... at large; and the value of a wetland as part of an integrated landscape(h4itsch .... progressively use oxidized soil substrates as electron acceptors for their ...
Carbon in Tropical Wetlands H.U. Neuel* J.L. Gauntl, Z.P. Wan@, P. Becker-Heidmann3, C. Quijanol. llnternational Rice Research Institute, Los Bafios, Philippines, 2Louisiana State University, Baton Rouge, Louisiana , USA., 3University of Hamburg, Allende-Platz 2, Hamburg, Germany. Introduction. Estimated coverage of wetlands range between 700 million ha (Aselmann and
Crutzen 1990, Sanchez and Buol 1985) and 900 million ha (Armentano T.V. 1980, Mitch and Gosselink 1986) of the word's land area. The importance of wetlands to global biogeochemistry, wildlife, and human food production is much greater than their proportional surface area on Earth (up to 6.4%) would suggest. Both natural and agricultural wetlands are valuable resources and important ecosystems. Only two major tropical crops, rice and taro, adapt readily to production on wetland soils. Rice is grown on 11% of the world's arable land and 88% of these 148 million ha are wetlands. In Asia the harvested rice area accounts between 10% of arable land in Pakistan to 124% in Indonesia. The world's production of 520 million tons of rough rice provides 20% of global human per capita energy and 15% of per capita protein (IRRI 1993). In Asia rice provides 35-80% of total calories consumed. Asia accounts for 59% of the global population, about 92 of the world's rice production, and 90% of global consumption. With year round water supply and short duration, photoperiod insensitive rice cultivars, two or three rice crops may be grown each year resulting in nearly permanently waterlogged soils. Natural Wetlands have been significantly reduced by human activity in the last 100 years. In the past, wetland management mostly meant converting natural wetlands to agricultural and aquaculture production. Except for rice cultivation drainage was the major concept for managing wetland. With the recognition of wetland values, objectives, such as to preserve wetlands wildlife population, to maintain and improve hydrological cycles and water quality, and to keep or increase the sink strength for carbon have become important wetland management tasks. As a result of conflicting wetland uses, it is difficult to balance the denominators of values of various wetlands. There are conflicts between a private owner's interest in wetlands, the perception that accrues to the public at large; and the value of a wetland as part of an integrated landscape(h4itsch and Gosselink, 1993). Wetlands
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Wetlands are transitional between terrestrial and aquatic systems that support predominantly hydrophytes at least periodically. Wetlands occur in areas where soils are naturally or artificially inundated or saturated by water due to high groundwater or surface water during part or all of the year. Wetlands are common in river deltas and estuarine, floodplains, tidal areas, and are widespread in river beds, depressions, footslopes, and terraces of undulating landscapes. Wetland ecosystems maybe discriminated on the basis of hydrology, soils, and vegetation (Cowardin et al., 1979) and generally include swamps, marshes, bdgs, fens, floodplains and shallow lakes. In an attempt to serve the needs of agriculture and at the same time maintain practical and sensible boundaries to natural wetlands, Brinkman and Blokhuis (1986) defined wetland as having free
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water at or near the surface for at least the major part of the growing season of arable crops, or for at least 2 months of the growing season of perennial crops, grassland, forest, or other vegetation. The water is suficiently shallow to allow the growth of a crop or of natural vegetation rooted in the soil. Free water may occur naturally or may be retained by field bunds, puddled plow layers, or traffic pans fiom rainfall, run-off, or irrigation sources. Wetlands as defined within this review have at least one wet growing season, but may be dry, moist, or without surface water in other seasons. Wetland soils may therefore alternately support wetland and dryland crops. The boundary between wetland and dryland is often gradual. The boundary may fluctuate fiom year to year depending on variations in precipitation. If water (drainage and irrigation) can be hlly controlled it is within f m e r s discretion to establish, either wet- or drylands. But in most tropical wetlands drainage capacities are insufficient to prevent periodic soil submergence during the rainy season. Estimates about the area of wetlands are very uncertain because there is no common clear definition of wetlands. Since wet grasslands contain histosols or gleysols, and the boreal forest, tundra, and certain tropical forests contain additional organic deposits, the actual area of world organic soils could exceed 900 million ha (Duxbury et al. 1979; Annentano 1980) Tropical wetlands, as defined here, may therefore cover more than 500 million ha and contain the most . productive agricultural and natural ecosystems on earth (Downing et al., 1993). Wetland soils Wetland soils development and properties are influenced by temporary or permanent saturation in the upper part of the pedon. If anaerobic conditions impose permanent characteristics on the soil the terms "gley-phenomena" (Moonnann and van de Wetering, 1985) or "hydromorphic propertiesu(FAO, 1974) are commonly used. Soil classifications do not deal with wetland soils but with hydromorphic soili, i.e. soils with defined long lasting signs of periodically or permanently reducing soil conditions. Reducing conditions may not occur in wetland soils that contain considerable dissolved ,oxygen, lack decomposable organic matter in combination with high contents of calcium carbonate, or suppress activity of reducing microorganisms ,(Moorman and van de Wetering 1985). Many rice growing countries have developed classification systems that discriminate naturally wet soils and rice (paddy) soils. The only soil systems applicable worldwide are the Legend of the FAO-UNESCO soil map of the world (FAO, 1974) and the Soil Taxonomy (USDA, 1975). In the FAO-UNESCO Legend for the soil map of the world (FAO, 1974) Gleysols, Fluvisols, Planosols, and Histosols make up most of the wetland soils. It has been proposed so separate Plinthosols fiom the Ferrasols because the formation of plinthite causes waterlogging by surface water. Gleyic subunits of; for example, Acrisols, Luvisols, or Podsols are mostly wetland soils as well. Soil Taxonomy (USDA, 1975) recbgnizes hydromorphic,,soils at ,he suborder level by an aquic moisture regime that has caused defined signs of reduction (mainly weqand soils), and soils with hydromorphism in some horizons at the subgroup ievq. ,Aquic subwoups generally are not wetland soils since signs of wetness are only found in subsoil horizons. All soil orders, except
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Histosols, Vertisols, and Aridisoh, have aquic suborders. Practically, all Aridisols are dryland soils while Histosols are wetland soils per se. Vertisols are found in wetlands but water saturation in Vertisols is always a surface feakre which does not qualifL for an aquic moisture regime. Recently the definition of the aquic conditions has been widened in soil taxonomy (SMSS, 1992), discriminating endosaturation, episaturation, and anthfic saturation (a variant of episaturation, associated with controlled flooding) at the suborder level in all orders, except Aridisols and Histosols. Histosols are much less defined, probably because they are less used by man. About 10% of the world's histosols are being f m e d while only 5% of organic soils in the tropics may be used for rice growing and grazing (Armentano 1980). Recent reports, however, indicate a growing emphasis on reclgiming swamps by drainage as in ~ a l i m b t a nand Sumatra (Indonesia) which have 26 million ha of swamps, and in the Sudd (Sudan) with permanent swamps of 13 million ha, in the Patanal (Brazil) with 17 million ha of swamps. In the Sudd many of the soils are mapped as entisols and vertisols though these soils are overlain by organic material up to 1.5 m deep (Rzoska, 1974). Biogeochemistry of wetland soils' The biogeochemistry of wetlands is controlled by flooding and the resulting status and pattern of oxidation and reduction reactions. Terrestrial ecosystems within a watershed highly s e c t flooding pattern, groundwater level, water quality, sedimentation, and erosion in wetlands . Irrigation, water harvesting, drainage, and cultivation practices influence the biogeochemistry of wetland soils used for agriculture. Flooding a soil drastically changes its hydrosphere, atmosphere, and biosphere and bio eochemistry. Flooding decreases diffision of atmospheric oxygen to the soil by a factor of 10 and sets in motion a series of unique physical, chemical, and biological processes not observed in dryland soils. The nature, pattern, and extent of the processes depend on the physical and chemical properties of the soil, duration of flooding, quality of floodwater, biosphere of soil and floodwater, management practices, plant growth, and climatic conditions. Properties, chemistry, and fertility of wetland soils have recently been reviewed by several authors (Kyuma et at., 1986; Neue, 1989, 1990; Roger and Kurihara, 1988; Neue and Zhu Zhong-lin, 1990).
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After 0 2 is depleted by aerobic respiratioq facultative and obligate anaerobic organisms progressively use oxidized soil substrates as electron acceptors for their respiration. Denitritjling bacteria use nitrate as an alternative electron acceptor for the oxidation of organic matter below a redox potential of +420 mV at pH 7. When nitrate is depleted, ~ n + reduction 4 begins below +400mV, followed by the reduction of ~ e + at 3 -180mV. These reactions are catalyzed by various bacteria that use fermentation to obtain energy, with h 4 d 4 and ~ e + acting 3 indirectly as electron acceptors (Lovely and Philipps 1989). Bacteria have also been isolated that directly couple the reduction of Mn and Fe to the oxidation of simple organic substances (Lovely and Phillips 1988). Obligate anaerobes reduce sulfate when the redox drops below -215mV and methane is formed at -244mV. Sulfate reducing bacteria' produce a variety of s u k r gases, including hydrogen sulfide &S, dimethylsulfide [(CH3)2S],'and dimethyidisulfide [(CH3)2S2] (Schlesinger 1991). Once formed, hydrogen sulfide will readily react with F'e2+ or other heavy metal ions and precipitate or
form carbon-bonded sulfur that accumulates in peat sedii amounts of H2S are formed in organic soils low in F$+ and soils low in Fe increased H2S production, especially when ae 1984). In the soil solution he found concentrations of up to 60mg H2S/L. Castro and (1987) reported a flux of 1-1 10 mg S m-2 y f l for wetlands in Florida. Prior to emissions, the release of biogenic gases fiom wetlands was the suffir gases into the atmosphere (Warneck 1988). Although the reduction of flooded soils proceeds stepwise in a thermodynamic sequence, oxidation-reduction reactions are only partially applicable to field conditions where redox ' potentials of a given redox reaction span a fairly wide range (Neye, 1991). Mineral phases present in soils are not pure and chemical reactions that are favored thermodynamically may not necessarily be kinetically favored . The equilibrium depends strongly on microbial growth and behavior and on the degree to which reacting products diffise and mix: Patrick and Reddy (1 discussed the possibility of overlap between the individual reduction system.. Nitrate manganese reduction as well as manganese and iron reduction sulfate reduction will not occur in the presence of 02, NO3 or that the critical redox potential for initiation of CHq formation and overlaps with sulfate reduction. Lowering the redox to production. In calcareous soils we even found CHq formation However, given the heterogeneous nature of soil systems with its high spatial and tempor variability , different reduction processes may well occur simultaneously at separate locations.
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Soil reduction and accumulatibn of C02 and resultant HCO3- from degrading organic matter buffers the pH near neutral in flooded soils. The increase in pH of acid soils is initially brought about by soil reduction of Fe-oxyhydroxides. The pH decrease of sodic and calcareous soil and the final regulation of the pH rise in acid soils are the result of C02 accumulation. Accordingly, the pH values at steady state of flooded alkaline, calcareous, and acid soils are highly sensitive to the partial pressure of CO2. Up to 2.6 t C02/ha is produced in the puddled layer during the first few weeks of flooding (IRRI 1964). AAer addition of organic substrates, the partial pressure of C02 in a flooded soil may reach a peak of almost 100 kPa (Neue and Bloom , 198 Pomamperuma ,1985). At steady state typical values range fiom 5 to 20 kPa (Kundu, 1987; Patra, 1987). Carbon dioxide concentrations greater than 15 kPa retard root development, leading to wilting and reduced nutrient uptake (Dent 1986). Carbon dioxide profoundly influences the chemical equilibria of almost all divalent cations ( ~ a 2 +M~Z+, , F$+, ~ n 2 +~, n 2 + ) in flooded soils as well as methane formation. . The magnitude and intensity of soil reduction is controlled by the amount of easily degradable organic matter, their rate of decomposition, and the amount and kinds of reducible nitrates, manganese and iron oxides, sulfates, and organic substrates. The most'important redox buffer 1 ~ e 2 +and,organic compounds when they are system in wetland soils are ~e+3-ox~h~droxides mostly present in large amounts. For a range of wetland that the C/N ratio of decomposable organic matter influen wetting whereas the active iron content defined the reduction active iron but high in degradable organic matter may attaintredox values of less than -200m within 2 weeks after submergence (Pomamperuma 1972). In soils high both in degradable
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organic matter and reducible iron, the redox may rapidly fall to -50mV and then slowly decline further for weeks before levelling ofF. Decomposition of organic matter Soil organic matter is defined as the sum total of all organic-containing substances in soils which consist of a mixture of plant and animal residues at various stages of decomposition, substances synthesized microbiologically andlor chemically from breakdown products, and of the bodies of live and dead microorganisms and small animals (Schnitzer, 1991) . Soil organic matter has a diverse and ever changing composition that reflects the interaction of accumulation and decomposition processes of current and past environmental conditions and management. Major and minor components vary between ecosystems and, even within a single site microbial mineralization and spontaneous chemical reactions constantly alter the nature of the organic matter (Tate, 1987). , Flooding a soil considerably alters micro- and macrofaunal communities and activities. Fermentation of organic matter by bacterial anaerobes predominates and actinomycetes, hngi and yeast are less active in the soil. Decomposition of organic compounds in the absence of free oxygen, as in wetland soils,-relies on the re-oxidation of intracellular electron acceptors produced by catabolic reactions in exced to that required by anabolic respiration. The two general mechanisms of re-oxidation are fermentation and anaerobic respiration. Oxidation of organic substrates in soil requires the supply of reduced substrates. The sequence of reduction is governed by thermodynamics. A redox couple that has the highest affinity for electrons is reduced first and the energy released from this reaction being greatest. Most reactions require soil micro-organisms to provide enzymes or catalysts to increase the rate of reaction (Rowell, 1981). Sposito (1981) considered microorganisms as catalysts which affect the rate of reaction but not the energy released. Fermentation alone does not result in mineralization of carbon (except for some conversions like acetate to methane and carbon dioxide) because it does not involve externally supplied electron acceptors but instead uses organic acceptors intracellularly generated . Thus, one or more products in fermentation are partially oxidized compounds (Ehrlich 1993). Anaerobic fermentation, however, does play an important role in the decomposition of reduced carbon. It comprises the break down of complex substrates prior to oxidation, resulting in an array of substances, many of them transitory and not found in well-aerated soils. Pomamperuma (1984) listed various gases, hydrocarbons, alcohols, carbonyls, volatile fatty acids, nonvolatile fatty acids, phenolic acids, and volatile S compounds. Short-term H2 evolution immediately follows the disappearance of 0 2 in the first days after flooding. Thereafter C02 production ipcreases, and finally, with decreasing CO2, CKq formation increases (Takai, 1984; Neue and Scharpenseel, 1984). With rising temperature to 350C, decomposition rates increase. At high temperature, the formation of C02 and CHq occurs earlier and is stronger, while that of organic acids is also earlier but srnaller in amount. The period of occurrence and the amount of volatile acids and gaseous products depend largely on temperature and reducing conditions.
Waterlogging can greatly retard organic matter decomposition, leading to accumulation of organic matter as it is evident in peat soils. In the low oxygen environment of flooded muck soils, Tate (1979) found that the rate of catabolism of several carbon substrates markedly decreased compared to rates in the same soil in an aerobic environment. The rate of catabolism for amino acids, glucose, and acetate, however, was less sensitive to flooding than aromatic compounds such as salicylate. But decomposition of organic matter in tropical wetland soils may proceed as fast as under aerated dryland condition irrespective of water regimes (Neue and Scharpenseel, 1987, Neue 1991) Rice straw ( 1 4 labelled) ~ decomposed at similar rates in aerobic and anaerobic (continuously flooded) fertile rice fields (Neue and Scharpenseel, 1987) but its decomposition was retarded in a low fertility wetland soil (Neue 1991). The following conditions seem to favor rapid degradation and mineralization of organic matter in flooded soils: 0 0 0 0 0 0
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shallow floodwater; soil temperature of 30-350C; neutral soil pH; low soil bulk density and wide soil-water ratio; intensive puddling each cropping season; high and balanced nutrient supply; no long-lasting accumulation of organic acids; permanent supply of energy-rich photosynthetic aquatic and benthic biomass; bioturbation andlor puddling of topsoil ' high diversity of micro- and macroorganisms that provide successive fermentation
diurnal oversaturation of the floodwater with 02 due to photosynthetic aquatic biomass enhancing.
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limited in their nutritional and metabolic activities (Lynch and Hobbie, 1988). Thus anaerobic species are generally more dependent upon the activities of other organisms to supply nutrients and establish the required physicochemical conditions. The interaction of organisms was demonstrated by Lovely and Phillips (1989) who showed that in an ~ e 3 +reducing environment, the decomposition of glucose involved fermentation to form fatty acids which were then oxidized to CO2 by a consortium of fermentative, fatty-acid-oxidizing and F4e3+ reducing bacteria. Such consortia utilize ultrarnicroenvironments which occur on a scale greater .than the microenvironments associated with each individual organism (Dommergues, 1980). These ultrarnicroenvironments may be induced by organic or inorganic surfaces or, as in the case of biofilms, by other living organisms. Of particular importance under anaerobic cotiditions is the provision of sinks to dispose excesses of reducing equivalents. In hydrogen-transfer'communities one organism acts as an acceptor for excess electrons and hydrogen generated by another organism during ethanol fermentation and obtains energy from the oxidation of hydrogen to CHq, using C02 as its electron acceptor. The energetically unfavorable fenhentation of ethanol to acetate can then continue because inhibiting levels of hydrogen are prevented. Data from Benner et al. (1984) and Colberg and Young (1985a) indicate that anaerobic microbial communities have even the capability to decompose lignin to C02 and CHq . Anaerobic lignin degradation should be very slow and be delayed because more easily degradable substrates are commonly available. Humification Soil organic matter is divided into humic and non-humic substances. Non-humic substances still display recognizable physical and chemical characteristics of its origin, are easily degraded by soil microorganisms, and have short life-spans. According to Stevenson (1986) unhumified substances include, carbohydrates, fats, waxes, proteins, fats, and all the biochemical compounds synthesized by soil microorganisms. , Humification involves a series df very complicated microbiological and 6erhaps some pure chemical processes, which are reviewed elsewhere (Aiken et al 1985, Stevenson 1982, Paul and Clark 1989). Aromatic compounds, e.g. polyphenols and polyquinones are believed to provide the skeleton of soil humus (Kononova 1966), while intermediate products of organic matter degradation including peptides, amino acids and ammonium from protein degradation comprise the main components of soil humus. The relative importance of lignins and microorganisms as source of polyphenols for humus synthesis is unknown, and may depend upon environmental conditions in the soil. Polyphenols'derived from plants or synthesized by microorganisms are enzymatically converted to quinones which undergo self-condensation or combine with amino compounds ,to form N-containing polymers. The process is condensation rather than polymerization because the reactants involved are related but not identical compounds. ,
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Humid substahces consist of a 'series 'of highly acidic, yellow to black in color, hydrophilic, partly aromaticYihigh molecular-weight polyelectrolytes and have properties significantly different from the biopolymers'of living organisms. By convention, they are grouped into humic acid, fblvic acid, and humins by solubility in alkaline and acid solutions. The various humic fractions represent a system of polymers, that vary systematically in elemental content, acidity, degree of
polymerization, and molecular weight. Humus of soils that are flooded or alternately flooded and drained differ from that of dryland soil (Kuwatsuka et al 1978, Tsutsuki and Kuwatsuka 1978, Tsutsuki and Kumada 1980). The degree of hurniiication, unsaturation, and the content of carboxyl and phenolic groups is lower, while the content of H, N and alcoholic and methoxyl groups is higher. Humification indices in wetland rice fields given as the ratios of nonhumified : humified materials (Sequi et al., 1986) are high in topsoils (0-10 cm) and decrease with depth, Electrophoresis of the humified materials displays bands only in the low pH range, revealing mainly low molecular weight, highly o x i d i i substances in the range of fulvic acids. Net Primary Production Soil organic matter will attain a steady state at any site when detritus fiom primary production and allochthonous inputs balance the loss of organic matter throughout the soil profile. Losses may be due to decomposition, run off, leaching and erosion. Man has changd that balance in vast parts of the world, mostly by enhancing the losses: The net primary production at a given natural dryland site determines the organic matter input for that soil, The net primary production of respective wetland sites is usually greater. Additionally, wetlands receive additional inputs due to sediments from the whole watershed . Floodplains, on the other hand, also lose large amounts of debris into rivers and ocean (Cuffney ,1988). The net primary production of plant communities is highly affected by temperature, light, water, and nutrients. In general, water is not a limiting factor in wetlands but excess water (floods and deep water) and droughts may periodically limit net primary production of wetlands. Nutrient supply controls mainly the NPP in most tropical wetlands (Brinson et al., 1981). Nitrogen is the most limiting nutrient for plant growth in wettands, follywed by phosp~orus,and potassium. Zinc and sulfbr deficiencies are widespread on continuously waterloggqd soils. Iron and copper deficiency, hydrogen sulfide formation, and excess of organic acids may also limit plant growth on peat soils. Iron toxicity is common in wetland soils high in active iron but low in other nutrients. In coastal wetlands, salinity adversely affects plant growth. . ,
NPP in the floodwater ofwetlands depends on P concentrations as in frsshwater lakes while nitrogen is seldom a limiting factor. When the floodwater is shallow, much of the phosphorus is supplied by the soil. Larger grazing and soil organisms enhance the nutrient exchange between the soil and the floodwater. When nitrogen becomes limited, algae populations shift to N-iixing
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