Blue carbon: past, present and future, with emphasis on macroalgae

Abstract

Blue carbon did not originally include macroalgal ecosystems; however evidence is mounting that macroalgal ecosystems function in marine carbon sequestration. The great majority of present day marine macroalgal net primary productivity (NPP) involves haptophytic algae on eroding shores. For these organisms the long-term storage of particulate organic carbon involves export from the site of production of biomass that has evaded parasites and grazers, and that some of the exported biomass is sedimented and stored rather than being mineralized en route by detritivores (microbes and fauna). Export from eroding shores, and subsequent storage, of haptophytic marine macroalgal particulate organic carbon could have started by 1.6 Ga. Storage on depositing shores close to the site of NPP by rhizophytic macroalgae and then by rhizophytic coastal seagrasses, tidal marshes and mangroves began not less than 209 Ma ago. Future increases in surface ocean temperatures may bring tropical marine macroalgae to their upper temperature limit, while temperate marine macroalgae will migrate poleward, in both cases assuming that temperature increases faster than genetic adaptation to higher temperature. Increased CO₂ in the surface ocean will generally favour uncalcified over calcified marine macroalgae. This results in decreased CO₂ release from decreased calcification, as well as decreased ballasting by CaCO₃ of exported particulate organic carbon resulting in decreasing sedimentation. While much more work is needed, the available information suggests that macroalgae play a significant role in marine organic carbon storage.

1. Introduction

The focus in research on blue carbon, i.e. long-term storage of organic carbon produced in net primary productivity (NPP) of coastal vegentation, has been on halophilic flowering plants, i.e. tidal marshes, mangroves and seagrasses [1–4]. The coastal flowering plants live predominantly as rhizophytes [5,6] on depositing shores, where the fraction of macrophyte NPP that is not mineralized by grazers or parasites can be stored as particulate organic carbon in the rooting medium [1–4,7]. By contrast, macroalgae live predominantly on eroding shores as haptophytes [4–6] where there is little prospect of storage of particulate organic carbon near the site of its production [1–4,7]. The fraction of NPP that is not mineralized in situ by grazers, parasites or, for dead algal parts, detritivores, is exported to offshore sites where the implicit or explicit assumption is frequently that the particulate organic carbon is mineralized to inorganic carbon in the upper mixed layer rather than being stored in sediments or in suspension below the thermocline. Krause-Jensen et al. [8] and Smale et al. [9] point out the importance of studies of sources of, as well as sinks for, organic carbon, as interconnectivity of compartments, in blue carbon studies. The purpose of this paper is to examine evidence on storage near the site of production, or after export, of the particulate products of NPP by macroalgae in the past, today, and what might happen in the future. Previous analyses have focused on the present and, to a lesser extent, the future [1–4,7,9].

2. Past

The Global Oxygenation Event about 2.3 Ga ago required the evolution of oxygenic photosynthesis in cyanobacteria, and also marine O₂ production and organic carbon burial. Accumulation of O₂ also requires that organic carbon burial accounts for the O₂ consumed in Fe²⁺ and S²⁻ oxidation [10,11]. Organic carbon burial in the ocean also removes some of the nutrients (combined N, P, Fe) that limit marine productivity [4]. In the Palaeoproterozoic the only marine oxygenic primary producers were benthic (including stromatolitic) and planktonic cyanobacteria. The temporal sequence of marine macroalgae was red (Rhodophyta) (Mesoproterozoic, 1.2–1.6 Ga ago) [12,13], green (Chlorophyta), (Ulvophyceae: Dasycladales) (Cambrian, 541 Ma ago) [14], and brown (Phaeophyceae) algae with a poor fossil record [14] and a crown group radiation estimated as at the latest Triassic (200 Ma ago) [15]. The belief that marine macroalgae before 210 Ma ago were haptophytes [4–6] is based on the presence of a holdfast in Bangiomorpha [12] and the growth habit of Ramathallus [13], both more than 1 Ga old, and holdfasts of the Ediacaran (about 550 Ma) Chinggiskhaania [16] and Globusphyton [17]. However, there are very well-preserved marine macroalgal fossils from the Ediacaran and the Cambrian that lacked a means of attachment to the substrate [18,19]. Such permanently unattached macrophytes were termed pleustophytes by Luther [5], a term that now encompasses potentially attached, but detached but viable, haptophytes and rhizophytes [6] such as the green (Ulva) and golden (Sargassum) tide organisms [20]. Well characterized holdfasts on Ordovician macroalgal fossils shows that they were haptophytes [19].

Sandy and muddy substrates were presumably colonized solely by microscopic algae until the origin of rhizophytic marine macroalgae. The rhizophytic ulvophycean green alga Caulerpa originated some 209 Ma ago, i.e. at the Triassic–Jurassic boundary, based on time-calibrated molecular phylogenetics [21], although earlier occurrence of rhizophytic algae cannot be ruled out. Again using molecular phylogenetics, Zeng et al. [22] showed that the angiosperms originated about 225 Ma ago, and that the Mesangiospermae, including all the halophytes in the phylogeny of Flowers et al. [23], originated about 170 Ma ago. Although Flowers et al. [23] specify terrestrial halophytes, including mangroves and tidal marsh (= salt marsh) plants, some salt marsh plants are members of the Alismatales which also contains all of the seagrasses. These molecular data suggest that Caulerpa preceded seagrasses, salt marsh plants and mangroves as marine rhizophytes. The molecular ages, especially with few calibration points, are generally older than fossil ages: Herendeen et al. [24] find no reliable fossil angiosperms before the Cretaceous. These depositing shores would also have had allochthonous organic carbon input, so the present day mudflat (Humber estuary, UK) organic carbon storage of 1.3 mol organic C m⁻² yr⁻¹ [25] is an over-estimate of storage from autochthonous primary production by microalgae. The natural abundance of stable isotopes of carbon, nitrogen and sulfur can be used to estimate the fraction of allochthonous organic carbon input to total organic carbon on a case by case basis [26,27]. Furthermore, there are no global values for storage on depositing shores with only microalgal primary production. Before the Mesozoic when macrophytic rhizophytes evolved, the only autochthonous marine carbon burial on depositing shores would have come from benthic cyanobacteria and (from 1.6 Ga ago) eukaryotic microalgae, with allochthonous organic carbon from haptophytic and pleustophytic macroalgae and, increasingly from 500 Ma ago, riverine input from terrestrial primary producers [14]. Quantifying the difference in global organic carbon burial from coastal photolithotrophs before and after the origin of rhizophytic marine macrophytes is not possible as a result of environmental variations, not least the variations in the global area of eroding (haptophytic macrophytes) and of depositing (rhizophytic macrophytes) shores as a result of plate tectonics.

Some of the best preserved fossil marine macroalgae are the calcified green ulvophyceans [14,28] and coralline red floridiophyceans [14,29]. Since calcification is a CO₂-generating process (0.63 CO₂ produced per CaCO₃ precipitated), a larger fraction of coastal macroalgal habitats occupied by calcified algae would decrease net CO₂ assimilation relative to organic carbon production, and possibly decrease CO₂ sequestration. However, the association of particulate organic carbon with high density CaCO₃ ballast would increase the speed of sedimentation and decrease the possibility of mineralization of particulate organic carbon during sedimentation [30]. While calcification is determined by CO₂ concentration, with increasing CO₂ decreasing calcification [31], there are observed exceptions to this generalization based on observations of CO₂-enriched shallow marine vents [32]. Furthermore, there is little association of the occurrence of fossils, and origination-extinction of species, with past CO₂ availability [14,28,29]. The life form of calcareous algae from the mid-Mesozoic onwards could relate more to increasing herbivory than CO₂ availability [33]. Further discussion of buoyancy and ballasting mechanisms can be found in Krause-Jensen & Duarte [7].

In conclusion, haptophytic (on rock shores) and pleustophytic macroalgae were the only coastal macrophytes that could contribute to long-term storage of organic carbon between 2.6 Ga and 2.1 Ma ago. After 2.1 Ga rhizophytic macroalgae, and flowering plants, occurred on muddy and sandy shores.

3. Present

Table 2 of Duarte [3] and table 1 of Raven [4] give global values for NPP, and these two sources plus McLeod et al. [2] give carbon sequestration (burial plus export), for five marine ecosystems; the values are given in table 1 of this paper. The variations in values among three compilations used are a function of the sources consulted and the criteria the compilers applied to the reliability of the sources. The maximal values suggest that phytoplankton carbon storage is 28 times that from coastal macrophytes. Among the macrophytes, the maximal values show that carbon sequestration from the (almost all haptophytic) macroalgae, almost all as export, exceeds that from the (almost all rhizophytic) seagrasses, salt marshes and mangroves where there is very significant burial component [3,4,7,34]. Calcareous macroalgae, like photosynthetic coral reefs, are unlikely to be involved in net CO₂ sequestration [4]. Van den Heijden & Kamenos [35] give global values of NPP of 58 Tmol C per year and of inorganic carbon incorporation into CaCO₃ of 17 Tmol C per year for calcified macroalgae. With 0.63 CO₂ produced from converted to 1 CaCO₃, the global CO₂ incorporation by calcified macroalgae is 58 − (17 × 0.63) = 47 Tmol C per year. Neither Duarte [3] nor Raven [4] specifically deal with calcified macroalgae, so their values for global macroalgal NPP are over-estimates by 11 Tmol C per year the net CO₂ assimilated by the calcified macroalgae. Smeaton et al. [36] address carbon storage in Scottish fjords and find that CaCO₃-C significantly exceeds organic carbon: thus, storage of carbon in the fjord sediments results in net CO₂ production.

Table 1.

Global net primary productivity (NPP) and global carbon sequestration burial for the five ecosystems involved, using maximal values from the data in table 1 of Raven [4], table 2 of Duarte ([3]; values in parentheses) and table 1 of McLeod et al. ([2]; values in square brackets). (Organic carbon burial by seagrasses, salt marshes and mangroves is largely in the depositing sediments in which the primary production takes place. In situ burial also occurs for the minor contributions from rhizophytic macroalgae and microalgae on mud or sand. For haptophytic macroalgae and microalgae, and the minority of seagrasses that are haptophytic, as well as phytoplankton, carbon burial occurs in sites other than where the primary production occurs, i.e. in offshore sediments and in water below the thermocline [1,2,4,7]. ND, not determined.)

system	global NPP Tmol C per year	global carbon sequestration (local sediments plus export) Tmol C per year
phytoplankton	4.0–4.8. 103 (ND)	1100      (ND)        [ND]
macroalgae	80–210    (11–242)	0.8–22    (0.5–106)    [ND]
seagrasses	≤41      (5–162)	≤9      (2–66)      [4–9.3]
salt marshes	≤37      (14–35)	≤7      (45–12)     [0.4–7.3]
mangroves	≤12.5     (4.2–12.5)	≤2.1     (1.6–5)     [2.6–2.8]

The angiospermous marine macrophytes are derived from terrestrial angiosperms and maintain varying amounts of the recalcitrant macromolecules, lignin and cutin [37]. There are also recalcitrant organic compounds in marine macroalgae [37]. The decomposition rate of marine macroalgae is similar to that of the angiospermous marine macrophytes [1,37,38], and the decomposition rate of marine macrophytes does not correlate well with the inverse of the lignin content [39]. While there are few obvious lignin-degrading organisms in the ocean [40,41], both lignin and cutin from terrestrial (via rivers) and marine sources are relatively rapidly degraded in seawater [42–45]. One possibility for lignin breakdown in the surface ocean, or as wrack at high tide level, is photochemical destruction [46]. Problems in determining the source of marine sedimentary organic matter, and its differential breakdown, are discussed in references [47–49].

In conclusion, although not originally included in blue carbon, evidence is growing that marine macroalgae could make a significant to long-term storage of organic carbon.

4. Future

The future ocean will be warmer and have higher CO₂ and and lower pH and as global events, with other, more local, anthropogenic effects; both of these changes have implications for marine macroalgae [32,50–53]. Studies of recent (decadal) changes allow predictions of changes in macroalgal populations over the next few decades [50–53], as does investigation of high-CO₂ shallow water seeps [32]. The general predictions are a decrease in forests of Laminariales (Phaeophyceae) and similar large algae, and an increase in turf algae, on temperate rocky shores [51–53]. Predictions for tropical and subtropical macroalgae are less clear, although many tropical marine macroalgae are close to their upper temperature limit [50,54]. Further experiments are needed to determine how any increased tolerance of high temperatures interact with the effects of increased CO₂ [54]. While short-term (acclimation) experiments taking a year or more for one or, for ephemeral algae, several generations are useful, ideally genetic adaptation experiments should be undertaken. However, while such experimental evolution experiments involving 500 generations can take under two years for microalgae [55], they would take 50 years for even the macroalgae with shortest generation time (e. g. Ulva) of three to five weeks [56].

The prediction for calcified macroalgae (and corals) is for decreased calcification with increasing seawater CO₂, and for decreased organic productivity with increasing CO₂ if the decreased calcification in high CO₂ limits growth [31]. However, work on shallow-water marine CO₂ seeps shows that the prediction is not always borne out [32]. A further complication is the decreased CO₂ production resulting from the lower rate of calcification. Burial in near-shore sediments may decrease if there is less CaCO₃ ballast per unit particulate organic carbon in calcified macroalgae [30].

In conclusion, the available evidence suggests that there will be significant changes in the distribution of marine macroalgae in the coming decades, and presumably changes in contributions to long-term organic carbon burial [57,58].

5. Conclusion

Although macroalgal ecosystems were not originally included in blue carbon, evidence is mounting that they can function in marine carbon sequestration [1,3,4,8,9]. For the great majority of marine macroalgal NPP that occurs on eroding shores, long-term storage of particulate organic carbon involves export from the site of production with subsequent sedimentation and storage [1,3,4,7–9], starting from as early as 1.6 Ga ago [13]. Storage on depositing shores close to the site of production by rhizophytic macroalgae and then rhizophytic coastal marine flowering plants began not more than 209 Ma ago [21,22]. In the future, with increased ocean temperature, tropical marine macroalgae may reach their upper temperature limit and temperate marine macroalgae will migrate poleward, in both cases assuming that temperature increase exceeds the rate of genetic adaptation to higher temperature. Increased CO₂ will generally favour uncalcified over calcified marine macroalgae, with decreased CO₂ release from calcification and decreased ballasting of exported particulate organic carbon. Blue carbon accounting procedures must be modified to incorporate macroalgae, and interconnectivity to trace organic carbon from source to sink [8,9].

Data accessibility

All data used are in the references cited.

Competing interests

I declare I have no competing interests.

Funding

There was no funding for this study.