Impact of invasive species Parectopa robiniella (Gracillariidae) on fluorescence parameters of Robinia pseudoacacia in the conditions of the steppe zone of Ukraine
AbstractRobinia pseudoacacia L. is one of the most common and environmentally adaptable introduced tree species which has become an important element of artificial afforestation and landscaping in Ukraine over the past 150 years. Throughout the history of its introduction on the territory of Ukraine, this species was considered resistant because of the absence of dangerous phytophages. At the beginning of the XXI century, the phytosanitary situation changed as the result of the penetration and rapid spread of a number of North American invasive phytophages. The appearance and distribution of the miner Parectopa robiniella (Clemens, 1863) (Lepidoptera, Gracillariidae) feeding on R. pseudoacacia was recognized as the largest invasion in Ukraine. This paper considers the issues of studying the effect of P. robiniella caterpillars feeding on R. pseudoacacia in various forest-growing conditions in the steppe zone of Ukraine. The process of photosynthesis, as the most important physiological parameter, was chosen as indicator of condition. The study was conducted using biosensor technology which made it possible to measure the effect of caterpillar feeding on critical parameters of chlorophyll fluorescence (the Kautsky curve). The research has shown that the initial value of fluorescence induction was within the range of 196–284 RFU, and the maximum value of the background fluorescence parameter was recorded in undamaged leaves and under shading conditions. Both the effect of phytophages and the shading factor caused a significant decrease in the values of fluorescence induction of the “plateau” both in the conditions of an artificially washed sandbar, on the watershed area of a watershed-gully landscape, as well as on natural sandy-loam soil. The maximum values of photosynthetic fluorescence induction under the simultaneous influence of the studied factors had rather high variability. In contrast to the fluorescence induction parameter, the “plateau” of the highest maximum fluorescence induction was reached in the absence of pest damage under conditions of total shading. As revealed by dispersion and regression analyses, the maximum fluorescence index was most dependent on the amount of solar radiation and on the degree of the leaf surface damage by phytophages. Significantly higher values of the steady-state fluorescence induction parameter were determined in the absence of insect damage in both shading and lighting conditions. A statistically significant combined influence of abiotic and biotic factors on the “plateau” fluorescence induction parameter was determined in comparison with the mono-influence of individual factors. A highly significant dependence of the maximum efficiency indicator of primary photosynthesis processes on individual factors of exogenous influence was established, while the combined effect of these factors did not affect this parameter. The obtained data allow one to apply in practice the methods of analyzing chlorophyll fluorescence induction to establish the physiological state of tree flora in forest and garden farms.
Baranovski, B., Roschina, N., Karmyzova, L., & Ivanko, I. (2018). Comparison of commonly used ecological scales with the Belgard plant ecomorph system. Biosystems Diversity, 26(4), 286–291.
Brygadyrenko, V. V. (2015). Influence of moisture conditions and mineralization of soil solution on structure of litter macrofauna of the deciduous forests of Ukraine steppe zone. Visnyk of Dnipropetrovsk University, Biology, Ecology, 23(1), 50–65.
Brygadyrenko, V. V., & Nazimov, S. S. (2015). Trophic relations of Opatrum sabulosum (Coleoptera, Tenebrionidae) with leaves of cultivated and uncultivated species of herbaceous plants under laboratory conditions. Zookeys, 481, 57–68.
Bucher, S. F., Bernhardt-Römermann, M., & Römermann, C. (2018). Chlorophyll fluorescence and gas exchange measurements in field research: An ecological case study. Photosynthetica, 56, 1161–1170.
Burda, R. I., & Koniakin, S. N. (2019). The non-native woody species of the flora of Ukraine: Introduction, naturalization and invasion. Biosystems Diversity, 27(3), 276–290.
Bussotti, F., Gerosa, G., Digrado, A., & Pollastrini, M. (2020). Selection of chlorophyll fluorescence parameters as indicators of photosynthetic efficiency in large scale plant ecological studies. Ecological Indicators, 108, 105686.
Cardenas, A., & Gallardo, P. (2016). Relationship between insect damage and chlorophyll content in Mediterranean oak species. Applied Ecology and Environmental Research, 14, 477–491.
Carl, C., Lehmann, J. R. K., Landgraf, D., & Pretzsch, H. (2019). Robinia pseudoacacia L. in short rotation coppice: Seed and stump shoot reproduction as well as UAS-based spreading analysis. Forests, 10, 235.
Cendrero-Mateo, M. P., Carmo-Silva, A. E., Porcar-Castell, A., Hamerlynck, E. P., Papuga, S. A., & Moran, M. S. (2015). Dynamic response of plant chlorophyll fluorescence to light, water, and nutrient availability. Functional Plant Biology, 42(8), 746–757.
Cetner, M. D., Kalaji, H. M., Borucki, W., & Kowalczyk, K. (2020). Phosphorus deficiency affects the I-step of chlorophyll a fluorescence induction curve of radish. Photosynthetica, 58, 671–681.
Chaplygina, A. B., Savynska, N. O., & Brygadyrenko, V. V. (2018). Trophic links of the spotted flycatcher, Muscicapa striata, in transformed forest ecosystems of North-Eastern Ukraine. Baltic Forestry, 24(2), 304–312.
Cierjacks, A., Kowarik, I., Joshi, J., Hempel, S., Ristow, M., Lippe, M., Weber, E. (2013). Biological flora of the British Isles: Robinia pseudoacacia. Journal of Ecology, 101, 1623–1640.
Duysens, L. N. M. (1961). Cytochrome oxidation by a second photochemical system in the red alga Porphyridum cruentum. In: Christensen, B. C., & Buchmann, B. (Eds.). Progress in photobiology. Elsevier, Amsterdam. Pp. 135–142.
Faly, L. I., Kolombar, T. M., Prokopenko, E. V., Pakhomov, O. Y., & Brygadyrenko, V. V. (2017). Structure of litter macrofauna communities in poplar plantations in an urban ecosystem in Ukraine. Biosystems Diversity, 25(1), 29–38.
Flexas, J., Bota, J., Escalona, J. M., Sampol, B., & Medrano, H. (2002). Effects of drought on photosynthesis in grapevines under field conditions: An evaluation of stomatal and mesophyll limitations. Functional Plant Biology, 29, 461–471.
Giorio, P., & Sellami, M. H. (2021). Polyphasic OKJIP chlorophyll a fluorescence transient in a landrace and a commercial cultivar of sweet pepper (Capsicum annuum L.) under long-term salt stress. Plants, 10, 887.
Gritsan, Y., Sytnyk, S., Lovynska, V., & Tkalich, Y. (2019). Climatogenic reaction of Robinia pseudoacacia L. and Pinus sylvestris L. within Northern Steppe of Ukraine. Biosystems Diversity, 27(1), 16–20.
Guidi, L., Lo Piccolo, E., & Landi, M. (2019). Chlorophyll fluorescence, photoinhibition and abiotic stress: Does it make any difference the fact to be a C3 or C4 species? Frontiers in Plant Science, 10, 174.
Guimarães, Z., Santos, V., & Ferreira, M. (2022). Chlorophyll a fluorescence parameters are related to the leaf economics spectrum of tropical tree species in a mixed plantation. Trees, 36, 763–775.
Guo, X., Ren, X., & Eller, F. (2018). Higher phenotypic plasticity does not confer higher salt resistance to Robinia pseudoacacia than Amorpha fruticosa. Acta Physiology Plant, 4, 40–79.
Hallik, L., Niinemets, U., & Kull, O. (2012). Photosynthetic acclimation to light in woody and herbaceous species: A comparison of leaf structure, pigment content and chlorophyll fluorescence characteristics measured in the field. Plant Biology, 14, 88–99.
Hari, P., & Luukkanen, O. (2006). Field studies of photosynthesis as affected by water stress, temperature, and light in birch. Physiologia Plantarum, 32, 97–102.
He, L., Yu, L., Li, B., Du, N., & Guo, S. (2018). The effect of exogenous calcium on cucumber fruit quality, photosynthesis, chlorophyll fluorescence, and fast chlorophyll fluorescence during the fruiting period under hypoxic stress. BMC Plant Biology, 181, 1–10.
Holoborodko, K. K., Rusynov, V. I., Loza, I. M., & Pakhomov, O. Y. (2021). Adaptive features of the Phyllonorcyter robiniella (Clemens, 1859) (Gracillariidae Stainton, 1854) population in urban ecosystems. Ukrainian Journal of Ecology, 11(2), 27–34.
Holoborodko, K., Seliutina, O., Alexeyeva, A., Brygadyrenko, V., Ivanko, I., Shulman, M., Pakhomov, O., Loza, I., Sytnyk, S., Lovynska, V., Grytsan, Y., & Bandura, L. (2022). The impact of Cameraria ohridella (Lepidoptera, Gracillariidae) on the state of Aesculus hippocastanum photosynthetic apparatus in the urban environment. International Journal of Plant Biology, 13, 223–234.
Huang, W., Yang, Y. J., & Zhang, S. B. (2017). Specific roles of cyclic electron flow around photosystem I in photosynthetic regulation in immature and mature leaves. Journal of Plant Physiology, 209, 76–83.
Kautsky, H., & Hirsch, A. (1931). Neue Versuche zur Kohlensäureassimilation. Naturwissenschaften, 19, 964.
Kebbas, S., Lutts, S., & Aid, F. (2015). Effect of drought stress on the photosynthesis of Acacia tortilis subsp. raddiana at the young seedling stage. Photosynthetica, 53, 288–298.
Khan, N., Essemine, J., Hamdani, S., Qu, M., Lyu, M.-J. A., Perveen, S., Stirbet, A., Govindjee, G., & Zhu, X.-G. (2021). Natural variation in the fast phase of chlorophyll a fluorescence induction curve (OJIP) in a global rice minicore panel. Photosynthesis Research, 150, 137–158.
Kirichenko, N., Augustin, S., & Kenis, M. (2019). Invasive leafminers on woody plants: A global review of pathways, impact, and management. Journal of Pest Science, 92, 93–106.
Klisz, M., Puchałka, R., Netsvetov, M., Prokopuk, Y., Vítková, M., Sádlo, J., Matisons, M., Mionskowski, M., Chakraborty, D., Olszewski, P., Wojda, T., & Koprowski, M. (2021). Variability in climate-growth reaction of Robinia pseudoacacia in Eastern Europe indicates potential for acclimatisation to future climate. Forest Ecology and Management, 492, 119194.
Kostenko, S. М., Kytayev, O. І., & Kovalevskiy, S. В. (2004). Induktsiya fluorestsentsiyi hlorofilu listkiv predstavnikiv rodu Philadelphus v umovah mista Kieva [Induction of chlorophyll fluorescence of the genus Philadelphus L. leaves in Kyiv]. Scientific Bulletin of UNFU, 24(2), 209–213 (in Ukrainian).
Lichtenthaler, H. K., & Babani, F. (2022). Contents of photosynthetic pigments and ratios of chlorophyll a/b and chlorophylls to carotenoids (a+b)/(x+c) in C4 plants as compared to C3 plants. Photosynthetica, 60, 1–7.
Longoni, F. P., & Goldschmidt-Clermont, M. (2021). Thylakoid protein phosphorylation in chloroplasts. Plant and Cell Physiology, 62(7), 1094–1107.
Montecchiari, S., Tesei, G., & Allegrezza, M. (2020). Effects of Robinia pseudoacacia coverage on diversity and environmental conditions of Central-Northern Italian Quercus pubescents sub-Mediterranean forests (Habitat code 91AA*). Threshold Assessment, 10, 33–54.
Nentwig, W., Bacher, S., Kumschick, S., Pysek, P., & Vila, M. (2018). More than ‘‘100 worst’’ alien species in Europe. Biological Invasions, 20, 1611–1621.
Nicolescu, V., Rédei, K., & Mason, W. L. (2020). Ecology, growth and management of black locust (Robinia pseudoacacia L.), a non-native species integrated into European forests. Journal of Forest Resources, 31(4), 1081–1101.
Ouzounidou, G. (1993). Changes in variable chlorophyll fluorescence as a result of Cu-treatment dose response relations in Silene and Thlaspi. Photosynthetica, 29, 455–462.
Pashayeva, A., Wu, G., Huseynova, I., Lee, C. H., & Zulfugarov, I. S. (2021). Role of thylakoid protein phosphorylation in energy-dependent quenching of chlorophyll fluorescence in rice plants. International Journal of Molecular Sciences, 22(15), 7978.
Petrova, N., Stoichev, S., Paunov, M., Todinova, S. Taneva, S. G., & Krumova, S. (2019). Structural organization, thermal stability, and excitation energy utilization of pea thylakoid membranes adapted to low light conditions. Acta Physiology Plant, 41, 188.
Puchałka, R., Dyderski, M. K, Vítková, M., Sádlo, J., Klisz, M., Netsvetov, M., Prokopuk, Y., Matisons, R., Mionskowski, M., Wojda, T., Koprowski, M., & Jagodziński, A. M. (2021). Black locust (Robinia pseudoacacia L.) range contraction and expansion in Europe under changing climate. Global Change Biology, 27(8), 1587–1600.
Rumlerová, Z., Vilà, M., Pergl, J., Nentwig, W., & Pyšek, P. (2016). Scoring environmental and socioeconomic impacts of alien plants invasive in Europe. Biological Invasion, 18(12), 3697–3711.
Sáez, P. L., Rivera, B. K., Ramírez, C. F., Vallejos, V., & Bravo, L. A. (2018). Effects of temperature and water availability on light energy utilization in photosynthetic processes of Deschampsia antarctica. Physiologia Plantarum, 165, 511–523.
Shupranova, L. V., Holoborodko, K. K., Seliutina, O. V., & Pakhomov, O. Y. (2019). The influence of Cameraria ohridella (Lepidoptera, Gracillariidae) on the activity of the enzymatic antioxidant system of protection of the assimilating organs of Aesculus hippocastanum in an urbogenic environment. Biosystems Diversity, 27(3), 238–243.
Shvydenko, I. M., Stankevych, S. V., Goroshko, V. V., Bulat, A. G., Cherkis, T. M., Zabrodina, I. V., Lezhenina, I. P., & Baidyk, H. V. (2021). Adventitious leaf miner Parectopa robiniella Clemens, 1863 and Phyllonorycter robiniella Clemens, 1859 on a black locust tree in the Kharkiv Region. Ukrainian Journal of Ecology, 11(7), 22–32.
Šibíková, M., Jarolímek, I., & Hegedüšová, K. (2019). Effect of planting alien Robinia pseudoacacia trees on homogenization of Central European forest vegetation. Science of the Total Environment, 687, 1164–1175.
Sitzia, T., Campagnaro, T., Kotze, D. J., Nardi, S., & Ertani, A. (2018). The invasion of abandoned fields by a major alien tree filters understory plant traits in novel forest ecosystems. Scientific Report, 8(1), 8410.
Sitzia, T., Cierjacks, A., de Rigo, D., & Caudullo, G. (2016). Robinia pseudoacacia in Europe: Distribution, habitat, usage and threats. In: San-Miguel-Ayanz, J., de Rigo, D., Caudullo, G., Houston Durrant, T., Mauri, A. (Eds.). European atlas of forest tree species. Luxembourg. Pp. e014e79+.
Stirbet, A., & Govindjee, G. (2011). On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: Basics and applications of the OJIP fluorescence transient. Journal of Photochemistry and Photobiology B: Biology, 11, 78–92.
Stirbet, A., Lazár, D., Kromdijk, J., & Govindjee, G. (2018). Chlorophyll a fluorescence induction: Can just a one-second measurement be used to quantify abiotic stress responses? Photosynthetica, 56, 86–104.
Strasser, R. J., Tsimilli-Michael, M., & Srivastava, A. (2004). Analysis of the chlorophyll fluorescence transient. A Signature of Photosynthesis, Advances in Photosynthesis and Respiration, 9, 321–362.
Svyrydchenko, A. O., & Brygadyrenko, V. V. (2014). Trophic preferences of Rossiulus kessleri (Diplopoda, Julidae) for the litter of various tree species. Folia Oecologica, 41(2), 202–212.
Tsai, Y. C., Chen, K. C., Cheng, T. S., Lee, C., Lin, S. H., & Tung, C. W. (2019). Chlorophyll fluorescence analysis in diverse rice varieties reveals the positive correlation between the seedlings salt tolerance and photosynthetic efficiency. BMC Plant Biology, 19, 403.
Van Rensburg, L., & Kruger, G. H. J. (1993). Differential inhibition of photosynthesis (in vivo and in vitro) and changes in chlorophyll a fluorescence induction kinetics of four tobacco cultivars under drought stress. Journal of Plant Physiology, 141, 357–365.
Vítková, M., Müllerová, J., Sádlo, J., Pergl, J., & Pyšek, P. (2017). Black locust (Robinia pseudoacacia) beloved and despised: A story of an invasive tree in Central Europe. Forest Ecology and Management, 384, 287–302.
Vítková, M., Sádlo, J., & Roleček, J. (2020). Robinia pseudoacacia – dominated vegetation types of Southern Europe: Species composition, history, distribution and management. Science of the Total Environment, 707, 134857.
Wagner, V., Chytrý, M., Jiménez-Alfaro, B., Pergl, J., Hennekens, S., Biurrun, I., & Pyšek, P. (2017). Alien plant invasions in European woodlands. Diversity and Distributions, 23(9), 969–981.
Wilkaniec, A., Borowiak-Sobkowiak, B., Irzykowska, L., Breś, W., Świerk, D., Pardela, L., Durak, R., Środulska-Wielgus, J., & Wielgus, K. (2021). Biotic and abiotic factors causing the collapse of Robinia pseudoacacia L. veteran trees in urban environments. PLoS One, 16(1), e0245398.
Zhang, P., Zhang, Z., Li, B., Zhang, H., Hu, J., & Zhao, J. (2020). Photosynthetic rate prediction model of newborn leaves verified by core fluorescence parameters. Scientific Reports, 10, 3013.
Zhou, W. L., Liu W. K., & Yang, Q. C. (2012). Quality changes in hydroponic lettuce grown under pre-harvest short-duration continuous light of different intensities. Journal of Horticultural Science and Biotechnology, 87, 429–434.
Zverkovskyi, V., Sytnyk, S., Lovynska, V., Kharytonov, M., Lakyda, I., Mykolenko, S., Pardini, G., Margui, E., & Gispert, M. (2018). Remediation potential of forest forming tree species within northern steppe reclamation stands. Ekológia (Bratislava), 37(1), 69–81.
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons «Attribution» 4.0 License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.