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The anthropogenic CO2 budget considering the lateral transport from land to ocean
A substantial amount of atmospheric carbon taken up on land through photosynthesis and
chemical weathering is transported laterally along the aquatic continuum from upland terrestrial
ecosystems into the ocean. So far, global carbon budget estimates implicitly assumed that this
lateral transport and the myriad of transformation processes along this pathway of the
“boundless carbon cycle” have remained unchanged since pre-industrial times. We show here
that the anthropogenic perturbations to the boundless carbon cycle may have increased the flux
of carbon to inland waters by as much as 1 Pg C yr-1 since preindustrial times, with the majority
coming from enhanced soil leaching. Most of this input to upstream rivers is either lost back to
the atmosphere by CO2 outgassing (~0.4 PgC yr-1) or sequestered in sediments (~0.5 PgC yr-1)
along the freshwater-estuarine-coastal waters continuum, leaving only a perturbation carbon
input of ~0.1 PgC yr-1 to the open ocean. This anthropogenic perturbation to the boundless
carbon cycle needs to be taken into consideration when assessing the fate of the anthropogenic
CO2 emitted into the atmosphere.
1. Introduction
During the past two centuries, human activities have greatly modified the exchange of carbon and
nutrients between the land, atmosphere, freshwaters, coastal zone and the open ocean (e.g.18).Together, 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 have
modified the delivery of these elements through the aquatic continuum from land to ocean, with major
impacts on global biogeochemical cycles (e.g. 9-13).
Although the importance of the aquatic continuum from land to ocean in terms of its impact for lateral
carbon fluxes has been known for more than two decades (e.g.14), the magnitude of its anthropogenic
perturbation has only recently become apparent (e.g. 8,11,15-17). Through the aquatic continuum, carbon
is transferred laterally across ecosystems and regional boundaries, from one filter to the next, i.e., from
soil water, to rivers and streams, to lakes and reservoirs, to estuaries and coastal zones and finally to
the open ocean. Along this continuum, carbon is transformed and sequestered and exchanged vertically
with the atmosphere, often as greenhouse gases or precursors thereof.
The lateral transport of carbon from land to sea has long been regarded as a natural, “background” loop
of the global carbon cycle, and the anthropogenic perturbation of this flux is currently neglected in
assessments of the budget of anthropogenic CO2 (e.g., 18-22). Quantifying lateral carbon fluxes between
land and ocean and their implications for CO2 exchange with the atmosphere, is not only important to
further our understanding of the mechanisms driving the natural carbon cycle along the aquatic
continuum (e.g. 23,24), but also for closing the carbon budget of the ongoing anthropogenic perturbation.
Data related to the boundless carbon cycle are too sparse to provide a global coverage, with insufficient
inland water sampling, uncertain hydraulics, unknown surface area extent, lack of direct pCO2 and other
carbon relevant measurements (see e.g. 25,26). Idealized global box models (e.g 7) have been employed
to explore the magnitude of these fluxes and their anthropogenic perturbations, but the processes
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remained highly parameterized. The current generation of three-dimensional Earth System Models
(ESM), used for quantifying the coupling between the carbon cycle and the physical climate system,
ignores lateral flows of carbon (and nutrients) altogether.
Major challenges in the study of carbon 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, e.g., by incorporating these
processes in ESMs. 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 strategies (Ciais et al., 2011).
The term ‘boundless carbon cycle’ was introduced by Battin et al. (2009)16 to designate the present-day
lateral and vertical carbon fluxes to and from inland waters only. Here, we extend this concept to all
components of the global carbon cycle that are connected to inland waters (Box 1) and discuss possible
changes relative to the natural carbon cycle. In this paper, we deal with total C-fluxes (inorganic and
organic), but occasionally highlight the chemical composition. We first review the magnitude of the
present-day bulk C fluxes pertaining to the boundless carbon cycle, and then attempt to provide new
separate estimates of the natural and anthropogenic perturbation terms. This distinction is important
because in some instances, bulk fluxes have been compared to perturbation fluxes such as the net land
carbon sink of anthropogenic CO2 (e.g. 16,27), which may cause confusion.
2. Lateral carbon fluxes: contemporary estimates
Soil, rock carbon and sewage input to freshwaters. The present-day bulk carbon flux (natural plus
anthropogenic) attributed to these sources was recently estimated from upscaling of local C budgets as
~ 2.7-2.9 PgC yr-1 (16,25), and it is composed of four fluxes.
The first flux is the soil-derived C (28) leaching to inland waters, mainly in organic form (particulate and
dissolved) but also as free dissolved CO2 from soil respiration (F1 in Fig.1a). It is evaluated at 2.2 PgC
yr-1, by subtracting the second and third contribution from a total flux estimate of 2.8 PgC yr -1. This soilderived C flux is part of the terrestrial ecosystem carbon cycle (Box 1) and represents about 5% of the
soil heterotrophic respiration (FT6 and FT7 in Fig.1a). Current soil respiration estimates neglect the C
leached to inland waters. A downward revision of the estimate of soil heterotrophic respiration to
account for the term F1 channeled to inland freshwater systems would nevertheless remain within the
uncertainty of this flux (29).
The second flux is the chemical weathering of continental surfaces (carbonate and silicate rocks). It is
part of the inorganic (often called ‘geological’) carbon cycle (Box 1) and causes an additional ~0.5 PgC
yr-1 input to upstream rivers (F2; range 0.35-0.6 PgC yr-1) (30-34). About two-thirds of the carbon flux F2 is
due to removal of atmospheric CO2 in weathering reactions (F3) and the remaining fraction originates
from dissolution of carbon contained in rocks. Note that the pathway for F3 is largely indirect with most
of the CO2 removed from the atmosphere being soil CO2, having passed through photosynthetic
fixation. Weathering releases carbon to the aquatic continuum in the form of dissolved inorganic carbon,
mainly bicarbonate, given the average pH of freshwater aquatic systems in the range 6-8 (e.g.35).
Following the reasoning of Kempe36, in contrast to soil-derived organic carbon, the assumption is made
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that the carbon derived from weathering of rocks will not degas to the atmosphere during its transfer
through inland waters.
The third flux is the carbon dissolved in sewage water originating from biomass consumption by humans
and domestic animals, which releases an additional flux F4 ~ 0.1 PgC yr-1 (37,38) as an input to inland
waters.
The fourth flux is the physical erosion of particulate inorganic carbon (F5 ~ 0.2 PgC yr-1, 39) and of
organic carbon that is resistant to mineralization (F5 ~ 0.1 PgC yr-1,40). Although the fate of this
physically eroded C is difficult to trace, it is likely to be refractory at the centennial timescale (e.g.41,42)
and most likely channeled through inland waters and estuaries to the open ocean without significant
exchange with the atmosphere. It is thus treated separately in Fig. 1a.
Inland waters
During the transport of carbon 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 in Fig.1a). CH4 is also emitted
from lakes and some rivers (F6 ≈ 0.1 PgC yr-1,27), but this flux represents a small fraction of the laterally
transported C flux. Although these methane fluxes are explicitly included in our global budget analysis
(Fig.1), due to space constraints, they are not discussed in detail in this study.
Outgassing of CO2 to the atmosphere. Data-driven estimates of the water-to-atmosphere CO2 efflux
have been obtained for individual components of the inland freshwater continuum (e.g. 15,16,43). 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, as shown by one recent regional study (44), the addition of carbon from fringing and
riparian wetlands, counted as soil carbon input to freshwaters in Fig 1a, may also contribute significantly
to the freshwater outgassing. Close to 12,000 sampling locations of the inorganic carbon cycle are now
reported in inland water databases (Fig.2a) and calculation of CO2 from these data indicates that 96 %
are oversaturated while 82 % have a concentration at least twice that of the atmosphere (Glorich –
unpublished data base;45).
Although robust measurements of the freshwater CO2 efflux are available for some regions of the globe
such as the Rhine catchment, Scandinavia or the conterminous United States (e.g. 36,44-47), the lack of
direct CO2 measurements, the incomplete spatial coverage of pCO2 samplings coupled with the
difficulty in determining inland surface area and scaling the gas transfer velocity in inland freshwaters
causes large challenges to attain robust global-scale estimates (Fig.2a). In particular, many rivers and
lakes that contribute a significant fraction to the aquatic carbon flux remain poorly surveyed for pCO2 (34,
Glorich). These include the rivers of South-East Asia, the Amazon and the Ganges and, to a lesser
extent, large tropical African watersheds in the Tropics, which receive disproportionally high organic
carbon loads due to their unique 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 explains the large uncertainty in the CO2
outgassing from freshwaters, with a range from 0.7 to 1.4 PgC yr-1 (8,15,25,44 and references therein). The
values at the higher end of the spectrum include also the contribution of streams and small lakes, which
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are typically not considered (25). We estimate a most likely value of the outgassing flux of 1.1 PgC yr-1
(F7) with a medium-to-low confidence.
Burial of carbon in freshwater sediments is a process which sequesters carbon in freshwater
sediments, at a rate in the range between ~ 0.2 and 1.6 PgC yr-1. The lower estimate refers to lakes,
ponds, and reservoirs only (0.2 to 0.6 PgC yr-1;15,25), while the upper one includes also sedimentation in
floodplains (0.5 to 1.6 PgC yr-1; 6,48,49). The factor of eight difference between the lower and higher
bound estimates of this burial flux clearly highlights the limited observational data available to constrain
this term at the global-scale. Within this very large uncertainty, we adopt the value proposed by Tranvik
et al. (2009) (updated from Cole et al., 2007) for the carbon burial in inland water sediments (0.6 PgC yr1, F8), associated with a low confidence.
From the mass balance of the C input, outgassing and burial fluxes in inland waters adopted here, the
output of the freshwater ‘filter’ is a lateral carbon flux going into the downstream estuarine filter (F9 in Fig
1a) of 1.0 PgC yr-1. Thus our estimate is close both to the 0.87 PgC yr-1 proposed by Cai (2011)50 based
upon a compilation of field data (39,51), and to the results of the GlobalNEWS model of carbon and water
flows (52). The conventional wisdom is that the magnitude of the flux of particulate and dissolved organic
carbon is each of about 0.2 PgC yr-1, and the flux of dissolved inorganic carbon is about 0.4 PgC yr-1
(e.g. 39,51,53,54). However Richey (2004)8 suggested that this lateral carbon flux entering the estuarine
filter could be underestimated by as much as 0.4 PgC yr-1. Inspection of uncertainties for inland water
fluxes (weathering, outgassing, burial and export) indicates also that the soil-derived C flux (F1, 2.2
PgC.yr-1) is certainly not known any better than within ± 1 PgC.yr-1.
Estuaries
Recent syntheses indicate that estuaries (defined as in55) emit CO2 to the atmosphere, within the range
of 0.25 ± 0.25 PgC yr-1 (F10,26,50). 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 (56), with a significant fraction of the required organic carbon coming from adjacent marsh
ecosystems (F11). Although Duarte et al. (2005)57 suggested that coastal vegetation may leach to
estuaries as much as 0.77–3.18 Pg C yr−1, we use here a more conservative estimate of ~ 0.3 ± 0.1
PgC yr-1 for this carbon leaching from coastal vegetation such as marsh and mangrove environments,
after Cai (2011)50 who extrapolated data from a detailed regional budget for the Southeastern U.S.
To our knowledge, no global estimates exist for carbon burial in all estuarine sediments, but the longterm burial in mangroves and salt marshes could amount to roughly 0.1 ± 0.05 PgC yr-1 (F12, 17,58).
Combining upstream rivers and coastal vegetation inputs with the average estuarine outgassing of CO2
to the atmosphere and the first-order estimate for burial in estuarine sediments and vegetated
ecosystems (F12) as shown in Fig. 1 suggests a carbon delivery from the estuarine filter to the coastal
ocean of 0.95 PgC yr-1 (F13). This amounts to about one third of the initial carbon flux released from
soils, rocks and sewage as input to inland freshwater systems.
The coastal ocean and beyond
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Recent syntheses of the air-sea CO2 fluxes in coastal waters (here defined as in 55 with a total area of
31x106 km2) suggest that the coastal ocean currently takes up between 0.22 (59) and 0.45 Pg C yr-1 (60).
We choose here a lower estimate of 0.2 PgC yr-1 for the coastal ocean sink of CO2, based on a recent
analysis by Wanninkhof et al. (2012)61 (F14 in Fig.1a ). This value is based on the assumption that the
zonal CO2 flux pattern in the coastal ocean is similar to that of the open ocean, i.e., that one can
extrapolate the open ocean data toward the coasts. It is, however, important to recognize that the
limited spatial coverage of pCO2 data in the coastal zone (Fig. 2b) and the heterogeneous nature of the
coastal seas confine the confidence to low-to-medium.
Significant differences are observed between different coastal regions (e.g.59). In general, temperate
and high latitudes coastal seas act as CO2 sinks while low latitude coastal seas are net CO2 sources to
the atmosphere, due to net ocean heat uptake promoting degassing, high riverine input of terrestrial
carbon, and carbonate deposition in coral reefs and other carbonate environments. Note that the
influence of terrestrial carbon input on air-sea CO2 fluxes extends much beyond the limit of the shelf in
the discharge plume of large tropical rivers such as the Amazon (e.g.50,62).
The coastal ocean sediments may sequester between 0.2 and 0.5 PgC yr-1 of organic carbon and
calcium carbonate (F15; e.g. 63,64 and references therein), although Dunne et al. (2007)65 have reported
significantly higher values. We choose here a central estimate of 0.35 PgC yr-1 of which sediment
carbon burial solely for seagrass meadows of shallow coastal seas could contribute 0.05-0.1 PgC yr-1
(17). In addition, the most probable repository for much of the recalcitrant terrestrial carbon related to
physical weathering (F5, 0.3 PgC yr-1), is likely to be in coastal sediments carbon pools (66,67).
Furthermore, the net pumping of anthropogenic CO2 from the atmosphere into coastal waters may
increase the dissolved inorganic carbon storage by about 0.05 PgC yr-1 (Fig. 1a) (68).
Because of data paucity, a direct global estimate of lateral carbon fluxes at the boundary between the
coastal and open ocean, delineated by the shelf break (e.g. 55), is currently not achievable solely
through observational means (e.g. 11,62,69). Thus, based on mass-balance calculations using the above
flux estimates, we propose with a low confidence that the net inorganic and organic carbon export from
the coastal ocean to the open ocean is ~0.75 PgC yr-1 (F16) as shown in Fig 1a.
3. The anthropogenic perturbation of the boundless carbon cycle fluxes
Changes in riverine C and nutrient exports. Reconstructions of the historical evolution (pre-industrial
to present) of the global aquatic fluxes have so far relied primarily on globally averaged box models
(7,66). These highly parameterized models are driven by increasing fossil fuel emissions and
atmospheric CO2, land-use changes, N and P fertilizer application, C, N and P sewage discharge and
global surface temperature. Simulations with these models suggest that the riverine carbon export (F9)
has increased by about 20% since 1750, from about 0.75 PgC yr-1 in 1750 to 0.9-0.95 PgC yr-1 today.
The existence of such an enhanced riverine delivery is supported by the available literature data
(3,8,39,70), and has been attributed to deforestation, and more intensive cultivation practices that
enhanced soil degradation and erosion. These processes increase the leaching of organic and inorganic
carbon to the aquatic system (71). For instance, erosion of particulate organic carbon from agricultural
land alone could possibly be as high as 0.4-1.2 PgC yr-1 (6,13,72 and references therein). However, only a
percentage of this flux may represent a lateral transfer of anthropogenic CO2 (Stallard, 1998; Smith et
al., 2001; Van Oost et al., Billings et al., 2010).
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The inland freshwater filter. Although budgets have been established for present day conditions
(e.g.15,25), there is no observation-based estimate of the pre-industrial flux from soils to inland waters,
nor of the associated CO2 outgassing and carbon burial fluxes in fresh water systems in pre-industrial
times. In addition, we are not aware of any spatially explicit model simulation of the CO2 outgassing and
carbon burial fluxes in inland aquatic systems during the industrial period at the global scale. Cole et al.
(2007)15 reviewed the potential anthropogenic effects on carbon cycling in various inland aquatic
systems, and overall, these authors concluded that a quantitative estimate of the anthropogenic
perturbation remained to be assessed. The bulk fluxes (Fig 1a) are nevertheless large enough that even
a small change would alter the global carbon budget of anthropogenic CO2.
For example, it is highly likely that damming and freshwater utilization impacted CO2 outgassing and
organic carbon burial rates since pre-industrial through their effect on surface area and residence time
of inland waters (e.g.2,6,8). In particular, the evolution in agricultural practices and the construction of
man-made impoundments during the last century have most likely led to enhanced outgassing and
carbon burial that can be directly attributed to anthropogenic activities. Cole et al. (2007)15 report an
outgassing flux of 0.3 PgC yr-1 for man-made reservoirs alone. Furthermore, Tranvik et al. (2009)25
estimate a C burial in reservoirs and small agricultural ponds of 0.35 PgC yr-1(see also 2,6,8,15,48,73).
To estimate the extent to which other inland water components such as lakes, streams, and rivers have
been perturbed by human activities since the end of the pre-industrial period, we assume that CO2
outgassing and burial fluxes in these systems linearly scale with the estimated increase (~ 20 %) in soilderived carbon exported from rivers to estuaries (F9) and the coastal zone (see above and 74; Fig 1).
This leads to a perturbation of ~ 0.1 PgC.yr-1 for the outgassing flux and ~ 0.05 PgC.yr-1 for the burial
flux. The linear scaling assumption implies that CO2 outgassing and sedimentation are first order
processes with respect to the aquatic C concentration derived from enhanced soil leaching. This
assumption is likely reasonable for the air-water flux, while the change in burial flux is almost surely
more complex (8).
Sewage inputs to upstream rivers (F4) are inferred to add another 0.1 PgC yr-1 to the anthropogenic
perturbation and we make the assumption that this very labile organic carbon is entirely outgassed
within inland waters. Combining all contributions, the budget analysis gives outgassing (F7) and C burial
(F8) fluxes under pre-industrial conditions of 0.6 and 0.2 PgC yr-1, respectively (Fig1b). The remainder
extra outgassing (0.5 PgC yr-1) and extra burial (0.4 PgC yr-1) fluxes are then attributed to the
anthropogenic perturbation (Fig. 1c).
Increased chemical weathering of continental surfaces by human caused climate change and elevated
CO2 contributes to the enhanced riverine export flux of C derived from rock weathering (F2, 75,76). The
anthropogenic perturbation could possibly reach 0.1 PgC yr-1, mainly through enhanced dissolution of
carbonate rocks (76). The impact of land-use change on weathering rates may have started 3.000 years
ago (Bayon et al., 2012) but its effect on atmospheric CO2 is difficult to assess77,78. Carbon leached by
agricultural liming is, for instance, a source of enhanced land-use fluxes (77) and an anthropogenic
disturbance of 1 g CO2 sequestered m-2 yr-1 on agricultural and urban landscapes would result in a sink
of ~0.05Pg.
Summing up, the total present-day flux from soils, bedrock and sewage to aquatic systems of 2.8 PgC
yr-1 shown in Fig. 1a (F1+F2+F4) can be decomposed as the sum of a natural flux of ~1.7 PgC yr-1 (Fig.
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1b) and an anthropogenic perturbation flux of ~ 1.1 PgC yr-1 (Fig. 1c), a value which is similar to that
suggested by Richey (2004)8. Roughly 40 % of this anthropogenic perturbation (0.5 PgC yr-1) is respired
back to the atmosphere in freshwater systems (F7), while the remainder contributes to enhanced C
burial (F8) and enhanced export to estuaries (F9) and, perhaps, to the coastal ocean (F13, Fig.1c).
The estuarine filter. Historical drainage and human caused conversion of salt marshes and mangroves
as well as the channelization of estuarine conduits have modified the estuarine C balance. For instance,
McLeod et al. (2011)17 estimated that the total percent loss of carbon from these intertidal carbon pools
could be as high as 25-50 % over the last century, mainly because of land-use change. Assuming that
the reduction in the carbon flux from marshes and mangrove ecosystems to the estuaries C (F 11) is
proportional to the reduction in the surface area of these ecosystems, we estimate that the pre-industrial
flux of carbon leached by coastal vegetation to estuaries must have been about 0.15 PgC yr-1 larger
compared to the present-day value of 0.30 PgC yr-1. We hypothesize that carbon burial in estuaries
sediments has been reduced from pre-industrial times to the present by the same relative factor,
amounting to an anthropogenic reduction of 0.05 PgC yr-1 of the estuarine sediment 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). Taken together, and imposing the constraint
of closing the mass balance of the pre-industrial and present-day estuarine C budgets requires that the
carbon export to the coastal ocean (F13) may have increased by ~0.1 PgC yr-1 since 1750, from 0.85 to
0.95 PgC yr-1.
The coastal ocean filter. Lacking observational evidence, we have to rely on process-based
arguments and models to separate today’s fluxes into pre-industrial and anthropogenic components.
Perhaps the most constrained flux is the uptake of anthropogenic CO2 across the air-sea interface,
which amounts to about 0.2 Pg C yr-1 (F14, Fig. 1a-b), estimated on the basis that this uptake has the
same flux density as that of the mean ocean, namely about 0.5 mol m-2 yr-1 (e.g. 79). Much less certain is
the degree to which the enhanced nutrient and carbon input to the coastal ocean could have modified
the air-sea CO2 balance.
Box models simulations for the global coastal ocean suggested that the enhanced supply of nutrients
from land may not only have increased coastal productivity and the C burial in coastal sediments (F 15)
(from about 0.2 PgC yr-1 to 0.35 PgC yr-1,80), but might also have caused a substantial increase in the
air-to-sea CO2 flux (F14) by of up to 0.2-0.4 PgC yr-1 (11,66). The efficiency by which the additional
nutrients brought into the coastal areas are actually reducing pCO2, and enhancing the net uptake of
CO2 is however uncertain and extremely variable. For instance, on continental shelves the enhanced
supply of nitrogen (< 50 Tg N yr-1) (81,82) may stimulate a maximal additional growth of about 0.3 Pg C yr1 of which only a portion is exported to depth, and of which only a portion of less than 50% is replaced
by uptake of CO2 from the atmosphere (83). We estimate that coastal eutrophication has caused an
increase in the air-to-sea CO2 flux no larger than ~0.1 PgC yr-1. The response of the highly
heterogeneous, very shallow coastal ocean including reefs, banks and bays (<50 m, 12x106 km2)
remains largely unknown. However, it is in this region that the nutrient impact on biological productivity,
organic carbon burial and area-specific CO2 fluxes is expected to be the highest. Therefore, the
anthropogenic air-coastal water CO2 flux is only known with very low confidence. We estimate a
conservative value of 0.2 PgC.yr-1 for this anthropogenic flux (F14, Fig.1c), which is significantly lower
than the value of 0.5 PgC. yr-1 suggested in recent syntheses (see e.g.,62).
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The fate of the additional carbon received from the estuaries (F13) (Fig 1c) is unclear. Some of this
carbon is likely sequestered in coastal sediments, together with some of the additional organic carbon
produced in response to the nutrient input, amounting to a flux of perhaps 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 about 0.1 Pg C yr-1 (F16). This value is again significantly
lower than the one suggested by Liu et al. (2010)62, highlighting that our confidence in these numbers is
very low.
Summary. Although accurate quantification remains challenging, one can firmly conclude that during
the Industrial Era, the laterally transported carbon fluxes and the vertically exchanged atmospheric CO 2
fluxes relevant to the boundless carbon cycle have been significantly modified. The main anthropogenic
drivers are land-use changes including soil alteration and erosion, the modification of salt marshes and
mangroves, fertilizer application, sewage inputs, damming of water courses, water withdrawal and
human-induced climatic change. Our analysis suggests that out of the ~1.1 PgC yr-1 of extra
anthropogenic carbon delivered to the continuum of land-ocean aquatic systems (0.9 PgC yr-1 from
soils, 0.1 PgC yr-1 from weathering; 0.1 PgC yr-1 from sewage), approximately 50% currently is
sequestered in inland water, estuarine and coastal sediments, less than 20% is exported to the open
ocean and the remaining >30% is re-emitted to the atmosphere as CO2. The uncertainties associated
with this breakdown are large and represent a fundamental obstacle for global carbon cycle
assessments (see also Fig. 3)
4. Implications for the global carbon budget
The proper consideration of the boundless carbon cycle and its anthropogenic perturbation has key
implications for how terrestrial carbon fluxes ought to be assessed and how the sinks of anthropogenic
CO2 over land and ocean need to be attributed.
Implications for terrestrial ecosystems carbon cycling. The land carbon cycle is driven by the
carbon input to ecosystems by Net Primary Productivity (NPP) of ~ 59 PgC yr-1 (FT1, Fig.1a). A small
fraction of NPP is utilized by ecosystems to increase carbon stocks as evidenced, e.g., by the net
growth of many forests (84), while most of it is returned to the atmosphere as CO2 by heterotrophic
respiration (FT7) and fires (FT3), after some time of residency in ecosystems (see supplementary
information for further details). Analysis of NPP in the boundless carbon cycle requires consideration of
the fraction of NPP that is channeled to freshwaters (3.7 %), resulting into lower soil heterotrophic
respiration rates (by 4.5 %) (Fig 1a).
Implications for ecosystem carbon models. In the majority of global ecosystem model formulations,
the lateral C fluxes from soils to freshwaters are not represented, and modelers assume 1-D closure of
carbon between terrestrial ecosystem pools and the atmosphere. Consequently, soil heterotrophic
respiration and vegetation carbon storage change (Net Biome Productivity, NBP) is overestimated in
these models.
Implications for atmospheric inversions. Atmospheric CO2 inversion models estimate regional scale
net land-atmosphere CO2 fluxes from CO2 concentration gradients measured by surface network
stations. The lateral transport of carbon (F1, F2 and F4 in Fig 1a) at the surface necessitated in a
boundless carbon cycle thus is not seen by inversion modeling, which only detects vertical CO2 fluxes.
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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. Perhaps satellite CO2 observations with better spatial
coverage and high resolution will help in the future to identify outgassing of CO2 from large rivers (e.g.,
the Amazon or Russian rivers). 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 boundless carbon cycle, in particular the net outgassing of the riverine carbon (85).
Implications for ocean carbon inventory. Changes in the open ocean carbon inventory over the
historical period have been used to infer the cumulated oceanic carbon sink. Most recently, Khatiwala et
al. (2012)86 estimated a global oceanic storage of anthropogenic carbon of 155 ± 30 PgC for the period
from 1800 to 2010. This storage includes “just” that part that has been taken up through the air-sea
interface in response to the increase in atmospheric CO2, aka the anthropogenic CO2. Not included in
this oceanic net carbon sink estimate is any additional air-sea CO2 flux that was driven by other
anthropogenically-driven processes, such as coastal nutrient input and consequent enhanced
productivity and burial of organic carbon. If we take our estimate of ~0.1 PgC yr-1 (F14), and assume that
it can be scaled in time with the rise in atmospheric CO2 concentrations, this might have caused an
additional oceanic storage of 10 PgC over the Industrial Era that needs to be added to the global
increase in oceanic storage.
Implications for the global anthropogenic CO2 budget. In the global CO2 budget reported for
instance by the IPCC and by the Global Carbon Project (Fig.3a) (20,21,87) the ‘land residual sink’
(RLSGCP) is deduced as a difference between fossil fuel and land use change emissions and
atmospheric accumulation and open ocean uptake, the latter being estimated from forward and inverse
models (e.g. 20,88). This method implicitly assumes that the land-atmosphere and ocean-atmosphere
CO2 fluxes associated with the boundless carbon cycle are globally balanced and have remained
constant since pre-industrial times. 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’ (TES) of
anthropogenic CO2 comprising the contribution of the living land vegetation, the soils and the bedrock
and (2) sources/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 ~2.9 PgC 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 GCP (Fig. 3a 20and updates) because a fraction of this flux is
returned to the atmosphere by outgassing along the aquatic ecosystems of the continuum. However,
only 0.9 PgC yr-1 of this sink (TES) is actually sequestered on net in biomass and soil of land
ecosystems, since 1 Pg C yr-1 is lost again to the atmosphere by land use change and a similar amount
(1 PgC yr-1) is exported to the water continuum. The net biomass and soil sequestration flux estimates
calculated here are consistent with the ‘bottom-up’ estimates reported in Fig.1c from biomass and soil
carbon inventories (Pan et al., 2011) (0.8 PgC. yr-1), thus providing additional support to our
independent estimation of the anthropogenic carbon delivered to the water continuum (see
supplementary information). Note that enhanced weathering of rocks contributes also to the
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anthropogenic perturbation (Fig.3b, 0.1 PgC yr-1). The anthropogenic carbon delivered to freshwaters is
partly outgassed to the atmosphere as CO2 (FEO = 0.65 PgC yr-1), partly sequestered in sediments
(0.35 PgC yr-1) and partly exported to the coastal ocean (0.1 PgC yr-1). The coastal ocean contributes
also to the anthropogenic CO2 budget (COU = 0.2 PgC yr-1 sink), resulting into both a total net source of
anthropogenic CO2 of 0.45 PgC yr-1 (FEO – COU) and a net anthropogenic carbon storage increase for
the entire freshwater/estuarine/coastal ocean continuum of 0.55 PgC.yr-1 (Fig. 3b).
The terrestrial ecosystem CO2 sink (TES = 2.9 PgC yr-1) is thus more than three times larger than the
terrestrial anthropogenic carbon stock increase (0.9 PgC yr-1) because of land use change and because
of the lateral export of anthropogenic carbon from soils to inland waters. This distinction is important
because processes that control the interannual variability and long term evolution of the terrestrial
stocks are different from those controlling land use change and the aquatic stocks and fluxes (e.g., for
respiration,89). This also shows that more than half of the net ‘sequestration service’ (TES – LUC) from
terrestrial ecosystems (mainly forest) is negated by leakage of carbon from soils to freshwater aquatic
systems, and to the atmosphere. Therefore from the point of view of the budget of CO2, the net land
anthropogenic CO2 uptake from terrestrial and freshwater/estuarine aquatic ecosystems is only about
1.3 PgC yr-1 (TES – LUC – FEO) , while the ocean uptake of anthropogenic CO2 (coastal and open
ocean) is about 2.5 PgC yr-1. It is also important to stress that because of lateral transport of
anthropogenic C by the boundless carbon cycle, the carbon storage changes14,90 in the different
reservoirs is different from the anthropogenic CO2 fluxes.
Although we showed here that it is possible to establish closed carbon and anthropogenic CO2 budgets
which are broadly consistent with the current growth rate of atmospheric CO2, the component fluxes of
the boundless C cycle currently cannot be adequately quantified through a robust statistical treatment of
available datasets. The data are also too sparse to resolve fully the diversity of soil types, inland water,
estuaries and coastal systems. Nevertheless, revised anthropogenic CO2 budgets need to include the
anthropogenic perturbation to the boundless carbon cycle and future assessments require:


A considerably denser carbon and CO2 flux observation system, based on direct measurements
of CO2, gas transfer velocities and surface areas. Regional priority areas are the Amazon and
the Congo riverine basins and their tropical coastal currents. The Ganges River system and the
Bay of Bengal, the Indonesian Archipelago and the South East Asian Seas and the Arctic
Rivers are other critical regions due to their large carbon inputs into the coastal seas. Extreme
climatic events (heatwaves, high precipitation events, etc.) should also be more fully monitored
and assessed in terms of their physical characteristics because they propagate their effects on
the C-cycle to distant rivers, lakes, estuaries, coastal seas and even the open ocean.
A quantitative mechanistic understanding of key processes controlling the outgassing and
preservation of C in the soil/inland water/estuary/coastal zone continuum. Our knowledge of the
sources, transport pathways and degradation states of accumulating organic and inorganic C,
be it in soils, the aquatic system or the seafloor, is incomplete. This limits our ability to predict
the present and future contribution of the aquatic fluxes to the global budget of anthropogenic
CO2.
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BOX 1: Definitions
The Boundless carbon cycle: 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 preindustrial land-ocean loops: Part of the boundless carbon cycle was already active under
pre-industrial conditions and 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 thus formed 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 the partial pressure of dissolved CO2 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, i.e., they were globally balanced.
Anthropogenic perturbation of the boundless C cycle: Human perturbations to the boundless
carbon cycle have moved this 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 (last 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 pre-industrial conditions as the natural contribution.
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SUPPLEMENTARY INFORMATION
Contemporary global terrestrial NPP has been estimated to amount about 59 PgCy-1 (Haberl et al.,
2007), although satellite derived estimate are slightly lower (Zhao and Running, 2010). Prior to
significant human intervention (defined here as 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 favour of agricultural land-use and agricultural intensification
through fertilisation, irrigation and species selection. Where deforestation is expected to have decreased
the global NPP, intensified land-use in combination with increasing atmospheric CO2 concentrations is
expected to have increased the global NPP. Based on the Haberl et al. estimate of potential NPP
(before human appropriation) and on DGVMs response to the historical atmospheric CO 2 increase, we
estimate the net-effect of both processes to represent an increase in NPP of 4 PgC y-1. Hence, natural
global terrestrial NPP is estimated to be around 55 PgC y-1, but both this value and the contemporary
one remain poorly constrained.
The increasing human population and affluence has increased the human appropriation of NPP
(HANPP) to reach the current value of 4.4 PgC y-1 and is due to crop harvest (1.3 PgC y-1, Ciais et al.,
2007), wood harvest (0.9 PgC yr-1, Hurtt et al., 2006), biofuels production (0.9 PgC yr-1, Yevich and
Logan, 2003) and cattle grazing (1.3 PgC yr-1, Haberl et al., 2007). 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, and
0.2 PgC yr-1 are estimated to accumulate as harvest products (Pan et al. 2011). The effect of an
increasing human population on fire intensity remains also difficult to assess. According to van der Werf
et al. (2010), average global fire carbon emissions are 2.0 PgC yr−1 for present-day conditions, 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 accounted that although the largest fraction of these carbon fluxes is released as CO 2, a small
fraction is released as methane (CH4). We assume that 0.25 PgC yr−1 of HANPP emitted to the
atmosphere is released at CH4 from cattle, rice paddies and landfills (Denman et al., 2007). Likewise we
assume that 0.05 PgC yr−1 is emitted as CH4 from fires and 0.15 PgC yr−1 of CH4 are being released by
wetlands (Denman et al., 2007)
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 products
(Pan et al., 2011). However, this sink is partially offset by emissions from gross deforestation of tropical
forests (2.8 PgC yr-1,Pan et al., 2011). 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 repartition of this net C increase (1.0 PgC yr-1 without the
harvest products) between biomass, litter and soil is not reported in Pan et al. Previous studies
suggested that soil carbon loss accounts for 13 to 37% of total gross deforestation emissions
(Houghton, 2010). 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.
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The annual carbon flux from the vegetation to the soil decreased from 53.5 PgC y-1 prior to human
disturbances to 51.95 Pg C y-1 at present. Despite the decreasing C-inputs, soil C-sequestration is
thought to have increased by 0.2 PgC yr-1 over forested areas (Pan et al., 2011). However, this increase
is offset by drainage of peatlands, which leads to an estimated carbon loss of 0.35 PgC yr -1, (Hoijer et
al., 2009; Joosten, 2009). The total present-day soil C is thus losing about 0.15 PgC yr-1, compared to a
natural sink of 0.05 PgC yr-1 due to peat accumulation (Yu et al., 2011). Lateral C export through run-off
and leaching is thought to have increased by 0.9 PgC yr-1 up to its current level of 2.2 PgC yr-1.
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 decrease during the Anthropocene. Regionally such a
decrease may be caused by increased harvest levels and increased N-deposition which may inhibit
decomposition (Janssens et al). In the absence of data-driven global estimates of heterotrophic
respiration, this flux was used to close the terrestrial budget.
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References
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
Likens, G. E., Mackenzie, F. T., Richey, J. E., Sedwell, J. R. & Turekian, K. K. Flux of Organic
Carbon from the Major Rivers of the World to the Oceans. U.S. D.O.E. Report CONF-8009140
TIS U.S. Department of Commerce, Springfield, Virginia, (1981).
Mulholland, P. J. & Elwood, J. W. The role of lake and reservoir sediments as sinks in the
perturbed global carbon cycle. Tellus 34, 490-499, doi:10.1111/j.2153-3490.1982.tb01837.x
(1982).
Wollast, R. & Mackenzie, F. T. Global biogeochemical cycles and climate. NATO ASI series
Series C, Mathematical and physical sciences, 453-473 (1989).
Degens, E. T., Kempe, S., Richey, J. E., Environment, I. C. o. S. U. S. C. o. P. o. t. & Programme,
U. N. E. Biogeochemistry of major world rivers. (Published on behalf of the Scientific
Committee on Problems of the Environment (SCOPE) of the International Council of Scientific
Unions (ICSU), and the United Nations Environment Programme (UNEP) by Wiley, 1991).
Smith, S. V. & Hollibaugh, J. T. Coastal metabolism and the oceanic organic carbon balance.
Rev. Geophys. 31, 75-89, doi:10.1029/92RG02584 (1993).
Stallard, R. F. Terrestrial sedimentation and the carbon cycle: coupling weathering and
erosion to carbon burial. Global Biogeochemical Cycles 12, 231-257 (1998).
Ver, L. M. B., Mackenzie, F. T. & Lerman, A. Biogeochemical responses of the carbon cycle to
natural and human perturbations: Past, present, and future. American Journal of Science 299,
762-801 (1999).
Richey, J. E. Pathways of atmospheric CO2 through fluvial systems. In C. B. Field and M. R.
Raupach (eds.), The Global Carbon Cycle, Integrating Humans, Climate, and the Natural
World. Island Press, Washington, Covelo, London, 329-340 (2004).
Aumont, O. et al. Riverine-driven interhemispheric transport of carbon. Global
Biogeochemical Cycles 15, 393-405 (2001).
AGU. Global Nutrient Exports from Watersheds. American Geophysic Union, Washington,
D.C. (2005).
Mackenzie, F. T., Andersson, A. J., Lerman, A. & Ver, L. M. Boundary exchanges in the global
coastal margin: Implications for the organic and inorganic carbon cycles. In: Robinson, A.R.
Brink, K.H. (Eds.) The Sea, Vol.13, Harvard University Press, Cambridge, 193-225 (2005).
Cotrim da Cunha, L., Buitenhuis, E. T., Le Quéré, C., Giraud, X. & Ludwig, W. Potential impact
of changes in river nutrient supply on global ocean biogeochemistry. Global Biogeochemical
Cycles 21 (2007).
Quinton, J. N., Govers, G., Van Oost, K. & Bardgett, R. D. The impact of agricultural soil
erosion on biogeochemical cycling. Nature Geoscience 3, 311-314 (2010).
Sarmiento, J. L. & Sundquist, E. T. Revised budget for the oceanic uptake of anthropogenic
carbon dioxide. Nature 356, 589-593 (1992).
Cole, J. J. et al. Plumbing the global carbon cycle: Integrating inland waters into the terrestrial
carbon budget. Ecosystems 10, 171-184 (2007).
Battin, T. J. et al. The boundless carbon cycle. Nature Geoscience 2, 598-600 (2009).
McLeod, E. et al. A blueprint for blue carbon: Toward an improved understanding of the role
of vegetated coastal habitats in sequestering CO 2. Frontiers in Ecology and the Environment
9, 552-560 (2011).
Sarmiento, J. L. & Gruber, N. Sinks for Anthropogenic Carbon. Physics Today 55, 30-36 (2002).
Denman, K. L. et al. in Climate Change 2007: The Physical Science Basis. Contribution of
Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate
Change (eds S. Solomon et al.) (Cambridge University Press, 2007).
15
REGNIER ET AL.
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
2/10/16
Le Quéré, C. et al. Trends in the sources and sinks of carbon dioxide. Nature Geoscience 2,
831-836 (2009).
Peters, G. P. et al. Rapid growth in CO 2 emissions after the 2008-2009 global financial crisis.
Nature Climate Change 2, 2-4 (2012).
GCP. Global Carbon Project. Carbon budget and trends 2010,
[www.globalcarbonproject.org/carbonbudget]. (2011).
Ludwig, W. & Probst, J. L. River sediment discharge to the oceans: Present-day controls and
global budgets. American Journal of Science 298, 265-295 (1998).
Archer, D. Fate of fossil fuel CO2 in geologic time. Journal of Geophysical Research C: Oceans
110, 1-6 (2005).
Tranvik, L. J. et al. Lakes and reservoirs as regulators of carbon cycling and climate. Limnology
and Oceanography 54, 2298-2314 (2009).
Laruelle, G. G., Dürr, H. H., Slomp, C. P. & Borges, A. V. Evaluation of sinks and sources of CO2
in the global coastal ocean using a spatially-explicit typology of estuaries and continental
shelves. Geophysical Research Letters 37 (2010).
Bastviken, D., Tranvik, L. J., Downing, J. A., Crill, P. M. & Enrich-Prast, A. Freshwater methane
emissions offset the continental carbon sink. Science 331, 50 (2011).
Ittekkot, V., Humborg, C., Rahm, L. & Nguyen, T. A. Carbon silicon interactions. In: Melillo JM,
Field CB, Moldan B, Eds. Scope 61. Interactions of the major biogeochemical cycles: Global
change and human impacts, vol 357. Washington DC: Island Press. pp 311–22 (chap.17)
(2004).
Luyssaert, S. et al. CO 2 balance of boreal, temperate, and tropical forests derived from a
global database. Global Change Biology 13, 2509-2537 (2007).
Garrels, R. M. & MacKenzie, F. T. Evolution of Sedimentary Rocks. (Norton, 1971).
Holland, H. D. The chemistry of the atmosphere and oceans. (Wiley, 1978).
Gaillardet, J., Dupré, B., Louvat, P. & Allègre, C. J. Global silicate weathering and CO 2
consumption rates deduced from the chemistry of large rivers. Chemical Geology 159, 3-30
(1999).
Munhoven, G. Glacial - Interglacial changes of continental weathering: Estimates of the
related CO2 and HCO3 - flux variations and their uncertainties. Global and Planetary Change
33, 155-176 (2002).
Hartmann, J., Jansen, N., Dürr, H. H., Kempe, S. & Köhler, P. Global CO 2-consumption by
chemical weathering: What is the contribution of highly active weathering regions? Global
and Planetary Change 69, 185-194 (2009).
Mackenzie, F. T. & Lerman, A. Carbon in the Geobiosphere—Earthʻs Outer Shell. (Springer,
2006).
Kempe, S. in Transport of carbon and minerals in major world rivers part 1 (ed E. T. Degens)
91-332 (Geologisch-Paläontologisches Institut Universität Hamburg, 1982).
Prairie, Y. T. & Duarte, C. M. Direct and indirect metabolic CO2 release by humanity.
Biogeosciences 4, 215-217 (2007).
Mackenzie, F. T., Lerman, A. & Ver, L. M. Recent past and future of the global carbon cycle.
In: Gerhard, L.C., Harrison, W.E., Hanson, B.M. (Eds.), GeologicalPerspectives of Global
Climate Change. AAPG Studies in Geology No. 47.AmericanAssociation of Petroleum
Geologists, Tulsa, OK, 51-82 (2001).
Meybeck, M. Carbon, nitrogen, and phosphorus transport by world rivers. American Journal
of Science 282, 401-450 (1982).
Copard, Y., Amiotte-Suchet, P. & Di-Giovanni, C. Storage and release of fossil organic carbon
related to weathering of sedimentary rocks. Earth and Planetary Science Letters 258, 345-357
(2007).
Galy, V. et al. Efficient organic carbon burial in the Bengal fan sustained by the Himalayan
erosional system. Nature 450, 407-410 (2007).
16
REGNIER ET AL.
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
63
2/10/16
Arndt, S. et al. Quantifying the degradation of organic matter in marine sediments: a review
and synthesis. Earth Science Reviews (Submitted).
Sobek, S., Tranvik, L. J. & Cole, J. J. Temperature independence of carbon dioxide
supersaturation in global lakes. Global Biogeochemical Cycles 19, 1-10 (2005).
Butman, D. & Raymond, P. A. Significant efflux of carbon dioxide from streams and rivers in
the United States. Nature Geoscience 4, 839-842 (2011).
Sobek, S., Tranvik, L. J., Prairie, Y. T., Kortelainen, P. & Cole, J. J. Patterns and regulation of
dissolved organic carbon: An analysis of 7,500 widely distributed lakes. Limnology and
Oceanography 52, 1208-1219 (2007).
Cole, J. J., Caraco, N. F., Kling, G. W. & Kratz, T. K. Carbon dioxide supersaturation in the
surface waters of lakes. Science 265, 1568-1570 (1994).
Humborg, C. et al. CO2 supersaturation along the aquatic conduit in Swedish watersheds as
constrained by terrestrial respiration, aquatic respiration and weathering. Global Change
Biology 16, 1966-1978 (2010).
Smith, S. V., Renwick, W. H., Buddemeier, R. W. & Crossland, C. J. Budgets of soil erosion and
deposition for sediments and sedimentary organic carbon across the conterminous United
States. Global Biogeochemical Cycles 15, 697-707 (2001).
Aufdenkampe, A. K. et al. Riverine coupling of biogeochemical cycles between land, oceans,
and atmosphere. Frontiers in Ecology and the Environment 9, 53-60 (2011).
Cai, W. J. Estuarine and coastal ocean carbon paradox: CO 2 sinks or sites of terrestrial
carbon incineration? Annual Review of Marine Science 3, 123-145 (2011).
Meybeck, M. C, N, P, and S in rivers: From sources to global inputs. In Interactions of C, N, P
and S: Biogeochemical cycles, edited by R. Wollast, F. T. MacKenzie, and L. Chou. Berlin:
Springer Verlag (1991).
Beusen, A. H. W., Dekkers, A. L. M., Bouwman, A. F., Ludwig, W. & Harrison, J. Estimation of
global river transport of sediments and associated particulate C, N, and P. Global
Biogeochemical Cycles 19 (2005).
Schlesinger, W. H. & Melack, J. M. Transport of organic carbon in the world's rivers. Tellus 33,
172-187 (1981).
Degens, E. T. Riverine carbon: An overview. In Transport of carbon and minerals in major
world rivers, Part 1, edited by E. T. Degens. SCOPE/UNEP Sonderbd. Mitteilungenausdem
Geologisch-Paläontologischen Institut der UniversitätHamburg 52, 1–12 (1982).
Laruelle, G. G. et al. Global multi-scale segmentation of continental and coastal waters from
the watersheds to the continental margins. Hydrol. Earth Syst. Sci. Discuss. 9, 11319-11361,
doi:10.5194/hessd-9-11319-2012 (2012).
Borges, A. V. & Abril, G. Carbon Dioxide and Methane Dynamics in Estuaries. In: Wolanski E.
and McLusky D.S. (eds.) Treatise on Estuarine and Coastal Science 5, 119–161 (2012).
Duarte, C. M., Middelburg, J. J. & Caraco, N. Major role of marine vegetation on the oceanic
carbon cycle. Biogeosciences 2, 1-8 (2005).
Breithaupt, J. L., Smoak, J. M., Smith, T. J., Sanders, C. J. & Hoare, A. Organic carbon burial
rates in mangrove sediments: Strengthening the global budget. Global Biogeochemical Cycles
26 (2012).
Cai, W. J., Dai, M. & Wang, Y. Air-sea exchange of carbon dioxide in ocean margins: A
province-based synthesis. Geophysical Research Letters 33 (2006).
Borges, A. V., Delille, B. & Frankignoulle, M. Budgeting sinks and sources of CO2 in the coastal
ocean: Diversity of ecosystem counts. Geophysical Research Letters 32, 1-4 (2005).
Wanninkhof, R. et al. Global ocean carbon uptake: magnitude, variability and trends.
Biogeosciences Discuss. 9, 10961-11012, doi:10.5194/bgd-9-10961-2012 (2012).
Liu, K. K., Atkinson, L., Quiñones, R. & Talaue-McManus, L. Carbon and Nutrient Fluxes in
Continental Margins: A Global Synthesis. (Springer, 2010).
Muller-Karger, F. E. et al. The importance of continental margins in the global carbon cycle.
Geophys. Res. Lett. 32, L01602, doi:10.1029/2004GL021346 (2005).
17
REGNIER ET AL.
64
65
66
67
68
69
70
71
72
73
74
75
76
77
78
79
80
81
82
83
84
2/10/16
Krumins, V., Gehlen, M., Arndt, S., van Cappellen, P. & Regnier, P. Dissolved inorganic carbon
and alkalinity fluxes from coastal marine sediments: model estimates for different shelf
environments and sensitivity to global change. Biogeosciences Discuss. 9, 8475-8539,
doi:10.5194/bgd-9-8475-2012 (2012).
Dunne, J. P., Sarmiento, J. L. & Gnanadesikan, A. A synthesis of global particle export from
the surface ocean and cycling through the ocean interior and on the seafloor. Global
Biogeochemical Cycles 21 (2007).
Andersson, A. J., MacKenzie, F. T. & Lerman, A. Coastal ocean and carbonate systems in the
high CO2 world of the anthropocene. American Journal of Science 305, 875-918 (2005).
Blair, N. E. & Aller, R. C. The fate of terrestrial organic carbon in the Marine environment.
Annual Review of Marine Science 4, 401-423 (2012).
Mackenzie, F. T., De Carlo, E. H. & Lerman, A. Coupled C, N, P, and O Biogeochemical Cycling
at the Land-Ocean Interface. in: Treatise on Estuarine and Coastal Science, Chapter 5.10,
Elsevier (2012).
Jahnke, R. Global Synthesis. In: Liu K.-K. et al. (eds.), Carbon and Nutrient Fluxes in
Continental Margins, Global Change – The IGBP Series, 3, Springer-Verlag Berlin Heidelberg,
597-615 (2010).
Milliman, J. & Meade, R. World-Wide Delivery of River Sediment to the Oceans. The Journal
of Geology 91, 1 - 21, doi:10.1086/628741 (1983).
Raymond, P. A., Oh, N. H., Turner, R. E. & Broussard, W. Anthropogenically enhanced fluxes
of water and carbon from the Mississippi River. Nature 451, 449-452 (2008).
Van Oost, K. et al. The impact of agricultural soil erosion on the global carbon cycle. Science
318, 626-629 (2007).
Smith, S. V., Renwick, W. H., Bartley, J. D. & Buddemeier, R. W. Distribution and significance
of small, artificial water bodies across the United States landscape. Science of the Total
Environment 299, 21-36 (2002).
Mackenzie, F. T., Ver, L. M. & Lerman, A. Century-scale nitrogen and phosphorus controls of
the carbon cycle. Chemical Geology 190, 13-32 (2002).
Gislason, S. R. et al. Direct evidence of the feedback between climate and weathering. Earth
and Planetary Science Letters 277, 213-222 (2009).
Beaulieu, E., Goddëris, Y., Donnadieu, Y., Labat, D. & Roelandt, C. High sensitivity of the
continental-weathering carbon dioxide sink to future climate change. Nature Climate Change
2, 346-349 (2012).
Oh, N. H. & Raymond, P. A. Contribution of agricultural liming to riverine bicarbonate export
and CO2 sequestration in the Ohio River basin. Global Biogeochemical Cycles 20 (2006).
Hamilton, S. K., Kurzman, A. L., Arango, C., Jin, L. & Robertson, G. P. Evidence for carbon
sequestration by agricultural liming. Global Biogeochemical Cycles 21 (2007).
Gruber, N. et al. Oceanic sources, sinks, and transport of atmospheric CO2. Global
Biogeochemical Cycles 23 (2009).
Lerman, A., Mackenzie, F. T. & Ver, L. M. Coupling of the perturbed C-N-P cycles in industrial
time. Aquatic Geochemistry 10, 3-32 (2004).
Seitzinger, S. P., Harrison, J. A., Dumont, E., Beusen, A. H. W. & Bouwman, A. F. Sources and
delivery of carbon, nitrogen, and phosphorus to the coastal zone: An overview of Global
Nutrient Export from Watersheds (NEWS) models and their application. Global
Biogeochemical Cycles 19 (2005).
Gruber, N. & Galloway, J. N. An Earth-system perspective of the global nitrogen cycle. Nature
451, 293-296 (2008).
Jin, X., Gruber, N., Frenzel, H., Doney, S. C. & McWilliams, J. C. The impact on atmospheric
CO2 of iron fertilization induced changes in the ocean's biological pump. Biogeosciences 5,
385-406 (2008).
Pan, Y. et al. A large and persistent carbon sink in the world's forests. Science 333, 988-993
(2011).
18
REGNIER ET AL.
85
86
87
88
89
90
2/10/16
Jacobson, A. R., Fletcher, S. E. M., Gruber, N., Sarmiento, J. L. & Gloor, M. A joint
atmosphere-ocean inversion for surface fluxes of carbon dioxide: 1. Methods and globalscale fluxes. Global Biogeochemical Cycles 21 (2007).
Khatiwala, S. et al. Global ocean storage of anthropogenic carbon. Biogeosciences Discuss. 9,
8931-8988, doi:10.5194/bgd-9-8931-2012 (2012).
Friedlingstein, P. et al. Update on CO2 emissions. Nature Geosci 3, 811-812 (2010).
Sarmiento, J. L. et al. Trends and regional distributions of land and ocean carbon sinks.
Biogeosciences 7, 2351-2367 (2010).
Yvon-Durocher, G. et al. Reconciling the temperature dependence of respiration across
timescales and ecosystem types. Nature 487, 472-476, doi:doi: 10.1038/nature11205 (2012).
Tans, P. P., Fung, I. Y. & Enting, I. G. Storage Versus Flux Budgets: The Terrestrial Uptake of
CO2 During the 1980s. in Woodwell, G. M. and Mackenzie, F. T. (eds.), Biotic Feedbacks in the
Global Climatic System. Will the Warming Feed the Warming?, Oxford University Press, New
Yor, 351–366 (1995).
19