Soil biological quality in rhizosphere, growth, and yield of upland rice grown on acid soil after amended biochar enriched sap of Kappaphycus alvarezii




Abstract. Rakian TC, Kilowasid LMH, Afa LO, Riskyana A, Nurazizah, Wijayanti Y, Bahrun A, Subair I, Rahni NM, Alam S, Sarawa, Karimuna L. 2023. Soil biological quality in rhizosphere, growth, and yield of upland rice grown on acid soil after amended biochar enriched sap of Kappaphycus alvarezii. Biodiversitas 24: 6780-6792. Biological soil quality is essential in evaluating soil management practices using biochar enriched for upland rice growth on acid soil. Therefore, the study aimed to (i) analyze the effect of biochar-enriched sap of Kappaphycus alvarezii (K-sap) on the abundance of Arbuscular Mycorrhizae Fungi (AMF), bacteria, and protozoa in rhizosphere soil, growth, and yield of upland rice, and (ii) the relationship between the abundance of soil biota and the growth and yield components, as well as straw N, P, and K content on acid soil. Four upland rice were grown on acid soil incubated with biochar-enriched sap for two weeks in pots. Nine treatments of the biochar-enriched sap were tested, namely control, 5% biochar-0% K-sap, 5% biochar-5% K-sap, 5% biochar -10% K-sap, 5% biochar-15% K-sap, 7.5% biochar-0% K-sap, 7.5% biochar-5% K-sap, 7.5% biochar-10% K-sap, and 7.5% biochar-15% K-sap. Each treatment was three replicates in a randomized block design. The results demonstrated that the AMF spores quantity decreased while flagellates increased in the soil rhizosphere. The P and K content increased, the N:P decreased, and P:K ratio varied in the straw of the upland rice. Plant height and total spikelets increased, while root dry weight and roots to shoots ratio (R:S) decreased with biochar enriched. The abundance of AMF spores and flagellates correlated positively and negatively with R:S. Furthermore, R:S was negatively correlated with plant height and total spikelets. Plant height and total spikelets showed a positive correlation, while root dry weight and R:S was negatively correlated with K content in shoot tissue. The P and K contents with N:P ratio and N:P with P:K were negatively correlated. In conclusion, biochar-enriched K-sap effectively regulated the activity and composition of soil biota in the rhizosphere, influencing upland rice's growth, yield, and nutrient balance uptake on acid soils.


Agathokleous E, Belz RG, Kitao M, Koiko T, Calabrese EJ. 2019. Does the root to shoot ratio show a hormetic response to stress? an ecological and environmental perspective. J. For. Res. 30:1569–1580.
Alimi AA, Adeleke R, Moteetee A. 2021. Soil environmental factors shape the rhizosphere arbuscular mycorrhizal fungal communities in South African indigenous legumes (Fabaceae). Biodiversitas 22(5): 2466-2476. DOI: 10.13057/biodiv/d220503.
Aslan LOM, Embi AL, Hasriah R, Ansa A, Iba W, Patadjai AB, Rahim M, Armin. 2020. Grafting of the seaweed Kappaphycus alvarezii (Rhodophyta, Gigartinales) in SE-Sulawesi, Indonesia. Aquaculture Research 52(3): 1327-1331.
Ayaz M, Feizien? D, Tilvikien? V, Akhtar K, Stulpinait? U, Iqbal R. 2021. Biochar role in the sustainability of agriculture and environment. Sustainability 13:1330.
Azeem M, Hale L, Montgomery J, Crowley D, McGiffen ME, Jr. 2020. Biochar and compost effects on soil microbial communities and nitrogen induced respiration in turfgrass soils. PLoS ONE 15(11): e0242209. 10.1371/journal.pone.0242209.
Baki MZI, Suzuki K, Takahashi K, Chowdhury SA, Asiloglu R, Harada N. 2021. Molecular genetic characterization of arbuscular mycorrhizal fungi associated with upland rice in Bangladesh. Rhizosphere 18:100357.
Bandumula N. 2018. Rice production in Asia: key to global food security. Proc Natl Acad Sci India Sect B: Biol Sci. 88: 1323-1328.
Barus J. 2016. Utilization of crops residues as compost and biochar for improving soil physical properties and upland rice productivity. J. Degrade. Min. Land Manage. 3(4): 631-637. DOI:10.15243/jdmlm.2016.034.631.
Basavaraja PK, Yogendra ND, Zodape ST, Prakash R, Ghosh A. 2018. Effect of seaweed sap as foliar spray on growth and yield of hybrid maize. J. Plant Nutr. 41(14): 1851-1861. DOI: 10.1080/01904167.2018.1463381.
Bennett JA, Klironomos J. 2018. Mechanisms of plant–soil feedback: interactions among biotic and abiotic drivers. New Phytol. 222: 91–96. doi: 10.1111/nph.15603.
Blanco-Vargas A, Chacón-Buitrago MA, Quintero-Duque MC et al. 2022. Production of pine sawdust biochar supporting phosphate-solubilizing bacteria as an alternative bioinoculant in Allium cepa L. culture. Sci Rep 12: 12815.
Bonilla-Bedoya S, Valencia K, Herrera MA, Lopez-Ulloa M, Donoso DA, Pezzopane JEM. 2023. Mapping 50 years of contribution to the development of soil quality biological indicators. Ecol. Indic. 148:110091.
Borkar SG. 2018. Laboratory Techniques in Plant. CRC Press Taylor & Francis Group, London.
Brundrett MC, Bougher N, Dell B, Grove T, Malajczuk N. 1996. Working with Mycorrhizas in Forestry and Agriculture. AClAR Monograph, Canberra, Australia.
Campos López A, Uribe López JA, Cázares Ordoñez V, Garibay Orijel R, Valdez Cruz NA, Trujillo Roldán MA. 2022. Quercetin and 1 methyl 2 oxindole mimic root signaling that promotes spore germination and mycelial growth of Gigaspora margarita. Mycorrhiza 32: 177-191.
Campo S, Martín-Cardoso H, Olivé M, Pla E, Catala-Forner M, Martínez-Eixarch M, Segundo BS. 2020. Effect of root colonization by arbuscular mycorrhizal fungi on growth, productivity and blast resistance in rice. Rice 13:42.
Chao SJ, Kim MH, Lee YO. 2016. Effect of pH on soil bacterial diversity. Journal of Ecology and Environment 40:10.
Chen CL, Song WL, Sun L, Qin S, Ren CG, Yang JC, Feng DW, Liu N, Yan J, Cui BB, Zhong ZH, Li QQ, Liu ZD, Liu ZY. 2022. Effects of seaweed extract supplement on rice rhizosphere bacterial community in tillering and heading stages. Agronomy 12:342.
Chowdhury S, Lange M, Malik AA et al. 2022. Plants with arbuscular mycorrhizal fungi efficiently acquire Nitrogen from substrate additions by shaping the decomposer community composition and their net plant carbon demand. Plant Soil 475: 473–490.
Cox J, Hue NV, Ahmad A, Kobayashi KD. 2021. Surface-applied or incorporated biochar and compost combination improves soil fertility, Chinese cabbage and papaya biomass. Biochar 3:213-227.
Dalpé Y, Séguin SM. 2013. Microwave-assisted technology for the clearing and staining of arbuscular mycorrhizal fungi in roots. Mycorrhiza 23: 333–340.
Das SK, Ghosh GK, Avasthe R. 2023. Application of biochar in agriculture and environment, and its safety issues. Biomass Conv. Bioref. 13: 1359-1369.
Deolu?Ajayi AO, van der Meer IM, van der Werf A, Karlova R. 2022. The power of seaweeds as plant biostimulants to boost crop production under abiotic stress. Plant Cell Environ. 45:2537–2553. DOI: 10.1111/pce.14391.
de Vries FT, Caruso T. 2016. Eating from the same plate? Revisiting the role of labile carbon inputs in the soil food web. Soil Biol. Biochem. 102:4-9.
Egamberdieva D, Ma H, Shurigin V, Alimov J, Wirth S, Bellingrath-Kimura SD. 2022. Biochar additions alter the abundance of P-cycling-related bacteria in the rhizosphere soil of Portulaca oleracea L. under salt stress. Soil Syst. 6:64. soilsystems6030064.
Fageria NK, Oliveira JP. 2014. Nitrogen, phosphorus and potassium interactions in upland rice. J. Plant Nutr. 37(10): 1586-1600. DOI:10.1080/01904167.2014.920362.
Gafur S, Umran I. 2019. Upland rice growth after low-input amendments on upland soil in West Kalimantan, Indonesia. J. Trop Soils 24(3): 119-128. Doi: 10.5400/jts.2019.v24i3.119.
Hagemann N, Joseph S, Schmidt HP et al. 2017. Organic coating on biochar explains its nutrient retention and stimulation of soil fertility. Nat. Commun. 8:1089. DOI: 10.308/s41467-017-01123-0.
Hines S, van der Zwan T, Shiell K, Shotton K, Prithiviraj B. 2021. Alkaline extract of the seaweed Ascophyllum nodosum stimulates arbuscular mycorrhizal fungi and their endomycorrhization of plant roots. Sci. Rep. 11:13491.
Holatko J, Hammerschmiedt T, Kinti A et al. 2021. Effect of carbon-enriched digestate on the microbial soil activity. Plos One 16(7): e0252262.
Hossain MZ, Bahar MM, Sarkar B et al. 2020. Biochar and its importance on nutrient dynamics in soil and plant. Biochar 2: 379-420.
Iqbal MT, Ahmed IAM, Isik M, Sultana F, Orta? I. 2020. Role of mycorrhizae inoculations on nutrient uptake in rice grown under aerobic and anaerobic water management. J. Plant Nutr. 44(4):550-568. DOI: 10.1080/01904167.2020.1845375.
Jabborova D, Annapurna K, Al-Sadi AM et al. 2021. Biochar and Arbuscular mycorrhizal fungi mediated enhanced drought tolerance in Okra (Abelmoschus esculentus) plant growth, root morphological traits and physiological properties. Saudi J. Biol. Sci. 28: 5490–5499.
Kalamulla R, Sandaruwan D, Karunarathna SC et al. 2022. Assessment of community dynamics of arbuscular mycorrhizal fungi in the rice (Oryza sativa L.) rhizosphere and potential application as biofertilizer. Sustainability 14: 16537. su142416537.
Kasim, M. 2016. Makroalga: Kajian biologi, ekologi, pemanfaatan, dan budidaya. Penebar Swadaya, Jakarta.
Kikuta M, Makihara D, Pasolon YB, Rembon FS, Miyazaki A, Yamamoto Y. 2020. Agronomic traits and grain quality of upland rice cultivated in southeast Sulawesi, Indonesia. J Intl Cooper Agric Dev. 18: 41-47.
Kikuta M, Yamamato Y, Pasolon YB, Rembon FS, Miyazaki A, Makihara D. 2016. How growth and yield of upland rice vary with topographic conditions: a case of slash-and-burn rice farming in South Konawe Regency, Southeast Sulawesi Province, Indonesia. Trop. Agr. Develop. 60(3): 162-171.
Kikuta M, Yamamoto Y, Pasolon YB, Rembon FS, Miyazaki A, Makihara D. 2018. Effect of slope-related soil properties on upland rice growth and yield under slash-and-burn system in South Konawe Regency, Southeast Sulawesi Province, Indonesia. Trop. Agr. Develop. 62(2): 60-67.
Kilowasid LMH, Hasmar LOJ, Afa LO, Sutariati GAK, Namriah, Rakian TC. 2021. Effect of cogongrass (Imperata cylindrica L.) root extract on earthworms, arbuscular mycorrhizae fungi spore, and growth of upland rice (Oryza sativa L.) for local Kambowa variety. IOP Conf. Seri.: Earth Environ. Sci. 87:032034. doi:10.1088/1755-1315/807/032034.
Kilowasid LMH, Manik DS, Nevianti, Komang GA, Mutmainna P, Afa LO, Rakian TC, Hisein WSA, Ramadhan LOAN, Alam S. 2023a. The quality of acid soils treated with seaweed (Kappapychus alvarezii) sap enriched biochar from Southeast Sulawesi, Indonesia. J. Degrade. Min. Land Manage. 10 (2): 4255-4269. doi:10.15243/jdmlm.2023.102.4255.
Kilowasid LMH, Manik DS, Nevianti, Afa LO, Rakian TC, Hisein WSA, Sadimantara GR, Sarawa, Halim. 2023b. Effect of biochar on arbuscular mycorrhizae fungi, nutrient uptake and growth of local upland rice, Southeast Sulawesi, Indonesia. IOP Conf. Seri.: Earth Environ. Sci. 1162:012006. doi:10.1088/1755-1315/1162/1/012006.
Krauss M, Berner A, Perrochet F, Frei R, Niggli U, Mäder P. 2020. Enchanced soil quality with reduced tillage and solid manures in organic farming-a synthesis of 15 years. Sci. Rep. 10:4403.
Kuwada K, Wamocho LS, Utamura M, Matsushita I, Isii T. 2006. Effects of red and green extracts on hyphal growth of arbuscular mycorrhizal fungi, and on mycorrhizal development and growth of papaya and passionfruit. Agron. J. 98:1340-1344. doi:10.1234/agronj2005.0354.
Leboffe MJ, Pierce BE. 2011. A photographic atlas for the microbiology laboratory. 4th edition, Morton, Colorado.
Lee J, Kim H-S, Jo HY, Kwon MJ. 2021. Revisiting soil bacterial counting methods: Optimal soil storage and pretreatment methods and comparison of culture-dependent and -independent methods. PLoS ONE 16(2): e0246142. pone.0246142.
Liu M, Che Y, Wang L, Zhao Z, Zhang Y, Wei L, Xiao Y. 2019a. Rice straw biochar and phosphorus inputs have more positive effects on the yield and nutrient uptake of Lolium multiflorum than arbuscular mycorrhizal fungi in acidic Cd-contaminated soils. Chemosphere 235:32-39.
Liu T, Yang L, Hu Z et al., Xue J, Lu Y, Chen X, Griffiths BS, Whalen JK, Liu M. 2020. Biochar exerts negative effects on soil fauna across multiple trophic levels in a cultivated acidic soil. Biol. Fertil. Soils 56:597-606.
Liu X, Feng Z, Zhu H, Yao Q. 2019b. Exogenous abscisic acid and root volatiles increase sporulation of Rhizophagus irregularis DAOM 197198 in asymbiotic and pre-symbiotic status. Mycorrhiza 29:581–589.
Marizal S, Muzakir, Syariyah A. 2016. The diversity of arbuscular mycorrhiza fungus (AMF) indigenous in peanuts (Arachis hypogea L) rhizosphere under different elevation. J Trop Soils 21 (2): 109-114. DOI: 10.5400/jts.2016.21.2.109.
Murniati K, Mutolib A. 2020. The impact of climate change on the household food security of upland rice farmers in Sidomulyo, Lampung Province, Indonesia. Biodiversitas 21(8): 3487-3493. DOI:10.13057/biodiv/d210809.
Nasslahsen B, Prin Y, Ferhout H, Smouni A, Duponnois R. 2022. Mycorrhizae helper bacteria for managing the mycorrhizal soil infectivity. Front. Soil Sci. 2:979246. doi: 10.3389/fsoil.2022.979246.
Ndoung OCN, de Figueiredo CC, Ramos MLG. 2021. A scoping review on biochar-based fertilizer: enrichment technique and agro-environmental application. Heliyon 7: e08473.
Olubodea AA, Babalolaa OA, Darea OM, Adeyemi NO, Aderibigbe SG, Okonji CJ, Sakariyawo OS. 2020. Diversity of indigenous arbuscular mycorrhizal fungi in rhizosphere of upland rice (Oryza sativa L.) varieties in Southwest Nigeria. Acta Fytotech. Zootech. 23(2): 42–48.
Ordoñez YM, Fernandez BR, Lara LS, Rodriguez A, Uribe-Vélez D, Sanders IR. 2016. Bacteria with phosphate solubilizing capacity alter mycorrhizal fungal growth both inside and outside the root and in the presence of native microbial communities. PLoS ONE 11(6): e0154438. doi:10.1371/journal.pone.0154438.
Ouyang W, Yin X, Yang J, Struik PC. 2021. Do shoot anatomical characteristics allow rice to grow well under water deficit? J. Agron. Crop Sci. 208 (6): 763-955. DOI: 10.1111/jac.12509.
Panahi HKS, Dehhaghi M, Ok YS, Nizami AS, Khoshnevisan B, Mussatto SI, Aghbashlo M, Tabatabaei M, Lam SS. 2020. A comprehensive review of engineered biochar: Production, characteristics, and environmental applications. J. Clean. Prod. 270:122462.
Pang Z, Zhao Y, Xu P, Yu D. 2020. Microbial diversity of upland rice roots and their influence on rice growth and drought tolerance. Microorganisms 8(9): 1329. DOI: 10.3390/microorganisms8091329.
Peng J, Han X, Lin N et al. 2021. Combined application of biochar with fertilizer promotes nitrogen uptake in maize by increasing nitrogen retention in soil. Biochar 3:367-379.
Powers EM. 1995. Efficacy of the ryu nonstaining KOH technique for rapidly determining gram reactions of food-borne and waterborne bacteria and yeasts. Appl. Environ. Microbiol. 61(10): 3756–3758. doi: 10.1128/aem.61.10.3756-3758.1995.
Pressler Y, Foster EJ, Moore JC, Cotrufo MF. 2017. Coupled biochar amendment and limited irrigation strategies do not affect a degraded soil food web in a maize agroecosystem, compared to the native grassland. GCB Bioenergy 9:1344–1355. doi: 10.1111/gcbb.12429.
Sainju UM, Allen BL, Lenssen AW, Ghimire RP. 2017. Root biomass, root/shoot ratio, and soil water content under perennial grasses with different nitrogen rates. Field Crops Res. 210: 183-191
Saleem M, Fetzer I, Harms H, Chatzinotas A. 2016 Trophic complexity in aqueous systems: bacterial species richness and protistan predation regulate dissolved organic carbon and dissolved total nitrogen removal. Proc. R. Soc. B 283: 20152724.
Sarkodee-Addo E, Yasuda M, Lee CG, Kanasugi M, Fujii Y, Omari RA, Abebrese SO, Bam R, Asuming-Brempong S, Dastogeer KMG, Okazaki S. 2020. Arbuscular mycorrhizal fungi associated with rice (Oryza sativa L.) in Ghana: effect of regional locations and soil factors on diversity and community assembly. Agronomy 10: 559. doi:10.3390/agronomy10040559.
Sefrila M, Ghulamahdi M, Purwono, Melati M, Mansur I. 2021. Diversity and abundance of arbuscular fungi mycorrhizal (AMF) in rhizosphere Zea mays in tidal swamp. Biodiversitas 22 (11): 5071- 5076 DOI: 10.13057/biodiv/d221144.
Shi Y, Li Y, Yang T, Chu H. 2021. Threshold effects of soil pH on microbial co-occurrence structure in acidic and alkaline arable lands. Sci. Total Environ. 800:149592.
Sudewi S, Ala A, Baharuddin, Farid M. 2020. The isolation, characterization endophytic bacteria from roots of local rice plant Kamba in, Central Sulawesi, Indonesia. Biodiversitas 21(4): 1614-1624. DOI: 10.13057/biodiv/d210442.
Sugiura Y, Akiyamaa R, Tanakab S et al. 2020. Myristate can be used as a carbon and energy source for the asymbiotic growth of arbuscular mycorrhizal fungi. PNAS 117 (41): 25779–25788.
Sujarwo, Hanani N. 2016. Development of food security in Indonesia. Agricultural Socio-Economics Journal XVI (01): 12-20.
Sustr M, Soukup A, Tylova E. 2019. Potassium in root growth and development. Plants 8:435. doi:10.3390/plants8100435.
Syaf H, Pattah MA, Kilowasid LMH. 2021. Quality of soil from the nickel mining area of Southeast Sulawesi, Indonesia, engineered using earthworms (Pheretima sp.). J. Degrade. Min. Land Manage. 8(4): 2995-3005. doi: 10.15243/jdmlm.2021.084.2995.
Syahrinudin, Hartati W, Sudarmadji T, Krisdianto N, Ibrahim. 2019. Biochar enriched with organic fertilizer improves the survival and growth rate of Anthocepalus cadamba seedlings planted on degraded spodosols. Biodiversitas 20(12): 3471-3750.
Temjen W, Singh MR, Ajungla, T. 2022. Effect of shifting cultivation and fallow on soil quality index in Mokokchung District, Nagaland, India. Ecol Process 11:42.
Tian X, Li Z, Wang Y, Li B, Wang L. 2021. Evaluation on soil fertility quality under biochar combined with nitrogen reduction. Sci. Rep. 11:13792.
Vafa ZN, Sohrabi Y, Mirzaghaderi G, Heidari G. 2022. Soil microorganisms and seaweed application with supplementary irrigation improved physiological traits and yield of two dryland wheat cultivars. Front. Plant Sci. 13:855090. doi: 10.3389/fpls.2022.855090.
Vaghela P, Das AK, Trivedi K, Anand KGV, Shinde P, Ghosh A. 2022. Characterization and metabolomics profiling of Kappaphycus alvarezii seaweed extract. Algal Res. 66:102774.
Videgain-Marco M, Marco-Montori P, Martí-Dalmau C, Jaizme-Vega Md C, Manyà-Cervelló JJ, García-Ramos FJ. 2021. The Effects of Biochar on Indigenous Arbuscular Mycorrhizae Fungi from Agroenvironments. Plants 10:950. plants10050950.
Vieira FCS, Nahas E. 2005. Comparison of microbial numbers in soils by using varioua culture media and temperatures. Microbiol. Res. 160:197-202. doi:10.1016/j.micres.2005.01.004.
Wang C, Chen D, Shen J, Yuan Q, Fan F, Wei W, Li Y, Wu J. 2021. Biochar alters soil microbial communities and potential functions 3–4 years after amendment in a double rice cropping system. Agric. Ecosyst. Environ. 311:107291.
Wang Y, Chen YF, Wu WH. 2021. Potassium and phosphorus transport and signaling in plants. J. Integr. Plant Biol. 63: 34–52.
Xu W, Whitman WB, Gundale MJ, Chien CC, Chiu CY. 2020. Functional response of the soil microbial community to biochar applications. GCB Bioenergy 13:269–281. DOI: 10.1111/gcbb.12773.
Yin D, Li H, Wang H, Guo X, Wang Z, Lv Y, Ding G, Jin L, Lan Y. 2021. Impact of different biochars on microbial community structure in the rhizospheric soil of rice grown in Albic soil. Molecules 26:4783.
Ying HS, Wasli MEB, Perumal, M. 2018. Soil characteristics under intensified shifting cultivation for upland rice cultivation in upland Sabal, Sarawak, Malaysia. Biotropia 25(1): 72 – 83. DOI: 10.11598/Btb.2018.25.1.799.
Zhang J, Shen JL. 2022. Effects of biochar on soil microbial diversity and community structure in clay soil. Ann. Microbiol. 72:35.
Zheng N, Yu Y, Shi W, Yao H. 2019. Biochar suppresses N2O emissions and alters microbial communities in an acidic tea soil. Environ Sci Pollut Res 26:35978–35987.

Most read articles by the same author(s)