Palabras clave
control biológico
macrófitas acuáticas
plantas terrestres
actividad alelopática
Cómo citar
Resumen
Los florecimientos de cianobacterias tóxicas son una amenaza para la salud de los ecosistemas acuáticos y de los seres humanos en todo el mundo. En el presente trabajo, mediante un análisis documental, se cuantificó el número de las plantas acuáticas y terrestres reportadas para control de estos florecimientos y las metodologías que se utilizan para determinar la actividad alelopática, con el objetivo de proporcionar a los investigadores un panorama general de los avances realizados en la última década. Se identificaron 74 especies de plantas, 44 macrófitas acuáticas y 30 terrestres. Según la CE50, los compuestos puros son más eficientes que los extractos crudos, con la desventaja de ser más costosos. Finalmente, se determinó que existen 4 técnicas para analizar la actividad alelopática de las plantas sobre las cianobacterias, siendo la experimentación en mesocosmos y en coexistencia las que más se aproximan a las condiciones naturales de un cuerpo de agua.
Citas
Bullerjahn, G. S., McKay, R. M., Davis, T. W., Baker, D. B., Boyer, G. L., D’Anglada, L. V., Doucette, G. J., Ho, J. C., Irwin, E. G., Kling, C. L., Kudela, R. M., Kurmayer, R., Michalak, A. M., Ortiz, J. D., Otten, T. G., Paerl, H. W., Qin, B., Sohngen, B. L., Stumpf, R. P., Visser, P. M., & Wilhelm, S. W. (2016). Global solutions to regional problems: Collecting global expertise to address the problem of harmful cyanobacterial blooms. A Lake Erie case study. Harmful Algae, 54, 223–238. https://doi.org/10.1016/j.hal.2016.01.003.
Cantoral, U., Asencio, M., & Aboal, S. M. 2017. Cianotoxinas: efectos ambientales y sanitarios. Medidas de prevención. Hidrobiológica, 27(2), 241-251. https://doi.org/10.24275/uam/izt/dcbi/hidro/2017v27n2/Cantoral.
Carmichael, W. W., & Boyer, G. L. (2016). Health impacts from cyanobacteria harmful algae blooms: Implications for the North American Great Lakes. Harmful Algae, 54, 194–212. https://doi.org/10.1016/j.hal.2016.02.002.
Cha, Y., Park, S. S., Kim, K., Byeon, M., & Stow, C. A. (2014). Probabilistic prediction of cyanobacteria abundance in a Korean reservoir using a Bayesian Poisson model. Water Resources Research, 50(3), 2518–2532. https://doi.org/10.1002/2013WR014372.
Chang, X., Eigemann, F., & Hilt, S. (2012). Do macrophytes support harmful cyanobacteria? Interactions with a green alga reverse the inhibiting effects of macrophyte allelochemicals on Microcystis aeruginosa. Harmful Algae, 19, 76–84. https://doi.org/10.1016/j.hal.2012.06.002.
Chen, J., Zhang, H., Han, Z., Ye, J., & Liu, Z. (2012). The influence of aquatic macrophytes on Microcystis aeruginosa growth. Ecological Engineering, 42, 130–133. https://doi.org/10.1016/j.ecoleng.2012.02.021.
Chen, S., Zheng, T., Ye, C., Huannixi, W., Yakefu, Z., Meng, Y., Peng, X., Tian, Z., Wang, J., Ma, Y., Yang, Y., Ma, Z., & Zuo, Z. (2018). Algicidal properties of extracts from Cinnamomum camphora fresh leaves and their main compounds. Ecotoxicology and Environmental Safety, 163, 594–603. https://doi.org/10.1016/j.ecoenv.2018.07.115.
Cheng, L., Cao, X., & Yu, X. (2017). Mechanism of growth inhibition effect of aquatic plants on water cyanobacteria. Insight: Biology, 1, 1–9.
Chicalote, C. D., Ramírez, G. P., & Macías, R. M. L. (2017). Allelopathic effects among selected species of phytoplankton and macrophytes. Journal of Environmental Biology, 38(Special issue), 1221-1227. DOI: 10.22438/jeb/38/6(SI)/07.
Cobo, F. (2015). Métodos de control de las floraciones de cianobacterias en aguas continentales. Limnetica, 34(1), 247-268. DOI: 10.23818/limn.34.20.
Ghobrial, M. G., Nassr, H. S., & Kamil, A. W. (2015). Bioactivity effect of two macrophyte extracts on growth performance of two bloom-forming cyanophytes. The Egyptian Journal of Aquatic Research, 41(1), 69-81. https://doi.org/10.1016/j.ejar.2015.01.001.
Grattan, L. M., Holobaugh, S. J. & Morris, G. Jr. (2016). Harmful algal blooms and public health. Harmful Algae, 57(Part B), 2-8. DOI: 10.1016/j.hal.2016.05.003.
He, Y., Hong, Z. Q., Yun, L. B., Cheng, L., Yun T. L., Yuan, Z. Y., & Bin, W. Z. (2016). Programmed cell death in the cyanobacterium Microcystis aeruginosa induced by allelopathic effect of submerged macrophyte Myriophyllum spicatum in co-culture system. Journal of Applied Phycology, 28(5), 2805–2814. https://doi.org/10.1016/j.hal.2016.05.003.
Hong, Y., Hu, H. Y., Sakoda, A., & Sagehashi, M. (2010). Isolation and characterization of antialgal allelochemicals from Arundo donax L. Allelopathy Journal 25(2), 357-368. http://www.allelopathyjournal.org/archives/?Year=2010&Vol=25&Issue=2&Month=4.
Huisman, J., Codd, G. A., Paerl, H. W., Ibelings, B. W., Verspagen, J. M. H., & Visser, P. M. (2018). Cyanobacterial blooms. Nature Reviews Microbiology, 16, 471–483. https://doi.org/10.1038/s41579-018-0040-1.
Jančula, D., Gregorová, J., & Maršálek, B. (2010). Algicidal and cyanocidal effects of selected isoquinoline alkaloids. Aquaculture Research, 41, 598-601. https://doi.org/10.1111/j.1365-2109.2009.02342.x.
Kaminski, A., Chrapusta, E., Bober, B., Adamski, M., Latkowska, E., & Bialczyk, J. (2015). Aquatic macrophyte Lemna trisulca (L.) as a natural factor for reducing anatoxin-a concentration in the aquatic environment and biomass of cyanobacterium Anabaena flos-aquae (Lyngb.) de Bréb. Algal Research, 9, 212–217. https://doi.org/10.1016/j.algal.2015.03.014.
Le Rouzic, B., Thiébaut, G., & Brient, L. (2016). Selective growth inhibition of cyanobacteria species (Planktothrix agardhii) by a riparian tree leaf extract. Ecological Engineering, 97, 74–78. https://doi.org/10.1016/j.ecoleng.2016.07.021.
Li, F. M., & Hu, H. Y. (2005). Isolation and characterization of a novel antialgal allelochemical from Phragmites communis. Applied and Environmental Microbiology, 71(11), 6545–6553. https://doi.org/10.1128/AEM.71.11.6545–6553.2005.
Li, J., Liu, Y., Zhang, P., Zeng, G., Cai, X., Liu, S., Yin, Y., Hu, X., Hu, X., & Tan, X. (2016). Growth inhibition and oxidative damage of Microcystis aeruginosa induced by crude extract of Sagittaria trifolia tubers. Journal of Environmental Sciences, 43, 40-47. https://doi.org/10.1016/j.jes.2015.08.020.
Lu, Y., Wang, J., Yu, Y., Su, W., & Kong, F. (2013). Inhibition of Camellia sinensis (L.) O. Kuntze on Microcystis aeruginosa and isolation of the inhibition factors. Biotechnology Letters, 35(7), 1029-1034. https://doi.org/10.1007/s10529-013-1188-4.
Lu, Z., Sha, J., Tian, Y., Zhang, X., Liu, B., & Wu, Z. (2017). Polyphenolic allelochemical pyrogallic acid induces caspase-3(like)-dependent programmed cell death in the cyanobacterium Microcystis aeruginosa. Algal Research, 21, 148-155. https://doi.org/10.1016/j.algal.2016.11.007.
Lürling, M., & Beekman, W. (2010). Anti-cyanobacterial activity of Moringa oleifera seeds. Journal of Applied Phycology, 22(4), 503-510. https://doi.org/10.1007/s10811-009-9485-y.
Lürling, M., van Oosterhout, F., & Faassen, E. (2017). Eutrophication and warming boost cyanobacterial biomass and microcystins. Toxins, 9(2), 1-16. https://doi.org/10.3390/toxins9020064.
Matthijs, H. C. P., Jančula, D., Visser, P. M., & Maršálek, B. (2016). Existing and emerging cyanocidal compounds: new perspectives for cyanobacterial bloom mitigation. Aquatic ecology, 50(3), 443–460. https://doi.org/10.1007/s10452-016-9577-0.
Meng, P., Pei, H., Hu, W., Liu, Z., Li, X., & Xu, H. (2015). Allelopathic effects of Ailanthus altissima extracts on Microcystis aeruginosa growth, physiological changes and microcystins release. Chemosphere, 141, 219-226. https://doi.org/10.1016/j.chemosphere.2015.07.057.
Mohamed, Z. A., & Al Shehri A. M. (2010). Differential responses of epiphytic and planktonic toxic cyanobacteria to allelopathic substances of the submerged macrophyte Stratiotes aloides. International Review of Hydrobiology, 95(3), 224-234. https://doi.org/10.1002/iroh.200911219.
Mowe, M. A. D., Song, Y., Sim, D. Z. H., Lu, J., Mitrovic, S. M., Tan, H. T. W., & Yeo, D. C. J. (2019). Comparative study of six emergent macrophyte species for controlling cyanobacterial blooms in a tropical reservoir. Ecological Engineering, 129, 11-21. https://doi.org/10.1016/j.ecoleng.2018.12.026.
Nakai, S., Inoue, Y., & Hosomi, M. (2001). Algal growth inhibition effects and inducement modes by plant-producing phenols. Water Research, 35(7), 1855–1859. https://doi.org/10.1016/s0043-1354(00)00444-9.
Ni, L., Acharya, K., Hao, X., & Li, S. (2012a). Isolation and identification of an anti-algal compound from Artemisia annua and mechanisms of inhibitory effect on algae. Chemosphere, 88(9), 1051–1057. https://doi.org/10.1016/j.chemosphere.2012.05.009.
Ni, L., Acharya, K., Hao, X., Li, S., Li, Y., & Li Y. (2012b). Effects of Artemisinin on Photosystem II performance of Microcystis aeruginosa by in vivo chlorophyll fluorescence. Bulletin of Environmental Contamination and Toxicology, 89(6), 1165–1169. https://doi.org/10.1016/j.chemosphere.2012.05.009.
Paerl, H. W., Gardner, W. S., Havens, K. E., Joyner, A. R., McCarthy, M. J., Newell, S. E., Qin, B., & Scott, J. T. (2016). Mitigating cyanobacterial harmful algal blooms in aquatic ecosystems impacted by climate change and anthropogenic nutrients. Harmful Algae, 54, 213-222. https://doi.org/10.1016/j.hal.2015.09.009.
Pakdel, F. M., Sim, L., Beardall, J., & Davis, J. (2013). Allelopathic inhibition of microalgae by the freshwater stonewort, Chara australis, and a submerged angiosperm, Potamogeton crispus. Aquatic Botany, 110, 24–30. https://doi.org/10.1016/j.aquabot.2013.04.005.
Pham, T. N., Pham, H. D., Dang, D. K., Duong, T. T., Le, T. P. Q., Nguyen, Q. D., & Nguyen, T. D. (2018). Anticyanobacterial phenolic constituents from the aerial parts of Eupatorium fortunei Turcz. Natural Product Research, 33(9), 1345- 1348. https://doi.org/10.1080/14786419.2018.1476511.
Rigosi, A., Hanson, P., Hamilton, D. P., Hipsey, M., Rusak, J. A., Bois, J., Sparber, K., Chorus, I., Watkinson, A. J., Qin, B., Kim, B., & Brookes, J. D. (2015). Determining the probability of cyanobacterial blooms: the application of Bayesian networks in multiple lake systems. Ecological Applications, 25(1), 186–199. https://doi.org/10.1890/13-1677.1.
Rodrígez, R. O. A., & Luna-Nemecio, J. (2019). Educación musical para el desarrollo sostenible: una revisión documental. Revista da Abem, 27(43), 132-149. https://doi.org/10.33054/ABEM2019b4307.
Santonja, M., Le Rouzic, B., & Thiébaut, G. (2018). Seasonal dependence and functional implications of macrophyte–phytoplankton allelopathic interactions. Freshwater Biology, 63(9), 1161-1172. https://doi.org/10.1111/fwb.13124.
Shao, J., Li, R., Lepo, J. E., & Gu, J. D. (2013). Potential for control of harmful cyanobacterial blooms using biologically derived substances: Problems and prospects. Journal of Environmental Management, 125, 149–155. https://doi.org/10.1016/j.jenvman.2013.04.001.
Sinang, S. C., Daud, N., Kamaruddin, N., & Poh, K. B. (2019). Potential growth inhibition of freshwater algae by herbaceous plant extracts. Acta Ecologica Sinica, 39, 229–233. https://doi.org/10.1016/j.chnaes.2018.12.005.
Takeda, F., Nakano, K., Nishimura, O., Shimada, Y., Fukuro, S., Tanaka, H., Hayashi, N., & Inamori Y. (2011). Allelopathic potential of Potamogeton pusillus community against Microcystis aeruginosa. Journal of Water and Environment Technology, 9(1), 21-28. https://doi.org/10.2965/jwet.2011.21.
Tan, K., Huang, Z., Ji, R., Qiu, Y., Wang, Z., & Liu, J. (2019). A review of allelopathy on microalgae. Microbiology, 165, 587–592. https://doi.org/10.1099/mic.0.000776.
Tebaa, L., Douma, M., Tazart, Z., Manaut, N., Mouhri, K., & Loudiki, M. (2017). Algicidal effects of Achillea ageratum L.and Origanum compactum Benth. plant extracts on growth of Microcystis aeruginosa. Applied Ecology and Environmental Research, 15(4), 719-728. https://doi.org/10.15666/aeer/1504_719728.
Tebaa, L., Douma, M., Tazart, Z., Manaut, N., Mouhri, K., & Loudiki, M. (2018). Assessment of the potentially algicidal effects of Thymus satureioides Coss. and Artemisia herba alba L. against Microcystis aeruginosa. Applied Ecology and Environmental Research 16(1), 903-912. https://doi.org/10.15666/aeer/1601_903912.
Techer, D., Fontaine, P., Personne, A., Viot, S., & Thomas, M. (2016). Allelopathic potential and ecotoxicity evaluation of gallic and nonanoic acids to prevent cyanobacterial growth in lentic systems: A preliminary mesocosm study. Science of the Total Environment, 547, 157–165. https://doi.org/10.1016/j.scitotenv.2015.12.164.
Vanderstukken, M., Declerck, S., Decaestecker, E., & Muylaert, K. (2014). Long-term allelopathic control of phytoplankton by the submerged macrophyte Elodea nuttallii. Freshwater Biology, 59(5), 930–941. https://doi.org/10.1111/fwb.12316.
Vanderstukken, M., Mazzeo, N., van Colen, W., Declerck, S. J., & Muylaert, K. (2011). Biological control of phytoplankton by the subtropical submerged macrophytes Egeria densa and Potamogeton illinoensis: a mesocosm study. Freshwater Biology, 56, 1837–1849. https://doi.org/10.1111/j.1365-2427.2011.02624.x.
Vázquez, V. P. T., Meza, G. R., Gutiérrez, M. F. A., Ruíz, V. V. M., Villalobos, M. J. J., Montes, M. J. A., & Fernández, T. A. A. J. (2018). Determination of LC50 and EC50 from endosulfan lactone and diazinon in earthworm (Eisenia foetida). Agroproductividad, 11(4), 105-111. http://www.revista-agroproductividad.org/index.php/agroproductividad/issue/view/66.
Visser, P. M., Verspagen, J. M. H., Sandrini, G., Stal, L. J., Matthijs, H. C. P., Davis, T. W., Paerl, H. W., & Huisman, J. (2016). How rising CO2 and global warming may stimulate harmful cyanobacterial blooms. Harmful Algae, 54, 145–159. https://doi.org/10.1016/j.hal.2015.12.006.
Wang, H. Q., Cheng, S. P., Zhang, S. H., He, F., Liang, W., Zhang, L. P., Hu, C. Y., Ge, F. J., & Wu, Z. B. (2010). Chemical composition in aqueous extracts of Potamogeton malaianus and Potamogeton maackianus and their allelopathic effects on Microcystis aeruginosa. Polish Journal of Environmental Studies, 19(1), 213-218. http://www.pjoes.com/Issue-1-2010,3830.
Wang, H., Liang, F., & Zhang, L. (2015). Composition and anti-cyanobacterial activity of essential oils from six different submerged macrophytes. Polish Journal of Environmental Studies, 24(1), 333-338. https://doi.org/10.15244/pjoes/26383.
Wang, H., Liang, F., Qiao, N., Dong, J., Zhang, L., & Guo, Y. (2014). Chemical composition of volatile oil from two emergent plants and their algae inhibition activity. Polish Journal of Environmental Studies, 23(6), 2371-2374. http://www.pjoes.com/Issue-6-2014,429.
Wang, H., Zhang, L., & Wang, Y. (2016b). Isolating and identifying organic acids from Portulaca oleracea and determining their anti-cyanobacterial activity. Polish Journal of Environmental Studies, 26(1), 441-445. https://doi.org/10.15244/pjoes/64465.
Wang, H., Zhong, G., Yan, H., Liu, H., Wang, Y., & Zhang, C. (2012). Growth control of cyanobacteria by three submerged macrophytes. Environmental Engineering Science, 29(6), 420-425. https://doi.org/10.1089/ees.2010.0286.
Wang, X., Jiang, C., Szeto, Y., Li, H., Yam, K. L., & Wang, X. (2016a). Effects of Dracontomelon duperreanum defoliation extract on Microcystis aeruginosa: physiological and morphological aspects. Environmental Science and Pollution Research, 23(9), 8731–8740. https://doi.org/10.1007/s11356-016-6119-1.
Wen, J., Sheng, H., Hao, C., Yunguo, L., Luhua, J., Quan, H., & Zhili, Y. (2018). Allelochemicals extracted from Eleocharis dulcis and their Inhibitory effects on Microcystis aeruginosa. Journal of Chemical Engineering & Process Technology, 9(2), 1-6. https://doi.org/10.4172/2157-7048.1000377.
Wu, X., Wu, H., Chen, J., & Ye, J. (2013). Effects of allelochemical extracted from water lettuce (Pistia stratiotes Linn.) on the growth, microcystin production and release of Microcystis aeruginosa. Environmental Science and Pollution Research, 2(11), 8192–8201. https://doi.org/10.1007/s11356-013-1783-x.
Wu, Y., Ge, H., & Zhou, Z. (2014). Effects of Fructus ligustri lucidi on the growth, cell integrity, and metabolic activity of the Microcystis aeruginosa. Environmental Science and Pollution Research, 22(11), 8471-8479. https://doi.org/10.1007/s11356-014-3997-y.
Yakefu, Z., Huannixi, W., Ye, C., Zheng, T., Chen, S., Peng, X., Tian, Z., Wang, J., Yang, Y., Ma, Z., & Zuo, Z. (2018). Inhibitory effects of extracts from Cinnamomum camphora fallen leaves on algae. Water Science & Technology, 77(11), 2545-2554. https://doi.org/10.2166/wst.2018.199
Yan, R., Ji, H., Wu, Y., Kerr, P.G., Fang, Y., & Yang, L. (2012). An investigation into the kinetics and mechanism of the removal of cyanobacteria by extract of Ephedra equisetina root. PloS One, 7(8), 1-8. https://doi.org/10.1371/journal.pone.0042285.
Yang, W., Tang, Z., Zhou, F., Zhang, W., & Song, L. (2013). Toxicity studies of tetracycline on Microcystis aeruginosa and Selenastrum capricornutum. Environmental Toxicology and Pharmacology, 35(2), 320–324. https://doi.org/10.1016/j.etap.2013.01.006.
Yi, Y., Lei, Y., Yin, Y., Zhang, H., Wang, G. 2012. The antialgal activity of 40 medicinal plants against Microcystis aeruginosa. Journal of Applied Phycology, 24(4), 847–856. https://doi.org/10.1007/s10811-011-9703-2.
Żak, A., & Kosakowska, A. (2016). Cyanobacterial and microalgal bioactive compounds – the role of secondary metabolites in allelopathic interactions. Oceanological and Hydrobiological Studies, 45(1) 131-143. https://doi.org/10.1515/ohs-2016-0013.
Zhang, C., Ling, F., Lei, Y. Y., Yu, Z. H., Xue, W. G. (2014). Algicidal activity and potential mechanisms of ginkgolic acids isolated from Ginkgo biloba exocarp on Microcystis aeruginosa. Journal of Applied Phycology, 26(1), 323–332. DOI: 10.1007/s10811-013-0057-9.
Zhang, C., Yi, Y., Hao, K., Liu, G., & Wang, G. (2013). Algicidal activity of Salvia miltiorrhiza Bung on Microcystis aeruginosa—Towards identification of algicidal substance and determination of inhibition mechanism. Chemosphere, 93(6), 997–1004. https://doi.org/10.1016/j.chemosphere.2013.05.068.
Zhang, S., Guo, L., Cao, J., & Chang, J. (2015). Allelopathic activities of three emergent macrophytes on several monospecific cyanobacterial species and natural phytoplankton assemblages. Polish Journal of Environmental Studies, 24(1), 397- 402. https://doi.org/10.15244/pjoes/26972.
Zhang, S., Zhang, S., & Li, G. (2016). Acorus calamus root extracts to control harmful cyanobacteria blooms. Ecological Engineering, 94, 95-101. https://doi.org/10.1016/j.ecoleng.2016.05.053
Zhang, T. T., He, M., Wu, A. P., & Nie, L. W. (2012). Inhibitory effects and mechanisms of Hydrilla verticillata (Linn.f.) Royle extracts on freshwater algae. Bulletin of Environmental Contamination and Toxicology, 88(3), 477–481. https://doi.org/10.1007/s00128-011-0500-z.
Zhang, T. T., Wang, L. L., He, Z. X., & Zhang, D. (2011). Growth inhibition and biochemical changes of cyanobacteria induced by emergent macrophyte Thalia dealbata roots. Biochemical Systematics and Ecology, 39(2), 88–94. https://doi.org/10.1016/j.bse.2011.01.004.
Zhao, W., Zheng, Z., Zhang, J., Roger SF., & Luo, X. (2019). Allelopathically inhibitory effects of eucalyptus extracts on the growth of Microcystis aeruginosa. Chemosphere, 225, 424-433. https://doi.org/10.1016/j.chemosphere.2019.03.070.
Zhou, S., Shao, Y., Gao, N., Deng, Y., Qiao, J., Ou, H., & Deng, J. (2013). Effects of different algaecides on the photosynthetic capacity, cell integrity and microcystin-LR release of Microcystis aeruginosa. Science of the Total Environment, 463–464, 111–119. https://doi.org/10.1016/j.scitotenv.2013.05.064.