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CITATION Honjo, S., T.I. Eglinton, C.D. Taylor, K.M. Ulmer, S.M. Sievert, A. Bracher, C.R. German, V. Edgcomb, R. Francois, M.D. Iglesias-Rodriguez, B. van Mooy, and D.J. Repeta. 2014. Understanding the role of the in the global cycle: An imperative for science. Oceanography 27(3):10–16, http://dx.doi.org/10.5670/oceanog.2014.78.

DOI http://dx.doi.org/10.5670/oceanog.2014.78

COPYRIGHT This article has been published inOceanography , Volume 27, Number 3, a quarterly journal of The Oceanography Society. Copyright 2014 by The Oceanography Society. All rights reserved.

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DOWNLOADED FROM HTTP://WWW.TOS.ORG/OCEANOGRAPHY COMMENTARY UNDERSTANDING THE ROLE OF THE BIOLOGICAL PUMP IN THE GLOBAL An Imperative for Ocean Science

BY SUSUMU HONJO, TIMOTHY I. EGLINTON, CRAIG D. TAYLOR, KEVIN M. ULMER, STEFAN M. SIEVERT, ASTRID BRACHER, CHRISTOPHER R. GERMAN, VIRGINIA EDGCOMB, ROGER FRANCOIS, M. DEBORA IGLESIAS-RODRIGUEZ, BENJAMIN VAN MOOY, AND DANIEL J. REPETA

Anthropogenically driven climate the basis for marine biodiversity and abyssopelagic and hadalpelagic zones) change will rapidly become Earth’s key food resources that support the is by far the single largest inventory of dominant transformative influence in the human population. Our understanding bio-C on Earth. It contains 3,150 Pmol coming decades. The oceanic biological of the biological pump is far from (Pmol = 1015 mole; Figure 1), more pump—the complex suite of processes complete. Moreover, how the biological than 50 times greater than the amount that results in the transfer of particulate pump and the deep ocean of CO2-C in the atmosphere, currently and from the will respond to the rapid and ongoing estimated to be about 62.5 Pmol (pre- surface to the deep ocean—constitutes anthropogenic changes to our planet— industrial levels are estimated to have the main mechanism for removing CO2 including warming, acidification, and been about 48.3 Pmol; IPCC, 2007), and from the atmosphere and sequestering deoxygenation of ocean waters—remains more than an order of magnitude greater carbon at depth on submillennium time highly uncertain. To understand than all the bio-C held in terrestrial scales. Variations in the efficacy of the and quantify present-day and future vegetation, soils, and microbes com- biological pump and the strength of changes in biological pump processes bined. The sink-strength (or “feedback the deep ocean carbon sink, which is requires sustained global observations efficiency”; Falkowski et al., 2000) of this larger than all other bioactive carbon coupled with extensive modeling studies reservoir is critical in buffering Earth’s reservoirs, regulate Earth’s climate and supported by international scientific atmosphere from a rapid CO2 increase. have been implicated in past glacial-​ coordination and funding. Operating in parallel, the inorganic interglacial cycles. The numerous bio- gas-exchange pump (which includes the logical, chemical, and physical processes BACKGROUND /bicarbonate buffer-driven involved in the biological pump are The pelagic and coastal , together ) is estimated to account inextricably linked and heterogeneous with the Great Lakes, contain over 90% for only ~ 10% of the total transfer of over a wide range of spatial and temporal of Earth’s bioactive carbon (bio-C) and dissolved inorganic carbon (DIC) from scales, and they influence virtually the exert a major influence on the global surface to deep waters in the modern entire ocean ecosystem. Thus, the func- environment by modulating fluxes ocean (e.g., Sarmiento and Gruber, tioning of the oceanic biological pump and transformations between various 2006). In this article, we exclusively focus is not only relevant to the modulation carbon reservoirs. In particular, the on the biological pump. of Earth’s climate but also constitutes ocean’s bathypelagic zone (including The biological pump starts in the

10 Oceanography | Vol. 27, No.3 EARTH’S BIOACTIVE CARBON CYCLE Flux: petamol C yr –1 –1 Sink: petamol C Terrestrial POC Atmospheric CO2: 62.5 pmol C + 0.28 pmol yr Figure 1. A simplified conceptual diagram of Euphotic zone Earth’s bioactive carbon cycle with the size Ventilation DOC : 3? (petamol C) of the atmospheric reservoir as 53.6 CO2 (CO2-C). The deep ocean sink is shown Greater export in red, and key fluxes (petamol C yr–1) are in Biological yellow. The current CO -C inventory in Earth’s pump 2 POC consumption atmosphere (62.5 petamol C) is increasing at the rate of 0.28 petamol C yr–1. POC (particulate Mesopelagic zone organic carbon) exported to the bathypelagic zone by the biological pump is estimated at 0.04 petamol C yr–1. This zone, containing M/B boundary 3,150 petamol C, represents Earth’s master reser- voir of bioactive C. For clarity, the solubility pump, Bathypelagic zone 0.04 which is estimated to account for ~ 10% of the total transfer of DOC (dissolved organic carbon) Master bio-C reservoir from surface to deep waters in the modern ocean 3,150 (Sarmiento and Gruber, 2006), is not included. M/B = mesopelagic/bathypelagic. Subsurface sediment

Crust microbes

euphotic zone with the photosynthetic ocean by direct transport of POC is with our limited knowledge of their fixation of inorganic carbon into phyto- ~ 0.04 Pmol yr–1 (Figure 1; Honjo et al., roles in biogeochemical processes. A plankton biomass. Current estimates 2008). Notably, this flux represents only complete mechanistic and quantitative of global oceanic primary production 14% of the current annual increase of understanding of the biological pump is –1 (G-PP) are between 3 and 4 Pmol C yr carbon as atmospheric CO2, highlighting essential for determining its importance

(e.g., Berger, 1989; Antoine, 1996; the importance of understanding how in modulating atmospheric CO2 and Behrenfeld and Falkowski, 1997; Chavez the biological pump will respond to predicting its future behavior. Programs et al., 2011). Research undertaken increasing atmospheric CO2 concen- such as the Global Carbon Project during the US Joint Global Ocean Flux trations, and whether the bathypelagic (http://www.globalcarbonproject.org) Study (US JGOFS, ca. 1987–2005) and carbon reservoir can remain a sink for as well as other global carbon flux subsequent programs clarified that a this anthropogenic carbon. modeling efforts are in need of far more fraction of this bio-C is rapidly removed There are serious deficiencies in our extensive and comprehensive ocean data from surface waters and exported to the ability to place these processes in a to further refine their predictive capabil- ocean’s interior in the form of partic- quantitative context, to determine their ities. Input from this community will be ulate organic matter (POM) through a dynamics, and to assess how the ocean critical in guiding the prioritization for complex interplay of biological processes will respond to, or exacerbate, climate measurements needed to address current combined with gravity (eco-dynamic change, pollution, and over-exploitation deficiencies in our models. transport; e.g., Honjo et al., 2008; of marine resources. For example, Online Supplement, Section 1). our recognition of the large stock of ADDRESSING KNOWLEDGE Chemoautotrophic processes in the prokaryotic biomass throughout the GAPS: THE GRAND CHALLENGE meso- and bathypelagic realms may also ocean and in subsurface and subseafloor Current global flux estimates of bio-C play important roles in modulating deep environments (e.g., Whitman, et al., generally stem from data acquired from ocean carbon inventories (e.g., Arístegui 1998; Arístegui, et al., 2009; Lauro highly diverse and often asynchronous et al., 2009; Swan et al., 2011; Online and Bartlett, 2008; Kallmeyer et al., observations. There is considerable Supplement, Section 2). 2012) and of dissolved organic carbon uncertainty in these estimates due to Prior studies suggest that the annual residing in ocean waters (Hansell sparse and heterogeneous data coverage flux of bio-C to the bathypelagic and Carlson, 2013) sharply contrasts that may fail to capture seasonal

Oceanography | September 2014 11 variability or incorporate geographical 2009) and on the fate of this photosyn- and Silver, 1988). Quantitative research biases. For example, although US JGOFS thetically derived carbon. While new on these microbes is greatly needed for provided a wealth of new insights, constraints on organic carbon export are understanding the transport of bio-C derivation of global-scale carbon fluxes being realized through coupling of satel- throughout the water column (Online from this and other programs is fraught lite observations with food web models Supplement, Section 3). with uncertainty because discontinuous (Siegel et al., 2014), high-resolution The bathypelagic zone or “prokaryotic observations spanned > 10 years and time-series measurements (e.g., Taylor domain” comprising Earth’s bio-C various parameters were not measured and Howes, 1994) would provide greatly master reservoir (Figures 1 and 2) is simultaneously. These deficiencies reflect improved assessment of carbon and crucial in the context of the oceanic both a lack of technology and limited biomineral production throughout carbon cycle, yet it remains grossly opportunities for ocean observations of the euphotic zone and of autotrophic undersampled. The metabolic activity the type and scope required to develop processes at all ocean depths (Figure 2). of prokaryotic/eukaryotic communities precise constraints on the biological In the mesopelagic zone, or “pro- largely controls in situ organic matter pump on temporal and spatial scales karyote/zooplankton domain,” both remineralization to ∑CO2-aq in the suitable for assessing links and sensitiv- prokaryotic and eukaryotic organisms bathypelagic water column and under- ity to global change. are understood to strongly influence bio- lying sediment because of the scarcity of geochemical processes. However, their zooplankton in this zone. Globally, the SPATIAL AND TEMPORAL impacts on the net flux and composition amount of prokaryote biomass in sub- VARIATIONS IN BIO-C CYCLING of settling particulate organic carbon surface ocean sediments remains a topic In the euphotic zone, or “phytoplankton (POC), and of dissolved organic carbon of debate. The standing crop of bio-C in domain,” accurate constraints on (DOC), remains poorly constrained subsurface sediment is estimated to be marine primary production must be (e.g., Steinberg et al., 2002; Buesseler 25 Pmol C (40% of the amount of cur- established in terms of absolute flux, et al., 2007). In particular, the diel ver- rent atmospheric CO2-C) and includes photoautotrophic community structure, tical shuttling of zooplankton through diverse assemblages of microorganisms and biomineral (ballast) production and the mesopelagic zone (e.g., Angel and (Whitman et al., 1998; Kallmeyer et al., removal rates. Satellite-based surface Baker, 1982) involves complex eco-​ 2012; Figure 1). Further research is ocean color observations have yielded dynamic transport and transformation necessary to elucidate and quantify rates the most spatially comprehensive view of POC (Figure 2), imposing serious of carbon transformation in bathypelagic of G-PP (e.g., Behrenfeld and Falkowski, challenges to the characterization and waters and underlying sediments. 1997) and will be indispensable in future parameterization of this important but The dynamics of ocean margin ocean observing efforts. However, these elusive component of the biological ecosystems and associated bio-C are measurements probe only the surface pump. Microbes occur abundantly in even more complex than pelagic ocean layers of the euphotic zone and presently mesozooplankton guts (e.g., Gowing dynamics. The margins are regions of deliver only restricted information and Wishner, 1998), free settling fecal large ecological diversity (Levin and on the diversity of primary producers pellets (Honjo, 1997) and Sibuet, 2012) and of high carbon pro- (e.g., Alvain et al. 2005; Bracher et al., (e.g., Alldredge and Cox, 1982; Alldredge ductivity, export, and burial (Tsunogai

Susumu Honjo ([email protected]) is Scientist Emeritus, Wood Hole Oceanographic Institution (WHOI), Woods Hole, MA, USA. Timothy I. Eglinton ([email protected]) is Professor, Eidgenössische Technische Hochschule, Zurich, Switzerland, and Adjunct Scientist, WHOI, Woods Hole, MA, USA. Craig D. Taylor is Associate Scientist, WHOI, Woods Hole, MA, USA. Kevin M. Ulmer is Executive Director, Seaquester, Inc., East Sandwich, MA, and Guest Investigator, WHOI, Woods Hole, MA, USA. Stefan M. Sievert is Associate Scientist, WHOI, Woods Hole, MA, USA. Astrid Bracher is Professor, Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany. Christopher R. German is Senior Scientist, WHOI, Woods Hole, MA, USA. Virginia Edgcomb is Associate Scientist, WHOI, Woods Hole, MA, USA. Roger Francois is Professor, University of British Columbia, Vancouver, Canada. M. Debora Iglesias-Rodriguez is Professor, University of California, Santa Barbara, CA, USA. Benjamin Van Mooy is Associate Scientist, WHOI, Woods Hole, MA, USA. Daniel J. Repeta is Senior Scientist, WHOI, Woods Hole, MA, USA.

12 Oceanography | Vol. 27, No.3 et al., 1999; Thunell et al., 2000; OCEANIC ZONES AND DOMAINS OF ORGANISMS SUPPORTING THE GLOBAL BIOLOGICAL PUMP Muller-Karger et al., 2010; Montes et al., Zones Main organisms 2012). Characterizing processes on the Euphotic zone Primary production domain Phytoplankton continental margins and their influence POC on deep ocean bio-C inventories is Export production, EP therefore a prerequisite for developing a complete understanding of the Eco-dynamic transport Mesopelagic zone Zooplankton, microbe domain Zooplankton, global carbon cycle, yet ocean margins microbes wilight zone remain woefully underrepresented in T global carbon databases and models M/B boundary (e.g., Thunell et al., 2007). Bathypelagic zone Gravitational transport THE GLOBAL Microbes, Master bio-C reservoir BIOGEOCHEMICAL FLUX Microbial plankton domain microbial eukarayotes OBSERVATORY CONCEPT Subsurface sediment domain The rapid pace of atmospheric carbon Subsurface zone accumulation is likely to increase as a Upper crust Upper crust domain Crust microbes result of positive feedback mechanisms: Figure 2. Schematic illustration of major oceanic zones and biological domains between the air-sea inter- ocean warming, deoxygenation, face and the deep ocean floor, including the subsurface zone. Below the mesopelagic/bathypelagic (M/B) and acidification are proceeding at boundary, there is little zooplankton activity, so, hypothetically, the large population of prokaryotes near measurable rates and on a global scale. the bottom of the water column is supported by gravitational transport of biomineral-ballasted particles that descend from surface waters. Assessment of the impacts of these and other perturbations related to global climate change on ocean biogeochemical observation and sampling program established technologies and advanced processes can only be addressed via that complements elements of the autonomous instrumentation operated sustained observations (e.g., Wunsch US Ocean Observatory Initiative (OOI) synchronously. Among the key facets et al., 2013). Linking changes in the and other ocean observatory programs of the GBF-O that distinguish it from physical/chemical environment with (e.g., http://www.oceansites.org, the OOI are an emphasis on long-term biological and biogeochemical properties http://www.ioc-goos.org), as well as sample acquisition, preservation of the and processes and accurate modeling other observational approaches, such as samples for subsequent retrieval of max- and prediction of the effects of global satellite-based global investigations of imum biogeochemical (e.g., genomic) change (e.g., Siegel, et al., 2014) requires marine primary productivity (Behrenfeld information, and return of the samples scientists across multiple ocean research and Falkowski, 1997), shipboard time-​ for detailed laboratory-based analyses disciplines to develop and build upon series programs (Church et al., 2013), (Online Supplement, Section 3). These technological innovations toward and widespread dissemination of floats elements are vital for extracting the cost-effective implementation of reliable and gliders equipped with sensors for greatest level of information and for systems. It is also important to instill in constraining ocean biogeochemical pro- developing a sample legacy that will be society appreciation of the ocean as a cesses (Johnson et al., 2009). The GBF-O invaluable for future research as new vital global resource, understanding of concept is based on a combination of analytical technologies emerge. its role in maintaining the habitability of our fragile planet, and recognition of The authors recognize the effort and dedication of members of the Global Biogeochemical Flux Workshop Scientific Steering Committee not listed as authors of this paper: Claudia Benitez-Nelson, University of the need for multidecadal observations South Carolina • Ken Buesseler, WHOI • Francisco Chavez, Monterey Bay Aquarium Research Institute of ocean processes. • Kendra Daly, University of South Florida • John Delaney, University of Washington • John Dunne, The Global Biogeochemical Flux US National Oceanic and Atmospheric Administration Geophysical Fluid Dynamics Laboratory • Stephanie Dutkiewicz, Massachusetts Institute of Technology • Roberta Hamme, University of Victoria Observatory (GBF-O) concept offers a • Susan Neuer, Arizona State University • Cindy Pilskaln, University of Massachusetts Dartmouth framework for implementing a sustained • Oscar Schofield, Rutgers University Coastal Ocean Observation Laboratory• Heidi Sosik, WHOI

Oceanography | September 2014 13 Methodology associated instruments and supporting 25 major time-series devices as well as Key methodological elements of the materials be designed and manufactured many contextual sensors and “guest” GBF-O concept are: to produce consistent results. Mass instruments. Further details of the 1. Observations from the air-sea production of instruments and mooring GBF-O array and instruments are in the interface through the euphotic, platforms is crucial to ensure broad Online Supplement, Section 4. mesopelagic, and bathypelagic zones availability of serviceable, cost-effective A single array of this type, equipped to the seafloor systems that meet rigorous specifications. with the instrumentation capabilities 2. Sustained, synchronized time-series depicted in Figure 3, would yield a observational modes to monitor the Orchestration of GBF-O Arrays wealth of new information. Deployment seasonal and interannual rhythms of Synchronization of instruments and of multiple arrays throughout the major the biological pump sensors within and between observatory ocean basins would form the basis for a 3. Ecosystem characterization arrays is critical for understanding the GBF-O. Selection of specific locations for encompassing a broad spectrum of rhythms of global ocean biogeochemi- array deployments would be based on organisms from pelagic to benthic cal processes. The majority of POC (often multidisciplinary perspectives and con- communities, and from prokaryotes 70% to 90% of annual export) and other sensus in order to maximize our level of to zooplankton biogenic particulates are produced understanding and predictive capability 4. Implementation and maintenance of during episodes that usually occur only regarding biological pump processes. centralized laboratories for accurate once or a few times a year in response Criteria for determining array locations and precise determination of core to seasonal phytoplankton blooms would, for example, involve assessments biogeochemical flux parameters (e.g., Wefer et al., 1988). The resulting of primary production based on ocean 5. Incorporation of profiling and fixed- sharp export pulses gradually diminish color (e.g., Behrenfeld and Falkowski, depth contextual instrumentation in amplitude with depth (reviewed in 1997), ocean biogeochemical provinces 6. Construction of a long-term archive Honjo et al., 2008). Defining the annual (e.g., Longhurst et al., 1995), observa- that acquires and preserves samples pattern and evolution of this curve tions from prior studies (e.g., Honjo for future in-depth “omics” and related throughout the water column represents et al., 2008), bathymetric variations, and studies associated with biogeochemical an important aspect of constraining the maritime logistics. and paleoceanographic research functioning of the biological pump and (Online Supplement, Section 2) its impact on ocean-atmosphere carbon CONCLUSION balances (Kwon et al., 2009). Our ability to model the workings Technical Readiness of the oceanic biological pump The challenges of implementing the Preliminary Vision for GBF-O comprehensively and accurately is a GBF-O approach are formidable, but they Implementation critical component of global efforts must be met in order to fully understand Figure 3 presents one vision of a stand- to forecast the trajectory and effects the workings of the biological pump and alone GBF-O instrument. Although of anthropogenic climate change. We associated processes in the context of dependent upon local bathymetric have begun to understand the major global change. Autonomous observation conditions, the moorings within the features of the biological pump and its of ocean properties represents a major array would typically be set from several key role in the sequestration of carbon new emphasis within the ocean science to 12 nm apart (to allow for unob- in the ocean, but we are still blind to community (e.g., Johnson et al., 2009; structed deployment). Each mooring many of its characteristics and far from Bishop, 2009), and remote observation would be kept in vertical alignment by developing comprehensive mechanistic capabilities are continuously being devel- a single syntactic-foam sphere with the and quantitative constraints on its oped. Mooring systems that support full appropriate buoyancy. In this example of myriad processes. Assessment of the ocean depth biogeochemical experiments a GBF-O array, samplers are deployed at impact of climate change on ocean bio- also have advanced during US JGOFS specific intervals along each mooring to geochemical processes and ecosystems, and related programs. As for any cover different water column domains. and vice versa, can only be addressed observatory, it is essential that all of the Such an array could host more than via global, standardized, sustained,

14 Oceanography | Vol. 27, No.3 synchronous observations over coming decades. Indeed, we hope to galvanize the oceanographic community to cham- pion the need for a century of ocean observation—deploying a truly global array of state-of-the-art sensors and other instrumentation that will be neces- sary for understanding not only carbon flow in the ocean but also all of the ocean’s intimately related inhabitants. Recent rapid progress in underwater technologies, particularly ocean robotics and novel in situ sensors, experimentation platforms, and discrete samplers, has made it feasible to develop high-endurance sentry instruments capable of operating in diverse ocean environments to provide these essential Figure 3. A preliminary vision of a Global Biogeochemical Flux Observatory (GBF-O) instru- data. However, the magnitude of the mented mooring array for sustained deployment at a given ocean location. The array consists undertaking will require international of five moorings that include (A) primary production measurements, (B) in situ time-series scientific coordination and funding. We (TS) water samplers and quantitative prokaryote collectors that preserve RNA, (C) TS sediment traps to capture settling POC and other particulate matter, (D) a moored profiler for seamless must strive as a community to integrate recording of conductivity-temperature-depth, current, and acoustic ecosystem imaging data, all emerging ocean observatories to and (E) quantitative zooplankton samplers with autonomous RNA fixing processors. Further forge the best possible global planetary details are in the Online Supplement, Section 4. observation network and elevate its priority above that which already exists for other bodies in our solar system on GBF-O design. We are indebted to REFERENCES and far beyond. The scientific and D. Hansell and an anonymous reviewer Alldredge, A.L., and J.L. Cox. 1982. Primary productivity and chemical composition of societal imperatives are clear—and the who generously offered valuable sug- marine snow in surface waters of the Southern clock is ticking. gestions for improving the manuscript. California Bight. Journal of Marine Research 30:517–527. We thank K. Doherty, R. Krishfield, Alldredge, A.L., and M.W. Silver. 1988. ACKNOWLEDGEMENTS and J. Kemp (WHOI) for development Characteristics, dynamics and sig- nificance of marine snow. Progress in We thank the National Science of and improvements in the highly Oceanography 20:41–82, http://dx.doi.org/​ Foundation for support of ocean instrumented mooring arrays used for 10.1016/0079-6611(88)90053-5. biogeochemical flux studies, including this work; S. Manganini (WHOI) for his Alvain, S., C. Moulin, Y. Dandonneau, and F.M. Breon. 2005. Remote sensing of the US JGOFS program throughout efforts to improve GBF sample analysis phytoplankton groups in case 1 waters from its tenure; OCE 9986766 to S. Honjo; procedures; and J. Cook (WHOI) for global SeaWiFS imagery. Deep Sea Research 52(11):1,989–2,004, http://dx.doi.org/10.1016/​ and OCE-0425677, OCE-0851350, and expertly prepared graphics presented in j.dsr.2005.06.015. OPP-0909377 to T. Eglinton. The Ocean this manuscript. The final completion Angel, M.V., and A. de C. Baker. 1982. Vertical distribution of the standing crop of plankton Carbon and Biochemistry Program sup- of this article was partially supported by and micronekton at three stations in the north- ported the GBF Observatory Workshop WHOI’s Visionaries Fund. east Atlantic. Biological Oceanography 2:1–30. in 2011. We are deeply indebted to Antoine, D.M. 1996. Oceanic primary production: Part 1. Adaptation of a spectral the technologists at Woods Hole ONLINE SUPPLEMENT light- model in view of Oceanographic Institution and McLane The Online Supplement can be accessed application to satellite chlorophyll observations. Global Biogeochemical Cycles 10:43–55, Research Laboratories, East Falmouth, at http://www.tos.org/oceanography/ http://dx.doi.org/10.1029/95GB02831. MA, who provided countless suggestions archive/27-3_honjo.html.

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