Soil microbial nutrient constraints along a tropical forest elevation gradient: a belowground test of a biogeochemical paradigm

Abstract. Aboveground primary productivity is widely considered to be limited by phosphorus (P) availability in lowland tropical forests and by nitrogen (N) availability in montane tropical forests. However, the extent to which this paradigm applies to belowground processes remains unresolved. We measured indices of soil microbial nutrient status in lowland, sub-montane and montane tropical forests along a natural gradient spanning 3400 m in elevation in the Peruvian Andes. With increasing elevation there were marked increases in soil concentrations of total N, total P, and readily exchangeable P, but a decrease in N mineralization determined by in situ resin bags. Microbial carbon (C) and N increased with increasing elevation, but microbial C : N : P ratios were relatively constant, suggesting homeostasis. The activity of hydrolytic enzymes, which are rich in N, decreased with increasing elevation, while the ratio of enzymes involved in the acquisition of N and P increased with increasing elevation, further indicating an increase in the relative demand for N compared to P with increasing elevation. We conclude that soil microorganisms shift investment in nutrient acquisition from P to N between lowland and montane tropical forests, suggesting that different nutrients regulate soil microbial metabolism and the soil carbon balance in these ecosystems.

[1]  Y. Malhi,et al.  Climate Warming and Soil Carbon in Tropical Forests: Insights from an Elevation Gradient in the Peruvian Andes , 2015, Bioscience.

[2]  Wenhao Yu,et al.  Supplementary material , 2015 .

[3]  A. Austin,et al.  Microbial community composition explains soil respiration responses to changing carbon inputs along an Andes-to-Amazon elevation gradient , 2014, The Journal of ecology.

[4]  Y. Malhi,et al.  Gross Primary Productivity of a High Elevation Tropical Montane Cloud Forest , 2014, Ecosystems.

[5]  Roberta E. Martin,et al.  Landscape-scale changes in forest structure and functional traits along an Andes-to-Amazon elevation gradient , 2013 .

[6]  Mollie E. Brooks,et al.  A direct test of nitrogen and phosphorus limitation to net primary productivity in a lowland tropical wet forest. , 2013, Ecology.

[7]  Benjamin L Turner,et al.  Root and arbuscular mycorrhizal mycelial interactions with soil microorganisms in lowland tropical forest. , 2013, FEMS microbiology ecology.

[8]  Y. Malhi,et al.  New views on “old” carbon in the Amazon River: Insight from the source of organic carbon eroded from the Peruvian Andes , 2013 .

[9]  C. Richardson,et al.  Differential Nutrient Limitation of Soil Microbial Biomass and Metabolic Quotients (qCO2): Is There a Biological Stoichiometry of Soil Microbes? , 2013, PloS one.

[10]  R. Sinsabaugh,et al.  Soil enzymes in a changing environment: Current knowledge and future directions , 2013 .

[11]  Benjamin L Turner,et al.  The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest , 2013, Biogeochemistry.

[12]  Benjamin L Turner,et al.  Soil microbial biomass and the fate of phosphorus during long-term ecosystem development , 2012, Plant and Soil.

[13]  J. Dukes,et al.  Modeling the effects of temperature and moisture on soil enzyme activity: Linking laboratory assays to continuous field data , 2012 .

[14]  Joshua B. Fisher,et al.  Nutrient limitation in rainforests and cloud forests along a 3,000-m elevation gradient in the Peruvian Andes , 2012, Oecologia.

[15]  M. Silman,et al.  Diurnal, seasonal, and altitudinal trends in microclimate across a tropical montane cloud forest , 2012 .

[16]  M. Silman,et al.  Intra- and interspecific tree growth across a long altitudinal gradient in the Peruvian Andes. , 2012, Ecology.

[17]  B. Waring A Meta-analysis of Climatic and Chemical Controls on Leaf Litter Decay Rates in Tropical Forests , 2012, Ecosystems.

[18]  Benjamin L Turner,et al.  Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition , 2012 .

[19]  E. Veldkamp,et al.  Nitrogen availability links forest productivity, soil nitrous oxide and nitric oxide fluxes of a tropical montane forest in southern Ecuador , 2011 .

[20]  P. Hietz,et al.  Long-Term Change in the Nitrogen Cycle of Tropical Forests , 2011, Science.

[21]  Stephen Porder,et al.  Relationships among net primary productivity, nutrients and climate in tropical rain forest: a pan-tropical analysis. , 2011, Ecology letters.

[22]  R. B. Jackson,et al.  A Large and Persistent Carbon Sink in the World’s Forests , 2011, Science.

[23]  Michael Kaspari,et al.  Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. , 2011, Ecology.

[24]  W. McDowell,et al.  Effects of nitrogen additions on above- and belowground carbon dynamics in two tropical forests , 2011 .

[25]  Y. Malhi,et al.  Upslope migration of Andean trees , 2011 .

[26]  Sarah D Burton,et al.  Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. , 2011, Ecology.

[27]  Y. Malhi,et al.  The sensitivity of tropical leaf litter decomposition to temperature: results from a large-scale leaf translocation experiment along an elevation gradient in Peruvian forests. , 2011, The New phytologist.

[28]  S. Hättenschwiler,et al.  Leaf traits and decomposition in tropical rainforests: revisiting some commonly held views and towards a new hypothesis. , 2011, The New phytologist.

[29]  J. Elser,et al.  The origins of the Redfield nitrogen-to-phosphorus ratio are in a homoeostatic protein-to-rRNA ratio. , 2011, Ecology letters.

[30]  James W. C. White,et al.  Multi-element regulation of the tropical forest carbon cycle , 2011 .

[31]  S. Reed,et al.  Phosphorus Cycling in Tropical Forests Growing on Highly Weathered Soils , 2011 .

[32]  S. Porder,et al.  Linking chronosequences with the rest of the world: predicting soil phosphorus content in denuding landscapes , 2011 .

[33]  Y. Malhi,et al.  Temporal variation and climate dependence of soil respiration and its components along a 3000 m altitudinal tropical forest gradient , 2010 .

[34]  Luiz E. O. C. Aragão,et al.  Net primary productivity allocation and cycling of carbon along a tropical forest elevational transect in the Peruvian Andes , 2010 .

[35]  F. Woodward,et al.  Terrestrial Gross Carbon Dioxide Uptake: Global Distribution and Covariation with Climate , 2010, Science.

[36]  E. Veldkamp,et al.  Impact of elevated N input on soil N cycling and losses in old-growth lowland and montane forests in Panama. , 2010, Ecology.

[37]  A. Arneth,et al.  Variations in chemical and physical properties of Amazon forest soils in relation to their genesis , 2010 .

[38]  B. Hill,et al.  Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment , 2010, Nature.

[39]  S. Allison,et al.  Evolutionary-Economic Principles as Regulators of Soil Enzyme Production and Ecosystem Function , 2010 .

[40]  Stephen Porder,et al.  Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. , 2010, Ecological applications : a publication of the Ecological Society of America.

[41]  Patrick Meir,et al.  Altitudinal variation in leaf mass per unit area, leaf tissue density and foliar nitrogen and phosphorus content along an Amazon-Andes gradient in Peru , 2009 .

[42]  Alexander R. Barron,et al.  The Nitrogen Paradox in Tropical Forest Ecosystems , 2009 .

[43]  O. Phillips,et al.  Above- and below-ground net primary productivity across ten Amazonian forests on contrasting soils , 2009 .

[44]  R. Dudley,et al.  Sodium shortage as a constraint on the carbon cycle in an inland tropical rainforest , 2009, Proceedings of the National Academy of Sciences.

[45]  J. Elser,et al.  Shifts in Lake N:P Stoichiometry and Nutrient Limitation Driven by Atmospheric Nitrogen Deposition , 2009, Science.

[46]  Benjamin L Turner,et al.  Short‐Term Changes in Extractable Inorganic Nutrients during Storage of Tropical Rain Forest Soils , 2009 .

[47]  E. Veldkamp,et al.  Soil N cycling in old-growth forests across an Andosol toposequence in Ecuador , 2009 .

[48]  S. Allison,et al.  Stoichiometry of soil enzyme activity at global scale. , 2008, Ecology letters.

[49]  J. Libarkin,et al.  Rise of the Andes , 2008, Science.

[50]  Michael Kaspari,et al.  Multiple nutrients limit litterfall and decomposition in a tropical forest. , 2007, Ecology letters.

[51]  Helmut Hillebrand,et al.  Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. , 2007, Ecology letters.

[52]  C. Körner The use of 'altitude' in ecological research. , 2007, Trends in ecology & evolution.

[53]  C. Cleveland,et al.  C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? , 2007 .

[54]  Benjamin L Turner,et al.  Changes in enzyme activities and soil microbial community composition along carbon and nutrient gradients at the Franz Josef chronosequence, New Zealand , 2007 .

[55]  A. Townsend,et al.  Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere , 2006, Proceedings of the National Academy of Sciences.

[56]  J. Six,et al.  Bacterial and Fungal Contributions to Carbon Sequestration in Agroecosystems , 2006 .

[57]  Ming Xu,et al.  Effects of nutrient additions on ecosystem carbon cycle in a Puerto Rican tropical wet forest , 2006 .

[58]  S. Reed,et al.  Nutrient regulation of organic matter decomposition in a tropical rain forest. , 2006, Ecology.

[59]  P. Vitousek,et al.  Responses of extracellular enzymes to simple and complex nutrient inputs , 2005 .

[60]  Kathleen C. Weathers,et al.  Influence of Tree Species on Forest Nitrogen Retention in the Catskill Mountains, New York, USA , 2005, Ecosystems.

[61]  T. Daufresne,et al.  SCALING OF C:N:P STOICHIOMETRY IN FORESTS WORLDWIDE: IMPLICATIONS OF TERRESTRIAL REDFIELD‐TYPE RATIOS , 2004 .

[62]  D. Wardle,et al.  Ecological Linkages Between Aboveground and Belowground Biota , 2004, Science.

[63]  P. Brookes,et al.  Measuring soil microbial biomass , 2004 .

[64]  J. Elser,et al.  Growth rate–stoichiometry couplings in diverse biota , 2003 .

[65]  P. Matson,et al.  NUTRIENT STATUS OF TROPICAL RAIN FORESTS INFLUENCES SOIL N DYNAMICS AFTER N ADDITIONS , 2003 .

[66]  Robert W. Sterner,et al.  Are bacteria more like plants or animals? Growth rate and resource dependence of bacterial C : N : P stoichiometry , 2003 .

[67]  Brandon K. Fornwalt,et al.  Phosphorus Limitation of Coastal Ecosystem Processes , 2003, Science.

[68]  J. Elser,et al.  Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere , 2002 .

[69]  A. Townsend,et al.  Phosphorus Limitation of Microbial Processes in Moist Tropical Forests: Evidence from Short-term Laboratory Incubations and Field Studies , 2002, Ecosystems.

[70]  P. Vitousek,et al.  EFFECTS OF SOIL NUTRIENT AVAILABILITY ON INVESTMENT IN ACQUISITION OF N AND P IN HAWAIIAN RAIN FORESTS , 2001 .

[71]  P. Vitousek,et al.  Regulation of soil phosphatase and chitinase activityby N and P availability , 2000 .

[72]  L. Nagy,et al.  Effects of nitrogen and phosphorus fertilization in a lowland evergreen rainforest. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[73]  Peter M. Vitousek,et al.  EXPERIMENTAL INVESTIGATION OF NUTRIENT LIMITATION OF FOREST GROWTH ON WET TROPICAL MOUNTAINS , 1998 .

[74]  T. Ando,et al.  Measurement of soil microbial biomass phosphorus by an anion exchange membrane method , 1995 .

[75]  F. Scatena,et al.  Tropical Montane Cloud Forests , 1995, Ecological Studies.

[76]  D. Moorhead,et al.  Resource allocation to extracellular enzyme production: A model for nitrogen and phosphorus control of litter decomposition , 1994 .

[77]  D. Wardle,et al.  A COMPARATIVE ASSESSMENT OF FACTORS WHICH INFLUENCE MICROBIAL BIOMASS CARBON AND NITROGEN LEVELS IN SOIL , 1992 .

[78]  D. J. Ross Influence of sieve mesh size on estimates of microbial carbon and nitrogen by fumigation-extraction procedures in soils under pasture , 1992 .

[79]  V. Kapos,et al.  Nitorgen and Phosphorus Fertilization Effects on Venezuelan Montane Forest Trunk Growth and Litterfall , 1992 .

[80]  G. Sparling,et al.  Estimation of soil microbial c by a fumigation-extraction method: use on soils of high organic matter content, and a reassessment of the kec-factor , 1990 .

[81]  J. Proctor,et al.  CHANGES IN SOIL NITROGEN-MINERALIZATION AND NITRIFICATION ALONG AN ALTITUDINAL TRANSECT IN TROPICAL RAIN FOREST IN COSTA RICA , 1988 .

[82]  P. Brookes,et al.  AN EXTRACTION METHOD FOR MEASURING SOIL MICROBIAL BIOMASS C , 1987 .

[83]  Robert L. Sanford,et al.  Nutrient Cycling in Moist Tropical Forest , 1986 .

[84]  P. Brookes,et al.  Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil , 1985 .

[85]  Peter M. Vitousek,et al.  Litterfall, Nutrient Cycling, and Nutrient Limitation in Tropical Forests , 1984 .

[86]  A. C. Redfield The biological control of chemical factors in the environment. , 1960, Science progress.