Abstract
The present work explores the use of weed extracts and purified compounds as environmentally friendly antifouling additives with a possible application in marine paints. Two species were selected as case studies: Verbena bonariensis L., Verbenaceae, and Tillandsia tenuifolia L., Bromeliaceae. The extracts of both species showed promising antifouling activity in laboratory experiments (byssal thread formation of the mussel Mytilus edulis) and also in field assays by incorporation to soluble-matrix paints, which were used to coat acrylic tiles that were submerged in the sea for a period of 45 days. In the case of the Verbena extract, it was not possible to identify a major bioactive component, and aralidioside, the main iridoid, did not show antifouling activity. However, in the case of the Tillandsia extract, the main component, which was isolated and identified as cycloartenone, displayed potent antifouling activity in laboratory and field assays. Since both species have high growth rates, these results may help overcome the sustainability issues of the use of natural products as antifoulants. At the same time, the technological use of these untapped biological resources may offer a new possibility for weed management.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agostini VO, Macedo AJ, Muxagata E, da Silva MV, Pinho GLL (2020) Non-toxic antifouling potential of Caatinga plant extracts: effective inhibition of marine initial biofouling. Hydrobiologia 847:45–60. https://doi.org/10.1007/s10750-019-04071-6
Amara I, Miled W, Ben Slama R, Ladhari N (2018) Antifouling processes and toxicity effects of antifouling paints on marine environment. A Review Environ Toxicol Phar 57:115–130. https://doi.org/10.1016/j.etap.2017.12.001
Anisimov AV, Mikhailova MA, Uvarova EA (2019) Modern approaches to the development of marine antifouling coatings. Inorg Mater Appl Res 10:1384–1389. https://doi.org/10.1134/S2075113319060029
Benvenuti S, Cioni PL, Flamini G, Pardossi A (2017) Weeds for weed control: Asteraceae essential oils as natural herbicides. Weed Res 57(342):353. https://doi.org/10.1111/wre.12266
Bianco EM, Rogers R, Laneuville Teixeira V, Crespo Pereira R (2009) Antifoulant diterpenes produced by the brown seaweed Canistrocarpus cervicornis. J Appl Phycol 21:341–346. https://doi.org/10.1007/s10811-008-9374-9
Bohlin L, Göransson U, Alsmark C, Wedén C, Backlund A (2010) Natural products in modern life science. Phytochem Rev 9:279–301. https://doi.org/10.1007/s11101-009-9160-6
Cabrera GM, Seldes AM (1995) Hydroperoxycycloartanes from Tillandsia recurvata. J Nat Prod 58:1920–1924. https://doi.org/10.1021/np50126a020
Cabrera GM, Gallo M, Seldes AM (1996) Cycloartane derivatives from Tillandsia usneoides. J Nat Prod 59:343–347. https://doi.org/10.1021/np960075+
Callow ME, Callow JA (2002) Marine biofouling: a sticky problem. Biologist 49:1–5
Carter GT, Crews P (2011) Harnessing the biosynthetic capacity of marine-derived organisms. Bioorg Med Chem 19:6556
Casanova E, García-Mina JM, Calvo MI (2008) Antioxidant and antifungal activity of Verbena officinalis L. leaves. Plant Food Hum Nutr 63:93–97. https://doi.org/10.1007/s11130-008-0073-0
Chen CC, Huang HY, Shen CC, Huang YL, Ou JC (2003) Chemical constituents of Verbena bonariensis. Taiwan Pharm J 55:65–70. https://doi.org/10.7019/CPJ.200302.0065
Claver FK, Alaniz FJ, Cald D (1983) Tillandsia spp.: epiphytic weeds of trees and bushes. Forest Ecol Manag 6:367–372. https://doi.org/10.1016/0378-1127(83)90044-0
Escobar A, Pérez M, Sathicq A, García M, Paola A, Romanelli G, Blustein G (2019) Alkyl 2-furoates obtained by green chemistry procedures as suitable new antifoulants for marine protective coatings. J Coat Technol Res 16:159–166. https://doi.org/10.1007/s11998-018-0110-3
Ferraro DO, Ghersa CM (2013) Fuzzy assessment of herbicide resistance risk: glyphosate-resistant Johnsongrass, Sorghum halepense (L.) Pers., in Argentina’s croplands. Crop Prot 51:32–39. https://doi.org/10.1016/j.cropro.2013.04.004
Figueiredo AMG, Nogueira CA, Saiki M, Milian FM, Domingos M (2007) Assessment of atmospheric metallic pollution in the metropolitan region of São Paulo, Brazil, employing Tillandsia usneoides L. as biomonitor. Environ Pollut 145:279–292. https://doi.org/10.1016/j.envpol.2006.03.010
Foster MS, Harrold C, Hardin DD (1991) Point vs. photo quadrat estimates of the cover of sessile marine organisms. J Exp Mar Biol Ecol 146:193–203. https://doi.org/10.1016/0022-0981(91)90025-R
Francolini I, Vuotto C, Piozzi DG (2017) Antifouling and antimicrobial biomaterials: an overview. APMIS 125:392–417. https://doi.org/10.1111/apm.12675
Fusetani N (2011) Antifouling marine natural products. Nat Prod Rep 28:400–410. https://doi.org/10.1039/C0NP00034E
Hong J (2012) Natural product diversity and its role in chemical biology and drug discovery. Curr Op Chem Biol 15:350–354. https://doi.org/10.1016/j.cbpa.2011.03.004
Jägerbrand A, Brutemark A, Svedén JB, Gren IM (2019) A review of the environmental impacts of shipping on aquatic and nearshore ecosystems. Sci Total Environ 695:133637. https://doi.org/10.1016/j.scitotenv.2019.133637
Jain SC, Singh B, Jain R (2001) Antimicrobial activity of triterpenoids from Heliotropium ellipticum. Fitoterapia 72:666–668. https://doi.org/10.1016/S0367-326X(01)00267-2
Jensen SR, Nielsen BJ (1980) Iridoid glucosides in Griselinia, Aralidium and Toricelia. Phytochemistry 19:2685–2688. https://doi.org/10.1016/S0031-9422(00)83944-8
Kikuchi T, Ishii K, Ogihara E, Zhang J, Ukiya M, Tokuda H, Iida T, Tanaka R, Akihisa T (2014) Cytotoxic and apoptosis-inducing activities, and anti-tumor-promoting effects of cyanogenated and oxygenated triterpenes. Chem Biodiv 11:491–504. https://doi.org/10.1002/cbdv.201300395
Krug PJ (2006) Defense of benthic invertebrates against surface colonization by arvae. A chemical arms race. In: Fusetani N, Clare AS Antifouling compounds. Springer, Berlin, pp 1–53
Kyei SK, Darko G, Akaranta O (2020) Chemistry and application of emerging ecofriendly antifouling paints: a review. J Coat Technol Res 17:315–332. https://doi.org/10.1007/s11998-019-00294-3
Lewis J (1998) Marine biofouling and its prevention on underwater surfaces. Mater Forum 22:41–61
Liu LL, Wu CH, Qian PY (2020) Marine natural products as antifouling molecules – a mini review (2014–2020). Biofouling 36:1210–1236. https://doi.org/10.1080/08927014.2020.1864343
Lowe HIC, Toyang NJ, Bryant J (2013a) In vitro and in vivo anti-cancer effects of Tillandsia recurvata (ball moss) from Jamaica. W Indian Med J 62:177–180. https://doi.org/10.7727/wimj.2013.091
Lowe HIC, Toyang NJ, Watson C, Badal S, Bahado-Singh P, Bryant J (2013b) In vitro anticancer activity of the crude extract and two dicinnamate isolates from the Jamaican Ball Moss (Tillandsia recurvata L.). Ame Int J Contemp Res 3:93–96
Maréchal JP, Hellio C (2009) Challenges for the development of new non-toxic antifouling solutions. Int J Mol Sci 10:4623–4637. https://doi.org/10.3390/ijms10114623
Pagani F (1984) Constituents of Verbena bonariensis L. (Verbenaceae). Boll Chim Farm 123:477–482
Pandey RK, Dobhal M, Graham A, Oseroff A (2005) Iridoid-saccharide compound and method of using same. Eur Pat Appl EP1527783
Patiño Cano LP, Quitana Manfredi R, Pérez M, García M, Blustein G, Cordeiro R, Pérez CD, Schejter L, Palermo JA (2018) Isolation and antifouling activity of azulene derivatives from the Antarctic gorgonian Acanthogorgia laxa. Chem Biodiv 15:e1700425
Paz EA, Cerdeiras MP, Fernandez J, Ferreira F, Moyna P, Soubes M, Vázquez A, Vero S, Zunino L (1995) Screening of Uruguayan medicinal plants for antimicrobial activity. J Ethnopharmacol 45:67–70. https://doi.org/10.1016/0378-8741(94)01192-3
Pérez M, Sánchez M, Stupak M, García M, Rojo de Almeida MT, Oberti JC, Palermo JA, Blustein G (2014) Antifouling activity of celastroids isolated from Maytenus species, natural and sustainable alternatives for marine coatings. Ind Eng Chem Res 53:7655–7659. https://doi.org/10.1021/ie4033507
Pérez M, Sánchez M, García M, Patiño Cano LP, Blustein G, Palermo JA (2019) Antifouling activity of peracetylated cholic acid, a natural bile acid derivative. Steroids 149:108414. https://doi.org/10.1016/j.steroids.2019.05.006
Protopapa M, Kotsiri M, Mouratidis S, Roussis V, Ioannou E, Dedos SK (2019) Evaluation of antifouling potential and ecotoxicity of secondary metabolites derived from red algae of the genus Laurencia. Mar Drugs 17:346. https://doi.org/10.3390/md17110646
Qi SH, Ma X (2017) Antifouling compounds from marine invertebrates. Mar Drugs 15:263. https://doi.org/10.3390/md15090263
Qian PY, Xu Y, Fusetani N (2009) Natural products as antifouling compounds: recent progress and future perspectives. Biofouling 26:223–234. https://doi.org/10.1080/08927010903470815
Rittschof D (2017) Off the shelf fouling management. Mar Drugs 15:176. https://doi.org/10.3390/md15060176
Rubiano-Buitrago P, Duque F, Puyana M, Ramos FA, Castellanos L (2019) Bacterial biofilm inhibitor diterpenes from Dictyota pinnatifida collected from the Colombian Caribbean. Phytochem Lett 30:74–80. https://doi.org/10.1016/j.phytol.2019.01.021
Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611. https://doi.org/10.1093/biomet/52.3-4.591
Siless G, García M, Pérez M, Blustein G, Palermo J (2018) Large-scale purification of pachydictyol A from the brown alga Dictyota dichotoma obtained from algal wash and evaluation of its antifouling activity against the freshwater mollusk Limnoperna fortunei. J Appl Phycol 30:629–636. https://doi.org/10.1007/s10811-017-1261-9
Silva ACO, Santana EF, Saraiva AM, Coutinho FN, Castro RHA, Pisciottano MNC, Amorim ELC, Albuquerque UP (2013) Which approach is more effective in the selection of plants with antimicrobial activity? Evid-Based Compl Alt 308980. https://doi.org/10.1155/2013/308980
Singh B, Dubey MM (2001) Estimation of triterpenoids from Heliotropiun marifolium Koen. ex Retz. in vivo and in vitro. I Antimicrobial Screening. Phytother Res 15:231–234. https://doi.org/10.1002/ptr.759
Stepp J (2004) The role of weeds as sources of pharmaceuticals. J Ethnopharmacol 92:163–166. https://doi.org/10.1016/j.jep.2004.03.002
Stepp JR, Moerman DE (2001) The importance of weeds in ethnopharmacology. J Ethnopharmacol 75:19–23. https://doi.org/10.1016/S0378-8741(00)00385-8
Techato K, Salaeh A, van Beem NC (2014) Use of atmospheric epiphyte Tillandsia usneoides (Bromeliaceae) as biomonitor. APCBEE Procedia 10:49–53. https://doi.org/10.1016/j.apcbee.2014.10.014
Tundis R, Loizzo MR, Menichini F, Statti G, Menichini F (2008) Biological and pharmacological activities of iridoids: recent developments. Mini-Rev Med Chem 8:399–420. https://doi.org/10.2174/138955708783955926
Wester S, Zotz G (2010) Growth and survival of Tillandsia flexuosa on electrical cables in Panama. J Trop Ecol 26:123–126. https://doi.org/10.1017/S0266467409990459
Yebra DM, Kiil S, Dam-Johansen K (2004) Antifouling technology—past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog Org Coat 50:75–104. https://doi.org/10.1016/j.porgcoat.2003.06.001
Zambrano EE, Casas AG, Di Venosa GM, Uriburu ML, Duran FJ, Palermo JA (2017) Synthesis and cytotoxicity evaluation of A-ring derivatives of cycloartanone. Phytochem Lett 21:200–205. https://doi.org/10.1016/j.phytol.2017.06.021
Acknowledgements
We thank Lic. Amalia Suarez and Dr. Sabina Donadío (Darwinion Botanical Institute) for the plant taxonomy. EEZ thanks CONICET for a doctoral fellowship. MP, LRF, MLU, MS, GB and JAP are researchers of CONICET. The authors also thank the Club de Motonáutica of Mar del Plata for the permission to use their marine testing site.
Funding
Research at UMYMFOR-FCEN-UBA was supported by grants from CONICET to JAP (PIP 2014–2016 Nº 11220130100523CO), UBA (UBACyT 2014–2017 Nº 20020130100457BA) and ANPCyT (PICT 2014–2063).
Author information
Authors and Affiliations
Contributions
MP, MG and GB performed and analysed all the laboratory and field antifouling experiments. LF and MS performed the phytochemical work with V. bonariensis at UBA, while EZ and MLU worked with T. tenuifolia at UNS. JP and GB directed the project and wrote the manuscript.
Corresponding author
Ethics declarations
Competing Interests
The authors declare no competing interests.
Additional information
Dr. Blustein and Dr. Palermo share main co-authorship.
Rights and permissions
About this article
Cite this article
Pérez, M., Fernández, L.R., Zambrano, E.E. et al. Use of Weed Extracts as Antifouling Additives for Marine Paints: Two Case Studies. Rev. Bras. Farmacogn. 31, 420–428 (2021). https://doi.org/10.1007/s43450-021-00165-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s43450-021-00165-2