Seaweed forests are carbon sinks that may help mitigate CO 2 emissions: a comment on Gallagher et al. (2022)

Recently, Gallagher et al. (2022) suggested that seaweed ecosystems are net heterotrophic carbon sources due to CO 2 released from the consumption of external subsidies. Here we outline several flaws in their argument, which we believe confuse research on the blue carbon potential of seaweed ecosystems, and unjustifiably generate doubt around initiatives to protect and restore seaweed forests. Gallagher et al. ’s evidence relies on 18 studies with highly variable measures of net ecosystem production, which do not statistically support their conclusion that most seaweed ecosystems are heterotrophic. This dataset is also inappropriate as it is incomplete and misrepresents seaweed ecosystems globally, particularly seaweed forests, which contribute disproportionately to global seaweed productivity. We maintain that the climate change mitigation value of an ecosystem depends on the net difference in CO 2 uptake between the original ecosystem and its replacement ecosystem. We provide evidence that most seaweed ecosystems, which drawdown the largest carbon flux of any vegetated coastal habitat, are indeed net autotrophic ecosystems. We recognize that substantial uncertainties remain concerning the magnitude of CO 2 drawdown by seaweed ecosystems and recommend that carbon fluxes around seaweed ecosystems should be considered more broadly and taken into account in estimates of their CO 2 mitigation potential.


Main text
The paper-seaweed ecosystems may not mitigate CO 2 emissions (Gallagher et al., 2022)-claims that seaweed ecosystems could be carbon sources rather than carbon sinks because "respiration subsidies" (from inputs of allochthonous organic carbon) create negative net ecosystem production (NEP).This implies that seaweed ecosystems produce more CO 2 than they drawdown, and thus may not mitigate CO 2 emissions.Gallagher et al. (2022) draw this inference from a compiled dataset that shows that, on average, seaweed ecosystems are net heterotrophic.Here, we discuss four flaws in the study presented by Gallagher et al. (2022) which we believe confuse research on the CO 2 mitigation potential of seaweed ecosystems, and unjustifiably seed doubt around motivations and initiatives to protect and restore seaweed forests to deliver climate benefits.
(1) The dataset assembled by Gallagher et al. (2022) conflates vastly different seaweed ecosystems, many of which play a minor role in global seaweed carbon cycling.The average NEP they present is, therefore, not representative of seaweed ecosystems in general or seaweed forests (e.g.kelp forests) in particular, which dominate both global seaweed productivity and the current scientific discussion on the CO 2 mitigation po-tential of seaweed ecosystems.Indeed, a regrouping of Gallagher et al.'s data into seaweed forests and other seaweed ecosystems suggests that seaweed forests may in fact be net autotrophic.
(2) Gallagher et al. (2022) present a limited data compilation that shows large variability in both NEP measures from individual studies as well as in the overall mean NEP.This negates the statistical basis of the argument.(3) Gallagher et al.'s dataset repurposes studies that are not appropriate for measuring carbon sequestration in coastal ecosystems.This biases their data compilation towards heterotrophy.(4) Gallagher et al. (2022) misrepresent the CO 2 mitigation potential of an ecosystem.It is not, as they claim, whether the ecosystem is autotrophic or heterotrophic per se.Rather, it is the effect of losses or gains of the ecosystem on net CO 2 emissions, including long-term carbon storage beyond the ecosystem, that determines the mitigation potential.
Below, we discuss each of these four elements.We highlight additional evidence that most seaweed forests are indeed net autotrophic, and we explore how to best incorporate community respiration components into seaweed carbon sequestration estimates.We also reinforce that Gallagher et al.'s assess-ment of the climate change mitigation potential of seaweed ecosystems does not fully consider changes in CO 2 emissions when replacing seaweed forests with other ecosystems, which is critical to assessing the role of seaweed ecosystems in mitigating CO 2 emissions.

Conflating vastly different seaweed ecosystems obscures evidence that seaweed forests are autotrophic
Gallagher et al.'s dataset does not reflect known patterns of relative seaweed abundance and associated carbon fluxes, nor does it capture natural variation adequately.The global extent and carbon fluxes of seaweed ecosystems are overwhelmingly dominated by seaweed forests (Mann, 1973;Wernberg et al., 2019), which contribute disproportionately to ecosystem net primary productivity (Newell et al., 1982;Tait and Schiel, 2013).The dominant role of seaweed forests for total global seaweed productivity is also emphasized by recent global assessments (Duarte et al., 2022;Pessarrodona et al., 2022), which were not available at the time Gallagher et al. (2022) published their paper.Globally, seaweed forests (primarily composed of species belonging to the orders Laminariales and Fucales; sensu Fraser, 2012;Wernberg and Filbee-Dexter, 2019) drawdown >70% of the carbon assimilated by all seaweeds, making them by far the most productive vegetated ecosystem in the coastal ocean (Duarte et al., 2022).Yet, over half of the NEP measures used by Gallagher et al. (2022) are from ecosystems that are fundamentally different from seaweed forests and, in some cases, represent the replacement ecosystems when seaweed forests are lost (e.g.Peleg et al., 2020).These include sea urchin barrens, turf reefs, red algal reefs, and intertidal seaweed turfs (Gattuso et al., 1997;Bensoussan and Gattuso, 2007;Miller et al., 2009;Gruber et al., 2017;Rovelli et al., 2019), all of which are effectively missing a productive canopy component.Gallagher et al.'s dataset also includes a synthetic community installed in an artificial "ocean" in the Arizona desert (Falter et al., 2001).Whilst calcifying algae are only estimated to draw ∼5% of the carbon assimilated by seaweeds globally (Duarte et al., 2022), >20% of the studies in Gallagher et al.'s dataset contain estimates from this group (Bensoussan and Gattuso, 2007;Attard et al., 2014;Roth et al., 2019;Rovelli et al., 2019).The inappropriate representation of global seaweed ecosystems in Gallagher et al.'s compilation (n = 18) obscures the dominant feature (i.e.seaweed forests) of global seaweed carbon cycling and sequestration.The suggestion that seaweed ecosystems as a whole are net heterotrophic counters long-established knowledge, based on the fate of their net primary production, community metabolism, and export fluxes (Smith, 1981;Duarte and Cebrián, 1996;Gattuso et al., 1998).Indeed, when the studies complied by Gallagher et al. (2022) are divided into seaweed forests versus replacement ecosystems, it supports the notion that seaweed forests are net autotrophic (Table 1).

The NEP calculations are based on uncertain, incomplete, and biassed data
Gallagher et al.'s dataset (n = 18 total) does not hold much value as a global estimate of the NEP of seaweed ecosystems as the search criteria or data selection decisions taken by the authors seems to have failed to capture much of the literature on macroalgal carbon metabolism.For instance, a re-cent compilation of primary production studies in seaweed ecosystems reports that >100 studies used benthic chambers (Pessarrodona et al., 2022), many of which used similar methods as the ones used by Gallagher et al. (2020) to estimate NEP (in situ incubations measuring oxygen or carbon fluxes on reefs).Importantly, Gallagher et al. (2020) appear to have missed numerous studies reporting large positive NEP (i.e.autotrophic) in several seaweed ecosystems.For example, NEP in Sargassum forests in Japan ranged from 302 to 1378 mmol C m −2 d −1 depending on the season (Watanabe et al., 2020), whilst Macrocystis forests are reported have NEP values of up to 1250 mmol C m −2 d −1 in the Southern Ocean (Delille et al., 2000(Delille et al., , 2009)).Dominant seaweed communities in the Mediterranean are reported to be net autotrophic (NEP = 17.8 ± 0.5 mmol C m −2 d −1 ), whilst their replacement ecosystems (e.g.algal turfs and invasive algae) are net heterotrophic (Peleg et al., 2020).Kelp forests in the northwest Pacific are also net carbon sinks (positive NEP), drawing down an average of 59 mmol C m −2 d −1 (range 20-180 mmol C m −2 d −1 [Ikawa and Oechel, 2015]).Other evidence that seaweed forests are net autotrophic comes from carbon budgets for these ecosystems such as those reported in the global review by Duarte et al. (2005) (362 mmol C m −2 d −1 , mean across all seaweed species) and Duarte and Agusti (1998), which are consistent with observations of persistent pCO 2 sub-saturation in seaweed ecosystems (Delille et al., 2000;Krause-Jensen et al., 2016).
For the few studies captured by Gallagher et al. (2022) the actual NEP is inadequately reported.For example, Gallagher et al. (2022) report a biassed NEP estimate of −47.9 and −8.57mmol C m −2 d −1 (i.e.net heterotrophic) from Miller et al. (2011), as the former includes only a fraction of the total ecosystem net production, and does not incorporate the significant phytoplankton production measured within the seaweed habitat.Gallagher et al.'s decision to include this study (with only part of the NPP) contradicts their argument that whole ecosystem metabolism must be considered in estimates of carbon sequestration, and challenges their assertion that the contribution of phytoplankton production is negligible in all seaweed ecosystems, countering other current evidence (Kavanaugh et al., 2009;Pfister et al., 2019).Gallagher et al. (2022) also incorrectly assume that daytime community respiration is the same as nighttime, even though nighttime respiration tends to be lower (Barrón and Duarte, 2009;Miller et al., 2011).
Additionally, a third of Gallagher et al.'s compiled studies do not consider seasonal variation, and of those seasonal studies, twice as many were conducted in winter compared to summer, including the lowest and third lowest NEP measures from benthic chamber studies on turf seaweeds (−164 mmol C m -2 d -1 ) and foliose algae (−32.6 mmol C m -2 d -1 ) (Miller et al., 2009).This is problematic and has likely biassed the estimates towards low values, as NEP can be >200 times lower in winter compared to spring and summer (Attard et al., 2019a), when intense macroalgal growth generally occurs (Delille et al., 2000;Rodgers and Shears, 2016;Wernberg et al., 2019;Pedersen et al., 2020).
Most importantly, the interpretations and conclusions of Gallagher et al. (2022) are not supported by their own dataset.The authors conclude that "the [negative] average NEP suggests that seaweed ecosystems are a C source."Yet, statistical analysis of their dataset shows that the mean of their studies is not significantly different from 0 (two-sided t-test, p > 0.95), with the standard error being three times larger than the mean.This high variability also exists at the level of the individual studies, with several studies reporting standard errors 1-2 times greater than the mean (Edwards et al., 2020;Sullaway and Edwards, 2020).Gallagher et al. (2022) ignore this variability, and yet their dataset cannot reject the null hypothesis that seaweed ecosystems in their dataset are in metabolic balance (i.e.neither net carbon sources nor sinks).

NEP as calculated by Gallagher et al. (2022) cannot resolve seaweed carbon mitigation potential
NEP represents the total amount of organic carbon in an ecosystem available for storage, export as organic carbon, or nonbiological oxidation (Lovett et al., 2006).Accurately quantifying NEP in order to infer available organic carbon at the relevant spatial scales remains an important challenge in marine ecosystems (Attard et al., 2019b), as these are open systems characterized by highly dynamic fluxes of production and respiration from benthic and pelagic sources (Jahnke, 2010;Bauer et al., 2013;Smale et al., 2018;Santos et al., 2021).Over half of Gallagher et al.'s NEP estimates come from benthic chamber studies, which yield an unrealistic account of the carbon available for export or storage [note that Bordeyne et al. (2020) are incorrectly reported to have used the Aquatic Eddy Covariance method (AEC)].This is because benthic chambers enclose only a small volume (typically <1 m 3 ) of a benthic community for a short time period (typically <24 h), which allows in situ measurements of the metabolism of confined and selected species, but is unlikely to capture the broader exchange of organic matter across the entire ecosystem (Champenois et al., 2007;Olivé et al., 2016).Chamber studies may underestimate ecosystem photosynthesis and overestimate respiration (Rodgers and Shears, 2016;White et al., 2021) and are therefore largely inappropriate to make inferences on global carbon balances and sequestration budgets-which indeed was not the aim of any of the chamber studies compiled.Crucially, studies that provide estimates of NEP over larger spatial scales (10 s of m sinks.The few studies using AEC available show that seaweed forests are highly autotrophic (Attard et al., 2019a(Attard et al., , 2019b)), whereas ecosystems not dominated by large seaweeds (e.g.sea urchin barrens and sandy sediments with sparse seaweeds) are slightly heterotrophic (Attard et al., 2014), which further supports evidence of net uptake of carbon by the former.Continuous measurements of air-sea CO 2 flux for seven years near a kelp forest using the AEC method revealed the kelp forest to be a major CO 2 sink, with the strength of the flux being strongly related to the extent and productivity of the ecosystem (Ikawa and Oechel, 2015).

Climate change mitigation depends on the net change in greenhouse gases, carbon sequestration, and CO 2 emissions
As pointed out by Gallagher et al. (2022), the climate change mitigation value of an ecosystem ultimately depends on the difference in CO 2 uptake capacity between the original ecosystem and its replacement ecosystem (Lovelock and Duarte, 2019).Gallagher et al. (2022) assert that the change in carbon mitigation following the loss of seaweed forests is "mixed", citing evidence that algal turfs are more heterotrophic than seaweed forests, whereas sea urchin barrens are not (Edwards et al., 2020).The fact that the replacement of seaweed forests by turfs would imply a reduction in NEP and a substantial loss of CO 2 mitigation capacity is not a minor point, as this is indeed what is happening to large areas of seaweed forests impacted by climate change globally (Krumhansl et al., 2016;Filbee-Dexter and Wernberg, 2018;Pessarrodona et al., 2021).Indeed, a study not included by Gallagher et al. (2022) shows how shallow reefs turn from net carbon sinks to net carbon sources when seaweed forests are lost (Peleg et al., 2020).As far as sea urchin barrens are concerned, Gallagher et al. (2022) do not mention that their cited study actually appeared to exclude sea urchins, resulting in unnaturally elevated productivity inside the benthic chambers due to the lack of urchin respiration and concurrent growth of benthic microalgal mats (Edwards et al., 2020), which might have made them unnaturally autotrophic.Hence, contrary to Gallagher et al.'s suggestion, it seems that the loss of seaweed forests would lead to a net reduction in CO 2 uptake capacity even if the seaweed forests were slightly heterotrophic.It follows, therefore, that avoiding losses of seaweed forests and restoring degraded habitats could represent a nature-based solution to reduce net CO 2 emissions.Although the potential for seaweed forests-which dominate the global seaweed biome-to contribute to climate change mitigation is increasingly recognized (Hill et al., 2015;Krause-Jensen et al., 2018;Macreadie et al., 2019), the amount of seaweed carbon that reaches carbon sinks is still poorly quantified and not spatially resolved (Hurd et al., 2022).Gallagher et al.'s study does not contribute to resolving any of these outstanding uncertainties.Instead of also capturing long-term carbon storage beyond the habitat, Gallagher et al. (2022) only calculate the balance between respiration and production of seaweed ecosystems (including external subsidies) in the coastal zone-a region of high exchange where much of the consumed organic material is recycled back to CO 2 and dissolved nutrients that are immediately available for subsequent primary production (Passow and Carlson, 2012).The extent to which these external subsidies would get respired in the presence or absence of seaweed forests remains debatable, and Gallagher et al. (2022) do not convincingly articulate that these external subsidies would only be respired if the seaweed ecosystem is present.Even assuming seaweed forests facilitate the respiration of allochthonous carbon, what is more relevant are the pathways through which carbon produced in the coastal zone can become sequestered in the long term.There is evidence that these pathways are enhanced when seaweed forests are present, through export to and long-term burial in shelf sediments (Frigstad et al., 2021) and transport to deep ocean regions with slow ventilation times (Ortega et al., 2019;Baker et al., 2022;Filbee-Dexter et al., 2022).

Conclusion
Gallagher et al.'s suggestion that seaweed ecosystems are net heterotrophic carbon sources misrepresents NEP in seaweed ecosystems, is based on a limited and inappropriate data selection, and lacks statistical support.We provide evidence that most seaweed forests, which drawdown the largest carbon flux of any vegetated habitat in the coastal ocean, are indeed net autotrophic ecosystems (i.e.carbon sinks), and export substantial amounts of organic matter that may contribute to carbon sequestration.Therefore, actions to restore seaweed forests, improve their condition, and/or halt their decline may contribute to climate change mitigation through increased drawdown of CO 2 , although quantifying their actual contribution to mitigation remains challenging.We recognize and recommend that carbon (and other greenhouse gases) fluxes around seaweed ecosystems should be considered more broadly and integrated into estimates of their climate change mitigation potential.This requires better resolving long-term carbon cycling by associated fauna, better understanding the fluxes of CO 2 between the atmosphere and seaweed forests, better understanding the exchange of carbon between seaweed ecosystems and their surrounding environments, and improving measures of productivity and NEP for existing and replacement ecosystem states such as turf reefs and sea urchin barrens.Substantial uncertainties also remain regarding the role of other biogeochemical processes, such as calcification and nutrient reallocation, as well as altered ocean albedo, fluxes of other climatically active gases, and inorganic fluxes in the magnitude of CO 2 drawdown by seaweed ecosystems (Bach et al., 2021, Santos et al., 2021, Hurd et al., 2022).These processes warrant full exploration in order to properly assess the carbon sequestration potential of seaweed forests and ecosystems, which rival, in area and productivity, the Amazonian forest (Duarte et al., 2022).In this context, Gallagher et al.'s arguments do not inform the debate on the role of seaweeds in mitigating CO 2 emissions.

Table 1 .
Edwards et al., (2020))/academic.oup.com/icesjms/advance-article/doi/10.1093/icesjms/fsad107/7220133 by Havforskningsinstituttet user on 07 August 2023 Seaweed forests are carbon sinks that may help mitigate CO 2 emissions 3 Average net ecosystem production (NEP) for seaweed forests and replacement ecosystems selected from the dataset compiled byGallagher et al. (2022).Seaweed forests include laminarian and fucalean kelp species.Replacement ecosystems include turf reefs, sea urchin barrens, and understory communities where canopy kelps were removed.Edwards et al., (2020)are listed in two categories because they report NEP for kelp forests and barrens.