Journal:
2022. 30 (1)The effect of gall mites (Acariformes, Eriophyoidea) on leaf morphology and pigment content of deciduous trees in West Siberia
About authors:
Larissa A. Ivanova,X-BIO Institute, Tyumen State University, Tyumen, Russia;
Institute Botanic Garden, Ural Branch, Russian Academy of Sciences, Ekaterinburg, Russia
e-mail: ivanova.larissa@list.ru
Zoological Institute, Russian Academy of Sciences, Saint-Petersburg, Russia; Saint-Petersburg State University, Saint-Petersburg, Russia
X-BIO Institute, Tyumen State University, Tyumen, Russia; Institute Botanic Garden, Ural Branch, Russian Academy of Sciences, Ekaterinburg, Russia
X-BIO Institute, Tyumen State University, Tyumen, Russia
X-BIO Institute, Tyumen State University, Tyumen, Russia
Saint-Petersburg State University, Saint-Petersburg, Russia
X-BIO Institute, Tyumen State University, Tyumen, Russia; e-mail: a.v.tolstikov@utmn.ru
Acknowledgments:
The reported study was performed within the framework of the state assignment FEWZ-2020-0009 from the Ministry of Education and Science of the Russian Federation, in accordance with the budget themes of the Botanic Garden UB RAS and of the Zoological Institute RAS 122031100263-1, as well as the Russian Foundation for Basic Research (RFBR) grant No. 21-54-46003 СТ_а.
Annotation:
Phytophagous mites of the superfamily Eriophyoidea are capable of inducing gall formation on various organs of higher vascular plants. However, the question of how gallogenesis affects leaf assimilation surface and photosynthetic activity of the host plants is poorly understood. We have examined the influence of gall-forming mites from the genera Eriophyes and Acalitus on leaf size, shape and photosynthetic pigment content in five deciduous tree species near the city of Tyumen, West Siberia. The gall mite infestation resulted in chlorosis, destruction of photosynthetic apparatus in gall-infected leaf parts, leaf deformation and a decrease in leaf area. The magnitude of the effects on leaf size and shape varied among the studied mite–tree systems and did not depend on the infection severity. On the contrary, chlorophyll and carotenoid amounts per leaf decreased in an infection severity-dependent manner in all mite–host plant variants. Mite-induced galls did not influence the pigment concentration in green uninfected gaps between galls. Additionally, the chlorophyll amount in the infected leaves has decreased due to the destruction of the pigment complex in the galled leaf areas and a decrease of the whole-leaf area. As a result, the losses of chlorophylls and carotenoids in leaves of all studied trees were directly related to the infection severity (quantified as the proportion of damaged leaf area to the total leaf area). Our results may help developing an approach to assess the effect of gall mites on the chlorophyll content and the photosynthetic productivity of trees, based on the direct or remote analysis of damaged leaf surface.
DOI: 10.21684/0132-8077-2022-30-1-89-98
Bibliography:
Ajoykumar, K.N. and Subitha, P.P. 2019. Physiochemical changes associated with foliar gall formation by a psyllid insect Trioza pallida Haupt. in Mallotus philippensis Muell. Arg. International Journal of Research in Advent Technology, 7 (2): 721–728.
Albert, S., Padhiar, A., Gandhi, D. and Nityanand, P. 2011. Morphological, anatomical and biochemical studies on the foliar galls of Alstonia scholaris (Apocynaceae). Rev Bras Bot, 34: 343–358.
Chetverikov, P.E., Vishyakov, A.E., Dodueva, I.T., Osipova, M.A., Sukhareva, S.I. and Shavarda, A.L. 2015. Gallogenesis induced by eryophyoid mites (Acariformes: Eriophyoidea). Entomological Review, 95 (8): 1137–1143. DOI: 10.1134/S0013873815080217
Chetverikov, P.E., Dodueva, I.E., Pautov, A.A., Krylova, E.G., Paponova, S.S. and Shavarda, A.L. 2018. Metabolomic changes in a model system of gallogenesis induced by eriophyoid mites. In: Abstract Book of XV International Congress of Acarology. Antalya, Turkey, p. 210.
De Lillo, E., Pozzebon, A., Valenzano, D. and Duso, C. 2018. An intimate relationship between eriophyoid mites and their host plants—a review. Frontiers in Plant Science, 9: 1786.
Dengler, N.G. and Kang, J. 2001.Vascular patterning and leaf shape. Current Opinion in Plant Biology, 4: 50–56.
Desnitskiy, A.G. and Chetverikov, P.E. 2022. Induction of leaf galls by four-legged mites (eriophyoidea) as a problem of developmental biology. Russian Journal of Developmental Biology, 53 (1): 6–14. DOI: 10.1134/S1062360422010039
Dorchin, N., Cramer, M.D. and Hoffmann, J.H. 2006. Photosynthesis and sink activity of wasp‐induced galls in Acacia pycnantha. Ecology, 87: 1781–1791.
Fay, P.A., Hartneet, D.C. and Knapp, A.K. 1993. Increased photosynthesis and water potentials in Silphium integrifolium galled by cynipid wasps. Oecologia 93: 114–120.
Fernandes, G.W., Coelho, M.S. and Lüttge, U. 2010. Photosynthetic efficiency of Clusia arrudae leaf tissue with and without Cecidomyiidae galls. Brazilian Journal of Biology, 70: 723–728.
Huang, M.Y., Chou, H.M., Chang, Y.D. and Yang, C.M. 2014. The number of cecidomyiid insect galls affects the photosynthesis of Machilus thunbergii host leaves. Journal of Asia‐Pacific Entomology, 17: 151–154.
Ivanov, L.A., Ivanova, L.A., Ronzhina, D.A. and Yudina, P.K. 2013. Changes in the chlorophyll and carotenoid contents in the leaves of steppe plants along a latitudinal gradient in South Ural. Russian Journal of Plant Physiology, 30: 812. DOI: 10.1134/S1021443713050075
Ivanov, L.A., Ronzhina, D.A., Yudina, P.K., Zolotareva, N.V., Kalashnikova, I.V. and Ivanova, L.A. 2020. Seasonal dynamics of the chlorophyll and carotenoid content in the leaves of steppe and forest plants on species and community level. Russian Journal of Plant Physiology, 67 (3): 453–462. DOI: 10.1134/S1021443720030115
Ivanova, L.A., Yudina, P.K., Ronzhina, D.A., Ivanov, L.A. and Hölzel, N. 2018. Quantitative mesophyll parameters rather than whole-leaf traits predict response of C3 steppe plants to aridity. New Phytologist, 217 (2): 558–570. DOI: 10.1111/nph.14840
Ivanova, L.A., Ivanov, L.A., Ronzhina, D.A., Yudina, P.K., Migalina, S.V., Shinehuu, T., Tserenkhand, G., Voronin, P.Yu., Anenkhonov, O., Bazha, S.N. and Gunin, P.D. 2019. Leaf traits of C3- and C4-plants indicating climatic adaptation along a latitudinal gradient in Southern Siberia and Mongolia. FLORA, 254: 122–134. DOI: 10.1016/j.flora.2018.10.008
Jiang, Y.F., Veromann, L.L., Ye, J.Y. and Niinemets, Ü. 2018. Oak gall wasp infections of Quercus robur leaves lead to profound modifications in foliage photosynthetic and volatile emission characteristics. Plant Cell Environ, 41: 160–175.
Jiang, Y., Ye, J., Veromann-Jürgenson, L. and Niinemets, Ü. 2021. Gall- and erineum-forming Eriophyes mites alter photosynthesis and volatile emissions in an infection severity-dependent manner in broad-leaved trees Alnus glutinosa and Tilia cordata. Tree Physiology, 41 (7): 1122–1142. DOI: 10.1093/treephys/tpaa173
Kalashnikova, I., Migalina, S., Ronzhina, D., Ivanov, L. and Ivanova, L. 2021. Functional response of Betula species to edaphic and nutrient stress during restoration of fly ash deposits in the Middle Urals (Russia). Environmental Science and Pollution Research, 28: 12714–12724. DOI: 10.1007/s11356-020-11200-5
Kane, N.A., Jones, C.S. and Vuorisalo, A.T. 1997. Development of galls on leaves of Alnus glutinosa and Alnus incana (Betulaceae) caused by the eriophyid mite Eriophyes laevis (Nalepa). International Journal of Plant Sciences, 158: 13–23.
Kołątaj K.T. 2016. Leaf blister mites (Eriophyes sp.) as significant pests in orchards. In: Scientific Proceedings of the 5th International Scientific Horticulture Conference, pp. 55–59.
Lambers, H., Chapin, F.S., III and Pons, T.L. 2008. Plant Physiological Ecology. Springer, New York. 605 pp. DOI: 10.1007/978-0-387-78341-3
Lichtenthaler, H.K., Ač, A., Marek, M.V., Kalina, J. and Urban, O. 2007. Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species. Plant Physiology and Biochemistry, 45: 577. DOI: 10.1016/j.plaphy.2007.04.006
Lindquist, E.E. 1996. Chapter 1.1 External anatomy and systematics 1.1.1. External anatomy and notation of structures. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Eds.). World Crop Pests. Elsevier, pp. 3–31.
Migalina, S.V., Ivanova, L.A. and Makhnev, A.K. 2009. Size of the leaf as a marker of birch productivity at a distance from the climatic optimum. Russian Journal of Plant Physiology, 56 (6): 857–861.
Migalina, S.V., Ivanova, L.A. and Makhnev, A.K. 2010. Changes in leaf morphology in Betula pendula Roth and B. pubescens Ehrh. along a zonal–climatic transect in the Urals and Western Siberia. Russian Journal of Ecology, 41 (4): 263–271.
Moghe, M. 1980. Studies on the insect gall of Ficus racemosa Linn. Ph.D. Thesis. The Maharaja Sayajirao University, Vadodara.
Nyman, R. and Julkunen-Tiitto, R. 2001. Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proceedings of the National Academy of Sciences, 97: 13184–13187.
Paponova, S.S., Chetverikov, P.E., Pautov, A.A., Yakov-leva, O.V., Zukoff, S.N., Vishnyakov, A.E., Sukhareva, S.I., Krylova, E.G., Dodueva, I.E. and Lutova, L.A. 2018. Gall mite Fragariocoptes setiger (Eriophyoidea) changes leaf developmental program and regulates gene expression in the leaf tissues of Fragaria viridis (Rosaceae). Annals of Applied Biology, 172 (1): 33–46. DOI: 10.1111/aab.12399
Patankar, R., Starr, G., Mortazavi, B., Oberbauer, S.F. and Rosenblum, A. 2013. The effects of mite galling on the ecophysiology of two arctic willows. Arctic, Antarctic, and Alpine Research, 45 (1): 99–106. DOI: 10.1657/1938-4246-45.1.99
Poorter, H., Niinemets, Ü., Ntagkas, N., Siebenkäs, A., Mäenpää, M., Matsubara, S. and Pons, T.L. 2019. A meta‐analysis of plant responses to light intensity for 70 traits ranging from molecules to whole plant performance. New Phytologist, 223: 1073–1105.
Qian, X., Zhang, Y., Liu, L. and Du, S. 2019. Exploring the potential of leaf reflectance spectra for retrieving the leaf maximum carboxylation rate. International Journal of Remote Sensing 40: 5411–5428.
Skoracka, A., Smith, L., Oldfield, G., Cristofaro, M., Amrine, J.W. 2010. Host-plant specificity and specialization in eriophyoid mites and their importance for the use of eriophyoid mites as biocontrol agents of weeds. Experimental and Applied Acarology, 51: 93–113. DOI: 10.1007/s10493-009-9323-6
Soika, G. and Kozak, M. 2013. Eriophyes species (Acari: Eriophyoidea) inhabiting lime trees (Tilia spp.: Tiliaceae)—supplementary description and morphological variability related to host plants and female forms. Zootaxa, 3646: 349–385.
Tooker, J.F. and De Moraes, C.M. 2008. Gall insects and indirect plant defenses: a case of active manipulation? Plant Signaling and Behavior, 3: 503–504.
Wellburn, A.R. 1994. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology, 144 (3): 307–313. DOI: 10.1016/S0176-1617(11)81192-2
Westphal, E. and Manson, D.C. M. 1996. Chapter 1.4.6. Feeding effects on host plants: Gall formation and other distortions. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Eds.). Eriophyoid Mites: Their Biology, Natural Enemies and Control. World Crop Pests. Elsevier Science Publishing, Amsterdam, The Netherlands, vol 6, pp. 231–242. DOI: 10.1016/S1572-4379(96)80014-5
Ye, J., Jiang, Y., Veromann-Jürgenson, L.L. and Niinemets, Ü. 2019. Petiole gall aphid (Pemphigus spyrothecae) infestation of Populus × petrovskiana leaves alters foliage photosynthetic characteristics and leads to enhanced emissions of both constitutive and stress-induced volatiles. Trees: Structure and Function, 33: 37–51.