In addition to the largest existing expanse of tropical forests, the Brazilian Amazon has among the largest area of mangroves in the world. While recognized as important global carbon sinks that, when disturbed, are significant sources of greenhouse gases, no studies have quantified the carbon stocks of these vast mangrove forests. In this paper, we quantified total ecosystem carbon stocks of mangroves and salt marshes east of the mouth of the Amazon River, Brazil. Mean ecosystem carbon stocks of the salt marshes were 257 Mg C ha −1 while those of mangroves ranged from 361 to 746 Mg C ha −1 . Although aboveground mass was high relative to many other mangrove forests (145 Mg C ha −1 ), soil carbon stocks were relatively low (340 Mg C ha −1 ). Low soil carbon stocks may be related to coarse textured soils coupled with a high tidal range. Nevertheless, the carbon stocks of the Amazon mangroves were over twice those of upland evergreen forests and almost 10-fold those of tropical dry forests.

1. Background

While it is recognized that the forests of the Brazilian Legal Amazon are significant global carbon sinks, this region also is among the largest expanses of mangrove forests in the world. There are approximately 1 071 084 ha of mangroves in Brazil [1], which is more than any other nation in the Americas. Approximately 85% of Brazil's mangroves are located on the northern Atlantic coast [2,3].

Given their potential values for the mitigation of climate change, numerous studies have focused on the carbon stocks of Amazonian upland forests, but few have investigated its blue carbon stocks. Our objectives were to quantify ecosystem carbon stocks of the salt marshes and mangroves of the legal Amazon in the state of Pará, Brazil. Additionally, we compared these mangroves to (i) mangroves from drier climates in Northeast (NE) Brazil, (ii) other mangroves of the world, and (iii) dominant upland vegetation types of northern Brazil. We hypothesized that ecosystem carbon stocks of the Amazon tidal wetlands would be greater than those of uplands because of greater carbon storage coupled with lower decomposition in wetland soils. Furthermore, we hypothesized that the ecosystem carbon stocks of Amazon mangroves would exceed those of drier regions of NE Brazil. This study is important because the mangrove forest along the equatorial Brazilian coastline is among the largest on earth. Yet few studies have quantified its ecosystem carbon stocks. Like most tropical coastal ecosystems, these areas are vulnerable to pressures from both land conversion and climate change.

2. Methods

We sampled total ecosystem carbon stocks (TECSs) of nine mangroves and three salt marshes east of the mouth of the Amazon River. Five mangroves and all the salt marshes were within the Rio Caeté Estuary near the city of Bragança. Three mangroves were sampled along the Rio Maruipe near the city of Salinópolis and one mangrove was sampled on the Rio Barreto near the city of São Caetano de Odivelas (table 1). All sampled stands of mangroves were tall (17–28 m in height) and largely dominated by red mangrove (Rhizophora mangle), black mangrove (Avicennia germinans) and white mangrove (Laguncularia racemosa). The salt marshes sampled included a low, medium and high salt marsh distributed along a gradient of increasing elevation from those ecotonal to mangroves to those located near upland ecotones. The low marsh was dominated by Distichlis sp., the medium marsh by Eleocharis sp. and the high marsh by Schoenoplectus sp.

Table 1.Site descriptive variables of mangroves and salt marshes of the Brazilian Amazon. Numbers are mean ± one standard error. Collapse site salinity (ppt) pH tree height (m) soil depth range (cm) tidal range (m) latitude longitude Mangroves São Caetano 17 ± 3 6.4 ± 0.1 29 ± 4 > 300 0.5–4.9 S00 44.949 W048 00.824 Caeté 20 ± 1 6.2 ± 0.1 28 ± 2 180–> 300 0.6–4.6 S00 58.860 W046 43.379 Mangue Sul 21 ± 2 6.5 ± 0.1 22 ± 1 > 300 0.6–4.6 S00 55.082 W046 40.759 Furo Do Chato 21 ± 1 6.2 ± 0.1 20 ± 1 150–195 0.6–4.6 S00 52.873 W046 39.138 Furo Grande 18 ± 2 6.5 ± 0.0 19 ± 1 260–> 300 0.6–4.6 S00 50.480 W046 38.316 Boca Grande 26 ± 1 6.2 ± 0.0 27 ± 1 220–> 300 0.6–4.6 S00 51.070 W046 38.224 Maruipe 8 ± 1 6.5 ± 6.6 25 ± 1 135–206 0.6–4.6 S00 39.296 W047 23.654 Barreto 23 ± 3 6.2 ± 6.0 17 ± 1 190–> 300 0.6–4.6 S00 39.335 W047 21.068 Salina 18 ± 3 6.5 ± 6.6 26 ± 1 170–270 0.6–4.6 S00 37.952 W047 22.044 Marshes Marisma high 3 ± 1 5.0 ± 0.2 — 165–> 300 0.6–4.6 S00 54.944 W046 40.890 Marisma medium 9 ± 0 4.5 ± 0.3 — > 300 0.6–4.6 S00 54.741 W046 40.998 Marisma low 21 ± 1 5.7 ± 0.1 — > 300 0.6–4.6 S00 54.812 W046 41.565

To determine the ecosystem carbon stocks, we closely followed methods that are thoroughly described in other studies [4,5]. Ecosystem carbon stocks include quantification of the carbon stored in trees, downed wood and soils (see detailed descriptions of all methods in the electronic supplementary material). In each sampled mangrove and salt marsh, we established six subplots and TECSs were determined in each sub-plot. Site results are the means of these subplots. Composition, tree density and mass of the mangroves were quantified through identification of the species and measurement of the diameter at 1.3 m height of all trees rooted within six 7-m radius circular plots at each subplot. The planar intersect technique, adapted for mangroves, was used to determine downed wood mass [4,6]. Soil carbon pools to the depths of indurated layers were measured at each of six subplots at all sites. Differences between carbon stocks in mangroves and marshes were tested with analysis of variance of untransformed data.

3. Results and discussion

In the salt marshes, increasing levels of soil salinity were unexpectantly coupled with increasing ecosystem carbon stocks along the gradient from high to low marshes (table 1 and figure 1). The total carbon stocks ranged from 197 Mg C ha−1 in the high marsh to 353 Mg C ha−1 in the low marsh. In addition to their location at the high end of the tidal gradient (ecotonal and above mangroves), marsh soils were finer textured (clayey) and less reduced than those of the mangroves. The mean soil carbon stocks of these marshes (257 Mg C ha−1; electronic supplementary material, table 1) are similar to, or slightly higher than, the Intergovernmental Panel on Climate Change (IPCC) default values for salt marshes on mineral soils (i.e. 226 Mg C ha−1, [7]). Figure 1. Ecosystem carbon stocks (Mg C ha−1) of mangroves and salt marshes from the Brazilian Amazon, Pará Brazil. TAGC, tree aboveground carbon; TBGC, tree belowground carbon.

In mangroves, the average aboveground tree biomass was 145 Mg C ha−1 and the average downed wood mass was 14 Mg C ha−1 (figure 1; electronic supplementary material, table 1). Total aboveground biomass comprised about 31% of the ecosystem carbon stock. The ecosystem carbon stocks of mangroves were significantly larger than those of salt marshes (p = 0.008; figure 1), although mean soil carbon did not significantly differ (p = 0.63).

The mean ecosystem carbon stocks of the Amazon mangroves, with an average precipitation of ≈2300 mm yr−1 [8], was 511 Mg C ha−1 (a range of 362 Mg C ha−1 to 746 Mg C ha−1; figure 2a). The mean ecosystem carbon stocks of mangroves from semiarid environments (≈1024 mm yr−1) ≈1000 km in distance but at similar latitudes (Ceará State, Brazil) were 413 Mg C ha−1 [5]. Ecosystem carbon stocks of these two regions were not significantly different (figure 2b). By contrast, other studies have reported a significant correlation of mangrove ecosystem carbon stocks with increasing rainfall [11]. We found no such relationship at the regional level, suggesting precautions with environmental modelling of C stocks based upon precipitation. However, aboveground biomass of the Amazon mangroves (159 Mg C ha−1) was significantly greater than that of the semiarid Northeast (72 Mg C ha−1; p = 0.001). This further underscores the difficulty of predicting TECSs based upon aboveground biomass and structure. Figure 2. Ecosystem carbon stocks of mangroves compared with other blue carbon and upland ecosystems. Panel (a) is a box and whisker plot of TECS of Brazilian mangroves and salt marshes. The rectangular part of the plots extend from the lower quartile to the upper quartile, covering the central half of each sample. The central lines within each box show the location of the sample medians. The plus signs indicate the location of the sample means. The whiskers extend from the box to the minimum and maximum values in each sample. There was NSD between mangroves from NE Brazil and the Amazon (p = 0.29). The carbon stocks between mangroves and marshes of the Amazon were significant (p = 0.004). Panel (b) shows the TECS of selected ecosystems of Brazil. The Amazon mangroves and salt marsh are from this study; the semiarid mangroves are from Kauffman et al. [5]; Amazon forest data are from Kauffman et al. [9]; Caatinga forest and Cerrado (savanna) data are from De Castro & Kauffman [10].

Combining mangroves of NE Brazil with those of this study, we calculated the mean ecosystem carbon stock of northern Brazil mangroves to be 473 Mg C ha−1. This is substantially below the global mangrove mean of 885 Mg C ha−1 [12]. This large difference between the global mean and that of the mangroves of NE Brazil and the Amazon lie in the soil carbon pool. The global mean soil carbon pool of mangroves (749 Mg C ha−1) [12] was twice that of Brazil Amazon mangroves (341 Mg C ha−1). Soil carbon pools of the Amazon mangroves were also much lower compared to carbon pools of tall mangroves from Liberia or Indonesia (901 or 879 Mg C ha−1, respectively [12,13]. However, the soil carbon pools were similar to those tall mangroves from the Ndougou Lagoon, Gabon (392 Mg C ha−1; [12]).

Possible explanations for the low carbon concentrations and pools of the Amazon mangroves could lie in the region's large tidal range, which may diminish anoxic soil conditions that would facilitate carbon accumulation [14]. Furthermore, the soils of the Amazon mangroves (and those of the Ndougou Lagoon, Southern Gabon) were coarse-textured, where soil organic matter would be more susceptible to decomposition and less likely to be sequestered to the extent found in mangroves with finer textured soils [15].

We found that the blue carbon stocks exceed those of upland tropical forest ecosystems in Brazil (figure 2b). The mean carbon stocks of the Amazon mangroves were over twice those of upland Amazon evergreen forests, exceeding their mean by about 245 Mg C ha−1. The mean carbon stocks of mangroves of NE Brazil were eight-fold greater than the surrounding upland tropical dry forests, exceeding their carbon mass by 364 Mg C ha−1. Finally, the mean carbon stocks of herbaceous-dominated salt marshes were almost two-fold greater than those of upland savannas of the Brazilian Cerrado, exceeding their mean ecosystem C stocks by 113 Mg C ha−1.

Soils and roots comprised a mean of 69% of the TECS, while 31% was sequestered in aboveground pools in mangroves. By contrast, about 32% of the carbon stock of upland tropical forests are in soils [16]. In addition to differences in the partitioning of carbon stocks, soil carbon in mangroves is lost in greater quantities following deforestation (land use). For example, greenhouse gas emissions arising from mangrove conversion to agriculture or aquaculture are 1067–3003 Mg CO 2 e ha−1 compared with emissions of 583 Mg CO 2 e ha−1 when Amazon rainforests are converted to cattle pasture [17]. Unlike the uplands, most of the greenhouse gas emissions (84%) associated with mangrove conversion originated from soil carbon pool losses. The vast extent of Brazilian mangroves coupled with the large quantities of greenhouse gas emissions that results from their deforestation underscores their potential value in climate change mitigation and for inclusion in adaptation strategies.

Ethics

Research was conducted according to Oregon State University ethical guidelines. There was no approval required for sampling in the locations where plots were established.

Data accessibility

The datasets supporting this article have been uploaded as part of the electronic supplementary material.

Authors' contributions

All of the authors: made substantial contributions to conception and design, and acquisition of data, and contributed to the analysis and interpretation of data; made contributions to the drafting of the article and revisions critical for important intellectual content; gave the final approval of the version to be published, and are in agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Competing interests

We have no competing interests.

Funding

Research funds were from the US Agency for International Development – the Sustainable Wetlands Adaptation and Mitigation Program. A.F.B. and L.E.O.G. were supported by CNPq/FAPES PELD-HCES grants 441243/2016-9 and 79054684/17, respectively. T.O.F. was supported by the National Council for Scientific and Technology Development (CNPq, process 308288/2014-9).

Footnotes

A contribution to the special feature ‘Blue Carbon' organised by Catherine Lovelock Electronic supplementary material is available online at http://dx.doi.org/10.6084/m9.figshare.c.4202267.