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

Volumn 74, Issue , 2014, Pages 1-11

  Tischer, Alexander ^a   Blagodatskaya, Evgenia ^b   Hamer, Ute ^a,c  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b INSTITUTE OF PHYSICOCHEMICAL AND BIOLOGICAL PROBLEMS IN SOIL SCIENCE   (Russian Federation)

^c UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Extracellular enzymes; Land use change; Low nutrient status; Microbial resource stoichiometry; P demand; Tropical mountain rainforest

Indexed keywords

EID: 84886246927     PISSN: 09291393     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.apsoil.2013.09.007     Document Type: Article

References (104)

1. Alef K., Nannipieri P. Cellulase activity. Methods in Applied Soil Microbiology and Biochemistry 1995, 345-349. Academic Press, London, San Diego. K. Alef, P. Nannipieri (Eds.).
2. Alef K., Nannipieri P., Trazar-Cepeda C. Phosphatase activity. Methods in Applied Soil Microbiology and Biochemistry 1995, 335-344. Academic Press, London, San Diego. K. Alef, P. Nannipieri (Eds.).
3. Allison S.D., Martiny J.B.H. Resistance, resilience, and redundancy in microbial communities. Proc. Natl. Acad. Sci. U.S.A. 2008, 105(Supplement 1):11512-11519.
4. Allison S.D., Vitousek P.M. Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol. Biochem. 2005, 37(5):937-944.
5. Allison S.D., Wallenstein M.D., Bradford M.A. Soil-carbon response to warming dependent on microbial physiology. Nat. Geosci. 2010, 3(5):336-340.
6. Allison S.D., Weintraub M.N., Gartner T.B., Waldrop M.P. Evolutionary-economic principles as regulators of soil enzyme production and ecosystem function. Soil Enzymology 2011, 229-243. Springer, Berlin. G. Shukla, A. Varma (Eds.).
7. Allison V.J., Condron L.M., Peltzer D.A., Richardson S.J., Turner B.L. Changes in enzyme activities and soil microbial community composition along carbon and nutrient gradients at the Franz Josef chronosequence, New Zealand. Soil Biol. Biochem. 2007, 39(7):1770-1781.
8. Baldrian P. Microbial enzyme-catalyzed processes in soils and their analysis. Plant Soil Environ. 2009, 55(9):370-378.
9. Barroso C.B., Nahas E. The status of soil phosphate fractions and the ability of fungi to dissolve hardly soluble phosphates. Appl. Soil Ecol. 2005, 29(1):73-83.
10. Beck E., Bendix J., Kottke I., Makeschin F., Mosandl R. Gradients in a Tropical Mountain Ecosystem of Ecuador 2008, 525. Springer-Verlag, Berlin, Heidelberg.
11. Bendix J., Homeier J., Cueva Ortiz E., Emck P., Breckle S.W., Richter M., Beck E. Seasonality of weather and tree phenology in a tropical evergreen mountain rain forest. Int. J. Biometeorol. 2006, 50(6):370-384.
12. Bendix J., Rollenbeck R., Richter M., Fabian P., Emck P. Climate. Gradients in a Tropical Mountain Ecosystem of Ecuador 2008, vol. 198:63-74. Springer, Berlin.
13. Bray R.H., Kurtz L.T. Determination of total, organic and available forms of phosphorus in soils. Soil Sci. 1945, 59:39-45.
14. Burke D.J., Weintraub M.N., Hewins C.R., Kalisz S. Relationship between soil enzyme activities, nutrient cycling and soil fungal communities in a northern hardwood forest: knowledge gaps in soil C and N interactions. Soil Biol. Biochem. 2011, 43(4):795-803.
15. Burns R.G., DeForest J.L., Marxsen J., Sinsabaugh R.L., Stromberger M.E., Wallenstein M.D., Weintraub M.N., Zoppini A. Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol. Biochem. 2013, 58:216-234.
16. Cañizares R., Moreno B., Benitez E. Bacterial β-glucosidase function and metabolic activity depend on soil management in semiarid rainfed agriculture. Ecol. Evol. 2012, 2(4):727-731.
17. de Cesare F., Garzillo A.M.V., Buonocore V., Badalucco L. Use of sonication for measuring acid phosphatase activity in soil. Soil Biol. Biochem. 2000, 32(6):825-832.
18. Cleveland C., Liptzin D. C:N:P stoichiometry in soil: is there a Redfield ratio for the microbial biomass?. Biogeochemistry 2007, 85(3):235-252.
19. Craine J.M., Morrow C., Fierer N. Microbial nitrogen limitation increases decomposition. Ecology 2007, 88(8):2105-2113.
20. Cusack D.F., Torn M.S., McDowell W.H., Silver W.L. The response of heterotrophic activity and carbon cycling to nitrogen additions and warming in two tropical soils. Glob. Change Biol. 2010, 16(9):2555-2572.
21. Cusack D.F., Torn M.S., McDowell W.H., Silver W.L. The response of heterotrophic activity and carbon cycling to nitrogen additions and warming in two tropical soils: corrigendum. Glob. Change Biol. 2012, 18(1):400.
22. Davidson E.A., de Carvalho C.J.R., Figueira A.M., Ishida F.Y., Ometto J.P.H.B., Nardoto G.B., Saba R.T., Hayashi S.N., Leal E.C., Vieira I.C.G., Martinelli L.A. Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 2007, 447(7147):995-998.
23. Demetz M., Insam H. Phosphorus availability in a forest soil determined with a respiratory assay compared to chemical methods. Geoderma 1999, 89(3-4):259-271.
24. Dilly O., Nannipieri P. Response of ATP content, respiration rate and enzyme activities in an arable and a forest soil to nutrient additions. Biol. Fertil. Soils 2001, 34(1):64-72.
25. Don A., Schumacher J., Freibauer A. Impact of tropical land-use change on soil organic carbon stocks - a meta-analysis. Glob. Change Biol. 2011, 17(4):1658-1670.
26. Doolette A.L., Smernik R.J. Soil organic phosphorus speciation using spectroscopic techniques. Phosphorus in Action: Biological Processes in Soil Phosphorus Cycling 2011, vol. 100:3-36. Springer Berlin, Heidelberg.
27. Ehrenfeld J.G., Ravit B., Elgersma K. Feedback in plant-soil system. Annu. Rev. Environ. Resour. 2005, 30(1):75-115.
28. FAO World Reference Base for Soil Resources 2006: A Framework for International Classification, Correlation and Communication 2006, 128. Food and Agriculture Organization of the United Nations, Rome.
29. Fierer N., Jackson R.B. The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. U.S.A. 2006, 103(3):626-631.
30. Fontaine S., Barot S. Size and functional diversity of microbe populations control plant persistence and long-term soil carbon accumulation. Ecol. Lett. 2005, 8(10):1075-1087.
31. Gerique A. Biodiversity as a Resource: Biodiversity as a Resource: Plant Use and Land Use Among the Shuar, Saraguros, and Mestizos in Tropical Rainforest Areas of Southern Ecuador 2010, Friedrich-Alexander Universität Erlangen-Nürnberg, Dissertation.
32. German D.P., Chacon S.S., Allison S.D. Substrate concentration and enzyme allocation can affect rates of microbial decomposition. Ecology 2011, 92(7):1471-1480.
33. German D.P., Weintraub M.N., Grandy A.S., Lauber C.L., Rinkes Z.L., Allison S.D. Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol. Biochem. 2011, 43(7):1387-1397.
34. Göttlicher D., Obregón A., Homeier J., Rollenbeck R., Nauss T., Bendix J. Land-cover classification in the Andes of southern Ecuador using Landsat ETM+ data as a basis for SVAT modelling. Int. J. Remote Sens. 2009, 30(8):1867-1886.
35. Grandy A.S., Neff J.C., Weintrau M.N. Carbon structure and enzyme activities in alpine and forest ecosystems. Soil Biol. Biochem. 2007, 39:2701-2711.
36. Günter S., Gonzalez P., Ãlvarez G., Aguirre N., Palomeque X., Haubrich F., Weber M. Determinants for successful reforestation of abandoned pastures in the Andes: soil conditions and vegetation cover. For. Ecol. Manag. 2009, 258(2):81-91.
37. Hamer U., Potthast K., Burneo J., Makeschin F. Nutrient stocks and phosphorus fractions in mountain soils of Southern Ecuador after conversion of forest to pasture. Biogeochemistry 2013, 112(1-3):495-510.
38. Hamer U., Unger M., Makeschin F. Impact of air-drying and rewetting on PLFA profiles of soil microbial communities. J Plant Nutr. Soil Sci. 2007, 170:259-264.
39. Hartig K., Beck E. The bracken fern (Pteridium arachnoideum (Kaulf.) Maxon) dilemma in the Andes of southern Ecuador. Ecotropica (Bonn) 2003, 9(1-2):3-13.
40. Homeier J., Breckle S.-W., Günter S., Rollenbeck R.T., Leuschner C. Tree diversity, forest structure and productivity along altitudinal and topographical gradients in a species-rich ecuadorian montane rainforest. Biotropica 2010, 42(2):140-148.
41. Homeier J., Hertel D., Camenzind T., Cumbicus N.L., Maraun M., Martinson G.O., Poma L.N., Rillig M.C., Sandmann D., Scheu S., Veldkamp E., Wilcke W., Wullaert H., Leuschner C. Tropical andean forests are highly susceptible to nutrient inputs-rapid effects of experimental N and P addition to an ecuadorian montane forest. PLoS ONE 2012, 7(10):e47128.
42. Homeier J., Werner F.A. Spermatophyta. Ecotropical Monogr. 2007, 4:15-58.
43. Hoppe H.-G. Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Mar. Ecol. Prog. Ser. 1983, 11:299-308.
44. Hughes R.F., Kauffman J.B., Cummings D.L. Dynamics of aboveground and soil carbon and nitrogen stocks and cycling of available nitrogen along a land-use gradient in Rondonia, Brazil. Ecosystems 2002, 5(3):244-259.
45. Joergensen R.G. Organic matter and micro-organisms in tropical soils. Soil Biology and Agriculture in the Tropics 2010, 17-44. Springer, Berlin, Heidelberg. P. Dion (Ed.).
46. Joergensen R.G., Emmerling C. Methods for evaluating human impact on soil microorganisms based on their activity, biomass, and diversity in agricultural soils. J. Plant Nutr. Soil Sci. 2006, 169(3):295-309.
47. Kandeler E., Luxhøi J., Tscherko D., Magid J. Xylanase, invertase and protease at the soil-litter interface of a loamy sand. Soil Biol. Biochem. 1999, 31(8):1171-1179.
48. Kauffman J., Cummings D.L., Ward D.E. Fire in the Brazilian Amazon 2. Biomass, nutrient pools and losses in cattle pastures. Oecologia 1998, 113(3):415-427.
49. Kingston H.M., Jassie L.B. Microwave energy for acid decomposition at elevated temperatures and pressures using biological and botanical samples. Anal. Chem. 1986, 58(12):2534-2541.
50. Kögel-Knabner I. The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol. Biochem. 2002, 34(2):139-162.
51. Kovarova-Kovar K., Egli T. Growth kinetics of suspended microbial cells: from single-substrate-controlled growth to mixed-substrate kinetics. Microbiol. Mol. Biol. Rev. 1998, 62(3):646-666.
52. Landon J.R. Booker Tropical Soil Manual: A Handbook for Soil Survey and Agricultural Land Evaluation in the Tropics and Subtropics 1991, Booker Tate Ltd., Longman Group UK Ltd., Masters Court Thame.
53. Lauber C.L., Strickland M.S., Bradford M.A., Fierer N. The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol. Biochem. 2008, 40(9):2407-2415.
54. Legendre P., Legendre L. Numerical Ecology 1998, Elsevier, Amsterdam, XV, 853. 2nd ed.
55. Leinweber P., Jandl G., Baum C., Eckhardt K.-U., Kandeler E. Stability and composition of soil organic matter control respiration and soil enzyme activities: special section: functional microbial ecology: molecular approaches to microbial ecology and microbial habitats 18th world congress of soil science. Soil Biol. Biochem. 2008, 40(6):1496-1505.
56. eff) of soils. J. Plant Nutr. Soil Sci. 2000, 163(5):555-557.
57. Makeschin F., Haubrich F., Abiy M., Burneo J.I., Klinger T. Pasture management and natural soil regeneration. Gradients in a Tropical Mountain Ecosystem of Ecuador 2008, vol. 198:397-408. Springer, Berlin.
58. Marx M.C., Kandeler E., Wood M., Wermbter N., Jarvis S.C. Exploring the enzymatic landscape: distribution and kinetics of hydrolytic enzymes in soil particle-size fractions. Soil Biol. Biochem. 2005, 37(1):35-48.
59. Merilä P., Smolander A., Strömmer R. Soil nitrogen transformations along a primary succession transect on the land-uplift coast in western Finland. Soil Biol. Biochem. 2002, 34:373-385.
60. Metcalfe A.C., Krsek M., Gooday G.W., Prosser J.I., Wellington E.M.H. Molecular analysis of a bacterial chitinolytic community in an upland pasture. Appl. Environ. Microbiol. 2002, 68(10):5042-5050.
61. Miller M., Palojärvi A., Rangger A., Reeslev M., Kjöller A. The use of fluorogenic substrates to measure fungal presence and activity in soil. Appl. Environ. Microbiol. 1998, 64(2):613-617.
62. Moorhead D.L., Sinsabaugh R.L. A theoretical model of litter decay and microbial interaction. Ecol. Monogr. 2006, 76(2):151-174.
63. Moser G., Leuschner C., Hertel D., Graefe S., Soethe N., Iost S. Elevation effects on the carbon budget of tropical mountain forests (S Ecuador): the role of the belowground compartment. Glob. Change Biol. 2011, 17(6):2211-2226.
64. Murty D., Kirschbaum M.U.F., McMurtrie R.E., Mcgilvray H. Does conversion of forest to agricultural land change soil carbon and nitrogen? a review of the literature. Glob. Change Biol. 2002, 8(2):105-123.
65. Nannipieri P., Giagnoni L., Landi L., Renella G. Role of phosphatase enzymes in soil. Phosphorus in Action: Biological Processes in Soil Phosphorus Cycling 2011, vol. 100:215-243. Springer, Berlin, Heidelberg.
66. Nannipieri P., Paul E. The chemical and functional characterization of soil N and its biotic components. Soil Biol. Biochem. 2009, 41(12):2357-2369.
67. Nottingham A., Turner B., Chamberlain P., Stott A., Tanner E. Priming and microbial nutrient limitation in lowland tropical forest soils of contrasting fertility. Biogeochemistry 2011, 1-19.
68. Parfitt R.L., Yeates G.W., Ross D.J., Mackay A.D., Budding P.J. Relationships between soil biota, nitrogen and phosphorus availability, and pasture growth under organic and conventional management. Appl. Soil Ecol. 2005, 28(1):1-13.
69. Soil Microbiology, Ecology and Biochemistry 2007, Academic Press, Oxford. 3rd ed. E.A. Paul (Ed.).
70. Potthast K., Hamer U., Makeschin F. Impact of litter quality on mineralization processes in managed and abandoned pasture soils in Southern Ecuador. Soil Biol. Biochem. 2010, 42:56-64.
71. Potthast K., Hamer U., Makeschin F. In an Ecuadorian pasture soil the growth of Setaria sphacelata, but not of soil microorganisms, is co-limited by N and P. Appl. Soil Ecol. 2012, 62(0):103-114.
72. Potthast K., Hamer U., Makeschin F. Land-use change in a tropical mountain rainforest region of southern Ecuador affects soil microorganisms and nutrient cycling. Biogeochemistry 2012, 111(1-3):151-167.
73. Microbial Lipids 1988, Academic Press Inc, San Diego. C. Ratledge, S.G. Wilkinson (Eds.).
74. Reed S.C., Vitousek P.M., Cleveland C.C. Are patterns in nutrient limitation belowground consistent with those aboveground: results from a 4 million year chronosequence. Biogeochemistry 2011, 106:323-336.
75. Schimel J.P., Bennett J. Nitrogen mineralization: challenges of a changing paradigm. Ecology 2004, 85(3):591-602.
76. Schimel J.P., Weintraub M.N. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol. Biochem. 2003, 35(4):549-563.
77. Silva B., Roos K., Voss I., König N., Rollenbeck R., Scheibe R., Beck E., Bendix J. Simulating canopy photosynthesis for two competing species of an anthropogenic grassland community in the Andes of southern Ecuador: simulating ecosystem functioning of tropical mountainous cloud forests in southern Ecuador. Ecol. Model. 2012, 239(0):14-26.
78. Sinsabaugh R.L. Enzymic analysis of microbial pattern and process. Biol. Fertil. Soils 1994, 17(1):69-74.
79. Sinsabaugh R.L., Lauber C.L., Weintraub M.N., Ahmed B., Allison S.D., Crenshaw C., Contosta A.R., Cusack D., Frey S., Gallo M.E., Gartner T.B., Hobbie S.E., Holland K., Keeler B.L., Powers J.S., Stursova M., Takacs-Vesbach C., Waldrop M.P., Wallenstein M.D., Zak D.R., Zeglin L.H. Stoichiometry of soil enzyme activity at global scale. Ecol. Lett. 2008, 11(11):1252-1264.
80. Six J., Frey S.D., Thiet R.K., Batten K.M. Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci. Soc. Am. J. 2006, 70(2):555-569.
81. StatSoft I. Statistica for Windows. Version 9.0, Tulsa 2009.
82. Steinweg J.M., Jagadamma S., Frerichs J., Mayes M.A. Activation Energy of Extracellular Enzymes in Soils from Different Biomes. PLoS ONE 2013, 8(3):e59943.
83. Stemmer M., Lützow M.v., Kandeler E., Pichlmayer F., Gerzabek M.H. The effect of maize straw placement on mineralization of C and N in soil particle size fractions. Eur. J. Soil Sci. 1999, 50.
84. Sterner R.W., Elser J.J. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere 2002, Princeton University Press, Princeton, xxi, 439.
85. Stres B., Tiedje J.M. New frontiers in soil microbiology: how to link structure and function of microbial communities?. Soil Biology. Nucleic Acids and Proteins in Soil 2006, 1-22. Springer, Berlin, Heidelberg. P. Nannipieri, K. Smalla (Eds.).
86. Štursová M., Žifčáková L., Leigh M.B., Burgess R., Baldrian P. Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers. FEMS Microbiol. Ecol. 2012, 80(3):735-746.
87. Suzuki Y., Kishigami T., Abe S. Production of extracellular alpha-glucosidase by a thermophilic Bacillus species. Appl. Environ. Microbiol. 1976, 31(6):807-812.
88. Swift M.J., Heal O.W., Anderson J.M. Decomposition in Terrestrial Ecosystems 1979, Blackwell Scientific Publications, Oxford.
89. Tate R.L. Microbiology and enzymology of carbon and nitrogen cycling. Enzymes in the Environment. Activity, Ecology, and Applications 2002, 227-248. Marcel Dekker, New York. R.G. Burns, R.P. Dick (Eds.).
90. ter Braak C.J.F., Smilauer P. CANOCO Reference Manual and CanoDraw for Windows User's Guide: Software for Canonical Community Ordination. Version 4.5 2002, Biometris, Wageningen.
91. Terahara T., Ikeda S., Noritake C., Minamisawa K., Ando K., Tsuneda S., Harayama S. Molecular diversity of bacterial chitinases in arable soils and the effects of environmental factors on the chitinolytic bacterial community. Soil Biol. Biochem. 2009, 41(3):473-480.
92. Treseder K.K., Kivlin S.N., Hawkes C.V. Evolutionary trade-offs among decomposers determine responses to nitrogen enrichment. Ecol. Lett. 2011, 14(9):933-938.
93. Turner B.L. Variation in pH optima of hydrolytic enzyme activities in tropical rain forest soils. Appl. Environ. Microbiol. 2010, 76(19):6485-6493.
94. Vance E.D., Brookes P.C., Jenkinson D.S. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 1987, 19(6):703-707.
95. Vitousek P.M., Hättenschwiler S., Olander L., Allison S. Nitrogen and nature. Ambio 2002, 31(2):97-101.
96. Waldrop M.P., Balser T.C., Firestone M.K. Linking microbial community composition to function in a tropical soil. Soil Biol. Biochem. 2000, 32(13):1837-1846.
97. Wallenstein M.D., Weintraub M.N. Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biol. Biochem. 2008, 40(9):2098-2106.
98. Wardle D.A. A comperative assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biol. Rev. 1992, 67(3):321-358.
99. Webster R. Analysis of variance, inference, multiple comparisons and sampling effects in soil research. Eur. J. Soil Sci. 2007, 58:74-82.
100. Wilcke W., Yasin S., Schmitt A., Valarezo C., Zech W. Soils along the altitudinal transect and in catchments. Gradients in a Tropical Mountain Ecosystem of Ecuador 2008, vol. 198:75-85. Springer, Berlin.
101. Wong K.K., Tan L.U., Saddler J.N. Multiplicity of beta-1,4-xylanase in microorganisms: functions and applications. Microbiol. Rev. 1988, 52(3):305-317.
102. Zelles L. Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol. Fertil. Soils 1999, 29(2):111-129.
103. Zelles L., Bai Q.Y., Rackwitz R., Chadwick D., Beese F. Determination of phospholipid- and lipopolysaccharide-derived fatty acids as an estimate of microbial biomass and community structures in soils. Biol. Fertil. Soils 1995, 19(2-3):115-123.
104. Zuur A.F., Ieno E.N., Smith G.M. Analysing Ecological Data 2007, 672. Springer, New York.