Phytoliths of pteridophytes

South African Journal of Botany 77 (2011) 10 – 19

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Phytoliths of pteridophytes J. Mazumdar UGC Centre for Advanced Study, Department of Botany, The University of Burdwan, Burdwan-713104, India 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; Ferns; Pteridophytes; Phytolith; Silicification

1. Introduction Many plants deposit silica as solid hydrated Silicone dioxide (SiO2, nH2O) in the cell lumen or in intercellular spaces, where it is known as “phytoliths” or “plant stones” (Greek, phyto = plant, lithos = stone) or “silicophytoliths” or “opal phytoliths” or “plant opal” or “opaline silica” or “biogenic silica” or “bioliths”. The term “phytolith” may also be applied to other mineral 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 migrate through it to the same extent as do other microfossils, such as pollen and diatoms (Prychid et al., 2004). Many plants produce phytoliths with characteristic, distinguishable shapes, and which are known accordingly as “diagnostic” phytoliths. Diagnostic phytoliths recovered from soil provide valuable information about the identity and possibly concentration of source plant species, and are useful for the reconstruction of palaeoenvironments, investigation of ancient agricultural practices, study of crop plant evolution, monitoring vegetation and climate change, radiometric dating, identification of drug plants, crop processing (Harvey and Fuller, 2005), forensic investigations, indicator of diets of ancient animals (more discussion in Prychild et al., 2004; Piperno, 2006 and citations therein), and recently for nanotechnology (Neethirajan et al., 2009).

E-mail address: [email protected].

In spite of environmental effects on silica uptake, ongoing investigations indicate that phytolith formation is primarily under genetic control (Piperno, 2006). Phytoliths have been used successfully as taxonomic tools in angiosperms, especially in monocots (Piperno, 1988; Tubb et al., 1993). Less information is available about pteridophytic phytoliths. The objective of this review is to evaluate the present status and future prospects of phytolith research in pteridophytes.

2. Phytoliths in pteridophytes The umbrella terms “pteridophytes” and “ferns and fern allies” were used to denote a group of spore bearing, seed-less vascular plants that demonstrated many aspects of early evolution of land plants and undergone considerable taxonomic treatments. Based on morphological and molecular data “Lycopods” or “Lycopsids”, previously placed in fern allies are now separated as clade “Lycophytes” sister to all other land plants and “Whisk ferns” and “Horsetail”, also previously considered under fern allies are now included within “Ferns” or “Monilophytes” or “Moniloformopses” (cf. Smith et al., 2006). In a recent treatment Chase and Reveal (2009) recognized “Lycophytes” as Subclass Lycopodiidae Beketov and placed 5 subclasses — Subclass Equisetidae Warm., Subclass Marattiidae Klinge, Subclass Ophioglossidae Klinge, Subclass Polypodiidae Cronquist, and Subclass Psilotidae Reveal under “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

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Fig. 1. Phyoliths of Huperzia selago (A), Blechnum orientale (B), Vittaria himalayaensis (C), Equisetum diffusum (D) and Selaginella bryopteris (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 of Ferns and Lycophytes. Davy (1814) was one of the first to investigate the form of silica in plants, including the epidermis of Equisetum, and Mettenius (1864) coined the terms “Deckzellen” (cover cells) or “Stegmata” (from the Greek stegium, a roof or covering) for cells that contain inclusions and lie over sclerenchyma in ferns; these cells contained calcium oxalate crystals in Cyatheaceae, silica concretions in Dryopteris and true stegmata (cells containing silica bodies) in most Trichomanes species (cf. Prychid et al., 2004). In pteridophytes silica bodies in different plant parts have been observed by several authors, including Mettenius (1864), Pant and Srivastava (1961), Kaufman et al. (1971), Dengler and Lin (1980), Parry et al. (1985), Rolleri et al. (1987), Piperno (1988), Le Coq et al. (1991), Lanning and Eleuterius (1994), Stevenson and Loconte (1996), Thorn (2006) and others (cited by Sundue, 2009). However, distinguishable forms or “diagnostic” forms of silica bodies or phytoliths, useful for delineation of family, genus or species are known for only few taxa (Table 2). Mazumdar and Mukhopadhyay (2009a,b, 2010) surveyed 47 species of pteridophytes and suggested that phytoliths could be useful for taxonomic purposes as some plate or sheet-like phytoliths show distinct features in different species. Using scanning electron microscope Page (1972) made detailed observations on surface micromorphology of silicified aerial shoots of Equisetum and proposed three sections under Subgenus Equisetum — Section I: Equisetum sect. nov. (contains E. fluviatile and E. arvense), Section 2: Subvernalia A.Br. (contains E. pratense and E. sylvaticum) and Section 3: Palustria sect. nov. (contains E. bogotense, E . diffusum, E. palustre and E. telmateia) on the basis of variability of shape, size and distribution of pilulae (bead like projections), mamillae (rounded or conical projections) and stomatal cell area (paired cells around each stomatal pore). He also noted variations

among silica deposition patterns in Subgenus Hippochaete (smooth or amorphous type depositions) and Sebgenus Equisetum (granular type depositions). But, Hauke (1974) considered that the available information was insufficient to formulate a sectional classification of the subgenus Equisetum (cf. Guillon, 2004) and this treatment was not accepted widely. However, variations in surface micromorphological features among different species of Equisetum indicated their possible use for identification at species level. Filippini et al. (1995) utilized micromorphological features like, size of mamillae and pilulae distribution over the surface of stomata for identification of E. arvense in finely powdered form of commercially available drug Herba equiseti. Sundue (2009) studied epidermal phytoliths from leaves of ferns belonging to Family Pteridaceae sensu Schuettpelz et al. (2007). The occurrence of phytoliths were found to be a potential synapomorphy for the adiantoid clade, several smaller clades of pteridoid clade, including Pityrogramma and the sister group of Actiniopteris and Onychium. Phytoliths were not found in Ceratopteridoid or cryptogrammatoid clades. But phytoliths were diagnostic in adiantoid and pteridoid clades (Table 2) and diverse in cheilanthoid clade, reflecting independent origins of these major lineages. This study also indicated that phytoliths were evolved once in adiantoid and twice in pteridoid clades. But this analysis was scored by two characters (presence/ absence and location of phytoliths) and use of morphological features like shape, margin, and surface ornamentations of phytoliths might provide better resolution of interrelationships of clades. Although this study reported the absence of phytoliths in Pteris vittata, they were found in lamina and vein area in pinnule by Chauhan et al. (2009). Also, more sampling is required for Ceratopteridoid and cryptogrammatoid ferns to confirm the absence of phytoliths in these clades. For extraction of phytoliths from plant tissues Chauhan et al. (2009) used dry ashing method in which samples were heated in

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J. Mazumdar / South African Journal of Botany 77 (2011) 10–19

muffle furnace at 500–600 °C for 4–6 h, then digested with nitric acid (HNO3), washed with distilled water, dried and mounted in Canada balsam. Mazumdar and Mukhopadhyay (2009a,b, 2010) used modified wet oxidation method of Piperno (2006) in which plant materials were digested with concentrated HNO3 (instead of potassium chlorate + HNO3) in water bath, boiled with 10% hydrochloric acid (HCl) to remove calcium, washed with distilled water, dried with acetone and mounted in 10% glycerine. Sundue (2009) used wet oxidation method of Piperno (1988) in which materials were digested with sulfuric acid (H2SO4) and chromic trioxide or hydrogen peroxide (H2O2). He also visualized epidermal phytoliths of leaf lamina at 60× magnification in dissection microscope. Kao et al. (2008) found partial polarization light microscopy technique and cryo-tabletop-scanning electron microscopy technique useful for direct visualization of Spicular cells or venuloid idioblasts (long and silica containing epidermal cells) in lamina of Pteris grevilleana. For confirming chemical nature of silica bodies they successfully utilized silica specific dyes Silver-ammine chromate, Crystal Violet Lactone and Methyl Red (developed by Dayanandan et al., 1983) and energy dispersive X-ray spectrometer. 3. Biological significance of phytoliths The occurrence of silicon (Si) within the plant is a result of its uptake, in the form of soluble Si(OH)4 or Si(OH)3O2, from the soil and its controlled polymerization at a final location (Currie and Perry, 2007). The occurrence of silicon as silica bodies or phytolith in many plants has been correlated with mechanical support (Kaufman et al., 1973), reduction of water loss (Gao et al., 2004), protection from herbivores (Vicari and Bazely, 1993), prevention of entry of pathogens (Nanda and Gangopadhyay, 1984), protection from metal toxicity (Hodson and Evans, 1995), root elongation (Hattori et al., 2003), increased capture of light for photosynthesis (Yoshida et al., 1959), and in cooling of leaves (Wang et al., 2005). Recent findings indicate that silicon protects the plants from various biotic and abiotic stresses by enhancing the production of enzymes and various compounds (like, chitinases, peroxidases, polyphenol oxidases, flavonoid phytoalexins, etc) related to stress resistance, but the detailed mechanism has yet to be fully elucidated (cf. Currie and Perry, 2007). Chen and Lewin (1969) found that silicon is an essential element for the healthy growth of E. arvense and silicon deficient plants showed symptoms like necrosis of the branch tips, wilting or drooping of the branches. In vitro study with E. hyemale by Hoffman and Hillson (1979) indicated that silicon is a required nutrient for spore viability and essential for completion of the life cycle of this plant. Developmental studies also indicated the importance of silicification in mechanical strengthening (Kaufman et al., 1973) and in negative geotropism (Srinivasan et al., 1979) in E. hyemale var. affine. However, evolutionary advantages offered by silicon deposited as silica are still not clearly understood. Chauhan et al. (2009) observed silica deposition of biological origin in

different parts of 14 species of pteridophytes (Lycopodium japonicum, Selaginella bryopteris, Actiniopteris australis, Adiantum caudatum, A. phillippense, A. peruvianum, A. venustum, Cyathea gigentea, Doryopteris sagittifolia, Drynaria quercifolia, Gleichenia microphylla, Hemionitis arifolia, Lygodium flexuosum and Pteris vittata) and proposed that the presence of silica in the early land plants suggests that the mechanism of silica absorption and accumulation was developed early in the evolution of terrestrial vegetation, because silica was important for the survival of terrestrial life as it gave mechanical stability of tissues, protection against fungi and pests, and resistance against drought by checking evaporation. In general, however, Silicon concentration in shoots is shown to have declined among land plants in the sequence liverworts N horsetails N clubmosses N mosses N angiosperms N gymnosperms N ferns, and relative shoot Silicon concentrations were, in general, low in angiosperms, gymnosperms and ferns (Hodson et al., 2005). 4. Experimental works on silica with pteridophytes Experimental works with some pteridophytes can provide important insight into the mechanisms by which plants accumulate and deposit silica in various organs. Soluble silica, the raw material for phytolith production, is absorbed as monosilicic or orthosilicic acid [Si(OH)4] from the soil through roots. Different plant species show different modes of silica uptake, notably active, passive or rejective, through low affinity transporter, etc (cf. Currie and Perry, 2007). Fu et al. (2002) documented a novel mechanism of obtaining nutrients and accelerating the weathering of soil minerals in fern Matteuccia. This fern may physically incorporate silicate mineral particles into the root cortex, dissolve inorganic nutrients from the silicate minerals to leave silica particles in the cortex nearly in pure form. Further investigation is required for proper understanding about the silica uptake process in other pteridophytes. Equisetum accumulate high amounts of silica in their plant body and have been used as a model system for understanding silica deposition (bio-silicification) and the ultra-structure of silicified layers in plants. Various techniques such as Electron microprobe analysis by Kaufman et al. (1971), scanning and transmission electron microscopy by Perry and Fraser (1991) and Holzhüter et al. (2003), microtomography, energy dispersive X-ray elemental mapping, small-angle and wide-angle scattering of X-rays by Sapei et al. (2007) and Raman microscopy by Sapei et al. (2007) and Gierlinger et al. (2008) have been used to elucidate ultra-structure details of silicified layers. Kaufman et al. (1971) observed that Silica was deposited primarily in discrete knobs and rosettes on the epidermal surface in E. arvense, but essentially in a uniform pattern on and in the entire outer epidermal cell walls of E. hyemale var. affine. In E. arvense the surface micromorphology was found to be very complex and principally fibrillar, globular and sheet-like ultra-structural motifs of silica were found by Perry and Fraser (1991). Silica was present as a thin layer on the outer surface

J. Mazumdar / South African Journal of Botany 77 (2011) 10–19

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Table 1 List of pteridophytes studied for phytoliths. Family

Species

Studied plant parts

Lycopodiaceae

Lycopodium clavatum L.

Whole plant +

"

L. japonicum Thunb.

" " Selaginellaceae " " " " " " " " Isoetaceae " Ophioglossaceae " " Psilotaceae Equisetaceae Marattiaceae Osmundaceae Hymenophyllaceae Gleicheniaceae

Dipteridaceae Matoniaceae Lygodiaceae Anemiaceae Schizaeaceae Marsileaceae " Salviniaceae " Thyrsopteridaceae Loxomataceae Culcitaceae Plagiogyriaceae Cibotiaceae Cyatheaceae " Dicksoniaceae Metaxyaceae Lindsaeaceae " Saccolomataceae Dennstaedtiaceae Pteridaceae " " " "

Aerial branch Palhinhaea cernua (L.) Franco and Vasc. Aerial branch Huperzia selago (L.) Bernh. ex Schrank and Aerial Mart. branch Selaginella bryopteris (L.) Bak. Whole plant Selaginella inaequalifolia (Hook. and Grev.) Spring Selaginella involvens (Sw.) Spring Selaginella monospora Spring Selaginella pentagona Spring Selaginella plana (Desv. ex Poir.) Hieron. Selaginella tenera (Hook. and Grev.) Spring Selaginella chrysocaulos (Hook. and Grev.) Spring Selaginella velutina A.R. Smith Isöetes coromandelina L. Isöetes weberi Herter Botrychium virginianum (L.) Sw. Helminthostachys zeylanica (L.) Hook. Ophioglossum reticulatum L. Not studied Equisetum diffusum D. Don Angiopteris evecta (Forst.) Hoffm. Not studied *Hymenophyllum sp. *Trichomanes sp. Dicranopteris linearis (Burm. f.) Und. Gleichenia gigantea Wall. ex Hook. Gleichenia microphylla R. Br. Not studied Not studied Lygodium flexuosum (L.) Sw. Not studied Not studied Marsilea ancylopoda A. Braun Marsilea minuta L. Azolla pinnata R. Br. Salvinia molesta Mitch. Not studied Not studied Not studied Not studied Not studied Cyathea gigentea (Wall. ex Hook.) Holtt. Cyathea spinulosa Wall. ex Hook. Not studied Not studied Lindsaea odorata Roxb. Sphenomeris chinensis (L.) Maxon Not studied Hypolepis punctata (Thunb.) Mett. ex Kuhn Acrostichum danaeifolium Langsd. and Fisch Actiniopteris australis Link Adiantopsis radiata (L.) Fée Adiantum abscissum Schrad. Adiantum adiantoides (J. Sm.) C. Chr.

Occurrence Status References M

Chauhan et al. (2009), Mazumdar and Mukhopadhyay (2009b) Mazumdar and Mukhopadhyay (2009b)

+

N

+

M

+

D

+

D

Aerial shoot +

M

Chauhan et al. (2009), Mazumdar and Mukhopadhyay (2009b), Author (unpublished) Mazumdar and Mukhopadhyay (2009b),

Aerial shoot Aerial shoot Aerial shoot Aerial shoot Aerial shoot Aerial shoot

+ + + + + +

N N M N M N

Mazumdar and Mukhopadhyay (2009b) Mazumdar and Mukhopadhyay (2009b) Mazumdar and Mukhopadhyay (2009b) Mazumdar and Mukhopadhyay (2009b) Mazumdar and Mukhopadhyay (2009b) Mazumdar and Mukhopadhyay (2009b)

Leaf Leaf Leaf Leaf, spike Leaf Leaf

+ + + + + +

D M D M M D

cf. Piperno (2006) Mazumdar and Mukhopadhyay (2009b) Iriarte and Paz (2009) Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010), Author (unpublished)

Leaf, stem Leaf

+ +

D M

cf. Piperno (2006), Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010)

Leaf Leaf Leaf Leaf Whole plant

− + + + +

D M M M

cf. Piperno (2006) cf. Piperno (2006) Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010) Chauhan et al. (2009)

Whole plant +

M

Chauhan et al. (2009)

Leaf Leaf Whole plant Leaf

+ + + +

N M M N

Iriarte and Paz (2009) Author (unpublished) Author (unpublished) Author (unpublished)

Whole plant + Leaf +

N M

Chauhan et al. (2009) Mazumdar and Mukhopadhyay (2010)

Leaf Leaf

+ +

M M

Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010)

Leaf Leaf Whole plant Leaf Leaf Leaf

+ − + − + +

M

Mazumdar and Mukhopadhyay (2010) Sundue (2009) Chauhan et al. (2009), Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009)

D D D

Mazumdar and Mukhopadhyay (2009b), Author (unpublished) Mazumdar and Mukhopadhyay (2009b)

(continued on next page)

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Table 1 (continued) Family

Species

Studied plant parts

Occurrence Status References

" " " " " " " "

Adiantum andicola Liebm. Adiantum argutum Splitg. Adiantum cajennense Willd. Adiantum capillus-junonis Rupr. Adiantum capillus-veneris L. Adiantum caryotideum H. Christ Adiantum caudatum L. Adiantum concinnum Humb. and Bonpl. ex Willd. Adiantum cordatum Maxon Adiantum delicatulum Mart. Adiantum delicatulum Hook Adiantum dolosum Kunze Adiantum formosum R. Br. Adiantum fructuosum Poepp. ex Spreng. Adiantum glaucescens Klotzsch Adiantum hispidulum Sw. Adiantum humile Kunze Adiantum incertum Lindman Adiantum intermedium Sw. Adiantum jordanii C.H. Mull Adiantum kaulfusii Kunze Adiantum kendalii Jenman Adiantum krameri B. Zimmer Adiantum latifolium Lam. Adiantum leprieurii Hook. Adiantum lucidum (Cav.) Spreng. Adiantum lunulatum Burm.f. Adiantum macrophyllum Sw. Adiantum malesianum J. Ghatak Adiantum mcvaughii Mickel and Beitel Adiantum multisorum Sampaio Adiantum oaxacanum Mickel and Beitel Adiantum obliquum Desv. Adiantum paraense Hieron. Adiantum patens Willd. Adiantum peruvianum Klotzsch Adiantum petiolatum Desv. Adiantum phillippense L. Adiantum phyllitidis J. Sm. Adiantum platyphyllum Sw. Adiantum poeppigianum (Kuhn) Hieron. Adiantum poiretii Wikstr. Adiantum polyphyllum Willd. Adiantum pulverulentum L. Adiantum pyramidale (L.) Willd. Adiantum raddianum C. Presl Adiantum reniforme L. Adiantum scalare R.M. Tryon Adiantum seemanii Hook. Adiantum serratodentatum Willd. Adiantum tenerum Sw. Adiantum terminatum Kunze ex Miq. Adiantum tetraphyllum Humb. and Bonpl. ex Willd. Adiantum tomentosum Klotzsch Adiantum trapeziforme L. Adiantum trichochlaenum Mickel and Beitel Adiantum tricholepis Fée Adiantum venustum D. Don Adiantum villosissimum Kuhn Adiantum villosum L. Adiantum vogellii Mett. ex Keys Adiantum wilsonii Hook.

Leaf Leaf Leaf Leaf Leaf Leaf Whole plant Leaf

+ + + + + + + +

D D D D D D D D

Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Chauhan et al. (2009), Sundue (2009) Sundue (2009)

Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Whole plant Leaf Whole plant Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf

+ + − + + + + + + + + − + + + + + + + + + + + + + + + + + + + + + − + + + + − + + + + + +

D D

D D D D D D D D D D D D D D D D D D D D D

D D D D D D

Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Chauhan et al. (2009), Sundue (2009) Sundue (2009) Chauhan et al. (2009), Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009)

Leaf Leaf Leaf Leaf Whole plant Leaf Leaf Leaf Leaf

+ + + + + + + + +

D D D D D D D D D

Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Chauhan et al. (2009), Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009)

"

" " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " "

D D D D D D D D

D D D D

J. Mazumdar / South African Journal of Botany 77 (2011) 10–19

15

Table 1 (continued) Family

Species

Studied plant parts

Occurrence Status References

" " " " "

Afropteris repens Alston Aleuritopteris argentea (S.G.Gmel.) Fée Aleuritopteris aurantiacea (Cav.) Ching Aleuritopteris farinosa (Forssk.) Fée Ananthacorus angustifolius (Sw.) Underw. and Maxon Anetium citrifolium (L.) Splitg. Anogramma leptophylla (L.) Link Anopteris hexagona (L.) C. Chr. Antrophyum boryanum (Willd.) Spreng. Antrophyum callifolium Blume Antrophyum latifolium Bl. Antrophyum lineatum (Sw.) Kaulf. Antrophyum mannianum Hook. Antrophyum minersum Bory Antrophyum plantagineum Cav. Antrophyum reticulatum (Forst.) Kaulf. Antryophum brasilianum (Desv.) C. Chr. Antryophym obovatum Baker Argyrochosma limitanea (Maxon) Windham Aspidotis californica (Hook.) Nutt. ex Copel. Aspidotis densa (Brack) Lellinger Astrolepis sinuata (Lag. ex Sw.) D.M. Benham and Windham Austrogramme decipiens (Mett.) Hennipman Bommeria hispida (Mett. ex Kuhn) Underw. Ceratopteris pteridoides (Hook.) Hieron. Ceratopteris richardii Brongn. Cheilanthes alabamensis (Buckley) Kunze Cheilanthes albomarginata Clarke Cheilanthes angustifolia Kunth Cheilanthes cuneata Kaulf. ex Link Cheilanthes decomposita (M. Martens and Galeotti) Fée Cheilanthes eatonii Baker Cryptogramma cripsa (L.) R. Br. ex Hook. Doryopteris ludens (Wall ex Hook.) J. Sm. Doryopteris sagittifolia J. Sm. Eriosorus hispidulus (Kunze) Vareschi Haplopteris anguste-elongata Hay Haplopteris elongata (Sw.) E.H. Crane Haplopteris ensiformis Sw. Haplopteris flexuosa Fée Haplopteris forestiana Ching Haplopteris zosterifolia Willd. Hecistopteris pumila (Spreng.) J. Sm. Hemionitis arifolia (Burm.) Moore. Hemionitis rufa (L.) Sw. Jamesonia verticalis Kunze Llavea cordifolia Lag. Mildella intramarginalis (Kaulf. ex Link) Trevis. Monogramma graminea (Poir.) Monogramma paradoxa (Fée) Neurocalis praestantissima Bory ex Fée Onychium japonicum Blume Onychium siliculosum (Desv.) C. Chr. Pentagramma triangularis (Kaulf.) Yatsk., Windham and E.Wollenw. Pityrogramma austroamericana Domin Pityrogramma calomelanos (L.) Link Pityrogramma ebenea (L.) Proctor Pityrogramma trifoliata (L.) R.M. Tryon

Leaf Leaf Leaf Leaf Leaf

+ − − − +

D

Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf

+ − − + + + + + + + + + + − + + −

D

Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf

− − − − − + − − −

Leaf Leaf Leaf Whole plant Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Whole plant Leaf Leaf Leaf Leaf

− − − + − + + + + + + + + − − − +

Leaf Leaf Leaf Leaf Leaf Leaf

+ + − + + −

Leaf Leaf Leaf Leaf

+ + + +

" " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " " "

D

D D D D D D D D D D N N

N

N D D D D D D D N

D D D D D

D D D D

Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009), Mazumdar and Mukhopadhyay (2010) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009), Mazumdar and Mukhopadhyay (2010) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Chauhan et al. (2009), Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Chauhan et al. (2009), Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) (continued on next page)

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Table 1 (continued) Family

Species

Studied plant parts

Occurrence Status References

" " "

Platyzoma microphyllum R. Br. Polytaenium cajenense (Desv.) Spreng. Polytaenium chlorosporum (Mickel and Beitel) E.H.Crane Polytaenium guayanense (Hieron.) Alston Polytaenium lanceolatum (L.) Desv. Polytaenium lineatum (Sw.) J. Sm. Polytaenium urbanii (Brause) Alain Pteris arborea L. Pteris argyraea T. Moore Pteris mulitifida Poir. Pteris propinqua J. Agardh Pteris quadriaurita Retz. Pteris ryukyuensis Tagawa Pteris tremula R. Br. Pteris vittata L. Pterozonium brevifrons (A.C. Sm.) Lellinger Radiovittaria gardneriana (Fée) E.H. Crane Radiovittaria minima (Benedict) E.H. Crane Radiovittaria remota (Fée) E.H. Crane Scoliosorus ensiformis (Hook.) T. Moore Vittaria amboinensis Fee Vittaria carcina Christ. Vittaria elongata Sw. Vittaria flavicosta Mickel and Bietel Vittaria graminifolia Kaulf. Vittaria himalayensis Ching Vittaria isoetifolia Bory Vittaria lineata (L.) J.E. Sm. Vittaria sikkimensis Kuhn Vittaria zosterifolia Willd. Not studied Athyrium nigripes (Bl.) Moore Diplazium esculentum (Retz.) Sw. Ampelopteris prolifera (Retz.) Copel. Christella dentata (Forssk.) Brownsey and Jermy Cyclosorus interruptus (Willd.) H. Itô Pronephrium nudatum (Roxb. ex Griff.) Holtt. Pseudocyclosorus tylodes (Kunze) Ching Pseudophegopteris pyrrhorhachis var. glabrata (Clarke) Holtt. Blechnum orientale L.

Leaf Leaf Leaf

− + +

Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Whole plant Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf Leaf

+ + − + − − + − − + − + + + + + + + + + + + + + + + +

D D D D D D D D D D D D D D D D

Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Chauhan et al. (2009), Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Sundue (2009) Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010) Sundue (2009) Sundue (2009) Mazumdar and Mukhopadhyay (2010) Sundue (2009) Sundue (2009) Mazumdar and Mukhopadhyay (2010b) Mazumdar and Mukhopadhyay (2010)

Leaf Leaf Leaf Leaf

+ + + +

M M M M

Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010)

Leaf Leaf Leaf Leaf

+ + + +

M M M M

Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010)

Leaf

+

D

Mazumdar and Mukhopadhyay (2010), Author (unpublished)

Leaf Leaf Leaf

+ + +

M M M

Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010) Mazumdar and Mukhopadhyay (2010)

Leaf

+

M

Mazumdar and Mukhopadhyay (2010)

Leaf + Whole plant + Leaf +

M M M

Mazumdar and Mukhopadhyay (2010) Chauhan et al. (2009) Mazumdar and Mukhopadhyay (2010)

" " " " " " " " " " " " " " " " " " " " " " " " " " " Aspleniaceae Woodsiaceae " Thelypteridaceae " " " " " Blechnaceae Onocleaceae Dryopteridaceae

Lomariopsidaceae Tectariaceae Oleandraceae Davalliaceae *Polypodiaceae

Not studied Leucostegia immersa (Wall. ex Hook.) Presl Peranema cyatheoides D. Don Polystichum squarrosum (D. Don) Fee Not studied Not studied Oleandra wallichi (Hook.) Pr. Not studied Arthromeris wallichiana (Spreng.) Ching Drynaria quercifolia (L.) J. Sm. Phymatopteris griffithiana Pic. Ser.

D D D D D

D

D

Sundue (2009) Sundue (2009) Sundue (2009)

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 arrangement of silica particles was found beneath this, suggesting the agglomeration of silica (Holzhüter et al., 2003).

Some studies provided insight into the mechanism of biosilicification and its regulation. Hydrated amorphous silica is a 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 Schrank and Mart. (Lycopodiaceae) Selaginellaceae

Smooth or granular plates with projecting margins (Fig. 1A) Elongated epidermal bodies with small cone like projections (Fig. 1E) Epidermal cells like angular, polyhedral bodies Epidermal plates with smooth surface and sinuate margins Smooth or granular epidermal plates with elevated projections along the edges (Fig. 1D) Nearly rectangular granular epidermal plates with dentate margins (Fig. 1D) Roughly bowl-shaped Elliptical shape, tapered ends and undulate sides (Fig. 1C) Blunt ends and sides that are smooth, denticulate sparsely denticulate or shallowly lobed Elongated epidermal plates with smooth surface and lobed margins (Fig. 1B) Elongated flat base and a surface with two undulating ridges parallel to each other

Aerial branch

Species level

Leaf

Family level

Leaf

Species level

Mazumdar and Mukhopadhyay (2009b), Author (unpublished) cf. Piperno (2006), Chauhan et al. (2009), Mazumdar and Mukhopadhyay (2009b) Iriarte and Paz (2009)

Leaf

Species level

Leaf, stem

Family level

Leaf, stem

Species level

Mazumdar and Mukhopadhyay (2010)

Leaf Leaf

Family level Clade level

Leaf

Clade level

cf. Piperno (2006) Sundue (2009), Chauhan et al. (2009), Mazumdar and Mukhopadhyay (2010) Sundue (2009), Chauhan et al. (2009)

Leaf

Species level

Leaf

Family level

Isöetes weberi Herter (Isoetaceae) Ophioglossum reticulatum L. (Ophioglossaceae) Equisetaceae

Equisetum diffusum D. Don (Equisetaceae) Hymenophyllaceae Adiantoid clade (Pteridaceae) Pteridoid clade (Pteridaceae)

Blechnum orientale L. (Blechnaceae) Polypodiaceae

microscopic and macroscopic forms. Protein containing biosilica extracts from E. telmateia was found to influence the kinetics of silica formation and structure (Perry and Keeling-Tucker, 2003). The close association of silica with cell wall polymers suggests that they may act as a polymeric template that controls the shape and size of the colloidal silica particles (Sapei et al., 2007). Gierlinger et al. (2008) suggested the roles of pectin and hemicelluloses in silica deposition in E. hyemale. Currie and Perry (2009) found the association of silicon with soluble carbohydrate and proteinaceous components in cell walls of E. arvense and suggested the possible role of silicon in cross-linking the cell wall polymers, thereby providing a modest improvement in rigidity or stability of the cell wall against biotic and abiotic stresses. 5. Conclusion Phytoliths of pteridophytes can provide important insights into past vegetations (Piperno, 2006). Table 1 showed that 225 pteridophytic species have been studied and phytoliths were detected in 168 species. In 168 species studied, phytoliths were diagnostic in 121 species, might be diagnostic in 34 species and not diagnostic in 13 species. So, Table 1 indicated that phytoliths in pteridophytes have immense probability to be useful as taxonomic tools in future for delineation of family (e.g., Polypodiaceae), genus (e.g., Equisetum) and species (e.g., Isöetes weberi) (other examples in Table 2) and also for phylogenetic analysis (e.g., Pteridaceae). As shown in Table 1 only Pteridaceae is the more studied family than others. No investigations were conducted in 19 families (Psilotaceae, Osmundaceae, Dipteridaceae, Matoniaceae, Anemiaceae, Schizaeaceae, Thyrsopteridaceae, Loxomata-

Mazumdar and Mukhopadhyay (2010), Author (unpublished) cf. Piperno (2006), Mazumdar and Mukhopadhyay (2010)

Mazumdar and Mukhopadhyay (2010), Author (unpublished) cf. Piperno (2006)

ceae, Culcitaceae, Plagiogyriaceae, Cibotiaceae, Dicksoniaceae, Metaxyaceae, Saccolomataceae, Aspleniaceae, Onocleaceae, Lomariopsidaceae, Tectariaceae, and Davalliaceae) and less sampling was made in 20 families (Lycopodiaceae, Selaginellaceae, Isoetaceae, Ophioglossaceae, Equisetaceae, Marattiaceae, Hymenophyllaceae, Gleicheniaceae, Lygodiaceae, Marsileaceae, Salviniaceae, Cyatheaceae, Lindsaeaceae, Dennstaedtiaceae, Woodsiaceae, Thelypteridaceae, Blechnaceae, Dryopteridaceae, Oleandraceae, and Polypodiaceae). Also, leaves were extensively studied (in 181 species) than other parts like aerial branches (in 11 species), rhizomes (in 11 species) and roots or whole plants (in 15 species). Epidermal phytoliths were found to be more useful as diagnostic characters in all investigations. However, Chauhan et al. (2009) noted silicified hairs in Cyathea gigentea, silicified hair bases in Lygodium flexuosum, silicified tracheids in Actiniopteris australis, etc. But, taxonomic utility of these phytoliths require further investigations. Phytoliths are also important for normal growth and survival of pteridophytes as exemplified by works on some species of Equisetum. Experimental works with pteridophytes will elucidate the mechanism by which plants uptake silica from soil, deposit in distinct layers and regulate the formation of silica micro and macro structures. It might be helpful in generation of new materials with specific form and function for industrial application (Perry and Keeling-Tucker, 2003) and also in nanotechnology (Neethirajan et al., 2009). Acknowledgements I express my sincere thanks to Dr. J. Manning, Review Board Editor, South African Journal of Botany and reviewers for

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J. Mazumdar / South African Journal of Botany 77 (2011) 10–19

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Edited by JC Manning

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