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An architectural model for Eleocharis: morphology and development of Eleocharis cellulosa (Cyperaceae)¹

Department of Biological Sciences, Florida International University, Miami, Florida 33199 USA

Received for publication October 1, 2005. Accepted for publication February 22, 2006.

ABSTRACT

Species of Eleocharis are prominent in aquatic and wetland habitats and serve as models for study of physiological adaptations to aquatic environments. The genus has an unusual morphology because the major photosynthetic organ is the stem. In order to define an architectural model for the genus to understand the evolution of this morphology, we examined mature morphology and development of E. cellulosa in living and fixed material using light and scanning electron microscopy. Eleocharis cellulosa has sympodial, vertical shoots that produce the photosynthetic culms and horizontal shoots that mix monopodial and sympodial development. Each sympodial unit produces three bracts, an elongated photosynthetic internode, then a fourth bract and an inflorescence that either aborts on vegetative culms or expands on reproductive culms. On each sympodium, the first bract subtends a precocious axillary bud that reiterates the sympodial unit; the second bract subtends a bud that develops the horizontal shoot. In both horizontal and vertical shoots, the internode below the second bract is produced by both the second bract and the renewal shoot. Sympodial growth is present in seedlings. In other species of Eleocharis, the structure of the sympodial unit is conserved but morphological diversity develops from variation in horizontal shoot growth.

Key Words: branching • Cyperaceae • Eleocharis elongata • Eleocharis geniculata • Everglades • southern Florida, USA • shoot dimorphism • sympodial

The genus Eleocharis R. Br., which includes approximately 200 species that are distributed worldwide in aquatic and wetland habitats, has a highly modified morphology in which the major photosynthetic organ is an unbranched shoot or culm (Svenson, 1929 , 1932 , 1934 , 1937 , 1939 , 1947 ; Tucker, 1987 ; Smith et al., 2002 ). Species of the genus are often prominent components of wetland ecosystems and have served as models for research on physiological adaptations to aquatic environments (Sorrell and Boon, 1994 ; Sorrell et al., 1994 , 1997 ; Sorrell and Tanner, 2000 ; Ueno, 2001 , 2004 ; Busch et al., 2004 ). To understand developmental constraints and patterns of morphological evolution within the genus and to correctly interpret physiological results, we need a model for shoot architecture in the genus.

Different growth forms and both perennial and annual life cycles occur in the genus. Species are usually rooted, emergent aquatics, but some species form floating or submersed mats. The most common growth form is tufted (cespitose), but species are often rhizomatous and sometimes stoloniferous (Svenson, 1929 , 1932 , 1934 , 1937 , 1939 , 1947 ; Smith et al., 2002 ). The tufted forms produce culms that are clustered together and have short or long horizontal shoots between tufts. The rhizomatous forms often have solitary or a few clustered culms and produce elongated horizontal shoots between these culms. The culm terminates in a spikelet (Evans, 1965 ; Tucker, 1987 ; Bruhl, 1995 ). Eleocharis species spread by growth of their horizontal stems, as well as by dispersal of seeds and tubers or, in some species, by proliferation of the culm tip (Stevens and Merrill, 1980 ; Routledge, 1987 ; Smith et al., 2002 ). Tufted and rhizomatous growth forms exploit their environments and display photosynthetic surfaces differently, thus each form has a distinct ecological strategy with respect to competition and occupying space.

Tufted and rhizomatous or stoloniferous forms of Eleocharis differ in development of the horizontal branches. Rhizomatous and stoloniferous species must have a branch dimorphism, producing horizontal as well as vertical branches. The pattern of branching or branch architecture, however, has not been adequately documented for any species of Eleocharis. Some species of the genus have been described as having an unusual sympodial growth form in which the vertical stems are the distal parts of a sympodium, while the horizontal stems are formed from the fusion of an axillary bud and the proximal parts of the sympodium; after the horizontal stem becomes orthotropic, an axillary bud continues horizontal growth, forming the next sympodium (Walters, 1950 ; Mora, 1960 ). This type of growth has been described in other sedge genera but is considered rare in the family (Goetghebeur, 1985 ).

The purpose of this study was to describe shoot growth and branching patterns in E. cellulosa Torr. in order to provide a model for the architecture of a spikerush species. Eleocharis cellulosa belongs to the subgenus Limnochloa (González-Elizondo and Peterson, 1997 ; Smith et al., 2002 ); the monophyly of this subgenus has been supported by recent molecular phylogenies of the genus (Roalson and Friar, 2000 ; Yano et al., 2004 ). Eleocharis cellulosa, which occurs from the southeastern United States west to Texas and south to Nicaragua (Smith et al., 2002 ), is an important component of the Everglades ecosystem of southern Florida (Stober et al., 2001 ). It is the dominant macrophyte in a southern Florida wet prairie community called spikerush and sedge flats (Gunderson, 1994 ). We used morphological and developmental studies of both adult and seedling plants to describe the architecture and development of vertical and horizontal components of the shoot system and to establish whether growth in E. cellulosa is sympodial or monopodial. We also documented patterns of seasonal variation in horizontal and vertical shoot morphology for E. cellulosa in the Everglades wet prairie community.

Terminology
We use the following terms to designate different parts of the E. cellulosa shoot system: a culm is the upright photosynthetic shoot; a horizontal shoot is the plagiotropic portion of the shoot system; a vertical shoot is the orthotropic portion of the shoot system that has short, relatively thick internodes, bears roots and culms, and is not photosynthetic. The adult plant does not have photosynthetic leaves but produces membranous bracts on the shoots or smaller but thicker bracts on the inflorescence. In the literature on Eleocharis, bracts on the vegetative shoot have been referred to as "leaf sheaths," while those on the inflorescence have been referred to as "floral scales" or "glumes" (e.g., the treatment of Eleocharis in the Flora of North America [Smith et al., 2002 ]). The fourth bract on each shoot, however, does not fit into these categories, and the homology of these modified leaves to each other and to leaves in other members of the Cyperaceae has not been studied in detail. To avoid implying homologies, all modified leaves are referred to as bracts (B) and are numbered in the order of their production along an axis (i.e., B1, B2, B3 ...). Similarly, when referring to culms or branching units produced along a vertical shoot, these are numbered successively from older to younger (e.g., S1, S2...). The internode associated with a bract is the internode below the bract node.

MATERIALS AND METHODS

Mature shoot morphology
Eleocharis cellulosa shoot structure was investigated in plants from a natural population at the Florida International University (FIU)–Singeltary property south of Florida City, USA (25°23'47.7''N, 80°28'06.0''W). To examine variation in architecture between the wet and dry season, 30 plants were collected from the site at the end of the wet season (October 2003), and an additional 30 were collected at the end of the dry season (April 2004). These plants were producing culms and had produced at least one horizontal shoot that had turned upward. Additional plants were collected from this site for dissections, sectioning, and scanning electron microscopy.

These samples were taken back to the laboratory, dissected, and their morphology was mapped. To quantify variation in internode length along a shoot and determine whether this variation was associated with the production of vertical vs. horizontal shoots, the length and number of internodes were measured along the entire horizontal shoot until it turned upright and started to produce a vertical shoot and culms. The length and diameter of up to three recently matured culms on each sample were recorded. Lengths were measured with a metric ruler, and diameters were measured with electronic calipers. These culms were sampled beginning two culms back from obviously immature culms. The number of bracts on the upright culms were counted, and bract lengths were measured. Axils of all bracts were examined with a dissecting microscope for the presence of axillary buds.

Determination of sympodial vs. monopodial shoot growth
Whether shoots are sympodial or monopodial was determined by examining developing leaves and apices (1) in dissections observed with a dissecting microscope; (2) in developing shoots that were embedded in paraffin, sectioned, and examined with a compound light microscope; and (3) in material prepared for and viewed with scanning electron microscopy (SEM).

For compound light microscopy, horizontal shoot apices that were producing upright shoots were harvested from the shoots collected at the FIU-Singletary property and fixed in CRAF III solution (Berlyn and Miksche, 1976 ). This material was supplemented with material of developing horizontal shoots grown outdoors in an artificial pond in Miami, Florida. Apices were embedded in paraffin, serially sectioned at 5 µm, stained with hematoxylin-safranin, and examined with a Leitz Dialux 20 compound light microscope (Leitz, Wetzlar, Germany). The relationship of shoot apices, leaves, and axillary buds in early development was documented photographically with a Nikon CoolPix 995 digital camera (Nikon U.S.A., Melville, New York). For SEM, fixed and dissected vertical shoot apices and axillary buds were critical point dried in CO₂, coated with gold-palladium, and examined with a JSM 5900LV scanning electron microscope at 20 kV (JEOL-USA, Peabody, Massachusetts, USA) at the Florida Center for Analytical Electron Microscopy at FIU. Paraffin sections and SEMs were examined for evidence of the adnation process, that has been described for upright and horizontal shoots of Eleocharis species, and for sympodial vs. monopodial growth.

Juvenile growth pattern
To determine when architectural patterns were established in development, seeds of E. cellulosa collected at the FIU–Singeltary site were germinated in the FIU greenhouse, and the seedling leaf morphology, culm production, and branching were analyzed. Seeds were placed in saturated but not submerged soil. Germination occurred after approximately 5 mo.

Statistical analysis
Statistical analyses were performed using the SPSS 13.0 (SPSS, Chicago, Illinois, USA) statistical package for Windows and Microsoft Windows XP Excel (Microsoft, Richmond, Washington, USA). Analysis of variance was used to assess seasonal differences in morphology. Linear regressions in Excel were used to assess relationships in morphological variables between the wet and dry season.

RESULTS

Shoot architecture
General morphology
Eleocharis cellulosa has a horizontal stem that turns vertically to produce upright photosynthetic stems, the culms, from a thickened vertical stem (Figs. 1, 2). The horizontal stem bears hyaline bracts that ensheath the stem, but these bracts are ephemeral and are absent on older horizontal shoots or present only as tattered remnants (Fig. 3). No buds are visible in the axils of these bracts when examined with the dissecting microscope. Roots occasionally develop along the horizontal shoot just below the nodes. In field-collected plants the horizontal stems are 120 ± 62 mm in length (N = 60). The number of internodes on the horizontal stem varies from 3 to 8 (Table 1). Individual internodes average 23 ± 17 mm (N = 317) in length, although internode length varies along the horizontal shoot. The first bract or prophyll internode on the horizontal stem typically does not elongate, so it is approximately 1 mm or less. Subsequent internodes increase in length, so that the middle internodes are longest (30 ± 16 mm for internodes 3, 4, and 5; N = 161); internodes then decrease in length and the horizontal shoot apex turns upward (Fig. 2). After the stem becomes vertical, internodes are 1–4 mm in length, and the stem thickens (Figs. 2–4). Roots typically develop on the vertical shoot internodes in a localized region below the culms (Figs. 4, 8–10). The vertical part of the shoot system produces a variable number of photosynthetic culms, while new horizontal shoots are initiated on the vertical shoot (Fig. 1).

View larger version (98K): [in this window] [in a new window]   Figs. 1–10. Morphology of Eleocharis cellulosa from southern Florida, USA. 1. Overview of an actively growing plant; arrows mark the tip of the ensheathing B3 bract on the culms. 2. Close-up of the transition from horizontal shoot to vertical shoot. Arrow marks terminal peg of S3. 3. Tip of the horizontal shoot after transition to sympodial growth. 4. Close-up of the vertical shoot with older sympodia removed; arrows indicate roots below the B2 buds. 5. Terminal spikelet on a reproductive culm. 6. Tip of a vegetative culm; arrow marks the B4 node. 7. Tip of the vegetative culm in Fig. 6 sectioned longitudinally to show the aborted spikelet; arrow marks the B4 node. 8. Close-up of a vertical shoot showing two B2 nodes; the B2 bud enclosed by B2 is visible at the upper node; the arrow marks one root primordium; the white star marks the B1 node; brackets mark B2 + B1' internodes. 9. Close-up of a vertical shoot showing the base of one sympodium with the B2 bud breaking through the base of B2 and roots emerging from the B2 + B1' internode below the B2 bud; B1 has been pulled aside to reveal the internode; the arrow marks one emerging root tip. 10. Close-up of older vertical shoot sympodia with a B2 bud growing through the B2 base and roots growing from B2 + B1' internodes below B2 buds. Fig. 1, bar = 3 cm; Fig. 2, bar = 2 mm; Figs. 3, 4, 10, bar = 1 mm; Fig. 5, bar = 5 mm; Figs. 6–9, bar = 500 µm. Figure abbreviations: B1, first bract or prophyll; B11, first bract of next sympodium; B2b, bud in axil of second bract; B2IN, internode below B2; DS, distal parts of a sympodium = second and third bracts, culm, and shoot tip; DS1, distal parts of next sympodium; C, culm or fourth bract internode; HS, horizontal shoot; R, roots; S1–S5, sympodium 1 through 5 on a vertical shoot; TP, terminal peg or the aborted distal parts of a sympodium; VS, vertical shoot.

The first bract or prophyll on the shoot, B1, subtends an axillary bud that reiterates the vertical shoot sympodial unit. This axillary bud produces a prophyll (B1) that subtends an axillary bud, B2, B3, and B4 (Figs. 11–14). This bud is always present in the axil of B1 on the vertical shoot, and it develops sylleptically, i.e., without dormancy. Bract B2 also subtends an axillary bud (Figs. 8–10, arrow in Fig. 14), but B3 does not. The B2 bud, although always present, does not always expand and often goes dormant. Roots are initiated in a V-shaped pattern on the B2 internode below the position of the B2 axillary bud (Figs. 8–10); these roots form the root system of the plant.

View larger version (194K): [in this window] [in a new window]   Figs. 11–16. Scanning electron micrographs (Figs. 11–13, 15–16) and paraffin cross-sections (Fig. 14) of Eleocharis cellulosa shoots from southern Florida. 11. Vertical shoot sympodium that has had B1 removed and the upper parts of the sympodium and renewal shoot cut transversely to reveal bracts, culms, and the structures inside B1 of the renewal shoot. 12. Close-up of renewal shoot in Fig. 11; B1, which is addorsed to the distal parts of the previous sympodium, ensheaths B2, B3, and the shoot tip; B1 of the next sympodium (B11) is addorsed to B2. 13. An older vertical shoot cut transversely to reveal four sympodial units; the bracket indicates the oldest sympodium, while B11 plus DS1 and B12 plus DS2 are successively younger sympodia, and S3 shows the youngest, clearly visible sympodium; an even younger sympodium is visible but not labeled. 14. Cross-section of a horizontal shoot that has initiated sympodial growth; five sympodia are visible; the distal parts of the first two sympodia aborted to produce terminal pegs, while the distal parts of the next three sympodia were developing culms. 15. Unexpanded B2 bud with initial bracts removed; the initial bracts do not subtend axillary buds and the axis terminates in a terminal peg that is ensheathed by B5; B4 has a precociously developing axillary bud, in the bracket, whose prophyll (B11) has been removed; this axillary bud has a sympodial structure and B21 surrounds the distal parts of the sympodium, which will develop into a terminal peg; the renewal shoot bud in the axil of B11 is enclosed by B12. 16. Close-up of sympodial tip of Fig. 15. Fig. 11, bar = 500 µm; Figs. 12, 16, bar = 100 µm; Figs. 13, 15, bar = 200 µm. Figure abbreviations: as in Figs. 1–10; numbers after a label indicate order on a sympodium; subscripts indicate sympodium order in a series of sympodia, e.g., B12 = first bract on the second sympodium.

Growth of the horizontal shoot
When the B2 axillary bud grows out, it produces a horizontal shoot (Fig. 1). Initial growth of the horizontal shoot differs from the sympodial pattern of growth seen in the rest of the adult shoot. The horizontal shoot apex produces 2–4 (median = 3, N = 23) bracts that do not subtend axillary buds (e.g., B2, B3 in Fig. 15). After the prophyll, these first bracts produce longer internodes that average 30 ± 15 mm (N = 161) in length. The bract produced after these initial 2–4 bracts (i.e., the third, fourth or fifth bract) subtends an axillary bud that develops precociously and overtops the original apex in early development (Figs. 15, 16). The original horizontal shoot apex produces two more bracts and a reduced culm-like structure, while growth of the horizontal shoot is continued by the axillary bud (Figs. 2, 3, 15, 16). This axillary bud develops sylleptically and as a sympodium with the same structure as sympodia on the vertical shoot, but it continues growth of the horizontal shoot, producing a combined B2 + B1' internode that is similar in length to the previous internodes. After sympodial growth is initiated, each subsequent internode of the horizontal shoot consists of one sympodial unit. The bracts on the horizontal shoot in this distal phase of growth are thus the prophylls or B1 bracts of the unit (Fig. 3).

Subsequent growth of the horizontal shoot is by successive sympodial units, but the B2 + B1' internodes of these sympodia are shorter than the initial sympodia, and the internodes begin to turn upward (Fig. 2); the underdeveloped culm on each sympodium, which initially forms a terminal peg at the distal end of the B2 + B1' internode (Figs. 3, 15, 16), gradually increases in size (Figs. 2, 14), until photosynthetic culms are produced on a vertical shoot. Sympodial growth of the horizontal shoot is initiated prior to outgrowth of the B2 bud, and dormant B2 buds that have already initiated sympodial growth can be found on older vertical shoots.

Seasonal variation in shoot morphology
Architecture and branching patterns of E. cellulosa do not vary between the southern Florida wet and dry seasons, but the size of different parts of the shoot system do (Table 1). Plants sampled in October, the wet season, have significantly longer, wider culms with longer bracts than plants sampled in April, the dry season (Table 1). The wet season plants also produce more horizontal shoot internodes, and the average length of the median horizontal shoot internode is greater (Table 1).

Culm lengths and diameters of plants sampled at the end of the wet season (October) are not significantly correlated (r² = 0.03), but these variables are significantly correlated (r² = 0.60) in the dry season (April). The lengths of B2 and B3 also are not as strongly correlated in October (r² = 0.07) as they are in April (r² = 0.54).

Seedling morphology and growth
Seedlings produce sympodial units similar to the adult units immediately upon germination. The seedling initially produces three leaves, each larger than the previous leaf, then terminates in a small culm (Figs. 17, 18). These first leaves are not bracts; each has a rounded unifacial lamina and sheathing leaf base (Figs. 17–19). The branching pattern of the initial sympodium differs from the adult pattern, in that the first renewal shoot of the sympodium develops from the axil of the second leaf, rather than the first (Figs. 18, 19). The first two leaves on this second sympodium are membranous bracts, but the third leaf has a lamina. On subsequently produced sympodia, all leaves are bracts and the sympodial renewal shoot is produced in the axil of the first bract, i.e., the adult pattern of sympodial growth is followed.

View larger version (25K): [in this window] [in a new window]   Figs. 17–19. Seedlings of Eleocharis cellulosa. 17. Seedling emerging from tubercled fruit; L1 has a sheathing base and unifacial lamina. 18. First sympodium of a seedling with three leaves and a culm fully expanded; the second sympodium is developing from the bud axillary to L2 on the first sympodium; the three leaves on the first sympodium have sheathing leaf bases and unifacial laminae. 19. First sympodium with three unifacial leaves with sheathing leaf bases and a culm; the second sympodium has expanded from a bud in the axil of the second leaf. Fig. 17, bar = 0.5 mm; Figs. 18, 19, bar = 1 mm. Figure abbreviations: C, culm; L1–3, juvenile leaves; S2, second sympodium on the vertical stem.

Shoot architecture
Growth of the vertical shoot system in E. cellulosa is well-defined with respect to the number of nodes and how those nodes expand, while growth of the horizontal shoot system is less precisely defined. Our results allowed us to model the architecture and growth pattern of E. cellulosa (Fig. 20). This model provides a framework for studies of other species of Eleocharis in order to understand the ecology and evolution of this highly modified sedge genus.

View larger version (11K): [in this window] [in a new window]   Fig. 20. Model of Eleocharis cellulosa architecture. (A) Basic sympodial unit with three bracts with short internodes, a fourth bract with a long internode, and a terminal spikelet; the first two bracts of the sympodial unit subtend axillary buds. Asterisks mark the position on the internode below the second bract that will initiate roots; "X" indicates the position of the terminal spikelet. Black ovals represent buds axillary to the first bract, while gray ovals represent buds axillary to the second bract. The third and fourth bracts lack visible buds. (B) Growth of the bud axillary to the first bract produces a new sympodial unit; the first internode on the sympodial unit has been elongated in the diagram in order to separate the successive sympodia; this internode is very short on living plants. (C) Continued termination of each sympodium by a spikelet combined with outgrowth of the bud axillary to the first bract builds up a succession of photosynthetic culms on the same vertical axis. (D) Growth of the bud axillary to the second bract forms a horizontal stem that grows plagiotropically initially, then turns upward to produce a new vertical axis bearing photosynthetic stems (orthotropic phase not depicted). Figure abbreviations: HS, horizontal stem; S1, S2, S3, first, second, and third sympodia on a vertical stem; 1, 2, 3, 4, bracts 1, 2, 3, and 4 on a sympodium.

An unusual aspect of development in E. cellulosa is development of the internodes in the distal sympodial part of the horizontal shoot. This portion of the horizontal shoot is produced by superimposition of sympodia, with one internode of each sympodium forming an internode of the horizontal shoot. This internode is beneath both B2 of the original sympodium and the prophyll (B1) of its renewal shoot. Because the renewal shoot develops precociously and overtops the previous sympodium, this internode appears to be the B1 internode; its growth displaces B2 and the rest of the sympodium from its original position to the distal end of the internode. Thus, the internode itself is below both the B1 bud prophyll and the distal parts of the previous sympodium. This dual nature has been described as a fusion of these two internodes in other species of Eleocharis (Walters, 1950 ; Mora, 1960 ), but it is probably better thought of as the localization of meristematic activity into a unified cylinder when the entire sympodial unit is meristematic and the internodes of these structures are condensed and confluent (e.g., Figs. 11, 16; see suggestion in Goetghebeur, 1985 , p. 630). A similar condition has been described in Carex arenaria L. (Kukkonen and Enroth, 2004 ). When the renewal shoot bud develops precociously, while the sympodium aborts, this cylindrical region appears to belong to the prophyll. When development of these two internodes is more balanced in the vertical shoot, where the culm of the sympodium is much larger and develops over a longer period, this same internode does not elongate and is more closely associated with B2 of the sympodium (Fig. 4). Development of the next renewal shoot, however, still influences growth of this internode, which is shorter beneath the renewal shoot, giving the internode an asymmetry (left vs. right sides of B2IN, Fig. 4). An analogous asymmetry is seen in some sympodial spikelets of the Schoeneae (Zhang et al., 2004 ). This mode of development has been described in other Cyperaceae, although it is considered to be rare in the family (Goetghebeur, 1985 ; Kukkonen and Enroth, 2004 ). Abortion of parts of the sympodia involved, such as the culms on the horizontal shoot sympodia, makes it difficult to recognize their extra-axillary position, however, so the possibility of this type of growth should be considered when investigating the morphology of other members of the family.

Recognition of the strictly defined sympodial structure and iterative nature of the morphology of E. cellulosa provides a basis for examining morphology of other members of the genus. We propose that the sympodial unit described here is characteristic of the genus. Evans (1965 , 1967 ) noted that the culm of E. acuta has a scale leaf and two closely appressed sheaths and terminates in a dead tip enclosed by scale leaves or in a spikelet, while Walters (1950) illustrated three leaves on the culms of E. palustris (L.) Roem. & Schult. The recent Flora of North America treatment of Eleocharis describes the structure characteristic of the genus as "Leaves basal, 2 per culm; ... Inflorescences terminal; spikelet 1... " (Smith et al., 2002 , p. 60). The two leaves are B2 and B3 of the sympodial unit; the B4 internode forms the culm. Based on an examination of the figures in H. K. Svenson's treatment of the genus (Svenson, 1929 , 1932 , 1934 , 1937 , 1939 , 1947 ), variations on the basic pattern described for E. cellulosa might also be found throughout the genus. What has not previously been recognized for Eleocharis is the nature of the bud and shoot dimorphism and how variations in expression of this dimorphism can provide additional characters to distinguish species and, perhaps, sections and subgenera. For example, a character used to distinguish some sections of Eleocharis is the presence or absence of rhizomes or stolons in a species (Smith et al., 2002 ), so evolution of aspects of the shoot dimorphism may have provided phylogenetic innovation in the genus.

Preliminary observations on E. elongata Chapm., which also belongs to subgenus Limnochloa, indicate that this species is morphologically similar to E. cellulosa, except that the horizontal shoot, which arises from the B2 bud, appears to be sympodial from initiation. Additionally, the terminal portion of the horizontal shoot sympodium is more developed than in E. cellulosa, producing a recognizable unit that can develop into a normal culm along the horizontal shoot. The horizontal shoot of E. elongata also forms roots at the distal end of the internode more frequently than does E. cellulosa (J. H. Richards, unpublished data). Similarly, E. geniculata (L.) Roem. & Schult., which is in the subgenus Eleocharis, sect. Eleogenus, is a nonstoloniferous, tufted species (Smith et al., 2002 ). This species has the same sympodial structure as E. cellulosa and forms vertical shoots from reiteration of the sympodium from B1 axillary buds (J. H. Richards, personal observation). The tufts are built up from branching of the B2 buds. Like E. elongata, these buds are sympodial from initiation; but the internodes on the B2 bud do not elongate, and the sympodia grow vertically rather than horizontally. Thus, the B2 buds of E. geniculata make new vertical shoots and so multiply the shoot system, like the B2 buds in E. cellulosa and E. elongata; but the B2 buds of E. geniculata lack the horizontal phase of growth seen in E. elongata.

This brief survey indicates that one of the unique aspects of the morphology of E. cellulosa is the initial phase of growth of the B2 bud and that the variables that can differ among species in B2 growth are amount of internodal elongation, shoot orientation (geotropic response), and timing of initiation of strict sympodial growth. The degree of outgrowth of culms on the horizontal shoot system also varies among species. In E. palustris, growth of the rhizome appears to result from growth of the B1 bud, and single culms are spread along the rhizome (Walters, 1950 ). Similarly, E. sphacelata R. Br. forms a horizontal rhizome with one, or occasionally two, culms per node (Sorrell et al., 1997 ).

A number of species of Eleocharis proliferate from the tips of the culm, especially in species that grow as submerged aquatics. Presumably this comes from activation of the shoot apex at the tip of the culm, which is enclosed by the B4 bract. Whether the proliferations are composed of typical Eleocharis sympodial units and which buds are active in producing the proliferation remain to be determined.

Well-defined uninterrupted meristems have been found at the internodes of horizontal shoots in E. cellulosa with localized distal meristematic regions in the internodes (Fisher and French, 1978 ). In contrast, the aerial axes produce intercalary meristems at the base of the elongated internodes (Fisher and French, 1978 ). The structure of this intercalary meristem has been described for E. acuta (Evans, 1965 , 1967 ). Our study has shown that the differences between these internodes are more profound developmentally than differences in total length and orientation, because the culm internode is the B4 internode, while the horizontal internodes are either a distal B2 + B1' internode or one of the initial monopodial internodes.

The confinement of roots to the B2 node below the position of the terminal portion of a sympodium occurs in the other species of Eleocharis examined. When roots appear on the horizontal shoot, they also occur in this position. Thus, the root system of the plant is built from aggregation of the root systems of individual sympodial units, a well-defined example of a shoot-borne root topology (Groff and Kaplan, 1988 ). We do not know what these morphological relationships mean for patterns of nutrient uptake and translocation or for clonal integration. Eleocharis cellulosa responds to some environmental changes by changes in root–shoot allocation (Edwards et al., 2003 ; Busch et al., 2004 ; Chen et al., 2005 ), but whether this results from changes in the newly formed roots on the growing sympodia (e.g., more root primordia or longer, more highly branched roots producing an increase in root allocation) or from elaboration of the extant root system has not been studied. In an experiment to look at growth in response to different water phosphorus and oxidation reduction (Eh) levels, Chen et al. (2005) reported the greatest increase in tissue P in newly produced roots of E. cellulosa as opposed to roots present at the beginning of their experiment, although both sets of roots had increased tissue P at the highest level of P.

The tight structural coupling of a root system to a sympodium may imply an equally tight functional coupling. In E. sphacelata the emergent culm aerates the root system, as well as providing for convective flow that flushes the submerged parts of the shoot system (Sorrell, 1994 ; Sorrell et al., 1994 , 1997 ; Sorrell and Tanner, 2000 ). It would be interesting to know how this aeration works in the context of the sympodial architecture of the plant, i.e., do the culms of one sympodium flush the roots of other sympodia, and how does connectivity of sympodia on a single vertical shoot compare to that of sympodia separated by horizontal shoots?

Phenological variation
Water levels fluctuate seasonally in southern Florida (Duever et al., 1994 ). When water level was manipulated experimentally, plants of E. cellulosa that were transferred from deep water to shallow water had shoots that died quickly (Edwards et al., 2003 ). When shallow-water shoots were transferred to deep water, shoots elongated rapidly (Edwards et al., 2003 ). Total shoot length of E. cellulosa was greater in flooded conditions than in shallow conditions (Busch et al., 2004 ). Results presented here found culm length and diameter and bract length to be greater at the end of the wet season when water was high, than at the end of the dry season, when water was low. Thus, these field data corroborate the experimental data of Edwards et al. (2003) and provide evidence that E. cellulosa adjusts shoot length throughout the year in response to water level. Similar results have been reported for responses of E. interstincta (Vahl) Roem. & Schult. to seasonal and induced changes in water level (dos Santos and Esteves, 2002 ). The lack of correlation among parts of the shoot in the wet as opposed to dry season reflects the plasticity of the E. cellulosa shoot system in response to water level; this wet season response appears to override the innate developmental correlations found in the dry season plants.

FOOTNOTES

¹ The authors thank Dr. J.F. Meeder and RMC Singeltary, Inc. for research support and access to the FIU-Singeltary property and the FIU FCAEM Laboratory for support of scanning electron microscopy.

² Present address: 91-05 197th St., Hollis, NY 11423 USA

³ Author for correspondence (Richards{at}fiu.edu )

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