Methods for Measuring Carbon Dioxide Uptake and Permanence: Review and Implications for Macroalgae Aquaculture

Abstract

Carbon dioxide removal (CDR) is gaining recognition as a necessary action in addition to emissions reduction to prevent some of the worst effects of climate change. Macroalgae aquaculture has been identified as a potential CDR strategy and significant research investments have been made in this area. This article reviews current methods for monitoring carbon to assess the potential for application in the context of macroalgae aquaculture as a CDR strategy. In total, 382 papers were included in the review and categorized by carbon uptake methods, carbon permanence methods, and comprehensive frameworks for assessing carbon capture. While methods for measuring carbon uptake are well established, methods to assess the permanence of carbon in the natural life cycle of macroalgae and in products following harvest are lacking. To achieve the full benefit of macroalgae cultivation as a climate solution, monitoring, reporting, and verification standards and improved methods for assessing carbon uptake and permanence need to be developed.

1. Introduction

Carbon dioxide removal (CDR) is gaining recognition as a necessary action to prevent some of the most severe effects of climate change due to greenhouse gas emissions [1,2]. CDR technologies can leverage technological pathways to capture or convert carbon dioxide (CO₂), or biological pathways that rely on photosynthesis to fix CO₂ into other forms of carbon. CO₂ is present in and can be removed from either the air or the ocean to satisfy CDR goals. Marine CDR (mCDR) refers to the removal of CO₂ from anthropogenic activities that has dissolved into the ocean based on partial pressures to reach equilibrium [3]. Excess CO₂ in the ocean lowers the pH of the seawater, resulting in ocean acidification, which can reduce calcification rates in shell-building organisms and corals, with far-reaching negative environmental and economic consequences [4,5,6].

The global ocean is a natural carbon sink, sequestering “blue” carbon in coastal and marine ecosystems [7,8,9,10,11]. Blue carbon includes habitats such as tidal marshes, seagrass meadows, mangrove forests, and macroalgae (including seaweed and kelp), as well as phytoplankton [8,12,13,14,15,16,17,18,19,20,21,22,23,24]. In addition to restoration or preservation of these natural blue carbon ecosystems [12,17,25,26,27], many mCDR methods such as electrochemical methods [28], alkalinity enhancement [29,30,31], enhanced weathering [32,33,34], aquaculture [35,36,37], and more are being explored to mitigate the effects of climate change and ocean acidification [7,38,39,40,41,42,43].

The use of macroalgae cultivation to capture carbon through photosynthesis and sequester it in the deep ocean, sediments, or long-lived products is a promising and priority mCDR strategy, with relatively low costs and high potential for social and environmental co-benefits [7,36,43,44,45,46,47,48,49,50,51]. However, there are significant challenges to measuring carbon capture and permanence of sequestration in macroalgae [41,45,52,53,54,55,56]. The actual potential of large-scale macroalgae cultivation for carbon sequestration purposes is still unknown [45,56,57,58,59,60], especially considering variability between species [53,61,62], future changes in climate [63,64,65,66,67], and biophysical limits to growth [68]. At present there are no established monitoring, reporting, and verification (MRV) protocols for assessing carbon capture and sequestration in macroalgae products or end uses [7,37,54,69]. To understand the potential of macroalgae aquaculture as a mCDR strategy, it will be important to understand both the quantity of carbon captured (“uptake”) and the duration that the carbon will be sequestered (“permanence”), considering interactions across the carbon cycle and life cycle of a product instead of assuming permanent sequestration without sufficient data [56,70,71,72,73].

This paper reviews methods for monitoring CO₂ capture and sequestration across a variety of applications in various settings to identify potential applicability for macroalgae CDR monitoring and carbon accounting. Numerous methods and programs exist for carbon monitoring across multiple research sectors (e.g., [19,73,74,75,76,77,78,79,80]) that can be leveraged for novel ocean applications. Consideration of various existing methods will enable identification of the opportunities and limitations to accurately assess the uptake and permanence of carbon in cultivated macroalgae and inform the development of MRV approaches for biological ocean carbon capture.

2. Methods

This review conducted a structured literature search using Web of Science with the following keywords: “marine carbon dioxide removal” OR “ocean carbon dioxide removal” OR “ocean-based carbon” OR “carbon monitoring” OR “ocean deacidification” OR “blue carbon sink” OR “ocean carbon sequestration” OR “marine carbon sequestration”; and another search for “kelp” OR “seaweed” OR “macroalgae” (All Fields) AND “carbon dioxide” OR “carbon sequestration” OR “blue carbon” (All Fields) and “monitor” OR “measure” OR “assess” OR “evaluate” OR “method” (All Fields).

A total of 1008 search results were returned and reviewed by a single person for relevance, out of which 479 were retained after review of title and removal of duplicates, and 382 remained after review of abstracts (complete collection available on request). Papers were removed that were unavailable in English; focused on ocean acidification, emissions, or supercritical CO₂ processing; and general monitoring or review papers that were not specific to carbon. The 382 papers were reviewed for their approach to CDR, ocean or terrestrial focus, methods approach, and the species or setting (if applicable). The extent of application for carbon uptake (defined as presence of methods for measuring carbon quantity) and carbon permanence (defined as presence of methods considering time and the ultimate fate of captured carbon) was assessed as either “Yes” or Not Applicable (“NA”). The applicability and relevance of each method for macroalgae aquaculture was assessed using the following scale:

• Not Applicable (NA): the method has no imaginable relevance for measuring carbon in macroalgae;
• Low: the method has limited applicability to macroalgae aquaculture due to the metrics sampled or nature of sampling;
• Medium: the method may currently be used in assessing carbon in macroalgae with existing caveats, or may not be currently used but could be applied with caution;
• High: the method is currently used in assessing macroalgae and is easy to translate information collected in various scenarios.

3. Results

A total of 382 papers were retained in the review that included information on monitoring carbon across a variety of CDR methods and contexts (Figure 1). The majority of papers reviewed (72%) focused on biological or life cycle approaches to CDR, for example, blue carbon or terrestrial forests (Figure 1a). About half of the papers reviewed included monitoring of carbon in the ocean or coastal context (Figure 1b), and 18% were specific to macroalgae (Figure 1c). Only 8% of papers reviewed described a product formed as part of the CDR process (Figure 1d), which included biofuels, multiple harvested seaweed products, other aquaculture products, and biochar.

Monitoring methods ranged from simple sensors (for pH, dissolved inorganic, or organic carbon [81]) and sampling routines (e.g., [82]) to complex models coupled with remotely sensed data (e.g., [14,83,84]). Methods can be grouped into three general categories of application: monitoring carbon uptake, methods for monitoring carbon permanence, and comprehensive frameworks for analyzing carbon capture. A synthesized list of methods for monitoring carbon is provided in

Table 1. Methods for monitoring carbon synthesized from the literature review.

		Method	Sample Metrics	Carbon Uptake	Carbon Permanence	Macroalgae Relevance
	Uptake Methods	Remote sensing *	Aboveground biomass, reflectance, crown segmentation, eddy covariance, canopy height, chlorophyll, temperature, ocean and land color, leaf spectroscopy, net primary productivity	Yes	NA	Low
		Physical sampling **	Reflectance, biomass, dissolved inorganic carbon, sap flow, diameter breast height, isotopes, fecal pellet, phaeopigment, dissolved oxygen, salinity, frond length, sinking speeds, light use efficiency	Yes	NA	Medium
Permanence Methods		Mesocosm experiments	Photosynthetic rates, pH, growth rate, degradation or decomposition rates, electron transport rates, dye decolorization, regrowth rate, assimilation, net primary productivity	Yes	Yes	High
		Sediment sampling	Organic matter, inorganic/organic carbon, carbon-13	Yes	Yes	High
		Modeling	Atmospheric aridity, circulation, light use efficiency, mechanistic particle flux, soil respiration, waveform to biomass, transit time, carbon loss through exudation and erosion	Yes	Yes	High
	Comprehensive Frameworks	Life cycle analysis	Global warming potential over 100 years	Yes	Yes	High
		Forensic carbon accounting	Seaweed standing stock, primary production, CO2 influx	Yes	Yes	High
		Carbon accounting framework	Disposal rate, service life, processing efficiency	Yes	Yes	Medium
		Ecosystem service assessment	Carbon stock, carbon flow	Yes	Yes	Medium
		Reducing emissions from deforestation and forest degradation (REDD+)	Deforestation rate, forest carbon stock	Yes	Yes	NA

* Remote sensing methods include satellites, unoccupied aerial or underwater vehicles, LiDAR, synthetic aperture radar, spectrometry, and photoacoustic spectroscopy. ** Physical sampling methods include collection from plots, scuba divers, biomass collection, sensors, vessel cruises, and environmental DNA.

, showing the applicability of each method for macroalgae aquaculture.

3.1. Monitoring Carbon Uptake

A total of 322 papers (84%) described or discussed methods for monitoring carbon removal in terms of uptake. For biological CDR, this is often assessed by measuring standing biomass of carbon-containing organisms, photosynthetic efficiency, or monitoring the change in carbon content of the surrounding environment over time (e.g., [83,85,86,87]). Additional metrics identified in the review are available in Table 1 above. The carbon removal rates reported for macroalgae range greatly, from less than 0.1 to 1 gigatons of CO₂ per year based on the size of farms and species cultivated [7,88,89,90,91], with net primary production ranging from 91–522 g of carbon per square meter, per year [45,92,93].

Across all CDR contexts, both remote sensing and physical sampling techniques are used. Remote sensing methods rely on imagery classification, absorbance, reflectance, color, or other visual attributes to calculate approximate biomass to estimate carbon content. Remote sensing techniques are used less often for assessing blue carbon than in terrestrial settings, as kelp and seagrasses typically have limited surface expression compared to forests that can be easily monitored with satellite or LiDAR imagery (e.g., [94,95,96]). Campbell et al. [76] reviewed monitoring methods for what they call “wet carbon” (which includes ocean and coastal blue carbon, but does not mention macroalgae) using remote sensing techniques. In addition, some remote sensing platforms have been used and recommended in kelp aquaculture applications for canopy forming kelps, including airborne and underwater autonomous vehicles [97,98,99] as well as algorithms for classifying satellite data [84]. For blue carbon specifically, pH sensors, carbon flux measurements, sampling to estimate biomass (typically in terms of wet weight), and manipulative experiments (such as mesocosms or established sampling plots measuring growth rates under various environmental conditions) are used more often [12].

Measuring the carbon captured by macroalgae is relatively straightforward, but the time and cost intensity of methods can vary. Photosynthetic rate or net primary productivity can be calculated using controlled experiments [100,101], time series [87,102,103,104], or in situ sensors to measure changes in pH [105], or samples of the algae can be taken back to a lab for carbon or isotopic analyses [106,107,108]. Core samples of sediments can be collected to assess the historical quantity of carbon captured, especially coupled with isotopic analyses [109]. Numerical models can be applied to extrapolate the quantity of carbon captured from the scale of an individual to the scale of an aquaculture farm or forest, as well as to predict the upper limits of carbon removal based on additional limiting growth factors in a particular environment (like temperature, nitrogen, and phosphorus) [59,110,111]. Combination methods are also commonly used. For instance, the Greenwave Kelp Climate Fund uses a simple methodology to calculate carbon uptake, taking monthly foot-long blade samples that are translated to the full scale of the farm, coupled with harvest wet weight adjusted by a preset ratio [112].

3.2. Monitoring Carbon Permanence

In contrast to carbon uptake, carbon sequestration requires an additional consideration and measurement of the time component in which carbon remains fixed, typically defined as 100 years [55]. A total of 112 papers reviewed (29%) discussed methods for monitoring at least some aspect of carbon permanence. Terrestrial CDR approaches to permanence assessment consider natural life expectancy of forests, disturbance (e.g., deforestation or degradation, harvest, wildfire, land use change, soil tilling), and production and consumption of products. These can be assessed with compilation of datasets such as forest inventories, repeated surveys (either remotely sensed or physically measured), continously monitored experimental forest sites, or physical sampling to determine the effects of disturbance on carbon composition, or development of numerical models that predict disturbance impacts. Seven papers described monitoring the permanence of CO₂ directly injected into the ocean, and 73 papers considered the permanence of biological CDR in the ocean. Carbon permanence is more difficult to assess in marine waters than in terrestrial contexts due to many levels of interconnected carbon cycling [19], dissolved organic and inorganic carbon export by photosynthetic organisms [41,46,109,113,114,115], decomposition rates [63,116,117,118,119,120,121,122,123,124], and leakage of carbon between habitats [18,45,62,125,126] (Figure 2).

Sediment cores can be collected to estimate the amount of carbon exported to the deep sea [17,127,128,129,130,131]. Environmental DNA (eDNA) methods can be used to identify species contributing to carbon in detritus and sediments [20,23,132,133], from which permanence can be inferred. Mesocosm experiments can be used to estimate degradation or erosion rates under various conditions and time periods to assess permanence [118,119,119]. Dolliver and O’Connor [41] used a mixed methods approach to estimate carbon sequestration potential of cultivated kelp, physically sampling to calculate biomass, measuring the proportion of blades that fell off, and using numerical models to estimate the amount of carbon lost through erosion and exudation. Numerical models have also been used to explore the permanence of sinking macroalgae for mCDR [37,73,92], though the authors of these studies noted that many uncertainties remain.

3.3. Comprehensive Frameworks

The literature review identified 15 studies that assess various aspects of carbon capture and permanence in a structured, comprehensive manner. Of these, methods relevant for macroalgae include life cycle analysis (LCA), ecosystem services assessment, a carbon accounting framework, and forensic carbon accounting. Reducing emissions from deforestation and forest degradation (REDD+) [134] was also identified as a comprehensive framework in the literature review, though it was determined to be not applicable to macroalgae aquaculture as it only focuses on terrestrial forest management, and will not be discussed further. Each of these methods relies on multiple data inputs and as such cannot be isolated from other methods of monitoring carbon uptake and permanence.

• LCA is common in assessing the environmental impacts of novel products throughout the production phases, and many LCAs have been performed on macroalgae products (e.g., [135,136,137,138,139,140]). Most LCAs consider carbon uptake and/or permanence under the category of global warming potential (GWP), often over a 100-year time scale. GWP is measured in kg of CO₂ equivalent, which can include emissions from production of macroalgae farm equipment, transportation emissions, and emissions from energy sources used for processing, in addition to carbon captured in macroalgae biomass. Several tools and templates have been developed to aid in conducting LCAs for CDR (e.g., [141,142,143,144]), but these have not been widely implemented.
• Ecosystem services assessment is a tool that has been used in many coastal and marine contexts to assign value to critical benefits provided by natural habitats [116,145,146] and has been applied to aquaculture [147,148,149]. The framework itself describes the categories of provisioning services, cultural services, supporting services, and regulating services (which includes carbon uptake and permanence) to present a holistic approach to assessing value across environmental, economic, and social aspects.
• A carbon accounting framework developed for harvested wood products [150] was identified in the literature review and retained for its possible application to macroalgae aquaculture in terms of permanence of products. The framework utilizes biomass information from harvest data and traces the flow of carbon to various product carbon pools, including fuels, biochar, disposable products, compostable products, and theoretical innovative products.
• Forensic carbon accounting [151] is an approach proposed to analyze carbon flows in macroalgae (specifically seaweeds), both in natural habitats and aquaculture settings. A checklist of parameters to measure is provided and includes many of the methods listed in Table 1 for assessing both carbon uptake and permanence (e.g., net primary productivity, carbon content of biomass, respiration, grazing, and sediment sampling). LCA is also proposed as a component within the forensic carbon accounting framework to assess the fate of carbon in macroalgae products.

4. Discussion

While many methods for monitoring carbon uptake and permanence exist from a variety of contexts, the literature has yet to coalesce around a single, integrated approach for any form of ocean carbon monitoring. As such, this is a pivotal moment to ensure that future methods for mCDR monitoring are accurate, rigorous, and informed by the body of work already available across many contexts. The growth of macroalgae cultivation across the United States and globally [152,153,154,155], coupled with the pressing need to remove CO₂ from the biosphere, make this an excellent time to pause, evaluate the existing tools available, and chart a path forward.

4.1. Limitations of Existing Methods and Applicability to Macroalgae Aquaculture

The prevalence of blue carbon monitoring methods is overrepresented in this review, as these were assumed to be the most applicable for macroalgae and thus represented better in the literature search terms. Terrestrial methods for carbon monitoring are much more well established, better reviewed [156,157], and have already developed best practices [158] and standards (e.g., [159,160,161,162]). Verification methodologies are being developed for some blue carbon approaches (e.g., Verra’s conservation and restoration methodology for tidal wetlands [163], Frontier and CarbonPlan’s CDR Verification Framework [164]), and forensic carbon accounting and the CDR Verification Framework have been proposed for macroalgae, but have yet to be truly tested or implemented. Comprehensive analysis of the carbon flows has been recommended [56] and several research frameworks have been recently developed for cultivated macroalgae [43,165]. Continued progress on these topics is needed and this review contributes to the timely assessment of carbon uptake and permanence in macroalgae for evaluation moving forward.

The categories of methods identified in Table 1 represent somewhat artificial distinctions, as many multi-pronged approaches are described in the literature for particular applications. However, separating methods for measuring carbon uptake and carbon permanence is helpful to understand the breadth of existing approaches, and allows learning from other terrestrial CDR monitoring methods or other blue carbon contexts to be evaluated and applied.

Table 2. Synthesis of opportunities and limitations of specific methods for monitoring carbon uptake and/or permanence in macroalgae, with examples.

Method	Examples	Opportunities (as Applied to Macroalgae)	Limitations (as Applied to Macroalgae)
Remote sensing	Classification of optical satellite images Landsat 8 [166,167] Gao-Fen 1 [84]	Successfully trialed for macroalgae farms in China Can be used for aerial extent of farms with surface expression	Requires development (and validation) of complex classification schemes or algorithms Misclassification can occur in turbid waters or due to clouds Requires surface expression or visibility Not generalizable for all species Some only relevant for very large farms or forests Cloud cover limitations require estimation Monthly variation in quality of maps Limited ability to assess condition Estimates carbon indirectly based on areal extent
	Unoccupied aerial vehicles [98,99,168,169,170]	Have been used for mapping changes in kelp canopy, eelgrass recovery, and beach wrack Classification can distinguish between species Better spatial resolution than satellite Hyperspectral sensors can assess submerged kelp	Optical data collection requires surface expression or visibility For automated classification, detection algorithms needed Tidal height and current speed introduce variability to abundance estimates Prohibitively expensive if operated by a single farm or research study Estimate carbon indirectly based on areal extent
	LiDAR [171,172,173,174]	Has been used for kelp and other blue carbon Can assess bathymetry and subsurface structure	Typically used for terrestrial applications, measuring aboveground biomass Estimates carbon indirectly based on areal extent Requires validation (through field surveys) and development of classification schemes
	Underwater autonomous or remotely operated vehicles [97,175,176]	Have been used at kelp farms Easy to operate on longline farms Can utilize underwater color imagery or sonar (split-beam or side-scan) to measure species without surface expression Able to assess juvenile growth stages	Could be prohibitively expensive if operated by a single farm or research study Typically, low spatial extent due to power and data transmission needs Require development of visual classification model
	Autonomous sensor for DIC [177]	Capable of multi-year deployments More accurate than pH or pCO2 sensors used to estimate DIC	Not tested yet at macroalgae farms to assess detection of carbon uptake or respiration
Physical sampling	Hole punch [122,122,178]	Used at operational kelp farms to calculate biomass and composition Has been used to assess erosion in the context of carbon sequestration	Destructive to some of product Requires repeated vessel time
	Scuba divers [126]	Precise sampling or observations	Require specialized training Not appropriate in offshore contexts
	eDNA [20,23,132,179]	Has been used to identify macroalgae species and quantities in sediment samples qPCR is quantitative, easy to use, and inexpensive eDNA findings can be correlated to quantity of organic carbon in marine sediments Can also assess biodiversity (as a co-benefit of macroalgae farms)	Sequencing primers are for specific groups of seaweed species (green, brown, and red); may require specialized design Does not account for carbon flows in the food web (i.e., consumed, then sunk to sediments)
	Sediment cores [15,17,45,57,127,129]	Enable calculation of total organic matter and organic carbon Have been used to quantify contributions of various blue carbon habitats	Variations along flow gradient due to current velocities and mixing Difficult to identify species unless coupled with other methods (e.g., eDNA, stable isotope signatures) Difficult to collect in deep water
	Isotopes [20,109,131]	Isotopic signature of macroalgae is preserved, such that flows can be traced through food webs to sediments	Usually cannot identify macroalgae compared to seagrasses or mangroves
Mesocosm experiments	Lateral carbon flows [113,180,181]	Applied for several species of cultivated kelp Enable assessment of the role of macroalgae in carbon cycling Correlated with net primary production, which represents carbon uptake	Inorganic carbon is fixed and released as DOC within hours, such that this method does very little to advance understanding of significant sequestration
	Degradation rates [114,118,119,182]	Calculated for several species of macroalgae Degraded DOC is itself a carbon pool	Vary seasonally Spatially dependent water flows determine permanence of carbon sink
Modeling	Distribution and possibilities [59,183,184,185,186]	Enable harvest biomass estimations (for carbon content or business purposes) Limited data collection required Can be used for siting plans	Species-specific, may also vary based on cultivation or natural forests May not consider true limiting factors—cost, nutrient availability, processing capabilities, future climate
	Allometric models [187,188]	Developed from limited field data Non-destructive biomass estimates	Species-specific relationship measurements
	Primary production via PhycoCanopy [111]	Enables exploration of parameter sensitivity Developed for canopy-forming macroalgae	Requires multiple data inputs and user experience with the tool
	Sinking [92,124,165,189]	Models have been developed specifically for cultivated macroalgae Leverage information on natural sinking and erosion Incorporate multiple phases in a cultivation cycle and end uses	Contains assumptions about conditions needed for permanence May exclude key environmental impacts

Acronyms used in table: dissolved inorganic carbon (DIC); dissolved organic carbon (DOC); environmental deoxyribonucleic acid (eDNA), quantitative polymerase chain reaction (qPCR); partial pressure of carbon dioxide (pCO₂).

provides a critical synthesis of the limitations of existing methods and the opportunities for application to assessment of cultivated macroalgae.

Numerous methods exist for measuring the carbon uptake in macroalgae, so the choice of tools for monitoring CDR at a farm depends more on costs, access, and harvest practices. Remote sensing via satellite or aerial vehicles has been used more for species identification or basic areal mapping [166,167,190,191,192,193], without taking a next step to carbon assessment, though estimations could be applied. This method could be expensive, if acquisition of a remotely operated or autonomous vehicle is needed, or inexpensive if publicly available satellite datasets are available and the expertise needed to extract relevant information is already developed. Physical sampling methods vary greatly in terms of cost and design to estimate carbon uptake, especially if underwater work is required at depth. However, for cultivated macroalgae, it is fairly easy to predict carbon content in a harvest based on modeled estimates of biomass, which can then be confirmed by weighing at harvest. The ratio of carbon content to wet weight is available for many species of macroalgae based on previous controlled experiments, and is around 30% (e.g., Laminaria hyperborea [126], Macrocystis pyrifera [194], Ecklonia radiata [88], Euchema spinosum [195]). Variability in species and the influence of environmental variables should also be taken into account [103,104,110,196,197].

Like other blue carbon habitats, macroalgae serve at least as a short-term CO₂ sink, fixing more carbon than is respired over a growing season [62]. However, for the carbon in macroalgae to be permanently sequestered, it must be exported to anaerobic sediments [198], calcified (corraline macroalgae only, [199]), sunk (either deliberately or naturally) [54,58,200], or converted to a long-lived carbon-containing product [54,201]. Many products can be made from harvested macroalgae, including biofuels, textiles, building materials, food, fertilizer, and more, but assessment of permanence requires consideration of the entire life cycle of the product and its carbon composition [56,202]. At present, the permanence of carbon in macroalgae is assessed by sampling sediments under macroalgae aquaculture farms to estimate the fraction of carbon exported to the deep sea [45], and emerging combination methods for eDNA and isotopic analyses are promising to trace carbon flows and estimate sequestration on the seafloor [20,23]. However, these methods only represent the carbon sequestered throughout the natural life cycle and exclude harvested product potential.

Comprehensive frameworks identified in the literature review attempt to assess the uptake and permanence of carbon in products and ecosystems, but they fall short in many cases. LCAs often define system boundaries to exclude end-of-life scenarios and are not designed to track carbon. As it is only one piece of a larger assessment, the carbon captured in macroalgae in the cultivation phase is represented simplistically, not clearly reported, or ignored on the assumption that all carbon captured will be released back into the atmosphere at the end of the product life [203,204]. Hasselström et al. [202] proposed a life cycle carbon accounting framework for seaweed that addresses some of these limitations in LCA, though they do not provide monitoring methods to accompany the outline. Quantifying ecosystem services includes an assessment or estimate of carbon uptake and permanence that relies on previously described methods (such as biogeochemical models of the ocean carbon cycle), combined with other factors like the social cost of carbon [205]. However, as the goal of an ecosystem services assessment is much broader than simply carbon accounting, other factors are considered more heavily. Macroalgae provide regulating services in removing both carbon and other excess nutrients from the water, with potential for permanent sequestration dependent on end uses, in addition to provisioning services when harvested for food [148,149,206]. The carbon accounting framework [150] was the only study from the literature review that presented a method for assessing carbon uptake and permanence in harvested biomass, including processing and end of life scenarios. However, this method would need to be adapted to be applicable for macroalgae, as the workflow is specific to timber processes and products, which are distinctly different. Forensic carbon accounting [151] is an approach that has recently been developed for natural seaweed beds and coastal aquaculture, though it has yet to be tested. The framework is most relevant for assessing natural ecosystems or cultivated macroalgae up to the point of harvest, but still fails to address the product carbon end-of-life scenarios, relying on LCA.

4.2. Methods for Valuing Temporary Storage

While permanent carbon removal is considered the highest value storage and durability is a key consideration in carbon credit markets [207], and is required for some corporate net-zero standards (e.g., [208]), many studies have highlighted the value of temporary carbon storage as it relates to mitigating climate impacts to increase the options available for offset purchases (e.g., [209,210,211,212,213,214,215]). This could be an excellent arena for cultivated macroalgae, considering the life span of macroalgae while they are growing at a farm, the fraction that has demonstrated permanent sequestration in export to deep sea sediments [45], and the carbon transformed into products following harvest. Blue carbon trading markets are still merely hypothetical [216], and understanding possibilities for a variety of sale methods and pricing structures will be needed to move toward the realities of adoption for cultivated macroalgae.

Ruseva et al. [209] synthesize how current carbon credit schemes deal with permanence and argue that permanence is less important than buying time, and temporary storage can still provide climate benefits. Coastal blue carbon is considered as an approach, though macroalgae are not discussed. They argue that governance frameworks are needed to incentivize the development of CDR methods, even those that are not permanent, to maximize overall carbon storage.

Matthews et al. [211] explore the climate effects of nature-based solutions (specifically, land-based storage due to reforestation). Through a modeling approach, they found that temporary carbon storage could decrease the magnitude of global temperature increases when deployed on a large enough scale (on the order of 10.4 Gt CO₂ per year) and coupled with ambitious emission reductions. This shows that carbon removal alone is not enough, but even semi-permanent approaches could add up to significant benefit.

In addition to modeling efforts like Matthews et al. [211], several methods for valuing temporary carbon storage have emerged in the literature. Ton-year accounting approaches (including Moura Costa [217] and Lashof [218]) calculate how many tons of CO₂ need to be stored in order to be equivalent to avoiding the emission in the first place, creating the unit of ton years to represent quantity and time [219]. Critiques of this method, in particular, of the Moura Costa approach [220] note that the climate benefit of temporary storage can be exaggerated or essentially the same as delayed emissions, contrary to supporting true removal of carbon that is required for climate benefits. Kim et al. [221] describe a function for a simple price discounting approach for impermanent land-based carbon credits compared to a “perfect offset”. The issuance of temporary [220] or rented [222] emissions credits has also been proposed for temporary carbon storage projects, though it is difficult to imagine this approach selected in the voluntary carbon markets that currently exist.

Both Jørgensen et al. [214] and Brandão et al. [215] discuss the possibility of accounting for temporary carbon storage in LCAs of products. While no conclusive recommendations have been made, both papers describe important considerations and possibilities for temporary storage to have measurable positive climate impacts. Jørgensen et al. [214] introduce the concept of the “climate tipping potential”, a modeling approach used to assess the potential of temporarily stored carbon in biopolymers to prevent or delay the crossing of a climate threshold (e.g., a certain amount of atmospheric CO₂ parts per million or a global temperature increase). This approach could likely be adapted from terrestrial biomass products to cultivated macroalgae products, as the duration of storage considered ranges from two years to 50 years.

In all of these options for valuing the temporary storage of carbon in macroalgae, it should be emphasized that temporary storage alone is not enough to mitigate the effects of climate change (e.g., [211,223]). Rapid decarbonization and emissions reductions are necessary alongside a variety of carbon removal methods to prevent further negative effects of global climate change due to decades of unchecked anthropogenic emissions. Realistic, rigorous assessment of the potential for macroalgae to contribute to either permanent or temporary carbon removals is needed to avoid the sale of questionable carbon credits that do not represent real outcomes.

4.3. Considering Non-Carbon Benefits of Macroalgae Aquaculture

While the carbon capture and sequestration potential of macroalgae is a key focus of this review, there are many additional benefits provided through cultivation that should be noted [49,224]. Macroalgae remove nitrogen and phosphorous from the water [46,49,101,225,226,227,228], provide habitat functions (even in cultivated longlines) [148,149,229], protect other cultivated or naturally occurring species from ocean acidification [230,231,232,233,234,235], and can generate valuable products that support coastal communities [152,236,237,238,239,240,241], including food [49,242,243], and could even have further carbon sequestration benefits (e.g., biochar as a soil amendment [244,245] or bioenergy with carbon capture and storage [246]). Switching from fishing pressure to macroalgae farming can help restore ecosystems, retain traditional values, and increase gender equity in the ocean food industry [247,248,249]. For example, a study in Maine found that non-fed aquaculture (such as seaweed or shellfish) was four times more accessible to women than the historically dominant lobster fishery, with women holding half of the Limited Purpose Aquaculture seaweed licenses [250].

In considering all of these benefits, it should be noted that environmental concerns remain around macroalgae aquaculture (e.g., impacts to existing habitats, nutrient removal, introduction of foreign or invasive species) [251,252,253,254], and still need to be addressed in assessments and permitting decisions in conjunction with local values and existing legal frameworks [255]. In some cases, monitoring carbon uptake and permanence at macroalgae farms could go together with monitoring additional environmental impacts or benefits. In particular, ecosystem services assessment is one way to identify and assess both the carbon value and these additional values (e.g., [146,148,149,205,256]). LCA can also be applied to assess additional impacts as well as benefits in the processing or product phases, for example, nitrogen and phosphorus are often already considered in metrics for eutrophication (e.g., [139,227,257]).

As a final note, several private companies already have efforts underway to explore the possibility of sinking large quantities of kelp or seaweeds for the purposes of carbon sequestration. Concerns about these efforts, such as negative effects on ecosystems [92,258,259] or significant remaining research gaps [165,260], suggest the need for pursuit of multiple, alternative pathways to permanent carbon sequestration. Sinking is just one of many uses for cultivated macroalgae, and many other products or uses could contribute to carbon removal efforts with additional co-benefits [261]. Simply restoring natural marine ecosystems is another approach to be explored, mirroring terrestrial restoration efforts that currently have MRV protocols and for which carbon credits can be issued. Long-lived products made from macroalgae, such as building materials, extracts like alginate that can be used in cement, and textiles could also sequester carbon on significantly permanent time scales [240,262,263], while generating profits. Considering the costs and feasibility of these options is an emerging area of research [68,264] that will become increasingly relevant in terms of voluntary or involuntary carbon markets. The further development of methodologies for assessing the potential of these alternative efforts is needed to minimize cost and maximize the overall value that can be gained from farming the ocean to remove CO_2, as part of global efforts to develop and deploy innovative climate solutions.

5. Conclusions

This review of 382 papers identifies methods for monitoring carbon uptake and permanence in various contexts and discusses the possible opportunities and limitations as applied to cultivated macroalgae. Monitoring carbon uptake is necessary to understand the quantity of carbon removed from the marine environment, while monitoring carbon permanence is needed to understand the duration of the carbon removed to assess the resulting effect on the global carbon cycle and ultimately climate change mitigation. While numerous methods exist and are utilized to measure carbon in the ocean and on land, the research community has yet to coalesce around a unified approach or set of methods. There is a clear need to continue to pursue and test novel methods of tracing the flow of carbon in macroalgae systems, learn from other contexts, combine multiple methods, and leverage existing frameworks and tools to move toward a comprehensive understanding. In particular, methods to assess the permanence of carbon in the natural life cycle of macroalgae and the permanence in products following harvest need to be more fully developed.

While it is clearly documented that macroalgae have many co-benefits in addition to carbon sequestration, this review reveals that there are many unknowns when it comes to assessing the permanence or climate mitigation potential of the captured carbon. Until the carbon sequestration potential of cultivated macroalgae is fully documented and verified, the research community would be remiss to promise climate benefits or sell carbon credits with wishful thinking at best and duplicity at worst. As this is an active area of research, with many high-profile organizations involved globally, it will be important to realistically assess the carbon benefits from macroalgae cultivation to maintain accountability and comparability with other CDR methods. The full benefits of macroalgae cultivation as an effective climate solution will only be achieved through collaborative research between private industry, governments, and academia to develop monitoring, reporting, and verification standards in addition to thorough methods for realistically assessing carbon uptake and permanence.