Research, 48: distribution in the East China biogeochemical and ecosystem and Hawaii Time-series data. Deep- 1507–1528. Sea. Aquatic Microbial Ecology, 30: functioning. EOS, November. Sea Research, 49: 175–192. 37–48. Bates, N.R. 2001. Regional Lopez-Lozano, A., Diez, J., Saito, M.A., and Moffett, J.W. testbeds: Interannual variability of Jiao, N. Z., Y. H. Yang, H. El Alaoui, S., Coreno-Vivian, 2002. Temporal and spatial the oceanic carbon cycle at the Koshikawa, S. Harada, and M. C., Garcia-Fernandez, J.M. variability of cobalt in the Atlantic USA JGOFS Bermuda Atlantic Watanabe. 2002. Responses 2002. Nitrate is reduced by Ocean. Geochimica Et Cosmochimica Time-series Study (BATS) site. In of picoplankton to nutrient heterotrophic bacteria but not Acta, 66: 1943–1953. WOCE International Project Office, perturbation in the South China transferred to Prochlorococcus Schnetzer, A., and Steinberg, Report of the WOCE/JGOFS Sea, with special reference to in non-axenic cultures. Fems Ocean Transport Workshop, the coast-wards distribution of Microbiology Ecology, 41: 151–160. D.K. 2002. Active transport of particulate organic carbon and WOCE Report No. 174/2001, pp. Prochlorococcus. Acta Botanica Sinica, 43–46. 44: 731–739. Lutz, M., Dunbar, R., and nitrogen by vertically migrating Caldeira, K. 2002. Regional zooplankton in the Sargasso Sea. Bates, N.R., Samuels, L., and Kim, G., and T. M. Church. variability in the vertical Marine Ecology-Progress Series, 234: Merlivat, L. 2001. The influence 2002. Wet deposition of trace flux of particulate organic 71–84. of short-term wind variability on elements and radon daughter carbon in the ocean interior. air-sea CO exchange. Geophysical systematics in the South and Global Biogeochemical Cycles, Schnetzer, A., and Steinberg, 2 D.K. 2002. Natural diets of Research Letters, 28(17), 3281– equatorial Atlantic atmosphere. 16,doi:10.1029/2000GB001383. 3284. Global Biogeochemical Cycles, vertically migrating zooplankton 16,doi:10.1029/2001GB001407. Memery, L., Levy, M., Verant, in the Sargasso Sea. Marine Biology, Bates, N.R., Samuels, L, and S., and Merlivat, L. 2002. The 141: 89–99. Merlivat, L. 2001. Biogeochemical Koksharova, O. A., and C. P. relevant time scales in estimating Sheridan, C.C., Steinberg, D.K., and physical factors influencing Wolk. 2002. Genetic tools for the air-sea CO2 exchange in a mid- and Kling, G.W. 2002. The seawater fCO2, and airsea CO2 cyanobacteria. Applied Microbiology latitude region. Deep-Sea Research, exchange on the Bermuda coral and Biotechnology, 58: 123–137. 49: 2067–2092. microbial and metazoan community associated with reef. Limnology and Oceanography, Kuhnert, H., J. Patzold, B. Nelson, N.B., and Siegel, D.A. colonies of Trichodesmium spp,.: 46: 833–846. Schnetger, and G. Wefer. 2002. Chromophoric DOM in the a quantitative survey. Journal of Carlson, C.A., Bates, N.R., and 2002. Sea-surface temperature open ocean. In: Biogeochemistry of Plankton Research, 24: 913–922. Hansell, D.A., 2001. Ocean variability in the Marine Dissolved Organic Matter Steinberg, D.K., Goldthwait, Carbon Cycling. In Encyclopedia of at Bermuda inferred from (eds. D.A. Hansell, C.A. Carlson). Marine Science. coral records. Palaeogeography Academic Press, Amsterdam, pp. S.A., and Hansell, D.A. Palaeoclimatology Palaeoecology, 179: 547–578. 2002. Zooplankton vertical 159–171. migration and the active transport of dissolved organic and inorganic nitrogen in the Sargasso Sea. Deep- Sea Research, 49: 1445–1461.

55 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Cavender-bares, K.K., Karl, Fennel, K., Losch, M., Schroter, McGillicuddy, D.J., Kosneyrev, Sigel, D.A., and others. 2001. D.M., and Chisholm, S.W. J., and Wenzel, M. 2001. Testing K., Ryan, J.P., and Yoder, J.A. Bio-optical modeling of primary 2001. Nutrient gradients in a marine ecosystem model: 2001. Covariation of mesoscale production on regional scales: the the western North Atlantic sensitivity analysis and parameter ocean color and sea-surface Bermuda BioOptics project. Deep- Ocean: Relationship to microbial optimization. Journal of Marine temperature patterns in the Sea Research Part II—Topical Studies in community structure and Systems, 28: 45–63. Sargasso Sea. Deep-Sea Research II, Oceanography, 48: 1865–1896. comparison to patterns in the 48: 1823–1836. Pacific Ocean. Deep-Sea Research, Gregori, G., Colosimo, A., and Spitz, Y.H., Moisan, J.R., and 48: 2373–2395. Denis, M. 2001. Phytoplankton McGillicuddy, D.J., and Abbott, M.R. 2001. Configuring group dynamics in the Bay of Kosneyrev, V.K. 2001. Dynamical an ecosystem model using data Chang, F.C., and Smith, E.A. Marseilles during a 2-year survey interpolation of mesoscale flows from the Bermuda Atlantic 2001. Hydrological and dynamical based on analytical flow cytometry. in the TOPEX/poseidon diamond Time Series (BATS). Deep-Sea characteristics of summertime Cytometry, 44: 247–256. surrounding the US Joint Global Research Part II—Topical Studies in droughts over US Great Plains. Ocean Flux Study Bermuda Oceanography, 48: 1733–1768. Journal of Climate, 14: 2296–2316. Gundersen, K., Orcutt, K.M., Atlantic Time-series Study site. Purdie, D.A., Michaels, A.F., Journal of Geophysical Research— Steglich, C. and others Conte, M.H., Ralph, N., and and Knap, A.H. 2001. Particulate Oceans, 106: 16641–16656. 2001. Nitrogen deprivation Ross, E.H. 2001. Seasonal and organic carbon mass distribution strongly affects Photosystem II interannual variability in deep at the Bermuda Atlantic Time- Nelson, N.B. Bates, N.R., but not phycoerythrin level in the ocean particle fluxes at the series Study (BATS) site. Deep-Sea Siegel, D.A., and Michaels, A.F. divinyl- chlorophyll b-containing Oceanic Flux Program (OFP)/ Research II, 48: 1697–1718. 2001. Spatial variability of the CO2 cyanobacterium Prochlorococcus Bermuda Atlantic Time Series sink in the Sargasso Sea. Deep-Sea marinus. Biochimica Et Biophysica (BATS) site in the western Sargasso Hansell, D.A., and Carlson, C.A. Research Part II, 48: 1801–1821. Acta-Bioenergetics, 1503: 341–349. Sea near Bermuda. Deep-Sea 2001. Biogeochemistry of total Research II, 48: 1471–1505. organic carbon and nitrogen in the Ono, S., Ennyu, A., Najjar, R.G., Steinberg, D.K., Carlson, Sargasso Sea: control by convective and Bates, N.R. 2001. Shallow C.A., Bates, N.R., Johnson, Conte, M.H., Weber, J.C., overturn. Deep-Sea Research II, 48: remineralization in the Sargasso R.J., Michaels, A.F., and Knap, King, L.L., and Wakeham, S.G. 1649–1667. Sea estimated from seasonal A.H. 2001. Overview of the US 2001. The alkenone temperature variations in oxygen, dissolved JGOFS Bermuda Atlantic Time- signal in western North Atlantic Haidar, A.T., and Thierstein, H.R. inorganic carbon and nitrate. Deep- series Study (BATS): a decade- surface waters. Geochimica Et 2001. Coccolithophore dynamics Sea Research Part II—Topical Studies in scale look at ocean biology Cosmochimica Acta, 65: 4275–4287. off Bermuda (N. Atlantic). Deep- Oceanography, 48: 1567–1582. and biogeochemistry. Deep-Sea Sea Research II, 48: 1925–1956. Research Part II—Topical Studies in Crosbie, N.D., and Furnas, Orcutt, K.M., Lipschultz, F., Oceanography, 48: 1405–1447. M.J. 2001. Net growth rates of Hood, R.R., Bates, N.R., Gundersen, K., Arimoto, R., picocyanobacteria and nano-/ Capone, D.G., and Olson, D.B. Michaels, A.F, Knap, A.H., and microphytoplankton inhabiting 2001. Modeling the effect of Gallon, J.R.. 2001. A seasonal 2000 shelf waters of the central (17 nitrogen fixation on carbon and study of the significance of N-2 Bates, N.R., Merlivat, L., degrees S) and southern (20 nitrogen fluxes at BATS. Deep-Sea fixation by Trichodesmium spp. Beaumont, L., and Pequignet, degrees S) Great Barrier Reef. Research II, 48: 1609–1648. at the Bermuda Atlantic Time- A.C. 2000. Intercomparison Aquatic Microbial Ecology, 24: Karl, D.M., Dore, J.E., series Study (BATS) site. Deep-Sea of shipboard and moored 209–224. Michaels, A.F., and Bates, N.R. Research II, 48: 1583–1608. CARIOCA buoy seawater fCO2 2001. The USA JGOFS Time- measurements in the Sargasso Sea. Curry, R.G., and McCartney, Renaud, S., and Klass, C. Marine Chemistry, 72: 239–255. M.S. 2001. Ocean gyre circulation series Observation Programs. 2001. Seasonal variations changes associated with the Oceanography (November issue). in the morphology of the Bates, N.R., and Carlson, C.A. North Atlantic Oscillation. Journal Kiber, R.J., Cooper, W.J., coccolithophore Calcidiscus 2000. Linkages between ocean of Physical Oceanography, 31: Willey, J.D., and Avery, G.B. leptoporus off Bermuda (N. biogeochemistry at BATS and 3374–3400. 2001. Hydrogen peroxide at the Atlantic). Journal of Plankton modes of climate variability Bermuda Atlantic Time Series Research, 23: 779–795. (i.e., NAO, ENSO). USA JGOFS Dickey, T.D. and others Newsletter, 10 (3), 5–6. 2001. Physical and biogeochemical Station. Part 1: Temporal variability Rossby, T. and Zhang, H.M. variability from hours to years at of atmospheric hydrogen 2001. The near-surface velocity Binder, B. 2000. Cell cycle the Bermuda Testbed Mooring peroxide and its influence on and potential vorticity structure of regulation and the timing site: June 1994–March 1998. Deep- seawater concentrations. Journal of the Gulf Stream. Journal of Marine of chromosome replication Sea Research II, 48: 2105–2140. Atmospheric Chemistry, 39: 1–13. Research, 59: 949–975. in a marine Synechococcus (cyanobacteria) during light— Durand, M.D., Olson, Kim, G., and Church, T.M. Saito, M.A., and Moffett, J.W. 2001. Seasonal biogeochemical and nitrogen-limited growth. R.J., and Chisholm, S.W. 2001. Complexation of cobalt Journal of Phycology, 36: 120–126. 2001. Phytoplankton population fluxes of Th–234 and Po–210 in by natural organic ligands in dynamics at the Bermuda Atlantic the upper Sargasso Sea: Influence the Sargasso Sea as determined Buesseler, K.O. and others. Time series station in the Sargasso from atmospheric iron deposition. by a new high-sensitivity 2000. A comparison of the Sea. Deep-Sea Research II, 48: Global Biogeochemical Cycles, 15: electrochemical cobalt speciation quantity and composition of 1983–2003. 651–661. method suitable for open ocean material caught in a neutrally work. Marine Chemistry, 75: 49–68. buoyant versus surface-tethered Dutkiewicz, W., Follows, M., Lipschultz, F. 2001. A Time-series assessment of the nitrogen cycle sediment trap. Deep-Sea Research I, Marshall, J., and Gregg, W.W. Schartau, M., Oschlies, A., and 47: 277–294. 2001. Interannual variability of at BATS. Deep-Sea Research II, 48: Willebrand, J. 2001. Parameter phytoplankton abundances in the 1897–1924. estimates of a zero-dimensional Draschba, S., Patzold, J., and North Atlantic. Deep-Sea Research II, Madin, L.P., Horgan, ecosystem model applying the Wefer, G. 2000. North Atlantic 48: 2323–2344. E.F., and Steinberg, D.K. adjoint method. Deep-Sea Research climate variability since AD 2001. Zooplankton at the II, 48: 1769–1800. 1350 recorded in delta O-18 El Alaoui, S., Diez, J., Humanes, and skeletal density of Bermuda L., Toribio, F., Partensky, F., Bermuda Atlantic Time-series Siegel, D.A., Karl, D.M., Study (BATS) station: diel, seasonal corals. International Journal of Earth and Garcia-Fernandez, J.M. and Michaels, A.F. Sciences, 88: 733–741. 2001. In vivo regulation of and interannual variation in 2001. Interpretations of glutamine synthetase activity biomass, 1994–1998. Deep-Sea biogeochemical processes from Esaias, W.E., Iverson, R.L., in the marine chlorophyll b– Research II, 48: 2063–2082. the US JGOFS Bermuda and and Turpie, K. 2000. Ocean containing cyanobacterium Hawaii Time-series sites. Deep-Sea province classification using ocean Prochlorococcus sp strain PCC 9511 Research II, 48: 1403–1404. colour data: observing biological (oxyphotobacteria). Applied and signatures of variations in physical Environmental Microbiology, 67: dynamics. Global Change Biology, 6: 2202–2207. 39–55.

56 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Gilboy, T.P., Dickey, T.D., Sato, O.T., Polito, P.S. and Hurtt, G.C., and Armstrong, R.A. Carlson, C.A., Bates, N.R., and Sigurdson, D.E., Yu, Z., Liu, W.T. 2000. Importance of 1999. A pelagic ecosystem model Steinberg, D.K. 1998. BATS Time- and Manov, D. 2000. An salinity measurements in the heat calibrated with BATS and OWSI series celebrates a decade of ocean intercomparison of current storage estimation from TOPEX/ data. Deep-Sea Research I, 46: 27–61. research. USA JGOFS Newsletter, measurements using a vector POSEIDON. Geophysical Research November 1998. measuring current meter, an Letters, 27: 549–551. Keigwin, L.D., and Boyle, E.A. acoustic Doppler current profiler, 1999. Surface and deep ocean Carlson, C.A., Ducklow, H.W., and a recently developed Steinberg, D.K., Carlson, C.A., variability in the northern Sargasso Hansell, D.A., and Smith, W.O. acoustic current meter. Journal of Bates, N.R., Goldthwait, S.A., Sea during marine isotope stage 3. 1998. Organic carbon partitioning Atmospheric and Oceanic Technology, Madin, L.P., and Michaels, A.F. Paleoceanography, 14: 164–170. during spring phytoplankton 17: 561–574. 2000. Zooplankton vertical blooms in the polynya migration and the active transport Kim, G., Alleman, L.Y., and and the Sargasso Sea. Limnology and Haidar, A.T., Thierstein, H.R., and of dissolved organic and inorganic Church, T.M. 1999. Atmospheric Oceanography, 43: 375–386. Deuser, W.G. 2000. Calcareous carbon in the Sargasso Sea. Deep- depositional fluxes of trace phytoplankton standing stocks, Sea Research I, 47: 137–158. elements, Pb–210, and Be–7 to the Curry, R.G., McCartney, M.S., fluxes and accumulation in Sargasso Sea. Global Biogeochemical Joyce, T.M. 1998. Oceanic sediments off Bermuda Valdes, J.R., and Prices, J.F. Cycles, 13: 1183–1192. transport of subpolar climate 2000. A neutrally buoyant, upper signals to mid-depth subtropical (N. Atlantic). Deep-Sea Research II, Liu, H.B., Bidigare, R.R., Laws, E., 47: 1907–1938. ocean sediment trap. Journal of waters. Nature, 391: 575–577. Atmospheric and Oceanic Technology, Landry, M.R., and Campbell, L. Johnson, Z., and Howd, P. 17: 62–68. 1999. Cell cycle and physiological Dacey, J.W.H., Howse, F.A., 2000. Marine photosynthetic characteristics of Synechococcus Michaels, A.F., and Wakeham, performance forcing and Williams, R.G., Mclaren, A.J., and (WH7803) in chemostat culture. S.G. 1998. Temporal variability periodicity for the Bermuda Follows, M.J. 2000. Estimating Marine Ecology—Progress Series, 189: of dimethylsulfide and di- Atlantic Time Series, 1989– the convective supply of nitrate 17–25. methylsulfoniopropionate in the and implied variability in export Sargasso Sea. Deep-Sea Research I, 1995. Deep-Sea Research I, 47: McGillicuddy, D.J., Johnson, 1485–1512. production over the North 45 (12): 2085–2093. Atlantic. Global Biogeochemical R.K., Sigel, D.A., Michaels, A.F., Joyce, T.M., Deser, C., and Spall, Cycles, 14: 1299–1313. Bates, N.R., and Knap, A.H. Dickey, T.D., and others M.A. 2000. The relation between 1999. Mesoscale variations of 1998. Initial results from the biogeochemical properties in the Bermuda Testbed Mooring decadal variability of subtropical 1999 mode water and the North Sargasso Sea. Journal of Geophysical program. Deep-Sea Research Part I Atlantic Oscillation. Journal of Bates, N.R., and Hansell, D.A. Research—Oceans, 104: 13381– Oceanographic Research Papers, 45: Climate, 13: 2550–2569. 1999. A high resolution study 13394. 771–794. of surface layer hydrographic Mahadevan, A., and Archer, D. and biogeochemical properties McNeil, J.D., Jannasch, H.W., Flagg, C.N., Schwartze, G., 2000. Modeling the impact of between Chesapeake Bay and Dickey, T.D., McGillicuddy, D.J., Gottliev, E., and Rossby T. fronts and mesoscale circulation Bermuda. Marine Chemistry, 67: Brezezinski, M., and Sakamoto, 1998. Operating an acoustic on the nutrient supply and 1–16. C.M. 1999. New chemical, bio- Doppler current profiler aboard biogeochemistry of the upper optical and physical observations a container vessel. Journal of ocean. Journal of Geophysical Bissett, W.P., Walsh, J.J., of upper ocean response to the Atmospheric and Oceanic Technology, Research—Oceans, 105: 1209–1225. Dieterle, D.A., and Carder, passage of a mesoscale eddy off 15: 257–271. K.L. 1999. Carbon cycling in the Bermuda. Journal of Geophysical Oschilies, A., Koeve, W., and upper waters of the Sargasso Research—Oceans, 104: 15537– Gin, K.Y., Guo, J.H., Cheong, H.F. Garcon, V. 2000. An eddy- Sea: I. Numerical simulation of 15548. 1998. A size-based ecosystem permitting coupled physical- differential carbon and nitrogen model for pelagic waters. Ecological biological model of the North fluxes. Deep-Sea Research I, 46: Sachs, J.P., and Lehman, S.J. Modelling, 112: 53–72. 1999. Subtropical North Atlantic Atlantic 2. Ecosystem dynamics 205–269. Goericke, R. 1998. Response and comparison with satellite and temperatures 60,000 to 30,000 Carlson, C.A., Bates, N.R., and years ago. Science, 286: 756–759. of phytoplankton community JGOFS local studies data. Global structure and taxon-specific Biogeochemical Cycles, 14: 499–523. Steinberg, D.K. 1999. Ten years of BATS data. Earth System Monitor, Shipe, R.F., Brzezinski, M.A., growth rates to seasonally varying Palinska, K.A., Jahns, T., June 1999, p. 9–10. Pilskaln, C., and Villareal, physical forcing in the Sargasso Rippka, R., and De Marsac, N.T. T.A. 1999. Rhizosolenia mats: Sea off Bermuda. Limnology and 2000. Prochlorococcus marinus Caron, D.A., Peele, E.R., An overlooked source of silica Oceanography, 43: 921–935. Lim, E.L., and Dennett, production in the open sea. strain PCC 9511, a picoplanktonic Goericke, R., and Welschmeyer, cyanobacterium, synthesizes the M.R. 1999. Picoplankton and Limnology and Oceanography, 44: nanoplankton and their trophic 1282–1292. N.A. 1998. Response of Sargasso smallest urease. Microbiology—UK, Sea phytoplankton biomass, 146: 3099–3107. coupling in surface waters of the Sargasso Sea south of Bermuda. Siegel, D.A., McGillicuddy, D.J., growth rates and primary Polito, P.S., Sato, O.T., and Liu, Limnology and Oceanography, 44: and Fields, E.A. 1999. Mesoscale production to seasonally varying W.T. 2000. Characterization and 259–272. eddies, satellite altimetry, and new physical forcing. Journal of Plankton validation of the heat storage production in the Sargasso Sea. Research, 20: 2223–2249. Doherty, K.W., Frye, D.E., Journal of Geophysical Research— variability from TOPEX/Poseidon Gruber, N., Keeling, C.D., and at four oceanographic sites. Journal Liberatore, S.P., and Toole, Oceans, 104: 13359–13379. J.M. 1999. A moored profiling Stocker, T.F. 1998. Carbon-13 of Geophysical Research—Oceans, 105: constraints on the seasonal 16911–16921. instrument. Journal of Atmospheric 1998 and Oceanic Technology, 16: 1816– inorganic carbon budget at the Rippka, R., and others 1829. Bates, N.R., Knap, A.H., and BATS site in the northwestern 2000. Prochlorococcus marinus Michaels, A.F. 1998. The effect of Sargasso Sea. Deep-Sea Research I, Chisholm et al., 1992 subsp Gin, K.Y.H., Chisholm, S.W., and hurricanes on the local to global 45: 673–717. pastoris subsp nov strain Olson, R.J. 1999. Seasonal and air-sea exchange of CO2. Nature, depth variation in microbial size 395, 58–61. Jenkins, W.F. 1998. Studying PCC 9511, the first axenic subtropical thermocline ventilation chlorophyll a(2)/b(2)– spectra at the Bermuda Atlantic Bates, N.R., Takahashi, T., and circulation using tritium containing cyanobacterium time series station. Deep-Sea Chipman, D.W., and Knap, A.P. and He–3. Journal of Geophysical (Oxyphotobacteria). International Research I, 46: 1221–1245. 1998. Variability of pCO on Research—Oceans, 103: 15817– Journal of Systematic and Evolutionary 2 Hoffmann, L. 1999. Marine diel to seasonal timescales in the 15831. Microbiology, 50: 1833–1847. cyanobacteria in tropical regions: Sargasso Sea near Bermuda. Journal diversity and ecology. European of Geophysical Research—Oceans, 103: Journal of Phycology, 34: 371–379. 15567–15585.

57 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Jickells, T.D., Dorling, S., Deuser, Veron, A.J., Church, T.M., and Nelson, D.M. and Brzezinski, Doney, S.C., 1996. A synoptic W.G., Church, T.M., Arimoto, Flegal, A.R.. 1998. Lead isotopes M.A., 1997. Diatom growth and atmospheric surface forcing data R., and Prospero, J.M. 1998. Air- in the western North Atlantic: productivity in an oligotrophic set and physical upper ocean borne dust fluxes to a deep water Transient tracers of pollutant lead midocean gyre: A 3-yr record from model for the US JGOFS Bermuda sediment trap in the Sargasso Sea. inputs. Environmental Research, 78: the Sargasso Sea near Bermuda. Atlantic Time-series Study site. Global Biogeochemical Cycles, 12: 104–111. Limnology and Oceanography, 42: Journal of Geophysical Research— 311–320. 473–486. Oceans, 101: 25615–25634. Wu, J.F., and Boyle, E.A. Lessard, E.J., and Murrell, M.C. 1998. Determination of iron Veldhuis, M.J.W., Cucci, T.L. and Doney, S.C., Glover, D.M., 1998. Microzooplankton herbivory in seawater by high-resolution Sieracki, M.E., 1997. Cellular DNA and Najjar, R.G., 1996. A new and phytoplankton growth in the isotope dilution inductively content of marine phytoplankton coupled, one-dimensional northwestern Sargasso Sea. Aquatic coupled plasma mass spectrometry using two new fluorochromes: biological-physical model for the Microbial Ecology, 16: 173–188. after Mg(OH)(2) coprecipitation. Taxonomic and ecological upper ocean: Applications to the Analytica Chimica Acta, 367: implications. Journal of Phycology, JGOFS Bermuda Atlantic Time- McGillicuddy, D.J., Robinson, 183–191. 33: 527–541. series Study (BATS) site. Deep-Sea A.R., Siegel, D.A., Jannasch, Research II, 43: 591–624. H.W., Johnson, R.J., Dickey, T.D., McNeil, J, Michaels, A.F., 1997 1996 Follows, M.J., Williams, R.G. and and Knap, A.H. 1998. Influence Bates, N.R., 1997. Seasonal Andersen, R.A., Bidigare, R.R., Marshall, J.C., 1996. The solubility of mesoscale eddies on new variability of the oceanic CO2 Keller, M.D. and Latasa, M., pump of carbon in the subtropical production in the Sargasso Sea. system and the air-sea flux of CO2 1996. A comparison of HPLC gyre of the North Atlantic. Journal Nature, 394: 263–266. at the BATS site in the Sargasso pigment signatures and electron of Marine Research, 54: 605–630. Sea. In: 2nd JGOFS North Atlantic microscopic observations for McGillicuddy, D.J., Johnson, Planning Report (Ducklow, H., oligotrophic waters of the North Gundersen, K., Bratbak, G. R.J., Siegel, D.A., and Bates, Marra, J., and Goyet, C. eds.), Atlantic and Pacific Oceans. Deep- and Heldal, M., 1996. Factors N.R. 1998. BATS validation JGOFS Report Number, 20, JGOFS Sea Research Part II Topical Studies in influencing the loss of bacteria activities document mesoscale Planning Office, Woods Hole, MA, Oceanography, 43: 517–537. in preserved seawater samples. biogeochemical variations in the pp. 7–10. Marine Ecology Progress Series, 137 vicinity of the time series. USA Bates, N.R., Michaels, A.F. and (1–3): 305–310. JGOFS Newsletter, April 1998. Boyles, E. A., 1997. Characteristics Knap, A.H., 1996. Alkalinity of the deep ocean carbon system changes in the Sargasso Sea: Hess, W.R., Partensky, F., Nelson, N.B., Siegel, D.A., and during the past 150,000 years: Geochemical evidence of Vanderstaay, G.W.M., Garcia- Michaels, A.F. 1998. Seasonal Fernandez, J.M., Borner, T and Sigma CO2 distributions, deep calcification? Marine Chemistry, dynamics of colored dissolved water flow patterns, and abrupt 51: 347–358. Vaulot, D., 1996. Coexistence of material in the Sargasso Sea. Deep- climate change. Proceedings of the phycoerythrin and a chlorophyll Sea Research I, 45: 931–957. National Academy of Sciences of Bates, N.R., A.F. Michaels, and a/b antenna in a marine Knap, A.H., 1996. Seasonal and prokaryote. Proceedings of the Nelson, N.B. 1998. Spatial and the United States of America, 94: 8300–8307. interannual variability of oceanic National Academy of Sciences of temporal extent of sea surface carbon dioxide species at the US the United States of America, 93: temperature modifications by Carlson, C.A., Bates, N.R. and JGOFS Bermuda Atlantic Time- 11126–11130. hurricanes in the Sargasso Sea Steinberg, D.K., 1997. Time-series series Study (BATS) site. Deep-Sea during the 1995 season. Monthly data sets: a valuable resource for Research II, 43: 347–383. Hurtt, G.C., and Armstrong, Weather Review, 126: 1364–1368. synthesis and modelling phase of R.A., 1996. A pelagic ecosystem Brzezinski, M.A. and Kosman model calibrated with BATS data. Robbins, P.E., and Jenkins, W.J. USA JGOFS. USA JGOFS Newsletter, July 1997. C.A., 1996. Silica production in the Deep-Sea Research Part II Topical 1998. Observations of temporal Sargasso Sea during spring 1989. Studies in Oceanography, 43: changes of tritium–He–3 age Garver, S.A. and Siegel, D.A., Marine Ecology—Progress Series, 142: 653–683. in the eastern North Atlantic 1997. Inherent optical property 39–45. thermocline: Evidence for changes inversion of ocean color Joyce, T.M., and Robbins, in ventilation? Journal of Marine spectra and its biogeochemical Brzezinski, M.A., and Nelson, P., 1996. The Long-term Research, 56: 1125–1161. interpretation. 1. Time series D.M., 1996. Chronic substrate hydrographic record at Bermuda. limitation of silicic acid uptake Journal of Climate, 9: 3121–3131. Rossby, T., ad Gottlieb, E. from the Sargasso Sea. Journal of Geophysical Research—Oceans, 102: rates in the western Sargasso Sea. 1998. The Oleander project: Deep-Sea Research II, 43: 437–453. Karl, D.M., and Michaels, A.F., Monitoring the variability of 18607–18625. 1996. The Hawaiian ocean the Gulf Stream and adjacent Gruber, N., and Sarmiento, Calais, E., and Minster, Time-series (HOT) and Bermuda waters between and J.L., 1997. Global patterns J.B., 1996. GPS detection of Atlantic Time-series study (BATS) Bermuda. Bulletin of the American of marine nitrogen fixation ionospheric perturbations —Preface. Deep-Sea Research Part Meteorological Society, 79: 5–18. and denitrification. Global following a Space Shuttle ascent. II—Topical Studies in Oceanography, Biogeochemical Cycles, 11: 235–266. Geophysical Research Letters, 23: 43: 127–128. Rothschild, B.J. 1998. Year class 1897–1900. strengths of zooplankton in the Hall, A., and Manabe, S., Keigwin, L.D. 1996. The Little Ice North Sea and their relation to cod 1997. Can local linear stochastic Campos, M., Farrenkopf, A.M., Age and and abundance. Journal of theory explain sea surface Jickells, T.D. and Luther, G.W., in the Sargasso Sea. Science, 274: Plankton Research, 20: 1721–1741. temperature and salinity 1996. A comparison of dissolved 1504–1508. iodine cycling at the Bermuda Spitz, Y.H., Moisan, J.R., variability? Climate Dynamics, 13: Lawson, L.M., Hofmann, E.E. 167–180. Atlantic Time-series station and Abbott, M.R., and Richman, Hawaii Ocean Time-series Station. and Spitz, Y.H., 1996. Time series J.G. 1998. Data assimilation Keim, B.D., 1997. Preliminary Deep-Sea Research II, 43: 455–466. sampling and data assimilation in and a pelagic ecosystem model: analysis of the temporal patterns a simple marine ecosystem model. parameterization using time series of heavy rainfall across the Carlson, C.A. and Ducklow, H.W., Deep-Sea Research II, 43: 625–651. observations. Journal of Marine 1996. Growth of bacterioplankton southeastern United States. Lessard, E.J., and Murrell, M.C.. Systems, 16: 51–68. Professional Geographer, 49: 94–104. and consumption of dissolved organic carbon in the Sargasso 1996. Distribution, abundance and Stramska, M., and Dickey, T.D. Moffett, J. W. 1997. The Sea. Aquatic Microbial Ecology, 10: size composition of heterotrophic 1998. Short-term variability of importance of microbial Mn 69–85. dinoflagellates and ciliates in the the underwater light field in the oxidation in the upper ocean: a Sargasso Sea near Bermuda. Deep- oligotrophic ocean in response to comparison of the Sargasso Sea Carlson, C.A., Ducklow, H.W. Sea Research I, 43: 1045–1065. surface waves and clouds. Deep-Sea and equatorial Pacific. Deep-Sea and Sleeter, T.D., 1996. Stocks Research I, 45: 1393–1410. Research I, 44: 1277–1291. and dynamics of bacterioplankton in the northwestern Sargasso Sea. Deep-Sea Research II, 43: 491–515.

58 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Lipshultz, F., Zafiriou, O.C. and Brzezinski, M.A., and Nelson, Michaels, A.F., Caron, D.A., Howden, S.D., Watts, D.R., L.A. Ball, L.A., 1996. Seasonal D.M., 1995. The annual Silica cycle Swanberg, N.R., F.A. Howse, and Tracey, K.L., and Rossby, H.T., fluctuations of nitrite in the Sargasso Sea near Bermuda. Michaels C.M., 1995. Planktonic 1994. An Acoustic Telemetry concentrations in the deep Deep-Sea Research I, 42: 1215–1237. sarcodines (Acantharia, Radiolaria, System Implemented for Real-Time oligotrophic ocean. Deep-Sea Foraminifera) in surface waters Monitoring of the Gulf-Stream Research II, 43: 403–419. Calder, D.R., 1995. Hydroid near Bermuda—abundance, with Inverted Echo Sounders. assemblages on holopelagic biomass and vertical Flux. Journal of Journal of Atmospheric and Oceanic Lo, W.T., and Biggs, D.C., Sargassum from the Sargasso Sea at Plankton Research, 17: 131–163. Technology, 11: 567–571. 1996. Temporal variability in Bermuda. Bulletin of MarineScience, the night-time distribution of 56: 537–546. Moffet, J.W., 1995. Temporal Jickells, T., Church, T., epipelagic siphonophores in the and Spatial Variability of Copper Vernon, A. and Arimoto, R., North Atlantic Ocean at Bermuda. Caron, D.A., Michaels, A.F., Complexation by Strong Chelators 1994. Atmospheric Inputs of Journal of Plankton Research, 18: Swanberg, N.R. and Howse, in the Sargasso Sea. Deep-Sea Manganese and Aluminum to the 923–939. F.A.. 1995. Primary Productivity Research I, 42: 1273–1295. Sargasso Sea and Their Relation by symbiont-bearing planktonic to Surface-Water Concentrations. Marchal, O., Monfray, P. and Sarcodines (Acantharia, Radiolaria, Mullins, T.D., Britschgi, T.B., Marine Chemistry, 46: 283–292. Bates, N.R., 1996. Spring summer Foraminifera) in surface waters Krest, R.L. and S.J. Giovannoni, imbalance of dissolved inorganic near Bermuda. Journal of Plankton S.J., 1995. Genetic Comparisons Laine, E.P., W.D. Gardner, carbon in the mixed layer of Research, 17: 103–129. Reveal the Same Unknown Richardson, M.J. and Kominz, the northwestern Sargasso Sea. Bacterial Lineages in Atlantic M., 1994. Abyssal Currents Tellus Series B-Chemical and Physical Caron, D.A., and others and Pacific Bacterioplankton and Advection of Resuspended Meteorology, 48: 115–134. 1995. The contribution of Communities. Limnology and Sediment Along the Northeastern microorganisms to particulate Oceanography, 40: 148–158. Bermuda Rise. Marine Geology, 119: Michaels, A.F and Knap, A.H., carbon and nitrogen in surface 159–171. 1996. Overview of the US JGOFS waters of the Sargasso Sea near Roman, M. R. and others, Bermuda Atlantic Time—series Bermuda. Deep-Sea Research I, 42: 1995. Spatial and Temporal Michaels, A.F., Knap, A.H., Dow, Study and the Hydrostation S 943–972. Changes in the Partitioning of R.L., K. Gundersen, Johnson, program. Deep-Sea Research II, 43: Organic-Carbon in the Plankton R.J., J. Sorensen, Close, A., 157–198. Dam, H.G., Roman, M.R., Community of the Sargasso Sea Knauer, G.A., S.E. Lohrenz, Asper, and Youngbluth, M.J., Off Bermuda. Deep-Sea Research I, V.A., Tuel, M., and Bidigare, R. Michaels, A.F, Olson, D., 1995. Downward Export of 42: 973–992. 1994. Seasonal Patterns of Ocean Sarmiento, J.L., Ammerman, Respiratory Carbon and Dissolved Biogeochemistry at the United- J.W., Fanning, K., Jahnke, R., Inorganic Nitrogen by Diel- Sayles, F.L., and Martin, W.R., States JGOFS Bermuda Atlantic Knap, A.H., Lipshultz, F. and Migrant Mesozooplankton at 1995. In-Situ Tracer Studies Time-series Study Site. Deep-Sea Prospero, J.M., 1996. JM Inputs, the Jgofs Bermuda Time-series of Solute Transport across the Research I, 41: 1013–1038. losses and transformations of Station. Deep-Sea Research Part I Sediment-Water Interface at the nitrogen and phosphorus in the Oceanographic Research Papers, 42: Bermuda Time-series Site. Deep- Michaels, A.F., Bates, N.R., pelagic North Atlantic Ocean. 1187–1197. Sea Research I, 42: 31–52. Buesseler, K.O., Carlson, C.A., Biogeochemistry, 35 (1): 181–226. and Knap, A.H., 1994. Carbon- Ducklow, H.W., Carlson, C.A., Siegel, D.A., Michaels, A.F., Cycle Imbalances in the Sargasso Sayles, F.L., Deuser, W.G., Bates, N.R., Knap, A.H. and Sorensen, J.C., Obrien, M.C. and Sea. Nature, 372: 537–540. Goudreau, J.E., Dickinson, Michaels, A.F.. 1995. Dissolved Hammer, M.A.. 1995. Seasonal W.H., Jickells, T.D. and King, Organic-Carbon as a Component Variability of Light Availability and Sayles, F.L., Martin, W.R., and P., 1996. The benthic cycle of of the Biological Pump in the Utilization in the Sargasso Sea. Deuser, W.G., 1994. Response biogenic opal at the Bermuda North-Atlantic Ocean. Philosophical Journal of Geophysical Research— of Benthic Oxygen-Demand to Atlantic Time Series site. Deep-Sea Transactions of the Royal Society of Oceans, 100: 8695–8713. Particulate Organic-Carbon Supply Research I, 43: 383–409. London Series B-Biological Sciences, in the Deep-Sea near Bermuda. 348: 161–167. Nature, 371: 686–689. Siegel, D.A., and Michaels, 1994 A.F., 1996. Quantification of Hansell, D.A., Bates, N.R. and Bissett, W.P., Meyers, M.B., Schultz, E.T., and Cowen, R.K., non-algal light attenuation in Gundersen, K., 1995. Bacterial Walsh, J.J. and Muller-Karger, 1994. Recruitment of Coral-Reef the Sargasso Sea: Implications mineralization of DOC in the F.E., 1994. The Effects of Temporal Fishes to Bermuda-Local Retention for biogeochemistry and remote Sargasso Sea. Marine Chemistry, 51, Variability of Mixed-Layer Depth or Long-Distance Transport. sensing. Deep-Sea Research II, 43: 201–212. on Primary Productivity around Marine Ecology—Progress Series, 109: 321–345. Bermuda. Journal of Geophysical 15–28. Jewell, P.W., 1995. A Simple Research—Oceans, 99: 7539–7553. Talley, L.D. 1996. North Atlantic Surface-Water Biogeochemical circulation and variability, reviewed Model .2. Simulation of Selected Buesseler, K.O., Michaels, 1993 for the CNLS conference. Physica Lacustrine and Marine Settings. A.F., Siegel, D.A., and Knap Fasham, M.J.R., Sarmiento, J.L., D, 98: 625–646. Water Resources Research, 31: A.H., 1994. A 3-Dimensional Slater, R.D., H.W. Ducklow, and 2059–2070. Time-Dependent Approach to Williams, R., 1993. Ecosystem Waser, N.A.D., Bacon, M.P. and Calibrating Sediment Trap Fluxes. behavior at Bermuda Station-S Michaels, A.F., 1996. Natural Lohmann, G.P., 1995. A Model Global Biogeochemical Cycles, 8: and Ocean India activities of P–32 and P–33 and for Variation in the Chemistry 179–193. —a general-circulation model the P–33/P–32 ratio in suspended of Planktonic-Foraminifera and observational analysis. Global particulate matter and plankton in Due to Secondary Calcification Carlson, C.A., Ducklow, H.W. Biogeochemical Cycles, 7: 379–415. the Sargasso Sea. Deep-Sea Research and Selective Dissolution. and Michaels, A.F., 1994. Annual II, 43: 421–436. Paleoceanography, 10: 445–457. Flux of Dissolved Organic-Carbon Fuhrman, J.A., McCallum, K., and from the Euphotic Zone in the Davis, A.A., 1993. Phylogenetic Michaels, A.F., 1995. Ocean Time- 1995 Northwestern Sargasso Sea. diversity of subsurface marine series research near Bermuda: Nature, 371: 405–408. microbial communities from the Arenovski, A.L., Lim, E.L. and The hydrostation S Time-series Atlantic and Pacific Oceans. Applied Caron, D.A., 1995. Mixotrophic and the Bermuda Atlantic Time- Gust G., Michaels, A.F., Johnson, and Environmental Microbiology, 59: nanoplankton in oligotrophic series Study (BATS) program. R.J., Deuser, W.G. and Bowles, 1294–1302. surface waters of the Sargasso In: Ecological Time Series (T.M. W., 1994. Mooring line motions Sea may employ phagotrophy to Powell, J.H. Steele), Chapman & and sediment trap hydromechanics Hinrichsen, H.H., and obtain major nutrients. Journal of Hall Publishing, New York. Pp. —in situ intercomparison of 3 Tomczak, M., 1993. Optimum Plankton Research, 17: 801–820. 181–208. common deployment designs. Multiparameter Analysis of the Deep-Sea Research I, 41 (5–6): Water Mass Structure in the 831–857 MAY–JUN 1994. Western North-Atlantic Ocean. Journal of Geophysical Research— Oceans, 98: 10155–10169.

59 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Malone, T.C., Pike, S.E., and Vernon, A.J., Church, T.M., Sherrell, R.M., and Boyle, Schweitzer, P.N., and Lohmann, Conley, D.J., 1993. Transient Flegal, A.R., Patterson, C.C., and E.A.. 1992. The Trace-Metal G.P., 1991. Ontogeny and Variations in Phytoplankton Erel, Y., 1993. Response of Lead Composition of Suspended Habitat of Modern Menardiiform Productivity at the Jgofs Cycling in the Surface Sargasso Sea Particles in the Oceanic Water Planktonic-Foraminifera. Journal of Bermuda Time-series Station. to Changes in Tropospheric Input. Column near Bermuda. Earth Foraminiferal Research, 21: 332–346. Deep-Sea Research I, 40: 903–924. Journal of Geophysical Research— and Planetary Science Letters, 111: Oceans, 98: 18269–18276. 155–174. Suttle, C.A., Chan, A.M., and Michaels, A.F., Siegel, D.A., Fuhrman, J.A.. 1991. Dissolved Johnson, R.J., Knap, A.H., and Wilson, W.H., Joint, I.R., Sherrell, R.M., and Boyle, E.A., Free Amino-Acids in the Sargasso Galloway, J.N., 1993. Episodic Carr, N.G. and Mann, N.H., 1992. Isotopic Equilibration Sea—Uptake and Respiration inputs of atmospheric nitrogen to 1993. Isolation and Molecular between Dissolved and Suspended Rates, Turnover Times, and the Sargasso Sea—Contributions Characterization of 5 Marine Particulate Lead in the Atlantic- Concentrations. Marine Ecology— to new production and Cyanophages Propagated on Ocean-Evidence from Pb–210 Progress Series, 70: 189–199. phytoplankton blooms. Global Synechococcus Sp Strain Wh7803. and Stable Pb Isotopes. Journal of Biogeochemical Cycles, 7: 339–351. Applied and Environmental Geophysical Research—Oceans, 97: 1990 Microbiology, 59: 3736–3743. 11257–11268. Roman, M.R., Dam, H.G., Tesch, F.W., and Wegener, G., Gauzens, A.L., and Napp, J.M.., Wei, K.Y., Zhang, Z.W., and 1990. The Distribution of Small 1993. Zooplankton Biomass and 1992 Wray, C., 1992. Shell Ontogeny Larvae of Anguilla sp Related Grazing at the JGOFS Sargasso Altabet, M.A., Bishop, of Globorotalia inflata .1. Growth to Hydrographic Conditions Sea Time-series Station. Deep-Sea J.K.B., and McCarthy, J.J., Dynamics and Ontogenic Stages. 1981 between Bermuda and Research I, 40: 883–901. 1992. Differences in Particulate Journal of Foraminiferal Research, 22: Puerto-Rico. Internationale Revue Nitrogen Concentration and 318–327. Der Gesamten Hydrobiologie, 75: Sharp, J.H., Benner, R., Bennett, Isotopic Composition for Samples 845–858. L., Carlson, C.A., Dow, R., Collected by Bottles and Large- and Fitzwater, S.E., 1993. Re- 1991 Volume Pumps in Gulf-Stream 1989 evaluation of High-Temperature Warm-Core Rings and the Sargasso Brooks, A.L., and Saenger, Combustion and Chemical Sea. Deep-Sea Research, 39: S405– R.A., 1991. Vertical Size-Depth Fuhrman, J.A., Sleeter, T.D., Oxidation Measurements of S417. Distribution Properties of Carlson, C.A., and Proctor, L.M., Dissolved Organic-Carbon Midwater Fish Off Bermuda, with 1989. Dominance of bacterial in Seawater. Limnology and Bender, M., Ducklow, H.W., Comparative Reviews for Other biomass in the Sargasso Sea and Oceanography, 38: 1774–1782. Kiddon, J., J. Marra, and Martin, Open Ocean Areas. Canadian its ecological implications. Marine J., 1992. The Carbon Balance Journal of Fisheries and Aquatic Ecology Progress Series, 57 (3): Sholkovitz, E.R., Church, T.M., During the 1989 Spring Bloom in Sciences, 48: 694–721. 207–217. and Arimoto, R., 1993. Rare- the North-Atlantic Ocean, 47– Earth Element Composition Dicarlo, B.S., Ianora, A., Degrees–N, 20–Degrees–W. Deep- 1988 of Precipitation, Precipitation Sea Research, 39: 1707–1725. Mazzocchi, M.G., and Scardi, M.. Particles, and Aerosols. Journal of 1991. -Ii Cruise-Uniformity Jickells, T.D., Boyd, S.S., and Geophysical Research—Atmospheres, Lohrenz, S.E., Knauer, of Deep Copepod Assemblages in Knap, A.H., 1988. Iodine Cycling 98: 20587–20599. G.A., Asper, V.L., Tuel, M., the Mediterranean Sea. Journal of in the Sargasso Sea and the Michaels, A.F., and Knap, A.H., Plankton Research, 13: 263–277. Veldhuis, M.J.W., and Kraay, Bermuda Inshore Waters. Marine 1992. Seasonal Variability in Chemistry, 24: 61–82. G.W.. 1993. Cell abundance and Primary Production and Particle- fluorescence of picoplankton in Flux in the Northwestern Sargasso relation to growth irradiance and Sea-United States JGOFS Bermuda nitrogen availability in the Red-Sea. Atlantic Time-series Study. Deep- Netherlands Journal of Sea Research, Sea Research, 39: 1373–1391. 31: 135–145.

60 Sargasso Sea Alliance – Oceanography of the Sargasso Sea Sargasso Sea Alliance Science Series

The following is a list of the reports in the Sargasso Sea Alliance Science Series. All can be downloaded from www.sargassoalliance.org:

1 2 3 4 Angel, M.V. 2011. The Ardron, J., Halpin, P., Gollock, M. 2011. European Hallett, J. 2011. The pelagic ocean assemblages Roberts, J., Cleary, J., eel briefing note for Sargasso importance of the Sargasso Sea of the Sargasso Sea around Moffitt, M. and J. Donnelly Sea Alliance. Sargasso Sea and the offshore waters of the Bermuda. Sargasso Sea 2011. Where is the Sargasso Alliance Science Report Bermudian Exclusive Economic Alliance Science Report Sea? Sargasso Sea Alliance Series, No 3, 11 pp. Zone to Bermuda and its people. Series, No 1, 25 pp. Science Report Series, Sargasso Sea Alliance Science No 2, 24 pp. Report Series, No 4, 18 pp.

5 6 7 8 Lomas, M.W., Bates, N.R., Lomas, M.W., Bates, N.R., Miller, M.J. and R. Hanel. Parson, L. and R. Edwards Buck, K.N. and A.H. Knap. Buck, K.N. and A.H. Knap. 2011. The Sargasso Sea 2011. The geology of the (eds) 2011a. Oceanography 2011b. Notes on “Microbial subtropical gyre: the spawning Sargasso Sea Alliance Study of the Sargasso Sea: Overview productivity of the Sargasso Sea and larval development area Area, potential non-living of Scientific Studies. Sargasso and how it compares to elsewhere” of both freshwater and marine marine resources and an Sea Alliance Science Report and “The role of the Sargasso Sea eels. Sargasso Sea Alliance overview of the current Series, No 5, 64 pp. in carbon sequestration—better Science Report Series, territorial claims and coastal than carbon neutral?” Sargasso No 7, 20 pp. states interests. Sargasso Sea Sea Alliance Science Report Alliance Science Report Series, No 6, 10 pp. Series, No 8, 17 pp.

9 10 11 12 Roberts, J. 2011. Maritime Siuda, A.N.S. 2011. Stevenson, A. 2011. Sumaila, U. R., Vats, V., Traffic in the Sargasso Sea: Summary of Sea Education Research and W. Swartz. 2013. An Analysis of International Association long-term Sargasso Project, Bermuda. Sargasso Values from the resources of Shipping Activities and their Sea surface net data. Sargasso Sea Alliance Science Report the Sargasso Sea. Sargasso Potential Environmental Sea Alliance Science Report Series, No 11, 11 pp. Sea Alliance Science Report Impacts. Sargasso Sea Series, No 10, 18 pp. Series, No 12, 24 pp. Alliance Science Report Series, No 9, 45 pp. SARGASSO SEA ALLIANCE

Since the initial meetings the partnership around the Sargasso Sea Alliance has expanded. Led by the Government of Bermuda, the Alliance now includes the following organisations. Partner Type of Organisation

Department of Environmental Protection Government of Bermuda

Department of Conservation Services Government of Bermuda

Mission Blue / Sylvia Earle Alliance Non-Governmental Organisation

International Union for the Conservation of Nature (IUCN) and its World Commission on Protected Areas Multi-lateral Conservation Organisation

Marine Conservation Institute Non-Governmental Organisation

Woods Hole Oceanographic Institution Academic

Bermuda Institute for Ocean Sciences Academic

Bermuda Underwater Exploration Institute Non-Governmental Organisation

World Wildlife Fund International Non-Governmental Organisation

Atlantic Conservation Partnership Non-Governmental Organisation