Systematic Botany (2009), 34(2): pp. 312–323
© Copyright 2009 by the American Society of Plant Taxonomists
A Morphology-Based Cladistic Analysis of Digitaria (Poaceae, Panicoideae, Paniceae)
Andrea S. Vega,1 Gabriel H. Rua,1 Liliana T. Fabbri,1 and Zulma E. Rúgolo de Agrasar2
1
Cátedra de Botánica Agrícola, Facultad de Agronomía, Universidad de Buenos Aires, Avenida San Martín 4453,
C1417DSE Buenos Aires, Argentina
2
Instituto de Botánica Darwinion, Labardén 200, Casilla de correo 22, B1642HYD San Isidro, Argentina
1
Author for correspondence (avega@agro.uba.ar)
Communicating Editor: Kenneth M. Cameron
Abstract—A phylogenetic analysis was performed on 67 species of Digitaria belonging to four subgenera and 26 of the 32 sections recognized in Henrard’s monograph. The analysis was based on 113 discrete and six continuous morphological characters. In the resulting topologies the genus Digitaria was monophyletic. In spite of the low support for most groupings, several clades were recovered. The subdivision of
Digitaria in the four subgenera proposed by Henrard was not supported since the large subgenus Digitaria appears as a paraphyletic assemblage within which the other three subgenera are nested. Nevertheless, the monophyly of some of Henrard’s sections was supported. This is
the first approach to the phylogeny of Digitaria.
Resumen—Se llevó a cabo un análisis cladístico. Se incluyeron 67 especies de Digitaria pertenecientes a los 4 subgéneros y a 26 de las 32 secciones reconocidas en la monografía de Henrard. El análisis fue basado en 113 caracteres morfológicos discretos y 6 continuos En las topologías
resultantes el género Digitaria resultó monofilético. A pesar del bajo soporte de la mayoría de los grupos, fueron recuperados varios clados. Los
resultados no fueron consistentes con la subdivisión de Digitaria en 4 subgéneros propuesta por Henrard, ya que el extenso subgénero Digitaria
aparece como un agregado parafilético dentro del cual se hallan anidados los otros tres subgéneros. Sin embargo, la monofilia de algunas
secciones fue confirmada. El presente estudio constituye el primer análisis filogenético de Digitaria.
Keywords—Cladistic, Digitaria, Paniceae, phylogeny, Poaceae, systematics.
The genus Digitaria Haller emend. A. S. Vega & Rúgolo
(Vega and Rúgolo de Agrasar 2001) comprises ca. 220 species distributed in tropical, subtropical, and temperate areas
worldwide (Watson and Dallwitz 1992 onwards). It includes
foraging species, minor cereals, turf plants, and soil binders, as well as some weeds (Henrard 1950; Veldkamp 1973;
Rúgolo de Agrasar 1974; Clayton and Renvoize 1986; Nicora
and Rúgolo de Agrasar 1987; Guzmán et al. 1989; Molina
Sánchez 1990; Watson and Dallwitz 1992 onwards). Species of
Digitaria can be recognized by their cartilaginous upper florets, with fertile lemmas having noninrolled, membranous
margins, scarcely exposing the fertile palea. This character
is used to distinguish Digitaria from allied genera: Axonopus
P. Beauv., Panicum L. and Paspalum L. Another taxonomic
character of Digitaria is the position of fertile lemmas toward
the axis of the inflorescences; lower glumes and lemmas are
abaxial, and upper glumes and lemmas are adaxial. This character distinguishes Digitaria from Axonopus, the latter also
without a lower glume (Henrard 1950).
An historical survey of Digitaria shows that several authors
have considered it as an infrageneric entity (section, series,
or subgenus) within Panicum and Paspalum (Haller 1768;
Trinius 1826; Nees von Esenbeck 1829; Steudel 1853; Gray
1856; Bentham 1878 pp. 463–464; Hackel 1901; Camus 1912).
Walter (1788) described Syntherisma as a new genus, and Nees
(1829) described Trichachne, including Acicarpa Raddi in its
synonymy.
Hackel (1901) first divided Panicum subg. Digitaria into
three well-marked, but not quite natural, series: Solitaria,
Binata, and Ternata. Digitaria ser. Solitaria comprises species
with single, sessile spikelets along the inflorescence branches;
D. ser. Binata includes species with one spikelet subsessile
and the other pedicellate, and in D. ser. Ternata each short paraclade comprises three or more spikelets, one subsessile and
the others pedicellate. In her treatment of Paniceae, Chase
(1906) recognized three genera, Valota Adans. (= Trichachne
Nees), Syntherisma Walter, and Leptoloma Chase. According to
Chase (1906), Valota includes species with lanceolate-acuminate
upper florets and upper glumes and lower lemmas clothed
with long hairs exceeding the length of the spikelets;
Syntherisma, as well as Leptoloma, has elliptic upper florets,
and upper glumes and lower florets clothed with short hairs
or glabrous. Syntherisma differed from Leptoloma by having
“spikelets disposed in 1-sided racemes which are digitate
or racemose” rather than “panicles divergent at maturity”
(Chase 1906).
According to Stapf (1919) the varied and distinguishable
types of hairs in the spikelets, when correlated with other
characters, constitute a guide to the main groups of species
in Digitaria. This author defined two sections of Digitaria in
Tropical Africa, sect. Setariopsis and sect. Eu-Digitaria, the latter composed of nine subsections.
Hitchcock (1927, 1950) recognized Digitaria, Leptoloma, and
Trichachne as valid genera, and considered Valota as a synonym of Trichachne.
Parodi (1928) mentioned the necessity of transferring the
species of Valota (Trichachne) to Digitaria on the basis of morphological characteristics, and Henrard (1950) formally transferred species in Valota, Syntherisma, and Leptoloma to Digitaria,
while making some nomenclatural changes.
Even though taxonomic studies on Digitaria have been carried out by several authors (Hackel 1901; Chase 1906; Stapf
1919; Rúgolo de Agrasar 1968, 1969, 1970, 1974, 1976, 1990,
1992, 1993, 1994; Veldkamp 1973; Webster 1983; Rúgolo de
Agrasar and Sánchez 1989; Wipff and Hatch 1994; CantoDorow 2001; Canto-Dorow and Longhi-Wagner 2001; Vega
and Rúgolo de Agrasar 2001, 2002a, 2002b, 2003, 2005, 2006a,
2006b, 2007; Renvoize et al. 2006, among others), the only
available comprehensive treatment is Henrard’s (1950) monograph. He subdivided Digitaria into four subgenera: Leptoloma
(Chase) Henrard, Setariopsis (Stapf) Henrard, Solitaria (Hack.)
Henrard, and Digitaria, the latter with 32 sections (Table 1).
Nevertheless, Henrard’s classification has been partially
questioned (Veldkamp 1973; Rúgolo de Agrasar 1974) and the
relationships between species and groups of species remain
unclear.
Some recent molecular studies on Panicoideae throw some
light on the systematic position of Digitaria within the sub312
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VEGA ET AL.: PHYLOGENY OF DIGITARIA
313
Table 1. Classification of Digitaria with subgenera and sections recognized by Henrard (1950). The total number of species included in each subgenus or section is mentioned between brackets, including additions (*) from Rúgolo de Agrasar (1976, 1992) and Wipff and Hatch (1994). Taxa considered
in this study are listed below.
Digitaria
Subg. Solitaria (Hack.) Henrard (8 spp.)
Subg. Setariopsis (Stapf) Henrard (9 spp.)
Subg. Leptoloma (Chase) Henrard (4 spp.*)
Subg. Digitaria
Sect. Aequiglumae Henrard (16 spp.)
Sect. Atrofuscae Henrard (10 spp.)
Sect. Biformes Henrard (2 spp.)
Sect. Calvulae (Stapf) Henrard (18 spp.)
Sect. Capitipilae Henrard (4 spp.)
Sect. Cirripilae (Stapf) Henrard (12 spp.)
Sect. Clavipilae (Stapf) Henrard (22 spp.)
Sect. Corynotrichae Henrard (10 spp.)
Sect. Debiles Henrard (1 spp.)
Sect. Erianthae Henrard (33 spp.)
Sect. Flaccidulae (Stapf) Henrard (4 spp.)
Sect. Gibbosae Henrard (1 spp.)
Sect. Glabratae Henrard (9 spp.)
Sect. Heteranthae Henrard (2 spp.)
Sect. Horizontales Henrard (18 spp.)
Sect. Laniflorae Henrard (2 spp.)
Sect. Leianthae Henrard (8 spp.)
Sect. Leucostachyae Henrard (1 spp.)
Sect. Monodactylae (Stapf) Henrard (1 spp.)
Sect. Orthotrichae Henrard (14 spp.)
Sect. Parviflorae Henrard (11 spp.)
Sect. Parviglumae Henrard (7 spp.)
Sect. Pennatae (Stapf) Henrard (8 spp.)
Sect. Remotae Henrard (2 spp.)
Sect. Sanguinales (Stapf) Henrard (26 spp.)
Sect. Subeffusae Henrard (4 spp.)
Sect. Transversales Henrard (1 spp.)
Sect. Trichachne (Nees) Henrard (10 spp.*)
D. mariannensis Merr.
D. diagonalis (Nees) Stapf
D. minutiflora Stapf
D. arenicola (Swallen) Beetle
D. cognata (Schult.) Pilg.
D. pubiflora (Vasey) Wipff
D. eriostachya Mez
D. aequiglumis (Hack. & Arechav.) Parodi
D. fuscescens (J. Presl) Henrard
D. curvinervis (Hack.) Fernald
D. bicornis (Lam.) Roem. & Schult.
D. badia (Scribn. & Merr.) Fernald
D. phaeotrix (Trin.) Parodi var. hackelii (Arechav.) Henrard
D. maitlandii Stapf & C. E. Hubb.
D. gazensis Rendle
D. botryostachya Stapf
D. balansae Henrard
D. ternata (A. Rich.) Stapf
D. thouaresiana (Flüggé) Camus
D. atra Luces emend A. S. Vega & Rúgolo
D. argyrostachya (Steud.) Fernald
D. melanochila Stapf
D. bonplandii Henrard
D. gerdesii (Hack.) Parodi
D. chaseae Henrard
D. debilis (Desf.) Willd.
D. eriantha Steud.
D. nodosa Parl.
D. nitens Rendle
not represented
D. abyssinica (Hochst. ex A. Rich.) Stapf
D. heterantha (Hook. f.) Merr.
D. horizontalis Willd.
D. pearsonii Stapf
D. perrottetii (Kunth) Stapf
D. brownii (Roem. & Schult.) Hughes
D. leiantha (Hack.) Parodi
D. katangensis Robyns
not represented
D. monodactyla (Nees) Stapf
D. argillacea (Hitchc. & Chase) Fernald
D. fragilis (Steud.) Luces
D. cayoensis Swallen
D. lecardii (Pilg.) Stapf
D. parviflora (R. Br.) Hughes
D. gymnostachys Pilg.
D. ammophila (F. Muell.) Hughes
D. coenicola (F. Muell.) Hughes
D. divaricatissima (R. Br.) Hughes
D. pennata (Hochst.) T. Cooke
not represented
D. sanguinalis (L.) Scop.
D. ciliaris (Retz.) Koeler
D. junghuhniana (Nees ex Steud.) Henrard
not represented
D. similis Beetle ex Gould
D. californica (Benth.) Henrard
D. swalleniana Henrard
D. sacchariflora (Nees) Henrard
D. insularis (L.) Fedde
D. tenuis (Nees) Henrard
D. hitchcockii (Chase) Stuck.
D. laxa (Rchb.) Parodi
D. patens (Swallen) Henrard
D. catamarcensis Rúgolo
(Continued)
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Table 1.
SYSTEMATIC BOTANY
[Volume 34
Continued
Digitaria
Sect. Tricholaenoides Henrard (4 spp.)
Sect. Trichophorae Henrard (3 spp.)
Sect. Verrucipilae (Stapf) Henrard (24 spp.)
Sect. Xanthotrichae Henrard (1 spp.)
family. A DNA sequence data analysis from the chloroplast
gene ndhF (Giussani et al. 2001) suggests that Panicoideae is
divided into three well supported clades: two corresponding
to the long-recognized tribe Paniceae and the remainder corresponding to the Andropogoneae. The splitting of Paniceae into
two clades correlates with base chromosome numbers x = 9
and x = 10. Digitaria belongs to the x = 9 Paniceae, and appears
as sister to the remaining genera within this clade. A second
analysis using sequences from the rpoC2 insert (Duvall et al.
2001) also supports the monophyly of Digitaria and its relationship with the remaining x = 9 Paniceae. Thus, the hypothesis of affinity of Digitaria with Paspalum, Axonopus, and other
genera with chromosome base number x = 10 proposed by
earlier authors (Henrard 1950; Butzin 1970; Rúgolo de Agrasar
1974) would be rejected on the basis of molecular and chromosome base number. However, the position of Digitaria is still
uncertain, whether sister to all x = 9 Paniceae or sister to the
Setaria/Urochloa/Panicum clade (Giussani et al. 2001).
Since no hypothesis regarding the phylogeny within
Digitaria is currently available, the aim of the present paper
is to explore phylogenetic relationships within the genus, and
to test the monophyly of the currently recognized subgeneric
entities on the basis of morphological evidence. This analysis
will be complementary to an ongoing study based on molecular data (Vega et al. unpubl.).
Materials and Methods
Ingroup Taxa—A set of 67 species of Digitaria was considered in our
analysis, including representatives of subgenera Leptoloma, Setariopsis,
Solitaria, and 26 of the 32 sections of subgenus Digitaria (Table 1).
Outgroup Taxa—Three further representatives of the x = 9 clade of
Paniceae were included in our analysis: Echinochloa pyramidalis (Lam.)
Hitchc. & Chase, Urochloa brizantha (Hochst. ex A. Rich.) R. D. Webster,
and Panicum repens L. Anthaenantia lanata (Kunth) Benth., a member of the
x = 10 Paniceae, was also included and used for the purpose of rooting.
Because “the resolution among multiple outgroup terminals […] may
affect both the position of the ingroup relative to outgroups and the topology of relationships within the ingroup” (Nixon and Carpenter 1993:
422), some characters were included in our analysis to resolve outgroup
relationships.
Material—Morphological characters (vegetative, reproductive, and
anatomical) were scored from herbarium material. Specimens belonging to the following herbaria were examined (acronyms after Holmgren
et al. 1990): AAU, BAA, C, CANB, CTES, G, K, L, LIL, MO, P, PRE, SI,
SJ, UB, US, VEN, and WU. Only one or two representative specimens
of each taxon are listed in Appendix 1. Whenever possible, morphological data were corroborated with living material, through field observations as well as examination of plants cultivated in the “Lucien Hauman”
Botanical Garden, Facultad de Agronomía, Universidad de Buenos Aires,
Argentina for D. aequiglumis, D. argyrotricha, D. bicornis, D. californica,
D. catamarcensis, D. ciliaris, D. diagonalis, D. eriantha, D. fuscescens, D. insularis,
D. laxa, D. phaeotrix, D. similis, D. swalleniana, D. ternata, and D. sanguinalis.
Morphological characters related to inflorescence structure and growth
habit were scored according to Rua (2003).
not represented
D. pittieri (Hack.) Henrard
D. eggersii (Hack.) Henrard
D. argyrotricha (Andersson ex Peters) Chiov.
D. angolensis Rendle
D. violascens Link
D. mollicoma (Kunth) Henrard
not represented
Anatomical Studies—Segments of the middle portion of the penultimate leaf blade of a fertile innovation were used in anatomical studies.
Leaf blades of all studied species were taken from living plants when
available, or from herbarium specimens and soaked in a nonionic detergent solution at 70°C for 1 hr. Materials were either hand sectioned and
stained with safranin, or embedded in paraffin and cut with a rotary
microtome, dehydrated in an ethanol series, and double stained with
safranin-fast green (D’Ambrogio de Argüeso 1986). Transverse sections
were studied under a Wild M20 light microscope.
Observations and measurements of epidermal cells of the upper lemma
were made with an optical microscope (Zeiss Axioplan, Zeiss, Oberkochen,
Germany) connected to an image analyzer (Imagenation Px, Imagenation
Corp., Beaverton, Oregon). Upper lemmas were dissected from the spikelets and mounted in gelatine-glycerine. Measurements of cell width and
relation between the maximum (outer) and minimum (inner) distance of
undulations in horizontal anticlinal walls (Ellis 1979) were taken from
three cells of each specimen.
Longitudinal sections of the spikelets as well as different types of
pilose indumentum were selected, mounted and coated with a goldpalladium (40% - 60%) alloy by a Thermo VGScientific, and observed
using a ZEISS DSM 940A Scanning Electron Microscope (SEM) at the
Instituto de Botánica Darwinion, Argentina, and a Phillips XL 30 (Phillips,
The Netherlands) SEM at the Museo Bernardino Rivadavia, Argentina.
Characters—The matrix included 113 discrete plus six continuous morphological characters (Appendix 2); 105 of these showed variation at the
ingroup level. The remaining 14 characters were included either as possible synapomorphies joining the genus Digitaria with outgroup terminals,
or as informative characters for the outgroups. Autapomorphies were not
included in our analysis. Polymorphic characters were scored as such, as
recommended when the polarity of the characters are unknown from previous analysis (Kornet and Turner 1999). Missing data (including unavailable as well as inapplicable data) represent 5.7% of the entries in the data
matrix. Continuous characters were analized as such, using the methodology implemented in TNT (Goloboff et al. 2005).
Data Analysis—The data matrix (Supplemental Appendix 3) was analized using TNT (Goloboff et al. 2003a). Data matrix and trees were submitted to TreeBASE (Study number S2186). A heuristic search strategy was
adopted, consisting of 100 random addition sequences followed by TBR
swapping, using Wagner trees as starting trees and holding a maximum of
two trees each time. The trees obtained were submitted to a round of TBR
swapping, then to 1,000 iterations of Parsimony Ratchet (Nixon 1999), and
then to an additional round of TBR. Branches with ambiguous support
(min. length = 0) were collapsed. Group support was quantified through:
(1) the decay index of Bremer (BS, Bremer 1994), and (2) the symmetric
jackknife group frequency (SJF, Goloboff et al. 2003b).
Because of the high homoplasy of the data set, tree searches were
performed using implied weights (Goloboff 1993, Goloboff et al. 2008).
When using implied weights, TNT downweights homoplastic characters in proportion to their amount of extra steps (homoplasy), and saves
trees that minimize ‘distortion’ (D), which is an increasing function of the
homoplasy (Goloboff et al. 2003a). Distortion is quantified with the equation, D = e/(e + k), where e = extra steps, and k = constant of concavity. The strength with which a homoplastic character is downweighted
depends on the concavity value (k) of the weighting function: the lower
the k value the stronger the weighting function. To explore the stability of
the results, analyses were performed under 33 different k values. Since distortion is not a linear function of concavity, k values were selected in such
a way that they produce regular distortion increments of 1.25%, within a
range of 50–90% related to an average nonhomoplastic character (Mirande
2007). To test tree stability related to variations of k, comparisons between
pairs of contiguous trees (i.e. between trees obtained using kn and kn-1)
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VEGA ET AL.: PHYLOGENY OF DIGITARIA
315
Fig. 1. Majority rule consensus of cladograms resulting from parsimony analysis using implied weighting, with k = 4.2–37.9 (for details see text).
Numbers above branches indicate the branch frequency (higher than 50%) in all trees.
316
SYSTEMATIC BOTANY
were performed through calculation of (1) SPR-difference, i.e. the number
of SPR-swaps required to convert tree n into tree n-1; (2) number of shared
taxa (= nodes in agreement subtree), and (3) number of shared groups
(= nodes in strict consensus tree). Calculation of k values, tree searches,
and calculation of stability measures were all performed using a TNT
script written by J. Marcos Mirande (unpublished), who kindly made it
available to us. Since support measures are not comparable when using
different weighting functions, BS and SJF values were independently calculated for each concavity.
Results
Thirty-three trees were found, using 33 k values ranging between 4.2 and 37.9. These results are summarized in
the majority rule consensus tree presented in Fig. 1, which
shows the groups being more stable across the range of k values tried. Sixteen of the obtained topologies were different.
Values of k ranging between 12 and 17 yielded the more stable topology (Fig. 2). Support measures shown in Fig. 2 were
calculated under k = 15.
In all trees Digitaria was monophyletic (Fig. 1) and relatively well supported by several synapomorphies. In most
cases, clades that were more robust in relation to weighting
intensity (i.e. having higher frequencies in the majority rule
consensus, Fig. 1) were also the better supported (Fig. 2). The
following clades (Figs. 1, 2) merit some comments:
[Volume 34
1) A clade including representatives of sect. Trichachne
and Trichophorae (hereafter the [Trichachne + Trichophorae]
clade), which splits into two subclades, one of them comprising South American species of the sect. Trichachne characterized by large, acuminate spikelets (D. laxa, D. swalleniana,
D. similis, D. catamarcensis, D. insularis, and D. sacchariflora,
hereafter the ‘core-Trichachne’ clade), the other one including
the Trichophorae [D. pittieri + D. eggersii] plus D. californica and
D. tenuis.
2) A clade characterized by ‘tumbleweed’ inflorescences
composed of primary branches with a spikelet-free proximal
portion, the basalmost [sub]verticillate (hereafter, the ‘tumbleweed’ clade); this clade includes D. gymnostachys as sister to a
subclade which splits into two monophyletic groups: [D. pubiflora + D. arenicola + D. cognata] (i.e. Digitaria subg. Leptoloma)
and [D. pennata + D. ammophila + D. divaricatissima + D. coenicola] (D. sect. Pennatae). In most topologies, the ‘tumbleweed’
clade is sister to [D. brownii + D. patens], two “peripheral”
members of the sect. Trichachne native to Australia and North
America respectively.
3) A large clade characterized by having spikelets with
glumes and lemmas approximate, i.e. not separated by conspicuous internodes (hereafter, the [Digitaria + Ternatae] clade).
Most topologies favored the splitting of this clade into two
subclades, one including species with decumbent to creeping
Fig. 2. Most parsimonious tree obtained under k = 12.6–16.8. Numbers above branches represent Bremer support, number below branches refer to
symmetric jackknife group frequencies; both support measures calculated under k = 15.
2009]
VEGA ET AL.: PHYLOGENY OF DIGITARIA
317
culms allied to the type species D. sanguinalis (hereafter the
‘core-Digitaria’ clade), the other subclade including most
species with ternate short paraclades (hereafter the ‘Ternata’
clade). Species of Digitaria sections Atrofuscae and Verrucipilae,
which have ternate short paraclades, were intermingled and
separate into two clades, one of them nested within the coreDigitariae (D. fuscescens, D. violascens, D. argyrotricha, D. mollicoma) and the other one within the Ternatae (D. angolensis,
D. curvinervis). Digitaria mariannensis, the only species of the
subgenus Solitaria included in our analysis, was also placed
within the core-Digitaria clade. Digitaria subgenus Setariopsis
and a clade including most species of the section Clavipilae
were nested within the Ternatae.
Discussion
Monophyly of Digitaria—The present analysis supports the
monophyly of Digitaria which is unambiguously supported
by several morphological synapomorphies. Our results are in
agreement with previous analyses based on molecular data
(Giussani et al. 2001; Duvall et al. 2001).
Subgeneric Classification—Chase distinguished the genera Trichachne (sub. nom. Valota Adans.) and Leptoloma from
Digitaria (sub. nom. Syntherisma Walt.), but her concept was
disregarded by Henrard (1950), who defined Digitaria in a
comprehensive way by including Leptoloma and Trichachne.
Instead, Henrard subdivided Digitaria into four subgenera
(Leptoloma, Setariopsis, Solitaria, and Digitaria). The species of
the former genus Trichachne were divided by Henrard into
two sections, D. sect. Trichachne and sect. Trichophorae, whereas
the Australian species of Leptoloma were included in D. sect.
Pennatae. The North American Digitaria cognata was grouped
together with the Indian D. tomentosa (Schult.) Pilg. into
D. subg. Leptoloma.
Our analysis is more consistent with Chase’s rather than
Henrard’s concept. Indeed, species of both Digitaria sect.
Trichachne and D. subg. Leptoloma form a clade outside the
core Digitaria clade. Nevertheless, a clade containing both
Trichachne and Leptoloma species was recovered under k = 7
(tree not shown). Henrard’s Digitaria sect. Trichophorae, formerly placed within Valota (Chase 1906), and D. sect. Laniflorae,
also included by Webster (1983) in the D. sect. Trichachne, were
also aligned outside the core Digitaria, as well as the D. sect.
Pennatae, which is sister to Leptoloma.
According to our data Digitaria appears to be composed of
a major clade corresponding to a core Digitaria, and a doubtfully resolved portion including the D. subg. Leptoloma and
D. sections Trichachne, Trichophorae, Laniflorae, and Pennatae.
Clearly, the subgeneric scheme of Henrard must be rejected,
since the three minor subgenera Leptoloma, Setariopsis, and
Solitaria appear nested within a paraphyletic D. subg. Digitaria. The validity of some of Henrard’s sections will be discussed below.
Our analysis is the first preliminary cladistic contribution to the understanding of the phylogeny within Digitaria.
Nevertheless, taxonomic decisions seem premature at this
time until molecular analyses are completed (A. S. Vega et al.
unpubl.).
Evolution of Selected Characters within Digitaria—
Spikelet Indumentum—Stapf (1919) was the first agrostologist to use the varied nature of the hairs in the spikelets as
a guide to the infra-generic taxonomy of Digitaria. Henrard
Fig. 3. A–E. Types of pilose indumentum of the spikelets. SEM photographs. A–B. Linear hairs with acute or obtuse apex. A. Smooth walls
[D. aequiglumis, Schinini et al. 18993 (CTES)]. Bar = 1 µm. B. Verrucose walls
[D. violascens, Klein 11249 (SI)]. Bar = 10 µm. C. Hairs with a slightly dilated
and mucronate apex [D. phaeotrix var. adusta, Stuckert 18615 (G)]. Bar =
20 µm. D–E. Claviform hairs. D. Type Clavipilae [D. filiformis, Bittmore 799a
(L)]. Bar = 10 µm. E. Type Corynotrichae [D. gerdesii, Hassler 8384 (G)]. Bar =
20 µm.
(1950) based several sections on this feature, in combination
with other, more general characters. Spikelets of Digitaria are
typically pilose, although glabrous spikelets occur as well,
and a few sections are characterized by glabrous spikelets.
Indumentum is varied, usually restricted to upper glume
and lower lemma, and occasionally present on the back of the
reduced lower palea. Pubescence on the back of a cartilaginous upper lemma had mistakenly been reported in D. atra
(Luces 1942); however, the cartilaginous bract corresponds to
the lower lemma (Vega and Rúgolo de Agrasar 2001).
The distribution of indumentum on the upper glume and
lower lemma has been considered a taxonomically valuable
character due to its constancy in each taxon with the exception of D. ischaemum, where two types of hair indumentum
were reported (Veldkamp 1973). Nevertheless, distribution
of the indumentum on the spikelet bracts is highly homoplasious and carries poor phylogenetic information.
Two general types of hairs were recognized in Digitaria species: linear hairs, with smooth or verrucose walls with acute
or obtuse apices (Fig. 3A, B) and hairs with a dilated apex and
smooth walls (Fig. 3C–E). Within this last type, two morphological subtypes can further be recognized: hairs with slightly
dilated apices, sometimes provided with an acumen (Fig. 3C),
and claviform hairs which are dark at maturity (Fig. 3D, E).
Claviform hairs have different forms, which have been used
by Henrard (1950) to characterize different sections within
the genus: Clavipilae (Fig. 3D), Corynotrichae (Fig. 3E), and
Capitipilae.
Hairs with more or less dilated apices are synapomorphic for a large group within the ‘Ternatae’, and species
with plainly dilated hairs form a clade nested within a more
general group with slightly dilated hairs (Fig. 4A). Section
Clavipilae, including species distributed in temperate and
tropical regions of both hemispheres, forms a well supported
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SYSTEMATIC BOTANY
[Volume 34
Fig. 4. A–D. Mapping of the apices of spikelet hairs (character (ch.) 6, cladogram (cl.) A), walls of spikelet hairs (ch. 8, cl. B), elongation of the first
rachilla internode (ch. 13, cl. C), and life cycle (ch. 79, cl. D) onto the topology of Fig. 2.
2009]
VEGA ET AL.: PHYLOGENY OF DIGITARIA
clade. Under some concavity values (i.e. 4.2, 6.0, and 6.7), the
Clavipilae are nested within a clade composed of all species
sharing clavate hairs (trees not shown), which also includes
species belonging to sections Capitipilae and Corynotrichae,
endemic to tropical Africa and South America respectively,
as well as the African D. monodactyla, a species with nondilated hairs.
Due to difficulties in placing taxa with glabrous spikelets in
the current subgeneric classification, Henrard (1950) created
some sections exclusively based on this character, e.g. D. sect.
Atrofuscae and sect. Glabratae. Species with glabrous spikelets
occur together with species having pilose spikelets in other
sections.
According to our analysis, species of D. section Atrofuscae
appear intermingled with representatives of D. sect. Verrucipilae, characterized by verrucose hairs. Species belonging
to D. sections Verrucipilae and Atrofuscae formed a clade under
stronger weighting functions (trees not shown). Digitaria
mollicoma and D. fuscescens, in D. sect. Verrucipilae and sect.
Atrofuscae, respectively, form a highly supported clade under
all concavity values explored (Figs. 1, 2). Digitaria abyssinica,
the only species of D. sect. Glabratae included in our analysis,
floats across the core Digitaria as the weighting constant varies.
Spikelet hairs seem to have been lost in several independent
lineages during the evolution of this character in Digitaria. On
the other hand, verrucose hairs could have evolved once or
twice (Fig. 4B) within the genus.
Rachilla Internodes—Digitaria section Trichachne was
distinguished from other groups of Digitaria based on elongate
spikelets with conspicuous internodes (Henrard 1950; Rúgolo
de Agrasar 1974) [Fig. 5A]. Elongated rachilla internodes also
occur in D. subg. Leptoloma and in D. sections Trichophorae,
Laniflorae, and Pennatae, where at least the first rachilla
internode is conspicuously elongated. Elongated rachilla
internodes occur frequently among the x = 9 Paniceae, and
seem to be plesiomorphic for Digitaria. Inconspicuous rachilla
internodes (Fig. 5B) are synapomorphic for a large clade which
includes the typical species D. sanguinalis and other common
weeds like D. ciliaris (Fig. 4C). An elongate first rachilla internode is autapomorphic for D. debilis (Fig. 5C, D), a species
probably related to D. heterantha and clearly nested within the
‘core Digitaria’ clade.
Upper Lemma Shape and Epidermal Features—In
Digitaria, the upper floret is cartilaginous, composed of an
upper lemma with membranous flat margins that embrace
a similar, subequal upper palea (Fig. 6A). The apex of the
upper florets can be obtuse, acute or acuminate (Fig. 6B,
C) and both bracts are visibly striate due to the presence of
rows of epidermal cells, each one containing an excentric
papilla (Fig. 6D). The texture of the upper floret depends
on the characteristics of these epidermal cells, which can
show differences in length and width as well as in the number and depth of lateral indentations. Although acuminate
upper florets seem to have been acquired several times during spikelet diversification in Digitaria, they are possibly
synapomorphic of a clade including most species of sect.
Trichachne. On the other hand, width of the epidermal cells
and depth of the cell wall indentations, as well as the other
continuous characters, were informative at several levels of
the tree topologies.
Caryopsis Dispersal—Many dispersal mechanisms have
been described among the Paniceae, including endozoochory, adhesive dispersal by animals, ant dispersal, and wind
319
Fig. 5. Spikelets showing rachilla internodes and bract insertion.
SEM photographs. A–B, D. Spikelet view in longitudinal section showing rachilla internodes: A. Conspicuous internodes [D. similis, Hitchcock
9008 (US)]. Bar = 200 µm. B. Inconspicuous internodes [D. ciliaris, Johnston
683 (US)]. Bar = 200 µm. C. Spikelet showing bracts distantly inserted [D.
debilis, Simon & Williamson 1595 (US)]. Bar = 500 µm. D. Conspicuous internodes [D. debilis, Simon & Williamson 1595 (US)]. Bar = 200 µm. References:
lg. Lower glume; ll. Lower lemma; lp. Lower palea; pe. Pedicel; ra. Rachilla;
uf. Upper flower; ug. Upper glume; ul. Upper lemma; up. Upper palea.
dispersal (Davidse 1987). One syndrome favoring wind dispersal is the production of tumbleweeds through detachment
of the entire inflorescence, as occurring in species of Digitaria,
Panicum, and some less species-rich genera.
Inflorescence tumbleweed species define a well supported
clade composed of members of D. sections Parviglumae and
Pennatae, and D. subg. Leptoloma. In the remaining taxa, the
unit of dispersal is the spikelet. The small size of Digitaria
spikelets and the different hair types and hair distribution
patterns on the bracts seem to be adaptations for wind and
adhesive dispersal (Davidse 1987).
Inflorescence Diversity—The synflorescence of Digitaria usually consists of a main axis and a variable number
of primary branches (“long paraclades”) along the proximal
portion (Rua 2003). Both the primary branches and the distal
portion of the main axis bear grouplets of two, three or more
spikelets or, more rarely, solitary spikelets (‘short paraclades’,
see below). The number of long paraclades and their length
relative to that of the main axis is responsible for the overall
appearance of the inflorescence, which can vary from a more
or less paniculate aspect to a typically digitate one. Therefore,
the genus is appropriately named. Some evolutionary patterns can be traced upon the tree topologies, e.g. diverse
320
SYSTEMATIC BOTANY
Fig. 6. Upper floret. SEM photographs. A. Middle portion, view from
the back of the upper palea. Note membranous and flat margins of the
upper lemma. [D. bonplandii, Hassler 11927 (G)]. Bar = 100 µm. B–C. Upper
middle, view from the back of the upper lemma: B. Apex acute. [D. ternata,
Nicora 8746 (SI)]. Bar = 250 µm. C. Apex acuminate. [D. californica var. villosissima, Parodi 14052 (BAA)]. Bar = 500 µm. D. Upper lemma epidermis
[D. violascens, Dusén 15176 (G)]. Bar = 10 µm. References: pa. Papilla; ul.
Upper lemma; up. Upper palea.
degrees of truncation of the main axis occur in the clade of
D. sanguinalis and relatives, elongation of internodes and pedicels occur among the Pennatae and D. subg. Leptoloma, and
solitary as well as ternate spikelets arose from plesiomorphic
binate short paraclades. The morphological diversification of
inflorescences in Digitaria will be extensively revisited in an
ongoing paper (G. H. Rua and A. S. Vega, unpubl. results).
Spikelet Grouping—The spikelets of Digitaria can be solitary (Fig. 7A) or, more usually, grouped in pairs (Fig. 7B)
or triads/tetrads (Fig. 7C), arranged as ‘short paraclades’
(Weberling et al. 1993) along the main axis and the primary
branches of the inflorescences.
As stated above, Hackel (1901) divided the genus in three
series, according to spikelet grouping. Binate spikelets are
plesiomorphic within Digitaria. Single, sessile spikelets occur
in a few species (Henrard’s subgenus Solitaria), of which only
one species was included in our analysis. They are clearly
apomorphic within the genus and they seem to have evolved
from binate spikelets through reduction. Short paraclades
composed of three or more spikelets are also apomorphic,
and they seem to have arisen at least two times during inflorescence diversification, although a unique acquisition of this
character was favored under k = 18.2–19.5.
Leaf Anatomy Features—Leaf anatomy has been fragmentarily studied in the genus Digitaria (Rúgolo de Agrasar
and Sánchez 1989). Anatomical studies have referred to leaf
blades in transverse section, epidermis in paradermal view,
and features related to the type of photosynthetic pathway
(Metcalfe 1960; Ellis 1977; Brown 1977; Webster 1983, 1987;
Renvoize 1987; Rúgolo deAgrasar and Sánchez 1989). The typical
photosynthetic pathway among Digitaria species is C4 NADP-
[Volume 34
Fig. 7. A–C. Spikelet grouping. Portion of the main axis bearing short
paracladia composed of 1–4 axes of successive branching order. SEM photographs. A. Solitary spikelets [D. mariannensis, Metzner 45 a (L)]. Bar = 0.3
mm. B. In pairs, composed of one subsessile and other pedicellate young
spikelets [D. sacchariflora, Rua et al. 34 (BAA)]. Bar = 0.5 mm. C. In triads or
more: one subsessile and three pedicellate young spikelets. [D. phaeotrix,
Rua s.n. (BAA 22205)]. Bar = 0.25 mm. References: ss. Solitary spikelet; su.
Subsessile spikelet; ps. Pedicellate spikelet.
ME. Ellis (1977) doubtfully mentioned two African species
representative of D. sect. Flaccidulae as possible PCK species
(one, D. nitens, was included here), based on the absence of
Kranz sheaths in lateral primary bundles and their progressive development toward the median bundle. This characteristic is not typical of PCK type species (Hattersley 1987).
The PCK photosynthetic pathway is apparently restricted to
a clade of Paniceae containing Urochloa and related genera
(Giussani et al. 2001), and Digitaria sect. Flaccidulae is probably
not closely related. Other anatomical leaf characters included
in our analysis were highly homoplastic.
Growth Form Features—The growth form of a plant is
determined by a particular combination of vegetative features
(Mühlberg 1967; Meusel 1970; Rua and Gróttola 1997), some
of which are frequently underscored in taxonomic treatments.
Ancestral growth form reconstruction includes perenniality,
short rhizomes sheltered by cataphylls, and erect culms, i.e.
a character syndrome for Digitaria sect. Trichachne (Rua 2003).
Annuality is apomorphic in Digitaria, and restricted to members of the [Digitaria + Ternatae] clade (Fig. 4D), as well as
lacking cataphylls, whereas decumbent or creeping culms are
synapomorphic for the core-Digitaria.
Although our analysis allow us to gain some insight into the
evolution of morphological characters in Digitaria, character
evolution hypotheses should be considered cautiously until
they can be tested by a phylogeny using molecular data.
Acknowledgments. We are indebted to the curators of the herbaria
for making the material available, to J. Marcos Mirande for kindly making
available his unpublished TNT script, to Florencia Agrasar for language
assistance, and to Gabriela Zarlavsky for anatomical preparations. This
work received financial support through grants UBACyT G027/2001-2002
2009]
VEGA ET AL.: PHYLOGENY OF DIGITARIA
and G105/2004-2007. ASV, GHR, and ZERA are members of the “Carrera
del Investigador” of the “Consejo Nacional de Investigaciones Científicas
y Técnicas (CONICET)”, Argentina.
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Appendix 1. Taxa of Digitaria and outgroups considered in this
study including at least one representative specimen used for anatomical observations.
Anthaenantia lanata (Kunth) Benth., G. H. Rua & Boccaloni 151 (BAA
22785). Echinochloa pyramidalis (Lam.) Hitchc. & Chase, G. H. Rua s.n. (BAA
22207). Panicum repens L., G. H. Rua et al. 270 (BAA 22959). Urochloa brizantha (Hochst. ex A. Rich.) R. D. Webster, G. H. Rua et al. 68 (BAA 22682).
Digitaria abyssinica (Hochst. ex A. Rich.) Stapf, R. Pohl 11386 (US). D. aequiglumis (Hack. & Arechav.) Parodi, A. Da Silva 2520 (BAA). D. ammophila
(F. Muell.) Hughes, Thompson GAL191 (CANB). D. angolensis Rendle, M.
Reekmans 9850 (BAA). D. arenicola (Swallen) Beetle, J. Swallen 10588 (US).
D. argillacea (Hitchc. & Chase) Fernald, J. Reeder & C. Reeder 4445 (US).
D. argyrostachya (Steud.) Fernald, W. Harris 11413 (US 755154). D. argyrotricha (Anderss.) Chiov., G. H. Rua 526 (BAA). D. atra Luces emend A. S. Vega
& Rúgolo, Müller s.n. (VEN 222492). D. badia (Scribn. & Merr.) Fernald, G.
& J. Davidse 9904 (BAA). D. balansae Henrard, G. Davidse et al. 11001 (MO).
D. bicornis (Lam.) Roem. & Schult., G. H. Rua et al. 272 (BAA); G. H. Rua
et al. 561 (BAA). D. bonplandii Henrard, Gottsberger 1021-80R-16371 (MO).
D. botriostachya Stapf, A. McKinnon S. 65 (UB). D. brownii (Roem. & Schult.)
Hughes, R. Roe 502 (CANB); R. Pullen & Galore 4688 (CANB). D. californica (Benth.) Henrard, L. R. Parodi 13982 (BAA). D. catamarcensis Rúgolo,
T. Killeen 1571 (SI). D. cayoensis Swallen, C. L. Lundell 6670 (K, US).
D. chaseae Henrard, A. Chase 10764 (US). D. ciliaris (Retz.) Koeler, Vera
Santos 7561 (L). D. coenicola (F. Muell.) Hughes, W. Moir s.n. (CANB). D. cognata (Schult.) Pilg., J. Lerew Kan-2-175 (US). D. curvinervis (Hack.) Fernald,
E. Ekman 1049 (AAU, C, K, P). D. debilis (Desf.) Willd., Sampaio s.n. (WU
2071). D. diagonalis (Nees) Stapf, G. H. Rua 536 (BAA). D. divaricatissima
(R. Br.) Hughes, C. Hubbard 5350 (CANB); C. Hubbard 5071 (CANB).
D. eggersii (Hack.) Henrard, Proctor 48361 (SJ, US). D. eriantha Steud.,
[Volume 34
Z. Rúgolo 2118 (SI). D. eriostachya Mez, B. Rosengurtt 5461 (BAA). D. fragilis (Steud.) Luces, A. Chase 10833 (MO). D. fuscescens (J. Presl) Henrard,
Sarmento s.n. (BAA). D. gazensis Rendle, G. Davidse et al. 6515 (BAA).
D. gerdesii (Hack.) Parodi, G. Davidse et al. 11385 (MO). D. gymnostachys Pilg.,
K. L. Tinley 598 (PRE); R. P. Ellis 3644 (PRE). D. heterantha (Hook. f.) Merr.,
Kondo & Edaño s.n. Phil. Nat. Herb. 36605 (L). D. hitchcockii (Chase) Stuck.,
J. Roybal 48 (US 1935901). D. horizontalis Willd., G. H. Rua et al. 72 (BAA).
D. insularis (L.) Fedde, Krapovickas & Schinini 31450 (BAA). D. junghuhniana (Nees ex Steud.) Henrard, Kievih 1701 (L). D. katangensis Robyns,
M. Reekmans 5954 (BAA). D. laxa (Rchb.) Parodi, T. Meyer 2562 (BAA).
D. lecardii (Pilg.) Stapf, Meinzingen & Conert 549 (LIL). D. leiantha (Hack.)
Parodi, A. Schinini et al. 8322 (BAA, LIL). D. maitlandii Stapf & C. E. Hubb.,
M. Reekmans 6778 (BAA). D. mariannensis Merr., J. Metzner 45 a (L). D. melanochila Stapf, H. Schlieben 4644 (UB). D. minutiflora Stapf, J. Lambinon 78/234
(BAA). D. mollicoma (Kunth) Henrard, Lugd. Batav. s.n. (L). D. monodactyla
(Nees) Stapf, E. van Jaarsveld 83 (PRE). D. nitens Rendle, R. Davies 2951
(SI). D. nodosa Parl., J. Duvigneaud 77 (BAA). D. parviflora (R. Br.) Hughes,
C. Hubbard 5923 (L). D. patens (Swallen) Henrard, E. Bongsch S-214 (US).
D. pearsonii Stapf, P. Ndabaneze 3 (BAA). D. pennata (Hochst.) T. Cooke,
M. Gilbert 1649 (UB). D. perrottetii (Kunth) Stapf, P. Ndabaneze 48 (BAA).
D. phaeotrix (Trin.) Parodi var. hackelii (Arechav.) Henrard, G. H. Rua & I.
B. Boccaloni 159 (BAA). D. pittieri (Hack.) Henrard, P. Standley 35968 (US);
O. Jimenez L. 707 (US). D. pubiflora (Vasey) Wipff, A. S. Hitchcock 5157
(US). D. sacchariflora (Nees) Henrard, Seidel 2704 (SI); G. H. Rua et al. 34
(BAA). D. sanguinalis (L.) Scop., G. H. Rua s.n. (BAA 24590). D. similis
Beetle ex Gould, Seidel & Vargas 2119 (SI). D. swalleniana Henrard, A. Schulz
4013 (CTES). D. tenuis (Nees) Henrard, R. Smith 5313 (VEN). D. ternata
(A. Rich.) Stapf, G. H. Rua 525 (BAA). D. thouaresiana (Flüggé) Camus,
M. Reekmans 9945 (BAA). D. violascens Link, A. Chase 8520 (BAA).
Appendix 2.
analysis.
Morphological characters used for phylogenetic
1. Inflorescence primary branches. 2. Depth of epidermal cell indentations. 3. Epidermal cell width. 4. Spikelet length [mm]. 5. Spikelet-width
[mm]. 6. Anther length [mm]. 7. Spikelet, hair apex: not dilated [0], slightly
dilated [1], dilated (claviform hairs) [2]. 8. Spikelet, hair apex: acute [0],
apiculate-rounded [1], rounded [2]. 9. Spikelet, hair walls: smooth [0], verrucose [1]. 10. Spikelet, hair apex: straight [0], recurved [1]. 11. Spikelet,
hair length: up to 2 mm [0], 3-5 mm [1]. 12. Spikelet, hair pigmentation:
silver-white [0], isabelline [1], brownish [2]. 13. Spikelet, purple-tinged
hairs: wanting [0], present [1]. 14. Spikelet, first rachilla internode: elongated [0], inconspicuous [1]. 15. Spikelet, second rachilla internode: elongated [0], inconspicuous [1]. 16. Spikelet position: Upper lemma abaxial
[0], Upper lemma adaxial [1]. 17. Spikelet compression: biconvex [0], plano-convex [1], dorsiventrally flattened [2]. 18. Lower glume, whether
present or not: wanting [0], present [1]. 19. Lower glume, shape: truncate,
reduced to a rim [0], ovate, acute [1], obtuse [2], bi-lobed, very short and
tiny [3]. 20. Lower glume, margins: not clasping [0], stem-clasping at the
base [1], clasping, with overlapping margins [2]. 21. Lower glume texture:
membranous [0], hyaline [1]. 22. Lower glume, number of nerves: manynerved [0], 3-nerved [1], without nerves [2]. 23. Upper glume, number of
lateral veins on each glume half: 0 [0], 1 [1], 2 [2], 3 or more [3]. 24. Upper
glume, apex: acuminate [0], acute [1], obtuse [2]. 25. Upper glume, relative
length: obsolete [0], shorter than the lower lemma [1], (sub)equal to the
lower lemma [2], longer than the lower lemma [3]. 26. Upper glume, relative width: wider than the upper floret, the glume covers the upper floret
sides [0], narrower than the upper floret (upper floret laterally visible) [1].
27. Upper glume indumentum: wanting [0], present [1]. 28. Upper glume,
distribution of indumentum: pilose throughout [0], alternate, inner
internervial spaces pilose [1], pilose between margins and outer veins,
otherwise glabrous [2], alternate, inner internervial spaces glabrous [3],
distal portion pilose [4]. 29. Upper glume, scabrousness of nerves: smooth
[0], scabrous [1]. 30. Upper glume, distribution of nerves: equidistant [0],
unequidistant, lateral nerves contiguous [1]. 31. Upper glume, distal convergence of lateral nerves: not convergent [0], convergent [1]. 32. Lower
lemma, number of lateral veins on each lemma half: 1 [0], 2 [1], 3 [2], 4 or
more [3]. 33. Lower lemma, apex: acuminate [0], acute [1], obtuse [2], apiculate [3]. 34. Lower lemma, texture: papyraceous [0], membranous [1],
hyaline [2], cartilaginous [3]. 35. Lower lemma, indumentum: wanting [0],
present [1]. 36. Lower lemma, distribution of indumentum: pilose between
margins and outer veins, otherwise glabrous [0], alternate, inner internervial space glabrous [1], inner internervial space glabrous, otherwise pilose
[2], all internervial spaces fringed with hairs [3], pilose throughout [4]. 37.
Lower lemma, scabrousness of nerves: smooth [0], scabrous [1]. 38. Lower
2009]
VEGA ET AL.: PHYLOGENY OF DIGITARIA
lemma, pectinate bristles: lacking [0], present in subsessile and pedicellate
spikelets [1], present in pedicellate spikelets only [2]. 39. Lower lemma,
vein distribution: equidistant [0], unequidistant, lateral nerves contiguous
[1], unequidistant, three central nerves contiguous [2]. 40. Lower lemma,
distal convergence of lateral veins: not convergent [0], convergent [1]. 41.
Lower lemma, axillary flower: lacking [0], reduced to a palea [1], malefertile [2]. 42. Upper floret, abscission: not occurring [0], occurring [1]. 43.
Upper floret, lemma apex: closed [0], open [1]. 44. Upper floret, lemma
texture: membranous [0], cartilaginous with membranous margins [1],
crustaceous [2]. 45. Upper floret, lemma and palea surface: smooth [0],
papillose [1]. 46. Upper floret, disposition of lemma margins: enrolled
around the palea [0], folded upon the palea [1]. 47. Upper floret, short, stiff
prickles towards lemma apex: wanting [0], present [1]. 48. Upper floret,
pigmentation at maturity: stramineous to ochraceous [0], brown [1], dark
purple [2]. 49. Upper floret, relative length: longer than the lower lemma
[0], (sub)equal to the lower lemma [1], shorter than the lower lemma [2].
50. Upper floret, apex: acute [0], acuminate [1], obtuse [2], apiculate [3]. 51.
Upper floret, nerves of the upper lemma: 3 nerves distinguishable [0], 5
nerves distinguishable [1], 7 nerves distinguishable [2]. 52. Flower, pigmentation of anthers: yellow [0], purplish [1]. 53. Flower, pigmentation of
stigmata: pale [0], purplish [1]. 54. Caryopsis, outline: elliptical/oblong
[0], obovate [1], orbicular [2]. 55. Caryopsis, pigmentation: pale [0], brown
[1]. 56. Reproduction, cleistogamy: none [0], occurring [1]. 57. Inflorescence,
distribution of LPc along the main axis: racemes always alternate [0],
proximal racemes (frequently) verticillate [1], distal racemes conjugate,
otherwise alternate [2]. 58. Inflorescence, relative length of primary order
branches: decreasing towards apex [0], about the same length throughout
[1], longer at the middle, inflorescence fusiform [2]. 59. Inflorescence,
length of racemes relative to main axis: racemes not reaching the apex [0],
the lowermost racemes (almost) reaching the apex [1], racemes overtopping the apex [2]. 60. Inflorescence, orientation of LPc: ascending [0],
spreading [1], rigidly horizontal [2]. 61. Inflorescence abscission as tumbleweed: not occurring [0], occurring [1]. 62. Inflorescence, homogenization: paniculate [0], proximally paniculate, homogenized distally [1], kPc
homogeneous throughout [2]. 63. Inflorescence, main florescence (= terminal spikelet) and distal kPc: wanting [0], present [1]. 64. Inflorescence, long
paraclades: wanting [0], present [1]. 65. Inflorescence, phyllotaxis: distichous [0], polystichous [1]. 66. Inflorescence, second order long paraclades:
wanting (occasionally a reduced secondary LPc on the proximal raceme)
[0], regularly present [1]. 67. Inflorescence, pulvini at the base of racemes:
inconspicuous (lacking?) [0], conspicuous, bulky [1]. 68. Inflorescence,
pulvini at the base of pedicels: lacking [0], present [1]. 69. Inflorescence,
peduncle indumentum: glabrous [0], distally hirsute [1], hirsute throughout [2]. 70. Inflorescence, rachis of racemes: trichetrous [0], narrowly
winged [1]. 71. Inflorescence, rachis indumentum: glabrous to scabrous
[0], hirsute [1], ventrally pubescent [2]. 72. Inflorescence, pedicel development: very brief, spikelets subsessile [0], developed, normal [1], extraordinarily developed [2]. 73. Inflorescence, pedicel indumentum: glabrescent
[0], scabrous to antrorse-echinulate (more-than-scabrous) [1], puberulous
[2], hirsute/ciliolate [3]. 74. Inflorescence, pedicel apex (sensu Webster
1983): truncate [0], cupuliform [1], discoid [2]. 75. Inflorescence, coronula
at the apex of pedicels: lacking [0], composed of short hairs [1], composed
of long cilia [2]. 76. Inflorescence, (the more frequent) number of spikelets
per node: one [0], two [1], three or more [2]. 77. Inflorescence, pedicel con-
323
crescence: pedicels free [0], pedicels concrescent with the rachis [1]. 78.
Inflorescence, whether (sub)sessile or pedunculate racemes: (sub)sessile
[0], with long peduncles [1]. 79. Inflorescence, relative length of raceme
internodes: short (less than twice the length of the spikelets) [0], long
(more than twice the length of the spikelets) [1]. 80. Growth form, life
cycle: annual [0], perennial [1]. 81. Growth form, branching of culms:
unbranched [0], branched [1]. 82. Growth form, growth direction of culms:
orthotropous to geniculate [0], decumbent [1], plainly plagiotropous,
stoloniferous [2]. 83. Growth form, internode indumentum: glabrous [0],
distally hirsute [1]. 84. Growth form, stypochitum: wanting [0], present
[1]. 85. Growth form, leaf sequence along tillers: the prophyll is followed
by cataphylls [0], the prophyll if followed by foliage leaves [1]. 86. Leaves,
pubescence of cataphylls: glabrous [0], pubescent [1]. 87. Growth form,
direction of growth in the innovation zone: orthotropous [0], mainly
orthotropous, but shortly plagiotropous proximally [1], plainly plagiotropous [2]. 88. Growth form, rhizome internodes: all internodes short [0],
elongated in the plagiotropous portion, distally shortened [1], all elongated [2]. 89. Growth form, accessory innovation zones along the culm:
lacking [0], present [1]. 90. Growth form, transition from short to long
internodes: abrupt [0], gradual [1]. 91. Growth form, culm internodes: hollow [0], solid [1]. 92. Leaves, leaf sheath indumentum: glabrous [0], pubescent/pilose [1]. 93. Leaves, prefoliation: convolute [0], conduplicate [1].
94. Leaves, indumentum of the ligular region: glabrous [0], hirsute/pubescent [1]. 95. Leaves, ligule outline: truncate [0], acute [1], obtuse [2]. 96.
Leaves, ligule margin: entire [0], irregular, erose [1]. 97. Leaves, type of
ligule: entirely membranous [0], membranous with a ciliate margin [1],
ciliate, without a conspicuous membranous portion [2]. 98. Leaves, ligule
development: well developed, conspicuous [0], reduced to an inconspicuous ridge [1]. 99. Leaves, leaf blade outline: narrowly lanceolate, acuminate [0], lanceolate [1], filiform [2]. 100. Leaves, leaf blade consistence:
papiraceous [0], coriaceous [1]. 101. Leaves, mature leaf blade exposition:
plane [0], involute [1]. 102. Leaf anatomy, midrib: differentiate, distinct [0],
undifferentiate [1]. 103. Leaf anatomy, adaxial papillae: lacking [0], present [1]. 104. Leaf anatomy, adaxial prickles on rib zones: lacking [0], present [1]. 105. Leaf anatomy, abaxial prickles on rib zones: lacking [0], present
[1]. 106. Leaf anatomy, differentiation of costal and intercostal adaxial
regions: undifferentiate [0], slightly noticeable [1], noteworthy [2]. 107.
Leaf anatomy, differentiation of costal and intercostal abaxial regions:
undifferentiate [0], slightly noticeable [1], noteworthy [2]. 108. Leaf anatomy, location of bulliform cells: only adaxial [0], both adaxial and abaxial
[1]. 109. Leaf anatomy, colorless parenchyma associated to midrib: adaxial
[0], both adaxial and abaxial [1], none [2]. 110. Leaf anatomy, macrohairs:
lacking [0], present [1]. 111. Leaf anatomy, crystals in chlorenchymatous
cells: lacking [0], present [1]. 112. Leaf anatomy, abaxial microhairs: lacking [0], present [1]. 113. Leaf anatomy, adaxial microhairs: lacking [0],
present [1]. 114. Leaf anatomy, chlorenchyma arrangement: diffuse [0],
radiate [1]. 115. Leaf anatomy, cell layers forming radiate chlorenchyma:
one layer [0], more than one [1]. 116. Leaf anatomy, shape of chlorenchymatous cells: tabular [0], isodiametric [1]. 117. Leaf anatomy, chlorenchymatous cells between radiate chlorenchyma: lacking, radiate chlorenchyma
of contiguous bundles in contact [0], present, separating radiate chlorenchyma of contiguous bundles [1]. 118. Leaf anatomy, abaxial papillae:
lacking [0], present [1]. 119. Leaf anatomy, photosynthetic pathway: C3 [0],
NADPme [1], PCK or PCK-like NADme [2].