The use of soil biostructures created by soil fauna ecosystem engineers fed with different organic materials as inoculum source of arbuscular mycorrhiza fungi on cocoa seedling

Laode Muhammad Harjoni Kilowasid, Muhammad Fahyu Sanjaya, Laode Sabaruddin, Rachmawati Hasid, Darwis Sulaeman, Andi Nurmas

Abstract

Soil fauna as ecosystem engineers have the ability to create soil biostructures, with the capacity to save arbuscular mycorrhizal fungi (AMF) spores. This study therefore aims to investigate the AMF spore density in the biostructures created by cooperation between earthworms and ants with a different organic matter composition, and to analyze the biostructures’ potential as a source of AMF inoculum on cocoa seedlings. In the first experiment, a combination of earthworms and ants composition, as well as a mixture of G. sepium leaf (GLP), cocoa shell bean (CSB), and sago dregs (SD), was tested. Meanwhile, in the second experiment, the effect of biostructures on cocoa seedlings grown in unsterile soil,was examined. According to the results, the highest AMF spore density was obtained using 20 earthworms+10 ants with 50%GLP+50%CSB + 0%SD treatment. Furthermore, the total AMF spores were positively correlated with the total P value, but negatively correlated with the C/N ratio. Therefore, biostructure application increased AMF spores number in rhizosphere and the cocoa seedling’s root infection. Furthermore, biostructures resulting from the collaborative activity between different soil fauna ecosystem engineers were able to transmit AMF spores to infected plant roots growing in non-sterile soil.

Full Text:

PDF

References

Aggangan, N. S., Cortes, A. D., & Reaño, C. E. (2019). Growth response of cacao (Theobroma cacao L.) plant as affected by bamboo biochar and arbuscular mycorrhizal fungi in sterilized and unsterilized soil. Biocatalysis and Agricultural Biotechnology, 22, 101347. https://doi.org/10.1016/j.bcab.2019.101347

Alimi, A., Adeleke, R., & Moteetee, A. (2021). Soil environmental factors shape the rhizosphere arbuscular mycorrhizal fungal communities in South African indigenous legumes (Fabaceae). Biodiversitas Journal of Biological Diversity, 22(5). https://doi.org/10.13057/biodiv/d220503

Almeida, A., Mitchell, A. L., Boland, M., Forster, S. C., Gloor, G. B., Tarkowska, A., Lawley, T. D., & Finn, R. D. (2019). A new genomic blueprint of the human gut microbiota. Nature, 568(7753), 499-504. https://doi.org/10.1038/s41586-019-0965-1

Asano, K., Kagong, W. V. A., Mohammad, S. M. B., Sakazaki, K., Talip, M. S. A., Sahmat, S. S., Chan, M. K. Y., Isoi, T., Kano-Nakata, M., & Ehara, H. (2021). Arbuscular Mycorrhizal Communities in the Roots of Sago Palm in Mineral and Shallow Peat Soils. Agriculture, 11(11), 1161. https://doi.org/10.3390/agriculture11111161

Azizah Chulan, H. (1991). Effect of fertilizer and endomycorrhizal inoculum on growth and nutrient uptake of cocoa (Theobroma cacao L.) seedlings. Biology and Fertility of Soils, 11(4), 250-254. https://doi.org/10.1007/BF00335843

Bagy Araji, D. J., & Powell, C. L. (1985). Effect of vesicular-arbuscular mycorrhizal inoculation and fertiliser application on the growth of marigold. New Zealand Journal of Agricultural Research, 28(1), 169-173. https://doi.org/10.1080/00288233.1985.10427012

Bahrun, A., Fahimuddin, M., Safuan, L., Kilowasid, L. M., & Singh, R. (2018). Effects of cocoa pod husk biochar on growth of cocoa seedlings in Southeast Sulawesi-Indonesia. Asian J. Crop Sci, 10(1), 22-33. https://doi.org/10.3923/ajcs.2018.22.30

Boots, B., Keith, A. M., Niechoj, R., Breen, J., Schmidt, O., & Clipson, N. (2012). Unique soil microbial assemblages associated with grassland ant species with different nesting and foraging strategies. Pedobiologia, 55(1), 33-40. https://doi.org/10.1016/j.pedobi.2011.10.004

Bottinelli, N., Jouquet, P., Capowiez, Y., Podwojewski, P., Grimaldi, M., & Peng, X. (2015). Why is the influence of soil macrofauna on soil structure only considered by soil ecologists? Soil and Tillage Research, 146, 118-124. https://doi.org/10.1016/j.still.2014.01.007

Briones, M. J. I. (2014). Soil fauna and soil functions: a jigsaw puzzle [Review]. Frontiers in Environmental Science, 2(7). https://doi.org/10.3389/fenvs.2014.00007

Cely, M. V. T., de Oliveira, A. G., de Freitas, V. F., de Luca, M. B., Barazetti, A. R., dos Santos, I. M. O., Gionco, B., Garcia, G. V., Prete, C. E. C., & Andrade, G. (2016). Inoculant of Arbuscular Mycorrhizal Fungi (Rhizophagus clarus) Increase Yield of Soybean and Cotton under Field Conditions [Original Research]. Frontiers in Microbiology, 7(720). https://doi.org/10.3389/fmicb.2016.00720

Cobb, A. B., Wilson, G. W. T., Goad, C. L., & Grusak, M. A. (2018). Influence of alternative soil amendments on mycorrhizal fungi and cowpea production. Heliyon, 4(7). https://doi.org/10.1016/j.heliyon.2018.e00704

Cunha, L., Brown, G. G., Stanton, D. W. G., Da Silva, E., Hansel, F. A., Jorge, G., McKey, D., Vidal-Torrado, P., Macedo, R. S., Velasquez, E., James, S. W., Lavelle, P., Kille, P., & Network, t. T. P. d. I. (2016). Soil Animals and Pedogenesis: The Role of Earthworms in Anthropogenic Soils. Soil Science, 181(3/4), 110-125. https://doi.org/10.1097/ss.0000000000000144

de Menezes, A. B., Prendergast-Miller, M. T., Macdonald, L. M., Toscas, P., Baker, G., Farrell, M., Wark, T., Richardson, A. E., & Thrall, P. H. (2018). Earthworm-induced shifts in microbial diversity in soils with rare versus established invasive earthworm populations. FEMS Microbiology Ecology, 94(5), fiy051. https://doi.org/10.1093/femsec/fiy051

Dhar, P. P., & Mridha, M. A. U. (2012). Arbuscular mycorrhizal associations in different forest tree species of Hazarikhil forest of Chittagong, Bangladesh. Journal of Forestry Research, 23(1), 115-122. https://doi.org/10.1007/s11676-012-0241-9

Directorate General of Estates. (2019). Tree Crop Estate Stitistics of Indonesia 2018-2020: Cocoa. Secretariate of Directorate General of Estates, Directorate General of Estates, Ministry of Agriculture. https://ditjenbun.pertanian.go.id/?publikasi=buku-publikasi-statistik-2018-2020

Ehrle, A., Potthast, K., Tischer, A., Trumbore, S. E., & Michalzik, B. (2019). Soil properties determine how Lasius flavus impact on topsoil organic matter and nutrient distribution in central Germany. Applied Soil Ecology, 133, 166-176. https://doi.org/10.1016/j.apsoil.2018.08.021

Forey, E., Chauvat, M., Coulibaly, S. F. M., Langlois, E., Barot, S., & Clause, J. (2018). Inoculation of an ecosystem engineer (Earthworm: Lumbricus terrestris) during experimental grassland restoration: Consequences for above and belowground soil compartments. Applied Soil Ecology, 125, 148-155. https://doi.org/10.1016/j.apsoil.2017.12.021

Franco, A. L. C., Cherubin, M. R., Cerri, C. E. P., Guimarães, R. M. L., & Cerri, C. C. (2017). Relating the visual soil structure status and the abundance of soil engineering invertebrates across land use change. Soil and Tillage Research, 173, 49-52. https://doi.org/10.1016/j.still.2016.08.016

Fukami, T. (2015). Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annual Review of Ecology, Evolution, and Systematics, 46, 1-23. https://doi.org/10.1146/annurev-ecolsys-110411-160340

Harinikumar, K. M., & Bagyaraj, D. J. (1994). Potential of earthworms, ants, millipedes, and termites for dissemination of vesicular-arbuscular mycorrhizal fungi in soil. Biology and Fertility of Soils, 18(2), 115-118. https://doi.org/10.1007/BF00336456

Hayashi, M., Niwa, R., Urashima, Y., Suga, Y., Sato, S., Hirakawa, H., Yoshida, S., Ezawa, T., & Karasawa, T. (2018). Inoculum effect of arbuscular mycorrhizal fungi on soybeans grown in long-term bare-fallowed field with low phosphate availability. Soil Science and Plant Nutrition, 64(3), 306-311. https://doi.org/10.1080/00380768.2018.1473007

INVAM. (2019). Enumeration of Spores. International Culture Collection of (Vesicular) Arbuscular Mycorrhizal Fungi, West Virginia University. https://invam.wvu.edu/methods/spores/enumeration-of-spores

Jouquet, P., Janeau, J.-L., Pisano, A., Sy, H. T., Orange, D., Minh, L. T. N., & Valentin, C. (2012). Influence of earthworms and termites on runoff and erosion in a tropical steep slope fallow in Vietnam: A rainfall simulation experiment. Applied Soil Ecology, 61, 161-168. https://doi.org/10.1016/j.apsoil.2012.04.004

Kameoka, H., Tsutsui, I., Saito, K., Kikuchi, Y., Handa, Y., Ezawa, T., Hayashi, H., Kawaguchi, M., & Akiyama, K. (2019). Stimulation of asymbiotic sporulation in arbuscular mycorrhizal fungi by fatty acids. Nature Microbiology, 4(10), 1654-1660. https://doi.org/10.1038/s41564-019-0485-7

Kilowasid, L. M. H., Budianto, W., Syaf, H., Tufaila, M., & Safuan, L. O. (2015). Using of ants and earthworm to modify of soil biological quality and its effect on cocoa seedlings growth. AIP Conference Proceedings, 1677(1), 110004. https://doi.org/10.1063/1.4930775

Kim, S. J., Eo, J.-K., Lee, E.-H., Park, H., & Eom, A.-H. (2017). Effects of Arbuscular Mycorrhizal Fungi and Soil Conditions on Crop Plant Growth. Mycobiology, 45(1), 20-24. https://doi.org/10.5941/MYCO.2017.45.1.20

Lavelle, P., Spain, A., Blouin, M., Brown, G., Decaëns, T., Grimaldi, M., Jiménez, J. J., McKey, D., Mathieu, J., Velasquez, E., & Zangerlé, A. (2016). Ecosystem Engineers in a Self-organized Soil: A Review of Concepts and Future Research Questions. Soil Science, 181(3/4). https://doi.org/10.1097/SS.0000000000000155

Lee, K. K., Reddy, M. V., Wani, S. P., & Trimurtulu, N. (1996). Vesicular-arbuscular mycorrhizal fungi in earthworm casts and surrounding soil in relation to soil management of a semi-arid tropical Alfisol. Applied Soil Ecology, 3(2), 177-181. https://doi.org/10.1016/0929-1393(95)00082-8

Lucas, J., Bill, B., Stevenson, B., & Kaspari, M. (2017). The microbiome of the ant-built home: the microbial communities of a tropical arboreal ant and its nest. Ecosphere, 8(2), e01639. https://doi.org/10.1002/ecs2.1639

Mandyam, K. G., & Jumpponen, A. (2015). Mutualism–parasitism paradigm synthesized from results of root-endophyte models [Hypothesis and Theory]. Frontiers in Microbiology, 5(776). https://doi.org/10.3389/fmicb.2014.00776

Mau, A. E., & Utami, S. R. (2014). Effects of biochar amendment and arbuscular mycorrhizal fungi inoculation on availability of soil phosphorus and growth of maize [arbuscular mycorrhizal fungi; biochar; calcareous soil; maize; phosphorus uptake]. 2014, 1(2), 6. https://doi.org/10.15243/jdmlm.2014.012.069

Medina-Sauza, R. M., Álvarez-Jiménez, M., Delhal, A., Reverchon, F., Blouin, M., Guerrero-Analco, J. A., Cerdán, C. R., Guevara, R., Villain, L., & Barois, I. (2019). Earthworms Building Up Soil Microbiota, a Review [Systematic Review]. Frontiers in Environmental Science, 7(81). https://doi.org/10.3389/fenvs.2019.00081

Mei, L., Yang, X., Cao, H., Zhang, T., & Guo, J. (2019). Arbuscular Mycorrhizal Fungi Alter Plant and Soil C:N:P Stoichiometries Under Warming and Nitrogen Input in a Semiarid Meadow of China. International Journal of Environmental Research and Public Health, 16(3), 397. https://doi.org/10.3390/ijerph16030397

Melo, C. D., Walker, C., Krüger, C., Borges, P. A. V., Luna, S., Mendonça, D., Fonseca, H. M. A. C., & Machado, A. C. (2019). Environmental factors driving arbuscular mycorrhizal fungal communities associated with endemic woody plant Picconiaazorica on native forest of Azores. Annals of Microbiology, 69(13), 1309-1327. https://doi.org/10.1007/s13213-019-01535-x

Moreira, S. D., França, A. C., Rocha, W. W., Tibães, E. S., & Neiva, E. (2018). Inoculation with mycorrhizal fungi on the growth and tolerance to water deficit of coffee plants. Revista Brasileira de Engenharia Agrícola e Ambiental, 22, 747-752. https://doi.org/10.1590/1807-1929/agriambi.v22n11p747-752

Powell, C. L., & Bagyaraj, D. J. (2017). Va Mycorrhizae: Why all the Interest? In C. L. Powell & D. J. Bagyaraj (Eds.), VA Mycorrhiza. CRC Press. https://doi.org/10.1201/9781351077514

Prasad, M., Chrysargyris, A., McDaniel, N., Kavanagh, A., Gruda, N. S., & Tzortzakis, N. (2020). Plant Nutrient Availability and pH of Biochars and Their Fractions, with the Possible Use as a Component in a Growing Media. Agronomy, 10(1), 10. https://doi.org/10.3390/agronomy10010010

Rillig, M. C., Aguilar-Trigueros, C. A., Anderson, I. C., Antonovics, J., Ballhausen, M.-B., Bergmann, J., Bielcik, M., Chaudhary, V. B., Deveautour, C., Grünfeld, L., Hempel, S., Lakovic, M., Lammel, D. R., Lehmann, A., Lehmann, J., Leifheit, E. F., Liang, Y., Li, E., Lozano, Y. M., Manntschke, A., Mansour, I., Oviatt, P., Pinek, L., Powell, J. R., Roy, J., Ryo, M., Sosa-Hernández, M. A., Veresoglou, S. D., Wang, D., Yang, G., & Zhang, H. (2020). Myristate and the ecology of AM fungi: significance, opportunities, applications and challenges. New Phytologist, 227(6), 1610-1614. https://doi.org/10.1111/nph.16527

Salim, M. A., Budi, S. W., Setyaningsih, L., Iskandar, Wahyudi, I., & Kirmi, H. (2020). Root colonization by arbuscular mycorrhizal fungi (AMF) in various age classes of revegetation post-coal mine. Biodiversitas Journal of Biological Diversity, 21(11). https://doi.org/10.13057/biodiv/d211105

Sanjaya, M. F., Kilowasid, L. M. H., Sabaruddin, L., Sulaeman, D., & Nurmas, A. (2020). Pengaruh Bahan Organik terhadap Spora Fungi Mikoriza Arbuskula dalam Tanah, dan Potensi Tanahnya Sebagai Sumber Inokulum. Berkala Penelitian Agronomi, 8(1), 11-22. http://ojs.uho.ac.id/index.php/agronomi/article/view/12938

Sankar, A. S., & Patnaik, A. (2018). Impact of soil physico-chemical properties on distribution of earthworm populations across different land use patterns in southern India. The Journal of Basic and Applied Zoology, 79(1), 50. https://doi.org/10.1186/s41936-018-0066-y

Schultz, T. R., Sosa-Calvo, J., Brady, S. G., Lopes, C. T., Mueller, U. G., BacciJr., M., & Vasconcelos, H. L. (2015). The Most Relictual Fungus-Farming Ant Species Cultivates the Most Recently Evolved and Highly Domesticated Fungal Symbiont Species. The American Naturalist, 185(5), 693-703. https://doi.org/10.1086/680501

Seutra Kaba, J., Abunyewa, A. A., Kugbe, J., Kwashie, G. K. S., Owusu Ansah, E., & Andoh, H. (2021). Arbuscular mycorrhizal fungi and potassium fertilizer as plant biostimulants and alternative research for enhancing plants adaptation to drought stress: Opportunities for enhancing drought tolerance in cocoa (Theobroma cacao L.). Sustainable Environment, 7(1), 1963927. https://doi.org/10.1080/27658511.2021.1963927

Shukla, R. K., Singh, H., & Rastogi, N. (2016). How effective are disturbance – tolerant, agroecosystem – nesting ant species in improving soil fertility and crop yield? Applied Soil Ecology, 108, 156-164. https://doi.org/10.1016/j.apsoil.2016.08.013

Sivakumar, N. (2013). Effect of edaphic factors and seasonal variation on spore density and root colonization of arbuscular mycorrhizal fungi in sugarcane fields. Annals of Microbiology, 63(1), 151-160. https://doi.org/10.1007/s13213-012-0455-2

Sugiura, Y., Akiyama, R., Tanaka, S., Yano, K., Kameoka, H., Marui, S., Saito, M., Kawaguchi, M., Akiyama, K., & Saito, K. (2020). Myristate can be used as a carbon and energy source for the asymbiotic growth of arbuscular mycorrhizal fungi. Proceedings of the National Academy of Sciences, 117(41), 25779. https://doi.org/10.1073/pnas.2006948117

Syaf, H., Pattah, M. A., & Kilowasid, L. M. H. (2021). Quality of soil from the nickel mining area of Southeast Sulawesi, Indonesia, engineered using earthworms (Pheretima sp.) [biostructure; ecosystem engineer; soil ecological engineering; soil quality]. 2021, 8(4), 11. https://doi.org/10.15243/jdmlm.2021.084.2995

Taylor, A. R., Lenoir, L., Vegerfors, B., & Persson, T. (2019). Ant and Earthworm Bioturbation in Cold-Temperate Ecosystems. Ecosystems, 22(5), 981-994. https://doi.org/10.1007/s10021-018-0317-2

Verbruggen, E., van der Heijden, M. G. A., Rillig, M. C., & Kiers, E. T. (2013). Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytologist, 197(4), 1104-1109. https://doi.org/10.1111/j.1469-8137.2012.04348.x

Verzeaux, J., Nivelle, E., Roger, D., Hirel, B., Dubois, F., & Tetu, T. (2017). Spore Density of Arbuscular Mycorrhizal Fungi is Fostered by Six Years of a No-Till System and is Correlated with Environmental Parameters in a Silty Loam Soil. Agronomy, 7(2), 38. https://doi.org/10.3390/agronomy7020038

Vogt, D. J., Tilley, J. P., & Edmonds, R. L. (2015). Soil and Plant Analysis for Forest Ecosystem Characterization. Berlin, München, Boston: De Gruyter. https://doi.org/10.1515/9783110290479

Wang, P., Wang, Y., Shu, B., Liu, J.-F., & Xia, R.-X. (2015). Relationships Between Arbuscular Mycorrhizal Symbiosis and Soil Fertility Factors in Citrus Orchards Along an Altitudinal Gradient. Pedosphere, 25(1), 160-168. https://doi.org/10.1016/S1002-0160(14)60086-2

Wang, S., Li, J., Zhang, Z., Chen, M., Li, S., & Cao, R. (2019). Feeding-strategy effect of Pheidole ants on microbial carbon and physicochemical properties in tropical forest soils. Applied Soil Ecology, 133, 177-185. https://doi.org/10.1016/j.apsoil.2018.10.006

Werner, G. D. A., & Kiers, E. T. (2015). Order of arrival structures arbuscular mycorrhizal colonization of plants. New Phytologist, 205(4), 1515-1524. https://doi.org/10.1111/nph.13092

Wills, B. D., & Landis, D. A. (2018). The role of ants in north temperate grasslands: a review. Oecologia, 186(2), 323-338. https://doi.org/10.1007/s00442-017-4007-0

Zanella, A., Ponge, J.-F., & Briones, M. J. I. (2018). Humusica 1, article 8: Terrestrial humus systems and forms – Biological activity and soil aggregates, space-time dynamics. Applied Soil Ecology, 122, 103-137. https://doi.org/10.1016/j.apsoil.2017.07.020

Zanella, A., Ponge, J.-F., Topoliantz, S., Bernier, N., & Juilleret, J. (2018). Humusica 2, Article 15: Agro humus systems and forms. Applied Soil Ecology, 122, 204-219. https://doi.org/10.1016/j.apsoil.2017.10.011

DOI: https://doi.org/10.20961/stjssa.v18i2.51500

Refbacks

  • There are currently no refbacks.