Floresta e Ambiente
Floresta e Ambiente
Original Article Silviculture

Structure of AMF Community in an Agroforestry System of Coffee and Macauba Palm

Paulo Prates Júnior, Sandro Lucio Silva Moreira, Thuany Cerqueira Jordão, Aristides Osvaldo Ngolo, Bruno Coutinho Moreira, Ricardo Henrique Silva Santos, Raphael Bragança Alves Fernandes, Maria Catarina Megumi Kasuya

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Coffee crop in Brazil is typically grown as a monoculture. However, we hypothesized that agroforestry system is favorable association for arbuscular mycorrhizal fungi (AMF), affecting its community structure and potentially impacting crop productivity and agroecosystem health. This study evaluated how the microclimate, soil depth, macauba field spacing and distance between coffee plants and palms affect the structure of the AMF community. The structure of the AMF community was influenced by the soil depth, microclimate features, soil moisture, maximum air temperature, and photosynthetically active radiation (PAR). The distance at which coffee-macauba influences ecological diversity indices of AMF, and higher diversity are related to the proximity between plants. AMF diversity (Richness and Shannon) in the agroforestry system exceeded that observed in the full-sun coffee in the 0-20 soil depth layer. Our results showed that the microclimate, soil depth, plant density, and distance between coffee from macauba affected the AMF community structure.


Arbuscular mycorrhizal fungi; Acrocomia aculeata; Soil Quality; Microclime; Coffea arabica


  • Aldrich-Wolfe L, Black KL, Hartmann EDL, Shivega WG, Schmaltz LC, McGlynn RD et al. Taxonomic shifts in arbuscular mycorrhizal fungal communities with shade and soil nitrogen across conventionally managed and organic coffee agroecosystems. Mycorrhiza 2020; 30(4): 513-527. https://doi:10.1007/s00572-020-00967-7
    » https://doi.org/https://doi:10.1007/s00572-020-00967-7

  • Andrade SAL, Mazzafera P, Schiavinato MA, Silveira APD. Arbuscular mycorrhizal association in coffee. J Agric Sci. 2009; 147: 105-115. https://doi.org/10.1017/S0021859608008344
    » https://doi.org/https://doi.org/10.1017/S0021859608008344

  • Araújo FHV, Cruz RS, Porto DWB, Machado CMM, França AC. Effects of mycorrhizal association and phosphate fertilization on the initial growth of coffee plants. Pesq. Agropec. Trop. 2020; 50: e58646. https://doi.org/10.1590/1983-40632020v5058646
    » https://doi.org/https://doi.org/10.1590/1983-40632020v5058646

  • Arias RM, Heredia-Abarca G, Sosa VJ, Fuentes-Ramírez LE. Diversity and abundance of arbuscular mycorrhizal fungi spores under different coffee production systems and in a tropical montane cloud forest patch in Veracruz, Mexico. Agrofor Syst. 2012; 85: 179-193. https://doi.org/10.1007/s10457-011-9414-3
    » https://doi.org/https://doi.org/10.1007/s10457-011-9414-3

  • Banks JE, Cline E, Castro S, Urena N, Nichols K, Hannon L, Chandler M. Effects of Synthetic Fertilizer on Coffee Yields and Ecosystem Services: Parasitoids and Soil Glomalin in a Costa Rican Coffee Agroecosystem. J. Crop. Improv. 2011; 25(6): 650-663. https://doi.org/10.1080/15427528.2011.599919
    » https://doi.org/https://doi.org/10.1080/15427528.2011.599919

  • Belay Z, Negash M, Kaseva J, Vestberg M, Kahiluoto H. Native forests but not agroforestry systems preserve arbuscular mycorrhizal fungal species richness in southern Ethiopia. Mycorrhiza 2020; 30: 749-759. https://doi.org/10.1007/s00572-020-00984-6
    » https://doi.org/https://doi.org/10.1007/s00572-020-00984-6

  • Bennett AE, Classen AT. Climate change influences mycorrhizal fungal-plant interactions, but conclusions are limited by geographical study bias. Ecology 2020; e02978. https://doi.org/10.1002/ecy.2978
    » https://doi.org/https://doi.org/10.1002/ecy.2978

  • Bhattacharya S, Bagyaraj DJ. Effectiveness of Arbuscular Mycorrhizal Fungal Isolates on Arabica Coffee (Coffea arabica L.), Biol Agric Hortic. 2002; 20: 125-131. https://doi.org/10.1080/01448765.2002.9754956
    » https://doi.org/https://doi.org/10.1080/01448765.2002.9754956

  • Boeing, Embraer, Fapesp, Unicamp, 2013. Flight path to aviation biofuels in Brazil: action plan, p. 60 [cited 2021 fev. 23]. Available from: Available from: http://www.fapesp.br/publicacoes/flightpath-to-aviationbiofuels- in-brazil-action-plan.pdf
    » http://www.fapesp.br/publicacoes/flightpath-to-aviationbiofuels- in-brazil-action-plan.pdf

  • Bonfim JA, Matsumoto SN, Lima JM, César FRCF, Santos MAF. Fungos micorrízicos arbusculares (FMA) e aspectos fisiológicos em cafeeiros cultivados em sistema agroflorestal e a pleno sol. Bragantia 2010; 69: 201-206. https://doi.org/10.1590/S0006-87052010000100025
    » https://doi.org/https://doi.org/10.1590/S0006-87052010000100025

  • Cardoso IM, Boddington C, Janssen BH, Oenema O, Kuyper W, Kuyper TW. Distribution of mycorrhizal fungal spores in soils under agroforestry and monocultural coffee systems in Brazil. Agrofor Syst. 2003; 58: 33-43. https://doi.org/10.1023/A:1025479017393
    » https://doi.org/https://doi.org/10.1023/A:1025479017393

  • Cardoso IM, Kuyper TW. Mycorrhizas and tropical soil fertility. Agric Ecosyst Environ. 2006; 116: 72-84. https://doi.org/10.1016/j.agee.2006.03.011
    » https://doi.org/https://doi.org/10.1016/j.agee.2006.03.011

  • Cornejo P, Azcó-Aguilar C, Barea JM, Ferrol N. Temporal temperature gradient gel electrophoresis (TTGE) as a tool for the characterization of arbuscular mycorrhizal fungi. FEMS Microbiol Lett. 2004; 241: 265-270. https://doi.org/10.1016/j.femsle.2004.10.030
    » https://doi.org/https://doi.org/10.1016/j.femsle.2004.10.030

  • Cruz RS, Araújo FHV, França AC, Sardinha LT, Machado CMM. Physiological responses of Coffea arabica cultivars in association with arbuscular mycorrhizal fungi. Coffee. Sci. 2020; 15: e151641. https://doi.org/10.25186/cs.v15i.1641
    » https://doi.org/https://doi.org/10.25186/cs.v15i.1641

  • Davison J, de León DG, Zobel M, Moora M, Guilherme Bueno C, Barceló M, et al. Plant functional groups associate with distinct arbuscular mycorrhizal fungal communities. New Phytol. 2020; 226: 1117-1128. https://doi.org/10.1111/nph.16423
    » https://doi.org/https://doi.org/10.1111/nph.16423

  • Davison J, Moora M, Semchenko M, Adenan SB. et al. Temperature and pH define the realized niche space of arbuscular mycorrhizal fungi. New Phytol . 2021. https://doi.org/10.1111/nph.17240
    » https://doi.org/https://doi.org/10.1111/nph.17240

  • Díaz-Ariza LA, Rivera EL, Sánchez N. Occurrence of arbuscular mycorrhizal fungi in leaf litter and roots of shaded coffee plantations under organic and conventional management. Rev Bras Cienc Solo. 2021;45:e0200110. https://doi.org/10.36783/18069657rbcs20200110
    » https://doi.org/https://doi.org/10.36783/18069657rbcs20200110

  • Dias HCT, Sato AY, Neto SNO, Morais TC, Freire A, Bento PS. Cultivo da macauba: ganhos ambientais em áreas de pastagens. Inf. Agropecu. 2011; 32:52-60.

  • Dobo B, Asefa F, Asfaw Z. Effect of tree-enset-coffee based agro-forestry practices on arbuscular mycorrhizal fungi (AMF) species diversity and spore density. Agrofor Syst. 2018; 92: 525-540. https://doi.org/10.1007/s10457-016-0042-9
    » https://doi.org/https://doi.org/10.1007/s10457-016-0042-9

  • Dransfield J, Uhl NW, Asmussen CB, Baker WJ, Harley MM, Lewis CE. Genera Palmarum: the Evolution and Classification of Palms. Royal Botanic Gardens Richmond, UK, Kew; 2008.

  • Fernandes RA, Ferreira DA, Saggin-Junior OJ, Stürmer SL, Paulino HB, Siqueira JO, Carneiro MAC. Occurrence and species richness of mycorrhizal fungi in soil under different land use. Can J Soil Sci. 2016; 96: 271-280. https://doi.org/10.1139/cjss-2015-0011
    » https://doi.org/https://doi.org/10.1139/cjss-2015-0011

  • Freire-Cruz A. Effect of light-emitting diodes on arbuscular mycorrhizal fungi associated with bahiagrass (Paspalum notatum Flügge) and millet [Pennisetum glaucum (L.) R. Br]. Bioagro, 2016; 28(3): 163-170.

  • Gerdemann JW, Nicolson TH. Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc. 1963; 46:235-244. https://doi.org/10.1016/S0007-1536(63)80079-0
    » https://doi.org/https://doi.org/10.1016/S0007-1536(63)80079-0

  • Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D. Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza . 2010; 20(8): 519-530. https//doi:10.1007/s00572-010-0333-3
    » https://doi.org/https//doi:10.1007/s00572-010-0333-3

  • Giovannini L, Palla M, Agnolucci M, Avio L, Sbrana C, Turrini A, Giovannetti M. Arbuscular Mycorrhizal Fungi and Associated Microbiota as Plant Biostimulants: Research Strategies for the Selection of the Best Performing Inocula. Agronomy. 2020; 10, 106. https://doi.org/10.3390/agronomy10010106
    » https://doi.org/https://doi.org/10.3390/agronomy10010106

  • Gomes LC., Bianchi FJJA., Cardoso IM., Fernandes RBA., Filho EIF., Schulte RPO. Agroforestry systems can mitigate the impacts of climate change on coffee production: A spatially explicit assessment in Brazil. 2020; 294:106858. https://doi.org/10.1016/j.agee.2020.106858
    » https://doi.org/https://doi.org/10.1016/j.agee.2020.106858

  • Heinemeyer A, Fitter AH. Impact of temperature on the arbuscular mycorrhizal (AM) symbiosis: growth responses of the host plant and its AM fungal partner, J Exp Bot. 2004; 55: 525-534. https://doi.org/10.1093/jxb/erh049
    » https://doi.org/https://doi.org/10.1093/jxb/erh049

  • Helgason T, Daniell TJ, Husband R, Fitter AH, Young JP. Ploughing up the wood-wide web? Nature 1998; 394: 431. https://doi.org/10.1038/28764
    » https://doi.org/https://doi.org/10.1038/28764

  • Ismail Y, McCormick S, Hijri M. The arbuscular mycorrhizal fungus, Glomus irregulare, controls the mycotoxin production of Fusarium sambucinum in the pathogenesis of potato. FEMS. Microbiol. Lett. 2013; 348(1): 46-51. https://doi.org/10.1111/1574-6968.12236
    » https://doi.org/https://doi.org/10.1111/1574-6968.12236

  • Jaitieng S, Sinma K, Rungcharoenthong P, Amkha S. Arbuscular mycorrhiza fungi applications and rock phosphate fertilizers enhance available phosphorus in soil and promote plant immunity in robusta coffee. Soil Science and Plant Nutrition. 2020; 1-5. https://doi.org/10.1080/00380768.2020.1848343
    » https://doi.org/https://doi.org/10.1080/00380768.2020.1848343

  • Jaramillo-Botero C, Santos RHS, Martinez HEP, Cecon PR, Fardin MP. Production and vegetative growth of coffee trees under fertilization and shade levels. Sci. Agric. 2010; 67: 639-645. https://doi.org/10.1590/S0103-90162010000600004
    » https://doi.org/https://doi.org/10.1590/S0103-90162010000600004

  • Konvalinková T, Jansa J. Lights off for arbuscular mycorrhiza: on its symbiotic functioning under light deprivation. Front plant Sci. 2016; 7: 1-11. https://doi.org/10.3389/fpls.2016.00782
    » https://doi.org/https://doi.org/10.3389/fpls.2016.00782

  • Kowalchuk GA, de Souza FA, van Veen JA. Community analysis of arbuscular mycorrhizal fungi associated with Ammophila arenaria in Dutch coastal sand dunes. Mol Ecol. 2002; 11: 571-81. https://doi.org/10.1046/j.0962-1083.2001.01457.x
    » https://doi.org/https://doi.org/10.1046/j.0962-1083.2001.01457.x

  • Lewin, B., Giovannucci, D., Varangis, P. Coffee Markets: New paradigms in global supply and demand. Agriculture and Rural Development. [cited 2021 fev. 23]. Available from:Available from:http://documents1.worldbank.org/curated/pt/899311468167958765/pdf/283000REVISED0Coffee1Markets01PUBLIC1.pdf
    » http://documents1.worldbank.org/curated/pt/899311468167958765/pdf/283000REVISED0Coffee1Markets01PUBLIC1.pdf

  • Liang Z, Drijber RA, Lee DJ, Dwiekat IM, Harris SD, Wedin DA. A DGGE-cloning method to characterize arbuscular mycorrhizal community structure in soil. Soil Biol Biochem. 2008; 40: 956-966. https://doi.org/10.1016/j.soilbio.2007.11.016
    » https://doi.org/https://doi.org/10.1016/j.soilbio.2007.11.016

  • Moreira SLS, Imbuzeiro HMA, Dietrich OHS, Henriques E, Pereira-Flores ME, Pimentel LD, Fernandes RBA. Root distribution of cultivated macauba trees. Ind Crop Prod. 2019; 137: 646-651. https://doi.org/10.1016/j.indcrop.2019.05.064
    » https://doi.org/https://doi.org/10.1016/j.indcrop.2019.05.064

  • Moreira SLS, Imbuzeiro HMA, Silvert C, Dietrich OHS, Pimentel LD, Fernandes RBA. Above- and below-ground carbon accumulation in cultivated macauba palm and potential to generate carbon credits. J Clean Prod. 2020; 265: 121628. https://doi.org/10.1016/j.jclepro.2020.121628
    » https://doi.org/https://doi.org/10.1016/j.jclepro.2020.121628

  • Moreira SLS, Pires CV, Marcatti GE, Santos RHS, Imbuzeiro HMA, Fernandes RBA. Intercropping of coffee with the palm tree, macauba, can mitigate climate change effects. Agr Forest Meteorol. 2018; 256-257: 379-390. https://doi.org/10.1016/j.agrformet.2018.03.026
    » https://doi.org/https://doi.org/10.1016/j.agrformet.2018.03.026

  • Motoike SY, Carvalho M, Pimentel LD, Kuki KN, Paes JMV, Dias HCT, Sato AY. A Cultura da Macauba- implantação e manejo de cultivos racionais. Viçosa, MG. UFV, 2013.

  • Mukhtar H, Lin C-M, Wunderlich RF, Cheng L-C, Ko M-C, Lin Y-P. Climate and land cover shape the fungal community structure in topsoil. Science of the total environment. 2021; 751: 141721. https://doi.org/10.1016/j.scitotenv.2020.141721
    » https://doi.org/https://doi.org/10.1016/j.scitotenv.2020.141721

  • Muleta D, Assefa F, Nemomissa S, Granhall U. Distribution of arbuscular mycorrhizal fungi spores in soils of smallholder agroforestry and monocultural coffee systems in southwestern Ethiopia. Biol Fertil Soils. 2008; 44: 653-659. https://doi.org/10.1007/s00374-007-0261-3
    » https://doi.org/https://doi.org/10.1007/s00374-007-0261-3

  • Oehl F, Sieverding E, Ineichen K, Ris E, Boller T, Wiemken A. Community in extensively soil and intensively different depths managed agroecosystems. New Phytol . 2005; 165: 273-283. https://doi.org/10.1111/j.1469-8137.2004.01235.x
    » https://doi.org/https://doi.org/10.1111/j.1469-8137.2004.01235.x

  • Perea Rojas Y C, Arias RM, Medel Ortiz R, Aguilar DT, Heredia G, Yon YR. Effects of native arbuscular mycorrhizal and phosphate-solubilizing fungi on coffee plants. Agrofor. Syst. 2019; 93: 961-972. https://doi.org/10.1007/s10457-018-0190-1
    » https://doi.org/https://doi.org/10.1007/s10457-018-0190-1

  • Posada RH, Sánchez de Prager M, Heredia-Abarca G, Sieverding E. Effects of soil physical and chemical parameters, and farm management practices on arbuscular mycorrhizal fungi communities and diversities in coffee plantations in Colombia and Mexico. Agroforest Syst. 2018; 92: 555-574. https://doi.org/10.1007/s10457-016-0030-0
    » https://doi.org/https://doi.org/10.1007/s10457-016-0030-0

  • Prates Júnior P, Moreira BC, Silva MCS, Veloso TGR, Stürmer SL, Fernandes RBA, Mendonça ES, Kasuya MCM. Agroecological coffee management increases arbuscular mycorrhizal fungi diversity. PlosOne 2019; 8: e0209093. https://doi.org/10.1371/journal.pone.0209093
    » https://doi.org/https://doi.org/10.1371/journal.pone.0209093

  • Prates Júnior P, Veloso TGR, da Silva MCS, da Luz JMR, Oliveira SF, Kasuya MCM. Soil microorganisms and quality of the coffee beverage. In: Pereira LL, Moreira TR (eds). Quality Determinants In Coffee Production. Springer Nature. 2020. https://doi.org/10.1007/978-3-030-54437-9_3
    » https://doi.org/https://doi.org/10.1007/978-3-030-54437-9_3

  • Püschel D, Bitterlich M, Rydlová J. et al. Facilitation of plant water uptake by an arbuscular mycorrhizal fungus: a Gordian knot of roots and hyphae. Mycorrhiza 2020; 30:299-313. https://doi.org/10.1007/s00572-020-00949-9
    » https://doi.org/https://doi.org/10.1007/s00572-020-00949-9

  • R Core Team. A Language and Environment for Statistical Computing. 2017. https://www.R-project.org/
    » https://www.R-project.org/

  • Rao MV, Rice RA, Fleischer RC, Muletz-Wolz CR. Soil fungal communities differ between shaded and sun-intensive coffee plantations in El Salvador. PlosOne , 2020; 15(4): e0231875. https://doi.org/10.1371/journal.pone.0231875
    » https://doi.org/https://doi.org/10.1371/journal.pone.0231875

  • Rena, AB., Guimarães, PTG. Sistema radicular do cafeeiro: estrutura, distribuição, atividade e fatores que o influenciam. EPAMIG, Belo horizonte, pp. 80 (Documento,37), 2000.

  • Ribeiro AC, Guimarães PTG, Venegas-Alvarez VH. Recomendações para o uso de Corretivos e Fertilizantes em Minas Gerais (5a Aproximação). CSFSEMG/UFV, Viçosa, MG, 1999.

  • Rigal C, Xu J, Hu G, Qiu M, Vaast P. Coffee production during the transition period from monoculture to agroforestry systems in near optimal growing conditions, in Yunnan Province. Agricultural Systems, 2020; 177: 102696. https://doi.org/10.1016/j.agsy.2019.102696
    » https://doi.org/https://doi.org/10.1016/j.agsy.2019.102696

  • Sánchez C, Caballero D, Cupull R, Gonzáles C, Urquiaga S, Rivera R. Los abonos verdes y La inoculación micorrízica de plántulas de Coffea arabica sobre suelos cambisoles gléyicos. Cultivos Tropicales, 2009; 30: 25-30.

  • Santos R, Rodrigues L, Lima C, Jaramill-Botero C. Coffee Yield and Microenvironmental Factors in a Native Tree Agroforestry System in Southeast Minas Gerais, Brazil, Journal of Sustainable Agriculture, 2012; 36: 54-68. https://doi.org/10.1080/10440046.2011.608468
    » https://doi.org/https://doi.org/10.1080/10440046.2011.608468

  • Schleppi P, Conedera M, Sedivy I, Thimonier A. Correcting non-linearity and slope effects in the estimation of the leaf area index of forests from hemispherical photographs. Agric. For. Meteorol. 2007; 144: 236-242. https://doi.org/10.1016/j.agrformet.2007.02.004
    » https://doi.org/https://doi.org/10.1016/j.agrformet.2007.02.004

  • Simon L, Lalonde M, Bruns TD. Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microbiol. 1992; 58: 291-295. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC195206/pdf/aem00042-0311.pdf
    » https://www.ncbi.nlm.nih.gov/pmc/articles/PMC195206/pdf/aem00042-0311.pdf

  • Siqueira JO, Saggin-Júnior OJ, Flores-Aylas WW, Guimarães PTG. Arbuscular mycorrhizal inoculation and superphosphate application influence plant development and yield of coffee in Brazil. Mycorrhiza 1998; 7:293-300. https://doi.org/10.1007/s005720050195
    » https://doi.org/https://doi.org/10.1007/s005720050195

  • Smith SE, Smith FA. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Ver. Plant Biol. 2011; 62: 227-250. https://doi: 10.1146/annurev-arplant-042110-103846.
    » https://doi.org/https://doi: 10.1146/annurev-arplant-042110-103846

  • Steidinger BS, Croiwther TW, Liang J, Nuland MV. et al. Climatic controls of decomposition drive the global biogeography of forest - tree symbioses. Nature . 2019; 569: 404-408. https://doi.org/10.1038/s41586-019-1128-0
    » https://doi.org/https://doi.org/10.1038/s41586-019-1128-0

  • Veloso TGR, da Silva MCS, Cardoso WS. et al. Efeitos de fatores ambientais na microbiota de frutos e solo de Coffea arabica no Brasil. Sci Rep 2020; 10: 14692. https://doi.org/10.1038/s41598-020-71309-y
    » https://doi.org/https://doi.org/10.1038/s41598-020-71309-y

  • Viana, M.C.M., Silva, E.A., Queiroz, D.S., Paes, J.M.V., Albernaz, W.M., Fraga, G. Cultivo de macaúba em sistemas agrossilvipastoris. Inf. Agropecu. 2011; 32: 70-80.

  • Whitford KR, Colquhoun IJ, Lang ARG, Harper BM. Measuring leaf are index in a sparse eucalypt forest: a comparison of estimates from direct measurement, hemispherical photography, sunlight transmittance and allometric regression. Agric. For. Meteorol. 1995; 74: 237-249. https://doi.org/10.1016/0168-1923(94)02189-Q
    » https://doi.org/https://doi.org/10.1016/0168-1923(94)02189-Q

  • Zhang J, Tang X, Zhong S, Yin G, Gao Y, He X. Recalcitrant carbon components in glomalin-related soil protein facilitate soil organic carbon preservation in tropical forests. Sci Rep . 2017; 7: 2391. https://doi.org/10.1038/s41598-017-02486-6
    » https://doi.org/https://doi.org/10.1038/s41598-017-02486-6

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