Carbon Stocks of Mangroves and Losses Arising from Their Conversion to Cattle Pastures in the Pantanos De Centla, Mexico

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Carbon stocks of mangroves and losses arising from their conversion to cattle pastures in the Pantanos de Centla, Mexico

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J. Boone Kauffman, Humberto Hernandez Trejo, Maria del Carmen Jesus Garcia, Chris Heider & Wilfrido M. Contreras

Wetlands Ecology and Management

ISSN 0923-4861

Wetlands Ecol Manage DOI 10.1007/s11273-015-9453-z

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Wetlands Ecol Manage DOI 10.1007/s11273-015-9453-z

ORIGINAL PAPER

Carbon stocks of mangroves and losses arising from their conversion to cattle pastures in the Pantanos de Centla, Mexico

J. Boone Kauffman . Humberto Hernandez Trejo . Maria del Carmen Jesus Garcia . Chris Heider . Wilfrido M. Contreras

Received: 23 January 2015 / Accepted: 1 August 2015 Ó Springer Science+Business Media Dordrecht 2015

Abstract The conservation of mangroves and other conversion and 3-fold greater than emissions from coastal ‘‘blue carbon’’ ecosystems is receiving height- Amazon forest to pasture conversion. However, we ened attention because of recognition of their high found that limiting ecosystem carbon stocks differ- ecosystem carbon stocks as well as vast areas under- ences to the surface 1 m or even 2 m soil depth will going land conversion. However, few studies have miss losses that occurred from deeper horizons. paired intact mangroves with degraded sites to deter- Mangrove conversion to other land uses comes at a mine carbon losses due to land conversion. To address great cost in terms of greenhouse gas emissions as well this gap we quantiﬁed total ecosystem carbon stocks in losses of other important ecosystem services. mangroves and cattle pastures formed from mangroves in the large wetland complex of the Pantanos de Keywords Blue carbon Á Carbon stocks Á Carbon Centla in SE Mexico. The mean total ecosystem dynamics Á Cattle pastures Á Climate change carbon stocks of fringe and estuarine tall mangroves mitigation Á Emissions Á Land use Á Mangroves was 1358 Mg C/ha. In contrast the mean carbon stocks of cattle pastures was 458 Mg C/ha. Based upon a biomass equivalence of losses from the top 1 m Introduction of mangrove soils, the losses in carbon stocks from mangrove conversion are conservatively estimated at Mangroves are highly productive ecosystems which

1464 Mg CO2e/ha. These losses were 7-fold that of are ecologically and economically important at local emissions from tropical dry forest to pasture to global scales (Alongi 2014, UNEP 2014). Their disproportionate contribution to carbon storage sug- gest that their conservation and restoration can be a J. B. Kauffman (&) Department of Fisheries and Wildlife Oregon State pathway to help ameliorate greenhouse gas emissions. University, Corvallis, OR 97331, USA Carbon emissions resulting from mangrove con- e-mail: [email protected] version are uncertain, owing in part to a lack of broad- scale data on the amount of carbon stored in these H. Hernandez Trejo Á M. del Carmen Jesus Garcia Á W. M. Contreras ecosystems, particularly belowground and how land Universidade Juarez Autonoma de Tabasco, use may affect these stocks (Donato et al. 2011). While Villahermosa, TAB, Mexico there is a growing but limited body of literature on the carbon stocks of mangroves (see Alongi 2014; Donato C. Heider Watershed Professionals Network, Philomath, OR 97370, et al. 2011; UNEP 2014), the carbon stock losses and USA greenhouse gas emissions associated with land use are 123 Author's personal copy

Wetlands Ecol Manage practically non-existent (but see Kauffman et al. (Fig. 1). The Pantanos de Centla is the large wetland 2014b). This is a barrier to the establishment of complex of the delta of Grijalva and Usumacinta ecosystem values related to mangrove conservation or Rivers. These two rivers contain 28 % of all the restoration activities for either climate change miti- surface water in Mexico. This basin is second to the gation or adaptation strategies. Mississippi River basin in freshwater contribution to Our first objective of this study was to quantify the the Gulf of Mexico, and seventh in discharge world- carbon stocks of fringe and estuarine mangroves of the wide (Arriaga Cabrera et al. 1998). Most of the sites Pantanos de Centla, Mexico. While carbon stocks were located in the Rio San Pedro y Pablo Pedro information has been reported for the Caribbean regions watershed which is a distributary of the Rio Usumac- of Mexico (Adame et al. 2013) we know of no studies inta which flows directly into the Gulf of Mexico. The that have measured mangrove carbon stocks associated rainfall in the region averages 1693 mm per year with with the Mexican side of the Gulf of Mexico. the majority falling during the months of June to Conversion of tropical forest to cattle pastures has October. The mean annual temperature is 27 °C. been a common practice throughout the Neotropics. In All mangroves were tall with a mean height [10 m uplands, most of the carbon emissions associated with and usually occurring on the margins of rivers, conversion is from the loss of the aboveground estuaries and coastal fringe (Table 1). In addition to biomass. This is unlike conversion of mangroves to mangroves, we sampled three cattle pastures that had shrimp ponds where large losses of soil carbon pools been formed from, and were surrounded by, tall followed conversion (Kauffman et al. 2014b). Con- mangroves. Based upon interviews with local people, version of mangrove to cattle pasture has been a two of the pastures were established about 30 years common land use in Mexico and other areas of Central before sampling (the Cometa and Vidal pastures) and and South America although many are apparently now one had been cleared 6–7 years prior to sampling (the being abandoned (Guerra-Martıńez and Ochoa-Gaona Gallego pasture). All pastures were currently being 2008). To obtain an idea of how this land conversion grazed by cattle. affects carbon stocks and hence greenhouse gas emissions, we paired three mangrove sites with Field sampling adjacent cattle pastures. Our objectives were to examine how mangrove conversion to cattle pasture We determined the composition, structure, and ecosys- affects the structure and size of carbon stocks, and how tem carbon stocks of 10 different coastal wetlands this might compare to pasture conversion in upland including three coastal fringe mangrove sites; four forests riverine or estuarine mangrove sites, and three cattle Our specific research questions included: What are pastures. The coastal fringe mangroves occur along the the carbon stocks of the mangroves of the Pantanos de fringes of protected shorelines and islands (Lugo and Centla? How do they differ between oceanic (coastal Snedaker 1974). Fringe mangroves were ecotonal to fringe) and estuarine mangroves? What are the carbon beach or beach-strand communities and the open ocean. stocks of cattle pastures that were formed on sites The estuarine mangroves were the floodplain forests previously occupied by mangroves? What are the occurring along river and creek drainages of the San potential emissions that could arise from conversion of Pedro y Pablo and Grijalva rivers. The riverine or mangrove to cattle pasture? And finally, how do these estuarine mangroves sampled in this study were located compare to losses associated with conversion of between 6 and 19 km upstream from the mouth of the upland tropical forest to pastures? rivers (Fig. 1;Table 1). They bordered both blackwater and clear water riverine systems. Within each site, ecosystem C stocks (above- and Methods belowground) were measured following methodolo- gies outlined by Kauffman and Donato (2012) and Study site Kauffman et al. (2014a). At each mangrove and pasture site, six plots were established 20 m apart The study area is located in The Pantanos de Centla along a 100 m transect positioned in a perpendicular Mexico in the states of Tabasco and Campeche direction from the marine or riverine ecotone. At each 123 Author's personal copy

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Fig. 1 Plot locations within the Pantanos de Centla study area, Tabasco and Campeche, Mexico. Mangroves were delineated by Giri et al. (2013). Triangles represent the mangrove sample sites. The dark line represents the 25 km focus area along the San Pedro y San Pablo River

plot, we collected data necessary to calculate total C the first three in the plots that we sampled; C. erectus stocks derived from standing tree biomass, downed was only observed on the upland edges of the wood (dead wood on forest floor), grasses, and soils to mangroves. Composition, tree density, and basal the depths of the marine sands. area of the mangroves were quantified through measurements of the species and diameter at 1.3 m Biomass of trees and shrubs height (diameter at breast height or dbh) of all trees rooted within each plot of each transect. Plot size for Four species of mangroves occur in the mangrove stands tree measurements was 154 m2 (7 m radius) for sampled: Rhizophora mangle L. (Rhizophoraceae), Avi- trees [5 cm dbh and a nested plot with a radius of cennia germinans (L.) Stearn (Avicenniaceae), Lagun- 2 m for trees with a dbh of \5 cm. The diameter of cularia racemosa (L.) Gaertn., (Combretaceae) and trees of R. mangle was measured at the main branch, Conocarpus erectus L. (Combretaceae). We encountered 30 cm above the highest prop root.

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Table 1 Characteristics of sampling locations within the Pantanos de Centla, Mexico Location Type Latitude Longitude Salinity pH Soil depth Dominant species (ppt) (cm) (density- trees/ha)

Forests Grijalva Coastal Fringe N18°36.3370 W092°41.0450 8.0 ± 1.4 7.0 ± 0.0 108 ± 18 R. mangle (5121) Boca Pedro Oeste Coastal Fringe N18°39.1120 W092°27.4750 3.3 ± 0.2 7.4 ± 0.1 227 ± 11 R. mangle (1523) Boca Pedro Este Coastal Fringe N18°38.9080 W092°28.4780 4.0 ± 0.5 7.7 ± 0.1 191 ± 29 R. Mangle (1164) Sabalo Estuarine-Black water N18°35.6380 W092°28.0520 13.3 ± 0.8 6.7 ± 0.0 275 ± 25 R. mangle (1219) Cometa Estuarine-Black water N18°29.5300 W092°25.7190 4.0 ± 0.6 7.1 ± 0.1 [300 L. racemosa (1821) Vidal Estuarine-Clear water N18°34.0260 W092°25.9340 10.9 ± 2.6 6.7 ± 0.0 [300 R. mangle (2923) Gallego Estuarine-Clear water N18°35.7100 W092°26.9060 18.7 ± 1.6 6.9 ± 0.0 [300 L. racemosa (6355) Pastures Pastizal Cometa Estuarine-Black water N18°29.7290 W092°25.3880 1.7 ± 0.6 7.5 ± 0.2 [300 Grass/sedge Pastizal Vidal Estuarine-Clear water N18°34.0260 W092°25.9340 13.4 ± 2.5 7.5 ± 0.1 [300 Grass/sedge Pastizal Gallego Estuarine-Clear water N18°35.6250 W092°26.8560 11.8 ± 1.0 7.1 ± 0.1 [300 Grass/sedge

Allometric equations were used to calculate tree (Kauffman and Donato 2012). The biomass of trees biomass. We examined several equations developed of Status 3 was calculated as the biomass of the for the species encountered in this study. Of consid- mainstem only (Table 2). This also required estima- eration was the importance of using locally-derived tion of the dead tree height in this decay class. equations, those encompassing the dbh range of the mangroves in this study, and a sufﬁcient sample size to Biomass of grasses and grass-likes develop a realistic estimate of biomass. The allometric equations presented by Day et al. (1987) were The plot design in pastures was identical to that of developed in the Pantanos de Centla region but only mangroves except we also collected graminoid for trees 0–10 cm dbh, which would not account for biomass. In each of the six macroplots established the numerous individuals larger than this that were along the 100 m transect in pastures we harvested all encountered in this study. As such, other species- aboveground graminoid biomass in two 720 cm2 speciﬁc models were selected. For L. racemosa we microplots (18.5 9 39 cm rectangular plots). These used the equations developed in Florida by Smith and microplots were established on two of the wood Whelan (2006). For R. mangle and A. germinans we transects at a distance of 5 m from the plot center. used the equations developed in French Guiana by These samples were placed in a paper bag and Fromard et al. (1998). These equations were selected transported back to the laboratory where they were for analysis as they represented the best combination dried to a constant mass for dry-weight biomass of diameter range and sample size and most closely determination. Belowground biomass from pastures tracked the relationship of diameter with biomass to was predicted using a root: shoot ratio of 0.58 which those of the Day et al. (1987) study. Belowground root was developed from grasses of cattle pastures in biomass for mangrove trees was calculated using the Veracruz, Mexico (Jaramillo et al. 2003a, Hughes formula by Komiyama et al. (2005). Tree carbon et al. 2000). Root carbon stocks were calculated based content (C) was calculated from biomass by multiply- upon the mean carbon concentration of roots in these ing by a factor of 0.48 for aboveground and 0.39 for plots which was 43.7 % (Hughes et al. 2000). belowground biomass (Kauffman and Donato 2012). Standing dead trees were included in aboveground Downed wood biomass calculations. For each dead tree, the dbh was measured and assigned to one of three decay classes: We used the planar intersect technique adapted for Status 1- dead trees without leaves, Status 2- dead mangroves to calculate mass of dead and downed trees without secondary branches, and Status 3- dead wood (Kauffman and Donato 2012; Adame et al. trees without primary or secondary branches 2013). At the center of each plot, four 14 m transects

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Table 2 Plant related biomass and carbon pools (Mg/ha) of tall mangroves of the Pantanos de Centla, Mexico Site name Live AG* Dead AG Live BG Dead Live AG Live Dead Dead Downed Total AG tree tree biomass BG C (trees) BG C BG C AG C wood C carbon biomass biomass biomass

Grijalva 223 ± 88 98 ± 49 141 ± 29 24 ± 8 107 ± 42 55 ± 11 10 ± 324± 811± 3 141 ± 45 Boca Pedro Oeste 264 ± 22 24 ± 895± 812± 3 127 ± 11 37 ± 35± 112± 410± 1 149 ± 11 Boca Pedro Este 217 ± 58 4 ± 280± 24 3 ± 1 104 ± 28 31 ± 91± 12± 116± 4 122 ± 27 Sabalo 265 ± 49 64 ± 34 127 ± 28 27 ± 14 127 ± 23 50 ± 11 11 ± 631± 16 17 ± 4 174 ± 13 Cometa 114 ± 20 3 ± 184± 14 4 ± 155± 10 33 ± 61± 11± 07± 163± 9 Vidal 255 ± 30 156 ± 84 191 ± 18 52 ± 28 122 ± 14 74 ± 720± 11 74 ± 40 40 ± 7 236 ± 36 Gallego 117 ± 15 8 ± 388± 11 5 ± 256± 734± 42± 14± 119± 778± 7 Fringe mangroves 234 ± 15 42 ± 29 105 ± 18 13 ± 6 113 ± 741± 75± 212± 612± 2 137 ± 8 Estuarine mangroves 187 ± 42 58 ± 36 122 ± 25 22 ± 11 90 ± 20 48 ± 10 9 ± 428± 17 21 ± 7 138 ± 41 All mangroves 208 ± 25 51 ± 22 115 ± 15 18 ± 7 100 ± 12 45 ± 67± 321± 10 17 ± 4 138 ± 22 Data are mean and standard error * AG aboveground biomass, BG belowground biomass were established. The first was established in a were not encountered before 100 cm depth). At each direction that was offset 45o from the azimuth of the sampling site, the depth to parent materials (marine main transect. The other three were established 90o sediments/sands) was measured. The soil depth was clockwise from the first transect. Along each transect, measured at three locations near the center of each plot the diameter of any downed wood intersecting using a graduated aluminum probe. When soils thetransect was measured. Wood debris C2.5 cm were [3 m in depth we limited the calculation of soil but \7.5 cm in diameter (hereafter ‘‘small’’ debris) carbon pools to 3 m. We also determined pore water at the point of intersection was measured along the last salinity at the time of sampling with a refractometer 5 m of the transect. Wood debris C7.5 cm in diameter and soil pore water pH with a portable pH meter. (hereafter ‘‘large’’ debris) at the point of intersection Samples of a known volume were collected in the was measured from the second meter to the end of the field, dried at 60 °C to constant mass, and then transect (12 m length in total). Large downed wood weighed to determine bulk density. was separated in two decay categories: sound and Laboratory analysis was conducted at analytical rotten. Wood debris was considered rotten if it visually laboratory at Universidad Jua´rez Autońoma de appeared decomposed and broke apart when kicked. Tabasco (UJAT). In the laboratory, the concentration To determine wood mass we used data of specific of C and N were determined using the dry combustion gravity of downed wood from mangroves of the method (induction furnace) with a Shimadzu TOC Yucatan, Mexico and reported by Adame et al. (2013). Analyzer. This analyzer determines both total carbon Downed wood was converted to C using factor of 0.50 as well as inorganic carbon enabling us to accurately (Kauffman and Donato 2012). report total organic carbon in our samples. Bulk density and carbon concentration were then combined Soil carbon and nutrients with plot-specific soil depth measurements to determine the soil C stocks. At each plot, fixed-volume soil samples were collected Differences among soil properties, biomass, and for bulk density and nutrient concentration using a carbon stocks among vegetation types were tested peat auger consisting of a semi-cylindrical chamber of with analysis of variance (ANOVA). This included a 6.4 cm radius. This auger is efficient for collecting tests between the mangrove types and tests between relatively undisturbed cores from wet soils in man- the paired mangrove and cattle pastures. If the groves (Donato et al. 2011). The core was systemat- ANOVA was significant, a least significant difference ically divided into depth intervals of 0–15, 15–30, (LSD) test was performed to determine which means 30–50, 50–100 cm and [100 cm (if parent materials were significantly different.

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Emissions from conversion of forests to cattle Calculating losses only to 1 m also allowed compar- pasture isons of losses from mangrove forest conversion with emissions that arise from the conversion of Neotropical We calculated the potential emissions from conversion upland forests to cattle pastures. The ecosystem losses of mangrove to pasture using two different protocols. are reported as potential CO2 emissions, or CO2 One common Intergovernmental Panel on Climate equivalents (CO2e)—obtained by multiplying C values Change (IPCC) protocol for tracking changes in carbon by 3.67, the molecular ratio of CO2 to C. While reported stocks and predicting emissions from land cover change as the CO2e, these estimates account only for changes in in forestry is the stock-change approach (IPCC 2003). ecosystem C in situ. While likely to be small compared Using this approach, we calculated potential emissions to greenhouse gas emissions, some of the carbon lost in that occurred over the life of the pastures sampled in this the pastures may be transferred to other communities via study. Included in this analysis was all aboveground erosion, groundwater transfer, or during the frequent biomass and soils to a depth of 3 m. pasture fires (particulate losses in smoke) which would Differences in carbon stocks were converted to reduce the losses via atmospheric emissions. emissions using the formula: Scaling carbon stocks of mangroves to watershed DCLU ¼ DC þ DC þ DC þ DC AB BB DW SOC scales where CLU = change in carbon stocks (or total C emissions or sequestration) due to land use; CAB = We scaled site level carbon stock measurements to a Change in aboveground biomass C pool; CBB = landscape bounded by the lower reaches of the Change in belowground biomass C pool; CDW = subwatersheds of Rio Grijalva, Rio Usumacinta, and Change in dead wood C pool; CSOC = Change in soil Rio San Pedro y San Pablo Rivers. We also included organic carbon. the Laguna de Pomi y Atasta in the Laguna de Soil collapse due to deforestation (Krauss et al. Te´rminos watershed (Fig. 1). The inland extent 2010; Langat et al. 2014), the influences of trampling followed natural terrain boundaries at or near the (Kauffman et al. 2004), and the absence of a reliable upper limits of mapped mangrove vegetation (Giri marker in the deep alluvial soils of the sampled et al. 2010). This area is approximately 290,000 ha in mangroves and pastures compounds difficulties in the size and extends *130 km along the coastline from comparisons of soil properties based upon depth or Paraiso (Tabasco) in the west to Ciudad del Carmen volume. At a similar depth there is simply more mass (Campeche) in the east. This area includes the lower of soil in the pastures than in the mangroves. Therefore 990 km2, or 37 % of the Pantanos de Centla Biosphere we also analyzed carbon loss and potential emissions Reserve) (Fig. 1). Approximately 84,523 ha (29 %) of from conversion of mangrove to pasture based upon the assessment area were dominated by mangroves. the biomass equivalence of the mass of mineral soil in only the top 1 m of the mangrove sites. Land cover change—GHG emissions In the biomass equivalence approach, the differ- from conversion to pastures at the watershed scale ences in soil carbon were determined by calculating the mineral soil mass in the top 1 or 2 m meter of soils The majority of the field sampling was concentrated in in intact mangroves and then calculating the equiva- the mangrove area within 500 m of the banks of the lent depth or volume of that mass in the adjacent San Pedro y San Pablo River (Fig. 1). To scale pastures. Mineral soil mass was determined through changes in carbon stocks due to land conversion from subtraction of the carbon density from the soil bulk mangroves to a watershed scale, we determined land density. Similar methods have been used to determine cover in a 1930 ha area that extended 500 m from both losses of carbon due to conversion in cattle pastures in sides of the river edge and extended 25 km upstream Amazonian uplands (Kauffman et al. 1998). This is a from the river terminus. more conservative measure of carbon emissions as we Land cover types were manually delineated and only compare losses from the top meter of mangrove interpreted at fine scales (1:4000) within this zone to soil under the assumption that there are few distur- include the major broad land cover types: mangrove, bances below this depth. pastures, marsh/wetland areas (no trees), other forest 123 Author's personal copy

Wetlands Ecol Manage types, infrastructure (roads, towns), and other minor pasture, some residual wood was still present and features (river oxbows and coastal strand). Polygons totaled 7 Mg C/ha. The total aboveground carbon pool were digitized using available aerial image data (ESRI of the pastures was 9 Mg C/ha which was only about 2006) with a targeted minimum polygon size of 7 % of the mean aboveground carbon pool of the 0.5 ha. A total of 136 polygons were delineated and paired mangroves (127 Mg C/ha, Tables 2, 3). interpreted with a median polygon size of 3.7 ha (average 14.2 ha) for the 1930 ha area. Soils

Soil depths were greater in the estuarine mangroves Results compared to the fringe mangroves (Table 1). This was especially true for the Grijalva fringe mangrove site Aboveground biomass and pools with a mean depth to the marine sands of 108 cm. The other two sampled fringe mangroves had depths of 227 All of the mangroves sampled in this study were and 191 cm. In contrast mean depth of the estuarine dominated by R. mangle (mean density of 1535 ± 521/ sites was 275 cm for the Sabalo site and [300 cm for ha) with the exception of the Cometa and Gallego sites the others. We found few other differences comparing which were dominated by L. racemosa (Table 1). soil properties of the fringe and estuarine mangroves. Avicennia germinans was not common (mean density Soils of the Grijalva fringe mangrove were consis- of 17 ± 10/ha) and this may reflect the fact that all the tently lower in carbon that the other mangrove sites. In soils of the sampled sites were relatively low in salinity contrast, the two sampled estuarine sites associated with a range of 3–19 ppt. This salinity level reflects the with blackwater estuaries (Cometa and Sabalo) had large inputs of freshwater into these mangroves during consistently higher carbon concentrations for the full flooding events. Total mean tree density of the sites was soil profile depth (i.e., [13 % at all sampled depths; 2875 ± 783/ha; density was as high as 6355 trees/ha in Table 4). the Gallego site, characterized as a dense stand of young The total soil carbon pools varied greatly among the L. racemosa. tall mangroves; from 137 Mg C/ha at the Grijalva site Aboveground tree biomass ranged from 114 Mg/ha to 2002 Mg C/ha at the Cometa site. At the low end, in the Cometa site to 265 Mg/ha in the Boca Pedro the Grijalva site was significantly different from all Oeste site (Table 2). There were no significant differ- other sites. In contrast, at the high end the soil carbon ences when comparing the estuarine to the fringe sites stocks of the Boca Pedro Oeste, Boca Pedro Este, and but significant differences at the site level did exist. Cometa sites all exceeded 1330 Mg C/ha and were The Cometa and Gallego sites were ecotonal to cattle significantly different than the other sampled man- pastures with apparent recent use (i.e., logging was groves (P \ 0.05). apparent at these sites). These sites were the lowest in There were dramatic differences in the soil prop- aboveground tree biomass and in total aboveground erties between the mangroves and pastures (Table 4). carbon (P = 0.0005). The mean bulk density of the pasture soils was twice While all sites were dominated by tall mangroves that of mangroves (1.02 compared to 0.49 g/cm3 for there was high variation in the total aboveground carbon mangroves; (P \ 0.0001). The mean soil carbon pools, with a range of 63–236 Mg C/ha among sites. The concentration in mangroves was 13.1 % compared to lowest aboveground carbon pools were measured in the 3.1 % for cattle pastures (P \ 0.0001). Finally, the exploited Cometa and Gallego mangrove sites. How- carbon density was 0.038 g C/cm3 in mangroves and ever, even in sites with no apparent disturbances and 0.023 g C/cm3 in the pastures (P \ 0.0001). These dominated by R. mangle, aboveground carbon pools differences were apparent even at soil ranged from 122 to 236 Mg C/ha (P \ 0.001). depths [100 cm. For example, at this depth soil bulk Cattle pastures were dominated by grasses and density at the Cometa sites was 0.23 g/cm3 in the sedges with few woody plants present. The mean mangrove and 1.29 g/cm3 in the pasture. The carbon aboveground graminoid biomass of all pastures was concentration in the mangrove at this site was 34.4 % 14 ± 2 Mg/ha (Table 2). In the younger Gallego compared to 0.67 % in the pasture (Table 4).

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Total ecosystem carbon stocks significant difference when testing among the soil carbon pools of the pasture sites. The soil carbon and The total ecosystem stocks for mangrove sites varied the ecosystem carbon stocks of the younger 7-year old greatly from a minimum of 342 Mg C/ha at the Gallego pasture was significantly higher than that of Grijalva site to a maximum of 2099 Mg C/ha at the the older (30-year) Cometa and Vidal pastures. Soil Cometa site (Fig. 2). The mean ecosystem carbon carbon loss was 23 % in the Gallego pasture compared stock for the mangroves was 1358 Mg C/ha and was to [70 % in the older pastures, suggesting there may 458 Mg C/ha for the cattle pastures. Similar to soil be continued soil carbon loss for years after pasture pools, the Grijalva site was significantly different than formation. all other sites at the low end and the Cometa, Boca Finally, we can examine potential greenhouse

Pedro Oeste and Boca Pedro Este were significantly emissions on a CO2 equivalence (CO2e) basis arising different than all other sites at the high end. Soil from conversion of mangroves to pastures (Fig. 3b; carbon pools comprised a mean of 86 % of the total IPCC 2003). The mean potential emission from ecosystem pool with range of 59 at the Grijalva site to mangrove conversion to pasture was 1464 Mg CO2e/ 97 % at the Cometa site. Soils comprised [79 % of ha. Of this emission estimate, about 863 Mg CO2e/ha the total ecosystem carbon pool at all other sites. Soils arose from soil sources with about 601 Mg CO2e/ha comprised [98 % of the total ecosystem carbon stock coming from plant carbon pools. The total potential in the pastures. emissions ranged from 786 in the Gallego site to 2173 In comparing the mass of mineral soil between in the Vidal site (Fig. 3b). mangroves and pastures, we found that the equivalent soil mass of 1 m in the mangroves occurred at 23.9 cm depth in the Cometa pasture, 80.6 cm in the Gallego Mangrove carbon stocks at the landscape scale pasture, and 42.1 cm in the Vidal pasture. At all pasture sites the carbon stocks were significantly lower The 290,000 ha landscape dominated by the wetland than those of the paired mangrove sites (P \ 0001; associated with the Grijalva, Usumacinta and eastern Fig. 3a). Carbon stock declines due to pasture con- side of the Laguna Terminos watersheds is a diverse version ranged from 214 Mg C/ha in the younger mosaic of marshes, freshwater and upland tropical Gallego pasture to 592 Mg C/ha in the older Vidal forests, livestock pastures and approximately pasture with a mean loss of 399 Mg C/ha using the 84,523 ha of mangroves. We estimate the ecosystem biomass equivalence approach to a 1 m depth. The soil carbon stocks associated with the mangroves to be 115 component accounted for a mean of 59 % of the Tg C (95 % confidence range: 65–165 Tg C). ecosystem carbon loss due to conversion. The above Within the 1930 ha focus area along the low- ground carbon stocks declined by 94 % and soil er *25 km of the San Pedro y San Pablo River, carbon stocks declined by 43 % due to conversion mangroves and pastures were the dominant land cover (Fig. 3a). type, representing nearly the same cover area (38 % of Soil carbon pools were not significantly different the total). Mangroves covered an area of 727 ha and when testing between the three mangrove sites that pastures covered 736 ha. Marshes and other non- had been paired with pastures. Yet there was a forested wetlands represented 17 % of the land area

Table 3 Aboveground pasture biomass (Mg/ha) and the non-soil carbon pools (Mg/ha) of pastures, Pantanos de Centla, Mexico Pasture site AG* graminoid biomass AG graminoid C Downed wood C BG C Total AG C pool

Pastizal cometa 15 ± 37± 10± 04± 110± 2 Pastizal gallego 8 ± 10 4 ± 17± 22± 06± 1 Pastizal vidal 19 ± 58± 20± 05± 114± 3 All pastures 14 ± 26± 12± 24± 19± 1 Numbers are mean ± one standard error * AG aboveground, BG belowground

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Table 4 The bulk density (g/cm3), carbon density (g/cm3), carbon concentration (%), and carbon mass (Mg/ha) of soils partitioned by depth in mangroves and pastures, Pantanos de Centla, Mexico Site Soil depth (cm) 0–15 15–30 30–50 50–100 [100

Grijalva Bulk density 0.45 ± 0.14 0.53 ± 0.16 0.85 ± 0.16 0.92 ± 0.12 0.00 ± 0.00 Carbon density 0.01 ± 0.01 0.02 ± 0.00 0.01 ± 0.01 0.01 ± 0.00 0.00 ± 0.00 Carbon concentration 4.06 ± 2.84 4.72 ± 2.22 5.73 ± 4.94 0.86 ± 0.44 0.00 ± 0.00 Carbon mass 18.43 ± 9.63 24.42 ± 6.87 28.38 ± 14.30 29.97 ± 15.45 0.00 ± 0.00 Boca Pedro Oeste Bulk density 0.42 ± 0.05 0.59 ± 0.05 0.49 ± 0.03 0.39 ± 0.03 0.26 ± 0.01 Carbon density 0.04 ± 0.00 0.04 ± 0.00 0.04 ± 0.01 0.06 ± 0.01 0.08 ± 0.02 Carbon concentration 9.91 ± 1.01 7.52 ± 0.95 7.71 ± 1.70 15.68 ± 3.04 29.24 ± 6.09 Carbon mass 58.61 ± 2.92 62.92 ± 4.98 71.31 ± 14.54 298.38 ± 57.37 1124.53 ± 236.99 Boca Pedro Este Bulk density 0.39 ± 0.03 0.29 ± 0.05 0.35 ± 0.03 0.44 ± 0.06 0.49 ± 0.17 Carbon density 0.02 ± 0.01 0.03 ± 0.01 0.05 ± 0.01 0.04 ± 0.01 0.04 ± 0.01 Carbon concentration 6.39 ± 2.05 14.29 ± 3.62 15.77 ± 1.87 9.67 ± 3.38 13.76 ± 5.66 Carbon mass 35.91 ± 11.98 49.54 ± 10.91 109.25 ± 3.51 182.79 ± 48.27 711.85 ± 240.58 Sabalo Bulk density 0.22 ± 0.01 0.25 ± 0.01 0.34 ± 0.05 0.32 ± 0.05 0.37 ± 0.13 Carbon density 0.04 ± 0.00 0.04 ± 0.00 0.04 ± 0.01 0.04 ± 0.01 0.05 ± 0.02 Carbon concentration 18.24 ± 1.41 16.79 ± 1.08 13.39 ± 1.28 15.58 ± 3.35 22.47 ± 7.48 Carbon mass 59.37 ± 2.96 63.91 ± 4.58 88.74 ± 12.29 211.01 ± 32.72 1022.49 ± 316.87 Manglar Cometa Bulk density 0.12 ± 0.01 0.18 ± 0.05 0.33 ± 0.06 0.39 ± 0.07 0.23 ± 0.01 Carbon density 0.03 ± 0.00 0.04 ± 0.00 0.05 ± 0.01 0.04 ± 0.01 0.08 ± 0.01 Carbon concentration 28.02 ± 2.77 28.16 ± 4.41 17.44 ± 2.95 12.74 ± 2.44 34.44 ± 3.71 Carbon mass 49.37 ± 4.34 60.87 ± 4.99 103.27 ± 12.39 215.35 ± 7.14 1573.09 ± 175.33 Manglar Vidal Bulk density 0.42 ± 0.09 0.47 ± 0.11 0.59 ± 0.13 0.65 ± 0.14 0.90 ± 0.05 Carbon density 0.04 ± 0.00 0.04 ± 0.01 0.02 ± 0.01 0.04 ± 0.01 0.02 ± 0.00 Carbon concentration 12.73 ± 2.88 10.60 ± 2.78 6.18 ± 2.53 9.59 ± 3.63 2.41 ± 0.53 Carbon mass 62.20 ± 6.11 55.46 ± 8.27 47.58 ± 15.16 190.32 ± 57.60 424.79 ± 97.95 Manglar Gallego Bulk density 0.44 ± 0.06 0.53 ± 0.03 0.59 ± 0.05 0.59 ± 0.05 0.97 ± 0.11 Carbon density 0.04 ± 0.00 0.04 ± 0.00 0.04 ± 0.00 0.03 ± 0.00 0.02 ± 0.00 Carbon concentration 8.54 ± 0.78 7.78 ± 0.66 6.62 ± 0.71 6.03 ± 0.76 2.28 ± 1.06 Carbon mass 54.58 ± 5.09 58.32 ± 2.81 98.19 ± 17.68 171.27 ± 14.22 335.56 ± 92.19 Pastizal Cometa Bulk density 0.64 ± 0.03 0.97 ± 0.07 1.22 ± 0.02 1.29 ± 0.04 1.29 ± 0.04 Carbon density 0.05 ± 0.01 0.05 ± 0.01 0.01 ± 0.00 0.01 ± 0.00 0.01 ± 0.00 Carbon concentration 7.89 ± 1.05 5.325 ± 1.25 0.90 ± 0.27 0.67 ± 0.36 0.67 ± 0.36 Carbon mass 73.66 ± 7.70 72.99 ± 16.00 21.99 ± 5.68 41.84 ± 10.15 167.38 ± 40.60 Pastizal Vidal Bulk density 1.20 ± 0.05 1.35 ± 0.12 1.21 ± 0.09 1.34 ± 0.13 1.07 ± 0.09 Carbon density 0.03 ± 0.01 0.02 ± 0.00 0.01 ± 0.00 0.01 ± 0.00 0.01 ± 0.00 123 Author's personal copy

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Table 4 continued Site Soil depth (cm) 0–15 15–30 30–50 50–100 [100

Carbon concentration 2.66 ± 0.73 1.70 ± 0.48 1.01 ± 0.25 0.59 ± 0.14 1.28 ± 0.46 Carbon mass 45.31 ± 11.44 31.49 ± 7.27 22.20 ± 4.62 37.81 ± 8.27 266.28 ± 87.04 Pastizal Gallego Bulk density 0.47 ± 0.05 0.67 ± 0.07 0.70 ± 0.06 0.78 ± 0.02 1.04 ± 0.05 Carbon density 0.03 ± 0.00 0.04 ± 0.00 0.03 ± 0.01 0.02 ± 0.01 0.01 ± 0.00 Carbon concentration 7.94 ± 1.20 6.67 ± 1.35 5.15 ± 1.37 2.40 ± 0.71 1.26 ± 0.21 Carbon mass 51.85 ± 3.94 61.19 ± 6.50 67.15 ± 18.32 90.73 ± 26.37 259.05 ± 41.46 Numbers are mean ± one standard error

2500

Live AGC Dead AGC 2000 Downed wood LIVE BGC Dead BGC 0-15 15-30 1500 30-50 50-100 >100

1000 C Stock (Mg/ha)

500

0 Griljavla Boca Pedro Boca Pedro Sabalo M Cometa M Gallego M Vidal P Cometa P Gallego P Vidal Oeste Este

Fig. 2 The total ecosystem carbon stocks (Mg/ha) of mangroves, and cattle pastures converted from mangroves at the Pantanos de Centla, Mexico. Vertical bars are one standard error

(336 ha) and other (non-mangrove) forested lands estimated to result in a total net loss of 6 accounted for 5 % (94 ha) of the area. Other land 1.08 9 10 Mg CO2e. cover types including roads and towns, coastal strand and other water features represented only a minor amount of land area (\2 % of the plot). Discussion The carbon stock associated with the 727 ha of mangroves within the 1,930 ha focus area was Mangroves are among the most carbon-rich forests in estimated to be 9.87 9 105 Mg C. Although nearly the tropics, containing on average about 965 Mg/ha equal in area to mangroves, carbon stocks in pastures (UNEP 2014). The mangroves in this study ranged would only be about one-third of that of mangroves from 342 to 2098 Mg/ha with a mean of 1358 Mg/ha, (3.37 9 105 Mg C). Using the conservative estimate which is substantially higher than the global mean. But based on loss to 1 m soil depths of 1464 Mg CO2e/ha, given the large quantity of freshwater in an area of the conversion of 736 ha of mangrove to pasture is relatively low frequency of natural disturbances this

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Fig. 3 a Ecosystem C stocks (to a 1 m equivalence of soil mass) in mangrove and adjacent pastures, MX. Vertical bars are 95 % CI. b Predicted emissions (Mg CO2e/ha) arising from the conversion of mangrove forest to cattle pasture in the Pantanos de Centla, Mexico based upon a 1 m equivalence of soil mass and to a 3 m depth based upon a stock-change approach. Vertical bars above the means are one standard error

would be expected. We also found no significant ecosystem carbon pools (r2 = 0.02). Total ecosystem differences in carbon stocks between the coastal fringe carbon for this region cannot be accurately estimated and estuarine mangroves 1252 and 1445 Mg/ha, on the basis of aboveground structure. respectively. This is similar to conclusions of Donato There was a significant difference in the structure et al. (2011) in the Indo-Pacific region who also found and biomass of the 7-year Gallego pasture compared no significant differences in carbon stocks between to the older Cometa and Vidal pastures. There was still these geomorphic settings. We also found no relation- residual wood and stumps from the mangrove in the ship between aboveground biomass and total younger pasture. But the greatest differences were in

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Wetlands Ecol Manage the carbon stocks of the sites. While the carbon stock We based soil emissions estimated through com- of the Gallego pasture was significantly lower than its parisons of losses on an equivalent mass of mineral paired mangrove, it was significantly greater than the soil in the top 1 m of mangrove soils (1464 Mg CO2e/ older sampled pastures (Figs. 2, 3a). This suggests that ha). However the assumption that there would be few carbon emissions and losses from soils in the wetlands differences in soil properties below 1 m in the pasture will continue for years after establishment. This may cannot be supported by this study. We found effects of well be a significant difference in the carbon dynamics land use on soil properties throughout the soil profile between pastures converted from uplands compared to including depths [1 m. At depths of [1 m, soils in those converted in the wetlands. Hughes et al. (1999) pastures were higher in bulk density but lower in examined upland pastures and cornfields converted carbon concentration, carbon density, and carbon mass from Mexican tropical forest along a 45-year land use (Table 4). Based upon these results, estimates based chronosequence. While aboveground pools decreased upon mass equivalence difference to 2 m in soil depth over this time period they could not find differences in might be more realistic and would increase potential soil carbon pools. This is quite different from the emissions to a mean of 2584 ± 925 Mg CO2e/ha. This mangrove pastures of this study where soil pools estimate at even 2 m yielded a much more conserva- were C112 Mg C/ha higher in the younger compared tive estimate of carbon loss compared to an estimate to older pastures (P \ 0.001). Over the 23 year derived by the stock-change approach, which included difference in age among these pastures, this is aboveground pools and soils to a 3 m soil depth. By equivalent to the loss of 17.9 Mg CO2e/ha/yr in the this approach, the estimated mean emissions from pasture sites. mangrove to pasture conversion is 3264 Mg CO2e/ha Mean carbon stock differences between intact (Figs. 3, 4). Limiting ecosystems carbon stocks forests and pastures converted from such sites will differences to the surface 1 or even 2 m of soil may vary depending on the size of the initial ecosystem be missing losses occurring from deeper horizons. carbon stock, the intensity of land use, and the degree Overall, the 84,523 ha of mangroves present along of soil loss associated with land use change (Fig. 4). the Campeche-Tabasco coast (Fig. 1) store substantial

We found that there was a mean loss of 1052 Mg CO2e/ quantities of carbon. Using data from the World ha from the soil carbon pools when mangroves are Health Organization and GHG equivalency equations converted to pasture. In contrast, few changes in soil from the US Environmental Protection Agency, the carbon were noted with upland tropical forest conver- carbon storage within these mangroves (422 Tg CO2- sion. For example, Kauffman et al. (1995) found that e) is equivalent to nearly 3 years of annual GHG Amazon slash fires resulted in a mean soil C loss of emissions of all 31 million registered vehicles in 6.6 Mg/ha during slash fires. However, Kauffman et al. Mexico (WHO 2009, USEPA 2014). (1998) did not find significant differences in either soil The pastures identified in the smaller 1930 ha focus concentration or mass when comparing surface soil area were largely surrounded by mangroves, with carbon in Amazon tropical forests and pastures. some of the land area adjacent to non-forested Carbon losses from conversion of upland Amazon wetlands. Given the assumption that the 736 ha of forests were largely from aboveground pools totaling pastures were derived from the conversion of man-

481 Mg CO2e/ha (Fig. 4). In pastures converted from groves, the total emissions arising from this land use tropical dry forests in eastern Mexico losses were along a single 25 km reach of the river would be 6 equivalent to 194 Mg CO2e/ha and were largely from 1.08 9 10 Mg CO2e using our conservative estimate aboveground pools. In productive tropical evergreen of losses based on a 1 m soil depth equivalence and as 6 forests on relatively rich volcanic soils of Veracruz, high as 2.42 9 10 Mg CO2e using a stock change Mexico, Jaramillo et al. (2003a) and Hughes et al. estimate to a 3 m soil depth. This is equivalent to the (2000) reported total losses equivalent to 867 Mg standing stocks of 216 and 482 ha of mangroves,

CO2e/ha. The losses in carbon stocks from mangrove respectively. This suggests that restoration of man- conversion (1464 Mg CO2e/ha) were 7-fold that of groves in areas where land uses have declined or are emissions from dry forests and 3-fold greater than marginally proﬁtable could sequester large quantities emissions from Amazon forest to pasture conversion. of carbon.

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1600 Torres of the Laboratorio de Cata´lisis Heteroge´nea, Universidad Aboveground ´ Belowground Juarez Autonoma de Tabasco for carbon analysis. 1400 Funding This study was possible through funding provided 1200 by the Commission for Environmental Cooperation with

Mg/ha) leveraged funding provided by the United States Agency for

e 1000 2 International Development—The sustainable Wetlands Adap- O C ( tation and Mitigation Project. 800

600

400 References Carbon Emissions 200 Adame MF, Kauffman JB, Medina I, Gamboa JN, Torres O, 0 Caamal J, Reza M, Herrera-Silveira JM (2013) Carbon stocks of tropical coastal wetlands within the karstic landscape of the Mexican caribbean. PLoS One 8(2):e56569. doi:10.1371/journal.pone.0056569 Fig. 4 Predicted cumulative greenhouse gas emission (Mg Alongi DM (2014) Carbon cycling and storage in mangrove Co2e/ha) arising from the conversion of forest to pasture. Data forests. Annu Rev Mar Sci 6:195–219 for tropical dry forest, MX are from Jaramillo et al. 2003b), Arriaga Cabrera L, Va´zquezDomıńguez E, Gonza´lez Cano J, Amazon forest, Brazil emissions are calculated from Kauffman Jimeńez Rosenberg R, Munõz Lo´pez E, Aguilar Sierra V, et al. (1995, 1998) and emissions from tropical wet forest, (coordinadores) (1998). Regiones Marinas Prioritarias de Mexico are from Hughes et al. (2000) and Jaramillo et al. Me´xico. Comisioń Nacional para el Conocimiento y uso de (2003a). Mangrove emissions are from this study la Biodiversidad. Me´xico Day JW Conner WH, Ley-Lou F, Day RH, Navarro AM (1987) The productivity and composition of mangrove forests, Lagunade Terminos, Mexico. Aquat Bot 27:267–284 Few studies have examined the carbon losses Donato DC, Kauffman JB, Murdiyarso D, Kurnianto S, Stidham arising from mangrove conversion (but see also M, Kanninen M (2011) Mangroves among the most car- Pendleton et al. 2012). Yet this is necessary informa- bon-rich forests in the tropics. Nat Geosci 4:293–297. doi:10.1038/NGEO1123 tion for participation of mangrove conservation or Environmental Systems Research Institute (ESRI) (2006) restoration projects in carbon markets or climate World30 imagery Map Background. World Imagery change mitigation activities, Kauffman et al. (2014b) accessed via services.arcgis.online. SPOT 5 image source, found that emissions from abandoned shrimp ponds 15 m resolution, 2006 Fromard F, Puig H, Mougin E, Marty E, Betoulle JL, Cadamuro converted from mangroves potentially ranged from L (1998) Structure, above-ground biomass and dynamics 2165 to 3554 Mg CO2e/ha. Similar to the losses of mangrove ecosystems: new data from French Guiana. reported here, the vast majority of carbon loss Oecologia 115:39–53 occurred from depletion of soil carbon pools. From Giri C, Ochieng E, Tieszen LL, Zhu Z, Singh A, Loveland T, Masek J, Duke N (2010) Status and distribution of man- these studies, it is clear that mangrove conversion to grove forests of the world using earth observation satellite other land uses comes at a great cost in terms of large data. Glob Ecol Biogeogr 20:154–159 quantities of greenhouse gas emissions as well losses Giri C, Ochieng E, Tieszen LL, Zhu Z, Singh A, Loveland T, in other important ecosystem services. The large Masek J, Duke N (2013). Global mangrove forests distribution, 2000. NASA Socioeconomic Data and Applica- carbon stocks, high rates of deforestation of man- tions Center (SEDAC), Palisades. doi:10.7927/ groves, and subsequent high greenhouse gas emissions H4J67DW8. Accessed Nov 2014 points to the relevance for inclusion of mangroves in Guerra-Martıńez V, Ochoa-Gaona S (2008) Evaluacioń del nationally appropriate climate change mitigation and programa de manejo de La Reserva de la Biosfera Pantanos de Centla en Tabasco, Me´xico. Univ y Cienc adaptation strategies. 24(2):135–146 Hughes RF, Kauffman JB, Jaramillo VJ (1999) Biomass, car- Acknowledgments We wish to thank Jose Antonio Sanchez bon, and nutrient dynamics of secondary forests in a humid Jesus, Norma Daniela Lopez Perez, Guadalupe de la Cruz tropical region of Mexico. Ecology 80:1892–1907 Sanchez, Maria del Rosario Richardez Jimenez, Raul Mendez Hughes RF, Kauffman JB, Jaramillo VJ (2000) Ecosystem-scale Garcia, Leysi Daniela Mena Leon, and Tyler McFadden for impacts of deforestation and land use in a humid tropical assistance in the field. We also wish to thank Dr. Jose´ Gilberto region of Mexico. Ecol Appl 10:515–527

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