Reply to the comment by Filbee-Dexter et al. (2023) “Seaweed forests are carbon sinks that may help mitigate CO₂ emissions” Open Access

Abstract

Filbee-Dexter et al. provided commentary on Gallagher et al.’s assertion regarding the limitations of seaweed ecosystems in mitigating CO₂ emissions. However, Filbee-Dexter et al. appear to have different understandings of several key aspects, and claims of heterotrophic bias contradict their cited literature upon which our analysis was based. Filbee-Dexter et al.’s reliance on net primary production fails to consider the consumption and remineralization of said production. Their endorsements of high levels of seaweed ecosystem autotrophy taken from the literature were either conceptually, temporally, or community assemblage-inappropriate. The existing literature does not substantiate their claim of methodological bias between different types of net ecosystem production (NEP) measurements. Additionally, all of these direct measurements account for any photo-re-assimilation of respiratory subsidies. Contrary to Filbee-Dexter et al.’s claim, Gallagher et al. consider the export of sequestered seaweed. The study revealed that respiratory subsidies offset the exported sequestration rates from an average of +173 million tonnes C yr⁻¹ as a carbon sink to a carbon source of around −54 million tonnes C yr⁻¹. Nonetheless, there are also points of consensus. It will be necessary to weight NEP for the types of seaweed ecosystems, and account for differences with a seaweeds’ particular degraded or alternative state as more data becomes available. Finally, more research is required to better understand the fate of export, and the impact of net calcification on the atmospheric exchange of CO₂.

Introduction

Since S. V. Smith's seminal article in 1981, there has been a recognition of the potential importance of natural seaweed ecosystems in marine carbon sequestration (Gallagher, 2014, 2015; Krause-Jensen and Duarte, 2016; Filbee-Dexter and Wernberg, 2020). The rationale for this claim is the large amount of seaweed detritus exported from the deep ocean and coastal sediments. The amount of this sequestered export depended on the amount of seaweed net primary production (NPP) that survived consumption and remineralization within the ecosystem, as well as the amount of export that survived consumption and/or degradation outside the ecosystem (Gallagher, 2015; Krause-Jensen and Duarte, 2016). However, this departure from the established primacy of net ecosystem production (NEP; Chapin et al., 2006) in favour of NPP as the predictor variable is applicable solely to ecosystems that are isolated from organic imports. In such cases, NEP is considered equivalent to the amount exported from the ecosystem [Figure 1a and equations (1) and (2), see Gallagher et al., 2022]. Sequestration then becomes a measure of how much of that NEP is counterbalanced by the export consumed, prior to reaching the deep ocean and coastal sediments.

Similar to coastal wetlands, seaweed ecosystems, however, are not isolated from inputs of allochthonous organic carbon (Zuercher and Galloway, 2019). Unlike coastal wetlands, the majority of allochthonous organic carbon in seaweed ecosystems is supplied by adjacent coastal waters in the form of phytoplankton, holoplankton, and meroplankton. This organic carbon is then consumed and respired by the seaweed ecosystems’ heterotrophic community (Schaal et al., 2009; Zuercher and Galloway, 2019). As a consequence, NEP is no longer equivalent to the amount of export [equation (3), Gallagher et al., 2022]. As the allochthonous carbon is consumed, these respiratory subsidies offset the NEP from an autochthonous standpoint, and thereby reduce the biologically mediated CO₂ air–sea flux over the canopy (Smith, 1985). In many cases, this offset turns the water columns’ dissolved inorganic carbon (DIC) deficit from an atmospheric sink (+NEP) to a source (−NEP). Furthermore, Gallagher et al. (2022) calculated that on average, these respiratory subsidy offsets surpass the amount of export sequestered in the deep ocean and coastal sediments. As a result, seaweed ecosystems are more likely to function as a large carbon source, estimated at −54 million tonnes yr⁻¹, rather than a large carbon sink of +173 million tonnes (Krause-Jensen and Duarte, 2016). Nonetheless, to assess the capacity of seaweed ecosystems to mitigate CO₂ emissions, it is essential to consider the carbon dynamics of anthropogenically degraded seaweed ecosystems or their alternative states. Alternative states have the potential to function as larger carbon sources or smaller carbon sinks (Gallagher et al., 2022).

Given the previous findings of Krause-Jensen and Duarte (2016), the re-evaluation of seaweed ecosystem sequestration by Gallagher et al. (2022) has been met with some surprise. The commentary by Filbee-Dexter et al. (2023) thus presents a useful occasion to address various concerns and examine how seaweed ecosystems are best positioned to offset carbon emissions. I delve into Filbee-Dexter et al.’s (2023) major points in support of a carbon sink and their secondary critiques of existing concepts. Moreover, I also identify areas of agreement and propose that by integrating elements from both the NPP and NEP paradigms, we can achieve a higher level of predictability for sequestration and mitigation. This, in turn, will instill confidence in those estimates for future investments in seaweed preservation, restoration, and aquaculture.

Conflating different seaweeds obscures the “evidence” that seaweed forests are autotrophic?

Bias from not weighting for different types of seaweed ecosystems?

According to Filbee-Dexter et al. (2023), the average global NEP reported by Gallagher et al. (2022) exhibits a heterotrophic bias because it does not account for the area of highly productive kelp forests. While the need for sampling stratification and weighting is accepted, our data and classification suggest that such a weighting would produce a more heterotrophic global average (Table 1, see Gallagher et al., 2022). Filbee-Dexter et al.’s (2023) inclusion of the autotrophic Fucus wracks with kelp forests is misleading. Unlike many kelp systems, Fucus wracks are restricted to sheltered intertidal waters of the temperate northern hemisphere. Such sheltered sites can be expected to receive a reduced supply of allochthonous carbon subsidies (Schaal et al., 2009) to offset autotrophy, as well as a smaller fraction of their NPP exported to deeper waters and coastal sediments. Nor does citing >100 examples of kelp forest NPP estimates (Duarte et al., 2022; Pessarrodona et al., 2022) support their claim of a greater global average NEP than the dataset of Gallagher et al. (2022) suggests. Regardless of respiratory subsidies, the NPP solely represents the difference between the rate of carbon fixation (gross primary production) and the respiration required for seaweed metabolism. Consequently, NPP does not measure the ecosystems’ DIC deficit. That is to say, NPP does not consider the CO₂ respired when seaweed is consumed by the ecosystems’ fauna and microflora (average of 33.6–37.3%, respectively; Duarte and Cebrián, 1996).

The basis behind Filbee-Dexter et al. (2023) equating seaweeds’ higher NPP with greater NEP, as the water columns’ DIC deficit remains unclear. It is possible that this conflation stems from a notion that the amount of seaweed consumed does not increase in proportion to its NPP. However, this is not the case, because consumption of seaweed increases in direct proportion to NPP (Cebrián, 2002). Nor does NPP account for further autotrophic offsets from respiratory subsidies. Moreover, the amount of allochthonous carbon consumption appears to be independent of a seaweed ecosystem’s NPP. For example, Schaal et al. (2009) found that consumption of allochthonous organic carbon appeared to be greater in less sheltered habitats for the same species of kelp and across the same area. Indeed, open-water kelp ecosystems have been found to be heterotrophic (Table 1, see Gallagher et al., 2022). This not only demonstrates the fallacy of conflating high seaweed NPP with NEP but also the fallacy of solely stratifying examples from other less productive smaller, canopy ecosystems, when based on NPP. Nonetheless, as more NEP data becomes available for all seaweed ecosystems, it may be necessary to incorporate some form of weighting to establish a representative global average.

Bias from calcification?

Filbee-Dexter et al. (2023) raised the issue of an overabundance of calcifying seaweeds in the dataset of Gallagher et al. (2022). However, the underlying assertion behind this statement suggests that not accounting for calcification will either overestimate those autotrophic seaweed ecosystems as a global carbon sink or underestimate those heterotrophic seaweed ecosystems as a global carbon source (Bach et al., 2021). This contradicts Filbee-Dexter et al.’s (2023) thesis that Gallagher et al. (2022) underestimated the ability of seaweed ecosystems to sequester atmospheric CO₂. Nonetheless, it is important to note that NEP estimates for calcifying seaweed ecosystems as reported by Gallagher et al. (2022) were based on organic metabolism. Corrections had been made in the cited articles for changes in DIC due to calcification, and changes in oxygen concentration were converted by Gallagher et al. (2022) to metabolic carbon equivalents. Nonetheless, the need for further research on seaweed calcification is acknowledged and must also include calcification rates from the ecosystems’ benthic and epibiont faunal communities. Either way, two questions remain unanswered. First, what is the amount of CO₂ generated from the balance between calcareous production and dissolution in seawater (Gattuso et al., 1997)? Second, how much of this CO₂ from calcification is supplied to NPP, and what impact does it have on the CO₂ air–sea flux (Smith and Veeh, 1989)?

Is it well established that seaweed ecosystems are autotrophic?

Filbee-Dexter et al. (2023) claim that all seaweed ecosystems are widely recognized as autotrophic, which is clearly not the case (Table 1, see Gallagher et al., 2022). This appears to be based on their reliance on studies that consider only seaweed production, consumption, and export (Smith, 1981; Duarte and Cebrián, 1996; Duarte and Agusti, 1998; Gattuso et al., 1998; Duarte et al., 2005). In other words, interpretation is predicated on ecosystems closed to external inputs. Adopting such a limited conceptual model would inevitably lead to ecosystems that function as carbon sinks. In the best-case scenario, an ecosystem without organic inputs may only achieve carbon neutrality by assuming an improbable 100% efficiency in the consumption and remineralization of seaweed production. In reality, inputs play an integral role in the form and function of aquatic ecosystems. Inputs facilitate new production through light and dissolved nutrients (Dugdale and Goering, 1967) and enhance rates of secondary and tertiary production through the supply of allochthonous organic carbon (Pace et al., 2007; Scharnweber et al., 2014). Consequently, numerous studies have demonstrated the prevalence of heterotrophy in lakes, wetlands, and coastal waters because of respiratory subsidies from consumption and remineralization of allochthonous organic carbon (Duarte and Prairie, 2005; Duarte et al., 2013; Gounand et al., 2018). Seaweed ecosystems are not exempt from such inputs. The notable difference being that respiratory subsides come mostly from adjacent coastal waters, rather than rivers (Schaal et al., 2009; Zuercher and Galloway, 2019).

Uncertain, incomplete, and supposedly biased NEP data?

Filbee-Dexter et al. (2023) suggested that Gallagher et al.’s (2022) dataset contained an indeterminate level of heterotrophic bias and considerable variability. In support of their argument, they (1) present additional NPP data, seemingly as a proxy for the biological water column DIC deficit; (2) cite additional, but questionable, NEP data; and (3) point to sampling periods that are not representative of annual changes, irrespective of whether these periods would under or overestimate annual NEP rates.

Additional NPP data

Filbee-Dexter et al. (2023) suggested that additional support for highly autotrophic examples can be found in a recent compilation of seaweed NPP estimates (Duarte et al., 2022). However, it is crucial to emphasize that this assertion overlooks the fundamental distinctions between NPP and NEP (see section “Bias from not weighting different types of seaweed ecosystems”).

Additional NEP data to support seaweed ecosystem autotrophy?

It is important to note that Gallagher et al. (2022) obtained the NEP values through a systematic literature search. Each article underwent careful evaluation prior to selection. The selection criteria required articles reporting an appropriate concept for a DIC deficit or surplus (i.e. NEP, the result of organic metabolism), an appropriate ecosystem assemblage (i.e. algal, epibiont, and benthic communities), and more than one diurnal experiment across a season or year. Gallagher et al. (2022) had already applied the same criteria to the articles cited by Filbee-Dexter et al. (2023) and deemed them inappropriate. In the following sections, I will address each of those citations by first summarizing their limitations, followed by providing explanations for the reasons behind them.

Citation (Watanabe et al., 2020)

NCP measurements were limited to the seaweed thallus and its epibiont community.

The NEP values reported for Sargassum spp. by Watanabe et al. (2020; 302–1378 mmol C m⁻² day⁻¹) overstate their role as a large annual carbon sink from two standpoints. First, measurements were taken during only the spring growing period. Second, measurements were confined to bags that only enclosed the Sargassum thallus, disregarding the respiratory contributions from benthic faunal and microfloral assemblages. As a result, the reported NEP values are more indicative of NPP for a thallus relatively free of epibionts. Furthermore, these high NEP values starkly contrast with a recent study that had examined two holdfast Sargassum sp habitats from the same region and over the same growing period (Sato et al., 2022). This study reported NEP values from water column oxygen mass balances of only −9.36 mmol C m⁻² day⁻¹ and +9.36 mmol C m⁻² day⁻¹ when normalized to average depths reported by Watanabe et al. (2020). Sato et al.’s (2022) NEP estimates also fall within the quartile ranges of the compiled dataset in Figure 2 of Gallagher et al. (2022) and do not alter the overall picture of a heterotrophic global average NEP.

Citations (Delille et al., 2000, 2009; Ikawa and Oechel, 2015)

The experiments performed by Delille et al. (2000) were limited to the daytime and did not report the DIC deficit as NEP. Delille et al. (2009) reported one NEP measurement at maximum solar radiation. Ikawa and Oechel (2015) did not report NEP measurements but instead focused on atmospheric flux far from the kelp forest. Their arguments lacked conviction due to questionable correlations with inappropriate DIC deficit concepts within the kelp forest and a few flux measurements over another kelp forest during the daytime.

Delille et al. (2000) only sampled surface waters once a day in the early afternoon to report pCO₂ levels below saturation within a kelp forest, rather than NEP. Such limited daytime sampling greatly overestimates the average diurnal pCO₂ deficit (Honkanen et al., 2021) and cannot be used in isolation to estimate the NEP rates (Lockwood et al., 2012). In contrast, Delille et al. (2009) did account for diurnal cycles in pCO₂ but only reported one value for a NEP when solar radiation was at its peak, by assuming minimal atmospheric exchange.

The study conducted by Ikawa and Oechel (2015) off the California coast (USA) utilized atmospheric eddy covariance. However, Ikawa and Oechel (2015) did not report NEP but direct measurements of CO₂ atmospheric flux. This contrasts with the assumption made by Delille et al. (2009) of a kelp ecosystem in equilibrium with the atmosphere. Moreover, measurements were taken over a nonvegetated coastal site, which Ikawa and Oechel (2015) claimed represented the CO₂ dynamics of the kelp forest 1.5 km away. However, their arguments behind this claim was not justified. First, the correlation they observed between an increasing CO₂ flux and subsequent increases in kelp area and the kelp NPP was only valid for the following year. Second, it is not NPP but NEP that serves as a measure of the water columns’ DIC deficit, which drives the biologically mediated CO₂ air–sea flux (Lockwood et al., 2012). Lastly, Ikawa and Oechel (2015) reference a few similar atmospheric flux measurements, taken from a boat over a larger kelp forest located >19 km away. However, these measurements were obtained over a limited number of summer and spring days, and only during daylight hours. As a result, this dataset would overestimate the annual average atmospheric flux of CO₂. Such findings could equally suggest that the eddy covariance site may have been a larger carbon sink than a kelp forest from this area.

Citations (Duarte and Cebrián, 1996; Duarte and Agusti, 1998; Duarte et al., 2005)

They reported only the fraction of seaweed NPP that was not consumed within the ecosystem. Duarte et al. (2005) reported an average NEP for only seaweed production and consumption. Duarte and Agusti (1998) reported NEP integrated across all coastal water habitats.

It is important to note that Duarte and Cebrián (1996) did not claim that the average carbon balance between autotrophic production and consumption for marine macroalgae across the globe was synonymous with NEP. Such a statement was made by Duarte et al. (2005) after reworking the data from Duarte and Cebrián (1996) (Table 2 in Duarte et al., 2005). As mentioned earlier, this type of bottom-up reconstruction of NEP does not consider respiratory offsets by the consumption and remineralization of organic subsidies. It is possible that this statement of a global average NEP is the origin of the contention that all seaweed ecosystems around the world are autotrophic. It is certainly not from Filbee-Dexter et al.’s (2023) referral to Duarte and Agusti (1998), as the article deals with coastal ecosystems as a whole, and are not sub-categorized. Consequently, it is not possible to estimate the extent to which subsidies have offset or failed to offset global seaweed autotrophy.

The dataset contained ecosystem seasonal bias?

It is agreed that increasing the number of NEP examples for seaweed ecosystems worldwide can enhance representative sampling, reducing bias by improving estimates of both the global population mean and variance. Although, it was not made clear what would be the minimal number of samples required to represent the population mean, given that the population number and variance are unknown. Nevertheless, what we can say is that our NEP dataset was not overtly biased by latitude, genera, or continent (Table 1, see Gallagher et al., 2022). Moreover, the inclusion of NEP data from a more recent publication on two Japanese Sargassum spp. forests (Sato et al., 2022) adds another region to the dataset and further supports a global heterotrophic mean (see section “Additional NEP data to support seaweed ecosystem autotrophy”).

Filbee-Dexter et al. (2023) expressed concerns about potential heterotrophic bias resulting from seasonal studies being included in the dataset. As noted by Gallagher et al. (2022), their inclusion was unlikely to have led to any overt global heterotrophic bias. The data from the short polar summer example would greatly underestimate the annual NEP due to long polar winters characterized by a low light regime, enhanced by ice and snow cover. On the other hand, the temperate to late spring examples, when considered separately, could moderately underestimate the annual NEP. Nonetheless, when taken together, they more closely balance the overestimation of annual polar NEP.

No consideration of the complete algal assemblage carbon balance?

Filbee-Dexter et al.’s (2023) claim that Gallagher et al. (2022) did not consider phytoplankton production and consumption in seaweed ecosystems is incorrect. The NEP measurement methods employed in the data compilation capture the phytoplankton and seaweed assemblages in the water column, as re-emphasized by Gallagher and Shelamoff (2022), including data from Miller et al. (2011).

Methodological bias?

Like many methods in environmental science, pragmatic choices made in real time in the field may introduce biases. These biases are typically considered unimportant or overshadowed by measurement variability. They have been consistently addressed through the convergence of different independent methods, each with its own biases (Bycroft, 2010). Furthermore, the studies cited by Filbee-Dexter et al. (2023), Champenois and Borges (2012), and Olivé et al. (2015) as evidence of methodological bias, in actuality, support convergence between methods because they show no significant diurnal dependence.

“Monthly averages of GPP and CR based on the open water mass balance approach compared well in terms of intensity and seasonality with the GPP and CR values derived from incubations in benthic chambers.” (Champenois and Borges, 2012, where GPP is the gross primary production of the seagrass ecosystem assemblage and CR is the ecosystem’s community respiration)

“Metabolic budgets obtained in this work for 12 and 24 h agreed well with literature values while those obtained with shorter incubations (1.5–2 h) were always clearly higher ….” (Olivé et al., 2015)

Additionally, contrary to the assertions of Filbee-Dexter et al. (2023), Miller et al. (2011) explicitly state that they did not measure night-time metabolism, while Champenois and Borges (2012) and Olivé et al. (2015) demonstrated that seagrass had higher respiration during the day than at night and that benthic chamber measurements of NEP converged with open water mass balance approaches. Furthermore, it is important to note that the studies of Rodgers and Shears (2016) and White et al. (2021), cited by Filbee-Dexter et al. (2023), as examples of benthic chamber methodological bias, conflate NPP with NEP. Net primary production measurements cannot account for any changes in benthic and epibiont community night-time respiration. In fact, Filbee-Dexter and those co-authors, who contributed to Pessarrodona et al. (2022), point to an agreement between benthic chamber NPP measurements and increases in seaweed biomass outside the chamber. This observation further supports the use of benthic chambers as a robust means to study seaweed productivity, if not the complete ecosystem carbon balance.

NEP from Gallagher et al. (2022) cannot resolve a global average level of heterotrophy?

The rationale for Filbee-Dexter et al.’s (2023) comparison of the mean and variability of our NEP dataset to an arbitrary mean of zero, implying some kind of heterotrophic sample bias, was unclear. By the same token, our average NEP and variance could be compared to a heterotrophic population mean, which would be equally arbitrary. Whether the global average seaweed system is heterotrophic or autotrophic is irrelevant. It is possible that Filbee-Dexter et al. (2023) misunderstood the question addressed in our study. As outlined above, the first question is how much respiratory subsidies have offset ecosystem autotrophy. In many cases, the existence of an offset was directly apparent by measurable levels of heterotrophy and values close to carbon neutrality. However, this does not mean that measurably autotrophic systems (+NEP) had not been offset by respiratory subsidies. The second question examines how these autotrophic offsets impact the sequestration of seaweed that survives consumption before being stored in the deep ocean and coastal sediments (Figure 1b, see Gallagher et al., 2022).

To address the first question, a statistically more meaningful test is to determine whether respiratory subsidies significantly offset the seaweed ecosystems’ autotrophy. This can be achieved by comparing the global mean and variability of our directly measured NEP dataset (−4.02 mmol C m⁻² day⁻¹, SD = 57.8 mmol C m⁻² day⁻¹, n = 18)—which includes offsets for any respiratory subsidies—with a global mean NEP that only considers the production and consumption of seaweeds within their ecosystem. Such a global mean was calculated by Duarte et al. (2005; 393 mmol C m⁻² day⁻¹). Not only is this NEP two orders of magnitude greater than the mean of our dataset, but the difference was highly significant [p (same) = 9.4 × 10⁻¹⁷, Students'onesample t-test]. Moreover, the sample mean estimated by Duarte et al. (2005) would need to exhibit an egregious level of bias of an order of magnitude smaller to demonstrate no statistical difference with our dataset [21.7 mmol C m⁻² day⁻¹; p (same) > 0.05]. Conversely, our datasets’ variability would need to be more than a magnitude larger. Indeed, Filbee-Dexter et al. (2023) seem to imply that we should have pooled the within-site variability. However, that would represent pseudo-replication (Hurlbert, 1984). This point was seemingly recognized by Filbee-Dexter et al. (2023) in their recent work (Duarte et al., 2022) in which they compiled and compared only the seascape means of seaweed ecosystems’ NPP from across the globe.

Climate-change mitigation depends on the net change in greenhouse gases, carbon sequestration, and CO₂ emissions?

Differences in NEP between seaweeds and their degraded or replacement states

A notable area of agreement was the concept of mitigation potential, which refers to the disparity in carbon balances between a degraded state and its alternative parental seaweed ecosystem. Indeed, this comparison is used in coastal wetland abatement methodologies (Lovelock and Duarte, 2019; Gallagher, 2022). Gallagher et al. (2022) cautioned against drawing robust conclusions given the small amount of data available and mixed results. Filbee-Dexter et al. (2023), however, expressed a more decisive viewpoint. They contended that seaweed ecosystems will always be more autotrophic or indeed less heterotrophic than their replacement states. This claim was based on the supposition and inclusion of additional data on respiration from an urchin population within a degraded state, and the possibility this could invert the carbon balances relative to the alternative seaweed-dominated state. However, these additional cited data from Peleg et al. (2020) had already been considered during our literature search and deemed unreliable for inclusion due to the following reasons.

Peleg et al. (2020) conducted a comparison between the NEP of a seaweed forest ecosystem and a turf and shrub ecosystem. However, the experiment was representative of only one day. This period was considered by Gallagher et al. (2022) as a marginal choice to have been included in our dataset as seaweed ecosystems vary between autotrophy to heterotrophy on a daily basis (Sato et al., 2022). Moreover, in their 1-h benthic chamber experiment conducted over noon, Peleg et al. (2020) implicitly assumed that respiratory parameters remain constant throughout the day and night. This disregards some of the earlier concerns raised by Filbee-Dexter et al. (2023). Nonetheless, the study did suggest that seaweed forests over this 1 day were more autotrophic than turf or “shrub” ecosystems. It would then seem worthy to extend the duration of the study to confirm what was considered the potential of ecosystem state shifts to invert the carbon balance.

A minor role of respiratory subsidies on the seaweed ecosystem and global carbon balance?

Filbee-Dexter et al. (2023) contend that respiratory subsidies play only a minor role in the mitigation of CO₂ emissions by seaweed ecosystems. They arguments appeared to be based on the uncertainty of how much of the CO₂ produced from respiratory subsidies is re-assimilated by the seaweed assemblage and its degraded or alternative ecosystem algal assemblage. I agree that the amount of CO₂ re-assimilated from both autotrophic and allochthonous organic remineralization is largely unknown. However, Filbee-Dexter et al.’s (2023) concerns are based on conflating direct measurements of NEP with a bottom-up reconstruction of individual vectors across the production and consumption cycles. In other words, direct measurements of NEP are the result of the balance across the production and consumption cycles, including any photo-re-assimilation of respiratory CO₂. Consequently, measurements of NEP are considered a reliable concept to determine CO₂ atmospheric exchange (Lockwood et al., 2012). Moreover, evidence of the importance of respiratory subsidies to the seaweeds’ water column DIC deficit is reflected in the measurements of extensive NEP offsets [see section “NEP from Gallagher et al. (2022) cannot resolve a global average level of heterotrophy?”]. If Filbee-Dexter et al. (2023), however, are suggesting that the respiratory subsidies do not play a role in mitigation services between a seaweed ecosystem and its degraded or alternative state, then they may have misconstrued the distinction between supply and consumption. Specifically, the rate of allochthonous subsidy supply would remain unchanged, barring a possible reduction due to canopy dampening of tidal and wind-driven currents. However, the proportion of this input consumed would likely vary due to differences in benthic and epibiont community biomass and composition.

Filbee-Dexter et al. (2023) suggested that our article did not account for the exported detritus sequestered in the deep ocean. However, I would like to clarify that this was not the case. We did provide a clear illustration of this inclusion in Figure 1b (Gallagher et al. 2022), supported by a set of arithmetic equations and substitutions [equations (1)–(3), see Gallagher et al., 2022]. The only difference between the two conceptual models is an additional vector, namely, emissions of CO₂ from respiratory subsidies. As we noted earlier, the NPP paradigm already incorporates the NEP concept as equivalent to the amount of export before it is consumed and/or degraded prior to sequestration. The difference between the two conceptual models is in the manner in which sequestration is estimated. The NPP paradigm measures the export of seaweed detritus to the deep ocean and coastal sediments. Whereas, a more complete conceptual model requires both the NEP, the amount of seaweed detritus exported from the ecosystem, and how much of that export finds itself in the deep ocean and coastal sediments [equations (3)–(4), Gallagher et al., 2022]. Nonetheless, it is acknowledged that more research is necessary on a case-by-case basis to determine the fraction of NPP exported and the corresponding fraction sequestered (Krause-Jensen and Duarte, 2016; Pedersen et al., 2020; Smale et al., 2021).

Conclusions

The comment by Filbee-Dexter et al. (2023) encapsulates the struggle to separate the rapid growth of seaweed from the inability of the ecosystem to effectively sequester carbon. However, it is not about how fast seaweed can grow (i.e. the NPP) or whether the ecosystem is autotrophic or heterotrophic per se. Instead, it revolves around finding a balance between the amount of seaweed stored in the deep ocean and buried in coastal sediments and the extent to which this storage is offset by respiratory subsidies.

While Filbee-Dexter et al. (2023) did not make a case for the inaccuracy of our dataset and conclusions, nonetheless, there were areas of consensus. First, there is a need for more data on NEP, for both degraded states and their parental seaweed ecosystems. This is to better estimate carbon mitigation services. Second, there may be a need to eventually stratify NEP for different types of seaweed ecosystems and weight for their areas to obtain a representative global mean. Third, more data are required on a how the amount of seaweed exported and sequestered on a case-by-case basis (Pedersen et al., 2020; Smale et al., 2021). Fourth, there might be a need to consider measurements for autotrophic offsets resulting from the balance between calcareous dissolution and production. However, if this can only be achieved from gravimetric increases in net calcification (Bach et al., 2021), then this must be tempered by an understanding of how much of that DIC is recycled into algal productivity and how much is available for atmospheric exchange (Smith and Veeh, 1989).

Only by considering the above factors collectively can we achieve a balance between simplicity and latent power to enable predictions across a wider range of circumstances (Fagerström, 1987, p. 260). This will enable investors to maximize the potential of CO₂ mitigation services and inform the identification of natural hotspots for preservation, restoration, and the application of seaweed aquaculture.

Author contributions

JBG: conceptualization and writing—original draft preparation.

Conflict of interest

The authors have no conflicts of interest to declare.

References