Abstract
Background and aims
Fine-root functioning is a major driver of plant growth and strongly influences the global carbon cycle. While fine-root over-yielding has been shown in the upper soil layers of mixed-species forests relative to monospecific stands, the consequences of tree diversity on fine-root growth in very deep soil layers is still unknown. Our study aimed to assess the consequences of mixing Acacia mangium and Eucalyptus grandis trees on soil exploration by roots down to the water table at 17 m depth in a tropical planted forest.
Method
Fine roots (diameter < 2 mm) were sampled in a randomized block design with three treatments: monospecific stands of Acacia mangium (100A), Eucalyptus grandis (100E), and mixed stands with 50% of each species (50A50E). Root ingrowth bags were installed at 4 depths (from 0.1 m to 6 m) in the three treatments within three different blocks, to study the fine-root production over 2 periods of 3 months.
Results
Down to 17 m depth, total fine-root biomass was 1127 g m−2 in 50A50E, 780 g m−2 in 100A and 714 g m−2 in 100E. Specific root length and specific root area were 110–150% higher in 50A50E than in 100A for Acacia mangium trees and 34% higher in 50A50E than in 100E for Eucalyptus grandis trees. Ingrowth bags showed that the capacity of fine roots to explore soil patches did not decrease down to a depth of 6 m for the two species.
Conclusions
Belowground interactions between Acacia mangium and Eucalyptus grandis trees greatly increased the exploration of very deep soil layers by fine roots, which is likely to enhance the uptake of soil resources. Mixing tree species might therefore increase the resilience of tropical planted forests through a better exploration of deep soils.






Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Adriano E, Laclau J-P, Rodrigues JD (2017) Deep rooting of rainfed and irrigated orange trees in Brazil. Trees 31:285–297
Bakker M, Jolicoeur E, Trichet P, Augusto L, Plassard C, Guinberteau J, Loustau D (2009) Adaptation of fine roots to annual fertilization and irrigation in a 13-year-old Pinus pinaster stand. Tree Physiol 29:229–238
Batjes N (2014) Total carbon and nitrogen in the soils of the world. Eur J Soil Sci 65:10–21
Battie-Laclau P, Laclau JP, Domec JC, Christina M, Bouillet JP, Cassia Piccolo M, Moraes Gonçalves JL, Krusche AV, Bouvet JM, Nouvellon Y (2014) Effects of potassium and sodium supply on drought-adaptive mechanisms in Eucalyptus grandis plantations. New Phytol 203:401–413
Bauhus J, Messier C (1999) Soil exploitation strategies of fine roots in different tree species of the southern boreal forest of eastern Canada. Can J For Res 29:260–273
Bauhus J, Khanna P, 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
Beyer F, Hertel D, Leuschner C (2013) Fine root morphological and functional traits in Fagus sylvatica and Fraxinus excelsior saplings as dependent on species, root order and competition. Plant Soil 373:143–156
Bini D, Dos Santos CA, Bouillet J-P, de Morais Goncalves JL, Cardoso EJBN (2013) Eucalyptus grandis and Acacia mangium in monoculture and intercropped plantations: evolution of soil and litter microbial and chemical attributes during early stages of plant development. Appl Soil Ecol 63:57–66
Binkley D, Campoe OC, Gspaltl M, Forrester DI (2013) Light absorption and use efficiency in forests: why patterns differ for trees and stands. For Ecol Manag 288:5–13
Blaser WJ, Shanungu GK, Edwards PJ, Venterink HO (2014) Woody encroachment reduces nutrient limitation and promotes soil carbon sequestration. Ecol Evol 4:1423–1438. https://doi.org/10.1002/ece3.1024
Bolte A, Villanueva I (2006) Interspecific competition impacts on the morphology and distribution of fine roots in European beech (Fagus sylvatica L.) and Norway spruce (Picea abies (L.) Karst.) Eur J For Res 125:15–26
Bonifas KD, Lindquist JL (2009) Effects of nitrogen supply on the root morphology of corn and velvetleaf. J Plant Nutr 32:1371–1382
Booth TH (2013) Eucalypt plantations and climate change. For Ecol Manag 301:28–34
Bouillet J-P, Laclau J-P, Gonçalves JLM, Moreira M, Trivelin P, Jourdan C, Silva E, Piccolo MC, Tsai S, Galiana A (2008) Mixed-species plantations of Acacia Mangium and Eucalyptus Grandis in Brazil: 2: nitrogen accumulation in the stands and biological N2 fixation. For Ecol Manag 255:3918–3930
Bouillet J-P, Laclau J-P, Gonçalves JLM, Voigtlaender M, Gava JL, Leite FP, Hakamada R, Mareschal L, Mabiala A, Tardy F, Levillain J, Deleporte P, Epron D, Nouvellon Y (2013) Eucalyptus and acacia tree growth over entire rotation in single- and mixed-species plantations across five sites in Brazil and Congo. For Ecol Manag 301:89–101. https://doi.org/10.1016/j.foreco.2012.09.019
Brassard BW, Chen HY, Cavard X, Jo L, Reich PB, Bergeron Y, Pare D, Yuan Z (2013) Tree species diversity increases fine root productivity through increased soil volume filling. J Ecol 101:210–219
Brunner I, Bakker MR, Björk RG, Hirano Y, Lukac M, Aranda X, Børja I, Eldhuset TD, Helmisaari H-S, Jourdan C (2013) Fine-root turnover rates of European forests revisited: an analysis of data from sequential coring and ingrowth cores. Plant Soil 362:357–372
Canham CA, Froend RH, Stock WD, Davies M (2012) Dynamics of phreatophyte root growth relative to a seasonally fluctuating water table in a Mediterranean-type environment. Oecologia 170:909–916. https://doi.org/10.1007/s00442-012-2381-1
Canham CA, Froend RH, Stock WD (2015) Rapid root elongation by phreatophyte seedlings does not imply tolerance of water table decline. Trees 29:815–824. https://doi.org/10.1007/s00468-015-1161-z
Cardinael R, Mao Z, Prieto I, Stokes A, Dupraz C, Kim JH, Jourdan C (2015) Competition with winter crops induces deeper rooting of walnut trees in a Mediterranean alley cropping agroforestry system. Plant Soil 391:219–235
Christina M, Laclau J-P, Gonçalves J, Jourdan C, Nouvellon Y, Bouillet J-P (2011) Almost symmetrical vertical growth rates above and below ground in one of the world's most productive forests. Ecosphere 2:1–10
Christina M, Nouvellon Y, Laclau J-P, Stape JL, Bouillet J-P, Lambais GR, le Maire G, Tjoelker M (2017) Importance of deep water uptake in tropical eucalypt forest. Funct Ecol 31:509–519. https://doi.org/10.1111/1365-2435.12727
da Silva EV, de Moraes Gonçalves JL, de Freitas Coelho SR, e Moreira RM, de Miranda Mello SL, 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
Derrien D, Plain C, Courty P-E, Gelhaye L, Moerdijk-Poortvliet TCW, Thomas F, Versini A, Zeller B, Koutika L-S, Boschker HTS, Epron D (2014) Does the addition of labile substrate destabilise old soil organic matter? Soil Biol Biochem 76:149–160. https://doi.org/10.1016/j.soilbio.2014.04.030
Epron D, Nouvellon Y, Mareschal L, Moreira RM, Koutika L-S, Geneste B, Delgado-Rojas JS, Laclau J-P, Sola G, Gonçalves JLM, Bouillet J-P (2013) Partitioning of net primary production in eucalyptus and acacia stands and in mixed-species plantations: two case-studies in contrasting tropical environments. For Ecol Manag 301:102–111. https://doi.org/10.1016/j.foreco.2012.10.034
Fontaine S, Barot S, Barré P, Bdioui N, Mary B, Rumpel C (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450:277–280
Forrester DI (2014) The spatial and temporal dynamics of species interactions in mixed-species forests: from pattern to process. For Ecol Manag 312:282–292
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
Freschet GT, Valverde-Barrantes OJ, Tucker CM, Craine JM, McCormack ML, Violle C, Fort F, Blackwood CB, Urban-Mead KR, Iversen CM, Bonis A, Comas LH, Cornelissen JHC, Dong M, Guo D, Hobbie SE, Holdaway RJ, Kembel SW, Makita N, Onipchenko VG, Picon-Cochard C, Reich PB, Riva EG, Smith SW, Soudzilovskaia NA, Tjoelker MG, Wardle DA, Roumet C (2017) Climate, soil and plant functional types as drivers of global fine-root trait variation. J Ecol. https://doi.org/10.1111/1365-2745.12769
Gill RA, Polley HW, Johnson HB, Anderson LJ, Maherali H, Jackson RB (2002) Nonlinear grassland responses to past and future atmospheric CO2. Nature 417:279–282
Gonçalves JLM, Alvares CA, Higa AR, Silva LD, Alfenas AC, Stahl J, de Barros Ferraz SF, de Paula Lima W, PHS B, Hubner A (2013) Integrating genetic and silvicultural strategies to minimize abiotic and biotic constraints in Brazilian eucalypt plantations. For Ecol Manag 301:6–27
Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24
IBA (2016) Brazilian tree industry. http://iba.org/images/shared/Biblioteca/IBA_RelatorioAnual2016_.pdf. Accessed 29 jan 2017
Jackson RB, Mooney H, Schulze E-D (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci 94:7362–7366
Jourdan C, Silva E, Gonçalves JLM, Ranger J, Moreira R, Laclau J-P (2008) Fine root production and turnover in Brazilian eucalyptus plantations under contrasting nitrogen fertilization regimes. For Ecol Manag 256:396–404
Keenan RJ, Reams GA, Achard F, de Freitas JV, Grainger A, Lindquist E (2015) Dynamics of global forest area: results from the FAO global forest resources assessment 2015. For Ecol Manag 352:9–20
Kell DB (2012) Large-scale sequestration of atmospheric carbon via plant roots in natural and agricultural ecosystems: why and how. Philos Trans R Soc B 367:1589–1597
Kuznetsova A, Brockhoff PB, Christensen RHB (2015) lmerTest: tests in linear mixed effects models. R package version 2.0-33. https://CRAN.Rproject.org/package=lmerTest. Accessed 10 Jul 2017
Laclau J-P, Bouillet J-P, Gonçalves J, Silva E, Jourdan C, Cunha M, Moreira M, Saint-André L, Maquère V, Nouvellon Y (2008) Mixed-species plantations of Acacia mangium and Eucalyptus grandis in Brazil: 1. Growth dynamics and aboveground net primary production. For Ecol Manag 255:3905–3917
Laclau J-P, Ranger J, de Moraes Goncalves JL, Maquere V, Krusche AV, M’Bou AT, Nouvellon Y, Saint-Andre L, Bouillet J-P, de Cassia PM (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
Laclau JP, da Silva EA, Rodrigues Lambais G, Bernoux M, le Maire G, Stape JL, Bouillet JP, Goncalves JL, Jourdan C, Nouvellon Y (2013a) Dynamics of soil exploration by fine roots down to a depth of 10 m throughout the entire rotation in Eucalyptus grandis plantations. Front Plant Sci 4:243. https://doi.org/10.3389/fpls.2013.00243
Laclau JP, Nouvellon Y, Reine C, Goncalves JL, Krushe AV, Jourdan C, le Maire G, Bouillet JP (2013b) Mixing eucalyptus and acacia trees leads to fine root over-yielding and vertical segregation between species. Oecologia 172:903–913. https://doi.org/10.1007/s00442-012-2526-2
Le Maire G, Nouvellon Y, Christina M, Ponzoni FJ, Gonçalves JLM, Bouillet J-P, Laclau J-P (2013) Tree and stand light use efficiencies over a full rotation of single-and mixed-species Eucalyptus grandis and Acacia mangium plantations. For Ecol Manag 288:31–42
Lehmann J (2003) Subsoil root activity in tree-based cropping systems. Plant Soil 255:319–331
Lei P, Scherer-Lorenzen M, Bauhus J (2012) Belowground facilitation and competition in young tree species mixtures. For Ecol Manag 265:191–200. https://doi.org/10.1016/j.foreco.2011.10.033
Ma Z, Chen HY (2016) Effects of species diversity on fine root productivity in diverse ecosystems: a global meta-analysis. Glob Ecol Biogeogr 25:1387–1396
Ma Z, Chen HY (2017) Effects of species diversity on fine root productivity increase with stand development and associated mechanisms in a boreal forest. J Ecol 105:237–245
Maeght JL, Gonkhamdee S, Clement C, Isarangkool Na Ayutthaya S, Stokes A, Pierret A (2015) Seasonal Patterns of Fine Root Production and Turnover in a Mature Rubber Tree (Hevea brasiliensis Mull. Arg.) Stand-Differentiation with Soil Depth and Implications for Soil Carbon Stocks. Front Plant Sci 6:1022. https://doi.org/10.3389/fpls.2015.01022
Makita N, Hirano Y, Mizoguchi T, Kominami Y, Dannoura M, Ishii H, Finér L, Kanazawa Y (2011) Very fine roots respond to soil depth: biomass allocation, morphology, and physiology in a broad-leaved temperate forest. Ecol Res 26:95–104
Maquere V (2008) Dynamics of mineral elements under a fast-growing eucalyptus plantation in Brazil. Implications for soil sustainability. Ph.D. Thesis, Agroparitech, Paris
Marsden C, Nouvellon Y, M’Bou AT, Saint-Andre 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
Maurice J, Laclau J-P, Re DS, de Moraes Gonçalves JL, Nouvellon Y, Bouillet J-P, Stape JL, Ranger J, Behling M, Chopart J-L (2010) Fine root isotropy in Eucalyptus grandis plantations. Towards the prediction of root length densities from root counts on trench walls. Plant Soil 334:261–275
McCormack ML, Guo D (2014) Impacts of environmental factors on fine root lifespan. Front Plant Sci 5:205
McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppalammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518. https://doi.org/10.1111/nph.13363
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739
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
Nouvellon Y, Laclau JP, Epron D, Le Maire G, Bonnefond JM, Goncalves JL, Bouillet JP (2012) Production and carbon allocation in monocultures and mixed-species plantations of Eucalyptus grandis and Acacia mangium in Brazil. Tree Physiol 32:680–695. https://doi.org/10.1093/treephys/tps041
Ostonen I, Lõhmus K, Helmisaari H-S, Truu J, Meel S (2007) Fine root morphological adaptations in scots pine, Norway spruce and silver birch along a latitudinal gradient in boreal forests. Tree Physiol 27:1627–1634
Paquette A, Messier C (2010) The role of plantations in managing the world's forests in the Anthropocene. Front Ecol Environ 8:27–34
Paula RR, Bouillet J-P, Ocheuze Trivelin PC, Zeller B, Leonardo de Moraes Gonçalves J, Nouvellon Y, Bouvet J-M, Plassard C, Laclau J-P (2015) Evidence of short-term belowground transfer of nitrogen from Acacia mangium to Eucalyptus grandis trees in a tropical planted forest. Soil Biol Biochem 91:99–108. https://doi.org/10.1016/j.soilbio.2015.08.017
Pierret A, Maeght JL, Clement C, Montoroi JP, Hartmann C, Gonkhamdee S (2016) Understanding deep roots and their functions in ecosystems: an advocacy for more unconventional research. Ann Bot. https://doi.org/10.1093/aob/mcw130
Pinheiro RC, de Deus JC, Nouvellon Y, Campoe OC, Stape JL, Aló LL, Guerrini IA, Jourdan C, Laclau J-P (2016) A fast exploration of very deep soil layers by eucalyptus seedlings and clones in Brazil. For Ecol Manag 366:143–152. https://doi.org/10.1016/j.foreco.2016.02.012
Pradier C, Hinsinger P, Laclau J-P, Bouillet J-P, Guerrini IA, Gonçalves JLM, Asensio V, Abreu-Junior CH, Jourdan C (2017) Rainfall reduction impacts rhizosphere biogeochemistry in eucalypts grown in a deep Ferralsol in Brazil. Plant Soil 414:339–354
Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine north American trees. Ecol Monogr 72:293–309
Prieto I, Roumet C, Cardinael R, Dupraz C, Jourdan C, Kim JH, Maeght JL, Mao Z, Pierret A, Portillo N (2015) Root functional parameters along a land-use gradient: evidence of a community-level economics spectrum. J Ecol 103:361–373
Radville L, McCormack ML, Post E, Eissenstat DM (2016) Root phenology in a changing climate. J Exp Bot 67:3617–3628. https://doi.org/10.1093/jxb/erw062
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 30:1192–1208
Santos FM, de Carvalho BF, dos Santos Ataíde DH, Diniz AR, Chaer GM (2016) Dynamics of aboveground biomass accumulation in monospecific and mixed-species plantations of eucalyptus and acacia on a Brazilian sandy soil. For Ecol Manag 363:86–97
Solomon S, Plattner G-K, Knutti R, Friedlingstein P (2009) Irreversible climate change due to carbon dioxide emissions. Proc Natl Acad Sci 106:1704–1709
Sun Z, Liu X, Schmid B, Bruelheide H, Bu W, Ma K (2017) Positive effects of tree species richness on fine-root production in a subtropical forest in SE-China. J Plant Ecol 10:146–157
Tchichelle SV, Epron D, Mialoundama F, Koutika LS, Harmand J-M, Bouillet J-P, Mareschal L (2017) Differences in nitrogen cycling and soil mineralisation between a eucalypt plantation and a mixed eucalypt and Acacia mangium plantation on a sandy tropical soil. South For J For Sci 79:1–8
Team R (2013) R development core team. RA Lang Environ Stat Comput 55:275–286
Voigtlaender M, Laclau J-P, de Moraes Gonçalves JL, de Cássia PM, Moreira MZ, Nouvellon Y, Ranger J, Bouillet J-P (2012) Introducing Acacia mangium trees in Eucalyptus grandis plantations: consequences for soil organic matter stocks and nitrogen mineralization. Plant Soil 352:99–111
Weemstra M, Mommer L, Visser EJ, Ruijven J, Kuyper TW, Mohren GM, Sterck FJ (2016) Towards a multidimensional root trait framework: a tree root review. New Phytol 211:1159–1169
Weemstra M, Sterck FJ, Visser EJ, Kuyper TW, Goudzwaard L, Mommer L (2017) Fine-root trait plasticity of beech (Fagus sylvatica) and spruce (Picea abies) forests on two contrasting soils. Plant Soil 415:175–188
Williams LJ, Paquette A, Cavender-Bares J, Messier C, Reich PB (2017) Spatial complementarity in tree crowns explains overyielding in species mixtures. Nat Ecol Evol 1:0063
Acknowledgements
We are truly grateful to Daise Silva Ferreira for the huge work carried out in the field and in the laboratory. We would like to thank Agence national de la recherche (Intens&fix Project ANR-2010-STRA-004-03) and São Paulo Research foundation (FAFESP, projects 2015/24911-8 and 2011/20510-8) for their financial support. The study belongs to the SOERE F-ORE-T, which is supported annually by Ecofor, Allenvi and the French National Research Infrastructure ANAEE-F (http://www.anaee-france.fr/fr/). We are grateful of the technical support of Rildo M. Moreira and the staff of Itatinga Research Station (ESALQ/USP) as well as Eder Araujo da Silva (http://www.floragroapoio.com.br).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Michael Luke McCormack.
Rights and permissions
About this article
Cite this article
Germon, A., Guerrini, I.A., Bordron, B. et al. Consequences of mixing Acacia mangium and Eucalyptus grandis trees on soil exploration by fine-roots down to a depth of 17 m. Plant Soil 424, 203–220 (2018). https://doi.org/10.1007/s11104-017-3428-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-017-3428-1



