Abstract
Background and Aims
To increase yield, cacao is planted increasingly in unshaded monocultures, replacing a more traditional cultivation under shade. We investigated how shade tree cover and species diversity affect the root system and its dynamics.
Methods
In a replicated study in Sulawesi (Indonesia), we studied the fine and coarse root system down to 3 m soil depth in three modern and more traditional cacao cultivation systems: unshaded cacao monoculture (Cacao-mono), cacao under either the legume Gliricidia sepium (Cacao-Gliricidia), or a diverse (> 6 species) shade tree cover (Cacao-multi). We analysed the vertical distribution of fine, large and coarse roots as well as fine root production, turnover and morphology on the species level.
Results
Stand-level fine root biomass showed a doubling with increasing shade tree cover (from 206 to 432 g m−2), but a tendency for a decrease in cacao fine root biomass. The presence of Gliricidia roots seemed to shift the cacao fine roots to a more shallow distribution, while the presence of shade tree roots in the Cacao-multi systems caused a biomass reduction and relative downward shift of the cacao roots. The turnover of cacao fine roots was much higher in the Cacao-multi stands than in the other two cultivation systems, although stand-level root production remained unchanged across the three systems. According to the stable isotope signature, Gliricidia extracted water from deeper soil layers than cacao, while no soil water partitioning was observed in the Cacao-multi stands.
Conclusions
Our data suggest that the cacao trees altered their fine root distribution patterns in response to root competition. Both interspecific competition and root system segregation seem to play an important role in cacao agroforests with different shade tree cover.
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References
Aber J, Melillo J, Nadelhoffer K (1985) Fine root turnover in forest ecosystems in relation to quantity and form of nitrogen availability: a comparison of two methods. Oecologia 66:317–321
Abou Rajab Y, Leuschner C, Barus H, Tjoa A, Hertel D (2016) Cacao cultivation under diverse shade tree cover allows high carbon storage and sequestration without yield losses. PLoS One 11:e0149949
Achard F, Eva HD, Stibig H-J, Mayaux P, Gallego J, Richards T, Malingreau J-P (2002) Determination of deforestation rates of the world’s humid tropical forests. Science 297:999–1002
Aerts R, Bakker C, De Caluwe H (1992) Root turnover as determinant of the cycling of C, N, and P in a dry heathland ecosystem. Biogeochemistry 15:175–190
Akinnifesi FK, Rowe EC, Livesley SJ, Kwesiga F, Vanlauwe B, Alegre J (2004) Tree root architecture. In: Belowground interactions in tropical agroecosystems: concepts and models with multiple plant components. CAB International, Wallingford, p 61–81
Beer J (1987) Advantages, disadvantages and desirable characteristics of shade trees for coffee, cacao and tea. Agrofor Syst 5:3–13
Beer J, Muschler R, Kass D, Somarriba E (1998) Shade management in coffee and cacao plantations. Agrofor Syst 38:139–164
Belsky J, Siebert S (2003) Cultivating cacao: implications of sun-grown cacao on local food security and environmental sustainability. Agric Hum Values 20:277–285
Bisseleua D, Missoup A, Vidal S (2009) Biodiversity conservation, ecosystem functioning, and economic incentives under cocoa agroforestry intensification. Conserv Biol 23:1176–1184
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
Defrenet E, Roupsard O, Van den Meersche K, Charbonnier F, Pérez-Molina JP, Khac E, Prieto I, Stokes A, Roumet C, Rapidel B, de Melo Virginio Filho E, Vargas VJ, Robelo D, Barquero A, Jourdan C (2016) Root biomass, turnover and net primary productivity of a coffee agroforestry system in Costa Rica: effects of soil depth, shade trees, distance to row and coffee age. Ann Bot 118:833–851
Ehleringer JR, Dawson TE (1992) Water uptake by plants: perspectives from stable isotope composition. Plant Cell Environ 15:1073–1082
Ehleringer JR, Osmond CB (1989) Stable isotopes. In: Pearcy PRRW, Ehleringer JR, Mooney HA (eds) Plant physiological ecology: field methods and instrumentation. Kluwer Academic Publishers, London, pp 281–300
Ehleringer JR, Roden J, Dawson TE (2000) Assessing ecosystem-level water relations through stable isotope ratio analyses. In: Sala OE, Jackson RB, Mooney HA, Howarth RW (eds) Methods in ecosystem science. Springer, New York, pp 181–198
Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL (2000) Building roots in a changing environment: implications for root longevity. New Phytol 147:33–42
Ewel J, Mazzarino M (2008) Competition from below for light and nutrients shifts productivity among tropical species. Proc Natl Acad Sci U S A 105:18836–18841
Freckleton RP, Watkinson AR (2001) Asymmetric competition between plant species. Funct Ecol 15:615–623
Gale MR, Grigal DF (1987) Vertical root distribution of northern tree species in relation to successional status. Can J For Res 17:829–834
Gamfeldt L, Snäll T, Bagchi R, Jonsson M, Gustafsson L, Kjellander P, Ruiz-Jaen MC, Fröberg M, Stendahl J, Philipson CD, Mikusinski G, Andersson E, Westerlund B, Andrén H, Moberg F, Moen J, Bengtsson J (2013) Higher levels of multiple ecosystem services are found in forests with more tree species. Nat Commun 4:1340
Gaul D, Hertel D, Borken W, Matzner E, Leuschner C (2008) Effects of experimental drought on the fine root system of mature Norway spruce. For Ecol Manag 256:1151–1159
Gehre M, Geilmann H, Richter J, Werner RA, Brand WA (2004) Continuous flow 2H/1H and 18O/ 16O analysis of water samples with dual inlet precision. Rapid Commun Mass Spectrom 18:2650–2660
Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova SA, Tyukavina A, Thau D, Stehman SV, Goetz SJ, Loveland TR, Kommareddy A, Egorov A, Chini L, Justice CO, Townshend JRG (2013) High-resolution global maps of 21st-century forest cover change. Science 342:850–853
Harteveld M, Hertel D, Wiens M, Leuschner C (2007) Spatial and temporal variability of fine root abundance and growth in tropical moist forests and agroforestry systems (Sulawesi, Indonesia). Ecotropica 13:111–120
Hertel D, Leuschner C (2002) A comparison of four different fine root production estimates with ecosystem carbon balance data in a Fagus–Quercus mixed forest. Plant Soil 239:237–251
Hertel D, Leuschner C, Harteveld M, Wiens M (2007) Fine root mass, distribution and regeneration in disturbed primary forests and secondary forests of the moist tropics. In: Tscharntke T, Leuschner C, Zeller M, Guhardja E, Bidin A (eds) The stability of tropical rainforest margins: linking ecological, economic and social constraints of land use and conservation. Springer Verlag, Berlin, pp 89–108
Isaac ME, Anglaaere LCN, Borden K, Adu-Bredu S (2014) Intraspecific root plasticity in agroforestry systems across edaphic conditions. Agric Ecosyst Environ 185:16–23
John B, Pandey HN, Tripathi RS (2001) Vertical distribution and seasonal changes of fine and coarse root mass in Pinus kesiya royle ex.Gordon forest of three different ages. Acta Oecol 22:293–300
Köhler M, Hanf A, Barus H, Hendrayanto, Hölscher D (2014) Cacao trees under different shade tree shelter: effects on water use. Agrofor Syst 88:63–73
Kummerow J, Kummerow M, Souza Da Silva W (1982) Fine-root growth dynamics in cacao (Theobroma cacao). Plant Soil 65:193–201
Lehmann J (2003) Subsoil root activity in tree-based cropping systems. Plant Soil 255:319–331
Leuschner C, Harteveld M, Hertel D (2009) Consequences of increasing forest use intensity for biomass, morphology and growth of fine roots in a tropical moist forest on Sulawesi, Indonesia. Agric Ecosyst Environ 129:474–481
Leuschner C, Hertel D, Coners H, Büttner V (2001) Root competition between beech and oak: a hypothesis. Oecologia 126:276–284
Leuschner C, Moser G, Hertel D, Erasmi S, Leitner D, Culmsee H, Schuldt B, Schwendenmann L (2013) Conversion of tropical moist forest into cacao agroforest: consequences for carbon pools and annual C sequestration. Agrofor Syst 87:1173–1187
Leuschner C, Wiens M, Harteveld M (2006) Patterns of fine root mass and distribution along a disturbance gradient in a tropical montane forest, Central Sulawesi (Indonesia). Plant Soil 283:163–174
Lewis SL, Edwards DP, Galbraith D (2015) Increasing human dominance of tropical forests. Science 359:827–832
Liang J, Crowther TW, Picard N, Wiser S, Zhou M, Alberti G, Schulze E-D, McGuire D, Bozzato F, Pretzsch H, De-Miguel S, Paquette A, Hérault B, Scherer-Lorenzen M, Barrett CB, Glick HB, Hengeveld GM, Nabuurs G-J, Pfautsch S, Viana H, Vibrans AC, Ammer C, Schall P, Verbyla D, Tchebakova N, Fischer M, Watson JV, Chen HYH, Lei X, Schelhaas M-J, Lu H, Gianelle D, Parfenova EI, Salas C, Lee E, Lee B, Kim HS, Bruelheide H, Coomes DA, Piotto D, Sunderland T, Schmid B, Gourlet-Fleury S, Sonké B, Tavani R, Zhu J, Brandl S, Vayreda J, Kitahara F, Searle EB, Neldner VJ, Ngugi MR, Baraloto C, Frizzera L, Bałazy R, Oleksyn J, Zawiła-Niedźwiecki T, Bouriaud O, Bussotti F, Finér L, Jaroszewicz B, Jucker T, Valladares F, Jagodzinski AM, Peri PL, Gonmadje C, Marthy W, O’Brien T, Martin EH, Marshall A, Rovero F, Bitariho R, Niklaus PA, Alvarez-Loayza P, Chamuya N, Valencia R, Mortier F, Wortel V, Engone-Obiang NL, Ferreira LV, Odeke DE, Vasquez RM, Reich PB (2016) Positive biodiversity–productivity relationship predominant in global forests. Science 354:196
Livesley SJ, Gregory PJ, Buresh RJ (2000) Competition in tree row agroforestry systems. 1. Distribution amd dynamics of fine root length and biomass. Plant Soil 227:149–161
Makumba W, Akinnifesi FK, Janssen BH (2009) Spatial rooting patterns of gliricidia, pigeon pea and maize intercrops and effect on profile soil N and P distribution in southern Malawi. Afr J Agric Res 4:278–288
Margono BA, Potapov PV, Turubanova S, Stolle F, Hansen MC (2014) Primary forest cover loss in Indonesia over 2000–2012. Nat Clim Change 4:1–6
Meinzer FC, Andrade JL, Goldstein G, Holbrook NM, Cavelier J, Wright SJ (1999) Partitioning of soil water among canopy trees in a seasonally dry tropical forest. Oecologia 121:293–301
Meißner M, Köhler M, Schwendenmann L, Hölscher D (2012) Partitioning of soil water among canopy trees during a soil desiccation period in a temperate mixed forest. Biogeosciences 9:3465–3474
Miettinen J, Shi C, Liew SC (2011) Deforestation rates in insular Southeast Asia between 2000 and 2010. Glob Change Biol 17:2261–2270
Moser G, Leuschner C, Hertel D, Hölscher D, Köhler M, Leitner D, Michalzik B, Prihastanti E, Tjitrosemito S, Schwendenmann L (2010) Response of cocoa trees (Theobroma cacao) to a 13-month desiccation period in Sulawesi, Indonesia. Agrofor Syst 79:171–187
Muñoz F, Beer J (2001) Fine root dynamics of shaded cacao plantations in Costa Rica. Agrofor Syst 51:119–130
Nygren P, Leblanc H (2009) Natural abundance of 15N in two cacao plantations with legume and non-legume shade trees. Agrofor Syst 76:303–315
Nygren P, Leblanc H, Lu M, Luciano C (2013) Distribution of coarse and fine roots of Theobroma cacao and shade tree Inga edulis in a cocoa plantation. Ann For Sci 70:229–239
Ong CK, Corlett JE, Singh RP, Black CR (1991) Above and below ground interactions in agroforestry systems. For Ecol Manag 45:45–57
Ong CK, Kho RM, Radersma S (2004) Ecological interactions in multispecies agroecosystems: concepts and rules. CABI Publishing, Wallingford
Persson H (1980) Fine-root dynamics in a Scots pine stand with and without near-optimum nutrient and water regimes. Acta Phytogeogr Suec 68:101–110
Pierret A, Maeght J-L, Clément C, Montoroi J-P, Hartmann C, Gonkhamdee S (2016) Understanding deep roots and their functions in ecosystems: an advocacy for more unconventional research. Ann Bot 118:621–635
van Praag HJ, Sougnez-Remy S, Weissen F, Carletti G (1988) Root turnover in a beech and a spruce stand of the Belgian Ardennes. Plant Soil 105:87–103
Prieto I, Roumet C, Cardinael R, Dupraz C, Jourdan C, Kim JH, Maeght J-L, Mao Z, Pierret A, Portillo N, Roupsard O, Thammahacksa C, Stokes A (2015) Root functional parameters along a land-use gradient: evidence of a community-level economics spectrum. J Ecol 103:361–373
Rice RA, Greenberg R (2000) Cacao cultivation and the conservation of biological diversity. Ambio: J Hum Environ 29:167–173
Schenk HJ (2006) Root competition: Beyond resource depletion. J Ecol 94:725–739
Schroth G (1995) Tree root characteristics as criteria for species selection and systems design in agroforestry. Agrofor Syst 30:125–143
Schroth G, Kolbe D, Pity B, Zech W (1996) Root system characteristics with agroforestry relevance of nine leguminous tree species and a spontaneous fallow in a semi-deciduous rainforest area of West Africa. For Ecol Manag 84:199–208
Schroth G, Zech W (1995) Above- and below-ground biomass dynamics in a sole cropping and an alley cropping system withGliricidia sepium in the semi-deciduous rainforest zone of West Africa. Agrofor Syst 31:181–198
Schwendenmann L, Veldkamp E, Moser G, Hölscher D, Köhler M, Clough Y, Anas I, Djajakirana G, Erasmi S, Hertel D, Leitner D, Leuschner C, Michalzik B, Propastin P, Tjoa A, Tscharntke T, van Straaten O (2010) Effects of an experimental drought on the functioning of a cacao agroforestry system, Sulawesi, Indonesia. Glob Change Biol 16:1515–1530
Steffan-Dewenter I, Kessler M, Barkmann J, Bos MM, Buchori D, Erasmi S, Faust H, Gerold G, Glenk K, Gradstein SR, Guhardja E, Harteveld M, Hertel D, Höhn P, Kappas M, Köhler S, Leuschner C, Maertens M, Marggraf R, Migge-Kleian S, Mogea J, Pitopang R, Schaefer M, Schwarze S, Sporn SG, Steingrebe A, Tjitrosoedirdjo SS, Tjitrosemito S, Twele A, Weber R, Woltmann L, Zeller M, Tscharntke T (2007) Tradeoffs between income , biodiversity , and ecosystem functioning during tropical rainforest conversion and agroforestry intensification. Proc Natl Acad Sci U S A 104:4973–4978
Tscharntke T, Clough Y, Bhagwat SA, Buchori D, Faust H, Hertel D, Hölscher D, Juhrbandt J, Kessler M, Perfecto I, Scherber C, Schroth G, Veldkamp E, Wanger TC (2011) Multifunctional shade-tree management in tropical agroforestry landscapes—a review. J Appl Ecol 48:619–629
Vogt KA, Vogt DJ, Bloomfield J (1998) Analysis of some direct and indirect methods for estimating root biomass and production of forests at an ecosystem level. Plant Soil 200:71–89
West AG, Patrickson SJ, Ehleringer JR (2006) Water extraction times for plant and soil materials used in stable isotope analysis. Rapid Commun Mass Spectrom 20:1317–1321
Acknowledgements
This study received financial support by the German Research Foundation (DFG) in the framework of the interdisciplinary German-Indonesian research project ELUC (‘Environmental and land-use change in Sulawesi, Indonesia’) and the collaborative research center CRC990 ‘Ecological and Socioeconomic Functions of Tropical Lowland Rainforest Transformation Systems (Sumatra, Indonesia)’. Special thanks go to Andrea Hanf for collaboration in field work and data analysis. We are very thankful to our local assistants in the Kulawi valley and in Palu for supporting our study and we particularly thank RISTEK, the village heads and local plot owners for making this study possible. Last but not least, we want to thank two anonymous reviewers for their constructive and very helpful comments on an earlier manuscript version.
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Rajab, Y.A., Hölscher, D., Leuschner, C. et al. Effects of shade tree cover and diversity on root system structure and dynamics in cacao agroforests: The role of root competition and space partitioning. Plant Soil 422, 349–369 (2018). https://doi.org/10.1007/s11104-017-3456-x
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DOI: https://doi.org/10.1007/s11104-017-3456-x