Advertisement

Plant and Soil

, Volume 404, Issue 1–2, pp 125–139 | Cite as

Root quality and decomposition environment, but not tree species richness, drive root decomposition in tropical forests

  • Nathaly R. Guerrero-RamírezEmail author
  • Dylan Craven
  • Christian Messier
  • Catherine Potvin
  • Benjamin L. Turner
  • I. Tanya Handa
Regular Article

Abstract

Background and aims

Tropical forests contribute significantly to the global carbon cycle, yet the relative importance of tree diversity on key ecosystem processes such as root decomposition remains unknown.

Methods

We examined the influence of tree species richness on root decomposition over 485 days at two sites in Panama with contrasting soil fertility. Diversity effects on decomposition rates were calculated where 1) overstory tree species richness and composition matched that occurring inside root decomposition bags and 2) where roots of contrasting species richness decomposed under a common tree overstory. In addition, we tested 27 root traits to identify those that contribute to predict root decomposition in tropical forests.

Results

Tree species richness did not affect root decomposition rates, neither when species were manipulated within bags nor with varying tree overstory richness. Root carbon quality and micronutrient concentrations such as manganese explained 47 and 81 % of the variation in decomposition rates in the fertile and infertile site, respectively, demonstrating that the relative importance of traits was modulated by the soil environment.

Conclusions

Our results suggest that root decomposition in tropical forests is mediated by root functional composition and the soil environment rather than by species richness.

Keywords

Biodiversity experiments Belowground processes Non-additive effects Nutrient cycling Functional traits Soils 

Notes

Acknowledgments

This study was made possible due to the collaboration of members of the Sardinilla Project, the Agua Salud Project, the Smithsonian Tropical Research Institute (STRI) and the Center for Forest Research (CFR). We thank Jefferson Hall for permission to work at Agua Salud and for his feedback during project development. We thank Jose Ceballos (STRI) for microscopy assistance; Jose Monteza, Santiago, Abdiel, and Lady Mancilla for field and logistical assistance (Sardinilla); Daniela Weber, Anabel Rivas and, Federico for field and logistical assistance (Agua Salud); Tania Romero, Dayana Agudo, and Luis Ramos for support in the soil lab (STRI), Bill Parsons for C, N and fibre analysis assistance (CFR) and Alain Paquette and Steven Kembel for revising earlier versions of this manuscript. This study received support from a Young Researcher’s start-up grant by the Fonds de Recherche, Nature et Technologie du Québec to ITH, NSERC Discovery grants to ITH, CM and CP and a fellowship from the Quebec Centre for Biodiversity Science to NGR.

Supplementary material

11104_2016_2828_MOESM1_ESM.docx (3.2 mb)
ESM 1 Supplementary material (DOCX 3.19 MB)

References

  1. Abraham M (2004) Spatial variation in soil organic carbon and stable carbon isotope signature in a pasture and a primary forest in Central Panamá. Departament of Geography. McGill University, Montreal, CanadaGoogle Scholar
  2. Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophonics International 11:36–42Google Scholar
  3. Adair EC, Hobbie SE, Hobbie RK (2010) Single - pool exponential decomposition models: potential pitfalls in their use in ecological studies. Ecology 91:1225–1236CrossRefPubMedGoogle Scholar
  4. Alvarez-Clare S, Kitajima K (2007) Physical defence traits enhance seedling survival of neotropical tree species. Funct Ecol 21:1044–1054CrossRefGoogle Scholar
  5. Aulen M, Shipley B, Bradley R (2012) Prediction of in situ root decomposition rates in an interspecific context from chemical and morphological traits. Ann Bot 109:287–297. doi: 10.1093/aob/mcr259 CrossRefPubMedGoogle Scholar
  6. Baldrian P, Snajdr J (2011) Lignocellulose-degrading enzymes in soils. In: Shukla G, Varma A (eds) Soil enzymology. Springer, Berlin, HeidelbergGoogle Scholar
  7. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1-48Google Scholar
  8. Birouste M, Kazakou E, Blanchard A, Roumet C (2011) Plant traits and decomposition: are the relationships for roots comparable to those for leaves? Ann Bot 1-10. doi: 10.1093/aob/mcr297
  9. Bradford MA, Warren RJ II, Baldrian P, Crowther TW, Maynard DS, Oldfield EE, Wieder WR, Wood SA, King JR (2014) Climate fails to predict wood decomposition at regional scales. Nature Climate Chahnge 4:625–630CrossRefGoogle Scholar
  10. Brandtberg P-O, Lundkvist H, Bengtsson J (2000) Changes in forest-floor chemistry caused by birch admixture in Norway spruce stands. For Ecol Manag 130:253–264CrossRefGoogle Scholar
  11. Bunker DE, DeClerck F, Bradford JC, Colwell RK, Perfecto I, Phillips OL, Sankaran M, Naeem S (2005) Species loss and aboveground carbon storage in a tropical forest. Science 310:1029–1031CrossRefPubMedGoogle Scholar
  12. Cardinale BJ, Matulich KL, Hooper DU, Byrnes JE, Duffy E, Gamfeldt L, Balvanera P, Connor MIO, Gonzalez A (2011) The functional role of producer diversity in ecosystems. Am J Bot 98:1–21CrossRefGoogle Scholar
  13. Carrasquilla LG (2005) Árboles y arbustos de Panamá. Trees and shubs of Panama. Editora Novo Art. Universidad de Panamá y Autoridad Nacional del Ambiente, PanamaGoogle Scholar
  14. Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2009) Towards a worldwide wood economics spectrum. Ecol Lett 12:351–366CrossRefPubMedGoogle Scholar
  15. Chave J, Muller-Landau HC, Baker TR, Easdale TA, Steege H, Webb CO (2006) Regional and phylogenetic variation of wood density across 2456 neotropical tree species. Ecol Appl 16:2356–2367CrossRefPubMedGoogle Scholar
  16. Coll L, Potvin C, Messier C, Delagrange S (2008) Root architecture and allocation patterns of eight native tropical species with different successional status used in open-grown mixed plantations in Panama. Trees 22:585–596CrossRefGoogle Scholar
  17. Condit R, Engelbrecht BMJ, Pino D, Perez R, Turner BL (2013) Species distributions in response to individual soil nutrients and seasonal drought acrooss a community of tropical trees. PNAS 110:5064–5068CrossRefPubMedPubMedCentralGoogle Scholar
  18. Cong W-F, van Ruijven J, van der Werf W, De Deyn GB, Mommer L, Berendse F, Hoffland E (2015) Plant species richness leaves a legacy of enhanced root litter-induced decomposition in soil. Soil Biol Biochem 80:341–348Google Scholar
  19. Coq S, Weigel J, Butenschoen O, Bonal D, Hättenschwiler S (2011) Litter composition rather than plant presence affects decomposition of tropical litter mixtures. Plant Soil 343:273–286CrossRefGoogle Scholar
  20. Cornwell WK, Cornelissen JHC, Allison SD, Baus J, Eggleton P, Preston CM, Scarff F, Weedon JT, Wirth C, Zanne AE (2009) Plant traits and wood fates across the globe: rotted, burned, or consumed? Glob Chang Biol 15:2431–2449CrossRefGoogle Scholar
  21. Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Gosoy O, Hobbie SE, Hoorens B, Kurokawa H, Pérez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, Pv B, Brovkin V, Chatain A, Callaghan TV, Díaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worlwide. Ecol Lett 11:1065–1071CrossRefPubMedGoogle Scholar
  22. Cusack DF, Chou WW, Yang WH, Harmon ME, Silver WL, Team TL (2009) Controls on long-term root and leaf litter decomposition in neotropical forests. Glob Chang Biol 15:1339–1355CrossRefGoogle Scholar
  23. Dale SE, Turner BL, Bardgett RD (2015) Isolating the effects of precipitation, soils, and litter quality on leaf litter decomposition in lowland tropical forests. Plant Soil 394:225–238CrossRefGoogle Scholar
  24. Eisenhauer N, Schadler M (2011) Inconsistent impacts of decomposer diversity on the stability of aboveground and belowground ecosystem functions. Oecologia 2:403–415CrossRefGoogle Scholar
  25. Ettema CH, Wardle DA (2002) Spatial soil ecology. Trend in Ecology & Evolution 17:177–183CrossRefGoogle Scholar
  26. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. PNAS 103:626–631Google Scholar
  27. Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249CrossRefPubMedGoogle Scholar
  28. Freschet GT, Aerts R, Cornelissen JHC (2012a) Multiple mechanisms for trait effects on litter decomposition: moving beyond home-field advantage with a new hypothesis. J Ecol 100:619–630CrossRefGoogle Scholar
  29. Freschet GT, Aerts R, Cornelissen JHC (2012b) A plant economics spectrum of litter decomposability. Funct Ecol 26:56–65CrossRefGoogle Scholar
  30. Fyles JW, Fyles IH (1993) Interaction of Douglas-fir with red alder salal foliage litter during decomposition. Can J for Res 23:358–361CrossRefGoogle Scholar
  31. García-Palacios P, McKie BG, Handa IT, Frainer A, Hättenschwiler S (2016) The importance of litter traits and decomposers for litter decomposition: a comparison of aquatic and terrestrial ecosystems within and across biomes. Functional Ecology 1–11. doi: 10.1111/1365-2435.12589
  32. Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246CrossRefGoogle Scholar
  33. Gessner MO, Swan CM, Dang CK, McKie BG, Bardgett RD, Wall DH, Hättenschwiler S (2010) Diversity meets decomposition. Trend in Ecology & Evolution 25:372–380. doi: 10.1016/j.tree.2010.01.010 CrossRefGoogle Scholar
  34. Gijsman AJ, Alarcón HF, Thomas RJ (1997) Root decomposition in tropical grasses and legume, as affected by soil texture and season. Soil Biol Biochem 29:1443–1450CrossRefGoogle Scholar
  35. Goebel M, Hobbie SE, Bulaj B, Zadworny M, Archibald DD, Oleksyn J, Reich PB, Eissenstat DM (2011) Decomposition of the finest root branching order: linking belowground dynamics to fine-root function and structure. Ecol Monogr 81:89–102Google Scholar
  36. Guo D, Xia M, Wei X, Chang W, Liu Y, Wang Z (2008) Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three chinese temperate tree species. New Phytol 180:673–683CrossRefPubMedGoogle Scholar
  37. Handa IT, Aerts R, Berendse F, Berg MP, Bruder A, Butenschoen O, Chauvet E, Gessner MO, Jabiol J, Makkonen M, McKie BG, Malmqvist B, Peeters ETHM, Scheu S, Schmid B, van Ruijven J, Vos VCA, Hättenschwiler S (2014) Consequences of biodiversity loss for litter decomposition across biomes. Nature 509:218–221Google Scholar
  38. Hansen RA, Coleman DC (1998) Litter complexity and composition are determinants of diversity and species composition of oribatid mites (acari: oribatida) in litterbags. Appl Soil Ecol 9:17–23CrossRefGoogle Scholar
  39. Hassler SK, Zimmermann B, van Breugel M, Hall J, Elsenbeer H (2011) Recovery of saturated hydraulic conductivity under secondary succession on former pasture in the humid tropics. For Ecol Manage 261:1634–1642Google Scholar
  40. Hättenschwiler S, Coq S, Barantal S, Handa IT (2011) Leaf traits and decomposition in tropical rainforests: revisiting some commonly held views and towards a new hypothesis. New Phytol 189:950–965CrossRefPubMedGoogle Scholar
  41. Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218CrossRefGoogle Scholar
  42. Healy C, Gotelli NJ, Potvin C (2008) Partitioning the effects of biodiversity and environmental heterogeneity for productivity and mortality in a tropical tree plantation. J Ecol 96:903–913Google Scholar
  43. Hobbie SE (2015) Plant species effects on nutrient cycling: revisiting litter feedbacks. Trend in Ecology & Evolution. 30:357–363CrossRefGoogle Scholar
  44. Hobbie SE, Oleksyn J, Eissenstat DM, Reich PB (2010) Fine root decomposition rates do not mirror those of leaf litter among temperate tree species. Oecologia 162:505–513CrossRefPubMedGoogle Scholar
  45. Hooper DU, Adair EC, Cardinale BJ, Byrnes JEK, Hungate BA, Matulich KL, Gonzalez A, Duffy JE, Gamfeldt L, O’Connor MI (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105–108PubMedGoogle Scholar
  46. John R, Dalling JW, Harms KE, Yavitt JB, Stallard RF, Mirabello M, Hubbell SP, Valencia R, Navarrete H, Vallejo M, Foster RB (2007) Soil nutrients influence spatial distributions of tropical tree species. PNAS 104:864–869CrossRefPubMedPubMedCentralGoogle Scholar
  47. Kaspari M, Garcia MN, Harms KE, Santana M, Wright SJ, Yavitt JB (2008) Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecol Lett 11:35–43PubMedGoogle Scholar
  48. Keller AB, Reed SC, Townsend AR, Cleveland CC (2013) Effects of canopy tree species on belowground biogeochemistry in a lowland wet tropical forest. Soil Biol Biochem 58:61–69CrossRefGoogle Scholar
  49. Kembel SW, Mueller RC (2014) Plant traits and taxonomy drive host assocations in tropical phyllosphere fungal communities. Botany 92:303–311CrossRefGoogle Scholar
  50. Kucharik CJ, Foley JA, Delire C, Fisher VA, Coe MT, Lenters JD, Young-Molling C, Ramankutty N (2000) Testing the performance of a dynamic global ecosystem model: Water balance, carbon balance, and vegetation structure. Global Biogeomical Cycles 14:795–825CrossRefGoogle Scholar
  51. Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415Google Scholar
  52. Loreau M (1998) Separating sampling and other effects in biodiversity experiments. Oikos 82:600–602CrossRefGoogle Scholar
  53. Lummer D, Scheu S, Butenschoen O (2012) Connecting litter quality, microbial community and nitrogen transfer mechanisms in decomposing litter mixtures. Oikos 121:1649–1655CrossRefGoogle Scholar
  54. Makkonen M, Berg MP, Handa IT, Hättenschwiler S, van Ruijven J, van Bodegom PM, Aerts R (2012) Highly consistent effects of plant litter identity and functional traits on decomposition across a latitudinal gradient. Ecol Lett 15:1033–1041Google Scholar
  55. Malhi Y (2012) The productivity, metabolism and carbon cycle of tropical forest vegetation. J Ecol 100:65–75CrossRefGoogle Scholar
  56. Malhi Y, Grace J (2000) Tropical forest and atmospheric carbon dioxide. Tree 15:332–337PubMedGoogle Scholar
  57. Manzoni S, Trofymow JA, Jackson RB, Porporato A (2010) Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol Monogr 80:89–106CrossRefGoogle Scholar
  58. Martens H, Hoy M, Westad F, Folkenberg D, Martens M (2001) Analysis of designed experiments by stabilised PLS Regression and jack-knifing. Chemometrics And Intelligent Laboratoy Systems 58:151–170CrossRefGoogle Scholar
  59. Mevik B-H, Wehrens R (2007) The pls package: principal component and partial least square regression in R. J Stat Softw 18:1–24Google Scholar
  60. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining r2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142CrossRefGoogle Scholar
  61. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Vegan: community ecology package. R Package Version 2:1–7Google Scholar
  62. Olson JS (1963) Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44:322–331Google Scholar
  63. Paul GS, Montagnini F, Berlyn GP, Craven DJ, van Breugel M, Hall J (2012) Foliar herbivory and leaf traits of five native tree species in a young plantation of Central Panama. New For 43:69–87Google Scholar
  64. Pérez R (2008) Árboles de los Bosques del Canal de Panamá. Instituto Smithsonian de Investigaciones Tropicales, PanamáGoogle Scholar
  65. Poorter L, McDonald I, Alarcón A, Fichtler E, Licona J-C, Peña-Claros M, Sterck F, Villegas Z, Sass-Klaassen U (2010) The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species. New Phytol 185:481–492CrossRefPubMedGoogle Scholar
  66. Potvin C, Whidden E, Moore T (2004) A case study of carbon pools under three different land - uses in Panama. Clim Chang 67:291–307CrossRefGoogle Scholar
  67. Pregitzer KS, Deforest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine north american trees. Ecol Monogr 72:293–309CrossRefGoogle Scholar
  68. Prescott CE, Grayston SJ (2013) Tree species influence on microbial communities in litter and soil: current knowledge and research needs. For Ecol Manag 309:19–27CrossRefGoogle Scholar
  69. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  70. Robinson D (2007) Implications of a large global root biomass for carbon sink estimates and for soil carbon dynamis. Proc R Soc B 274:2735–2759CrossRefGoogle Scholar
  71. Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. The ISME Journal 4:1340–1351CrossRefPubMedGoogle Scholar
  72. Scherer-Lorenzen M, Bonilla JL, Potvin C (2007) Tree species richness affects litter production and decomposition rates in a tropical biodiversity experiment. Oikos 116:2108–2124CrossRefGoogle Scholar
  73. Scherer-Lorenzen M, Potvin C, Koricheva J, Schmid B, Hector A, Bornik Z, Reynolds G, Schulze E-D (2005) The desing of experimental tree plantations for functional biodiversity research. In: Scherer-Lorenzen M, Körner C, Schulze E-D (eds) Forest diversity and function: Temperate And Boreal Systems. Springer-Verlag, Berlin HeidelbergCrossRefGoogle Scholar
  74. Schimel JP, Hättenschwiler S (2007) Nitrogen tranfer between decomposing leaves of different N status. Soil Biol Biochem 39:1428–1436CrossRefGoogle Scholar
  75. Silver WL, Miya RK (2001) Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia 129:407–419CrossRefGoogle Scholar
  76. Sitch S, Smith B, Prentice IC, Arneth A, Bondeau A, Cramer W, Kaplan JO, Levis S, Lucht W, Sykes MT, Thonicke K, Venevsky S (2003) Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model. Glob Chang Biol 9: 161–185Google Scholar
  77. Soepadmo E (1993) Tropical rain forests as carbon sinks. Chemosphere 27:1025–1039CrossRefGoogle Scholar
  78. Stewart RH, Stewart JL, Woodring WP (1980) Geological map of the Panama Canal and vicinity, Republic of Panama. Map I-1232. United States Geological Surveys, Boulder CO.Google Scholar
  79. Vaieretti MV, Díaz S, Vile D, Garnier E (2007) Two measurement methods of leaf dry matter content produce similar results in a broad range of species. Ann Bot 99:955–958Google Scholar
  80. van Breugel M, Hall JS (2008) Experimental desing of the “Agua Salud” native timber species plantation 2008. Smithsonian Tropical Research Institute and HSBC Climate Partnership, PanamaGoogle Scholar
  81. van Geffen KG, Poorter L, Sass-Klaassen U, van Logtestijn RSP, Cornelissen JHC (2010) The trait contribution to wood decomposition rates of 15 neotropical tree species. Ecology 91:3686–3697Google Scholar
  82. 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 huma-modified tropical landscape. PlosOne 8(e82433). doi: 10.1371/journal.pone.0082433
  83. Violle C, Navas M-K, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892CrossRefGoogle Scholar
  84. Vitousek PM, Sanford RL (1986) Nutrient cycling in moist tropical forest. Ann Rev Ecol Syst 17:137–167Google Scholar
  85. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH , Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304: 1629–1633Google Scholar
  86. Wardle DA, Bonner KI, Nicholson KS (1997) Biodiversity and plant litter: experimental evidence which does not support the view That Enhanced Species Richness Improves Ecosystem Function. Oikos 79:247–258CrossRefGoogle Scholar
  87. Warton DI, Duursma RA, Falster DS, Taskinen S (2012) Smart 3 - an R package for estimation and inference about allometric lines. Methods Ecol Evol 3:257–259CrossRefGoogle Scholar
  88. Yang X, Chen J (2009) Plant litter quality influences the contribution of soil fauna to litter decomposition in humud tropical forests, Southwestern China. Soil Biol Biochem 41:910–918CrossRefGoogle Scholar
  89. Zeugin F, Potvin C, Jansad J, Scherer-Lorenzen M (2010) Is tree diversity an important driver for phosphorus and nitrogen acquisition of a young tropical plantation? For Ecol Manage 260:1424–1433Google Scholar
  90. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Nathaly R. Guerrero-Ramírez
    • 1
    • 2
    • 3
    Email author
  • Dylan Craven
    • 2
    • 3
  • Christian Messier
    • 1
    • 4
  • Catherine Potvin
    • 5
    • 6
  • Benjamin L. Turner
    • 5
  • I. Tanya Handa
    • 1
  1. 1.Département des Sciences Biologiques, Center for Forest Research (CFR)Université du Québec à MontréalMontréalCanada
  2. 2.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany
  3. 3.Institute for BiologyUniversity of LeipzigLeipzigGermany
  4. 4.Département des Sciences Naturelles, ISFORTUniversité du Québec en OutaouaisGatineauCanada
  5. 5.Smithsonian Tropical Research InstituteBalboaRepublic of Panama
  6. 6.Department of BiologyMcGill UniversityMontréalCanada

Personalised recommendations