Emissions of methane and carbon dioxide during anaerobic decomposition of aquatic macrophytes from a tropical lagoon (São Paulo, Brazil)

Emissões de metano e dióxido de carbono da decomposição de macrófitas aquáticas de uma lagoa tropical (São Paulo, Brasil)

BIOLOGICAL LIMNOLOGY

Emissions of methane and carbon dioxide during anaerobic decomposition of aquatic macrophytes from a tropical lagoon (São Paulo, Brazil)

Emissões de metano e dióxido de carbono da decomposição de macrófitas aquáticas de uma lagoa tropical (São Paulo, Brasil)

Irineu Bianchini Jr.^I,II; Marcela Bianchessi da Cunha-Santino^I; Francisco Romeiro^II; Alexandre Luccas Bitar^II

^ILaboratório de Bioensaios e Modelagem Matemática, Departamento de Hidrobiologia, Universidade Federal de São Carlos - UFSCar, Rod. Washington Luis, Km 235, CP 676, CEP 13565-905, São Carlos, SP, Brazil e-mail: [e-mail], [e-mail] ^IIPrograma de Pós-graduação em Ecologia e Recursos Naturais - PPG-ERN, Universidade Federal de São Carlos - UFSCar, Rod. Washington Luis, Km 235, CP 676, CEP 13565-905, São Carlos, SP, Brazil e-mail: [e-mail]

ABSTRACT

AIM: Massive accumulations of aquatic sedimentary plant are the main source of CH₄ and CO₂ emissions in floodplain lakes. To examine this connection, this study measured CO₂ and CH₄ formation during anaerobic decomposition of aquatic macrophytes from a floodplain lake;

METHODS: Methane formation was determined to the intrinsic characteristics of the debris, and the experimental (physical and chemical) conditions. Production of CH₄ and CO₂ were measured during anaerobic degradation of seven aquatic macrophytes: Cabomba furcata, Cyperus giganteus, Egeria najas, Eichhornia azurea, Ludwigia inclinata, Oxycaryum cubense, and Utricularia breviscapa, all of which inhabit the littoral zone of the lagoon studied;

RESULTS: Overall, methanogenesis was more sensitive to temperature variation than gross anaerobic mineralization. Although the metabolic routes that generate CO₂ were always predominant, as a competing process methanogenesis was favored by increasing temperature to the detriment of CO₂ formation. Although several factors (such as pH, redox potential, salinity and nutrients availability) influenced yields of the final degradation products, temperature and detritus chemical composition were, in a first approach, the key factors in CH₄ formation. In the oxbow lakes of the Mogi-Guaçu River Floodplain, especially Óleo Lagoon, on average, 10% of the total carbon can be regarded as the yield of CH₄ formation derived from aquatic macrophyte decay, while the remaining carbon (90%) became CO₂.

Keywords: methane, anaerobic decomposition, aquatic macrophytes, wetland, floodplain lakes, Mogi-Guaçu River, Óleo Lagoon.

RESUMO

OBJETIVO: Acúmulos intensos de plantas nos sedimentos são importantes fontes de emissões de CH₄ e CO₂ em lagoas de várzea de inundação. Nesse estudo foram determinadas as formações de CH₄ e CO₂ da decomposição anaeróbia de macrófitas aquáticas de uma lagoa marginal;

MÉTODOS: A formação do metano foi determinada com base nas características intrínsecas dos detritos e das condições experimentais. As produções de CH₄ e CO₂ foram determinadas durante a degradação de sete espécies de macrófitas aquáticas: Cabomba furcata, Cyperus giganteus, Egeria najas, Eichhornia azurea, Ludwigia inclinata, Oxycaryum cubense, and Utricularia breviscapa, todas provenientes da zona litorânea da lagoa marginal selecionada;

RESULTADOS: De modo geral, a mentanogênese foi mais sensível à variação da temperatura que os demais processos de mineralização. Embora as rotas metabólicas que geraram o CO₂ sempre predominaram, a formação do metano foi favorecida com o incremento da temperatura em detrimento da geração de CO₂. Enquanto vários fatores (e.g. pH, potencial redox, salinidade, disponibilidade de nutrientes) influenciaram os rendimentos dos produtos finais da degradação, a temperatura e a composição química dos detritos foram, de modo geral, os fatores mais importantes para a formação do CH₄. Nas lagoas marginais da várzea de inundação do rio Mogi-Guaçu e em especial na lagoa do Óleo, em média, 10% do carbono dos detritos de macrófitas devem ser convertidos em CH₄ enquanto os demais (90%) em CO₂.

Palavras-chave: metano, decomposição aneróbia, macrófitas aquáticas, pântano, lagos de várzea, rio Mogi-Guaçu, lagoa do Óleo.

1. Introduction

Floodplain wetlands are among the most productive natural environments and are often characterized as having large inputs of detritus (Merritt andLawson, 1992; Neiff et al., 2006). These systems are driven by hydrologic pulses, produced by oscillations in river water level and lateral overflow that determine floodplain conditions (Powell et al., 2008). Thus, floods are a key factor controlling the biota and biogeochemical cycles in floodplain systems (Junk et al., 1989; Neiff, 1990a, b). Some flooding areas contain mainly shallow lakes, environments favorable for the growth of aquatic macrophyte communities (Scheffer, 2004). Furthermore, aquatic macrophytes support the food webs, provide shelter for small animals, change the nutrient dynamics of the system, and hamper sediment resuspension (Dorn et al., 2001; Thomaz et al., 2006).

Typically, the aquatic macrophytes tissues and phytoplankton cells are the major sources of autochthonous detritus within wetlands. The cytoplasm and the exudates of these plants comprise the main source of labile organic carbon (Peret and Bianchini Jr., 2004; Hanamachi et al., 2008). The supporting tissues of macrophytes are a significant source of refractory carbon (i.e. particulate organic matter). Aquatic plant detritus accumulates heavily over sediments and may be the main source of CH₄ and CO₂ emissions in floodplain lakes. Tropical systems may account for 60% of global atmospheric CH₄ emissions (Wang et al., 1996). Pantanal floodplain in Brazil, a tropical wetland, is estimated to contribute with 3.3% of global CH₄ emission (Marani and Alvalá, 2007). Methane production is regulated mainly by O₂ concentration, pH, temperature, salinity, organic substrates, and nutrient availability. The amount of CH₄ emitted from wetlands is further influenced by a large number of factors, including plant physiology, community composition, and hydrology. In addition to their direct effects on methanogen physiology, these factors influence the process indirectly by regulating the flow of methanogenic substrates from fermenting and syntrophic microorganisms. Methanogenesis can be limited by any single link in the chain of reactions that begins with detrital inputs (Megonigal et al., 2004).

Considering the high production of detritus from aquatic macrophyte in tropical wetlands (Bianchini Jr. and Rocha, 2006; Batzer et al., 2007) and the importance of environmental variables over CH₄ production, we conducted a study to understand the mechanisms that control CH₄ formation; by evaluating CO₂ and CH₄ production, during anaerobic decomposition of seven species of aquatic macrophytes from an oxbow lake located in a tropical floodplain area. We hypothesized that CH₄ formation is controlled by the chemical composition of organic resource, i.e. species of macrophyte and its structures (e.g. roots, rhizomes and leaves and labile and refractory compounds) and the physical (i.e. temperature) and chemical (i.e. interactions between particulate and dissolved organic matter) characteristics of the environment (i.e. extrinsic factors).

2. Material and Methods

2.1. Site description

Water and aquatic macrophyte samples were collected from the Óleo Lagoon (21° 36' S and 47° 49' W), which is located in the municipality of Luiz Antônio (São Paulo State, Brazil). The lagoon, part of a group of floodplain lakes, is located inside the Jataí Ecological Station. The regional climate has two well-defined seasons (Ballester and Santos, 2001): rainy (November-April) and dry (May-October), with average temperatures of 26.8 ± 1.7 °C and 22.4 ± 1.3 °C, respectively (Cunha-Santino, 2003); the regional climate is AW according to Köppen climate classification (i.e. rainy summer and dry winter).

The lagoon system, a part of the Mogi-Guaçu river floodplain, is formed by shallow oxbow lakes with heavy aquatic macrophyte density (Nogueira and Esteves, 1990); flooding connects some of these lakes to the river (Santos and Mozeto, 1992). Anoxic conditions usually occur in the rainy season (Ballester and Santos, 2001). Anoxic conditions are established at 2.5 cm depth in the Óleo Lagoon sediments (Cunha-Santino, 2003). Temperatures at the sediment level of the lagoon (ca. 5 m) range between 15.8 and 25.6 °C with an average of 21.7 ± 2.8 °C (Petracco, 2006). The littoral zone is highly colonized by aquatic macrophytes. The following species were registered Cabomba furcata, Ceratophyllum submersum, Egeria najas, Eichhornia azurea, Ricciocarpus natans, Cyperus giganteus, Ludwigia inclinata, Najas conferta, Salvinia auriculata, Oxycaryum cubense, Utricularia breviscapa and Utricularia foliosa (Cunha-Santino, 2003; Petracco, 2006).

2.2. Experiments

The aquatic macrophytes (Cabomba furcata, Cyperus giganteus, Egeria najas, Eichhornia azurea, Ludwigia inclinata, Oxycaryum cubense, and Utricularia breviscapa) were harvested from various points of the littoral zone of Óleo Lagoon. The plants were washed within lagoon water to remove periphyton, sediment particles, and coarse material (Ogburn et al., 1987). In the laboratory, the plants were washed with tap water, oven-dried (40 °C), and ground. Prior to the assays with C. furcata and C. giganteus, leachate was extracted by adding 10 g DW (dry weight) of ground plant (previously sterilized by autoclaving for 15 minutes, at 1 atm and 121 °C; Ward and Johnson, 1996) to a flask containing 1 L of sterilized deionized water. After 24 hours of cold aqueous extraction (4 °C) (MΦller et al., 1999), the leachate was fractionated from particulate organic matter (POM) by centrifugation (1048 g, 1 hour) and filtered through 0.45 µm pore size cellulose ester (Millipore). The remaining POM (i.e. fibers) was considered refractory tissue. Concentrations of dissolved inorganic carbon (DIC) and dissolved organic carbon (DOC) in the leachate were determined by combustion (TOC Analyzer Shimadzu, Model 5000A). Prior to the assays with O. cubense, the plants were also fractionated into roots, rhizomes, and leaves. Cell wall fractions (CWF ≈ lignin, cellulose and hemicellulose; n = 3 for each species) of the plant tissues were determined using neutral detergent and the reflux method (Van Soest and Wine, 1967). Thus, POM was constituted of the fibrous material remainder from the aqueous extraction and or from the leaching during decomposition, and CWF basically refers to the cell wall components, extracted by chemical method.

Water samples for the experiments were collected with a Van Dorn underwater sampler at three lagoon depths (surface, 1.5, and 3.0 m). To obtain an integrated sample of lake water, equivalent volumes from different depths were then mixed for sampling in the laboratory. These were filtered through a cellulose ester membrane (Millipore; pore size: 0.45 µm). The DIC and DOC concentrations were determined by combustion (TOC analyzer). To quantify CH₄ and CO₂ emissions, for each condition, selected incubations were prepared in 1.12 L glass flasks. Three contained plant fragments (7.0 g DW) and lagoon water (1.0 L) as source of indigenous microorganisms; the other two had only lagoon water (control). After prepared, the incubations were bubbled with nitrogen (to reach anaerobic condition) and the flasks were kept in the dark under controlled temperature (ca. 20 °C). In the incubations (with fragments of E. najas, E. azurea, L. inclinata, and U. breviscapa) subjected to temperature variation (from 15 to 30 °C), CH₄ and mineralized carbon (MC) yields were used to calculate the Q₁₀ temperature coefficient (the rate of change of a biological or chemical reaction as a result of increasing the temperature by 10 °C), according to Winkler et al. (1996). The temperature range chosen for the experiments comprised the seasonal variation registered to the Óleo Lagoon (Petracco, 2006). Periodically, during a span of 140 to 200 d, CO₂ and CH₄ production was estimated by sampling the gases enclosed in the incubation headspaces (120 mL). Samples were taken with a syringe (1.0 mL) by piercing the silicone septa that sealed the flask. The gas samples were analyzed using gas chromatography (CG Construmaq, Model 370; with thermal conductivity detector and Porapak N column; carrier gas: hidrogen). Peak areas were quantified from CO₂ and CH₄ standard curves. After being measured, gases were expurgated from incubations by nitrogen bubbling (during 5 minutes) to keep the determinations on a daily rates basis. Measuring procedures continued until CH₄ daily rates became null.

At the end of the experiments the residues were fractionated by filtration through nylon mesh (0.4 mm). The filtrate was then centrifuged (1048 g, 1 hour) and the supernatant were filtered through cellulose-ester membranes (0.22 µm Millipore, previously washed with 250 mL distilled water). The particulate material was dried (at 50 °C for 48 hour) and then weighed. The carbon contents of particulate detritus were quantified by a CHN analyzer (Carlo Erba model EA 1110). The DOC and DIC concentrations were measured with a TOC analyzer, as describes previous. From the CO₂ and CH₄ measures and initial and final carbon contents (DOC, DIC, POC) the entire carbon budget and the yields of CO₂ and CH₄ were calculated. The temperature variation and C-budgets were used to compare the methanogenesis from the organic resources (i.e. entire macrophytes, leachate, roots, leaves and rhizomes of the Scirpus cubenses and POM and leachate of the Cabomba furcata and Cyperus giganteus) decompositions. Linear correlations were also used to compare the results (CO₂ and CH₄ yields) with chemical composition of resources.

3. Results

The cell wall fraction (CWF) varied from 27.5% (C. furcata) to 80.7% (O. cubense), which on average represented 55.6% of the cell wall tissues of the selected aquatic plants (Table 1). Macrophyte fragments showed the predominance of particulate organic matter over the soluble fractions (i.e. leachate: mean 30.8%, SD 5.3%). On average, POM represented 69.2% of plant tissues; dissolution potential (i.e. hydrosoluble cytoplasm compounds) corresponded to 30.8%. Leachate varied from 22.0 (C. furcata) to 35.9% (O. cubense). Inorganic compounds prevailed in the soluble fractions (mean: 21.6%, SD: 8.2%); C content from leachate varied from 4.6% (C. giganteus) to 17.0% (U. breviscapa; Table 1).

Overall, tree stages were identified for methanogenesis: in the first, CH₄ was not produced (lag stage); in the second, CH₄ began to be produced, reaching the highest rates; the third stage was characterized by a decrease in the rates, until reaching zero. The changes of daily rates of the CO₂ and CH₄ formation (from O. cubense decomposition at 20 °C) were exemplified in the Figure 1. On a carbon basis, decay of E. najas at 27 °C produced highest methane amounts (31.3%) followed by its decomposition at 22.4 °C and the decay of O. cubense (27.1%) at 20 °C. The pathway for CO₂ formation in all experiments predominated over methanogenesis; in some cases, methane production was not recorded (decompositions of POM and leachate from C. giganteus, and incubations maintained under low temperatures). On average, considering similar temperatures (ca. 20 °C), 10.1% of the carbon was converted into CH₄ by anaerobic decay of aquatic macrophytes (Table 2).

Considering the 4 assays (incubations with E. najas, E. azurea, L. inclinata, and U. breviscapa) methane generation and anaerobic mineralization yields depended on the temperature. Among the selected macrophytes, methane formation from U. breviscapa degradation (Q₁₀: 6.49) was more susceptible to temperature changes, a result followed by decay of L. inclinata (Q₁₀: 4.42), E. najas (Q₁₀: 2.29), and E. azurea (Q₁₀: 1.12). On the other hand, Q₁₀ values of anaerobic decay of macrophytes were very similar (E. najas: 1.36; E. azurea: 1.22; L. inclinata: 1.13; U. breviscapa: 1.54). Considering Q₁₀ values, methane formation (mean: 3.58) was ca. 3-fold more affected by temperature than was anaerobic mineralization (mean: 1.31). The CH₄-Q₁₀ values were inversely proportional to CWF (r² = 0.99). In all experiments, the time required to initiate methane formation decreased with temperature. The yields of CH₄ formation at the same temperature (ca. 20 °C) comprise the relation with the chemical characteristics of plant tissues (CWF, POM, leachate, C-leachate, IN-leachate); Table 2.

After 140 days, CH₄ formation and mineralization yields were higher in incubation with non-fractionated detritus of O. cubense (27.1 and 19.0%, respectively), followed by that of decayed roots (C-CH₄: 21.7% and CM: 17.0%); Table 2.

4. Discussion

Macrophyte primary production affects the dynamics and metabolism of several aquatic ecosystems, especially the shallower ones (Wetzel, 2001). Detritus generated in such areas usually support the detritus food chains of littoral zones and might be exported to benthic and pelagic regions. Depending on the environment, most debris produced in littoral regions is composed of aquatic macrophyte detritus, which contributes to sediment diagenesis and biogenic gas emissions. The present study showed methane quantity varying with the type of detritus (i.e. macrophyte species) and its structure (i.e. fibers, leachate, roots, rhizomes, and leaves). In spite of the similarity among the percentages of macrophyte derived POM, macrophyte leachate, C-leachate, and IN-leachate, methane formation varied widely in incubation (at ca. 20 °C) yields for E. azurea (2.4%) and O. cubense (27.1%). In contrast, O. cubense presented a CWF 57% higher than the average of other plants (CWF = 51.4%), which we attribute to CH₄ formation to decomposition of CWF. A nutrient balance study on these species in a lagoon of this floodplain showed that O. cubense accumulated 1.4 times more nutrients than E. azurea in the dry period and 6.9-fold in the rainy season (Nogueira et al., 2000). Thus, aquatic macrophytes can be the main nutrient suppliers of these shallow aquatic environments. Moreover, the nutritional composition influences decomposition pathways, in this case favoring methane formation. As for anaerobic decomposition of morphological structures (i.e. roots, rhizomes, and leaves) of O. cubense, heterotrophic organisms showed heavy root consumption (MC = 47.0%) whereas rhizomes were the most refractory detritus (MC = 25.8%). In addition, debris with higher ash content (a surrogate of nutrients) was found to lead to higher CH₄ production (Romeiro and Bianchini Jr., 2006). Besides the nutrient content of the detritus as a supply source in methane formation, anaerobic degradation of U. breviscapa showed strong evidence that the CH₄ formation were concomitant with cellulase activity (Cunha-Santino, 2003) and, therefore, dependent on anaerobic degradation of cellulose (Leschine, 1995).

Beyond the specific requirements of methanogenic archaea (e.g. temperature, pH, nutrient and labile carbon availability), in agreement with observed in the present study, enable us to assume that in the Óleo Lagoon methane formation during decomposition of aquatic macrophytes depends overwhelmingly on the input of aquatic macrophyte detritus, i.e. the temporal intensity variation, and on the type and chemical composition of the detritus. In this context, in the Óleo Lagoon, asynchronies were observed between the predominance of the detritus input (autumn - winter) and of the higher values of CH₄ emission and denitrification (spring - summer) (Ballester, 1994; Gianotti and Santos, 2000). A mass balance study of aquatic macrophyte detritus for another lake of this floodplain also registered asynchronies (ca. 80 days) between senescence and accumulation of particulate debris in the sediments (Bianchini Jr. and Rocha, 2006). In the case of U. breviscapa of Óleo Lagoon, biomass decreases during the cold months (mainly in June-July). Therefore, it can be assumed that during this period senescence of this macrophye contributed strongly to the detritus input (Cunha-Santino, 2003). On the other hand, lesser quantities of Utricularia sp. (i.e. input of detritus) has been reported in Infernão Lagoon (also situated in Mogi-Guaçu River Floodplain) in February (Carlos, 1991), which was attributed to several factors: reduction of sub-aquatic radiation, turbidity increase, high rainfall index, and flooding.

Considering the yields, methane formation appears not to depend on aquatic macrophyte type (i.e. submersed or emergent). Yields of CH₄ formation at around 20 °C during degradation were found for both submersed (C. furcata: 11.5%; E. najas: 23.3%; and U. breviscapa: 0.4%) and emergent species (C. giganteus: 3.6%; E. azurea: 2.4%; L. inclinata: 2.3%; and O. cubense: 27.1%). The results suggest that, besides the chemical composition of the detritus (i.e. nutrients content, labile and refractory organic fractions), the incubation temperature also interferes in CH₄ formation. A similar experiment showed that CH₄ formation was inhibited by a pH decrease due to intense CO₂ formation during the beginning of C. piauhyensis (i.e. Cabomba furcata) degradation. In this same study, since there were few labile materials, CH₄ formation was registered only during O. cubense degradation (Cunha-Santino et al., 2006).

Exclusive degradation of the leachate hindered CH₄ formation; for C. giganteus leachate (which represents 27.2% of the detritus mass) methanogenesis may have been blocked by insufficient organic carbon availability (4.6%) in comparison to that of inorganic compounds (22.6%). In support of this argument, we supposed that CH₄ formation during leachate degradation of C. furcata occurred due to higher organic carbon availability (14.3%) in its elemental composition. Comparing degradation yields of unfractionated macrophyte detritus with leachate and POM, leachate was assumed to be supplied with sufficient inorganic elements to maintain catabolic routes during unfractionated detritus decomposition.

As commonly verified, temperature was a key factor in CH₄ formation (Nozhevnikova et al., 1997) and also in anaerobic mineralization of the aquatic macrophytes (Cunha-Santino, 2003; Bitar et al., 2006). Comparing the results, methanogenesis was more sensitive to temperature changes than was gross anaerobic mineralization. The Q₁₀ values for CH₄ production are inside the range usually registered; a compilation of temperature-response studies using wetland soils report an average Q₁₀ of 4.1 for CH₄ production (Segers, 1998). Although the metabolic routes that culminate in CO₂ were always predominant; methanogenesis rather than CO₂ formation was favored by increasing temperature. This variable abbreviated the time required for methanogenesis to begin. Another factor that explain the necessary time for CH₄ production is the consumption of alternative electrons acceptor (i.e. denitrification, Fe(III)-reduction and sulfate reduction); in this case, such processes would also be abbreviated with the increase of the temperature (Megonigal et al., 2004). The inverse correlation between CWF and CH₄-Q₁₀ suggest that the cell wall content of detritus induced a differentiation of microorganisms or pathways involved in the formation of the methane. This way, the processes related with the degradation of refractory compounds were less sensitive to the temperature change.

In conclusion, several factors (e.g. temperature, detritus chemical composition) influence the process related to final carbon degradation products. In the case of the oxbow lakes of the Mogi-Guaçu floodplain, with reference to the Óleo Lagoon, this approach supposes that the mean value of methane formation (10% of carbon total) can be considered as the mean yield of CH₄ formation derived from aquatic macrophyte decay. The remaining carbon (90%) formed CO₂.

Acknowledgements

The authors thank Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (CAPES; Process: 33001014003P2), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq: Processes: 134457/2003-0 and 300959/2004-4) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for financing these assays (Processes: 98/12564-4, 98/15011-6 and00/09297-6). We thank Dr. Osvaldo N. Oliveira Jr. (IFSC-USP) and two anonymous reviewers, whose comments improved considerably our manuscript.

Received: 16 February 2010

Accepted: 20 August 2010

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Publication Dates

• Publication in this collection
  12 Apr 2011
• Date of issue
  June 2010

History

• Received
  16 Feb 2010
• Accepted
  20 Aug 2010