Physiological responses of pedunculate oak (Quercus robur L.) to Corythucha arcuata (Say, 1832) attack
Keywords:
mineral element concentrations, oak lace bug, oxidative stress, photosynthesis, QuercusAbstract
Paper description:
- Herbivory insects can affect photosynthetic characteristics, foliar nutrients and the oxidative status of plant tissues in different host species.
- To our knowledge, this is the first report on the effect of oak lace bug (Corythucha arcuate) feeding on the photosynthetic characteristics and gas-exchange parameters, mineral nutrient concentrations and potential defense mechanisms (activities of some antioxidant enzymes) on the leaves of Quercus roburL. (pedunculate oak).
- Elucidation of the physiological responses should contribute to an improved understanding of the mechanisms involved in the response of host plants to stress induced by insect herbivory.
Abstract: The spread and occurrence of the oak lace bug Corythucha arcuata out of its natural distribution area across European and Asian countries has been reported during the past decades. The ecological and economic significance of oak stands and the vulnerability of plants to various abiotic and/or biotic factors requires in-depth knowledge of plant-pest interaction. The present study examined the influence of C. arcuata feeding on the photosynthetic characteristics and gas-exchange parameters, mineral nutrient concentrations and defense mechanisms (the activities of some antioxidant enzymes) of leaves of pedunculate oak. The rate of photosynthesis, transpiration and stomatal conductance were lowered by 58.84, 21.66 and 35.71%, respectively, in comparison to non-infested plants. The concentrations of photosynthetic pigments and activities of antioxidant enzymes, catalase and ascorbate peroxidase, were affected by the presence of C. arcuata. To our knowledge this is the first paper providing a report on the physiological responses of Quercus robur plants exposed to C. arcuata infestation. Understanding the impact of pests, such as the invasive species C. arcuata on physiological processes and vitality of young plants and plant responses, could provide a foundation for efficient preservation of oak forests endangered by the oak lace bug.
https://doi.org/10.2298/ABS180927058N
Received: September 27, 2018; Revised: November 30, 2018; Accepted: December 14, 2018; Published online: December 26, 2018
How to cite this article: Nikolić N, Pilipović A, Drekić M, Kojić D, Poljaković-Pajnik L, Orlović S, Arsenov D. Physiological responses of Pedunculate oak (Quercus robur L.) to Corythucha arcuata (Say, 1832) attack. Arch Biol Sci. 2019;71(1):167-76.
Downloads
References
Rabitsch W. Alien True Bugs of Europe (Insecta: Hemiptera: Heteroptera). Zootaxa. 2008;1827:1-44.
Mutun S, Ceyhan Z, Sözen C. Invasion by the oak lace bug, Corythucha arcuata (Say) (Heteroptera: Tingidae), in Turkey. Turk J Zool. 2009;33:263-8.
Bernardinelli I, Zandigiacomo P. Prima segnalozione di Corythucha arcuata (Say) (Heteroptera, Tingidae) in Europe. Inf Fitopatol. 2000;12:47-9.
Mutun S. First report of the oak lace bug, Corythucha arcuata (Say, 1832) (Heteroptera: Tingidae) from Bolu, Turkey. Israel J Zool. 2003;49(4):323-4.
Forster B, Giacalone I, Moretti M, Dioli P, Wermelinger B. Die amerikanische Eichennetzwanze Corythucha arcuata (Say) (Heteroptera, Tingidae) hat die Südschweiz erreicht. Mitt Schweiz Entomol Ges. 2005;78:317-23.
Samin N, Linnavuori RE. A contribution to the Tingidae (Heteroptera) from north and northwestern Iran. Entomofauna. 2011;32(25):373-80.
Dobreva M, Simov N, Georgiev G, Mirchev P, Georgieva M. First record of Corythucha arcuata (Say) (Heteroptera: Tingidae) on the Balkan Peninsula. Acta Zool Bulgar. 2013;65(3):409-12.
Hrašovec B, Posarić D, Lukić I, Pernek M. First record of oak lace bag (Corythucha arcuata) in Croatia. Šumarski list. 2013;9-10:499-503.
Csóka G, Hirka A, Somlyai M. First record of oak lace bag (Corythucha arcuata Say, 1832) in Hungary. Növényvédelem. 2013;49(7):293-6.
Pap P, Drekić M, Poljaković-Pajnik L, Marković M, Vasić V. Forest health monitoring in Vojvodina in 2015. Topola. 2015;195/196:117-33.
Don I, Don CD, Sasu LR, Vidrean D, Brad ML. Insect pests on the trees and shrubs from the Macea Botanical garden. Studia Universitatis ‘Vasile Goldiş’ Arad Seria Ştiinţe Inginereşti şi Agro-Turism. 2016;11(2): 23-8.
Neimorovets VV, Shchurov VI, Bondarenko AS, Skvortsov MM, Konstantinov FV. First documented outbreak and new data on the distribution of Corythucha arcuata (Say, 1832) (Hemiptera: Tingidae) in Russia. Acta Zool Bulg. 2017;9:139-42.
Jurc M, Jurc D. The first record and the beginning of the spread of oak lace bug, Corythucha arcuata (Say, 1832) (Heteroptera: Tingidae), in Slovenia. Šumarski list. 2017;9-10:485-8.
Dautbašić M, Zahirović K, Mujezinović O, Margaletić J. First record of oak lace bug (Corythucha arcuata) in Bosnia and Herzegovina. Šumarski list. 2018;3-4:179-81.
Connor EF. Plant water deficits and insect responses: the preference of Corythucha arcuata (Heteroptera: Tingidae) for the foliage of white oak, Quercus alba. Ecol Entomol. 1988;13:375-81.
Zhang Y, Hanula JL, O’Brien J, Horn S, Braman K, Sun J. Evaluation of the impacts of herbivory by lace bugs on Chinese privet (Ligustrum sinense) survival and physiology. Biol Control. 2013;64:299-304.
Bernardinelli I. European host plants and potential distribution of Corythucha arcuata (Say) (Heteroptera: Tingidae). In: Csóka Gy, Hirka A, Koltay A, editors. Biotic damage in forests. Methodology of forest pest and disease survey in Central Europe; 2006 Sep 12-16; Mátrafüred, Hungary. Mátrafüred, Hungary: Hungarian Forest Research Institute Agroinform Publishing House; 2006. p. 10-7.
Drew WA, Arnold DC. Tingoidea of Oklahoma (Hemiptera). Proc Okla Acad Sci. 1977;57:29-31.
Nair S, Braman SK, Knauft DA. Resistance mechanisms in Pieris taxa (Ericaceae) to Stephanitis takeyai (Hemiptera: Tingidae). Environ Entomol. 2012;41(5):1153-62.
Barber NA. Light environment and leaf characteristics affect distribution of Corythucha arcuata (Hemiptera: Tingidae). Environ Entomol. 2010;39(2):492-7.
European and Mediterranean Plant Protection Organization (EPPO) [Internet]. Paris: Mini data sheet on Corythucha arcuata; 2003 [modified 2007 Mar; cited 2018 Aug 15]. Available from: https://gd.eppo.int/download/doc/1059_minids_CRTHAR.pdf.
De Bruyn L, Scheirs J, Verhagen R. Nutrient stress, host plant quality and herbivore performance of a leaf-mining fly on grass. Oecologia. 2002;130:594-9.
Behmer ST. Insect herbivore nutrient regulation. Annu Rev Entomol. 2009;54:165-87.
Cockfield SD. Relative availability of nitrogen in host plants of invertebrate herbivores: three possible nutritional and physiological definitions. Oecologia. 1988;77:91-4.
Kozlowski TT, Kramer PJ, Pallardy SG. The Physiological Ecology of Woody Plants. New York, Tokyo, London, Toronto, Sydney: Academic Press; 1991. 277-9 p.
Welter SC. Arthropod impact on plant gas exchange. In: Bernays EA, editor. Insect–plant interactions. Boca Raton, FL: CRC Press; 1989. p. 135-51.
Buntin GD, Braman SK, Gilbertz DA, Phillips DV. Chlorosis, photosynthesis, and transpiration of azalea leaves after azalea lace bug (Heteroptera: Tingidae) feeding injury. J Econ Entomol. 1996;89:990-5.
Zangerl AR, Hamilton JG, Miller TJ, Crofts AR, Oxborough K, Berenbaum MR, DeLucia EH. Impact of folivory on photosynthesis is greater than the sum of its holes. Proc Natl Acad Sci. 2002;99:1088-91.
Haile FJ, Higley LG. Changes in soybean gas-exchange after moisture stress and spider mite injury. Environ Entomol. 2003;32(3):433-40.
Gutsche AR, Heng-Moss TM, Higley LG, Sarath G, Mornhinweg DW. Physiological responses of resistant and susceptible barley, Hordeum vulgare to the Russian wheat aphid, Diurpahis noxia (Mordvilko). Arthropod Plant Interact. 2009;3:233-40.
Casotti G, Bradley JS. Leaf nitrogen and its effects on the rate of herbivory on selected eucalypts in the jarrah forest. Forest Ecol Manag. 1991;41:167-7.
Silva AA, Varanda EM, Primavesi AC. Effect of the inherent variation in the mineral concentration of alfalfa cultivars on aphid populations. Bragantia. 2005;64:233-9.
Johnson SN, Hawes C, Karley AJ. Reappraising the role of plant nutrients as mediators of interactions between root- and foliar-feeding insects. Funct Ecol. 2009;23:699-706.
Bi JL, Felton GW. Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites and reactive oxygen species as components of induced resistance. J Chem Ecol. 1995;21(10):1511-30.
Łukasik I, Goławska S, Wójcicka A. Effect of cereal aphid infestation on ascorbate content and ascorbate peroxidase activity in triticale. Pol J Environ Stud. 2012;21(6):1937-41.
Bittner N, Trauer-Kizilelma U, Hilker M. Early plant defense against insect attack: involvement of reactive oxygen species in plant responses to insect egg deposition. Planta. 2017;245(5):993-1007.
Taggar GK, Gill RS, Gupta AK, Sadhu JS. Fluctuations in peroxidase and catalase activities of resistant and susceptible black gram (Vigna mungo (L.) Hepper) genotypes elicited by Bemisia tabaci (Gennadius) feeding. Plant Signal Behav. 2012;7(10):1321-9.
Franzen LD, Gutsche AR, Heng-Moss TM, Higley LG, Sarath G, John D. Burd JD. Physiological and biochemical responses of resistant and susceptible wheat to injury by Russian wheat aphid. J Econ Entomol. 2007;100(5):1692-703.
Hu ZH, Shen YB, Shen FY, Su XH. Effects of feeding Clostera anachoreta on hydrogen peroxide accumulation and activities of peroxidase, catalase, and ascorbate peroxidase in Populus simonii × P. pyramidalis ‘Opera 8277’ leaves. Acta Physiol Plant. 2009;31:995-1002.
Zhao H, Sun X, Xue M, Zhang X, Li Q. Antioxidant enzyme responses induced by whiteflies in tobacco plants in defense against aphids: catalase may play a dominant role. PLoS One. 2016;11(10):e0165454.
Von Wettstein D. Chlorophyll-letale und der submikroskopische formwechsel der plastiden. Exp Cell Res. 1957;12:427-506.
Schwanz P, Polle A. Differential stress responses of antioxidative systems to drought in pedunculate oak (Quercus robur) and maritime pine (Pinus pinaster) grown under high CO2 concentrations. J Exp Bot. 2001;52:133-43.
Aebi H. Catalase in vitro. Method Enzymol. 1984;105:121-6.
Polle A, Chakrabarti K, Schürmann W, Rennenberg H. Composition and properties of hydrogen peroxide decomposing systems in extracellular and total extracts from needles of norway spruce (Picea abies L., Karst.). Plant Physiol. 1990;94:312-9.
Hageman RH, Reed AJ. Nitrate reductase from higher plants. Methods Enzymol. 1980;69:270-9.
Gericke S, Kurmies B. Die kolorimetrische phosphorsäurebestimmung mit ammonium-vanadat-molybdat und ihre anwendung in der pflanzenanalyse. Z Pflanz Bodenkunde. 1952;59:235-47.
Nelson DW, Sommers LE. Determination of total nitrogen in plant material. Agron J. 1973;65:109-12.
Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia, EH. Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ. 2010;33:1597-613.
.Kerchev PI, Fenton B, Foyer CH, Hancock RD. Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. Plant Cell Environ. 2012;35:441-53.
Schwachtje J, Baldwin IT. Why does herbivore attack reconfigure primary metabolism? Plant Physiol. 2008;146:845-51.
Mohanta TK, Occhipinti A, Zebelo SA, Foti M, Fliegmann J, Bossi S, Maffei ME, Bertea CM. Ginkgo biloba responds to herbivory by activating early signaling and direct defenses. PLoS One. 2012;7(3):e32822.
Passardi F, Cosio C, Penel C, Dunand C. Peroxidases have more functions than a Swiss army knife. Plant Cell Rep. 2005;24:255-65.
Apel K, Hirt H. Reactive oxygen species: Metabolism, Oxidative Stress and Signal Transduction. Annu Rev Plant Biol. 2004;55:373-99.
Haukioja E, Ruohomäki K, Suomela J, Vuorisalo T. Nutritional quality as a defense against herbivores. Forest Ecol Manag. 1991;39:237-45.
Nikolić N, Krstić B, Pajević S, Orlović S. Variability of leaf characteristics in different pedunculate oak genotypes (Quercus robur L.). Proc Nat Sci Matica Srpska. 2006;110:95-105.
Barbehenn RV, Kapila M, Kileen S, Nusbaum CP. Acquiring nutrients from tree leaves: effects of leaf maturity and development type on a generalist caterpillar. Oecologia. 2017;184:59-73.
Cease AJ, Fay M, Elser JJ, Harrison JF. Dietary phosphate affects food selection, post-ingestive phosphorus fate, and performance of a polyphagous herbivore. J Exp Biol. 2016;219:64-72.
Coley PD, Bateman ML, Kursar TA. The effects of plant quality on caterpillar growth and defense against natural enemies. Oikos. 2006;115:219-28.
Basset Y. Influence of leaf traits on the spatial distribution of insect herbivores associated with an overstorey rainforest trees. Oecologia. 1991;87:388-93.
Kaur M, Kumar R, Upendrabhai DP, Singh IP, Kaur S. Impact of sesquiterpenes from Inula racemosa (Asteraceae) on growth, development and nutrition of Spodoptera litura (Lepidoptera: Noctuidae). Pest Manag Sci. 2017;73:1031–38.
Downloads
Published
How to Cite
Issue
Section
License
Authors grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work’s authorship and initial publication in this journal.