Resistance of seedlings of native and alien species of the genus Bidens (Asteraceae) from different geographic populations to the action of heavy metals

Keywords: heavy metals; Bidens frondosa; Bidens tripartita; morphometric indicators; tolerance index


One approach to assessing the competitiveness of invasive species is a comparative analysis of the morphological, physiological, and reproductive traits of this species with native species of the same genus. The invasive species Bidens frondosa L. from the Asteraceae family, included in the list of the 50 most common and most aggressive invasive species in Europe, occupies the same ecological niche as the native species B. tripartita L., and displaces it from natural habitats. There is an obvious and growing interest in the sustainability of B. tripartita and B. frondosa in extreme conditions of existence, one of which is the action of heavy metals. Our research was performed in laboratory conditions with seedlings that developed from seeds collected from populations of the Upper and Middle Volga region. The seeds were germinated in Ni2+ and Cu2+ solutions at various concentrations. At the end of the experiment, morphometric parameters were measured and the index of tolerance was determined. Seedlings from different populations under the influence of nickel ions developed at concentrations of 1–50 mg/l, under the influence of copper ions – at 1–100 mg/l. The nickel and copper ions had the greatest toxic effect on the growth and development of the root system – at 25 mg/l and above, the main root was completely necrotic, while the action of copper ions simultaneously increased the number of adventitious roots. The tolerance index (“root test”) under the action of nickel ions was higher among the seedlings from the population of the Middle Volga region, while under the action of copper ions there were no significant differences among the seedlings from different populations. However, it decreased with the action of both heavy metals at a concentration of 10 mg/l. High concentrations of both metals significantly reduced the length of the hypocotyl, cotyledon, and the true leaf. It was also found that copper ions are more toxic for the root system (main root and adventitious roots), nickel ions – for above-ground organs (hypocotyl, cotyledons, and true leaves). We noted differences between the populations to the action of nickel and copper. From the population of the Upper Volga region, the seedlings of B. frondosa were more stable. For seedlings from the population of the Middle Volga, a smaller toxic effect was confirmed for B. tripartita. It can be assumed that the resistance of B. frondosa to the action of heavy metals as a stress factor in the Upper Volga region is one of the reasons for the suppression of B. tripartita by the invasive species.


Abramova, L. M., & Nurmieva, S. V. (2013). K biologii invazionnogo vida Bidens frondosa L. v Predural'e respubliki Bashkortostan [Biology of invasive species Bidens frondosa L. in the Urals of the Republic of Bashkortostan]. Proceedings of the Samara Scientific Center of the Russian Academy of Sciences, 15(3), 358–360 (in Russian).

Borisova, E. A. (2010). Osobennosti rasprostraneniya invazionnykh vidov rastenij po territorii Verkhnevolzhskogo regiona [Peculiarities of distribution invasive plant species on the territory of the upper Volga region]. Russian Journal of Biological Invasions, 4, 2–9 (in Russian).

Brandel, M. (2004). Dormancy and germination of heteromorphic achenes of Bidens frondosa. Flora, 199, 228–233.

Chen, C., Huang, D., & Liu, J. (2009). Functions and toxicity of nickel in plants: Recent advances and future prospects. Review: Clean, 37 (4–5), 304–313.

Chukina, N. V., & Borisova, G. G. (2010). Structural and functional parameters of higher aquatic plants from habitats differing in levels of anthropogenic impact. Inland Water Biology, 3(1), 44–50.

Chytry, M., Maskell, L. C., Pino, J., Pyšek, P., Vila, M., Font, X., & Smart, S. M. (2008). Habitat invasions by alien plants: A quantitative comparison among Mediterranean, subcontinental and oceanic regions of Europe. Journal of Applied Ecology, 45, 448–458.

Galkina, M. A., Vinogradova, Y. K., & Cancer, I. A. (2015). Biomorfologicheskie osobennosti i mikroehvolyutsiya invazionnykh vidov roda Bidens L. [Biomorphological peculiarities of microevolution of invasive species of Bidens L.]. Bulletin of the Russian Academy of Sciences Biological Series, 4, 382 (in Russian).

Hovick, S. M., Peterson, C. J., & Carson, W. P. (2012). Predicting invasiveness and range size in wetland plants using biological traits: A multivariate experimental approach. Journal of Ecology, 100, 1373–1382.

Ivanov, V. B., Bystrova, E. I., & Seregin, I. V. (2003). Comparative impacts of heavy metals on root growth as related to their specificity and selectivity. Russian Journal of Plant Physiology, 50(3), 398–406.

Ivanova, E. M., Kholodova, V. P., & Kuznetsov, V. V. (2010). Biological effects of high copper and zinc concentrations and their interaction in rapeseed plants. Russian Journal of Plant Physiology, 57(6), 806–814.

Khapugin, A. A., Vargot, E. V., & Gladunova, N. V. (2016). Bidens frondosa L. (Asteraceae) in the republic of Mordovia (Russia). Russian Journal of Biological Invasions, 7(2), 129–136.

Kostrakiewicz-Gierałt, K., & Zając, M. (2014). The influence of habitat conditions on the performance of two invasive, annuals – Impatiens glandulifera and Bidens frondosa. Biologia, 69(4), 449–462.

Kovalchuk, I. A., & Tokhtar, V. K. (2013). K khronologii rasprostraneniya invazionnykh vidov roda Bidens L. (Asteraceae) v Vostochnoj Evrope [On the chronology of the spread of invasive species of the genus Bidens L. (Asteraceae) in Eastern Europe]. Fundamental Research, 113, 1361–1363 (in Russian).

Krylova, E. G. (2011). The effect that nickel, copper, and zinc salts have on seed germination and initial ontogenesis of water parsnip (Sium latifolium L.) and wood clubrush (Scirpus silvaticus L.). Inland Water Biology, 4(4), 468–474.

Krylova, E. G., & Vasilyeva, N. V. (2011a). Prorastanie semyan i razvitie prorostkov predstavitelej roda Bidens (Asteraceae) v rastvorakh sul'fata medi [Germination of seeds and development of seedlings of representatives of the genus Bidens (Asteraceae) in copper sulfate solutions]. Bulletin of the Tomsk State University, 352, 207–210 (in Russian).

Krylova, E. G., & Vasilyeva, N. V. (2011b). Dejstvie sul'fata nikelya na nachal'nye ehtapy ontogeneza rastenij trekh vidov roda Bidens (Asteraceae) [The effect of nickel sulphate on the initial stages of ontogeny of plants of three species of the genus Bidens (Asteraceae)]. Plant Resources, 47(1), 65–71 (in Russian).

Lapirov, A. G., Sigareva, L. E., Krylova, E. G., & Timofeeva, N. A. (2017). Effect of nickel chloride on seed germination and mor-phophysiological parameters of seedlings of Alisma plantago-aquatica L. and Sium latifolium L. Inland Water Biology, 10(3), 308–314.

Makarova, Y. V. (2009). Izmenchivost' morfometricheskikh pokazatelej fasoli obyknovennoj pri kratkosrochnom vozdejstvii kadmiya, tsinka i medi [Variability of morphometric parameters of kidney beans with short-term effects of cadmium, zinc and copper]. Bulletin of SamSU Natural Science Series, 72(6), 159–169 (in Russian).

Maksymiec, W. (2007). Signaling responses in plants to heavy metal stress. Acta Physiologiae Plantarum, 29, 177–187.

Molas, J. (1997). Changes in morphological and anatomical structure of cabbage (Brassica oleraceae L.) outer leaves and in ultrastructure of their chloroplasts caused by in vitro excess of nickel. Photosyntetica, 34, 513–522.

Moya, J. L., Ros, R., & Picazo, I. (1993). Influence of cadmium and nickel on growth, Net photosynthesis and carbohydrate distribution in rice plants. Photosynthesis Research, 36, 75–80.

Obrucheva, N. V., Bystrovaet, E. I., Ivanova, V. B., Antipova, O. V., & Seregin, I. V. (1998). Root growth responses to lead in young maize seedlings. Plant and Soil, 200(1), 55–61.

Pyšek, P., Jarošik, V., Hulme, P. E., Pergl, J., Hejda, M., Schaffner, U., & Vila, M. (2012). A global assessment of invasive plant impacts on resident species, communities and ecosystems: The interaction of impact measures, invading species' traits and environment. Global Change Biology, 18, 1725–1737.

Pyšek, P., Richardson, D. M., Pergl, J., Jarošík, V., Sixtová, Z., & Weber, E. (2008). Geographical and taxonomic biases in invasion ecology. Trends in Ecology and Evolution, 23, 237–244.

Rozentsvet, O. A., Nesterov, V. N., & Sinyutina, N. F. (2011). Ekologo-fiziologicheskie i biokhimicheskie aspekty vliyaniya ionov tyazhelykh metallov na vodnoe rastenie Hydrilla verticillata [Ecological, physiological and biochemical aspects of the influence of heavy metal ions on an aquatic plant Hydrilla verticillata]. Povolzhsky Ecological Journal, 2, 185–192 (in Russian).

Samantarey, S., Rout, G. R., & Das, P. (1997). Tolerance of rice to nickel in nutrient solution. Biologia Plantarum., 40, 295–298.

Seregin, I. V., & Kozhevnikova, A. D. (2006). Physiological role of nickel and its toxic effects on higher plants. Russian Journal of Plant Physiology, 53(2), 257–277.

Sharma, S. S., & Dietz, K. J. (2009). The relationship between metal toxicity and cellular redox imbalance. Trends in Plant Science, 14, 43–50.

Timofeeva, N. A., Sigareva, L. E., Krylova, E. G., & Lapirov, A. G. (2016). Influence of copper and nickel on morphophysiological indicators of seedlings of coastal aquatic plants. Biology Bulletin, 43(3), 244–251.

Titov, A. F., Kaznina, N. M., & Talanova, V. V. (2014). Tyazhelye metally i rasteniya [Heavy metals and plants]. Karelian Scientific Center of the Russian Academy of Sciences, Petrozavodsk (in Russian).

Van Kleunen, M., Dawson, W., Essl, F., Pergl, J., Winter, M., Weber, E., Kreft, H., Weigelt, P., Kartesz, J., Nishino, M., Antonova, L. A., Barcelona, J. F., Cabezas, F. J., Cárdenas, D., Cárdenas-Toro, J., Castaño, N., Chacón, E., Chatelain, C., Ebel, A. L., Figueiredo, E., Fuentes, N., Groom, Q. J., Henderson, L., Inderjit Kupriyanov, A., Masciadri, S., Meerman, J., Morozova, O., Moser, D., Nickrent, D. L., Patzelt, A., Pelser, P. B., Baptiste, M. P., Poopath, M., Schulze, M., Seebens, H., Shu, W., Thomas, J., Velayos, M., Wieringa, J. J., & Pyšek, P. (2015). Global exchange and accumulation of non-native plants. Nature, 525, 100–103.

Vasilyeva, N. V., & Papchenkov, V. G. (2011). Mekhanizmy vozdejstviya invazionnoj B. frondosa na aborigennye vidy cheredy [Mechanisms of influence of invasive B. frondosa on native types of succession]. Russian Journal of Biological Invasions, 1, 15–22 (in Russian).

Vinogradova, Y. K., Galkina, M. A., & Mayorov, S. R. (2014). Variability of the taxa of the Bidens L. genera and the problem of hybridization. Russian Journal of Biological Invasions, 5(1), 1–11.

Vinogradova, Y. K., Mayorov, S. R., & Khorun, L. V. (2010). Chernaya kniga flory Srednei Rossii: Chuzherodnye vidy rastenii v ekosistemakh Srednei Rossii [The Black Book of Flora of Central Russia: Alien plant species in ecosystems of Central Russia]. Geos, Moscow (in Russian).

Wilkins, D. A. (1978). The measurement of tolerance to edaphic factors by means of root growth. New Phytologist, 80, 623–633.

Yan, X. H. (2016). Reproductive biological characteristics potentially contributed to invasiveness in an alien invasive plant Bidens frondosa. Plant Species Biology, 31(2), 107–116.

Yruela, I. (2005). Copper in plants. Brazilian Journal of Plant Physiology, 17(1), 145–156.

Yruela, I. (2009). Copper in plants: Acquisition, transport and interactions. Functional Plant Biology, 36, 409–430.

Yusuf, M., Fariduddin, Q., Hayat, S., & Ahmad, A. (2011). Nickel: An overview of uptake, essentiality and toxicity in plants. Bulletin of Environmental Contamination and Toxicology, 86(1), 1–17.


Most read articles by the same author(s)

Obs.: This plugin requires at least one statistics/report plugin to be enabled. If your statistics plugins provide more than one metric then please also select a main metric on the admin's site settings page and/or on the journal manager's settings pages.