دورية أكاديمية
أعرض في EDS

Trees adjust nutrient acquisition strategies across tropical forest secondary succession.

التفاصيل البيبلوغرافية
العنوان: Trees adjust nutrient acquisition strategies across tropical forest secondary succession.
المؤلفون: Wong MY; Cary Institute of Ecosystem Studies, Millbrook, NY, 12545, USA.; Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, 06520, USA., Wurzburger N; Odum School of Ecology, University of Georgia, Athens, GA, 30602, USA., Hall JS; ForestGEO, Smithsonian Tropical Research Institute, Ancón, 0843-03092, Panama, Panama., Wright SJ; Smithsonian Tropical Research Institute, Apartado, 0843-03092, Balboa, Panama., Tang W; School of Geography and Priestley International Centre for Climate, University of Leeds, Leeds, LS2, UK., Hedin LO; Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, 08544, USA., Saltonstall K; Smithsonian Tropical Research Institute, Apartado, 0843-03092, Balboa, Panama., van Breugel M; ForestGEO, Smithsonian Tropical Research Institute, Ancón, 0843-03092, Panama, Panama.; Department of Geography, National University of Singapore, Singapore, 119077, Singapore.; Yale-NUS College, Singapore, 138527, Singapore., Batterman SA; Cary Institute of Ecosystem Studies, Millbrook, NY, 12545, USA.; Smithsonian Tropical Research Institute, Apartado, 0843-03092, Balboa, Panama.; School of Geography and Priestley International Centre for Climate, University of Leeds, Leeds, LS2, UK.
المصدر: The New phytologist [New Phytol] 2024 Jul; Vol. 243 (1), pp. 132-144. Date of Electronic Publication: 2024 May 14.
نوع المنشور: Journal Article; Meta-Analysis
اللغة: English
بيانات الدورية: Publisher: Wiley on behalf of New Phytologist Trust Country of Publication: England NLM ID: 9882884 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1469-8137 (Electronic) Linking ISSN: 0028646X NLM ISO Abbreviation: New Phytol Subsets: MEDLINE
أسماء مطبوعة: Publication: Oxford : Wiley on behalf of New Phytologist Trust
Original Publication: London, New York [etc.] Academic Press.
مواضيع طبية MeSH: Trees* , Tropical Climate* , Forests* , Phosphorus*/metabolism , Nitrogen*/metabolism , Mycorrhizae*/physiology , Nutrients*/metabolism, Plant Roots/metabolism ; Plant Roots/microbiology ; Phosphoric Monoester Hydrolases/metabolism ; Panama
مستخلص: Nutrient limitation may constrain the ability of recovering and mature tropical forests to serve as a carbon sink. However, it is unclear to what extent trees can utilize nutrient acquisition strategies - especially root phosphatase enzymes and mycorrhizal symbioses - to overcome low nutrient availability across secondary succession. Using a large-scale, full factorial nitrogen and phosphorus fertilization experiment of 76 plots along a secondary successional gradient in lowland wet tropical forests of Panama, we tested the extent to which root phosphatase enzyme activity and mycorrhizal colonization are flexible, and if investment shifts over succession, reflective of changing nutrient limitation. We also conducted a meta-analysis to test how tropical trees adjust these strategies in response to nutrient additions and across succession. We find that tropical trees are dynamic, adjusting investment in strategies - particularly root phosphatase - in response to changing nutrient conditions through succession. These changes reflect a shift from strong nitrogen to weak phosphorus limitation over succession. Our meta-analysis findings were consistent with our field study; we found more predictable responses of root phosphatase than mycorrhizal colonization to nutrient availability. Our findings suggest that nutrient acquisition strategies respond to nutrient availability and demand in tropical forests, likely critical for alleviating nutrient limitation.
(© 2024 The Authors. New Phytologist © 2024 New Phytologist Foundation.)
References: Aidar MPM, Carrenho R, Joly CA. 2004. Aspects of arbuscular mycorrhizal fungi in an atlantic forest chronosequence parque estadual turístico do Alto Ribeira (petar), SP. Biota Neotropica 4: 1–15.
Allen EB, Allen MF. 1990. The mediation of competition by mycorrhizae in successional and patchy environments. In: Grace JB, Tilman D, eds. Perspectives on plant competition. Cambridge, UK: Academic Press, 367–389.
Allen K, Fisher JB, Phillips RP, Powers JS, Brzostek ER. 2020. Modeling the carbon cost of plant nitrogen and phosphorus uptake across temperate and tropical forests. Frontiers in Forests and Global Change 3: 43.
Bachelot B, Uriarte M, Muscarella R, Forero‐Montaña J, Thompson J, McGuire K, Zimmerman J, Swenson NG, Clark JS. 2018. Associations among arbuscular mycorrhizal fungi and seedlings are predicted to change with tree successional status. Ecology 99: 607–620.
Bartoń K. 2020. MuMIn: multi‐model inference. R Package, V.1.43.17. [WWW document] URL https://CRAN.R‐project.org/package=MuMIn [accessed 26 April 2024].
Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed‐effects models using lme4. Journal of Statistical Software 67: 1–48.
Batterman SA, Hedin LO, Van Breugel M, Ransijn J, Craven DJ, Hall JS. 2013a. Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502: 224–227.
Batterman SA, Wurzburger N, Hedin LO. 2013b. Nitrogen and phosphorus interact to control tropical symbiotic N2 fixation: a test in Inga punctata. Journal of Ecology 101: 1400–1408.
Bloom AJ, Chapin FS, Mooney HA. 1985. Resource limitation in plants‐an economic analogy. Annual Review of Ecology and Systematics 16: 363–392.
Bolan NS. 1991. A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant and Soil 134: 189–207.
van Breugel M, Craven D, Lai HR, Baillon M, Turner BL, Hall JS. 2019. Soil nutrients and dispersal limitation shape compositional variation in secondary tropical forests across multiple scales. Journal of Ecology 107: 566–581.
Brienen RJW, Phillips OL, Feldpausch TR, Gloor E, Baker TR, Lloyd J, Lopez‐Gonzalez G, Monteagudo‐Mendoza A, Malhi Y, Lewis SL et al. 2015. Long‐term decline of the Amazon carbon sink. Nature 519: 344–348.
Browman MG, Tabatabai MA. 1978. Phosphodiesterase activity of soils. Soil Science Society of America Journal 42: 284–290.
Cabugao KG, Yaffar D, Stenson N, Childs J, Phillips J, Mayes MA, Yang X, Weston DJ, Norby RJ. 2021. Bringing function to structure: root–soil interactions shaping phosphatase activity throughout a soil profile in Puerto Rico. Ecology and Evolution 11: 1150–1164.
Cárate‐Tandalla D, Camenzind T, Leuschner C, Homeier J. 2018. Contrasting species responses to continued nitrogen and phosphorus addition in tropical montane forest tree seedlings. Biotropica 50: 234–245.
Chazdon R. 2016. Carbon sequestration potential of second‐growth forest regeneration in the Latin American tropics. Science Advances 333: 988–993.
Cunha HFV, Andersen KM, Lugli LF, Santana FD, Aleixo IF, Moraes AM, Garcia S, Di Ponzio R, Mendoza EO, Brum B et al. 2022. Direct evidence for phosphorus limitation on Amazon forest productivity. Nature 608: 558–562.
Davidson EA, de Carvalho CJR, Figueira AM, Ishida FY, Ometto JPHB, Nardoto GB, Sába RT, Hayashi SN, Leal EC, Vieira ICG et al. 2007. Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447: 995–998.
Davidson EA, de Carvalho CJR, Vieira ICG, De Figueiredo R, Moutinho P, Ishida FY, Santos MTP, Guerrero JB, Kalif K, Sabá RT. 2004. Nitrogen and phosphorus limitation of biomass growth in a tropical secondary forest. Ecological Applications 14: 150–163.
Davidson EA, Howarth RW. 2007. Nutrients in synergy. Nature 449: 1000–1001.
Davidson EA, Martinelli LA. 2009. Nutrient limitations to secondary forest regrowth. Geophysical Monograph Series 186: 299–309.
Delavaux CS, Smith‐Ramesh LM, Kuebbing SE. 2017. Beyond nutrients: a meta‐analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology 98: 2111–2119.
Doughty CE, Goldsmith GR, Raab N, Girardin CAJ, Farfan‐Amezquita F, Huaraca‐Huasco W, Silva‐Espejo JE, Araujo‐Murakami A, da Costa ACL, Rocha W et al. 2018. What controls variation in carbon use efficiency among Amazonian tropical forests? Biotropica 50: 16–25.
Fick SE, Hijmans RJ. 2017. WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37: 4302–4315.
Fleischer K, Rammig A, De Kauwe MG, Walker AP, Domingues TF, Fuchslueger L, Garcia S, Goll DS, Grandis A, Jiang M et al. 2019. Amazon forest response to CO2 fertilization dependent on plant phosphorus acquisition. Nature Geoscience 12: 736–741.
Freschet GT, Roumet C, Comas LH, Weemstra M, Bengough AG, Rewald B, Bardgett RD, De Deyn GB, Johnson D, Klimešová J et al. 2021. Root traits as drivers of plant and ecosystem functioning: current understanding, pitfalls and future research needs. New Phytologist 232: 1123–1158.
Friedlingstein P, O'sullivan M, Jones MW, Andrew RM, Gregor L, Hauck J, Le Quéré C, Luijkx IT, Olsen A, Peters GP et al. 2022. Global carbon budget 2022. Earth System Science Data 14: 4811–4900.
Guadarrama P, Castillo S, Ramos‐Zapata JA, Hernández‐Cuevas LV, Camargo‐Ricalde SL. 2014. Arbuscular mycorrhizal fungal communities in changing environments: the effects of seasonality and anthropogenic disturbance in a seasonal dry forest. Pedobiologia 57: 87–95.
Guariguata MR, Ostertag R. 2001. Neotropical secondary forest succession: changes in structural and functional characteristics. Forest Ecology and Management 148: 185–206.
Hart MM, Reader RJ. 2002. Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytologist 153: 335–344.
Hedges LV, Gurevitch J, Curtis PS. 1999. The meta‐analysis of response ratios in experimental ecology. Ecology 80: 1150.
Herbert DA, Williams M, Rastetter EB. 2003. A model analysis of N and P limitation on carbon accumulation in Amazonian secondary forest after alternate land‐use abandonment. Biogeochemistry 65: 121–150.
Hodge A, Fitter AH. 2010. Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proceedings of the National Academy of Sciences, USA 107: 13754–13759.
Jakobsen I, Rosendahl L. 1990. Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytologist 115: 77–83.
Johnson NC, Graham JH, Smith FA. 1997. Functioning of mycorrhizal associations along the mutualism‐parasitism continuum. New Phytologist 135: 575–585.
Kauffman JB, Cummings DL, Ward DE, Babbitt R. 1995. Fire in the Brazilian Amazon: 1. Biomass, nutrient pools, and losses in slashed primary forests. Oecologia 104: 397–408.
Koch AM, Antunes PM, Maherali H, Hart MM, Klironomos JN. 2017. Evolutionary asymmetry in the arbuscular mycorrhizal symbiosis: conservatism in fungal morphology does not predict host plant growth. New Phytologist 214: 1330–1337.
Leigh EG. 1999. Tropical forest ecology: a view from Barro Colorado Island. New York, NY, USA: Oxford University Press.
Lenth RV. 2021. emmeans: estimated marginal means, aka least‐squares means. R Package, V.1.6.1. [WWW document] URL https://CRAN.R‐project.org/package=emmeans [accessed 26 April 2024].
Levy‐Varon JH, Batterman SA, Medvigy D, Xu X, Hall JS, van Breugel M, Hedin LO. 2019. Tropical carbon sink accelerated by symbiotic dinitrogen fixation. Nature Communications 10: 5637.
Lu M, Hedin LO. 2019. Global plant–symbiont organization and emergence of biogeochemical cycles resolved by evolution‐based trait modelling. Nature Ecology & Evolution 3: 239–250.
Lynch JP, Ho MD, Phosphorus L. 2005. Rhizoeconomics: carbon costs of phosphorus acquisition. Plant and Soil 269: 45–56.
Manu R, Corre MD, Aleeje A, Mwanjalolo MJG, Babweteera F, Veldkamp E, van Straaten O. 2022. Responses of tree growth and biomass production to nutrient addition in a semi‐deciduous tropical forest in Africa. Ecology 103: 1–15.
Marklein AR, Houlton BZ. 2012. Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytologist 193: 696–704.
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA. 1990. A new method which gives an objective measure of colonization of roots by vesicular—arbuscular mycorrhizal fungi. New Phytologist 115: 495–501.
McGrath DA, Smith CK, Gholz HL, de Assis Oliveira F. 2001. Effects of land‐use change on soil nutrient dynamics in Amazônia. Ecosystems 4: 625–645.
Nagy RC, Rastetter EB, Neill C, Porder S. 2017. Nutrient limitation in tropical secondary forests following different management practices. Ecological Applications 27: 734–755.
Nasto MK, Winter K, Turner BL, Cleveland CC. 2019. Nutrient acquisition strategies augment growth in tropical N2‐fixing trees in nutrient‐poor soil and under elevated CO2. Ecology 100: e02646.
Neill C, Piccolo MC, Cerri CC, Steudler PA, Melillo JM. 2006. Soil solution nitrogen losses during clearing of lowland Amazon forest for pasture. Plant and Soil 281: 233–245.
Ogden FL, Crouch TD, Stallard RF, Hall JS. 2013. Effect of land cover and use on dry season river runoff, runoff efficiency, and peak storm runoff in the seasonal tropics of Central Panama. Water Resources Research 49: 8443–8462.
Pan Y, Birdsey RA, Fang J, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Lewis SL, Canadell JG et al. 2011. A large and persistent carbon sink in the world's forests. Science 333: 988–993.
Poorter L, Bongers F, Aide TM, Almeyda Zambrano AM, Balvanera P, Becknell JM, Boukili V, Brancalion PHS, Broadbent EN, Chazdon RL et al. 2016. Biomass resilience of Neotropical secondary forests. Nature 530: 211–214.
Poorter L, Rozendaal DMA, Bongers F, Almeida DJS, Álvarez FS, Andrade JL, Arreola Villa LF, Becknell JM, Bhaskar R, Boukili V et al. 2021. Functional recovery of secondary tropical forests. Proceedings of the National Academy of Sciences, USA 118: e2003405118.
R Core Team. 2020. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Reichert T, Rammig A, Fuchslueger L, Lugli LF, Quesada CA, Fleischer K. 2022. Plant phosphorus‐use and ‐acquisition strategies in Amazonia. New Phytologist 234: 1126–1143.
Sheldrake M, Rosenstock NP, Mangan S, Revillini D, Sayer EJ, Olsson PA, Verbruggen E, Tanner EVJ, Turner BL, Wright SJ. 2018. Responses of arbuscular mycorrhizal fungi to long‐term inorganic and organic nutrient addition in a lowland tropical forest. ISME Journal 12: 2433–2445.
Sheldrake M, Rosenstock NP, Revillini D, Olsson PA, Mangan S, Sayer EJ, Wallander H, Turner BL, Tanner EVJ. 2017. Arbuscular mycorrhizal fungal community composition is altered by long‐term litter removal but not litter addition in a lowland tropical forest. New Phytologist 214: 455–467.
Smith SE, Smith FA. 2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 62: 227–250.
Steidinger BS, Crowther TW, Liang J, Van Nuland ME, Werner GDA, Reich PB, Nabuurs G, de‐Miguel S, Zhou M, Picard N et al. 2019. Climatic controls of decomposition drive the global biogeography of forest‐tree symbioses. Nature 569: 404–408.
Sullivan BW, Nifong RL, Nasto MK, Alvarez‐Clare S, Dencker C, Soper FM, Shoemaker KT, Ishida FY, Zaragoza‐Castells J, Davidson EA et al. 2019. Biogeochemical recuperation of lowland tropical forest during succession. Ecology 100: 1–14.
Sulman BN, Shevliakova E, Brzostek ER, Kivlin SN, Malyshev S, Menge DNL, Zhang X. 2019. Diverse mycorrhizal associations enhance terrestrial C storage in a global model. Global Biogeochemical Cycles 33: 501–523.
Tabatabai MA. 1994. Soil enzymes. In: Page AL, ed. Methods of soil analysis: part 2 microbiological and biochemical properties. Madison, WI, USA: The American Society of Agronomy, 775–833.
Tang W. 2022. Will nutrients limit the tropical forest carbon sink? PhD thesis, University of Leeds, Leeds, UK.
Terrer C, Jackson RB, Prentice IC, Keenan TF, Kaiser C, Vicca S, Fisher JB, Reich PB, Stocker BD, Hungate BA et al. 2019. Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass. Nature Climate Change 9: 684–689.
Treseder KK. 2004. A meta‐analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytologist 164: 347–355.
Treseder KK. 2013. The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content. Plant and Soil 371: 1–13.
Treseder KK, Vitousek PM. 2001. Effects of soil nutrient availability on investment in acquistion of N and P in Hawaiian rain forests. Ecology 82: 946–954.
Tummers B. 2006. DataThief III. [WWW document] URL https://www.datathief.org/ [accessed 5 June 2024].
Turner BL. 2008. Resource partitioning for soil phosphorus: a hypothesis. Journal of Ecology 96: 698–702.
Turner BL, Baxter R, Ellwood NTW, Whitton BA. 2001. Characterization of the phosphatase activities of mosses in relation to their environment. Plant, Cell & Environment 24: 1165–1176.
Turner BL, Brenes‐Arguedas T, Condit R. 2018. Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature 555: 367–370.
Turner BL, Wright SJ. 2014. The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry 117: 115–130.
Turner BL, Yavitt JB, Harms KE, Garcia MN, Romero TE, Wright SJ. 2013. Seasonal changes and treatment effects on soil inorganic nutrients following a decade of fertilizer addition in a lowland tropical forest. Soil Science Society of America Journal 77: 1357–1369.
Vallicrosa H, Lugli LF, Fuchslueger L, Sardans J, Ramirez‐Rojas I, Verbruggen E, Grau O, Bréchet L, Peguero G, Van Langenhove L et al. 2023. Phosphorus scarcity contributes to nitrogen limitation in lowland tropical rainforests. Ecology 104: e4049.
Van Breugel M, Hall JS, Craven D, Bailon M, Hernandez A, Abbene M, Van Breugel P. 2013. Succession of ephemeral secondary forests and their limited role for the conservation of floristic diversity in a human‐modified tropical landscape. PLoS ONE 8: e82433.
Vicca S, Luyssaert S, Peñuelas J, Campioli M, Chapin FS, Ciais P, Heinemeyer A, Högberg P, Kutsch WL, Law BE et al. 2012. Fertile forests produce biomass more efficiently. Ecology Letters 15: 520–526.
Viechtbauer W. 2010. Conducting meta‐analyses in R with the metafor package. Journal of Statistical Software 36: 1–48.
Vitousek PM. 1984. Litterfall, nutrient cycling, and nutrient fimitation in tropical forests. Ecology 65: 285–298.
Wang YP, Houlton BZ, Field CB. 2007. A model of biogeochemical cycles of carbon, nitrogen, and phosphorus including symbiotic nitrogen fixation and phosphatase production. Global Biogeochemical Cycles 21: 1–15.
Waring BG, Pérez‐Aviles D, Murray JG, Powers JS. 2019. Plant community responses to stand‐level nutrient fertilization in a secondary tropical dry forest. Ecology 100: 1–12.
Warton DI, Hui FKC. 2011. The arcsine is asinine: the analysis of proportions in ecology. Ecology 92: 3–10.
Whiteside MD, Werner GDA, Caldas VEA, van't Padje A, Dupin SE, Elbers B, Bakker M, Wyatt GAK, Klein M, Hink MA et al. 2019. Mycorrhizal fungi respond to resource inequality by moving phosphorus from rich to poor patches across networks. Current Biology 29: 2043–2050.
Wieder WR, Cleveland CC, Smith WK, Todd‐Brown K. 2015. Future productivity and carbon storage limited by terrestrial nutrient availability. Nature Geoscience 8: 441–444.
Wright SJ. 2019. Plant responses to nutrient addition experiments conducted in tropical forests. Ecological Monographs 89: e01382.
Wright SJ, Turner BL, Yavitt JB, Harms KE, Kaspari M, Tanner EVJ, Bujan J, Griffin EA, Mayor JR, Pasquini SC et al. 2018. Plant responses to fertilization experiments in lowland, species‐rich, tropical forests. Ecology 99: 1129–1138.
Wurzburger N, Wright SJ. 2015. Fine‐root responses to fertilization reveal multiple nutrient limitation in a lowland tropical forest. Ecology 96: 2137–2146.
Yang X, Thornton PE, Ricciuto DM, Hoffman FM. 2016. Phosphorus feedbacks constraining tropical ecosystem responses to changes in atmospheric CO2 and climate. Geophysical Research Letters 43: 7205–7214.
Yavitt JB, Harms KE, Garcia MN, Mirabello MJ, Wright SJ. 2011. Soil fertility and fine root dynamics in response to 4 years of nutrient (N, P, K) fertilization in a lowland tropical moist forest, Panama. Austral Ecology 36: 433–445.
Yokoyama D, Imai N, Kitayama K. 2017. Effects of nitrogen and phosphorus fertilization on the activities of four different classes of fine‐root and soil phosphatases in Bornean tropical rain forests. Plant and Soil 416: 463–476.
Zalamea PC, Turner BL, Winter K, Jones FA, Sarmiento C, Dalling JW. 2016. Seedling growth responses to phosphorus reflect adult distribution patterns of tropical trees. New Phytologist 212: 400–408.
Zangaro W, Rostirola LV, de Souza PB, de Almeida Alves R, Lescano LEAM, Rondina ABL, Nogueira MA, Carrenho R. 2013. Root colonization and spore abundance of arbuscular mycorrhizal fungi in distinct successional stages from an Atlantic rainforest biome in southern Brazil. Mycorrhiza 23: 221–233.
معلومات مُعتمدة: Leverhulme Trust; Frank and Kristin Levinson; Heising-Simons Foundation; Hoch family; Stanley Motta; NE/M019497/1 Natural Environment Research Council; NE/N012542/1 Natural Environment Research Council; 275556724 British Council; U Trust; Carbon Mitigation Initiative, Princeton University
فهرسة مساهمة: Keywords: mycorrhizal fungi; nitrogen; nutrient acquisition strategies; nutrient limitation; phosphorus; root phosphatase; secondary succession; tropical forests
المشرفين على المادة: 27YLU75U4W (Phosphorus)
N762921K75 (Nitrogen)
EC 3.1.3.2 (Phosphoric Monoester Hydrolases)
تواريخ الأحداث: Date Created: 20240514 Date Completed: 20240606 Latest Revision: 20240607
رمز التحديث: 20240607
DOI: 10.1111/nph.19812
PMID: 38742309
قاعدة البيانات: MEDLINE
الوصف
تدمد:1469-8137
DOI:10.1111/nph.19812