The potential of seaweed cultivation to achieve carbon neutrality and mitigate deoxygenation and eutrophication

The data on seaweed production and cultivation area are from the China Fishery Statistical Yearbook for the years of 2000–2020. Annual productivity of seaweeds was calculated by dividing production by cultivation area. Only cultivated seaweeds are involved in these data. Seaweeds are cultivated in coastal seawaters along the coastline of China from Liaoning Province in the North of China to Hainan Province in the South of China. The culture period varies with different species (table S7 available online at stacks.iop.org/ERL/17/014018/mmedia). The census method is used to estimate the production and cultivation area of seaweeds in China, in which data are collected from each local farmer and then compiled (Gao 2015). Although there may be some errors during the data collection and compilation, census is considered to a reliable statistical method because all the items are taken into account (Baffour et al 2013). It is very difficult to know the uncertainties of such Statistical Yearbook data because the 'real' data are unavailable. The parameter that would affect the assessment of seaweed potential to achieve carbon neutrality and mitigate deoxygenation and eutrophication is annual productivity. The highest annual productivity (18 tonnes DW ha⁻¹ yr⁻¹ in 2019) of U. prolifera documented by the Statistical Yearbook is close to that (20 tonnes DW ha⁻¹ yr⁻¹ in 2019) of U. prolifera, the same species, cultivated in Japan (Hiraoka and Oka 2008). Based on this comparison, the data from the Statistical Yearbook seem reliable.

The combination of published data and data measured by ourselves on tissue C, N and P content was used (tables S1–S3). The published data were obtained through a search of ISI Web of Science, CNKI and Scholar Google on 11 May 2021, using the terms 'carbon, nitrogen, phosphorus, seaweed and China' as keywords, and hence all literature published before 11 May 2021 was screened. Twenty seven papers were finally selected after double-checking whether the reported seaweeds were from Chinese seas.

In terms of the data from the present study, Pyropia haitanensis (January 2021) and Gracilariopsis lemaneiformis (March 2021) were collected in Sansha Bay in Fujian Province, China, Betaphycus gelatinum was collected in a seaweed farm in Changjiang, Hainan Province, China in March 2021, and Ulva prolifera was from Xiangshan Bay, Zhejiang Province, China in March 2021. Content of tissue carbon and nitrogen was measured by an Elementar Vario EL Cube (Elementar, Germany). Tissue phosphorus content was determined according to the method in Solórzano and Sharp (1980).

Mean C, N and P contents of seven farmed seaweeds were calculated based on the published data and our own data. To better represent the current status of cultivated seaweeds, the average seaweed annual production (harvested biomass, P) during 2015–2019, rather than 1999–2019, combined with the mean C, N and P contents (C_C/N/P), was used to calculate the removal amount of C, N and P (RA_C/N/P) from coastal waters. The removal capacity of C, N or P (RC_C/N/P) for each seaweed species is calculated by dividing removal amount of C, N or P by the cultivation area (A). The corresponding formulas are as follows:

$$\begin{equation}{\textrm{R}}{{\textrm{A}}_{{\textrm{C/N/P}}}}\left( {{\textrm{tonne y}}{{\textrm{r}}^{ - 1}}} \right) = P\; \times \;{C_{{\textrm{C/N/P}}}}\end{equation} \tag{ 1 }$$

$$\begin{equation}{\text{R}}{{\text{C}}_{{\text{C/N/P}}}}\left( {{\text{tonne h}}{{\text{a}}^{ - 1}}{\text{y}}{{\text{r}}^{ - 1}}} \right) = R{{\text{A}}_{{\text{C/N/P}}}}/ {{A}} \end{equation} \tag{ 2 }$$

The removed carbon will be released into the atmosphere if seaweeds are used for food. However, it can be sequestered if the negative emission technology of BECCS (bioenergy with carbon capture and storage) is deployed (Hanssen et al 2020).

Carbon sequestration is defined as the amount of carbon that could be stored in the ocean in the long-term (>100 years). Carbon sequestration by seaweed cultivation occurs because a large part of the plant matter is not extracted (harvested) but disintegrates in the ocean, breaking up into particle organic carbon (POC) that falls to the ocean floor and is stored in sediment, or remaining as refractory organic carbon dissolved in the water. The amount of sequestration can be calculated based on the following formulas:

$$\begin{align} &{\text{Carbon sequestration }}\left( {{\text{Cs}}} \right) \nonumber\\ &\quad = {\text{PO}}{{\text{C}}_{{{b1}}}} + {\text{PO}}{{\text{C}}_{{{b2}}}} + {\text{PO}}{{\text{C}}_e} + {\text{rDOC,}}\end{align} \tag{ 3 }$$

$$\begin{align} &{\text{Net primary productivity }}\left( {{\text{NPP}}} \right) \nonumber\\ &\quad = {\text{PO}}{{\text{C}}_h}\; + \;{\text{PO}}{{\text{C}}_l} + \;{\text{DO}}{{\text{C}}_e},\end{align} \tag{ 4 }$$

The formulas (3) and (4) are based on the integration of Krause-Jensen and Duarte (2016) and Zhang et al (2017), where POC_{b 1} = POC buried in the algal bed, POC_{b 2} = POC buried in the shelf, POC_e = POC exported to the deep sea, rDOC = refractory DOC (dissolved organic carbon), POC_h = harvested POC, POC_l = lost POC due to remineralization, grazing, detachment, breakoff, etc, equal to the sum of the remineralized and grazed POC, POC_{b 1}, POC_{b 2} and POC_e , DOC_e = excreted DOC by seaweeds. Please see figure 1 for the whole picture of the carbon pathways of cultivated seaweeds and the sequestrated carbon is marked in blue. According to Krause-Jensen and Duarte (2016), the ratios of POC_{b 1}, POC_{b 2} and POC_e to NPP are 0.004, 0.009, 0.023, respectively; according to Wada et al (2008) and Watanabe et al (2020), the ratio of rDOC to DOC_e is 0.562; according to Zhang et al (2012), the ratio of harvested POC to lost POC is 0.622; according to Krause-Jensen and Duarte (2016), the ratio of DOC_e to NPP is 0.233. Therefore, it can be calculated that the ratio of harvested POC to NPP is 0.294 and the ratio of carbon sequestration to harvested POC is 0.568. It is worth noting that these ratios are generalized and different seaweeds would have different values. The specific ratios for each seaweed species are unavailable and we have to use the generalized ones in this study for now.

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The required area (A_Ci) to achieve carbon neutrality for each seaweed species was calculated according to the formula of

$$\begin{equation}A_{{\text{Ci}}} = {T_{\text{C}}}{\text{/Csi,}}\end{equation} \tag{ 5 }$$

where T_C is the total CO₂ amount that is needed to be sequestrated annually to achieve the China carbon neutrality goal by 2060, which is 2.5 Gt CO₂ according to Fuhrman et al (2020); Csi is the carbon sequestration capacity (Cs in formula (3)) for each seaweed species.

A sensitivity analysis was undertaken to identify which component of the seaweed cultivation contributes most directly to the required area to achieve carbon neutrality of China. For this analysis, every input factor had a ±30% change from its baseline value that was shown in section 2.3, while all other input factors remained constant, to detect its effect on the required area.

The amount of oxygen released by seaweed cultivation was calculated according to the photosynthesis equation:

$$\begin{equation}{\text{6C}}{{\text{O}}_{\text{2}}}{\text{ + 6}}{{\text{H}}_{\text{2}}}{\text{O}} \to {{\text{C}}_{\text{6}}}{{\text{H}}_{{\text{12}}}}{{\text{O}}_{\text{6}}}{\text{ + 6}}{{\text{O}}_{\text{2}}},\end{equation} \tag{ 6 }$$

when every tonne of carbon is fixed, 2.67 tonnes of O₂ are generated. Here the carbon that is involved includes harvested carbon and sequestrated carbon.

Released N and P by fish mariculture were calculated by the following formulas:

$$\begin{equation}{\textrm{Nr }}\left( {{\textrm{or Pr}}} \right) = F \times C{\mkern 1mu} \times {\mkern 1mu} \left( {1 - R} \right),\end{equation} \tag{ 7 }$$

$$\begin{equation}F = P \times {\textrm{Fc}},\end{equation} \tag{ 8 }$$

The formulas (7) and (8) are based on Lazzari and Baldisserotto (2008), where Nr and Pr are released N and P, F = feed amount, C = content of N or P in feeds, R = retention rate of feed N or P in fish, P = fish production, and Fc = feed coefficient, the feed consumption per unit weight increase of fish. Here, the assumption is that half of the fish increase in weight is from artificial feeds and the other half is from wild feeds (fresh trash fish) based on recent investigations (Wang 2016, Li et al 2021). The contents of N and P in artificial feeds are 6.85% and 1.40%, respectively (table S4) and for wild feeds they are 2.68% and 0.48% respectively (table S5). The retention rate of feed N or P in fish is set at 30% based on previous studies (Xu et al 2007, Lazzari and Baldisserotto 2008, Herath and Satoh 2015). The fish average annual production is 1392 435 tonnes based on the China Fishery Statistical Yearbook 2016–2020. The feed coefficient is 1.52 and 6.49 for artificial and wild feeds, respectively (table S6).

The areas required to remove N (A_N) and P (A_P) released by fish mariculure were calculated by the formulas

$$\begin{equation}A_{\text{N}} = {T_{\text{N}}}{\text{/ Ni}}\end{equation} \tag{ 9 }$$

and

$$\begin{equation}{A_{\text{P}}} = {T_{\text{P}}}{\text{/ Pi,}}\end{equation} \tag{ 10 }$$

where T_N and T_P are the total N and P amounts released by fish mariculture, respectively; Ni and Pi are the N and P removal capacities for each seaweed, respectively. The amounts of N and P released by fish mariculture could be calculated using formulas (7) and (8).

Blue carbon plants (mangroves, salt marshes and seagrasses) have a NPP of 817–1100 g C m⁻² yr⁻¹ (Duarte et al 2013). Compared to them, wild seaweeds have lower NPP, being in the range 420–750 g C m⁻² yr⁻¹ (Duarte et al 2013, Krause-Jensen and Duarte 2016), which may be related to their seasonal fluctuations in biomass. However, this study shows that farmed seaweeds usually have a higher NPP (265–3260 g C m⁻² yr⁻¹) compared to wild ones. The NPP of some farmed seaweeds are even higher than those of blue carbon plants. It was reported that Macrocystis pyrifera farmed in the USA had a productivity of 38–62 tonnes DW ha⁻¹ yr⁻¹ (Chynoweth 2002), equal to 1140–1860 g C m⁻² yr⁻¹ assuming that the carbon content is 30% DW (Stewart et al 2009). The annual productivity of U. lactuca cultivated in Denmark could achieve 45 ton DW ha⁻¹ yr⁻¹ (Bruhn et al 2011), equal to 2214 g C m⁻² yr⁻¹ using the carbon content of 41% DW (table 1). These values are lower than the highest productivity (3260 g C m⁻² yr⁻¹ for G. lemaneiformis) shown in the present study. The key reason for a higher NPP in our study is that the calculation includes lost POC and excreted DOC while previous studies exclude these two portions. According to Zhang et al (2012) and Krause-Jensen and Duarte (2016), the lost POC and excreted DOC can account for 47% and 23% of NPP, respectively. Therefore, Macrocystis pyrifera and U. lactuca in previous studies would have higher NPP than seaweeds reported in this study if lost POC and excreted DOC are taken into account. It is worth noting that G. lemaneiformis has the highest NPP among the seven cultivated seaweeds. This may not be due to high net photosynthetic rates since Ulva species have higher growth rates (Gao et al 2016, Ji et al 2019). Therefore, its high NPP could instead be attributed to its year-round cultivation period in some areas of China while U. prolifera is cultivated for only 2–4 months (table S7). On the other hand, the low growth rates (0.63–4.60% d⁻¹) of Eucheuma result in a lower NPP although they are cultivated all year round in China (Liang 2010). Therefore, the NPP of cultivated seaweeds depends on their both growth rate and cultivation period.

In spite of the lower NPP compared to other blue carbon plants, wild seaweeds have a very high total net primary production (173 Tg C yr⁻¹). Despite this, their contribution to blue carbon has been controversial because how much carbon can be sequestration by seaweeds has been uncertain (Macreadie et al 2019). Recently, Ortega et al (2019) confirmed that seaweeds can be exported to the open ocean and the deep sea. Seaweeds can reach to 5000 km from coastal areas worldwide and 24% of seaweeds available at the surface can be transported to the seafloor at a depth of 4000 m, indicating that the carbon fixed by seaweeds can be sequestrated for a long time in the deep ocean. Krause-Jensen and Duarte (2016) evaluated the amount of carbon sequestration by seaweeds as being 173 g C m⁻² yr⁻¹, which is much higher than any other blue carbon plant (11–44 g C m⁻² yr⁻¹), suggesting the importance of seaweeds in global carbon sequestration.

In terms of farmed seaweeds, it was assessed that an upper limit to the CO₂ capture potential of seaweed cultivation can be calculated at 0.68 Tg C per year (Duarte et al 2017). In this study, the total carbon removal of seven farmed seaweeds in China during 2015–2019 is 0.61 Tg year⁻¹. The reason that carbon removal of farmed macroalgae in China has so higher a proportion of the global amount may be due to two aspects. Durate et al (2017) assumed that all of the 27.3 million tonnes of fresh weight farmed in 2014 were dedicated to carbon capture with an average carbon content of 24.8% of dry seaweed and a fresh weight: dry weight ratio of 10. We used the total dry weight of 2.09 million tons recorded by the China Fishery Statistical Yearbook 2016–2020 and the actual carbon content of the seven farmed seaweeds. The average carbon content of seven farmed seaweeds is 32.9% (median of 31.0%), noticeably higher than 24.8%. While, to the best of our knowledge, previous studies focused on short-term carbon fixation and removal, no data has been reported about the amount of long-term carbon sequestration by farmed seaweeds. By integrating previous studies (Wada et al 2008, Zhang et al 2012, Krause-Jensen and Duarte 2016, Watanabe et al 2020), we used the ratio of sequestrated carbon to removed carbon (0.568) by harvested seaweeds to calculate the carbon sequestration of farmed seaweeds. The total carbon sequestration of farmed seaweeds in China is 344 128 tonnes per year. G. lemaneiformis has the highest carbon sequestration capacity and thus requires the smallest area to achieve carbon neutrality, due mainly to its high carbon content and productivity. The required areas for G. lemaneiformis to achieve carbon neutrality based on carbon sequestration and carbon sequestration + removal capacities are 12.52 × 10⁷ and 4.54 × 10⁷ha, respectively. The marine area of China is ∼3 × 10⁸ ha, which means that about one-seventh of Chinese seas will be occupied to achieve carbon neutrality if harvested seaweeds are transformed to recalcitrant carbon or BECCS is deployed. The cultivation area will be further reduced if productivity is enhanced and other NETs are employed. In terms of the availability of suitable cultivation areas, it was reported that the distance to coastline could be as far as 20 km for kelp cultivation in China (Liu et al 2019). Therefore, the rough estimate for a suitable cultivation area is 3.94 × 10⁷ ha if the length of 19.7 × 10³ km is used for the coastline of China (Hou et al 2016), which is less than the required areas for G. lemaneiformis. Therefore, it seems that seaweed cultivation by itself is not enough to achieve the carbon neutrality target of China. Meanwhile, we have to admit that this is a very rough estimate. Although different seaweed species can be cultivated in areas with different temperatures along the coastline in China, seaweed productivity would be inhibited when nutrient availability is low in offshore waters. Therefore, species selection, environmental (temperature, nutrient, currents, etc) and socioeconomic aspects of the sites must be carefully assessed before conducting the cultivation.

The cost for large-scale cultivation is another issue that should be considered. The current cost for kelp cultivation in China is about $85 per tonnes dry weight (Liu et al 2019), which is much higher than the current carbon price of $8–15 per tonnes of CO₂. Therefore, it is economically unfeasible to cultivate seaweeds to achieve carbon neutrality without subsidies. An obvious solution is to sell the harvested parts of the seaweeds to cover the cultivation cost. The market price of kelp for food is ∼$3000 per tonne dry weight, but current consumption is only 1.62 × 10⁶ tonnes DW, far less than the 4.32 × 10⁹ ton DW that would be available under our model. A possible solution is therefore to combine its use in food, feed, medicine and biofuel. Bioenergy uses in particular would seem to be hopeful. The use of bio-methane from seaweeds is very close to profitability (Gao et al 2020). Therefore, the combination of low-volume high-value (food, medicine) and high-volume lower-value (biofuel) use could be considered. It is worth noting that climate change and the changes it will bring to seaweed productivity may influence carbon sequestration capacity and the required cultivation areas. Although market demand has been driving the increase in seaweed production and cultivation area, improved techniques and strains contribute to increased productivity for most seaweed species (Ferdouse et al 2018), resulting in a general rising trend during the past 21 years. However, there are different rates of productivity increase for each species, which may be related to environmental changes. It has been documented that climate-driven changes including warming and marine heatwaves have led to a 0.45 Tg C loss of standing stock and a 0.06 Tg C reduction in sequestration annually in Australian kelp forests during the past decades (Filbee-Dexter and Wernberg 2020). On the other hand, ocean acidification increased the biomass yield of Saccharina japonica and Ulva prolifera (Gao et al 2017b, Zhang et al 2021), which may increase the carbon sequestration of these seaweeds. Therefore, the impacts of climate change on the carbon sequestration of seaweeds are complex and need to be further illuminated by future studies.

Ocean deoxygenation is raising considerable concerns because of its potential ecological impacts on marine ecosystems (Laffoley and Baxter 2019). There are faster deoxygenation rates in coastal seawaters due to the combination of eutrophication and ocean circulation shift (Claret et al 2018). The present study demonstrates that, apart from carbon sequestration, seaweed cultivation also contributes to oxygen enrichment in seawaters. Our study shows that seaweed cultivation generates 2532 221 tonnes oxygen annually, which is equivalent to increasing the dissolved oxygen in aquaculture waters (3 m in depth) by 21% daily if the current dissolved oxygen (DO) level is 8.16 mg L^-1 and the gas exchange is excluded. Rising nutrient loads coupled with climate change are causing oxygen decline in the global ocean and coastal waters, impacting processes ranging from biogeochemistry to food security (Breitburg et al 2018). Therefore, it is extremely important to be aware that seaweed cultivation seems to be able to compensate for the DO loss due to ocean warming and supply enough DO for the survival of marine organisms, contributing importantly to the health of the marine ecosystem.

Seaweeds are known to be good bioremediators particularly for N and P removal (He et al 2008, Xiao et al 2017). He et al (2008) reported that farmed Porphyra yezoensis in the open sea reduced the concentrations of NH₄–N, NO₂–N, NO₃–N and PO₄–P by 50%–94%, 42%–91%, 21%–38% and 42%–67%, respectively and had N and P removal capacities of 0.049 and 0.008 ton ha⁻¹ yr⁻¹. In the present study, the N (0.10 ton ha⁻¹ yr⁻¹) and P (0.01 ton ha⁻¹ yr⁻¹) removal capacity of Pyropia was higher. Apart from different cultivation scales and N and P contents in algal tissues, the gap may be due to different productivity. In the present study, cultivated Pyropia includes both P. haitanensis and P. yezoensis, with P. haitanensis in a dominant position. P. haitanensis has higher growth rates and productivity compared to P. yezoensis (Xu et al 2016). Xiao et al (2017) assessed the nutrient removal of Chinese seaweed cultivation and found approximately 75 000 t nitrogen and 9500 t phosphorus were removed annually from Chinese coastal waters. In this study, it is shown that seven seaweeds remove 70 615 t nitrogen and 8515 t phosphorus annually. The lower values in this study are probably due to lower N and P contents being used since the seaweed production in both studies are very close (2.09 vs 2.00 million t DW). N and P contents in Xiao et al (2017)'s study are based on published data on seaweeds both in China and other countries until December 2015 while our study integrated recent studies by May 2021 and all data are from Chinese seaweeds. For instance, the extremely high P content of 4.87% in Kappaphycus striatus from Indonesia was used in Xiao et al (2017).

Fish aquaculture is a major pollution source because most N and P in the feeds are finally released to the environments (Xu et al 2007, Herath et al 2015). Fish production from mariculture reached 1605 802 tonnes in 2019 in China. To show the bioremediation capacity of farmed seaweeds in China, we compared the N and P removed by farmed seaweeds and released by fish mariculture and calculated the gap for the first time. Although seaweed cultivation could remove a large amount of N and P, it is not enough to offset the N and P released by fish mariculture. One important cause of this is that a considerable proportion of N and P in the feeds is released into the seawater through the decomposition of uneaten feeds and the discharge by fish after digestion (Xu et al 2007, Herath and Satoh 2015). To completely bioremediate the N and P released by fish mariculture, two times and three times higher production of seaweeds than the current one are required, respectively. To reduce fish mariculture or improve the feed utilization efficiency is another approach to solve the gap apart from increasing cultivation area and productivity of seaweeds. Coculturing seaweeds with fish would be an effective way to enhance seaweed productivity and reduce the cultivation area. This study supplies essential data for adjusting aquaculture structure and developing sustainable and green mariculture.