REVIEW ARTICLE
PUBLISHED ONLINE: 9 JUNE 2013 | DOI: 10.1038/NGEO1830
Anthropogenic perturbation of the carbon fluxes
from land to ocean
Pierre Regnier et al.†
A substantial amount of the atmospheric carbon taken up on land through photosynthesis and chemical weathering is transported
laterally along the aquatic continuum from upland terrestrial ecosystems to the ocean. So far, global carbon budget estimates
have implicitly assumed that the transformation and lateral transport of carbon along this aquatic continuum has remained
unchanged since pre-industrial times. A synthesis of published work reveals the magnitude of present-day lateral carbon
fluxes from land to ocean, and the extent to which human activities have altered these fluxes. We show that anthropogenic
perturbation may have increased the flux of carbon to inland waters by as much as 1.0 Pg C yr-1 since pre-industrial times, mainly
owing to enhanced carbon export from soils. Most of this additional carbon input to upstream rivers is either emitted back to
the atmosphere as carbon dioxide (~0.4 Pg C yr-1) or sequestered in sediments (~0.5 Pg C yr-1) along the continuum of freshwater
bodies, estuaries and coastal waters, leaving only a perturbation carbon input of ~0.1 Pg C yr-1 to the open ocean. According to
our analysis, terrestrial ecosystems store ~0.9 Pg C yr-1 at present, which is in agreement with results from forest inventories
but significantly differs from the figure of 1.5 Pg C yr-1 previously estimated when ignoring changes in lateral carbon fluxes. We
suggest that carbon fluxes along the land–ocean aquatic continuum need to be included in global carbon dioxide budgets.
D
uring the past two centuries, human activities have greatly
modified the exchange of carbon and nutrients between the
land, atmosphere, freshwater bodies, coastal zones and the
open ocean1–9. Together, land-use changes, soil erosion, liming,
fertilizer and pesticide application, sewage-water production, damming of water courses, water withdrawal and human-induced climatic change have modified the delivery of these elements through
the aquatic continuum that connects soil water to the open ocean
through rivers, streams, lakes, reservoirs, estuaries and coastal zones,
with major impacts on global biogeochemical cycles10–14. Carbon is
transferred through the aquatic continuum laterally across ecosystems and regional geographic boundaries, and exchanged vertically
with the atmosphere, often as greenhouse gases (Box 1).
Although the importance of the aquatic continuum from land
to ocean in terms of its impact on lateral C fluxes has been known
for more than two decades15, the magnitude of its anthropogenic
perturbation has only recently become apparent 8,12,16–18. The lateral
transport of C from land to sea has long been regarded as a natural loop in the global C cycle unaffected by anthropogenic perturbations. Thus, this flux is at present neglected in assessments
of the budget of anthropogenic CO2 reported, for instance, by the
Intergovernmental Panel on Climate Change (IPCC) or the Global
Carbon Project 19–23. Quantifying lateral C fluxes between land and
ocean and their implications for CO2 exchange with the atmosphere
is important to further our understanding of the mechanisms driving the natural C cycle along the aquatic continuum24,25, as well as
for closing the C budget of the ongoing anthropogenic perturbation.
Data related to the C cycle in the aquatic continuum from land
to ocean are too sparse to provide a global coverage, with insufficient water sampling, poorly constrained hydrology and surface
area extent of various ecosystems, and few direct pCO2 and other
carbon-relevant measurements26,27. Global box models have been
used to explore the magnitude of these fluxes and their anthropogenic perturbations, but the processes remain highly parameterized7. The current generation of three-dimensional Earth system
models includes the coupling between the C cycle and the physical
climate system, but ignores lateral flows of C (and nutrients) altogether 28. Major challenges in the study of C in the aquatic continuum include the disentangling of the anthropogenic perturbations
from the natural transfers, identifying the drivers responsible for
the ongoing changes and, ultimately, forecasting their future evolution, for example, by incorporating these processes in Earth system models. Resolving these issues is not only necessary to refine
the allocation of greenhouse-gas fluxes at the global and regional
scale, but also to establish policy-relevant regional budgets and
mitigation strategies29.
The term ‘boundless carbon cycle’ was introduced to designate
the present-day lateral and vertical C fluxes to and from inland
waters only 17. Here, we extend this concept to all components of the
global C cycle that are connected by the land–ocean aquatic continuum (Box 1) and discuss possible changes relative to the natural C cycle by providing new separate estimates for the present day
and the anthropogenic perturbation. This distinction is important
because, in some instances, bulk fluxes have been compared with
perturbation fluxes, such as the net land C sink of anthropogenic
CO2, which may cause confusion17,30. Here we deal with the total C
fluxes, but do not systematically distinguish between inorganic and
organic, as this is still poorly known at the global scale for several
of the components of the land–ocean continuum. However, we do
highlight the exact chemical composition where it is sufficiently well
constrained. Supplementary Table S1 is a compilation of the major
flux estimates from the literature and estimated in this paper with
a measure of confidence involving transfer of C from one global
domain to another. A brief justification of our proposed estimate for
each of these fluxes is also provided.
Contemporary estimates of lateral carbon fluxes
In this section, we derive contemporary estimates of the carbon fluxes
along the continuum of the spectrum of land–ocean aquatic systems.
We first look at the C transports involving inland waters and then
consider their links to C flows through estuaries and the coastal ocean
and beyond.
A full list of authors and their affiliations appears at the end of the paper.
†
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REVIEW ARTICLE
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Box 1 | Land–ocean carbon flux concepts
The land–ocean aquatic continuum. This can be represented
as a succession of chemically and physically active biogeochemical systems, all connected through the continuous water film
that starts in upland soils and ends in the open ocean. Carbon
is transferred along this continuum. These systems are often
referred to as filters, because carbon is not only transferred, but
also processed biogeochemically and sequestered in sediments
or exchanged with the overlying atmosphere as greenhouse
gases (Fig. 1a).
The pre-industrial land–ocean loops. Lateral carbon transfer
through the aquatic continuum was already active under preindustrial conditions and the boundless carbon cycle consists
of two loops. The organic carbon loop starts with the lateral
leakage of some of the organic carbon that is fixed into the
terrestrial biosphere by photosynthesis. This carbon is then
transferred horizontally through aquatic channels down to the
coastal and open ocean where C is returned to the atmosphere
as CO2. The inorganic loop is driven by the land-based weathering of silicate and carbonate rocks that consumes atmospheric CO2, and the subsequent transport of the weathering
products of cations, anions and dissolved inorganic carbon to
the ocean, where part of the CO2 is returned to the atmosphere
through ocean carbonate sediment formation (a process that
increases pCO2 in seawater). The other part is returned by volcanism. Both loops are generally assumed to have been in a
quasi-steady-state initial condition in pre-industrial times, that
is, they were globally balanced at the millennial timescale.
Anthropogenic perturbation of the lateral carbon fluxes.
Human perturbations to the lateral carbon fluxes have moved
the boundless carbon cycle away from this global balance,
causing imbalances in the fluxes and stocks, such as the C
inputs from soils to inland water systems, the strength of the
air–water CO2 exchange fluxes, the C storage reservoirs and,
thus, the chain of lateral C fluxes through the successive filters.
Because the reconstruction of lateral carbon fluxes entails large
uncertainties, we only attempt quantification for pre-industrial
and present-day (past decade) conditions. We thus regard the
change in the fluxes and stocks since the pre-industrial period
as the anthropogenic perturbation, and treat the average preindustrial conditions as the natural contribution.
Inland waters. The present-day bulk C input (natural plus anthropogenic) to freshwaters was recently estimated at 2.7–2.9 Pg C yr–1,
based on upscaling of local C budgets17,26. This input is composed of
four fluxes. The first and largest one is soil-derived C that is released
to inland waters, mainly in organic form (particulate and dissolved),
but also as free dissolved CO2 from soil respiration31 (F1 in Fig. 1a
and Table 1). The flux is evaluated at 1.9 Pg C yr–1, by subtracting,
from a total median estimate of 2.8 Pg C yr–1, the smaller contributions from the other three fluxes: chemical weathering (F2), sewage
(F4) and net C fixation (F5). The soil-derived C flux is part of the
terrestrial ecosystem C cycle (Box 1) and represents about 5% of soil
heterotrophic respiration (FT7). Current soil respiration estimates
neglect the C released to inland waters. A downward revision of the
estimate of soil heterotrophic respiration to account for the soil C
channelled to inland freshwater systems would nevertheless remain
within the uncertainty of this flux 32.
The second flux involves the chemical weathering of continental
surfaces (carbonate and silicate rocks). It is part of the inorganic
2
(often called ‘geological’) C cycle (Box 1) and causes an additional
~0.5 Pg C yr–1 input to upstream rivers33–37 (F2). About two-thirds
of this C flux is due to removal of atmospheric CO2 in weathering
reactions (F3) and the remaining fraction originates from chemical weathering of C contained in rocks. The pathway for chemical weathering is nevertheless largely indirect with most of the
CO2 removed from the atmosphere being soil CO2, having passed
through photosynthetic fixation. Weathering releases C to the
aquatic continuum in the form of dissolved inorganic C, mainly
bicarbonate, given that the average pH is in the range of 6–8 for
freshwater aquatic systems38. In contrast to soil-derived organic C,
it is assumed that C derived from rock weathering will not degas to
the atmosphere during its transfer through inland waters39.
The third flux represents the C dissolved in sewage water originating from biomass consumption by humans and domestic animals (F4), which releases an additional ~0.1 Pg C yr–1 as an input to
freshwaters40,41. The fourth flux involves photosynthetic C fixation
within inland waters, potentially high on an areal basis16. A substantial fraction of this C is returned to the atmosphere owing to
decomposition within inland waters42, but a percentage remains
for export and burial43,44, and priming of terrestrial organic matter
decomposition45. Thus, although aquatic systems can emit CO2 to
the atmosphere, they still can be autotrophic46. We estimate with
low confidence that 20% of the organic C buried and exported from
inland waters (see below for estimations) is autochthonous (F5).
Physical erosion of particulate inorganic C (~0.2 Pg C yr–1) and
of organic C that is resistant to mineralization (~0.1 Pg C yr–1)
represents another C source to the aquatic continuum47,48 (FR).
Although the fate of this physically eroded C is difficult to trace, it is
likely to be refractory at the centennial timescale49 and is most likely
channelled through inland waters and estuaries to the open ocean
without significant exchange with the atmosphere. It is thus treated
separately in Fig. 1a.
During the transport of C from soils to the coastal ocean, a
fraction of the lateral flux that transits through inland waters is
emitted to the atmosphere, mainly as CO2 (F7). CH4 is also emitted
from lakes and some rivers (F6), but this flux represents a small
fraction of the laterally transported C flux 30. Data-driven estimates
of the water-to-atmosphere CO2 efflux have been obtained for
individual components of the inland freshwater continuum16,17,50.
This efflux is sustained by CO2 originating from root and soil
respiration, aquatic decomposition of dissolved and particulate
organic matter, and decomposition of organic C from sewage, as
detailed above. Furthermore, the addition of C from fringing and
riparian wetlands, counted as soil C input to freshwaters in Fig. 1a,
may also contribute significantly to freshwater CO2 outgassing 51.
Approximately 12,000 sampling locations of the inorganic C cycle
are now reported in inland water databases (Fig. 2a). Calculation
of pCO2 from alkalinity and pH indicates that 96% of inland
waters are oversaturated with respect to CO2 relative to its atmospheric concentration, while 82% have a concentration of at least
twice that of the atmosphere (Global River Chemistry Database
(GloRiCh), unpublished data; ref. 52).
Numerous measurements of the freshwater CO2 efflux are available for some regions of the globe, such as the Rhine catchment,
Scandinavia and the conterminous United States39,42,51–53. However,
lack of direct CO2 flux measurements, incomplete spatial coverage
of pCO2 sampling locations coupled with the difficulty in determining the surface area of inland waters, and scaling the gas-transfer
velocity in freshwaters, causes large uncertainties and prevents us
from obtaining robust global-scale estimates (Fig. 2a). In particular,
many rivers and lakes that contribute a significant fraction to the
aquatic C flux remain poorly surveyed in terms of pCO2 (GloRiCh,
unpublished data). These include the rivers of Southeast Asia, tropical Africa and the Ganges and, to a lesser extent, the waters of the
Amazon Basin54,55, which carry disproportionally high organic
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REVIEW ARTICLE
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a
Present day
FT3 FT6
FT2 FT4 FT7
FF
FT1
7.9
59
F5
F6
0.1
49.9 0.3
0.3
3.85
F7
F11
0.3+
1.1
0.15
Biomass
∆C = 1.0
Inland
waters
1.9
0.25
1.85
F13
F9
0.5
0.6
0.1
F8
Sediments
F16
∆C = 0.05
∆C ≈ 0
0.3
0.75
∆C = +2.4
0.3
F12
0.35
FR
0.2
∆C = +0.95 FO2
F15
F2 FR
LOAC
Bedrock
Natural
FT3 FT6
FT2 FT FT7
FT1
FF
F5
4
52.2
1.5
0.15
55
0
0
F6
0.2
53.5
F7
F11
Inland
waters
0.25
0.45
0.15
0.65
F9
F13
F16
∆C = 0
0.3
∆C = 0
0.2
Sediments
Open
ocean
0.85
∆C = 0
0.4
Coastal
ocean
0.8
∆C = 0.05
0.15
F8
F12
∆C = 0
0.3
FR
0.2
F15
F2 FR
Fossil fuel reserves
Atmosphere
FO1
FG
∆C = –0.55
0
Estuaries
F1
Soils
F14
Marshes and
mangroves
∆C ≈ 0
1.1
F4 0
F3 0.3
F10
0.45+
0.6
0.1
0
Biomass
∆C = 0
FT5
c
0.15
Open
ocean
0.95
∆C ≈ 0
∆C = –7.9
b
Atmosphere
FG
Coastal
ocean
1.0
∆C = –0.15
Fossil fuel reserves
FO1
0.2
Estuaries
F1
Soils
F4 0.1
F3 0.35
F14 ∆C = +3.65
Marshes and
mangroves
∆C ≈ 0
1.95
FT5
51.95
F10
0.2
∆C = 0.5
FO2
LOAC
Bedrock
Anthropogenic perturbation
FF
FT1
FT2 FT3
7.9
4
3.85
FT4
0.15
FT6 FT7
0.15
2.3
F5
F6
0.1
F7
0
F11
–0.15+
0.5
Biomass
∆C = 1.0
Inland
waters
FT5 –1.55
0.1
F3
∆C = –0.2
0.05
0
Atmosphere
FG
FO1
2.3
0
Open
ocean
0.1
0.1
F9
F13
F16
∆C ≈ 0
0.4
Sediments
Coastal
ocean
0.2
∆C ≈ 0
0.1 0
∆C = –7.9
F8
∆C = +2.4
∆C = 0.05
–0.05
F12
F2 FR
Fossil fuel reserves
∆C = +4.2
0.2
Estuaries
0.8
F1
Soils
F14
Marshes and
mangroves
∆C ≈ 0
0.45
F4
F10
Bedrock
0
FR
0.15
F15
LOAC
0
∆C = +0.5 FO2
∆C = –0.05
Figure 1 | Global carbon budget and its anthropogenic perturbation. Estimates are shown for a, the present day (2000–2010), b, the natural C cycle
(~1750) and c, the anthropogenic perturbation only. All fluxes are in Pg C yr–1, rounded to ±0.05 Pg C yr–1, and refer to total C fluxes (organic and inorganic
C). The numbers associated with the arrows are fluxes between reservoirs. Boxed ΔC refers to C accumulation within each reservoir. The red box
delineates the succession of lateral C filters along the land–ocean aquatic continuum (LOAC). The + sign indicates that C sequestration from estuaries and
adjacent coastal vegetation are merged in the figure. The stars in panel a indicate the confidence interval associated to the flux estimates, based on The
First State of the Carbon Cycle Report99. A black star means 95% certainty that the actual estimate is within 50% of the estimate reported; a grey star means
95% certainty that the actual value is within 100% of the estimate reported; a white star corresponds to an uncertainty greater than 100%. Flux symbols
are defined in Table 1.
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close to values based on compilation of field data47,58 and the results
of the Global Nutrient Export from Watersheds model of carbon
and water flows59, although higher values have also been suggested8.
A flux of particulate and dissolved organic C, each equivalent to
about 0.2 Pg C yr–1, and a flux of dissolved inorganic C of about
0.4 Pg C yr–1 is the conventional partitioning among the different
C pools47,58,60,61. If we take into account the uncertainty for each of
the individual inland water fluxes (weathering, outgassing, burial
and export), the balance also indicates that the soil-derived C flux
(F1, 1.9 Pg C yr–1) is certainly not known any better than within
~±1.0 Pg C yr–1.
Table 1 | Definition of carbon flux symbols used in Fig. 1.
Symbol
Flux name
FF
Fossil-fuel emissions
FT1
Net primary production of terrestrial ecosystems
FT2
Harvest, cattle and biofuels emissions (CO2)
FT3
Fire emissions (CO2)
FT4
Cattle, landfills and fire emissions (CH4)
FT5
Terrestrial biomass to soil C flux
FT6
Rice paddies and wetland emissions (CH4)
FT7
Soil heterotrophic respiration (CO2)
F1
Total soil C input to inland waters
F2
Inorganic C input to inland waters from weathering
F3
Atmospheric CO2 uptake by bedrock weathering
F4
Organic C inputs to inland waters (sewage)
F5
Photosynthetically fixed C not respired in inland waters
FR
Physical erosion of total recalcitrant C
F6
CH4 emissions from inland waters to the atmosphere
F7
CO2 emissions from inland waters to the atmosphere
F8
Total C burial in inland water sediments
F9
Total lateral C flux from inland waters to estuaries
F10
CO2 emissions from estuaries to the atmosphere
F11
CO2 uptake from marsh ecosystems and subsequent organic C
input to estuaries
F12
Total C burial in estuarine sediments and coastal vegetated
ecosystems
F13
Total lateral C flux from estuaries to the coastal ocean
F14
Atmospheric CO2 uptake by coastal waters
F15
Total C burial in coastal ocean sediments
F16
Total C export from the coastal to the open ocean
FO1
Air–sea CO2 flux in the open ocean
FO2
Total C burial in open ocean sediments
FG
Geological fluxes (volcanism, metamorphism and oxidation of
fossil organic C)
carbon loads owing to their combination of high terrestrial productivity, high decomposition rates and high uniform precipitation
rates (Fig. 2a). The scarcity of direct pCO2 measurements and lack of
knowledge on regional surface area and gas-transfer velocity explain
the large uncertainty in the CO2 outgassing from freshwaters8,16,26,51,
with a range of 0.6–1.25 Pg C yr–1. The values at the higher end of the
spectrum also include the contribution of streams and small lakes,
which are typically not considered in flux estimates26. We estimate a
most likely value of the CO2 outgassing flux of 1.1 Pg C yr–1 (F7) with
a medium-to-low confidence.
The burial rate in freshwater sediments has been estimated to
be between ~0.2 and 1.6 Pg C yr–1. The lower estimate refers to
lakes, ponds and reservoirs only 16,26 (0.2–0.6 Pg C yr–1), whereas
the upper one also includes sedimentation in floodplains6,56,57 (0.5–
1.6 Pg C yr–1). The factor of eight between the lower and higher
bound estimates of this burial flux highlights the limited observational data available to constrain this term at the global scale.
Within this large uncertainty, we adopt with a low confidence a
value of 0.6 Pg C yr–1 for the C burial in inland water sediments (F8).
Part of this burial is carbon transported, by erosion processes, from
soils to lake sediments and floodplains.
From the mass balance of the C input from soils to fresh waters
minus CO2 outgassing and C burial fluxes in inland waters adopted
here, the output represents a lateral C flux transported downstream
into estuarine systems (F9) of 1.0 Pg C yr–1. Thus our estimate is
4
Estuaries. In our analysis, estuaries (total area of 1.1 x 106 km2)
correspond to the boundary between inland aquatic systems
and the coastal ocean, represented mainly by the shelves of the
world’s oceans62. Recent syntheses of observational data indicate
that estuaries emit CO2 to the atmosphere27,63, within the range of
0.25 ± 0.25 Pg C yr–1 (F10). Field measurements suggest that about
10% of the CO2 outgassing from estuaries is sustained by the input
from upstream freshwaters (F9) and 90% by local net heterotrophy 64, with a significant fraction of the required organic C coming
from adjacent marsh ecosystems (F11). Although coastal vegetated
environments (salt marshes, mangroves, seagrasses, macroalgae and coral reefs) may export as much as 0.77–3.18 Pg C yr–1 to
the coastal ocean65, we use here a more conservative estimate of
~0.3 ± 0.1 Pg C yr–1 for the common estuarine vegetation of mangroves and salt marshes, which is based on an upscaling of a detailed
regional budget for the southeastern United States63. Furthermore,
to our knowledge, no global estimates exist for C burial in all
estuarine sediments, but a long-term burial in mangroves and salt
marshes of 0.1 ± 0.05 Pg C yr–1 has been proposed18,66 (F12). If we
combine our upstream river and coastal vegetation inputs with our
average estuarine CO2 outgassing estimate to the atmosphere and
the first-order estimate for burial of C in estuarine sediments and
vegetated ecosystems (F12), we obtain a C delivery from estuaries to
the coastal ocean of 0.95 Pg C yr–1 (F13). This estimate amounts to
about one-third of the initial C flux released from soils, rocks and
sewage as input to inland freshwater systems.
Coastal ocean and beyond. Materials leaving estuaries transit into
the coastal ocean and beyond to the open ocean. Recent syntheses of the air–sea CO2 fluxes in coastal waters (total area of 31 x 106
km2)62 suggest that at present between 0.22 and 0.45 Pg C yr–1 are
taken up by the coastal ocean67,68. We choose here a lower estimate
of 0.2 Pg C yr–1 for the coastal ocean sink of CO2, based on a recent
analysis for the global ocean69 (F14). This value relies on the observation that, outside the nearshore environments, the net CO2 fluxes
in the coastal regions are of similar strengths and directions to
those in the adjacent ocean regions, that is, that low-latitude coastal
regions tend to be sources of CO2 to the atmosphere, whereas highlatitude regions tend to be sinks67,68. This allows the extrapolation of
the open-ocean CO2 exchange values towards the coasts. Although
this extrapolation is an oversimplification, the most recent estimate
(0.25 Pg C yr–1) based on the upscaling from a few sites with good
observational coverage suggests a similar value63. Nevertheless, it
is important to recognize that the limited spatial coverage of pCO2
data in the coastal ocean (Fig. 2b) and its heterogeneous nature confine the confidence to low-to-medium. Furthermore, the influence
of terrestrial C input on air–sea CO2 fluxes extends considerably
beyond the limit of the shelf in the discharge plumes of large tropical rivers, such as the Amazon63,70. These plumes should be considered as an integral part of the land–ocean continuum.
Coastal ocean sediments may sequester between 0.2 and
0.5 Pg C yr–1 of organic C and calcium carbonate71,72, although significantly higher values have been reported73 (F15). We choose here
a central estimate of 0.35 Pg C yr–1, of which a sediment C burial of
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a
b
Density of pCO2 data
0.000
0.000–0.003
0.003–0.010
0.010–0.030
0.030–0.100
0.100–0.300
0.300–1.000
Figure 2 | Density of pCO2 data for the continuum of land–ocean aquatic systems. pCO2 values are shown for a, inland waters (Global River Chemistry
database) and b, continental shelf seas (Surface Ocean Carbon Atlas database). The index reports the data density with respect to spatial coverage (using
a 0.5° resolution) and seasonality. Inland waters are represented by 150 meta-watersheds100, and coastal waters by 45 continental shelf segments62.
The surface area of inland waters within each segment is available at www.biogeomod.net/geomap. The index is calculated following the equation
n
I = (∑i=1
ci )/(n×12) where I is the index itself, n is the number of 0.5° grid cells and ci is the count corresponding to the number of months for which at
least one pCO2 value exists within the grid cell i. A value of 0 indicates a complete absence of data and a value of 1 indicates the presence of at least one
pCO2 value every month in each of the grid cells of the considered area. The black lines in a represent the limits of hotspot areas for CO2 evasion to the
atmosphere. All the inland water pCO2 values were calculated from alkalinity, pH and water temperature.
0.05–0.1 Pg C yr–1 is attributed solely to the seagrass meadows of
shallow coastal seas18. In addition, the most probable repository for
much of the recalcitrant terrestrial C related to physical weathering (FR) is likely to be in coastal sediment C pools74,75. Furthermore,
the net pumping of anthropogenic CO2 from the atmosphere into
coastal waters may increase the dissolved inorganic carbon storage in the water column76, by about 0.05 Pg C yr–1. Because of data
paucity, a direct global estimate of lateral C fluxes at the boundary between the coastal and open ocean, delineated by the shelf
break62, is not at present achievable solely through observational
means12,70,77. Thus, based on mass-balance calculations using the
above flux estimates, we propose with a low confidence that the net
inorganic and organic C export from the coastal ocean to the open
ocean is ~0.75 Pg C yr–1 (F16) as shown in Fig. 1a.
Anthropogenic perturbation of lateral carbon fluxes
As with the contemporary lateral C fluxes, we now trace sequentially
the route of the perturbed C fluxes through the global system of
inland waters to estuaries to coastal waters and beyond.
Inland waters. Reconstructions of the historical evolution (preindustrial, around the year 1750, to present) of the global aquatic
C cycle and its fluxes have so far relied primarily on globally averaged box models7,74. Increasing concentrations of atmospheric CO2,
land-use changes, nitrogen and phosphorus fertilizer application,
C, nitrogen and phosphorus sewage discharge and global surface
temperature change drive these highly parameterized models.
Model simulations suggest that the transport of riverine C (F9) has
increased by about 20% since 1750, from ~0.75 Pg C yr–1 in 1750 to
0.9–0.95 Pg C yr–1 at present. The existence of such an enhanced riverine delivery of C is supported by the available literature data3,8,47,78,
and has been attributed to deforestation and more intensive cultivation practices that have increased soil degradation and erosion.
This leads to an increase in the export of organic and inorganic C
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to aquatic systems9. For example, erosion of particulate organic C in
the range 0.4–1.2 Pg C yr–1 has been reported for agricultural land
alone6,14,79. However, only a percentage of this flux represents a lateral transfer of anthropogenic CO2 fixed by photosynthesis6,56,79,80.
Although budgets have been established for present-day conditions16,26, there is no observationally based estimate of the preindustrial C flux from soils to inland waters, nor of the associated
CO2 outgassing and C burial fluxes in freshwater systems in preindustrial times. Furthermore, we are not aware of any spatially
explicit model simulation of the CO2 outgassing and C burial
fluxes in inland aquatic systems during the industrial period at the
global scale. The potential anthropogenic effects on C cycling in
various inland aquatic systems have been reviewed16, but a quantitative estimate of the anthropogenic perturbation remains to be
assessed. The bulk fluxes are nevertheless large enough that even a
small change would alter the global C budget of anthropogenic CO2.
For example, it is highly likely that damming and freshwater withdrawal have impacted the CO2 outgassing fluxes and organic carbon
burial rates since pre-industrial time through their effect on surface area and residence time of inland waters2,6,8. In particular, the
evolution in agricultural practices and the construction of humanmade impoundments during the past century have most likely led
to enhanced CO2 outgassing. A CO2 evasion of 0.3 Pg C yr–1 for
human-made reservoirs alone has been reported16. Furthermore, a
C burial flux in the sediments of reservoirs and small agricultural
ponds of 0.35 Pg C yr–1 has also been estimated2,6,8,16,26,56, with C
probably from terrestrial and autochthonous sources.
To estimate the extent to which other inland water environments
such as lakes, streams and rivers have been perturbed by human
activities, we assume that CO2 outgassing and C burial fluxes in
these systems linearly scale with the estimated increase (~20%) in
soil-derived C exported from rivers to estuaries (F9) and the coastal
zone81 (see also above). This leads to a perturbation of ~0.1 Pg C yr–1
for the CO2 outgassing flux and ~0.05 Pg C yr–1 for the C burial flux.
The linear scaling assumption implies that CO2 outgassing and the
C sedimentation rate are first order processes with respect to the
additional C concentration derived from enhanced exports from
soil in the freshwater aquatic systems. This assumption is probably
reasonable for the air–water flux, but the change in C burial flux is
almost surely more complex 8.
Sewage inputs to upstream rivers (F4) are inferred to add another
0.1 Pg C yr–1 to the anthropogenic perturbation, and we make the
assumption that this labile organic C is entirely outgassed within
inland waters. Combining all contributions, the budget analysis gives CO2 outgassing (F7) and C burial (F8) fluxes under preindustrial conditions of 0.6 and 0.2 Pg C yr–1, respectively (Fig. 1b).
The remaining extra outgassing (0.5 Pg C yr–1) and extra burial
(0.4 Pg C yr–1) fluxes are then attributed to the anthropogenic perturbation (Fig. 1c). Furthermore, increased chemical weathering
of continental surfaces caused by human-induced climate change
and increased CO2 levels contributes to the enhanced riverine
export flux of C derived from rock weathering 82,83 (F2). The anthropogenic perturbation could possibly reach 0.1 Pg C yr–1, mainly
through enhanced dissolution of carbonate rocks83. The impact of
land-use change on weathering rates may have started 3,000 years
ago84 but its effect on atmospheric CO2 is difficult to assess85,86. For
example, C mobilized from the practice of agricultural liming is a
source of enhanced land-use C fluxes85 and could result in a sink of
~0.05 Pg C yr–1.
Summing up, the total present-day flux from soils, bedrock and
sewage to aquatic systems of 2.5 Pg C yr–1 shown in Fig. 1a can be
decomposed as the sum of a natural flux of ~1.5 Pg C yr–1 (Fig. 1b)
and an anthropogenic perturbation flux of ~1.0 Pg C yr–1 (Fig. 1c)
— a value that is similar to a previously published estimate8.
Roughly 50% of this anthropogenic perturbation (0.5 Pg C yr–1) is
respired back to the atmosphere in freshwater systems (F7), while
6
the remainder contributes to enhanced C burial (F8) and export to
estuaries (F9) and, perhaps, to the coastal ocean (F13, Fig.1c).
Estuaries. The perturbation of historical drainage and humancaused conversion of salt marshes and mangroves, as well as the
channelization of estuarine conduits, have modified the estuarine C
balance. For instance, the total loss of C from these intertidal C pools
could be as high as 25–50% over the past century, mainly because of
land-use change18. Assuming that the reduction in the C flux from
marshes and mangrove ecosystems to estuaries (F11) is proportional
to the reduction in the surface area of these ecosystems, we estimate
that the pre-industrial flux of C transported from coastal vegetation
to estuaries must have been about 0.15 Pg C yr–1 larger than that of
the present-day value of 0.30 Pg C yr–1. We predict that C burial in
estuarine sediments has been reduced from pre-industrial times to
the present by the same relative factor, amounting to an anthropogenic reduction of 0.05 Pg C yr–1 of the estuarine sediment C burial
flux (F12) in Fig. 1b. In the absence of independent evidence, we
assume that the air–sea estuarine flux of CO2 has remained constant since pre-industrial times (F10, Fig.1c). With the constraints
mentioned above, closing the mass balance of the pre-industrial and
present-day estuarine C budgets requires that the C export to the
coastal ocean (F13) has increased by ~0.1 Pg C yr–1 since 1750, from
0.85 to 0.95 Pg C yr–1.
Coastal ocean and beyond. Lacking sufficient observational evidence, we have to rely on process-based arguments and models to
separate present-day C fluxes for the coastal ocean into pre-industrial and anthropogenic components. Perhaps the best constrained
flux component is the uptake of anthropogenic CO2 across the air–
sea interface, which has been estimated to about 0.2 Pg C yr–1, on the
basis that this uptake has the same flux density as that of the mean
ocean69, namely about 6 g C m–2 yr–1. This assumption is warranted
as the oceanic uptake flux of anthropogenic CO2 is to first order controlled by the surface area. Much less certain is the degree to which
the enhanced nutrient and C inputs to the coastal ocean could have
modified the air–sea CO2 balance. Box model simulations for the
global coastal ocean suggested that the enhanced supply of nutrients
from land may have increased coastal productivity and C burial in
coastal sediments87, from about 0.2 Pg C yr–1 to 0.35 Pg C yr–1, as
well as contributing to a substantial increase in the air-to-sea CO2
flux 12,74, by up to 0.2–0.4 Pg C yr–1. However, the efficiency by which
the additional nutrient supply delivered to the coastal ocean is actually reducing pCO2 and enhancing the net uptake of CO2 is globally uncertain. For example, on continental shelves, the enhanced
supply of nitrogen (<50 Tg N yr–1)88,89 may stimulate a maximal
additional growth of about 0.3 Pg C yr–1, of which only a portion is
exported to depth, and of which less than 50% is replaced by uptake
of CO2 from the atmosphere90. We estimate that coastal eutrophication has caused an increase in the air-to-sea CO2 flux no larger than
~0.1 Pg C yr–1. The response of the highly heterogeneous, very shallow coastal ocean, including reefs, banks and bays (<50 m, 12 x 106
km2)62, remains largely unknown. However, it is in this region that
the nutrient impact on biological productivity, organic C burial and
area-specific CO2 fluxes is expected to be the highest. Therefore, the
anthropogenic air–coastal water CO2 flux is only known with low
confidence. We estimate a conservative value of 0.2 Pg C yr–1 for this
anthropogenic flux (F14), which is significantly lower than the value
of 0.5 Pg C yr–1 suggested in recent syntheses70.
The fate of the additional C received from the estuaries (F13)
is unclear. Some of this C is probably sequestered in coastal sediments, together with some of the additional organic C produced in
response to the nutrient input, amounting to a flux potentially as
large as 0.1–0.15 Pg C yr–1 (F15). The remainder is exported to the
open ocean, together with some of the anthropogenic CO2 taken
up from the atmosphere, amounting to a flux of approximately
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REVIEW ARTICLE
a
Traditional (2000–2010)
Open ocean
b
Boundless (2000–2010)
Ocean CO2 sink
2.3 ± 0.5
ΔC = 2.3 ± 0.5
Fossil fuel
7.9 ± 0.5
Open ocean
Ocean CO2 sink
2.3 ± 0.5
Fossil fuel
7.9 ± 0.5
ΔC = 2.4 ± 0.5
COUBCC
0.2 ± 0.1*
Freshwaters, estuaries
and coastal seas
FEOBCC
LUC
1.0 ± 0.7
ΔC = 4.1 ± 0.2
LUC
1.0 ± 0.7
‘Intact’ terrestrial ecosystems
RLSGCP
2.5 ± 1
ΔC = 4.1 ± 0.2
0.55
± 0.28*
ΔC = 0.55 ± 0.28*
‘Intact’ terrestial ecosystems
TESBCC
2.85 ± 1.1
0.05
ΔC = 1.5 ± 1.2
ΔC = 0.9 ± 1.4
‘LUC’ affected ecosystems
0.9
Bedrock
ΔC = –0.05
Ecoystems to LOAC export LOAC to open ocean export
1.0 ± 0.5*
0.1 ± > 0.05*
NATURE GEOSCIENCE DOI: 10.1038/NGEO1830
0.1
‘LUC’ affected ecosystems
Figure 3 | Global budget of anthropogenic CO2. Only the perturbation fluxes are shown in this figure (see Fig. 1 for natural fluxes). Units are Pg C yr–1.
a, Global budget from the Global Carbon Project (GCP), in which the sum of fossil-fuel and land-use change (LUC) net annual emissions to the atmosphere is
partitioned between the ocean sink of CO2, the observed atmospheric annual CO2 increase and the atmosphere-to-land CO2 flux in ecosystems not affected
by LUC. The latter is deduced as a difference from all other terms and is called the residual land sink of CO2 (RLSGCP). The land storage change is calculated as
RLSGCP – LUC emissions. Reported uncertainties correspond to 1σ confidence interval of Gaussian error distributions. b, Same budget in presence of ‘boundless’
carbon cycle processes, which includes the land–ocean aquatic continuum (LOAC) fluxes. TESBCC, terrestrial ecosystem CO2 sink; FEOBCC, freshwater and
estuarine aquatic ecosystem outgassing; COUBCC, coastal ocean uptake. The processes represented on the right-hand side of the figure move carbon laterally
from land ecosystems to the oceans, resulting in (1) a net terrestrial ecosystem carbon storage increase smaller than the residual terrestrial sink of CO2, (2)
burial of displaced carbon downstream into freshwater and coastal sediments, (3) outgassing of CO2 to the atmosphere en route between land and the coastal
ocean, and (4) a net open ocean carbon storage increase larger than the atmosphere to ocean CO2 flux. For clarity, reservoirs to atmosphere fluxes of CO2
are in black, lateral fluxes of carbon displaced at the surface are in green, and changes in (anthropogenic) carbon storage of each reservoir are given in red.
In the figure, TESBCC = RLSGCP + FEOBCC – COUBCC. The ‘net atmosphere–terrestrial ecosystems CO2 sink’ is equal to TESBCC – LUC. The ‘net anthropogenic CO2
outgassing’ for the freshwater–estuary–coastal zone continuum is FEOBCC – COUBCC. Uncertainties on fluxes are from the GCP, except for the LOAC fluxes
(identified by an asterisk), where indicative estimates are given based on the categorization proposed in The First State of the Carbon Cycle Report99 and for
TESBCC (see below). The same applies for the uncertainty on the LOAC carbon storage change. The uncertainty on TES is calculated from the atmospheric
mass balance, assuming quadratic errors propagation, and a similar approach is used for the uncertainty on carbon storage (ΔC) for the terrestrial ecosystems
and open ocean, based on their respective mass balance. The uncertainty associated to each LOAC flux was estimated using the categories proposed in The
First State of the Carbon Cycle Report. These categories have then been converted to uncertainty values assuming that they follow a Gaussian error distribution.
1σ ≈ μ/4: 95% certain that the estimate is within 50% of the proposed value. 1σ ≈ μ/2: 95% certain that the estimate is within 100% of the proposed value. 1σ
> μ/2: uncertainty greater than 100%. μ = mean value.
0.1 Pg C yr–1 (F16). This value is again significantly lower than previous estimates70, highlighting that our confidence in these numbers
is very low.
In summary, although accurate quantification remains challenging, one can firmly conclude that during the industrial era, the laterally transported C fluxes and the vertically exchanged atmospheric
CO2 fluxes relevant to the land–ocean aquatic continuum have been
significantly altered by human activities, the main driver being landuse changes. Our analysis suggests that out of the ~1.1 Pg C yr–1 of
extra anthropogenic C delivered to the continuum of land–ocean
aquatic systems (0.8 Pg C yr–1 from soils, 0.1 Pg C yr–1 from weathering, 0.1 Pg C yr–1 from sewage, 0.1 Pg C yr–1 from enhanced C
fixation in inland waters), at present approximately 50% is sequestered in inland water, estuarine and coastal sediments, <20% is
exported to the open ocean and the remaining >30% is emitted to
the atmosphere as CO2. CO2 fluxes along the land–ocean continuum may not only be altered directly by increased anthropogenic
C export from soil and subsequent respiration, but also indirectly
by enhanced decomposition of autochthonous organic materials
triggered by priming. This indirect process may be a quantitatively
relevant contribution to the estimated fluxes and the observed net
heterotrophy of many systems, but cannot yet be quantified45,91. The
uncertainties associated with our breakdown are large and represent
a fundamental obstacle for global C cycle assessments and a fertile
avenue for future research (see also Fig. 3). Future work that succeeds in narrowing down the uncertainties on the anthropogenic
perturbations may overrule our conclusions on the quantitative
value of each flux in the analysis, but is unlikely to affect our conclusion that the anthropogenic perturbation to the aquatic continuum
C fluxes is important for the global carbon budget.
Implications for the global carbon budget
Quantitative assessment of the C fluxes through the land–ocean
aquatic continuum in a so-called boundless C cycle analysis has
important implications for how terrestrial C fluxes ought to be evaluated and how the sinks of anthropogenic CO2 over land and ocean
need to be attributed. This assessment has implications for terrestrial ecosystem C cycling, global terrestrial and ocean C models,
atmospheric inversions, ocean C inventories and the global anthropogenic CO2 budget. The land C cycle (see Supplementary Note for
further details) is driven by the C input to ecosystems due to net
primary productivity of ~59 Pg C yr–1 (FT1, Fig. 1a). A small fraction of net primary productivity is used by ecosystems to increase
C stocks, as evidenced by the net growth of many forests92. Humans
and fires consume another fraction (FT2 and FT3), and litter production (FT5) is thus actually lower now than what it was for the natural
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7
REVIEW ARTICLE
NATURE GEOSCIENCE DOI: 10.1038/NGEO1830
cycle. After some time of residency in ecosystems, most of the C
is returned to the atmosphere as CO2 by heterotrophic respiration
(FT7), while a small fraction is channelled to freshwaters.
In the majority of global terrestrial ecosystem model formulations, the lateral C fluxes from soils to freshwaters are not represented, and modellers assume one-dimensional closure of C between
terrestrial ecosystem pools and the atmosphere. Consequently, soil
heterotrophic respiration is overestimated in these models relative
to observations. Similarly, global ocean biogeochemistry models use
prescribed lateral input of C (or nutrients) from land as an input for
the open ocean. At present, their coarse resolution does not resolve
the coastal ocean well, and their simple, globally tuned formulations
of ecosystem and biogeochemical processes may not be able to capture fully the complexity of the impacts of the enhanced terrestrial
inputs of C and nutrients on the coastal ocean.
Atmospheric CO2 inversion models estimate regional scale net
land–atmosphere CO2 fluxes from CO2 concentration gradients
measured by surface network stations. Thus, the lateral transport
of C at the surface is not a process generally considered in inversion modelling, which only detects vertical CO2 fluxes. Inversion
estimates of land–atmosphere CO2 fluxes do include CO2 exchange
with inland waters and estuaries in their regional output. However,
the spatial resolution of inversion CO2 exchange estimates is too
coarse, and the atmospheric sampling too sparse to separate CO2
fluxes from inland waters from those exchanged by terrestrial ecosystems. The same caveat applies for atmospheric inversions of the
air–sea CO2 fluxes. These inversion approaches evaluate the net flux
across the air–sea interface, which includes the effect of the lateral
and vertical C exchanges along the aquatic continuum, in particular
the net outgassing of the riverine carbon93.
Changes in the open-ocean C inventory over the historical period
have been used to infer the cumulated oceanic C sink. Most recently,
a global oceanic storage of anthropogenic C of 155 ± 30 Pg C for
the period from 1800 to 2010 has been estimated94. This storage
includes ‘only’ that part of the C that has been taken up through the
air–sea interface in response to the increase in atmospheric CO2,
that is, the anthropogenic CO2. Not included in this oceanic net C
sink estimate is any additional air–sea CO2 flux that was driven by
other anthropogenically driven processes, such as coastal nutrient
inputs and consequent enhanced productivity and burial of organic
carbon. If we take our estimate of ~0.1 Pg C yr–1, and assume that it
can be scaled in time with the increase in atmospheric CO2 concentrations, this might have caused an additional oceanic C storage of
10 Pg C over the industrial era that needs to be added to the global
increase in oceanic storage.
In the global CO2 budget reported for instance by the IPCC
and by the Global Carbon Project (Fig. 3a) the ‘land residual sink’
is deduced as a difference between fossil-fuel and land-use-change
emissions of C and atmospheric accumulation and open-ocean
uptake21,22,95, the ocean component being estimated from forward
and inverse models21,96. This method implicitly assumes that the
pre-anthropogenic global carbon budget was at steady state and
the fluxes along the land–ocean aquatic continuum, unlike most
other fluxes, have no anthropogenic component. Thus, these ‘classical’ budgets ignore the anthropogenic perturbation of the boundless carbon cycle displayed in Fig. 1c. Our new estimation of these
fluxes allows us to deconvolute the ‘land residual sink’ into (1) a
‘terrestrial ecosystem sink’ of anthropogenic CO2 comprising the
contribution of the land vegetation, litter, soils and the bedrock,
and (2) sources and sinks of anthropogenic CO2 occurring in the
aquatic ecosystems of the freshwater–estuarine–coastal ocean continuum (Fig. 3b). We find that the ‘terrestrial ecosystem sink’ in the
boundless carbon cycle is removing ~2.85 Pg C yr–1 of anthropogenic CO2 from the atmosphere (Fig. 3b). This sink of CO2 is larger
than the residual land sink estimates reported by the IPCC or the
Global Carbon Project 21 (Fig. 3a) because a fraction of this flux is
8
returned to the atmosphere by CO2 outgassing along the ecosystems
of the land–ocean aquatic continuum. However, only 0.9 Pg C yr–1 of
this terrestrial ecosystem sink is actually sequestered in biomass and
soil of land ecosystems, as 1.0 Pg C yr–1 is released to the atmosphere
owing to land-use changes, and a similar amount (1.0 Pg C yr–1) is
exported to the land–ocean aquatic continuum. The net biomass
and soil sequestration estimate calculated here is consistent with the
‘bottom-up’ estimates reported in Fig. 1c from biomass and soil-carbon inventories92 (0.8 Pg C yr–1), thus providing additional support
to our independent estimation of the anthropogenic C delivered to
the water continuum (see Supplementary Note). Enhanced rock
weathering contributes also to the anthropogenic perturbation
(Fig. 3b, 0.1 Pg C yr–1). The anthropogenic C delivered to freshwaters is partly outgassed to the atmosphere as CO2 (0.55 Pg C yr–1),
partly sequestered in sediments (0.35 Pg C yr–1) and partly exported
to the coastal ocean (0.1 Pg C yr–1). The coastal ocean also contributes to the anthropogenic CO2 budget (0.2 Pg C yr–1 air–sea uptake,
0.2 Pg C yr–1 sequestered in coastal sediments and water column).
As a result, the land–ocean aquatic continuum is both a net source
of anthropogenic CO2 to the atmosphere of 0.35 Pg C yr–1 and a net
anthropogenic C storage in sediments of 0.55 Pg C yr–1 (Fig. 3b).
Of importance is the finding that the terrestrial ecosystem CO2
sink (2.85 Pg C yr–1) is more than three times larger than the terrestrial anthropogenic C stock increase (0.9 Pg C yr–1) because of landuse changes, as already accounted in global carbon budgets, but also
because of the lateral export of anthropogenic C from soils to inland
waters. This distinction is important because processes that control
the interannual variability and long-term evolution of the terrestrial
stocks of C are different from those controlling the aquatic stocks and
fluxes97. This also shows that more than half of the net ‘sequestration
service’ (terrestrial ecosystem sink minus land-use change) from terrestrial ecosystems (mainly forest) is negated by leakage of carbon
from soils to freshwater aquatic systems, and to the atmosphere.
Therefore, from a CO2 budget point of view, the net land anthropogenic CO2 uptake from terrestrial, freshwater and estuarine aquatic
ecosystems is only about 1.3 Pg C yr–1, while the ocean uptake of
anthropogenic CO2 (coastal and open ocean) is about 2.5 Pg C yr–1. It
is also important to stress that because of lateral transport of anthropogenic C by the boundless C cycle, the carbon storage changes15,98
in the different reservoirs of the land–ocean aquatic continuum are
considerably different from the net CO2 fluxes exchanged with the
atmosphere. Furthermore, the significant uncertainty on the aquatic
continuum flux results in a larger uncertainty in the terrestrial ecosystem (and open ocean) carbon storage than what is reported in the
traditional Global Carbon Project budget.
Critical quantifications
Although we have demonstrated that it is possible to establish closed
C and anthropogenic CO2 budgets, broadly consistent with the current growth rate of atmospheric CO2, the component fluxes for the
land–ocean aquatic continuum cannot be adequately quantified
through a robust statistical treatment of available datasets yet. The
data are also too sparse to resolve fully the diversity of soil types,
inland waters, estuaries and coastal systems. In particular, wetland
and riparian ecosystems lateral fluxes are not known. Nevertheless
and importantly, revised anthropogenic CO2 budgets need to consider and assess quantitatively the anthropogenic perturbation to the
aquatic continuum. Any improved estimates will certainly at least
require a considerably denser carbon and CO2 flux observation system, based on direct measurements of CO2 gas-transfer velocities and
ecosystem surface areas. These measurements should be completed
by an expansion of pCO2 sampling and, in some cases, of flux towers
into wetlands and aquatic systems, to have continuous monitoring.
Areas of regional priority include the Amazon and the Congo riverine
basins and their tropical coastal currents. The Ganges River system,
the Bay of Bengal, the Indonesian Archipelago, the Southeast Asian
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NATURE GEOSCIENCE DOI: 10.1038/NGEO1830
seas and the Arctic rivers are other critical regions having significantly large carbon inputs into the coastal seas. Furthermore, a quantitative mechanistic understanding of the key processes controlling
CO2 outgassing and preservation of C in the land–ocean continuum
is needed. An important unknown involves knowledge of the sources,
transport pathways and lability and rates of degradation of accumulating organic and inorganic C, be it in soils, the aquatic system or the
sea floor. The mechanistic understanding is necessary to parameterize the various processes involving C and their sensitivity to external
perturbations at the larger scales of Earth system models. At present,
this lack of understanding limits our ability to predict the present and
future contribution of the aquatic continuum fluxes to the global C
budget involving anthropogenic CO2.
Received 16 October 2012; accepted 23 April 2013;
published online 9 June 2013
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Acknowledgements
This paper is the outcome of the workshop ‘Exploring knowledge gaps along the global
carbon route: a hitchhiker’s guide for a boundless cycle’ held in Eprave, Belgium, in
November 2011. The authors would like to thank S. Bonneville, L. Chou, P. Cox, H.
Durr, T. Eglinton, K. Fleischer, J. Kaplan, T. Kleinen, D. Dan Li, A. Mouchet, H. Nick,
C. Pallud, C. Prentice, D. Schimel, M. Serrano, J-L. Tison, P. Van Cappellen, C. Volta
and J. Zhou for their input during the workshop. The workshop was officially endorsed
by the Global Carbon Project (GCP) and by the Analysis, Integration and Modeling
of the Earth System (AIMES) of the International Geosphere-Biosphere Programme
(IGBP) and received financial support from the government of the Brussels-Capital
region (Innoviris — Brains Back to Brussels award to P.R.), the Walloon Agency for
Air and Climate (AWAC), the Fonds National de la Recherche Scientifique of Belgium
(FNRS), The Belgian Federal Science Policy Office (BELSPO), the Université Libre de
Bruxelles (Belgium), the Netherlands Organization for Scientific Research (NWO), the
King Abdullah University of Science and Technology (KAUST) Center-in-Development
Award to Utrecht University (The Netherlands), the University of Waterloo (Canada)
and the University of Exeter (UK). The research leading to these results received funding
from the European Union’s Seventh Framework Program (FP7/2007–2013) under grant
agreement number 283080, project GEOCARBON.
Author contributions
P.R. and P.F. initiated the Eprave workshop that led to this paper. P.R. coordinated and
participated at all stages of the conception and writing of the paper. P.F., P.C., F.T.M. and
N.G. were central to the conception of the paper and to the writing of the manuscript. I.A.J.
proposed the overall design of Fig. 3. G.G.L. and R.L. produced Fig. 2, using the GloRiCh
database for inland waters assembled by J. Hartmann and co-workers. S.L. took a leading
role in the quantification of the terrestrial ecosystem budget. All other authors contributed
to specific aspects of the budget analysis and commented on various versions of the
manuscript. F.T.M. was instrumental to the genesis of this paper through his pioneering
work in the field.
Additional information
Supplementary information accompanies this paper on www.nature.com/geoscience.
Reprints and permission information is available online at www.nature.com/reprints.
Correspondence and requests for materials should be addressed to P.R.
Competing financial interests
The authors declare no competing financial interests.
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NATURE GEOSCIENCE DOI: 10.1038/NGEO1830
REVIEW ARTICLE
Pierre Regnier1*, Pierre Friedlingstein2, Philippe Ciais3, Fred T. Mackenzie4, Nicolas Gruber5,
Ivan A. Janssens6, Goulven G. Laruelle1, Ronny Lauerwald1,7, Sebastiaan Luyssaert3,
Andreas J. Andersson8, Sandra Arndt9, Carol Arnosti10, Alberto V. Borges11, Andrew W. Dale12,
Angela Gallego-Sala13, Yves Goddéris14, Nicolas Goossens1, Jens Hartmann7, Christoph Heinze15,16,17,
Tatiana Ilyina18, Fortunat Joos19, Douglas E. LaRowe20, Jens Leifeld21, Filip J. R. Meysman22,23,
Guy Munhoven24, Peter A. Raymond25, Renato Spahni19, Parvadha Suntharalingam26 and
Martin Thullner27
Department of Earth and Environmental Sciences, CP160/02, Université Libre de Bruxelles, 1050 Bruxelles, Belgium, 2College of Engineering, Mathematics
and Physical Sciences, University of Exeter, Exeter EX4 4QF, UK, 3Laboratoire des Sciences du Climat et l’Environnement, 91190 Gif-sur-Yvette, France,
4
Department of Oceanography, School of Ocean and Earth Science and Technology, University of Hawai’i at Mãnoa, Honolulu, Hawaii 96822, USA,
5
Environmental Physics, Institute of Biogeochemistry and Pollutant Dynamics, Department of Environmental Sciences, ETH Zürich, 8092 Zurich,
Switzerland, 6Departement Biologie, Universiteit Antwerpen, 2160 Wilrijk, Belgium, 7Institute for Biogeochemistry and Marine Chemistry, KlimaCampus,
D-20146 Hamburg, Germany, 8Scripps Institution of Oceanography, University of California San Diego, La Jolla, California 92093-0202, USA,
9
School of Geographical Sciences, University of Bristol, University Road, Bristol BS8 1SS, UK, 10Department of Marine Sciences, University of North
Carolina, Chapel Hill, North Carolina 27599, USA, 11University of Liège, Chemical Oceanography Unit, Institut de Physique (B5), B-4000 Liège, Belgium,
12
GEOMAR Helmholtz-Zentrum für Ozeanforschung Kiel, Wischhofstraβe 1-3, 24148 Kiel, Germany, 13Department of Geography, University of Exeter,
Exeter EX4 4RJ, UK, 14Géosciences Environnement Toulouse, Centre National de la Recherche Scientifique, Observatoire Midi-Pyrénées, Université
Toulouse III, 31400 Toulouse, France, 15Geophysical Institute, University of Bergen, N-5007 Bergen, Norway, 16Bjerknes Centre for Climate Research,
N-5007 Bergen, Norway, 17Uni Bjerknes Centre, Uni Research, N-5007 Bergen, Norway, 18Max Planck Institute for Meteorology, 20146 Hamburg,
Germany, 19Climate and Environmental Physics, Physics Institute, and Oeschger Centre for Climate Change Research, University of Bern, Bern CH3012, Switzerland, 20Department of Earth Sciences, University of Southern California, Los Angeles, California 90089, USA, 21Agroscope Research
Station ART, Reckenholzstrasse 191, 8046 Zurich, Switzerland, 22Royal Netherlands Institute of Sea Research, 4401 NT Yerseke, The Netherlands,
23
Department of Analytical and Environmental Chemistry, Vrije Universiteit Brussel, 1050 Brussel, Belgium, 24Laboratoire de Physique Atmosphérique
et Planétaire, Université de Liège, B-4000 Liège, Belgium, 25Yale School of Forestry and Environmental Studies, New Haven, Connecticut 06511, USA,
26
School of Environmental Sciences, University of East Anglia, Norwich, NR4 7TJ, UK, 27Department of Environmental Microbiology, Helmholtz Centre for
Environmental Research, Leipzig 04318, Germany.
*e-mail: [email protected]
1
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11
SUPPLEMENTARY INFORMATION
DOI: 10.1038/NGEO1830
Anthropogenic
perturbation of the carbon fluxes
Anthropogenic perturbation of the land to ocean carbon fluxes
from land to ocean
Supplementary Note: The terrestrial ecosystem C cycle
Supplementary Table 1: Synthesis of C fluxes for th
Summary: Synthesis of land-ocean aquatic continuu
anthropogenic perturbation.
Contemporary global terrestrial NPP (FT1) has been estimated to amount about 59 PgC y-1, although
Format type: pdf
satellite derived estimates are slightly lower1,2. Prior to significant human intervention (defined here as
Size: 0.9MB
the ‘natural’ carbon cycle), the terrestrial net primary production was significantly lower. With an
increasing human population, the demand for food, fiber and shelter was met through deforestation in
Supplementary Note: The terrestrial ecosystem C cy
favour of agricultural land-use and agricultural intensification through fertilisation, irrigation and species
Summary: The terrestrial ecosystem C cycle and its
selection. Where deforestation is expected to have decreased the global NPP, intensified land-use in
Format type: pdf
combination with increasing atmospheric CO2 concentrations is expected to have increased the global
Size: 0.4MB
NPP. Based on an estimate of potential NPP1 (before human appropriation) and on DGVMs response to
the historical atmospheric CO2 increase, we estimate the net-effect of both processes to represent an
increase in NPP of 4 PgC y-1 (FT1). Hence, natural global terrestrial NPP is assessed to be around 55
PgC y-1, but both this value and the contemporary one remain poorly constrained.
In addition, the increasing human population and affluence have increased the human appropriation of
NPP (HANPP) to reach the current value of 4.4 PgC yr-1 and is due to crop harvest3 (1.3 PgC yr-1),
wood harvest4 (0.9 PgC yr-1), biofuels production5 (0.9 PgC yr-1;) and cattle grazing1 (1.3 PgC yr-1). Most
of this HANPP, 4.1 PgC yr-1, is emitted to the atmosphere, a small fraction (0.1 PgC yr-1) is released to
inland waters as sewage (F4), and 0.2 PgC yr-1 are estimated to accumulate as harvest products6. We
also accounted that a large fraction of these carbon fluxes is released to the atmosphere as CO 2 (3.85
PgC yr−1; FT2) and a small fraction (0.25 PgC yr−1) as methane from cattle, rice paddies and landfills7.
The effect of an increasing human population on fire intensity remains also difficult to assess. Average
global fire carbon emissions have been estimated at 2.0 PgC yr−1 for present-day conditions8, of which
carbon emissions from anthropogenic disturbances such as tropical deforestation, degradation, and
peatland fires contribute on average 0.5 PgC yr−1. We also assume that 0.05 PgC yr−1 are emitted as
1
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1
© 2013 Macmillan Publishers
Limited.
All rights reserved.
CH4 from fires, thus leaving a CO2 flux of 1.95 PgC yr−1 (FT3). CH4 emissions from fire, cattle and
landfills are attributed to the terrestrial biomass reservoir (0.15 PgC yr-1, FT4), while emissions from rice
paddies (0.15 PgC yr-1) are attributed to soils, together with another 0.15 PgC yr−1 of CH4 released by
wetlands7 (FT6).
Typically croplands and grasslands consist of annual plants and as such the biomass accumulation is
essentially restricted to forests. Consecutive forest inventories indicate a substantial 4.0 PgC yr-1 sink in
forest with 2.9 PgC yr-1 in biomass, 0.9 PgC yr-1 in litter and soil, and 0.2 PgC yr-1 in harvest products6.
However, this sink is partially offset by emissions from gross deforestation of tropical forests6 (2.8 PgC
yr-1). As a result, the net C increase in forest is 1.2 PgC yr-1, of which 0.2 PgC yr-1 is stored in harvest
products. The partition of this net C increase (1.0 PgC yr-1 without the harvest products) between
biomass, litter and soil is not reported in ref. 6. Previous studies suggested that soil carbon loss
accounts for 13 to 37% of total gross deforestation emissions9. Here we adopt an average value of 25%,
leading to about 0.8 PgC yr-1 accumulating in biomass and 0.2 PgC yr-1 accumulating in litter and soil.
The annual carbon flux from the vegetation to the soil decreased from 53.5 PgC yr-1 prior to human
disturbances to 51.95 PgC yr-1 at present (FT5). Despite the decreasing C-inputs, soil C-sequestration is
thought to have increased by 0.2 PgC yr-1 over forested areas6. However, this increase is offset by
drainage of peatlands10,11, which leads to an estimated carbon loss of 0.35 PgC yr-1. The total presentday soil C reservoir is thus losing about 0.15 PgC yr-1, compared to a natural sink of 0.05 PgC yr-1 due
to peat accumulation12 (ΔC = - 0.2 PgC yr-1). Lateral C export to inland waters is thought to have
increased by 0.8 PgC yr-1 up to its current level of 1.9 PgC yr-1 (F1).
Simultaneously lower input fluxes into the litter and soil pool and higher output fluxes into inland waters
are not fully compensated by the recorded decrease in soil carbon, hence the decomposition of litter
and soil organic matter has also significantly decreased during the Anthropocene. Regionally such a
decrease may be caused by increased harvest levels and increased N-deposition which may inhibit
2
© 2013 Macmillan Publishers Limited. All rights reserved.
decomposition13. In the absence of data-driven global estimates of heterotrophic respiration, this flux
was used to close the terrestrial budget.
References
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3
© 2013 Macmillan Publishers Limited. All rights reserved.
Anthropogenic perturbation of the land to ocean carbon fluxes
Supplementary Table 1: Synthesis of C fluxes for the Land-Ocean Aquatic Continuum (LOAC).
Values are given for present-day conditions, as reported in the literature (black) and in our own budget
analysis (red). The magnitude of the anthropogenic perturbation is also given. The anthropogenic
transient is mainly attributed to land-use changes and soil erosion, liming, fertilizer and pesticide
application, sewage water production, damming of water courses, water withdrawal and human-induced
climatic change. The confidence in the selected values is specified for the present-day fluxes, using the
SOCCR nomenclature1. ***: 95% certainty that the actual estimate is within 50% of the estimate
reported; **: 95% certainty that the actual value is within 100% of the estimate reported; *: uncertainty
greater than 100%. The method used in the published estimates is: r = review of existing numbers; d =
data; m = model; b = budget. A brief justification of our proposed estimate for each of these present-day
fluxes and anthropogenic perturbation is also provided.
1
© 2013 Macmillan Publishers Limited. All rights reserved.
Domain
F1: Total C input from soils
to inland waters
Present day
(PgC yr-1)
Confidence
Perturbation
(PgC yr-1)
1.9
**
0.8
1.9a
2.1a
0.9a
[0.4-1.4]b
1
[0.3,0.55]b
[0.47,0.61]b
1.4b
[0.4-1.2]b
F2: Inorganic C input from
bedrock to inland waters
0.5
***
0.1
0.35
***
0.3
[0.3,0.44]
0.26
0.22
0.29
0.1
0.1
***
0.1
0.1
FR: Physical erosion of
total recalcitrant C
0.3
F7: CO2
m
m
m
d
d
m
Hartmann et al., 200910
Amiotte Suchet et al., 200311
Munhoven et al., 200212
Gaillardet et al., 199913
Garrels & Mackenzie, 197114
Beaulieu et al., 201215
0.3
*
0.1
0.1
0.1
1.1
0.63e
**
0
0.5
0.28f
F8: Total C burial in inland
waters
F9: Total C inputs from
rivers to estuaries
*
m
m
m
m
d
d
(d)
Beaulieu et al., 201215
Hartmann et al., 200910
Amiotte Suchet et al., 200311
Munhoven, 200212
Gaillardet et al., 199913
Gislason et al., 200916
Oh and Raymond, 200617
m
m
Mackenzie et al., 200118
Ver et al., 199919
F10: Emissions from
estuaries to the atmosphere
CH4
This study
CO2
m
m
d
Copard et al., 200720
Mackenzie & Lerman, 200621
Meybeck, 1982 22
This study
This study
F11: CO2 uptake by coastal
vegetation & organic C
export to estuaries
This study
Bastviken et al., 201123
This study
Cole et al., 20074
0.4
Aufdenkampe et al., 201124
Tranvik et al., 20093
Battin et al., 20092
Richey, 20045
This study
d
d
r
r
d
m
r(m)
d
Tranvik et al., 20093
Cole et al., 20074
Aufdenkampe et al., 201124
Battin et al., 20092
Smith et al., 20018
Stallard, 19989
Richey, 20045
Mulholland & Elwood, 198225
0.87
0.9
0.9
0.9
[0.8 1.2]
0.7
m
m
r(dm)
r
r
r(d)
r
m
0.8
m
0.85
0.2k
0.53l
0.4l
0.45m
d
m
d
d
d
Andersson et al., 200526
Mackenzie et al., 201227
Cai, 201128
Battin et al., 20092
Tranvik et al., 20093
Cole et al., 20074
Richey, 20045
Ludwig et al., 199829; 199830
Sarmiento & Sundquist,
199231
Meybeck, 198222, 199132
Beusen et al., 200533
Stallard, 19989
Schlesinger & Melack, 198134
Kempe, 197935
1.0
0.35
[0.16-0.2]j
h
1
[0.6, 1.5]
0.2j
0.2j
***
0.95
This study
d
0.6
d
d
d
d
0.6
[0.19-0.27]i
[0.5,1.5]
0.6
This study
d
**
1.2g
1.25e
1.05e
1.0
This study
0
0.1c
0.1c
0.17d
F5: Photosynthetically fixed
C not respired in inland
waters
Emissions from inland
waters to the atmosphere
F6: CH4
Battin et al., 20092
Tranvik et al., 20093
Cole et al., 20074
Richey, 20045
Richey, 20045
Quinton et al., 20106
Van Oost et al., 20077
Smith et al., 20018
Stallard, 19989
0.1
0.1
0.1
*
b
b
b
b
r
r(d)
m
d
d
0.05
increase
0.05
F4: Organic C input from
sewage to inland waters
Reference
0.1
0.33
0.36
0.31
0.44
0.37
F3: Atmospheric CO2
uptake by bedrock
Method
0
0.006
0.25
0.27
0.25
0.27
0.12
0.36
0.32
0.43
0.60
0.3
[0.17,0.4]
0.77 - 3.18
2
© 2013 Macmillan Publishers Limited. All rights reserved.
0.2
0.2
This study
0
d
**
0
d
d
d
d
d
d
d
d
**
-0.15
This study
Borges & Abril, 201236
This study
Borges & Abril, 201236
Cai, 201128
Laruelle et al., 201037
Cole et al., 20074
Chen & Borges, 200938
Borges et al., 200539
Borges, 200540
Abril & Borges, 200441
This study
d
d
Cai, 201128
Duarte et al., 200542
F12: Total C burial in
estuarine sediments &
coastal vegetation
**
-0.05
0.03n
0.03-0.12o
F13: Total C inputs from
estuaries to coastal ocean
F14: Atmospheric CO2
uptake by coastal ocean
0.95
**
0.2
**
0.1
**
0.35
0.41p
0.05-0.1s
0.67q
0.17q
0.28
0.06q
0.36
0.49
0.16r
0.2q
0.23q
F16: Total C inputs from
coastal to the open ocean
0.75
*
0.9
Inorganic C accumulation in
coastal waters
m
r
r(d)
m
b
m
m
b
m
d
b
b
Present-day fluxes
F1: Estimated as the sum of literature values reported for aquatic-estuarine fluxes (F9),
outgassing (F7) and burial (F8) minus the contribution from bedrock weathering (F2) and
photosynthetic C fixation (F5). A higher weight was given to the more recent estimates by
Battin et al. (2009)2 and Tranvik et al. (2009)3 which take into account a more complete
estimate of outgassing and burial including the contributions from streams, smaller lakes
and agricultural ponds
Lerman et al., 2004 49
Krumins et al., 201350
Mcleod et al., 201144
Dunne et al., 200751
Sarmiento & Gruber, 200652
Andersson et al., 200526
Muller-Karger et al., 200553
Chen et al., 200354
Mackenzie et al., 199855
Milliman & Droxler, 199656
Wollast, 199157
Wollast & Mackenzie, 198958
F2: Average of literature values from studies referring mainly to fairly pristine watersheds
plus first order estimate of anthropogenic perturbations. Also consistent with values used
in Earth System models for long-term climate studies (e.g. Climber 2)
F3: Average of literature values from studies referring mainly to fairly pristine watersheds
plus first order estimate of anthropogenic perturbation
This study
b
Liu et al., 201045
m
Mackenzie et al., 201227
0.05
0.05
Mackenzie et al., 201227
Liu et al., 201045
Wanninkhof et al., 201246
Cai, 201128
Laruelle et al., 201037
Borges, 200540
Borges et al., 200539
Thomas et al., 200447
Mackenzie et al., 200548
Andersson et al., 200526
This study
0.1
0.45
*
This study
m
b
d
d
d
d
d
d
m
m
0.15
0.15
Breithaupt et al., 201243
Mcleod et al., 201144
This study
0.2
0.2
0.5
[0.2,0.4]
0.35
This study
d
r(d)
0.2
0.3
0.18
0.22
0.21
0.37
0.45
0.4
F15: Total carbon burial in
coastal sediments
reported value minus 0.8 PgC y-1 attributed in this study to weathering and photosynthetic C
fixation; b POC flux only. For the anthropogenic perturbation, values refer to agricultural soils
and assume that erosion by water reach the aquatic continuum. It is also assumed that the C
eroded is recently fixed atmospheric CO2; c fossil organic carbon only; d particulate inorganic
carbon only; e reported value minus 0.15 PgC y-1 reported by Cole et al. (2007)4 for estuaries; f
outgassing from reservoirs only; g reported value excluding wetlands; h storage in reservoirs
and small agricultural ponds; i storage in lakes and reservoirs; j storage in reservoirs only; k
particulate organic carbon only; l total organic carbon only; m dissolved inorganic carbon only; n
mangroves only; o saltmarshes & mangroves only; p average of literature values; q POC only; r
PIC only; s sea grass meadows only.
a
0.1
This study
F4: Taken from Ver et al. (1999)19 and Mackenzie et al. (2001)18
F5: Assuming that 20% of the C burial and export in inland waters is autochthonous
FR: Sum of literature estimates on particulate inorganic carbon and fossil particulate
organic carbon stemming from rocks
F6: CH4 flux taken from Bastviken et al. (2011)23
3
© 2013 Macmillan Publishers Limited. All rights reserved.
Perturbation
F7: Average of literature values excluding the study by Cole et al. (2007)4, which did not
include streams and smaller lakes and reservoirs, and excluding emissions from wetlands
reported in Aufdenkampe et al. (2011)24
F1: Estimated from a mass-balance on all other perturbed C fluxes through inland water
systems. Broadly consistent with the anthropogenic POC erosion fluxes reported in the
literature. Up to now, no estimates on perturbations of DOC and CO2 fluxes to freshwater
systems are available
F8: The recent value by Tranvik et al. (2009)3 was selected, which was updated from
Cole et al. (2007)4 based on suggestion by Downing et al. (2008)59. The very high values
by Stallard (1998)9 and Smith et al. (2001)8 where discarded. This value could still be an
upper-bound value considering the extreme environments investigated by Downing et al.
(2008)59 and used for upscaling. The fact that the natural C burial in all ecosystems
combined (F8, F12 and F15) is somewhat larger than the geological fluxes could also
corroborate this view.
F2: Taken from the literature. This estimate combines possible effects of increased CO2
and land use
F3: Taken from the literature. This estimate combines possible effects of increased CO2
and land use. Considering the high uncertainty of the effect of CO2 increase on weathering
rate, a lower-bound value was selected
F9: Calculated as mass balance on all preceding flux estimates. Our value is consistent
with those reported in the literature
F4: Taken from Ver et al. (1999)19 and Mackenzie et al. (2001)18
F10: Estimated from the three most recent publications
F5: Assuming that 20% of the perturbation on C burial and export in inland waters is
attributed to autochthonous C fixation
(2011)28,
F11: Taken from the average reported in Cai et al.
discarding the high value from
Duarte et al. (2005)42 which also includes the contribution of seagrasses, macroalgae and
coral reefs. Note that the burial in coastal vegetation and estuary have been lumped
together
FR: Assumed 0. This flux has thus no effect on the anthropogenic CO2 budget for the
atmosphere
F7: Accounts for the outgassing of CO2 from reservoirs (from Cole et al. 2007)4 and
increased CO2 flux from other freshwater systems (due to e.g. sewage inputs and
increased soil inputs), based on a linear scaling hypothesis on the increased riverine
export flux (F9)
F12: Taken from McLeod et al. (2011)44
F13: Calculated from mass-balance on all preceding fluxes
F14: A lower estimate was chosen. Also consistent with the recent analysis by Wanninkhof
et al. (2012)46 and Mackenzie et al. (2012)27
F8: Accounts for burial in reservoirs and agricultural ponds (Tranvik et al. 2009)3 plus a
highly uncertain enhanced burial (0.05 Pg C yr-1) attributed to other freshwater bodies
(linear scaling hypothesis)
F15: Average of literature values, excluding the high estimate from Dunne et al. (2007)51
F9: Taken from Andersson et al. (2005)26 and Mackenzie et al. (2012)27
F16: Calculated from mass-balance on all preceding fluxes, plus the change in inorganic C
inventory in the global coastal ocean
F10: Conservative estimate (no values reported in the literature). Changes in outgassing
due to enhanced carbon inputs from terrestrial ecosystem could be partially offset by
decreased carbon inputs from coastal vegetation
4
© 2013 Macmillan Publishers Limited. All rights reserved.
F11: Based on the surface area reduction of salt marshes and mangroves (Mcleod et al.
2011)44
F12: Based on the surface area reduction of salt marshes and mangroves (Mcleod et al.
2011)44
F13: Calculated as a mass-balance on all other estuarine carbon fluxes
F14: Based on the model-derived value by Mackenzie et al. (2012)27 and arguments in
Wanninkhof et al. (2012)46 (conservative estimate). See also main text for further
discussion
F15: Based on the model-derived value by Lerman et al. (2004)49
F16: Calculated as mass-balance on all other coastal ocean carbon fluxes, including
increased inorganic C inventory in coastal waters (Mackenzie et al. 2012)27
5
© 2013 Macmillan Publishers Limited. All rights reserved.
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