Systematics and Biology of Silica Bodies in Monocotyledons Author(s): Christina J. Prychid, Paula J.

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The BotanicalReview 69(4): 377-440

Systematics and Biology of Silica Bodies in Monocotyledons

PAULAJ. RUDALL,ANDMARY GREGORY J. PRYCHID, CHRISTINA
Jodrell Laboratory Royal Botanic Gardens Kew, Richmond,Surrey TW93AB, England

................................................... I. Abstract. II. Introduction .................................................... III. Historical Review ................................................. ........................................ IV. Composition of Silica in Plants . V. Techniques................................................. VI. Uptake and Deposition ................................................ VII. Morphology and Location.............................................. VIII. Ecology................................................. IX. Functions . ................................................... X. Applications................................................. A. Soils and Archaeology .............................................. ...................... B. AgriculturalCrops and Their Evolution .......... C. Medical Studies ................................................. D. Animal Diets................................................. E. Other Applications ................................................. XI. Systematic Distribution ................................................ A. Orchidaceae ................................................... B. Commelinids................................................. 1. Arecaceae ................................................... .......... 2. ZHC Clade (Zingiberales, Commelinales and Hanguana) ..... ................................................... 3. Poales . 4. Dasypogonaceae................................................. XII. LiteratureCited .................................................

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I. Abstract
Many plants take up soluble monosilicic acid from the soil. Some of these plants subsestructure. This articledescribesthe distriquentlydeposit it as cell inclusionsof characteristic bution and diversityof opaline silica bodies in monocotyledonsin a phylogeneticframework, togetherwith a review of techniquesused for theirexamination,and the ecology, functionand forms economic applicationsof these cell inclusions.Thereare severaldifferentmorphological of silica in monocot tissues, and the numberof silica bodies per cell may also vary.The most common type is the "druse-like" sphericalbody, of which there is normallya single body per fragmentary cell, more in some cases. Otherforms includethe conical type and an amorphous, type (silica sand). Silica bodies are most commonly found either in the epidermis (e.g., in
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grasses, commelinas and sedges) or in the sheath cells of vascular bundles (e.g., in palms, bananasand orchids). Silica-bearingcells are most commonly associatedeither with subepidermalsclerenchymaor bundle-sheathsclerenchyma.Silica bodies are found only in orchids and commelinids,not in other lilioid or basal monocots. In orchids, silica bodies are entirely absent from subfamiliesVanilloideaeand Orchidoideaeand most Epidendroideae but present in some Cypripedioideae and in the putativelybasal orchidsubfamilyApostasioideae.Among commelinidmonocots,silica bodies arepresentin all palms,DasypogonaceaeandZingiberales but presentor absentin differenttaxa of Poales and Commelinales,with at least four separate losses of silica bodies in Poales.

II. Introduction
Most plants have non-protoplasmic inclusions in some of their cells, such as calcium oxalate crystals,starchgrains,tanninsand silica bodies. In some groupsthe presenceof such cell inclusions may representa potentiallysignificanttaxonomic character. For example, calcium oxalatestyloidsarea characteristic featureof the familyIridaceae et al., 1984;Rudall, (Goldblatt 1994); also crystal druses are largely restrictedto some basal monocotyledons:Acorus and Alismatales (Prychid& Rudall, 1999, 2000; Keating, 2003). Silica bodies of various shapes and sizes occur in leaves of severalgroupsof monocotyledons,always in well-definedtissues. This articlereviews the presence, form and distribution of silica bodies in one large group of floweringplants,the monocotyledons,in the contextof both a historicalreview and a phylogenetic framework. Recentsystematicanalysesof monocotyledons thathave consideredthis characterhave recordedonly presenceor absenceof silica bodies. However,theirformandposition, which arenot greatlyinfluencedby environmental factorsbut areclearlygeneticallycontrolled, may also have considerablesystematicpotential. Silica in the form of bodies or particlesdepositedwithin or on cells, as distinctfrom silica in cell walls or completely filling hairs and other cells, -occursin certaingroups incorporated the plantkingdom,includingSelaginella (Bienfaitet al., 1985;Le Coq et al., 1991), throughout Equisetum(Laroche, 1968; Kaufmanet al., 1971), some ferns (Rolleri et al., 1987) and to a small extentgymnospermleaves andwood (Jiang& Zhou, 1989;Hodsonet al., 1997; Sangster et al., 1997), as well as some angiospermfamilies.Pipemo (1988) listed pteridophytes, gymnospermsand angiospermsthatcontainsilica bodies, with notes on theirabundance andposition. Silica bodies may be foundin all plantparts,althoughless commonlyin roots.In wood they are sometimes termed"silica grains"and are characteristically situatedin the ray or axial parenchyma cells of certaingenera in about 55 dicot families (see lists in Welle, 1976; Metcalfe & Chalk, 1983; Espinozade Pemia, 1987). In reproductive partsthey may be differentin shape from those in vegetative parts,as Pipemo (1989) showed in many tropicalangiosperms.

III. Historical Review

The early historyof this subjectwas well coveredby Netolitzky (1929), but since his book is not easily available a summaryis given here. Davy (1814) was one of the first people to investigatethe form of silica in plants,includingthe epidermisof Triticum, Avena,Arundoand Equisetum.Struve (1835) demonstrated for "tabaschir" in bamboo stems that silicified parts remain intact after ashing but dissolve in caustic potash solution. Criuger (1857) found silica bodies in Cauto bark (Moquilea or Hirtella species, Chrysobalanaceae) and Calamusparenchyma;he used both Schulze's solution (nitricacid and potassiumchloride)and a mixtureof sulphuricand chromic acids to isolate the silica, which he thoughtwas always deposited in dead cells. Von Mohl (1861) corroboratedCruiger'sobservations but disagreed with the

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hypothesisthat silica depositionalways occurs in dead cells. He found silica grains(reminiscent of starchgrains)and silica filling entirecells in variousplants and used hydrofluoricacid to dissolve the silica and leave organicmaterial.To obtaina silica skeletonhe heatedthe material in Schulze's solution, then heated it in waterand transferred it to alcohol before ashing in a platinumcrucible.Kuister (1897) tested for silica with phenol, in which silica grains appear reddishor bluish. Wiesner(1867) distinguishedshort"silica cells" from long epidermalcells in Zea andSaccharumbut thoughtthey consisted of a wall thickeningand silica incrustation; Wieler (1893, 1897) and Grob(1896) realizedthatthe cell luminaare filled with silica. In SaccharumWieler (1893, 1897) showed that silicificationproceeds inwardfrom a silicified wall and eventually fills the entirecell. The tiny cavities thatare sometimespresentin silica bodies of grasseswere thoughtto be remainsof cytoplasmor gas bubbles(Frohnmeyer,1914; Molisch, 1918). Mettenius(1864) coinedthe terms"Deckzellen" (covercells) or "Stegmata" (fromthe Greek stegium,a roof or covering)for cells thatcontaininclusionsand lie over sclerenchyma in ferns; these cells enclosed calcium oxalate crystalsin Cyatheaceae,silica concretionsin Dryopteris and true stegmatain most Trichomanes species. However, most subsequentauthorshave applied the term "stegmata" only to silica-containingcells. Rosanoff (1871) termedthese silica cells "Scheidenzellen"(sheath cells) because they often surroundvascular bundles; he describedthem in many orchids,palms, bamboos and Marantaceae, where they contain one or sometimestwo to three silica bodies per cell; the cells are often in axial files. Pfitzer (1877) pointed out the positional homology between silica cells (stegmata)in orchids and crystal-containing cells in similar locations accompanyingthe vascularbundles in many plants. Possession of eithersilica or calcium oxalate crystalsin cells overlyingvascular bundlesoccursfrequentlyin plants;e.g., in ferns(crystalsand/orsilica), palms (silica:Molisch, 1913), Pandanaceae(crystals: Kohl, 1889), Xanthorrhoea(crystals:Rudall & Chase, 1996) and Iridaceae(crystals:Goldblattet al., 1984). Konstanty(1926) showed that files of crystal cells, or so-called chamberedcrystal fibers, develop from division of parenchymacells, not fiber cells, and Netolitzky (1929) thought it likely that stegmata develop in a similar way. Rosanoff(1871, translated from Russianof 1867) studiedthe developmentof such cells in the root of Phoenix dactyliferaand Syagrusbotryophora; he observedthatsilica is laid down at a very earlystage in these cells, while they arestill thinwalled andcontaincytoplasm.He did not find any increasein numberof the cells duringdevelopment,althoughthey are axially shorter thanadjacentsclerenchymaandparenchyma cells; he thereforeconcludedthatin these species the silica cells lose the capacityto grow and divide at an early stage. Stegmataare characterized by a thickenedwall adjacentto the underlyingsclerenchyma cells, with progressivelythinnerlateralwalls and thin outer walls. The wall next to sclerenchyma is often pitted,the pits corresponding to those of the sclerenchymacell. Silica bodies in stegmatamay be spherical,conical, hat shapedor of intermediate type and may resemblecrystal druses (e.g., Ravenala, Strelitzia).The surface of the body is rarely completely smooth, often spinulose or nodularor with a crater-likecavity (e.g., Musa). The thin outer walls of stegmataoften borderlarge or small intercellular spaces. The term "stegmata" is not normallyappliedto epidermalsilica cells, even when they lie over sclerenchymaassociatedwith vascularbundlesandpossess the thickenedinnerpericlinal wall characteristic of stegmata, although Tomlinson (1969: 325) referred to "epidermal stegmata" in Phenakospermum (Strelitziaceae).Epidermalsilica cells frequentlylie over sclerenchyma fibers, either restrictedto those accompanyingvascularbundles as caps or girders or above independent fiber strands.However,silica also occurs in intercostalcells, where it is often of a differentform from that in costal cells (e.g., many Cyperaceaeand Poaceae).

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IV. Composition of Silica in Plants Silicais animportant of many mineral component soilsandis thesecond mostabundant eleintheEarth's ment after &Evans, Soluble therawmaterial crust, oxygen (Hodson of 1995). silica, silica bodyformation, is released intothesoilbyweathering of silicate minerals asquartz such and Forexample, feldspar insoil,is hydrolyzed (Piperno, orthoclase a mineral 1988). feldspar, present by thehydrogen andhydroxyl intothemineral ionsof water in therelease of kaolinite, resulting intosolution. ionsandmonosilicic Monosilicic in water potassium acid(Si(OH)4) acidis soluble givinga concentration of ca.2mMat250C, that concentrations higher forms implying polymeric of silicaarepresent & Evans, Theselatter twocomponents arethentaken (Hodson 1995). upby roots in xylemsap. plant andtransported theplant throughout
4KA1Si308 + 4H+ +
orthoclasefeldspar

18H20

-e

Si4Al4O10(OH)8 + 4K+ + 8Si(OH)4

kaolinite monosilicic acid

of weathering; Minerals intheir rates forexample, vary aluminosilicate aremore clayminerals to weathering thanis quartz susceptible aretwoproposed mechanisms (Brady, of 1990).There soluble silicauptake: active orpassive, flowin the transport bymetabolic nonselective processes stream transpiration (Piperno, 1988).In planttissuessilicicacidbecomes highlypolymerized, in the deposition resulting of solid, generally amorphous silicondioxide (non-crystalline)
withinorexternal to cells,oftenreferred (SiO2.nH2O),either to as "opal" or"opaline silica" (Piperno,

This canoccur ataveryearly 1988). process ofplant inalmost stage development, tissue. anyplant Silica inmature particles (ca. 10nmin diameter) hairs of thelemma of Phalaris canariensis may be laiddownin lines,thereby resembling rods, mayform sheet-like of discrete arrangements particlesor maybe packed intodisorganized arrays (Mann et al., 1983a,1983b). Kaufman et al. (1970)andLawton on Avena (1980),working sativaandLolium temulentum respectively, sugthat gested thesilicabodies inthesespecies aremade silicarodsthat upof smaller to grow appear from thesidesof thecelltoward thecenter. InOryza sativa, individual silicabodies eachconsist of about100,000 silicarods,eachrodca.2.5 gm longand0.4 ,umwide(Dayanandan, 1983). The silicaparticles ineachrodhavea diameter of 1-2 nm.Similarly, Jones et al.(1966)demonstrated that silicainvarious taxais composed of spherical particles upto 100nmindiameter. Ontheother hand, Hodson et al.(1984)cautioned that thespherical particles andtheimpression that thesilica hadaggregated intorodscouldallbe artifacts dueto thesectioning of thematerial. Thewater content of thesilicaranges from4%to 9%.Crystalline siliconphases havebeen reported (Lanning, 1960;Sterling, 1967;Wilding & Drees,1974),andit hasbeenshownthat thecomposition of amorphous silicachanges intoa crystalline formas it ages(Wilding et al., 1977).Silicabodiesmayalsocontain significant amounts of nitrogen andcarbon, either within the bodyitselfor on its surface, possiblyarising fromcytoplasmic material, celluloseand/or lignin.Other elements, suchas aluminum, chlorine, copper, iron,manganese, phosphorus and titanium, may also be present. Plantsilicais optically isotropic, ranging in refractive index from1.41to 1.47,hasa specific gravity from1.5to 2.3 and,witha lightmicroscope, ranges in appearance fromcolorless orlightbrown to opaque (Jones & Beavers, 1963).Carbon pigmentation maycausethedarker formsof silicabodies.Frohnmeyer (1914)noticed that,in young material of Saccharum officinarum, silicabodiesareonlyweaklyrefractive. V. Techniques Several different havebeenutilized techniques to examine silicain plants, although light microscopyis the primarymethod,often using standard anatomicalmethodsof wax

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embeddingandsectioningor epidermal peels (e.g., Frohnmeyer, 1914;Parry& Smithson,1958; Tomlinson,1966; Blackman,1969; Hodson & Sangster,1988). Silica may be observedin situ or extractedvia variousprocedures,such as dry ashing underhigh temperatures (spodogram technique:Parry& Smithson,1958; Lanninget al., 1980). The ash may be assessed for silicon dioxide content by difference of weights before and after treatmentwith hydrofluoricacid (Lanning & Eleuterius, 1989). Wet ashing involves extractionby liquids, such as sulphuric acid (Dayanandan,1983), or digestion of organic materialwith nitric and perchloric acids (Hayward& Parry,1980). For example, Blackman(1971) made observationson silica morphology in 26 species of grassesusing eitherthe spodogram techniqueor treatment with hydrogen peroxideand/orchromicacid. Parret al. (2001) investigateda microwavedigestionmethod for the extractionof phytolithsfromherbarium and/orfreshplantmaterialwithoutthe need for wet or dry ashing. They foundthatphytolithassemblagescomparable to those of conventional dry ashing were obtainedquickly and without cross-contamination. Localizationof unstainedand essentiallytransparent silica bodies using a light microscope relies on differencesin refractiveindices between the mountingmedium and silica (Parry& Smithson, 1958; Dayanandan,1983). However,thereare a numberof stainingtechniques.For example,silica deposits(actuallythe silanol [SiOH] groupson the surfacesof silica particles), may be localized by stainingwith silver-aminechromate,methylred and crystalviolet lactone (Dayanandan,1983). Sections may also be stainedwith phenol (Davis et al., 1973), any silica presentgiving a magentacolor reaction,and comparedbefore and aftertreatment with hydrofluoricacid, which dissolves the silica (Gattusoet al., 1998). Anionic dyes may also be used to visualize silica (Allingham et al., 1958). Total silica content may be determinedcolorimetrically by a chemical process that results in the formationof a blue silica-molybdatecomplex (Blackman,1968; Yoshidaet al., 1976; Gattusoet al., 1998). Enzyme localizationtechniqueswere used by Blackman(1969) on developing silica cells in the leaf sheathof wheat Triticum aestivumto look for metabolicpeculiaritiesof potentialand developingsilica cells. In additionto the greaterlevel of succinic dehydrogenase activityfound in potentialsilica cells, the cells may containsubstanceswith a specific activityrelatedto silica accumulationand precipitationor may even be manufacturing enzymes that will eventually degradethe cell contentsduringsilica body formation. The scanningelectronmicroscope(SEM) and image analysis systems have also been used to evaluateand quantifyvariationsin silica body morphologicalparameters and to investigate of silica deposits within tissues (Sangster,1968; Hayward& Parry,1980; Hodson distribution & Sangster,1988; Rovner& Russ, 1992; Ball et al., 1993; Whanget al., 1998). Sophisticated statisticalprogramscan pick up significant differences between phytolithsproducedin one tissue type and those producedin another(Ball et al., 1993). Silica bodies sampled from a single plant tissue may not necessarilybe representative of those producedby the plant as a whole. The SEM has also been used in conjunctionwith X-ray microanalysisto locate silica andassess silica content(for reviews, see Parryet al., 1984;Harvey,1986;Hodson& Sangster, 1989a, 1989b; Larcheret al., 1991; Dorweiler & Doebley, 1997; Gattuso et al., 1998). For example, silica was localized in specific wall layers of the stomatalapparatus of sugarcaneby SakaiandThom (1979). The techniquerelies on the productionof a characteristic X-ray wavelength for each element in the sample. If the wavelengthsare recorded,they yield a list of the elementspresent.Thus, images of only the areasproducinga characteristic X-ray wavelength are localizationsof a particular elementwithinthe sample.Similarly,silica has been detectedin the leaves of variousgrassesusing two analyticalelectron-microscopical techniques,ElectronEnergy-Loss-Spectroscopy (EELS) and Electron-Spectroscopic-Imaging (ESI) (Bode et al., 1994). Brandenburg et al. (1985) visualized silica bodies in grass leaves using the SEM with

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electron imaging;previously this techniquehad mainly been used by materials backscattered scientists and biomedical researchers.Hodson and Sangster (1989a) used this technique to aestivum),andWhanget locate silica depositionin the inflorescencebractsof wheat (Triticum al. (1998) studiedthe variationof epidermalsilica bodies in rice (Oryza).The techniquerelies electron signal being proportional to the averageatomic upon the intensityof a backscattered the signal.Areas of the higherthe atomicnumberthe brighter numberof the sampleirradiated, high silica depositionwould appearbrighteron the image than areasof low silica deposition. potassium, However,if otherelements of higheratomicnumber,such as calcium,phosphorus, sodium or sulphur,were also present in significantquantitiesthese areas would also appear brightand could thus be confused with the silica signal. Wavelengthdispersive electron probe microanalysisprovides electron images of a specielement of interest. image for the particular men and also a corresponding X-ray distribution Numerous studies have been carriedout using this technique,includingthat of Sangsterand Parry(1976), who investigatedthe occurrenceof silica in relationto endodermalthickening and meristematiczones in Sorghumroots. Parryand Hodson (1982) and Parryet al. (1986) in the caryopsisandinflorescencebractsof Setariaitalica andleaves mappedsilica distribution of Bidenspilosa respectively,in relationto implicationsof plant silica in esophagealcancer. Ultrastructural experimentsusing transmissionelectronmicroscopy(TEM)to examineupinto cell-wall silica were carriedout by take of silicic acid and its subsequentincorporation Sowers and Thurston(1979). They grew Urticapilulifera plants,which bearsilicified stinging cells on their leaves, in hydroponicsolutions with and without supplementsof silicic acid to determinewhether silicon starvationwould affect plant growth. Ultrathinsections of plant with hydrofluoricacid for comparison. tissues were micrographed before and after treatment by Chen and Lewin (1969) on Equisetum;they found Similar experimentswere undertaken thatsuccessive reductionsin availablesilicon in the growthsolutionresultedin an increasingly stuntedhabit. Ultrastructural localizationof soluble silicon has been carriedout using freeze substitution to preserveand embed specimenmaterial(Ashton& Jones, 1976). This technique reducesthe loss of soluble componentsfromthe cells. Radioisotopeshave been used in several studies of silicon metabolism in higher plants as labels for silicic acid (Rothbuhr& Scott, 1957). Silica bodies or phytolithsthathave been releasedinto the soil throughplantdecay can be radiocarbon-dated withinthe body.Amorphoussilica gel has by utilizingthe carbontrapped very high X-ray absorptivities; Agarie et al. (1996) used soft X-ray analysisto determinesilica body distributionand relative frequencyin whole leaves of Oryzasativa. Dried leaves were with X rays on soft X-ray film; silica bodies appearedas black spots on the film. irradiated Scanning transmissionelectron microscopy (STEM) has also been used (Hodson et al., 1984; Hodson & Sangster,1993) to localize silica. For instance,Hodson and Sangster(1993) used the techniqueto look at the interaction between silicon and aluminumin the freeze-dried roots of Sorghumbicolor. The higher resolutionof the STEM meant that the authorscould localize the aluminum/silicondeposit of the root epidermisto the outertangentialwall.

VI. Uptake and Deposition

Lewin and Reismann(1969) and Raven (1983) reviewedthe evidence for passive uptakeof monosilicic acid in certainplants. A mechanism of this type would allow predictionof the amount of deposited silicon in a plant from the concentrationof silicic acid in the growth medium,as Jones and Handreck(1965) inferredin oat plants.However,thereis also evidence for active uptakeof soluble silica in some species. For example, in rice shoots, silicic acid can gradient(Okuda& Takahashi,1964). Hodson pass into xylem sap even againsta concentration

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andEvans(1995) foundthatmore silica is takenup by wetlandgrassesthanwould be predicted from the quantityof silica presentin the soil solutionandthe transpiration rate,therebyimplying an active uptakemechanism.Piperno(1988) suggestedthatboth active andpassive absorption may occur in differentspecies or even, sometimes,in differentregions of the same plant. Silica accumulation & Miyake, 1977) is characteristic (sensu Takahashi of some plantfamilies, whereas othersproducelittle or no silica. Species with little silica controlthe amountof silicic acid thatentersthe root or passes fromthe rootto the aerialtissues of the plants(Piperno, 1988). Jones and Handreck(1969) proposeda hypotheticalbarrierin root epidermalcells of clover (Trifolium thatrestricted the flow of silicic acid intothe transpiration incarnatum) stream. Experiments undertaken by ParryandWinslow(1977) on pea seedlings(Pisumsativum)showed that there is some mechanismat the root surfacewhich disallows the passage of monosilicic acid into the root. In otherspecies, such as Viciafabia and Ricinus communis,a layer of fatty substanceon the root-hairsurfacemay form the barrier(Parry& Winslow, 1977). In monocotyledons,relativelyfew studies on opaline silica bodies have considereddevelopmental aspects, especially using modem methods. Grob (1896), Frohnmeyer(1914) and Prat(1931) examinedsilica depositionin Poaceae.They found differingtypes, rangingfrom a fine-grainedsilica network, with accumulatingsilica continuingto fill the cell centripetally (Grob, 1896), to the formationof a "silica ring" aroundthe cell peripheryenclosing the cell contents, which later increases, restrictingthe cell lumen (Frohnmeyer,1914). Maturesilica bodies have characteristic vesicular cavities within them; Grob (1896) relatedthe position of these cavities to the stage of silica deposition. In Saccharumofficinarum,silica deposition occursrapidly,and there is layeringor stratification in the peripheral silica (Blackman,1969). Frohnmeyer(1914) suggested that rapid deposition of silica results in homogeneous silica bodies, whereasslow depositionresultsin non-homogeneoussilica masses. In Arundodonax a thin silica ring is formedaroundthe peripheryof the cell, andthe cell lumenis then filled either by formationof a fine networkor by growthof a silica ring, a form of depositionintermediate between the two previous types. Silica may also be deposited on a dispersedorganicmatrix withinthe cell, since brokensilica bodies have a porousinternal structure (Grob,1896;Sangster, 1968). Prat(1931) suggestedthattransparent silica bodies originatefrom an opaquesilica gel stage and that granular inclusionswithin them are the remainsof the nucleus and cytoplasmic contents. In additionto infillings of the cell lumen, silica may also be laid down as deposits within the cell wall or between the cellulose wall and the plasmamembrane(cell-wall deposition or membranesilicification:Drum, 1968), or in corticalintercellular spaces (Montgomery & Parry,1979). Cell-wall incrustations are common in dicotyledons,whereas infilling of the cell lumen occurs more frequentlyin monocotyledons(Piperno, 1988). Developing silica cells in the leaf sheathof wheat (Triticum aestivum)have an apparently normalcuticle but differ from surrounding cells in having smallernucleoli and thinnerouter cellulose walls (Blackman, 1969). Thin outer cellulose walls may result in a higher rate of transpiration, facilitatingan influx of silica as monosilicic acid. Jones and Handreck(1967), Sangsterand Parry(1971) and Raven (1983) all cited transpiration or water loss as a major factorin silica polymerization. In some species, greateramountsof silica aredepositedin those regions of the plant where water loss is highest. However, this is not always the case, since silica is often deposited in tissues that restrictwater loss, such as sclerenchyma.Indeed, the associationbetween developmentof silica bodies and sclerenchymarequiresfurtherexploration, since the two are often associated;for example, in orchids(M0ller & Rasmussen,1984). Parryet al. (1984) consideredthat a passive, transpiration-based process cannot account for many cases of localized silica deposition. Such highly localized silica distributionpatterns indicategenetic controlthat is phylogeneticallymediated.

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beforesilicabodiesareformed,resultingin "empty" Nuclei andothercell contentsdegenerate cells possessing no apparent cell contentsor silica bodies. The small size and rapiddegeneration of nuclei indicate that protein synthesis in the cell is at a minimum (Lowary & Avers, 1965). As the concentrationof monosilicic acid in the cell increases, the solution becomes supersaturated, changingto a sol form andthen to a highly polymerizedgel (SiO2.nH2O). This process could resultfrom a reductionin cellularpH to 5.0-6.0, probablycausedby the breakdown of the cellularbufferingsystem as the cytoplasmdegenerates(Iler, 1955). The polymerization and gelling processes may also be catalyzedby the presenceof organicmolecules. The mechanism of silica deposition is also thought to involve other mineral ions (Perry et al., 1984a, 1984b; Hodson & Bell, 1986). Often the polymerizedsilicic acid fills the cell lumen and binds to the cellulose cell walls, forminga silico-cellulose membrane; thus cell walls can be silicified (Lewin & Reismann,1969; Schwarz,1973). The increasingconcentration of silica in the cell results in highly refractivemature silica bodies that typically fill the whole cell (Blackman, 1969). The genetic control of silica deposition is also under investigation.For example, a single
Mendelian locus located on maize chromosome 4, teosinte glume architecture I (tgal), has a

majorinfluenceon severalaspectsof cupulatefruit-wallmorphology,both in maize (Zea mays

ssp. mays) and its wild progenitor, teosinte (Zea mays ssp. parviglumis). Dorweiler and Doebley

(1997) demonstrated thattheteosinteallele (tgal + teosinte)increasescellulardeposition of silica. They suggested that tgal regulates which cells of the glume and rachis epidermis become silicified, since it apparently activatessilica depositionin certaincells or repressesit in others. VII. Morphology and Location Thereare severalmorphologicalformsof silica in monocottissues, andthe numberof silica bodies per cell may also vary.Classificationof phytolithsis invariablybased on theirsizes and shapes; for example, Bertoldi de Pomar (1971) proposed two morphological groups: microsilicophytoliths andmacrosilicophytoliths. The most commontype of silica body in monocots is the "druse-like"spherical, spherical-rugose (nodular) or spherical-spinulose type (Fig. 2B), usually a single body per cell but sometimes more. Otherforms include the "hatshaped"type (sometimes called a "truncated conical," Fig. 2A), trough-shaped (Fig. 3C) and an amorphous, fragmentary type (silica sand,Figs. 2E, 2F). These shapesareconsistentenough within genera or tribes to be used as charactersin taxonomic studies (e.g., Stebbins, 1956; Metcalfe,1960)andas an aid in identification (e.g., Wilding& Drees, 1968;Dormaar & Lutwick, 1969; Lutwick& Johnston,1969; Twiss et al., 1969). Anothervariablefeatureis the relative location of silica bodies in plant tissues. They are most commonly found either in the epidermis(e.g., in grasses, commelinasand sedges) or in the sheathcells of vascularbundles (e.g., in palms, bananasand orchids).Silica-bearingcells are most commonly associatedwith sclerenchyma,either subepidermal sclerenchyma(in the case of epidermalsilica) or bundle-sheath sclerenchyma,althoughthereare exceptionsto this. VIII. Ecology A numberof ecological factors,includingclimate,soil variability, moistureavailabilityand plant age, affect silica body developmentby regulatingthe concentrations of dissolved silica that is availableto plants (for a review, see Pipemo, 1988). In many species, leaves of older plantscontaingreateramountsof silica thando theiryoungercounterparts, possibly due in part to cellularchangesrequired to obtainsilica andin partto an increasedavailabilityof deposition sites (Bezeau et al., 1966; Blackman, 1968, 1969; Lanning & Eleuterius, 1985). In some

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species, an increasein the amountof dissolved silica in a growthmediumincreasesthe amount of plantsilica (measured as a percentage of dryweight)in directproportion (Okuda& Takahashi, of silicate mineralsis thoughtto be acceleratedby 1961;Jones & Handreck,1965). Weathering wet climates, thereby liberatinggreaterquantitiesof soluble silica into the soil than in dry climates (Dunne, 1978), partlyexplainingthe relativelygreaterconcentrations of silica in wet tropicalsoils (Siever, 1967). Tropicalplant root systems are extremelyefficient in absorbing of silica in these plants (Lovering, any soil nutrientspresent,resultingin high concentrations 1959; Riquier, 1960; Pipemo, 1985). Plants of the same species grown in differentsoils can containdifferentamountsof silica. Substancessuch as iron and aluminumoxides, which may be presentin the soil, are known to interactwith silica under appropriate conditions,producingcolloidal complexes that are not takenup by biological systems (Birchall, 1990; Exley & Birchall, 1992, 1993), therebyreducing the amountof solublesilica available.Indeed,the amountof aluminum and silica thatplants in theirtissuesvariesconsiderably, transport andthereis some evidencethatvery high aluminum andvery high silica accumulation accumulation aremutuallyexclusive(Hodson& Evans, 1995). Exley andBirchall(1993) postulated thatsilicic acid inhibitsthe nucleation of aluminum hydroxide by forming hydroxyaluminosilicate complexesandthatthisprocesswas foundto increase with increasing pH. Independent of these substances,soluble silica concentration has been shown to reach a maximumat a soil pH of 8-9 (McKeague & Cline, 1963), with the result that more soluble silica is availableto plants growing in acid soils. However, silica solubilityrises considerablyabove pH 9.0 due to silicate ion formation(Hodson & Evans, 1995). Increasedsoil watercontentmay resultin increasedsilica uptake(Jones& Handreck,1967). For example,grasses grown in the floodwaterfields of Egypthad greatersilica depositionthan did grasses grown in areaswhere rainfallagriculture was practiced(Miller, 1980). The amount of solid silica in the plant decreaseswhen high concentrations of nitrogenand phosphorus are presentin the soil. Soluble silica also increaseswith an increasein the amountof decomposed in the soil. On the otherhand,silica bodiesareoftenpresentin epiphyticorchids, organicmaterial which do not have access to soluble silica in groundwater but insteadobtainit fromrainwater. Terrestrial orchid species often lack silica (see section XI, "SystematicDistribution"). Although silica uptake and concentrationare affected by environmentalfactors, they are primarilyundergenetic control(Pipemo, 1988). Families consideredto be non-accumulators do not accumulatesilica regardlessof the environmental conditions.Plantsthat show different morphologicalforms of silica retain their individualsilica morphologieswhen grown under identical environmentalconditions.

IX. Functions
Silica is consideredto be an important factorfor normalgrowthanddevelopment(Agarieet al., 1996). The study of silicon metabolismis beyond the scope of the presentreview. We are concemedhere with depositsof silica, which have sometimesbeen regarded as a waste product or as a form of storage, from which silicon can be mobilized if needed to interactwith other elements;e.g., aluminum(Hodson& Evans, 1995). It has been suggestedthatepidermalsilica bodies may act to reducetranspiration in leaves (Yoshida,1965; Lanning& Eleuterius,1983), therebyimprovingwateruse efficiency (Yoshidaet al., 1959). HuttonandNorrish(1974) found a direct correlationbetween the silicon percentagein wheat husks and the quantityof water transpired. The "window"hypothesispostulatedthatthe presenceof epidermalsilica bodies facilitates the transmissionof light throughthe epidermis to the photosyntheticmesophyll or to stem corticaltissue, consequentlyincreasingphotosynthesisand plant growth (e.g., Takeokaet al.,

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THE BOTANICAL REVIEW

1979). However, Kaufmanet al.'s (1979, 1981, 1985) investigationsdid not supportthe suggestion, andAgarie et al. (1996) disprovedthis hypothesisin rice. Silica may help to maintainrigidity in stems and linear leaves (Ishizuka, 1971), although leaf stiffnessmay also be relatedto the degreeof lignification(Matsudaet al., 1983). Silica has been shown to improvelodging resistancein wheat (Gartner et al., 1984). Silica contentmay be relatedto grazingof grasses by herbivores(Vicari& Bazely, 1993). McNaughtonand Tarrants (1983) and McNaughtonet al. (1985) found that silica contentwas higher in heavily grazed grasslandsthan in others and that more silica was present in plant tissues producedearly in the growing season. In a feeding experiment, prairievoles (Microtus ochrogaster)preferentiallyate grasses with low silica content (Gali Muhtasibet al., 1992). Wadhamand Parry(1981) investigatedthe relationshipbetween silica contentand slug resistance. Djaminand Pathak(1967) tested severalrice varietiesand foundthatthose with high silica contentshowed greaterresistanceto Asiatic stem borer(Chilo suppressalis)thanothers,probwith boringand feeding of the larvae;selecting rice varieties ably because the silica interfered with a high silica contentwas more economicalthanapplyingsilicate to the soil. Hanifaet al. (1974) studied the role of silica in the resistance of rice to the leaf roller (Cnaphalocrocis medinalis), and Moore (1984) examined the relationshipof silica to stem-borerinfection by Oscinella species in Lolium. Silica body contentmay be correlated with resistanceto fungaldiseases;for instance,brown spot disease of rice (Nanda& Gangopadhyay, 1984) and blast disease of rice (Suzuki, 1937). X. Applications
A. SOILSAND ARCHAEOLOGY

Silica bodies and othersilicified plantparts,such as silicified hairsandcell walls, occurring in soils, dust, etc., are termed"phytoliths," or sometimes "silicophytoliths," "opalphytoliths" or "plantopal."The term "phytolith" of plant may also be appliedto othermineralstructures origin,suchas calciumoxalatecrystals,butis moreusuallyrestricted to silicaparticles. Deflandre (1963) reportedthat Ehrenberg(1841) was one of the first scientists to recognize that these particleswere, at least in part, of plant origin; Ehrenbergstudiedthem in soils and classified them by shape,termingthem "phytolitharia." The studyof phytolithsin soils and archaeological materialhas proved a valuableaid for determining vegetationtypes in a particular locality at various ages in the past and thus reconstructing as well as for investipalaeoenvironments, gating ancientagricultural practicesand crop-plant evolution.Phytolithsare extremelydurable in soil and may not migrate throughit to the same extent as do other microfossils, such as pollen and diatoms.However,while phytolithsderivedfrom grasses and sedges may be abundant,those from some vegetationtypes may be underrepresented or absent;for example,gymnospermsand fems (Horrockset al., 2000). This is a vast subject,andwe referthe readerto relevanttexts for moreinformation (Rovner, 1986; Pipemo, 1988; Mulholland,1989; Pearsall, 1989; Rapp & Mulholland,1992; Wang & Lu, 1993; Pinilla et al., 1997). As an example of this work, we can cite Blinnikov (1994), who found differentphytolithassemblagesin changingalpineplant communitiesin the northwestem Caucasus,andMadella(1997), who analyzedthe phytolithcontentof sedimentsfrommodern and palaeosols in Tadjikistan and was able to show that at certain periods grasses predominated, whereas at others there were also gymnospermsand dicot trees in the vegetation. Runge and Runge (1997) demonstrated rain-forestdegradation andvegetationchangesin East Africa by examinationof phytoliths in sediments and comparisonwith those extracted

SILICABODIESIN MONOCOTYLEDONS

387

from species composingdifferentpresent-day plant communities.Changesin forest andgrassland vegetation in Arizona were examined by Kems et al. (2001) and Kems (2001) and in WashingtonState by Blinnikov et al. (2002). The spreadof grasslandsin the Late Tertiary of Nebraskawas investigatedby Stromberg (2002). Such studiesrely on a comprehensivereference collection of plantsfrom the areaof study,as has been providedby Palmerand othersfor EastAfricangrasses(Stewart,1965;Palmer& Tucker,1981, 1983;Palmeret al., 1985;Palmer & Gerberth Jones, 1986,1988), Brown(1984), Mulholland andTieszen(1994) (1989), Fredlund and Pipemo and Pearsall(1998) for the USA, andKealhoferandPipemo (1998) for the Southeast Asian flora. Archaeological studies are very varied, ranging from analysis of the phytoliths or wear associatedwith prehistoric or recenthuman(Puechet al., 1983; Laluezaet al., 1996;Cummings & Magennis, 1997; Juan-Tresserras et al., 1997; Gugel et al., 2001) or animal (Baker et al., 1959; Armitage, 1975; Acuna-Mesen & Garcia-Diaz, 1998) teeth and the informationthey provide about diet to investigationsof ancient settlements(e.g., Kajale & Eksambekar, 1997) andbasketry(Ollendorfet al., 1988). Rosen (1992) demonstrated thatit was possible to distinguish between cereal straw and husks in archaeologicalsettlementsby the use of silica skeletons of epidermalcells. The occurrenceof palm remains,includingphytoliths,at New Worldarchaeologicalsites provides evidence for palm dispersalby humans(Morcote-Rios& Bemal, 2001). Stegmatain fossil palm stems have been demonstrated by Ancibor (1995). B. AGRICULTURAL CROPS ANDTHEIR EVOLUTION An importantfield of researchdeals with changes in agricultural practicesover time and with ancientcrop plants and theirevolution. Thereis a large body of literature on maize (e.g., Pipemo, 1988; Bush et al., 1989; Russ & Rovner, 1989; Pearsall& Pipemo, 1990; Doolittle & Frederick,1991;Bozarth,1993;Pipemo & Pearsall,1993;Dorweiler& Doebley, 1997;Pipemo & Flannery,2001), rice (Fujiwara& Sasaki, 1978; Fujiwaraet al., 1990; Sato et al., 1990; Udatsu& Fujiwara,1993; Cailinet al., 1994; Pearsallet al., 1995; Whanget al., 1998;Zhao et al., 1998; Huang& Zhang,2000) and wheat (Ball et al., 1993). Musaphytoliths(distinguished fromEnsete) have been foundin refusepits datedto the firstmillenniumB.C. in Cameroonand provide evidence for early bananacultivationand contacts with Asia, where Musa is native (Mbida Mindzie et al., 2001); edible bananasdo not producepollen or seeds, so in this case phytolithevidence is particularly useful. C. MEDICAL STUDIES The identificationof drug plants may be aided by the study of phytoliths (Umemoto & Hozumi, 1971a, 1971b;Umemoto et al., 1973). Silica particlesin dust fromplantfragmentsin theatmosphere havebeenfoundto affectthehealthof workers(Baker,1961;Hodson& Sangster, 1988, 1989a), while silicified particlesin cereal foods have been implicatedin causing esophageal cancer(Bennett& Parry,1981; Hodson et al., 1982; O'Neill et al., 1982, 1986; Parry& Hodson, 1982; Newman & Mackay, 1983; Sangsteret al., 1983). Silica of plant origin was reportedin humanintestinesas long as 150 years ago (Quekett,1852), and it may be the cause of urinarycomplaintsin cattle (Bezeau et al., 1966) and sheep (Bakeret al., 1961). D. ANIMAL DIETS Analysis of phytolithsfrom teeth or in the digestive system or feces has been used to help determine the dietof herbivorous mammals(Bakeret al., 1961;Cherouvrier et al., 1975;Chapuis,

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THE BOTANICAL REVIEW

Acorus Alismatales Petrosaviaceae Dioscoreales Pandanales Liliales

L__ other Asparagales

6 ~Orchidaceae I Arecaceae Dasypogonaceae Zingiberales commelinids Hanguana Commelinales Poales

Asparagales

Fig. 1. Generalizeddiagramof monocot relationshipsbased on Chase et al. (2000), showing silica distribution.

1980), insects (Gueguenet al., 1975) and snails (Chevalieret al., 2001). It may even be used to study the diet of extinct species such as the moa (Kondo et al., 1994) andAmericanmastodon (Gobetz & Bozarth,2001). The digestibilityof animal foodstuffs may be relatedto the silica content (Van Soest & Jones, 1968; Harberset al., 1981; Balasta et al., 1989). E. OTHER APPLICATIONS of phytolithassemblagesin soils from differentsites may be useful in forensic Comparison investigations (Marumo & Yanai, 1986). Silica extractedfrom plants has been used in the constructionof solar cells (Amick, 1982). Rice husks have been utilized in the manufacture of compositeboard(Cote, 1974) andas a fillerto enhanceproperties of natural rubber vulcanizates (Sae-Oui et al., 2002). The silica extractedfrom rice husks has been tested for use in highconcrete(Chandrasekhar et al., 2002) and as a filler in epoxy resin for embedding performance materialin electronicdevices (Suwanprateeb & Hatthapanit, 2002).

XI. Systematic Distribution

Recentanalysesof molecularsequencedata(e.g., Chaseet al., 2000; Stevensonet al., 2000) have identified several well-supported major monocot clades. However, even combined multigeneanalyses(e.g., Chaseet al., 2000) have yielded an unresolvedpolytomybetween six of these clades (perhapsrepresenting a relativelydeep, rapidradiation): the four lilioid orders (Asparagales, the largecommelinidclade andthe small Liliales, DioscorealesandPandanales), bigeneric family Petrosaviaceae(Fig. 1). The major clades can be grouped for convenience into: 1) basal monocots (AcorusandAlismatales);2) a polyphyleticassemblageof five clades of lilioid monocots (Asparagales,Liliales, Dioscoreales,Pandanalesand Petrosaviaceae); and 3) a monophyleticgroup encompassingall the commelinidmonocots, includingbromeliads, grasses, sedges, rushes,palms and gingers (Fig. 1). Silica bodies are not found in basal monocots or lilioid monocots(apparent reportsarebased on confusionwith crystals);with the single exception of the asparagoidOrchidaceae,which are thus the only non-commelinidmonocots with silica bodies (TableI).

SILICA BODIES IN MONOCOTYLEDONS

389

Table I
Distribution of silica bodies in families of monocotyledons Order,family Basal monocots Acoraceae Alismatales Araceae, Alismataceae, Aponogetonaceae, Butomaceae, Cymodoceaceae, Hydrocharitaceae, Juncaginaceae, Lilaeaceae, Limnocharitaceae,Najadaceae, Potamogetonaceae, Scheuchzeriaceae,Tofieldiaceae, Zannichelliaceae, Zosteraceae Lilioid monocots Petrosaviaceae Pandanales Cyclanthaceae,Pandanaceae,Stemonaceae, Triuridaceae, Velloziaceae Dioscoreales Burmanniaceae(incl. Thismiaceae), Dioscoreaceae (incl. Stenomeridaceae,Taccaceae, Trichopodaceae),Nartheciaceae Asparagales Higher asparagoids:.Agapanthaceae,Agavaceae, Alliaceae, Amaryllidaceae,Anemarrhenaceae, Anthericaceae,Aphyllanthaceae,Asparagaceae,Behniaceae, Hyacinthaceae,Laxmanniaceae,Ruscaceae (incl. Eriospermaceae, Convallariaceae,Dracaenaceae,Nolinaceae), Themidaceae Lower asparagoids: Asphodelaceae, Asteliaceae, Blandfordiaceae, Boryaceae, Doryanthaceae,Hypoxidaceae, Iridaceae, Ixioliriaceae, Lanariaceae,Tecophilaeaceae,Xanthorrhoeaceae, Xeronemataceae Orchidaceae Liliales Alstroemeriaceae,Campynemataceae,Colchicaceae, Corsiaceae, Liliaceae, Luzuriagaceae,Melanthiaceae,Philesiaceae, Smilacaceae Commelinid monocots Arecaceae (Palmae) (c. 190 genera, 2000 spp.) Dasypogonaceae (4 genera, 8 spp.) Hanguanaceae(1 genus, 5+ spp.) Commelinales Commelinaceae (incl. Cartonemataceae) (2 subfamilies, 4 tribes, 41 genera, 650 spp.) Haemodoraceae(2 subfamilies, 13 genera, 100 spp.) Philydraceae(4 genera, 5 spp.) Pontederiaceae(9 genera, 33 spp.) Poales Anarthriaceae(1 genus, 7 spp.) Bromeliaceae (56 genera, 2600+ spp.) Centrolepidaceae(3 genera, 35 spp.) Cyperaceae(104 genera, 5000+ spp.) Ecdeiocoleaceae (2 genera, 2 spp.) Eriocaulaceae(10 genera, 700-1400 spp.) Flagellariaceae (1 genus, 4 spp.) Hydatellaceae (2 genera, 10 spp.) Joinvilleaceae (1 genus, 2 spp.) Present (Table III) Present (Table X) Present(Table IV) Present or absent (Table IV) Present or absent (Table IV) Absent Absent Absent Present (Table VI) Present or absent (Table VI) Present (Table IX) Present (Table VI) Absent Present (Table VI) Absent Present (Table VI) Absent Absent Absent Absent Silica bodies

Absent

Absent

Absent

Present or absent (Table II) Absent

390

THE BOTANICAL REVIEW Table I, continued

Order, family continued Commelinid monocots,

Poales, continued

Silicabodies

350 spp.) Juncaceae (8 genera, Mayacaceae (1 genus,4-10 spp.) Poaceae (Gramineae) (700+genera,10,000+spp.) Rapateaceae (16 genera; 80 spp.) 490 spp.) Restionaceae (55 genera; Thumiaceae (1 genus;3 spp.) 16-30 spp.) Typhaceae (2 genera; (incl.Sparganiaceae) 300 spp.) Xyridaceae (5 genera; Zingiberales Cannaceae (1 genus,25 spp.) Costaceae (4 genera,100spp.) Heliconiaceae (1 genus,200 spp.) Lowiaceae (1 genus,10 spp.) 550 spp.) Marantaceae (31 genera, Musaceae 40 spp.) (2 genera, 7 spp.) Strelitziaceae (3 genera, Zingiberaceae (50 genera,1300spp.)

Present orabsent (Table VI) Absent Present (Table VI) Present (Table VIII) Present orabsent (Table VII) Present (Table VI) Absent Absent Present (Table V) Present (Table V) Present (Table V) Present (Table V) Present (Table V) Present (Table V) Present (Table V) Present (Table V)

Recent molecularanalyses have found Orchidaceaeto be monophyleticand placed in the orderAsparagales(sensu APQ 1998), either as the sole sister taxon to all otherAsparagales clade of Asparagales(in analysesof rbcL (Fay et al., 2000) or as sisterto the earliest-diverging alone: e.g., Chaseet al., 1995a; Rudallet al., 1997), althoughthey are at best weakly supported in these positions. On present phylogenetic evidence, the presence of silica bodies in both as a commelinids and orchids in contrastto all other monocots must thereforebe interpreted homoplasy;i.e., de novo developmentof silica bodies in two closely relatedtaxa,as M0llerand Rasmussen(1984) suggested.This homoplasymay be adaptive,as a resultof similarenvironmentalconstraints, or it could have resultedfrom an iterativegene mutationat a time of rapid monocot radiation.Silica body structure and distribution within tissues are closely similar in orchids and putatively "basal"commelinids such as palms. Evolutionaryevents, such as a secondaryloss of silica bodies in some groupsand theirapparent regain in others,presumably reflect underlyingdifferencesin cell chemistry. A. ORCHIDACEAE The most widely used orchid classificationis still that of Dressler (1993). However, even this classificationrequiressome revision following a recent analysis of moleculardata from rbcL (Cameronet al., 1999) thatproducedfive majororchidclades, roughlycorresponding to the five traditionalsubfamilies Epidendroideae (including Vandeae,Dendrobieae,Neottieae and othertribes), Orchidoideae(includingDiurideae,Cranichideae, Diseae and Spirantheae), Vanilloideae,Cypripedioideae and Apostasioideae.SubfamiliesApostasioideae,Vanilloideae and Cypripedioideaeare all relatively poor in numbers of genera and species. Most of the taxonomicdiversityin orchidsis encompassedby Orchidoideae andespeciallyEpidendroideae. The bigeneric subfamilyApostasioideae(Apostasia and Neuwiedia) is traditionally regarded as the sister groupto otherorchids(reviewed by Dressler, 1993). Furthermore, all of the most recentmolecularandmorphologicalanalysessupportthis basalposition (Cameronet al., 1999; Freudenstein & Rasmussen, 1999; Cameron & Chase, 2000; Freudenstein et al., 2000).

SILICABODIESIN MONOCOTYLEDONS

391

Following Apostasioideae,the next-branching orchid subfamily is either Cypripedioideae or Vanilloideae (cf. Cameronet al., 1999;Pridgeonet al., 2001; Cameron& Chase,2000; Molvray et al., 2000; K. Cameron,pers. comm., 2001). M0ller and Rasmussen(1984) reviewed early work on silica bodies in orchids and added many original observations.In orchids, silica bodies occur in stegmataoverlying sclerenchymatous vascularbundle sheaths,especially adjacentto the phloem, or over independentfiber strandsin leaves and stems (includingrhizomesandpseudobulbs),absentfrom the epidermis, In the leaf of a few Maxillaria species silica cells have althoughthey may be subepidermal. been recorded in hypodermalor chlorenchymacells independentof sclerenchyma(Davies, 1999). In stems the stegmataare on the outersurfaceof a sclerenchyma ring, in which vascular bundles may be embedded, or in connection with vascular bundles scatteredin the ground tissue. The only reports for roots are in three Cymbidium spp. (Cyrtopodiinae)(Yukawa& Stem, 2002), one Maxillariasp. (Maxillariinae) and a few species of Lycastinae(Holtzmeieret al., 1998; Yukawa& Stem, 2002). Interestingly,Cameronet al. (1999) suggested that tribes CymbidieaeandMaxillarieae may be closely related,basedon rbcLsequencedata,andYukawa & Stem (2002) consideredthat root stegmatamight be a synapomorphy in the CymbidieaeMaxillarieaeclade. Silica bodies areentirelyabsentfromtwo orchidsubfamilies,Vanilloideae andOrchidoideae (TableII). In Cypripedioideae they are eitherconical, rod-likeor absent.Silica bodies are also absent from most tribes or subtribesof Epidendroideae but presentin Apostasioideae,which are the putativesister groupto all otherOrchidaceae. The most parsimoniousinterpretation is thereforethatsilica bodies aresecondarilylost in groupsthatlack them entirely.The altemative would requiremultipleorigins of silica bodies within orchids,which seems less plausible.In some (but by no means all) of the subtribeslacking silica bodies, sclerenchymais also absent (M0ller & Rasmussen, 1984). Orchid stegmataare small cells that are usually arrangedin continuousor discontinuous axial files; in some cases a file may borderone axially elongatedair canal. Thereis generally one silica body per cell. Silica bodies are of two types in orchids: 1) conical or hat shaped, sometimesspiny (Fig. 2A), or 2) spherical,often with a rough,wartyor spiny surface(Fig. 2B). The conical type is by far the most common in orchids.Silica and crystalsfrequentlyoccur in the same plant.Sphericalsilica bodies arerestricted to threegroupswithin orchids,one species of Apostasioideae (see below) and two groups of Epidendroideae: 1) subtribes Eriinae, Podochilinaeand Dendrobiinaeof tribe Podochileae,and 2) all three subtribesof Vandeae.In a few of these groups conical bodies also occur occasionally, but the only group in which M0ller and Rasmussen(1984) recordedboth conical and sphericaltypes was Podochilinae,in which Agrostophyllum had conical bodies and the other two genera examinedhad spherical ones. However,Agrostophyllum has since been transferred to Glomerinaein Dressler'ssystem, in which all the genera have conical silica bodies. Yan Peng Ng (pers. comm., 2000) also reportedrecordsof both conical and sphericalsilica bodies in the large andpossibly polyphyletic genus Eria. Moller and Rasmussen (1984) and Rasmussen (1986) noted that spherical bodies occur only in epiphyticorchids,whereasconical ones are presentin both epiphyticand terrestrial species. They suggestedthatthe conical type and terrestrial state might be ancestral andthatsphericalbodies mighthave evolved at least twice. Given ourcurrent knowledgeof the phylogenetic distributionof the two types in orchids, their assessment is certainlypossible, despite the fact that in commelinidsthe sphericaltype is apparently the plesiomorphiccondition. However,the putativelybasal subfamilyApostasioideaeis interestingin this context because the single orchid species so far known to possess both conical and sphericalbodies is Apostasiawallichii, which has spiny conical bodies in the leaf andspiny sphericalbodies in the
(Textcontinues on p. 397)

Table II
Key to location: L leaf, R

Distribution of silica bodies in Orchidaceae (classification of Dressle root; S = stem (including rhizome and pseudobulb. Key to type: C = Brackets indicate few seen or variable. No. studied 2 3 Location / organs studied L, S L

Subfamily, tribe, subtribe Apostasioideae Cypripedioideae Spiranthoideae Diceratosteleae Tropidieae Cranichideae Goodyerinae Prescottiinae Spiranthinae Manniellinae Pachyplectroninae Cranichidinae Orchidoideae Diurideae Chloraeinae Caladeniinae Drakaeinae Pterostylidinae Acianthinae Cryptostylidinae

No. of genera 2 4

Type L: C; S: Sph, C, Abs (C), (rod), Abs

Notes

Refer

C (L) & Sph (S) in M0lle I sp. (Stern et al.)

Soler 19

1 2 35 7 41 1 1 9

1 2 13 2 6 1 1 2

L, S L, S L, S L, S L, S L L L

C C Abs Abs Abs Abs Abs Abs

Stern M0lle

Molle M01l M0lle Stern Stern Molle

6 10 5 1 5 2

1 9 5 1 1 1

L L L L L L, S

Abs Abs Abs Abs Abs Abs

Molle Pridg Molle Molle Molle Stern

Diuridinae Thelymitrinae Rhizanthellinae Prasophyllinae Orchideae Orchidinae Habenariinae Diseae Huttonaeinae Satyriinae Coryciinae Disinae Epidendroideae Neottieae Limodorinae Listerinae
Palmorchideae

3 2 1 3 35 24 I 3 5 5

1
-

L L L, S, R L, S, R L, S L, S L, S L, S

Abs Abs Abs Abs Abs Abs Abs Abs

Moller

1 13 4 I 3 4 5

Moller

Kohl, Ra Molle

Kurzw Molle Molle Molle

4 2 I 3 4 5 1 6 3 1 1

2 2
-

L L

C, Abs Abs

C in 1 sp.

Kohl, 19 Kohl,

Triphoreae Vanilleae Galeolinae Vanillinae Lecanorchidinae Gastrodieae Gastrodiinae Epipogiinae Wullschlaegeliinae Nervilieae

4 4 1 2 1 1 1 (L), S, R L, S, R S, R L, S, R S S, R L, S Abs Abs Abs Abs Abs Abs Abs

Stern Kohl, Ra Stern

Molle Molle Molle Molle

Table I1, continued

No. of genera 6 9 No. studied 3 3 Location / organs studied L, S L, S

Subfamily,tribe, subtribe Cymbidioid phylad Malaxideae Calypsoeae Cymbidieae Goveniinae Bromheadiinae Eulophiinae Thecostelinae Cyrtopodiinae

Type Abs Abs

Notes

Refer

Solere 19 Solere 19

1 1 6 2 12 1 5 1 30 8 8

1 1 5 1 11 1 5
-

L, S, R L, S L, S, R L, S L, S, R

C (rough) in L C (rough) in L C (rough) in L, S C (rough) in L, S C (rough) in L, S

Acriopsidinae Catasetinae Maxillarieae Cryptarrheninae Zygopetalinae Lycastinae Maxillariinae

L, S, R L, S, R

C (rough) in L, S C (rough) in L, S

Stem M0lle M0lle M0lle C in pericycle of R Soler 19 of 3 Cymbidium spp. M0lle ka Abs in S of 1 genus M0ole

3 3 4

L, S

C, ? C C (rough)

L, S, (R)

Stanhopeinae

22

19

L, S, R

C in L, S

Telipogoninae

C, Abs

Kohl, In R of a few spp. Soler Y of 5 genera C in R of 1 Maxil- Soler 19 laria sp. 19 Soler 19 19 M0lle

Ornithocephalinae Oncidiinae

14 77

13 14

L L, S

C, Abs C (irreg.)

C in spp. of 5 genera

M0lle

Pfitze M 19

Epidendroidphylad Arethuseae Arethusinae Bletiinae Chysine Coelogyneae Thuniinae Coelogyninae EpidendreaeI Sobraliinae Arpophyllinae Meiracylliinae Coeliinae Laeliinae Pleurophallidinae EpidendreaeII Glomerinae Adrorhizinae Polystachyinae

2 21 1 1 20

9 1 1 6

L, (S) L L, S L, S

C, Abs C C C, (Abs)

Abs. in S

Soler 19 Soler

Pfitze Zorm R

4 1 1 1 43 28

2 1 7 4

L, S L, S

Abs C C C, irreg., Abs

Soler 19 M0lle

L L, S

Kohl, R Kohl, St

7 2 4

3 1 1

L, S L L, S

C C Abs

M0lle M0lle Molle

Table II, continued

No. of genera No. studied Location / organs studied

Subfamily,tribe, subtribe Dendrobioid subclade Podochileae Eriinae

Type

Notes

Refer

10

L, S

Sph, Abs, (C)

C (nodular) in 1 Eria sp.

Podochilinae Thelasiinae Ridleyellinae Dendrobiinae

6 6 1 6

2 2 6

L, S L, S L, S

Sph Abs Sph (rough), Abs

Soler 19 (p Soler 19 M0lle

Bulbophyllinae Vandeae Aeridinae Angraecinae Aerangidinae Unplaced Arundinae Collabiinae Pogoniinae

15

L, S

Abs

Abs in 6 Pseuderia Kohl, & 2 Dendrobium R spp. et Soler 19

102 19 36

14 3 4

L, (S) L, (S) L, S

Sph Sph Sph Irreg. in S

Kohl, M Herin R Herin R

2 3 5

1 1
-

L, S L, S

C Abs

M0lle M0lle

SILICA BODIES IN MONOCOTYLEDONS

397

silicabodymorphologies andthe orderCommefoundin Orchidaceae, Arecaceae Fig. 2. Various

linales. A. Cephalantherapal/ens (Orchidaceae),conical silica bodies with truncatedtops (hat shaped) adjacent to phloem cells (bar =10 /,am). B. Angraecum chevalieri (Orchidaceae), spherical bodies bundle-sheath cells(bar= 10 trm). C. Drymophloeusbeguinil (Arecaceae), overlying sclerenchymatous irregularlyspherical bodies in vascular bundle-sheathcells (bar = 10 Arm).D. Cyanotis arachnoidea

bodiesin epidermnal small,spherical, cells, apparently (Commelinaceae), spinulose followingthe cell wall(bar= 20 ptm). E. Conostylis bract of silicasandin vascueata (Haemodoraceae), largequantities cells conlarbundle-sheath cells (bar= 10 gin). F. Anigozanthosflavida (Haemodoraceae) epidermal silicasand(bar= 10 grn). taining stem (Judd et al., 1993; Stem et al., 1993a). Since their basal position makes apostasioids criticalin evolutionaryassessmentsof orchidstructures, this recordof both types of silica body in a single species (A. wallichii) indicatesthatboth types originallyoccurredin the family and thateitherboth types or the sphericaltype alone were laterlost, with a subsequentregainof the spherical type in two epidendroid groups.However,independent originof bothtypes in Apostasia is equally plausible.

398

THE BOTANICAL REVIEW B. COMMELINIDS

The commelinids(or commelinoids)have been identifiedas a monophyleticclade in several successive molecularand combinedmorphological/molecular analyses (e.g., Chase et al., 1995a, 1995b,2000; Stevensonet al., 2000). Some highly consistentnon-molecular (anatomical) characterssupportthe commelinid clade: 1) the presence of cell-wall ferulates,almost entirely absent from non-commelinid monocotyledons (Harris & Hartley, 1980; Rudall & Caddick, 1994); 2) the presence of silica bodies in many commelinidtaxa, absent from most non-commelinid surfacewaxes monocotyledons exceptorchids;3) thepresenceof Strelitzia-type (long, often curly, extrudedwax ribbons) in some commelinids, virtually absent from noncommelinids(Barthlott& Frolich, 1983; Frolich& Barthlott,1988); and 4) stomataldevelopment by non-obliquecell division, as opposed to oblique division in most non-commelinids (Tomlinson, 1974; Rudall, 2000). Several taxa formerly had controversialsystematic placement in monocotyledons. Pandanaceae, Cyclanthaceaeand Velloziaceae were previously consideredcommelinid (for example, by Dahlgrenet al., 1985), but recent molecularsystematic studies (e.g., Chase et al., 1995b, 2000) have conclusively demonstratedthat they are more closely related to noncommelinid groups. Apparentreportsof silica bodies are based on confusion with crystals; e.g., Lim and Stone (1971) for Freycinetia. They all lack silica bodies (Table I), which is consistentwith a non-commelinid placement(although,admittedly, absenceof silica bodies is non-informative for systematicsin this context, since it is the plesiomorphicconditionfor this character within monocotyledons).On the otherhand,the presenceof silica bodies in Dasypogonaceae(Rudall& Chase, 1996), Hanguanaceae (Solereder& Meyer, 1929; Smithson, 1956; Tomlinson, 1969; Tillich & Sill, 1999) and Haemodoraceae(Prychid et al., 2003) supports theirinclusion in the commelinidclade, togetherwith othermorphologicaland moleculardata (see below). Although Dasypogonaceae remain unplaced among the commelinids, three other major commelinid clades have been identified (e.g., Chase et al., 2000; Stevenson et al., 2000): 1) Arecales (Arecaceae);2) a broadlycircumscribed Poales; and 3) a "ZHC"clade consisting of Zingiberales,Commelinalesand Hanguana. However, phylogeneticrelationshipsbetween these clades remain unresolved, pending furtheranalyses. A stable phylogeny is critical in evolutionary assessments of characterssuch as presence of silica bodies. For example, if Arecaceae are sister to other commelinids, as tentatively indicated by some analyses (e.g., Givnish et al., 1999; Chase et al., 2000), it would seem likely thatthe presenceof silica bodies is a synapomorphy for the commelinidclade and that its absence from some taxa (Table III) representsone or more secondaryreversals. 1. Arecaceae The earliestwork on silica in palms was mentionedabove (see section III, "HistoricalReview"). The first comprehensiveanatomicalstudy of palms was that of Tomlinson(1961b), who describedthe types and distribution of silica bodies in all the majortaxonomic groups. Silica bodies occur in stegmatain continuousor discontinuouslongitudinalfiles adjacentto fiberssheathingvascularbundlesor independent fiberstrands. They aremost frequentin leaves and stems but are also seen next to cortical sclerenchymatous strandsin roots. They do not occur in the epidermis,but hypodermalstegmatamay occasionallyintrudebetween epidermal cells and thereforewrongly appearto be epidermal(e.g., in Borassus: Eberwein, 1903). Thereare two types of silica body and silica cell in palms, in both cases with a single silica body per cell: 1) conical or hat-shaped bodies with a smoothbase, a roughor spiny surfaceand

Table III

Distribution of silica bodies in leaf of Arecaceae (classification of Uhl & D Key: cont. = continuous; discont. = discontinuous; Hat = hat shaped; incl. = includin Sph = spherical; vb(s) = vascular bundles(s). Brackets indicate rare or Subfamily, tribe Coryphoideae Corypheae No. of No. genera studied 31 20 Location of silica in leaf Over fibers, vb or not (incl. transverse vbs) Over fibers, vb or not Over fibers, vb or not (incl. transverse vbs) Type + Sph, spiny Notes

In cont. or discont. basal wall thick stem, fruit

Phoeniceae Borasseae

1 7

+ Sph Sph, spiny (+ Hat in Lodoicea)

In cont. files, basal thick; also stem

In ? cont. files, bas wall thick; also root

Calamoideae Calameae

19

13

Over fibers, vb or not (occ. transverse vbs) Over fibers, vb or not (incl. transversevbs in 1 genus) Over fibers, vb or not

+ Sph, spiny

Lepidocaryeae

+ Sph, spiny

Nypoideae

Hat

In cont. or discont. basal wall thick stem (absent fro root) In discont. files (ba wall thick in 1 g nus); also stem In discont. files, ba wall scarcely th ened

Ceroxyloideae Cyclospatheae Ceroxyleae Hypophorbeae

1 5 5

1 1 4

Over fibers, vb or not Over fibers, vb Over fibers, mainly vb

Sph, large + Sph Hat (+ sand in mesophyll of 1 genus)

In ? cont. files, bas wall ? unthicke In cont. or discont. basal wall thick In cont. files, basal scarcely thicken also stem in 1 g

Table III, continued

Subfamily, tribe Arecoideae Caryoteae Triarteae Podococceae Areceae, except 2 subtribes: No. of No. genera studied 3 6 1 86 3 4 0 35 Location of silica in leaf Over fibers, vb or not Over fibers, vb (not transverse vbs) No data Over fibers, vb or not (not transversevbs) (also mesophyll in 1 genus, epidermis in 1 genus) Over fibers, vb or not Over fibers, vb or not Over fibers, vb or not (incl. transverse vbs) Over fibers, vb or not (& over sclereids in 1 genus) Over fibers, vb or not Type Hat Hat Notes

In discont. files, ba wall scarcely th ened; also stem In cont. files, basal scarcely thicken

? Sph or ellipti-

cal (rarely sand in hypodermis) + Hat to elliptical Hat + Sph (+ sand in 1 genus in hypodermis) Hat

In cont. or discont. basal wall thick stem

Oraniinae Sclerospermatinae Cocoeae, except 1 subtribe: Bactridinae

2 2 22

1 1 8

In discont. files, ba wall slightly thi ened In discont. files, ba wall ? unthick Most in discont. file sal wall thick; a stem, root, fruit

Geonomeae

+ Sph (rarely elliptical) Sph

In cont. or discont. basal wall scarc thickened; also root In cont. or discont. basal wall most thick

Phytelephantoideae

Over fibers, vb or not

In cont. files, basal thick; also stem

SILICA BODIES IN MONOCOTYLEDONS

401

a basal cell wall that is only slightly thickenedand not conspicuouslypitted;and 2) spherical bodies, usually ratherirregular, sometimesmore or less ellipsoidal,also with a rough or spiny surface(Fig. 2C), with a basal cell wall thatis thickened,often pitted,and sometimeslignified or suberizedandwith otherwalls thatare thin. The developmentof the sphericaltype has been studiedby Schmittet al. (1995) in Calamusauxillaris.These two types have not been foundto occurtogetherexcept in Lodoicea,wheremost bodies are sphericalbut wherelarge,hat-shaped veins in the lamina(Tomlinson, ones up to 23 ,umin diameterarepresentadjacentto transverse 1961b). Raphidecrystalsare also common in all partsof palms. silica bodies arepresentin the informal Tomlinson(196 lb) notedthatconical or hat-shaped "iriartoid"and groups, which he designated as "bactroid,""caryotoid,""chamaedoroid," "nypoid" palms, while sphericalbodies occur in the arecoid,borassoid,cocoid, lepidocaryoid, and sabaloidpalms and in some isolated genera. In TableIII his phoenicoid,phytelephantoid data have been rearranged accordingto the classificationof Uhl and Dransfield(1987). Each subtribeusually possesses only one type of silica body, apartfrom Lodoicea of Borasseae. all have sphericalsilica bodCalamoideaeand Phytelephantoideae SubfamiliesCoryphoideae, ies, and Nypoideae have hat-shapedsilica bodies. Ceroxyloideae comprise two tribes with sphericaland one with hat-shaped bodies, while Arecoideaehave some tribesor subtribeswith sphericaland otherswith hat-shapedbodies. 2. ZHC Clade (Zingiberales, Commelinales, and Hanguana) This clade is polymorphicfor presence or absence of silica bodies. In the taxonomically isolated genus Hanguana (Hanguanaceae), silica bodies are presentas irregular granulardeposits, mainly in or near the foliar bundle-sheath cells ratherthan the epidermis(Solereder& Meyer, 1929; Smithson, 1956; Tomlinson, 1969; Rudall et al., 1999; Tillich & Sill, 1999). Hanguanabelongs in a clade togetherwith the ordersZingiberalesand Commelinales,but its within this clade remaindisputed.Morphologicaldataindicatean affinity preciserelationships with Zingiberales(e.g., Rudall et al., 1999), whereas most recent analyses of moleculardata place it within Commelinales(e.g., Chase et al., 2000; APG II, 2003). ApartfromHanguana,thereare four families in the orderCommelinales: Haemodoraceae, Commelinaceae,Philydraceaeand Pontederiaceae(Table IV). Silica bodies are absent from Philydraceaeand Pontederiaceaeand present in only some genera of Commelinaceaeand Haemodoraceae.Evans et al. (2000) did not include presence or absence of silica bodies in theirmorphologicalcladisticanalysisof Commelinaceae. In Commelinaceae, silica bodies had been thought to be restrictedto the tribe Tradescantieae of the subfamily Commelinoideae (Tomlinson,1969), where they represented a relativelyconsistentpotentialsynapomorphy for this group, although silica bodies are absent from some genera that were embeddedwithin Tradescantieaein the morphologicalanalysis, such as Murdannia(Faden & Inman, 1996). However, Faden (pers. comm., 2003) has also observed silica bodies in Dictyospermum,a genus of the tribe Commelineae,which appearas large, silica infillings of the cell. These bodies differ greatlyfrom the epidermal(severalper cell) small, sphericalspinulosebodies of the Tradescantieae thatare often embeddedin the outercell wall (Fig. 2D). One exceptionto these sphericalbodies is a possible observationof epidermalsilica sand in Zebrinapendula. This mirrors observationsin Haemodoraceae, wherethe silica almostalways takesthe form of silica sand, the only exception to this being rare sightings of sphericalbodies, possibly formed by sand coalescence, in two generathat also possess sand. Presence of silica sand is restrictedto the subfamily Conostylidoideae(Prychid et al., 2003) and is mainly located in the vascular bundle-sheath cells (Fig. 2E), resemblingthe case in Hanguana.Only one genus (Anigozanthos) has exclusively epidermalsilica sand (Fig. 2F).
(Textcontinues on p. 406)

Table IV

Distribution of silica bodies in Hanguana and Commelinales (tribes based on classific "Basal wall thickened" refers to the wall adjacent to sclerenchym Silica presence/location Hanguana (1 genus; 5+ spp.; silica seen in 1 sp.) 1) Endodermoid sheath cells; 2) Hypodermis, occasionally in mesophyll Type & no. per cell 1) Small, irregular, granular;several per cell; 2) Large bodies

No

Ce

Commelinaceae (2 subfamilies, 4 tribes, 41 genera, 650 spp.) Cartonemoideae Cartonemateae Cartonema (6 spp., 2 examined) Triceratelleae Triceratella (1 sp., 1 examined) Commelinoideae Tradescantieae(several genera not examined) SubtribePalisotinae Palisota (18 spp., 4 examined) SubtribeCyanotinae Belosynapsis (4 spp., 2 examined) Cyanotis (50 spp., 1 examined)

Absent Absent

Absent Absent Epidermis, intercostal

Small, spherical, spinulose, up to lOum, few to many per cell Small, spherical, spinulose, up to 1Oum, few to many per cell Small, spherical, spinulose

No

SubtribeColeotrypinae Amischotolype (Forrestia) (20 spp., 1 examined) Coleotrype (9 spp., 1 examined)

Epidermis, costal & intercostal Epidermis, costal, rarely intercostal

In

Al

SubtribeDichorisandrinae Cochliostema (2 spp., 2 examined) Dichorisandra (25 spp., 2 examined) Geogenanthus (5 spp., 1 examined) Siderasis (2/3 spp., 1 examined) SubtribeThyrsantheminae Tinantia(13 spp., 1 examined) SubtribeTradescantiinae Callisia (incl. Hadronemas) (20 spp., 7 examined)

Absent Absent Absent Absent Absent Epidermis, costal

Gibasis (17 spp., 6 examined)

Tradescantia(incl. Campelia and Zebrina) (ca. 70 spp., 17 examined)

Tripogandra(21 spp., 3 examined)

Als 1) Small, spherical, spinulose, up to 10 ,um, few to many per cell; 2) Tiny, 1-2 ,m, many in outer cell wall Epidermis, costal, and in- Small, spherical, spinuAls tercostal lose, 3-8 ,m, few to many per cell; also on outer wall Present in some species; 1) Small, sperical, spinu- See epidermis, costal, lose; 2) Silica sand rarely intercostal seen in Zebrina, although not by Tomlinson, 1969 Epidermis, costal Als 1) Small, spherical spinulose; 2) Tiny, 1-2,um, many in outer cell wall Absent Absent

Commelineae (several genera not examined) Aneilema (64 spp., 8 examined) Anthericopsis (1 sp., 1 examined in Tomlinson) Commelina(170 spp., 1Oexamined)

Absent

Table IV, continued Silica presence/location Commelinaceae,continued Commelinoideae, continued Commelineae, continued Dictyospermum(5 spp., 1 examined) Floscopa (20 spp., 2 examined) Murdannia(50 spp., 5 examined) Pollia (17 spp., 5 examined) Polyspatha (3 spp., 2 examined) Stanfleldiella (4 spp., 1 examined) Haemodoraceae(2 subfamilies, 14 genera, ca. 81 spp.) Conostylidoideae Anigozanthos (ca. 10 spp., 7 examined) Absent Absent Absent Absent Absent Type & no. per cell

No

Large, silica infillings of the cell

Epidermis

Sand

Sa

Blancoa (I sp., I examined)

Conostylis (ca. 25 spp., 14 examined)

1) Bundle-sheath cells in Sand leaf blade; 2) Adaxial epidermal cells of leaf sheath 1) Bundle sheath cells; Sand 2) Palisade mesophyll cells, in some spp.; 3) Spongy parenchyma cells, in some spp.; 4) Rarely, unlignified adaxial epidermal cells of leaf sheaths

Oc

Macropidia (1 sp., I examined) Phlebocarya (3 spp., 3 examined)

Small amounts of sand Bundle-sheath cells 1) Bundle sheath cells; 2) Sand Epidermalcells

Sm

Tribonanthes(5 spp., 1 examined) Haemodoroideae (several genera not examined) Dilatris (5 spp., 3 examined) Haemodorum (20 spp., 6 examined) Lacnanthes (I sp., I examined) Wachendorfia(5 spp., 2 examined)

Bundle-sheath cells Absent Absent Absent Absent

Small amounts of sand

Philydraceae(4 genera, 5 spp.) Helmholtzia, Orthothylax,Philydrum, Absent Phildrella (all species examined) Pontederiaceae(9 genera, 33 spp.) 5 genera, ca. 20 spp. examined Absent

406

THE BOTANICAL REVIEW

Withinthe orderZingiberales,silica bodies arepresentin all families (TableV) (Tomlinson, to the vascularbundle-sheath cells (in Cannaceae(Fig. 3A), Costaceae 1969), mostly restricted (Fig. 3B), Heliconiaceae (Figs. 3C, 3D), Lowiaceae (Fig. 3E), Marantaceae(Figs. 3F, 3G), Musaceae(Figs. 4A, 4B), and some generaof Strelitziaceae (Figs. 4C, 4D), often in a hypodermal region adjacentto bundle-sheath Thereare occasionalrecordsof silica bodsclerenchyma. ies in other mesophyll cells (Heliconiaceae,Marantaceae, Zingiberaceae),and they are also present in the epidermisin Phenakospermum (Strelitziaceae)and most Zingiberaceae(Figs. 4F, 4G) (Tomlinson, 1969). Silica bodies in Zingiberalesare druse-like(i.e., sphericalwith a rugose surface) in most genera, but with some exceptions: they are more or less conical in Orchidantha (Lowiaceae) (Fig. 3E) and some Marantaceae, "troughshaped"(i.e., rectangular with a centralshallow depression)in most Heliconiaceaeand Musaceaeandpresentas epidermal silica sand in some Zingiberaceae,rarely in Marantaceae,Strelitziaceaeand Musaceae (Fig. 3H). Kress et al. (2001) discussed evolutionaryrelationshipsof Zingiberalesfamilies using molecularand morphologicaldata.They concludedthat Zingiberalesare monophyletic, with three sets of sister families: Strelitziaceae+ Lowiaceae, Costaceae+ Zingiberaceaeand Cannanceae+ Marantaceae. Of these, Costaceaeand Marantaceae have broadlysimilarsilica body types and locations, Lowiaceae and Strelitziaceaehave bodies in similar locations but differentshapes,CostaceaeandZingiberaceae differin thatCostaceaehave bodies over sclerenchymatousbundle sheaths,while Zingiberaceaehave predominantly sand or small bodies in epidermalcells. 3. Poales A broadcircumscription of the orderPoales is now widely adopted(e.g., APG, 1998; Chase et al., 2000;APG II,2003). Therearetwo well-definedmajorclades,the sedge clade(Cyperaceae, Juncaceae,Thumiaceaeand Prioniaceae)and the grass clade (Poaceae, Restionaceaeandtheir allies), plus several other families (Bromeliaceae,Hydatellaceae,Mayacaceae,Rapateaceae, andXyridaceae) Sparganiaceae, Typhaceae whose relationships remainunresolved. Silicabodies are absentfrom several families of Poales (TableVI), andthis may representa synapomorphy for some groups. In particular, the absence of silica bodies in Hydatellaceaemay supporta putative relationship between them and Xyridaceae, Eriocaulaceae and Mayacaceae (Michelangeliet al., 2003), all of which lack silica bodies.In contrast to manyothercommelinids (especiallyZingiberalesandpalms), in most Poales thatpossess silica bodies they arerestricted to the epidermis, with the exception of some species of Bromeliaceae, Ecdeiocoleaceae, Flagellariaceae, Joinvilleaceae,Juncaceae, Restionaceae(TableVII) andThumiaceae,in which they occur in other tissues, especially the vascularbundle sheath. In Rapateaceae,all genera possess characteristic sphericalsilica bodies in the epidermis(Table VIII) (Carlquist,1966; Carlquistin Tomlinson, 1969), rathersimilarto those of Commelinaceae-Tradescantieae, althoughthis must be regardedas a homoplasy,since the two groupsbelong in differentclades within the commelinids. In the sedge clade, silica bodies are common in most groupsof Cyperaceae(TableIX), in which they possess a conical form, often with small spines (satellites) aroundthe base (Figs. 5A, 5B), but rareor absentin some generaof the sedge tribeHypolytreae,which is the putative sister groupto the rest of the family (Muasyaet al., 1998, 2000). The distribution andtypes of silica bodies in leaves of Cyperaceaehave been describedby Metcalfe (1971), who summarized early work on the family; subsequentresearchhas extended the observationsbut not alteredthe main conclusions. The most characteristic type of silica body is conical, with the base resting on the usually thickened, inner periclinal wall of an epidermalcell (rarely on anticlinalor outerpericlinalwalls). Theremay be one to numerousbodies per cell on a single
(Textcontinues on p. 422)

Table V

Distribution of silica bodies in Zingiberales (classification from Kubit Key: LS = longitudinal section; par = parenchyma; scl = sclerenchyma; vb(s) = Basal wall refers to wall adjacent to sclerenchyma. Silica presence / location in leaf Cannaceae(Igenus, 10-25 spp.) Canna (4 spp. examined) Over vb scl sheath; hypodermis Type & no. per cell Druse-like, 1 per cell, in thin-walled cells, in files in LS Druse-like to irregularly spiny, 1 per cell; cells often forming complete layer aroundvbs 1) Trough shaped; spines projecting from base into pits in wall; 1 per cell; 2) irregularlyspherical, 1 per cell + Conical; top may be truncated, I per cell; small fingers of silica may project from the base of the body into the cell wall

Notes

In pe n

Costaceae (4 genera, 100 spp.) Costus (3 spp. examined); Tapeinochilus(1 sp. examined) Heliconiaceae (1 genus, 200 spp.) Heliconia (14 spp. examined)

Over vb scl sheath

In pe n

1) Over vb sheath fibers & over par sheath; 2) Palisade of 1 sp.

Basa in st ro

Lowiaceae (1 genus, 10 spp.) Orchidantha(3-4 spp. examined)

Over vb fibers

Basa in pe

Table V, continued Silica presence / location in leaf Type & no. per cell

Note

Marantaceae(31 genera, 550 spp.; no currentlyaccepted subfamilies or tribes) 17 genera, 37 spp. examined 1) Over vb scl sheath (rarely hypo- 1) Hat shaped, base flat; dermis); 2) Over scl of transnodular or spiny, up to verse vbs; 3) Mesophyll, below 20,um, 1 per cell; 2) As palisade in 1), but smaller, 1 per cell; 3) Druse-like, up to 35 m, 1 per cell

Calathea, Ctenanthe,Ischnosiphon, Maranta, Monotagma, Stromanthe,etc. Donax, Saranthe Musaceae (2 genera, 40 spp.) Ensete (4 spp. examined); Musa (ca. 25 spp. examined)

Mesophyll, usually in palisade

Druse-like, or elongated, most small, 3-5 gm (up to 20 ,um in Ctenanthe) Sand 1) Rectangularin surface view, with central shallow depression (trough shaped) ; spines projecting from base into pits in wall, 1 per cell; 2) Irregularly spherical, 1 per cell

1) Ba ce 2 ce te in la c v g a r b o Possi o o

1) Over vb sheath fibers; 2) In parenchymatous sheath of transverse vbs & occasionally in transverse septa

In fil a d se a

Strelitziaceae (3 genera, 6 spp.) Phenakospermum(1 sp. examined)

1) Over vb sheath fibers & girders; also in transverse septa; 2) Epidermis over scl 1) Over vb sheath fibers & girders; also in transverse septa; 2) Epidermis over scl 1) Over vb sheath fibers & girders; also in transverse septa; 2) Epidermis over scl

Ravenala (1 sp. examined)

Strelitzia (4-5 spp. examined)

1) & 2) Spherical, spiny, in thin-walled cells, 1 per cell; 1) Sand may also be present 1) & 2) Spherical, spiny, in thin-walled cells, 1 per cell; 1) Sand may also be present 1) & 2) Spherical, spiny, in thin-walled cells, 1 per cell; 1) Sand may also be present 1) Small, irregularlyspherical, 1 per cell; 2) Sand Sand; Kaempferia: small, irregularly spherical, 1 per cell 1) Small, irregularlyspherical, 1 per cell; 2) Sand Sand

In file n

Zingiberaceae (50 genera, ca. 1300 spp.) Alpinieae (21 genera, ca. 700 Epidermis over scl (internal in spp.) (8 genera, 15 spp. Hornstedtia conica only) examined) Hedychieae (19 genera, ca. 300 Epidermis (rarely mesophyll, vb spp.) (9 genera, 23 spp. sheath) (internal in Kaempferia examined) only) Zingibereae (1 genus, ca. 100 Epidermis over scl spp.) (Zingiber: 2 spp. examined) Globbeae (4 genera, ca. 110 Vb sheath spp.) (Globba: 4 spp. examined)

Sand ro E

Smal co co G (P

410

THE BOTANICAL REVIEW

oooi

~~~~~~~~~~~~~~~~~~~~

found in the orderZingiberales. A. Cannaedulis (Cannaceae), Fig. 3. Varioussilica body morphologies 1 a_m). druse-likesilica bodies over vascularbundlesheath(bar I0 B. Costusenglerianus(Costaceae),druselike silica bodies over bundle-sheath cells (bar =20 Am). C. Heliconiapsittacorum(Heliconiaceae), troughshaped silica bodies over vascular bundle-sheath fibers (bar = 20 Am). D. Heliconia aff. tortuosa silica bodieswith silica fingersprojecting fromthe base intothe cell wall (bar (Heliconiaceae), trough-shaped = 10,4.m).E. Orchidantha conical silica bodiesoverlyinga vascularbundle(bar= sp. (Lowiaceae),truncated 10 /Ltm). F. Marantaarundinacea(Marantaceae), costal silica bodies in mesophyll cells (bar = 10 nm). a druse-likeintercostalsilica body in a mesophyllcell (bar = 20 G. Marantochloa purpurea(Marantaceae), H. Musaschizocarpa(Musaceae),intercostal, silica sand (bar= 10 Atm). akm). epidermal

SILICA BODIES IN MONOCOTYLEDONS

411

Fig. 4. Varioussilica body morphologiesfound in the orderZingiberales,continued.A. Musacoccinea silica bodies overlyinga vascularbundle(bar 1 I0 /tm). B. Musasp. (Musaceae), (Musaceae),trough-shaped silica bodies with silica fingers projectingfrom the base into cell-wall pits (bar= 10 gm). trough-shaped C. Ravenala madagascariensis(Strelitziaceae),spiny silica bodies in vascularbundle-sheathcells (bar = 10 /.tm).D. Strelitziaaugusta (Strelitziaceae),a bundle-sheath cell containinga druse-likesilica body (bar = 20 gtm). E. Kaempferia aethiopia (Zingiberaceae), an internal costal silica body (bar = 10 gtm). F. Hornstedtia conica (Zingiberaceae), epidermal, intercostal silica sand (bar = 10 /.tm). G Alpinia conchigera Zingiberaceae), two forms of silica: intercostal silica sand and costal spherical bodies in epidermalcells (bar = 10 gm).

Table VI
Distribution of silica bodies in Poales. Key: LS = longitudinal section; scl = sclerenchyma; vb = vascular Silica presence / location Anarthriaceae(1 genus, 7 spp.) Anarthria(5 spp. examined) Absent Spherical, spinulose, up to 10,um, 1 per cell; bodies larger over scl, may be absent from cells over thin-walled hypodermis Spherical, spinulose, aggregates of several per cell Silica sand Type & no. of silica bodies per cell

Not

Bromeliaceae (56 genera, 2600+ spp.) Most genera (37 genera, 106 spp. examined) Epidermis, intercostal & costal

Out

Cryptanthus(1 sp. examined) Tillandsia(20 spp. examined)

Epidermis, intercostal & costal Epidermis, intercostal

Pre

8 genera (some spp.)

Outer bundle sheath

Silica sand (Irregular,in 1 sp.) (Particles or sand in 2 spp.) (Rectangular,in 1 sp.)

Centrolepidaceae(3 genera, 35 spp.) Aphelia (5 spp., 5 examined) (Epidermis) Centrolepis (c. 28 spp., 10 (Epidermis, ground tissue) examined) Gaimardia (3 spp., 3 exam(Epidermis) ined) Cyperaceae(104 genera, 5000+ spp.) Most genera & 86 spp. examEpidermis, costal (rarely inined tercostal)

Sili Sili

Sili

Conical +/- satellites (rarely nodular, bridges, other types)

See

Ecdeiocoleaceae (2 genera, 2 spp.) Ecdeiocolea (1 sp., I examChlorenchyma(culm); epiined) dermis, costal (culm) Eriocaulaceae(10 genera, 700-1400 spp.) 9 genera (6 examined) Absent Flagellariaceae (1 genus, 4 spp.) Flagellaria (1 sp. examined)

Sand (culm)

Non

N/A

Above & below vb fibrous sheaths

Small, irregular,in small cells; I per cell N/A N/A 1) Smooth cubical bodies, 1 per cell, filling lumen; 2) Irregularnodular bodies, 1 per cell; cells in files in LS N/A

Nev

Hydatellaceae (2 genera, 10 spp.) Hydatella (2 spp., 1 examined) Absent Trithuria(3 spp., 2 examined) Absent Joinvilleaceae (1 genus, 2 spp.) Joinvillea (2 spp. examined) 1) Epidermis, short cells; 2) Vb fiber sheath

Sho

Juncaceae(7 genera, 350 spp.) Marsippospermum, Rostkovia, Distichia, Patosia, Oxychloe, Luzula Juncus Mayacaceae (1 genus, 4-10 spp.) Mayaca (4 spp., 3 examined)

Absent

1) Vb fiber sheath; 2) Rarely mesophyll Absent

Sand

N/A Many shapes, not usually conical or spherical

Poaceae (700+ genera, 10,000+ spp.) Epidermis

Abs s d l

Table VI, continued

Silica presence / location Prioniaceae(1 genus) Prionium Rapateaceae(16 genera; 80 spp.) Epidermis Spherical; see Table VIII for details Absent Type & no. of silica bodies per cell N/A

Not

See

Restionaceae (55 genera; 490 spp.) 1) Bundle sheaths; 2) Parenchyma sheath, ground tissue Thumiaceae (I genus; 3 spp.) Thurnia(2 spp. examined) 1) Spherical-nodular;2) Irregularor granular

Sili

Epidermis (1 sp.); Parenchyma

(1 sp.)

Nodular, several per cell, over scl; sand

Als

Typhaceae(2 genera; 16-30 spp.) Sparganium (14 spp., 10 examined)

Absent

N/A

Typha(8-13 spp., 8 examined)

Absent

N/A

Xyridaceae (5 genera; 300 spp.) Abolboda, Achlyphila, Aratity- Absent opea, Orectanthe,Xyris

N/A

Table VII
Key: Abs
=

Distribution of silica bodies in culm of Restionaceae (classification of Lind absent; chlor = chlorenchyma; epid = epidermis; par = parenchyma; scl = scleren Brackets indicate rarely present or present in a few taxa. Genera for which no data are available have been omitted from the No. of species No. studied 2 3 1 1 or 2 Distribution Australia Australia Type and location in culm Abs Abs Notes

Genus Hopkinsia Lyginia

Now Hop separ Crystals separ Hygi

Staberoha Ischyrolepis Elegia Chondropetalum, Dovea, Askidosperma Platycaulos, Restio

ca. 9 ca. 48 ca. 35 ca. 24

5 1+? 21 16

South Africa South Africa South Africa South Africa

Abs + Sph in par sheath & ground tissue Abs Abs

ca. 100

ca. 60

South Africa, Zaire, Madagascar

Calopsis

ca. 23

South Africa

Thamnochortus

ca. 34

20

South Africa

Sph in par sheath (& chlor); granularin par sheath &/or ground tissue, protective cells, chlor; Abs in many spp. Abs in 5 spp.; Sph in par sheath or chlor (2 spp.); irregularin protective cells (1 sp.) Abs (irregularin epid in T bachmannii only)

Restio gr ler; a spp. n gener

South Af pus s

Granula bund body Possi T sca pers.

Table VII, continued

Genus Rhodocoma Ceratocarya Cannomois Anthochortus Mastersiella No. of species No. studied 7 ca. 6 ca. 7 ca. 15 3 2 1? 6 2+? 3? Distribution South Africa South Africa South Africa South Africa South Africa Type and location in culm Abs Sph in par sheath Sph in par sheath & scl ribs Sph in par sheath Notes

Hypodiscus Willdenowia

ca. 15 ca. 12

ca. 9 7

South Africa South Africa

Incl. Phy Hypo Sph in scl sheath; granular Incl. Hyp in ground tissue or Abs Sph in scl sheath or Abs

Lepyrodia

22

ca. 9

Australia

Sporadanthus Calorophus Empodisma Coleocarya Desmocladus Harperia

7 2 2 1 16 4

5 1 2 1 ? 1

Australia, New Zealand Australia Australia, New Zealand Australia Australia Australia

Sph in par sheath or scl sheath; granularin ground tissue Sph, 1 per cell in epid; granularin ground tissue (some spp.) & par sheath (1 sp.) granularin epid (2 spp.); Abs (3 spp.) Abs Sph in par sheath; granular in ground tissue Sph in par sheath

Lepyrod Cutle

Lepyrod rada See also 2 spp. se Calo

Incl. in H ler Sph in scl sheath; irregular & granularin epid & ground tissue Sph in par sheath, 1 per cell

Onychosepalum

Australia

Lepidobolus

Australia

Australiangenera separatedfrom Restio Dielsia

ca. 36

24

Australia

Australia

Loxocarya Leptocarpus, Meeboldina

5 13

5? ca. 8

Australia Australia

Hypolaena

Australia

Chaetanthus Dapsilanthus Apodasmia

3 4

1 1? 2?

Australia Australia, Southeast Asia, New Guinea Australia, New Zealand, Chile

Sph in par sheath & ground tissue; granular in ground tissue Sph in par sheath or scl Restio gr sheath in most spp.; in Cu (granularin ground tissue in few spp.) Sph in par sheath Sand in la media centr bund chid, Sph in par sheath or scl sheath African L Sph in par sheath or scl sheath; irregularor now i granularin pillar cells, chlor, ground tissue Sph in scl sheath Hypolaen Cutle spp.) Sph in par sheath; granular in pillar cells Sph in scl sheath Separate pus; a Cutle Sph in scl sheath; granular Separate in chlor, ground tissue, pus; a hairs L. sim

Table VIII

Distribution of silica bodies in Rapateaceae (14 genera; 80 sp (data from Carlquist, 1966; Carlquist, in Tomlinson, 1969; Prychid, p Type and location Saxofridericioideae Saxofridericieae:Epidryos (1 sp. examined), Phelpsiella (1 sp. examined), Saxofridericia (2 spp. examined), Stegolepis (2 spp. examined), Amphiphyllum(1 sp. examined), Marahuacea not examined Rapateoideae Rapateae:Rapatea (7 spp. examined), Cephalostemon (1 sp. examined), Duckea (3 spp. examined), Spathanthus(2 spp. examined) Present in leaf epidermis; small, spherical, rough or spiny; several per cell

Monotremeae:Monotrema(4 spp. examined), Maschalocephalus (1 sp. examined), Potarophytum (1 sp. examined), Windsorinanot examined

Present in leaf epidermis, sometimes over fibers in Rapatea; in Rapatea, Cephalostemon and Duckea spherical, rough or spiny, several to many per cell; in Spathanthuslarge, rough, 1 per cell or aggregates of sand Present in leaf epidermis; spherical, rough or spiny, several to many per cell, and/or silica sand

Table IX

Distribution of silica bodies in leaf of Cyperaceae (classification of Goetg Key to location: Abs = absent; epc = epidermis, costal regions; epic = epidermis par = parenchyma; subep = subepidermis; vb = vascular bund Key to type: Br = bridge; C = conical; C+sat = conical with satellites; Nod = nodular; Pyr = py Brackets indicate occasionally present or present in a few tax Subfamily, tribe Mapanioideae Hypolytreae No. of genera 9 No. studied 8 Type of silica, no. of bodies per cell and location in leaf Abs or C, Br, wedges (warty), 1-3(-l 1) per cell, in epc/epic (subep) Abs or C (C+sat) in epc C (C+sat), (Nod), 1-2 or numerous in 1(-3) rows in epc Notes In sinuations of anticlinal walls (rarely in lumina) Walls may be silicified Also on outer walls; also in culm, rhizome, achene

Refe

Pfei 1

Chrysitricheae Cyperoideae Scirpeae

4 6

3 3

Pfei

Fuireneae

C (C+sat), 1-5+ in epc; plates, rods in epic C+sat (elongated), 1-20+ in 1(-2) rows in epc

Also in culm, achene; in wall sinuations Si projections of vb sheath cell walls; also in culm, achene (Rarely in sinuations of anticlinal walls, epic); occasionally in culm, achene Also in culm and achene

Eleocharideae

Abildgaardieae

C+sat (C, Nod), 1-4(-8) in 1(-2) rows in epc

Cypereae

19

10

C+sat (Nod), 1-8(-10) in 1(-2) rows in epc (+ epic in 1 genus & over vb sheath in 1 genus)

Duv 1 S O D Duv d a Heib 1 1 D Rikl 1 G 1 Duv 1 1 1 G M

Table IX, continued Subfamily, tribe No. of genera No. studied 2 24 Type of silica, no. of bodies per cell and location in leaf C (C+sat), 1-5+ in epc C (C+sat), (Nod, Pyr), 1-6-numerous in epc (epic); C, cubical, rods, warty, spicules (wedges), 1-3+ in epic; (C, 2+ in par vb sheath) C (C+sat), (domed), 1-4 in 1(-2) rows in epc/epic C (C+sat), (Nod), 1-numerous in 1(-3) rows in epc (epic) C (C+sat); warty, 1-3(-7) in epc; Sph etc., 1-2 in epic Notes Also in culm Rods etc. in wall sinuations; also C on outer walls; warty may be in pairs on opposite sides of anticlinal walls; also in culm, rhizome, root, achene

Refe

Cyperoideae, continued Dulichieae 3 Schoeneae 29

Pfei c Duv P P

Sclerioideae Cryptangieae Trilepideae

4 4

4 4

Pfei May be 2 sizes; also in culm

Pfei

Sclerieae

Bisboeckelereae

C (C+sat), (Nod), 1-3+ in epc; Sph, warty, 1-2(-3), & particles in epic C+sat, (Nod), 1-6(+) in 1(-2) rows in epc (epic)

Sph in pairs on opposite sides of anticlinal walls; Si particles in wall sinuations; also in culm & achene Sph etc. in pairs on opposite sides of anticlinal walls; also Si in mesophyll Rarely over sclerenchyma of vb sheath; also in culm, achene

Cril

Pfei

Caricoideae Cariceae

Duv

& K

SILICA BODIES IN MONOCOTYLEDONS

421

6,

Fig. 5. Varioussilica body morphologiesfound in the orderPoales and in Dasypogonaceae.A. Carex intermedia(Cyperaceae),lateralview of a conical silica body with tiny spines projectingnear the base B. Abildgaardiamonostachya(Cyperaceae),conical bodies with satellites in epidermnis (bar 10 Axm). cells (bar= 20 /am). D. Juncus (bar 10 Arn).C. Juncus inflexus(Juncaceae),silica sand in bundle-sheath arabicus (Juncaceae), silica sand in vascular bundle-sheath cells (bar = 10 Atm).E. Thamnochortus of silica observed in epidermnal cells (bar =10 floribundus (Restionaceae),an irregularor granularformn Am). F. Anthochortusecklonii (Restionaceae), spherical silica bodies overlying the sclerenchymatous 10 m) G. Thurniaj'enmanil.(Thumiaceae), numerous small spherical/nodular bundle sheath (bar IO 1 Axm). bodies in epidermalcells (bar I0 H. Kingia australis (Dasypogonaceae), sphericalsilica bodies with a rugose surface in epidermalcells (bar = 10 Atm).J. Dasypogon bromeliifolius(Dasypogonaceae),
epidermal silica sand (bar = 20 Am).

422

THE BOTANICAL REVIEW

basal plate (Le Cohu, 1973), most frequentlyin one row per cell as seen in surfaceview but sometimes in two or threerows. Silica cells often occur in longitudinalfiles; thereis no differof Poaceae,with rareexceptions(bractof entiationinto long cells and shortcells characteristic Epischoenusvillosus and Mesomelaenastygia). The numberof bodies and rows per cell may be diagnosticfor a species, but there is always a range of values, and variationdue to age of leaf, environmentalconditions, etc. must be taken into account (see Ollendorf, 1992). Each as seen in surface large cone may be surrounded by a circle of small cones, termed"satellites," view; the extent to which satellites are developed tends to vary within a species. to the wartyor nodular A conical body may have two or more peaks, when it is transitional type, which may be conical, spherical or irregularlyshaped. In certain genera and species, smooth or warty hemisphericalbodies are formed on anticlinalwalls of adjoiningepidermal 1969b, 1975; Metcalfe, 1971). Other cells; e.g., in Rhynchosporaand Scleria (Govindarajalu, types of body have been describedas wedge shaped,often based on sinuationsin the anticlinal of walls, or bridge shaped,when they traversethe cell lumina;these types are characteristic Hypolytreae.In certaingenera,small silica particles,rods, plates or cubicalbodies may occur, especially in intercostalregions,where individualcells, includingstomatalguardor subsidiary cells and prickles,may be completely silicified. Silica cells occurboth adaxiallyandabaxiallyin the leaf epidermis,butthe frequencyvaries sclerenchymastrandsor girders,which in some genaccordingto the numberof subepidermal era are nearly equally numerouson both surfaces, while in others they are more numerous abaxially(rarelyadaxially).Silica bodies are sporadicallypresentin intercostalregions of the cells (e.g., in the leaf of Cladiumarticulatum: epidermisandrarelyin mesophyll or diaphragm cells overlyingthe Peisl, 1957). Kaphahn(1904-1905) noted silica bodies in parenchymatous sclerenchymatous vascularbundle sheathand at bordersof sclerenchymagirdersin the leaf of Cladiumgermanicum.They were seen in a similar position by Pfeiffer (1921b) in leaf and culm of Cyperusmariscus. Silica bodies, usually of similartype to those in the leaf, arepresentin the epidermisof leaf sheathandculm and,rarely,in otherpositions;for example,in cells overlyingvascularbundles. Silica projectionsfrom parenchymatous bundle-sheathcell walls borderingair cavities were observedin Eleocharisplantaginea culm by Schilling (1918) and Mehraand Sharma(1963). Bodies have been observed infrequentlyin the rhizome (Wille, 1926) and rarely in the root 1975). (e.g., in some exodermalcells of Rhynchosporaspp.: Govindarajalu, Wilczek (1892) was one of the first to investigateachenes of Cyperaceaefor silica bodies. He examinedseven generabut found bodies only in Carexspecies, where therewas one conical body per epidermalcell. More recently,several taxonomic studieshave includedobservations of bodies in achenes, often using SEM; e.g., Bulbostylis (Goetghebeur& Coudijzer, 1985), Carex(Walter,1975;Toivonen& Timonen,1976;Wujek& Menapace,1986;Menapace & Wujek, 1987; Crins & Ball, 1988; Standley, 1990; Waterway,1990; Lucenfo,1992; Oh & Lee, 2001; Oh et al., 2001; Starr& Ford, 2001), Eriophorumand Scirpus (Schuyler, 1971; & Vanden Borre, 1989), Tucker& Miller, 1990), Lipocarphaandrelatedgenera(Goetghebeur Rhynchospora (Ragoneseet al,. 1984) and Uncinia(Starret al., 2003), althoughnone was seen in 3 species of Abildgaardiaor 19 species of Fimbristylis(Goetghebeur& Coudijzer,1984). TableVIII shows the type and numbersof silica bodies in the leaf of tribesof Cyperaceae. The data are taken mainly from Metcalfe (1971), but the observationsfor individualgenera have been regroupedaccordingto Goetghebeur'sclassificationin Kubitzki(1998), to which the numbersof genera refer. The conical type (+ satellites) is dominantin epidermalcells which together overlying sclerenchymain all tribes except Hypolytreaeand Chrysitricheae, constitutethe Mapanioideae; to smallcones in sinuations here silica bodies areabsent,restricted

SILICABODIESIN MONOCOTYLEDONS

423

of anticlinalwalls, or wedge or bridgeshaped,rarelyof the typical conical type. The composition of the Mapanioideaehas not changed since Clarke's (1908) classification, except that with conicalbodies,has beenremovedandincludedin Rhynchospora. TheCariceae Syntrinema, have also remainedalmost unalteredand are characterized by 1-5 or more conical bodies with satellitesper cell, sometimes in two rows. An alternativesuprageneric classification,based on cladistic analyses of 122 generausing was proposedby Bruhl(I995); he included morethan300 morphologicalandothercharacters, and his articleshould be silica body type and position in culm and leaf among his characters, consulted for a full discussion of the differences between his classification and that of Goetghebeur(1986). Conical silica bodies are typical for most Cyperaceae,but they are not confined to this andArecaceae,althoughin the family; for example,they are also presentin some Orchidaceae two latterfamilies there is usually only one body per cell, and they are never epidermal. Although Prionium was traditionallyplaced either in Juncaceae or in its own family, Prioniaceae (Munro& Linder,1998), analysesof moleculardataplace it as sisterto Thumiaceae (e.g., Chase et al., 2000; Michelangeli et al., 2003). However, silica bodies are apparently absent from Prionium and all Juncaceaeapartfrom Juncus, which possesses silica sand in vascular bundle-sheathcells (Figs. 5C, SD), but present in Thurnia(Cutler, 1965, 1969) as small, spherical bodies (Fig. SG). Thus, this distributionof silica bodies may indicate two separatelosses of silica bodies in the sedge clade. There is also at least one loss of silica bodies in the grass clade. Flagellaria, which possesses silica bodies, is sisterto two subclades,one comprisingRestionaceaeandtheirallies; the other, grasses and their allies. In the first subclade, three genera (Anarthria,Hopkinsia and Lyginia) form a clade that is sister to Restionaceae. Hopkinsia and Lyginia are former Restionaceaethatwere recentlyproposedas separatefamilies, Hopkinsiaceaeand Lyginiaceae (Briggs & Johnson,2000), since a molecularanalysis (Briggs et al., 2000) found them to be isolatedfromRestionaceaeand sisterto Anarthria(Anarthriaceae). all threegenInterestingly, era (Anarthria, lack silica bodies. Hopkinsiaand Lyginia) apparently Solerederand Meyer (1929) were the first to recognize silica bodies in Restionaceae,but the first major anatomicalstudy was by Cutler(1969); his observationswere confirmedby Linder(1984). TableVII is based on Cutler's(1969) data,rearranged accordingto the classification of Linderet al. (1998). Many generaare leafless, and most availabledataare for culms. Silica bodies occur in the leaf or leaf base of a few species and occasionally in rhizomes but have not been seen in roots. The recent taxonomy of Restionaceae is complex, with many genera and species transferred to differenttaxa (Linder,2000). Cutler's(1969) work showed that there were anatomicaldifferencesbetweenAfrican andAustralianspecies that had previously been placed in the same genera;e.g., Restio andLeptocarpus.Certainspecies have subsequentlybeen transferred to othergenera,so thatthere is now no genus with a distribution in both SouthAfrica andAustralia.Silica is absentfrom severalgeneraand from some species in other genera. When present, silica is found in two main forms in Restionaceae: 1) granular silica, usually filling cell lumina,in cells of parenchymatous sheath and centralgroundtissue andoccasionallyin pillarcells, protectivecells (see Cutler,1969, for definitionsof these terms) and chlorenchymabut rarely in the epidermis (Fig. 5E); and 2) spherical-nodular bodies in unspecializedcells or in stegmata,formingpart of the parenchymatous bundle sheath or the outer layer of the sclerenchymatoussheath (Fig. SF). Stegmatahave thickened, lignified or suberizedinner and anticlinalwalls and thin outer walls. Both types may be present in one species, andthey occur in both SouthAfricanandAustralianspecies, as does absenceof silica. Cutler(1969) dividedLepyrodiaspecies into two main groupsbased on anatomicalcharacters,

424

THE BOTANICAL REVIEW

Fig. 6. Variousilicaboymorphoogiesfondinthe rl cs of P . A. A a s costal dumbbell-shaped silicabodies(bar 10lpm).B. Brachiariajubata, a_ form of silica_termediate

lines6 (bariou20silmca saddle-shapednsilicas bodiesc(bar A.10risLm)a GeAgropron F.dAstoebhaogiquarrosa a conicalsilicabody(bar 20 Am) elongatum, one of which was the presence of granularsilica alone in one group and spherical-nodular bodies in the othergroup;species in the groupwith only granularsilica have since been transferred to Sporadanthus.Silica bodies have not been observed in any species examined of Staberohaor in the large generaElegia and Chondropetalum. In the othergrass subclade(grasses and their allies), the bigeneric family Ecdeiocoleaceae is putatively sister to Poaceae, with Joinvillea sister to this pair (Michelangeli et al., 2003). Silica is present in all three families, although only as silica sand in culms of Ecdeiocolea (Ecdeiocoleaceae).Silica bodies arepresentin most species of Poaceae,includingAnomochloa, and Pharus, which are putativelysister to the rest of the family (GPWG, 2001). Streptochaeta T'here is a diverse range of silica bodies in Poaceae, includingdumbbell-shaped, cross-shaped

SILICABODIESIN MONOCOTYLEDONS Table X Distributionof silica bodies in Dasypogonaceae

Genus Baxteria No. of species 1 Type and location of silica Spherical silica bodies with rugose surface present in leaf epidermalcells, generally one per cell Fine silica sand or amorphouscrystals present in leaf epidermis Fine silica sand or amorphouscrystals present in leaf epidermis Spherical silica bodies with rugose surface, present in the leaf epidermalcells, generally one per cell References

425

Fahn, 1954; Rudall & Chase, 1996 Rudall & Chase, 1996 Rudall & Chase, 1996 Fahn, 1954; Rudall & Chase, 1996

Calectasia Dasypogon Kingia

3 3 1

intermediates between these two types, horizontallyelongatedshapes with smooth or sinuous outlines, saddle shaped, conical shaped and numerousothers (Figs. 6A-6G) (see Metcalfe, 1960). The distributionand structureof silica bodies in Poaceae will be discussed in more detail in a separatepublication. 4. Dasypogonaceae The phylogeneticpositionof Dasypogonaceaewithinthe commelinidcladeremainsequivocal. For example, a relationshipwith palms was tentativelyindicatedby moleculardata, but without bootstrapsupport(Chase et al., 1995a, 2000; Givnish et al., 1999). Rudall and Chase (1996) noted that habit and method of growth would support a relationship between Dasypogonaceaeand Arecaceae,but ovule structure and silica position and morphologyindicate an affinitywith Rapateaceae.WithinDasypogonaceae(TableX), calcium oxalate crystals areabsent,but silica is presentin all fourgenera(Rudall& Chase, 1996). InKingiaandBaxteria, spherical(druse-like)silica bodies with a rugose surfacearepresentin the leaf epidermalcells, generally one per cell (Fig. 5H). These were previously reportedby Fahn (1954) as druses (clusteredcrystals of calcium oxalate), but X-ray and SEM examinationeffectively demonstrated their silicaceous nature. Silica is also present in the epidermis of Dasypogon and Calectasiain the formof fine silica sandor amorphous crystals,presentin most epidermalcells in Dasypogon (Fig. 5J) but less frequentin Calectasia.

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