Теоретическая и прикладная экология1995-43012618-840610.25750/1995-4301-2026-2-200-209OtherСостояние фотосинтетического аппарата и уровень окислительного стресса хвои Abies sibirica L. на разных стадиях усыхания деревьев, поражённых уссурийским полиграфом (Polygraphus proximus Blandford) в лесных насаждениях Пермского краяPhotosynthetic apparatus state and oxidative stress level in needles of Abies sibirica L. at different stages of tree dieback infested with the four-eyed fir bark beetle (Polygraphus proximus Blandford) in forest stands of the Perm KraiШелякинМ. А.ShelyakinM. A.shelyakin@ib.komisc.ruhttps://orcid.org/0000-0001-8537-6995ГармашЕ. В.GarmashE. V.https://orcid.org/0000-0001-8104-5048СилинаЕ. В.SilinaE. V.https://orcid.org/0000-0002-9632-3431ЯдрихинскийК. В.YadrikhinskyK. V.https://orcid.org/0009-0002-1190-9271РотэрмельЭ. Е.RotermelE. E.https://orcid.org/0009-0007-0238-9178ИванчинаЛ. А.IvanchinaL. A.https://orcid.org/0000-0001-9476-8683Perm State UniversityPermRussiaInstitute of Biology of the Komi Science Centre of the Ural Branch of the Russian Academy of SciencesSyktyvkarRussiaПермский государственный национальный исследовательский университетПермьРоссияИнститут биологии Коми научного центра Уральского отделения Российской академии наукСыктывкарРоссия250620262200209http://envjournal.ru/ari/v2026/v2/26220.pdf

Массовое усыхание пихты (Abies sibirica L.) в таёжной зоне России спровоцировано инвазионным стволовым вредителем - уссурийским полиграфом (Polygraphus proximus). Ранняя диагностика очагов поражения требует разработки экспресс-методов дистанционного зондирования и новых вегетационных индексов, чувствительных к изменению физиолого-биохимических параметров хвои. Исследования проводили на 15 участках хвойно-широколиственных лесов Пермского края. Выделены следующие категории санитарного состояния деревьев пихты (КСС): здоровое (I), ослабленное (II), сильно ослабленное (III), усыхающее (IV), среди категории погибших деревьев исследовали свежий (V) и старый сухостой (VI). Изучали состояние фотосинтетического аппарата хвои по содержанию пигментов и показателям индуцированной флуоресценции хлорофилла, а также уровень окислительного стресса - по концентрации H2O2 и продуктов перекисного окисления липидов. В хвое деревьев первых трёх КСС с увеличением степени их усыхания параметры флуоресценции хлорофилла, отражающие эффективность использования световой энергии (Fv/Fm, ΦPSII, ETR), проявляли тенденцию к снижению на фоне стабильного содержания фотосинтетических пигментов и их соотношений. При этом коэффициент нефотохимического тушения флуоресценции хлорофилла (NPQ) и концентрация прооксидантов незначительно, но повышались, что указывало на мобилизацию защитных механизмов. Заметные повреждения фотосинтетического аппарата, характеризующиеся деградацией хлорофиллов, ослаблением фотосинтетической активности и усилением окислительных реакций, зафиксированы в хвое уже усыхающих деревьев (КСС IV). У хвои погибших деревьев (V-VI) содержание пигментов резко снижалось, фотосинтез прекращался, а уровень прооксидантов заметно падал, что свидетельствовало о прекращении жизненных процессов. Намечены перспективы применения параметров состояния фотосинтетического аппарата и прооксидантного статуса хвои пихты для создания моделей дистанционного мониторинга на основе спектральных характеристик отражения крон.

The invasive stem pest, four-eyed fir bark beetle Polygraphus proximus, drives the Abies sibirica L. massive dieback in the Russian taiga zone. Early detection of infestation hotspots requires the development of rapid remote sensing methods and novel vegetation indices sensitive to changes in the physiological and biochemical parameters of needles. Research was completed across 15 sites in coniferous-broadleaf forests in the Perm Krai. The following categories of fir tree sanitary condition (CSC) were identified: healthy (I), weakened (II), severely weakened (III), dying (IV); and among dead trees: recent deadwood (V) and old deadwood (VI). We assessed the photosynthetic apparatus state in the needles by photosynthetic pigment content and chlorophyll fluorescence parameters. Oxidative stress level was evaluated by measuring H2O2 and lipid peroxidation products concentration in the needles. In the needles of the I-III CSC trees, with increasing desiccation rate, chlorophyll fluorescence parameters reflecting the efficiency of light energy using (Fv/Fm, ΦPSII, ETR) tended to decrease while photosynthetic pigment content and ratios were stable. Concurrently, the non-photochemical quenching coefficient (NPQ) and pro‐oxidant content slightly increased, indicating a mobilization of protective mechanisms. Significant damage of the photosynthetic apparatus, characterized by chlorophyll degradation, weakened photosynthetic activity, and increased oxidative reactions, was recorded in the dying trees’ (CSC IV) needles. In the needles of dead trees (V-VI), pigment content dropped sharply, photosynthesis ceased, and pro‐oxidant level declined markedly, indicating the cessation of vital processes. Prospects for using parameters of the photosynthetic apparatus and the pro‐oxidant status of fir needles are outlined for creating remote monitoring models based on the spectral reflectance of tree crowns.

Abies sibiricaфлуоресценция хлорофиллафотосинтетические пигментыпероксид водородаперекисное окисление липидовусыханиеPolygraphus proximusAbies sibiricachlorophyll fluorescencephotosynthetic pigmentshydrogen peroxidelipid peroxidationdiebackPolygraphus proximusИсследование выполнено при поддержке гранта РНФ 24-76-10057 «Исследование по оперативному автоматизированному выявлению усыханий елово-пихтовых древостоев с применением геоинформационных технологий».1. Chebakova N.M., Bazhina E.V., Parfenova E.I., Senashova V.A. In search of an X factor: A review of publications on the issue of dark-needled forest decline/dieback in Northern Eurasia // Russ. Meteorol. Hydrol. 2022. V. 47. P. 405–417. doi: 10.3103/S10683739220500902. Kharuk V.I., Im S.T., Petrov I.A., Dvinskaya M.L., Shushpanov A.S., Golyukov A.S. Climate-driven conifer mortality in Siberia // Global Ecology and Biogeography. 2021. V. 30. No. 2. P. 543–556. doi: 10.1111/geb.132433. Krivets S.A., Kerchev I.A., Bisirova E.M., Volkova E.S., Astapenko S.A., Efremenko A.A., Kosilov A.Yu., Kudryavtsev P.P., Kuznetzova Yu.P., Ponomarev V.I., Potapkin A.B., Taraskin E.G., Titova V.V., Shilonosov A.O., Baranchikov Yu.N. Overview of the current secondary range of the four-eyed fir bark beetle (Polygraphus proximus Blandford) in the Russian Federation // Russian Journal of Biological Invasions. 2024. V. 17. No. 1. P. 49–69 (in Russian). doi: 10.35885/1996-1499-17-1-49-694. Zhilа S.V., Furyaev I.V., Kovaleva N.M. Assessment of stocks of forest combustible materials in fir stands, damaged by the four-eyed fir bark beetle in Krasnoyarsk Krai // Sibirskij Lesnoj Zurnal (Sib. J. For. Sci.). 2023. No. 6. P. 76–84 (in Russian). doi: 10.15372/SJFS202306085. Saltsevich Yu.V., Buryak L.V., Golovina A.N., Kukavskaya E.A. Assessment of the state of forest disturbed by fires, logging, and insects in the foothills of the Eastern Sayan Mountains // Sibirskij Lesnoj Zurnal (Sib. J. For. Sci.). 2023. No. 6. P. 63–75 (in Russian). doi: 10.15372/SJFS202306076. Ivаnchinа L.A., Rotermel’ Е.Е., Bol’shakov Е.G., Shilonosov A.O. The influence of the type of forest on the resistance of fir stands in the southern taiga subzone of Perm Krai to colonization by the four-eyed fir bark beetle // Geographical Bulletin. 2025. No. 2 (73). P. 130–140 (in Russian). doi: 10.17072/2079-7877-2025-2-130-1407. Kerchev I.A. Ecology of four-eyed fir bark beetle Polygraphus proximus Blandford (Coleoptera; Curculionidae, Scolytinae) in the west Siberian region of invasion // Russ. J. Biol. Invasions. 2014. V. 5. P. 176–185. doi: 10.1134/S20751117140300728. Ecke S., Dempewolf J., Frey J., Schwaller A., Endres E., Klemmt H-J., Tiede D., Seifert T. UAV-based forest health monitoring: A systematic review // Remote Sens. 2022. V. 14. Article No. 3205. doi: 10.3390/rs141332059. Peguero-Pina J.J., Camarero J.J., Abadía A., Martín E., González-Cascón R., Morales F., Gil-Pelegrín E. Physiological performance of silver-fir (Abies alba Mill.) populations under contrasting climates near the south-western distribution limit of the species // Flora. 2007. V. 202. P. 226–236. doi: 10.1016/j.flora.2006.06.00410. D’Odorico P., Schönbeck L., Vitali V., Meusburger K., Schaub M., Ginzler C., Zweifel R., Velasco V.M.E., Gisler J., Gessler A., Ensminger I. Drone-based physiological index reveals long-term acclimation and drought stress responses in trees // Plant Cell Environ. 2021. V. 44. No. 11. P. 3552–3570. doi: 10.1111/pce.1417711. Trubin A., Kozhoridze G., Zabihi K., Modlinger R., Singh V.V., Surový P., Jakuš R. Detection of susceptible Norway spruce to bark beetle attack using PlanetScope multispectral imagery // Front. For. Glob. Change. 2023. V. 6. Article No. 1130721. doi: 10.3389/ffgc.2023.113072112. Richardson A.D., Berlyn G.P., Gregoire T.G. Spectral reflectance of Picea rubens (Pinaceae) and Abies balsamea (Pinaceae) needles along an elevational gradient, Mt. Moosilauke, New Hampshire, USA // Am. J. Bot. 2001. V. 88. No. 4. P. 667–676. doi: 10.2307/265706713. Zhang Y., Luan Q., Jiang J., Li Y. Prediction and utilization of malondialdehyde in exotic pine under drought stress using near-infrared spectroscopy // Front. Plant Sci. 2021. V. 12. Article No. 735275. doi: 10.3389/fpls.2021.73527514. Foyer C.H., Noctor G. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria // Physiologia Plantarum. 2003. V. 119. No. 3. P. 355–364. doi: 10.1034/j.1399-3054.2003.00223.x15. Golovko T.K., Silina E.V., Lashmanova E.A., Kozlovskaya A.V. Reactive oxygen species and antioxidants in living systems: An integrative review // Theoretical and Applied Ecology. 2022. No. 1. P. 17–26 (in Russian). doi: 10.25750/1995-4301-2022-1-017-02616. Garmash E.V., Velegzhaninov I.O., Grabelnych O.I., Borovik O.A., Silina E.V., Voinikov V.K., Golovko T.K. Expression profiles of genes for mitochondrial respiratory energy-dissipating systems and antioxidant enzymes in wheat leaves during de-etiolation // J. Plant Physiol. 2017. V. 215. P. 110–121. doi: 10.1016/j.jplph.2017.05.02317. Shelyakin M.A., Silina E.V., Golovko T.K. Age and adaptive changes in pro-/antioxidant metabolism indicators and respiration of the winter-green herbaceous plant Ajuga reptans L. in natural conditions of the taiga zone // Russ. J. Plant Physiol. 2024. V. 71. Article No. 31. doi: 10.1134/S102144372460439718. Gechev T.S., Van Breusegem F., Stone J.M., Denev I., Laoli C. Reactive oxygen species as signals that modulate plant stress responses and programmed cell death // BioEssays. 2006. V. 28. No. 11. P. 1091–1101. doi: 10.1002/bies.2049319. Mubarakshina M.M., Ivanov B.N., Naydov I.A., Hillier W., Badger M.R., Krieger-Liszkay A. Production and diffusion of chloroplastic H2O2 and its implication to signalling // J. Exp. Bot. 2010. V. 61. No. 13. P. 3577–3587. doi: 10.1093/jxb/erq17120. Safonova A., Tabik S., Alcaraz-Segura D., Rubtsov A., Maglinets Yu., Herrera F. Detection of fir trees (Abies sibirica) damaged by the bark beetle in unmanned aerial vehicle images with deep learning // Remote Sens. 2019. V. 11. Article. 643. doi: 10.3390/rs1106064321. Volkova E.S., Kerchev I.A., Krivets S.A., Melnik M.A. Experience of mapping invasions by forest alien pest insects in Western Siberia using GIS tools // Geography and Natural Resources. 2023. V. 44. No. S5. P. 146–153 (in Russian). doi: 10.15372/GIPR2023051822. Ivanchina L.A., Shilonosov L.A., Shikhov A.N. Estimation of drying out of dark coniferous forests caused by the spread of the four-eyed fir bark beetle in Perm Krai based on satellite and field observations // Sovremennye problemy distantsionnogo zondirovaniya Zemli iz Kosmosa. 2025. V. 22. No. 3. P. 149–160 (in Russian). doi: 10.21046/2070-7401-2025-22-3-149-16023. Goltsev V.N., Kalaji H.M., Paunov M., Bąba W., Horaczek T., Mojski J., Kociel H., Allakhverdiev S.I. Variable chlorophyll fluorescence and its use for assessing physiological condition of plant photosynthetic apparatus // Russ. J. Plant Physiol. 2016. V. 63. P. 869–893. doi: 10.1134/S102144371605005824. Lichtenthaler H.K. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes // Methods in Enzymology / Eds. S.P. Colowick, N.O. Kaplan. San Diego: Academic Press, 1987. P. 350–382. doi: 10.1016/0076-6879(87)48036-125. Heath R.L., Packer L. Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation // Arch. Biochem. Biophys. 1968. V. 125. No. 1. P. 189–198. doi: 10.1016/0003-9861(68)90654-126. Bellincampi D., Dipierro N., Salvi G., Cervone F., De Lorenzo G. Extracellular H2O2 induced by oligogalact-uronides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants // Plant Physiol. 2000. V. 122. No. 4. P. 1379–1386. doi: 10.1104/pp.122.4.137927. Golovko T.K., Yatsko Ya.N., Dymova O.V. Seasonal changes in the state of the photosynthetic apparatus of three boreal coniferous species in the middle taiga subzone of the European Northeast // Hvojnye boreal’noj zony. 2013. V. 31. No. 1–2. P. 73–78 (in Russian).28. Dymova O.V., Golovko T.K. Plant pigments: Biological, ecological, and evolutionary aspects (an overview) // Journal of General Biology. 2025. V. 86. No. 5. P. 361–380 (in Russian). doi: 10.31857/S004445962505004729. Latowski D., Dymova O., Maslova T., Strzałka K. The xanthophylls cycle and its physiological functions // Photosynthetic pigments: chemical structure, biological function and ecology / Eds. T.K. Golovko, E.I. Gruszecki, M.N.V. Prasad, K. Strzałka. Syktyvkar: Institute of Biology of Komi Scientific Centre of the Ural Branch of the Russian Academy of Sciences, 2014. P. 183–206 (in Russian).30. Masaitis G., Mozgeris G., Augustaitis A. Spectral reflectance properties of healthy and stressed coniferous trees // iForest. 2013. V. 6. No. 1. P. 30–36. doi: 10.3832/ifor0709-00631. Pakharkova N.V., Gaevsky N.A., Gette I.G. Parameters of Pinus sibirica photosynthetic apparatus for phenotyping trees in the high-altitude zone of the western Sayan // J. Sib. Fed. Univ. Biol. 2024. V. 17. No. 2. P. 119–133 (in Russian).32. Ganthaler A., Bauer H., Gruber A., Mayr M., Oberhuber W., Mayr S. Effects of the needle bladder rust (Chrysomyxa rhododendri) on Norway spruce: implications for subalpine forests // Eur. J. Forest Res. 2014. V. 133. P. 201–211. doi: 10.1007/s10342-013-0770-633. Pakharkova N.V., Kisteeva M.O. Changes in photosynthetic activity of Siberian fir needles upon infection by ophiostomatoid fungi – associates of the four-eyed fir bark beetle // Monitoring sostoyaniya prirodnyh kompleksov i mnogoletnie issledovaniya na osobo ohranyaemyh prirodnyh territoriyah. 2019. No. 3. P. 84–88 (in Russian).34. Perks M.P., Monaghan S., O’Reilly C., Osborne B., Mitchell D.T. Chlorophyll fluorescence characteristics, performance and survival of freshly lifted and cold stored Douglas fir seedlings // Ann. For. Sci. 2001. V. 58. P. 225–235. doi: 10.1051/forest:200112235. Gil-Pelegrín E., Peguero-Pina J.J., Sancho-Knapik D., Arrechea E., Camarero J.J. How warmer and drier conditions drive forest dieback and tree death: A review and conceptual model for silver fir // Plants. 2025. V. 14. Article No. 3308. doi: 10.3390/plants1421330836. Ruban A.V., Johnson M.P., Duffy C.D.P. The photoprotective molecular switch in the photosystem II antenna // Biochim. Biophys. Acta. 2012. V. 1817. No. 1. P. 167–181. doi: 10.1016/j.bbabio.2011.04.00737. Pliūra A., Bajerkevičienė G., Labokas J., Lygis V., Jankauskienė J., Suchockas V., Verbylaitė R. The effects of different combinations of simulated climate change-related stressors on juveniles of seven forest tree species grown as mono-species and mixed cultures // Baltic Forestry. 2020. V. 26. No. 1. Article No. 326. doi: 10.46490/BF32638. Felicijan M., Novak M., Krasevec N., Urbanek Krajnc A. Antioxidant defences of Norway spruce bark against bark beetles and its associated blue-stain fungus // Agricultura. 2015. V. 12. No. 1–2. P. 9–18. doi: 10.1515/agricultura-2016-000239. Netherer S., Kandasamy D., Jirosová A., Kalinová B., Schebeck M., Schlyter F. Interactions among Norway spruce, the bark beetle Ips typographus and its fungal symbionts in times of drought // Journal of Pest Science. 2021. V. 94. P. 591–614. doi: 10.1007/s10340-021-01341-y