Diversity and Distributions (2003) 9, 73 – 8 7
BIODIVERSITY RESEARCH
Morphological variations of lobate phytoliths from grasses
in China and the south-eastern United States
Blackwell Science, Ltd
HOUYUAN LU 1,2 * and KAM-BIU LIU 2 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 useful
tool in palaeoenvironmental and archaeobotanical research. Lobate phytolith is one of the most
important morphotypes of grass phytoliths. This
study describes morphological variations of diagnostic 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 parameters: (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
INTRODUCTION
Grasses (Family: Gramineae) are an important
group of plants in a variety of environments
(Gould & Shaw, 1983). They are often the dominant 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
* Corresponding author.
a definite relationship with the genera that
produce them, because grasses can only produce
a limited range of lobate shapes that often overlap 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 environmental 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 palaeoclimatic reconstruction.
Key words. Dumbbell, grasses, palaeoenvironment,
palynology, phytoliths, phytolith-lobate, silica
bodies, taxonomy.
grasses from fossil assemblages are of great significance 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 reconstruction is limited. Grass phytoliths, on the
other hand, offer a promising means to differentiate grasses at subfamily levels and, accordingly,
to infer subtle changes in palaeoenvironmental
conditions (Piperno, 1988; Rapp & Mulholland,
1992; Fredlund & Tieszen, 1994, 1997; Alexandre
et al., 1997; Runge, 1999). In this paper, we focus
© 2003 Blackwell Publishing Ltd. http://www.blackwellpublishing.com/journals/ddi
73
74
H. Lu and K.-b. Liu
on the predominant type of grass phytoliths — the
lobate phytoliths, based on an investigation of
250 species of grasses from China and the southeastern 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 phytolith 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 (µm) to about 150 µm.
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 different
phytolith shapes; for example, grasses of the
subfamily Panicoideae produce dumbbell and
cross-shaped phytoliths, whereas Pooideae (Festucoideae) grasses produce rondels and sinuous
types, and Chloridoideae grasses produce saddleshaped phytoliths (Twiss et al., 1969). All members 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. Existing 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. redundancy) (Rovner, 1971). In order to use phytoliths
as a tool in environmental reconstruction and
taxonomy, it is necessary to recognize morphological 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 morphological term for the shape of some intercostal
short cell phytoliths. It has gradually become a
name given to a loosely defined group of phytoliths 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 more
comprehensible to non-English-speakers. For this
reason, we follow the convention of these subsequent 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,
© 2003 Blackwell Publishing Ltd, Diversity and Distributions, 9, 73– 87
Morphological variations of lobate phytolith
75
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
Andropogon ternaries Michx.
Anthaenantia rufa (Nutt.) Schult.
Aristida desmantha Trin. & Rupr.
Cenchrus incertus M. Curtis
Chasmanthium laxum (L.) Yates.
Chasmanthium ornithorhynchum
(Steud.) Yates
Ctenium aromaticum (Walter)
A.W. Wood
Erianthus strictus Spreng.
Leersia oryzoides (L.) Sw.
Panicoideae
Panicoideae
Panicoideae
Chloridoideae
Panicoideae
Arundinoideae
Arundinoideae
Generally on wet sites
Edge of pine forest
Pine forest
Sandy soil along coast
Dry sand
Edge of forest
Moist area in pine flatwoods
17
20
62
10
72
16
18
Chloridoideae
Edge of forest
41
Panicoideae
Oryzoideae
19
37
Panicum amarum Elliott
Panicum dichotomiflorum Michx.
Panicoideae
Panicoideae
Panicum hemitomon Schult.
Panicoideae
Panicum verrucosum Muhl.
Panicoideae
Panicum virgatum L.
Panicoideae
Saccharum officinarum L.
Setaria sp.
Sorghastrum nutans (L.) Nash
Panicoideae
Panicoideae
Panicoideae
Edge of pine forest and disturbed areas
Wet roadside ditches and edges of
lakes, streams, and other wet areas
Sandy soil along coast
Disturbed areas, especially in moist
regions, throughout United States
Coastal marsh, wet areas and in the
inland part of coastal sites
Frequent; disturbed areas and edges
of forests, mostly in the pine regions
Frequent; edges of pine forests and
remnant strips in prairie regions; cheniers and
spoil banks in coastal freshwater marsh
Cultivated in tropical regions of the world
Sorghum halepense (L.) Pers.
Zizaniopsis miliacea (Michx.)
Doell & Aschers.
Panicoideae
Oryzoideae
83
84
85
31
64
68
9
21
Edge of forest and disturbed areas in
pine and prairie regions
Widespread throughout the world
63
Edges of lakes, streams, wet roadside ditches 38
* See the sample numbers in Fig. 3.
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 application 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 presented 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 nomenclature 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.
© 2003 Blackwell Publishing Ltd, Diversity and Distributions, 9, 73– 87
Subfamily
Ecology or distribution
Apluda mutica L.
Arthraxon hispidus Makino var. cryptatherus (Hack.) Honda
Arundinella hirta (Thunb.) Tanaka
Panicoideae
Panicoideae
Panicoideae
Arundinella setosa Trin.
Bothriochloa ischaemum (L.) Keng
Brachiaria ramose (L.) Stapf
Capillipedium assimile (Steud.) A. Camus
Capillipedium parviflorum (R.Br.) Stapf
Coix lacryma var. ma-yuen (Roman.) Stapf
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Coix lacryma-jobi L.
Panicoideae
Cymbopogom goeringii Steud
Cyrtococcum patens (L.) A. Camus
Digitaria adscendens (H. B.K.) Henrard
Digitaria sanguinalis (L.) Scop.
Digitaria sanguinalis var. ciliaris (Retz.) Parl.
Digitaria violascens Link
Dimeria ornithopoda Trin
Eccoilopus cotulifer (Thunb.) A. Camus
Echinochloa colonum (L.) Link
Echinochloa crusgalli (L.) Beauv.
Echinochloa crusgalli var. mitis (Pursh) Peterm
Eragrostis ferruginea (Thunb.) Beauv.
Eragrostis japonica (Thunb.) Trin.
Eriochloa villosa (Thunb.) Kunth
Eulalia speciosa (Debeaux) Kuntze
Hackelochloa granularia (L.) Kuntze
Imperata cylindrical (L.) Beauv. Var. major (Nees) C.E. Hubb.
Isachne dispar Trin.
Ischaemum aristatum L.
Ischaemum antephoroides (Steud.) Miq.
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Chloridoideae
Chloridoideae
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Chloridoideae
Panicoideae
Panicoideae
Southern China, edge of woodlands, side of streams
Temperate regions of China, hillside, moist area
East China, frequent growing in valley, side of
streams, wetter sites
Southern China, hillside
Temperate regions of the world, hillside, roadside
Tropical regions of the world
East China, hillside
East China, hillside, roadside
Temperate and subtropical regions of
the world, wet areas
Temperate and subtropical regions of
the world, wet areas
Hillside
Southern China, edge of forest
Field, throughout China
Hillside, field, throughout China
Southern China
Southern China, roadside, hillsidefield
Southern China, wet areas, hillside
Southern China, hillside, field
East China, wet areas, roadside
Temperate regions of the world, swamp, rice paddy
Temperate regions of the world, swamp, wet areas
East China, roadside, field
Southern China, hillside, field
East China, wet areas
East China, hillside
Tropical regions of the world, edges of streams
Throughout China, dry soils
Southern China, hillside, forest and edges of streams
East China, hillside, roadside, coast
Southern China, hillside, field, coast
Sample
no.*
28
48
1
4
59, 60
82
30
61
76
75
40
44
55
54
14
49
15
2
79
80
66
27
26
58
3
74
22
39
53
50
H. Lu and K.-b. Liu
© 2003 Blackwell Publishing Ltd, Diversity and Distributions, 9, 73– 87
Name
76
Table 2 List of modern grasses from China used for the analysis of lobate phytoliths
Sample
no.*
Name
Subfamily
Ecology or distribution
Ischaemum indicum (Houtt.) Merr.
Leersia hexandra Swartz
Panicoideae
Oryzoideae
51
36
Leptochloa chinensis (L.) Nees
Chloridoideae
Microstegium vimineum (Trin.) A. Camus
Microstegium vimineum (Trin.) A. Camus var. imberbe
(Nees) Honda
Miscanthus floridulus (Labill.) Warb
Miscanthus sinensis Anderss
Oplismenus compositus (L.) Beauv
Oplismenus undulatifolius (Arduino) Roem. Et Schult
Oryza sativa L.
Panicum austro-asiaticum Ohwi
Panicum bisulcatum Yhunb
Panicoideae
Panicoideae
Southern China, hillside, roadside, coast
Southern China, a perennial grass growing in standing
water or very damp ground
Southern China, a common annual of waste fields
and paddy fields
East China, moist area
East China, moist area
70
71
45
42
35
46
56
Panicum notatum Retz
Panicum repens L.
Paspalum dilatatum Porst
Paspalum orbiculare G. Forst
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Pennisetum alopecuroides (L.) Spreng
Pennisetum purpureum Schumach
Panicoideae
Panicoideae
Pogonatherum crinitum (Thunb.) Kunth
Panicoideae
Rottboellia exaltata L. f.
Saccharum arundinaceum Retz
Saccharum sinensis Roxb
Sacciolepis myosuroides (R.Br.) A. Camus
Schizachyrium brevifolium (Sw.) Nees ex Buse
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Setaria faberi Herrm.
Setaria glauca (L.) Beauv.
Panicoideae
Panicoideae
Southern China, hillside wet areas, forest
Hillside, edges of streams
Southern China, wet areas, shady places under trees
East China, wet areas, edge of forest
Cultivated worldwide
Southern China, wet areas
East China, wet areas, edges of lakes, streams, wet
roadside ditches
Southern China, edge of forest
Tropical and subtropical zones, waterside, coast
Wet areas
Tropical and subtropical regions of the
world, hillside, field
Disturbed areas throughout China
Elephant grass, native to Africa, a robust perennial
with culms 2–4 meters tall
Southern China, banks, edges of streams, often in
sandy places.
Southern China, hillside, roadside
Southern China, hillside, edges of streams
Cultivated in tropical regions of the world
Southern China, paddy field
East China, an annual grass of rocky places with
poor soil, hillside
China, north of Yangtze River
Temperate and tropical zones, field and roadside
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Oryzoideae
Panicoideae
Panicoideae
33
32
52
13
73
81
78
11
12
47
29
69
67
43
25
77
5
8
Morphological variations of lobate phytolith
© 2003 Blackwell Publishing Ltd, Diversity and Distributions, 9, 73– 87
Table 2 continued.
All collected plant samples were cleaned with
distilled water in a water bath to remove adhering particles. Leaves and culms of each species
were placed in 20 mL of saturated nitric acid for
over 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 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 were
mounted 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 percentages of different lobate categories were calculated
on the basis of a sum consisting of all lobate
phytoliths.
Classification of lobate phytoliths
* See the sample numbers in Fig. 3.
Southern China, valley, hillside
Southern China, valley, wet areas
Cultivated in temperate regions of the world
Temperate regions of the world, hillside, forest
Southern China, hillside grassplot, edges of streams
East, China, dry hillside
Cultivated worldwide
Southern China, streams, marsh
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Panicoideae
Oryzoideae
Setaria palmifolia (Koen.) Stapf
Setaria plicata (Lamk.) T. Cooke
Sorghum vulgare Pers.
Spodipogon sibiricus Trin.
Themeda gigantean var. caudate (Nees) Keng
Themeda triandra var. japonica (Willd.) Makino
Zea mays L.
Zizania caduciflora (Turcz. Ex Trin.) Hand.-Mazz.
Name
Ecology or distribution
7
6
65
57
23
24
77
34
Laboratory procedure for phytolith analysis
Subfamily
Sample
no.*
H. Lu and K.-b. Liu
Table 2 continued.
78
Lobate phytoliths are originated from the short
cells of grasses with identifiable shape characteristics. Metcalfe (1960) identified three types of
dumbbell or bilobate phytoliths. The Panicoid
division in Twiss’s classification is composed of
11 types of dumbbells and crosses (Twiss et al.,
1969). Brown (1984) recognized bilobates, polylobates 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 characterize 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 parameters are relatively stable among different Panicoideae plants. We develop a lobate classification
matrix based on these two criteria (Fig. 2). Pearsall
© 2003 Blackwell Publishing Ltd, Diversity and Distributions, 9, 73– 87
Morphological variations of lobate phytolith
Fig. 1 Morphological
phytolith.
components
of
a
lobate
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 longitudinally
along 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, connecting 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, forming 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 of
the 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
Type
Type
Type
Fig. 2 Classification of lobate phytoliths according
to two criteria: outline of the lobes (A – F), and
length ratio between shank and lobe (1– 4). See text
for explanation.
& Piperno (1990) used a somewhat different
approach to distinguish domesticated corn phytoliths on the basis of cross-shaped phytolith size
(Pearsall, 1978) and cross-shaped three-dimensional
structures (Piperno, 1984).
79
1:
2:
3:
4:
a < 1/3b
1/3b < a < b
a ≈ b
a >b
We divide lobate phytoliths into 20 types
according to the combination of these two criteria. 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
a– e, 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 twodimensional 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-dimensional 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
© 2003 Blackwell Publishing Ltd, Diversity and Distributions, 9, 73– 87
80
H. Lu and K.-b. Liu
Table 3 List of 25 lobate phytolith types and their representative grass taxa
Lobate
types Representative Taxa
A1
A2
A3
A4
B1
B2
B3
B4
C1
C2
C3
C4
D1
D2
D3
D4
E1
E2
E3
E4
Fa
Fb
Fc
Fd
Fe
Isachne dispar
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
Digitaria sanguinalis, D. sanguinalis var. ciliaris, D. adscendens
Sacciolepis myosuroides
Arundinella hirta, Eccoilopus cotulifer, Eulalia speciosa, Arundinella setosa, Setaria faberi, Pennisetum
alopecuroides, P. purpureum, Echinochloa. crusgalli, Paspalum dilatatum, Brachiaria ramosa
Setaria glauca, Aristida desmantha, Echinochloa crusgalli var. mitis, Saccharum sinensis, Sorghum
vulgare, Saccharum arundinaceum, Miscanthus floridulus, Miscanthus sinensis, Cenchrus incertus
Setaria glauca, Aristida desmantha, Pennisetum alopecuroides, P. purpureum, Panicum notatum
Arundinella setosa, Schizachyrium brevifolium, Digitaria sanguinalis
Oryza sativa, Leersia hexandra, Zizaniopsis miliacea, Z. caduciflora, Panicum amarum
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
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
Schizachyrium brevifolium, Eragrostis japonica, Eragrostis ferruginea
Leersia oryzoides, Zizaniopsis miliacea, Anthaenantia rufa
Leersia oryzoides, Zizania caduciflora, Microstegium vimineum var. imberbe, Leptochloa chinensis
Arundinella setosa, Setaria faberi, S. plicata, S. palmifolia
Cymbopogom goeringii, Ctenium aromaticum
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
Coix lacryma-jobi, Coix lacryma var. ma-yuen, Zea mays
Setaria palmifolia, Themeda triandra var. japonica, Panicum dichotomiforom
?
Capillipedium assimile, Panicum verrucosum
Eulalia speciosa, Rottboellia exaltata, Capillipedium assimile, Panicum verrucosum, Oplismenus
undulatifolius
Sacciolepis myosuroides
Panicum bisulcatum, Spodipogon sibiricus
Apluda mutica
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 observation. However, in order to avoid misclassification
due to imperfect angles of observation it is
important to use liquid mount in making phytolith slides, which allows rotation of object and
more accurate measurement of lobe shape and
shank length.
RESULTS
Figure 3 shows the relative abundance of different 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
© 2003 Blackwell Publishing Ltd, Diversity and Distributions, 9, 73– 87
Morphological variations of lobate phytolith
© 2003 Blackwell Publishing Ltd, Diversity and Distributions, 9, 73– 87
81
Fig. 3 Percentages of lobate phytolith morphotypes calculated based on the sum of lobate phytolith counts for each grass samples. Sample numbers on
the 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 ornithopoda
16, Chasmanthium laxum 17, Andropogon glomeratus 18, Chasmanthium ornithorhynchum 19, Erianthus strictus 20, Andropogon ternaries 21, Sorghastrum nutans
22, 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 chinensis
34, Zizania caduciflora 35, Oryza sativa 36, Leersia hexandra 37, L. oryzoides 38, Zizaniopsis miliacea 39, Isachne dispar 40, Cymbopogom goeringii 41, Ctenium
aromaticum 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 vimineum
var. 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 halepense
64, Panicum virgatum 65, Sorghum vulgare 66, Echinochloa crusgalli var. mitis 67, Saccharum sinensis 68, Saccharum officinarum 69, Saccharum arundinaceum
70, 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 amarum
84, Panicum dichotomiflorum 85, P. hemitomon. The order of arrangement of different grass species is based on the results of cluster analysis.
82
H. Lu and K.-b. Liu
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.
© 2003 Blackwell Publishing Ltd, Diversity and Distributions, 9, 73– 87
Morphological variations of lobate phytolith
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 and
are found commonly in wet areas such as lakeshores, 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. Representative species of B2 are Aristida desmantha
(Fig. 3, no. 10), Saccharum sinensis (sugar cane,
Fig. 3, no. 43), Sorghum vulgare (kaoliang or
sorghum, 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 relatively
low 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 35–38). Among other
grasses, only Panicum amarum (Fig. 3, no. 83) of
the Panicoideae subfamily, a typical aquatic and
hygrophytic species, produces this type of phytoliths in significant abundance. C2 is well represented 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. sinensis, 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,
83
Chasmanthium laxum, Andropogon glomeratus
(Fig. 3, nos 14 –17), Erianthus strictus, Sorghastrum nutans and Imperata cylindrica. These are
mainly heliophytes and drought-enduring mesophytes and xerophytes, growing typically on
mountain slopes in both southern and northern
China, and on forest edges and disturbed areas
of pine woodlands and prairie regions in the
United States. The C4 group is basically diagnostic 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 goeringii and
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), species
found typically in warm and wet subtropical
environments.
Type E is phytoliths with branched outer margins at the end of the lobes. E1 is a typical crossshape, the size and shape of which is somewhat
variable. This type of phytolith occurs predominantly in a number of species that include
(although not restricted to) some important agricultural crops in the temperate and tropical regions
of the world, such as Zea mays (maize), Coix
lacryma-jobi (Job’s 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
(Job’s tears), a crop cultivated commonly in China.
Incidentally, Coix lacryma var. ma-yuen and
other members of the Maydeae subfamily produce 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).
© 2003 Blackwell Publishing Ltd, Diversity and Distributions, 9, 73– 87
84
H. Lu and K.-b. Liu
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, Oplismenus 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 different 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 phytoliths
from 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 subfamily, and Oplismenus compositus, O. compositus,
Sacciolepis myosuroides and Isachne dispar of
the Panicoideae subfamily. Lobate phytoliths in
Oryzoideae are characterized by high proportions 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 Panicoideae subfamilies in this study are adapted typically 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 subfamily have been reported by Brown (1984) and
Mulholland (1989). In this study, many variations in lobate phytoliths were observed in
Chloridoideae (including Eragrostis japonica, E.
ferruginea, Ctenium aromaticum, Aristida desmantha and Leptochloa chinensis).
Eragrostis japonica, E. ferruginea and Ctenium
aromaticum produce different phytolith assemblages in which 40 – 98% 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 classification system of Watson et al., 1985). The sample of Aristida desmantha was collected from dry
sand 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 redundancy 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
© 2003 Blackwell Publishing Ltd, Diversity and Distributions, 9, 73– 87
Morphological variations of lobate phytolith
the subfamily level, much less for genus (Fredlund
& Tieszen, 1994).
In this study, we tried to find a potential relationship between the morphological variations
in lobate phytoliths and the grass genera that
produce them (Fig. 3, Table 3). We found some
interesting 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; subfamily Chloridoideae) produce almost exclusively
the C4 type of lobate phytoliths. Zizania caduciflora, 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 lobate
phytoliths. Miscanthus yields primarily B2 and
C2 types of phytoliths. Maydeae (Coix lacrymajobi, 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 assemblages 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
85
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 members
of 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 E2
types. 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 vice
versa. The environmental significance of the progression from types A–E is less clear at this point.
What is the cause of morphological variability
in lobate phytoliths? Is it environmental phenotype or genotype? Wang & Lu (1993) compared
morphological changes in short cell phytoliths
from the same species of grasses growing in different 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 considerable 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
© 2003 Blackwell Publishing Ltd, Diversity and Distributions, 9, 73– 87
86
H. Lu and K.-b. Liu
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 diagnostic 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 parameters: 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 and
Arundinoideae subfamilies. In some cases, the
identification of tribe or even genus is possible
based on the differences in lobate shape parameters or the composition of assemblages. However, 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 grasses
of the Oryzoideae subfamily produce characteristic 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 40 –98% of phytoliths are
C4 and D4 types with a very long shank between
the lobes. This group of grasses is widely distributed 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 additional 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 and
I. 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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