The effect of gall mites (Acariformes, Eriophyoidea) on leaf morphology and pigment content of deciduous trees in West Siberia

Journal:

2022. 30 (1)

Publicatione: 

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


Philipp E. Chetverikov,

Zoological Institute, Russian Academy of Sciences, Saint-Petersburg, Russia; Saint-Petersburg State University, Saint-Petersburg, Russia


Leonid A. Ivanov,

X-BIO Institute, Tyumen State University, Tyumen, Russia; Institute Botanic Garden, Ural Branch, Russian Academy of Sciences, Ekaterinburg, Russia


Shinekhuu Tumurjav,

X-BIO Institute, Tyumen State University, Tyumen, Russia


Igor V. Kuzmin,

X-BIO Institute, Tyumen State University, Tyumen, Russia


Alexey G. Desnitskiy, e-mail

Saint-Petersburg State University, Saint-Petersburg, Russia


Andrei V. Tolstikov,

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 Lttge, 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.