Abstract
Biological weathering of soil minerals is important from soil fertility and soil evolution points of view. Little information is available on the interaction influence of earthworm and rhizosphere on soil mineral bio-weathering and nutrient release. The objectives of this investigation were (a) to examine if earthworm could alter phlogopite (a micaceous mineral) and (b) to study root-induced weathering and potassium (K) release. A mixture of cow manure and phlogopite was incubated with or without the earthworm Eisenia fetida for two time periods of 3 and 6 months to produce enriched vermicompost and compost, respectively. A greenhouse pot experiment was then carried out where barley was grown for 2 months in the pots containing phlogopite-enriched vermicompost or compost produced in the first experiment. Mineralogical changes in phlogopite and also selected chemical properties were evaluated. The results showed a significant effect of earthworm activity and incubation period on phlogopite weathering, C/N ratio (from 24.3 to 13.9), available K (from 1.24 to 1.34%), and HNO3-extractable K (from 2 to 2.4%). The highest dry weight and the concentration and uptake of K were found in the plants cultivated in vermicompost incubated for 6 months. Also, the results indicated that under the incubation conditions, earthworm activities resulted in the dominance of the vermiculitization process. In contrast, transformation to smectite was dominant in the barley rhizosphere. Earthworm activities accelerated the rate of mineral transformation and element release, which led to an increase in the available form of elements. Such an element release was also enhanced in plant rhizosphere, which consequently increased the yield.
Similar content being viewed by others
References
Balachandar R, Baskaran L, Yuvaraj A, Thangaraj R, Subbaiya R, Ravindran B, Chang SW, Karmegam N (2020) Enriched pressmud vermicompost production with green manure plants using Eudrilus eugeniae. Bioresour Technol 299:122578. https://doi.org/10.1016/j.biortech.2019.122578
Barker WW, Welch SA, Banfield JF (1997) Biogeochemical weathering of silicate minerals. In: Banfield JF, Nealson KH (eds) Geomicrobiology: interactions between microbes and minerals. Reviews in Mineralogy. Mineralogical Society of America, Washington, DC, 391–428
Basak BB, Biswas DR (2009) Influence of potassium solubilizing microorganism (Bacillus mucilaginosus) and waste mica on potassium uptake dynamics by Sudan grass (Sorghum vulgare Pers.) grown under two Alfisols. Plant Soil 317:235–255. https://doi.org/10.1007/s11104-008-9805-z
Basak BB, Sarkar B, Biswas DR, Sarkar S, Sanderson P, Naidu R (2017) Bio-intervention of naturally occurring silicate minerals for alternative source of potassium: challenges and opportunities. Adv Agron 141:115–145. https://doi.org/10.1016/bs.agron.2016.10.016
Basker A, Macgregor AN, Kirkman JH (1992) Influence of soil ingestion by earthworms on the availability of potassium in soil: An incubation experiment. Biol Fertil Soils 14:300–303. https://doi.org/10.1007/BF00395467
Bigham JM, Bhatti TM, Vuorinen A, Tuovinen OH (2001) Dissolution and structural alteration of phlogopite mediated by proton attack and bacterial oxidation of ferrous iron. Hydrometallurgy 59:301–309. https://doi.org/10.1016/S0304-386X(00)00186-9
Binet F, Fayolle L, Pussard M, Crawford JJ, Traina SJ, Tuovinen OH (1998) Significance of earthworms in stimulating soil microbial activity. Biol Fertil Soils 27:79–84. https://doi.org/10.1007/s003740050403
Biruntha M, Karmegam N, Archana J, Selvi BK, Paul JAJ, Balamuralikrishnan B, Chang SW, Ravindran B (2020) Vermiconversion of biowastes with low-to-high C/N ratio into value added vermicompost. Bioresour Technol 297:122398. https://doi.org/10.1016/j.biortech.2019.122398
Bityutskii NP, Maiorov EI, Orlova NE (2012) The priming effects induced by earthworm mucus on mineralization and humification of plant residues. Eur J Soil Biol 50:1–6. https://doi.org/10.1016/j.ejsobi.2011.11.008
Blouin M, Hodson ME, Delgado EA, Baker G, Brussaard L, Butt KR, Dai J, Dendooven L, Pérès G, Tondoh JE (2013) A review of earthworm impact on soil function and ecosystem services. Eur J Soil Sci 64:161–182. https://doi.org/10.1111/ejss.12025
Bremner JM (1996) Nitrogen‐total. In: Sparks D (ed) Methods of soil analysis: Part 3 Chemical methods. SSSA/ASA, Madison, 1085–1121
Brown GG, Edwards CA, Brussaard L (2004) How earthworms affect plant growth: burrowing into the mechanisms. In: Edwards CA (ed) Earthworm ecology. CRC Press Boca Raton, FL, pp 13–49
Calvaruso C, Mareschal L, Turpault M-P, Leclerc E (2009) Rapid clay weathering in the rhizosphere of Norway spruce and oak in an acid forest ecosystem. Soil Sci Soc Am J 73:331–338. https://doi.org/10.2136/sssaj2007.0400
Carpenter D, Hodson ME, Eggleton P, Kirk C (2007) Earthworm induced mineral weathering: preliminary results. Eur J Soil Biol 43:S176–S183. https://doi.org/10.1016/j.ejsobi.2007.08.053
Darwin C (1881) The formation of vegetable mould through the action of worms: with observations on their habits. John Murray, London
De Souza MEP, Cardoso IM, de Carvalho AMX, Lopes AP, Jucksch I (2019) Gneiss and steatite vermicomposted with organic residues: release of nutrients and heavy metals. Int J Recycl Org Waste Agric 8:233–240. https://doi.org/10.1007/s40093-019-0244-z
De Souza MEP, Cardoso IM, De Carvalho AMX, Lopes AP, Jucksch I, Janssen A (2018) Rock powder can improve vermicompost chemical properties and plant nutrition: an on-farm experiment. Commun Soil Sci Plant Anal 49:1–12. https://doi.org/10.1080/00103624.2017.1418372
De Souza MEP, de Carvalho AMX, de Cássia DD, Jucksch I, Brown GG, Mendonça ES, Cardoso IM (2013) Vermicomposting with rock powder increases plant growth. Appl Soil Ecol 69:56–60. https://doi.org/10.1016/j.apsoil.2013.01.016
Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms. Springer Science and Business Media, Germany
Edwards CA, Fletcher KE (1988) Interactions between earthworms and microorganisms in organic matter breakdown. Agric Ecosyst Environ 24:235–247. https://doi.org/10.1016/0167-8809(88)90069-2
Fageria NK, Stone LF (2006) Physical, chemical, and biological changes in the rhizosphere and nutrient availability. J Plant Nutr 29:1327–1356. https://doi.org/10.1080/01904160600767682
Fanning DS, Keramidas VZ, El-Desoky MA (1989) Micas. In: Dixon J, Weed S (eds) Minerals in soil environments. SSSA, Madison, WI, pp 551–634
Glowa KR, Arocena JM, Massicotte HB (2004) Properties of soils influenced by ectomycorrhizal fungi in hybrid spruce [Picea glauca × engelmannii (Moench.) Voss]. Can J Soil Sci 84:91–102. https://doi.org/10.4141/S03-031
Hinsinger P, Elsass F, Jaillard B, Robert M (1993) Root-induced irreversible transformation of a trioctahedral mica in the rhizosphere of rape. J Soil Sci 44:535–545. https://doi.org/10.1111/j.1365-2389.1993.tb00475.x
Horn MA, Schramm A, Drake HL (2003) The earthworm gut: an ideal habitat for ingested N2O-producing microorganisms. Appl Environ Microbiol 69:1662–1669. https://doi.org/10.1128/AEM.69.3.1662-1669.2003
Hu L, Xia M, Lin X, Xu C, Li W, Wang J, Zeng R, Song Y (2018) Earthworm gut bacteria increase silicon bioavailability and acquisition by maize. Soil Biol Biochem 125:215–221. https://doi.org/10.1016/j.soilbio.2018.07.015
Jackson ML (1979) Soil chemical analysis: advanced course. University of Wisconsin, Madison
Jakobsen I, Leggett ME, Richardson AE (2005) Rhizosphere microorganisms and plant phosphorus uptake. In: Sims J, Sharpley A (eds) Phosphorus: agriculture and the environment. SSSA, Madison, WI, pp 437–494
Khayamim F, Khademi H, Sabzalian MR (2011) Effect of Neotyphodium endophyte-tall fescue symbiosis on mineralogical changes in clay-sized phlogopite and muscovite. Plant Soil 341:473–484. https://doi.org/10.1007/s11104-010-0659-9
Knudsen D, Peterson GA, Pratt PF (1983) Lithium, sodium, and potassium. In: Page A (ed) Methods of soil analysis: Part 2 Chemical and microbiological properties. SSSA/ASA, Madison, pp 225–246
Lee KE (1985) Earthworms: their ecology and relationships with soils and land use. Academic Press Inc.
Lim CH, Jackson ML (1983) Dissolution for total elemental analysis. In: Page A (ed) Methods of soil analysis: Part 2 Chemical and microbiological properties. SSSA/ASA, Madison, pp 1–12
Liu D, Lian B, Wang B, Jiang G (2011) Degradation of potassium rock by earthworms and responses of bacterial communities in its gut and surrounding substrates after being fed with mineral. PLoS ONE 6:1–17. https://doi.org/10.1371/journal.pone.0028803
Needham SJ, Worden RH, Mcilroy D (2004) Animal-sediment interactions: the effect of ingestion and excretion by worms on mineralogy. Biogeosciences 1:113–121. https://doi.org/10.5194/bg-1-113-2004
Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. In: Sparks D (ed) Methods of soil analysis: Part 3 Chemical methods. SSSA/ASA, Madison, pp 961–1010
Norouzi S, Khademi H (2010) Ability of alfalfa (Medicago sativa L.) to take up potassium from different micaceous minerals and consequent vermiculitization. Plant Soil 328:83–93. https://doi.org/10.1007/s11104-009-0084-0
OECD (1984) OECD guideline for testing of chemicals. No. 207. Earthworm, acute toxicity tests. OECD-guideline for testing chemicals, Paris
Rahimzadeh N, Khormali F, Olamaee M, Amini A, Dordipour E (2015) Effect of canola rhizosphere and silicate dissolving bacteria on the weathering and K release from indigenous glauconite shale. Biol Fertil Soils 51:973–981. https://doi.org/10.1007/s00374-015-1043-y
Rini J, Deepthi MP, Saminathan K, Narendhirakannan RT, Karmegam N, Kathireswari P (2020) Nutrient recovery and vermicompost production from livestock solid wastes with epigeic earthworms. Bioresour Technol 313:123690. https://doi.org/10.1016/j.biortech.2020.123690
Senapati BK, Dash MC, Rana AK, Panda BK (1980) Observation on the effect of earthworm in the decomposition process in soil under laboratory conditions. Comp Physiol Ecol 5:140–142
Shahrokh V, Khademi H, Cano AF, Acosta JA (2019) Different forms of soil potassium and clay mineralogy as influenced by the lemon tree rhizospheric environment. Int J Environ Sci Technol 16:3979–3988. https://doi.org/10.1007/s13762-018-1805-9
Suzuki Y, Matsubara T, Hoshino M (2003) Breakdown of mineral grains by earthworms and beetle larvae. Geoderma 112:131–142. https://doi.org/10.1007/s13762-018-1805-9
Szmigielska AM, Van Rees KCJ, Cieslinski G, Huang PM (1996) Low molecular weight dicarboxylic acids in rhizosphere soil of durum wheat. J Agric Food Chem 44:1036–1040. https://doi.org/10.1021/jf950272z
Vandevivere P, Welch SA, Ullman WJ, Kirchman DL (1994) Enhanced dissolution of silicate minerals by bacteria at near-neutral pH. Microb Ecol 27:241–251. https://doi.org/10.1007/BF00182408
Wilson MJ (2004) Weathering of the primary rock-forming minerals: processes, products and rates. Clay Miner 39:233–266. https://doi.org/10.1180/0009855043930133
Zhu X, Lian B, Yang X, Liu C, Zhu L (2013) Biotransformation of earthworm activity on potassium-bearing mineral powder. J Earth Sci 24:65–74. https://doi.org/10.1007/s12583-013-0313-6
Acknowledgements
The authors are grateful to the Iranian National Science Foundation (grant no. 96002378) for financially supporting this research. They are also very thankful to Isfahan University of Technology, Iran, and Technical University of Cartagena, Spain, for helping in sample analyses. We would like to thank four anonymous reviewers who carefully reviewed the original or the revised version of this manuscript. Their great comments and suggestions improved the quality of this paper substantially.
Funding
This study was supported by the Iranian National Science Foundation (96002378).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Jafari, F., Khademi, H., Shahrokh, V. et al. Earthworm- and Rhizosphere-Induced Biological Weathering of Phlogopite. J Soil Sci Plant Nutr 22, 416–427 (2022). https://doi.org/10.1007/s42729-021-00658-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-021-00658-y