How can blue carbon burial in seagrass meadows increase long-term, net sequestration of carbon? A critical review

Global estimates of organic carbon stock in seagrass meadow sediment depend on knowing the extent of seagrass habitat. The extent of the seagrass biome may be modelled, based on occurrence records and environmental variables (especially sea surface temperature and distance from land) (Jayathilake and Costello 2018). Alternatively, the existing extent of seagrass may be estimated using a satellite-based approach, including ocean colour or acoustic measurements (Harcourt et al 2018, Sani et al 2019). These values are sometimes converted to carbon burial using carbon conversion factors (Sani et al 2019). Based on published values, Macreadie et al (2021) estimated that the area covered by seagrass meadows could be increased by 8.3–25.4 million ha globally, with a large associated increase in carbon storage.

Local or regional case studies are carried out by measuring the total organic carbon stored in the uppermost layer of sediment over a specified depth. International protocols (e.g. IPCC 2019) call for a sum over the top 1 m of sediment. Regional studies vary in the depth of sediment assessed, with a range of 5 cm–3 m (table 1). In areas with low sedimentation, there might only be a shallow layer of sediment overlying rock, in which case the shallow layer represents the total stock.

Sometimes only a shallower depth can be assessed because the deeper sediment has become too compressed to force the corer any deeper, in which case the stock is generally reported to the 'depth of refusal' and extrapolated to 1 m (e.g. Green et al 2018). Extrapolation would usually overestimate the 1 m stock, because organic carbon is remineralized with depth in marine sediment (e.g. Stolpovsky et al 2015), leaving the highest concentration at the surface. Conversely, where the % organic carbon increases with depth due to some change that has occurred in the ecosystem, extrapolation from a shallow surface layer would underestimate the stock.

It should be noted that the top meter does not always represent all of the carbon stock in a particular location. For example, working in a seagrass meadow in the American Pacific Northwest, Kauffman et al (2020) determined that the top 1 m of sediment contained only 48%–53% total ecosystem C stock, while >98% resided in the top 3 m.

A review by Githaiga et al (2016) identified a major, regional gap in carbon stock estimates: although they found some studies of seagrass extent in Africa, particularly in east Africa, they found no reports of sediment carbon stock from that continent. Githaiga et al (2017) subsequently measured carbon stock in a seagrass meadow in Kenya, and Gullström et al (2018) published sedimentary carbon data from southeastern Africa (Tanania to Mozambique). Even so, the lack of data from the whole west coast of Africa represents a significant uncertainty for global estimates.

Blue carbon stock is vulnerable to degradation and re-release to the atmosphere as CO₂ (Lovelock et al 2017). These losses may be localized within the seagrass meadow (i.e. greater loss in the center of a patch during a marine heat wave; Aoki et al 2021), or the losses may be widespread. Lafratta et al (2020) reported that 75%–90% of stored organic carbon was remineralized in the top meter in Australian Posidonia meadows following their loss and partial restoration. A shading experiment in the Gulf of Mexico that induced a small-scale die off resulted in a 50%–65% loss of organic matter in the top 8 cm of sediment, including 50% lost from the top 1 cm (Trevathan-Tackett et al 2017). In a disturbed former seagrass bed, Macreadie et al (2015) estimated that 72% of the carbon, which had taken hundreds of thousands of years to accumulate, had been lost. They warned that 'disturbance to seagrass ecosystems can cause release of ancient carbon, with potentially major global warming consequences.'

Protecting existing stock does not reduce the amount of CO₂ in the atmosphere, so protection alone does not qualify for carbon credits under the Verified Carbon Standard (Emmer et al 2015b). Only the expansion of burial counts. However, the stock is important to determine, because it is a measure of the vulnerable carbon that could be re-released due to storms, slope failure, dredging, or climate change.

3.1.1. Macroalgae

A variety of biomarkers has been used to identify sources of sequestered C. The most commonly used are the stable isotopes of carbon and nitrogen (δ¹³C, δ¹⁵N) measured in bulk organic matter or sediment. Recent examples include work in Japan (Tanaya et al 2018), on the eastern coast of the Red Sea (Garcias-Bonet et al 2019) and in eastern North America (Greiner et al 2016). Combined with organic carbon concentration or the ratio of organic carbon to total nitrogen, these stable isotopes provide useful information about the relative proportions of allochthonous (mainly terrigenous) and autochthonous (seagrass + macroalgae + phytoplankton) material.

Bulk stable isotopes, while convenient to use, do not separate multiple marine sources very well (Geraldi et al 2019). Other biomarkers for seagrasses include fatty acids (e.g. Dongen et al 2000), lignins (Barry et al 2018), hydrogen isotopes (Duarte et al 2018b), polysaccharides (Kaal et al 2020), and environmental DNA (Reef et al 2017). In some cases, the chemical biomarker results can be confirmed by microscopy (Dongen et al 2000).

In a broad review and critique of biomarker methods, Geraldi et al (2019) recommended the use of a combination of complementary methods, particularly stable isotopic analysis of lipids combined with eDNA analysis, although they noted that the method still required validation. Using multiple biomarkers helps to compensate for the weaknesses of individual methods. For example, lignin ratios can be different in sediment from those in the nearby, fresh seagrass (Barry et al 2018). Similarly, Nakakuni et al (2021) noted that the contribution of long-chain fatty acids in near-surface sediment declined with depth (apparently due to degradation), while lignin phenols were selectively preserved.

Since different methods give different information and can shore up each others areas of weakness, a combination of biomarkers seems the most powerful approach. Endmembers will likely need to be defined locally, or at least regionally, before the combined biomarkers will give reliable, quantitative information about the flux and burial of organic carbon from seagrasses.

3.3.1. Meadow connectivity

3.3.2. Grainsize

3.3.3. Bioturbation

Coastal sediment is nearly always bioturbated. Bioturbation distributes material deeper into the sediment than would have been the case in an undisturbed sediment and increases the rate of remineralization in surface sediment (Johannessen and Macdonald 2016). The global mean depth of the sediment surface mixed layer is 9.8 ± 4.5 cm, probably as a result of the energetic cost of burrowing (Boudreau 1994). A model based on food availability and the intensity of bioturbation (Boudreau 1998) predicted a similar global average (9.7 cm). Neglecting bioturbation tends to exaggerate sediment accumulation rates, whether they are based on ²¹⁰Pb or on a tracer that represents a known time horizon (Johannessen and Macdonald 2016). This has been a widespread problem in the blue carbon literature.

Remineralization reduces the amount of organic carbon available to be buried (Thomson 2017). During a lab experiment in which seagrass fronds were buried in sediment with or without bioturbating shrimp (Thomson 2017, Thomson et al 2019), the treatment with shrimp released 2–5 times as much CO₂ as the control without shrimp (figure 2).

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3.3.4. Nutrients, bacteria and microbial priming

3.3.5. Herbivores and predators

3.3.6. Emissions of other GHGs

3.3.7. Role of calcium carbonate

Calcium carbonate can be precipitated, buried, remineralized and/or dissolved in seagrass meadows. This is relevant to the net drawdown of carbon dioxide, because CO₂ is released when calcium carbonate forms (calcification) and consumed when it dissolves (figure 3) (Frankignoulle et al 1994).

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Carbonate is often enriched in seagrass sediment (Gullström et al 2018). Some of this comes from calcium carbonate structures in seagrasses themselves, some from associated CaCO₃-producing organisms, and some is washed in from terrigenous sources. The molar ratio of CO₂ released to CaCO₃ formed varies but is generally about 0.6 in the modern ocean (Gullström et al 2018). However, as pH declines globally due to ocean acidification, the CO₂:CaCO₃ ratio will increase, resulting in a positive feedback that leads to acidification, and reducing the net burial of carbon (Frankignoulle et al 1994). Lower sedimentary carbon storage under low-pH conditions was observed near two CO₂ vent systems in the Mediterranean (Vizzini et al 2019), emphasizing that, although acidification might favour the growth of seagrass, it does not necessarily favour carbon sequestration in sediment.

Calcium carbonate formed in situ in a seagrass meadow can offset the CO₂-drawdown effect of the burial of organic carbon (Saderne et al 2019, Sanders et al 2019). However, the accumulation of even carbonate-rich sediment can have a beneficial effect of helping seafloor accretion to keep pace with sea-level rise (Saderne et al 2019).

The ratio of inorganic to organic carbon stored in sediment varies around the world. In the western Indian Ocean (Tanzania to Mozambique), % organic C in seagrass sediment is positively related to % CaCO₃ (Gullström et al 2018). Sediment in Brazil and Florida has higher CaCO₃ than organic C burial, which might negate atmospheric drawdown of CO₂ by organic C burial (Howard et al 2018). In coastal sediment of the temperate west coast of Canada, in contrast, the concentration of organic carbon in sediment and sinking particles can be an order of magnitude higher that of inorganic carbon (e.g. Johannessen et al 2019). Overall, CaCO₃ burial is higher in the tropics than in temperate waters (Saderne et al 2019).

Both organic and inorganic carbon come from a mixture of autochthonous and allocthonous sources (York et al 2018), and not all buried organic or inorganic carbon is equally reactive. The variability among sites and seasons depends on local factors (Howard et al 2018), so the CaCO₃ offset/buffering effect needs to be studied along with organic C storage.

Macreadie et al (2017b) summarized the main uncertainties around the net effect of carbonate burial in seagrass meadows: the stoichiometry varies; some released CO₂ could be taken up by seagrasses and epiphytes; some carbonate in sediment comes from geological not local biological sources; and further acidification might redissolve precipitated CaCO₃, buffering the effect.

The magnitude and direction of the net effect of carbonate burial in seagrass meadows worldwide are unclear. The effect will need to be quantified site by site. Certainly it will be important to separate allochthonous from autochthonous carbonate. The reburial of terrigenous CaCO₃ could be considered a net zero effect (figure 3), since it is just a matter of moving the solid carbonate from one reservoir to another.

From the results reported above, it is clear that different factors determine the rate of net organic carbon sequestration in different environments: while biotic factors predominate in the tropics and subtropics, abiotic factors are more important in temperate seagrass meadows. Some recent review papers have also made this point.

In a broad review of studies of tropical, subtropical and some temperate seagrasses, Mazarrasa et al (2017) determined that the habitat characteristics that promoted high org C sequestration were: an extensive, continuous meadow, large persistent species, fine-grained sediment, a low-energy environment, clear water, moderate nutrient concentration, predator protection (to reduce grazing and bioturbation), protection against disturbance, and the ability to expand landward with sea-level rise. They also commented that for smaller, short-lived seagrasses such as Zostera, grainsize could be a useful indicator of carbon storage.

Despite the importance of seagrass species and meadows size in tropical and subtropical regions, Samper-Villarreal et al (2018) observed significant variation in carbon stock over a gradient of water turbidity, from riverine to coastal, in their subtropical study area. Mazarrasa et al (2021) found that different factors predominated, depending on bioregion, plant body size and environment (estuarine vs coastal).

A similar review centred on temperate, northern hemisphere Zostera marina meadows (Röhr et al 2018) determined that high organic carbon stock (measured to 25 cm) was promoted principally by abiotic factors (grainsize, dry density, degree of sorting, salinity, water depth). The authors found that those factors were more important to total organic carbon stock than plant-related parameters (biomass and shoot density). Based on δ¹³C measurements, less than half of the organic carbon buried in these systems came from seagrass, and this proportion was highly variable.

Environmental factors, particularly the relative energy of the environment, have also been found to determine carbon burial in temperate environments on the west coast of North America (Prentice et al 2019), Korea (Kim et al 2022), England (Lima et al 2020), and the northeastern United States (Novak et al 2020).

Carbon stored in surface sediments that undergo active re-mineralization or are vulnerable to resuspension cannot be said to be buried on the 100 year timescale required for carbon credits (figure 1). Only burial below the vulnerable surface layer represents sequestration. Quantifying carbon burial rates in seagrass meadows and comparing the calculated rates amongst sites globally has been problematic, due to the widespread lack of understanding of how to make that calculation.

Some authors use accretion above an introduced marker layer, such as a layer of crushed feldspar (e.g. Ewers Lewis et al 2018). Others divide the carbon inventory over the top few cm by the sedimentation rate determined from ²¹⁰Pb (e.g. Bedulli et al 2020). Some do not specify their burial rate methodology, and some use global average rates from Duarte et al (2013) and do not measure the local rates at all.

Lafratta et al (2020) commented that ²¹⁰Pb and ¹⁴C do not always work in low-depositional seagrass environments and that no additionality is demonstrable using these methods. That likely indicates that there is no significant accumulation of sediment or organic carbon at these sites.

Many authors use a sediment accumulation rate model known as constant rate of supply (CRS), which was designed for unmixed lake sediments (Appleby 2001). Appleby commented that the method was not suitable for use in bioturbated sediments (figure 2). Blue carbon researchers frequently note bioturbation in their cores but then use the CRS model, regardless. Some note bioturbation, but then assign unique dates to specific layers in their cores, or report different sedimentation rates or different carbon accumulation rates for different core segments, which is not possible in a mixed core (Johannessen and Macdonald 2016).

Reviews sometimes compare burial rates from different studies that used a variety of methods, some accounting for surface sediment mixing and others not. Although the lack of standard methodology limits the comparison of burial rates from one study to another, it does seem likely that carbon burial rates in temperate North America are lower than those in tropical and subtropical areas (Postlethwaite et al 2018, Prentice et al 2020).

A universal methodology would assist with inter-regional comparisons and global sums. One method that has been used for decades in coastal marine sediment outside seagrass meadows is illustrated in figure 4. First the sediment accumulation rate is determined from the decay of ²¹⁰Pb below the surface mixed layer, following Lavelle et al (1986). Next the burial concentration of organic carbon is determined from the depth profile of organic carbon, as the depth at which the organic carbon concentration has declined to a near-constant value (Krause et al 2022). The seagrass proportion of the organic carbon would ideally be determined using a combination of biomarkers, as noted above. Finally, the burial concentration of seagrass organic carbon is multiplied by the sediment accumulation rate (Johannessen and Macdonald 2016).

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If the organic carbon concentration does not decline to a constant value with depth, then either the burial depth has not yet been reached (if the concentration is still decreasing at the bottom of the core), or else something has changed in the environment. For example, a down-core increase indicates that the flux of organic carbon has decreased at that site.

Even the simple situation of down-core decline with depth due to remineralization can, in some situations, mask an increase in carbon flux. These two processes can be separated, but the only method developed to date (Johannessen et al 2020) requires multiple cores from the same area, which might be prohibitively expensive, depending on the situation.

The method described in figure 4 works for either mixed or unmixed sediment, where the sediment accumulation rate and carbon flux have remained approximately constant over the time represented by the core. It is more complicated if either of these rates has changed significantly, which might well have happened in areas where changes in vegetation or in human activities have changed the depositional environment.

If the flux of organic carbon has changed with time, but the sediment accumulation rate has remained the same, then the carbon flux can be modelled mathematically as a transient tracer (Guinasso and Schink 1975). If the sediment accumulation rate has also changed, this should be apparent as a break in the slope of the plot of ln(Excess ²¹⁰Pb) vs depth (in addition to the break at the base of the surface mixed layer; e.g. see figure 3 in Johannessen et al (2008)). However, the studies on transient tracers and changing sedimentation rates were not carried out in seagrass meadows. It would be useful to develop a method specifically for seagrass meadows, to account for changes in the fluxes of sediment and organic carbon.

In summary, the CRS method only applies where there is no bioturbation or other mixing, such as in lakes or in deep anoxic basins. For mixed cores, as in most marine sediments where seagrasses grow, the ²¹⁰Pb method described by figure 4 is better. For bioturbated cores where there has been a change in the rate of sediment accumulation or of organic carbon flux, the figure 4 method can still be applied, if the change in sedimentation rate was simple. For more complex situations, mathematical modelling is required. Until a method has been developed to deal with complex changes in flux in seagrass meadows, a conservative approach would be to multiply the lowest concentration of organic carbon measured in a core by the lowest sediment accumulation rate that fits the data.

3.5.1. Allochthonous carbon

Sea-level rise could result in an expansion of seagrass habitat in places where meadows are able to move landward; however, shoreline armouring, such as building seawalls, would result in a 'coastal squeeze' effect (Lovelock and Reef 2020), which could reduce the area of meadows and the potential for continued storage of carbon (figure 5, table 2). Sea-level rise is likely to reduce seagrass area and meadow carbon stocks, unless the shoreline is managed to permit landward migration of seagrass (Kauffman et al 2020).

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Submerged plants, such as seagrasses, are susceptible to temperature increase (Short et al 2016). Global warming is changing the geographic range of seagrasses, with losses in equatorial regions and expansion toward the poles (Duarte et al 2018a). Warming water might favour the expansion of seagrass habitat in temperate regions and the Arctic (Murphy et al 2021).

Short-term marine heat waves, which are becoming more common as a result of climate change (Oliver et al 2019), can cause local or widespread seagrass die-offs (e.g. Smale et al 2019, Strydom et al 2020, Murphy et al 2021). The loss of seagrasses can lead to the loss of associated carbon stocks (Arias-Ortiz et al 2018). These losses may be highly localized in some cases, with a loss of stored carbon at the centre of a patch, followed by a gain in subsequent years around the edges of the patch (Aoki et al 2021). More moderate temperature rise does not appear to threaten seagrass sediment carbon stock. When seagrass cores were transplanted along a thermal gradient generated by hot water released from a coastal power plant (Macreadie and Hardy 2018), there was no secular trend in carbon stock at a temperature elevation of 2 °C or 4 °C. Macreadie and Hardy (2018) speculated that the increased microbial degradation at higher temperatures reported in other studies might require higher temperatures, longer exposure times, or a combination of other stressors.

Overall genetic change is thought to be too slow to keep up with the rate of global change, but changes in microbiome and gene expression (epigenetics) may provide enough plasticity for individual adaptation (Duarte et al 2018a). A range of temperature-tolerance can occur within a single patch (DuBois et al 2022). In an experiment in which a Zostera marina meadow was subjected to five weeks of experimental warming (4.5 °C above ambient), Reynolds et al (2016) observed an initial increase in shoot production, followed by reduced shoot production and a 50% decrease in biomass after the temperature returned to normal. They also observed a change in genotype, favouring some genotypes that had not been dominant at normal temperatures. It seems that some adaptation is possible within genetically-diverse populations.

Deoxygenation is a widespread effect of climate change. Seagrasses experience a large diel range in oxygen concentration (e.g. Berger et al 2020, Altieri et al 2021). They produce oxygen photosynthetically, and are able to counteract the effects of local hypoxia on their associated heterotrophic communities by moving oxygen from blades to sediment and by releasing excess oxygen into the canopy (Altieri et al 2021). In contrast, increased exposure to oxygen—from dredging, for example—can release stored carbon from seagrass meadow sediments (Macreadie et al 2019). Macreadie et al (2019b) observed a marked increase in remineralization (34- to 38-fold) when deeply-buried, thermally-recalcitrant carbon was exposed to oxygen.

The hydrological cycle is also changing in ways that affect nearshore waters and coastal ecosystems. Warming accelerates the melting of glaciers and changes patterns of precipitation. This affects the flux and timing of particles, carbon and nutrients discharged into the coastal ocean (Bidlack et al 2021). Increasing turbidity due to storms or sudden, high-discharge events could reduce the available light and smother seagrass beds (Murphy et al 2021). Reduced light has been shown to reduce the subsurface sedimentary carbon even more than the surface carbon, possibly due to reduced release of dissolved organic carbon by the seagrass roots in low light (Premarathne et al 2021).

Ocean acidification, another effect of increased atmospheric CO₂, has a complex effect on carbon storage in seagrass meadow sediment. (See 'Role of calcium carbonate' section above.) Acidification might favour seagrass photosynthesis, but at the same time harm calcareous epiphytes (Murphy et al 2021). It will also increase the ratio of CO₂ released per mole of calcium carbonate formed (Frankignoulle et al 1994), reducing the net burial of carbon in sediment.

Declining coastal salinity in some temperate areas could reduce seagrass habitat; a salinity <20 (on the Practical Salinity Scale) has been observed to reduce growth and the establishment of seedlings (Murphy et al 2021), although some seagrass meadows were still healthy with salinity as low as 5 in Arctic waters.

The loss of coral reefs, particularly in the tropics, as a result of climate change, might also reduce seagrass meadow carbon storage; coral reefs can serve to reduce the energy of the environment, permitting greater sediment accumulation in sheltered meadows and reducing erosion (Guerra-Vargas et al 2020).

The effects of climate change on carbon storage in seagrass meadows will be mixed (table 2). The biggest climate-related threats to seagrass meadow carbon storage (and to the meadows themselves) are likely to be the coastal squeeze effect and increased water temperature, particularly as a result of extreme events such as marine heat waves.

Most papers in this field call for the protection of existing blue carbon stocks in seagrass meadows. Several protective measures have been proposed. For example, the protection of blue carbon stocks could be incorporated into the design of marine protected areas (Howard et al 2017, Sala et al 2021).

Seagrass management studies have been carried out in Australia, which is estimated to hold 5%–11% of the world's blue carbon stock (Kelleway et al 2020). There is interest in including blue carbon in Australia's Emissions Reduction Fund, with the potential to protect, restore and expand blue C ecosystems, using management actions such as reintroducing tidal flow through meadow areas (Kelleway et al 2020).

A model study evaluated several management options for blue carbon protection along the coastline of southeastern Australia (Moritsch et al 2021). The study compared the effects of: (a) managed retreat; (b) managed retreat + levee removal; (c) erosion of high-risk areas; and (d) erosion of moderate- to high-risk areas. The authors found that avoiding erosion was more effective than restoration, and that managed retreat + levee removal sequestered the most carbon. Levee removal alone contributed only a small portion to the total carbon sequestered, but the effect began sooner.

Other management actions with the potential to increase carbon sequestration in Australia and beyond include: reducing anthropogenic nutrient loading, restoring water circulation, and reducing the overpopulation of bioturbators (Macreadie et al 2017a). Overfishing of predatory fish can increase the population of grazers and bioturbators, reducing carbon storage in seagrass meadow sediment (Macreadie et al 2017a).

The potential monetary value of blue carbon restoration is as yet unclear. Taillardat et al (2018) commented that, although the global-scale effect of blue carbon was limited because of the small total area of vegetated ecosystems, it could be significant at a national level for countries that have long coastlines and low national emissions, such as Bangladesh. Case studies of carbon-financing in Kenya, India, Vietnam, and Madagascar indicate that small-scale projects under the voluntary carbon standard are the most effective (Wylie et al 2016).

There is still an urgent need to refine and correct blue carbon accounting before it is widely accepted for carbon financing (Johannessen and Macdonald 2016, Gallagher 2017). Recent controversy over land-based carbon crediting schemes in Australia (Macintosh et al 2022, Morton 2022) provide a cautionary tale.

Some of the controversy over blue carbon methodology likely results from real regional differences in ecosystems (figure 6). Seagrass meadows in tropical and subtropical waters tend to be dominated by large, long-lived species that produce extensive root mattes. The underlying sediment often contains high concentrations of carbonate, and the water is warm. In temperate waters, the seagrasses tend to be smaller, short-lived, with short, fine roots, and grow in principally siliciclastic sediment. The replacement ecosystems in the absence of seagrasses may also be different in different regions.

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Consequently, the primary controls on net carbon burial are different in different kinds of meadows. In areas with large seagrass species, the burial rate depends mainly on the type of seagrass and the meadow extent, while in areas with smaller seagrasses, abiotic factors are more important.

In addition, there are regional or even local differences in the importance of excess nutrients, tidal flow constriction, invasive species, bioturbation, and the likelihood that seagrasses will be able to migrate landward in response to sea-level rise. Even familiar indicators, like bulk stable isotopes, might have different meanings in different environments. For example, in the Red Sea lower δ¹⁵N in seagrass and macroalgae indicates oligotrophic conditions and more nitrogen fixation (Duarte et al 2018b), while off the west coast of Canada, lower δ¹⁵N in sinking particles indicates bloom conditions, with ample nutrients, and a short food chain (Johannessen et al 2005).

Given the extensive regional differences, it is not surprising that there has not been a single, consistent interpretation of the role of seagrass meadows in offsetting carbon emissions globally. Inter-regional cooperation could help to resolve this. Rather than making measurements in one type of environment and extrapolating to the world, it might be more effective to assess the potential to expand net, long-term carbon burial meadow by meadow, region by region, with techniques appropriate to each environment, and then sum the parts to estimate the whole. Collaboration among researchers from different parts of the world would facilitate this approach. It will be particularly important to include researchers from Africa, where there have been so few measurements to date.