Abstract
The consequences of diversity on belowground processes are still poorly known in tropical forests. The distributions of very fine roots (diameter <1 mm) and fine roots (diameter <3 mm) were studied in a randomized block design close to the harvest age of fast-growing plantations. A replacement series was set up in Brazil with mono-specific Eucalyptus grandis (100E) and Acacia mangium (100A) stands and a mixture with the same stocking density and 50 % of each species (50A:50E). The total fine root (FR) biomass down to a depth of 2 m was about 27 % higher in 50A:50E than in 100A and 100E. Fine root over-yielding in 50A:50E resulted from a 72 % rise in E. grandis fine root biomass per tree relative to 100E, whereas A. mangium FR biomass per tree was 17 % lower than in 100A. Mixing A. mangium with E. grandis trees led to a drop in A. mangium FR biomass in the upper 50 cm of soil relative to 100A, partially balanced by a rise in deep soil layers. Our results highlight similarities in the effects of directional resources on leaf and FR distributions in the mixture, with A. mangium leaves below the E. grandis canopy and a low density of A. mangium fine roots in the resource-rich soil layers relative to monospecific stands. The vertical segregation of resource-absorbing organs did not lead to niche complementarity expected to increase the total biomass production.
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References
Allen SC, Jose S, Nair PKR, Brecke BJ, Nkedi-Kizza P, Ramsey CL (2004) Safety-net role of tree roots: evidence from a pecan (Carya illinoensis K. Koch)-cotton (Gossypium hirsutum L.) alley cropping system in the southern United States. For Ecol Manag 192:395–407
Bauhus J, Khanna PK, Menden N (2000) Aboveground and belowground interactions in mixed plantations of Eucalyptus globulus and Acacia mearnsii. Can J For Res 30:1886–1894
Bauhus J, van Winden AP, Nicotra AB (2004) Aboveground interactions and productivity in mixed-species plantations of Acacia mearnsii and Eucalyptus globulus. Can J For Res 34:686–694
Binkley D, Senock R, Cromack KJ (2003) Phosphorus limitation on nitrogen fixation by Falcataria seedlings. For Ecol Manag 186:171–176
Brassard BW, Chen HYH, Bergeron Y, Paré D (2011) Differences in fine root productivity between mixed- and single-species stands. Funct Ecol 25:238–246
Cabral OMR, Rocha HR, Gash JHC, Ligo MAV, Freitas HC, Tatsch JD (2010) The energy and water balance of a Eucalyptus plantation in southeast Brazil. J Hydrol 388:208–216
Cairney JWG (2012) Extramatrical mycelia of ectomycorrhizal fungi as moderators of carbon dynamics in forest soil. Soil Biol Biochem 47:198–208
Callaway RW (2002) The detection of neighbors by plants. Trends Ecol Evol 17:104–105
Cardinale BJ, Wright JP, Cadotte MW, Carroll IT, Hector A, Srivastava DS, Loreau M, Weis JJ (2007) Impacts of plant diversity on biomass production increase through time because of species complementarity. Proc Natl Acad Sci USA 104:18123–18128
Cardinale BJ, Matulich KL, Hooper DU, Byrnes JE, Duffy E, Gamfeldt L, Balvanera P, O’Connor MI, Gonzalez A (2011) The functional role of producer diversity in ecosystems. Am J Bot 98:572–592
Christina M, Laclau J-P, Gonçalves JLM, Jourdan C, Nouvellon Y, Bouillet J-P (2010) Almost symmetrical vertical growth rates above and below ground in one of the world’s most productive forests. Ecosphere 2(3):1–10
Coomes DA, Grubb PJ (2000) Impact of root competition in forests and woodlands: a theoretical framework and review of experiments. Ecol Monogr 70:171–208
Forrester DI, Bauhus J, Cowie AL, Vanclay JK (2006) Mixed-species plantations of Eucalyptus with nitrogen-fixing trees: a review. For Ecol Manag 233:211–230
Forrester DI, Theiveyanathan S, Collopy JJ, Marcar NE (2010) Enhanced water use efficiency in a mixed Eucalyptus globulus and Acacia mearnsii plantation. For Ecol Manag 259:1761–1770
Fredericksen TS, Zedaker SM (1995) Fine root biomass, distribution, and production in young pine-hardwood stands. New For 10:99–110
Fridley JD (2001) The influence of species diversity on ecosystem productivity: how, where, and why? Oikos 93:514–526
Hector A, Schmid B, Beierkuhnlein C, Caldeira MC, Diemer M, Dimitrakopoulos PG, Finn JA, Freitas H, Giller PS, Good J, Harris R, Hogberg P, Huss-Danell K, Joshi J, Jumpponen A, Körner C, Leadley PW, Loreau M, Minns A, Mulder CPH, O’Donovan G, Otway SJ, Pereira JS, Prinz A, Read DJ, Scherer-Lorenzen M, Schulze ED, Siamantziouras ASD, Spehn EM, Terry AC, Troumbis AY, Woodward FI, Yachi S, Lawton JH (1999) Plant diversity and productivity experiments in European grasslands. Science 286:1123–1127
Hunt MA, Battaglia M, Davidson NJ, Unwin GL (2006) Competition between plantation Eucalyptus nitens and Acacia dealbata weeds in northeastern Tasmania. For Ecol Manag 233:260–274
Kelty MJ (2006) The role of species mixtures in plantation forestry. For Ecol Manag 233:195–204
Kueffer C, Schumacher E, Fleischmann K, Edwards PJ, Dietz H (2007) Strong below-ground competition shapes tree regeneration in invasive Cinnamomum verum forests. J Ecol 95:273–282
Laclau J-P, Ranger J, Nzila JD, Bouillet J-P, Deleporte P (2003) Nutrient cycling in a clonal stand of Eucalyptus and an adjacent savanna ecosystem in Congo. 2. Chemical composition of soil solutions. For Ecol Manag 180:527–544
Laclau J-P, Bouillet J-P, Gonçalves JLM, Silva EV, Jourdan C, Cunha MCS, Moreira MR, Saint-André L, Maquère V, Nouvellon Y, Ranger J (2008) Mixed-species plantations of Acacia mangium and Eucalyptus grandis in Brazil. 1. Growth dynamics and net primary production. For Ecol Manag 255:3905–3917
Laclau J-P, Ranger J, Gonçalves JLM, Maquère V, Krusche AV, M’Bou AT, Nouvellon Y, Saint-André L, Bouillet J-P, Piccolo CM, Deleporte P (2010) Biogeochemical cycles of nutrients in tropical Eucalyptus plantations: main features shown by intensive monitoring in Congo and Brazil. For Ecol Manag 259:1771–1785
le Maire G, Nouvellon Y, Christina M, Gonçalves JLM, Bouillet JP, Laclau JP (2012) Tree and stand light use efficiencies over a full rotation of mixed and pure Eucalyptus grandis and Acacia mangium plantations. For Ecol Manag, in press. doi:10.1016/j.foreco.2012.03.005
Lehmann J (2003) Subsoil root activity in tree-based cropping systems. Plant Soil 255:319–331
Lehmann J, Peter I, Steglich C, Gebauer G, Huwed B, Zech W (1998) Below-ground interactions in dryland agroforestry. For Ecol Manag 111:157–169
Lei P, Scherer-Lorenzen M, Bauhus J (2012) Belowground facilitation and competition in young tree species mixtures. For Ecol Manag 265:191–200
Leuschner C, Hertel D, Coners H, Büttner V (2001) Root competition between beech and oak: a hypothesis. Oecologia 126:276–284
Lilienfein J, Wilcke W, Ayarza MA, Vilela L, Lima SC, Zech W (2000) Soil acidification in Pinus caribaea forests on Brazilian savanna oxisols. For Ecol Manag 128:145–157
Luyssaert S et al (2007) CO2 balance of boreal, temperate, and tropical forests derived from a global database. Glob Change Biol 13:2509–2537
Maier CA, Albaugh TJ, Allen HL, Dougherty PM (2004) Respiratory carbon use and carbon storage in mid-rotation loblolly pine (Pinus taeda L) plantations: the effect of site resources on the stand carbon balance. Glob Change Biol 10:1335–1350
Marquard E, Weigelt A, Temperton VM, Roscher C, Schumacher J, Buchman N, Fischer M, Weisser W, Schmid I (2009) Plant species richness and functional composition drive overyielding in a six-year grassland experiment. Ecology 90:3290–3302
Marsden C, Nouvellon Y, Thongo A, Saint-André L, Jourdan C, Kinana A, Epron D (2008) Two independent estimations of stand-level root respiration on clonal Eucalyptus stands in Congo: up scaling of direct measurements on roots versus the trenched-plot technique. New Phytol 177:676–687
Meinen C, Hertel D, Leuschner C (2009) Biomass and morphology of fine roots in temperate broad-leaved forests differing in tree species diversity: is there evidence of below-ground overyielding? Oecologia 161:99–111
Moreno G, Obrador JJ, Cubera E, Dupraz C (2005) Fine root distribution in Dehesas of Central–Western Spain. Plant Soil 277:153–162
Mulia R, Dupraz C (2006) Unusual fine root distributions of two deciduous tree species in southern France: what consequences for modelling of tree root dynamics? Plant Soil 281:71–85
Newman EI (1973) Competition and diversity in herbaceous vegetation. Nature 244:310
Nouvellon Y, Epron D, Kinana A, Mabiala A, D’Annunzio R, Deleporte P, Saint-André L, Marsden C, Roupsard O, Bouillet J-P, Hamel O, Laclau J-P (2008) Soil CO2 efflux and soil carbon balance following savannah afforestation in Congo: comparison of two site preparation treatments. For Ecol Manag 255:1926–1936
Nouvellon Y, Stape JL, Le Maire G, Epron D, Gonçalves JLM, Bonnefond JM, Campoe O, Loos R, Chavez R, Bouillet J-P, Laclau J-P (2011) Factors controlling carbon and water balances on fast growing Eucalyptus plantations. Proceedings IUFRO 2011, Brazil, Improvement and culture of Eucalypts, pp 43–46
Nouvellon Y, Laclau J-P, Epron D, le Maire G, Bonnefond J-M, Gonçalves JLM, Bouillet J-P (2012) Carbon allocations throughout the development of monospecific and mixed-species plantations of Eucalyptus grandis and Acacia mangium in Brazil. Tree Physiol 32:680–695
Paquette A, Messier C (2011) The effect of biodiversity on tree productivity: from temperate to boreal forests. Glob Ecol Biogeogr 20:170–180
Pretzsch H, Schütze G (2009) Transgressive overyielding in mixed compared with pure stands of Norway spruce and European beech in Central Europe: evidence on stand level and explanation on individual tree level. Eur J For Res 128:183–204
Rewald B, Leuschner C (2009) Belowground competition in a broad-leaved temperate mixed forest: pattern analysis and experiments in a four-species stand. Eur J For Res 128:387–398
Richards AE, Forrester DI, Bauhus J, Scherer-Lorenzen M (2010) The influence of mixed tree plantations on the nutrition of individual species: a review. Tree Physiol 30:1992–1208
Schenk HJ (2006) Root competition: beyond resource depletion. J Ecol 94:725–739
Schmid I (2002) The influence of soil type and interspecific competition on the fine root system of Norway spruce and European beech. Basic Appl Ecol 3:339–346
Schmid I, Kazda M (2002) Root distributions in monospecific and mixed stands on different soils. For Ecol Manag 159:37–47
Schume H, Jost G, Hager H (2004) Soil water depletion and recharge patterns in mixed and pure forest stands of European beech and Norway spruce. J Hydrol 289:258–274
Silva EV, Gonçalves JLM, Coelho SRF, Moreira RM, Mello SLM, Bouillet J-P, Jourdan C, Laclau J-P (2009) Dynamics of fine root distribution after establishment of monospecific and mixed-species plantations of Eucalyptus grandis and Acacia mangium. Plant Soil 325:305–318
Silva EV, Bouillet J-P, Gonçalves JLM, Abreu Junior CA, Trivelin PCO, Hinsinger P, Jourdan C, Nouvellon Y, Stape JL, Laclau J-P (2011) Functional specialization of Eucalyptus fine roots: contrasting potential uptake rates for nitrogen, potassium and calcium tracers at varying soil depths. Funct Ecol 25:996–1006
Stape JL, Binkley D, Ryan MG, Fonseca S, Loos RA, Takahashi EN, Silva CR, Silva SR, Hakamada RE, Ferreira JMA, Lima AMN, Gava JL, Leite FP, Andrade HB, Alves JM, Silva GGC, Azevedo MR (2010) The Brazil Eucalyptus potential productivity project: influence of water, nutrients and stand uniformity on wood production. For Ecol Manag 259:1684–1694
Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:718–720
Vilà M, Vayreda J, Gracia C, Ibañez JJ (2003) Does tree diversity increase wood production in pine forests? Oecologia 135:299–303
Wang XL, Klinka K, Chen HYH, de Montigny L (2002) Root structure of western hemlock and western redcedar in single- and mixed-species stands. Can J For Res 32:997–1004
Warren J, Topping C, James P (2009) A unifying evolutionary theory for the biomass–diversity–fertility relationship. Theor Ecol 2:119–126
Acknowledgments
Our thanks to Agence Nationale de la Recherche (Intens&fix, ANR-2010-STRA-004), FAPESP Thematic Project (2010/16623-9), CIRAD (ATP Neucapalm), the USP-COFECUB project (No. 22193PA), and the European Integrated Project Ultra Low CO2 Steelmaking (ULCOS-Contract n515960) for their financial support. We thank EMBRAPA-Agrobiologia for providing selected Rhyzobium strains and the entire staff of the Itatinga experimental station for field measurements. We are particularly grateful to Rildo Moreira e Moreira (ESALQ) and Eder Araujo da Silva (http://www.floragroapoio.com.br) for their contribution to this study, as well as to Peter Biggins (CIRAD) for the revision of the English.
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Communicated by Christian Koerner.
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Laclau, JP., Nouvellon, Y., Reine, C. et al. Mixing Eucalyptus and Acacia trees leads to fine root over-yielding and vertical segregation between species. Oecologia 172, 903–913 (2013). https://doi.org/10.1007/s00442-012-2526-2
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DOI: https://doi.org/10.1007/s00442-012-2526-2