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Organic matter inputs shift soil enzyme activity and allocation patterns in a wet tropical forest

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Abstract

Soil extracellular enzymes mediate organic matter turnover and nutrient cycling yet remain little studied in one of Earth’s most rapidly changing, productive biomes: tropical forests. Using a long-term leaf litter and throughfall manipulation, we explored relationships between organic matter (OM) inputs, soil chemical properties and enzyme activities in a lowland tropical forest. We assayed six hydrolytic soil enzymes responsible for liberating carbon (C), nitrogen (N) and phosphorus (P), calculated enzyme activities and ratios in control plots versus treatments, and related these to soil biogeochemical variables. While leaf litter addition and removal tended to increase and decrease enzyme activities per gram soil, respectively, shifts in enzyme allocation patterns implied changes in relative nutrient constraints with altered OM inputs. Enzyme activity ratios in control plots suggested strong belowground P constraints; this was exacerbated when litter inputs were curtailed. Conversely, with double litter inputs, increased enzymatic investment in N acquisition indicated elevated N demand. Across all treatments, total soil C correlated more strongly with enzyme activities than soluble C fluxes, and enzyme ratios were sensitive to resource stoichiometry (soil C:N) and N availability (net N mineralization). Despite high annual precipitation in this site (MAP ~5 m), soil moisture positively correlated with five of six enzymes. Our results suggest resource availability regulates tropical soil enzyme activities, soil moisture plays an additional role even in very wet forests, and relative investment in C, N and P degrading enzymes in tropical soils will often be distinct from higher latitude ecosystems yet is sensitive to OM inputs.

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References

  • Aber JD, Melillo JM (1980) Litter decomposition—measuring relative contributions of organic-matter and nitrogen to forest soils. Can J Bot (Revue Canadienne De Botanique) 58(4):416–421

    Google Scholar 

  • Allison SD (2006) Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes. Biogeochemistry 81(3):361–373

    Article  Google Scholar 

  • Allison SD, Vitousek PM (2004) Extracellular enzyme activities and carbon chemistry as drivers of tropical plant litter decomposition. Biotropica 36(3):285–296

    Google Scholar 

  • Allison S, Wallenstein M, Bradford M (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340

    Article  Google Scholar 

  • Austin A, Vitousek P (1998) Nutrient dynamics on a precipitation gradient in Hawai’i. Oecologia 113:519–529

    Article  Google Scholar 

  • Beck T, Joergensen RG, Kandeler E, Makeschin F, Nuss E, Oberholzer HR, Scheu S (1997) An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C. Soil Biol Biochem 29(7):1023–1032

    Article  Google Scholar 

  • Berg B (2000) Litter decomposition and organic matter turnover in northern forest soils. For Ecol Manag 133(1–2):13–22

    Article  Google Scholar 

  • Bern CR, Townsend AR, Farmer GL (2005) Unexpected dominance of parent-material strontium in a tropical forest on highly weathered soils. Ecology 86(3):626–632

    Article  Google Scholar 

  • Berrange JP, Thorpe RS (1988) The geology, geochemistry and emplacement of the cretaceous tertiary ophiolitic Nicoya Complex of the Osa Peninsula, southern Costa-Rica. Tectonophysics 147(3–4):193–220

    Article  Google Scholar 

  • Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320(5882):1444–1449

    Article  Google Scholar 

  • Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil-nitrogen—a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17(6):837–842

    Article  Google Scholar 

  • Brzostek ER, Finzi AC (2011) Substrate supply, fine roots, and temperature control proteolytic enzyme activity in temperate forest soils. Ecology 92(4):892–902

    Article  Google Scholar 

  • Burns RG (1982) Enzyme-activity in soil—location and a possible role in microbial ecology. Soil Biol Biochem 14(5):423–427

    Article  Google Scholar 

  • Burns RG, Dick RP (2002) Enzymes in the environment: activity, ecology and applications. Marcel Dekker, New York

    Book  Google Scholar 

  • Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc Natl Acad Sci USA 104:4990–4995

    Article  Google Scholar 

  • Chai SL, Tanner E (2010) Are we losing the best parts of our protected areas in tropical mountains? Biotropica 42:739–747

    Article  Google Scholar 

  • Clark D, Piper S, Keeling C, Clark D (2003) Tropical rain forest tree growth and atmospheric carbon dynamics linked to interannual temperature variation during 1984–2000. Proc Natl Acad Sci USA 100:5852–5857

    Article  Google Scholar 

  • Cleveland CC, Townsend AR (2006) Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. Proc Natl Acad Sci USA 103(27):10316–10321

    Article  Google Scholar 

  • Cleveland CC, Townsend AR, Schimel D et al (1999) Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Biogeochemistry 13:623–645

    Google Scholar 

  • Cleveland CC, Townsend AR, Schmidt SK (2002) Phosphorus limitation of microbial processes in moist tropical forests: evidence from short-term laboratory incubations and field studies. Ecosystems 5(7):680–691

    Article  Google Scholar 

  • Cleveland CC, Reed SC, Townsend AR (2006) Nutrient regulation of organic matter decomposition in a tropical rain forest. Ecology 87(2):492–503

    Article  Google Scholar 

  • Cleveland CC, Wieder WR, Reed SC, Townsend AR (2010) Experimental drought in a tropical rain forest increases soil carbon dioxide losses to the atmosphere. Ecology 91(8):2313–2323

    Article  Google Scholar 

  • Cleveland C, Townsend A, Taylor P et al (2011) Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. Ecol Lett 14:939–947

    Article  Google Scholar 

  • Crews T, Kitayama K, Fownes J et al (1995) Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76:1407–1424

    Article  Google Scholar 

  • Cusack DF, Chou WW, Yang WH, Harmon ME, Silver WL, Team L (2009) Controls on long-term root and leaf litter decomposition in neotropical forests. Glob Change Biol 15(5):1339–1355

    Article  Google Scholar 

  • Cusack DF, Silver WL, Torn MS, Burton SD, Firestone MK (2011) Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. Ecology 92(3):621–632

    Article  Google Scholar 

  • Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281(5374):237–240

    Article  Google Scholar 

  • Freeman C, Ostle N, Kang H (2001) An enzymic ‘latch’ on a global carbon store—a shortage of oxygen locks up carbon in peatlands by restraining a single enzyme. Nature 409(6817):149

    Article  Google Scholar 

  • Fujii K, Hartono A, Funakawa S et al (2011) Fluxes of dissolved organic carbon in three tropical secondary forests developed on serpentine and mudstone. Geoderma 163:119–126

    Article  Google Scholar 

  • Geisseler D, Horwath WR (2009) Relationship between carbon and nitrogen availability and extracellular enzyme activities in soil. Pedobiologia 53(1):87–98

    Article  Google Scholar 

  • German DP, Weintraub MN, Grandy AS, Lauber CL et al (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397

    Article  Google Scholar 

  • Guariguata MR, Ostertag R (2001) Neotropical secondary forest succession: changes in structural and functional characteristics. For Ecol Manag 148:185–206

    Article  Google Scholar 

  • Hart SC, Stark JM, Davidson EA, Firestone MK (1994) Nitrogen mineralization, immobilization and nitrification. In: Weaver RW (ed) Methods of soil analysis, part 2: microbiological and biochemical properties. Soil Science Society of America, Madison, pp 985–1018

    Google Scholar 

  • Hedin LO, Brookshire E, Menge D, Barron A (2009) The nitrogen paradox in tropical forest ecosystems. Annu Rev Ecol Evol Syst 40:613–635

    Article  Google Scholar 

  • Herbert DA, Fownes JH (1995) Phosphorus limitation of forest leaf area and net primary production on a highly weathered soil. Biogeochemistry 29:223–235

    Article  Google Scholar 

  • Hernandez DL, Hobbie SE (2010) The effects of substrate composition, quantity, and diversity on microbial activity. Plant Soil 335(1–2):397–411

    Article  Google Scholar 

  • Houlton BZ, Sigman D, Hedin LO (2006) Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. Proc Natl Acad Sci USA 103:8745–8750

    Article  Google Scholar 

  • Ilstedt U, Singh S (2005) Nitrogen and phosphorus limitations of microbial respiration in a tropical phosphorus-fixing acrisol (ultisol) compared with organic compost. Soil Biol Biochem 37:1407–1410

    Article  Google Scholar 

  • Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647

    Article  Google Scholar 

  • Leff J, Nemergut D, Grandy A et al (2012a) The effects of soil bacterial community structure on decomposition in a tropical rain forest. Ecosystems 15:284–298

    Article  Google Scholar 

  • Leff J, Wieder W, Taylor P et al (2012b) Experimental litterfall manipulation drives large and rapid changes in soil carbon cycling in a wet tropical forest. Glob Change Biol 18:2969–2979

    Article  Google Scholar 

  • Lewis S, Lopez-Gonzalez G, Sonké B et al (2009) Increasing carbon storage in intact African tropical forests. Nature 457:1003–1006

    Article  Google Scholar 

  • Luo Y, Su B, Currie WS et al (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731

    Article  Google Scholar 

  • Malhi Y, Aragão L, Metcalfe DB et al (2009) Comprehensive assessment of carbon productivity, allocation and storage in three Amazonian forests. Glob Change Biol 15:1255–1274

    Article  Google Scholar 

  • Marklein A, Houlton B (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704

    Article  Google Scholar 

  • Martinelli L, Piccolo M, Townsend A et al (1999) Nitrogen stable isotopic composition of leaves and soil: tropical versus temperate forests. Biogeochemistry 46:45–65

    Google Scholar 

  • Mcgill WB, Cole CV (1981) Comparative aspects of cycling of organic C, N, S and P through soil organic-matter. Geoderma 26(4):267–286

    Article  Google Scholar 

  • Miettinen J, Shi C, Liew SC (2012) Two decades of destruction in Southeast Asia’s peat swamp forests. Front Ecol Environ 10:124–128

    Article  Google Scholar 

  • Montano NM, García-Oliva F, Jaramillo VJ (2007) Dissolved organic carbon affects soil microbial activity and nitrogen dynamics in a Mexican tropical deciduous forest. Plant Soil 295:265–277

    Article  Google Scholar 

  • Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76(2):151–174

    Article  Google Scholar 

  • Murty D, Kirschbaum M, Mcmurtrie R, Mcgilvray H (2002) Does conversion of forest to agricultural land change soil carbon and nitrogen? A review of the literature. Glob Change Biol 8:105–123

    Article  Google Scholar 

  • Nardoto GB, Ometto JPHB, Ehleringer JR et al (2008) Understanding the influences of spatial patterns on N availability within the Brazilian amazon forest. Ecosystems 11:1234–1246

    Article  Google Scholar 

  • Nemani RR, Keeling CD, Hashimoto H et al (2003) Climate-driven increases in global terrestrial net primary production from 1982 to 1999. Science 300:1560–1563

    Article  Google Scholar 

  • Nemergut DR, Cleveland CC, Wieder WR, Washenberger CL, Townsend AR (2010) Plot-scale manipulations of organic matter inputs to soils correlate with shifts in microbial community composition in a lowland tropical rain forest. Soil Biol Biochem 42(12):2153–2160

    Article  Google Scholar 

  • Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49(2):175–190

    Article  Google Scholar 

  • Parton W, Silver WL, Burke IC et al (2007) Global-scale similarities in nitrogen release patterns during long-term decomposition. Science 315(5814):361–364

    Article  Google Scholar 

  • Pendall E, Bridgham S, Hanson PJ et al (2004) Below-ground process responses to elevated CO2 and temperature: a discussion of observations, measurement methods, and models. New Phytol 162:311–322

    Article  Google Scholar 

  • Posada JM, Schuur EAG (2011) Relationships among precipitation regime, nutrient availability, and carbon turnover in tropical rain forests. Oecologia 165:783–795

    Article  Google Scholar 

  • Randerson JT, Hoffman FM, Thornton PE et al (2009) Systematic assessment of terrestrial biogeochemistry in coupled climate-carbon models. Glob Change Biol 15:2462–2484

    Article  Google Scholar 

  • Reed SC, Cleveland CC, Townsend AR (2007) Controls over leaf litter and soil nitrogen fixation in two lowland tropical rain forests. Biotropica 39:585–592

    Article  Google Scholar 

  • Reed SC, Vitousek PM, Cleveland CC (2010) Are patterns in nutrient limitation belowground consistent with those aboveground: results from a 4 million year chronosequence. Biogeochemistry 106:323–336

    Article  Google Scholar 

  • Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101:11001–11006

    Article  Google Scholar 

  • Reich PB, Hobbie SE, Lee T et al (2006) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440:922–925

    Article  Google Scholar 

  • Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34(9):1309–1315

    Article  Google Scholar 

  • Sanchez PA, Bandy DE, Villachica JH, Nicholaides JJ (1982) Amazon basin soils: management for continuous crop production. Science 216:821–827

    Article  Google Scholar 

  • Sayer EJ, Joseph Wright S, Tanner EVJ et al (2012) Variable responses of lowland tropical forest nutrient status to fertilization and litter manipulation. Ecosystems 15:387–400

    Article  Google Scholar 

  • Silver WL, Lugo AE, Keller M (1999) Soil oxygen availability and biogeochemistry along rainfall and topographic gradients in upland wet tropical forest soils. Biogeochemistry 44(3):301–328

    Google Scholar 

  • Sinsabaugh RL, Follstad Shah JJ (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol Syst 43:313–333

    Article  Google Scholar 

  • Sinsabaugh RL, Moorhead DL (1994) Resource-allocation to extracellular enzyme-production—a model for nitrogen and phosphorus control of litter decomposition. Soil Biol Biochem 26(10):1305–1311

    Article  Google Scholar 

  • Sinsabaugh RL, Carreiro MM, Repert DA (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60(1):1–24

    Article  Google Scholar 

  • Sinsabaugh RL, Lauber C, Weintraub M et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    Google Scholar 

  • Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462(7274):795–798

    Article  Google Scholar 

  • Stursova M, Crenshaw CL, Sinsabaugh RL (2006) Microbial responses to long-term N deposition in a semiarid grassland. Microb Ecol 51:90–98

    Article  Google Scholar 

  • Stursova M, Zifčáková L, Leigh MB et al (2012) Cellulose utilisation in forest litter and soil: identification of bacterial and fungal decomposers. FEMS Microb Ecol 80:735–746

    Article  Google Scholar 

  • Taylor PG (2012) Carbon and nutrient cycling in tropical forests: climatic, hydrologic and stoichiometric controls. Dissertation. University of Colorado, Boulder

    Google Scholar 

  • Tiessen H, Moir JO (1993) Characterization of available P by sequential extraction. In: Carter MR (ed) Soil sampling and methods of analysis. Lewis Publishers, Boca Raton, pp 75–86

    Google Scholar 

  • Townsend A, Vitousek P, Holland E (1992) Tropical soils could dominate the short-term carbon cycle feedbacks to increased global temperatures. Clim Change 22:293–303

    Article  Google Scholar 

  • Townsend A, Asner G, Cleveland C (2008) The biogeochemical heterogeneity of tropical forests. Trends Ecol Evol 23:424–431

    Article  Google Scholar 

  • Treseder KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82(4):946–954

    Article  Google Scholar 

  • Turner BL, Engelbrecht BMJ (2011) Soil organic phosphorus in lowland tropical rain forests. Biogeochemistry 103:297–315

    Article  Google Scholar 

  • Turner B, Romero T (2010) Stability of hydrolytic enzyme activity and microbial phosphorus during storage of tropical rain forest soils. Soil Biol Biochem 42:459–465

    Article  Google Scholar 

  • Vitousek P, Matson P (1988) Nitrogen transformations in a range of tropical forest soils. Soil Biol Biochem 20:361–367

    Article  Google Scholar 

  • Vitousek PM, Sanford RJ (1986) Nutrient cycling in moist tropical forest. Annu Rev Ecol Syst 17:137–167

    Article  Google Scholar 

  • Waldrop MP, Zak DR, Sinsabaugh RL (2004) Microbial community response to nitrogen deposition in northern forest ecosystems. Soil Biol Biochem 36(9):1443–1451

    Article  Google Scholar 

  • Walker T, Syers J (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19

    Article  Google Scholar 

  • Wallenstein MD, Weintraub MN (2008) Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biol Biochem 40(9):2098–2106

    Article  Google Scholar 

  • Wallenstein MD, McMahon SK, Schimel JP (2009) Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Glob Change Biol 15(7):1631–1639

    Article  Google Scholar 

  • Wieder WR, Cleveland CC, Townsend AR (2009) Controls over leaf litter decomposition in wet tropical forests. Ecology 90(12):3333–3341

    Article  Google Scholar 

  • Wieder WR, Cleveland CC, Townsend AR (2011) Throughfall exclusion and leaf litter addition drive higher rates of soil nitrous oxide emissions from a lowland wet tropical forest. Glob Change Biol. doi:10.1111/j.1365-2486.2011.02426.x

    Google Scholar 

  • Wieder WR, Cleveland CC, Taylor PG et al (2012) Experimental removal and addition of leaf litter inputs reduces nitrate production and loss in a lowland tropical forest. Biogeochemistry. doi:10.1007/s10533-012-9793-1

    Google Scholar 

  • Wood T, Lawrence D, Clark D, Chazdon R (2009) Rain forest nutrient cycling and productivity in response to large-scale litter manipulation. Ecology 90:109–121

    Article  Google Scholar 

  • Wright SJ (2005) Tropical forests in a changing environment. Trends Ecol Evol 20:553–560

    Article  Google Scholar 

  • Zak DR, Holmes WE, Burton AJ, Pregitzer KS, Talhelm AF (2008) Simulated atmospheric NO3− deposition increases soil organic matter by slowing decomposition. Ecol Appl 18(8):2016–2027

    Article  Google Scholar 

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Acknowledgments

We thank F. Campos Rivera, the Organización para Estudios Tropicales (OET) and the Ministerio de Ambiente, Energia y Telecommunicaciones (MINAET) for assisting with research permits and providing logistical support in Costa Rica, Marleny Jimenez and the Drake Bay Wilderness Camp for their generous access to field sites and W. Cambronero Castro for assistance in the field. We thank A. King and S. Schmidt for their support in conducting enzyme analyses. National Science Foundation Grants (DEB-0515744 and DEB-0852916) supported this research.

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Correspondence to Samantha R. Weintraub.

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Weintraub, S.R., Wieder, W.R., Cleveland, C.C. et al. Organic matter inputs shift soil enzyme activity and allocation patterns in a wet tropical forest. Biogeochemistry 114, 313–326 (2013). https://doi.org/10.1007/s10533-012-9812-2

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