morphological variations of lobate phytoliths from grasses

7/27/2019 Morphological Variations of Lobate Phytoliths From Grasses

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

BIODIVERSITY RESEARCH

Diversity and Distributions (2003) 9, 7387

BlackwellScience,Ltd

Morphological variations of lobate phytoliths from grasses

in China and the south-eastern United States

HOUYUAN LU 1, 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] Department of Geography and Anthropology, Louisiana State University, Baton Rouge, Louisiana

70803, U.S.A.

Abstract. Phytolith analysis of grasses is a useful

tool in palaeoenvironmental and archaeobotani-

cal research. Lobate phytolith is one of the most

important morphotypes of grass phytoliths. This

study describes morphological variations of diag-

nostic lobate phytoliths and produces a tentative

classification scheme based on 250 modern grass

species from China and the south-eastern U.S.A.

Eighty-five grass species were found to contain

lobate phytoliths. They are derived mainly from

Panicoideae, but also include the Chloridoideae,

Oryzoideae and Arundinoideae subfamilies.

Twenty-five lobate morphological types were

observed from different subfamilies, genera or

tribes 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 is

possible based on the differences in lobate shape

parameters or the composition of assemblages.

However, not all of the lobate assemblages have

a definite relationship with the genera that

produce them, because grasses can only produce

a limited range of lobate shapes that often over-

lap from one genus to another. Several C3 grasses

and Chloridoideae subfamily grasses also produce

characteristic lobate phytoliths. The variations of

lobate morphologies can be related to environmen-

tal factors, especially moisture. Typical hygrophytic

grasses tend to yield lobate phytoliths with very

short shank, whereas typical xerophytic grasses

tend to produce lobate phytoliths with a very

long shank. The potential link between phytolith

morphology, grass taxonomy and environmental

conditions opens the possibility that phytolith

morphology may be used as a proxy in palaeocli-

matic reconstruction.

Key words. Dumbbell, grasses, palaeoenvironment,

palynology, phytoliths, phytolith-lobate, silica

bodies, taxonomy.

INTRODUCTION

Grasses (Family: Gramineae) are an important

group 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 successional

communities, disturbed sites and in certain

aquatic communities. Many important crops are

grasses, such as maize, rice, wheat and sugar

cane. Thus, the identification and classification of

grasses from fossil assemblages are of great sig-nificance in palaeoecological reconstruction.

Unfortunately, except for Zea mays (maize), the

pollen of Gramineae cannot be identified below

the family level (Fearn & Liu, 1997). Thus, the

use of grass pollen in palaeoecological recon-

struction is limited. Grass phytoliths, on the

other hand, offer a promising means to differen-

tiate grasses at subfamily levels and, accordingly,

to infer subtle changes in palaeoenvironmental

conditions (Piperno, 1988; Rapp & Mulholland,

1992; Fredlund & Tieszen, 1994, 1997; Alexandreet al., 1997; Runge, 1999). In this paper, we focus* Corresponding author.


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74 H. Lu and K.-b. Liu

2003 Blackwell Publishing Ltd, Diversity and Distributions, 9, 7387

on the predominant type of grass phytoliths the

lobate phytoliths, based on an investigation of

250 species of grasses from China and the south-

eastern U.S.A. Our objectives are twofold: (1) to

document the morphological variations of lobate

phytoliths in relation to grass taxonomy and (2)to investigate the relationship between lobate phy-

tolith shapes and environmental factors, which may

be useful for palaeoenvironmental reconstruction.

Background

Phytoliths are opal-A particles that precipitate

within cells or between cells of living plant tissues

(Piperno, 1988). Although nonsilicic (calcareous)

phytoliths do exist (Cummings, 1992), most

researchers (including the authors of this paper)use the term phytoliths to denote only the opal

or silicic plant-cell inclusions, as defined above.

Thus, phytoliths are also called silica bodies in

the anatomical literature (Ellis, 1979). Their sizes

range from a few microns (m) to about 150 m.

They are well preserved in various sediments,

even in oxidized environments such as soils, loess

and sand dunes (Kelly et al., 1991; Wang & Lu,

1993; Lu et al., 1996; Horrocks et al., 2000).

Early phytolith researchers noted that the

different subfamilies of grasses produce differentphytolith shapes; for example, grasses of the

subfamily Panicoideae produce dumbbell and

cross-shaped phytoliths, whereas Pooideae (Fes-

tucoideae) grasses produce rondels and sinuous

types, and Chloridoideae grasses produce saddle-

shaped phytoliths (Twiss et al., 1969). All mem-

bers of the grass subfamilies Panicoideae and

Oryzoideae produce the bilobate (dumbbell)

type of phytoliths. However, bilobate (dumbbell)

phytoliths, thought previously to be the most

diagnostic marker of the Panicoideae subfamily

(Twiss et al., 1969), are also present in the

Chloridoideae and Arundinoideae subfamilies

(Mulholland, 1989; Lu, 1998; Piperno & Pearsall,

1998; Lu & Liu, in prep.).

Much confusion exists in the classification and

descriptive terminology of grass phytoliths. Exist-

ing classification of grass phytoliths is based on

the micromorphology of discrete silica bodies,

which is independent of the orientation of the

bodies in silica cells in the various vegetative

parts of the individual grass plant (Twiss, 1992).

Unfortunately for palaeoecologists, the same

grass species can produce different types of

phytoliths (i.e. multiplicity), and many different

species can produce the same shapes (i.e. redun-

dancy) (Rovner, 1971). In order to use phytoliths

as a tool in environmental reconstruction and

taxonomy, it is necessary to recognize morpho-logical variations in phytoliths in different species

of grasses.

Bilobate (dumbbell) phytolith, one of the most

important morphotypes in grass phytoliths, has

been identified consistently as a distinctive silica

body (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 intercostal

short cell phytoliths. It has gradually become aname given to a loosely defined group of phyto-

liths characterized by having two lobes joined by

a shank. However, many subsequent researchers,

including Brown (1984), Fredlund & Tieszen (1994,

1997) and Piperno & Pearsall (1998) avoided

using this term and favoured the alternative term

bilobate. As a morphological term, dumbbell

draws its analogy from an exercising equipment

and makes sense only in the English language,

whereas bilobate is rooted in Latin and has a

well-founded scientific meaning that is morecomprehensible to non-English-speakers. For this

reason, we follow the convention of these subse-

quent researchers and use the term lobate to

describe the morphological class of phytoliths

that has two or more lobes connected by a shank,

whereas the term bilobate refers only to the

largest subgroup, known formerly as dumbbell,

that has two lobes connected by a shank.

In this paper, we propose a classification system

for all lobate grass phytoliths, although our research

and discussion will focus on the bilobate types.

For the taxonomy and nomenclature of grasses

in China and the United States, we follow the

Institute 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 250

species of modern grass plants in China (tropical,


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Morphological variations of lobate phytolith 75


subtropical and temperate forests, grasslands)

and the subtropical Atlantic and Gulf coasts of

the south-eastern United States (salt marshes,

freshwater marshes, sand dunes and forests) were

collected for phytolith analysis. The rationale for

including samples from both China and the

United States in this study is to ensure that our

observations and conclusions have wide applica-

tion and are not limited to only one geographical

region. These 250 grass species include the

representatives of all six subfamilies (Pooideae,

Panicoideae, Chloridoideae, Bambusoideae,

Oryzoideae and Arundinoideae) according to the

classifications of the Institute of Botany, Chinese

Academy of Sciences (1977) and Gould & Shaw

(1983). Among these, 85 species, belonging mainly

to the subfamily Panicoideae, contain lobate

phytoliths. Panicoideae has about 32 genera and

325 species in the United States, and 190 genera

and 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 the

subfamilies Oryzoideae, Chloridoideae, and

Arundinoideae (Tables 1 and 2). It should be

pointed out that the classification and nomencla-

ture of grass subfamilies have recently been revised

(GPWG, 2001). More studies are needed in the

future to adapt our phytolith classification to the

new classification system of grass subfamilies.

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

of lobate phytoliths

Name Subfamily Ecology or distribution

Sample

no.*

Andropogon glomeratus (Walt.) BSP Panicoideae Generally on wet sites 17

Andropogon ternaries Michx. Panicoideae Edge of pine forest 20

Anthaenantia rufa (Nutt.) Schult. Panicoideae Pine forest 62

Aristida desmantha Trin. & Rupr. Chloridoideae Sandy soil along coast 10

Cenchrus incertus M. Curtis Panicoideae Dry sand 72

Chasmanthium laxum (L.) Yates. Arundinoideae Edge of forest 16

Chasmanthium 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 19

Leersia oryzoides (L.) Sw. Oryzoideae Wet roadside ditches and edges of

lakes, streams, and other wet areas

37

Panicum amarum Elliott Panicoideae Sandy soil along coast 83

Panicum dichotomiflorum Michx. Panicoideae Disturbed areas, especially in moist

regions, throughout United States

84

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 68

Setaria sp. Panicoideae 9Sorghastrum nutans (L.) Nash Panicoideae Edge of forest and disturbed areas in

pine and prairie regions

21

Sorghum halepense (L.) Pers. Panicoideae Widespread throughout the world 63

Zizaniopsis miliacea (Michx.)

Doell & Aschers.

Oryzoideae Edges of lakes, streams, wet roadside ditches 38

* See the sample numbers in Fig. 3.


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Ischaemum indicum (Houtt.) Merr. Panicoideae Southern China, hillside, roa

Leersia hexandra Swartz Oryzoideae Southern China, a perennial

water or very damp ground

Leptochloa chinensis (L.) Nees Chloridoideae Southern China, a common a

and paddy fields

Microstegium vimineum (Trin.) A. Camus Panicoideae East China, moist area

Microstegium vimineum (Trin.) A. Camus var. imberbe

(Nees) Honda

Panicoideae East China, moist area

Miscanthus floridulus (Labill.) Warb Panicoideae Southern China, hillside wet

Miscanthus sinensis Anderss Panicoideae Hillside, edges of streams

Oplismenus compositus (L.) Beauv Panicoideae Southern China, wet areas, s

Oplismenus undulatifolius (Arduino) Roem. Et Schult Panicoideae East China, wet areas, edge o

Oryza sativa L. Oryzoideae Cultivated worldwide

Panicum austro-asiaticum Ohwi Panicoideae Southern China, wet areas

Panicum bisulcatum Yhunb Panicoideae East China, wet areas, edges

roadside ditchesPanicum notatum Retz Panicoideae Southern China, edge of fore

Panicum repens L. Panicoideae Tropical and subtropical zon

Paspalum dilatatum Porst Panicoideae Wet areas

Paspalum orbiculare G. Forst Panicoideae Tropical and subtropical regi

world, hillside, field

Pennisetum alopecuroides (L.) Spreng Panicoideae Disturbed areas throughout C

Pennisetum purpureum Schumach Panicoideae Elephant grass, native to Afr

with culms 24 meters tall

Pogonatherum crinitum (Thunb.) Kunth Panicoideae Southern China, banks, edge

sandy places.

Rottboellia exaltata L. f. Panicoideae Southern China, hillside, roa

Saccharum arundinaceum Retz Panicoideae Southern China, hillside, edgSaccharum sinensis Roxb Panicoideae Cultivated in tropical regions

Sacciolepis myosuroides (R.Br.) A. Camus Panicoideae Southern China, paddy field

Schizachyrium brevifolium (Sw.) Nees ex Buse Panicoideae East China, an annual grass

poor soil, hillside

Setaria faberi Herrm. Panicoideae China, north of Yangtze Riv

Setaria glauca (L.) Beauv. Panicoideae Temperate and tropical zones

Name Subfamily Ecology or distribution

Table 2 continued.


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Setariapalmifolia(Koen.)

Stapf

Pan

icoideae

SouthernChina,v

alley,

hillside

7

Setariaplicata(Lamk.)

T.

Cooke

Pan

icoideae

SouthernChina,v

alley,wetareas

6

Sor

ghumv

ulgarePers.

Pan

icoideae

Cultivatedintemp

erateregionsoftheworld

65

Spo

dipogonsibiricusTrin.

Pan

icoideae

Temperateregions

oftheworld,

hillside,forest

57

The

medagiganteanvar.caudate(Nee

s)Keng

Pan

icoideae

SouthernChina,h

illsidegrassplot,edgesofstreams

23

The

medatriandravar.japonica(Willd.)

Makino

Pan

icoideae

East,

China,

dryh

illside

24

Zea

maysL.

Pan

icoideae

Cultivatedworldwide

77

Zizaniacaduciflora(Turcz.ExTrin.)

Hand.-

Mazz.

Ory

zoideae

SouthernChina,streams,marsh

34

*S

eethesamplenumbersinFig.

3.

Na

me

Sub

family

Ecologyordistribution

Sample

no.*

Laboratory procedure for phytolith analysis

All collected plant samples were cleaned with

distilled water in a water bath to remove adher-

ing particles. Leaves and culms of each species

were 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 goeringiiSteud,

were oxidized for 24 h because they contain more

vegetable tallow. The solutions were centrifuged

at 2000 r.p.m. for 10 min, decanted and rinsed

twice with distilled water, and then rinsed with

95% ethanol until the supernatants were clear.

The phytolith sediments were transferred to

storage vials. The residual subsamples weremounted onto microscopic slides in Canada

balsam medium for photomicrography and in

liquid medium for counting and line drawing.

Light photomicrography at 400 magnification

was used to record types of phytoliths found in

each plant sample. An average of 270 lobate

grains was counted in each sample. The percent-

ages of different lobate categories were calculated

on the basis of a sum consisting of all lobate

phytoliths.

Classification of lobate phytoliths

Lobate phytoliths are originated from the short

cells of grasses with identifiable shape character-

istics. Metcalfe (1960) identified three types of

dumbbell or bilobate phytoliths. The Panicoid

division in Twisss classification is composed of

11 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 phytoliths

with definite lobes, including the cross, sinuate

and dumbbell types. Based on our observation

and statistics of the lobate phytoliths from 85

species of modern grass plants, we found that

two important parameters can be used to char-

acterize the morphological variations in lobate

phytoliths: (1) the shape of the outer margins of

the two lobes and (2) the length of the shank in

the lobate structure (Fig. 1). These two parame-

ters are relatively stable among different Panicoi-

deae plants. We develop a lobate classification

matrix based on these two criteria (Fig. 2). PearsallTable2

continued.


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& Piperno (1990) used a somewhat different

approach to distinguish domesticated corn phyto-

liths on the basis of cross-shaped phytolith size

(Pearsall, 1978) and cross-shaped three-dimensional

structures (Piperno, 1984).

The first criterion is the shape or outline of

the lobe. We divide lobate phytoliths into A, B,

C, D and E types based on the characteristics

of ridged lines, rounded, truncated, concave and

branched outer margins, respectively (Fig. 2).

Type A has ridged lines running longitudinallyalong the whole length of the phytolith. The lines

may be radiating towards the distal ends of the

lobes. The shank is often wide and sturdy, con-

necting two indistinct lobes. The outline of the

lobes has obvious edges and corners. Types B is

characterized by having smooth and generally

round outlines on the two lobes. In type C, the

distal ends of the two lobes are truncated, form-

ing a generally straight edge. In type D, the distal

ends of the lobes are slightly indented, forming a

smooth, 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 < 1/3b

Type 2: 1/3b < a < b

Type 3: a b

Type 4: a > b

We divide lobate phytoliths into 20 types

according to the combination of these two crite-

ria. In addition, for the shapes of two half-lobes,

three lobes, three lobes with radiation lines, more

than four lobes and beaded lobes, we group them

under a special category, type F, which consists

of five subtypes (designated by lower-case letters

ae, respectively) according to the number of lobes

present. Thus type F encompasses the trilobate

and polylobate types that have been recognized

widely in previous studies (Brown, 1984; Piperno,

1988). Altogether, there are 25 morphological

types of lobate phytoliths in our classification

system (Fig. 2).

The above classification is based on a two-

dimensional view of phytolith shape, assuming

that a perfect lateral view of the phytolith can be

observed and measured. It should be pointed out

that phytolith, like pollen, is not a two-dimen-

sional object. In reality, phytoliths may be tilted

at an angle from the viewer while being observed

under the microscope. Consequently, great care

must be exercised in observing and describing

Fig. 1 Morphological components of a lobate

phytolith.

Fig. 2 Classification of lobate phytoliths according

to two criteria: outline of the lobes (AF), and

length ratio between shank and lobe (14). See text

for explanation.


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phytolith shapes. Fortunately, because phytoliths

are translucent or transparent, we can recognize

the structure or shape of the reverse side without

having to turn over the specimen under observa-

tion. However, in order to avoid misclassification

due to imperfect angles of observation it is

important to use liquid mount in making phyto-

lith slides, which allows rotation of object and

more accurate measurement of lobe shape and

shank length.

RESULTS

Figure 3 shows the relative abundance of dif-

ferent lobate phytolith types found in each of the

85 grass species. The identified morphotypes are

illustrated in Fig. 4. Table 3 lists the representative

grass taxa of different lobate phytolith types

from China and the south-eastern United States.

Type A is a phytolith with ridged lines on its

shank 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 dispar

A2 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. adscendens

A4 Sacciolepis myosuroides

B1 Arundinella hirta, Eccoilopus cotulifer, Eulalia speciosa, Arundinella setosa, Setaria faberi, Pennisetum

alopecuroides, P. purpureum, Echinochloa. crusgalli, Paspalum dilatatum, Brachiaria ramosa

B2 Setaria glauca, Aristida desmantha, Echinochloa crusgalli var. mitis, Saccharum sinensis, Sorghum

vulgare, Saccharum arundinaceum, Miscanthus floridulus, Miscanthus sinensis, Cenchrus incertus

B3 Setaria glauca, Aristida desmantha, Pennisetum alopecuroides, P. purpureum, Panicum notatum

B4 Arundinella setosa, Schizachyrium brevifolium, Digitaria sanguinalis

C1 Oryza sativa, Leersia hexandra, Zizaniopsis miliacea, Z. caduciflora, Panicum amarum

C2 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 ferruginea

D1 Leersia oryzoides, Zizaniopsis miliacea, Anthaenantia rufa

D2 Leersia oryzoides, Zizania caduciflora, Microstegium vimineum var. imberbe, Leptochloa chinensis

D3 Arundinella setosa, Setaria faberi, S. plicata, S. palmifolia

D4 Cymbopogom goeringii, Ctenium aromaticum

E1 Coix lacryma-jobi, Zea mays, Paspalum orbiculare, P. dilatatum, Echinochloa crusgalli, Brachiaria

ramosa, Themeda triandra var. japonica, Panicum dichotomiforom, Arundinella hirta, Cyrtococcumpatens, Oplismenus compositus, Bothriochloa ischaemum, Echinochloa crusgalli var. mitis, Saccharum

sinensis, Sorghum vulgare

E2 Coix lacryma-jobi, Coix lacryma var. ma-yuen, Zea mays

E3 Setaria palmifolia, Themeda triandra var. japonica, Panicum dichotomiforom

E4 ?

Fa Capillipedium assimile, Panicum verrucosum

Fb Eulalia speciosa, Rottboellia exaltata, Capillipedium assimile, Panicum verrucosum, Oplismenus

undulatifolius

Fc Sacciolepis myosuroides

Fd Panicum bisulcatum, Spodipogon sibiricus

Fe Apluda mutica


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Fig. 3 Percentages of lobate phytolith morphotypes calculated based on the sum of lobate phytolith counts for ea

the left axis: 1, Arundinella hirta 2, Eccoilopus cotulifer 3, Eulalia speciosa 4, Arundinella setosa 5, Setaria faberi 6, S. pl

S. sp. 10, Aristida desmantha 11, Pennisetum alopecuroides 12, P. purpureum 13, Panicum notatum 14, Digitaria sanguin

16, Chasmanthium laxum 17, Andropogon glomeratus 18, Chasmanthium ornithorhynchum 19, Erianthus strictus 20, Andr

22, Imperata cylindrica 23, Themeda gigantea var. caudate 24, Themeda triandra var. japonica 25, Schizachyrium br

ferruginea 28, Apluda mutica 29, Rottboellia exaltata 30, Capillipedium assimile 31, Panicum verrucosum 32, Microste

34, Zizania caduciflora 35, Oryza sativa 36, Leersia hexandra 37, L. oryzoides 38, Zizaniopsis miliacea 39, Isachne dispa

aromaticum42,

Oplismenus undulatifolius43,

Sacciolepis myosuroides44,

Cyrtococcum patens45,

Oplismenus compPogonatherum crinitum 48, Arthraxon hispidus var. cryptatherus 49, Digitaria violascens 50, Ischaemum antephoroides 5

var. imberbe 53, Ischaemum aristatum 54, Digitaria sanguinalis 55, Digitaria adscendens 56, Panicum bisulcatum 57, Spo

Bothriochloa ischaemum (Southern China) 60, B. ischaemum (Northern China) 61, Capillipedium parviflorum 62, A

64, Panicum virgatum 65, Sorghum vulgare 66, Echinochloa crusgallivar. mitis 67, Saccharum sinensis 68, Saccharum o

70, Miscanthus floridulus 71, M. sinensis 72, Cenchrus incertus 73, Panicum repens 74, Hackelochloa granularia 75, C

ma-yuen 77, Zea mays 78, Paspalum orbiculare 79, Echinochloa colonum 80, E. crusgalli81, Paspalum dilatatum 82,

84, Panicum dichotomiflorum 85, P. hemitomon. The order of arrangement of different grass species is based on th


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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, Zea

mays 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 ferruginea

22, Dimeria ornithopoda 23, Eragrostis japonica 26, 27, Paspalum orbiculare 28, Oplismenus compositus 29,

Apluda mutica 30, Oplismenus undulatifolius.


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dispar. A2 is represented by a wide range of grass

taxa that are distributed mainly in the hillsides,

grasslands, coasts and wetlands of southern

China up to the Yangtze River. A3 is represented

mainly by several species of Digitaria. Most of

these 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 (Sacciolepis

myosuroides) (Fig. 3, no. 43).

Type B are phytoliths with smooth rounded

lobes. B1 occurs in many species of grasses, but

its 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 in

fields and roadside habitats or in warm and

humid environments. Representatives of B3 are

Setaria glauca (Fig. 3, no. 8), Aristida desmantha,

Pennisetum alopecuroides, P. purpureum and

Panicum notatum (Fig. 3, nos 10, 11, 12, 13). They

grow mainly on the hillsides, roadsides and dry

sand dunes of relatively dry environments. B4 is

an uncommon type that occurs only at relativelylow frequencies in a few taxa.

Type C, a phytolith with truncated margins at

both ends of its lobes, has the largest number of

representative plants. To some extent, C1 may be

considered to be diagnostic of the Oryzoideae

subfamily, occurring abundantly in such species

as Oryza sativa (paddy rice), Leersia hexandra

(wild rice), Zizaniopsis miliacea and Z. caduciflora

(water bamboo) (Fig. 3, nos 3538). Among other

grasses, only Panicum amarum (Fig. 3, no. 83) of

the Panicoideae subfamily, a typical aquatic and

hygrophytic species, produces this type of phyto-

liths in significant abundance. C2 is well repre-

sented in a large number of grass taxa that notably

include Panicum bisulcatum, P. virgatum, Sorghum

halepense (Fig. 3, nos 56, 64, 63) Saccharum

officinarum, Miscanthus floridulus and M. sinen-

sis , among others. These grasses are distributed

widely in East China; most are hygrophytes and

mesophytes. C3 is found in a smaller range of

grasses than C2, but it occurs in great abundance

in several taxa including, for example, Digitaria

sanguinalis var. ciliaris, Dimeria ornithopoda,

Chasmanthium laxum, Andropogon glomeratus

(Fig. 3, nos 1417), Erianthus strictus, Sorghas-

trum nutans and Imperata cylindrica. These are

mainly heliophytes and drought-enduring meso-

phytes and xerophytes, growing typically on

mountain slopes in both southern and northernChina, and on forest edges and disturbed areas

of pine woodlands and prairie regions in the

United States. The C4 group is basically diagnos-

tic of Eragrostis japonica and E. ferruginea

(Fig. 3, nos 26, 27), as well as Schizachyrium

brevifolium (Fig. 3, no. 25). The genus Eragrostis,

a member of Chloridoideae, is found typically in

areas of warm and dry climatic conditions.

Type D is phytoliths with concave margins

at the end of the lobes. There are only a few

representative plants of D1 (Leersia oryzoides,Zizaniopsis miliacea and Anthaenantia rufa

(Fig. 3, no. 62) and D4 (Cymbopogom goeringiiand

Ctenium aromaticum (Fig. 3, nos 40, 41). The

representatives of D2 are Leersia oryzoides,

Zizania caduciflora, Microstegium vimineum var.

imberbe and Leptochloa chinensis, which grow

mainly in roadside wet ditches, stream channels

and other wet habitats such as lakeshores. D3

phytoliths 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 subtropical

environments.

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 somewhat

variable. 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 regions

of the world, such as Zea mays (maize), Coix

lacryma-jobi (Jobs tears), Saccharum sinensis

(sugar cane) and Sorghum vulgare (kaoliang or

sorghum) (Fig. 3, nos 77, 75, 67, 65). E2 occurs

abundantly only in Coix lacryma var. ma-yuen

(Jobs tears), a crop cultivated commonly in China.

Incidentally, Coix lacryma var. ma-yuen and

other members of the Maydeae subfamily pro-

duce only the E2 and E1 phytoliths. E3 can be

found in many plants, but by itself is diagnostic

of none. No E4 phytoliths were found in our

samples in this study, although this morphotype

has been observed in fossil assemblages (H.Y. Lu,

unpublished data).


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Type F has multiple lobes and can be found

in many plants. The plants that can produce the

F type include Capillipedium assimile, Panicum

verrucosum (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 are

distributed mainly in the southern parts of China.

It is worth noting that lobate phytoliths are

also found in a few Chloridoideae plants, for

example, in Leptochloa chinensis (C2), Eragrostis

japonica and E. ferruginea (C4). More studies are

needed on these non-Panicoideae grasses that

produce lobate phytoliths.

DISCUSSION

Morphological variations in lobate phytoliths

from C3 grasses

Early phytolith researchers noted that the differ-

ent subfamilies of grass plants produce different

phytolith shapes: Panicoideae produces dumbbell

and cross-shaped phytoliths; Festucoid forms

rondels and sinuous types, and Chloridoideae

yields saddles (Brown, 1984; Mulholland, 1989;

Fearn, 1998). The shape of individual phytolithsfrom grasses can be used as an indication of C3 or

C4 photosynthetic pathways. For example, saddle

phytolith indicates C4 short-grass prairie species

that flourish in warm, arid to semi-arid regions

where the available soil moisture is very low, whereas

dumbbell and cross phytoliths represent the grasses

of the C4 tall-grass prairies, which have high to

medium soil-moisture availability (Twiss, 1992).

In this study, we found that several C3

grasses (Waller et al., 1979; Gould & Shaw, 1983;

Lu & Wang, 1991) also produce characteristic

lobate morphotypes, such as Zizania caduciflora,

Oryza sativa, Leersia hexandra, L. oryzoides and

Zizaniopsis miliacea of the Oryzoideae sub-

family, and Oplismenus compositus, O. compositus,

Sacciolepis myosuroides and Isachne dispar of

the Panicoideae subfamily. Lobate phytoliths in

Oryzoideae are characterized by high propor-

tions of C1 and, to a lesser extent, D1 types with

very short shank between the lobes. Other C3

grasses from Panicoideae produce characteristic

A1 and A2 types with ridged lines on its lobes

and 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 are

distributed widely in tropical and subtropical

regions of the world.

Morphological variations in lobate phytoliths

from Chloridoideae

Lobate phytoliths from the Chloridoideae sub-

family have been reported by Brown (1984) and

Mulholland (1989). In this study, many varia-

tions in lobate phytoliths were observed in

Chloridoideae (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 4098% of the lobates are C4

and D4 types with very a long shank between the

lobes (Fig. 3, nos 26, 27, 41). These species are

distributed widely in warm and arid regions. B2

and B3 types are the dominant phytoliths of

Aristida desmantha (Fig. 3, no. 10) that also

belongs to the Chloridoideae subfamily (or the

Arundinoideae 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 United

States. Leptochloa chinensis (Fig. 3, no. 33) yields

only two phytolith types: D2 (83%) and D3 (17%).

Can we infer grass genera from lobate

phytolith assemblages?

The classification of phytolith shapes has long

been criticized due to the multiplicity and redun-

dancy of many grass morphotypes a problem

preventing the attribution of individual phytolith

to species or genus (Rovner, 1971; Brown, 1984;

Mulholland, 1989). Because the same shapes of

phytoliths can occur in different grass taxa, a

single phytolith morphotype cannot be ascribed

to a specific grass species. However, a phytolith

assemblage could, to some extent, allow us to

infer the predominant subfamily constituting the

grass associations. Recently, many researchers

have paid particular attention to this specific

taxonomic problem of redundancy for grass

phytolith classification. They indicated that it would

never be possible to eliminate all redundancies at


13/15



the subfamily level, much less for genus (Fredlund

& Tieszen, 1994).

In this study, we tried to find a potential rela-

tionship between the morphological variations

in lobate phytoliths and the grass genera that

produce 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 defined

by a high abundance of D3 type. The two species

of Eragrostis (E. japonica, E. ferruginea; sub-

family Chloridoideae) produce almost exclusively

the C4 type of lobate phytoliths. Zizania caduci-

flora, Oryza sativa, Leersia hexandra, L. oryzoides

and Zizaniopsis miliacea, all belonging to the

subfamily Oryzoideae, produce a significant amount

of C1 and, to some extent, D2 types of lobatephytoliths. Miscanthus yields primarily B2 and

C2 types of phytoliths. Maydeae (Coix lacryma-

jobi, C. l. var. ma-yuen, Zea mays) yields only E1

and E2 (cross) types. Remarkably, the three species

of Saccharum (S. sinensis, S. officinarum and S.

arundinaceum) produces different lobate phytolith

assemblages (Fig. 3). Saccharum sinensis (sugar

cane), in particular, is characterized by the

codominance of E1 (54%) and B2 (29%) types,

whereas S. officinarum is characterized by the

codominance of C2 (35%) and C3 (24%) types,and S. arundinaceum by the preponderance of

B2 (51%) mixed with some E1 and B1.

Unfortunately, not all lobate phytolith assem-

blages have a definite and consistent relationship

with the grass genera that produce them, because

grasses only produce a limited range of lobate

phytoliths, which often overlap from genus to

genus. Moreover, the relatively limited sample

size in each genus used in this study prevents us

from generalizing the characteristics of lobate

assemblages for all grass genera.

Morphological changes in lobate phytoliths

along an environmental gradient

Although different parts of plant body from

one species often contribute different lobate

phytoliths to an assemblage, many grasses do

produce predominantly a specific phytolith type

recognizable by distinct shape, sculpture or size

that can be assigned to a given taxon at various

levels. Morphological variations in phytoliths can

be produced by both botanical and environmental

factors (Mulholland et al., 1988). Thus, it is

possible to discuss the morphological changes in

lobate phytoliths along environmental gradients.

As shown in Fig. 3, the representatives of C1

are Oryzoideae that typically consist of aquatic

and hygrophytic grasses. The principal membersof B1 type are the grasses frequently growing in

wet areas and on lakeshores, such as Echinochloa

crusgalli (Fig. 3, no. 80) and Paspalum dilatatum

(Fig. 3, no. 81). Grasses from the Chloridoideae

subfamily (e.g. Eragrostis) and Panicoideae

subfamily (e.g. Cymbopogom goeringii, Ctenium

aromaticum; Fig. 3, nos 40, 41) that grow in dry

conditions produce predominantly C4 and D4

phytoliths. Grasses of the Maydeae subfamily,

found typically in warm and moist areas, yield

predominantly the cross phytoliths of E1 and E2types. The representative grasses of B3 and B4

types (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 that

the progression from type 1 to type 4 represents

an environmental gradient of decreasing moisture

(i.e. from wet to dry). In other words, grasses

growing in drier habitats or environments tend to

produce phytoliths with a longer shank and viceversa. The environmental significance of the pro-

gression from types AE is less clear at this point.

What is the cause of morphological variability

in lobate phytoliths? Is it environmental pheno-

type or genotype? Wang & Lu (1993) compared

morphological changes in short cell phytoliths

from the same species of grasses growing in dif-

ferent environmental conditions in China. They

showed that phytolith shapes are relatively stable,

but sizes can change slightly. Piperno (1988)

suggested that phytoliths formed in the short

cells of the grass epidermis are under a consider-

able degree of active genetic control. To date, no

strong evidence can be found from our data to

resolve the question of whether phytolith shapes

are phenotype or genotype.

Regardless of the cause of morphological

variations, our study suggests that in some ways

phytolith morphology could be linked to grass

taxonomy (e.g. C1 is diagnostic of Oryzoideae).

As many grass taxa tend to have certain typical

environmental adaptations (e.g. Oryzoideae

occurring typically in wet habitats), it may be


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possible to use phytolith morphology as a proxy

for environmental conditions. More work is

needed to substantiate this point.

CONCLUSIONS

This study documents the variability of 25 diag-

nostic lobate phytolith shapes occurring among

85 modern grass species collected from a variety

of environments in China and the south-eastern

United States. We propose a classification that is

based on two important morphological parame-

ters: the length of the lobate shank and the shape

of the outer margin of the two lobes. These two

morphological characteristics are relatively stable

among the 85 modern grass species belonging to

the Panicoideae, Chloridoideae, Oryzoideae andArundinoideae subfamilies. In some cases, the

identification of tribe or even genus is possible

based on the differences in lobate shape param-

eters or the composition of assemblages. How-

ever, we should point out that not all of the

lobate assemblages have a consistent and definite

relationship with the genera that produce them.

This is because grasses can only produce a

limited range of lobate shapes, and there is often

considerable 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 characterized

by a high proportion of C1 and D1 types and by

a very short shank between the lobes. Other C3

grasses from Panicoideae produce characteristic

A1 and A2 types with ridged lines and F type

with multiple lobes.

The Chloridoideae subfamily produces lobate

assemblages in which 4098% of phytoliths are

C4 and D4 types with a very long shank between

the lobes. This group of grasses is widely distrib-

uted in warm and arid regions.

We also found that the variations of lobate

morphologies can be related to environmental

factors, especially moisture. Typical hygrophytic

grasses tend to yield lobate phytoliths with a very

short shank, whereas typical xerophytic grasses

tend to produce lobate phytoliths with very long

shank. This relationship, if supported by addi-

tional studies of lobate phytoliths derived from

more grass species and from a wider range of

environmental conditions, offers potential for

using phytoliths in palaeoclimatic reconstruction.

ACKNOWLEDGMENTS

We thank Y.J. Wang, X.Y. Zhou, C.A. Reese and

C.M. Shen for providing modern grass reference

samples and for helpful discussion. We are

grateful to S.C. Mulholland, G.G. Fredlund andI. Rovner for valuable comments on an earlier

version of this manuscript. We also thank the two

anonymous reviewers for their helpful reviews of

our original manuscript. This work was supported

by NSFC (40024202, 49971077 and 49894174),

NKBRSF (G1998040810), the Risk Prediction

Initiative (RPI) of the Bermuda Biological Station

for Research (RPI-00-1-002) and the U.S.

National Science Foundation (SES-9122058;

BCS-0213884).

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