Ferns are part of the diet and traditional medicine in East Asia, North America, and Oceania, however, their importance has been forgotten in Europe. Here, the nutritional and antioxidant potential of young fern fronds (fiddleheads) of eight families were studied. Most of the tested fern species excelled in high antioxidant capacity when compared to the reference leafy vegetables spinach and rocket. On average, the total phenol content reached 220 mg·g-1 of extract dry weight for all fiddleheads, and 15 out of 24 tested species exceeded 1 g Trolox equivalent per gram of extract dry weight in Oxygen Radical Absorbance Capacity (ORAC) assay. On the other hand, fiddleheads contained a comparable amount of carotenoids and ascorbic acid with the reference vegetables. In the case of fatty acid composition, fiddleheads contained especially high amounts of essential omega-3 (n3) and omega-6 (n6) polyunsaturated fatty acids with a beneficial n6/n3 ratio. The n6/n3 ratio in all tested species was between 2 and 6.4, whereas the ratio in the reference vegetables was below 0.4. All in all, fiddleheads from European ferns are a rich source of valuable antioxidants and essential fatty acids with a desirable n-6/n-3 ratio and may thus form an alternative source of these compounds, especially for those people not consuming fish and fish products.

Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamýcká 129 CZ 16521 Prague Czech Republic

Faculty of Science University of South Bohemia Branisovska 1760 CZ 37005 Ceske Budejovice Czech Republic

The Czech Academy of Sciences Institute of Experimental Botany Rozvojova 263 CZ 16502 Prague Czech Republic

Zobrazit více v PubMed

Smith A.R., Pryer K.M., Schuettpelz E., Korall P., Schneider H., Wolf P.G. A classification for extant ferns. TAXON. 2006;55:705–731. doi: 10.2307/25065646. DOI

Shmakov A. A community-derived classification for extant lycophytes and ferns. J. Syst. Evol. 2016;54:563–603. doi: 10.1111/jse.12229. DOI

Liu Y., Wujisguleng W., Long C. Food uses of ferns in China: A review. Acta Soc. Bot. Pol. 2012;81:263–270. doi: 10.5586/asbp.2012.046. DOI

Crowe A. A Field Guide to the Native Edible Plants of New Zeeland. 2nd ed. Godwit Press; Auckland, New Zealand: 1997.

May L.W. The economic uses and associated folklore of ferns and fern allies. Bot. Rev. 1978;44:491–528. doi: 10.1007/BF02860848. DOI

Bergeron M.E., Lapointe L. Impact of one year crozier removal on long-term frond production in Matteuccia struthiopteris. Can. J. Plant Sci. 2001;81:155–163. doi: 10.4141/P99-176. DOI

Goswami H.K., Sen K., Mukhopadhyay R. Pteridophytes: Evolutionary boon as medicinal plants. Plant Genet. Resour. 2016;14:328–355. doi: 10.1017/S1479262116000290. DOI

Zhu Q.-F., Zhao Q.-S. Chemical constituents and biological activities of lycophytes and ferns. Chin. J. Nat. Med. 2019;17:887–891. doi: 10.1016/S1875-5364(19)30108-6. PubMed DOI

Cao H., Chai T.-T., Wang X., Morais-Braga M.F.B., Yang J.-H., Wong F.-C., Wang R., Yao H., Cao J., Cornara L., et al. Phytochemicals from fern species: Potential for medicine applications. Phytochem. Rev. 2017;16:379–440. doi: 10.1007/s11101-016-9488-7. PubMed DOI PMC

Jamieson G., Reid E.H. The fatty acid composition of fern lipids. Phytochemistry. 1975;14:2229–2232. doi: 10.1016/S0031-9422(00)91104-X. DOI

Delong J., Hodges D.M., Prange R., Forney C., Toivenon P., Bishop M.C., Elliot M., Jordan M. The unique fatty acid and antioxidant composition of ostrich fern (Matteuccia struthiopteris) fiddleheads. Can. J. Plant Sci. 2011;91:919–930. doi: 10.4141/cjps2010-042. DOI

Singleton V.L., Orthofer R., Lamuela-Raventós R.M., Lester P. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol. 1999;299:152–178.

Silva E.M., Souza J.N.S., Rogez H., Rees J.-F., Larondelle Y. Antioxidant activities and polyphenolic contents of fifteen selected plant species from the Amazonian region. Food Chem. 2007;101:1012–1018. doi: 10.1016/j.foodchem.2006.02.055. DOI

Cao G.H., Prior R.L. Measurement of oxygen radical absorbance capacity in biological samples. Methods Enzymol. 1999;299:50–62. doi: 10.1016/s0076-6879(99)99008-0. PubMed DOI

Delong J.M., Hodges D.M., Prange R.K., Forney C.F., Fan L., Bishop M.C., Elliot M.L., Jordan M.A., Doucette C. The influence of cold water storage on fatty acids, antioxidant content and activity, and microbial load in ostrich fern (Matteuccia struthiopteris) fiddleheads. Can. J. Plant Sci. 2013;93:683–697. doi: 10.4141/cjps2012-165. DOI

Chang H.-C., Huang G.-J., Agrawal D.C., Kuo C.-L., Wu C.-R., Tsay H.-S. Antioxidant activities and polyphenol contents of six folk medicinal ferns used as “Gusuibu”. Bot. Stud. 2007;48:397–406.

Farràs A., Cásedas G., Les F., Terrado E.M., Mitjans M., López V., Martínez A.F. Evaluation of anti-tyrosinase and antioxidant properties of four fern species for potential cosmetic applications. Forests. 2019;10:179. doi: 10.3390/f10020179. DOI

Kratchanova M., Denev P., Ciz M., Lojek A., Mihailov A. Evaluation of antioxidant activity of medicinal plants containing polyphenol compounds. Comparison of two extraction systems. Acta Biochim. Pol. 2010;57:229–234. doi: 10.18388/abp.2010_2399. PubMed DOI

Soare L.C., Ferdes M., Stefanov S., Denkova Z., Nicolova R., Denev P., Bejan C., Paunescu A. Antioxidant Activity, Polyphenols Content and Antimicrobial Activity of Several Native Pteridophytes of Romania. Not. Bot. Horti Agrobot. Cluj-Napoca. 2012;40:53–57. doi: 10.15835/nbha4016648. DOI

Vasco C., Ruales J., Kamal-Eldin A. Total phenolic compounds and antioxidant capacities of major fruits from Ecuador. Food Chem. 2008;111:816–823. doi: 10.1016/j.foodchem.2008.04.054. DOI

Langhansova L., Pumprova K., Haisel D., Ekrt L., Pavicic A., Zajíčková M., Vanek T., Dvorakova M. European ferns as rich sources of antioxidants in human diet. Food Chem. under review. PubMed

Davey M.W., Van Montagu M., Inze D., Sanmartin M., Kanellis A., Smirnoff N., Benzie I.J.J., Strain J.J., Favell D., Fletcher J. Plant L-ascorbic acid: Chemistry, function, metabolism, bioavailability and effects of processing. J. Sci. Food Agric. 2000;80:825–860. doi: 10.1002/(SICI)1097-0010(20000515)80:7<825::AID-JSFA598>3.0.CO;2-6. DOI

Bone R.A., Davey P.G., Roman B.O., Evans D.W. Efficacy of commercially available nutritional supplements: Analysis of serum uptake, macular pigment optical density and visual functional response. Nutrients. 2020;12:1321. doi: 10.3390/nu12051321. PubMed DOI PMC

Feng L., Nie K., Jiang H., Fan W. Effects of lutein supplementation in age-related macular degeneration. PLoS ONE. 2019;14:e0227048. doi: 10.1371/journal.pone.0227048. PubMed DOI PMC

Kopsell D.A., Lefsrud M.G., Kopsell D.E., Wenzel A.J., Gerweck C., Curran-Celentano J. Spinach cultigen variation for tissue carotenoid concentrations influences human serum carotenoid levels and macular pigment optical density following a 12-week dietary intervention. J. Agric. Food Chem. 2006;54:7998–8005. doi: 10.1021/jf0614802. PubMed DOI

Ozawa Y., Nagai N., Suzuki M., Kurihara T., Shinoda H., Watanabe M., Tsubota K. Effects of constant intake of lute-in-rich spinach on macular pigment optical density: A pilot study. Nippon Ganka Gakkai Zasshi. 2016;120:41–48. PubMed

Sanabria J.C., Bass J., Spors F., Gierhart D.L., Davey P.G. Measurement of carotenoids in perifovea using the macular pigment reflectometer. J. Vis. Exp. 2020:e60429. doi: 10.3791/60429. PubMed DOI

Cho S., Lee D.H., Won C.-H., Kim S.M., Lee S., Lee M.-J., Chung J.H. Differential effects of low-dose and high-dose beta-carotene supplementation on the signs of photoaging and type I procollagen gene expression in human skin in vivo. Dermatology. 2010;221:160–171. doi: 10.1159/000305548. PubMed DOI

Miyazono S., Isayama T., Delori F.C., Makino C.L. Vitamin A activates rhodopsin and sensitizes it to ultraviolet light. Vis. Neurosci. 2011;28:485–497. doi: 10.1017/S0952523811000423. PubMed DOI PMC

Carocho M., Barreiro M.F., Morales P., Ferreira I.C. Adding molecules to food, pros and cons: A review on synthetic and natural food additives. Compr. Rev. Food Sci. Food Saf. 2014;13:377–399. doi: 10.1111/1541-4337.12065. PubMed DOI

Carlsen M.H., Halvorsen B.L., Holte K., Bøhn S.K., Dragland S., Sampson L., Willey C., Senoo H., Umezono Y., Sanada C., et al. The total antioxidant content of more than 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutr. J. 2010;9:3. doi: 10.1186/1475-2891-9-3. PubMed DOI PMC

Villaverde P., Lajous M., Macdonald C.-J., Fagherazzi G., Bonnet F., Boutron-Ruault M.-C. High dietary total antioxidant capacity is associated with a reduced risk of hypertension in French women. Nutr. J. 2019;18:31. doi: 10.1186/s12937-019-0456-0. PubMed DOI PMC

Ninfali P., Mea G., Giorgini S., Rocchi M., Bacchiocca M. Antioxidant capacity of vegetables, spices and dressings relevant to nutrition. Br. J. Nutr. 2005;93:257–266. doi: 10.1079/BJN20041327. PubMed DOI

Wojcikowski K., Stevenson L., Leach D., Wohlmuth H., Gobe G. Antioxidant capacity of 55 medicinal herbs traditionally used to treat the urinary system: A comparison using a sequential three-solvent extraction process. J. Altern. Complement. Med. 2007;13:103–110. doi: 10.1089/acm.2006.6122. PubMed DOI

Wolfe K.L., Kang X., He X., Dong M., Zhang Q., Liu R.H. Cellular antioxidant activity of common fruits. J. Agric. Food Chem. 2008;56:8418–8426. doi: 10.1021/jf801381y. PubMed DOI

Shou S., Lu G., Huang X. Seasonal variations in nutritional components of green asparagus using the mother fern cultivation. Sci. Hortic. 2007;112:251–257. doi: 10.1016/j.scienta.2006.12.048. DOI

Zeb A., Ullah F. Reversed phase HPLC-DAD Profiling of carotenoids, chlorophylls and phenolic compounds in Adiantum capillus-veneris leaves. Front. Chem. 2017;5:29. doi: 10.3389/fchem.2017.00029. PubMed DOI PMC

Kösesakal T. Effects of seasonal changes on pigment composition of Azolla filiculoides Lam. Am. Fern J. 2014;104:58–66. doi: 10.1640/0002-8444-104.2.58. DOI

Lytle T., Lytle J.S., Caruso A. Hydrocarbons and fatty acids of ferns. Phytochemistry. 1976;15:965–970. doi: 10.1016/S0031-9422(00)84381-2. DOI

Nekrasov E.V., Svetashev V.I., Khrapko O.V., Vyssotski M.V. Variability of fatty acid profiles in ferns: Relation to fern taxonomy and seasonal development. Phytochemistry. 2019;162:47–55. doi: 10.1016/j.phytochem.2019.02.015. PubMed DOI

Gemmrich A.R. Fatty acid composition of fern spore lipids. Phytochemistry. 1977;16:1044–1046. doi: 10.1016/S0031-9422(00)86721-7. DOI

Robinson P.M., Smith D.L., Safford R., Nichols B.W. Lipid metabolism in the fern Polypodium vulgare. Phytochemistry. 1973;12:1377–1381. doi: 10.1016/0031-9422(73)80569-2. DOI

Nekrasov E.V., Shelikhan L.A., Svetashev V.I. Fatty acid composition of gametophytes of Matteuccia struthiopteris (L.) Tod. (Onocleaceae, Polypodiophyta) Bot. Pac. 2019;8:63–66. doi: 10.17581/bp.2019.08104. DOI

Orsavova J., Misurcova L., Ambrozova J.V., Vicha R., Mlcek J. Fatty acids composition of vegetable oils and its contribution to dietary energy intake and dependence of cardiovascular mortality on dietary intake of fatty acids. Int. J. Mol. Sci. 2015;16:12871–12890. doi: 10.3390/ijms160612871. PubMed DOI PMC

Virgilio A., Sinisi A., Russo V., Gerardo S., Santoro A., Galeone A., Taglialatela-Scafati O., Roperto F. Ptaquiloside, the major carcinogen of bracken fern, in the pooled raw milk of healthy sheep and goats: An underestimated, global concern of food safety. J. Agric. Food Chem. 2015;63:4886–4892. doi: 10.1021/acs.jafc.5b01937. PubMed DOI

Tourchi-Roudsari M. Multiple effects of Bracken fern under in vivo and in vitro Conditions. Asian Pac. J. Cancer Prev. 2014;15:7505–7513. doi: 10.7314/APJCP.2014.15.18.7505. PubMed DOI

O’Connor P., Alonso-Amelot M., Roberts S., Povey A. The role of bracken fern illudanes in bracken fern-induced toxicities. Mutat. Res. Mutat. Res. 2019;782:108276. doi: 10.1016/j.mrrev.2019.05.001. PubMed DOI

Saito K., Nagao T., Matoba M., Koyama K., Natori S., Murakami T., Saiki Y. Chemical assay of ptaquiloside, the carcinogen of pteridium aquilinum, and the distribution of related compounds in the pteridaceae. Phytochemistry. 1989;28:1605–1611. doi: 10.1016/S0031-9422(00)97808-7. DOI

Rasmussen L.H., Pedersen H.A. Screening for ptaquiloside in ferns: Using herbarium specimens for qualitative mapping purposes. Phytochem. Anal. 2017;28:575–583. doi: 10.1002/pca.2707. PubMed DOI

Murbach T.S., Béres E., Vértesi A., Glávits R., Hirka G., Endres J.R., Clewell A.E., Szakonyiné I.P. A comprehensive toxicological safety assessment of an aqueous extract of Polypodium leucotomos (Fernblock®) Food Chem. Toxicol. 2015;86:328–341. doi: 10.1016/j.fct.2015.11.008. PubMed DOI

Murbach T.S., Glávits R., Hirka G., Endres J.R., Clewell A.E., Szakonyiné I.P. A 28-day oral toxicology study of an aqueous extract of Polypodium leucotomos (Fernblock®) Toxicol. Rep. 2017;4:494–501. doi: 10.1016/j.toxrep.2017.09.002. PubMed DOI PMC

Mondal S., Panigrahi N., Sancheti P., Tirkey R., Mondal P., Almas S., Kola V. Evaluation of toxicological, diuretic, and laxative properties of ethanol extract from Macrothelypteris Torresiana (Gaudich) aerial parts with in silico docking studies of polyphenolic compounds on carbonic anhydrase II: An enzyme target for diuretic activity. Pharmacogn. Res. 2018;10:408. doi: 10.4103/pr.pr_16_18. DOI

Erhirhie E.O., Ilodigwe E.E. Sub-chronic toxicity evaluation of Dryopteris filix-mas (L.) schott, leaf extract in albino rats. Braz. J. Pharm. Sci. 2019;55:e18107. doi: 10.1590/s2175-97902019000118107. DOI

Socolsky C., Dominguez L., Asakawa Y., Bardon A. Unusual terpenylated acylphloroglucinols from Dryopteris wallichiana. Phytochemistry. 2012;80:115–122. doi: 10.1016/j.phytochem.2012.04.017. PubMed DOI

Wollenweber E., Stevens J.F., Ivanic M., Deinzer M.L. Acylphloroglucinols and flavonoid aglycones produced by external glands on the leaves of two dryopteris ferns and currania robertiana. Phytochemistry. 1998;48:931–939. doi: 10.1016/S0031-9422(97)01003-0. DOI

Hwang Y.-H., Ha H., Ma J.Y. Acute oral toxicity and genotoxicity of Dryopteris crassirhizoma. J. Ethnopharmacol. 2013;149:133–139. doi: 10.1016/j.jep.2013.06.011. PubMed DOI

The Impact of Pesticide Use on Tree Health in Riparian Buffer Zone

Metabolic and Oxidative Changes in the Fern Adiantum raddianum upon Foliar Application of Metals