JACEN  Vol.5 No.2 , May 2016
Assessment of the Influence of Oil Palm and Rubber Plantations in Tropical Peat Swamp Soils Using Microbial Diversity and Activity Analysis
Abstract: In this study, tropical peat swamp soils from Giam Siak Kecil-Bukit Batu Biosphere Reserve (GSKBB) in Indonesia was evaluated to assess the impact of oil palm and rubber plantations on this unique organic soil through comparisons with soils from a natural forest using a polyphasic approach (chemical and molecular microbial assays). Changes in the ammonium, nitrate and phosphate concentration were observed in soils converted to agricultural use. Soil enzyme activities in plantation soils showed reduced β-glucosidase, cellobiohydrolase and acid phosphatase activities (50% - 55% decrease). PCR-DGGE based analysis showed that the soil bacterial community from agricultural soils exhibited the lowest similarity amongst the different microbial groups (fungi and Archaea) evaluated (34% similarity to the natural forest soil). Shannon Diversity index values showed that generally the conversion of tropical peatland natural forest to rubber plantation resulted in a greater impact on microbial diversity (ANOVA p < 0.05). Overall, this study indicated substantial shifts in the soil microbial activity and diversity upon conversion of natural peatland forest to agriculture, with a greater change being observed under rubber plantation compared to oil palm plantation. These findings provided important data for future peatland management by relating changes in the soil microbial community and activities associated to agricultural practices carried out on peatland.
Cite this paper: Nurulita, Y. , Adetutu, E. , Kadali, K. , Shahsavari, E. , Zul, D. , Taha, M. and Ball, A. (2016) Assessment of the Influence of Oil Palm and Rubber Plantations in Tropical Peat Swamp Soils Using Microbial Diversity and Activity Analysis. Journal of Agricultural Chemistry and Environment, 5, 53-65. doi: 10.4236/jacen.2016.52006.

[1]   Sorensen, K.W. (1993) Indonesian Peat Swamp Forests and Their Role as a Carbon Sink. Chemosphere, 27, 1065- 1082.

[2]   Andriesse, J. (1988) Nature and Management of Tropical Peat Soils. Food and Agriculture Organization (FAO) of United Nations, Rome.

[3]   Agus, F. and Subiksa, I. (2008) Lahan Gambut: Potensi untuk Pertanian dan Aspek Lingkungan. Balai Penelitian Tanah dan World Agroforesty Centre (ICRAF), Bogor.

[4]   van der Werf, G.R., Morton, D.C., De Fries, R.S., Olivier, J.G., Kasibhatla, P.S., Jackson, R.B., Collatz, G.J. and Randerson, J. (2009) CO2 Emissions from Forest Loss. Nature Geoscience, 2, 737-738.

[5]   van der Werf, G., Randerson, J.T., Giglio, L., Collatz, G., Mu, M., Kasibhatla, P.S., Morton, D.C., DeFries, R., Jin, Y.V. and Leeuwen, T.V. (2010) Global Fire Emissions and the Contribution of Deforestation, Savanna, Forest, Agricultural, and Peat Fires (1997-2009). Atmospheric Chemistry and Physics, 10, 11707-11735.

[6]   Hadi, A., Haridi, M., Inubushi, K., Purnomo, E., Razie, F. and Tsuruta, H. (2001) Effects of Land-Use Change in Tropical Peat Soil on the Microbial Population and Emission of Greenhouse Gases. Microbes and Environments, 16, 79-86.

[7]   Martikainen, P.J., Nykänen, H., Crill, P. and Silvola, J. (1993) Effect of a Lowered Water Table on Nitrous Oxide Fluxes from Northern Peatlands. Nature, 366, 51-53.

[8]   Huat, B.B., Kazemian, S., Prasad, A. and Barghchi, M. (2011) State of an Art Review of Peat: General Perspective. International Journal of Physical Sciences, 6, 1988-1996.

[9]   Gunawan, H., Kobayashi, S., Mizuno, K. and Kono, Y. (2012) Peat Swamp Forest Types and Their Regeneration in Giam Siak Kecil-Bukit Batu Bioshere Reserve, Riau, East Sumatra, Indonesia. Mires and Peat, 10, 1-17.

[10]   Persic, A. and Ocloo, M. (2011) Biosphere Reserves, World Heritage Sites and People: Enhancing Synergies for Sustainable Forests, in Adapting to Change—The State of Conservation of World Heritage Forests in 2011. In: Patry, M., Horn, R. and Haraguchi, S., Eds., World Heritage Center—United Nations Educational, Scientific and Cultural Organization (UNESCO), Paris, 68-72.

[11]   Sukara, E. and Purwanto, Y. (2009) Biosphere Reserve: The Management of Conservation Areas for Sustainable Economic Development. The 3rd Humanosphere Science School: Scientific Exploration and Sustainable Management of Peat and Land Resorces in Giam Siak Kecil-Bukit Batu Biosphere Reserve Riau, Pekanbaru, 4-5 August 2009, 1-20.

[12]   Sutapa, I. (2009) Water Management System in Peat Swamp Region. The 3rd Humanosphere Science School: Scientific Exploration and Sustainable Management of Peat and Land Resorces in Giam Siak Kecil-Bukit Batu Biosphere Reserve Riau, Pekanbaru, 4-5 August 2009, 153-163.

[13]   Arias, M.E., González-Pérez, J.A., González-Vila, F.J. and Ball, A.S. (2005) Soil Health—A New Challenge for Microbiologists and Chemists. International Microbiology, 8, 13-21.

[14]   Wagg, C., Bender, S.F., Widmer, F. and van der Heijden, M.G. (2014) Soil Biodiversity and Soil Community Composition Determine Ecosystem Multifunctionality. Proceedings of the National Academy of Sciences of the United States of America, 111, 5266-5270.

[15]   Bowles, T.M., Acosta-Martínez, V., Calderón, F. and Jackson, L.E. (2014) Soil Enzyme Activities, Microbial Communities, and Carbon and Nitrogen Availability in Organic Agroecosystems across an Intensively-Managed Agricultural Landscape. Soil Biology and Biochemistry, 68, 252-262.

[16]   Brouns, K., Verhoeven, J.T. and Hefting, M.M. (2014) The Effects of Salinization on Aerobic and Anaerobic Decomposition and Mineralization in Peat Meadows: The Roles of Peat Type and Land Use. Journal of Environmental Management, 143, 44-53.

[17]   Mishra, S., Lee, W., Hooijer, A., Reuben, S., Sudiana, I., Idris, A. and Swarup, S. (2013) Microbial and Metabolic Profiling Reveal Strong Influence of Water Table and Land-Use Patterns on Classification of Degraded Tropical Peatlands. Biogeosciences Discussions, 10, 14009-14042.

[18]   Peralta, A.L., Ludmer, S. and Kent, A.D. (2013) Hydrologic History Influences Microbial Community Composition and Nitrogen Cycling under Experimental Drying/Wetting Treatments. Soil Biology and Biochemistry, 66, 29-37.

[19]   Andersen, R., Chapman, S. and Artz, R. (2013) Microbial Communities in Natural and Disturbed Peatlands: A Review. Soil Biology and Biochemistry, 57, 979-994.

[20]   Nannipieri, P., Giagnoni, L., Renella, G., Puglisi, E., Ceccanti, B., Masciandaro, G., Fornasier, F., Moscatelli, M. and Marinari, S. (2012) Soil Enzymology: Classical and Molecular Approaches. Biology and Fertility of Soils, 48, 743-762.

[21]   Schloter, M., Dilly, O. and Munch, J. (2003) Indicators for Evaluating Soil Quality. Agriculture, Ecosystems & Environment, 98, 255-262.

[22]   Taylor, J., Wilson, B., Mills, M. and Burns, R. (2002) Comparison of Microbial Numbers and Enzymatic Activities in Surface Soils and Subsoils Using Various Techniques. Soil Biology and Biochemistry, 34, 387-401.

[23]   Chen, R., Senbayram, M., Blagodatsky, S., Myachina, O., Dittert, K., Lin, X., Blagodatskaya, E. and Kuzyakov, Y. (2014) Soil C and N Availability Determine the Priming Effect: Microbial N Mining and Stoichiometric Decomposition Theories. Global Change Biology, 20, 2356-2367.

[24]   Shi, W. (2011) Agricultural and Ecological Significance of Soil Enzymes: Soil Carbon Sequestration and Nutrient Cycling. In: Shukla, G. and Varma, A., Eds., Soil Enzymology, Springer, Berlin, 43-60.

[25]   Tischer, A., Blagodatskaya, E. and Hamer, U. (2014) Extracellular Enzyme Activities in a Tropical Mountain Rainforest Region of Southern Ecuador Affected by Low Soil P Status and Land-Use Change. Applied Soil Ecology, 74, 1-11.

[26]   Zinck, J. (2011) Tropical and Subtropical Peats: An Overview. In: Zinck, J. and Huber, O., Eds., Peatlands of the Western Guayana Highlands, Venezuela, Springer, Berlin, 5-28.

[27]   Jackson, C.R., Foreman, C.M. and Sinsabaugh, R.L. (1995) Microbial Enzyme Activities as Indicators of Organic Matter Processing Rates in a Lake Erie Coastal Wetland. Freshwater Biology, 34, 329-342.

[28]   Jackson, C.R. and Vallaire, S.C. (2007) Microbial Activity and Decomposition of Fine Particulate Organic Matter in a Louisiana Cypress Swamp. Journal of the North American Benthological Society, 26, 743-753.

[29]   Williams, R.T. and Crawford, R.L. (1983) Microbial Diversity of Minnesota Peatlands. Microbial Ecology, 9, 201-214.

[30]   Puglisi, E., Zaccone, C., Cappa, F., Cocconcelli, P.S., Shotyk, W., Trevisan, M. and Miano, T.M. (2014) Changes in Bacterial and Archaeal Community Assemblages along an Ombrotrophic Peat Bog Profile. Biology and Fertility of Soils, 50, 815-826.

[31]   Tfaily, M.M., Cooper, W.T., Kostka, J.E., Chanton, P.R., Schadt, C.W., Hanson, P.J., Iversen, C.M. and Chanton, J.P. (2014) Organic Matter Transformation in the Peat Column at Marcell Experimental Forest: Humification and Vertical Stratification. Journal of Geophysical Research: Biogeosciences, 119, 661-675.

[32]   Mettrop, I.S., Cusell, C., Kooijman, A.M. and Lamers, L.P. (2014) Nutrient and Carbon Dynamics in Peat from Rich Fens and Sphagnum Fens during Different Gradations of Drought. Soil Biology and Biochemistry, 68, 317-328.

[33]   Girvan, M.S., Bullimore, J., Pretty, J.N., Osborn, A.M. and Ball, A.S. (2003) Soil Type Is the Primary Determinant of the Composition of the Total and Active Bacterial Communities in Arable Soils. Applied and Environmental Microbiology, 69, 1800-1809.

[34]   Tabatabai, M. and Bremner, J. (1969) Use of p-Nitrophenyl Phosphate for Assay of Soil Phosphatase Activity. Soil Biology and Biochemistry, 1, 301-307.

[35]   Nurulita, Y., Adetutu, E.M., Gunawan, H., Zul, D. and Ball, A.S. (2016) Restoration of Tropical Peat Soils: The Application of Soil Microbiology for Monitoring the Success of the Restoration Process. Agriculture, Ecosystems & Environment, 216, 293-303.

[36]   Steffan, R.J., Goksøyr, J., Bej, A. and Atlas, R. (1988) Recovery of DNA from Soils and Sediments. Applied and Environmental Microbiology, 54, 2908-2915.

[37]   Zhu, L., Xu, H., Zhang, Y., Fu, G., Wu, P.Q. and Li, Y. (2014) BOX-PCR and PCR-DGGE Analysis for Bacterial Diversity of a Naturally Fermented Functional Food (Enzyme®). Food Bioscience, 5, 115-122.

[38]   Kreader, C.A. (1996) Relief of Amplification Inhibition in PCR with Bovine Serum Albumin or T4 Gene 32 Protein. Applied and Environmental Microbiology, 62, 1102-1106.

[39]   Gardes, M. and Bruns, T.D. (1993) ITS Primers with Enhanced Specificity for Basidiomycetes—Application to the Identification of Mycorrhizae and Rusts. Molecular Ecology, 2, 113-118.

[40]   Muyzer, G., De Waal, E.C. and Uitterlinden, A.G. (1993) Profiling of Complex Microbial Populations by Denaturing Gradient Gel Electrophoresis Analysis of Polymerase Chain Reaction-Amplified Genes Coding for 16S rRNA. Applied and Environmental Microbiology, 59, 695-700.

[41]   White, T.J., Bruns, T., Lee, S. and Taylor, J. (1990) Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. Innis, M.A., Gelfand, D.H., Sninsky, J.J. and White, T.J., Eds., PCR Protocols: A Guide to Methods and Applications, Academic Press, Cambridge, MA, 315-322.

[42]   Jackson, C.R., Langner, H.W., Donaho-Christiansen, J., Inskeep, W.P. and McDermott, T.R. (2001) Molecular Analysis of Microbial Community Structure in an Arsenite-Oxidizing Acidic Thermal Spring. Environmental Microbiology, 3, 532-542.

[43]   Shannon, C.E. and Weaver, W. (1949) The Mathematical Theory of Communication. University of Illinois Press, Champaign.

[44]   Zech, W., Senesi, N., Guggenberger, G., Kaiser, K., Lehmann, J., Miano, T.M., Miltner, A. and Schroth, G. (1997) Factors Controlling Humification and Mineralization of Soil Organic Matter in the Tropics. Geoderma, 79, 117-161.

[45]   Nurulita, Y., Adetutu, E.M., Kadali, K.K., Zul, D., Mansur, A.A. and Ball, A.S. (2015) The Assessment of the Impact of Oil Palm and Rubber Plantation on the Biotic and Abiotic Properties of Tropical Peat Swamp Soil in Indonesia. International Journal of Agricultural Sustainability, 13, 150-166.

[46]   Zak, D.R., Blackwood, C.B. and Waldrop, M.P. (2006) A Molecular Dawn for Biogeochemistry. Trends in Ecology & Evolution, 21, 288-295.

[47]   Jackson, C.R., Liew, K.C. and Yule, C.M. (2009) Structural and Functional Changes with Depth in Microbial Communities in a Tropical Malaysian Peat Swamp Forest. Microbial Ecology, 57, 402-412.

[48]   Kanokratana, P., Uengwetwanit, T., Rattanachomsri, U., Bunterngsook, B., Nimchua, T., Tangphatsornruang, S., Plengvidhya, V., Champreda, V. and Eurwilaichitr, L. (2011) Insights into the Phylogeny and Metabolic Potential of a Primary Tropical Peat Swamp Forest Microbial Community by Metagenomic Analysis. Microbial Ecology, 61, 518-528.

[49]   Sinsabaugh, R., Antibus, R., Linkins, A., McClaugherty, C., Rayburn, L., Repert, D. and Weiland, T. (1993) Wood Decomposition: Nitrogen and Phosphorus Dynamics in Relation to Extracellular Enzyme Activity. Ecology, 74, 1586-1593.

[50]   Stone, M., DeForest, J. and Plante, A. (2014) Changes in Extracellular Enzyme Activity and Microbial Community Structure with Soil Depth at the Luquillo Critical Zone Observatory. Soil Biology and Biochemistry, 75, 237-247.

[51]   Lee-Cruz, L., Edwards, D.P., Tripathi, B.M. and Adams, J.M. (2013) Impact of Logging and Forest Conversion to Oil Palm Plantations on Soil Bacterial Communities in Borneo. Applied and Environmental Microbiology, 79, 7290-7297.

[52]   Marschner, P., Kandeler, E. and Marschner, B. (2003) Structure and Function of the Soil Microbial Community in a Long-Term Fertilizer Experiment. Soil Biology and Biochemistry, 35, 453-461.

[53]   Schweitzer, J.A., Fischer, D.G., Rehill, B.J., Wooley, S.C., Woolbright, S.A., Lindroth, R.L., Whitham, T.G., Zak, D.R. and Hart, S.C. (2011) Forest Gene Diversity Is Correlated with the Composition and Function of Soil Microbial Communities. Population Ecology, 53, 35-46.

[54]   Ng, E.-L., Patti, A., Rose, M., Schefe, C., Smernik, R. and Cavagnaro, T. (2014) Do Organic Inputs Alter Resistance and Resilience of Soil Microbial Community to Drying? Soil Biology and Biochemistry, 81, 58-66.

[55]   Orgiazzi, A., Lumini, E., Nilsson, R.H., Girlanda, M., Vizzini, A., Bonfante, P. and Bianciotto, V. (2012) Unravelling Soil Fungal Communities from Different Mediterranean Land-Use Backgrounds. PLoS ONE, 7, e34847.

[56]   Thormann, M.N. (2006) The Role of Fungi in Boreal Peatlands. In: Wieder, R.K. and Vitt, D.H., Eds., Boreal Peatland Ecosystems, Springer, Berlin, 101-123.

[57]   O’Donnell, A.G., Seasman, M., Macrae, A., Waite, I. and Davies, J.T. (2001) Plants and Fertilisers as Drivers of Change in Microbial Community Structure and Function in Soils. Plant and Soil, 232, 135-145.

[58]   Foster, W.A., Snaddon, J.L., Turner, E.C., Fayle, T.M., Cockerill, T.D., Ellwood, M.F., Broad, G.R., Chung, A.Y., Eggleton, P. and Khen, C.V. (2011) Establishing the Evidence Base for Maintaining Biodiversity and Ecosystem Function in the Oil Palm Landscapes of South East Asia. Philosophical Transactions of the Royal Society B: Biological Sciences, 366, 3277-3291.

[59]   Yahya, Z., Husin, A., Talib, J., Othman, J., Ahmed, O.H. and Jalloh, M.B. (2010) Soil Compaction and Oil Palm (Elaeis guineensis) Yield in a Clay Textured Soil. American Journal of Agricultural and Biological Sciences, 5, 15-19.

[60]   Fayle, T.M., Turner, E.C., Snaddon, J.L., Chey, V.K., Chung, A.Y., Eggleton, P. and Foster, W.A. (2010) Oil Palm Expansion into Rain Forest Greatly Reduces ant Biodiversity in Canopy, Epiphytes and Leaf-Litter. Basic and Applied Ecology, 11, 337-345.

[61]   Hassall, M., Jones, D.T., Taiti, S., Latipi, Z., Sutton, S.L. and Mohammed, M. (2006) Biodiversity and Abundance of Terrestrial Isopods along a Gradient of Disturbance in Sabah, East Malaysia. European Journal of Soil Biology, 42, S197-S207.

[62]   Torsvik, V. and Øvreas, L. (2002) Microbial Diversity and Function in Soil: From Genes to Ecosystems. Current Opinion in Microbiology, 5, 240-245.

[63]   Nannipieri, P., Ascher, J., Ceccherini, M., Landi, L., Pietramellara, G. and Renella, G. (2003) Microbial Diversity and Soil Functions. European Journal of Soil Science, 54, 655-670.