Seasonal variation of organic carbon in the urban tropical mangrove estuary El Salado, in Jalisco, Mexico

ABSTRACT In the El Salado estuary in the Mexican Pacific coast, we examined the seasonal variation of organic carbon (OC) in sediments, pore water and litterfall in three areas dominated by common mangrove species (Avicennia germinans, Laguncularia racemosa, and Rhizophora. mangle), as well as in the water and sediments in the main channel of the estuary. Mangrove sediment OC varied from 3.70% in the R. mangle area to 12.58% in the L. racemosa area, whereas variations in sediment pore water OC varied from 285.6 to 22.6 mg·L−1. OC from mangrove litterfall varied from 151.2 to 0.6 g·m−2 in the different mangrove species areas. OC values were higher in the dry season and lower in the rainy season. The observed OC among the different species in the dominated areas indicates that mangroves are able to release a considerable amount of OC through litterfall, with part of it sequestered in sediments.


Introduction
Owing to the effects of global climate change and global heating it is important to understand the extent to which mangroves protect coastal areas, adsorb CO 2 , and influence organic carbon (OC) sequestration in sediments [1], as well as its export to the adjacent coastal and marine zones [2], a transfer which has a positive influence on the detrital food web [3].By means of primary productivity, mangroves located in tropical and subtropical coastal areas produce great quantities of organic matter (mainly detritus from leaves and twigs) that enter into the detritus food web [3] or are sequestered in sediments.Kauffman et al. [1] estimate that mangroves globally store about 1.6 Pg C aboveground and 10.2 Pg C belowground.This great quantity of carbon sequestered in mangrove forests directly influences the mitigation of climate change.
Mangrove distribution and productivity are influenced by environmental conditions [4].In Mexico, mangroves are situated in the coasts of the Pacific, Gulf of Mexico and Caribbean where studies have focused on their coverage, distribution and productivity [5][6][7][8][9][10].Few studies have been carried out regarding the distribution of OC in the Mexican Pacific coast [11][12][13].It is well known that mangroves absorb more CO 2 than other ecosystems through primary productivity, and that they can store three times more OC than places like the Amazon rainforest [14][15][16].In 2006 it was calculated that mangrove forests around the world contain an average of 1,023 Mg OC•ha −1 , although a recent global estimation for mangrove OC storage has pointed to about 11.7 Pg C [1].
Mangrove forests in different regions present a myriad array of environmental conditions [1,17,18], and the amount of OC retention and export can therefore be assumed to vary considerably in different respects, such as geomorphology [19], forest structure, salinity, type of sediments [1,4,17], mangrove species [20], rainfall and tidal amplitude [21], and biotic influences, such as the activities of litter-retaining crabs [22] and microbes [23,24].In situ degradation and export of OC, as particulate and dissolved organic compounds (POC and DOC, respectively) to coastal areas, has had a positive influence on coastal productivity [3].It has been suggested that mangroves may be responsible for nearly 10% of the total terrestrial DOC transported to coastal regions [2], and for up to 15% of the total carbon accumulation in marine sediments [18].
Even though mangrove forests have ecological relevance, they have been under extensive degradation through socio-economic activities [25].El Salado estuary is an example of one of such disturbed area.Considered an urban estuary, it is completely surrounded by the city and port of Puerto Vallarta, Jalisco (Mexico).The objective of this study was to assess the spatial and seasonal variability of total organic carbon along the mangrove forest in El Salado estuary, in the main tidal channel of the estuary, which has been affected by port and urban developments.

Study area and samples collection
El Salado estuary (Figure 1), a natural protected area, is located on the coastal plain along the Pacific coast within the Mexican state of Jalisco (20° 41'−20° 39' N and 105° 15'−105° 13' W).This urban estuary is completely surrounded by the city of Puerto Vallarta and comprises 208 ha that include tidal channels, seasonal flood plains, tropical dry forest, as well as a substantial mangrove community [5].It has semidiurnal tides and a permanent connection to the Vallarta Marina and the ocean.The length of the main channel is ~2 km, with a 10 m average width, and a depth of 1 to 6 m.The climate is warm and subhumid, with a mean annual air temperature (T) of 21.8°C and a mean annual precipitation of 1,385 mm, mainly from July to September [26].The estuary supports three dominant species of mangrove: the black mangrove, Avicennia germinans; the white mangrove, Laguncularia racemosa; and the red mangrove, Rhizophora mangle.
Field sampling was conducted between the months of April (2011) until January (2012) at three monospecific mangrove stands along the study site.Specifically, zone A is dominated by A. germinans, zone B by L. racemosa, and zone C by R. mangle.Surface sediments and litterfall were collected in five random located quadrats (0.25 m 2 ) at each site.In each quadrat, a ~30 cm depth hole was dug to collect pore water.Samples were transported in coolers to the laboratory for analysis.Organic carbon in sediments and litterfall were determined with the Walkley-Black method [27].A WTW multiprobe (MIQ/C184 XT) was used for pore water salinity (S), pH and total OC, as well as to measure S, pH, dissolved oxygen (DO), and OC at the surface and bottom of the water column in the main tidal channel, along seven locations (Figure 1).Channel sediments were collected with a Van Veen grab to determine OC content.

Statistical analysis
For seasonal variability among the three mangrove species, we used a one-way variance analysis (ANOVA) in order to examine the average association among the mangrove species.Statistical analyses and graphs were implemented in Minitab-17 and OriginPro-8 Software.

Seasonal differences among the three mangrove species zones
Figure 2 shows the seasonal variability of OC, S and pH in pore water, as well as OC in sediments and litterfall.The only time when no significant differences (p > 0.05) were found among the three mangrove species zones in pore water from OC (~186 mg OC•L-1) was after the rainy season in November (Figure 2a).Rains tend to homogenise pore water from OC because of the litterfall leachates generated in mangrove forest sediments.Significant differences (p < 0.05) in the OC of sediments were found during the entire time period; e.g.zone B, dominated by L. racemosa (Figure 2b), had the highest OC content (12.58%November).There were only seasonal differences (p > 0.05) of OC content in litterfall during the rainy season, with the lowest OC values (0.56-1.26 mg OC•L −1 ) in August (Figure 2c).This low OC concentration was caused by the washing effect of the rains on the litterfall, which was mostly composed of leaves.Pore water S showed significant differences (p < 0.05) among the three mangrove zones during the entire time series, with the lowest values in the rainy season (August) and the highest in the cold dry season (January-April) (Figure 2d).There were no significant differences (p > 0.05) in pore water pH among the three locations (Figure 2e), because of the buffer capacity of seawater.

Variability among the hydrological parameters along the main tidal channel
Figure 3 shows the OC content in the water column (surface and bottom) of the tidal channel, as well as S, pH, and DO, and OC sediments.OC in the water column increases during the rainy season (August), with a top surface of up to 140 mg OC•L −1 and a bottom surface of 220 mg OC•L −1 (Figure 3a,).But, OC decreased on the surface water along the stations from the head and the opposite was observed in the case of the bottom water OC.Sediment OC (~7.22%) showed more seasonal variability with no apparent spatial variability (Figure 3c).S was higher during the dry months, from April to June (31.15psu), and decreased with the rains in August (0.79 psu), although the sampling period S lessened towards the head of the estuary (Figure 3d).There were no apparent pH changes (~7.39) along the tidal channel throughout the different seasons (Figure 3e).DO showed higher concentrations at the mouth of the estuary (4.2 mg O 2 •L −1 ) and much lower seasonal concentrations during the winter months of November and January (Figure 3f).

Discussion
In this study, we have examined the seasonal rate of OC in the environment of three common mangrove species distributed in a small urban estuary.Because of the relatively recent effects of climate change, especially in tropical and sub-tropical latitudes, it has become most important to understand to what degree monospecific mangrove stands of A. germinans, L. racemosa, and R. mangle influence the input of OC into sediments throughout the year and the export of dissolved OC to the adjacent coastal zone.Litterfall production of different mangrove species varies according to the geohydrological characteristics (i.e.tides, rains, topography, runoff, salinity, soil redox) of the site where they develop [28], which influence OC stock in the world'smangrove forests.Table 1 shows the estimated OC stock in different mangrove forests around the world: the minimum report being of 2.5 kg CO•m −2 , and a maximum of 220.87 kg OC•m −2 , with a mean OC stock of 73.89 kg OC•m −2 [29,30].In Mexico, reported OC stocks for mangroves vary from 53 to 1345 Mg OC•ha −1 .In general terms, the highest values are related to humid  climate conditions (southern Mexico), and the lower ones to semi-desert environments (northwestern Mexico) [31].
In the case of El Salado estuary, the highest values of litterfall for the three species were observed at the end of the dry season and the beginning of the rainy season (Figure 2c) [5,34], as reported for estuaries in Jalisco's coast and other costal lagoons of Mexico [35][36][37].Litterfall production for the different species in our study was A. germinans > L. racemosa > R. mangle, which is what we had found in a previous study in El Salado [34].In the coastal lagoon of Barra de Navidad [6], also located in Jalisco's coast, production was R. mangle > L. racemosa > A. germinans.
Our results for annual litterfall for El Salado estuary were 0.339 kg•m −2 , a higher figure than the previous 0.256 kg•m −2 reported [34].Applying the Van Bemmelen factor [38], OC represented 0.196 kg OC•m −2 and 0.148 kg OC•m −2 , respectively.Annual litterfall in El Salado estuary is lower than that reported for other lagoons in Mexico: 1.758 kg•m −2 for a semi-desert lagoon (Baja California Sur State) [36], 1.116 kg•m −2 for a tropical rainy area (Veracruz State) [35], and 1.100 kg•m −2 for a coastal lagoon with an ephemeral inlet (Sinaloa State) [37].This difference may be caused by urban activities that directly impact the estuary, mainly municipal wastewater, rubbish from the basin, and hydrocarbons washed from streets and the airport.
The cycle of nutrients begins when leaves, twigs, flowers, and branches fall from the mangroves and are subjected to a combination of leaching and biological (tanaidaceans, crabs, fungi, bacteria) degradation in sediments and water [24], generating particulate and dissolved OC [39,40].Part of this particulate and dissolved OC is trapped in sediments, and another part is exported to coastal areas.The head of the estuary (Zone B) in El Salado seemingly tends to accumulate more OC in sediments than in other zones, reaching up to 12.58% in sediments and 185 mg•L −1 in pore water (Figure 2a,b).Similar sediment values have been reported in Marismas Nacionales (State of Nayarit) [11], the largest mangrove forest in the Mexican Pacific.Based on the statistical results from our study, it is evident that OC varies among the mangrove species and according to seasonal environmental conditions [20].For instance, leaves of A. germinans decompose faster than those of L. racemosa and R. mangle, possibly owing to their higher nitrogen and lower tannin contents [20,41,42], whereas the presence of a thick-walled membrane in R. mangle leaves (Zone B) seems to delay decomposition processes [42] and allow OC accumulation in sediments.
Previous field works on weight loss of mangrove leaves from litter bags have indicated that leaching of water-soluble compounds is an important early stage in the decomposition of leaf material [21,24,43].Approximately 30-50% of the organic matter in mangrove leaves is leachable, and the remaining material is composed of structural polymers, cellulose, hemicellulose, and lignin [44].It has been suggested that submerged leaves release substantial amounts of OC to the surrounding estuarine environment within a relatively short period of time (hours) [45].The conversion of this OC into microbial biomass has been shown to be between 50% and 80% [24], suggesting that microbial growth at the expense of the easily used fraction of OC could be important in food web dynamics [20,42].Moreover, the rapidly used OC by bacteria on the sediment surface could reduce OC export to more distant areas [43].
Assessments of OC production rates in different mangrove species are of key importance, as OC can provide energy to the microbial communities in coastal waters adjacent to mangrove forests [44].Hence, this displacement of dissolved OC to the particulate stage through bacterial assimilation could provide OC to higher trophic levels [24].In fact, bacterial communities appear to be mostly active in secondary processing of primary production, as an efficient recycling process within the sediment and microbial food chains [43,45].Consequently, studies of OC in mangrove forests could help to understand the dangerous, huge effect of their elimination on global carbon budgets.This distinctive variability among and within mangrove forests worsens worldwide extrapolations.Thus, mangrove litterfalls play a key role in this process because littterfall contains up to 40% of water-soluble components which can be converted into bacterial biomass less than eight hours after falling into estuarine waters [24].

Conclusions
The processes of carbon dynamics in mangrove forests are very complex and are much debated.This study aimed to examine the OC rate at several locations within a small urban estuary.The observed differences of OC among mangrove species and seasonal environmental conditions indicate a clear pattern inasmuch as some of the mangroves are able to release a considerable amount of OC depending on environmental parameters (salinity, temperature, pH, etc.).Given the large geographic extent of mangrove areas impacted by socio-economic activities, there is an urgent need to research how mangroves could enhance the organic carbon cycle in tropical and subtropical coastal regions.Knowledge about the role of mangroves in the carbon cycle is relevant to current climate changes and adaptation measures.

Figure 1 .
Figure 1.Field sites location within the study area (map Google earth ©2021 Google LLC).Dots represent the locations of sampling sites (1-7) in the main channel.Letters represent the three locations for the monospecific mangrove stands: zone a -avicennia germinans, zone B -laguncularia racemosa, and zone C -rhizophora mangle.

Figure 2 .
Figure 2. Total organic content in pore water (a), sediments (b), litterfall (c), pore water salinity (d), and pore water pH (e).Error bars not shown are smaller than symbol size.Monospecific mangrove species locations within the estuary are: zone a -avicennia germinans, zone B -laguncularia racemosa, and zone C -rhizophora mangle.

Figure 3 .
Figure 3. Seasonal variability of total organic carbon in water column (a) surface, (b) bottom, (c) organic carbon content in sediments, (d) salinity, (e) pH and (f) dissolved oxygen.

Table 1 .
Organic carbon stock in different mangrove forests of the world.
*Some references present data in kg CO•m −2 we transform them to Mg CO•ha −1 .