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Home , Adiantum formosum, Adiantum reniforme, Adiantum trapeziforme, Argyrochosma limitanea, Equisetum arvense, Equisetum diffusum

South African Journal of 77 (2011) 10–19

Minireview Phytoliths of

J. Mazumdar

UGC Centre for Advanced Study, Department of Botany, The University of Burdwan, Burdwan-713104, Received 3 June 2010; received in revised form 14 July 2010; accepted 28 July 2010

Abstract

Study of phytoliths of pteridophytes is an emerging area of research. Literature on this aspect is limited but increasing. Some recent findings have shown that phytoliths may have systematic and phylogenetic utility in pteridophytes. Phytoliths are functionally significant for the development and survival of pteridophytes. Experiments with some pteridophytes have revealed various aspects of silica uptake, deposition and biological effects. © 2010 SAAB. Published by Elsevier B.V. All rights reserved.

Keywords: Biogenic silica; ; Pteridophytes; Phytolith; Silicification

1. Introduction In spite of environmental effects on silica uptake, ongoing investigations indicate that phytolith formation is primarily Many deposit silica as solid hydrated Silicone dioxide under genetic control (Piperno, 2006). Phytoliths have been (SiO2,nH2O) in the lumen or in intercellular spaces, where used successfully as taxonomic tools in angiosperms, especially it is known as “phytoliths” or “ stones” (Greek, phyto = in monocots (Piperno, 1988; Tubb et al., 1993). Less plant, lithos = stone) or “silicophytoliths” or “opal phytoliths” or information is available about pteridophytic phytoliths. The “plant opal” or “opaline silica” or “biogenic silica” or “bioliths”. objective of this review is to evaluate the present status and The term “phytolith” may also be applied to other mineral future prospects of phytolith research in pteridophytes. structures of plant origin, including calcium oxalate crystals, but is more usually restricted to silica particles (Prychid et al., 2004). Phytoliths are extremely durable in the soil and may not 2. Phytoliths in pteridophytes migrate through it to the same extent as do other microfossils, such as and diatoms (Prychid et al., 2004). Many plants The umbrella terms “pteridophytes” and “ferns and produce phytoliths with characteristic, distinguishable shapes, allies” were used to denote a group of bearing, -less and which are known accordingly as “diagnostic” phytoliths. vascular plants that demonstrated many aspects of early Diagnostic phytoliths recovered from soil provide valuable evolution of land plants and undergone considerable taxonomic information about the identity and possibly concentration of treatments. Based on morphological and molecular data source plant , and are useful for the reconstruction of “Lycopods” or “Lycopsids”, previously placed in fern allies palaeoenvironments, investigation of ancient agricultural prac- are now separated as clade “” sister to all other land tices, study of crop , monitoring vegetation and plants and “Whisk ferns” and “Horsetail”, also previously climate change, radiometric dating, identification of drug plants, considered under fern allies are now included within “Ferns” or crop processing (Harvey and Fuller, 2005), forensic investiga- “Monilophytes” or “Moniloformopses” (cf. Smith et al., 2006). tions, indicator of diets of ancient animals (more discussion in In a recent treatment Chase and Reveal (2009) recognized Prychild et al., 2004; Piperno, 2006 and citations therein), and “Lycophytes” as Subclass Lycopodiidae Beketov and placed 5 recently for nanotechnology (Neethirajan et al., 2009). subclasses — Subclass Warm., Subclass Marattii- dae Klinge, Subclass Klinge, Subclass Poly- podiidae Cronquist, and Subclass Psilotidae Reveal under E-mail address: [email protected]. “Monilophytes”. However, in the present account term

0254-6299/$ - see front matter © 2010 SAAB. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.sajb.2010.07.020 J. Mazumdar / South African Journal of Botany 77 (2011) 10–19 11

Fig. 1. Phyoliths of Huperzia selago (A), Blechnum orientale (B), himalayaensis (C), diffusum (D) and (E). (Bar in A=100 μm, in B, C and D =20 μm, in E=10 μm).

“pteridophytes” is used in broad sense, encompassing all clades among silica deposition patterns in Subgenus Hippochaete of Ferns and Lycophytes. (smooth or amorphous type depositions) and Sebgenus Davy (1814) was one of the first to investigate the form of Equisetum (granular type depositions). But, Hauke (1974) silica in plants, including the of Equisetum, and considered that the available information was insufficient to Mettenius (1864) coined the terms “Deckzellen” (cover cells) or formulate a sectional classification of the subgenus Equisetum “Stegmata” (from the Greek stegium, a roof or covering) for (cf. Guillon, 2004) and this treatment was not accepted widely. cells that contain inclusions and lie over sclerenchyma in ferns; However, variations in surface micromorphological features these cells contained calcium oxalate crystals in Cyatheaceae, among different species of Equisetum indicated their possible silica concretions in Dryopteris and true stegmata (cells use for identification at species level. Filippini et al. (1995) containing silica bodies) in most Trichomanes species (cf. utilized micromorphological features like, size of mamillae and Prychid et al., 2004). pilulae distribution over the surface of stomata for identification In pteridophytes silica bodies in different plant parts have been of E. arvense in finely powdered form of commercially observed by several authors, including Mettenius (1864), Pant available drug Herba equiseti. and Srivastava (1961), Kaufman et al. (1971), Dengler and Lin Sundue (2009) studied epidermal phytoliths from of (1980), Parry et al. (1985), Rolleri et al. (1987), Piperno (1988), ferns belonging to Family sensu Schuettpelz et al. Le Coq et al. (1991), Lanning and Eleuterius (1994), Stevenson (2007). The occurrence of phytoliths were found to be a and Loconte (1996), Thorn (2006) and others (cited by Sundue, potential synapomorphy for the adiantoid clade, several smaller 2009). However, distinguishable forms or “diagnostic” forms of clades of pteridoid clade, including Pityrogramma and the sister silica bodies or phytoliths, useful for delineation of family, genus group of Actiniopteris and . Phytoliths were not found or species are known for only few taxa (Table 2). in Ceratopteridoid or cryptogrammatoid clades. But phytoliths Mazumdar and Mukhopadhyay (2009a,b, 2010) surveyed 47 were diagnostic in adiantoid and pteridoid clades (Table 2) and species of pteridophytes and suggested that phytoliths could be diverse in cheilanthoid clade, reflecting independent origins of useful for taxonomic purposes as some plate or sheet-like these major lineages. This study also indicated that phytoliths phytoliths show distinct features in different species. Using were evolved once in adiantoid and twice in pteridoid clades. scanning electron microscope Page (1972) made detailed But this analysis was scored by two characters (presence/ observations on surface micromorphology of silicified aerial absence and location of phytoliths) and use of morphological of Equisetum andproposedthreesectionsunder features like shape, margin, and surface ornamentations of Subgenus Equisetum — Section I: Equisetum sect. nov. phytoliths might provide better resolution of interrelationships (contains E. fluviatile and E. arvense), Section 2: Subvernalia of clades. Although this study reported the absence of phytoliths A.Br. (contains E. pratense and E. sylvaticum) and Section 3: in vittata, they were found in lamina and vein area in Palustria sect. nov. (contains E. bogotense, E . diffusum, E. pinnule by Chauhan et al. (2009). Also, more sampling is palustre and E. telmateia) on the basis of variability of shape, required for Ceratopteridoid and cryptogrammatoid ferns to size and distribution of pilulae (bead like projections), mamillae confirm the absence of phytoliths in these clades. (rounded or conical projections) and stomatal cell area (paired For extraction of phytoliths from plant tissues Chauhan et al. cells around each stomatal pore). He also noted variations (2009) used dry ashing method in which samples were heated in 12 J. Mazumdar / South African Journal of Botany 77 (2011) 10–19 muffle furnace at 500–600 °C for 4–6 h, then digested with different parts of 14 species of pteridophytes ( nitric acid (HNO3), washed with distilled water, dried and japonicum, Selaginella bryopteris, Actiniopteris australis, mounted in Canada balsam. Mazumdar and Mukhopadhyay caudatum, A. phillippense, A. peruvianum, A. (2009a,b, 2010) used modified wet oxidation method of Piperno venustum, Cyathea gigentea, Doryopteris sagittifolia, Drynaria (2006) in which plant materials were digested with concentrated quercifolia, Gleichenia microphylla, arifolia, Lygo- HNO3 (instead of potassium chlorate+HNO3) in water bath, dium flexuosum and ) and proposed that the boiled with 10% hydrochloric acid (HCl) to remove calcium, presence of silica in the early land plants suggests that the washed with distilled water, dried with acetone and mounted in mechanism of silica absorption and accumulation was devel- 10% glycerine. Sundue (2009) used wet oxidation method of oped early in the evolution of terrestrial vegetation, because Piperno (1988) in which materials were digested with sulfuric silica was important for the survival of terrestrial life as it gave acid (H2SO4) and chromic trioxide or hydrogen peroxide mechanical stability of tissues, protection against fungi and (H2O2). He also visualized epidermal phytoliths of lamina pests, and resistance against drought by checking evaporation. at 60× magnification in dissection microscope. In general, however, Silicon concentration in shoots is shown to Kao et al. (2008) found partial polarization light microscopy have declined among land plants in the sequence liver- technique and cryo-tabletop-scanning electron microscopy wortsNhorsetails NclubmossesNmosses NangiospermsNgymn- technique useful for direct visualization of Spicular cells or ospermsNferns, and relative Silicon concentrations were, venuloid idioblasts (long and silica containing epidermal cells) in general, low in angiosperms, and ferns in lamina of Pteris grevilleana. For confirming chemical nature (Hodson et al., 2005). of silica bodies they successfully utilized silica specific dyes Silver-ammine chromate, Crystal Violet Lactone and Methyl 4. Experimental works on silica with pteridophytes Red (developed by Dayanandan et al., 1983) and energy dispersive X-ray spectrometer. Experimental works with some pteridophytes can provide important insight into the mechanisms by which plants 3. Biological significance of phytoliths accumulate and deposit silica in various organs. Soluble silica, the raw material for phytolith production, is absorbed as The occurrence of silicon (Si) within the plant is a result of its monosilicic or orthosilicic acid [Si(OH)4] from the soil through uptake, in the form of soluble Si(OH)4 or Si(OH)3O2, from the . Different plant species show different modes of silica soil and its controlled polymerization at a final location (Currie uptake, notably active, passive or rejective, through low affinity and Perry, 2007). The occurrence of silicon as silica bodies or transporter, etc (cf. Currie and Perry, 2007). Fu et al. (2002) phytolith in many plants has been correlated with mechanical documented a novel mechanism of obtaining nutrients and support (Kaufman et al., 1973), reduction of water loss (Gao et accelerating the weathering of soil minerals in fern Matteuccia. al., 2004), protection from (Vicari and Bazely, This fern may physically incorporate silicate mineral particles 1993), prevention of entry of pathogens (Nanda and Gang- into the cortex, dissolve inorganic nutrients from the opadhyay, 1984), protection from metal toxicity (Hodson and silicate minerals to leave silica particles in the cortex nearly in Evans, 1995), root elongation (Hattori et al., 2003), increased pure form. Further investigation is required for proper capture of light for (Yoshida et al., 1959), and in understanding about the silica uptake process in other cooling of leaves (Wang et al., 2005). Recent findings indicate pteridophytes. that silicon protects the plants from various biotic and abiotic Equisetum accumulate high amounts of silica in their plant stresses by enhancing the production of enzymes and various body and have been used as a model system for understanding compounds (like, chitinases, peroxidases, polyphenol oxidases, silica deposition (bio-silicification) and the ultra-structure of flavonoid phytoalexins, etc) related to stress resistance, but the silicified layers in plants. Various techniques such as Electron detailed mechanism has yet to be fully elucidated (cf. Currie and microprobe analysis by Kaufman et al. (1971), scanning and Perry, 2007). transmission electron microscopy by Perry and Fraser (1991) Chen and Lewin (1969) found that silicon is an essential and Holzhüter et al. (2003), microtomography, energy disper- element for the healthy growth of E. arvense and silicon sive X-ray elemental mapping, small-angle and wide-angle deficient plants showed symptoms like necrosis of the branch scattering of X-rays by Sapei et al. (2007) and Raman tips, or drooping of the branches. In vitro study with E. microscopy by Sapei et al. (2007) and Gierlinger et al. (2008) hyemale by Hoffman and Hillson (1979) indicated that silicon is have been used to elucidate ultra-structure details of silicified a required nutrient for spore viability and essential for layers. completion of the life cycle of this plant. Kaufman et al. (1971) observed that Silica was deposited Developmental studies also indicated the importance of primarily in discrete knobs and rosettes on the epidermal surface silicification in mechanical strengthening (Kaufman et al., in E. arvense, but essentially in a uniform pattern on and in the 1973) and in negative geotropism (Srinivasan et al., 1979)inE. entire outer epidermal cell walls of E. hyemale var. affine. hyemale var. affine. In E. arvense the surface micromorphology was found to be However, evolutionary advantages offered by silicon very complex and principally fibrillar, globular and sheet-like deposited as silica are still not clearly understood. Chauhan et ultra-structural motifs of silica were found by Perry and Fraser al. (2009) observed silica deposition of biological origin in (1991). Silica was present as a thin layer on the outer surface J. Mazumdar / South African Journal of Botany 77 (2011) 10–19 13

Table 1 List of pteridophytes studied for phytoliths. Family Species Studied Occurrence Status References plant parts Lycopodium clavatum L. Whole plant + M Chauhan et al. (2009), Mazumdar and Mukhopadhyay (2009b) " L. japonicum Thunb. Aerial +NMazumdar and Mukhopadhyay (2009b) branch " cernua (L.) Franco and Vasc. Aerial +MMazumdar and Mukhopadhyay (2009b), Author branch (unpublished) " Huperzia selago (L.) Bernh. ex Schrank and Aerial +DMazumdar and Mukhopadhyay (2009b) Mart. branch Selaginellaceae Selaginella bryopteris (L.) Bak. Whole plant + D Chauhan et al. (2009), Mazumdar and Mukhopadhyay (2009b), Author (unpublished) " Selaginella inaequalifolia (Hook. and Grev.) Aerial shoot + M Mazumdar and Mukhopadhyay (2009b), " Selaginella involvens (Sw.) Spring Aerial shoot + N Mazumdar and Mukhopadhyay (2009b) " Selaginella monospora Spring Aerial shoot + N Mazumdar and Mukhopadhyay (2009b) " Selaginella pentagona Spring Aerial shoot + M Mazumdar and Mukhopadhyay (2009b) " (Desv. ex Poir.) Hieron. Aerial shoot + N Mazumdar and Mukhopadhyay (2009b) " Selaginella tenera (Hook. and Grev.) Spring Aerial shoot + M Mazumdar and Mukhopadhyay (2009b) " Selaginella chrysocaulos (Hook. and Grev.) Aerial shoot + N Mazumdar and Mukhopadhyay (2009b) Spring " Selaginella velutina A.R. Smith Leaf + D cf. Piperno (2006) Isoetaceae Isöetes coromandelina L. Leaf + M Mazumdar and Mukhopadhyay (2009b) " Isöetes weberi Herter Leaf + D Iriarte and Paz (2009) Ophioglossaceae Botrychium virginianum (L.) Sw. Leaf, spike + M Mazumdar and Mukhopadhyay (2010) " Helminthostachys zeylanica (L.) Hook. Leaf + M Mazumdar and Mukhopadhyay (2010) " Ophioglossum reticulatum L. Leaf + D Mazumdar and Mukhopadhyay (2010),Author (unpublished) Psilotaceae Not studied Equisetum diffusum D. Don Leaf, stem + D cf. Piperno (2006), Mazumdar and Mukhopadhyay (2010) Angiopteris evecta (Forst.) Hoffm. Leaf + M Mazumdar and Mukhopadhyay (2010) Osmundaceae Not studied Hymenophyllaceae *Hymenophyllum sp. Leaf − cf. Piperno (2006) *Trichomanes sp. Leaf + D cf. Piperno (2006) Gleicheniaceae Dicranopteris linearis (Burm. f.) Und. Leaf + M Mazumdar and Mukhopadhyay (2010) Gleichenia gigantea Wall. ex Hook. Leaf + M Mazumdar and Mukhopadhyay (2010) Gleichenia microphylla R. Br. Whole plant + M Chauhan et al. (2009) Dipteridaceae Not studied Matoniaceae Not studied Lygodiaceae Lygodium flexuosum (L.) Sw. Whole plant + M Chauhan et al. (2009) Anemiaceae Not studied Schizaeaceae Not studied Marsileaceae Marsilea ancylopoda A. Braun Leaf + N Iriarte and Paz (2009) " Marsilea minuta L. Leaf + M Author (unpublished) Salviniaceae Azolla pinnata R. Br. Whole plant + M Author (unpublished) " Salvinia molesta Mitch. Leaf + N Author (unpublished) Thyrsopteridaceae Not studied Loxomataceae Not studied Culcitaceae Not studied Plagiogyriaceae Not studied Cibotiaceae Not studied Cyatheaceae Cyathea gigentea (Wall. ex Hook.) Holtt. Whole plant + N Chauhan et al. (2009) " Cyathea spinulosa Wall. ex Hook. Leaf + M Mazumdar and Mukhopadhyay (2010) Dicksoniaceae Not studied Metaxyaceae Not studied Lindsaeaceae Lindsaea odorata Roxb. Leaf + M Mazumdar and Mukhopadhyay (2010) " Sphenomeris chinensis (L.) Maxon Leaf + M Mazumdar and Mukhopadhyay (2010) Saccolomataceae Not studied Dennstaedtiaceae Hypolepis punctata (Thunb.) Mett. ex Kuhn Leaf + M Mazumdar and Mukhopadhyay (2010) Pteridaceae Acrostichum danaeifolium Langsd. and Fisch Leaf − Sundue (2009) " Actiniopteris australis Link Whole plant + D Chauhan et al. (2009), Sundue (2009) " Adiantopsis radiata (L.) Fée Leaf − Sundue (2009) " Adiantum abscissum Schrad. Leaf + D Sundue (2009) " Adiantum adiantoides (J. Sm.) C. Chr. Leaf + D Sundue (2009) (continued on next page) 14 J. Mazumdar / South African Journal of Botany 77 (2011) 10–19

Table 1 (continued) Family Species Studied Occurrence Status References plant parts " Adiantum andicola Liebm. Leaf + D Sundue (2009) " Adiantum argutum Splitg. Leaf + D Sundue (2009) " Adiantum cajennense Willd. Leaf + D Sundue (2009) " Adiantum capillus-junonis Rupr. Leaf + D Sundue (2009) " Adiantum capillus-veneris L. Leaf + D Sundue (2009) " Adiantum caryotideum H. Christ Leaf + D Sundue (2009) " Adiantum caudatum L. Whole plant + D Chauhan et al. (2009), Sundue (2009) " Adiantum concinnum Humb. and Bonpl. ex Leaf + D Sundue (2009) Willd. " Adiantum cordatum Maxon Leaf + D Sundue (2009) Adiantum delicatulum Mart. Leaf + D Sundue (2009) Adiantum delicatulum Hook Leaf − Sundue (2009) " Adiantum dolosum Kunze Leaf + D Sundue (2009) " Adiantum formosum R. Br. Leaf + D Sundue (2009) " Adiantum fructuosum Poepp. ex Spreng. Leaf + D Sundue (2009) " Adiantum glaucescens Klotzsch Leaf + D Sundue (2009) " Adiantum hispidulum Sw. Leaf + D Sundue (2009) " Adiantum humile Kunze Leaf + D Sundue (2009) " Adiantum incertum Lindman Leaf + D Sundue (2009) " Adiantum intermedium Sw. Leaf + D Sundue (2009) " Adiantum jordanii C.H. Mull Leaf − Sundue (2009) " Adiantum kaulfusii Kunze Leaf + D Sundue (2009) " Adiantum kendalii Jenman Leaf + D Sundue (2009) " Adiantum krameri B. Zimmer Leaf + D Sundue (2009) " Adiantum latifolium Lam. Leaf + D Sundue (2009) " Adiantum leprieurii Hook. Leaf + D Sundue (2009) " Adiantum lucidum (Cav.) Spreng. Leaf + D Sundue (2009) " Adiantum lunulatum Burm.f. Leaf + D Sundue (2009) " Adiantum macrophyllum Sw. Leaf + D Sundue (2009) " Adiantum malesianum J. Ghatak Leaf + D Sundue (2009) " Adiantum mcvaughii Mickel and Beitel Leaf + D Sundue (2009) " Adiantum multisorum Sampaio Leaf + D Sundue (2009) " Adiantum oaxacanum Mickel and Beitel Leaf + D Sundue (2009) " Adiantum obliquum Desv. Leaf + D Sundue (2009) " Adiantum paraense Hieron. Leaf + D Sundue (2009) " Adiantum patens Willd. Leaf + D Sundue (2009) " Adiantum peruvianum Klotzsch Whole plant + D Chauhan et al. (2009), Sundue (2009) " Adiantum petiolatum Desv. Leaf + D Sundue (2009) " Adiantum phillippense L. Whole plant + D Chauhan et al. (2009), Sundue (2009) " Adiantum phyllitidis J. Sm. Leaf + D Sundue (2009) " Adiantum platyphyllum Sw. Leaf + D Sundue (2009) " Adiantum poeppigianum (Kuhn) Hieron. Leaf + D Sundue (2009) " Adiantum poiretii Wikstr. Leaf − Sundue (2009) " Adiantum polyphyllum Willd. Leaf + D Sundue (2009) " Adiantum pulverulentum L. Leaf + D Sundue (2009) " Adiantum pyramidale (L.) Willd. Leaf + D Sundue (2009) " Adiantum raddianum C. Presl Leaf + D Sundue (2009) " Adiantum reniforme L. Leaf − Sundue (2009) " Adiantum scalare R.M. Tryon Leaf + D Sundue (2009) " Adiantum seemanii Hook. Leaf + D Sundue (2009) " Adiantum serratodentatum Willd. Leaf + D Sundue (2009) " Adiantum tenerum Sw. Leaf + D Sundue (2009) " Adiantum terminatum Kunze ex Miq. Leaf + D Sundue (2009) " Adiantum tetraphyllum Humb. and Bonpl. ex Leaf + D Sundue (2009) Willd. " Adiantum tomentosum Klotzsch Leaf + D Sundue (2009) " Adiantum trapeziforme L. Leaf + D Sundue (2009) " Adiantum trichochlaenum Mickel and Beitel Leaf + D Sundue (2009) " Adiantum tricholepis Fée Leaf + D Sundue (2009) " Adiantum venustum D. Don Whole plant + D Chauhan et al. (2009), Sundue (2009) " Adiantum villosissimum Kuhn Leaf + D Sundue (2009) " Adiantum villosum L. Leaf + D Sundue (2009) " Adiantum vogellii Mett. ex Keys Leaf + D Sundue (2009) " Adiantum wilsonii Hook. Leaf + D Sundue (2009) J. Mazumdar / South African Journal of Botany 77 (2011) 10–19 15

Table 1 (continued) Family Species Studied Occurrence Status References plant parts " Afropteris repens Alston Leaf + D Sundue (2009) " Aleuritopteris argentea (S.G.Gmel.) Fée Leaf − Sundue (2009) " Aleuritopteris aurantiacea (Cav.) Ching Leaf − Sundue (2009) " Aleuritopteris farinosa (Forssk.) Fée Leaf − Sundue (2009) " Ananthacorus angustifolius (Sw.) Underw. and Leaf + D Sundue (2009) Maxon " Anetium citrifolium (L.) Splitg. Leaf + D Sundue (2009) " Anogramma leptophylla (L.) Link Leaf − Sundue (2009) " Anopteris hexagona (L.) C. Chr. Leaf − Sundue (2009) " Antrophyum boryanum (Willd.) Spreng. Leaf + D Sundue (2009) " Antrophyum callifolium Blume Leaf + D Sundue (2009) " Antrophyum latifolium Bl. Leaf + D Sundue (2009) " Antrophyum lineatum (Sw.) Kaulf. Leaf + D Sundue (2009) " Antrophyum mannianum Hook. Leaf + D Sundue (2009) " Antrophyum minersum Bory Leaf + D Sundue (2009) " Antrophyum plantagineum Cav. Leaf + D Sundue (2009) " Antrophyum reticulatum (Forst.) Kaulf. Leaf + D Sundue (2009), Mazumdar and Mukhopadhyay (2010) " Antryophum brasilianum (Desv.) C. Chr. Leaf + D Sundue (2009) " Antryophym obovatum Baker Leaf + D Sundue (2009) " limitanea (Maxon) Windham Leaf − Sundue (2009) " Aspidotis californica (Hook.) Nutt. ex Copel. Leaf + N Sundue (2009) " Aspidotis densa (Brack) Lellinger Leaf + N Sundue (2009) " Astrolepis sinuata (Lag. ex Sw.) D.M. Benham Leaf − Sundue (2009) and Windham " Austrogramme decipiens (Mett.) Hennipman Leaf − Sundue (2009) " Bommeria hispida (Mett. ex Kuhn) Underw. Leaf − Sundue (2009) " Ceratopteris pteridoides (Hook.) Hieron. Leaf − Sundue (2009) " Ceratopteris richardii Brongn. Leaf − Sundue (2009) " alabamensis (Buckley) Kunze Leaf − Sundue (2009) " Cheilanthes albomarginata Clarke Leaf + N Sundue (2009), Mazumdar and Mukhopadhyay (2010) " Cheilanthes angustifolia Kunth Leaf − Sundue (2009) " Cheilanthes cuneata Kaulf. ex Link Leaf − Sundue (2009) " Cheilanthes decomposita (M. Martens and Leaf − Sundue (2009) Galeotti) Fée " Cheilanthes eatonii Baker Leaf − Sundue (2009) " Cryptogramma cripsa (L.) R. Br. ex Hook. Leaf − Sundue (2009) " Doryopteris ludens (Wall ex Hook.) J. Sm. Leaf − Sundue (2009) " Doryopteris sagittifolia J. Sm. Whole plant + N Chauhan et al. (2009), Sundue (2009) " Eriosorus hispidulus (Kunze) Vareschi Leaf − Sundue (2009) " Haplopteris anguste-elongata Hay Leaf + D Sundue (2009) " Haplopteris elongata (Sw.) E.H. Crane Leaf + D Sundue (2009) " Haplopteris ensiformis Sw. Leaf + D Sundue (2009) " Haplopteris flexuosa Fée Leaf + D Sundue (2009) " Haplopteris forestiana Ching Leaf + D Sundue (2009) " Haplopteris zosterifolia Willd. Leaf + D Sundue (2009) " Hecistopteris pumila (Spreng.) J. Sm. Leaf + D Sundue (2009) " Hemionitis arifolia (Burm.) Moore. Whole plant + N Chauhan et al. (2009), Sundue (2009) " Hemionitis rufa (L.) Sw. Leaf − Sundue (2009) " verticalis Kunze Leaf − Sundue (2009) " Llavea cordifolia Lag. Leaf − Sundue (2009) " Mildella intramarginalis (Kaulf. ex Link) Leaf + D Sundue (2009) Trevis. " Monogramma graminea (Poir.) Leaf + D Sundue (2009) " Monogramma paradoxa (Fée) Leaf + D Sundue (2009) " Neurocalis praestantissima Bory ex Fée Leaf − Sundue (2009) " Onychium japonicum Blume Leaf + D Sundue (2009) " Onychium siliculosum (Desv.) C. Chr. Leaf + D Sundue (2009) " Pentagramma triangularis (Kaulf.) Yatsk., Leaf − Sundue (2009) Windham and E.Wollenw. " Pityrogramma austroamericana Domin Leaf + D Sundue (2009) " Pityrogramma calomelanos (L.) Link Leaf + D Sundue (2009) " Pityrogramma ebenea (L.) Proctor Leaf + D Sundue (2009) " Pityrogramma trifoliata (L.) R.M. Tryon Leaf + D Sundue (2009) (continued on next page) 16 J. Mazumdar / South African Journal of Botany 77 (2011) 10–19

Table 1 (continued) Family Species Studied Occurrence Status References plant parts " Platyzoma microphyllum R. Br. Leaf − Sundue (2009) " Polytaenium cajenense (Desv.) Spreng. Leaf + D Sundue (2009) " Polytaenium chlorosporum (Mickel and Beitel) Leaf + D Sundue (2009) E.H.Crane " Polytaenium guayanense (Hieron.) Alston Leaf + D Sundue (2009) " Polytaenium lanceolatum (L.) Desv. Leaf + D Sundue (2009) " Polytaenium lineatum (Sw.) J. Sm. Leaf − Sundue (2009) " Polytaenium urbanii (Brause) Alain Leaf + D Sundue (2009) " Pteris arborea L. Leaf − Sundue (2009) " Pteris argyraea T. Moore Leaf − Sundue (2009) " Pteris mulitifida Poir. Leaf + D Sundue (2009) " Pteris propinqua J. Agardh Leaf − Sundue (2009) " Pteris quadriaurita Retz. Leaf − Sundue (2009) " Pteris ryukyuensis Tagawa Leaf + D Sundue (2009) " Pteris tremula R. Br. Leaf − Sundue (2009) " Pteris vittata L. Whole plant + D Chauhan et al. (2009), Sundue (2009) " Pterozonium brevifrons (A.C. Sm.) Lellinger Leaf + D Sundue (2009) " Radiovittaria gardneriana (Fée) E.H. Crane Leaf + D Sundue (2009) " Radiovittaria minima (Benedict) E.H. Crane Leaf + D Sundue (2009) " Radiovittaria remota (Fée) E.H. Crane Leaf + D Sundue (2009) " Scoliosorus ensiformis (Hook.) T. Moore Leaf + D Sundue (2009) " Vittaria amboinensis Fee Leaf + D Mazumdar and Mukhopadhyay (2010) " Vittaria carcina Christ. Leaf + D Mazumdar and Mukhopadhyay (2010) " Vittaria elongata Sw. Leaf + D Mazumdar and Mukhopadhyay (2010) " Vittaria flavicosta Mickel and Bietel Leaf + D Sundue (2009) " Vittaria graminifolia Kaulf. Leaf + D Sundue (2009) " Vittaria himalayensis Ching Leaf + D Mazumdar and Mukhopadhyay (2010) " Vittaria isoetifolia Bory Leaf + D Sundue (2009) " Vittaria lineata (L.) J.E. Sm. Leaf + D Sundue (2009) " Vittaria sikkimensis Kuhn Leaf + D Mazumdar and Mukhopadhyay (2010b) " Vittaria zosterifolia Willd. Leaf + D Mazumdar and Mukhopadhyay (2010) Aspleniaceae Not studied Woodsiaceae Athyrium nigripes (Bl.) Moore Leaf + M Mazumdar and Mukhopadhyay (2010) " Diplazium esculentum (Retz.) Sw. Leaf + M Mazumdar and Mukhopadhyay (2010) Thelypteridaceae Ampelopteris prolifera (Retz.) Copel. Leaf + M Mazumdar and Mukhopadhyay (2010) " Christella dentata (Forssk.) Brownsey and Leaf + M Mazumdar and Mukhopadhyay (2010) Jermy " Cyclosorus interruptus (Willd.) H. Itô Leaf + M Mazumdar and Mukhopadhyay (2010) " Pronephrium nudatum (Roxb. ex Griff.) Holtt. Leaf + M Mazumdar and Mukhopadhyay (2010) " Pseudocyclosorus tylodes (Kunze) Ching Leaf + M Mazumdar and Mukhopadhyay (2010) " Pseudophegopteris pyrrhorhachis var. glabrata Leaf + M Mazumdar and Mukhopadhyay (2010) (Clarke) Holtt. Blechnaceae Blechnum orientale L. Leaf + D Mazumdar and Mukhopadhyay (2010),Author (unpublished) Onocleaceae Not studied Dryopteridaceae Leucostegia immersa (Wall. ex Hook.) Presl Leaf + M Mazumdar and Mukhopadhyay (2010) Peranema cyatheoides D. Don Leaf + M Mazumdar and Mukhopadhyay (2010) Polystichum squarrosum (D. Don) Fee Leaf + M Mazumdar and Mukhopadhyay (2010) Lomariopsidaceae Not studied Tectariaceae Not studied Oleandraceae Oleandra wallichi (Hook.) Pr. Leaf + M Mazumdar and Mukhopadhyay (2010) Davalliaceae Not studied *Polypodiaceae Arthromeris wallichiana (Spreng.) Ching Leaf + M Mazumdar and Mukhopadhyay (2010) Drynaria quercifolia (L.) J. Sm. Whole plant + M Chauhan et al. (2009) Phymatopteris griffithiana Pic. Ser. Leaf + M Mazumdar and Mukhopadhyay (2010) Systematic positions of families and species of ferns were adapted from Smith et al. (2006). Abbreviations: + = phytoliths present, − = phytoliths absent, D = phytoliths diagnostic, M = phytoliths might be diagnostic but require further study, N = phytoliths not diagnostic, * = name of the species not mentioned in available literature.

with dense arrangement of silica spheres, and a loose Some studies provided insight into the mechanism of bio- arrangement of silica particles was found beneath this, silicification and its regulation. Hydrated amorphous silica is a suggesting the agglomeration of silica (Holzhüter et al., 2003). colloidal mineral that aggregate (polycondensates) into various J. Mazumdar / South African Journal of Botany 77 (2011) 10–19 17

Table 2 Features of diagnostic phytoliths. Taxa Features Plant parts Diagnostic at References Huperzia selago (L.) Bernh. ex Smooth or granular plates Aerial branch Species level Mazumdar and Mukhopadhyay (2009b), Schrank and Mart. (Lycopodiaceae) with projecting margins (Fig. 1A) Author (unpublished) Selaginellaceae Elongated epidermal bodies with small Leaf Family level cf. Piperno (2006), Chauhan et al. (2009), cone like projections (Fig. 1E) Mazumdar and Mukhopadhyay (2009b) Isöetes weberi Herter (Isoetaceae) Epidermal cells like angular, Leaf Species level Iriarte and Paz (2009) polyhedral bodies Ophioglossum reticulatum L. Epidermal plates with smooth Leaf Species level Mazumdar and Mukhopadhyay (2010), (Ophioglossaceae) surface and sinuate margins Author (unpublished) Equisetaceae Smooth or granular epidermal plates with Leaf, stem Family level cf. Piperno (2006), Mazumdar and elevated projections along the edges Mukhopadhyay (2010) (Fig. 1D) Equisetum diffusum D. Don Nearly rectangular granular epidermal Leaf, stem Species level Mazumdar and Mukhopadhyay (2010) (Equisetaceae) plates with dentate margins (Fig. 1D) Hymenophyllaceae Roughly bowl-shaped Leaf Family level cf. Piperno (2006) Adiantoid clade (Pteridaceae) Elliptical shape, tapered ends and Leaf Clade level Sundue (2009), Chauhan et al. (2009), undulate sides (Fig. 1C) Mazumdar and Mukhopadhyay (2010) Pteridoid clade (Pteridaceae) Blunt ends and sides that are smooth, Leaf Clade level Sundue (2009), Chauhan et al. (2009) denticulate sparsely denticulate or shallowly lobed Blechnum orientale L. (Blechnaceae) Elongated epidermal plates with smooth Leaf Species level Mazumdar and Mukhopadhyay (2010), surface and lobed margins (Fig. 1B) Author (unpublished) Polypodiaceae Elongated flat base and a surface with two Leaf Family level cf. Piperno (2006) undulating ridges parallel to each other

microscopic and macroscopic forms. containing biosilica ceae, Culcitaceae, Plagiogyriaceae, Cibotiaceae, Dicksoniaceae, extracts from E. telmateia was found to influence the kinetics of Metaxyaceae, Saccolomataceae, Aspleniaceae, Onocleaceae, silica formation and structure (Perry and Keeling-Tucker, 2003). Lomariopsidaceae, Tectariaceae, and Davalliaceae) and less The close association of silica with polymers suggests sampling was made in 20 families (Lycopodiaceae, Selaginella- that they may act as a polymeric template that controls the shape ceae, Isoetaceae, Ophioglossaceae, Equisetaceae, Marattiaceae, and size of the colloidal silica particles (Sapei et al., 2007). Hymenophyllaceae, Gleicheniaceae, Lygodiaceae, Marsileaceae, Gierlinger et al. (2008) suggested the roles of and Salviniaceae, Cyatheaceae, Lindsaeaceae, Dennstaedtiaceae, in silica deposition in E. hyemale. Woodsiaceae, Thelypteridaceae, Blechnaceae, Dryopteridaceae, Currie and Perry (2009) found the association of silicon with Oleandraceae, and Polypodiaceae). soluble carbohydrate and proteinaceous components in cell Also, leaves were extensively studied (in 181 species) than walls of E. arvense and suggested the possible role of silicon in other parts like aerial branches (in 11 species), (in 11 cross-linking the cell wall polymers, thereby providing a species) and roots or whole plants (in 15 species). Epidermal modest improvement in rigidity or stability of the cell wall phytoliths were found to be more useful as diagnostic characters against biotic and abiotic stresses. in all investigations. However, Chauhan et al. (2009) noted silicified hairs in Cyathea gigentea, silicified hair bases in 5. Conclusion Lygodium flexuosum, silicified in Actiniopteris australis, etc. But, taxonomic utility of these phytoliths require Phytoliths of pteridophytes can provide important insights further investigations. into past vegetations (Piperno, 2006). Table 1 showed that 225 Phytoliths are also important for normal growth and survival pteridophytic species have been studied and phytoliths were of pteridophytes as exemplified by works on some species of detected in 168 species. In 168 species studied, phytoliths were Equisetum. Experimental works with pteridophytes will diagnostic in 121 species, might be diagnostic in 34 species and elucidate the mechanism by which plants uptake silica from not diagnostic in 13 species. So, Table 1 indicated that soil, deposit in distinct layers and regulate the formation of phytoliths in pteridophytes have immense probability to be silica micro and macro structures. It might be helpful in useful as taxonomic tools in future for delineation of family generation of new materials with specific form and function for (e.g., Polypodiaceae), genus (e.g., Equisetum) and species (e.g., industrial application (Perry and Keeling-Tucker, 2003) and Isöetes weberi) (other examples in Table 2) and also for also in nanotechnology (Neethirajan et al., 2009). phylogenetic analysis (e.g., Pteridaceae). As shown in Table 1 only Pteridaceae is the more studied Acknowledgements family than others. No investigations were conducted in 19 families (Psilotaceae, Osmundaceae, Dipteridaceae, Matonia- I express my sincere thanks to Dr. J. Manning, Review Board ceae, Anemiaceae, Schizaeaceae, Thyrsopteridaceae, Loxomata- Editor, South African Journal of Botany and reviewers for 18 J. Mazumdar / South African Journal of Botany 77 (2011) 10–19 reviewing and improving the quality of manuscript. 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Edited by JC Manning