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Phil. Trans. R. Soc. A (2012) 370, 5613–5635
doi:10.1098/rsta.2012.0399
Pressures on the marine environment and the
changing climate of ocean biogeochemistry
BY ANDREW P. REES*
Plymouth Marine Laboratory, Prospect Place, The Hoe,
Plymouth PL1 3DH, UK
The oceans are under pressure from human activities. Following 250 years of industrial
activity, effects are being seen at the cellular through to regional and global scales. The
change in atmospheric CO2 from 280 ppm in pre-industrial times to 392 ppm in 2011
has contributed to the warming of the upper 700 m of the ocean by approximately 0.1◦ C
between 1961 and 2003, to changes in sea water chemistry, which include a pH decrease of
approximately 0.1, and to significant decreases in the sea water oxygen content. In parallel
with these changes, the human population has been introducing an ever-increasing level
of nutrients into coastal waters, which leads to eutrophication, and by 2008 had resulted
in 245 000 km2 of severely oxygen-depleted waters throughout the world. These changes
are set to continue for the foreseeable future, with atmospheric CO2 predicted to reach
430 ppm by 2030 and 750 ppm by 2100. The cycling of biogeochemical elements has proved
sensitive to each of these effects, and it is proposed that synergy between stressors may
compound this further. The challenge, within the next few decades, for the marine science
community, is to elucidate the scope and extent that biological processes can adapt or
acclimatize to a changing chemical and physical marine environment.
Keywords: climate; ocean; acidification; deoxygenation; hypoxia; eutrophication
1. Introduction
Biogeochemistry is the study of biological, chemical, physical and geological
processes and their interactions within and upon their environment. The cycling
of carbon, nitrogen and other elements is essential to the efficient functioning of
the biosphere and, from a Gaian perspective [1], is the controlling mechanism
that ensures homoeostatic control of the Earth’s environment, making it
suitable for habitation. In recent decades, it has become apparent that our
environment, including the oceans and biogeochemical cycles, is under pressure
from anthropogenic forcing [2]. On local and global scales, these pressures (which
include among others eutrophication [3], warming [4], deoxygenation [5] and
acidification [6]) have the potential to alter the biological, chemical and physical
characteristics of the oceans [7], and their understanding will continue to challenge
the scientific community for the foreseeable future.
*[email protected]
One contribution of 11 to a Theme Issue ‘Prospectus for UK marine science’.
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A. P. Rees
International efforts, which have included initiatives such as the Joint Global
Ocean Flux Study (JGOFS), Integrated Marine Biogeochemistry and Ecosystem
Research (IMBER), World Ocean Circulation Experiment (WOCE) and Surface
Ocean Lower Atmosphere Study (SOLAS), have sought to implement or foster
large-scale investigations of the contemporary ocean. Each has had its own
goals but they are intrinsically connected through their over-arching objectives.
Foremost is the aim to progress our understanding of the present marine
environment in order to predict the potential response of the ocean to the
pressures that may affect its function in the coming century. To take this
understanding further requires the determination of how the role of the ocean
may feed into the whole Earth system and ultimately impact on the social and
economic requirements of the human population.
The UK has been instrumental in the development and delivery of
these programmes and will continue to be so, albeit during a period of
increased financial pressure. Recent organizational activity has seen the
initiation of the multi-agency-funded UK Ocean Acidification Programme
(www.oceanacidification.org.uk) and a revision of the Natural Environment
Research Council (NERC) strategy document in order to reorganize the focus on
biogeochemical cycles and the interactions between the surface and deeper parts
of the Earth system (www.nerc.ac.uk/research/themes/earthsystem). There is
a significant challenge associated with the integration of ocean biogeochemistry
into Earth system science, but there is an obligation on society to meet this
challenge in order to comprehend the extent of this changing environment and
how it may impact on the functioning of global-scale processes. A number of
predicted changes are likely to alter the function of current regimes and challenge
physical, chemical and biological processes: under a warming climate, the retreat
and forecast disappearance of Arctic sea ice [8] is likely to promote the release
of methane [9], carbon dioxide and other climatically active gases into the
atmosphere, with parallel changes in ocean stratification, circulation [10] and the
sequestration of carbon. The deoxygenation of the ocean [5] as a consequence of
warming and enhanced stratification has implications for biogeochemical cycling
and for the fauna that exist within the ocean interior. If the effects of ocean
acidification [11,12] follow some predictions, then there will be shifts in biological
community structure and activity throughout the oceans.
The rate of progress in technological and procedural development that has
accompanied recent research has been exceptional. From an instrumental point of
view, this has included laboratory and shipboard hardware, autonomous vehicles
(including gliders and Autosub) and remote sensing. Progress in methodology has
challenged existing paradigms [13], facilitated the tracking of water movement
and air–sea exchange [14], discovered the most abundant photosynthetic cell
on the planet [15] and provided tools to interrogate the genetic composition
and activity of whole communities [16]. This degree of advancement will need
to continue, not necessarily in instrumentation but certainly in application, in
order to efficiently and economically improve our understanding of the intricacies
of ocean biogeochemistry. Twenty years ago, the deployment of autonomous
instrumentation, molecular biology, remote sensing and real-time oceanography
from shipboard instrumentation were all in their infancy. Today, they are
routine procedures that are relied upon to return an extraordinary amount
of information. The UK and international biogeochemistry communities have
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at their disposal fantastic research facilities and operational platforms, which
include coastal and offshore mesocosms, as well as ships and long-time-series
observatories. The Continuous Plankton Recorder (CPR) survey that is operated
by the Sir Alistair Hardy Foundation for Ocean Science has been collecting data
from the North Atlantic and the North Sea on the ecology and biogeography
of plankton since 1931. More recently, HOT and BATS—the Hawaii Ocean
Time-series (http://hahana.soest.hawaii.edu/hot/hot_jgofs.html) and Bermuda
Atlantic Time-series Study (www.bios.edu/research/bats.html)—were initiated
at sites in the Pacific and western Atlantic, respectively, while AMT—the
Atlantic Meridional Transect (www.amt-uk.org)—offers an annual transect over
approximately 100◦ of latitude through the Atlantic Ocean. We are charged as
a community with the challenge to determine the sensitivity of the ocean to the
stressors acting upon it and on the role that ocean biogeochemistry will play in
mitigating the impact of change on the Earth system and human society.
2. The recent history of ocean biogeochemistry
To perform a review of 20 years of ocean biogeochemistry requires the production
of a dedicated digest far beyond this paper, and indeed several bodies of work
that provide excellent reviews are already published and made available [17,18].
This section provides a summary review of recent biogeochemical research to set
the context of the current condition in order to address concerns for the ocean
that are both current and relevant to subsequent decades.
(a) The JGOFS era
The determination of what we now consider to be the fundamentals of
biogeochemistry are not necessarily based on new developments. A number
of techniques, paradigms and datasets that underpin current oceanographic
practices were developed over the last century:
—
—
—
—
—
1927 development of the Winkler titration for O2 analysis [19];
1930s initiation of English Channel Time-Series of nutrients [20];
1952 14 C method for primary production [21];
1967 15 N method for new production [22]; and
1979 f -ratio as estimate of carbon export [23].
Ocean biogeochemistry really came to the fore though in the mid- to late 1980s.
The impetus provided from the US Global Ocean Flux Study and the excitement
that was generated by the production of the first basin-scale chlorophyll image
in 1986 (figure 1) by Gene Feldman at NASA led to the initiation of the JGOFS
(1987–2003) with the aim [24]:
to assess more accurately, and understand better the processes controlling, regional to global
and seasonal to interannual fluxes of carbon between the atmosphere, surface ocean and
interior, and their sensitivity to climate changes.
The first internationally integrated study of ocean processes soon followed, with
the North Atlantic Bloom Experiment (NABE) [25] in 1989, which involved
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A. P. Rees
chlorophyll-a concentration (mg m–3)
0.01
0.03
0.10
0.30
1
3
10
Figure 1. The first global-scale chlorophyll image produced from the CZCS in 1986. This image
heralded the use of satellite imagery in modern biogeochemistry and provided the impetus to
Earth system science. This CZCS image was obtained from the NASA Ocean Colour website; I
acknowledge assistance from the NERC Earth Observation Data Acquisition and Analysis Service.
ships from the USA, UK, Canada, Germany and the Netherlands, and with
more than 12 nationalities represented on these vessels. Not only did this study
unite the nations in their joint efforts, but it proved to be a significant multidisciplinary effort in consolidating previously disparate oceanographic disciplines
into a concerted study of the biological, chemical and physical characteristics of
the pelagic North Atlantic during the biologically active period of spring and
summer. The success of this initial effort prompted further JGOFS coordinated
campaigns to key oceanographic areas, which included the Southern Ocean,
Arabian Sea and Equatorial Pacific.
The outputs from this work were almost revolutionary in their impact and
contributed significantly to the shape of future research in this field and
how we view the nature of biogeochemistry today. That mesoscale circulation
was intimately connected to the dynamics of phytoplankton activity, that
primary production was strongly linked to variability of CO2 , and that
nitrogen regeneration was active throughout the bloom period, with regenerated
production strongly linked to small cells, do not now seem surprising in any way.
(i) Ocean time series
Long-term time series have proved to be instrumental in resolving trends in
natural variability and in the examination of external pressures on the marine
ecosystem. The CPR survey has provided a significant insight into the sensitivity
of North Atlantic plankton populations to climate and human-induced changes,
which are discussed in detail with respect to the sustainable management of
European seas by McQuatters-Gollop in this issue [26].
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At about the same time as JGOFS was coming into being, funding was
provided by the US National Science Foundation (NSF) to establish the HOT
and BATS time series at deep-water positions in the western North Atlantic and
eastern North Pacific [27]. These two programmes in parallel with others around
the world (DYFAMED, ESTOC, KERFIX, KNOT, OSP and SEATS in the
Mediterranean, northeast Atlantic, Southern Ocean, southwest subarctic Pacific,
northeast subarctic Pacific and South China Sea, respectively) have made repeat
observations of biogeochemical and physical parameters on a regular basis since
1988. Through efforts at these stations, our understanding of ocean processes
has been advanced to recognize the dynamic nature of the world’s oceans and
the occurrence of regime or ecosystem shifts on variable time scales. Previously
recognized paradigms have been challenged, including those concerning new
production as defined by Dugdale & Goering [22] and elemental stoichiometry
associated with the Redfield ratio [28]. We now recognize the importance of
euphotic zone nitrification in the production of ‘regenerated’ nitrate, acknowledge
the wide variability to be found in elemental ratios, and realize how both of
these can have important implications on the efficiency of the biological carbon
pump. As a direct result of work performed at HOT and BATS, nitrogen fixation
was found to be integral to the productivity of the sub-tropical oceans, and the
importance of diazotrophic unicellular cyanobacteria is now recognized alongside
the more obvious filamentous Trichodesmium [29], which previously was held
wholly responsible.
Following the early successes of these fixed-point time series, Aiken et al. [30]
established the AMT in 1995. This is a regular (originally twice a year, currently
annual) transect through the Atlantic Ocean between the UK and destinations in
the South Atlantic (a distance of up to 13 500 km), which to date have been
the Falkland Islands, South Africa and Chile. This programme has provided
exceptional opportunities for biogeochemical oceanography through extremes of
environment (temperate shelf, coastal upwelling, sub-tropical gyres, equatorial
upwelling) and has delivered unique insights into biological carbon cycling and
air–sea exchange of radiatively active gases and aerosols. Work performed during
AMT cruises has refined definitions of ocean provinces [31], validated satellite
algorithms [32], revealed hemispheric differences in hydrography and provided
time-series assessment on basin scales [33].
(ii) The carbon cycle
During the early JGOFS research cruises, the refinement of analytical
procedures to determine the carbon chemistry of sea water was significant in
addressing the question of what controlled the variability of sea water pCO2 .
One of the great achievements of this period, following close collaboration
between JGOFS and WOCE, was the establishment of a global map
of the temporal and spatial variability of air–sea CO2 exchanges, and
the identification of dominant CO2 source and sink areas. Twenty years
hence, and with the significance of CO2 in sea water greater than ever,
this technology is used to inform on process studies and to provide a
network of observations using commercial ships. These data have proved
essential in informing on the variability of the ocean sink for atmospheric
CO2 [34].
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The Coastal Zone Color Scanner (CZCS) was the first instrument deployed in
space to determine ocean colour. It was from this system that Feldman produced
his basin-scale chlorophyll image, and although it was intended to provide
coverage only for a 12-month period as a proof of concept, it remained in operation
between 1978 and 1986. This proved invaluable in the development of procedures
for early global estimates of primary productivity [35]. The launch of the successor
to the CZCS, the SeaWiFS ocean colour scanner, was delayed by several years
until 1997. This no doubt hindered the rate of progress during the major part of
JGOFS, but the subsequent developments from the consolidation of ship-based
observations with remotely sensed data were huge. This collaboration of efforts,
which included modelled outputs, allowed the production of global composites of
primary productivity and carbon export. Consequently, regions were identified in
which oceanographic or biogeochemical processes were important in determining
the degree of productivity and highlighting the importance of recycling and
remineralization within the ocean interior.
The export of carbon from the upper to deep ocean through the biological
carbon pump plays an important role in controlling the capacity of the upper
ocean to hold atmospheric CO2 and to remove C from active exchange with
the atmosphere. The estimation of C export and the efficiency of the biological
carbon pump are impacted by many variables and have been, and continue to
be, approached with different methodologies. These include direct measurement
using sediment traps and indirect estimates using the radionuclide thorium-234
and the f -ratio as a proxy for carbon export. The relationship between primary
(new) production, export and deposition at the sea-bed was found to be regionally
and temporally variable. This made prediction of carbon sequestration difficult,
in part due to the large number of processes acting upon sedimenting material
and to the strong dependence on the community composition from which the
material originated [36]. The export of C is sensitive to a number of environmental
stressors currently acting upon the oceans: phytoplankton communities are
directly influenced by nutrient supply, and ballast material (calcite and opal)
and aggregation processes may be impacted by ocean acidification [37].
A major assumption of biological oceanography has been that the metabolic
balance between respiration and photosynthesis on appropriate scales of time
and space must be equal. This was challenged by observations [38], which
indicated significant regions and periods when respiration systematically exceeded
production in large areas, leaving the ocean in a net heterotrophic condition. The
resolution of this ocean enigma has yet to be found, and the debate continues over
which of the two processes (photosynthesis or respiration) plays the dominant role
in determining the balance between autotrophy and heterotrophy in the open
ocean [39].
(iii) Nutrient limitation
Alongside the development of international collaborations and sampling
observatories during the late 1980s and early 1990s, there were a number
of hypotheses introduced that have challenged the ocean biogeochemistry
community. In 1988, Martin & Fitzwater [40] published their seminal paper,
which provided initial evidence supporting Martin’s hypothesis that Fe limited
phytoplankton growth in high-nutrient low-chlorophyll (HNLC) areas of the
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oceans. An unprecedented number of laboratory, shipboard and mesoscale iron
addition experiments evolved from this, each of which aimed to examine regional
and seasonal variability in the degree of control by Fe over nutrient uptake,
phytoplankton growth and carbon export to the deep ocean. The unequivocal
findings from this work were that iron supply limits production in about one-third
of the global ocean where surface macronutrient concentrations are perennially
high and that iron exerts controls on the dynamics of plankton blooms, which in
turn affects the biogeochemical cycles of carbon, nitrogen, silicon and sulfur, and
ultimately influences the Earth’s climate system [41].
The concept of iron as a limiting nutrient in HNLC areas refuelled the longrunning debate over which nutrient exerted overall control of oceanic primary
production. Previously, this argument had largely been concerned with the
relative influence of nitrogen and phosphorus [42], but with the recognition of
the importance of nitrogen fixation, the role of iron, which is fundamental to
the structure of several essential enzymes, including nitrogenase, as the ultimate
limiting nutrient came to the fore. The debate over which single nutrient or
combination of nutrients provides the dominant control continues [43,44], and is
proving more relevant to our current understanding of the function of the oceans
as we recognize the role of atmospheric dust and aerosol deposition as sources of
iron, nitrogen [45,46] and other elements, and how this may alter under future
climate change predictions.
A further development from mesoscale addition experiments was the use of
sulfur hexafluoride (SF6 ) as an inert, conservative tracer added in parallel to iron
in order to track with great sensitivity the amended waters [14]. This technology
has been used with great success not only in this mode but also as a means of
estimating diffusive fluxes across pycnoclines [47] and fluxes across the sea–air
boundary [48].
(iv) Ocean–atmosphere interactions
The deployment of SF6 , often in parallel with a second tracer (e.g. 3 He),
has been used to parametrize the gas transfer coefficient across the sea–air
interface, which, in concert with gas concentration measurements, has enabled
the identification of sink and source areas of numerous gases in the oceans and
has contributed to our understanding of the role of the oceans in atmospheric
chemistry and global climate. The oceans contribute 30 per cent of the natural
N2 O source to the atmosphere, which is significant owing to its potency as an
efficient greenhouse gas and stratospheric ozone destroyer. Other gases having
oceanic sources that contribute to atmospheric chemistry include low-molecularweight halocarbons and dimethyl sulfide (DMS). The CLAW hypothesis, as
presented by Charlson et al. [49], suggested a negative feedback loop involving
DMS, a compound produced and released under several mechanisms by marine
phytoplankton. Following exchange with the atmosphere, DMS follows a stepwise pathway that, as was proposed, led to the formation of cloud condensation
nuclei (CCN) and ultimately contributes to cloud formation and cloud albedo.
The feedback loop responds to increases or decreases in solar insolation through
altered rates of primary production. An increase in light increases primary
production and therefore DMS production and so cloud albedo, which reflects
incident sunlight, and thus the loop continues. While this would seem a potentially
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A. P. Rees
important mechanism to buffer the effect of a warming environment, evidence
for the feedback loop is as yet equivocal [50]. A recent review of CLAW-related
research also casts some doubt over the strength of the link between DMS
emissions and CCN in the atmosphere [51] but raises an issue over the complexity
of other marine sources of CCN that are relevant to this discussion on the role
of the ocean in climate regulation. While the contribution of DMS to cooling of
the planet is still not proved, Lovelock has suggested that enhanced stratification
predicted as a result of warming may actually limit DMS production and provide
a positive feedback loop where temperature rise is intensified [52].
(b) Other significant developments
During the last two decades, the pace of biogeochemical research has
been maintained through parallel developments in remote sensing, modelling
and molecular biology, so that these three fields are now integral to most
observational research campaigns that are undertaken. As a result of these
combined approaches, the contribution and role of previously unexpected new
metabolic pathways that were revealed over the last 20 years using genomic
and other techniques are now integral to routine biogeochemical investigations.
These have included the discovery of anammox [53], the anaerobic oxidation of
ammonium, which provides a pathway through to N2 and contributes a poorly
quantified part of denitrification in anoxic sediments and ocean basins. Until the
late 1980s, the cyanobacterium Prochlorococcus was unknown. This organism,
whose presence was detected through the advent of analytical flow cytometry [15],
is now considered to be the most abundant photosynthetic cell in the oceans.
In the late 1980s and early 1990s, the ubiquitous abundance of marine viruses
was recognized so that now they are considered to be the most diverse and
numerous biogenic entities in the global marine biosphere, typically numbering
ten billion per litre [54]. Through the process of infecting and lysing their
hosts, viruses influence many biogeochemical and ecological processes, principally
through their release of dissolved, available nutrients.
The advent of the polymerase chain reaction (PCR) led to the discovery of
several groups of Archaea and, since then, they have been shown to be one of
the most abundant unicellular groups in the ocean. Archaea are distributed in
virtually all environments; Crenarchaeota have recently been recognized as the
main drivers of the oxidation of ammonia to nitrite in the ocean, though the
role of other Archaea in marine global biogeochemical cycles remains largely
unknown [55].
Numerical modelling of the marine environment is an essential tool that gives
us a means of synthesis and prediction and with which we can test our level
of understanding. In 1990, Fasham et al. [56] introduced an ecosystem model
designed to allow examination of seasonal cycles of plankton and nutrients in the
global ocean in order to further the understanding of the role of the oceans in the
regulation of atmospheric CO2 . This was to be the first stage in the development
of coupled basin-scale models of ocean circulation with biogeochemistry. This
compartmental (nutrients–phytoplankton–zooplankton–detritus; NPZD) model,
which included plankton and nutrient dynamics, is still used as the basis of
most ecosystem models. The use of nitrogen as a currency allowed, for the
first time, for primary production to be partitioned into new and regenerated
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productivity, reflecting the relative uptake of nitrate or ammonium. Data from
field programmes, from ocean time series and from satellite observations are used
extensively in the development of new model formulations and in the validation of
existing integrated model systems [57]. Doney et al. [57] reflect that the majority
of modelling within JGOFS came at the end of the programme and was not used
in the design of experimental approaches. A great legacy of JGOFS was a more
sophisticated range of biogeochemical models that are now used as an integral
component not only in the synthesis but also in the planning of observational
oceanography. The continued development of biogeochemical models has resulted
in the current generation of dynamic green ocean models (DGOMs). These are
similar to NPZD models but have a much greater complexity and are based
on plankton functional types. DGOMs aim to represent biogeochemical fluxes
specifically associated with ecological processes [58] and have the potential to
assess the effects of climate and environmental change on the ecosystem.
(c) IMBER and SOLAS
The mantle for ocean biogeochemistry coordination was taken from JGOFS by
both the IMBER project (since 2001) and the SOLAS programme (since 2004).
These two international programmes are complementary in their approach and
have brought us to our present understanding of the contemporary ocean and the
potential stressors that are likely to act upon it for the near future. IMBER was
initiated by the IGBP/SCOR Ocean Futures Planning Committee in 2001, with
the intention to identify the effects of global change on the ocean and the most
important biological and chemical aspects of the ocean’s role in global change.
IMBER has specific aims [59]:
to investigate the sensitivity of marine biogeochemical cycles and ecosystems to global
change, on time scales ranging from years to decades, and to provide a comprehensive
understanding of, and accurate predictive capacity for ocean responses to accelerating global
change and the consequent effects on the Earth System and human society.
SOLAS was developed to investigate the key climate linkages between sea and
sky and involved over 26 countries and more than 1600 associated researchers,
with the aim [60]:
to achieve quantitative understanding of the key biogeochemical–physical interactions and
feedbacks between the ocean and atmosphere, and of how this coupled system affects and is
affected by climate and environmental change.
The ethos of both IMBER and SOLAS lies firmly within the spirit of Earth
system science and has united traditional ocean biogeochemistry observations and
models with atmospheric chemistry, climate models and remote sensing. This is
an approach that will very much need to be followed into the future.
3. The current condition and future concerns
While our comprehension of the contemporary ocean is significantly greater now
than ever before, pressures that act upon the biogeochemical cycles therein are
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A. P. Rees
climate change
(winds, temperature, sea
ice, precipitation, run-off
and ocean circulation)
carbon dioxide
reactive
nitrogen
nutrients
deforestation
fossil fuels agriculture
and industry
coastal eutrophication
and hypoxia
altered primary
production
ocean uptake
and acidification
low O2 upwelling
deoxygenation
Figure 2. The over-arching pressures from human activity on ocean biogeochemistry that are
relevant to the contemporary and future ocean. Inputs may occur either directly via fluxes
of material into the ocean (dashed arrows) or indirectly via climate change and altered
ocean circulation (black arrows). The grey arrows denote the interconnections among ocean
biogeochemical dynamics. Adapted from [61]. Reprinted with permission from AAAS.
such that we are constantly playing catch-up in our need to fully understand
the stressors, the synergy between stressors and their impacts on the ecosystem
and its function. The next few decades will prove challenging as we strive
to comprehend the extent of external stressors and the effect that they will
have in disturbing natural systems, with a major challenge being to distinguish
enforced change from natural variability. The impact of human activity over
the last 200 years is now obvious and it is apparent that natural systems are
being altered by anthropogenic inputs on regional and global scales (figure 2).
Predictions into the near future indicate direct and indirect consequences of
perturbations made to the environment by mankind’s activities that will act
on oceanographic and biogeochemical functions [61]. Fossil fuel combustion
and agriculture have contributed to climate change, and these areas each
have significant influence over biogeochemical cycles in the ocean. Anomalous
conditions relative to our current understanding of ocean and biogeochemical
processes are associated with warming, acidification, deoxygenation and nutrient
enrichment. Each condition brings its own individual challenge but is unlikely to
exist without the contribution of one or more of the others.
(a) Climate change
It is without doubt that changes to our climate are happening and that the
main driver for this is human activities [2]. Natural processes do contribute
and include variations in solar radiation, deviations in the Earth’s orbit, plate
tectonics and changes in greenhouse gas concentrations. Anthropogenic inputs of
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radiatively active gases (which include CH4 , N2 O, ozone and water vapour) to
the atmosphere have increased since the industrial revolution, but it is CO2 that
has proved to be the dominant contributor to warming of the environment [62].
Atmospheric CO2 , following the burning of fossil fuels, cement manufacture and
land-use change, has changed from 280 ppm prior to the industrial revolution to
392 ppm in 2011 and is forecast to be approximately 430 ppm by 2030. Mean
global surface temperature rise during the twentieth century was 0.74◦ C and, for
the end of the twenty-first century, this is set to increase further in the range 1.5–
6.1◦ C, depending on CO2 emissions. The upper 700 m of the ocean increased in
temperature by approximately 0.1◦ C between 1961 and 2003 [62]. For the period
between 2003 and 2010, the ocean did not gain any significant amount of heat,
though this is explained as a pause in the overall warming trend as a result of
natural variability [63,64], and it would seem from recent observations that the
warming trend is set to continue [63]. There remains considerable uncertainty
about the details of spatial and temporal variability, but it is clear that climate
change is fundamentally altering ocean ecosystems [65]. Although warming is
the dominant direct effect, with impacts including sea-ice melting, changes to
phytoplankton activity, and distribution and food-web shifts, there are indirect
consequences that will also influence ocean biogeochemistry, including sea-level
rise, pH change, increased stratification, shoaling of mixed-layer depths and
changes to ocean circulation.
The effects of warming are being seen throughout the global oceans but it
is in the polar regions where impacts are most significant, with unprecedented
increases of winter surface temperature of 6◦ C over 50 years for the West Antarctic
Peninsula [66]. The Arctic is warming at about twice the rate of the global
average, with recent studies showing that the area of the Arctic covered by ice
each summer, and the ice thickness, have been shrinking [67] at unprecedented
rates. These rapidly changing conditions impact the physical hydrography, which
in turn influences changes in chemical and biological pathways. In the area of the
Southern Ocean associated with the West Antarctic Peninsula, phytoplankton
biomass has decreased by 12 per cent over the last 30 years, and there has been an
apparent shift from large to small phytoplankton cells [63]. This has implications
for the overall productivity of the region, as effects are seen across trophic levels,
including impacts on even the region’s higher predators. In Arctic waters, the
retreat of sea ice has been dramatic. Since records began in 1979, the extent
of sea-ice coverage has decreased at an average rate of 12 per cent per decade,
with 2011 having the second lowest cover (behind 2007), following higher than
average summer air temperatures. The disappearance of the sea-ice cover has
several implications, which include a positive feedback to warming as a result of
a reduction in surface albedo, the release of methane (another potent greenhouse
gas) following the destabilization of methane clathrates and the modification of
sea-water stratification. Alterations to the salinity and temperature of surface
waters are likely to alter local productivity in a manner similar to that described
for the West Antarctic Peninsula, and may also impact on deep water formation
and the Meridional Overturning Circulation—the driver for the Ocean Conveyor
Belt [62].
There is some contention over the impact of a warming environment on the
productivity of oceanic waters. Saba et al. [68] found, in a comparison of modelled
and in situ data, that net primary production (NPP) increased over a 20-year
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A. P. Rees
period at both HOT and BATS at a rate of nearly 2 per cent per year. By
contrast, Behrenfield et al. [69], using remotely sensed observations, recorded a
strong coupling between climate variability and NPP as a result of enhanced
stratification of the surface layers of the ocean during periods of increased
temperatures. Reductions of NPP, which occur during positive deviations to the
stratification anomaly, are attributed to a reduction in the transfer of nutrients
from the deep ocean to surface waters. Similar trends between variability in
sea surface temperature and primary production have been shown over a 7year period for all provinces of the Atlantic Ocean traversed by the AMT
programme [33], and Polovina et al. [70] show for a 9-year period that the spatial
extents of the north and south oligotrophic gyres of both Atlantic and Pacific
Oceans have increased by 1–4% per year. It would seem that methodological
approach may play some role in the contrasting findings of these different
studies [68], for which Saba et al. [68] suggest the need for ‘an integrated, multifaceted ocean observing system that incorporates both in situ observations and
satellite remote sensing in tandem’.
The oceans are a large sink for atmospheric carbon dioxide [34], which is
supported through a combination of primary production and particle sinking (the
biological pump) [36] and ocean circulation and mixing (the solubility pump).
Climate change will tend to suppress ocean carbon uptake through reductions
in CO2 solubility, suppression of vertical mixing by thermal stratification and
decreases in surface salinity. It is envisaged that climate-driven changes in any of
these physical mechanisms will have a subsequent impact on phytoplankton and
their ability to draw carbon from the atmosphere into the ocean. This will increase
the fraction of anthropogenic CO2 emissions that remain in the atmosphere this
century and produce a positive feedback on climate change.
(b) Ocean acidification
The oceans and atmosphere are intimately linked, so that changes to the partial
pressure of atmospheric CO2 (pCO2 ) result in proportional changes in dissolved
CO2 in the marine environment. As a result of this, the rise of global temperatures
has been buffered by the exchange of approximately 25 per cent of anthropogenic
CO2 into the oceans, and it is this condition that has resulted in a profound change
to ocean carbonate chemistry and the phenomenon of ocean acidification (OA) [6].
As a consequence, oceanic pH is on average approximately 0.1 units lower than
it was prior to the industrial revolution, and future pH levels are predicted to
decrease by an additional 0.2–0.3 units over the twenty-first century with recent
predictions of anthropogenic CO2 emissions [11]. In addition to decreasing pH,
the saturation state of calcium carbonate is lowered, which has implications
for organisms that use calcite in the formation of shells and skeletons. Current
evidence indicates that large and rapid changes to ocean pH will have adverse
effects on a range of marine organisms, with calcifying organisms (which include
benthic and pelagic communities) likely to be the most susceptible. While it is
recognized that the fixation of carbon into organic and inorganic material through
photosynthesis and calcification, respectively, has been shown to be sensitive to
increasing pCO2 [11,12], there is ambiguous evidence over the magnitude and even
the direction (increase or decrease) in which this will occur [37]. Elevated oceanic
pCO2 and the subsequent decrease in pH will have direct and indirect impacts on
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microbial nutrient cycling and carbon fixation, which may fundamentally alter
biogeochemical cycles. Current opinion and biogeochemical models assume that
phytoplankton and prokaryotic growth is limited in part by nutrient availability
(e.g. nitrogen, phosphorus and iron), and that carbon fixation and export are
tightly coupled to these nutrient cycles through elemental stoichiometries. Under
predicted OA scenarios, microbial activity and hence the biogeochemical cycles
they drive may come under pressure from direct and indirect means. Predicting
the response of ecosystems and resources is problematic owing to the range
of effects of high CO2 /low pH reported, the complexity of the whole system,
some conflicting experimental results and the unknown effects of acclimatization
and adaptation.
Early research efforts into the impact of OA on biogeochemical cycles were
largely centred around the fixation of organic and inorganic carbon. Data that
describe the impacts of OA on other key microbially driven ecosystem processes,
such as nitrogen cycling, are still sparse. A small number of studies have indicated
that nitrogen fixation may show a positive response to decreasing pH (e.g. [71])
and this may result in a negative feedback to OA. However, most of these
studies have been performed under laboratory conditions on Trichodesmium, a
single diazotroph species whose response is unlikely to be representative of other
nitrogen-fixing groups under natural conditions. Similarly, our understanding of
the impact of OA on nitrification is based on a small number of investigations.
Current evidence indicates that OA is inhibitory to pelagic nitrification (e.g. [72]),
−
which may result in changes in the NH+
4 : NO3 ratio and a decrease in the ocean
N2 O source. The implications for change to biochemical function due to increasing
OA are apparent, but the uncertainty over expected conditions is compounded
by the added influence of increasing temperatures and, for some areas, decreasing
oxygen levels.
(c) Ocean deoxygenation
The deoxygenation of oceanic waters occurs naturally in oxygen minimum
zones (OMZ), deep basins, eastern boundary upwelling systems and fjords [3],
but climate-driven changes as described in earlier sections are resulting in the
expansion of OMZs in the North Pacific and tropical and sub-tropical areas [5].
Low subsurface oxygen concentrations (hypoxia) exist owing to a combination of
weak ventilation that may occur in concert with or independently of organic
matter remineralization [61]. Ocean deoxygenation is occurring as the ocean
warms and the solubility of dissolved gases decreases, so that the magnitude
and volume of OMZs is increasing, with current predictions indicating declines in
the global ocean O2 content of 1–7% over the next century [73]. The outgassing
of O2 from the ocean to the atmosphere due to climate change could be
up to 125 Tmol yr−1 by 2100 as a result of the combined effects of increased
temperature and enhanced stratification, the thermal effect being responsible for
approximately 25 per cent of the overall change [74].
The concentration of dissolved oxygen controls the biogeochemical cycles
of carbon, nitrogen and other elements, and dictates the presence or absence
of macro-organisms. It therefore plays an important controlling factor in the
functioning of ecosystems. Low-oxygen waters are often classed as hypoxic (1–
30% O2 ), suboxic (less than 1% O2 ) or anoxic (zero O2 ). The OMZs associated
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A. P. Rees
with eastern boundary upwellings are characterized by high productivity, though
each is distinct in its biogeochemical character and oxygen inventory. Those in
the Pacific and Arabian Sea are largely considered suboxic, while those on the
eastern Atlantic are hypoxic. This impacts the cycling of elements in intermediatedepth water masses, but, in particular, the oxygen content plays a significant
controlling factor on the nitrogen biogeochemistry. Under suboxic to anoxic
conditions, denitrification and annamox are likely to be active processes that
+
act as a sink to fixed nitrogen (NO−
3 and NH4 , respectively) and thus modify the
degree of availability to phytoplankton in surface waters. Under these conditions,
denitrification may contribute a source of NO−
2 and N2 O and thus increase
the oceanic source of this effective greenhouse gas and ozone destroyer to the
atmosphere. Regions of suboxia are generally seen to be strong net producers
of N2 O [75]. Nitrification, an aerobic process, releases N2 O as waters become
increasingly hypoxic, while denitrification can act as either a source or sink under
suboxic conditions. There is a subtle balance in the degree of oxygen present that
dictates the net release of N2 O during denitrification and nitrification, which
makes changes to ocean oxygen content significant. Model predictions indicate
that not only are biogeochemical cycles sensitive to small changes in ocean
oxygen content but so also is the spatial extent of hypoxia [76] and that this
response is maximal in suboxic zones. Deutsch et al. [76] describe a direct control
imparted by climate change on the variability of low-oxygen zones, which also
results in large fluctuations in denitrification and therefore a direct link between
climate oscillations and nitrogen limitation of primary productivity. The balance
in oxygen content may also impact other microbial processes, and the distribution
of higher trophic levels, as lethal and sub-lethal thresholds vary greatly among
marine organisms. This may offer a further feedback to atmospheric chemistry,
as these areas are key regions in the budgets of other climatic gases, including
CO2 , CH4 and halogenated carbon compounds.
(d) Eutrophication and coastal hypoxia
Enhanced nutrient deposition to coastal waters, through fossil fuel burning,
fertilizer run-off and waste-water generation, has occurred on a global scale
during the industrial age. It is widely accepted that activities such as these
have more than doubled the global rate of terrestrial nitrogen fixation, with
even higher rates predicted for coming decades [77]. The obvious evidence of
this is an increase in primary productivity and algal biomass in coastal waters,
though it is the consumption of dissolved oxygen during microbial decomposition
of this and other organic material that presents the greatest cause for concern [78].
Under severe conditions of oxygen depletion, the so-called dead zones are created,
wherein there exists an absence or significant reduction in the presence of
expected macrofaunal communities. Often, these dead zones are associated with
stratified, semi-enclosed environments that have restricted water exchange, such
as areas within the Black Sea, the Gulf of Mexico and East China Sea, among
others. The occurrence of this phenomenon has increased dramatically since the
mid-twentieth century, when the use of industrially produced fertilizer began
increasing on a massive scale. In 2008, there were reported to be dead zones
associated with more than 400 coastal systems that affected an area of greater
than 245 000 km2 [78]. As described already, the depletion of oxygen can affect
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Changing ocean biogeochemistry
5627
not only the benthic faunal communities, but also the biogeochemical cycles
inherent to these systems. The death or migration of bioturbating animals that
ventilate sediments and influence porewater chemistry may have knock-on effects
to rates of nitrification and denitrification, in addition to those associated with the
direct effect of decreasing oxygen levels. As denitrifying organisms obtain oxygen
from NO−
3 under decreasing suboxia, there is a subsequent reduction of fixed
nitrogen and potential for increased N2 O production. Under anoxic conditions,
toxic hydrogen sulfide is produced, while the remineralization of organic matter
that has contributed to the hypoxic conditions also produces CO2 , so that there
exists a coupled OA and deoxygenation scenario that, in the warmer climate
of tomorrow, introduces a whole matrix of synergistic stressors on the marine
ecosystem [7,61].
4. The ongoing challenge
While it is apparent that a reduction in greenhouse gas emissions is essential in
order to minimize future levels of ocean acidification, warming and deoxygenation,
we are already committed to experience a certain degree of each [7,79]. There is
therefore an urgent need to reconcile our current understanding of biogeochemical
cycles with changes forced by anthropogenic activity. Specifically, during the next
two decades or so, there will be an emphasis on the determination of individual
and synergistic or antagonistic impacts of these stressors in order to inform
prediction and mitigation strategies.
We are therefore charged as a research community with the challenge to
determine the sensitivity of the ocean to the external forces acting upon it and to
the role that ocean biogeochemistry will play in alleviating (or exacerbating)
the impact of change on the Earth system and human society. To deliver
this, there is an ever-pressing need to fully integrate ocean biogeochemistry
with Earth system science by employing a comprehensive multidisciplinary
approach. The engagement across disciplines that include atmosphere, climate
and physical oceanography must necessarily link to the social and economic
sciences in order to create an effective dialogue between research and decisionmaking communities.
Boyd et al. [80] reviewed a series of laboratory, shipboard and field experiments
in order to comment on the design features of the experimental approach to be
taken when investigating the impact of climate change on oceanic phytoplankton.
A number of phytoplankton-group-specific limiting factors were noted, which led
to synergistic and antagonistic impacts on productivity or community structure.
Elevations in temperature and iron were shown to synergistically increase the
growth rate of Antarctic diatoms, while an antagonistic relationship was observed
between iron and light on the growth of Phaeocystis antarctica. Boyd et al. [80]
recommended that, in order to improve on existing approaches, it is necessary
to ensure the consideration of all environmental factors that are likely to be
impacted, and the interactions between them. Factorial matrix perturbation
experiments should be used to investigate subsets of conditions that are relevant
to specific phytoplankton groups. Further to improving the observational and
experimental approach is the requirement to incorporate the capability of
DGOMs [58] and other state-of-the-art ecosystem models [81] that are capable of
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A. P. Rees
resolving and predicting marine ecosystem function under actual or theoretical
climate change scenarios. From a biogeochemical perspective, the over-arching
question to be asked is huge: How will anthropogenic forced change, coupled
with natural climatic variability, affect biogeochemical functioning of the marine
ecosystem, from cellular process to ecosystem level, and how will such changes
feed back to the Earth system?
Even today, after more than a century of observational oceanography, it is
a widely held belief that the oceans are grossly undersampled [61]. Therefore,
a fundamental approach to address this is to significantly increase the spatial
and temporal extent of oceanographic and, from this paper’s perspective,
biogeochemical observations. This will enable us to determine the variability of
natural processes, and their sensitivity to changes in the environment, and to
detect and resolve the enigmatic decadal (and longer) trends in ocean character.
The most obvious example of a concerted effort of increasing coordinated
observations that is currently operational is the Global Ocean Observing System
(GOOS; http://gosic.org/ios/goos). GOOS is a global system for sustained
observations of chemical and physical variables in the ocean, which, together
with the Global Climate Observing System and the Global Terrestrial Observing
System, forms the Global Earth Observing System of Systems. GOOS maintains
a permanent system for observation, modelling and analysis of temperature,
salinity and, to a lesser extent, other variables, which include CO2 and O2 .
In addition to ship-based observations, data sources include remote sensing,
moored instruments and free-floating and profiling floats such as those used in
the ARGO programme. ARGO involves 23 countries and, as of January 2012, has
been responsible for the deployment of 3476 autonomous floats throughout the
oceans. These free-drifting profiling floats measure the temperature and salinity
of the upper 2000 m of the ocean and regularly transmit data, so that data
are publicly available within hours of collection. A limited number of ARGO
floats and similar profiling bodies have been exploited to carry additional sensor
packages. These include transmissometers to estimate particulate organic carbon
(POC) and carbon export [82,83], bio-optical sensors to determine chlorophyll-a
concentrations [83] and nitrate sensors [84]. The combination of these sensors,
if deployed on a sufficient number of floats, will provide a means to improve
validation of remotely sensed ocean colour products, which include chlorophyll,
phytoplankton carbon and improved bio-optical models of primary production.
One adaptation of such floats, Carbon Explorers, have been successfully used to
determine POC and particulate inorganic carbon fluxes and have the potential
to be further developed to determine the full extent of the carbon inventory [85].
A further development from profiling floats are autonomous underwater vehicles
or gliders that can carry a suite of sensors and, being propeller-driven, can be
used to deliver high-resolution surveys or longer transect-type studies. Vehicles
such as these are now being used to deliver high-resolution information on
physical, chemical and biological characteristics in a manner not possible from
ship-board observations or even through the combined observations of satellites
and profiling floats [86,87]. The integration of reliable nutrient (e.g. nitrate,
phosphate and iron) sensors with sufficient sensitivity for upper ocean conditions
into floats, moorings and autonomous vehicles now seems realistic after several
years of low-sensitivity instrumentation. Commercially available packages are
now available for moored deployments, which incorporate automated molecular
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Changing ocean biogeochemistry
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probes to inform on microbial community composition and its genomic and
proteomic activity, such as the Environmental Sample Processor [88]. The
next generation of these and other instrumentation packages are necessary to
facilitate a large-scale improvement in the extension of the current biogeochemical
observational capacity. The continued development of sophisticated, intricate and
high-resolution platforms that will improve predictive capacity and the resolution
of natural annual and decadal variability is essential to fully augment mechanistic
studies of the adaptive capability of ocean biogeochemistry.
It might seem, then, that the oceans are actually well sampled and that there
is an existing infrastructure in place to coordinate and output real-time data.
In effect, this is only the case for a very restricted set of variables. Future
biogeochemical research ought to be directed to extend the process-based studies
of the type performed under the auspices of JGOFS and SOLAS to include
mechanistic responses of organisms and biogeochemical cycles to the increasing
perturbations associated with the ocean stressors identified above. There is then
the need to take an Earth system approach to incorporate targeted experimental
process studies, as championed by Boyd et al. [80], with large-scale observations
using state-of-the-art autonomous instrumentation, which fully embraces the
application of the new generation of genomic approaches, integrated models and
remote sensing.
5. A role for the UK
The UK has a well-placed extensive experience base to address concerns
associated with ocean biogeochemistry. Existing centres, which include
universities, government agencies and NERC institutes and collaborative centres,
each have independent identities but are well versed in collaborative ventures
to provide the multidisciplinary approach required to address burning issues
such as those identified here. In 2011, the National Oceanography Centre
(NOC) Association (http://noc.ac.uk/about-us/noc-association) was formed and
in December of that year produced its publication ‘Setting Course’, which presents
the vision to create a more integrated UK marine science community to tackle
the environmental challenges ahead. The NOC Association comprises the NERCfunded marine science community of the UK. The vision is to guide UK marine
science into the future by the provision of large-scale infrastructure such as
ships and underpinning activities such as data management under a nationally
coordinated structure, and to place ocean research with atmospheric, polar and
terrestrial disciplines alongside living systems, including human society, together
in the context of a whole Earth system. The ‘Setting Course’ document calls
for a funding environment that ensures the health of our intellectual capital base
and stimulates collaborative research that nurtures a varied research environment
and facilitates fit-for-purpose national research infrastructure and capability. In a
societal environment that is globally economically fragile and politically dynamic,
it is difficult to predict funding and organizational structures far into the future,
but it is encouraging to be part of a unified approach to future marine research
priorities. From a biogeochemical point of view and with respect to previous
sections of this paper, the ‘Setting Course’ vision strongly advocates the need to
prioritize the understanding of the role of the ocean in the Earth system and on
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A. P. Rees
the human population, on time scales of days to centuries and from local to global
space scales. It recognizes fully the significant role of the oceans in regulating
climate and the pressures associated with a high-CO2 environment and enhanced
nutrient enrichment.
In summary, the UK has indicated its intent to approach this great challenge
head-on, and to direct resources with which to do so. In order to do justice to
this vision, there are a number of priorities that have been identified within this
paper, which should feature in our research agenda:
— maintain a global approach through the sustained involvement in
polar to tropical seas, which encourages and facilitates multidisciplinary
integration, and which allows the targeting of sensitive ocean areas;
— foster research programmes that are not constrained by short-term (3–5
year) funding, to allow realistic time frames within which to investigate
adaptation and acclimatization to changing environments;
— improve confidence in the ability to distinguish natural trends and
variability from those forced by anthropogenic activity;
— support the development, maintenance and operation of autonomous
instrumentation, which includes biogeochemically relevant sensors, for
deployment on a diverse fleet of profiling floats, gliders and moorings;
— increase sustained observations in time and space, and for observations
to be closely integrated with targeted measurements of biogeochemical
processes, which are supported by model and observational experimental
interrogation of relevant change scenarios;
— harness increasing computing power to run model experiments that can
direct multi-factorial experimental programmes and inform on appropriate
targets for process studies; and
— contribute to the security and continuity of satellite observations and
further develop the ability to estimate process rates, particle loads and
plankton composition from remote sensing.
It is without doubt that ocean biogeochemistry and the oceans in general are
facing increasing pressures from man’s activities and that, even if CO2 emissions
and nutrient additions were immediately reduced to pre-industrial levels, there
is sufficient inertia in the system to ensure that the effects of warming, ocean
acidification, deoxygenation and eutrophication will remain for several decades
into the future. The marine research community has wholly embraced these
concerns and has been pro-active in the development of research programmes to
inform on the degree to which organisms, ecosystems and biogeochemical cycles
may be impacted. The importance of the oceans to the well-being of human
society is absolute, and it is essential that this message be transferred clearly and
effectively to decision- and policy-makers.
I thank the editors of this Theme Issue, Harry Bryden, Carol Robinson and Gwyn Griffiths, for
inviting me to participate in this venture, and I take this opportunity to recognize particularly my
appreciation of the challenges and support regularly offered to me by Carol. The comments by an
anonymous reviewer and Phil Boyd greatly improved the manuscript.
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