Keywords

6.1 Introduction

Pteridophytes are the oldest primitive vascular plants constituting the second largest group of vascular plants contributing to the diversity of plant kingdom. Their global representation is more than 1200 species belonging to 204 genera. Pteridophytes are known to grow in varied climatic zones with different phytogeographical regimes depending on the microclimatic conditions. Being cosmopolitan, pteridophytes usually grow in the humid tropical, subtropical, temperate (Dryopteridaceae), alpine (Woodsiaceae), and arid (Cheilanthoideae and Pteridaceae) regions. Its sporophyte consists of roots, stem, leaves, and well-developed vascular strands. Although they prefer shady and moist habitats with moderate temperature regimes, they occupied a wide range of habitats including high altitude biomes. Medicinal and ethnobotanical uses of pteridophytes are less versatile compared to the angiosperms (Chowdury 1973; Vyas and Sharma 1998). Liu et al. (2012) documented about 52 species of ferns, which are edible in China. Caius (1935) documented several medicinal applications of ferns occurring in the Indian subcontinent. The in vitro propagation of pteridophytes is of great interest for the preservation of economically valued, medicinal, edible, and ornamental ferns (Bharti et al. 2013).

In the Indian subcontinent, the pteridophyte diversity is notable especially in the Himalayas, Western Ghats, and Eastern Ghats (Dixit 2000). They are more specifically distributed in temperate Himalayas and tropical ecoregions of Deccan Plateau (Shankar and Khare 1992; Vasudev 1999; Shrivastava 2007). Surveys in Kigga forests of the central Western Ghats revealed occurrence of 31 species of pteridophytes belonging to 20 families (Deepa et al. 2013). Surveys in Mudigere region of the Western Ghats resulted in documentation of 26 fern species belonging to 17 families with highest frequency of Selaginella monospora followed by Adiantum philippense, Pteris biaurita, Adiantum concinnum, and Tectaria paradoxa (Parashurama et al. 2016). Maridass and Raju (2010) documented up to 272 species of ferns and fern allies (95 genera belong to 34 families) from southern Western Ghats. Among them, 89 species were common, 33 species were rare, 26 were endemic species, 12 were near threatened, and 9 were very rare. Benjamin and Manickam (2007) described 61 medicinal pteridophytes (belong to 31 families) in the Western Ghats utilized by the native tribes to treat ailments like cold, cough, fever, stomach disorders, rheumatics, diabetes, and poisonous bites. The aim of the present chapter is to consolidate the usefulness of ferns especially nutraceutical value, bioactive potential, and functional attributes with emphasis on the values and relevance of different species of Diplazium.

6.2 Nutraceutical Importance

Bracken (Pteridium) fiddle heads are nutritionally rich sources in Korea, and they contain significant amounts of protein, fiber, vitamins, and minerals (Copeland 1942; Thakur et al. 1998). Table 6.1 provides proximal composition of different parts of 20 edible ferns. The range of proximal composition of ferns includes moisture, 25.6–91.1%; crude protein, 0.6–24.1%; total lipids, 0.2–21.5%; crude fiber, 0.5–62.2%; ash, 0.6–19.5%; and carbohydrates, 3.1–57.2%. The crude protein content in Pteridium aquilinum (leaves) is comparable to those of legume seeds (21.9–24.1%). The total lipids of stem and leaves of Dicksonia antarctica were higher than other ferns (21.5–15.5 vs. 0.2–6%). The crude fiber content was high in Azolla microphylla (leaves, 13.4%), A. pinnata (whole plant, 14.7%), and Acrostichum aureum (rhizome, 10.3%). The carbohydrate content was highest in roots of Diksonia antarctica (57.2%) followed by A. aureum (rhizome, 53.3%), A. microphylla (leaves, 37.7%), A. pinnata (whole plant, 33.8%), and D. antarctica (stem, 25.3%). The high ash content in leaves of A. microphylla (24.3%), whole plant of A. pinnata (19.5%), and leaves of Nephrolepis cordifolia (11%) reveals their rich mineral composition (Table 6.1).

Table 6.1 Proximal composition of 20 edible ferns (%)
Full size table

Several ferns are ideal source of major minerals (sodium, calcium, potassium, magnesium, and phosphorus) as well as trace elements (iron, copper, zinc, and manganese) (Oloyede et al. 2014). They possess remarkably high quantities of many essential amino acids (Deka et al. 2016; Zanariah et al. 1986; Sanginga and Hove 1989; Bhaskaran and Kannapan 2015). According to Delong et al. (2011), Matteuccia struthiopteris (ostrich fern) is known for higher quantity of rare fatty acids than green vegetable including ω-3 (arachidonic and eicosapentaenoic acids) and ω-6 fatty acids (γ-linolenic and dihomo-γ-linolenic acids). With ferns being nutritionally versatile, it is possible to preserve their fiddle heads (unfurled fronds) as source of food.

The process of preservation of fiddle heads is fairly simple, and cleaned fiddle heads should be steam boiled in hot water followed by sun drying or preserved in a salt layer, which could last long up to 2–3 years (Lee and Shin 2011). During requirement, the dried fiddle heads could be recooked (with mashed garlic, salt, sesame oil, and soybean sauces), while the salted fiddle heads should be rinsed with running water followed by cooking similar to dried ones. The fiddle heads are commonly boiled with butter followed by addition of cider or wine vinegar with a bit of pepper (Lee and Shin 2011).

Besides nutraceutical source to humans, some ferns such as Dryopteris wallichiana, Nephrolepis biserrata, and Ophioglossum grande are also useful as fodder in Nigeria (goat, sheep, and other ruminants) (Nwosu 2002; Oloyede et al. 2013). The aquatic fern Azolla pinnata is used as feed for broiler chicken, laying hens, goats, and calves of buffalo, while Azolla filiculoides serves as source of protein while rearing pigs (Becerra et al. 1990; Duran 1994; Samanta and Tamang 1995; Alalade et al. 2007; Balaji et al. 2009; Indira et al. 2009, Leterme et al. 2010; Cherryl et al. 2014).

6.3 Bioactive Potential

Although ferns bridge the gap between lower and higher plants, compared to angiosperms, ferns are underexplored as well as underutilized for their potency of phytochemicals (Cao et al. 2017). Ferns are also known to replace chemical herbicides owing to their inhibitory metabolites. Several studies documented therapeutic potential of ferns especially chemopreventive, hepatoprotective, cytotoxic, antihyperglycemic, leishmanicidal, trypanocidal, antimicrobial, antinociceptive, anti-inflammatory, and immunomodulatory properties (Wu et al. 2005; Wills and Asha 2006; Yonathan et al. 2006; Wills and Asha 2009; Radhika et al. 2010; Zheng et al. 2011a, b; Morais-Braga et al. 2013a, b; Socolsky et al. 2015; Cao et al. 2017). With expectation of a few (e.g., Lycopodium), ferns do not synthesize alkaloids. However, various phenolic compounds like acylphloroglucinols, nonprotein amino acids, cyanogenic glycosides, and flavonoids have been reported. Polyphenols are useful as antioxidants, and it is generally recognized to reduce the risks of many chronic diseases. Screening of 37 ferns and fern allies (Polystichum lepidocaulon and P. polyblepharum) showed presence of 13% total polyphenols in dried fronds and rhizomes (Shin 2010; Shin and Lee 2010). In addition, the dried fronds of Davallia mariesii and rhizomes of Athyrium niponicum, Cyrtomium fortunei, Dicranopteris pedata, and Dryopteris nipponensis possess >10% of total polyphenols.

6.3.1 Antioxidant Properties

In many countries, brackens are considered as poisoning plants owing to their carcinogenic and anti-thiamin properties (Somvanshi and Ravishankar 2004). However, the hot water extracts of dried bracken fiddle heads yielded acidic polysaccharides, which exhibits anticomplementary activities (Byeong et al. 1994). Antioxidant activities (DPPH radical and ABTS radical-scavenging) have been studied from the frond and rhizome extracts of several fern genera (Adiantum, Athyrium, Coniogramme, Cytominum, Davallia, Dicranopteris, Dryopteris, Hypolepis, Lycopodium, Lygodium, Matteuccia, Onoclea, Osmunda, Pteridium, Polypodium, Polystichum, Pteris, Pyrrosia, Selaginella, Thelypteris, and Woodsia) (Shin 2010). Many of them showed different antioxidant activities by scavenging DPPH and ABTS radicals. More specifically, fern families like Dryopteridaceae, Osmundaceae, and Woodsiaceae exhibited powerful antioxidant activities. The fiddle heads of Athyrium acutipinulum also showed strong antioxidant effects (Lee et al. 2005). Crude extracts of some ferns showed higher antioxidant activity than vitamin C (Soare et al. 2012). Thus, it is expected that analyzing antioxidant activities in ferns would result in the development of several healthcare products to combat aging as well as chronic diseases (Soare et al. 2012).

6.3.2 Antimicrobial Activities

Ferns are known for their efficient antimicrobial agents against several harmful microbes. They are also useful in developing antibiotic sprays, packing material, toothpaste, and handwash products and to protect human body from undesired microbes. The extracts obtained from ferns serve as effective antimicrobial agents against Gram-positive bacteria (e.g., Bacillus subtilis and Staphylococcus aureus), Gram-negative bacteria (e.g., Escherichia coli, Pseudomonas aeruginosa, and Salmonella typhi), and fungi (Banerjee and Sen 1980; Vincent and Kanna 2007; Lee et al. 2009). The genus Dryopteris exhibited vigorous antibiotic activities. Dryopteris crassirhizoma and D. filix-mas could be used to control methicillin-resistant Staphylococcus aureus (MRSA) (Lee et al. 2009), while D. cochleata serve against Gram-positive bacteria, Gram-negative bacteria, and fungi (Banerjee and Sen 1980). Because of high activity of D. crassirhizoma against Streptococcus, its anti-tooth decay substance has been patented in Korea. However, according to Shin (2010), fronds of Athyrium niponicum and Hypolepis punctata are more efficient than D. crassirhizoma against Streptococcus mutans and S. sobrinus.

6.3.3 Cosmeceutical Qualities

Ferns are also useful as cosmetic ingredients. For example, Dryopteris spp. possess strong inhibitory activities against acne causing Propionibacterium acnes on the skin (Yoon et al. 2006). Many fern extracts containing high phenolic compounds are currently used as ingredients of body and facial cosmetics (e.g., cleanser, toner, moisturizer, shampoo, and conditioner). Extracts of some ferns are useful and effective natural cosmetic ingredients. Furthermore, the phenolic compounds of ferns are beneficial in skin care owing to prevention of UV-induced skin damages, anti-wrinkle, and skin-whitening properties (Svobodová et al. 2003; Tanaka et al. 2004; An et al. 2005; Parvez et al. 2006). A number of ferns possess phytoecdysteroids (e.g., ecdysone) (which is not present in most of the angiosperms) helpful in promoting cell regeneration, refining skin texture, and strengthening skin barrier (Lin and Lin 1989; Meybeck et al. 1997). Since fern spores are not causing hay fever, cosmetics consisting of fern spores are patented in Korea, and such products are used as facial scrub (Moran 2004).

6.4 Functional Attributes

Physicochemical characteristics of proteins play a prominent role in quality control of food stuffs. The low-cost protein derived from green vegetables will meet the demand of food proteins in many industries. The food processing industries emphasize on leaf protein isolates owing to low lipid and fiber content (Rana et al. 2015). Green leaves possess protein up to 40–70% along with carotenoids, vitamin E, and minerals (Badar and Kulkarni 2011). Isolation of high quality of green leaf protein is simple, affordable, and favorable for commercial applications (Moure et al. 2002). However, the functional properties of fern proteins are less studied, and only countable research articles are available.

The rhizome starch fern is commonly employed in the food industry for preparation of vermicelli, cakes, and concentrated soups marketed in East Asian countries (Zhang et al. 2011). The fern starch is also useful in preparation of liquor and soft drinks in China (Liu et al. 2012). The starchy paste obtained from Marsilea drummondii is edible in Australia (Mannan et al. 2008). The starch purified from fern is significantly tough with suitable elastic properties (Cao et al. 2007). The starch granules from the rhizome of Acrostichum aureum possess high solubility (35%) as well as swelling power (12.3%) (Lobo and Gulimane 2015). The protein solubility is also remarkable in ferns, for example, high solubility is known in leaf protein concentrate of Nephrolepis biserrata (55.9%, pH 8), Arthropteris orientalis (45%, pH 10), and Diplazium esculentum (28.52%, pH 12) (Essuman et al. 2014; Rana et al. 2015). Ferns such as Nephrolepis biserrata and Arthropteris orientalis possess pH-dependent foam capacity and attain maximum foam capacity at pH 14. An epiphytic fern Metapolypodium memeiense is also used as a taste enhancer during cooking vegetables, and many ferns are available in local markets of China as dried fronds, salted fronds, packed fronds, fern starch, fern starch noodles, fern starch cakes, and fern leaf tea (Liu et al. 2012). Different parts of about 144 species of ferns are edible and utilized to replenish nutrition in China.

6.5 Diplazium: A Versatile Fern

Diplazium is a diverse genus belonging to the lady fern family (Athyriaceae). This fern has pantropical distribution and is separated from Allantodia based on the characteristic non-imparipinnate fronds and grooves from rachis to costa (Ching 1964). It is a terrestrial fern with erect to suberect rhizome forming caudex and strong roots. The fronds are large and pinnately compound with herbaceous lamina.

6.5.1 Diversity

The genus Diplazium consists of 400 species distributed in different pantropical regimes (e.g., Malesia, Neotropics, Afro-Madagascar region, and cold temperate regions of Eurasia) (Tryon and Tryon 1982; Wu and Ching 1991; Chu and He 1999; Pacheco and Moran 1999; Mickel and Smith 2004; Roux 2009). The rare and endangered endemic fern Diplazium molokaiense was reported in East Maui, Hawaii (Wood 2006). Diplazium fimbriatum has been reported as a new species from Brazil (Mynssen and Matos 2012). Several Diplazium spp. are known from Thailand (D. bantamense, D.cordifolium, D. crenatoseratum, D. esculentum, D. polypodioides, D. riparium, D. silvaticum, D. simplicivenium, D. sorzogonense, and D. tomentosum) (Boonkerd et al. 2008). Indonesia also possesses many Diplazium spp. (D. asperum, D. cordifolium, D. esculentum, D. lomariaceum, D. pallidum, D. simplicivenium, D. sorzogonense, and D. tomentosum) (Slik et al. 2006). Kholia (2011) has documented nearly 40 species of Diplazium in India, and up to 17 species have been reported in Sikkim alone. The common Diplazium in India include D. bellum, D. dilatatum, D. doederleinii, D. esculentum, D. forrestii, D. kawakamii, D. latifolium, D. laxifrons, D. longifolium, D. maximum, D. medogense, D. polypodioides, D. sikkimense, D. spectabile, D. squamigerum, and D. stoliczkae. The Diplazium species are also reported from the Western Ghats regions of Maharashtra, Karnataka, Kerala, and Tamil Nadu (Dudani et al. 2012, 2014; Das et al. 2013; Kavitha et al. 2015; Patil et al. 2016; Sathish and Vijayakanth 2016). It is possible to conserve Diplazium spp. by spore explant (initiation, multiplication, and differentiation), which is economical as well as rapid method of propagation (Nair et al. 2014).

6.5.2 Nutraceutical Value

Fiddle heads and tender pinna of Diplazium esculentum are commonly edible in the Western Ghats region, which is common along the rivers and swampy areas in the Western Ghats of India (Copeland 1942; Akter et al. 2014; Greeshma and Sridhar 2016; Sridhar and Karun 2017; Greeshma et al. 2018). It is one of the most commonly consumed fern in hilly tribes in Northeastern India and the Philippines (Copeland and Collado 1936). Fiddle heads of three Diplazium species reported from different regions are known to possess a wide range of crude protein (0.2–31.2%), total lipid (0.1–8.3%), crude fiber (0.4–12.7%), ash (1.4–17.6%), and carbohydrates (0.02–68.6%) (Table 6.2). The qualitative test showed presence of reducing sugars especially anthraquinones and anthranol glycosides (Tongco et al. 2014).

Table 6.2 The proximal composition of three Diplazium species (%)
Full size table

Fern shoots are excellent source of minerals and electrolytes (e.g., potassium, iron, manganese, and copper) (Seal 2012). Fresh shoots contain up to 7% of daily required quantities of potassium, which combats blood pressure as well as regulate heart contractions. Diplazium spp. are also composed of major minerals (calcium, sodium, potassium, magnesium, and phosphorus) and trace elements (iron, copper, zinc, and manganese) (Table 6.3). The mineral composition of Diplazium is dependent on the species as well as different segments used for analysis. Potassium and calcium are the most abundant minerals present in Diplazium spp. Different parts of Diplazium esculentum and D. sammatti fulfil the range of NRC-NAS (1989) standards for major minerals and trace elements required for infants, children, and adults. Besides, these ferns also meet the desired Na/K (<1) and Ca/P (>1) ratios; such ratios are known to combat the blood pressure and prevent the loss of calcium in urine to restore calcium in bones, respectively (Shills and Young 1988; Yusuf et al. 2007).

Table 6.3 Mineral composition of different parts of two Diplazium species (mg/100 g)
Full size table

Leaves and fiddle heads of Diplazium esculentum are also known for several indispensable and dispensable amino acids (Table 6.4). The fiddle heads possess higher amount of amino acids compared to leaves with exception of sulfur amino acids. Interestingly, sulfur amino acids were substantially higher in leaves than fiddle heads (methionine, 2.1 vs. 1.4 g/110 g protein; cystine, 4.2 vs. 0.5 g/100 g protein). The leaves fulfil the FAO-WHO (1991) stipulated standard for sulfur amino acids (6.3 vs. 2.5 g/100 protein). This offers nutraceutical advantage of use of fiddle heads along with desired quantity of leaves to gain sulfur amino acids. The fiddle heads also fulfil FAO-WHO (1991) standard for indispensable amino acids like histidine, isoleucine, leucine, lysine, threonine, and valine. Among the dispensable amino acids, glutamic acid was highest in leaves, while the glycine was highest fiddle heads followed by glutamic acid, alanine, proline, aspartic acid, serine, and arginine.

Table 6.4 Amino acid composition of Diplazium esculentum in comparison with FAO-WHO standard (g/100 g protein)
Full size table

6.5.3 Bioactive Potential

It is believed by the native tribes in India that D. esculentum is useful to counteract constipation and serve as an appetizer (Kala 2005; Das et al. 2008). Concoction of this fern is used to cure hemoptysis and cough, while the rhizomes serve as insecticides (Kaushik et al. 2011, 2012). Studies on D. esculentum also showed its usefulness as anaphylactic shock and mast cell stabilizer (Das et al. 2012). The fiddle heads contain only 34 calories of energy per 100 g, and nonetheless their high-quality nutraceutical profile is composed of health promoting antioxidants, vitamins, and essential fatty acids (ω-3 and ω-6).

Fresh fronds possess very high quantities of antioxidant vitamin A and carotenes. Fiddle heads weighing 100 g contain 3617 IU (or 120%) of recommended daily requirements of vitamin A. Further, they also endowed with small to moderate quantities of many B vitamins (e.g., niacin, riboflavin, and thiamine). Besides vitamins (essential for vision), fiddle heads also serve as powerful natural antioxidants required by the human body for maintaining the integrity of the skin and mucus membranes. Studies also suggested that natural foods rich in vitamin A help in protecting the body against lung and oral cancers. They are also excellent source of many natural polyphenolic flavonoids (α-carotene and β-carotene), and they will be converted into vitamin A in vitro. The fresh fiddle heads of 100 g contain 26.6 mg (44%) of daily required vitamin C content. Vitamin C is a moderately potential water-soluble antioxidant with flavonoid compound like carotenes, which helps scavenging harmful free radicals, offering protection from cancers, inflammation, viral cough, and cold. Unique sweet taste of fiddle heads comes from their richness in vitamin C.

Ethanolic extract of shade-dried fronds possesses high quantities of phenolics, flavonoids, and saponins than aqueous extract (Das et al. 2013). Further, the chromatogram of HPTLC revealed presence of different types of polyphenols as well as steroidal saponins. Aqueous and ethanolic extracts of the D. esculentum showed inhibitory effect against growth of many human as well as plant pathogenic bacteria. The positive results are comparable with tetracycline as standard antibiotic. It was found that mixing fern extract with antibiotic in equal proportions will be more effective against pathogenic bacteria than antibiotic alone (Amit et al. 2011).

6.6 Concluding Remarks

Pteridophytes distributed in a wide range of habitats prefer shady moist conditions with moderate temperature regimes. They are also versatile like angiosperms in ethnobotanical and medicinal properties. Fiddle heads of several ferns are nutritionally rich especially proteins, fiber, minerals, and vitamins. They are also known for remarkably high quantities of many essential amino acids and endowed with essential fatty acids. Starch from fern rhizomes is suitable for preparation of several foodstuffs and industrial products. In addition to the leaf protein and rhizome starch, ferns possess many valuable functional attributes useful in production of food as well as medicinal products. Many ferns are known for antimicrobial, cytotoxic, hepatoprotective, antihyperglycemic, antiprotozoal, antinociceptive, immunomodulatory, and chemopreventive properties. Ferns have the capability to serve as bioherbicide to replace chemical herbicides.

Diplazium is one of the versatile ferns distributed in pantropical regions. In India, this fern is widely distributed in the Western Ghats and Sikkim. The fiddle heads of Diplazium possess good proximal components and minerals. Diplazium shows high antioxidant activities due to presence of vitamin A and carotenoids. They possess many therapeutic potential like protection of mucus membranes, prevention of cancers, and protection against inflammation.

Pteridophytes have potential nutraceutical and bioactive components useful in human diet and therapeutics. Many ferns could be cultivated in different locations besides their native habitats like kitchen gardens, botanical gardens, and arboretum similar to those of orchids. Although Diplazium esculentum occurs naturally as riparian fern in the Western Ghats, it could be cultivated in lateritic soils of Southwest India without major efforts. Morphologically distinct 3–4 varieties (or landraces) of D. esculentum are known from the Western Ghats based on ethnic knowledge of locals and tribes. Serious efforts are warranted toward utilization of ferns in the direction of nutraceuticals, and health protective attributes would open up new avenues for food and pharmaceutical industries.