Abstract
Background
Agroforestry is a promising approach for sustainable agriculture due efficient resource cycling and improved soil fertility. Bombax ceiba (Malvaceae), a tall tree with red flowers blooming in spring, is traditionally planted in rice fields in tropical Asia. However, the role of B. ceiba in the agroforestry systems remains unexplored.
Methods
We collected 81 soil samples at different distances to B. ceiba (0 m (D0), 1 m (D1), and 5 m (D5)) at a typical B. ceiba-rice agroforestry system in Hainan Island (south China) during three reproductive stages of rice- booting, heading and maturity. We assessed spatiotemporal variations of soil nutrient properties (by a soil nutrient analyzer (YT-TRX03)), and soil bacterial and fungal communities (by sequencing 16S rRNA gene and internal transcribed spacer (ITS) region, respectively).
Results
B. ceiba improved the soil nutrient conditions in a rice field, particularly the availability of potassium and soil organic matter. Soil microbial communities were significantly affected by the distances to B. ceiba and the reproductive stages of rice. Available potassium was the principal driver of soil bacterial diversity and structure. In contrast, fungal diversity was negatively correlated with total nitrogen, while soil organic matter was the main factor shaping fungal community structure.
Conclusions. Our results show that B. ceiba has positive impacts on abiotic traits of rice-growing soils. B. ceiba can change soil microbial community structure, however, the principal soil driver varied according to microbial taxa. These findings support the ecological basis of traditional agroforestry systems prevalent in tropical Asia.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Acosta-Martínez V, Dowd SE, Sun Y, Wester D, Allen V (2010) Pyrosequencing analysis for characterization of soil bacterial populations as affected by an integrated livestock-cotton production system. Appl Soil Ecol 45:13–25. https://doi.org/10.1016/j.apsoil.2010.01.005
Araujo ASF, Leite LFC, Iwata BDF, Lira MDA, Xavier GR, Figueiredo MDVB (2012) Microbiological process in agroforestry systems. A review. Agron Sustain 32:215–226. https://doi.org/10.1007/s13593-011-0026-0
Asigbaase M, Dawoe E, Lomax BH, Sjogersten S (2021) Temporal changes in litterfall and potential nutrient return in cocoa agroforestry systems under organic and conventional management. Ghana Heliyon 7:e08051. https://doi.org/10.1016/j.heliyon.2021.e08051
Banerjee S, Baah-Acheamfour M, Carlyle CN, Bissett A, Richardson AE, Siddique T, Bork EW, Chang SX (2016) Determinants of bacterial communities in Canadian agroforestry systems. Environ Microbiol 18:1805–1816. https://doi.org/10.1111/1462-2920.12986
Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511. https://doi.org/10.1038/nature13855
Bardhan S, Jose S, Jenkins MA, Webster CR, Udawatta RP, Stehn SE (2012) Microbial community diversity and composition across a gradient of soil acidity in spruce–fir forests of the southern Appalachian Mountains. Appl Soil Ecol 61:60–68. https://doi.org/10.1016/j.apsoil.2012.04.010
Battistuzzi FU, Hedges SB (2009) A major clade of prokaryotes with ancient adaptations to life on land. Mol Biol Evol 26:335–343. https://doi.org/10.1093/molbev/msn247
Beule L, Karlovsky P (2021a) Early response of soil fungal communities to the conversion of monoculture cropland to a temperate agroforestry system. Peer J 9:e12236. https://doi.org/10.7717/peerj.12236
Beule L, Karlovsky P (2021b) Tree rows in temperate agroforestry croplands alter the composition of soil bacterial communities. PLoS One 16:e246919. https://doi.org/10.1371/journal.pone.0246919
Beule L, Corre MD, Schmidt M, Gobel L, Veldkamp E, Karlovsky P (2019) Conversion of monoculture cropland and open grassland to agroforestry alters the abundance of soil bacteria, fungi and soil-N-cycling genes. PLoS One 14(6):e0218779. https://doi.org/10.1371/journal.pone.0218779
Beule L, Heidrich V, O’rourke D, Karlovsky P (2021) Scaling with ranked subsampling. R Package Version 0.2.2. https://cran.r-project.org/web/packages/SRS/index.html. Accessed 12 Apr 2022.
Bolyen E, Rideout JR, Dillon MR et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9
Campbell BJ, Kirchman DL (2013) Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient. ISME J 7:210–220. https://doi.org/10.1038/ismej.2012.93
Cardinael R, Mao Z, Chenu C et al (2020) Belowground functioning of agroforestry systems: recent advances and perspectives. Plant Soil 453:1–13. https://doi.org/10.1007/s11104-020-04633-x
Chen H (2021) VennDiagram: Generate high-resolution venn and euler plots. R Package Version 1.7.1. https://cran.r-project.org/web/packages/VennDiagram/. Accessed 20 Apr 2022.
Chen C, Liu W, Wu J, Jiang X, Zhu X (2019) Can intercropping with the cash crop help improve the soil physico-chemical properties of rubber plantations? Geoderma 335:149–160. https://doi.org/10.1016/j.geoderma.2018.08.023
Chen L, He Z, Zhao W, Liu J, Zhou H, Li J, Meng Y, Wang L (2020) Soil structure and nutrient supply drive changes in soil microbial communities during conversion of virgin desert soil to irrigated cropland. Eur J Soil Sci 71:768–781. https://doi.org/10.1111/ejss.12901
Delgado-Baquerizo M, Maestre FT, Reich PB et al (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7:10541. https://doi.org/10.1038/ncomms10541
Dukunde A, Schneider D, Schmidt M, Veldkamp E, Daniel R (2019) Tree species shape soil bacterial community structure and function in temperate deciduous forests. Front Microbiol 10:1519. https://doi.org/10.3389/fmicb.2019.01519
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998. https://doi.org/10.1038/nmeth.2604
Esmaeilzadeh-Salestani K, Bahram M, Seraj RGM et al (2021) Cropping systems with higher organic carbon promote soil microbial diversity. Agric Ecosyst Environ 319:107521. https://doi.org/10.1016/j.agee.2021.107521
Hannula SE, Morrien E, de Hollander M, van der Putten WH, van Veen JA, de Boer W (2017) Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture. ISME J 11:2294–2304. https://doi.org/10.1038/ismej.2017.90
Hassan MO (2018) Leaf litter of Bombax ceiba L. threatens plant cover and floristic diversity in a new urban ecosystem. Flora 242:22–30. https://doi.org/10.1016/j.flora.2018.03.004
Heidrich V, Karlovsky P, Beule L (2021) ‘SRS’ R package and ‘q2-SRS’ QIIME 2 plugin: normalization of microbiome data using scaling with ranked subsampling (SRS). Appl Sci 11(23):11473. https://doi.org/10.3390/app112311473
Hombegowda HC, Köhler M, Röll A, Hölscher D (2020) Tree species and size influence soil water partitioning in coffee agroforestry. Agrofor Syst 94:137–149. https://doi.org/10.1007/s10457-019-00375-7
Homulle Z, George TS, Karley AJ (2021) Root traits with team benefits: understanding belowground interactions in intercropping systems. Plant Soil. https://doi.org/10.1007/s11104-021-05165-8
Isaac ME, Borden KA (2019) Nutrient acquisition strategies in agroforestry systems. Plant Soil 444:1–19. https://doi.org/10.1007/s11104-019-04232-5
Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453. https://doi.org/10.1038/ismej.2008.127
Kay S, Graves A, Palma JHN et al (2019) Agroforestry is paying off – economic evaluation of ecosystem services in European landscapes with and without agroforestry systems. Ecosyst Sevr 36:100896. https://doi.org/10.1016/j.ecoser.2019.100896
Koju R, Maharjan B, Gosai KR, Kittur S, Sundar KSG (2020) Ciconiiformes nesting on trees in cereal-dominated farmlands: importance of scattered trees for heronries in lowland Nepal. Waterbirds 42:355–453. https://doi.org/10.1675/063.042.0401
Lacombe S, Bradley RL, Hamel C, Beaulieu C (2009) Do tree-based intercropping systems increase the diversity and stability of soil microbial communities? Agric Ecosyst Environ 131(1–2):25–31. https://doi.org/10.1016/j.agee.2008.08.010
Lai J, Zou Y, Zhang J, Peres-Neto P (2022) Generalizing hierarchical and variation partitioning in multiple regression and canonical analyses using the rdacca.Hp R package. Methods Ecol Evol 13:782–788. https://doi.org/10.1111/2041-210X.13800
Li H, Li B, Zhang Z, Zhu C, Tian Y, Ye J (2018) Evolution of microbial communities during electrokinetic treatment of antibiotic-polluted soil. Ecotox Environ Safe 148:842–850. https://doi.org/10.1016/j.ecoenv.2017.11.057
Li X, Wang H, Li X, Li X, Zhang H (2019) Shifts in bacterial community composition increase with depth in three soil types from paddy fields in China. Pedobiologia 77:150589. https://doi.org/10.1016/j.pedobi.2019.150589
Li H, Wang H, Jia B, Li D, Fang Q, Li R (2021) Irrigation has a higher impact on soil bacterial abundance, diversity and composition than nitrogen fertilization. Sci Rep 11:16901. https://doi.org/10.1038/s41598-021-96234-6
Lin BB (2007) Agroforestry management as an adaptive strategy against potential microclimate extremes in coffee agriculture. Agric For Meteorol 144:85–94. https://doi.org/10.1016/j.agrformet.2006.12.009
Liu J, Liu X, Sui Y, Yu Z, Shi Y, Chu H, Jin J, Wang G (2015) Soil carbon content drives the biogeographical distribution of fungal communities in the black soil zone of Northeast China. Soil Biol Biochem 83:29–39. https://doi.org/10.1016/j.soilbio.2015.01.009
Liu M, Liu J, Chen X, Jiang C, Wu M, Li Z (2018) Shifts in bacterial and fungal diversity in a paddy soil faced with phosphorus surplus. Biol Fert Soils 54:259–267. https://doi.org/10.1007/s00374-017-1258-1
Liu C, Jin Y, Hu Y, Tang J, Xiong Q, Xu M, Bibi F, Beng KC (2019) Drivers of soil bacterial community structure and diversity in tropical agroforestry systems. Agric Ecosyst Environ 278:24–34. https://doi.org/10.1016/j.agee.2019.03.015
Mori AS, Isbell F, Seid R (2018) β-Diversity, community assembly, and ecosystem functioning. Trends Ecol Evol 33:549–564. https://doi.org/10.1016/j.tree.2018.04.012
Mwaheb MAMA, Hussain M, Tian J, Zhang X, Hamid MI, El-Kassim NA, Hassan GM, Xiang M, Liu X (2017) Synergetic suppression of soybean cyst nematodes by chitosan and Hirsutella minnesotensis via the assembly of the soybean rhizosphere microbial communities. Biol Control 115:85–94. https://doi.org/10.1016/j.biocontrol.2017.09.011
Nara K (2008) Community developmental patterns and ecological functions of ectomycorrhizal Fungi: implications from primary succession. Springer Berlin Heidelberg, Berlin, pp 581–599
Nguyen NH, Williams LJ, Vincent JB, Stefanski A, Cavender-Bares J, Messier C, Paquette A, Gravel D, Reich PB, Kennedy PG (2016) Ectomycorrhizal fungal diversity and saprotrophic fungal diversity are linked to different tree community attributes in a field-based tree experiment. Mol Ecol 25:4032–4046. https://doi.org/10.1111/mec.13719
Nilsson RH, Larsson K, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glöckner FO, Tedersoo L, Saar I, Kõljalg U, Abarenkov K (2019) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47:D259–D264. https://doi.org/10.1093/nar/gky1022
Oksanen J, Blanchet F G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin P R, O'Hara R B, Simpson G L, Solymos P, Stevens M H M, Szoecs E, Wagner H (2017) vegan: Community Ecology Package. R Package Version 2.4–2. https://CRAN.R-project.org/package=vegan
Oren A (2015) Halophilic microbial communities and their environments. Curr Opin Biotech 33:119–124. https://doi.org/10.1016/j.copbio.2015.02.005
Osman JR, Fernandes G, DuBow MS (2017) Bacterial diversity of the rhizosphere and nearby surface soil of rice (Oryza sativa) growing in the Camargue (France). Rhizosphere 3:112–122. https://doi.org/10.1016/j.rhisph.2017.03.002
Pardon P, Reubens B, Reheul D, Mertens J, De Frenne P, Coussement T, Janssens P, Verheyen K (2017) Trees increase soil organic carbon and nutrient availability in temperate agroforestry systems. Agric Ecosyst Environ 247:98–111. https://doi.org/10.1016/j.agee.2017.06.018
Podosokorskaya OA, Bonch-Osmolovskaya EA, Novikov AA, Kolganova TV, Kublanov IV (2013) Ornatilinea apprima gen. nov., sp. nov., a cellulolytic representative of the class Anaerolineae. Int J Syst Evol Micr 63:86–92. https://doi.org/10.1099/ijs.0.041012-0
Prober SM, Leff JM, Bates ST et al (2015) Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol Lett 18:85–95. https://doi.org/10.1111/ele.12381
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
Querné A, Battie-laclau P, Dufour L, Wery J, Dupraz C (2017) Effects of walnut trees on biological nitrogen fixation and yield of intercropped alfalfa in a Mediterranean agroforestry system. Eur J Agron 84:35–46. https://doi.org/10.1016/j.eja.2016.12.001
Rivest D, Lorente M, Olivier A, Messier C (2013) Soil biochemical properties and microbial resilience in agroforestry systems: effects on wheat growth under controlled drought and flooding conditions. Sci Total Environ 463-464:51–60. https://doi.org/10.1016/j.scitotenv.2013.05.071
Romaní AM, Fischer H, Mille-Lindblom C, Tranvik LJ (2006) Interactions of bacteria and fungi on decomposing litter: differential extracellular enzyme activities. Ecology 87(10):2559–2569. https://doi.org/10.1890/0012-9658(2006)87[2559:iobafo]2.0.co;2
Schmidt SK, Nemergut DR, Darcy JL, Lynch R (2014) Do bacterial and fungal communities assemble differently during primary succession? Mol Ecol 23:254–258. https://doi.org/10.1111/mec.12589
Stevenson A, Hallsworth JE (2014) Water and temperature relations of soil Actinobacteria. Env Microbiol Rep 6:744–755. https://doi.org/10.1111/1758-2229.12199
Tang Q, Yan X, Meng W (2015) Current status and developing strategy of rice production in Hainan. Hybrid Rice 30:1–5
Udawatta RP, Rankoth L, Jose S (2019) Agroforestry and biodiversity. Sustainability 11:2879. https://doi.org/10.3390/su11102879
van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11(3):296–310. https://doi.org/10.1111/j.1461-0248.2007.01139.x
Wang W, Wang J, Ye Z, Zhang T, Qu L, Li J (2019) Soil property and plant diversity determine bacterial turnover and network interactions in a typical arid inland river basin, Northwest China. Front Microbiol 10:2655. https://doi.org/10.3389/fmicb.2019.02655
Wang W, Li J, Ye Z, Wang J, Qu L, Zhang T (2021) Spatial factors and plant attributes influence soil fungal community distribution patterns in the lower reaches of the Heihe River basin, Northwest China. Environ Microbiol 23:2499–2508. https://doi.org/10.1111/1462-2920.15466
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 79:247–258. https://doi.org/10.2307/3546010
Wei J, Wang D, Wei Z, Qi Z (2013) Temporal and spatial distribution of soil pH in arable land of Changjiang, Hainan. Chin J Trop Crops 34(3):413–417
Xiang WQ, Ren MX (2019) Adaptive significance of yellow flowered Bombax ceiba (Malvaceae). Biodivers Sci 27:373–379. https://doi.org/10.17520/biods.2019003
Xiang WQ, Zhang JR, Tang L, Ren MX (2022) Filament union provides landing site for birds and increase pollen removal and deposition in an ornithophilous species. Flora 288:152025. https://doi.org/10.1016/j.flora.2022.152025
Xie J, Hu L, Tang J, Wu X, Li N, Yuan Y, Yang H, Zhang J, Luo S, Chen X (2011) Ecological mechanisms underlying the sustainability of the agricultural heritage rice-fish coculture system. PNAS 108:E1381–E1387. https://doi.org/10.1073/pnas.1111043108
Yang B, Sun D, Zhang Y, Zhong C, Huang G (2019) Effects of different paddy-upland multiple cropping rotation systems on soil organic carbon and its fractions in paddy field. Chinese. J Appl Ecol 30:456–462. https://doi.org/10.13287/j.1001-9332.201902.021
Zeng H, Yu L, Liu P, Wang Z, Chen Y, Wang J (2021) Nitrogen fertilization has a stronger influence than cropping pattern on AMF community in maize/soybean strip intercropping systems. Appl Soil Ecol 167:104034. https://doi.org/10.1016/j.apsoil.2021.104034
Zhu X, Liu W, Chen J et al (2020) Reductions in water, soil and nutrient losses and pesticide pollution in agroforestry practices: a review of evidence and processes. Plant Soil 453:45–86. https://doi.org/10.1007/s11104-019-04377-3
Acknowledgements
We thank fundings from Major Science and Technology Project of Hainan Province (ZDKJ2021018), National Natural Science Foundation of China (41871041), Scientific Research Foundation of Hainan University (KYQD(ZR)-21110) and Natural Science Foundation of Hainan Province (Youth Project, 322QN247). Help from Beijing Allwegene Company (Beijing, China) for analysis of high throughput sequencing data is acknowledged. We also thank Zi-Jie Long and Xin Yang for their help in field sampling.
Author information
Authors and Affiliations
Contributions
Ming-Xun Ren and Pastor L. Malabrigo Jr. contributed to the study conception and design. Material preparation, data collection and analysis were performed by Jing Wen, Wen-Juan Wang, Wen-Qian Xiang and Ming-Xun Ren. The first draft of the manuscript was written by Wen-Juan Wang, Ming-Xun Ren commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Responsible Editor: Rémi Cardinael.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 633 kb)
Rights and permissions
About this article
Cite this article
Wang, WJ., Wen, J., Xiang, WQ. et al. Soil bacterial and fungal communities respond differently to Bombax ceiba (Malvaceae) during reproductive stages of rice in a traditional agroforestry system. Plant Soil 479, 543–558 (2022). https://doi.org/10.1007/s11104-022-05542-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05542-x