Rubber-based agroforestry systems modify the soil fungal composition and function in Southwest China
Zhenyu Hong, Xinai Li, Debao Li, Jianping Wu
Rubber-based agroforestry systems modify the soil fungal composition and function in Southwest China
● Rubber-based agroforestry systems increased the complexity of fungal networks.
● Fungal community structure was strongly correlated with soil pH and SOC.
● Rubber-based agroforestry systems reduced the presence of certain pathogens.
Rubber-based agroforestry systems have been recognized as a practical and sustainable solution to promote the development of agriculture and the environment. However, interactions between fungal communities and these systems are still not sufficiently investigated. In this study, we compared the abundance, diversity, and community composition of soil fungi in four treatments, including rubber monoculture and three rubber-based agroforestry treatments involving intercropping with Camellia sinensis, Coffea liberica, and Theobroma cacao. The results revealed that the community composition exhibited significant variation between the four different treatments, while the overall soil α-diversity was relatively stable across all treatments. Soil pH and soil organic carbon were significantly related to the structure of the fungal community. In particular, the complexity of the functional fungal network increased in response to agroforestry treatments, promoting beneficial fungi and suppressing certain plant pathogens. These results suggest that rubber-based agroforestry systems can promote the health of soil microbial community composition, and therefore provide an effective approach to enhancing soil quality.
agroforestry system with intercropping / rubber monoculture / fungal community / fungal function / tropical forest
[1] |
Ali, M.F., Akber, M.A., Smith, C., Aziz, A.A., 2021. The dynamics of rubber production in Malaysia: Potential impacts, challenges and proposed interventions. Forest Policy and Economics127, 102449.
CrossRef
Google scholar
|
[2] |
Banerjee, S., Schlaeppi, K., van der Heijden, M.G.A., 2018. Keystone taxa as drivers of microbiome structure and functioning. Nature Reviews Microbiology16, 567–576.
CrossRef
Google scholar
|
[3] |
Baum, C., El-Tohamy, W., Gruda, N., 2015. Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: A review. Scientia Horticulturae187, 131–141.
CrossRef
Google scholar
|
[4] |
Benjlil, H., Elkassemi, K., Aït Hamza, M., Mateille, T., Furze, J.N., Cherifi, K., Mayad, E.H., Ferji, Z., 2020. Plant-parasitic nematodes parasitizing saffron in Morocco: Structuring drivers and biological risk identification. Applied Soil Ecology147, 103362.
CrossRef
Google scholar
|
[5] |
Bücking, H., Kafle, A., 2015. Role of arbuscular mycorrhizal fungi in the nitrogen uptake of plants: Current knowledge and research gaps. Agronomy (Basel)5, 587–612.
CrossRef
Google scholar
|
[6] |
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?. Geoderma335, 149–160.
CrossRef
Google scholar
|
[7] |
Chen, X., Chen, H.Y.H., Chen, C., Ma, Z., Searle, E.B., Yu, Z., Huang, Z., 2020. Effects of plant diversity on soil carbon in diverse ecosystems: a global meta-analysis. Biological Reviews of the Cambridge Philosophical Society95, 167–183.
CrossRef
Google scholar
|
[8] |
Chivenge, P., Vanlauwe, B., Gentile, R., Six, J., 2011. Organic resource quality influences short-term aggregate dynamics and soil organic carbon and nitrogen accumulation. Soil Biology & Biochemistry43, 657–666.
CrossRef
Google scholar
|
[9] |
Cruz-Paredes, C., Svenningsen, N.B., Nybroe, O., Kjøller, R., Frøslev, T.G., Jakobsen, I., 2019. Suppression of arbuscular mycorrhizal fungal activity in a diverse collection of non-cultivated soils. FEMS Microbiology Ecology95, fiz020.
CrossRef
Google scholar
|
[10] |
Davison, J., Moora, M., Semchenko, M., Adenan, S.B., Ahmed, T., Akhmetzhanova, A.A., Alatalo, J.M., Al-Quraishy, S., Andriyanova, E., Anslan, S., Bahram, M., Batbaatar, A., Brown, C., Bueno, C.G., Cahill, J., Cantero, J.J., Casper, B.B., Cherosov, M., Chideh, S., Coelho, A.P., Coghill, M., Decocq, G., Dudov, S., Fabiano, E.C., Fedosov, V.E., Fraser, L., Glassman, S.I., Helm, A., Henry, H.A.L., Hérault, B., Hiiesalu, I., Hiiesalu, I., Hozzein, W.N., Kohout, P., Kõljalg, U., Koorem, K., Laanisto, L., Mander, Ü., Mucina, L., Munyampundu, J., Neuenkamp, L., Niinemets, Ü., Nyamukondiwa, C., Oja, J., Onipchenko, V., Pärtel, M., Phosri, C., Põlme, S., Püssa, K., Ronk, A., Saitta, A., Semboli, O., Sepp, S., Seregin, A., Sudheer, S., Peña-Venegas, C.P., Paz, C., Vahter, T., Vasar, M., Veraart, A.J., Tedersoo, L., Zobel, M., Öpik, M., 2021. Temperature and pH define the realised niche space of arbuscular mycorrhizal fungi. New Phytologist231, 763–776.
CrossRef
Google scholar
|
[11] |
de Blécourt, M., Brumme, R., Xu, J., Corre, M.D., Veldkamp, E., 2013. Soil carbon stocks decrease following conversion of secondary forests to rubber (Hevea brasiliensis) plantations. PLoS One8, e69357.
CrossRef
Google scholar
|
[12] |
Faust, K., Raes, J., 2012. Microbial interactions: from networks to models. Nature Reviews Microbiology10, 538–550.
CrossRef
Google scholar
|
[13] |
Ferrand, A., Vergalli, J., Pagès, J., Davin-Regli, A., 2020. An intertwined network of regulation controls membrane permeability including drug influx and efflux in Enterobacteriaceae. Microorganisms8, 833.
CrossRef
Google scholar
|
[14] |
Finkel, O.M., Salas-González, I., Castrillo, G., Conway, J.M., Law, T.F., Teixeira, P.J.P.L., Wilson, E.D., Fitzpatrick, C.R., Jones, C.D., Dangl, J.L., 2020. A single bacterial genus maintains root growth in a complex microbiome. Nature587, 103–108.
CrossRef
Google scholar
|
[15] |
Frey, B., Walthert, L., Perez-Mon, C., Stierli, B., Köchli, R., Dharmarajah, A. and Brunner, I., 2021. Deep soil layers of drought-exposed forests harbor poorly known bacterial and fungal communities. Frontiers in Microbiology12, 674160.
CrossRef
Google scholar
|
[16] |
Guerra-Hincapié, J.J., Gil-Restrepo, J.P., Huertas-Beltrán, R.L., Gutiérrez-Vanegas, A.J., Correa-Pinilla, D.E., Córdoba-Gaona, O.D.J., 2023. Phenology and South American leaf blight of polyclonal seedlings population of natural rubber trees in Colombia. Industrial Crops and Products199, 116745.
CrossRef
Google scholar
|
[17] |
Guo, H.C., Wang, W.B., Luo, X.H., Wu, X.P., 2015. Characteristics of rhizosphere and bulk soil microbial communities in rubber plantations in Hainan island, China. Journal of Tropical Forest Science27, 202–212.
|
[18] |
Hemati, Z., Selvalakshmi, S., Xia, S., Yang, X., 2020. Identification of indicators: Monitoring the impacts of rubber plantations on soil quality in Xishuangbanna, Southwest China. Ecological Indicators116, 106491.
CrossRef
Google scholar
|
[19] |
Ilaede, G., Souza, A., Lucy, C., Granha, J., Souchie, E., Luis, R. and Berbara, R., 2010. Arbuscular mycorrhizal fungi in agricultural and forest systems. Global Science and Technology3, 1–9.
|
[20] |
Jatoi, M.T., Lan, G., Wu, Z., Sun, R., Yang, C., Tan, Z., 2019. Comparison of soil microbial composition and diversity between mixed and monoculture rubber plantations in Hainan Province, China. Tropical Conservation Science12, 1–9.
CrossRef
Google scholar
|
[21] |
Jiang, X.J., Liu, W., Wu, J., Wang, P., Liu, C., Yuan, Z., 2017. Land degradation controlled and mitigated by rubber-based agroforestry systems through optimizing soil physical conditions and water supply mechanisms: A case study in Xishuangbanna, China. Land Degradation & Development28, 2277–2289.
CrossRef
Google scholar
|
[22] |
Krashevska, V., Klarner, B., Widyastuti, R., Maraun, M., Scheu, S., 2015. Impact of tropical lowland rainforest conversion into rubber and oil palm plantations on soil microbial communities. Biology and Fertility of Soils51, 697–705.
CrossRef
Google scholar
|
[23] |
Lam, S.K., Goodrich, J.P., Liang, X., Zhang, Y., Pan, B., Schipper, L.A., Sulaeman, Y., Nelson, L., Chen, D., 2022. Mitigating soil greenhouse-gas emissions from land-use change in tropical peatlands. Frontiers in Ecology and the Environment20, 352–360.
CrossRef
Google scholar
|
[24] |
Lan, G., Wu, Z., Yang, C., Sun, R., Chen, B., Zhang, X., 2020. Tropical rainforest conversion into rubber plantations results in changes in soil fungal composition, but underling mechanisms of community assembly remain unchanged. Geoderma375, 114505.
CrossRef
Google scholar
|
[25] |
Lang, R., Goldberg, S.D., Blagodatsky, S., Piepho, H., Hoyt, A.M., Harrison, R.D., Xu, J., Cadisch, G., 2020. Mechanism of methane uptake in profiles of tropical soils converted from forest to rubber plantations. Soil Biology & Biochemistry145, 107796.
CrossRef
Google scholar
|
[26] |
Li, J., Sun, X., Li, M., Zou, J., Bian, H., 2022. Effects of stand age and soil organic matter quality on soil bacterial and fungal community composition in Larix gmelinii plantations, Northeast China. Land Degradation & Development33, 1249–1259.
CrossRef
Google scholar
|
[27] |
Li, X., Ge, T., Chen, Z., Wang, S., Ou, X., Wu, Y., Chen, H., Wu, J., 2020. Enhancement of soil carbon and nitrogen stocks by abiotic and microbial pathways in three rubber-based agroforestry systems in Southwest China. Land Degradation & Development31, 2507–2515.
CrossRef
Google scholar
|
[28] |
Li, Y., Liu, C., Zhang, J., Zhang, P., Xue, Y., 2021. Monitoring spatial and temporal patterns of rubber plantation dynamics using time-series landsat images and google earth engine. IEEE Journal of Selected Topics in Applied Earth Observations and Remote Sensing14, 9450–9461.
CrossRef
Google scholar
|
[29] |
Lindahl, B.D., Kyaschenko, J., Varenius, K., Clemmensen, K.E., Dahlberg, A., Karltun, E., Stendahl, J., 2021. A group of ectomycorrhizal fungi restricts organic matter accumulation in boreal forest. Ecology Letters24, 1341–1351.
CrossRef
Google scholar
|
[30] |
Liu, D., Liu, G., Chen, L., Wang, J., Zhang, L., 2018. Soil pH determines fungal diversity along an elevation gradient in Southwestern China. Science China Life Sciences61, 718–726.
CrossRef
Google scholar
|
[31] |
Liu, C., Liang, M., Nie, Y., Tang, J., Siddique, K.H.M., 2019a. The conversion of tropical forests to rubber plantations accelerates soil acidification and changes the distribution of soil metal ions in topsoil layers. Science of the Total Environment696, 134082.
CrossRef
Google scholar
|
[32] |
Liu, C., Jin, Y., Hu, Y., Tang, J., Xiong, Q., Xu, M., Bibi, F., Beng, K.C., 2019b. Drivers of soil bacterial community structure and diversity in tropical agroforestry systems. Agriculture, Ecosystems & Environment278, 24–34.
|
[33] |
Liu, W., Zhu, C., Wu, J., Chen, C., 2016. Are rubber-based agroforestry systems effective in controlling rain splash erosion?. Catena147, 16–24.
|
[34] |
Liu, Y., Shen, J., Zhang, C., Chen, Z., 2023. Impact of rubber-based land use changes on soil properties and carbon pools: A meta-analysis. Catena227, 107121.
CrossRef
Google scholar
|
[35] |
Marschner, P., Crowley, D., Yang, C.H., 2004. Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant and Soil261, 199–208.
CrossRef
Google scholar
|
[36] |
Mishra, A., Singh, D., Hathi, Z., Purohit, H.J., Jessy, M.D., Philip, A., Uthup, T.K., Singh, L., 2023. Soil microbiome dynamics associated with conversion of tropical forests to different rubber based land use management systems. Applied Soil Ecology188, 104933.
CrossRef
Google scholar
|
[37] |
Monkai, J., Hyde, K.D., Xu, J., Mortimer, P.E., 2017. Diversity and ecology of soil fungal communities in rubber plantations. Fungal Biology Reviews31, 1–11.
CrossRef
Google scholar
|
[38] |
Nguyen, N.H., Song, Z., Bates, S.T., Branco, S., Tedersoo, L., Menke, J., Schilling, J.S., Kennedy, P.G., 2016. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology20, 241–248.
CrossRef
Google scholar
|
[39] |
Qi, D., Wu, Z., Yang, C., Xie, G., Li, Z., Yang, X., Li, D., 2021. Can intercropping with native trees enhance structural stability in young rubber (Hevea brasiliensis) agroforestry system?. European Journal of Agronomy130, 126353.
CrossRef
Google scholar
|
[40] |
Qiu, Y., Guo, L., Xu, X., Zhang, L., Zhang, K., Chen, M., Zhao, Y., Burkey, K.O., Shew, H.D., Zobel, R.W., Zhang, Y., Hu, S., 2021. Warming and elevated ozone induce tradeoffs between fine roots and mycorrhizal fungi and stimulate organic carbon decomposition. Science Advances7, eabe9256.
CrossRef
Google scholar
|
[41] |
Rodriguez-Ramos, J.C., Cale, J.A., Cahill, J.F. Jr, Simard, S.W., Karst, J., Erbilgin, N., 2021. Changes in soil fungal community composition depend on functional group and forest disturbance type. New Phytologist229, 1105–1117.
CrossRef
Google scholar
|
[42] |
Rosseel, Y., 2012. lavaan: An R Package for structural equation modeling. Journal of Statistical Software48, 1–36.
CrossRef
Google scholar
|
[43] |
Rule, A., Dill, S., Sun, G., Chen, A., Khawaja, S., Li, I., Zhang, V., Rozelle, S., 2022. Challenges and opportunities in aligning conservation with development in China’s national parks: A narrative literature review. International Journal of Environmental Research and Public Health19, 12778.
CrossRef
Google scholar
|
[44] |
Schappe, T., Albornoz, F.E., Turner, B.L., Neat, A., Condit, R., Jones, F.A., 2017. The role of soil chemistry and plant neighbourhoods in structuring fungal communities in three Panamanian rainforests. Journal of Ecology105, 569–579.
CrossRef
Google scholar
|
[45] |
Selvalakshmi, S., Kalarikkal, R.K., Yang, X., 2020. Predicting the habitat distribution of rubber plantations with topography, soil, land use, and climatic factors. Environmental Monitoring and Assessment192, 598.
CrossRef
Google scholar
|
[46] |
Shinohara, Y., Ichinose, K., Morimoto, M., Kubota, T., Nanko, K., 2018. Factors influencing the erosivity indices of raindrops in Japanese cypress plantations. Catena171, 54–61.
CrossRef
Google scholar
|
[47] |
Song, Y.Y., Zeng, R.S., Xu, J.F., Li, J., Shen, X., Yihdego, W.G., 2010. Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS One5, e13324.
CrossRef
Google scholar
|
[48] |
Tetteh, E.N., Owusu Danquah, E., Abunyewa, A.A., Melenya Ocansey, C., Boakye, E.A., Tuffour, H.O., Logah, V., Twum-Ampofo, K., Dzomeku, B.M., Yeboah, S., Barnes, V.R., 2021. Plantain-tree rubber intercropping systems improved productivity in the tropical humid zone of Ghana, West Africa. International Journal of Agronomy2021, 1–16.
CrossRef
Google scholar
|
[49] |
Tongkaemkaew, U., Sukkul, J., Sumkhan, N., Panklang, P., Brauman, A., Ismail, R., 2018. Litterfall, litter decomposition, soil macrofauna, and nutrient contents in rubber monoculture and rubber-based agroforestry plantations. Forest and Society2, 138–149.
CrossRef
Google scholar
|
[50] |
Wagg, C., Schlaeppi, K., Banerjee, S., Kuramae, E.E., van der Heijden, M.G.A., 2019. Fungal-bacterial diversity and microbiome complexity predict ecosystem functioning. Nature Communications10, 4841.
CrossRef
Google scholar
|
[51] |
Walker, J.F., Aldrich-Wolfe, L., Riffel, A., Barbare, H., Simpson, N.B., Trowbridge, J., Jumpponen, A., 2011. Diverse Helotiales associated with the roots of three species of Arctic Ericaceae provide no evidence for host specificity. New Phytologist191, 515–527.
CrossRef
Google scholar
|
[52] |
Wang, J., Ren, C., Cheng, H., Zou, Y., Bughio, M.A., Li, Q., 2017. Conversion of rainforest into agroforestry and monoculture plantation in China: Consequences for soil phosphorus forms and microbial community. Science of the Total Environment595, 769–778.
CrossRef
Google scholar
|
[53] |
Wang, J., Zou, Y., Di Gioia, D., Singh, B.K., Li, Q., 2020. Conversion to agroforestry and monoculture plantation is detrimental to the soil carbon and nitrogen cycles and microbial communities of a rainforest. Soil Biology & Biochemistry147, 107849.
CrossRef
Google scholar
|
[54] |
Xiao, C., Li, P., Feng, Z., 2019. Monitoring annual dynamics of mature rubber plantations in Xishuangbanna during 1987–2018 using Landsat time series data: A multiple normalization approach. International Journal of Applied Earth Observation and Geoinformation77, 30–41.
CrossRef
Google scholar
|
[55] |
Yahya, M.S., Atikah, S.N., Mukri, I., Sanusi, R., Norhisham, A.R., Azhar, B., 2022. Agroforestry orchards support greater avian biodiversity than monoculture oil palm and rubber tree plantations. Forest Ecology and Management513, 120177.
CrossRef
Google scholar
|
[56] |
Yang, H., Zang, Y., Yuan, Y., Tang, J., Chen, X., 2012. Selectivity by host plants affects the distribution of arbuscular mycorrhizal fungi: evidence from ITS rDNA sequence metadata. BMC Evolutionary Biology12, 50.
CrossRef
Google scholar
|
[57] |
Yang, J., Zhai, D., Fang, Z., Alatalo, J.M., Yao, Z., Yang, W., Su, Y., Bai, Y., Zhao, G., Xu, J., 2023. Changes in and driving forces of ecosystem services in tropical southwestern China. Ecological Indicators149, 110180.
CrossRef
Google scholar
|
[58] |
Yu, L., Zi, H., Zhu, H., Liao, Y., Xu, X., Li, X., 2022. Rhizosphere microbiome of forest trees is connected to their resistance to soil-borne pathogens. Plant and Soil479, 143–158.
CrossRef
Google scholar
|
[59] |
Zeng, H., Wu, J., Singh, A.K., Zhu, X., Zhang, W., Hahn, P., Hölscher, D., Liu, W., 2022. Effect of intercrops complexity on water uptake patterns in rubber plantations: Evidence from stable isotopes (C-H-O) analysis. Agriculture, Ecosystems & Environment338, 108086.
CrossRef
Google scholar
|
[60] |
Zhang, C., Huang, C., Li, H., Liu, Q., Li, J., Bridhikitti, A., Liu, G., 2020. Effect of textural features in remote sensed data on rubber plantation extraction at different levels of spatial resolution. Forests11, 399.
CrossRef
Google scholar
|
[61] |
Zhang, J., Corlett, R.T., Zhai, D., 2019. After the rubber boom: good news and bad news for biodiversity in Xishuangbanna, Yunnan, China. Regional Environmental Change19, 1713–1724.
CrossRef
Google scholar
|
[62] |
Zhu, X., Chen, C., Wu, J., Yang, J., Zhang, W., Zou, X., Liu, W., Jiang, X., 2019. Can intercrops improve soil water infiltrability and preferential flow in rubber-based agroforestry system?. Soil & Tillage Research191, 327–339.
CrossRef
Google scholar
|
[63] |
Zou, X., Zhu, X., Zhu, P., Singh, A.K., Zakari, S., Yang, B., Chen, C., Liu, W., 2021. Soil quality assessment of different Hevea brasiliensis plantations in tropical China. Journal of Environmental Management285, 112147.
CrossRef
Google scholar
|
/
〈 | 〉 |