Evangelina Esmeralda Quiñones-Aguilar, Cuauhtémoc Hernández-Hernández, Gabriel Rincón-Enriquez, Luis López-Pérez, Philippe Lobit, Jhony Navat Enríquez-Vara


Background: The fall armyworm Spodoptera frugiperda is one of the main pests of maize in Mexico. Its control and management have been performed mainly with pesticides. One of the alternatives is to incorporate arbuscular mycorrhizal fungi (AMF) because of the benefits they provide to plants improving their growth and promoting their defense system against this pest. Objective: Evaluate the effect of AMF in creole maize growth in reducing leaf damage and development of Spodoptera frugiperda larvae. Methodology: In greenhouse conditions, creole maize plants were inoculated with 80 spores of Funneliformis mosseae, Rhizophagus intraradices and without AMF. Height and stem diameter were determined in mycorrhized plants at 15, 30, and 45 days after plant inoculation. After 45 days, plants were infested with three third-instar larvae of S. frugiperda and left to feed for 12 days; fresh weight and cephalic capsule width and size were measured. Once larvae were removed, leaf damage was determined in plants by means of a visual scale, leaf area and mycorrhizal colonization. Results: Root colonization of maize plants by AMF had a significant effect (Tukey’s p ≤ 0.05) in creole maize growth expressed in plant height at 30 days and at 45 days in stem diameter only in plants inoculated with F. mosseae (Tukey’s p ≤ 0.05). Leaf damage by the fall armyworm was similar between inoculated and uninoculated with AMF. Larvae that consumed plant leaves inoculated with R. intraradices showed greater fresh weight compared to those inoculated with F. mosseae. Moreover, width of the cephalic capsule and size were similar between larvae fed with plants inoculated with and without AMF. Implications: The results provide new perspectives and considerations to incorporate AMF in management of fall armyworm in creole maize. Conclusion: These results show that AMF partially promote plant growth of creole maize; leaf damage is similar between plants with and without AMF. Insect weight increased depending on AMF species, which influenced their development.


maize; insect development; arbuscular mycorrhizal fungi; plant growth; herbivory

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An, G.H., Kobayashi, S., Enoki, H., Sonobe, K., Muraki, M., Karasawa, T. and Ezawa, T., 2010. How does arbuscular mycorrhizal colonization vary with host plant genotype? An example based on maize (Zea mays) germplasms. Plant and Soil, 327(1–2), pp. 441–453.

Aroca, R., Porcel, R. and Ruiz-Lozano, J.M., 2007. How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses?. New Phytologist, 173(4), pp. 808–816.

Bennett, A.E., Alers-Garcia, J. and Bever, J.D., 2006. Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: Hypotheses and synthesis. The American Naturalist, 167, pp. 141–152.

Bernaola, L., Cosme, M., Schneider, R.W. and Stout, M., 2018. Belowground inoculation with arbuscular mycorrhizal fungi increases local and systemic susceptibility of rice plants to different pest organisms. Frontiers in Plant Science, 09, p.747.

Blanco, C.A., Pellegaud, J.G., Nava-Camberos, U., Lugo-Barrera, D., Vega-Aquino, P., Coello, J., Terán-Vargas, A.P. and Vargas-Camplis, J., 2014. Maize pests in Mexico and challenges for the adoption of integrated pest management programs. Journal of Integrated Pest Management, 5, pp. 1-9.

Borowicz, V.A., 2013. The impact of arbuscular mycorrhizal fungi on plant growth following herbivory: A search for pattern. Acta Oecologica, 52, pp. 1-9.

Cameron, D.D., Neal, A.L., van Wees, S.C.M. and Ton, J., 2013. Mycorrhiza-induced resistance: More than the sum of its parts?. Trends Plant Science, 18, pp. 539–545.

Davis, F. M., Ng, S. S. and Williams, W. P., 1992. Visual rating scales for screening whorl-stage corn for resistance to fall armyworm. Technical bulletin – Mississippi Agricultural and Forestry Experiment Station. Technical bulletin 186.

Faye, A., Dalp, Y., Ndung’u-Magiroi, K., Jefwa, J., Ndoye, I., Diouf, M. and Lesueur, D., 2013. Evaluation of commercial arbuscular mycorrhizal inoculants. Canadian Journal of Plant Science, 93(6), pp. 1201–1208.

Fritz, M., Jakobsen, I., Foged-Lyngkjaer, M., Thordal-Christensen, H. and Pons-Kuhnemann, J., 2006. Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza, 16, pp. 413–419.

Gange, A.C. and West, H.M., 1994. Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytologist, 128, pp. 79–87.

García?Gómez, G., Real?Santillán, R. O., Larsen, J., Pérez, L. L., Rosa, J. I. F., Pineda, S. and Martínez?Castillo, A. M., 2021. Maize mycorrhizas increase the susceptibility of the foliar insect herbivore Spodoptera frugiperda to its homologous nucleopolyhedrovirus. Pest Management Science,77, pp. 4701-4708.

Gavito, M. and Varela, L., 1995. Response of “criollo” maize to single and mixed species inocula of arbuscular mycorrhizal fungi. Plant and Soil, 176, pp. 101-105.

Gianinazzi, S., Gollotte, A., Binet, M.N., Tuinen, D. van, Redecker, D. and Wipf, D., 2010. Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza, 20, pp. 519–530.

Goverde, M., van der Heijden, M., Wiemken, A., Sanders, I. and Erhardt, A., 2000. Arbuscular mycorrhizal fungi influence life history traits of a lepidopteran herbivore. Oecologia, 125, pp. 362-369.

Gutiérrez-Moreno, R., Mota-Sanchez, D., Blanco, C.A., Whalon, M.E., Terán-Santofimio, H., Rodriguez-Maciel, J.C. and DiFonzo, C., 2019. Field-evolved resistance of the fall armyworm (Lepidoptera: Noctuidae) to synthetic insecticides in Puerto Rico and Mexico. Journal of Economic Entomology, 112, pp. 792–802.

Hartley, S. E. and Gange, A.C., 2009. Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annual Review Entomology, 54, pp. 323-342.

Hoffmann, D., Vierheilig, H. and Schausberger, P., 2011. Mycorrhiza-induced trophic cascade enhances fitness and population growth of an acarine predator. Oecologia, 166, pp. 141–149.

Johnson, N.C., Wilson, G.W.T., Bowker, M.A., Wilson, J. and Miller, R.M., 2010. Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proceedings National Academy Sciences, 107, pp. 2093–2098.

Jung, S.C., Martinez-Medina, A., Lopez-Raez, J.A. and Pozo, M.J., 2012. Mycorrhiza-induced resistance and priming of plant defenses. Journal of Chemical Ecology, 38, pp. 651-664.

Kaur, J., Chavana, J., Soti, P., Racelis, A. and Kariyat, R., 2020. Arbuscular mycorrhizal fungi (AMF) influences growth and insect community dynamics in sorghum-sudangrass (Sorghum x drummondii). Arthropod-Plant Interactions, 14, pp. 301-315.

Kempel, A., Schmidt, A.K., Brandl, R. and Schädler, M. 2010. Support from the underground: Induced plant resistance depends on arbuscular mycorrhizal fungi. Functional Ecology, 24, pp. 293–300.

Koricheva, J., Gange, A.C. and Jones, T., 2009. Effects of mycorrhizal fungi on insect herbivores: A meta-analysis. Ecology, 90, pp. 2088–2097.

Lauriano-Barajas, J. and Vega-Frutis, R., 2018. Infectivity and effectivity of commercial and native arbuscular mycorrhizal biofertilizers in seedlings of maize (Zea mays). Botanical Sciences, 96, pp. 395–404.

Lima, A. F., Bernal, J., Venâncio, M. G. S., Souza, B. H. S. de and Carvalho, G. A., 2022. Comparative tolerance levels of maize landraces and a hybrid to natural infestation of fall armyworm. Insects, 13, pp. 651.

López-Carmona, D. A., Alarcón, A., Martínez-Romero, E., Peña-Cabriales, J. J. and Larsen, J., 2019. Maize plant growth response to whole rhizosphere microbial communities in different mineral N and P fertilization scenarios. Rhizosphere, 9, pp. 38–46.

McGonigle, T.P., Miller, M.H., Evans, D.G., Fairchild, G.L. and Swan, J.A., 1990. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist, 115, pp. 495-501.

Mota-Sanchez D. and Wise J., 2020. Arthropod pesticide resistance database. [online] Available at [Accessed 5 October 2020].

Phillips, J.M. and Hayman, D.S., 1970. Improved procedure for clearing roots, and staining parasitic and vesicular-arbuscular mycorrizal fungi for rapid assessment of infection. Transactions of the British Mycological Society, 55, pp. 158-161.

Poitout, B. R., 1974. Elevage de chenilles de vingt-huit espèces de Lépidoptères Noctuidae et de deux espèces d’Arctiidae sur milieu artificiel simple. Particularités de l’élevage selon les espèces. Annales de Zoologie Ecologie Animale, 6, pp. 341–411.

Pozo, M.J., Albrectsen, B.R., Bejarano, E.R., de la Peña, E., Herrero, S., Martinez-Medina, A., Pastor, V., Ravnskov, S., Williams, M. and Biere, A., 2020. Three-way interactions between plants, microbes, and arthropods (PMA): Impacts, mechanisms, and prospects for sustainable plant protection. Teaching tools in plant biology: Lecture Notes. The Plant Cell, 32, pp. 1–11.

Rabin, L.B. and Pacovsky, R.S., 1985. Reduced larva growth of two lepidoptera (Noctuidae) on excised leaves of soybean infected with a mycorrhizal fungus. Journal of Economic Entomology, 78, pp.1358–1363.

Ramírez-Serrano, B., Querejeta, M., Minchev, Z., Gamir, J., Perdereau, E., Pozo, M. J., Dubreuil, G. and Giron, D., 2022. Mycorrhizal benefits on plant growth and protection against Spodoptera exigua depend on N availability. Journal of Plant Interactions, 17, 940–955.

Real-Santillán, R.O., del-Val, E., Cruz-Ortega, R., Contreras-Cornejo, H.A., González-Esquivel, C.E. and Larsen, J., 2019. Increased maize growth and P uptake promoted by arbuscular mycorrhizal fungi coincide with higher foliar herbivory and larval biomass of the fall armyworm Spodoptera frugiperda. Mycorrhiza, 29, pp. 615–622.

Reyes-Tena, A., López-Perez, L., Quiñones-Aguilar, E.E. and Rincon-Enriquez, G., 2015. Evaluación de consorcios micorrícicos arbusculares en el crecimiento vegetal de plantas de maíz, chile y frijol. Biologicas,17, pp. 35-42.

Rivero, J., Lidoy, J., Llopis-Giménez, Á., Herrero, S., Flors, V. and Pozo, M. J., 2021. Mycorrhizal symbiosis primes the accumulation of antiherbivore compounds and enhances herbivore mortality in tomato. Journal of Experimental Botany, 72, pp.1-13.

Roger, A., Getaz, M., Rasmann, S. and Sanders, I.R., 2013. Identity and combinations of arbuscular mycorrhizal fungal isolates influence plant resistance and insect preference. Ecological Entomology, 38, pp. 330-338.

Rosenthal, J.P. and Dirzo, R., 1997. Effects of life history, domestication and agronomic selection on plant defence against insects: Evidence from maizes and wild relatives. Evolutionary Ecology, 11, pp. 337-355.

Sangabriel-Conde, W., Negrete-Yankelevich, S., Maldonado-Mendoza, I. E. and Trejo-Aguilar, D., 2014. Native maize landraces from Los Tuxtlas, Mexico show varying mycorrhizal dependency for P uptake. Biology and Fertility of Soils, 50(2), pp. 405–414.

Shrivastava, G., Ownley, B.H., Augé, R.M., Toler, H., Dee, M., Vu, A., Kollner, T.G. and Chen, F., 2015. Colonization by arbuscular mycorrhizal and endophytic fungi enhanced terpene production in tomato plants and their defense against a herbivorous insect. Symbiosis, 65, pp. 65–74.

SIAP (Servicio de Información Agroalimentaria y Pesquera). 2019. Panorama Agroalimentario 2019. [pdf] México: Secretaria de Agricultura y Desarrollo Rural. Available at:<> [Accessed 5 October 2020].

Singh, G. M., Xu, J., Schaefer, D., Day, R., Wang, Z. and Zhang, F., 2022. Maize diversity for fall armyworm resistance in a warming world. Crop Science, 62, 1–19.

Smith, S.E. and Read, D.R., 2008. Mycorrhizal symbiosis. 3rd ed. New York: Academic Press.

Stratton, C. A., Ray, S., Bradley, B. A., Kaye, J. P., Ali, J. G. and Murrell, E. G., 2022. Nutrition vs association: plant defenses are altered by arbuscular mycorrhizal fungi association not by nutritional provisioning alone. BMC Plant Biology, 22, 400.

Szczepaniec, A., Widney, S., Bernal, J.S. and Eubanks, M.D., 2013. Higher expression of induced defenses in teosintes (Zea spp.) is correlated with greater resistance to fall armyworm, Spodoptera frugiperda. Entomologia Experimentalis et Applicata, 146, pp. 242– 251.

Turrent-Fernández, A., Wise, T.A. and, Garvey, E., 2012. Achieving México’s maize potential. Global Development and Environment Institute Working [online] Available at: < > [Accessed 10 August 2020].

Vannette, R. L. and Hunter, M. D., 2009. Mycorrhizal fungi as mediators of defence against insect pests in agricultural systems. Agricultural and Forest Entomology, 11, pp. 351–358.

Vannette, R.L. and Hunter, M.D., 2011. Plant defense theory re-examined: Nonlinear expectations based on the costs and benefits of resource mutualisms. Journal of Ecology, 99, pp. 66–76.

Vogelweith, F., Moreau, J., Thiery, D. and Moret, Y., 2015. Food-mediated modulation of immunity in a phytophagous insect: an effect of nutrition rather than parasitic contamination. Journal of Insect Physiology, 77, pp. 55–61.

Wang, B. and Qiu Y.L., 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza, 16, pp. 299-363.

Wiseman, B.R., Isenhour, D.J. and Bhagwat, V.R., 1991. Stadia, larval-pupal weight, and width of head capsules of corn earworm (Lepidoptera:Noctuidae) after feeding on varying resistance levels of maize silks. Journal of Entomological Science, 26, pp. 303-309.

Yan, W., Lin, X., Yao, Q., Zhao, C., Zhang, Z. and Xu, H., 2021. Arbuscular mycorrhizal fungi improve uptake and control efficacy of carbosulfan on Spodoptera frugiperda in maize plants. Pest Management Science, 77, pp. 2812-2819.



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