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Modeling carbon dioxide removal via sinking of particulate organic carbon from macroalgae cultivation

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Frontiers in Marine Science
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Macroalgae cultivation is receiving growing attention as a potential carbon dioxide removal (CDR) strategy. Macroalgae biomass harvesting and/or intentional sinking have been the main focus of research efforts. A significant amount of biomass is naturally lost through erosion and breakage of cultivated or naturally growing seaweed, but the contribution of the resulting particulates to carbon sequestration is relatively unexplored. Here, we use a fully coupled kelp-biogeochemistry model forced by idealized parameters in a closed system to estimate the potential of macroalgal-derived particulate organic carbon (POC) sinking as a CDR pathway. Our model indicates that at a kelp density of 1.1 fronds m⁻³, macroalgal POC sinking can export 7.4 times more carbon to the deep sea (depths > 500m) and remove 5.2 times more carbon from the atmosphere (equivalent to an additional 336.0 gC m⁻² yr⁻¹) compared to the natural biological pump without kelp in our idealized closed system. The results suggest that CDR associated with POC sinking should be explored as a possible benefit of seaweed farming and point to the need for further study on organic carbon partitioning and its bioavailability to quantify the effectiveness and impacts of macroalgal cultivation as a CDR strategy.
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Modeling carbon dioxide
removal via sinking of
particulate organic carbon from
macroalgae cultivation
Si Chen
1,2
, Jago Strong-Wright
1,2
and John R. Taylor
1,2
*
1
Department of Applied Mathematics and Theoretical Physics, University of Cambridge,
Cambridge, United Kingdom,
2
Centre for Climate Repair, Cambridge, United Kingdom
Macroalgae cultivation is receiving growing attention as a potential carbon
dioxide removal (CDR) strategy. Macroalgae biomass harvesting and/or
intentional sinking have been the main focus of research efforts. A signicant
amount of biomass is naturally lost through erosion and breakage of cultivated or
naturally growing seaweed, but the contribution of the resulting particulates to
carbon sequestration is relatively unexplored. Here, we use a fully coupled kelp-
biogeochemistry model forced by idealized parameters in a closed system to
estimate the potential of macroalgal-derived particulate organic carbon (POC)
sinking as a CDR pathway. Our model indicates that at a kelp density of 1.1 fronds
m
3
, macroalgal POC sinking can export 7.4 times more carbon to the deep sea
(depths >500m) and remove 5.2 times more carbon from the atmosphere
(equivalent to an additional 336.0 gC m
2
yr
1
) compared to the natural biological
pump without kelp in our idealized closed system. The results suggest that CDR
associated with POC sinking should be explored as a possible benet of seaweed
farming and point to the need for further study on organic carbon partitioning
and its bioavailability to quantify the effectiveness and impacts of macroalgal
cultivation as a CDR strategy.
KEYWORDS
macroalgae cultivation, carbon dioxide removal, carbon sequestration, particulate
organic carbon, kelp, climate change mitigation, ocean biogeochemical modeling,
ocean-based solution
1 Introduction
Macroalgae (seaweed) cultivation is receiving growing attention as a potential carbon
dioxide removal (CDR) strategy to mitigate climate change (Duarte et al., 2017;Gattuso et al.,
2021;National Academies of Sciences, E. and Medicine, 2022;de Ramon NYeurt et al., 2012).
The motivation behind this strategy stems from the high rate of primary production and
biomass accumulation of seaweed (Duarte and Cebrian, 1996;Schiel and Foster, 2015;Duarte
et al., 2017;Smale et al., 2020), the immense size of the ocean, the buffering capacity of
Frontiers in Marine Science frontiersin.org01
OPEN ACCESS
EDITED BY
Wei-Bo Chen,
National Science and Technology Center for
Disaster Reduction (NCDR), Taiwan
REVIEWED BY
Antoine De Ramon NYeurt,
University of the South Pacic, Fiji
Phillip Williamson,
University of East Anglia, United Kingdom
*CORRESPONDENCE
John R. Taylor
J.R.Taylor@damtp.cam.ac.uk
RECEIVED 21 December 2023
ACCEPTED 22 January 2024
PUBLISHED 12 February 2024
CITATION
Chen S, Strong-Wright J and Taylor JR (2024)
Modeling carbon dioxide removal via
sinking of particulate organic carbon
from macroalgae cultivation.
Front. Mar. Sci. 11:1359614.
doi: 10.3389/fmars.2024.1359614
COPYRIGHT
© 2024 Chen, Strong-Wright and Taylor . This is
an open-access article distributed under the
terms of the Creative Commons Attribution
License (CC BY). The use, distribution or
reproduction in other forums is permitted,
provided the original author(s) and the
copyright owner(s) are credited and that the
original publication in this journal is cited, in
accordance with accepted academic
practice. No use, distribution or reproduction
is permitted which does not comply with
these terms.
TYPE Brief Research Report
PUBLISHED 12 February 2024
DOI 10.3389/fmars.2024.1359614
seawater, and the durability of the ocean as carbon storage (Gruber
et al., 2019;Siegel et al., 2021). However, important questions remain
surrounding the effectiveness and impacts of this strategy (Boyd et al.,
2022;Gallagher et al., 2022;Stafford, 2022).
Two recent studies have examined macroalgae cultivation and
intentional harvesting or intentional sinking of the biomass as a
CDR method (Wu et al., 2022;Arzeno-Soltero et al., 2023). The
concept behind the intentional sinking strategy is that cultivated
macroalgae are harvested and sunk to the deep ocean where the
carbon will be potentially sequestered for a climate-relevant time
scale (GESAMP, 2019;Gattuso et al., 2021;National Academies of
Sciences, E. and Medicine, 2022). The results of Wu et al. (2022)
suggested that macroalgae cultivation and sinking have
considerable CDR potential which can be further boosted by
articial upwelling to alleviate nutrient limitation and that large-
scale deployment of the strategy would have signicant side effects,
including the reduction of phytoplankton net primary production
and the creation of new oxygen minimum zones on the seaoor.
Arzeno-Soltero et al. (2023) simulated the potential of seaweed
farming (including four seaweed types) to produce Gt-scale biomass
carbon under two nitrate scenarios without explicitly accounting for
feedback to nitrate cycling or competition with phytoplankton. The
results indicated that 1 GtC yr
1
biomass carbon could be harvested
by farming seaweed in the most productive 0.8% of exclusive
economic zones worldwide (>1 million km
2
).
Macroalgal habitats are characterized by rapid biomass turnover,
which results in large amounts of carbon entering the marine
environment as detritus (particulate organic carbon or POC)
through incremental blade erosion and dislodgement (Mann, 1973;
Krause-Jensen and Duarte, 2016). It has been estimated that 82% of
the global average productivity of kelp (large brown seaweeds that
make up the order Laminariales) beds or forests (864 gC m
2
yr
1
)
are channeled to the detrital pool (Krumhansl and Scheibling, 2012).
About 32% of the global carbon sequestration by macroalgae (173
TgC yr
1
) has been estimated to occur through POC sedimentation
and deep sea export (Krause-Jensen and Duarte, 2016). Similarly, for
cultivated macroalgae, an estimated 8-49.4% of the annual gross
production of Saccharina latissima was lost to the environment in
Norway (Fieler et al., 2021). Carbon loss from a Saccharina japonica
farm in China was estimated at about 61% of gross production
(Zhang et al., 2012). POC thus has the potential to serve as one of the
essential pathways of carbon sequestration and CDR (National
Academies of Sciences, E. and Medicine, 2022).
POC production and export from cultivated macroalage have
not been fully explored as a CDR pathway. In the model of Wu et al.
(2022), the eroded macroalgal biomass was directly converted back
to nutrients and dissolved inorganic carbon (DIC), and POC export
was not directly included. Arzeno-Soltero et al. (2023) predicted
potential seaweed biomass production for CDR, but didnt report
carbon export. The lack of quantitative data characterizing the POC
sinking from cultivated macroalgae is a major gap yet to be lled in
order to fully assess different CDR pathways and to develop a
feasible implementation strategy.
Along with uncertainties surrounding POC export, two
additional limitations of existing studies motivate us to develop a
new model to study the macroalgae cultivation for ocean-based
CDR. First, the CDR potential and the magnitude of possible
ecological side effects of macroalage cultivation will depend on
the macroalgal cultivation density (Boyd et al., 2022). Existing
studies have not explicitly varied the macroalgal cultivation
density, which limits our understanding of the impacts and
sequestration potential of large-scale CDR deployments. Second,
there has been a debate about the imported organic subsidies in an
open ecosystem and their impact on the global seaweed net carbon
balance (Gallagher et al., 2022;Stafford, 2022), which motivates us
to consider a closed system where we can readily track all forms of
carbon, nutrients, and other materials.
Here, we use OceanBioME (Strong-Wright et al., 2023a), an
environment for modeling the kelp-biogeochemical interactions in
an idealized closed 1D column conguration to study macroalgae
cultivation as a CDR strategy. This fully coupled kelp-
biogeochemical model enables us to predict macroalgae growth
based on ambient open ocean conditions and to quantify the impact
of kelp cultivation on the biogeochemistry and carbon uxes. We
focus on the vertical carbon ux due to sinking POC, referred to as
the gravitational pump (Resplandy et al., 2019) and the air-sea CO
2
ux, as a function of time and kelp cultivation density. The aims of
the study are to evaluate whether POC sinking alone can be an
effective pathway for carbon sequestration, to identify the
relationship between carbon uxes and kelp cultivation density,
and to deepen our understanding of the potential impacts of large-
scale macroalgae cultivation on the marine ecosystem.
Large-scale macroalgae cultivation in coastal waters may be
limited by the relatively small coastal areas available for farming, or
conict with other blue economic activities such as sheries,
tourism, and marine energy (Azevedo et al., 2019;Wu et al.,
2022). Here, we focus on macroalgae cultivation in the open
ocean, building on the previous work of (Strong-Wright and
Taylor, 2022) which modeled the growth potential of sugar kelp
in the North Atlantic. Whereas Strong-Wright and Taylor (2022)
did not consider the impacts of macroalgae cultivation on nutrients
or phytoplankton, our fully coupled model enables us to analyze the
two-way coupling between the seaweed and the ambient
environment. Using an idealized 1D column model in a closed
system, we are able to reproduce natural seasonal cycles and better
understand the sensitivity to key parameters.
2 Methods
2.1 OceanBioME overview
The model used in this study provided by OceanBioME is based
on a modied version of the Lodyc Ocean Biogeochemical
Simulation Tools for Ecosystem and Resources (LOBSTER)
model (Levy et al., 2005), coupled with a carbonate chemistry
model (Resplandy et al., 2009) and a kelp growth model (Broch
and Slagstad, 2012;Broch et al., 2013;Fossberg et al., 2018;Broch
et al., 2019). Details of the model formulation and implementation
are available in the archive Strong-Wright et al. (2023b).Saccharina
latissima (sugar kelp) was chosen because it is well-studied and
widely used in aquaculture and has been proposed as a candidate for
Chen et al. 10.3389/fmars.2024.1359614
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offshore macroalgae farms (Broch et al., 2019;RunningTide, 2021;
Strong-Wright and Taylor, 2022). To simulate kelp growth we use a
model for individual fronds which integrate three coupled
equations for the frond area, the carbon and the nitrogen
contents of the kelp. Specically, the kelp uptakes nitrate,
ammonium, and dissolved inorganic carbon from the
surrounding water and releases dissolved and particulate organic
matter. It is assumed that nitrogen is the limiting nutrient in the
kelp growth model because either its demand/supply ratio is higher
in the ocean compared with other nutrients [e.g. phosphorus
(Atkinson and Smith, 1983;Martiny et al., 2014)], or the
potential constraints of other micronutrients [e.g. iron (Paine
et al., 2023)] can be overcome by designing a cultivation platform
equipped with a nutrient supply. Similarly, in a global model of kelp
growth Arzeno-Soltero et al. (2023) assumed that nitrogen is the
limiting nutrient, while Wu et al. (2022) considered nitrogen and
phosphorous but neglected the limitation by micronutrients. If
additional nutrients limit kelp growth in the open ocean, this
would likely reduce the kelp primary production and CDR
potential, while potentially increasing competition between kelp
and phytoplankton. OceanBioME uses the uid dynamics package
Oceananigans (Ramadhan et al., 2020) to integrate the tracer
conservation equation and track the properties of biological
particles. A schematic of the model is presented in Figure 1 and
the details of the model are provided in the Supplementary Material.
2.2 Model conguration
Here, we run OceanBioME in a 1D column conguration. This
removes the direct inuence of advection and allows us to consider
the carbon uxes in a closed system. Although the 1D model does
not calculate horizontal gradients, we still need to specify a nominal
horizontal domain size to couple the kelp growth model with the
ecosystem and carbonate chemistry models. In all cases, we use a
nominal domain size of 20m×20m×600m (depth), and the vertical
grid spacing is 6m. We repeated the calculations with higher vertical
resolution and obtained very similar results. We integrate one kelp
growth model per vertical meter within the upper 100m of the water
column, mimicking kelp grown from a vertical rope. One way to
interpret this conguration is a very large kelp farm where
properties are homogeneous in the horizontal direction. Although
we always use one individual kelp model per vertical meter, we vary
the kelp density from 0.025 to 250 fronds m
3
scaling the
interactions between the kelp and the ecosystem and carbonate
chemistry models. The range of kelp densities that we selected was
chosen to cover a large range of densities in the literature (Broch
et al., 2013;Forbord et al., 2020;Wu et al., 2022).
The model is forced by an idealized annual cycle of surface PAR
data derived from observations (NASA Goddard Space Flight Center,
Ocean Ecology Laboratory, Ocean Biology Processing Group, 2021)
and temperature, salinity, and mixed layer depth (MLD) data from a
reanalysis product (E.U. Copernicus Marine Service Information,
2023a) averaged over the region between 20° and 25° W and 55° and
60° N in the North Atlantic (see the Supplementary Material).
Piecewise linear functions were used to idealize the forcing
parameters and the annual cycle of the mixed layer depth is made
up of distinct regimes due to the combination of mechanical and
surface density forcings such as winds, tides, solar radiation, heat and
freshwater exchange, etc. (Williams and Follows, 2011). Details of the
idealization of the forcing parameters are shown in the
Supplementary Material. Vertical mixing is parameterized by
prescribing a vertical diffusivity as a quadratic function of depth in
the mixed layer with a maximum diffusivity of 0.08 m
2
s
1
and a
constant diffusivity of 0.0001 m
2
s
1
below the mixed layer (see the
Supplementary Material for details). The characteristic values of
turbulent diffusivity were chosen to better match the results of the
Mercator model (see Section 2.3). The models were run for a period
of 2 years starting from 1 January with a time step of 3.5 minutes.
The initial conditions for the kelp state variables are A
0
= 0.1 dm
2
,
N
0
=0.01gN(gsw)
1
,andC
0
= 0.1 g C (g sw)
1
. The initial area A
0
is
much smaller than the area when the kelp is fully grown and hence
the model results are not very sensitive to the initial carbon, C
0
,and
nitrogen, N
0
,reserves(Strong-Wright and Taylor, 2022).
2.3 Model validation
We compared our model without kelp to a reanalysis product
(E.U. Copernicus Marine Service Information, 2023b, henceforth
referred to as the Mercator model). This allows us to ensure that
our baseline case without kelp (or the counterfactual to a kelp farm)
captures the key features of the biogeochemical state in the North
Atlantic ocean. Our baseline column model reproduces the key
features of the Mercator state estimate. For example, the timing
and the amplitude of phytoplankton blooms (Figure 2A) and the
seasonality of the partial pressure of CO
2
(pCO
2
) in surface seawater
(Figure 2B) agree well between our column model and the Mercator
model. In particular, both models show distinct regimes: a decreasing
pCO
2
in the spring as primary production removed inorganic carbon
from the water, an increasing pCO
2
in late spring and summer due to
reduced solubility of CO
2
associated with seasonal warming, a
decreasing pCO
2
in the autumn due to seasonal cooling, a
relatively constant pCO
2
in the winter and early spring due to the
balance between cooling, exchange of carbon-rich deep waters, and
low primary production. The small difference in the pCO
2
between
the OceanBioME and Mercator models might be due to the
idealization of the annual cycle used here in OceanBioME. The
simulation without kelp is referred to as the baseline case in the
following analysis.
3 Results
3.1 Seasonality of kelp growth and its
interactions with phytoplankton
Sugar kelp can perform luxury uptake, whereby they uptake
nutrients when the concentrations in the surrounding water are
high and use the nutrients later in the year. Sugar kelp growth also
exhibits distinct seasonal patterns due to varying light, temperature,
nutrient conditions, and innate seasonality (Broch and Slagstad,
Chen et al. 10.3389/fmars.2024.1359614
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2012). In our model, the rate of change in the frond area is negative
in summer (due to the relative rate of frond erosion being greater
than the specic growth rate) and remains low with the kelp
increasing carbohydrate reserves through photosynthesis until
mid-autumn. Figure 3A illustrates this by showing a time series
of kelp frond area and nitrogen and carbon reserves at a depth of
3m for a kelp density of 0.25 fronds m
3
. An increase in frond area
resumes from mid-autumn until winter, and during this period
stored carbohydrates are utilized for growth, as can be seen by the
corresponding reduction in carbon reserves.
Kelp interacts with phytoplankton by competing for nutrients.
Adding kelp reduces phytoplankton net primary production-the total
rate of organic carbon production byphytoplankton minus the rate of
respiration (Sigman and Hain, 2012), although this reduction is
highly seasonal and is largely conned to the period from April to
November (Figure 3B). Note, however, that when kelp are included,
the sum of kelp net primary production (KNPP) and phytoplankton
net primary production (PNPP) is signicantly larger than the PNPP
in the case without kelp. The reduction in PNPP with the inclusion of
kelp appears to occur due to nutrient reallocation(Bach et al., 2021)
which is evidenced by the reduction in the seawater nitrate
concentrations when kelp is included (Figure 3C).
The seasonal pattern of nitrate concentration is controlled by
the uptake by phytoplankton and kelp and the entrainment of
nutrient-rich waters during periods of mixed layer deepening.
During late autumn and early winter, the inuence of kelp on
PNPP is minimal. The kelp net primary production (KNPP) also
exhibits distinct seasonal patterns due to varying light that
inuences kelp photosynthesis and temperature that inuences
both photosynthesis and respiration of kelp.
In our model, we do not include the effect of shading from kelp.
This assumption is motivated by the relatively large effective
FIGURE 1
Schematic of OceanBioME. The state variables include phytoplankton (P), zooplankton (Z), nitrate (NO
3
), ammonium (NH
4
), semi-labile dissolved
organic matter (DOM), small particulate organic matter (sPOM), and big particulate organic matter (bPOM), expressed in terms of their nitrogen
content (mmolN m
3
), dissolved inorganic carbon (DIC) in mmolC m
3
, alkalinity (Alk) in meq m
3
, frond area in dm
2
, nitrogen reserves in gram N
per gram structural mass (g N (g sw)
1
), and carbon reserves in g C (g sw)
1
.
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BA
FIGURE 2
Model validation. (A) Time series of vertically integrated phytoplankton (P) concentration for the two models. (B) Time series of partial pressure of
CO
2
in surface seawater for the two models.
B
C
D
E
F
A
FIGURE 3
Time series and density dependence of kelp growth, volume-integrated NPP, and nitrate and DIC concentrations. (A) Time series of individual kelp
properties at 3 m depth (in the case of kelp cultivation density at 0.25 fronds m
3
): frond area, carbon reserves (gC (gsw)
1
), and nitrogen reserves
(gN (gsw)
1
) which are shown as 100-fold of its value for presentation purposes. (B) Comparison between volume-integrated KNPP and PNPP. PNPP
without kelp is given for reference. (C) Nitrate and DIC concentration comparison between cases with and without kelp at 3 m depth. (D) Density
dependence of individual kelp properties at 3 m depth: frond area, carbon reserves, and 100-fold nitrogen reserves. (E) Density dependence of
volume-integrated KNPP and PNPP. The dashed line represents the total time-averaged PNPP without kelp which is 137.1 gC day
1
.(F) Density
dependence of nitrate and DIC concentrations at 3 m depth. The dashed lines represent the time-averaged nitrate (blue) and DIC (red)
concentrations at 3 m depth without kelp respectively.
Chen et al. 10.3389/fmars.2024.1359614
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horizontal spacing (20m) between vertical lines of kelp in our
model. However, we do include the effect of shading from
phytoplankton. The effect of shading from phytoplankton is more
signicant during the spring bloom than at other times of the year,
which leads to a sharp decrease in KNPP in April (Figure 3B).
Figure 3D shows the two-year average of frond area and
nitrogen and carbon reserves for kelp at a depth of 3m as a
function of kelp density. The mean kelp area decreases rapidly
for densities above about 2.5 fronds m
3
. Commensurate with
this decrease in kelp area, the time-averaged nitrate
concentration in the seawater at 3m depth (Figure 3F)
decreases with increasing kelp density. In a model of sugar
kelp growth in the North Atlantic, Strong-Wright and Taylor
(2022) found that kelp did not grow well when the mean nitrate
concentration was below 0.5 mmol m
3
.NotefromFigure 3F
that the mean nitrate concentration only falls to this level for the
highest kelp densities, although this level occurs seasonally even
at relatively low kelp densities (Figure 3C). The KNPP increases
monotonically with kelp density, although the increase is
sublinear. The sublinear increase in KNPP can be explained by
the combination of the decrease in kelp frond area and the
increase in kelp cultivation density (Figure 3D). In contrast, the
PNPP decreases monotonically with kelp density due to nutrient
reallocation (Figure 3E).
3.2 Carbon ux
Both the gravitational pump and air-sea CO
2
ux show a strong
dependence on kelp density and seasonal patterns that reect the
kelp and phytoplankton growth (Figure 4). The gravitational pump,
or the carbon ux due to sinking particulates, is computed by
multiplying the concentration of POC at 500 m depth with the
sinking speed of POC. The gravitational pump (two-year average)
increases with kelp density and peaks at a density of 1.1 fronds m
3
(Figure 4C). Further increasing densities, characterized by smaller
frond areas, reduces the gravitational pump. It is likely that the exact
value of this limit is a result of the model assumptions, but since the
kelp growth is clearly suboptimal at these very high densities (with
low frond area and severe nutrient limitation), we do not focus on
the results at very high densities. Without kelp, the gravitational
pump peaks during late spring, coinciding with the peak of the
spring phytoplankton bloom (Figure 2A). When kelp dominates the
net primary production, the gravitational pump peaks in the late
winter or early spring and decreases during summer and autumn
(Figure 4A), reecting the period when the kelp frond area is
maximum (Figure 3A).
The air-sea CO
2
ux also exhibits a strong dependence on
kelp density and strong interseasonal uctuations when kelp
dominates the net primary production. The air-sea CO
2
ux
(two-year average) increases monotonically with kelp density and
appears to saturate at about -520 gC m
2
yr
1
(Figure 4C).
Remarkably, this is about 8 times larger than the air-sea CO
2
ux without kelp. The seasonality of air-sea CO
2
ux becomes
less signicant with increased kelp densities (Figure 4B). At high
kelp densities, the enhancement in the air-sea CO
2
ux occurs
very soon after the start of the model when the kelp area is still
small (Figure 3A).
It is important to note that we do not supply nutrients into our
system and due to the sinking of POC through the gravitational
pump, the system does not reach an equilibrium. The upper ocean
carbon budget is also unsteady as can be seen by comparing the
gravitational pump and the air-sea CO
2
ux (Figure 4C). For the
smaller kelp densities, the gravitational pump exceeds the air-sea
CO
2
ux while for large kelp densities, the gravitational pump is
smaller than the air-sea CO
2
ux. The reduction in the
gravitational pump associated with the production of POC at
high kelp density is accompanied by increased exudation of DOC.
The observation may be explained by the overow hypothesis,
whereby DOC is exuded to reduce the build-up of photosynthetic
products and maintain cellular homeostasis when low nutrient
levels limit the synthesis of cellular structural components (Fogg,
1983;Paine et al., 2021). This is consistent with the ndings of
Abdullah and Fredriksen (2004) who found in their in situ
incubation that more DOC was exuded from Laminaria
hyperborea during non-growth phase and suggested that the
decrease in growth is a consequence of the depletion of
nutrients. The difference in carbon ux between the air-sea CO
2
ux and the gravitational pump at high kelp cultivation density
contributes to both kelp biomass carbon and exuded DOC.
4 Discussion
Our model results suggest that sinking particulate organic
carbon resulting from natural erosion of kelp fronds (a byproduct
of seaweed aquaculture) could provide a signicant pathway for
removing carbon from the surface ocean and enhancing the air-sea
CO
2
ux. Our ndings further suggest that this pathway and the
impact on phytoplankton net primary production through nutrient
reallocation is highly dependent on the density at which the kelp
is planted.
When kelp density increases, the area of fronds decreases due to
nutrient limitation, leading to a decreased POC production for each
kelp frond. The kelp growth model assumes that erosion increases
with frond area and is negligible when the area is very small (Broch
and Slagstad, 2012), which is based on the observation that longer
fronds erode more easily than shorter ones (Sjøtun, 1993). The net
effect of the decreased POC production per frond and increased
kelp densities results in a maximum gravitational pump at a kelp
density of about 1.1 fronds m
3
. Since reduced POC production at
high densities is indeed due to nutrient limitation, the geometry and
environment external to the kelp farm will inuence this result.
Here, we model a closed system with no net inow of nutrients. In
an open system, ambient water owing into the kelp farm would
replenish the nutrients inside the farm to some extent, and alleviate
severe nutrient stress.
The shift from POC to DOC at high kelp densities has
implications for carbon export and storage. For example, previous
model results indicate that the DOC/POC export ux ratio
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decreases with depth (Hansell et al., 2009). The shift from POC to
DOC might change the relative contributions of both forms of
organic carbon to the biological pump. The increased exudation of
DOC by kelp at high cultivation densities could also enhance the
microbial carbon pump (MCP), the successive transformation of
labile DOC and semi-labile DOC through microbial activities to
recalcitrant DOC which is resistant to rapid bacterial degradation.
Jiao et al. (2010) proposed the MCP as a conceptual framework to
address the role of microbial generation of recalcitrant dissolved
organic matter. Further work is needed to assess the organic carbon
partitioning among biomass carbon, POC, and DOC (and its
bioavailability) in order to assess the role of large-scale
macroalgae cultivation on the global carbon cycle and the
effectiveness of different CDR pathways.
B
C
A
FIGURE 4
Carbon ux. (A) Time series of gravitational pump at varying kelp cultivation densities. (B) Time series of air-sea CO
2
ux. Refer to the legends in (A).
(C) Dependence of gravitational pump and air-sea CO
2
ux on kelp density. Frond areas corresponding to different kelp cultivation densities are
indicated on the color bar. The gravitational pump and air-sea CO
2
ux in the baseline case are -63.2 (blue dashed line) and -65.1 (red dashed line)
gC m
2
yr
1
respectively. At a kelp density of 1.1 fronds m
3
, macroalgae cultivation can export 7.4 times more carbon to the deep sea and remove
5.2 times more carbon from the atmosphere (equivalent to an additional 336.0 gC m
2
yr
1
) compared to the baseline case.
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Frontiers in Marine Science frontiersin.org07
The air-sea CO
2
ux is inuenced by the ability of sugar kelp to
deplete DIC (dened as the sum of the concentrations of the three
carbonate species: dissolved CO
2
, HCO
3and CO2
3) in the surface
water (Maberly, 1990). Restricted to low dissolved CO
2
concentration
in seawater, a large number of marine macroalgae use HCO
3for
photosynthesis. However, the ability to deplete HCO
3and, as a result,
DIC varies among species (Sand-Jensen and Gordon, 1984). The DIC
uptake rate of sugar kelp decreases when the DIC concentration is
reduced, and the minimum DIC achievable is estimated to be around
1282 mmol m
3
(Maberly, 1990).
It has been hypothesized that the relatively long equilibration
times associated with carbon uptake of low pCO
2
water (Jones et al.,
2014) can limit the effectiveness of ocean CDR (Bach et al., 2021).
Since our one-dimensional model does not include the subduction
of mixed layer water into the ocean interior, we are not able to test
this hypothesis. If the low pCO
2
water is subducted into the interior
before equilibrating with the atmosphere, the air-sea CO
2
ux could
be reduced. Future studies considering physical transport would be
necessary to provide a comprehensive quantication of CDR from
the atmosphere, for example studying the residence-time-limited
CDR potential.
The signicant enhancement of the gravitational pump when
the kelp density is lower than 2.2 fronds m
3
indicates that POC
sinking alone without biomass harvesting and intentional sinking
can be an effective pathway of exporting carbon to the deep ocean.
Since total harvest costs on average represent about 19% of total
seaweed farming costs (DeAngelo et al., 2023), POC sinking alone
without biomass harvesting and intentional sinking may be a cost-
effective CDR pathway at lower seaweed cultivation densities. A
kelp density of 1.1 fronds m
3
is found to maximize carbon export
through POC sinking in the current conguration. When the kelp
density is higher than this density, although air-sea CO
2
ux is still
signicant, more xed carbon by kelp is channeled to biomass
carbon or exuded DOC. In this case, intentional biomass harvesting
or sinking might be a more effective option to sequester carbon.
As acknowledged in Broch and Slagstad (2012), the erosion rate
and its dependence on parameters (hydrodynamic conditions,
frond age, etc.) are highly uncertain and more research is needed
to reduce this uncertainty. To test the inuence of the erosion rate
on the gravitational pump and air-sea CO
2
ux, we varied the
parameter controlling the dependence of the erosion rate on the
kelp area by ±50% for the case with a kelp density of 1.1 fronds m
3
and found that the maximum amplitude of the gravitational pump
and the air-sea CO
2
ux changed by at most 13.7% and 2.4%
respectively compared to the baseline value (see the Supplementary
Material for details).
Here, we only consider the portion of the water column above
500m depth. POC that sinks below this depth will either get
consumed in the water column (e.g. in the mesopelagic) or settle
on the seaoor. Benthic biological and physical processes will
determine the ultimate fate of the material that reaches the
seaoor and ultimately the sequestration time. The accumulation
of organic material on the seaoor could also have a major impact
on the benthic community structure and oxygen levels (Bach
et al., 2021).
Our model also indicates that kelp cultivation can have a
signicant impact on nutrient availability and phytoplankton net
primary production. Nutrient limitations driven by macroalgae
cultivation and lowered recycling rate of nutrients within the
macroalgal biomass (Chapman and Craigie, 1977) will also alter
phytoplankton community structure. The shift from small POC
(dominated by microalgal detritus) to large POC (dominated by
macroalgal detritus) and the shift in timing of maximum POC
export have implications for the food web. There may also be
signicant ecological effects on deep-ocean communities associated
with the enhanced particulate ux to the deep ocean (Boyd
et al., 2022).
In summary, the results presented here reveal an important
pathway for CDR and suggest that including POC export is
important for assessing macroalgal cultivation as a CDR strategy.
On the other hand, our model indicates that macroalgal cultivation
can signicantly inuence phytoplankton net primary production,
and the ecological impacts of this need to be fully assessed.
Data availability statement
The raw data supporting the conclusions of this article will be
made available by the authors, without undue reservation.
Author contributions
SC: Data curation, Formal Analysis, Investigation,
Methodology, Visualization, Writing original draft, Writing
review & editing. JSW: Methodology, Software, Writing original
draft, Writing review & editing. JRT: Conceptualization, Funding
acquisition, Methodology, Project administration, Resources,
Supervision, Writing original draft, Writing review & editing.
Funding
The author(s) declare nancial support was received for the
research, authorship, and/or publication of this article. This work is
funded by grants from the Centre for Climate Repair and the
Gordon and Betty Moore Foundation in collaboration with the Kelp
Forest Foundation.
Acknowledgments
The authors are grateful to the Centre for Climate Repair, the
Kelp Forest Foundation, and Running Tide for stimulating
conversations and encouraging this work. The authors also
thank Samantha Deane, Max Chaln, Dennis Hansell, Ole Jacob
Broch, Silje Forbord, and Brian von Herzen for helpful
discussions. This study has been conducted using data from
E.U. Copernicus Marine Service Information and NASAs Ocean
Biology Processing Group.
Chen et al. 10.3389/fmars.2024.1359614
Frontiers in Marine Science frontiersin.org08
Conict of interest
The authors declare that the research was conducted in the
absence of any commercial or nancial relationships that could be
construed as a potential conict of interest.
Publishers note
All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their afliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed or
endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online
at: https://www.frontiersin.org/articles/10.3389/fmars.2024.1359614/
full#supplementary-material
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A growing trend of interest for the cultivation of kelp is driven by predictions for high global demands of important commodities, which require the development of alternative supplies of natural resources. In this study the dynamics of loss of biomass from cultivated Saccharina latissima were studied from February to August 2018 at two kelp farms in Northern (69°45.26′N/019°02.18′E) and in Mid-Norway (63°42.28′N/08°52.23′E). Kelp fronds at each farm were individually followed throughout the growing season. Sectional regression was applied for conversion of measured frond lengths to estimated dry weights. The study shows that between 40 and 100% of all individuals in the studied kelp population constantly eroded slightly from their distal ends. However, until June the accumulated loss was only 8% of produced dry weight. Due to dislodgement of whole sporophytes this picture changed in July and August to heavy losses in Mid-Norway. Thus, the overall losses of kelp in terms of accumulated dry weight were only 8–13% of the gross growth until harvest in June in Mid-Norway and August in Northern Norway. Losses increased significantly in Mid-Norway during July and reached 49.4% of the annual production in August. The rates of losses were separated into specific erosion and dislodgement rates. Erosion rates over the whole experimental period for the two sites were not significantly different, while differences in dislodgement rates between farm sites proved to be highly significant. The exported annual amount of carbon was estimated on the basis of lost and measured carbon content in the tissue. From these data a scenario was built for a commercial Norwegian kelp farm growing S. latissima showing a carbon export of 63–88 g C m–2y–1. This is eight times less than has been reported from scenarios for kelp farms in China. This study confirms that optimal timing of harvest is the most important management tool for avoidance of heavy losses from kelp farms. In conclusion, an industry with early harvest will likely have a low carbon export, while a late-harvested bulk production could export four to six times as much carbon with an increased potential for carbon sequestration.
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This textbook for advanced undergraduate and graduate students presents a multidisciplinary approach to understanding ocean circulation and how it drives and controls marine biogeochemistry and biological productivity at a global scale. Background chapters on ocean physics, chemistry and biology provide students with the tools to examine the range of large-scale physical and dynamic phenomena that control the ocean carbon cycle and its interaction with the atmosphere. Throughout the text observational data is integrated with basic physical theory to address cutting-edge research questions in ocean biogeochemistry. Simple theoretical models, data plots and schematic illustrations summarise key results and connect the physical theory to real observations. Advanced mathematics is provided in boxes and appendices where it can be drawn on to assist with the worked examples and homework exercises available online. Further reading lists for each chapter and a comprehensive glossary provide students and instructors with a complete learning package.
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The role of animal (and plant) respiration in assessing the true carbon sequestration potential of a system is vital to acknowledge, and addressed in Gallagher et al. (2022). However, within this article, there is confusion around the respiration of kelp once exported to open waters from kelp ecosystems but respired before sequestration. From their consideration of a closed kelp ecosystem (but with import of phytoplankton and export of kelp), respiration of phytoplankton transported into the system is correctly considered in their net respiration figures (but not the fixation of carbon dioxide by the phytoplankton outside the system, again correct for a closed system). However, the respiration of kelp exported from the closed system is also considered as part of the kelp community respiration. A closed system must remove this respiration of exported kelp from calculations. Alternatively, an open system must consider also the carbon fixation by phytoplankton. The outcome of redefining open and closed systems is that the systems examined in Gallagher et al. (2022) will be net sinks of carbon, although, as yet, the magnitude of this sink is poorly quantified.
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