J. For. Sci., 2023, 69(6):244-253 | DOI: 10.17221/158/2022-JFS

The beneficial role of arbuscular mycorrhizal fungi on population rates of aboveground herbivory: Zyginella pulchra (Hemiptera, Cicadellidae) in plane treesOriginal Paper

Hamed Aalipour1, Ali Nikbakht1, Jahangir Khajehali2, Mohammad Taghizadeh3
1 Department of Horticulture, College of Agriculture, Isfahan University of Technology, Isfahan, Iran
2 Department of Plant Protection, College of Agriculture, Isfahan University of Technology, Isfahan, Iran
3 Agricultural and Natural Resources Research Center of Fars, Iran

Herbivorous pests and arbuscular mycorrhizal fungi (AMF) coexist on the same host plant, having an indirect effect on one another. We established an experiment in a randomised complete block design with four treatments and six replications to examine the impact of AMF on the population and the damage caused to plane trees by the leafhopper Zyginella pulchra. Manure, manure plus fertiliser, manure plus fertiliser plus AMF, and non-inoculated plants (control) were all of the treatments. The findings revealed that while the nutritional content and soluble carbohydrate content were significantly enhanced by all treatments, they largely reached their peak in the AMF-inoculated plants. When compared to control trees that were not inoculated, the concentrations of N, P, and Zn were boosted by 39%, 81%, and 425%, respectively. AMF inoculation increased the population of Z. pulchra nymphs and adults compared to the control. However, the plants with AMF inoculation eventually suffered greater leaf loss as a result of this rise in the pest population. The findings show that while AMF enhance nutrient absorption and are necessary to improve the nutritional state of the host trees, they also enhance the absorption of pests that are thought to be harmful to plane trees. However, AMF colonisation improved the potential attractiveness of Z. pulchra to plane trees.

Keywords: insect attractiveness; leaf damage; mycorrhizae; nutritional status; Platanus orientalis

Accepted: May 17, 2023; Prepublished online: June 20, 2023; Published: June 30, 2023  Show citation

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Aalipour H, Nikbakht A, Khajehali J, Taghizadeh M. The beneficial role of arbuscular mycorrhizal fungi on population rates of aboveground herbivory: Zyginella pulchra (Hemiptera, Cicadellidae) in plane trees. J. For. Sci. 2023;69(6):244-253. doi: 10.17221/158/2022-JFS.
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References

  1. Aalipour H., Nikbakht A., Etemadi N. (2019): Relationship between chlorosis, photosynthesis and the nutrient content of plane trees in the presence of chemical and organic fertilizers. Advances in Horticultural Science, 33: 171-177.
  2. Aalipour H., Nikbakht A., Ghasemi M., Amiri R. (2020): Morpho-physiological and biochemical responses of two turfgrass species to arbuscular mycorrhizal fungi and humic acid under water stress condition. Journal of Soil Science and Plant Nutrition, 20: 566-576. Go to original source...
  3. Aalipour H., Nikbakht A., Etemadi N., MacDonald J.E. (2021): Co-inoculation of Arizona cypress with mycorrhizae and rhizobacteria affects biomass, nutrient status, water-use efficiency, and glomalin-related soil protein concentration. Urban Forestry & Urban Greening, 60: 127050. Go to original source...
  4. Agrawal A.A. (2007): Macroevolution of plant defense strategies. Trends in Ecology and Evolution, 22: 103-109. Go to original source... Go to PubMed...
  5. Bennett A.E., Bever J.D. (2007): Mycorrhizal species differentially alter plant growth and response to herbivory. Ecology, 88: 210-218. Go to original source... Go to PubMed...
  6. Cardoza Y.J., Lait C.G., Schmelz E.A., Huang J., Tumlinson J.H. (2003): Fungus-induced biochemical changes in peanut plants and their effect on development of beet armyworm, Spodoptera exigua Hübner (Lepidoptera: Noctuidae) larvae. Environmental Entomology, 32: 220-228. Go to original source...
  7. Cornelissen T., Wilson Fernandes G., Vasconcellos-Neto J. (2008): Size does matter: Variation in herbivory between and within plants and the plant vigor hypothesis. Oikos, 117: 1121-1130. Go to original source...
  8. Currie A.F., Murray P.J., Gange A.C. (2011): Is a specialist root-feeding insect affected by arbuscular mycorrhizal fungi? Applied Soil Ecology, 47: 77-83. Go to original source...
  9. Eaton A.D., Clesceri L.S., Greenberg A.E., Franson M.A.H. (1995): Standard Methods for the Examination of Water and Wastewater. Washington D.C., American Public Health Association: 1-43.
  10. Elser J.J., Fagan W.F., Denno R.F., Dobberfuhl D.R., Folarin A., Huberty A., Interlandi S., Kilham S.S., McCauley E., Schulz K.L., Siemann E.H, Sterner R.W. (2000): Nutritional constraints in terrestrial and freshwater food webs. Nature, 408: 578-580. Go to original source... Go to PubMed...
  11. Frew A., Powell J.R., Hiltpold I., Allsopp P.G., Sallam N., Johnson S.N. (2017): Host plant colonisation by arbuscular mycorrhizal fungi stimulates immune function whereas high root silicon concentrations diminish growth in a soil-dwelling herbivore. Soil Biology and Biochemistry, 112: 117-126. Go to original source...
  12. Gange A.C. (2007): Insect-mycorrhizal interactions: patterns, processes, and consequences. In: Ohgushi T., Craig T.P., Price P.W. (eds): Ecological Communities: Plant Mediation in Indirect Interaction Webs. Cambridge, Cambridge University Press: 124-144. Go to original source...
  13. Gange A.C., West H.M. (1994): Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytologist, 128: 79-87. Go to original source... Go to PubMed...
  14. Gange A.C., Bower E., Brown V.K. (1999): Positive effects of an arbuscular mycorrhizal fungus on aphid life history traits. Oecologia, 120: 123-131. Go to original source... Go to PubMed...
  15. Garcia K., Doidy J., Zimmermann S.D., Wipf D., Courty P.E. (2016): Take a trip through the plant and fungal transportome of mycorrhiza. Trends in Plant Science, 21: 937-950. Go to original source... Go to PubMed...
  16. Gehring C.A., Whitham T.G. (1994): Comparisons of ectomycorrhizae on pinyon pines (Pinus edulis; Pinaceae) across extremes of soil type and herbivory. American Journal of Botany, 81: 1509-1516. Go to original source...
  17. Gehring C., Bennett A. (2009): Mycorrhizal fungal-plant-insect interactions: The importance of a community approach. Environmental Entomology, 38: 93-102. Go to original source... Go to PubMed...
  18. Hartley S.E., Gange A.C. (2009): Impacts of plant symbiotic fungi on insect herbivores: Mutualism in a multitrophic context. Annual Review of Entomology, 54: 323-342. Go to original source... Go to PubMed...
  19. He S., Long M., He X., Guo L., Yang J., Yang P., Hu T. (2017): Arbuscular mycorrhizal fungi and water availability affect biomass and C : N : P ecological stoichiometry in alfalfa (Medicago sativa L.) during regrowth. Acta Physiologiae Plantarum, 39: 199. Go to original source...
  20. Hoffmann D., Vierheilig H., Schausberger P. (2011): Arbuscular mycorrhiza enhances preference of ovipositing predatory mites for direct prey-related cues. Physiological Entomology, 36: 90-95. Go to original source...
  21. Javaid A. (2009): Arbuscular mycorrhizal mediated nutrition in plants. Journal of Plant Nutrition, 32: 1595-1618. Go to original source...
  22. Koricheva J., Gange A.C., Jones T. (2009): Effects of mycorrhizal fungi on insect herbivores: A meta-analysis. Ecology, 90: 2088-2097. Go to original source... Go to PubMed...
  23. Larsson S. (1989): Stressful times for the plant stress: Insect performance hypothesis. Oikos, 56: 277-283. Go to original source...
  24. Lee K.P., Simpson S.J., Wilson K. (2008): Dietary protein-quality influences melanization and immune function in an insect. Functional Ecology, 22: 1052-1061. Go to original source...
  25. Nevo E., Coll M. (2001): Effect of nitrogen fertilization on Aphis gossypii (Homoptera: Aphididae): Variation in size, color, and reproduction. Journal of Economic Entomology, 94: 27-32. Go to original source... Go to PubMed...
  26. Ng A., Wilson B.A., Frew A. (2022): Belowground plant responses to root herbivory depend on the composition and structure of their root-colonising arbuscular mycorrhizal fungi. Available at https://www.biorxiv.org/content/10.1101/2022.02.28.480478v1.abstract Go to original source...
  27. Pineda A., Zheng S.J., van Loon J.J.A., Pieterse C.M.J., Dicke M. (2010): Helping plants to deal with insects: The role of beneficial soil-borne microbes. Trends in Plant Science, 15: 507-514. Go to original source... Go to PubMed...
  28. Radjabi G., Mirzayans H. (1989): First report of Zyginella pulchra Low as a harmful insect on deciduous fruit trees in Iran. Entomologie et Phytopathologie Appliquees, 56: 101-103.
  29. Rasmann S., Agrawal A.A. (2009): Plant defense against herbivory: progress in identifying synergism, redundancy, and antagonism between resistance traits. Current Opinion in Plant Biology, 12: 473-478. Go to original source... Go to PubMed...
  30. Rathod A.N., Tanawal B., Shah V. (2013): Image processing techniques for detection of leaf disease. International Journal of Advanced Research in Computer Science and Software Engineering, 3: 397-399.
  31. Roger A., Getaz M., Rasmann S., Sanders I.R. (2013): Identity and combinations of arbuscular mycorrhizal fungal isolates influence plant resistance and insect preference. Ecological Entomology, 38: 330-338. Go to original source...
  32. Sabeti H. (1976): Forest, Trees and Shrubs of Iran. Tehran, Ministry of Information and Tourism Press: 874.
  33. Schmid-Hempel P. (2005): Evolutionary ecology of insect immune defenses. Annual Review of Entomology, 50: 529-551. Go to original source... Go to PubMed...
  34. Shrivastava G., Ownley B.H., Augé R.M., Toler H., Dee M., Vu A., Köllner T.G., 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: 65-74. Go to original source...
  35. Simon A.L., Wellham P.A., Aradottir G.I., Gange A.C. (2017a): Unravelling mycorrhiza-induced wheat susceptibility to the English grain aphid Sitobion avenae. Scientific Reports, 7: 1-11. Go to original source... Go to PubMed...
  36. Simon J.C., Biere A., Sugio A. (2017b): The promises and challenges of research on plant-insect-microbe interactions. Insect Science, 24: 904-909. Go to original source...
  37. Smith S.E., Read D.J. (2008): Mycorrhizal Symbiosis. 3rd Ed. Maryland Heights, Academic Press: 800.
  38. Treseder K.K. (2013): The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content. Plant and Soil, 371: 1-13. Go to original source...
  39. Triggs A., Knell R.J. (2012): Interactions between environmental variables determine immunity in the Indian meal moth Plodia interpunctella. Journal of Animal Ecology, 81: 386-394. Go to original source... Go to PubMed...
  40. Van Emden H.F. (1966): Studies on the relations of insect and host plant: III. A comparison of the reproduction of Brevicoryne brassicae and Myzus persicae: (Hemiptera: Aphididae) on brussels sprout plants supplied with different rates of nitrogen and potassium. Entomologia Experimentalis et Applicata, 9: 444-460. Go to original source...
  41. Vannette R.L., Hunter M.D. (2009): Mycorrhizal fungi as mediators of defence against insect pests in agricultural systems. Agricultural and Forest Entomology, 11: 351-358. Go to original source...
  42. Vannette R.L., Hunter M.D. (2011): Plant defence theory re-examined: Nonlinear expectations based on the costs and benefits of resource mutualisms. Journal of Ecology, 99: 66-76. Go to original source...
  43. Walling L.L. (2008): Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiology, 146: 859-866 Go to original source... Go to PubMed...
  44. Wang J.J., Tsai J.H., Broschat T.K. (2006): Effect of nitrogen fertilization of corn on the development, survivorship, fecundity and body weight of Peregrinus maidis (Hom., Delphacidae). Journal of Applied Entomology, 130: 20-25. Go to original source...
  45. Wilson M.R., Mühlethaler R. (2010): The nymph of Zyginella pulchra Löw, 1885 (Hemiptera, Cicadellidae, Typhlocybinae). Cicadina, 11: 43-45.
  46. Wooley S. C., Paine T. D. (2007): Can intra-specific genetic variation in arbuscular mycorrhizal fungi (Glomus etunicatum) affect a mesophyll-feeding herbivore (Tupiocoris notatus Distant)? Ecological Entomology, 32: 428-434. Go to original source...
  47. Wu Q.S., Srivastava A.K., Li Y. (2015): Effects of mycorrhizal symbiosis on growth behavior and carbohydrate metabolism of trifoliate orange under different substrate P levels. Journal of Plant Growth Regulation, 34: 499-508. Go to original source...
  48. Wu Q.S., Srivastava A.K., Zou Y.N., Malhotra S.K. (2017): Mycorrhizas in citrus: Beyond soil fertility and plant nutrition. Indian Journal of Agricultural Sciences, 87: 427-443. Go to original source...
  49. Wurst S., Forstreuter M. (2010): Colonization of Tanacetum vulgare by aphids is reduced by earthworms. Entomologia Experimentalis et Applicata, 137: 86-92. Go to original source...
  50. Züst T., Agrawal A.A. (2016): Mechanisms and evolution of plant resistance to aphids. Nature Plants, 2: 15206. Go to original source... Go to PubMed...

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