Skip to main content

Effects of experimental and seasonal drying on soil microbial biomass and nutrient cycling in four lowland tropical forests

Abstract

Changes in precipitation represent a major effect of climate change on tropical forests, which contain some of the earth’s largest terrestrial carbon (C) stocks. Such changes are expected to influence microbes, nutrients, and the fate of C in tropical forest soils. To explore this, we assessed soil microbial biomass, potential extracellular enzyme activities, and nutrient availability in a partial throughfall exclusion experiment in four seasonal lowland tropical humid forests in Panama with wide variation in precipitation and soil fertility. We hypothesized that throughfall exclusion would reduce microbial biomass and activity and accentuate dry season soil nutrient accumulation, with larger effects in wetter, less drought-resistant forests. We observed a baseline seasonal pattern of decreased microbial biomass and increased extractable dissolved organic C (DOC), total dissolved nitrogen (TDN), nitrate (NO3), and resin-extractable phosphorus (P) in the dry season, with the strongest patterns for nitrogen (N). However, potential enzyme activities showed no consistent seasonality. In line with seasonal drying, throughfall exclusion decreased soil microbial biomass in the wet season and increased TDN and NO3, especially in the dry season. In contrast to seasonal drying, throughfall exclusion decreased DOC and did not affect resin-extractable P, but slightly decreased potential phosphatase activities. Potential enzyme activities varied among sites and sampling times, but did not explain much variation in microbial biomass or substrate availability. We conclude that reduced rainfall in tropical forests might accentuate some dry season patterns, like reductions in microbial biomass and accumulation of extractable nutrients. However, our data also suggest new patterns, like reduced inputs of DOC to soils with drying, which could have cascading effects on soil ecological function and C storage.

Resumen

Los cambios en la precipitación representan un efecto principal del cambio climático en los bosques tropicales, los cuales contienen unas de las reservas terrestriales de carbono (C) más grandes del mundo. Se proyecta que tales cambios van a influir a los microbios, los nutrientes, y el destino del C en los suelos de los bosques tropicales. Aquí evaluamos la biomasa de microbios, la actividad potencial de enzimas extracelulares, y la disponibilidad de nutrientes del suelo en un experimento de exclusión parcial de lluvia en cuatro bosques húmedos tropicales estacionales de tierras bajas en Panamá, los cuales tienen variación grande en precipitación y fertilidad del suelo. Hipotetizamos que la exclusión de lluvia reduciría la biomasa y la actividad de microbios del suelo y acentuaría la acumulación de nutrientes en el suelo, los cuales occurren durante la estación seca. También hipotetizamos que la exclusión de lluvia tendría efectos más grandes en bosques relativamente más húmedos, los cuales probablemente son menos resistentes a la sequía. Observamos que la sequía estacional fue correlacionada con una reducción en la biomasa de microbios, con aumentos de C orgánico disuelto en los suelos (DOC), y con aumentos de nitrógeno soluble (TDN), nitrato (NO3), y fósforo extraíble por resinas (P) en la estación seca, con el efecto más fuerte en nitrógeno (N). Sin embargo, las actividades de enzimas extracelulares potenciales no cambiaron consistentemente con las estaciones. La exclusión parcial de lluvia experimental disminuyó la biomasa de microbios del suelo en la estación lluviosa y aumentó el TDN y NO3, especialmente en la estación seca, similar a los patrones naturales. En contraste con la sequía estacional, la exclusión de lluvia disminuyó el DOC. La exclusión parcial de lluvia no afectó el P extraíble, pero disminuyó un poco las actividades potenciales de las fosfatasas. Las actividades potenciales de enzimas extracelulares variaron entre sitios y fechas de colección, pero no explicaron mucha variación en la biomasa de microbios o la disponibilidad de sustratos. Estos resultados indican que las reducciones de lluvia en bosques tropicales pueden acentuar algunos patrones de la estación seca, como reducciones en la biomasa de microbios y la acumulación de nutrientes extraíbles. Sin embargo, nuestros datos también sugieren nuevos patrones, como ingresos reducidos de DOC al suelo, los cuales pueden causar efectos en cascada en las funciones ecológicas y el almacenamiento de C en los suelos.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Data availability

The raw data from this project is being submitted as Online Resource 2.

Code availability

The R code used in analyzing the data is being submitted as Online Resource 3.

References

  • Aber JD, Magill A, Boone R, Melillo JM, Steudler P (1993) Plant and soil responses to chronic nitrogen additions at the Harvard Forest, Massachusetts. Ecol Appl 3:156–166

    Article  Google Scholar 

  • Aleixo I, Norris D, Hemerik L, Barbosa A, Prata E, Costa F, Poorter L (2019) Amazonian rainforest tree mortality driven by climate and functional traits. Nat Clim Change 9:384–388. https://doi.org/10.1038/s41558-019-0458-0

    Article  Google Scholar 

  • Allen K, Dupuy JM, Gei MG et al (2017) Will seasonally dry tropical forests be sensitive or resistant to future changes in rainfall regimes? Environ Res Lett 12:023001. https://doi.org/10.1088/1748-9326/aa5968

    Article  Google Scholar 

  • Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 17:937–944

    Article  Google Scholar 

  • Batterman SA, Hedin LO, van Breugel M, Ransijn J, Craven DJ, Hall JS (2013) Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502:224–227. https://doi.org/10.1038/nature12525

    Article  Google Scholar 

  • Bobbink R, Hicks K, Galloway J et al (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59

    Article  Google Scholar 

  • Boisier JP, Ciais P, Ducharne A, Guimberteau M (2015) Projected strengthening of Amazonian dry season by constrained climate model simulations. Nat Clim Change 5:656–660. https://doi.org/10.1038/NCLIMATE2658

    Article  Google Scholar 

  • Bouskill NJ, Lim HC, Borglin S, Salve R, Wood TE, Silver WL, Brodie EL (2013) Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought. ISME J 7:384–394. https://doi.org/10.1038/ismej.2012.113

    Article  Google Scholar 

  • Bouskill NJ, Wood TE, Baran R et al (2016) Belowground response to drought in a tropical forest soil. I. Changes in microbial functional potential and metabolism. Front Microbiol 7:525. https://doi.org/10.3389/fmicb.2016.00525

    Google Scholar 

  • Bouskill NJ, Wood TE, Baran R, Hao Z, Ye Z, Bowen BP, Lim HC, Nico PS, Holman H-Y, Gilbert B, Silver WL, Northen TR, Brodie EL (2016) Belowground response to drought in a tropical forest soil. II. Change in microbial function impacts carbon composition. Front Microbiol 7:323. https://doi.org/10.3389/fmicb.2016.00323

    Google Scholar 

  • Bréchet L, Courtois EA, Saint-Germain T, Janssens IA, Asensio D, Ramirez-Rojas I, Soong JL, Van Langenhove L, Verbruggen E, Stahl C (2019) Disentangling drought and nutrient effects on soil carbon dioxide and methane fluxes in a tropical forest. Front Environ Sci 7:180. https://doi.org/10.3389/fenvs.2019.00180

    Article  Google Scholar 

  • Brokaw N, Mallory EP (2017) Vegetation of the Rio Bravo Conservation and Management Area, Belize. Manomet Bird Observatory, Manomet, MA, USA, and Programme for Belize, Belize City, Belize. https://mayaforestbelize.files.wordpress.com/2016/11/vegetation-of-rio-bravo3.pdf. accessed 3 May 2022

  • 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 17:837–842

    Article  Google Scholar 

  • Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14:319–329

    Article  Google Scholar 

  • Brookshire ENJ, Gerber S, Menge DNL, Hedin LO (2012) Large losses of inorganic nitrogen from tropical rainforests suggest a lack of nitrogen limitation. Ecol Lett 15:9–16. https://doi.org/10.1111/j.1461-0248.2011.01701.x

    Article  Google Scholar 

  • Cai M, Xing S, Cheng X, Liu L, Peng X, Shang T, Han H (2021) How elemental stoichiometric ratios in microorganisms respond to thinning management in Larix principis-rupprechtti Mayr. plantations of the warm temperate zone in China. Forests 12:684. https://doi.org/10.3390/f12060684

    Article  Google Scholar 

  • Canarini A, Kiær LP, Dijkstra FA (2017) Soil carbon loss regulated by drought intensity and available substrate: a meta-analysis. Soil Biol Biochem 112:90–99. https://doi.org/10.1016/j.soilbio.2017.04.020

    Article  Google Scholar 

  • Chacon SS, Cuack DF, Khurram A, Bill M, Dietterich LH, Bouskill NJ (2022) Divergent responses of soil microorganisms to throughfall exclusion across tropical forest soils driven by soil fertility and climate history.  https://doi.org/10.1002/essoar.10510766.1

  • Chomel M, Lavallee JM, Alvarez Segura N et al (2019) Drought decreases incorporation of recent plant photosynthate into soil food webs regardless of their trophic complexity. Glob Change Biol 25:3549–3561. https://doi.org/10.1111/gcb.14754

    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 91:2313–2323

    Article  Google Scholar 

  • Condit R, Engelbrecht BMJ, Pino D, Perez R, Turner BL (2013) Species distributions in response to individual soil nutrients and seasonal drought across a community of tropical trees. Proc Natl Acad Sci USA 110:5064–5068

    Article  Google Scholar 

  • Cornejo FH, Varela A, Wright SJ (1994) Tropical forest litter decomposition under seasonal drought: nutrient release, fungi and bacteria. Oikos 70:183–190

    Article  Google Scholar 

  • Corre MD, Veldkamp E, Arnold J, Wright SJ (2010) Impact of elevated N input on soil N cycling and losses in old-growth lowland and montane forests in Panama. Ecology 91(6):1715–1729

    Article  Google Scholar 

  • Cunja HFV, Andersen KM, Lugli LF, Santana FD, Aleixo IF, Moraes AM, Garcia S, Di Ponzio R, Mendoza EO, Brum B, Rosa JS, Cordeiro AL, Portela BTT, Ribeiro G, Coelho SD, de Souza ST, Silva LS, Antonieto F, Pires M, Salomão AC, Miron AC, de Assis RL, Domingues TF, Aragão LEOC, Meir P, Camargo JL, Manzi AO, Nagy L, Mercado LM, Hartley IP, Quesada CA (2022) Direct evidence for phosphorus limitation on Amazon forest productivity. Nature 608:558–562. https://doi.org/10.1038/s41586-022-05085-2

    Article  Google Scholar 

  • Cusack DF, Ashdown D, Dietterich LH, Neupane A, Ciochina M, Turner BL (2019) Seasonal changes in soil respiration linked to soil moisture and phosphorus availability along a tropical rainfall gradient. Biogeochemistry 10:9–22. https://doi.org/10.1007/s10533-019-00602-4

    Google Scholar 

  • Cusack DF, Dietterich LH, Sulman BN (2022.) Soil respiration in four tropical forests declines with seasonal and experimental drying, contradicting model predictions for drying effects on wetter forests.  Glob Biogeochem Cycles

  • Cusack DF, Markesteijn L, Condit R, Lewis OT, Turner BL (2018) Soil carbon stocks across tropical forests of Panama regulated by base cation effects on fine roots. Biogeochemistry 137:253–266. https://doi.org/10.1007/s10533-017-0416-8

    Article  Google Scholar 

  • Deng L, Peng C, Kim D-G et al (2021) Drought effects on soil carbon and nitrogen dynamics in global natural ecosystems. Earth Sci Rev 214:103501. https://doi.org/10.1016/j.earscirev.2020.103501

    Article  Google Scholar 

  • Dietterich LH, Karpman J, Neupane A, Ciochina M, Cusack DF (2021) Carbon content of soil fractions varies with season, rainfall, and soil fertility across a lowland tropical moist forest gradient. Biogeochemistry 155:431–452. https://doi.org/10.1007/s10533-021-00836-1

    Article  Google Scholar 

  • Dong H, Zhang S, Lin J, Zhu B (2021) Responses of soil microbial biomass carbon and dissolved organic carbon to drying-rewetting cycles: a meta-analysis. CATENA 207:105610. https://doi.org/10.1016/j.catena.2021.105610

    Article  Google Scholar 

  • Eaton WD (2001) Microbial and nutrient activity in soils from three different subtropical forest habitats in Belize, Central America before and during the transition from dry to wet season. Appl Soil Ecol 16:219–227

    Article  Google Scholar 

  • Elser JJ, Dobberfuhl DR, MacKay NA, Schampel JH (1996) Organism size, life history, and N:P stoichiometry. Bioscience 46:674–684

    Article  Google Scholar 

  • Engelbrecht BMJ, Comita LS, Condit R, Kursar TA, Tyree MT, Turner BL, Hubbell SP (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447:80–82. https://doi.org/10.1038/nature05747

    Article  Google Scholar 

  • Falkowski PG, Fenchel T, Delong EF (2008) The microbial engines that drive Earth’s biogeochemical cycles. Science 320:1034–1039

    Article  Google Scholar 

  • Feng X, Porporato A, Rodriguez-Iturbe I (2013) Changes in rainfall seasonality in the tropics. Nat Clim Change 3:811–815. https://doi.org/10.1038/nclimate1907

    Article  Google Scholar 

  • Field CB (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240

    Article  Google Scholar 

  • Fisher JB, Malhi Y, Torres IC et al (2013) Nutrient limitation in rainforests and cloud forests along a 3000-m elevation gradient in the Peruvian Andes. Oecologia 172:889–902. https://doi.org/10.1007/s00442-012-2522-6

    Article  Google Scholar 

  • Gao D, Bai E, Li M, Zhao C, Yu K, Hagedorn F (2020) Responses of soil nitrogen and phosphorus cycling to drying and rewetting cycles: a meta-analysis. Soil Biol Biochem 148:107896. https://doi.org/10.1016/j.soilbio.2020.107896

    Article  Google Scholar 

  • Gomez EJ, Delgado JA, Gonzalez JM (2021) Influence of water availability and temperature on estimates of microbial extracellular enzyme activity. PeerJ 9:e10994. https://doi.org/10.7717/peerj.10994

    Article  Google Scholar 

  • Hart SC, Stark JM, Davidson EA, Firestone MK (1994) Chap. 42. Nitrogen mineralization, immobilization, and nitrification. In: Weaver RW, Angle S, Bottomley P, Bezdicek D, Smith S, Tabatabai A, Wollum A (eds) Methods of soil analysis, part 2: microbiological and biochemical properties. Soil Science Society of America Inc, New York

    Google Scholar 

  • Hartman WH, Richardson CJ (2013) Differential nutrient limitation of soil microbial biomass and metabolic quotients (qCO2): Is there a biological stoichiometry of soil microbes? PLoS ONE 8:e57127. https://doi.org/10.1371/journal.pone.0057127

    Article  Google Scholar 

  • Hedwall P-O, Bergh J, Brunet J (2017) Phosphorus and nitrogen co-limitation of forest ground vegetation under elevated anthropogenic nitrogen deposition. Oecologia 185:317–326. https://doi.org/10.1007/s00442-017-3945-x

    Article  Google Scholar 

  • Holdridge L, Grenke W, Hatheway W, Liang T, Tosi J (1971) Forest environments in tropical life zones. Pergamon Press, New York

    Google Scholar 

  • Homyak PM, Allison SD, Huxman TE, Goulden ML, Treseder KK (2017) Effects of drought manipulation on soil nitrogen cycling: a meta-analysis. J Geophys Res 122:3260–3272. https://doi.org/10.1002/2017JG004146

    Article  Google Scholar 

  • IPCC (2021) Climate change 2021: the physical science basis. In: Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C, Berger S, Caud N, Chen Y, Goldfarb L, Gomis MI, Huang M, Leitzell K, Lonnoy E, Matthews JBR, Maycock TK, Waterfield T, Yelekçi O, Yu R, Zhou B (eds) Contribution of working group I to the sixth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

    Google Scholar 

  • Jobbágy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436

    Article  Google Scholar 

  • Joetzjer E, Douville H, Delire C, Ciais P (2013) Present-day and future Amazonian precipitation in global climate models: CMIP5 versus CMIP3. Clim Dyn 41:2921–2936. https://doi.org/10.1007/s00382-012-1644-1

    Article  Google Scholar 

  • Jones D, Willett VB (2006) Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem 38:991–999. https://doi.org/10.1016/j.soilbio.2005.08.012

    Article  Google Scholar 

  • Kallenbach CM, Frey SD, Grandy AS (2016) Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat Commun 7:13630. https://doi.org/10.1038/ncomms13630

    Article  Google Scholar 

  • Kharin VV, Zwiers FW, Zhang X (2007) Changes in temperature and precipitation extremes in the IPCC ensemble of global coupled model simulations. J Clim 20:1419–1444. https://doi.org/10.1175/JCLI4066.1

    Article  Google Scholar 

  • Koehler B, Corre MD, Veldkamp E, Wullaert H, Wright SJ (2009) Immediate and long-term nitrogen oxide emissions from tropical forest soils exposed to elevated nitrogen input. Glob Change Biol 15:2049–2066. https://doi.org/10.1111/j.1365-2486.2008.01826.x

    Article  Google Scholar 

  • Kouno K, Tuchiya Y, Ando T (1995) Measurement of soil microbial biomass phosphorus by an anion exchange membrane method. Soil Biol Biochem 27:1353–1357

    Article  Google Scholar 

  • LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379. https://doi.org/10.1890/06-2057.1

    Article  Google Scholar 

  • Looby CI, Treseder KK (2018) Shifts in soil fungi and extracellular enzyme activity with simulated climate change in a tropical montane cloud forest. Soil Biol Biochem 117:87–96. https://doi.org/10.1016/j.soilbio.2017.11.014

    Article  Google Scholar 

  • Lyra A, Imbach P, Rodriguez D, Chou SC, Georgiou S, Garofolo L (2017) Projections of climate change impacts on central America tropical rainforest. Clim Change 141:93–105. https://doi.org/10.1007/s10584-016-1790-2

    Article  Google Scholar 

  • Magrin GO, Marengo JA, Boulanger J-P et al (2014) Central and South America. In: Barros VR, Field CB, Dokken DJ, Mastrandrea MD, Mach KJ, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Climate change impacts, adaptation, and vulnerability. Part B regional aspects, contribution of working group II to the fifth assessment report on the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 1499–1566

    Google Scholar 

  • Marañón-Jiménez S, Asensio D, Sardans J, Zuccarini P, Ogaya R, Mattana S, Peñuelas J (2022) Seasonal drought in Mediterranean soils mainly changes microbial C and N contents whereas chronic drought mainly impairs the capacity of microbes to retain P. Soil Biol Biochem 165:108515. https://doi.org/10.1016/j.soilbio.2021.108515

    Article  Google Scholar 

  • McLaughlin MJ, Alston AM, Martin JK (1986) Measurement of phosphorus in the soil microbial biomass: a modified procedure for field soils. Soil Biol Biochem 18:437–443

    Article  Google Scholar 

  • Meir P, Wood TE, Galbraith DR, Brando PM, Da Costa ACL, Rowland L, Ferreira LV (2015) Threshold responses to soil moisture deficit by trees and soil in tropical rain forests: Insights from field experiments. Bioscience 65(9):882–892. https://doi.org/10.1093/biosci/biv107

    Article  Google Scholar 

  • Myers RG, Thien SJ, Pierzynski GM (1999) Using an ion sink to extract microbial phosphorus from soil. Soil Sci Soc Am J 63:1229–1237

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Oliveira RS, Dawson TE, Burgess SSO, Nepstad DC (2005) Hydraulic redistribution in three Amazonian trees. Oecologia 145:354–363. https://doi.org/10.1007/s00442-005-0108-2

    Article  Google Scholar 

  • O’Connell CS, Ruan L, Silver WL (2018) Drought drives rapid shifts in tropical rainforest soil biogeochemistry and greenhouse gas emissions. Nat Commun 9:1348. https://doi.org/10.1038/s41467-018-03352-3

    Article  Google Scholar 

  • Powers JS, Vargas GG, Brodribb TJ et al (2020) A catastrophic tropical drought kills hydraulically vulnerable tree species. Glob Change Biol 26:3122–3133. https://doi.org/10.1111/gcb.15037

    Article  Google Scholar 

  • Pyke CR, Condit R, Aguilar S, Lao S (2001) Floristic composition across a climatic gradient in a neotropical lowland forest. J Veg Sci 12:553–566

    Article  Google Scholar 

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Rasse DP, Rumpel C, Dignac M-F (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–356. https://doi.org/10.1007/s11104-004-0907-y

    Article  Google Scholar 

  • Ren C, Zhao F, Shi Z et al (2017) Differential responses of soil microbial biomass and carbon-degrading enzyme activities to altered precipitation. Soil Biol Biochem 115:1–10. https://doi.org/10.1016/j.soilbio.2017.08.0

    Article  Google Scholar 

  • Rodell M, Famiglietti JS, Wiese DN et al (2018) Emerging trends in global freshwater availability. Nature 557:651–659. https://doi.org/10.1038/s41586-018-0123-1

    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 34:1309–1315

    Article  Google Scholar 

  • Schaap KJ, Fuchslueger L, Hoosbeek MR et al (2022) Litter inputs and phosphatase activity affect the temporal variability of organic phosphorus in a tropical forest soil in the Central Amazon. pp 1–19. https://doi.org/10.1007/s11104-021-05146-x

  • Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394

    Article  Google Scholar 

  • Schimel JP (2018) Life in dry soils: effects of drought on soil microbial communities and processes. Annu Rev Ecol Evol Syst 49:409–432. https://doi.org/10.1146/annurev-ecolsys-110617-062614

    Article  Google Scholar 

  • Seidel DJ, Fu Q, Randel WJ, Reichler TJ (2008) Widening of the tropical belt in a changing climate. Nat Geosci 1:21–24

    Article  Google Scholar 

  • Siebert J, Sünnemann M, Auge H et al (2019) The effects of drought and nutrient addition on soil organisms vary across taxonomic groups, but are constant across seasons. Sci Rep. https://doi.org/10.1038/s41598-018-36777-3

    Article  Google Scholar 

  • Sinsabaugh RL, Lauber CL, Weintraub MN et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264. https://doi.org/10.1111/j.1461-0248.2008.01245.x

    Article  Google Scholar 

  • Stark JM, Firestone MK (1995) Mechanisms for soil moisture effects on activity of nitrifying bacteria. Appl Environ Microbiol 61:218–221

    Article  Google Scholar 

  • Steinweg JM, Dukes JS, Wallenstein MD (2012) Modeling the effects of temperature and moisture on soil enzyme activity: Linking laboratory assays to continuous field data. Soil Biol Biochem 55:85–92. https://doi.org/10.1016/j.soilbio.2012.06.015

    Article  Google Scholar 

  • Stewart R, Stewart J, Woodring W (1980) Geologic map of the Panama Canal and vicinity. Republic of Panama

  • STRI (2021) Physical Monitoring Program. https://biogeodb.stri.si.edu/physical_monitoring/research/barrocolorado.  accessed 17 Mar 2022

  • Subke J-A, Inglima I, Cotrufo MF (2006) Trends and methodological impacts in soil CO2 efflux partitioning: a metaanalytical review. Glob Change Biol 12:921–943. https://doi.org/10.1111/j.1365-2486.2006.01117.x

    Article  Google Scholar 

  • Tanner EVJ, Vitousek PM, Cuevas E (1998) Experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecology 79:10–22

    Article  Google Scholar 

  • Tian H, Chen G, Lu C et al (2015) Global methane and nitrous oxide emissions from terrestrial ecosystems due to multiple environmental changes. Ecosyst Health Sustain 1:4. https://doi.org/10.1890/EHS14-0015.1

    Article  Google Scholar 

  • Turner BL, Engelbrecht BMJ (2011) Soil organic phosphorus in lowland tropical rain forests. Biogeochemistry 103:297–315. https://doi.org/10.1007/s10533-010-9466-x

    Article  Google Scholar 

  • Turner BL, Romero TE (2009) Short-term changes in extractable inorganic nutrients during storage of tropical rain forest soils. Soil Sci Soc Am J 73:1972. https://doi.org/10.2136/sssaj2008.0407

    Article  Google Scholar 

  • Turner BL, Brenes-Arguedas T, Condit R (2018) Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature 555:367–370. https://doi.org/10.1038/nature25789

    Article  Google Scholar 

  • Umaña MN, Condit R, Pérez R, Turner B, Wright SJ, Comita LS (2020) Shifts in taxonomic and functional composition of trees along rainfall and phosphorus gradients in central Panama. J Ecol 1:260–211. https://doi.org/10.1111/1365-2745.13442

    Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Waring BG, Hawkes CV (2015) Short-term precipitation exclusion alters microbial responses to soil moisture in a wet tropical forest. Microb Ecol 69:843–854. https://doi.org/10.1007/s00248-014-0436-z

    Article  Google Scholar 

  • Waring BG, De Guzman ME, Du DV et al (2021) Soil biogeochemistry across Central and South American tropical dry forests. Ecol Monogr 91:e01453. https://doi.org/10.1002/ecm.1453

    Article  Google Scholar 

  • Windsor DM, Rand AS, Rand WM (1990) Características de la Precipitación de la Isla de Barro Colorado. In: Leigh EG Jr, Rand AS, Windsor DM (eds) Ecología de un bosque tropical: ciclos estacionales y cambios a largo plazo. Balboa, pp 53–71

  • Wood TE, Silver WL (2012) Strong spatial variability in trace gas dynamics following experimental drought in a humid tropical forest. Glob Biogeochem Cycles 26:GB3005. https://doi.org/10.1029/2010GB004014

    Article  Google Scholar 

  • Wright SJ (2019) Plant responses to nutrient addition experiments conducted in tropical forests. Ecol Monogr 89:e01382. https://doi.org/10.1002/ecm.1382

    Article  Google Scholar 

  • Wright SJ, Cornejo FH (1990) Seasonal drought and leaf fall in a tropical forest. Ecology 71:1165–1175

    Article  Google Scholar 

  • Xie S-P, Deser C, Vecchi GA et al (2010) Global warming pattern formation: sea surface temperature and rainfall. J Clim 23:966–986. https://doi.org/10.1175/2009JCLI3329.1

    Article  Google Scholar 

  • Yavitt JB, Wright SJ (1996) Temporal patterns of soil nutrients in a Panamanian moist forest revealed by ion-exchange resin and experimental irrigation. Plant Soil 183:117–129

    Article  Google Scholar 

  • Yavitt JB, Wieder RK, Wright SJ (1993) Soil nutrient dynamics in response to irrigation of a Panamanian Tropical Forest. Biogeochemistry 19:1–25

    Article  Google Scholar 

Download references

Funding

Funding was provided by the US Department of Energy (DOE) Grant DE-SC0015898 to D. F. Cusack. We thank Alice Lin, Frida Perez, Korina Valencia, Clayton Coleman, and Maíra Oliveira Macedo for field and laboratory support, and we thank the STRI Soils Lab, especially Dayana Agudo and Aleksandra Bielnicka, for laboratory support. We thank Cynthia Kallenbach, Edzo Veldkamp, and one anonymous reviewer for thoughtful comments which substantially improved the manuscript. Assistance with the map was provided by Matt Zebrowski, cartographer, UCLA.

Author information

Authors and Affiliations

Authors

Contributions

LHD and DFC led the experimental design and approach. LHD, MB, BC, SSC, LC, ALC, EHG, AAG, EG, AH, WK, GO, JR, CT, EV, AZ, and DFC assisted with experimental construction, maintenance, and data collection. BC, EHG, AAG, EG, and EV contributed valuable local knowledge and field expertise. LHD analyzed the data and wrote the manuscript. NJB, MB, SSC, LC, ALC, AH, WK, GO, JR, CT, AZ, and DFC assisted with literature review and manuscript editing.

Corresponding author

Correspondence to Lee H. Dietterich.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Responsible Editor: Cynthia Kallenbach.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 8313 kb)

Online Resource 1. Supplementary text and tables.

Supplementary material 2 (XLSX 796 kb)

Online Resource 2. Raw data produced and analyzed in this study.

Supplementary material 3 (R 153 kb)

Online Resource 3. R code used to analyze data and make figures.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dietterich, L.H., Bouskill, N.J., Brown, M. et al. Effects of experimental and seasonal drying on soil microbial biomass and nutrient cycling in four lowland tropical forests. Biogeochemistry 161, 227–250 (2022). https://doi.org/10.1007/s10533-022-00980-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-022-00980-2

Keywords