Anaerobic carbon oxidation in sediment of two Brazilian mangrove forests: the influence of tree roots and crab burrows
DOI:
https://doi.org/10.1590/Keywords:
Sulfate reduction, Iron reduction, Biogeochemistry, Mangrove roots, Crab burrowsAbstract
This study evaluated the effects of biogenic structures (tree roots and crab burrows) on sediment carbon (C), sulfur (S), and iron (Fe) biogeochemistry during the wet season in the Olaria mangrove forests near the city of Cananéia, São Paulo state, Brazil and the Nobrega mangrove forest approximately 2 km from the city. Anaerobic C oxidation pathways were assessed from sediment profiles and anaerobic incubations and related to the abundance of biogenic structures in the form of pneumatophores and crab burrows. Porewater depth profiles of dissolved inorganic carbon (DIC) and SO42- were less steep in the presence than absence of biogenic structures. While Fe(II) appeared unaffected by biogenic structures, Fe(III) levels were significantly higher in the upper 4 cm of the sediment in the presence than absence of vegetation and bioturbation. Surprisingly, the concentration of Fe(III) in this layer was 2-6 times higher in the Nobrega forest (6-13 µmol cm-3) than in the Olaria forest (1.5-6.5 µmol cm-3). Accordingly, depth integrated sulfate reduction (SR) tended to be highest at Olaria, while iron reduction (FeR) was highest at Nobrega. SR accounted for 54-83% of DIC production, with no diference between forested sites, while FeR accounted for 8-24% of DIC production, with a 2-3 times higher contribution in the Nobrega versus the Olaria forest. The results suggest that mangrove roots and crab burrows in mangrove sediments only promote FeR at the expense of SR in the Nobrega forest. It appears that anthropogenic discharge from Cananéia city may have overridden the impact of biogenic structures on sediment redox conditions at Olaria, thereby diminishing the role of FeR without strong stimulation of overall C oxidation rates.
References
AIDAR, E., SIGAUD-KUTNER, T. C. S., NISHIHARA, L., SCHINKE, K. P., BRAGA, M. C. C., FARAH, R. E. & KUTNER, M. B. B. 1997. Marine phytoplankton assays: effects of detergents. Marine Environmental Research, 43(1-2), 55-68.
ALLER, R. C. 1980. Quantifying solute distributions in the bioturbated zone of marine sediments by defining an average microenvironment. Geochimica et Cosmochimica Acta, 44(12), 1955-1965.
ALONGI, D. M. 2014. Carbon cycling and storage in mangrove forests. Annual Review of Marine Science, 6, 195-219.
ALONGI, D. M. 2020. Carbon cycling in the World’s mangrove ecosystems revisited: Significance of non-steady state diagenesis and subsurface linkages between the forest foor and the coastal ocean. Forests, 11(9), 977, DOI: https://doi.org/10.3390/f11090977
» https://doi.org/10.3390/f11090977
ALONGI, D. M., PFITZNER, J., TROTT, L. A., TIRENDI, F., DIXON, P. & KLUMPP, D. W. 2005. Rapid sediment accumulation and microbial mineralization in forests of the mangrove Kandelia candel in the Jiulongjiang Estuary, China. Estuarine, Coastal and Shelf Science, 63(4), 605-618.
ALONGI, D. M., SASEKUMAR, A., CHONG, V. C., PFITZNER, J., TROTT, L. A., TIRENDI, F., DIXON, P. & BRUNSKILL, G. J. 2004. Sediment accumulation and organic material fux in a managed mangrove ecosystem: estimates of land-ocean-atmosphere exchange in peninsular Malaysia. Marine Geology, 208(2-4), 383-402.
ALONGI, D. M., TIRENDI, F. & CLOUGH, B. F. 2000. Below-ground decomposition of organic matter in forests of the mangroves Rhizophora stylosa and Avicennia marina along the arid coast of Western Australia. Aquatic Botany, 68(2), 97-122.
ALONGI, D. M., TROTT, L. A., WATTAYAKORN, G. & CLOUGH, B. F. 2002. Below-ground nitrogen cycling in relation to net canopy production in mangrove forests of southern Thailand. Marine Biology, 140, 855-864.
ALONGI, D. M., WATTAYAKORN, G., PFITZNER, J., TIRENDI, F., ZAGORSKIS, I., BRUNSKILL, G. J., DAVIDSON, A. & CLOUGH, B. F. 2001. Organic carbon accumulation and metabolic pathways in sediments of mangrove forests in southern Thailand. Marine Geology, 179(1-2), 85-103.
ANDERSEN, F. Ø. & KRISTENSEN, E. 1988. Oxygen microgradients in the rhizosphere of the mangrove Avicennia marina. Marine Ecology Progress Series, 44, 201-204.
ARAÚJO, J. M. C., FERREIRA, T. O., SUAREZ-ABELENDA, M., NÓBREGA, G. N., ALBUQUERQUE, A. G. B. M., BEZERRA, A. C. & OTERO, X. L. 2016. The role of bioturbation by Ucides cordatus crab in the fractionation and bioavailability of trace metals in tropical semiarid mangroves. Marine Pollution Bulletin, 111(1-2), 194-202.
ASCHENBROICH, A., MICHAUD, E., GILBERT, F., FROMARD, F., ALT, A., LE GARREC, V., BIHANNIC, I., CONINCK, A. & THOUZEAU, G. 2017. Bioturbation functional roles associated with mangrove development in French Guiana, South America. Hydrobiologia, 794(1), 179-202.
BARCELLOS, R. L., BERBEL, G. B. B., BRAGA, E. S. & FURTADO, V. V. 2005. Distribuição e características do fósforo sedimentary no sistema estuarino lagunar de Cananéia-Iguape, Estado de São Paulo, Brasil. Geochimica Brasiliensis, 19, 22-36.
BERNARDINO, A. F., PAGLIOSA, P. R., CHRISTOFOLETTI, R. A., BARROS, F., NETTO, S. A., MUNIZ, P. & LANA, P. C. 2016. Benthic estuarine communities in Brazil: moving forward to long term studies to assess climate change impacts. Brazilian Journal of Oceanography, 64(spe 2), 81-96.
BRODERSEN, K. E., TREVATHAN-TACKETT, S. M., NIELSEN, D. A., CONNOLLY, R. M., LOVELOCK, C. E., ATWOOD, T. B. & MACREADIE, P. I. 2019. Oxygen consumption and sulfate reduction in vegetated coastal habitats: effects of physical disturbance. Frontiers in Marine Science, 6, 14, DOI: https://doi.org/10.3389/fmars.2019.00014
» https://doi.org/10.3389/fmars.2019.00014
CANFIELD, D. E., KRISTENSEN, E. & THAMDRUP, B. 2005. Aquatic geomicrobiology San Diego: Academic Press.
CHENG, H., LIU, Y., JIANG, Z. Y. & WANG, Y. S. 2020. Radial oxygen loss is correlated with nitrogen nutrition in mangroves. Tree Physiology, 44(11), 1548-1560.
CUNHA-LIGNON, M., MAHIQUES, M. M., SCHAEFFER-NOVELLI, Y., RODRIGUES, M., KLEIN, D. A., GOYA, S. C., MENGHINI, R. P., TOLENTINO, C. C., CINTRÓN-MOLERO, G. & DAHDOUH-GUEBAS, F. 2009. Analysis of mangrove forest succession, using sediment cores: a case study in the Cananéia-Iguape coastal system, Sao Paulo, Brazil. Brazilian Journal of Oceanography, 57(3), 161-174.
ESCH, M. E. S., SHULL, D. H., DEVOL, A. H. & MORAN, S. B. 2013. Regional patterns of bioturbation and iron and manganese reduction in the sediments of the southeastern Bering Sea. Deep-Sea Research II, 94, 80-94.
FERREIRA, T. O., OTERO, X. L., SOUZA JUNIOR, V. S., VIDAL-TORRADO, P., MACÍAS, F. & FIRME, L. P. 2010. Spatial patterns of soil attributes and components in a mangrove system in Southeast Brazil (São Paulo). Journal of Soils and Sediments, 10(6), 995-1006.
FERREIRA, T. O., OTERO, X. L., VIDAL-TORRADO, P. & MACÍAS, F. 2007. Effects of bioturbation by root and crab activity on iron and sulfur biogeochemistry in mangrove substrate. Geoderma, 142(1-2), 36-46.
FRIESS, D. A., ROGERS, K., LOVELOCK, C. E., KRAUSS, K. W., HAMILTON, S. E., LEE, S. Y., LUCAS, R., PRIMAVERA, J., RAJKARAN, A. & SHI, S. 2019. The state of the World’s mangrove forests: past, present, and future. Annual Review of Environment and Resources, 44, 89-115.
FURUKAWA, Y., BENTLEY, S. J. & LAVOIE, D. L. 2001. Bioirrigation modeling in experimental benthic mesocosms. Journal of Marine Research, 59(3), 417-452.
GIRI, C., OCHIENG, E., TIESZEN, L. L., ZHU, Z., SINGH, A., LOVELAND, T., MASEK, J. & DUKE, N. 2011. Status and distribution of mangrove forests of the world using earth observation satellite data. Global Ecology and Biogeography, 20(1), 154-159.
GRIBSHOLT, B., KOSTKA, J. E. & KRISTENSEN, E. 2003. Impact of fddler crabs and plant roots on sediment biogeochemistry in a Georgia salt marsh. Marine Ecology Progress Series, 259, 237-251.
HULTHE, G., HULTH, S. & HALL, P. O. J. 1998. Effect of oxygen on degradation rate of refractory and labile organic matter in continental margin sediments. Geochimica et Cosmochimica Acta, 62, 1319-1328.
JENSEN, M. M., THAMDRUP, B., RYSGAARD, S., HOLMER, M. & FOSSING, H. 2003. Rates and regulation of microbial iron reduction in sediments of the Baltic-North Sea transition. Biogeochemistry, 65, 295-317.
KHIRUL, M. A., CHO, D. & KWON, S. H. 2020. Behaviors of nitrogen, iron and sulfur compounds in contaminated marine sediment. Environmental Engineering Research, 25(3), 274-280.
KOSTKA, J. E., GRIBSHOLT, B., PETRIE, E., DALTON, D., SKELTON, H. & KRISTENSEN, E. 2002. The rates and pathways of carbon oxidation in bioturbated saltmarsh sediments. Limnology and Oceanography, 47(1), 230-240.
KRAAL, P., BURTON, E. D., ROSE, A. L., KOCAR, B. D., LOCKHART, R. S., GRICE, K., BUSH, R. T., TAN, E. & WEBB, S. M. 2015. Sedimentary iron-phosphorus cycling under contrasting redox conditions in a eutrophic estuary. Chemical Geology, 392, 19-31.
KRISTENSEN, E. & ALONGI, D. M. 2006. Control by fddler crabs (Uca vocans) and plant roots (Avicennia marina) on carbon, iron and sulfur biogeochemistry in mangrove sediment. Limnology and Oceanography, 51(4), 1557-1571.
KRISTENSEN, E. & ANDERSEN, F. Ø. 1987. Determination of organic carbon in marine sediments: a comparison of two CHN-analyzer methods. Journal of Experimental Marine Biology and Ecology, 109(1), 15-23.
KRISTENSEN, E., ANDERSEN, F. Ø., HOLMBOE, N., HOLMER, M. & THONGTHAM, N. 2000. Carbon and nitrogen mineralization in sediment of the Bangrong mangrove area, Phuket, Thailand. Aquatic Microbial Ecology, 22(2), 199-213.
KRISTENSEN, E., BOUILLON, S., DITTMAR, T. & MARCHAND, C. 2008. Organic carbon dynamics in mangrove ecosystems. Aquatic Botany, 89(2), 201-219.
KRISTENSEN, E., CONNOLLY, R. M., OTERO, X. L., MARCHAND, C., FERREIRA, T. O. & RIVERA-MONROY, V. H. 2017. Biogeochemical cycles: Global approaches and perspectives. In: RIVERA-MONROY, V. H., LEE, S. Y., KRISTENSEN, E. & TWILLEY, R. R. (eds.). Mangrove ecosystems: a global biogeographic perspective. Structure, function and ecosystem services Cham: Springer Nature, pp. 163-209.
KRISTENSEN, E. & HOLMER, M. 2001. Decomposition of plant materials in marine sediment exposed to different electron acceptors (O2, NO3-, and SO42-), with emphasis on substrate origin, degradation kinetics, and the role of bioturbation. Geochimica et Cosmochimica Acta, 65(3), 419-433.
KRISTENSEN, E., MANGION, P., TANG, M., FLINDT, M. R., HOLMER, M. & ULOMI, S. 2011. Microbial carbon oxidation rates and pathways in sediments of two Tanzanian mangrove forests. Biogeochemistry, 103(1-3), 143-158.
KRISTENSEN, E., PENHA-LOPES, G., DELEFOSSE, M., VALDEMARSEN, T., QUINTANA, C. O. & BANTA, G. 2012. What is bioturbation? Need for a precise definition for fauna in aquatic sciences. Marine Ecology Progress Series, 446, 285-302.
KRISTENSEN, E., RØY, H., DEBRABANT, K. & VALDEMARSEN, T. 2018. Carbon oxidation and bioirrigation in sediments along a Skagerrak-Kattegat-Belt Sea depth transect. Marine Ecology Progress Series, 604, 33-50.
KRISTENSEN E, VALDEMARSEN T, MORAES PC, GÜTH AZ, SUMIDA PYG, QUINTANA CO (2022) Pneumato-phores and crab burrows increase CO2 and CH4 emission from sediments in two Brazilian fringe mangrove forests. Marine Ecology Progress Series, 698, 29-39. https://doi.org/10.3354/meps14153
» https://doi.org/10.3354/meps14153
LOVLEY, D. R. & PHILLIPS, E. J. P. 1987. Rapid assay for microbially reducible ferric iron in aquatic sediments. Applied Environmental Microbiology, 53(7), 1536-1540.
MICHAELS, R. E. & ZIEMAN, J. C. 2013. Fiddler crab (Uca spp.) burrows have little effect on surrounding sediment oxygen concentrations. Journal of Experimental Marine Biology and Ecology, 448, 104-113.
NIELSEN, O. I., KRISTENSEN, E. & HOLMER, M. 2003. Impact of Arenicola marina (Polychaeta) on sediment sulfur dynamics. Aquatic Microbial Ecology, 33, 95-105.
PAN, F., LIU, H., GUO, Z., LI, Z., WANG, B., CAI, Y. & GAO, A. 2019. Effects of tide and season changes on the iron-sulfur-phosphorus biogeochemistry in sediment porewater of a mangrove coast. Journal of Hydrology, 568, 686-702.
PENHA-LOPES, G., KRISTENSEN, E., FLINDT, M., MANGION, P., BOUILLON, S. & PAULA, J. 2010. The role of biogenic structures on the biogeochemical functioning of mangrove constructed wetlands sediments – a mesocosm approach. Marine Pollution Bulletin, 60(4), 560-572.
PURNOBASUKI, H. & SUZUKI, M. 2005. Aerenchyma tissue development and gas-pathway structure in root of Avicennia marina (Forsk.) Vierh. Journal of Plant Research, 118(4), 285-294.
QUADROS, A. F., NORDHAUS, I., REUTER, H. & ZIMMER, M. 2019. Modelling of mangrove annual leaf litterfall with emphasis on the role of vegetation structure. Estuarine, Coastal and Shelf Science, 218, 292-299.
QUINTANA, C. O., SHIMABUKURO, M., PEREIRA C. O., ALVES, B. G., MORAES, P. C., VALDEMARSEN, T., KRISTENSEN, E. & SUMIDA, P. Y. G. 2015. Carbon mineralization pathways and bioturbation in coastal Brazilian sediments. Scientific Reports, 5, 16122.
ROBERTSON, D., WELSH, D. T. & TEASDALE, P. R. 2009. Investigating biogenic heterogeneity in coastal sediments with two-dimensional measurements of iron(II) and sulfde. Environmental Chemistry, 6(1), 60-69.
ROVAI, A. S., COELHO JUNIOR, C., ALMEIDA, R., CUNHA-LIGNON, M., MENGHINI, R. P., TWILLEY, R. R., CINTRÓN-MOLERO, G. & SCHAEFFER-NOVELLI, Y. 2021. Ecosystem-level carbon stocks and sequestration rates in mangroves in the Cananéia-Iguape lagoon estuarine system, southeastern Brazil. Forest Ecology and Management, 479, 118553, DOI: https://doi.org/10.1016/j.foreco.2020.118553
» https://doi.org/10.1016/j.foreco.2020.118553
SCHAEFFER-NOVELLI, Y., CINTRON-MOLERO, G., ADAIME, R. R. & CAMARGO, T. M. 1990. Variability of mangrove ecosystems along the Brazilian coast. Estuaries, 13, 204-218.
SCHAEFFER-NOVELLI, Y., SORIANO-SIERRA, E. J., VALE, C. C., BERNINI, E., ROVAI, A. S., PINHEIRO, M. A. A., SCHMIDT, A. J., ALMEIDA, R., JÚNIOR, C. C., MENGHINI, R. P. R., MARTINEZ, D. I., ABUCHAHLA, G. M. O., CUNHA-LIGNON, M., CHARLIER-SARUBO, S., SHIRAZAWA-FREITAS, J. & CINTRÓN-MOLERO, G. 2016. Climate changes in mangrove forests and salt marshes. Brazilian Journal of Oceanography, 64(spe 2), 37-52.
SCHWAMBORN, R. & GIARRIZZO, T. 2015. Stable isotope discrimination by consumers in a tropical mangrove food web: How important are variations in C/N ratio? Estuaries and Coasts, 38, 813-825.
SPALDING, E. A., KAINUMA, M. & COLLINS, L. 2011. World Atlas of Mangroves Kuala Lumpur: ITTO.
STOOKEY, L. L. 1970. Ferrozine - a new spectrophotometric reagent for iron. Analytical Chemistry, 42(7), 779-781.
TALLING, J. F. 1973. The application of some electrochemical methods to the measurement of photosynthesis and respiration in fresh water. Freshwater Biology, 3(4), 335-362
VALDEMARSEN, T. & KRISTENSEN, E. 2010. Degradation of dissolved organic monomers and short-chain fatty acids in sandy marine sediment by fermentation and sulfate reduction. Geochimica et Cosmochimica Acta, 74(5), 1593-1605.
XIMENES, A., MAEDA, E. E., ARCOVERDE, G. F. B. & DAHDOUH-GUEBAS, F. 2016. Spatial assessment of the bioclimatic and environmental factors driving mangrove tree species’ distribution along the Brazilian coastline. Remote Sensing, 8(6), 451, DOI: https://doi.org/10.3390/rs8060451
