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Processes of organic carbon in mangrove ecosystems
Acta Ecologica Sinica 31 (2011) 169–173
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Acta Ecologica Sinica journal homepage: www.elsevier.com/locate/chnaes
Processes of organic carbon in mangrove ecosystems Ye Yong a,⇑, Pang Baipeng a, Chen Guangcheng b, Chen Yan c a
State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361005, PR China Third Institute of Oceanography, State Oceanic Administration, Xiamen 361005, PR China c Minjiang University, Fuzhou 361005, PR China b
a r t i c l e
i n f o
Keywords: Mangrove Organic carbon Ecological processes
a b s t r a c t In addition to carbon accumulation in plants, processes of organic carbon in mangrove ecosystems include origins of sediment organic carbon, carbon fluxes between mangroves and their adjacent systems (coastal waters and atmosphere), and cycling processes. Sediment organic carbon originates from suspending solids in coastal waters, mangrove plants and benthic algae. In mangroves with low organic carbon content in sediments, tidal seawater is the main origin of sediment organic carbon, while in mangroves with high sediment organic carbon contents, sediment organic carbon mainly originates from mangrove plants. Due to tidal flush, there is large material exchange between mangrove ecosystems and their adjacent coastal waters. In China, exports of organic carbon in litter falls and dissolved organic carbon from mangroves to their adjacent coastal waters have not been documented. Processes of mangrove litter falls, including production, decomposition, export and animal consumption, determine linkages among organic carbon among mangrove plants, secondary production and coastal ocean. Consumers especially benthic animals may influence organic carbon in mangrove ecosystems, because (1) their consumption rates are high, and their selective feeding on some food sources will change the relative quantities of export, bury and mineralization of organic carbon from different origins; (2) their consumption is much more than assimilation, resulting in the changes in sizes, forms and qualities of nonassimilated organic matters, and then the changes in availability of export, consumption or mineralization of organic carbon. Respiration and sulfate reduction are important mineralization processes of organic carbon in mangrove sediments. Mineralization rates of organic carbon in mangrove sediments are influenced by quantities, activities and particle sizes of organic matters, and other factors such as forest ages, root activities and animal burrowing activities. Researches on processes of mangrove organic carbon should be based on open systems, and ecological processes of organic carbon should be coupled with vegetation restoration. Ó 2011 Ecological Society of China. Published by Elsevier B.V. All rights reserved.
1. Introduction
2. Origins of organic carbon in mangrove sediments
Processes of organic carbon are links of lots of functions of mangrove ecosystems, and they are closely related to social, ecological and economic benefits of mangroves such as coastal protection, pollution purification, biodiversity maintenance, and productivity [1–3]. Ecological processes of organic carbon in mangrove ecosystems are very complex, including origins of sediment organic carbon, carbon fluxes between mangroves and their adjacent systems (coastal waters and atmosphere), and cycling processes besides carbon accumulation in plants (primary production and plant respiration). In this paper, study progresses in these fields of processes of organic carbon in mangrove ecosystems were summarized and some research suggestions were put forward to give references in the role of mangroves in global carbon cycles.
Mangrove ecosystems can store lots of organic carbon, and some of them are rich in organic carbon in sediments deep in several meters [4]. Sediment organic carbon originates from suspending solids in coastal waters, mangrove plants (litter falls and underground roots) and benthic algae. Contribution rates of each origin are different in different literatures. Researches on carbon stable isotope indicated that mangrove plants were the main origin of organic carbon in mangrove sediments in southwest Brazil, Philippines, Vietnam and India [5–7]. In southwest Thailand mangroves, benthic algae, coastal waters and mangrove plants contributed 39%, 16% and 23% of sediment organic carbon, respectively [8]. Stable isotope compositions of organic carbon at two Tanzanian mangrove sites were different with stand species, and up to 35% of sediment organic carbon derived from coastal waters [9]. In Yucatan peninsula, Mexico, mangrove plants, phytoplankton and seagrass contributed to organic carbon in sediments but their
⇑ Corresponding author. E-mail address: [email protected] (Y. Yong).
1872-2032/$ - see front matter Ó 2011 Ecological Society of China. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.chnaes.2011.03.008
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contributions were different at different sites [10]. Bouillon et al. summarized that in mangroves with low carbon stocks, sediment organic carbon had low C/N and d13C, and suspending solids in coastal waters were the main origin of sediment organic carbon, while in mangroves with high carbon stocks, sediment organic carbon had high C/N and d13C similar to those of mangrove plants which were the main origin of sediment organic carbon [11]. In addition, most of organic carbon in mangroves was in the underground roots which could change sediment conditions through physiological processes. For example, the underground roots could release oxygen into mangrove sediments and increase the storage of sedimentary organic carbon through exudates of living roots and decomposition of dead roots. The accumulation of organic carbon in mangrove sediments at four sites along the Shark River estuary in south Florida were investigated with empirical measures and a process-based model. Model sensitivity analyses suggested that root production had more significant effects on sediment composition than litter falls [12].
3. Carbon fluxes between mangroves and their adjacent systems Through determination of sediment organic carbon origins, the difficultly-decomposing compositions of stored organic carbon are reflected, but the real-time carbon fluxes does not be known. For example, compared to organic matters from mangrove plants, those from the adjacent seawater are difficult to be decomposed and easily to be stored in mangrove sediments. Thus, even if the sediments have more organic carbon from phytoplankton, low carbon fluxes may be into the sediments. Carbon fluxes in mangrove ecosystems are mostly investigated between mangrove plants and atmosphere (photosynthesis stored carbon and respiration released carbon by plants). The net production of organic carbon in mangroves (primary production) may be accumulated in the local sediments or exported to the adjacent waters in the form of litter, debris and dissolved organic carbon, while organic carbon in adjacent waters can enter the sediments through sedimentation, forming organic carbon fluxes among mangrove plants, sediments and adjacent waters. Benthic algae and other photo-autotrophic microorganisms in surface sediments can also fix atmospheric CO2, and organic carbon entering the sediments can be released into atmosphere as CO2 and CH4 through various functions of the microbes, such as mineralization, resulting in carbon fluxes between sediments and atmosphere. Most of mangrove ecosystems are extremely open. Due to tide actions, there are lots of long-term material exchanges between mangroves and their adjacent waters, which is the significant difference between mangrove forests and inland forests (including inland wetlands). Mangrove ecosystems may provide organic carbon for coastal waters, and some foreign scholars studied output of mangrove organic matters [13]. Litter falls accounted for about 1/ 3 of the net production in mangrove forests [14]. In some cases mangroves exported organic carbon as litter and particular (or dissolved) forms to adjacent waters, and the ratio of litter output was up to 1/2 [14]. There were also evidences indicating that output of dissolved organic carbon was comparable to output of litter organic carbon in some mangroves [14]. However, so far there were few studies on the roles of mangroves in dissolved and particular organic carbon budget in coastal waters [15], and the published data were usually contradictory, due to the differences in research methods and difficulties in accurate determination of material fluxes between mangroves and their adjacent coastal waters. The difficulties in determination of material fluxes between mangroves and their adjacent coastal waters are that material fluxes largely changed with tidal actions, resulting in greatly random values, and there were large differences in tidal range, topography, sedi-
ment chemistry and community structure among the studied mangrove ecosystems [16]. In China, since early 1980s, mangrove litter production has been studied, but only temporal dynamics were reported [17], and output of litter and dissolved organic carbon are not documented. In addition, most of mangroves grow along deposit coastlines where large rivers flow and the flats are even, so they can accelerate sedimentation of suspended materials and become sinks of organic carbon of coastal waters during tide flooding periods. There are still few studies on input flux of organic carbon in mangroves, though the evidence indicated that flocculation of small particles in mangroves resulted in net input of organic carbon in a highly vegetated mangrove at Middle Creek, Cairns, Australia [18]. 4. Organic carbon cycling processes in mangrove ecosystems 4.1. Dynamic processes of litter falls Dynamic processes of litter falls in mangroves include production, decomposition, output and animal feeding, determining the relations among mangrove plants, secondary production, and coastal seawater organic carbon. So far studies on decomposition of mangrove litter falls and concomitant nutrient dynamics have been focused on the differences among tide levels [19], plant species and seasons [19–21] and litter components [22]. Rapid decomposition of organic matter in mangrove ecosystems seems to ensure that the majority of organic production circulated within the forest, which might reduce export of organic carbon from mangroves to their adjacent waters by tides [23]. Machiwa and Hallberg confirmed that dissolved organic carbon accounted for 80% of total export of organic carbon [24]. Three weeks’ leaching amount of organic carbon from mangrove debris by seawater accounted for about 33% of dry mass loss during the whole decomposing period of litter leaves of Rhizophora mangle, and leaching loss of organic carbon was rapid with a peak value on the second day of leaching experiment, indicating that dissolved organic carbon from decomposition of litter leaves might be the main output of mangrove matters [25]. About four decades ago, Odum proposed a groundbreaking hypothesis in coastal ecology according to which the outwelling of litter falls from coastal wetlands was a major source of energy that supported much of the secondary production of estuaries and coastal waters, but now this hypothesis is being questioned [26], because the main output of organic carbon from mangroves is dissolved organic carbon but not litter falls themselves. 4.2. Effects of benthic animals on dynamics of organic carbon Consumers, especially benthic animals, have great effects on the whole dynamics of organic carbon in mangrove ecosystems because (1) their consumption rates are high, and their selective feeding on some food sources will change the relative quantities of export, bury and mineralization of organic carbon from different origins, and (2) their consumption is much more than assimilation, resulting in the changes in sizes, forms and qualities of non-assimilated organic matters, and then the changes in availability of export, consumption or mineralization of organic carbon [26]. Consumption percents of mangrove litter leaf production by invertebrates (especially crabs) were much different in different mangroves, ranging from 10% to 90%, which is an important factor adjusting the output of organic carbon from mangroves, and is more efficient in retention of organic carbon from mangrove litter leaves and litter turnover compared to only microbial decomposition [27–29]. Foraging behaviors of mangrove animals influence characters and availability of organic matters through many mechanisms,
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and the usually reported is foraging mangrove litter leaves by Sesarma crabs. The high palatability of brown leaves compared with green and, in particular, yellow leaves probably results from improved nutritional values and removals of inhibitory compounds such as tannins by the aging process and yellow leaves just fallen from trees are poor in nitrogen and rich in tannins [30,31]. Direct feeding by Sesarma crabs reduces tidal output of litter organic carbon, and many crabs drag litter leaves into their caves where litter leaves continue to be decomposed [27,31,32]. Field experiments carried out in tropical mangroves dominated by R. harrisonii and R. mangle in Guayas River estuary in Ecuador demonstrated that the mangrove crabs could remove the whole daily produced litter leaves within 1 h, so the leaf turnover is much faster than that estimated based on only leaf decomposition [21]. Therefore, even in estuarine mangroves with strong tidal flushing, types of litter dynamics are also determined by crab foraging. Amount of consumption by Sesarma crabs is twice as much as that of assimilation [30], i.e., half of litter leaves foraged by crabs were changed into faecal materials to provide food for decomposers or debris food web, which is a very important ecological process because the faecal materials with fine organic particles and high nitrogen contents are easily used by other invertebrates [33], and the decomposition rates greatly increased compared to those of original litter materials [33,34], resulting in accelerating organic carbon turnover. In China, although there are many literatures on crab distribution in mangroves, data on feeding ecology of mangrove crabs are limited and most of them are descriptive, and litter leaf removals by crabs have not been well quantified, resulting in an incomplete understanding of food webs and biogeochemical cycles in mangroves. Therefore, few estimates could test that crab consumption might have an impact on the fate of mangrove litter leaves in most mangroves in China. There, the only two reports on leaf litter removal by crabs were carried out by us in a Kandelia candel forest in Jiulongjiang Estuary in Fujian [29,31]. Recently, the traditional views that mangrove plants are the main supplier of organic carbon and mangrove litter leaves are the main food source for benthic animals were challenged. It has become increasingly clear that mangrove invertebrates exploit a wide range of potential food resources, including mangrove litter, epiphytic algae, benthic microalgae, bacteria and fungi, as well as macro-algae and a mixture of organic sources imported from adjacent aquatic environments by tidal currents, thus, the degree of utilization of mangrove derived food sources depends partially on the degree of material exchange with adjacent systems [26]. 4.3. Dynamics of sedimentation of organic carbon in mangrove ecosystems Mangroves develop in hidden areas where fine sediments accumulate, and many plants have wide ground roots which can accelerate to capture silt and clay particles. To understand how sedimentation affects long-term sustainability of mangrove wetlands, it is important to recognize sedimentation dynamics in mangroves. There have been lots of reports on sedimentation rates in mangroves at abroad and few in China usually by 210Pb isotope method and sign stake method [35]. Although these methods can reflect sedimentary history in mangroves, we can know nothing on dynamic processes of sedimentation of organic carbon from them. Therefore, processes controlling sedimentation dynamics are not well understood, so it is hard to explain sediment budget of organic carbon and its role in coastal sedimentary environment. Kitheka et al. studied sediment exchanges in a degraded mangrove forest in south Kenya where they collected water samples at half of the tide water depth and measured concentrations of the total and particular organic suspending sediments [36]. Victor et al. conducted a six-month study on sedimentary rates in Pohn-
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pei mangroves in Micronesia with 5 cm diameter sediment traps which were fixed at the bottom for one month along transects [37]. Adame et al. also used similar method to study mangrove sedimentary dynamics in southeast Queensland, Australia [38]. Sedimentary dynamics of organic carbon in mangrove ecosystems can be availably studied with these relatively immediately sampling methods. 4.4. Mineralization processes of organic carbon in mangrove sediments Mineralization of organic carbon in mangrove sediments is also important in determining carbon stock in mangrove ecosystems. Respiration and sulfate reduction might be the most important mineralization processes of organic carbon in mangrove sediments, and each of them accounted for 40–50% of the total mineralization [26]. Most of mangrove sediments are rich in reducing inorganic sulfur with the forms of FeS2, sulfur and few FeS [39]. Traditionally, denitrification, manganese respiration and iron respiration are not considered important in mangrove sediments [40]. Aerobic respiration and anaerobic sulfate reduction are usually considered the most important microbial respiration processes, but recent evidences suggested that in mangrove sediments with high iron contents the role of iron respiration in mineralization of organic carbon may be similar to or even higher than that of sulfate reduction [26]. Besides contents, activities and sizes of organic matter, mineralization rates of organic carbon in mangrove sediments are also influenced by other factors such as forest age, physiological activities of the roots, extent of water-logging and intensity of faunal burrowing activities [26]. The study at the Matang Mangrove Forest Reserve in peninsular Malaysia showed that (1) sulfate reduction was the dominant mineralization process of organic carbon in mangrove sediments, accounting for 51–75% of total mineralization of organic carbon; (2) aerobic respiration and denitrification accounted for 5–20% and 25% of total mineralization of organic carbon, respectively; and (3) with the increase in mangrove age, efficiency of carbon burial in sediments increased from 16% to 27%, while the ratio of total mineralization of organic carbon in sediments to mangrove net primary production decreased from 28% to 7% [1]. In young Avicennia marina and R. apiculata stands, sulfate reduction accounted for 20–30% of total mineralization of organic carbon, but sulfate reduction increased with stand age and represented most of sediment total mineralization of organic carbon in old stands [41,42]. With the increase in stand age, input of organic carbon was enhanced and fresh organic matter increased, so sulfate reduction could be a dominant mineralization process of organic carbon. It seems that the roots of A. marina have complementary effects on the biogeochemistry of mangrove sediments as oxygen leaching by the roots keeps the rhizosphere deep in sediments oxidized and enriched in Fe3+ for use by iron reducers, and at the same time, leaching of labile dissolved organic carbon from roots appears to stimulate bulk sulfate reduction [43]. As sulfate reduction usually is hampered in the presence of more potent electron acceptors (e.g. O2 and Fe3+), this process becomes inferior to iron respiration when oxidizing roots and in-faunal burrows increase the Fe3+ content in mangrove sediments [44]. Sulfate reduction in the flat with animal caves was only half of that in the flat without animal caves [45]. 5. Carbon budget in mangrove ecosystems Studies on ecological processes of organic carbon in mangrove sediments are also important in oceanic and even global carbon budget [1,2,46]. Estuarine coast is one of the areas in biosphere with most active biogeochemical processes, while mangroves are
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the dominant ecosystems with high productivity in tropical and subtropical estuarine coast, so they have strong carbon processes [11]. Although mangroves has smaller area than other habitats, they account for about 11% of the total input of terrestrial carbon into the ocean and 15% of the total carbon accumulated in modem marine sediments [2,3]. These global estimates are still uncertain (based on only tropical mangroves), but at least they indicate the importance of processes of organic carbon in mangrove ecosystems in global oceanic carbon budget. Mangrove ecosystems are generally considered net autotrophic as they can enhance the accumulation of organic carbon in sediments and have high productivity and low ratio of sediment respiration to net primary production, resulting in a potential for mangrove sediments to accumulate organic carbon for a long time [47]. There are some documents about global carbon budget in mangrove ecosystems. For example, Twilley et al. estimated that global mangroves had carbon stock of 3 1014 mol C and net ecosystem production of 1.5 1013 mol C yr 1 [4], while Gattuso et al. estimated that global mangroves had gross primary production of 4.6 1013 mol C yr 1 in which the net ecosystem production was 1.8 1013 mol C yr 1 [48]. However, these estimates are based on only tropical areas, and most of them are based on mangrove plant community level but not at the ecosystem level, i.e. these estimates are not based on the systemic analyses of ecological processes of organic carbon in mangrove ecosystems and their availability may be questionable. The variability in carbon transformations and transport conditions among mangrove environments is affected by specific local conditions with respect to climate, degree of exposure to strong water movement, the vicinity of river discharges, soil and bedrock composition in the neighboring terrestrial system and, not the least, the local vegetation and fauna. Due to such inherent environmental variability combined with the rather limited data available, generalization on a global scale becomes troublesome [26]. Therefore, carbon budget in global mangrove ecosystems should be given based on more widely spatial and temporal data. In China, most of mangroves are in subtropical regions and the studies on mangrove carbon budget have not been carried out. Therefore, the studies on the processes of organic carbon in China may make contribution for the global mangrove carbon budget. In addition, the changes of carbon budget with vegetation development have not been reported in mangrove ecosystems. Currently, more than 80% of mangroves in China are secondary artificial forests, and this ratio of artificial mangroves will increase in global mangroves with the development of society. Therefore, the changes in processes of organic carbon with vegetation development in artificially restored mangroves should be studied and more attention should be paid to its role in oceanic carbon budget as well as global changes.
6. Perspectives and suggestions Over the past two decades, a large number of case studies have significantly increased our knowledge on carbon dynamics in mangrove ecosystems and on the importance of various biogeochemical processes. We still lack, however, a complete understanding of the underlying mechanisms controlling the spatial and temporal variability of these processes as a function of the changes in environmental conditions [26]. And further studies, especially those on stocks, accumulation history and sedimentation age, input and output, compositions and origins, dynamical parameters and characters of decomposition and transformation of organic carbon, should be carried out in subtropical mangroves. To give the global carbon budget and understand the roles of mangroves in global
carbon cycle, data on carbon budget should be improved in more mangrove areas. In China, studies on element cycles in mangroves have been carried out widely in Hainan, Guangxi, Fujian and Guangdong since early 1980s. Unfortunately, in all of these studies mangroves were considered as closed systems and material and energy exchanges between mangroves and their adjacent waters were not included, i.e. only plants and microorganisms were considered as the main parts in material cycles and all of litter falls were assumed to return into mangrove forests. Therefore, despite of some difficulties, it is necessary to study these fields based on open mangrove ecosystems. In addition, more than 80% of mangroves in China are secondary artificial forests, and this ratio will increase in global mangroves with the development of society, so more attention should be paid to the changes in processes of organic carbon in artificially restored mangroves with the development of mangrove vegetation.
Acknowledgements This project was supported by the National Natural Science Foundation of China (Nos. 40706042 and 41076049).
References [1] D.M. Alongi, A. Sasekumar, V.C. Chong, J. Pfitzner, L.A. Trott, F. Tirendi, P. Dixon, G.J. Brunskill, Sediment accumulation and organic material flux in a managed mangrove ecosystem: estimates of land–ocean–atmosphere exchange in peninsular Malaysia, Marine Geology 208 (2004) 83–402. [2] S. Bouillon, R.M. Connolly, S.Y. Lee, Organic matter exchange and cycling in mangrove ecosystems: recent insights from stable isotope studies, Journal Sea Research 59 (2008) 44–58. [3] T.C. Jennerjahn, V. Ittekkot, Relevance of mangroves for the production and deposition of organic matter along tropical continental margins, Naturwissenschaften 89 (2002) 23–30. [4] R.R. Twilley, R.H. Chen, T. Hargis, Carbon sinks in mangroves and their implications to carbon budget of tropical coastal ecosystems, Water, Air Soil Pollution 64 (1992) 265–288. [5] C.E. Rezende, L.D. Lacerda, A.R.C. Ovalle, C.A.R. Silva, L.A. Martinelli, Nature of POC transport in a mangrove ecosystem: a carbon isotopic study, Estuarine, Coastal Shelf Science 30 (1990) 641–645. [6] H. Kennedy, E. Gacia, D.P. Kennedy, S. Papadimitriou, C.M. Duarte, Organic carbon sources to SE Asian coastal sediments, Estuarine, Coastal Shelf Science 60 (2004) 59–68. [7] A.B.K. Prasad, A.L. Ramanathan, Organic matter characterization in a tropical estuarine-mangrove ecosystem of India: Preliminary assessment by using stable isotopes and lignin phenols, Estuarine, Coastal Shelf Science 84 (2009) 617–624. [8] T. Kuramoto, M. Minagawa, Stable carbon and nitrogen isotopic characterization of organic matter in a mangrove ecosystem on the southwestern coast of Thailand, Journal of Oceanography 57 (2001) 421–431. [9] A.N.N. Muzuka, J.P. Shunula, Stable isotope compositions of organic carbon and nitrogen of two mangrove stands along the Tanzanian coastal zone, Estuarine, Coastal Shelf Science 66 (2006) 447–458. [10] M.E. Gonneea, A. Paytan, J.A. Herrera-Silveira, Tracing organic matter sources and carbon burial in mangrove sediments over the past 160 years, Estuarine, Coastal Shelf Science 61 (2004) 211–227. [11] S. Bouillon, F. Dahdouh-Guebas, A.V.V.S. Rao, N. Koedam, F. Dehairs, Sources of organic carbon in mangrove sediments: variability and possible ecological implications, Hydrobiologia 495 (2003) 33–39. [12] R.H. Chen, R.R. Twilley, A simulation model of organic matter and nutrient accumulation in mangrove wetland soils, Biogeochemistry 44 (1999) 93–118. [13] F. Baltzer, M. Allison, F. Fromard, Material exchange between the continental shelf and mangrove-fringed coasts with special reference to the AmazonGuianas coast, Marine Geology 208 (2004) 115–126. [14] R.R. Twilley, Exchange of organic carbon in basin mangrove forests in southern Florida estuary, Estuarine, Coastal Shelf Science 20 (1985) 543–557. [15] Y. Akamatsu, S. Ikeda, Y. Toda, Transport of nutrients and organic matter in a mangrove swamp, Estuarine, Coastal Shelf Science 82 (2009) 233–242. [16] T. Ayukai, D. Miller, E. Wolanksi, S. Spagnol, Fluxes of nutrients and dissolved and particulate organic matter in two mangrove creeks in northeastern Australia, Mangroves Salt Marshes 2 (1998) 223–230. [17] F.Z. Zheng, P. Lin, C.Y. Lu, W.J. Zheng, Inter annual dynamic of litter full of Kandelia candel mangrove and energy flow through the litter in Jiulongjiang Estuary, Fujian province, China, Acta Ecologica Sinica 18 (2) (1998) 113–118. [18] K. Furukawa, E. Wolanski, H. Mueller, Currents and sediment transport in mangrove forests, Estuarine, Coastal Shelf Science 44 (1997) 301–310.
Y. Yong et al. / Acta Ecologica Sinica 31 (2011) 169–173 [19] P.L. Mfilinge, N. Atta, M. Tsuchiya, Nutrient dynamics and leaf litter decomposition in a subtropical mangrove forest at Oura Bay Okinawa Japan, Trees 16 (2002) 172–180. [20] P. Lin, H.Q. Fan, Seasonal model of the decomposition rates of Kandelia candel fallen leaves in Jiulongjiang River Estuary, Journal Xiamen University (Natural Science) 31 (1992) 428–434. [21] R.R. Twilley, M. Pozo, V.H. Garcia, V.H. Rivera-Monroy, R. Zambrano, A. Bodero, Litter dynamics in riverine mangrove forests in the Guayas River estuary, Ecuador, Oecologia 111 (1997) 109–122. [22] A.G. Van der Valk, P.M. Attiwill, Decomposition of leaf and root litter of Avicennia marina at Westernport Bay, Victoria, Australia, Aquatic Botany 18 (1984) 205–221. [23] M. Hemminga, F.J. Slim, J. Kazungu, G.M. Ganssen, J. Nieuwenhuize, N.M. Kruyt, Carbon outwelling from a mangrove forest with adjacent seagrass beds and coral reefs (Gazi Bay, Kenya), Marine Ecology Progress Series 106 (1994) 291–301. [24] J.F. Machiwa, R.O. Hallberg, An empirical model of the fate of organic carbon in a mangrove forest partly affected by anthropogenic activity, Ecological Modelling 147 (2002) 69–83. [25] S.E. Davis, C. Corronado-Molina, D.L. Childers, J.W. Day, Temporally dependent C, N, and P dynamics associated with the decay of Rhizophora mangle L. leaf litter in oligotrophic mangrove wetlands of the Southern Everglades, Aquatic Botany 75 (2003) 199–215. [26] E. Kristensen, S. Bouillon, T. Dittmar, C. Marchand, Organic carbon dynamics in mangrove ecosystems: A review, Aquatic Botany 89 (2008) 201–219. [27] A.I. Robertson, Leaf burying crabs: their influence on energy flow and export from mixed mangrove forests (Rhizophora sp.) in northeast Australia, Journal Experimental Marine Biology Ecology 102 (1986) 237–248. [28] J.O. Bosire, F. Dahdouh-Guebas, J.G. Kairo, J. Kazungu, F. Dehairs, N. Koedam, Litter degradation and CN dynamics in reforested mangrove plantations at Gazi Bay, Kenya, Biological Conservation 126 (2005) 287–295. [29] G.C. Chen, Y. Ye, C.Y. Lu, Seasonal variability of leaf litter removal by crabs in a Kandelia candel mangrove forest in Jiulongjiang Estuary, China, Estuarine, Coastal Shelf Science 79 (2008) 701–706. [30] N. Thongtham, E. Kristensen, Carbon and nitrogen balance of leaf eating sesarmid crabs (Neoepisesarma versicolor) offered different food sources, Estuarine, Coastal Shelf Science 65 (2005) 213–222. [31] G.C. Chen, Y. Ye, Leaf consumption by Sesarm aplicata in a mangrove forest at Jiulongjiang Estuary, China, Marine Biology 154 (2008) 997–1007. [32] M.W. Skov, R.G. Hartnoll, Paradoxical selective feeding on a low nutrient diet: why do mangrove crabs eat leaves? Oecologia 131 (2002) 1–7. [33] S.Y. Lee, Potential trophic importance of the faecal material of the mangrove sesarmine crab Sesarma messa, Marine Ecology Progress Series 159 (1997) 275–284. [34] P.L. Mfilinge, T. Meziane, Z. Bachok, M. Tsuchiya, Litter dynamics and particulate organic matter outwelling from a subtropical mangrove in
[35]
[36]
[37]
[38]
[39]
[40]
[41]
[42]
[43]
[44]
[45]
[46]
[47]
[48]
173
Okinawa Island, South Japan, Estuarine, Coastal Shelf Science 63 (2005) 301– 313. Q.M. Zhang, X.S. Wen, C.J. Song, S. Liu, The measurement and study on sedimentation rates in mangrove tidal flats, Tropic Oceanology 15 (4) (1996) 57–62. J.U. Kitheka, G.S. Ongwenyi, K.M. Mavuti, Fluxes and exchange of suspended sediment in tidal inlets draining a degraded mangrove forest in Kenya, Estuarine, Coastal Shelf Science 56 (2003) 655–667. S. Victor, L. Neth, Y. Golbuu, E. Wolanski, R.H. Richmond, Sedimentation in mangroves and coral reefs in a wet tropical island, Pohnpei, Micronesia, Estuarine, Coastal Shelf Science 66 (2006) 409–416. M.F. Adame, D. Neil, S.F. Wright, C.E. Lovelock, Sedimentation within and among mangrove forests along a gradient of geomorphological settings, Estuarine, Coastal Shelf Science 86 (2010) 21–30. M. Holmer, E. Kristensen, G. Banta, K. Hansen, M.H. Jensen, N. Bussawarit, Biogeochemical cycling of sulfur and iron in sediments of a southeast asian mangrove, Phuket Island, Thailand, Biogeochemistry 26 (1994) 145–161. E. Kristensen, M.H. Jensen, G.T. Banta, K. Hansen, M. Holmer, G.M. King, Transformation and transport of inorganic nitrogen in sediments of a southeast asian mangrove forest, Aquatic Microbial Ecology 15 (1998) 165– 175. D.M. Alongi, A. Sasekumar, F. Tirendi, P. Dixon, The influence of stand age on benthic decomposition and recycling of organic matter in managed mangrove forests of Malaysia, Journal Experimental Marine Biology Ecology 225 (1998) 197–218. D.M. Alongi, F. Tirendi, L.A. Trott, T.T. Xuan, Benthic decomposition rates and pathways in plantations of the mangrove Rhizophora apiculata in the Mekong delta Vietnam, Marine Ecology Progress Series 194 (2000) 87–101. E. Kristensen, D.M. Alongi, Control by fiddler crabs (Uca vocans) and plant roots (Avicennia marina) on carbon, iron and sulfur biogeochemistry in mangrove sediment, Limnology Oceanography 51 (2006) 1557–1571. O.I. Nielsen, E Kristensen, D.J. Macintosh, Impact of fiddler crabs (Uca spp.) on rates and pathways of benthic mineralization in deposited shrimp pond waste. Journal Experimental Marine Biology Ecology, 289 (2003) 59–81. E. Kristensen, F.O. Andersen, N. Holmboe, M. Holmer, N. Thongtham, Carbon and nitrogen mineralization in sediments of the bangrong mangrove area, Phuket, Thailand, Aquatic Microbial Ecology 22 (2000) 199–213. T. Dittmar, N. Hertkorn, G. Kattner, R.J. Lara, Mangroves, a major source of dissolved organic carbon to the oceans. Global Biogeochemical Cycles, 2006, 20, GB1012, doi:10.1029/2005GB002570. D.M. Alongi, G. Wattayakorn, T. Ayukai, B.F. Clough, E. Wolanski, G.J. Brunskill, An organic carbon budget for mangrove-fringed Sawi Bay, southern Thailand, Special Publication. Phuket Marine Biological Center 22 (2000) 79–85. J.P. Gattuso, M. Frankignoulle, R. Wollast, Carbon and carbonate metabolism in coastal aquatic ecosystems, Annual Reviews Ecology Systematics 29 (1998) 405–434.
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Acta Ecologica Sinica journal homepage: www.elsevier.com/locate/chnaes
Processes of organic carbon in mangrove ecosystems Ye Yong a,⇑, Pang Baipeng a, Chen Guangcheng b, Chen Yan c a
State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361005, PR China Third Institute of Oceanography, State Oceanic Administration, Xiamen 361005, PR China c Minjiang University, Fuzhou 361005, PR China b
a r t i c l e
i n f o
Keywords: Mangrove Organic carbon Ecological processes
a b s t r a c t In addition to carbon accumulation in plants, processes of organic carbon in mangrove ecosystems include origins of sediment organic carbon, carbon fluxes between mangroves and their adjacent systems (coastal waters and atmosphere), and cycling processes. Sediment organic carbon originates from suspending solids in coastal waters, mangrove plants and benthic algae. In mangroves with low organic carbon content in sediments, tidal seawater is the main origin of sediment organic carbon, while in mangroves with high sediment organic carbon contents, sediment organic carbon mainly originates from mangrove plants. Due to tidal flush, there is large material exchange between mangrove ecosystems and their adjacent coastal waters. In China, exports of organic carbon in litter falls and dissolved organic carbon from mangroves to their adjacent coastal waters have not been documented. Processes of mangrove litter falls, including production, decomposition, export and animal consumption, determine linkages among organic carbon among mangrove plants, secondary production and coastal ocean. Consumers especially benthic animals may influence organic carbon in mangrove ecosystems, because (1) their consumption rates are high, and their selective feeding on some food sources will change the relative quantities of export, bury and mineralization of organic carbon from different origins; (2) their consumption is much more than assimilation, resulting in the changes in sizes, forms and qualities of nonassimilated organic matters, and then the changes in availability of export, consumption or mineralization of organic carbon. Respiration and sulfate reduction are important mineralization processes of organic carbon in mangrove sediments. Mineralization rates of organic carbon in mangrove sediments are influenced by quantities, activities and particle sizes of organic matters, and other factors such as forest ages, root activities and animal burrowing activities. Researches on processes of mangrove organic carbon should be based on open systems, and ecological processes of organic carbon should be coupled with vegetation restoration. Ó 2011 Ecological Society of China. Published by Elsevier B.V. All rights reserved.
1. Introduction
2. Origins of organic carbon in mangrove sediments
Processes of organic carbon are links of lots of functions of mangrove ecosystems, and they are closely related to social, ecological and economic benefits of mangroves such as coastal protection, pollution purification, biodiversity maintenance, and productivity [1–3]. Ecological processes of organic carbon in mangrove ecosystems are very complex, including origins of sediment organic carbon, carbon fluxes between mangroves and their adjacent systems (coastal waters and atmosphere), and cycling processes besides carbon accumulation in plants (primary production and plant respiration). In this paper, study progresses in these fields of processes of organic carbon in mangrove ecosystems were summarized and some research suggestions were put forward to give references in the role of mangroves in global carbon cycles.
Mangrove ecosystems can store lots of organic carbon, and some of them are rich in organic carbon in sediments deep in several meters [4]. Sediment organic carbon originates from suspending solids in coastal waters, mangrove plants (litter falls and underground roots) and benthic algae. Contribution rates of each origin are different in different literatures. Researches on carbon stable isotope indicated that mangrove plants were the main origin of organic carbon in mangrove sediments in southwest Brazil, Philippines, Vietnam and India [5–7]. In southwest Thailand mangroves, benthic algae, coastal waters and mangrove plants contributed 39%, 16% and 23% of sediment organic carbon, respectively [8]. Stable isotope compositions of organic carbon at two Tanzanian mangrove sites were different with stand species, and up to 35% of sediment organic carbon derived from coastal waters [9]. In Yucatan peninsula, Mexico, mangrove plants, phytoplankton and seagrass contributed to organic carbon in sediments but their
⇑ Corresponding author. E-mail address: [email protected] (Y. Yong).
1872-2032/$ - see front matter Ó 2011 Ecological Society of China. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.chnaes.2011.03.008
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contributions were different at different sites [10]. Bouillon et al. summarized that in mangroves with low carbon stocks, sediment organic carbon had low C/N and d13C, and suspending solids in coastal waters were the main origin of sediment organic carbon, while in mangroves with high carbon stocks, sediment organic carbon had high C/N and d13C similar to those of mangrove plants which were the main origin of sediment organic carbon [11]. In addition, most of organic carbon in mangroves was in the underground roots which could change sediment conditions through physiological processes. For example, the underground roots could release oxygen into mangrove sediments and increase the storage of sedimentary organic carbon through exudates of living roots and decomposition of dead roots. The accumulation of organic carbon in mangrove sediments at four sites along the Shark River estuary in south Florida were investigated with empirical measures and a process-based model. Model sensitivity analyses suggested that root production had more significant effects on sediment composition than litter falls [12].
3. Carbon fluxes between mangroves and their adjacent systems Through determination of sediment organic carbon origins, the difficultly-decomposing compositions of stored organic carbon are reflected, but the real-time carbon fluxes does not be known. For example, compared to organic matters from mangrove plants, those from the adjacent seawater are difficult to be decomposed and easily to be stored in mangrove sediments. Thus, even if the sediments have more organic carbon from phytoplankton, low carbon fluxes may be into the sediments. Carbon fluxes in mangrove ecosystems are mostly investigated between mangrove plants and atmosphere (photosynthesis stored carbon and respiration released carbon by plants). The net production of organic carbon in mangroves (primary production) may be accumulated in the local sediments or exported to the adjacent waters in the form of litter, debris and dissolved organic carbon, while organic carbon in adjacent waters can enter the sediments through sedimentation, forming organic carbon fluxes among mangrove plants, sediments and adjacent waters. Benthic algae and other photo-autotrophic microorganisms in surface sediments can also fix atmospheric CO2, and organic carbon entering the sediments can be released into atmosphere as CO2 and CH4 through various functions of the microbes, such as mineralization, resulting in carbon fluxes between sediments and atmosphere. Most of mangrove ecosystems are extremely open. Due to tide actions, there are lots of long-term material exchanges between mangroves and their adjacent waters, which is the significant difference between mangrove forests and inland forests (including inland wetlands). Mangrove ecosystems may provide organic carbon for coastal waters, and some foreign scholars studied output of mangrove organic matters [13]. Litter falls accounted for about 1/ 3 of the net production in mangrove forests [14]. In some cases mangroves exported organic carbon as litter and particular (or dissolved) forms to adjacent waters, and the ratio of litter output was up to 1/2 [14]. There were also evidences indicating that output of dissolved organic carbon was comparable to output of litter organic carbon in some mangroves [14]. However, so far there were few studies on the roles of mangroves in dissolved and particular organic carbon budget in coastal waters [15], and the published data were usually contradictory, due to the differences in research methods and difficulties in accurate determination of material fluxes between mangroves and their adjacent coastal waters. The difficulties in determination of material fluxes between mangroves and their adjacent coastal waters are that material fluxes largely changed with tidal actions, resulting in greatly random values, and there were large differences in tidal range, topography, sedi-
ment chemistry and community structure among the studied mangrove ecosystems [16]. In China, since early 1980s, mangrove litter production has been studied, but only temporal dynamics were reported [17], and output of litter and dissolved organic carbon are not documented. In addition, most of mangroves grow along deposit coastlines where large rivers flow and the flats are even, so they can accelerate sedimentation of suspended materials and become sinks of organic carbon of coastal waters during tide flooding periods. There are still few studies on input flux of organic carbon in mangroves, though the evidence indicated that flocculation of small particles in mangroves resulted in net input of organic carbon in a highly vegetated mangrove at Middle Creek, Cairns, Australia [18]. 4. Organic carbon cycling processes in mangrove ecosystems 4.1. Dynamic processes of litter falls Dynamic processes of litter falls in mangroves include production, decomposition, output and animal feeding, determining the relations among mangrove plants, secondary production, and coastal seawater organic carbon. So far studies on decomposition of mangrove litter falls and concomitant nutrient dynamics have been focused on the differences among tide levels [19], plant species and seasons [19–21] and litter components [22]. Rapid decomposition of organic matter in mangrove ecosystems seems to ensure that the majority of organic production circulated within the forest, which might reduce export of organic carbon from mangroves to their adjacent waters by tides [23]. Machiwa and Hallberg confirmed that dissolved organic carbon accounted for 80% of total export of organic carbon [24]. Three weeks’ leaching amount of organic carbon from mangrove debris by seawater accounted for about 33% of dry mass loss during the whole decomposing period of litter leaves of Rhizophora mangle, and leaching loss of organic carbon was rapid with a peak value on the second day of leaching experiment, indicating that dissolved organic carbon from decomposition of litter leaves might be the main output of mangrove matters [25]. About four decades ago, Odum proposed a groundbreaking hypothesis in coastal ecology according to which the outwelling of litter falls from coastal wetlands was a major source of energy that supported much of the secondary production of estuaries and coastal waters, but now this hypothesis is being questioned [26], because the main output of organic carbon from mangroves is dissolved organic carbon but not litter falls themselves. 4.2. Effects of benthic animals on dynamics of organic carbon Consumers, especially benthic animals, have great effects on the whole dynamics of organic carbon in mangrove ecosystems because (1) their consumption rates are high, and their selective feeding on some food sources will change the relative quantities of export, bury and mineralization of organic carbon from different origins, and (2) their consumption is much more than assimilation, resulting in the changes in sizes, forms and qualities of non-assimilated organic matters, and then the changes in availability of export, consumption or mineralization of organic carbon [26]. Consumption percents of mangrove litter leaf production by invertebrates (especially crabs) were much different in different mangroves, ranging from 10% to 90%, which is an important factor adjusting the output of organic carbon from mangroves, and is more efficient in retention of organic carbon from mangrove litter leaves and litter turnover compared to only microbial decomposition [27–29]. Foraging behaviors of mangrove animals influence characters and availability of organic matters through many mechanisms,
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and the usually reported is foraging mangrove litter leaves by Sesarma crabs. The high palatability of brown leaves compared with green and, in particular, yellow leaves probably results from improved nutritional values and removals of inhibitory compounds such as tannins by the aging process and yellow leaves just fallen from trees are poor in nitrogen and rich in tannins [30,31]. Direct feeding by Sesarma crabs reduces tidal output of litter organic carbon, and many crabs drag litter leaves into their caves where litter leaves continue to be decomposed [27,31,32]. Field experiments carried out in tropical mangroves dominated by R. harrisonii and R. mangle in Guayas River estuary in Ecuador demonstrated that the mangrove crabs could remove the whole daily produced litter leaves within 1 h, so the leaf turnover is much faster than that estimated based on only leaf decomposition [21]. Therefore, even in estuarine mangroves with strong tidal flushing, types of litter dynamics are also determined by crab foraging. Amount of consumption by Sesarma crabs is twice as much as that of assimilation [30], i.e., half of litter leaves foraged by crabs were changed into faecal materials to provide food for decomposers or debris food web, which is a very important ecological process because the faecal materials with fine organic particles and high nitrogen contents are easily used by other invertebrates [33], and the decomposition rates greatly increased compared to those of original litter materials [33,34], resulting in accelerating organic carbon turnover. In China, although there are many literatures on crab distribution in mangroves, data on feeding ecology of mangrove crabs are limited and most of them are descriptive, and litter leaf removals by crabs have not been well quantified, resulting in an incomplete understanding of food webs and biogeochemical cycles in mangroves. Therefore, few estimates could test that crab consumption might have an impact on the fate of mangrove litter leaves in most mangroves in China. There, the only two reports on leaf litter removal by crabs were carried out by us in a Kandelia candel forest in Jiulongjiang Estuary in Fujian [29,31]. Recently, the traditional views that mangrove plants are the main supplier of organic carbon and mangrove litter leaves are the main food source for benthic animals were challenged. It has become increasingly clear that mangrove invertebrates exploit a wide range of potential food resources, including mangrove litter, epiphytic algae, benthic microalgae, bacteria and fungi, as well as macro-algae and a mixture of organic sources imported from adjacent aquatic environments by tidal currents, thus, the degree of utilization of mangrove derived food sources depends partially on the degree of material exchange with adjacent systems [26]. 4.3. Dynamics of sedimentation of organic carbon in mangrove ecosystems Mangroves develop in hidden areas where fine sediments accumulate, and many plants have wide ground roots which can accelerate to capture silt and clay particles. To understand how sedimentation affects long-term sustainability of mangrove wetlands, it is important to recognize sedimentation dynamics in mangroves. There have been lots of reports on sedimentation rates in mangroves at abroad and few in China usually by 210Pb isotope method and sign stake method [35]. Although these methods can reflect sedimentary history in mangroves, we can know nothing on dynamic processes of sedimentation of organic carbon from them. Therefore, processes controlling sedimentation dynamics are not well understood, so it is hard to explain sediment budget of organic carbon and its role in coastal sedimentary environment. Kitheka et al. studied sediment exchanges in a degraded mangrove forest in south Kenya where they collected water samples at half of the tide water depth and measured concentrations of the total and particular organic suspending sediments [36]. Victor et al. conducted a six-month study on sedimentary rates in Pohn-
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pei mangroves in Micronesia with 5 cm diameter sediment traps which were fixed at the bottom for one month along transects [37]. Adame et al. also used similar method to study mangrove sedimentary dynamics in southeast Queensland, Australia [38]. Sedimentary dynamics of organic carbon in mangrove ecosystems can be availably studied with these relatively immediately sampling methods. 4.4. Mineralization processes of organic carbon in mangrove sediments Mineralization of organic carbon in mangrove sediments is also important in determining carbon stock in mangrove ecosystems. Respiration and sulfate reduction might be the most important mineralization processes of organic carbon in mangrove sediments, and each of them accounted for 40–50% of the total mineralization [26]. Most of mangrove sediments are rich in reducing inorganic sulfur with the forms of FeS2, sulfur and few FeS [39]. Traditionally, denitrification, manganese respiration and iron respiration are not considered important in mangrove sediments [40]. Aerobic respiration and anaerobic sulfate reduction are usually considered the most important microbial respiration processes, but recent evidences suggested that in mangrove sediments with high iron contents the role of iron respiration in mineralization of organic carbon may be similar to or even higher than that of sulfate reduction [26]. Besides contents, activities and sizes of organic matter, mineralization rates of organic carbon in mangrove sediments are also influenced by other factors such as forest age, physiological activities of the roots, extent of water-logging and intensity of faunal burrowing activities [26]. The study at the Matang Mangrove Forest Reserve in peninsular Malaysia showed that (1) sulfate reduction was the dominant mineralization process of organic carbon in mangrove sediments, accounting for 51–75% of total mineralization of organic carbon; (2) aerobic respiration and denitrification accounted for 5–20% and 25% of total mineralization of organic carbon, respectively; and (3) with the increase in mangrove age, efficiency of carbon burial in sediments increased from 16% to 27%, while the ratio of total mineralization of organic carbon in sediments to mangrove net primary production decreased from 28% to 7% [1]. In young Avicennia marina and R. apiculata stands, sulfate reduction accounted for 20–30% of total mineralization of organic carbon, but sulfate reduction increased with stand age and represented most of sediment total mineralization of organic carbon in old stands [41,42]. With the increase in stand age, input of organic carbon was enhanced and fresh organic matter increased, so sulfate reduction could be a dominant mineralization process of organic carbon. It seems that the roots of A. marina have complementary effects on the biogeochemistry of mangrove sediments as oxygen leaching by the roots keeps the rhizosphere deep in sediments oxidized and enriched in Fe3+ for use by iron reducers, and at the same time, leaching of labile dissolved organic carbon from roots appears to stimulate bulk sulfate reduction [43]. As sulfate reduction usually is hampered in the presence of more potent electron acceptors (e.g. O2 and Fe3+), this process becomes inferior to iron respiration when oxidizing roots and in-faunal burrows increase the Fe3+ content in mangrove sediments [44]. Sulfate reduction in the flat with animal caves was only half of that in the flat without animal caves [45]. 5. Carbon budget in mangrove ecosystems Studies on ecological processes of organic carbon in mangrove sediments are also important in oceanic and even global carbon budget [1,2,46]. Estuarine coast is one of the areas in biosphere with most active biogeochemical processes, while mangroves are
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the dominant ecosystems with high productivity in tropical and subtropical estuarine coast, so they have strong carbon processes [11]. Although mangroves has smaller area than other habitats, they account for about 11% of the total input of terrestrial carbon into the ocean and 15% of the total carbon accumulated in modem marine sediments [2,3]. These global estimates are still uncertain (based on only tropical mangroves), but at least they indicate the importance of processes of organic carbon in mangrove ecosystems in global oceanic carbon budget. Mangrove ecosystems are generally considered net autotrophic as they can enhance the accumulation of organic carbon in sediments and have high productivity and low ratio of sediment respiration to net primary production, resulting in a potential for mangrove sediments to accumulate organic carbon for a long time [47]. There are some documents about global carbon budget in mangrove ecosystems. For example, Twilley et al. estimated that global mangroves had carbon stock of 3 1014 mol C and net ecosystem production of 1.5 1013 mol C yr 1 [4], while Gattuso et al. estimated that global mangroves had gross primary production of 4.6 1013 mol C yr 1 in which the net ecosystem production was 1.8 1013 mol C yr 1 [48]. However, these estimates are based on only tropical areas, and most of them are based on mangrove plant community level but not at the ecosystem level, i.e. these estimates are not based on the systemic analyses of ecological processes of organic carbon in mangrove ecosystems and their availability may be questionable. The variability in carbon transformations and transport conditions among mangrove environments is affected by specific local conditions with respect to climate, degree of exposure to strong water movement, the vicinity of river discharges, soil and bedrock composition in the neighboring terrestrial system and, not the least, the local vegetation and fauna. Due to such inherent environmental variability combined with the rather limited data available, generalization on a global scale becomes troublesome [26]. Therefore, carbon budget in global mangrove ecosystems should be given based on more widely spatial and temporal data. In China, most of mangroves are in subtropical regions and the studies on mangrove carbon budget have not been carried out. Therefore, the studies on the processes of organic carbon in China may make contribution for the global mangrove carbon budget. In addition, the changes of carbon budget with vegetation development have not been reported in mangrove ecosystems. Currently, more than 80% of mangroves in China are secondary artificial forests, and this ratio of artificial mangroves will increase in global mangroves with the development of society. Therefore, the changes in processes of organic carbon with vegetation development in artificially restored mangroves should be studied and more attention should be paid to its role in oceanic carbon budget as well as global changes.
6. Perspectives and suggestions Over the past two decades, a large number of case studies have significantly increased our knowledge on carbon dynamics in mangrove ecosystems and on the importance of various biogeochemical processes. We still lack, however, a complete understanding of the underlying mechanisms controlling the spatial and temporal variability of these processes as a function of the changes in environmental conditions [26]. And further studies, especially those on stocks, accumulation history and sedimentation age, input and output, compositions and origins, dynamical parameters and characters of decomposition and transformation of organic carbon, should be carried out in subtropical mangroves. To give the global carbon budget and understand the roles of mangroves in global
carbon cycle, data on carbon budget should be improved in more mangrove areas. In China, studies on element cycles in mangroves have been carried out widely in Hainan, Guangxi, Fujian and Guangdong since early 1980s. Unfortunately, in all of these studies mangroves were considered as closed systems and material and energy exchanges between mangroves and their adjacent waters were not included, i.e. only plants and microorganisms were considered as the main parts in material cycles and all of litter falls were assumed to return into mangrove forests. Therefore, despite of some difficulties, it is necessary to study these fields based on open mangrove ecosystems. In addition, more than 80% of mangroves in China are secondary artificial forests, and this ratio will increase in global mangroves with the development of society, so more attention should be paid to the changes in processes of organic carbon in artificially restored mangroves with the development of mangrove vegetation.
Acknowledgements This project was supported by the National Natural Science Foundation of China (Nos. 40706042 and 41076049).
References [1] D.M. Alongi, A. Sasekumar, V.C. Chong, J. Pfitzner, L.A. Trott, F. Tirendi, P. Dixon, G.J. Brunskill, Sediment accumulation and organic material flux in a managed mangrove ecosystem: estimates of land–ocean–atmosphere exchange in peninsular Malaysia, Marine Geology 208 (2004) 83–402. [2] S. Bouillon, R.M. Connolly, S.Y. Lee, Organic matter exchange and cycling in mangrove ecosystems: recent insights from stable isotope studies, Journal Sea Research 59 (2008) 44–58. [3] T.C. Jennerjahn, V. Ittekkot, Relevance of mangroves for the production and deposition of organic matter along tropical continental margins, Naturwissenschaften 89 (2002) 23–30. [4] R.R. Twilley, R.H. Chen, T. Hargis, Carbon sinks in mangroves and their implications to carbon budget of tropical coastal ecosystems, Water, Air Soil Pollution 64 (1992) 265–288. [5] C.E. Rezende, L.D. Lacerda, A.R.C. Ovalle, C.A.R. Silva, L.A. Martinelli, Nature of POC transport in a mangrove ecosystem: a carbon isotopic study, Estuarine, Coastal Shelf Science 30 (1990) 641–645. [6] H. Kennedy, E. Gacia, D.P. Kennedy, S. Papadimitriou, C.M. Duarte, Organic carbon sources to SE Asian coastal sediments, Estuarine, Coastal Shelf Science 60 (2004) 59–68. [7] A.B.K. Prasad, A.L. Ramanathan, Organic matter characterization in a tropical estuarine-mangrove ecosystem of India: Preliminary assessment by using stable isotopes and lignin phenols, Estuarine, Coastal Shelf Science 84 (2009) 617–624. [8] T. Kuramoto, M. Minagawa, Stable carbon and nitrogen isotopic characterization of organic matter in a mangrove ecosystem on the southwestern coast of Thailand, Journal of Oceanography 57 (2001) 421–431. [9] A.N.N. Muzuka, J.P. Shunula, Stable isotope compositions of organic carbon and nitrogen of two mangrove stands along the Tanzanian coastal zone, Estuarine, Coastal Shelf Science 66 (2006) 447–458. [10] M.E. Gonneea, A. Paytan, J.A. Herrera-Silveira, Tracing organic matter sources and carbon burial in mangrove sediments over the past 160 years, Estuarine, Coastal Shelf Science 61 (2004) 211–227. [11] S. Bouillon, F. Dahdouh-Guebas, A.V.V.S. Rao, N. Koedam, F. Dehairs, Sources of organic carbon in mangrove sediments: variability and possible ecological implications, Hydrobiologia 495 (2003) 33–39. [12] R.H. Chen, R.R. Twilley, A simulation model of organic matter and nutrient accumulation in mangrove wetland soils, Biogeochemistry 44 (1999) 93–118. [13] F. Baltzer, M. Allison, F. Fromard, Material exchange between the continental shelf and mangrove-fringed coasts with special reference to the AmazonGuianas coast, Marine Geology 208 (2004) 115–126. [14] R.R. Twilley, Exchange of organic carbon in basin mangrove forests in southern Florida estuary, Estuarine, Coastal Shelf Science 20 (1985) 543–557. [15] Y. Akamatsu, S. Ikeda, Y. Toda, Transport of nutrients and organic matter in a mangrove swamp, Estuarine, Coastal Shelf Science 82 (2009) 233–242. [16] T. Ayukai, D. Miller, E. Wolanksi, S. Spagnol, Fluxes of nutrients and dissolved and particulate organic matter in two mangrove creeks in northeastern Australia, Mangroves Salt Marshes 2 (1998) 223–230. [17] F.Z. Zheng, P. Lin, C.Y. Lu, W.J. Zheng, Inter annual dynamic of litter full of Kandelia candel mangrove and energy flow through the litter in Jiulongjiang Estuary, Fujian province, China, Acta Ecologica Sinica 18 (2) (1998) 113–118. [18] K. Furukawa, E. Wolanski, H. Mueller, Currents and sediment transport in mangrove forests, Estuarine, Coastal Shelf Science 44 (1997) 301–310.
Y. Yong et al. / Acta Ecologica Sinica 31 (2011) 169–173 [19] P.L. Mfilinge, N. Atta, M. Tsuchiya, Nutrient dynamics and leaf litter decomposition in a subtropical mangrove forest at Oura Bay Okinawa Japan, Trees 16 (2002) 172–180. [20] P. Lin, H.Q. Fan, Seasonal model of the decomposition rates of Kandelia candel fallen leaves in Jiulongjiang River Estuary, Journal Xiamen University (Natural Science) 31 (1992) 428–434. [21] R.R. Twilley, M. Pozo, V.H. Garcia, V.H. Rivera-Monroy, R. Zambrano, A. Bodero, Litter dynamics in riverine mangrove forests in the Guayas River estuary, Ecuador, Oecologia 111 (1997) 109–122. [22] A.G. Van der Valk, P.M. Attiwill, Decomposition of leaf and root litter of Avicennia marina at Westernport Bay, Victoria, Australia, Aquatic Botany 18 (1984) 205–221. [23] M. Hemminga, F.J. Slim, J. Kazungu, G.M. Ganssen, J. Nieuwenhuize, N.M. Kruyt, Carbon outwelling from a mangrove forest with adjacent seagrass beds and coral reefs (Gazi Bay, Kenya), Marine Ecology Progress Series 106 (1994) 291–301. [24] J.F. Machiwa, R.O. Hallberg, An empirical model of the fate of organic carbon in a mangrove forest partly affected by anthropogenic activity, Ecological Modelling 147 (2002) 69–83. [25] S.E. Davis, C. Corronado-Molina, D.L. Childers, J.W. Day, Temporally dependent C, N, and P dynamics associated with the decay of Rhizophora mangle L. leaf litter in oligotrophic mangrove wetlands of the Southern Everglades, Aquatic Botany 75 (2003) 199–215. [26] E. Kristensen, S. Bouillon, T. Dittmar, C. Marchand, Organic carbon dynamics in mangrove ecosystems: A review, Aquatic Botany 89 (2008) 201–219. [27] A.I. Robertson, Leaf burying crabs: their influence on energy flow and export from mixed mangrove forests (Rhizophora sp.) in northeast Australia, Journal Experimental Marine Biology Ecology 102 (1986) 237–248. [28] J.O. Bosire, F. Dahdouh-Guebas, J.G. Kairo, J. Kazungu, F. Dehairs, N. Koedam, Litter degradation and CN dynamics in reforested mangrove plantations at Gazi Bay, Kenya, Biological Conservation 126 (2005) 287–295. [29] G.C. Chen, Y. Ye, C.Y. Lu, Seasonal variability of leaf litter removal by crabs in a Kandelia candel mangrove forest in Jiulongjiang Estuary, China, Estuarine, Coastal Shelf Science 79 (2008) 701–706. [30] N. Thongtham, E. Kristensen, Carbon and nitrogen balance of leaf eating sesarmid crabs (Neoepisesarma versicolor) offered different food sources, Estuarine, Coastal Shelf Science 65 (2005) 213–222. [31] G.C. Chen, Y. Ye, Leaf consumption by Sesarm aplicata in a mangrove forest at Jiulongjiang Estuary, China, Marine Biology 154 (2008) 997–1007. [32] M.W. Skov, R.G. Hartnoll, Paradoxical selective feeding on a low nutrient diet: why do mangrove crabs eat leaves? Oecologia 131 (2002) 1–7. [33] S.Y. Lee, Potential trophic importance of the faecal material of the mangrove sesarmine crab Sesarma messa, Marine Ecology Progress Series 159 (1997) 275–284. [34] P.L. Mfilinge, T. Meziane, Z. Bachok, M. Tsuchiya, Litter dynamics and particulate organic matter outwelling from a subtropical mangrove in
[35]
[36]
[37]
[38]
[39]
[40]
[41]
[42]
[43]
[44]
[45]
[46]
[47]
[48]
173
Okinawa Island, South Japan, Estuarine, Coastal Shelf Science 63 (2005) 301– 313. Q.M. Zhang, X.S. Wen, C.J. Song, S. Liu, The measurement and study on sedimentation rates in mangrove tidal flats, Tropic Oceanology 15 (4) (1996) 57–62. J.U. Kitheka, G.S. Ongwenyi, K.M. Mavuti, Fluxes and exchange of suspended sediment in tidal inlets draining a degraded mangrove forest in Kenya, Estuarine, Coastal Shelf Science 56 (2003) 655–667. S. Victor, L. Neth, Y. Golbuu, E. Wolanski, R.H. Richmond, Sedimentation in mangroves and coral reefs in a wet tropical island, Pohnpei, Micronesia, Estuarine, Coastal Shelf Science 66 (2006) 409–416. M.F. Adame, D. Neil, S.F. Wright, C.E. Lovelock, Sedimentation within and among mangrove forests along a gradient of geomorphological settings, Estuarine, Coastal Shelf Science 86 (2010) 21–30. M. Holmer, E. Kristensen, G. Banta, K. Hansen, M.H. Jensen, N. Bussawarit, Biogeochemical cycling of sulfur and iron in sediments of a southeast asian mangrove, Phuket Island, Thailand, Biogeochemistry 26 (1994) 145–161. E. Kristensen, M.H. Jensen, G.T. Banta, K. Hansen, M. Holmer, G.M. King, Transformation and transport of inorganic nitrogen in sediments of a southeast asian mangrove forest, Aquatic Microbial Ecology 15 (1998) 165– 175. D.M. Alongi, A. Sasekumar, F. Tirendi, P. Dixon, The influence of stand age on benthic decomposition and recycling of organic matter in managed mangrove forests of Malaysia, Journal Experimental Marine Biology Ecology 225 (1998) 197–218. D.M. Alongi, F. Tirendi, L.A. Trott, T.T. Xuan, Benthic decomposition rates and pathways in plantations of the mangrove Rhizophora apiculata in the Mekong delta Vietnam, Marine Ecology Progress Series 194 (2000) 87–101. E. Kristensen, D.M. Alongi, Control by fiddler crabs (Uca vocans) and plant roots (Avicennia marina) on carbon, iron and sulfur biogeochemistry in mangrove sediment, Limnology Oceanography 51 (2006) 1557–1571. O.I. Nielsen, E Kristensen, D.J. Macintosh, Impact of fiddler crabs (Uca spp.) on rates and pathways of benthic mineralization in deposited shrimp pond waste. Journal Experimental Marine Biology Ecology, 289 (2003) 59–81. E. Kristensen, F.O. Andersen, N. Holmboe, M. Holmer, N. Thongtham, Carbon and nitrogen mineralization in sediments of the bangrong mangrove area, Phuket, Thailand, Aquatic Microbial Ecology 22 (2000) 199–213. T. Dittmar, N. Hertkorn, G. Kattner, R.J. Lara, Mangroves, a major source of dissolved organic carbon to the oceans. Global Biogeochemical Cycles, 2006, 20, GB1012, doi:10.1029/2005GB002570. D.M. Alongi, G. Wattayakorn, T. Ayukai, B.F. Clough, E. Wolanski, G.J. Brunskill, An organic carbon budget for mangrove-fringed Sawi Bay, southern Thailand, Special Publication. Phuket Marine Biological Center 22 (2000) 79–85. J.P. Gattuso, M. Frankignoulle, R. Wollast, Carbon and carbonate metabolism in coastal aquatic ecosystems, Annual Reviews Ecology Systematics 29 (1998) 405–434.