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Deep-Sea Research II
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Editorial
Introduction to: ‘‘Ecological and biogeochemical interactions in the
dark ocean’’
The deep sea, a vast, dark realm featuring distinctive organisms and serving as a massive reservoir of carbon, is the largest
and least explored ecosystem on Earth (Fig. 1). At a time when the
ocean is responding to anthropogenic forcings (Sabine et al., 2004;
Richardson, 2008; Doney et al., 2009), we note that considerably
less is known about ecological and biogeochemical processes in
the dark ocean (the dim mesopelagic or ‘twilight zone’ plus the
aphotic bathypelagic zone below) than in the euphotic zone–
the focus of several prior major interdisciplinary studies. The
biological pump connects surface processes to the deepest ocean
layers (Volk and Hoffert, 1985; Ducklow et al., 2001), where
biological processes occur at low rates, and the biota may adapt
unique metabolisms. These deep layers are characterized by
significant decomposition, recycling, and repackaging of
particulate and dissolved organic matter (see manuscripts in
this special issue). Thus, the interplay between biological and
geochemical processes at depth can have significant effects on the
magnitude and efficiency of the biological pump, which regulates
in part atmospheric CO2 and, hence, climate (Cermeño et al.,
2008; Riebesell et al., 2009; Lomas et al., 2010).
Most of the biogenic material exported from the euphotic zone
is remineralized within the mesopelagic zone (Martin et al., 1987;
Buesseler et al., 2007; 100–1000 m), with recent interdisciplinary field studies of that system focusing on particle fluxes
(Buesseler et al., 2008; Lee et al., 2009). The structure of the
planktonic food web exerts control on the vertical transport,
cycling, and composition of this particulate and dissolved organic
matter (Legendre and Lefevre, 1995; Carlson, 2002; Boyd and
Trull, 2007; Steinberg et al., 2008; Buesseler and Boyd, 2009), but
there are still many questions concerning how microbial and
metazoan diversity is linked to function in this zone. In addition,
ecological and biogeochemical approaches to estimating metabolic rates need to be reconciled (Arı́stegui et al., 2005; Burd et al.,
2010). While important processes regulating organic matter
transformations and remineralization in the mesopelagic can be
tightly coupled with the euphotic zone, the vast differences in
time and space scales of events within these two zones make
holistic study of the biological pump a challenge, particularly in
terms of its ability to sequester C in the deep ocean.
With residence times in the bathypelagic zone (taken here to
be inclusive of all ocean depths 41000 m) ranging from
centennial to millennial, and spanning the globe spatially, this
zone is only slowly ventilated and circulated (Van Aken, 2007).
Biogeochemical signals in the bathypelagic are thus integrative of
unique ecosystem and metabolic processes occurring slowly over
very long periods. Biological processes in the deepest ocean layers
0967-0645/$ - see front matter & 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.dsr2.2010.02.012
are intimately tied to particle dynamics and microbial food webs,
much of which remain to be characterized (Arı́stegui et al., 2009;
Nagata et al., 2010). These processes, while occurring at low rates,
can play important roles in global marine elemental cycling by
virtue of the incredible volume of the deep ocean, with feedbacks
to the climate system. Changes in ocean stratification, for
example, will elicit changes in the ecosystem functioning of the
deepest layers that will be reflected in changing biogeochemical
fields (e.g., dissolved oxygen concentrations). Slowly occurring
processes, which may happen throughout the ocean depths, are
hidden from view by the strong impacts of more dynamic
processes emanating from the upper ocean. Signals for these
cryptic metabolic and biophysical processes may only emerge in
the deepest layers where vertical and horizontal inputs are
greatly reduced.
The collection of papers in this volume on the ‘dark ocean’ are
a product of the first IMBER (Integrated Marine Biogeochemistry
and Ecosystem Research) IMBIZO (a Zulu word that means
‘‘gathering’’ or ‘‘meeting’’), entitled ‘‘Integrating Biogeochemistry
and Ecosystems in a Changing Ocean’’ and held in Coconut Grove,
Florida, USA, during November 9–13, 2008. The week-long
international conference involved participants in three concurrent
and interacting workshops of 25–40 people each, who contributed
to presentations and extensive discussions pertaining to each
workshop topic. The contributions are a mixture of synthesis
papers and new data papers from participants in two of the
workshops: ‘Ecological and Biogeochemical Interactions in the
Mesopelagic Zone’ and ‘Biogeochemistry and Microbial Dynamics
of the Bathypelagic Zone’. The papers highlight the current state
of our knowledge and our uncertainties about deep-ocean foodweb processes, particle flux and dynamics, and biogeochemical
cycling, and identify opportunities to be pursued in future
research of the dark ocean.
The contributions cover a cross section of disciplines, including
biogeochemistry, organic geochemistry, microbial and plankton
ecology, genomics, technology, and modeling – all of which
advance our understanding of the dark ocean. This special issue
begins with a series of papers on the biogeochemistry and organic
geochemistry of the deep ocean, with a focus on dissolved organic
matter (DOM). Dissolved organic carbon (DOC) is the largest pool
of organic matter in the ocean, is intimately tied to microbial
dynamics, and contributes significantly to C export via ocean
ventilation (Hansell et al., 2009). In the first paper, ‘‘Dissolved
organic carbon export and subsequent remineralization in the
mesopelagic and bathypelagic realms’’, Carlson et al. (2010)
present DOC concentration gradients in the deep North Atlantic
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Editorial / Deep-Sea Research II 57 (2010) 1429–1432
Fig. 1. Graphic representation of ocean volume relative to bottom depth,
illustrating that the deep ocean is the largest living space on Earth. The curve
shows the global volume of water above seafloor depths ranging from 0 to 10.9 km
(the Mariana Trench). The edge of the continental shelf at roughly 200 m is the
traditional boundary of the deep sea. Ecological depth zones of the oceanic water
column: epipelagic, upper 150–200 m; mesopelagic, down to 1000 m; bathypelagic, 1–4 km; abyssopelagic, 4–8 km; hadal, below 8 km. The displayed
volumes of terrestrial and benthic environments include the surface areas of the
dry land and the seafloor and the air or water above to a height of 1 km. (From
Robison, 2009; Data source: UN Atlas of the Oceans - www.oceansatlas.org/).
Ocean to develop a comprehensive picture of the transport and
decay of DOC, the contribution of DOC to apparent oxygen
utilization (AOU), and net DOC export rates from the euphotic
zone into the dark ocean.
In addition to spatial DOC distributions, temporal changes in
DOC in the dark ocean are important for determining DOC export
and controls on utilization. Santinelli et al. (2010), in ‘‘DOC
dynamics in meso- and bathypelagic layers of the Mediterranean
Sea’’, survey DOC distributions in this basin and from those they
infer dynamics. They highlight the role of deep-water formation
events in the export of DOC, finding that 490% of the AOU in
recently-ventilated deep water is due to DOC remineralization.
They also report very high rates of DOC consumption at depth.
These very high contributions and rates differ from the results
described by Carlson et al. (2010), where DOC makes a smaller
contribution to AOU and it is consumed more slowly; thus these
papers indicate contrasting system functionality and opportunity
for further study. Meador et al. (2010) further explore DOC
dynamics as they relate to prokaryotic activity in the deep
Mediterranean in ‘‘Biogeochemical relationships between ultrafiltered dissolved organic matter and picoplankton activity in the
Eastern Mediterranean Sea’’, revealing important relationships
between the chemical composition of DOM and heterotrophic
metabolism. Oxygen consumption and prokaryotic activity were
correlated with components of ultrafiltered DOM (e.g., amino
acids, monosaccharides) to varying degrees, uniquely relating
biochemical composition of DOM to its utilization in deep water
and contributing to our understanding of DOM respiration and
turnover.
The composition of deep-ocean DOM is furthered explored in
two subsequent papers. Yamashita et al. (2010), in ‘‘Fluorescence
characteristics of dissolved organic matter in the deep waters of
the Okhotsk Sea and the northwestern North Pacific Ocean’’,
identify one protein-like, two humic-like, and one uncertain
fluorophore in these waters. By comparing fluorescence intensities and ratios of the humic-like fluorophores with depth and
with AOU in the bathypelagic, differences in the composition of
humic-like fluorophores in epi- vs. meso- vs. bathypelagic waters
were noted. Both humic-like components may be produced in situ
as organic matter is catabolized by organisms. In ‘‘Polymer
dynamics of DOC networks and gel formation in seawater’’,
Verdugo and Santschi (2010) explore the paradox of how
deep-ocean DOM, that due to its low concentration should be
virtually unavailable to microorganisms, may become available to
bacteria – namely by DOM assembly/dispersion dynamics resulting in formation of microscopic gels. These self-assembled
microgels form patches of enriched nutrients that can be readily
utilized by bacteria. In this paper they explain the kinetics and
thermodynamics of DOC assembly/dispersion processes that
result in the formation of microgels.
The last paper pertaining to biogeochemistry of DOM in the
dark ocean is entitled ‘‘Constraining the 2-component model
of marine dissolved organic radiocarbon’’, by Beaupré and
Aluwihare (2010). These authors evaluated multiple Keeling plots
of DOC concentration and D14C depth profiles as tools to
investigate DOC delivery throughout the water column. DOC
variability in the epipelagic is dominated by biogeochemistry
rather than advection, but at greater depths the redistribution of
D14C-enriched DOC occurs primarily via water mass movement.
These findings highlight specific processes to be evaluated in the
deeper reaches of the ocean relative to those dominating the
upper ocean.
The next set of contributions addresses deep-sea food webs
and biogeochemical cycles. In ‘‘Mesopelagic zone ecology and
biogeochemistry – a synthesis’’, Robinson et al. (2010) review
what is known about the diversity and distribution of microbes
and metazoa (from viruses to fish) in relation to their activity and
impact on global biogeochemical cycles. They show how metazoans and microbes play different roles in controlling vertical
transport, cycling, and composition of POM and DOM, and
emphasize the importance of linking mesopelagic microbial and
metazoan diversity to function for understanding and predicting
the effects of global change on deep-ocean food webs and
C sequestration.
Recent findings regarding deep-sea microbial diversity, distribution, and function are reviewed in Nagata et al. (2010),
‘‘Emerging concepts on microbial processes in the bathypelagic
ocean – ecology, biogeochemistry, and genomics’’. This analysis
highlights the remarkable diversity and adaptations of microbes
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to high pressure, low temperatures, and complex organic matter
substrates, and covers the current state of knowledge of the
bathypelagic microbial food web from viruses, through Bacteria
and Archaea, to heterotrophic nanoflagellates (HNF) and ciliates.
Recently discovered communities of bathypelagic microbes and
their novel metabolic capabilities will undoubtedly fill gaps in our
understanding of biogeochemical cycling in the deep ocean. An
important question concerning microbial dynamics in the dark
ocean is how communities differ over large spatial scales. In ‘‘Fulldepth profiles of prokaryotes, heterotrophic nanoflagellates, and
ciliates along a transect from the equatorial to the subarctic
central Pacific Ocean’’, Sohrin et al. (2010) demonstrate that
latitudinal differences in heterotrophic microbial biomass, previously observed in the epipelagic zone, also occur in the mesoand bathypelagic zones. There are important differences in food
web dynamics with latitude and depth as inferred from ratios of
prokaryotes to their protist predators. Moving up a few trophic
levels, Robison et al. (2010) in ‘‘The bathypelagic community of
Monterey Canyon’’ report on the rich pelagic macrofauna
dominated by gelatinous zooplankton in the eastern North Pacific
off central California, as studied with a submersible remotely
operated vehicle (ROV). There are distinct ranges within the
bathypelagic zone for different taxa, some of which are known
detritivores, while abundance of some taxa such as the crustacean
grazers remained fairly constant with depth. This paper also
highlights the value of advanced technologies in our sampling and
interpretation of plankton community structure in the dark ocean.
A number of global budgets and local field studies suggest that
organic carbon utilization (respiration) exceeds organic C input to
the mesopelagic and bathypelagic zones (Boyd et al., 1999; del
Giorgio and Duarte, 2002; Reinthaler et al., 2006; Steinberg et al.,
2008; Baltar et al., 2009). This conundrum is reviewed by Burd
et al. (2010) in ‘‘Assessing the apparent imbalance between
geochemical and biochemical indicators of meso- and bathypelagic biological activity: What the @$#! is wrong with present
calculations of carbon budgets?’’. The imbalance implies either
unaccounted for sources of organic carbon or over-estimated
carbon sinks in the dark ocean. Burd et al. (2010) consider the
problem from both sides, discussing the various uncertainties
associated with environmental variability, measurement capabilities, conversion parameters, and processes that are not well
sampled.
One potential unaccounted source of C supply to the dark
ocean is discussed in ‘‘Major contribution of autotrophy to
microbial carbon cycling in the deep North Atlantic’s interior’’
(Reinthaler et al., 2010). Chemoautotrophic DIC fixation (measured by 14C-bicarbonate fixation) by Crenarchaeota in the dark
ocean was substantial and within the same order of magnitude as
heterotrophic microbial activity (measured by 3H-leucine incorporation). Thus, chemoautotrophy could be a substantial source of
autochthonously produced organic carbon in the dark ocean,
fueling heterotrophic microbial organic carbon demand. In
‘‘Carbon cycling and POC turnover in the mesopelagic zone of
the ocean: Insights from a simple model’’, Anderson and Tang
(2010) further explore carbon budgets of the dark ocean with a
food web model that traces turnover of sinking detrital POC
through to its respiration by particle-attached and free-living
bacteria, and by detritivorous zooplankton. They report that
bacteria account for most of the respiratory C demand and thus
are the primary sink for POC, whereas zooplankton mainly
transform the exported POC to suspended detritus or DOC rather
than respire it to CO2.
There have already been some significant advances in dark
ocean research since our discussions during the IMBER IMBIZO
(Aristegui et al., 2009; Hansell et al., 2009), with many more to
come. This collection of papers is thus timely as we attempt to
1431
shed light on the biogeochemistry and ecology of that vast, dark
Earth system.
Acknowledgments
First, we thank our co-chairs for the mesopelagic (Hiroaki Saito)
and bathypelagic (Gerhard Herndl) workshops as well as the other
members of the IMBIZO scientific organizing committee (Julie Hall,
Coleen Moloney, Wajih Naqvi, Michael Roman, Sylvie Roy, Sharon
Smith, Julie Hollenbeck, and Jing Zhang). We also thank the active
members of the scientific steering committees for the mesopelagic
workshop (Javier Arı́stegui, George Jackson, Carol Robinson, and
Richard Sempéré) and the bathypelagic workshop (Doug Bartlett,
Toshi Nagata, and Dan Repeta), and our invited plenary speakers
(Richard Lampitt and David Karl). Our gratitude to all the other
workshop participants, many of whom traveled half-way around
the globe, for stimulating and enjoyable presentations and
discussions, which led to this manuscript compilation. Many
thanks to the reviewers we solicited whose comments greatly
improved the quality of the manuscripts. Financial support for the
IMBER IMBIZO was provided by The Scientific Committee for
Ocean Research (SCOR), IMBER, the U.S. Ocean Carbon and
Biogeochemistry (OCB) program, EurOceans, Universite de Bretagne Occidentale, Global Ocean Ecosystem Dynamics (GLOBEC),
Centre National de la Recherche Scientifique, and the University of
Miami’s Rosenstiel School of Marine and Atmospheric Science and
Center for Oceans and Human Health. D.K.S. was partially
supported by NSF OCE-0628444 and D.A.H. by NSF OCE-0752972
during the compilation, review, and editing of this volume.
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Deborah K. Steinberg n
Virginia Institute of Marine Science,
The College of William and Mary, Gloucester Point, VA 23062
E-mail address: [email protected]
Dennis A. Hansell
Rosenstiel School of Marine and Atmospheric Science,
University of Miami, Miami, FL, 33149
Received 3 March 2010; accepted 3 March 2010
Corresponding author. Tel.: + 804 684 7838; fax: 804 684 7293.