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© 2003 Blackwell Publishing Ltd. http://www.blackwellpublishing.com/journals/ddi 73

BIODIVERSITY RESEARCH

Diversity and Distributions (2003) 9, 73–87

Blackwell Science, Ltd

Morphological variations of lobate phytoliths from grasses in China and the south-eastern United StatesHOUYUAN LU1,2* and KAM-BIU LIU2 1 Institute of Geology and Geophysics, Chinese Academy of Sciences, PO Box 9825, Beijing 100029, China, E-mail: [email protected] 2 Department of Geography and Anthropology, Louisiana State University, Baton Rouge, Louisiana 70803, U.S.A.

Abstract. Phytolith analysis of grasses is a usefultool in palaeoenvironmental and archaeobotani-cal research. Lobate phytolith is one of the mostimportant morphotypes of grass phytoliths. Thisstudy describes morphological variations of diag-nostic lobate phytoliths and produces a tentativeclassification scheme based on 250 modern grassspecies from China and the south-eastern U.S.A.Eighty-five grass species were found to containlobate phytoliths. They are derived mainly fromPanicoideae, but also include the Chloridoideae,Oryzoideae and Arundinoideae subfamilies.Twenty-five lobate morphological types wereobserved from different subfamilies, genera ortribes of grasses, based on two important param-eters: (1) the length of the lobate shank and (2)the shape of the outer margin of the two lobes.The identification of grass tribe or even genus ispossible based on the differences in lobate shapeparameters or the composition of assemblages.However, not all of the lobate assemblages have

a definite relationship with the genera thatproduce them, because grasses can only producea limited range of lobate shapes that often over-lap from one genus to another. Several C3 grassesand Chloridoideae subfamily grasses also producecharacteristic lobate phytoliths. The variations oflobate morphologies can be related to environmen-tal factors, especially moisture. Typical hygrophyticgrasses tend to yield lobate phytoliths with veryshort shank, whereas typical xerophytic grassestend to produce lobate phytoliths with a verylong shank. The potential link between phytolithmorphology, grass taxonomy and environmentalconditions opens the possibility that phytolithmorphology may be used as a proxy in palaeocli-matic reconstruction.

Key words. Dumbbell, grasses, palaeoenvironment,palynology, phytoliths, phytolith-lobate, silicabodies, taxonomy.

INTRODUCTION

Grasses (Family: Gramineae) are an importantgroup of plants in a variety of environments(Gould & Shaw, 1983). They are often the dom-inant plants in steppes or prairies, tundra,coastal marshes, pioneer or early successionalcommunities, disturbed sites and in certainaquatic communities. Many important crops aregrasses, such as maize, rice, wheat and sugarcane. Thus, the identification and classification of

grasses from fossil assemblages are of great sig-nificance in palaeoecological reconstruction.Unfortunately, except for Zea mays (maize), thepollen of Gramineae cannot be identified belowthe family level (Fearn & Liu, 1997). Thus, theuse of grass pollen in palaeoecological recon-struction is limited. Grass phytoliths, on theother hand, offer a promising means to differen-tiate grasses at subfamily levels and, accordingly,to infer subtle changes in palaeoenvironmentalconditions (Piperno, 1988; Rapp & Mulholland,1992; Fredlund & Tieszen, 1994, 1997; Alexandreet al., 1997; Runge, 1999). In this paper, we focus* Corresponding author.

74 H. Lu and K.-b. Liu

© 2003 Blackwell Publishing Ltd, Diversity and Distributions, 9, 73–87

on the predominant type of grass phytoliths — thelobate phytoliths, based on an investigation of250 species of grasses from China and the south-eastern U.S.A. Our objectives are twofold: (1) todocument the morphological variations of lobatephytoliths in relation to grass taxonomy and (2)to investigate the relationship between lobate phy-tolith shapes and environmental factors, which maybe useful for palaeoenvironmental reconstruction.

Background

Phytoliths are opal-A particles that precipitatewithin cells or between cells of living plant tissues(Piperno, 1988). Although nonsilicic (calcareous)phytoliths do exist (Cummings, 1992), mostresearchers (including the authors of this paper)use the term phytoliths to denote only the opalor silicic plant-cell inclusions, as defined above.Thus, phytoliths are also called silica bodies inthe anatomical literature (Ellis, 1979). Their sizesrange from a few microns (µm) to about 150 µm.They are well preserved in various sediments,even in oxidized environments such as soils, loessand sand dunes (Kelly et al., 1991; Wang & Lu,1993; Lu et al., 1996; Horrocks et al., 2000).

Early phytolith researchers noted that thedifferent subfamilies of grasses produce differentphytolith shapes; for example, grasses of thesubfamily Panicoideae produce dumbbell andcross-shaped phytoliths, whereas Pooideae (Fes-tucoideae) grasses produce rondels and sinuoustypes, and Chloridoideae grasses produce saddle-shaped phytoliths (Twiss et al., 1969). All mem-bers of the grass subfamilies Panicoideae andOryzoideae produce the bilobate (dumbbell)type of phytoliths. However, bilobate (dumbbell)phytoliths, thought previously to be the mostdiagnostic marker of the Panicoideae subfamily(Twiss et al., 1969), are also present in theChloridoideae and Arundinoideae subfamilies(Mulholland, 1989; Lu, 1998; Piperno & Pearsall,1998; Lu & Liu, in prep.).

Much confusion exists in the classification anddescriptive terminology of grass phytoliths. Exist-ing classification of grass phytoliths is based onthe micromorphology of discrete silica bodies,which is independent of the orientation of thebodies in silica cells in the various vegetativeparts of the individual grass plant (Twiss, 1992).Unfortunately for palaeoecologists, the same

grass species can produce different types ofphytoliths (i.e. multiplicity), and many differentspecies can produce the same shapes (i.e. redun-dancy) (Rovner, 1971). In order to use phytolithsas a tool in environmental reconstruction andtaxonomy, it is necessary to recognize morpho-logical variations in phytoliths in different speciesof grasses.

Bilobate (dumbbell) phytolith, one of the mostimportant morphotypes in grass phytoliths, hasbeen identified consistently as a distinctive silicabody (Twiss et al., 1969; Brown, 1984; Piperno,1988; Kondo et al., 1994; Rapp & Mulholland,1992; Wang & Lu, 1993). The term ‘dumbbell’was first used by Metcalfe (1960) as a morpho-logical term for the shape of some intercostalshort cell phytoliths. It has gradually become aname given to a loosely defined group of phyto-liths characterized by having two lobes joined bya shank. However, many subsequent researchers,including Brown (1984), Fredlund & Tieszen (1994,1997) and Piperno & Pearsall (1998) avoidedusing this term and favoured the alternative term‘bilobate’. As a morphological term, ‘dumbbell’draws its analogy from an exercising equipmentand makes sense only in the English language,whereas ‘bilobate’ is rooted in Latin and has awell-founded scientific meaning that is morecomprehensible to non-English-speakers. For thisreason, we follow the convention of these subse-quent researchers and use the term ‘lobate’ todescribe the morphological class of phytolithsthat has two or more lobes connected by a shank,whereas the term ‘bilobate’ refers only to thelargest subgroup, known formerly as ‘dumbbell’,that has two lobes connected by a shank.

In this paper, we propose a classification systemfor all lobate grass phytoliths, although our researchand discussion will focus on the bilobate types.For the taxonomy and nomenclature of grassesin China and the United States, we follow theInstitute of Botany, Chinese Academy of Sciences(1977) and Gould & Shaw (1983), respectively.

MATERIALS AND METHODS

Samples of modern grass plants for phytolith analysis

Leaves, culms and inflorescences from 250species of modern grass plants in China (tropical,

Morphological variations of lobate phytolith 75


subtropical and temperate forests, grasslands)and the subtropical Atlantic and Gulf coasts ofthe south-eastern United States (salt marshes,freshwater marshes, sand dunes and forests) werecollected for phytolith analysis. The rationale forincluding samples from both China and theUnited States in this study is to ensure that ourobservations and conclusions have wide applica-tion and are not limited to only one geographicalregion. These 250 grass species include therepresentatives of all six subfamilies (Pooideae,Panicoideae, Chloridoideae, Bambusoideae,Oryzoideae and Arundinoideae) according to theclassifications of the Institute of Botany, ChineseAcademy of Sciences (1977) and Gould & Shaw

(1983). Among these, 85 species, belonging mainlyto the subfamily Panicoideae, contain lobatephytoliths. Panicoideae has about 32 genera and325 species in the United States, and 190 generaand over 900 species in China (Institute of Botany,Chinese Academy of Sciences, 1977; Gould &Shaw, 1983). Some of the lobate phytoliths pre-sented in this study, however, come from thesubfamilies Oryzoideae, Chloridoideae, andArundinoideae (Tables 1 and 2). It should bepointed out that the classification and nomencla-ture of grass subfamilies have recently been revised(GPWG, 2001). More studies are needed in thefuture to adapt our phytolith classification to thenew classification system of grass subfamilies.

Table 1 List of modern grasses from the Atlantic and Gulf coasts of the United States used for the analysisof lobate phytoliths

Name Subfamily Ecology or distributionSampleno.*

Andropogon glomeratus (Walt.) BSP Panicoideae Generally on wet sites 17Andropogon ternaries Michx. Panicoideae Edge of pine forest 20Anthaenantia rufa (Nutt.) Schult. Panicoideae Pine forest 62Aristida desmantha Trin. & Rupr. Chloridoideae Sandy soil along coast 10Cenchrus incertus M. Curtis Panicoideae Dry sand 72Chasmanthium laxum (L.) Yates. Arundinoideae Edge of forest 16Chasmanthium ornithorhynchum (Steud.) Yates

Arundinoideae Moist area in pine flatwoods 18

Ctenium aromaticum (Walter) A.W. Wood

Chloridoideae Edge of forest 41

Erianthus strictus Spreng. Panicoideae Edge of pine forest and disturbed areas 19Leersia oryzoides (L.) Sw. Oryzoideae Wet roadside ditches and edges of

lakes, streams, and other wet areas37

Panicum amarum Elliott Panicoideae Sandy soil along coast 83Panicum dichotomiflorum Michx. Panicoideae Disturbed areas, especially in moist

regions, throughout United States84

Panicum hemitomon Schult. Panicoideae Coastal marsh, wet areas and in the inland part of coastal sites

85

Panicum verrucosum Muhl. Panicoideae Frequent; disturbed areas and edges of forests, mostly in the pine regions

31

Panicum virgatum L. Panicoideae Frequent; edges of pine forests and remnant strips in prairie regions; cheniers and spoil banks in coastal freshwater marsh

64

Saccharum officinarum L. Panicoideae Cultivated in tropical regions of the world 68Setaria sp. Panicoideae 9Sorghastrum nutans (L.) Nash Panicoideae Edge of forest and disturbed areas in

pine and prairie regions21

Sorghum halepense (L.) Pers. Panicoideae Widespread throughout the world 63Zizaniopsis miliacea (Michx.) Doell & Aschers.

Oryzoideae Edges of lakes, streams, wet roadside ditches 38

* See the sample numbers in Fig. 3.

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. Lu and K.-b. Liu

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Table 2 List of modern grasses from China used for the analysis of lobate phytoliths


Apluda mutica L. Panicoideae Southern China, edge of woodlands, side of streams 28Arthraxon hispidus Makino var. cryptatherus (Hack.) Honda Panicoideae Temperate regions of China, hillside, moist area 48Arundinella hirta (Thunb.) Tanaka Panicoideae East China, frequent growing in valley, side of 1

streams, wetter sitesArundinella setosa Trin. Panicoideae Southern China, hillside 4Bothriochloa ischaemum (L.) Keng Panicoideae Temperate regions of the world, hillside, roadside 59, 60Brachiaria ramose (L.) Stapf Panicoideae Tropical regions of the world 82Capillipedium assimile (Steud.) A. Camus Panicoideae East China, hillside 30Capillipedium parviflorum (R.Br.) Stapf Panicoideae East China, hillside, roadside 61Coix lacryma var. ma-yuen (Roman.) Stapf Panicoideae Temperate and subtropical regions of

the world, wet areas76

Coix lacryma-jobi L. Panicoideae Temperate and subtropical regions of the world, wet areas

75

Cymbopogom goeringii Steud Panicoideae Hillside 40Cyrtococcum patens (L.) A. Camus Panicoideae Southern China, edge of forest 44Digitaria adscendens (H. B.K.) Henrard Panicoideae Field, throughout China 55Digitaria sanguinalis (L.) Scop. Panicoideae Hillside, field, throughout China 54Digitaria sanguinalis var. ciliaris (Retz.) Parl. Panicoideae Southern China 14Digitaria violascens Link Panicoideae Southern China, roadside, hillsidefield 49Dimeria ornithopoda Trin Panicoideae Southern China, wet areas, hillside 15Eccoilopus cotulifer (Thunb.) A. Camus Panicoideae Southern China, hillside, field 2Echinochloa colonum (L.) Link Panicoideae East China, wet areas, roadside 79Echinochloa crusgalli (L.) Beauv. Panicoideae Temperate regions of the world, swamp, rice paddy 80Echinochloa crusgalli var. mitis (Pursh) Peterm Panicoideae Temperate regions of the world, swamp, wet areas 66Eragrostis ferruginea (Thunb.) Beauv. Chloridoideae East China, roadside, field 27Eragrostis japonica (Thunb.) Trin. Chloridoideae Southern China, hillside, field 26Eriochloa villosa (Thunb.) Kunth Panicoideae East China, wet areas 58Eulalia speciosa (Debeaux) Kuntze Panicoideae East China, hillside 3Hackelochloa granularia (L.) Kuntze Panicoideae Tropical regions of the world, edges of streams 74Imperata cylindrical (L.) Beauv. Var. major (Nees) C.E. Hubb. Panicoideae Throughout China, dry soils 22Isachne dispar Trin. Chloridoideae Southern China, hillside, forest and edges of streams 39Ischaemum aristatum L. Panicoideae East China, hillside, roadside, coast 53Ischaemum antephoroides (Steud.) Miq. Panicoideae Southern China, hillside, field, coast 50

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Ischaemum indicum (Houtt.) Merr. Panicoideae Southern China, hillside, roadside, coast 51Leersia hexandra Swartz Oryzoideae Southern China, a perennial grass growing in standing

water or very damp ground36

Leptochloa chinensis (L.) Nees Chloridoideae Southern China, a common annual of waste fields and paddy fields

33

Microstegium vimineum (Trin.) A. Camus Panicoideae East China, moist area 32Microstegium vimineum (Trin.) A. Camus var. imberbe (Nees) Honda

Panicoideae East China, moist area 52

Miscanthus floridulus (Labill.) Warb Panicoideae Southern China, hillside wet areas, forest 70Miscanthus sinensis Anderss Panicoideae Hillside, edges of streams 71Oplismenus compositus (L.) Beauv Panicoideae Southern China, wet areas, shady places under trees 45Oplismenus undulatifolius (Arduino) Roem. Et Schult Panicoideae East China, wet areas, edge of forest 42Oryza sativa L. Oryzoideae Cultivated worldwide 35Panicum austro-asiaticum Ohwi Panicoideae Southern China, wet areas 46Panicum bisulcatum Yhunb Panicoideae East China, wet areas, edges of lakes, streams, wet

roadside ditches56

Panicum notatum Retz Panicoideae Southern China, edge of forest 13Panicum repens L. Panicoideae Tropical and subtropical zones, waterside, coast 73Paspalum dilatatum Porst Panicoideae Wet areas 81Paspalum orbiculare G. Forst Panicoideae Tropical and subtropical regions of the

world, hillside, field78

Pennisetum alopecuroides (L.) Spreng Panicoideae Disturbed areas throughout China 11Pennisetum purpureum Schumach Panicoideae Elephant grass, native to Africa, a robust perennial

with culms 2–4 meters tall12

Pogonatherum crinitum (Thunb.) Kunth Panicoideae Southern China, banks, edges of streams, often in sandy places.

47

Rottboellia exaltata L. f. Panicoideae Southern China, hillside, roadside 29Saccharum arundinaceum Retz Panicoideae Southern China, hillside, edges of streams 69Saccharum sinensis Roxb Panicoideae Cultivated in tropical regions of the world 67Sacciolepis myosuroides (R.Br.) A. Camus Panicoideae Southern China, paddy field 43Schizachyrium brevifolium (Sw.) Nees ex Buse Panicoideae East China, an annual grass of rocky places with

poor soil, hillside25

Setaria faberi Herrm. Panicoideae China, north of Yangtze River 5Setaria glauca (L.) Beauv. Panicoideae Temperate and tropical zones, field and roadside 8


Table 2 continued.



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Laboratory procedure for phytolith analysis

All collected plant samples were cleaned withdistilled water in a water bath to remove adher-ing particles. Leaves and culms of each specieswere placed in 20 mL of saturated nitric acid forover 12 h to oxidize organic materials completely.Some species, such as Sporobolus dianger (Retz.)Beauv., S. indicus (L.) R.Br. var. purpurea-suffusus(Ohwi) T. koyama and Cymbopogon goeringii Steud,were oxidized for 24 h because they contain morevegetable tallow. The solutions were centrifugedat 2000 r.p.m. for 10 min, decanted and rinsedtwice with distilled water, and then rinsed with95% ethanol until the supernatants were clear.The phytolith sediments were transferred tostorage vials. The residual subsamples weremounted onto microscopic slides in Canadabalsam medium for photomicrography and inliquid medium for counting and line drawing.

Light photomicrography at 400× magnificationwas used to record types of phytoliths found ineach plant sample. An average of 270 lobategrains was counted in each sample. The percent-ages of different lobate categories were calculatedon the basis of a sum consisting of all lobatephytoliths.

Classification of lobate phytoliths

Lobate phytoliths are originated from the shortcells of grasses with identifiable shape character-istics. Metcalfe (1960) identified three types ofdumbbell or bilobate phytoliths. The Panicoiddivision in Twiss’s classification is composed of11 types of dumbbells and crosses (Twiss et al.,1969). Brown (1984) recognized bilobates, poly-lobates and crosses. Mulholland & Rapp (1992)proposed the lobate class to denote phytolithswith definite lobes, including the cross, sinuateand dumbbell types. Based on our observationand statistics of the lobate phytoliths from 85species of modern grass plants, we found thattwo important parameters can be used to char-acterize the morphological variations in lobatephytoliths: (1) the shape of the outer margins ofthe two lobes and (2) the length of the shank inthe lobate structure (Fig. 1). These two parame-ters are relatively stable among different Panicoi-deae plants. We develop a lobate classificationmatrix based on these two criteria (Fig. 2). PearsallT

able

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& Piperno (1990) used a somewhat differentapproach to distinguish domesticated corn phyto-liths on the basis of cross-shaped phytolith size(Pearsall, 1978) and cross-shaped three-dimensionalstructures (Piperno, 1984).

The first criterion is the shape or outline ofthe lobe. We divide lobate phytoliths into A, B,C, D and E types based on the characteristicsof ridged lines, rounded, truncated, concave andbranched outer margins, respectively (Fig. 2).Type A has ridged lines running longitudinallyalong the whole length of the phytolith. The linesmay be radiating towards the distal ends of thelobes. The shank is often wide and sturdy, con-necting two indistinct lobes. The outline of thelobes has obvious edges and corners. Types B ischaracterized by having smooth and generallyround outlines on the two lobes. In type C, thedistal ends of the two lobes are truncated, form-ing a generally straight edge. In type D, the distalends of the lobes are slightly indented, forming asmooth, concave curve. In type E, the distal ends ofthe lobes are deeply indented or distinctly branched.Type F is characterized by having multiple lobes.

The second criterion is the length of the shank(a) relative to the length of lobes (b) (Fig. 1).Four types are recognized:

Type 1: a < 1/3bType 2: 1/3b < a < bType 3: a ≈ bType 4: a > b

We divide lobate phytoliths into 20 typesaccording to the combination of these two crite-ria. In addition, for the shapes of two half-lobes,three lobes, three lobes with radiation lines, morethan four lobes and beaded lobes, we group themunder a special category, type F, which consistsof five subtypes (designated by lower-case lettersa–e, respectively) according to the number of lobespresent. Thus type F encompasses the trilobateand polylobate types that have been recognizedwidely in previous studies (Brown, 1984; Piperno,1988). Altogether, there are 25 morphologicaltypes of lobate phytoliths in our classificationsystem (Fig. 2).

The above classification is based on a two-dimensional view of phytolith shape, assumingthat a perfect lateral view of the phytolith can beobserved and measured. It should be pointed outthat phytolith, like pollen, is not a two-dimen-sional object. In reality, phytoliths may be tiltedat an angle from the viewer while being observedunder the microscope. Consequently, great caremust be exercised in observing and describing

Fig. 1 Morphological components of a lobatephytolith.

Fig. 2 Classification of lobate phytoliths accordingto two criteria: outline of the lobes (A–F), andlength ratio between shank and lobe (1–4). See textfor explanation.



phytolith shapes. Fortunately, because phytolithsare translucent or transparent, we can recognizethe structure or shape of the reverse side withouthaving to turn over the specimen under observa-tion. However, in order to avoid misclassificationdue to imperfect angles of observation it isimportant to use liquid mount in making phyto-lith slides, which allows rotation of object andmore accurate measurement of lobe shape andshank length.

RESULTS

Figure 3 shows the relative abundance of dif-ferent lobate phytolith types found in each of the85 grass species. The identified morphotypes areillustrated in Fig. 4. Table 3 lists the representativegrass taxa of different lobate phytolith typesfrom China and the south-eastern United States.

Type A is a phytolith with ridged lines on itsshank and lobes. A1 occurs exclusively in Isachne

Table 3 List of 25 lobate phytolith types and their representative grass taxa

Lobate types Representative Taxa

A1 Isachne disparA2 Sacciolepis myosuroides, Cyrtococcum patens, Oplismenus compositus, Panicum austro-asiaticum,

Pogonatherum crinitum, Arthraxon hispidus var. cryptatherus, Digitaria violascens, Ischaemum antephoroides, I. Indicum, I. aristatum, Microstegium vimineum var. imberb

A3 Digitaria sanguinalis, D. sanguinalis var. ciliaris, D. adscendensA4 Sacciolepis myosuroidesB1 Arundinella hirta, Eccoilopus cotulifer, Eulalia speciosa, Arundinella setosa, Setaria faberi, Pennisetum

alopecuroides, P. purpureum, Echinochloa. crusgalli, Paspalum dilatatum, Brachiaria ramosaB2 Setaria glauca, Aristida desmantha, Echinochloa crusgalli var. mitis, Saccharum sinensis, Sorghum

vulgare, Saccharum arundinaceum, Miscanthus floridulus, Miscanthus sinensis, Cenchrus incertusB3 Setaria glauca, Aristida desmantha, Pennisetum alopecuroides, P. purpureum, Panicum notatumB4 Arundinella setosa, Schizachyrium brevifolium, Digitaria sanguinalisC1 Oryza sativa, Leersia hexandra, Zizaniopsis miliacea, Z. caduciflora, Panicum amarumC2 Panicum bisulcatum, P. virgatum, Spodipogon sibiricus, Eriochloa villosa, Bothriochloa ischaemum,

Capillipedium parviflorum, Anthaenantia rufa, Sorghum halepense, Saccharum officinarum, Chasmanthium laxum, Miscanthus Anthaenantia rufloridulus, M. sinensis

C3 Digitaria sanguinalis var. ciliaris, Dimeria ornithopoda, Chasmanthium laxum, C. ornithorhynchum, Andropogon glomeratus, A. ternaries, Erianthus strictus, Sorghastrum nutans, Imperata cylindrica, Themeda gigantea var. caudate, Panicum virgatum

C4 Schizachyrium brevifolium, Eragrostis japonica, Eragrostis ferrugineaD1 Leersia oryzoides, Zizaniopsis miliacea, Anthaenantia rufaD2 Leersia oryzoides, Zizania caduciflora, Microstegium vimineum var. imberbe, Leptochloa chinensisD3 Arundinella setosa, Setaria faberi, S. plicata, S. palmifoliaD4 Cymbopogom goeringii, Ctenium aromaticumE1 Coix lacryma-jobi, Zea mays, Paspalum orbiculare, P. dilatatum, Echinochloa crusgalli, Brachiaria

ramosa, Themeda triandra var. japonica, Panicum dichotomiforom, Arundinella hirta, Cyrtococcum patens, Oplismenus compositus, Bothriochloa ischaemum, Echinochloa crusgalli var. mitis, Saccharum sinensis, Sorghum vulgare

E2 Coix lacryma-jobi, Coix lacryma var. ma-yuen, Zea maysE3 Setaria palmifolia, Themeda triandra var. japonica, Panicum dichotomiforomE4 ?Fa Capillipedium assimile, Panicum verrucosumFb Eulalia speciosa, Rottboellia exaltata, Capillipedium assimile, Panicum verrucosum, Oplismenus

undulatifoliusFc Sacciolepis myosuroidesFd Panicum bisulcatum, Spodipogon sibiricusFe Apluda mutica

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Fig. 3 Percentages of lobate phytolith morphotypes calculated based on the sum of lobate phytolith counts for each grass samples. Sample numbers onthe left axis: 1, Arundinella hirta 2, Eccoilopus cotulifer 3, Eulalia speciosa 4, Arundinella setosa 5, Setaria faberi 6, S. plicata 7, S. palmifolia 8, Setaria glauca 9,S. sp. 10, Aristida desmantha 11, Pennisetum alopecuroides 12, P. purpureum 13, Panicum notatum 14, Digitaria sanguinalis var. ciliaris 15, Dimeria ornithopoda16, Chasmanthium laxum 17, Andropogon glomeratus 18, Chasmanthium ornithorhynchum 19, Erianthus strictus 20, Andropogon ternaries 21, Sorghastrum nutans22, Imperata cylindrica 23, Themeda gigantea var. caudate 24, Themeda triandra var. japonica 25, Schizachyrium brevifolium 26, Eragrostis japonica 27, E.ferruginea 28, Apluda mutica 29, Rottboellia exaltata 30, Capillipedium assimile 31, Panicum verrucosum 32, Microstegium vimineum 33, Leptochloa chinensis34, Zizania caduciflora 35, Oryza sativa 36, Leersia hexandra 37, L. oryzoides 38, Zizaniopsis miliacea 39, Isachne dispar 40, Cymbopogom goeringii 41, Cteniumaromaticum 42, Oplismenus undulatifolius 43, Sacciolepis myosuroides 44, Cyrtococcum patens 45, Oplismenus compositus 46, Panicum austro-asiaticum 47,Pogonatherum crinitum 48, Arthraxon hispidus var. cryptatherus 49, Digitaria violascens 50, Ischaemum antephoroides 51, I. indicum 52, Microstegium vimineumvar. imberbe 53, Ischaemum aristatum 54, Digitaria sanguinalis 55, Digitaria adscendens 56, Panicum bisulcatum 57, Spodipogon sibiricus 58, Eriochloa villosa 59,Bothriochloa ischaemum (Southern China) 60, B. ischaemum (Northern China) 61, Capillipedium parviflorum 62, Anthaenantia rufa 63, Sorghum halepense64, Panicum virgatum 65, Sorghum vulgare 66, Echinochloa crusgalli var. mitis 67, Saccharum sinensis 68, Saccharum officinarum 69, Saccharum arundinaceum70, Miscanthus floridulus 71, M. sinensis 72, Cenchrus incertus 73, Panicum repens 74, Hackelochloa granularia 75, Coix lacryma-jobi 76, Coix lacryma var.ma-yuen 77, Zea mays 78, Paspalum orbiculare 79, Echinochloa colonum 80, E. crusgalli 81, Paspalum dilatatum 82, Brachiaria ramosa 83, Panicum amarum84, Panicum dichotomiflorum 85, P. hemitomon. The order of arrangement of different grass species is based on the results of cluster analysis.



Fig. 4 Photographs of some representative lobate phytoliths from grass plants 1, Ischaemum antephoroides 2,Saccharum arundinaceum 3, 24, 31, Oryza sativa 4, Miscanthus floridulus 5, 6, 11, Zizania caduciflora 7, Zeamays 8, Arthraxon hispidus var. cryptatherus 9, 10, Setaria faberi 12, 18, Themeda triandra var. japonica 13,Coix lacryma-jobi 14, Echinochloa crusgalli 15, Pennisetum purpureum 16, Schizachyrium brevifolium 17,Themeda gigantea var. caudate 19, Rottboellia exaltata 20, 25, Sacciolepis myosuroides 21, Eragrostis ferruginea22, Dimeria ornithopoda 23, Eragrostis japonica 26, 27, Paspalum orbiculare 28, Oplismenus compositus 29,Apluda mutica 30, Oplismenus undulatifolius.



dispar. A2 is represented by a wide range of grasstaxa that are distributed mainly in the hillsides,grasslands, coasts and wetlands of southernChina up to the Yangtze River. A3 is representedmainly by several species of Digitaria. Most ofthese grasses occur in subtropical South China andare found commonly in wet areas such as lake-shores, stream channels and wet roadside ditches.A4 has few representative species (Sacciolepismyosuroides) (Fig. 3, no. 43).

Type B are phytoliths with smooth roundedlobes. B1 occurs in many species of grasses, butits abundance in each species is relatively low(< 35%) compared to that of B2 and B3. Repre-sentative species of B2 are Aristida desmantha(Fig. 3, no. 10), Saccharum sinensis (sugar cane,Fig. 3, no. 43), Sorghum vulgare (kaoliang orsorghum, Fig. 3, no. 65), Saccharum arundinaceum,Miscanthus floridulus and Miscanthus sinensis(Fig. 3, nos 69, 70, 71). They grow typically infields and roadside habitats or in warm andhumid environments. Representatives of B3 areSetaria glauca (Fig. 3, no. 8), Aristida desmantha,Pennisetum alopecuroides, P. purpureum andPanicum notatum (Fig. 3, nos 10, 11, 12, 13). Theygrow mainly on the hillsides, roadsides and drysand dunes of relatively dry environments. B4 isan uncommon type that occurs only at relativelylow frequencies in a few taxa.

Type C, a phytolith with truncated margins atboth ends of its lobes, has the largest number ofrepresentative plants. To some extent, C1 may beconsidered to be diagnostic of the Oryzoideaesubfamily, occurring abundantly in such speciesas Oryza sativa (paddy rice), Leersia hexandra(wild rice), Zizaniopsis miliacea and Z. caduciflora(water bamboo) (Fig. 3, nos 35–38). Among othergrasses, only Panicum amarum (Fig. 3, no. 83) ofthe Panicoideae subfamily, a typical aquatic andhygrophytic species, produces this type of phyto-liths in significant abundance. C2 is well repre-sented in a large number of grass taxa that notablyinclude Panicum bisulcatum, P. virgatum, Sorghumhalepense (Fig. 3, nos 56, 64, 63) Saccharumofficinarum, Miscanthus floridulus and M. sinen-sis, among others. These grasses are distributedwidely in East China; most are hygrophytes andmesophytes. C3 is found in a smaller range ofgrasses than C2, but it occurs in great abundancein several taxa including, for example, Digitariasanguinalis var. ciliaris, Dimeria ornithopoda,

Chasmanthium laxum, Andropogon glomeratus(Fig. 3, nos 14–17), Erianthus strictus, Sorghas-trum nutans and Imperata cylindrica. These aremainly heliophytes and drought-enduring meso-phytes and xerophytes, growing typically onmountain slopes in both southern and northernChina, and on forest edges and disturbed areasof pine woodlands and prairie regions in theUnited States. The C4 group is basically diagnos-tic of Eragrostis japonica and E. ferruginea(Fig. 3, nos 26, 27), as well as Schizachyriumbrevifolium (Fig. 3, no. 25). The genus Eragrostis,a member of Chloridoideae, is found typically inareas of warm and dry climatic conditions.

Type D is phytoliths with concave marginsat the end of the lobes. There are only a fewrepresentative plants of D1 (Leersia oryzoides,Zizaniopsis miliacea and Anthaenantia rufa(Fig. 3, no. 62) and D4 (Cymbopogom goeringii andCtenium aromaticum (Fig. 3, nos 40, 41). Therepresentatives of D2 are Leersia oryzoides,Zizania caduciflora, Microstegium vimineum var.imberbe and Leptochloa chinensis, which growmainly in roadside wet ditches, stream channelsand other wet habitats such as lakeshores. D3phytoliths occur most abundantly in Setaria(S. faberi, S. plicata and S. palmifolia; Fig. 3, nos 5,6, 7) and Arundinella setosa (Fig. 3, no. 4), speciesfound typically in warm and wet subtropicalenvironments.

Type E is phytoliths with branched outer mar-gins at the end of the lobes. E1 is a typical cross-shape, the size and shape of which is somewhatvariable. This type of phytolith occurs predomi-nantly in a number of species that include(although not restricted to) some important agri-cultural crops in the temperate and tropical regionsof the world, such as Zea mays (maize), Coixlacryma-jobi (Job’s tears), Saccharum sinensis(sugar cane) and Sorghum vulgare (kaoliang orsorghum) (Fig. 3, nos 77, 75, 67, 65). E2 occursabundantly only in Coix lacryma var. ma-yuen(Job’s tears), a crop cultivated commonly in China.Incidentally, Coix lacryma var. ma-yuen andother members of the Maydeae subfamily pro-duce only the E2 and E1 phytoliths. E3 can befound in many plants, but by itself is diagnosticof none. No E4 phytoliths were found in oursamples in this study, although this morphotypehas been observed in fossil assemblages (H.Y. Lu,unpublished data).



Type F has multiple lobes and can be foundin many plants. The plants that can produce theF type include Capillipedium assimile, Panicumverrucosum (Fa), Eulalia speciosa, Rottboellia exaltata,Capillipedium assimile, Panicum verrucosum, Oplis-menus undulatifolius (Fb), Sacciolepis myosuroides(Fc), Panicum bisulcatum, Spodipogon sibiricus (Fd)and Apluda mutica (Fe). The plants of Type F aredistributed mainly in the southern parts of China.

It is worth noting that lobate phytoliths arealso found in a few Chloridoideae plants, forexample, in Leptochloa chinensis (C2), Eragrostisjaponica and E. ferruginea (C4). More studies areneeded on these non-Panicoideae grasses thatproduce lobate phytoliths.

DISCUSSION

Morphological variations in lobate phytoliths from C3 grasses

Early phytolith researchers noted that the differ-ent subfamilies of grass plants produce differentphytolith shapes: Panicoideae produces dumbbelland cross-shaped phytoliths; Festucoid formsrondels and sinuous types, and Chloridoideaeyields saddles (Brown, 1984; Mulholland, 1989;Fearn, 1998). The shape of individual phytolithsfrom grasses can be used as an indication of C3 orC4 photosynthetic pathways. For example, saddlephytolith indicates C4 ‘short-grass prairie’ speciesthat flourish in warm, arid to semi-arid regionswhere the available soil moisture is very low, whereasdumbbell and cross phytoliths represent the grassesof the C4 ‘tall-grass prairies’, which have high tomedium soil-moisture availability (Twiss, 1992).

In this study, we found that several C3grasses (Waller et al., 1979; Gould & Shaw, 1983;Lu & Wang, 1991) also produce characteristiclobate morphotypes, such as Zizania caduciflora,Oryza sativa, Leersia hexandra, L. oryzoides andZizaniopsis miliacea of the Oryzoideae sub-family, and Oplismenus compositus, O. compositus,Sacciolepis myosuroides and Isachne dispar ofthe Panicoideae subfamily. Lobate phytoliths inOryzoideae are characterized by high propor-tions of C1 and, to a lesser extent, D1 types withvery short shank between the lobes. Other C3grasses from Panicoideae produce characteristicA1 and A2 types with ridged lines on its lobesand F type with multiple lobes.

C3 grasses from both Oryzoideae and Panicoi-deae subfamilies in this study are adapted typi-cally to moist or marshy environments and aredistributed widely in tropical and subtropicalregions of the world.

Morphological variations in lobate phytoliths from Chloridoideae

Lobate phytoliths from the Chloridoideae sub-family have been reported by Brown (1984) andMulholland (1989). In this study, many varia-tions in lobate phytoliths were observed inChloridoideae (including Eragrostis japonica, E.ferruginea, Ctenium aromaticum, Aristida desman-tha and Leptochloa chinensis).

Eragrostis japonica, E. ferruginea and Cteniumaromaticum produce different phytolith assem-blages in which 40–98% of the lobates are C4and D4 types with very a long shank between thelobes (Fig. 3, nos 26, 27, 41). These species aredistributed widely in warm and arid regions. B2and B3 types are the dominant phytoliths ofAristida desmantha (Fig. 3, no. 10) that alsobelongs to the Chloridoideae subfamily (or theArundinoideae subfamily according to the classi-fication system of Watson et al., 1985). The sam-ple of Aristida desmantha was collected from drysand dunes on the Georgia coast of the UnitedStates. Leptochloa chinensis (Fig. 3, no. 33) yieldsonly two phytolith types: D2 (83%) and D3 (17%).

Can we infer grass genera from lobate phytolith assemblages?

The classification of phytolith shapes has longbeen criticized due to the multiplicity and redun-dancy of many grass morphotypes — a problempreventing the attribution of individual phytolithto species or genus (Rovner, 1971; Brown, 1984;Mulholland, 1989). Because the same shapes ofphytoliths can occur in different grass taxa, asingle phytolith morphotype cannot be ascribedto a specific grass species. However, a phytolithassemblage could, to some extent, allow us toinfer the predominant subfamily constituting thegrass associations. Recently, many researchershave paid particular attention to this specifictaxonomic problem of redundancy for grassphytolith classification. They indicated that it wouldnever be possible to eliminate all redundancies at



the subfamily level, much less for genus (Fredlund& Tieszen, 1994).

In this study, we tried to find a potential rela-tionship between the morphological variationsin lobate phytoliths and the grass genera thatproduce them (Fig. 3, Table 3). We found someinteresting patterns in several cases, as follows.Three grass plants belonging to the genus Setaria(S. faberi, S. plicata, S. palmifolia) were definedby a high abundance of D3 type. The two speciesof Eragrostis (E. japonica, E. ferruginea; sub-family Chloridoideae) produce almost exclusivelythe C4 type of lobate phytoliths. Zizania caduci-flora, Oryza sativa, Leersia hexandra, L. oryzoidesand Zizaniopsis miliacea, all belonging to thesubfamily Oryzoideae, produce a significant amountof C1 and, to some extent, D2 types of lobatephytoliths. Miscanthus yields primarily B2 andC2 types of phytoliths. Maydeae (Coix lacryma-jobi, C. l. var. ma-yuen, Zea mays) yields only E1and E2 (cross) types. Remarkably, the three speciesof Saccharum (S. sinensis, S. officinarum and S.arundinaceum) produces different lobate phytolithassemblages (Fig. 3). Saccharum sinensis (sugarcane), in particular, is characterized by thecodominance of E1 (54%) and B2 (29%) types,whereas S. officinarum is characterized by thecodominance of C2 (35%) and C3 (24%) types,and S. arundinaceum by the preponderance ofB2 (51%) mixed with some E1 and B1.

Unfortunately, not all lobate phytolith assem-blages have a definite and consistent relationshipwith the grass genera that produce them, becausegrasses only produce a limited range of lobatephytoliths, which often overlap from genus togenus. Moreover, the relatively limited samplesize in each genus used in this study prevents usfrom generalizing the characteristics of lobateassemblages for all grass genera.

Morphological changes in lobate phytoliths along an environmental gradient

Although different parts of plant body fromone species often contribute different lobatephytoliths to an assemblage, many grasses doproduce predominantly a specific phytolith typerecognizable by distinct shape, sculpture or sizethat can be assigned to a given taxon at variouslevels. Morphological variations in phytoliths canbe produced by both botanical and environmental

factors (Mulholland et al., 1988). Thus, it ispossible to discuss the morphological changes inlobate phytoliths along environmental gradients.

As shown in Fig. 3, the representatives of C1are Oryzoideae that typically consist of aquaticand hygrophytic grasses. The principal membersof B1 type are the grasses frequently growing inwet areas and on lakeshores, such as Echinochloacrusgalli (Fig. 3, no. 80) and Paspalum dilatatum(Fig. 3, no. 81). Grasses from the Chloridoideaesubfamily (e.g. Eragrostis) and Panicoideaesubfamily (e.g. Cymbopogom goeringii, Cteniumaromaticum; Fig. 3, nos 40, 41) that grow in dryconditions produce predominantly C4 and D4phytoliths. Grasses of the Maydeae subfamily,found typically in warm and moist areas, yieldpredominantly the cross phytoliths of E1 and E2types. The representative grasses of B3 and B4types (e.g. Setaria glauca, Aristida desmantha,Pennisetum alopecuroides; Fig. 3, nos 8, 10, 11)grow mainly in drier habitats such as hillsides,road sides and sand dunes of arid regions.

As a first-order generalization, it seems thatthe progression from type 1 to type 4 representsan environmental gradient of decreasing moisture(i.e. from wet to dry). In other words, grassesgrowing in drier habitats or environments tend toproduce phytoliths with a longer shank and viceversa. The environmental significance of the pro-gression from types A–E is less clear at this point.

What is the cause of morphological variabilityin lobate phytoliths? Is it environmental pheno-type or genotype? Wang & Lu (1993) comparedmorphological changes in short cell phytolithsfrom the same species of grasses growing in dif-ferent environmental conditions in China. Theyshowed that phytolith shapes are relatively stable,but sizes can change slightly. Piperno (1988)suggested that phytoliths formed in the shortcells of the grass epidermis are under a consider-able degree of active genetic control. To date, nostrong evidence can be found from our data toresolve the question of whether phytolith shapesare phenotype or genotype.

Regardless of the cause of morphologicalvariations, our study suggests that in some waysphytolith morphology could be linked to grasstaxonomy (e.g. C1 is diagnostic of Oryzoideae).As many grass taxa tend to have certain typicalenvironmental adaptations (e.g. Oryzoideaeoccurring typically in wet habitats), it may be



possible to use phytolith morphology as a proxyfor environmental conditions. More work isneeded to substantiate this point.

CONCLUSIONS

This study documents the variability of 25 diag-nostic lobate phytolith shapes occurring among85 modern grass species collected from a varietyof environments in China and the south-easternUnited States. We propose a classification that isbased on two important morphological parame-ters: the length of the lobate shank and the shapeof the outer margin of the two lobes. These twomorphological characteristics are relatively stableamong the 85 modern grass species belonging tothe Panicoideae, Chloridoideae, Oryzoideae andArundinoideae subfamilies. In some cases, theidentification of tribe or even genus is possiblebased on the differences in lobate shape param-eters or the composition of assemblages. How-ever, we should point out that not all of thelobate assemblages have a consistent and definiterelationship with the genera that produce them.This is because grasses can only produce alimited range of lobate shapes, and there is oftenconsiderable overlap from one genus to another.

In this study, we found that several C3 grassesof the Oryzoideae subfamily produce character-istic lobate morphotypes, which are characterizedby a high proportion of C1 and D1 types and bya very short shank between the lobes. Other C3grasses from Panicoideae produce characteristicA1 and A2 types with ridged lines and F typewith multiple lobes.

The Chloridoideae subfamily produces lobateassemblages in which 40–98% of phytoliths areC4 and D4 types with a very long shank betweenthe lobes. This group of grasses is widely distrib-uted in warm and arid regions.

We also found that the variations of lobatemorphologies can be related to environmentalfactors, especially moisture. Typical hygrophyticgrasses tend to yield lobate phytoliths with a veryshort shank, whereas typical xerophytic grassestend to produce lobate phytoliths with very longshank. This relationship, if supported by addi-tional studies of lobate phytoliths derived frommore grass species and from a wider range ofenvironmental conditions, offers potential forusing phytoliths in palaeoclimatic reconstruction.

ACKNOWLEDGMENTS

We thank Y.J. Wang, X.Y. Zhou, C.A. Reese andC.M. Shen for providing modern grass referencesamples and for helpful discussion. We aregrateful to S.C. Mulholland, G.G. Fredlund andI. Rovner for valuable comments on an earlierversion of this manuscript. We also thank the twoanonymous reviewers for their helpful reviews ofour original manuscript. This work was supportedby NSFC (40024202, 49971077 and 49894174),NKBRSF (G1998040810), the Risk PredictionInitiative (RPI) of the Bermuda Biological Stationfor Research (RPI-00-1-002) and the U.S.National Science Foundation (SES-9122058;BCS-0213884).

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