Estuarine, Coastal and Shelf Science 58 (2003) 587600

Phytoliths of common grasses in the coastal environments of southeastern USA

Houyuan Lua,b, Kam-biu Liub,*
Institute of Geology and Geophysics, Chinese Academy of Sciences, P.O. Box 9825, Beijing 100029, China b Department of Geography and Anthropology, Louisiana State University, Baton Rouge, LA 70803, USA Received 28 October 2002; received in revised form 8 May 2003; accepted 8 May 2003
a

Abstract Thirty-four grass species were collected for phytolith analysis from a variety of coastal environments in the southeastern USA (Georgia, Florida, and Louisiana), including salt marshes, freshwater/brackish marshes, pine/oak forests, maritime hardwood forests, and sand dunes. Phytoliths produced by these modern grasses include a large diversity of shapes and types. We propose a preliminary relationship between modern coastal plant communities and their predominant phytolith contents. The dominant grasses of coastal sand dunes, such as Uniola paniculata, produce primarily at tower and two-horned tower phytoliths. Rondel/ saddle ellipsoid phytoliths are mainly produced by Spartina alterniora, the most common plant in coastal salt marshes. Rondel and spool/horned tower phytoliths are common in brackish marsh grasses. Plants from interdune meadow produce primarily dumbbell phytoliths, as well as small cross and Cyperaceae-type phytoliths. These results provide a basis for the interpretation of fossil phytolith assemblages and the reconstruction of coastal environmental changes. 2003 Elsevier Ltd. All rights reserved.
Keywords: phytoliths; silica bodies; grasses; microfossils; coastal environments; Quaternary; southeastern USA

1. Introduction Phytoliths are microscopic silica bodies that precipitate in or between cells of living plant tissues. They occur in many plant families (Pearsall, 2000; Piperno, 1988, 2001), but are especially abundant, diverse, and distinctive in the grass family (Gramineae) (Blackman, 1971; Brown, 1984; Cliord & Watson, 1977; Grob, 1896; Piperno & Pearsall, 1998; Prat, 1936; Twiss, 2001). Many taxa in Gramineae are characterized by phytoliths with specic morphological characteristics, hence their taxonomic signicance. Phytoliths are released from plant tissues when they are decayed, burned, or digested. Released phytoliths thus become microfossils of the plants that produce them.

* Corresponding author. E-mail address: kliu1@lsu.edu (Kam-biu Liu). 0272-7714/03/$ - see front matter 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0272-7714(03)00137-9

Phytolith morphology and taxonomy, as well as the application of phytolith analysis to archaeological and paleoenvironmental research, have been the subject of many studies (Bowdery, Hart, Lentfer, & Wallis, 2001; Horrocks, Deng, Ogden, & Sutton, 2000; Kondo, Childs, & Atkinson, 1994; Lu et al., 1996; Madella, 1997; Meunier & Colin, 2001; Mulholland & Rapp, 1992; Pearsall & Piperno, 1993; Piperno, 1988; Rosen, 1992; Rovner, 1988; Wang & Lu, 1993). However, until recently very little attention had been paid to the use of phytoliths in the study of coastal environmental changes (Fearn, 1998; Horrocks et al., 2000). In this study, we conducted a pioneer investigation of phytoliths in modern grasses growing in the coastal environments of southeastern USA (Georgia, Florida, and Louisiana). The coastal zones of the southeastern USA consist of a variety of ecological habitats and vegetation types. Chief among them are sand dunes and interdune

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meadows, maritime or upland forests, swamps, fresh marshes, brackish marshes, and salt marshes (Bertness, 1999). These coastal environments pose special challenges to Quaternary paleoenvironmental reconstruction using conventional paleoecological techniques such as pollen analysis (e.g. Clark, 1986; Clark, Overpeck, Webb, & Patterson, 1986; Clark & Patterson, 1985; Davis, 1992). One of the constraints in the application of pollen analysis is that some key coastal environments, particularly salt and fresh/brackish marshes and to some extent sand dunes, are dominated by grasses, but, except for Zeas mays (maize), Gramineae pollen cannot be identied below the family level (Fearn & Liu, 1997). Here we demonstrate that this constraint can be overcome by phytolith analysis, because characteristic grasses of dierent coastal environments produce dierent phytolith assemblages.

2. Phytolith classication At present, the classication of phytoliths is principally based on the study of some modern Gramineae, Xylophyta, and a few other plants. Dierent researchers have suggested dierent terms and classication schemes because of the dierences in materials, classication criteria, and study areas. So far, no uniform and convenient classication scheme has been widely adopted for various conditions. Nevertheless, many important investigations have made a great contribution to phytolith classication. Taking Gramineae phytoliths as an example, Prat (1936) divided the Panicoideae subfamily into two groups by studying the shapes of short cells in the leaf veins of some genera of Gramineae. Twiss, Suess, and Smith (1969) classied Gramineae phytoliths into four groups after they summarized the achievements of Prat (1936) and other researchers. Brown (1984) classied Gramineae phytoliths into eight categories including more than 130 types after studying the phytoliths from dierent parts of 112 taxa of Gramineae plants. Piperno (1988) presented an index table of two dierent kinds of phytoliths. Mulholland and Rapp (1992) proposed one morphological classication of grass silica bodies after summarizing dierent researchers classications for the Gramineae family. Piperno and Pearsall (1998) summarized the distribution of short-cell phytoliths from the grasses, which were described as circular to oval-(rondels), saddle-, bilobate-, or cross-shaped, and well-established diagnostic features of the leaf epidermis. The above classication of phytoliths was mainly proposed by European and American botanists. Japanese researchers such as Sase and Kondo (1974) developed a morphological classication, which added the following three classes: fan-shape, point-shape, and

bambusoid. Kondo et al. (1994) classied Gramineae phytoliths into nine classes based on a modied classication of Kondo and Sase (1986). In China, Wang and Lu (1993) classied grass phytoliths into 15 classes. Table 1 attempts to compare and reconcile the main classications of grass phytoliths proposed by various researchers. The dumbbell (lobate) phytolith originates from the epidermal cells (shortcells) of Panicoideae and Oryzoideae, some Arundinoideae, and Chloridoideae subfamilies (Brown, 1984; Fearn, 1998; Lu & Liu, 2003; Mulholland, 1989). Table 1 shows that dierent researchers mostly subdivided the dumbbell into three groups: 1, dumbbell or bilobate, lobate; 2, complex dumbbell or multilobed, polylobates; and 3, cross. The Chloridoid class (Twiss et al., 1969) consists of only two types of saddle-shaped bodies; one is the Chloridoid type (Table 1), which originates from epidermal cells (short cells) of Chloridoideae, and some Bambusoideae and Arundinoideae subfamilies. They have the form of short saddles (short seat) with nonwrinkly surface, and have been described elsewhere as battle-axes with a double edge (Kondo et al., 1994; Prat, 1936). This type was referred to as the short saddle type, short plateau saddle type, or Chloridoid class by Wang and Lu (1993), Piperno and Pearsall (1998), and Kondo et al. (1994), respectively. Another is the thin Chloridoid type, which is saddle shaped, similar to Chloridoid type, but longer. They may have a wrinkly and/or a non-wrinkly surface. This type was called the long saddle type, tall collapsed saddle type, or Bambusid class by Wang and Lu (1993), Piperno and Pearsall (1998), and Kondo et al. (1994), respectively. Pearsall (1989) and Pearsall and Trimble (1983, 1984) found six commonly occurring phytolith types, then referred to as horned towers, at towers regular spools, irregular spool, angular, and half rotated. Kondo et al. (1994) developed both Chionochloid class and phytoliths from other short-cells class based on these shapes. It is dicult to relate these types to grass taxonomy and to infer moisture and temperature conditions from their occurrence (Pearsall, 1989, 2000). The Festucoid class (Twiss et al., 1969) contains several geometrical types that are circular, rectangular, elliptical, or oblong. Kondo et al. (1994) and Pearsall (1989) used the same term of Festucoid class to dene the short-cell phytolith types as originating from the epidermal cells of the Pooideae subfamily. They also used dierent geometrical termsboat-shape, hatshape, rectangular, and round/oblongto describe Twiss (1969) circular, rectangular, elliptical, and oblong types. Current groupings within the Festucoid class include two major geometrical types. One is trapezoids (Brown, 1984), which correspond to wavy trapezoid (Piperno & Pearsall, 1998), rectangular (Mulholland & Rapp, 1992; Pearsall, 1989), boat-shaped (Kondo et al.,

Table 1 Comparison of dierent grass phytolith classication systems Lu et al., 1996 and Wang and Lu, 1993 Dumbbell Piperno and Pearsall, 1998 (short cell) Bilobate Pearsall, 1989 and Pearsall and Trimble, 1983 Panicoid shapes (dumbbell, angular, nodular, cross, crenate, half dumbbell) Sase and Kondo, 1974 Panicoid Kondo et al., 1994 Panicoid class Mulholland and Rapp, 1992 (short cell) Dumbbell

Twiss et al., 1969 Panicoid class (dumbbell)

Brown, 1984 VI Bilobates

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Multilobed short cell Cross Long saddle Tall saddle/long saddle

(Complex dumbbell) (Cross) Chioridoid class (thin Chloridoid)

VII Polylobates? VIII Crosses IV Saddles Chloridoid shapes (saddles) Chloridoid Bambusid class

(Complex regular bilobate?) Cross Saddle: two concave edges Saddle: one concave edge Saddle: no concave edges

Collapsed saddle Narrow-elliptate Short saddle Short saddle Plateau saddle Conical? Bilobate/saddle conical irregular short cell Wavy trapezoid (Chloridoid) Horned towers, at towers, regular spools Half rotated, angular, irregular spool Festucoid shapes (square/rectangular) Chloridoid class Chionochloid class Phytolith from other short cell Festucoid class (boat-shaped)

Triangle? Pentagon? Sinuate: polyloate bilobate? Rectangle Rondel (entire, at, indented)

Multiple tooth

Festucoid class (circular rectangular elliptical oblong)

V Trapezoids

Pooid (Festuoid)

Weakly tooth Hat Fan type with raised ridge Fan type without raised ridge Square Rectangle Plate-like bar Point (joint) bar Smooth-bar Long-point Short-point

Rondel (circular to oval)

III Double outlines I Plates (IB)

(Round/oblong) Bulliform cells Fan-shaped

(Hat/cone-shaped) Fan-shaped class

Elongate class

I Plates (IA)

Long cells

Elongate

Elongate class

II Trichomes

Trichomes

Point-shaped

Point-shaped class

589

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1994), and tooth-shaped (Wang & Lu, 1993). Another is double outlines (Brown, 1984), which correspond to rondel (Mulholland & Rapp, 1992; Pearsall, 1989; Piperno & Pearsall, 1998) and hat/cone-shaped phytoliths (Kondo et al., 1994; Wang & Lu, 1993). Biogenic silica can also deposit in bulliform (motor) cells, prickle hairs (Trichomes), long cells, stomata, and vascular tissues of grass epidermis. They can also form in subepidermal cells, forming easily recognizable bodies. The phytolith shapes from bulliform cells, prickle hairs, long cells, and non-short cells of leaves have been described as fan, elongate, point, square, and plates by Twiss et al. (1969), Kondo et al. (1994), Wang and Lu (1993), and Brown (1984). These forms do not possess any subfamily or tribal characteristics, but have secondary features allowing further subdivision (Wang & Lu, 1993). As for non-Gramineae plants, Kondo and Pearson (1981) and Kondo and Sumda (1978) classied phytoliths of gymnosperm and monocotyledonous angiosperm trees into six groups, and those of dicotyledonous angiosperm trees into eight groups based on studies of a wide range of native and exotic trees in Japan. A great diversity of phytoliths shapes from dicotyledon species has been described by Bozarth (1992), Geis (1973), Piperno (1988), and Runge (1999). Ollendorf (1992) proposed a classication scheme for sedge (Cyperaceae) phytoliths. While all these various classication systems have advanced the young science of phytolith study, signicant shortcomings and discrepancies remain. Some classication systems are only suitable for detailed study of modern plants. Some other classication schemes are only applicable to regional oras. Phytoliths produced in grass epidermis can be divided into two broad morphological classesbodies in long cells and bodies in short cells (Metcalf, 1960). Long-cell silica bodies are variable in shape but tend to be elongate with sinuous, often interlocking borders. But like their bulliform or prickle hair counterparts, the elongate phytoliths also do not posses any subfamily or tribal characteristics. By contrast, short-cell phytoliths can be generally classied into distinctive grass subfamilies (Piperno & Pearsall, 1998; Twiss et al., 1969). Although the previously published grass short-cell phytolith classication schemes have much in common, signicant dierences in terminology and in emphasis on specic morphological characteristics remain. In this study, we use a descriptive name to describe each morpho-type. Each short-cell phytolith has been classied into one of 11 basic morpho-types based on Pearsall (1989), Piperno and Pearsall (1998), and this study. The 11 morpho-types are dumbbell, cross, long saddle, short saddle, plateau saddle, rondel, at tower, two-horned tower, spool/horned tower, rondel/saddle ellipsoid, and wavy trapezoid (Fig. 1).

3. Materials and methods 3.1. Samples of modern plants for analysis of phytoliths Sixty species of modern plants (including 34 species of grasses) were collected for phytolith analysis from the Atlantic and Gulf of Mexico coasts of the southeastern USA in the summers of 1999 and 2000. The principal sampling sites are Cumberland Island in southern Georgia and the Gulf coastal regions of northwestern Florida and Louisiana. The samples were collected from a variety of coastal or near-coastal environments, such as salt marshes, pine/oak forests, maritime hardwood forests, freshwater and brackish marshes, and sand dunes (Table 2). Each plant sample includes leaves, culms, inorescences, and roots. Twenty-ve grass genera representing all six subfamilies (Pooideae, Panicoideae, Chloridoideae, Bambusoideae, Oryzoideae, and Arundinoideae, see Gould & Shaw, 1983) were included in the samples. Twenty-ve of the 34 grass species included in this study belong to two subfamilies, Panicoideae and Chloridoideae. Grasses in Panicoideae are distributed widely in humid tropical or subtropical areas (Gould & Shaw, 1983). The most suitable growing condition for grasses of this subfamily is in the southeastern USA, while the poorest is in the northwest (Gould & Shaw, 1983). Although temperature is a primary limiting factor, a few species are adapted to dry conditions, and moisture supply becomes an important secondary limiting factor. The Chloridoideae is widely distributed over the North American continent, but its frequency is highest in the southwestern USA and northern Mexico (Gould & Shaw, 1983). There, under a warm and dry climate, over 50% of the grass species are Chloridoid. Although in this study we have not collected all the grass species occurring in the coastal ora, we focused on the typical or common grasses of the key coastal environments in the southeastern USA. For example, our samples include Uniola paniculata and Aristida desmantha of the sand dunes, Spartina alterniora of the salt marshes, Spartina patens of the brackish marshes, Arundinaria longifolia of the maritime forest edges, and Phragmites australis of the fresh marshes (Bertness, 1999; Gosselink, 1984; Wiegert & Freeman, 1990).

3.2. Methods of extracting phytoliths from modern plants All the collected plant samples were cleaned with distilled water in an ultrasonic water bath to remove adhering particles. Leaves and culms of each species were placed in 20 ml of saturated nitric acid for one night to oxidize organic materials completely. The solutions were centrifuged at 2000 rpm for 10 min,

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Fig. 1. Hand drawings of principal morpho-types of short-cell phytoliths found in the 34 species of coastal grasses from the southeastern USA.

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Table 2 List of 34 modern grasses from the US Atlantic and Gulf coasts used for the phytolith analysisa No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 Name Andropogon glomeratus (Walt.) BSP Andropogon ternaries Michx. Anthaenatia rufa (Nutt.) Schult. Aristida desmantha Trin. and Rupr. Arundinaria longifolia E. Fourn Arundinaria gigantea (Walt.) Muhl. Avena sativa L. Cenchrus incertus M. Curtis Chasmanthium laxum (L.) Yates. Chasmanthium ornithorhynchum (Steud.) Yates Ctenium aromaticum (Walter) A.W. Wood Dactyloctenium aegyptium (L.) Willd. Distichlis spicata (L.) Greene Eragrostis oxylepis (Torr.) Torr. Eragrostis cilianensis (All.) Vignolo-Lutati Erianthus strictus Spreng. Eustachys petraea (Sw.) Desv. Leersia oryzoides (L.) Sw. Panicum amarum Elliott Panicum dichotomiforom Michx. Panicum hemitomon Schult. Panicum verrucosum Muhl. Panicum virgatum L. Subfamily (Gould & Shaw, 1983) Panicoideae Panicoideae Panicoideae Chloridoideae Bambusoideae Bambusoideae Pooideae Panicoideae Arundinoideae Arundinoideae Chloridoideae Chloridoideae Chloridoideae Chloridoideae Chloridoideae Panicoideae Chloridoideae Oryzoideae Panicoideae Panicoideae Panicoideae Panicoideae Panicoideae Ecology or distribution of plants (Allen, 1992; Gould & Shaw, 1983) Generally on wet sites Edge of pine forest Pine forest Sandy soil along coast Edge of forest Pine forest or edge of atwoods Disturbed areas Dry sand Edge of forest Moist area Edge of forest, interdune meadow Southeast and west USA Saline areas in coastal marshes and islands, sandy beaches Sandy soil along the coast Sandy soil along the coast Edge of pine forest and disturbed areas Sandy soil along the coast Wet roadside ditches and edges of lakes, streams, and other wet areas Sandy soil along coast, interdune meadow Disturbed areas, especially in moist regions, throughout USA Coastal marshes, wet areas and in the inland part of coastal sites, interdune meadow Disturbed areas and edges of forests, mostly in pine regions Edges of pine forests and remnant strips in prairie regions; cheniers and spoil banks in coastal freshwater marshes Fresh to brackish water marshes Disturbed areas throughout USA Cultivated in tropical regions of the world ? Edge of forest and disturbed areas in pine and prairie regions Widespread throughout the world Salt marshes and sandy areas on coast Brackish to saline areas in coastal marshes Sandy soil along the coast Sandy soil along the coast Edges of lakes, streams, wet roadside ditches

24 25 26 27 28 29 30 31 32 33 34
a

Phragmites australis (Cav.) Trin. Ex Steud. Poa annua L. Saccharum ocinarum L. Setaria sp. Sorgastrum nutans (L.) Nash Sorghum halepense (L.) Pers. Spartina alterniora Loisel Spartina patens (Ait.) Muhl. Sporobolus virginicus (L.) Kunth. Uniola paniculata L. Zizaniopsis miliacea (Michx.) Doell and Aschers.

Arundinoideae Pooideae Panicoideae Panicoideae Panicoideae Panicoideae Chloridoideae Chloridoideae Chloridoideae Chloridoideae Oryzoideae

All plant samples are preserved in the Department of Geography and Anthropology, Louisiana State University, Baton Rouge, LA 70803, USA.

decanted, and rinsed twice with distilled water. They were then rinsed with 95% ethanol until the supernatant was 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 (glycerol) medium for counting and line drawing. A minimum of 350 phytolith grains were counted in each sample. Light photomicrography at 400 magnication was used to record typical types of phytoliths found in plant tissues. A multitude of phytolith types were isolated from the grass samples analyzed. A few of them have not been reported previously in the phytolith literature.

4. Results and discussion 4.1. Distribution of short-cell phytolith types observed in coastal grasses Eleven morpho-types of short-cell phytoliths were found among the 34 grass species included in this study (Fig. 1 and Table 3). The dierent morpho-types of selected common coastal grasses are illustrated or photomicrographed in Plates 13. Our photomicrographic and hand-drawn illustrative key herein is designed to aid the identication of phytoliths commonly found in Quaternary or archaeological deposits.

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Lobate phytoliths, including the dumbbell and cross types according to the traditional nomenclature, have been identied consistently as distinctive silica bodies (Lu & Liu, 2003). Dumbbells are characterized by having two somewhat rounded lobes connected by a shaft. Some (complex types) have one or two additional lobes on the shaft. Crosses are shorter, nearly equidimensional bodies with four distinct lobes. All specimens of plants from Panicoideae (Fig. 1 and Plate 1A, D) and Oryzoideae (Plate 1B) grasses in this study have typical dumbbell type. The crosses are mostly associated with the Panicoideae subfamily. Despite
Table 3 Distribution of short cell phytolith types observed in coastal grasses Taxon Panicoideae Andropogon glomeratus Andropogon ternaries Anthaenatia rufa Cenchrus incertus Erianthus strictus Panicum amarum Panicum dichotomiorum Panicum hemitomon Panicum verrucosum Panicum virgatum Saccharum ocinarum Setaria sp. Sorgastrum nutans Sorghum halepense Chloridoideae Aristida desmantha Ctenium aromaticum Dactyloctenium aegyptium Distichlis spicata Eragrostis oxylepis Eragrostis cilianensis Eustachys petraea Spartina alterniora Spartina patens Sporobolus virginicus Uniola paniculate Bambusoideae Arundinaria longifolia Arundinaria gigantean Pooideae Avena sativa Poa annua Arundinoideae Chasmanthium laxum Chasmanthium ornithorhynchum Phragmites australis Oryzoideae Leersia oryzoides Zizaniopsis miliacea A A C R R A A A*

being the most characteristic markers of the Panicoideae (Twiss et al., 1969), dumbbell and cross phytoliths are also found to be present in the Chloridoideae (Aristida desmantha and Ctenium aromaticum) and Arundinoideae (Chasmanthium laxum and Chasmanthium ornithorhynchum) subfamilies in this study (Table 3). The term dumbbell was rst used by Metcalf (1960) as a morphological term for the shape of some intercostal short-cell phytoliths. It has gradually become a name given to a loosely dened group of phytoliths characterized by having two lobes joined by a shank. However, many subsequent researchers, including Brown

Long Short Plateau Flat Two-horned Spool/horned Rondel/saddle Wavy Dumbbell Cross saddle saddle saddle Rondel tower tower tower ellipsoid trapezoid A* A* A* A* A* A* A* A* A* A* A* A* A* A* R? A? A* R A* A* A* R* R R C R R R R A

C C* R* R C C* C* R R R C R* A* A C C

C C R R C R R R C R C R R R* C* C R A

A A C R

A R

A* A*

R R

R R R R C R C

A* A*

A, abundant; C, common; R, rare; * diagnostic forms present, characteristic of taxons subfamily.

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Plate 1. Illustrations of long-cell and short-cell phytolith morpho-types in four common coastal grass species: A, Panicum verrucosum (mostly dumbbells); B, Leersia oryzoides (mostly dumbbells, some at towers); C, Aristida desmantha (mostly tower-shaped phytoliths, some dumbbells); D, Panicum hemitomon (mostly dumbbells). One scale 10 lm.

(1984), Fredlund and Tieszen (1994, 1997), and Piperno and Pearsall (1998) have avoided using this term and favored the alternative term bilobate. Recently Lu and Liu (2003) documented the variability of 25 diagnostic dumbbell (lobate) phytolith shapes occurring among 85 modern grass species collected from a variety of environments in China and the southeastern USA.

The short saddle morpho-type is produced in a high proportion by the Chloridoideae. The descriptive term, battle-axes with double edges (Prat, 1936), refers to the outline of the base when the body is oriented in top view. Saddle-shaped phytoliths are the dominant class of the Chloridoideae subfamily (Fig. 1 and Plate 3C). They are also common in two species of the Bambusoideae

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595

Plate 2. Illustrations and photomicrographs of dierent phytolith morpho-types in three common coastal grass species: A, Spartina alterniora (mostly rondel/saddle ellipsoid phytoliths); B, Uniola paniculata (mostly at towers, some two-horned towers and spool/horned towers); and C, Spartina patens (mostly spool/horned towers).

(Arundinaria longifolia, Arundinaria gigantea), and are present in Phragmites australis (Arundinoideae) as well (Table 3). A great quantity of rondel/saddle ellipsoid morphotypes are isolated from Spartina alterniora (Chloridoideae) (Fig. 1 and Plate 2A), with both round and saddle tendencies. Spartina alterniora (cordgrass) is a tall, sti-stemmed grass typically growing in salt marshes. On the other hand, the spool/horned tower type (Fig. 1

and Plate 2C) is produced primarily in brackish marsh grasses, such as Spartina patens (salt-meadow hay) and Distichlis spicata. This type is equal to the Chionochloid class of Kondo et al. (1994) and the regular spools of Pearsall (1989). A great number of phytoliths called plateau saddles are isolated from the leaves of Phragmites (Plate 3D). More study is needed before they can be assigned genusspecic status, but they can be used as a marker of the

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Plate 3. Photomicrographs of principal phytolith morpho-types in four common coastal grass species: A, Arundinaria longifolia (mostly long saddles); B, Avena sativa (mostly wavy trapezoid); C, Dactyloctenium aegyptium (mostly short saddles); and D, Phragmites australis (mostly plateau saddles) (bar unit in this plate is lm).

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Arundinoideae and to determine the possible presence of Phragmites in soil phytolith assemblages. Kondo and Sase (1986) distinguished the saddle from Phragmites as middle saddle, which is shorter than the long saddle from Bambusoideae and longer than the short saddle from Chloridoideae. Bambusoideae contributes a large number of diagnostic types at the family level, particularly the long saddle phytoliths with a wrinkly and/or non-wrinkly surface (Plate 3A). The length of saddle from Bambusoideae is longer than that from Chloridoideae. Rondels (circular to oval phytoliths) and wavy trapezoids (Mulholland, 1989) are most closely associated with Pooideae. Wavy trapezoid (Plate 3B), in particular, appears to be unique to Pooideae. The rondels are also found in the Chloridoideae (Table 3). Some types of phytoliths from coastal grasses do not lend themselves to easy description. For example, at towers, two-horned towers, and spool/horned towers (Fig. 1 and Plate 2B, C) are typically small, irregular phytoliths. Although some researchers avoided using these descriptive terms (at towers, two-horned towers, and spool/horned towers), no uniform or standard terminology has been adopted in the literature. These phytoliths warrant further investigation, as some of them are likely to be of precise taxonomic value. They have been isolated in great numbers from the Chloridoideae. In particular, at towers are produced in high proportions (>90%) by Uniola paniculata (sea oats) (Plate 2B), a C4 grass typically occurring in primary dunes or other sandy substrates along the coast. The sinuate elongate, smooth elongate, point, fanshaped, square, and rectangle morpho-types (Plate 1A, D) are derived from epidermic long cells, trichome cells, and bulliform cells of grasses. They have no taxonomic signicance in our classication. Non-Gramineae families from coastal environments can also produce typical phytolith morpho-types. For example, the cone-shaped morpho-type is attributed to the Cyperaceae (sedge) family, and the circular crenate to Sabal minor (saw palmetto). Even though this study has not described all the short cell phytoliths occurring in the coastal ora, our samples include grasses that are common or diagnostic of most of the ecologically important coastal environments in the southeastern USA. More studies are needed that would include additional species in the larger genera of the Gramineae, as well as in other non-Gramineae taxa. 4.2. Typical assemblages of grass phytoliths in coastal environments Grasses occur in nearly all habitats throughout the coastal environments of the southeastern USA (Bertness, 1999; Gosselink, 1984; Wiegert & Freeman, 1990). Vegetation in the coastal zone is strongly aected by

various environmental gradients. Perhaps the most important factors are topography and salinity. Some of the drier habitats on the coast include beach ridges and sand dunes, where Uniola paniculata (sea oats), Sporobolus virginicus (marshgrass, crabgrass), Aristida desmantha (curly threeawn), Distichlis spicata (saltgrass), and Eragrostis cilianensis (stinkgrass) occur. The coastal marsh is characterized by large populations of relatively few species. Spartina alterniora (cordgrass) is the dominant plant in salt marshes. Brackish marshes, developed extensively in estuaries and deltas, and on the peripheries of bays and lagoons, are often dominated by Spartina patens (salt-meadow hay). Other common grass species in brackish marshes include D. spicata, Leersia oryzoides, and Panicum hemitomon. Fresh marshes are dominated by Panicum virgatum, P. hemitomon, and Phragmites australis. Swamps occupy the area between upland forests and coastal marshes. In these wetland forests common trees include Taxodium distichum, Salix nigra, Sabal minor, Nyssa aquatica, and Quercus spp. Some grass species commonly found in the swamps are Panicum spp., Eragrostis spp., and Zizaniopsis miliacea. Phytolith analysis of the grasses from dierent coastal vegetation communities shows signicant variation in shapes and assemblages (Fig. 2). Rondel/saddle ellipsoid phytoliths are mainly produced by Spartina alterniora, the most common plant in the salt marshes. Thus the predominance of rondel/saddle ellipsoid phytoliths in a sediment sample may be a good indicator of salt marsh environment. Rondel and spool/horned tower phytoliths are common in grasses from brackish marshes, such as Spartina patens. Flat towers, twohorned towers, and short saddle-shaped phytoliths dominate the grass samples from sand dunes, especially Uniola paniculata. Plateau saddle and dumbbell phytoliths are common in the grass samples from fresh marshes, such as Phragmites australis. The grass samples from coastal swamps produce many dumbbell phytoliths. The long saddle phytoliths are exclusively derived from Bambusoideae such as Arundinaria spp., which commonly occurs on the edge of upland forests or maritime forests. They are distinctly larger than the plateau saddle phytoliths typically found in Phragmites. Trees from maritime forests also produce typical phytolith shapes such as the circular crenate type from palms (Pearsall, 1989, 2000), and tracheid, polyhedron shape from other broad-leaved hardwood trees (Kondo et al., 1994). Although our study is based on the phytolith contents of grass plants, the conclusions are supported by the results of phytolith analysis of soil samples collected from the corresponding coastal environments. In the 50 surface soil samples collected for phytolith analysis from dierent environments along the Atlantic and Gulf coasts of the southeastern USA (Lu & Liu, 2001), we found that the modern phytolith composition

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Fig. 2. An idealized transect of coastal environments in the southeastern USA showing major vegetation zones and their representative phytolith assemblages. The width of a black bar indicates relative abundance of each phytolith type.

in the primary dunes is well characterized by a high amount of two-horned towers (30 25%), at towers (13 7%), and short saddle (9 6%) phytoliths. The phytolith composition from the surface samples in interdune meadow shows very high values of dumbbell phytoliths (47 13%). Both the Palmae (circular crenate) morpho-types and other broad-leaved types account for more than 6080% of all phytoliths, and grass phytoliths account for less than 20% in the modern soils under maritime forests (Lu & Liu, 2001). Our study demonstrates the high potential of phytolith analysis as a tool for identifying vegetation in coastal environments. Each of the key coastal environments yielded abundant and distinctive phytolith assemblages.

5. Conclusions Phytolith analysis of modern grasses from various coastal environments including salt marshes, brackish marshes, freshwater marshes, pine/oak forests, maritime hardwood forests, and sand dunes in the southeastern USA has revealed a large diversity of phytolith shapes. The dominant grasses from coastal sand dunes, such as

Uniola paniculata, and Eragrostis spp., produce primarily at towers and two-horned towers, as well as small short saddle and dumbbell-shaped phytoliths. The grasses and sedges from interdune meadows, such as Panicum spp., Cenchrus incertus, and Cyperaceae, produce primarily dumbbell, small cross, and Cyperaceae phytoliths. The Pooideae and Bambusoideae subfamilies of grasses, which are generally common along the edges or on the understory of maritime forests, produce wavy trapezoid and long saddle phytolith, respectively. The dominant grasses of swamps produce primarily dumbbell and plateau saddle phytoliths. Rondel/saddle ellipsoid phytoliths are almost exclusively produced by Spartina alterniora, the dominant plant in salt marshes. Thus the predominance of rondel/saddle ellipsoid phytoliths in a sediment sample may be a good indicator of salt marsh environment. Rondel and spool/horned tower phytolith are common in grasses from brackish marshes. This study provides a basis for the interpretation of fossil grass phytolith assemblages recovered from coastal sediments for the reconstruction of coastal environmental changes. Some coastal environments, such as salt marshes and brackish marshes, may not be easily distinguishable based on their pollen assemblages

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(e.g. see Chmura, 1994; Clark, 1986; Clark & Patterson, 1985; Fearn, 1998). Other environments, such as sand dunes, are palynologically unidentiable because pollen is absent or rare due to poor preservation. Our investigation demonstrates that these key coastal environments (salt marshes, brackish marshes, and sand dunes) produce distinctive phytolith assemblages that can be used as a supplementary tool in coastal paleoenvironmental reconstructions (Lu & Liu, 2001). Acknowledgements We thank X.Y. Zhou and Carl A. Reese for providing modern grass reference samples and for helpful discussion. This work was supported by grants from Risk Prediction Initiative (RPI) of the Bermuda Biological Station for Research (RPI-00-1002), and by the US National Science Foundation (SES-8922033, SES-9122058, and BCS-0213884), and NSFC (40024202, 40271117). References
Allen, C. M. (1992). Grasses of Louisiana (320 pp.). Eunice: Cajun Prairie Habitat Preservation Society. Bertness, M. D. (1999). The ecology of Atlantic shorelines (417 pp.). Sunderland: Sinauer Associates. Blackman, E. (1971). Opaline silica in the Range Grasses of southern Alberta. Canadian Journal of Botany 49, 769781. Bowdery, D., Hart, D. M., Lentfer, C., & Wallis, L. (2001). A universal phytolith key. In J. D. Meunier, & F. Colin (Eds.), Phytoliths: Applications in earth sciences and human history (pp. 267278). Amsterdam: Balkema. Bozarth, S. R. (1992). Classication of opal phytoliths formed in selected dicotyledons native to the Great Plains. In G. Rapp, Jr., & S. C. Mulholland (Eds.), Phytolith systematics: Advances in archaeological and museum science (pp. 193214). New York: Plenum Press. Brown, D. A. (1984). Prospects and limits of a phytolith key for grasses in the central United States. Journal of Archaeological Sciences 11, 345368. Chmura, G. L. (1994). Palynomorph distribution in marsh environments in the modern Mississippi Delta plain. Geological Society of American Bulletin 106, 705714. Clark, J. S. (1986). Dynamism in the barrier-beach vegetation of Great South Beach, New York. Ecological Monographs 56, 97126. Clark, J. S., Overpeck, J. T., Webb, T., III., & Patterson, W. A. (1986). Pollen stratigraphic correlation and dating of barrier beach peat sections. Review of Palaeobotany and Palynology 47, 145168. Clark, J. S., & Patterson, W. A., III. (1985). The development of a tidal marsh: upland and oceanic inuences. Ecological Monographs 55, 189217. Cliord, H. T., & Watson, L. (1977). Identifying grasses: Data, methods and illustrations (146 pp.). St. Lucia: University of Queensland Press. Davis, O. K. (1992). Rapid climatic change in coastal southern California inferred from pollen analysis of San Joaquin Marsh. The Quaternary Research 37, 89100. Fearn, M. L. (1998). Phytolith in sediment as indicators of grass pollen source. Review of Palaeobotany and Palynology 103, 7581. Fearn, M. L., & Liu, K. B. (1997). Identication of maize pollen: reply to Eubanks. American Antiquity 62, 146148.

Fredlund, G. G., & Tieszen, L. L. (1994). Modern phytolith assemblages from the North American Great Plains. Journal of Biogeography 21, 321335. Fredlund, G. G., & Tieszen, L. L. (1997). Calibrating grass phytolith assemblages in climatic terms: application to late Pleistocene assemblages from Kansas and Nebraska. Palaeogeography Palaeoclimatology, Palaeoecology 136, 199211. Geis, J. W. (1973). Biogenic silica in selected species of deciduous angiosperms. Soil Science 116, 113130. Gosselink, J. G. (1984). The ecology of delta marshes of coastal Louisiana: A community prole (FWS/OBS-84/09, 134 pp.). Washington, DC: US Fish and Wildlife Service, Division of Biological Services. Gould, F. W., & Shaw, R. B. (1983). Grass systematics (416 pp.). College Station: A and M University Press. Grob, A. (1896). Beitrage Sur Anatomie der Epidermis der Gramineenblatter. Bibliotheca Botanica 36. Horrocks, M., Deng, Y., Ogden, J., & Sutton, D. (2000). A reconstruction of the history of a Holocene sand dune on Great Barrier Island, Northern New Zealand, using pollen and phytolith analyses. Journal of Biogeography 27, 12691277. Kondo, R., Childs, C., & Atkinson, I. (1994). Opal phytoliths of New Zealand (85 pp.). Canterbury: Manaaki Whenua Press. Kondo, R., & Pearson, T. (1981). Opal phytoliths in tree leaves (part 2): opal phytoliths in dicotyledonous angiosperm trees. Research Bulletin of Obihiro University 12, 217230 (in Japanese). Kondo, R., & Sase, T. (1986). Opal phytoliths, their nature and application. The Quaternary Research 25, 3163 (in Japanese with English summary). Kondo, R., & Sumda, T. (1978). Opal phytoliths in tree leaves (part 1): opal phytoliths in gymnosperm and monocotyledonous angiosperm tree. Soil Science and Plant Nutrition 49, 138144 (in Japanese). Lu, H. Y., & Liu, K. B. (2001). Phytolith indicators of hurricane overwash and coastal environmental changes. Abstract of the 97th Annual Meeting of the Association of American Geographers, New York. Lu, H. Y., & Liu, K. B. (2003). Morphological variations of lobate phytoliths from grasses in China and the southeastern USA. Diversity and Distributions 9(1), 7387. Lu, H. Y., Wu, N. Q., Liu, D. S., Han, J. M., Qin, X. G., Sun, X. J., & Wang, Y. J. (1996). Seasonal climatic variation recorded by phytolith assemblages from the Baoji loess sequence in central China over the last 150 000 a. Science in China (Series D) 39, 629 639. Madella, M. (1997). Phytoliths from a Central Asia loess-paleosol sequence and modern soils: their taphonomical and palaeoecological implication. In A. Pinilla (Ed.), The state of the art of phytoliths in plants and soils (pp. 4958). Madrid: Monograas del Centro de Ciencias Medambioentales. Metcalf, C. R. (1960). Anatomy of the monocotyledons: I. Gramineae (731 pp.). London: Oxford University Press. Meunier, J. D., & Colin, F. (2001). Phytoliths: Applications in earth sciences and human history (378 pp.). Amsterdam: Balkema. Mulholland, S. C. (1989). Phytolith shape frequencies in North Dakota grasses: a comparison to general patterns. Journal of Archaeological Sciences 16, 489511. Mulholland, S. C., & Rapp, G., Jr. (1992). A morphological classication of grass silica-bodies. In G. Rapp, Jr., & S. C. Mulholland (Eds.), Phytolith systematics: Advances in archaeological and museum science (pp. 6589). New York: Plenum Press. Ollendorf, A. L. (1992). Toward a classication scheme of sedge (Cyperaceae) phytolith. In G. Rapp, Jr., & S. C. Mulholland (Eds.), Phytolith systematics: Advances in archaeological and museum science (pp. 91111). New York: Plenum Press. Pearsall, D. M. (1989). Paleoethnobotany: A handbook of procedures (470 pp.). San Diego: Academic Press. Pearsall, D. M. (2000). Paleoethnobotany: A handbook of procedures (2nd ed., 700 pp.). San Diego: Academic Press.

600

H. Lu, K.B. Liu / Estuarine, Coastal and Shelf Science 58 (2003) 587600 Rosen, A. M. (1992). Preliminary identication of silica skeletons from Near Eastern archaeological sites: an anatomical approach. In G. Rapp, Jr., & S. C. Mulholland (Eds.), Phytolith systematics: Advances in archaeological and museum science (pp. 129147). New York: Plenum Press. Rovner, I. (1988). Macro- and micro-ecological reconstruction using plant opal phytolith data from archaeological sediments. Geoarchaeology 3, 155163. Runge, F. (1999). The opal phytolith inventory of soils in central Africaquantities, shapes, classication, and spectra. Review of Palaeobotany and Palynology 107, 2353. Sase, T., & Kondo, R. (1974). The study of opal phytoliths in the humus horizon of buried volcanic ash soils in Hokkaido. Research Bulletin of Obihiro University 8, 465483 (in Japanese with English summary). Twiss, P. C. (2001). A cormudgeons view of grass phytolitholog. In J. D. Meunier, & F. Colin (Eds.), Phytoliths: Applications in earth sciences and human history (pp. 725). Amsterdam: Balkema. Twiss, P. C., Suess, E., & Smith, R. M. (1969). Morphological classication of grass phytoliths. Soil Science Society of America Proceedings 33, 109115. Wang, Y. J., & Lu, H. Y. (1993). The study of phytolith and its application (in Chinese, 228 pp.). Beijing: China Ocean Press. Wiegert, R. G., & Freeman, B. J. (1990). Tidal saltmarshes of the southeastern Atlantic Coast: A community prole, Biological report 85 (7.29). Washington, DC: US Fish and Wildlife Service.

Pearsall, D. R., & Piperno, D. M. (1993). Current research in phytolith analysis: Applications in archaeology and paleoecology, MASCA research papers in science and archaeology Vol. 10. Philadelphia: The University Museum of Archaeology and Anthropology. Pearsall, D. M., & Trimble, M. K. (1983). Phytolith analysis of soil samples: report 18. In J. T. Clark, & P. V. Kirch (Eds.), Archaeological investigations of the Mudlane-Waimea-Kawaihae Road Corridor, Island of Hawaii: An interdisciplinary study of an environmental transect, Bernice P. Bishop Museum departmental report series 83-1 (pp. 472497). Pearsall, D. M., & Trimble, M. K. (1984). Identifying past agricultural activity through soil phytolith analysis: a case study from the Hawaiian Islands. Journal of Archaeological Sciences 11, 119 133. Piperno, D. R. (1988). Phytolith analysis: An archaeological and geological perspective (280 pp.). San Diego: Academic Press. Piperno, D. R. (2001). Phytoliths. In J. P. Smol, H. J. B. Birks, & W. M. Last (Eds.), Tracking environmental change using lake sediments, Terrestrial, algal, and siliceous indicators Vol. 3 (pp. 235251). Dordrecht: Kluwer Academic. Piperno, D. R., & Pearsall, D. M. (1998). The silica bodies of tropical American grasses: morphology, taxonomy, and implications for grass systematics and fossil phytolith identication. Annals of the Smithsonian Institution 85, 140. Prat, H. (1936). La systematique des Graminees. Annales des Sciences Naturelles, Botanique, Series 2 18, 165258.