The Phylogenetic Utility of Lemmatal Micromorphology in Leptochloa S. L. an Related Genera in Subtribe Eleusininae (Poaceae, Chloridoideae, Eragrostideae)

26 Pages·1996·20.8 MB·

by  Neil Snow

THE
PHYLOGENETIC
Neil Snow^
LEMMATAL
UTILITY OF
MICROMORPHOLOGY
IN
LEPTOCHLOA AND
S.L.
RELATED GENERA
IN
SUBTRIBE
ELEUSININAE
(POACEAE,
CHLORIDOIDEAE,
ERAGROSTIDEAE)^
Abstract
Micromorphological lemma
features of the were
investigated in the suhtribe Eleusininae (Poaceae) using scanning
electron microscopy. Ninety-two taxa were studied, which included 48 genera and
all currently recognized species of
lA>ptochloa S.I. All species of Uptochloa and a majority of genera in Eleusininae have cork cells, hut silica cells are
mostly ahsent in IjpptoMoa and most related genera Eleusininae. Enneapogonoid-type
in microhairs
are reported
for
Cladoraphis cyperoides and Psammagrostis
wiseana, representing only the second report Eleusininae. Although
in
bicellular microhairs occur most
in taxa. variations in microhair type, coupled with the occurrence of partitioning
membranes, them
give supra-specific phylogenelic utility. The occurrence of papillae on short and long
cells varies
within [j^piochloa and between
genera. Prickles are ubiquitous in Leptothloa and most related genera, Macrohairs are
present in all sj»ecies of Ij'ptochloa but a[>sent in some related genera. Clavicorniculate macrohairs are reported
for
one species eadi of Lt^ptochloa and Coelarhyninu and a corniculate macrohair was A
observed Cyrwdon.
in crispate
macrohair occurring in three species of Coelachynim is described for the first time and probably represents a syn-
apomorphy
The
in that genus. analysis oi Uptochloa suggests that micromorphological characters vary within a
little
genus, and thus have
the potential to ser\'e as phylogcnctic markers at the generic level. Uncertainty concerning the
homologous
relationships of papillae, hooks, prickles, and macrohairs is discussed in light of this study and previous
literature.
Resumen
Las
caracterfsticas micromorfol6gicas de la lenm en la sublribu Eleusininae (Poaceae) se examinaron utilizando
microscopfa electr6nica de barrido. Se estudiaron 92 taxa. 48 g^neros, y todas las especies de Leptochloa liasta ahora
reconocidas. Todas
las especies de Leptochloa y la mayorfa de los g^neros de Eleusininae tienen c^lulas suberificadas,
pero
las c^lulas silicfferas estdn ausentes en lA'ptochloa y en la mayorfa de los taxa de Eleusininae. Se reporta por
segunda
vez en Eleusininae la presencia de microjielos bicelulares de enneapogonoid
tipo para Cladoraphis cyperoides
Psammagrostis
wiseana. Auntjue micropelos
y los bicelulares se j)resentan en casi todos los taxa, variaciones en
el
de
tipo micropclo, junto con la presencia de membranas dlvisorlas les dan valor diagn6stico para estudios filogen^ticos
supraespecfficos. La presencia de papilas de c^lulas corlas y estrechas es variable en Leptochloa entre los otros
y
g^neros. Los aguijones se encuentran en todas especies de
las Ijeptochloa mayorfa de g^neros
y la los relacionados.
Los macropelos
estdn generalmente presentes en todas las especies de Ijeptochloa pero estdn ausentes en algunos taxa
relacionados. Se reportan macropelos clavicorniculados para un especie de ambos generos Leptochloa Coelaehyrum,
y
un macropelo
y corniculado se reporta para Cynodou. Un macropelo crispado en especies de Coelachyrum
tres es
descrilo por primera vez, y quizd represente una sinapomorffa de cierto nivel en ese g^nero. El andlisis de Leptochloa
que
indica
las caracterfsticas micromorfolr)gicas varfan poco, por tanto tienen valor para estudios filogen^ticos su-
y
La
praespecfficos. dificullad sobre las relaciones homologas de papilas. ganchos. aguijones, macrotricomas se discule
y
con base a lo halhulo en este estudio con datos anteriores de
y la literatura.
Cladistic eistirnationsof pliylogenctic history with easily defined character This tendency may
states.
morphological characters tend
to favor the use of reflect the potential pitfalls discussed by Chappill
distinct qualitative characters, or those possessing and Stevens
(1989) (1991) in the uncriti(^al use of
Mike
^ Veith facilitated the work with assistance at the Electron Microscopy Laboratory Washington University
at
I
thank the curators of B, BM, BHI, CANB, MO, PRE, and US for sending loans and granting pemiission sample
for lo
directly from herbarium specimens. Hatch an
S. sent original version of Morden's dissertation, and helpful discussions
Ann. Missouri Bot. Card. 504^529.
83: 1996.
Snow 505
Number
Volume 4
83,
Lemmatal Micromorphology
1996
Used documented thoroughly (Kaufman 1969;
quantitative characters (but see Thiele, 1993). et al.,
Kaufman 1970) and are evident in grass fos-
and due the perception of high levels of et al.,
alone, to
morphology have of Mi 1984)
homoplasy, characters of gross sils
been considered inadequate as phylogenetic mark- elongation of long cells follows the initial differ-
&
(Kaufman
and
ers in the grass family (Thomasson, 1978; Hilu entiation of long cells short cells et
& &
Campbell, 1987; Davis 1969; Kaufman 1970). In addition to
Wright, 1982; Kellogg et al.,
al.,
Soreng, 1993; Clark et al, 1995). Not surprisingly, their extended length, long cells (unlike short cells)
revisionary studies of grasses are turning to micro- frequently have sinuous margins (Metcalfe, 1960;
&
Chen
morphological characters for additional phyloge- Clifford Watson, 1977; Ellis, 1979; et al.,
and
between long
However, the distinction
netic data. 1993).
Thomasson
Epidermal micromorphological characters of always absolute.
short cells not
is
have systematic value between the ranks of long identifiable by
grasses (1978: Id) illustrated cells,
fig.
subfamily and species (Prat, 1932; Tateoka et al., sinuous margins, having similar dimensions to
{[^^
1959; Metcalfe, 1960; Ellis, 1979). Descriptive short cells for a fossilized species of the genus A^a5-
studies of micromorphological features in grasses (t^be Stipeae). The two types of short cells
^^//^
1932;
have focused on the surfaces of the leaf (Prat, recognized are cork cells (sometimes called suberin
&
summary 1976; see also Morden Hatch, (Kaufman
in Ellis, which accumulate suberin et al.,
eells),
& &
Annable,
1987; Ddvila Clark, 1990; Peterson which accumulate
^^d silica
^979)^ silica cells,
Chen
1990; Barker, 1993; Scholz, 1993; et al.,
observed bodies.
j^^^ readily silica
glumes (Lucas, 1979; Molina, 1993), the
1993), require
Microhairs are bicellular structures that
lemma Thomasson, 1986; Peterson,
(Hsu, 1965;
^h magnification for detection (Tateoka et al.,
&
1990;
1989; Soderstrom Zuloaga, 1989; Kellogg,
condition
1959). (For exceptions to the bicellular
&
&
Valdes-Reyna
Zuloaga Judziewicz, 1991;
and Zu-
Dahlgren 1985; Renvoize, 1985;
see al,
et
Hatch, 1991; Naredo et al., 1993; Ball et al., 1993), j^^^^ ^^ ^^^ jggg ^j^^^ ^^^ present throughout the
-^
&
(summary Consaul Aiken, 1993: &
and palea
in
^^^^^ ^^^^p^ subfamily PooiJeae (Johnston
j^^
micromor-
The phylogenetic application of
1651).
1975) Microhairs have teen classified as
^^^g^j^^
phological characters has been more limited (Pe-
"enneapogonoid,"
-^hloridoid," "panicoid," or
&
&
Annable, 1992; Barker, 1993; Visser
terson
1959;
^^^^^ ^^ typological variants (Tateoka et al.,
1994; Guala, 1995).
Spies,
1988
Only ontological status as a
1992). rarely their
is
An Overview Micromorphological
of
character uncertain. For example, as dis-
distinct
Characters
cussed by Barker the "long slender papil-
(1993),
common
&
l^e" (Clayton Renvoize, 1986: 165) to
micromorphological char-
Several categories of
genera Arundinoideae, given that they
several in
have been recognized. Short cells (which in-
acters
are reported to occasionally have the remains of a
and long bicel-
elude cork cells silica cells), cells,
may be
^^^all apical cell (Renvoize, 1986: 328),
and
microhairs, papillae, hooks, prickles,
lular
icroh
interpretable airs.
examples micromorphological
macrohairs are of
all
processes
Papillae are short, undifferentiated
characters (Metcalfe, 1960; Ellis, 1979). (See Ellis,
summary terms hooks that arise from the outer cell wall.
1979, for a of alternative for
Hooks have been considered processes having a
and
prickles.)
rounded base and an apex that at least slightly
is
Short cells and long cells are readily distin-
recognized as a
and (when pointed (Ellis, 1979), but are not
guished on the basis of relative size,
may synapomorphy category In this study (see Discussion). Prickles are
both are present) constitute a
and Poaceae Doyle basally swollen processes having short, sharp api-
uniting Joinvilleaceae (see also
& The ces that typically point toward the apex of the struc-
1992; Kellogg Linder, 1995). differ-
et al.,
ences between short cells and long cells have been ture
(1
Columbus
were provided by Filgueiras, D. Nicolson, G. L. Stebbins, aiiJ F. Zuloaga. The careful reviews of J. T.
T.
Spanish.
and G. Davidse improved the manuscript significantly F. Lorea assisted with preparation of the abstract in
Wash-
Garden (Andrew W. Mellon Foundation);
acknowledged Missouri Botanical
Financial support gratefully from:
is
Louis (Evolutionary & Population Biology Program); and the American Society of Plant Taxono-
ington University,
St.
and
This paper represents a portion of a doctoral dissertation to be submitted to the Graduate School of Arts
mists.
Sciences, Washington University Louis).
(St.
,
and Missouri
Department PO. Box 1137, Louis» Missouri 63130, U.S.A.,
^Washington University, of Biology, St.
Garden, PO. Box 299, Louis, Missouri 63166, U.S.A.
Botanical St.
506
Annals
of the
Missouri Botanical Garden
Macrohairs
arc generally unicellular structures with uncertain phylogenetic
affinity (Dalilgren
et
&
(but see Kabuye Wood, 1969) visible to the na- al., 1985; K(>]logg & Campbell, 1987; Doyle
et
al..
ked eye &
1992; Davis Soreng, 1993; Barker 1995;
et al..
Among
lemniatal niicromorphological &
structures, Clark 1995; Kellogg The
et al., Linder, 1995).
only niicTohairs have been
not reported to accu- subfamily Chloridoideae Rouy has about 13(X) spe-
mulate The
silica. presence of silica has been re- cies, which tend occupy warmer
to dry, climates
ported cork (Kaufman &
for cells et al., 1972); long (Hartley Slater, 1960). (Taxonomic concepts
fol-
&
&
cells (Ball et al., 1993); papillae (Terrell Wergin, low Clayton Renvoize, The
1986.) largest
tribe,
&
1981; Consaul Aiken,
1993); prickles (Soni Eragrostideae 80
et Stapf, has about genera and 1000
Kaufman
1970; 1972
al., et al., (as "trichomes"); species. Within Eragrostideae, the most diverse
& &
Terrell Wergin, 1981; Valdes-Reytia Hatch,
subtribe Eleusininae Dumort, and
is only the high-
1991; Ball et 1993); and macrohairs (Consaul
al., est latitudes arc excluded from the overall range of
&
Aiken,
1993). (Stomata occasionally occur on approximately 55
its genera. Relatively few genera
lemmas. They
are
sufficiently infrequent in the taxa in Eleusininae occur outside of a single continent
examined
thus far to be considered an abnormal Coelachyrum,
(e.g., Eragrostis, Leptochloa,
Irichn-
constituent lemma.
of the In a study of the leaf of neura, disregarding minor
exceptions and a few
Kaufman
Avena,
et al. (1972) were unable to find cosmopolitan weeds). Excluding
Eragrostis, with
its
silica in stomatal cells.) approximately 350 &
species
(Clayton Renvoize,
&
1986; Van den Borre Watson, most
1994), of the
Overview Lemma
of
MiCROMOFii'iii.ocY approximately 600
species in the subtribe occur
in
Up-
The lemma '"^^^»'^''1>' ^'"^'^ g^'"'"-^ (10 species or fewer).
is the lower of two bracts that (usu-
worldwide genus
^^''" ^*'^"''- "^^'^^
subtend each The ^- '" ^ <,f
ally) flower in grasses. upper
^f
many
^^"'"* ^'thougH continue
seg-
to
bract (the palea) not homologous lemma 'P*''^*^"'
the
is to
'"^f
the genus Dlplachne
(McNeill, 1979; Phil-
The lemma r^at*'
(Clifford, 1987).
a transformational
is
^
^^^^- ^'^''"" Simon,
D^^'^i'^' 1992; 1993;
homology
serial (de Pinna, 1991) of the leaf by
vir-
''I*''
^•''""'
l^^-"^)-
tue of "ontogenetic
its individualization" (sensu
mlergenenc
studies Eleusininae
^*-''''"* in
dif-
Wagner, 1989a, from
b) the leaf (Pfiilipson, 1934;
characters, and meth-
'" '^'^'^''^' analytical
Tran, 1973; Kellogg,
1990). transfonnational ^^ff
Its
^^u-h hampers
^^^^"g'*'^' meaningful comparisons
derivation from the leaf supported by rare
is ata-
&
between
the results (Phillips, 1982; Hilu
Wrijrht,
'^
•
progenit,or hI aving ^
afl
\ } ' ,^,^^
'
& . .
1982; Campbell, 1985; Hilu Esen, 1993; Duvall
sheath, ligule, and blade (Philipsou, dim-
1934),
its
""^ ^'•' ^'^^'^^- ^^'"^ 1"*"'*'"" '*'' '" »'»' g^'-
inuitive size relative to regular leaves, restricted ^P^''^-'^^^'^
its
"^"'' arrangement of Clayton and Renvoize
(1986:
occurrence
in the inflorescence, the occasional
non-mutually
exclusive
possi-
presence of Icmmatal stomata (common j"^^' '"S^"^"*" ^^''''''
to the leaf),
many
^7''''- leptochloa has close generic
and ^^> '''^'
the frequent
infraspecific differences of micro-
""^^l^^f';^^', that U-ptochloa^ evolutionarily basal
(2) is
morphological features between and lemma
the leaf
& to related genera, and that Leptochloa may be
(Thomasson, (3)
1978: 977; Terrell Wergin. 1981:
paraphyletic The
as currently recognized. mono-
706
^^'* chloridoid groups, ineluding Upto-
^'^^^^
The most "extensive work on lenuna ''^
micrornor-
'''^"'^'"' untested.
^^'^'''^
phology
Eleusininae was
in that of Vakles-Reyna
'^'^Z''
The
purpose
of this paper create a more
is to
and Hatch
(1991). Their sur\ey Eragrostideae
in of
^'^^ensive data set for inferring phylogenetic-
rela-
57
species (representing 30 genera) suggested such
^lonships in L-ptochloa and Chloridoideae (Snow,
characters might be
useful phylogenetic markers
in
^^^itio"' terminological
^" inconsisten-
the subtribe Eleusininae. This study extemled '" P'^f"'^'
U.eir
'ies throughout the literature, coupled with
re-
generic survey of niicromorphoh)gy (Valdes-Reyna tl
y'
& '"^*' ^^^'^ q"*'^''"" "'c onto-
Hatch, 1991) to include genera of Eleusininae '*'''^'"' I"""^'^*^ ^ '"
^''^*"' "*^ '^"^''^^ characters, and suggest the
^''^^
not previously examine<l, including a few other gen-
"'^^^'^ ^"' ^ ^''"*'^' reevaluation of the characters,
era and
in Chlori.loideae, to characterize these fea-
tures for all species in Leptochloa.
Material and Methods
An Overview
of the Svstematics of
The
lemma
adaxial surface of the was studied
f
ClILORrnOIDEAE
92
taxa using scanning electron microscopy (SEM)
The
composed
grasses are of at least four mono- the Electron Microscopy
at Lahorafor>' Washing-
at
phyletic suhfamilies and number
contain a of tribes ton University (Apj)endix Samples were
1). re-
Snow 507
Number
Volume 4
83,
Lemmatal Micromorphology
1996
was
moved from her])anum specimens. To as- (except those with question marks, Table 1)
directly
with a photomicrograph,
semaphorants 1981: verified
sure the use of (Wiley, 119), I
Cork Cork were abundant in the in-
sampled lemmas from splkelets that con- cells. cells
generally
and
mature caryopses. This precaution was Im- tercostal zones in all species of Leptochloa, al-
lained
As was of micro-
portant, because spikelets in early stages of ontog- temated with long cells. true all
when morphological characters studied, their distribution
cny may be present even the inflorescence is
lemma. There
Three specimens could vary significantly on a single
well exserted from the leaf sheath.
decrease
Some samples were was a general tendency for cork cells to
most were observed.
taxa
of
sonicated in xylene for 30 minutes to remove the in frequency near the apex.
Among Desmos-
OET, were absent
cork in
waxes can obscure surface fea- cells
epicuticular that
Ectro-
treatment was not always effective. tachya (Fig. 14), Ectrosia gulliveri (Fig. 17),
tures, but this
Psam-
and
mucronata
being placed on aluminum stubs the speci- siopsis, Odyssea (Fig. 60),
After
Odyssea
E5000 Unlike congener,
magrostis
mens were coated with gold using a Polaron (Fig. 65). its
The Apo-
has cork cork cells of
Samples were observed with 0*" paucinervis cells.
sputter coater. tilt
SEM Halopyrum and Neyraudia
20 kV on a Hitachi S-450 and photo- chiton (Fig. 2), (Fig. 23),
at
com-
graphed using Polaroid 55 positive-negative film. (Fig. 58) were not noticeably darkened, as is
SEM
mon under observation
mature cork
Except Figures 10 and 42. photomicrographs for cells
for all
&
However, since
lemma toward (Valdes-Reyna Hatch, 1991).
have the apex of the directed the
Attempts standardize the scale of photo- their size and location suggested cork cells, they
right. to
were recorded present (Table
micrographs proved unworkable, since various as 1).
OERG
except
Cork cells were present in all
magnifications were necessary.
Valdes-Reyna and Hatch Spartina (not shown). With the exception of a
The from
format
differs
Tragus shown), cork cells
microhairs and macroliairs are in- sparse distribution in (not
(1991) in that
common OERG.
my on were in
eluded, interpretation of papillae short cells
Some had resembling cork cells
different (see Results), and the degree of undu- taxa short cells
is
was and from which other structures could be
lation of the long cells with papillae not re- in size,
Valdes-Reyna and Hatch (1991) discussed seen developing, such as bicellular microhairs (e.g.,
corded.
Diplachne gigantea,
their findings based on four variations of cork cell Bewsia, Fig. 3), prickles (e.g.,
and macro-
occurrence: cork cells adjacent to silica cells; cork Fig. 38, Leptochloa rupestrls. Fig. 48),
L
nee-
Leptochloa fascicularis, Fig. 36,
cells not adjacent to silica cells; cork cells papil- hairs (e.g.,
Many
or cork cells not observed. This study merely sii, Fig. 45). taxa such as Eragrostiella (Fig.
late;
whose
had
and Indopoa short cells
character (present 20) (Fig. 26)
recorded t^ork cells as a binary^
and which were
were rounded
Eleusininae be- outer walls in profile,
or absent). will refer to taxa in
I
become
"Other Eleusininae Taxa" ontogenetically destined to cork cells. (Val-
Leptochloa as
sides
&
des-Reyna Hatch (1991: 536) referred to these
(OET), whereas other taxa in Eragrostideae (fide
& cork That they were destined to
Clayton Renvoize, 1986) will be designated as papillate cells.)
(OERG) become cork became evident by examining
LL Genera" cells
Other Eragrostoid
lemma,
development on a in
This study focused on the presence or absence different stages of
were
of characters. No attempt was made to measure which cells at the apical and basal portions
The
development.
stages of initially
quantitative variation of the characters, but distri- in different
and frequency on the lemma sometimes rounded outer walls of short cells appear to collapse
bution is
coincident with or prior to suberin deposition; this
discussed.
process was evident the shrunken tissue of the
in
coupled with darkened lumens of the
outer wall,
Results
Leptochloa
Leptocarydion, Fig. 28,
short cells
(e.g.,
A
summary lemmatal microcharacters ob- ig. 52).
of
ifl
were absent spe-
Table Sillica ceUs. Silica cells in all
monticola
Valdes-Reyna and Hatch (1991) are in- cies o( Leptochloa except for L. (Fig. 41),
results of'
specimens
Unless noted otherwise these re- which had abundant silica cells in all
tercalated therein.
L
Valdes-Reyna and Hatch examined, and one specimen {Snow 581 1-A) of
accord with those of
suits
which had a few silica cells
(1991) for taxa examined in both stuthes. Figures fascicularis (Fig. 35),
are presented at the end of the text, arranged in present in the intercostal regions.
OET
alphabetical order by genus name. Figures are not A majority of genera had silica cells. In
Halopyrum they were poorly
and characters observed or (Fig. 23, not visible)
presented taxa
for all
obscured
developed (minimal deposition?),
every character recorded silica
discussed, but virtually
508
Annals
of the
Missouri Botanical Garden
Table Summary- of lemmatal micromorphological
1. characters for species oi Leptochloa, most genera
in Eleusininae,
and a few genera in Eragrostideae outside Eleusininae &
(fide Clayton Renvoize, 1986). Genera not included in
Eleusininae
are indicated with a double asterisk. Taxa are arranged alphabetically, Taxa examined by Vald^s-Reyna
and Hatch
(1991) but not examined herein are followed by
single asterisk; their data are intercalated convenience
for
by: relying on Watson and
(1) Dallwitz (1992) for the type of microhair (as they determined from leaf blades);
(2)
examining herbarium
material for the presence of prickles and macrohairs (Appendix and by leaving a question
1); (3)
mark column
in the for papillate short since
cells, their interpretation of papillae differed (see Results). The generic
abbreviation
for species tentatively placed L-ptochloa
in that apparently lack a valid combination in the latter D.
is
_* *«
rx
/ j^ Di'pl'Mach1 ne)\ + ---fc + = BM
(for specific epithet. Abbreviations: =
present; absent;
bicellular microhairs
(C
P - E = = =
chloridoid, panicoid, enneapogonoid); Macrohairs (N normal, CC A CR
clavicorniculate,
apiculate,
PLC =
crispate); PSC
papillate short
cceelllls.
Ta xon BM
Cork PLC PSC
Silica
Prickles Macrohairs
Acrachne racemosa
C
Apochiton
burttii C
N
Beusia +
hiflora C
N
Bouteloua
curtipendula'^* C
N
Brachychloa schiemanniana
C
Chloris paniculata*'^
C +
N
Chloris
verticillata'^'^ c
N
Cladoraphis +
cyperoides
E
N
Cladoraphis
spinosa
m m
Coelachyru
c
brevifoliu CR
Coelarhyrum +
poiflorum c CR
Coelachyrum
stoloniferum c CR
Coelachyrum yemenicum +
c +
CC
Chondrosum
gracile*^
c +
N
Cynodon +
nlemfuerisis** c
A/N
*
Dactylocteruum
c
Desmostachya +
hipinnata
C/F +
Dinebra polycarpha
C +
N
-I-
H-
Dinebra
retroflexa C + N
Drake- Rrockmania +
haareri C +
N
Drake-Brockmania
somalemis
C
N
+
Ectrosia gullireri p
N
Ectrosia leporinn + p
-I-
Ectrosiopsis hisioclada
p
4-
Eleusine indica +
C
-I-
Eragrostiella
bifaria
C
*
Eragrostis spp.
C/P
Erioneuron
spp.*
C
N
Gouinia
rirgata
C
N
-I-
Habrochloa
bullockii
P
+
N
Halopyrum mucronatum
c +
+
N
Harpachne
schiniperi
c
Heterachne
abort iva P +
Indopoa paupercula
c
N
4-
Kengia
serotiria
c +
N
Ij'ptocarydion vulpiastrum +
c
+ N
-f-
Ijeptochloa aquatica c
+
N
D. caudata
c
N
Leptochloa +
chinerisis c +
+
N
+
Leptochloa
chloridiformis c
N
Leptochloa
ciliolata
N
Leptochloa
coerulcscens
c
+ N
-i-
D, ciispidata
+
N
Leptochloa decipiem
N
Ijeptochloa digitata c
N
Leptochloa +
divaricatissima c
N
Snow 509
Number
Volume 4
83,
Lemmatal Micromorphology
1996
Table Continued.
1.
BM
PLC PSC Macrohairs
Prickles
Cork
Taxon Silica
N
C
Leptochloa dubia
cc
+ C
D, eleusine
+ N
+ c
Leptochloa fascicularis
+ + N
+ c
Leptochloa
fiisca
I
+ c N/-
gigantea
D.
N
+ c
Leptochloa ligulata
I
N
+ c
Leptochloa longa
+ N
+ c
marquisemis
Leptochloa
+ N
+
c
Leptochloa monticola
N
c
mucronata 4|
Leptochloa
N
+ +
+
c
D, muelleri
+ N
+
c
Leptochloa nealleyi
N
+
c
Leptochloa neesii
N
c
Leptochloa
ohtusifiora
I N
+ c
panicea
Leptochloa
+ + + N
c
Leptochloa panicoides
N
c
D, parviflora
N
c
Leptochloa rupestris
I N
+ c
Leptochloa scabra
^- ^
Leptochloa sp. nov.
+ N
c
(Snow, in prep.)
I
+ I N
+ c
-h
Leptochloa squarrosa
I
N
c 4-
leptochloa
uniflora
N
+ c +
Leptochloa uninervia -f-
N
c
Leptochloa virgata
I
N
+ +
c
Leptochloa viscida
I
I
N
c
Leptochloa xerophila
+ N
c
Lintonia nutans**'
-i-
+ N
C/P
Lophacme
digitata
N
+ I
c ?
Munroa
squarrosa*
I
+ c
i-
Myriostachya wightiana
N
+ c
Neesiochloa barbata
N
+ p
Neyraudia reynauldiana
N
+ c
Ochthochloa compressa
+ N
+ c +
Odyssea mucronata
N
+ +
c
Odyssea paucinervis
+ + N
+ c
Orinus thoroldii -i-
I
N
c
Oropetium aristatum
N
c
Pogonarthria
Jieckii
N
c
Pogoneura
biflora -I-
+
E
Psammagrostis wiseana
+
+ c
Psilolemma jaegeri
c 9
Redfieldia flexuosa* 4^
N
+ c
Richardsiella eruciformis
I
c
macrostachyum
Sclerodactylon
+ + N
+ c
?
Scleropogon
brevifolius*
c
Sohnsia
filifolia*
N
r
+ c
Spartina pectinata**
I
+
+ c
barbata
Steirachne
+ + N
c
pedunculatus**
Tragus
N
+
c
grandiglumis
Trichoneura
I
N
+
c
?
Tridens spp.*
N
7
+
c
spp.*
Triplasis
N
+
c
Tripogon major
+ N
+ + p
andropogonoides
Triraphis
+ N
c 9
Vaseyochloa multinervosa* H-
+
+ +
madagascariensis
Viguierella
510
Annals
of the
Missouri Botanical Garden
by
epicuticular waxes,
or hoth. AVng/V/ (Fig. 27, not chiton and Triraphis were th(7 cotnnion. Nirora
and
visible) Eleusine (not illustrated) had a few sil- (1962: 9) illustrated eniu^apogotioid inierohairs
in
ica cells that were localized over the c^oslal zones. Eleusininae for JSecragrostis, which Clayton and
The
proximity
of silica cells to cork cells was a Renvoize (1986) included in Eragroslis, Tfie en-
character noted by Vald^s-Reyna and Hatch
neapogonoid
microhairs observed here CUido-
for
(1991). Silica cells were not adjacent to cork cells raphis cyperoides and Psammagrosiis wUeami
(Fig.
Desmostachya
in
(Fig. 14), Ectrosia gulliveri (Fig. 65) represent only the second
rc^port for this tyj)e
17), Ectrosiopsis (Fig. 19), Myriostachya (Fig. 56), in Eleusininae. All microhairs in Psammagrosiis
Odyssea mucronata and
(Fig. Steirachne had
60), (Fig. (Fig. 65) swt^llings <hstal to the base of the
were
69). Silica cells adjacent to cork cells in Cla- microhair, a condition observed
not clscwh(^r<\
OERG
ioraphis
(Fig. Ectrosia leporina Har-
7), (Fig. 18), All had chloridoid micro
hairs.
pachne
(Fig. 24), Odyssea paucinenis (not shown). Papillae, Papillae occuned singly on
short
Psilolemma
(Fig. Richardsiella and
66), (Fig. 67), cells or singly on the distal <Mids of long
cells.
Sclerodactylon
(Fig. In Pogonarthria Three
68). (Fig. 63) clarifications are needed prior to presenting
and
Triraphis
(Fig. 71) their location varied (cork observations
of papillae.
cells adjacent shown
to silica cells not for Trira- First, the distal ends of the outer walls of
<^pi-
phi^). It was uncertain whether the dark, narrow dermal hmg cells can be noticcal)ly swollen, as
in
hands some
adjacent
to silica cells in Heterachne Eragrostiella Indopoa and
(Fig. 20), (Fig. L'p-
26),
(Fig. 25) w<*re artifacts of preparation (e.g., shrink- tochloa virgata (Fig. 52). These swellings were rcc-
ing of cell walls adjacent to the silica bodies noted ognized by Valdcs-Reyna and Hatch
(1991:
23)
fig.
by Kaufman &
ct al, 1972: fig. 6, and Terrell Wer- in at least one instance as papillae. As
inlcrpn^t
I
gin, 1981) or whether the narrow bands were cork them,
outer walls that arc merely swollen are
dis-
cells that were partially obscured by overarching from The
tinct true papillae. distinction between
silica bodies; the uncertainty was enhanced be- long possessing
cells a single, distal papilla
(e.g..
cause
not all silica cells fiad adjacent bands. Since Leptochloa
coenilescens, Fig. 31) long
anil cells that
a few short cells with dark lumina were visible ad- are merely swollen can be seen with h^ptochJoa
chi-
some
jacenl
to silica cells, cork cells were scored nemis which
(Fig. 29), in a single pa[)illa evident
is
as present Heterachm\ obsene
for I did not silica atop the distal swelling of a long and
ct^ll, willi
/..
Lept
/'
by Valdes-Reyna and Hatch
(1991: fig. 24, tab. 2), pillalc or miMely swollen. Second, the outer wall of
they were recorded
as present (Table
1). short cells prior to diffen^ntiation can a|)pear round-
Among OERG,
silica cells were observed in ed (papillate, fide Valdes-Reyna & Hatch, 1991)
Spartina and Tragus, being more common when
in the viewed
in profile (e.g., Eragrostiella, Fig. 20;
'^**^^- Indopoa, The rounded
Fig. 26). outci* walls should
Bicellular microhairs, Chloridoid microhairs be confused
not with which
papillae, are
lo<-alized
were observed
in all species of Leptochloa except processes arising from the out(M- wall. Third,
tlic
L
L
cdiolata, Diplachne and
cuspidata,
decipicns. apical extensions
of the lateral walls of loni^ cells
Microhairs generally were
scattered, but in L;pto- of Leptocarydwn and
(Fig. 28) Steirachne
(Fig. 69)
L
and
c/t/oa cauf/a/a /on^^-a they were c(mmion near are distinct from Ime Palmer and
papilhu-; Gcr-
The
the apex. basal
cells of microhairs of L^pto- belh-Jones (1988: 94) have noticed a similar dis-
L
chloa panicoides and
(Fig. 47) viscida (Fig. 53) tinction in Phacelurus (Panicoidea<% Andropogo-
were
alypically thick and nontapering lowanl
their neae), as did Pt^t<'rson (1989) in Muhlenhcrgia
basal inserticm. Additional study needed
is to eval- (Chl(»ridoi<leae, S])(»robolInae). Thus, study
for this
uate whether shape
the of the basal can be
cell papillae arc taken to b<^ apically rounded, undif-
hypothesized
as a separate
character.
ferentiated processes from and
that arise are local-
Among
GET,
seven eleusinioid geru'ra had pan- ized on the outer cell wall, and which can b<u'ome
&
icoid microliairs {Ectrosia Habrochloa, &
gullivieri, silicified (Clark Gould, 1975; Temdl Wergin,
&
Heterachne, Neyraudia,
Steirachne, Triraphis, Vi- 1981; Consaul Aiken,
1993). (Ellis (1979) cited
GET
^mere//a), whereas the remaining had Mdcalfe
chlori- become
(1960) that papillae can
cutin-
doid microhairs. Microhairs were observed
not However,
in ized. Metcalfe
(1960: 668) indicated only
Cladoraphis
spinosa or Viguierella, the one
latter of spcci<'s {Trikeraia hookeri
(tribe Stipeac)) as
which needs
further study, since only one specimen having
cutinized
papilla<\ Furthermore, Mclcallc
was available for study (Table 1). As with species (1960) did not indicate how he di-lermined the
of Leptochloa, microhairs abundance
varied in and presence of
cutin.) It is imj)ortan1 to stress that oth-
were
generally scattered; only near the apex in Apo- er structures on grasses called papillae may not be
Snow 511
Number
Volume 4
83,
Lemmatal Micromorphology
1996
L
were Diplachne cuspidata, dig-
homologous the papillae described here (Clark prickles rare in
to
L
L
L
& occa-
Gould, 1975; Zuloaga, 1987: 26.2c; Ddvila itata, mucronata, rupestrh, uniflora,
fig.
L
common, cau-
1990 sional in most species, or as in
I
data.
1994).
I
A
OET.
were observed single
on Papillae on short cells Prickles for all
Papillae short
cells.
curred in several species of Leptochloa (L fas- prickle was ob serve d on Psilolemma\ however.
one was observed on three specimens,
since only
L L and L most and because apex was directed toward the lem-
panicoides, uninervia, viscida). In its
toward
cases they had a collapsed appearance, which may matal base (almost universally they point
have been an artifact of preparation, or, since the the apex in Eleusininae), it was considered an ab-
norm
been documented
has
of papillae
silicification
&
& fc-
(Clark Gould, 1975; Terrell Wergin, 1981; most abundant in CWora;>/it5 spp. (Figs. 6, 7),
& Gouinia
perhaps was an indication
Consaul Aiken, 1993),
pyrum and Oropetium Unlike
deposition had not occurred. Collapsed (Fig. 23), (Fig. 62).
that silica
Valdes-R^yna and Hatch (1991)
papillae on short cells are frequent in the literature
0 microscope) on herbar-
observed (with a dissecting
OET had on ium specimens of Tridens spp., Vaseyochloa multi-
Relatively few papillae short cells
and purpurea, although ihey v^ere
Drake-Brockmania nervosa, Triplasis
{Dinebra spp.; spp., Fig. 16;
present the apex.
Only Hal- occasionally only infrequently at
Halopyrum, Fig. 23; Orinus, Fig. 61). in
OERG.
opyrum were the papillae large. Unlike Prickles occurred on all Spartina (not
(Fig. 23)
Valdes-Reyna and Hatch (1991) did not detect shown) had prickles of widely different sizes. Prick-
I
awns
were generally most abundarit on the of
papillae on short cells of Eleusine (not shown). les
Among OERG, only Tragus (not shown) had pa- species bearing these structures (e.g., Lintonia, Fig,
Pogoneura, prickles restricted to the
pillae on the short cells. 54); in
Papillae on long In the 13 species oiLep- awn.
cells.
had
Leptochloa
tochloa having a single papilla on the long cells Macrohairs, All species of at
were more frequently present least some macrohairs on the lemmas. They were
(Table the papillae
1)
SEM
on Diplachne gigantea,
not observed using
/'
1551;
but analysis of an isotype {Vesey-Fitzgerald
ifl
BM) microscope revealed the
even over localized por- with a dissecting
consistent in this feature
^ ^ M A «
I
tions of the lemma; some long cells had papill presence of short macrohairs along the edges of the
_-r
some lemmas. some species they are
had only midrib of In
others did not. Leptochloa viscida (Fig. 53)
a few papillae near the lateral veins. The size of rare, such as the sparse basal occ on Lep-
Most macrohairs ob-
the papillae arising on long cells was more or less tochloa digitata (Fig. 32).
were having smooth
constant within Leptochloa, with the exception of L. served in Leptochloa typical in
which the papillae were edges and a rounded or acute tip. However, a "clav-
coerulescens (Fig. 31), in
was found D.
Tn some cases the papillae were icomiculate" type (see Discussion) in
noticeably longer.
was
which the subapical portion no-
weakly developed, as in Diplachne cuspidata (not eleusine, in
and above which occurred a cor-
shown) and Diplachne gigantea ticeably clavate,
(Fig. 38).
Although many OET had long cells with swollen niculate tip. This feature was noted eariier by Phil-
Coelachyrum
jemmicum,
ends Coe/ac/zjram lips (1974, 1982) for D, eleusine,
(e.g., BeM;5ia, Fig. 3;
The
compare with yemenicum, Lintonia, and Trichoneura. hairs
Fig. 12; Trichoneura, Fig. 70, in part;
and
Coelachyrum whic^h the long shown for Tribolium obliterum by Visser Spies
poiflorum. Fig. 10, in
may
have no swellings), relatively few had a single (1994: fig. 3b) be clavicomiculate, but this is
cells
shown.
Drake- uncertain since only their apices are
papilla on the long cells {Dinebra, Fig. 15;
OET
A lemma;
had macrohairs on the
Brockmania, Fig. 16; Kengia, Fig. 27; Odyssea, Fig. majority of
Acrachne Cladoraphis
and Oropetium, they were absent in (Fig.
60, not visible; Orinus, Fig. 61; Fig. 1),
Desmostachya Ectrosia
The greater basal diameter of pa- splrwsa (Fig. (Fig. 14),
significantly 7),
62).
Eleusine
//a/opjrum from other taxa in Eleu- leporina (Fig. 18), Ectrosiopsis (Fig. 19),
pillae in differs
Heterachne
smmae. (not shown), Eragrostiella (Fig. 20),
Psilolemma
Myriostachya (Fig.
Long with papillae were absent in the (Fig. 25), (Fig. 56),
cells
OERG
Steirachne
Sclerodactylon (Fig. 68), (Fig. 69),
66),
and Only two macrohairs were
Prickles were observed in every spe- Viguierella (Fig. 72).
Prickles.
specimen (Faden
base one
observed the very of
Leptochloa at
quency toward the apex. Among Leptochloa species et ai 74/613, Appendix 1) oi Harpachne schimperi
512
Annals
of the
Garden
Missouri Botanical
MO
The
study of several herbarium sheets
at re- phylogenetieally informative the generic
at level,
vealed that a few macrohairs occasionally occur on Cork were recorded when
cells as present only the
the edges near the hase of some lemmas. However, was
short cell substantially darkened viewed by
(as
they are at most infrequent and are always rela- SEM), whereas Palmer and associates generally
re-
tively short. Moreover, given their length, one could corded cork cells as present when any undifferen-
just as easily designate them
as (relatively long) tialed short cell occurred adjacent to a silica cell
prickles. Examinati(m of specimens of//, bogdanii Pahner
1985: and
(e.g., et al., pi. le, 2e, 3e, 4c,
(MO: Heady Bogdan
1466, many
4524), the other species others therein). agree with Columbus
I T.
J.
in the genus, also revealed a few short hairs near (pers. comm., January 1995)
that the extent
to
the base of some lemmas. Given
their sporadic oc- which suberin deposition and
actually occurs, the
currence and
their questionable status as hairs (vs. extent to which can be observed, needs further
it
relatively long prickles), have reeorded them
I as investigation. If suberin deposition in short cells
is
present or absent (Table The abundant macro-
eventually demonstrated be SEM,
1). to invisible to or
on ApochiUm made
hairs (Fig. 2) observation of oth- it is shown that "cork cells'' on lemmas are lacking
The
er features
(Hfficult. clavicornieulate liairs of in suberin, then their use as phylogenetic markers
Coehichyrum yemcnicum
appear
identical to those will need reccmsideration. These considerations
A
Diplachne
of &
eleiisine. crispate macrohair, iden- have
aside, followed others Vald^s-Reyna
I (e.g.,
by
tifiable the irregular ("crisped") surface and ap- Hatch, 1991) by recording eork
cells as either pres-
parently reported here for the first time in grasses ent or absent.
(Uphof, 1962; Metcalfe, 1960; Ellis 1976, 1979), Silica Cells, Lemmatal silica cells were mostly
was
observed Coelachyrum
for hrevifolium (Fig. 8), absent from Leptochloa, and thus have minimal
in-
C
poiflorum (Figs. and stohmiferum
9, 10), C, (Fig. frageneric phylogenetic value. Since only one spec-
The L
11). crisping is expressed most thoroughly to- imcn of fascicularis (Fig. 35) had a few silica
ward apex, and somewhat Some
tlie less so basally. cells, their occurrence on that specimen probably
is
macrohairs of Trichoneura gmndiglumis
(Fig. 70) similar to lemmatal stomata, which occasionally
were
swollen
at the base. reappear
as atavisms from
the transformationally
OERG
Among
the surveyed, only Spartina antecedent However,
leaves. in Leptochloa monti'
lacked macrohairs. Some specimens Cynodon
of cola (Fig. 41) silica cells are common, which
re-
nlemfuensLs had macrohairs
(Fig. 13) with distinct:llyy quires a reassessment of earlier research. Using
''apiculate'' (sensu Peterson, 1989)
tips. several lines of evidence. Vails (1978) suggested
L
monticola was
that generically misplaced. Based
on leaf anatomy and and
Discussion citing Clifford \\atson
(1977), Vails (1978) suggested a possible alliance
This study originated from morphologically
with Chionochloa Zotov
(Arundinoideae, Arundi-
based
cladistic studies of Leptochloa using various neae). To assess a possible alliance with Arundi-
combinations
of likely sister genera, as hypothc- neae, sampled lemmas from Chionochloa
conspl-
I
sized by Clayton and Renvoize The
use cua
(1986). sole (Forst. Zotov subsp. cunninghamii (Hook,
f.)
f.)
of gross morphology gave pooriy resolved consensus
Z<»tov, C. flavesceru Zotov, Danthonia dominguemis
&
and
trees elades with low support values (Snow, Hack. and Rytidosperma
Pilg., pilosum
(R. Br.)
&
unpublished). Moreover,
the use of a single data Connor Edgar (Appendix
set data not shown). Un-
1;
may L
have
resulted in artificial groupings, a poten- like monticola, which had chloridoid microhairs,
tial problem Hilu and Wright (1982) alluded to in the microhairs of C. conspicua van cunninghamii
their phenetic study of chloridoid grasses. These and pilosum were
R. panlcoid; fuilhermore, micro-
suggested
factors that additional characters miglit hairs were not seen domin-
for C. flavescens or D.
&
more
lead to "accurate" (sensu Hillis Bull, 1993) guensis. Of relevant note, Watson and Dallwitz
estimations of the phylogenetic relationships. Given (1992) reported panicoid microhairs
(for the abaxial
that micromorphological characters have known
leaf surface) for Danthonia, which does accord
not
systematic value in grasses (references in Introduc- with the chloridoid microhairs of Leptochloa mon-
study was undertaken
tion), this to enlarge extant ticola. In addition, the species of Chionochloa
data sets for purposes of phylogenetic inference. lacked cork which were L mon-
cells, present
in
Cork Given
Cells. their universality in Lepto- ticola. Morever, the dumbbell-shaped bodies
silica
L
chloa, cork cells are of no phylogeiK'tic value in in monticola differed from the saddle-shaped
sil-
the genus.
ica bodies of C. flavescens and D. domingueiisis
However,
the variable presence of cork Whereas each
cells in of these taxa has one
at least dis-
Eleusininae and L
Eragrostideae suggests they are crepancy when compared
monticola, lemmatal
to
Snow 513
Number
Volume 4
83,
Lemmatal Micromorphology
1996
Second, with few exceptions Eragroslis,
micromorphology alone does not support an obvious taxa. (e.g.,
&
L Watson microhairs can be readi-
Arundineae. Dallwitz, 1992),
monticola
relationship of to
& one morphological types:
assigned of three
Saddle-shaped Watson, 1977; Vails, ly to
(Clifford
enneapogonoid, based on
dumbbell-shaped 1978), and cross- chloridoid, panicoid, or
1978), (Vails,
and
bodies have been morphological differences of the basal distal
shaped (Metcalfe, 1960) silica
blades Leptochloa. Vails (1978: cells and their length ratios (Tateoka et al., 1959;
reported for leaf In
1988
82) has shown that both dumbell-shaped and sad-
&
below
son Dallwitz, 1992; but see also).
Lept
Ovate and saddle-shaped silica bodies were ob- The elongated aspect and thin wall of the distal
OET
Habroch-
seven
Odyssea mucronata. The presence of two cells in the microhairs of (e.g.,
served
for
L them panicoid micro-
shapes of silica bodies (m duhia and 0, mucron- loa. Fig. 22) characterize as
which cases accords with the
ata cautions against their uncritical use as diag- hairs (Table 1), in all
Watson and Dallwitz (1992) for
phylogenetic markers. Recognition of observations of
nostic or
shape differences of silica bodies as distinct char- 1 eaves.
on
seems premature The discovery of enneapogonoid microhairs
acters (or character states) thus
and Psam-
lemmas Cladoraphis cyperpides
can be demonstrated that infraspecific van- the of
until
it
wiseana represents the third report of en-
body shape minimal. This caveat magrostis
ation in silica is
& Pappo-
Kim, neapogonoid microhairs outside the tribe
Oryza
supported by studies in (\^1iang
is
& and second
phoreae (Chloridoideae) the in
and Zizania WVrgin, 1981) (both
1994) (Terrell
Amphi-
which documented exten- Eleusininae. They were first reported for
genera Oryzeae),
in tribe
Amarasinghe and
pogon (Arundinoideae) by
shape
sive infraspecific variation in the of silica strictus
(1988)
bodies.
moment body shape, and 232) were unable to find microhairs on leaf blades
Ignoring for the silica
cypewides from photographic material provid-
focusing on mere presence or absence, silica cells of C.
Of microhairs
appear be important phylogenetic markers, since ed by R, P. Ellis. the bicellular il-
to
they were not observed in over half of the OET and lustrated by Tateoka et al. (1959), the microhair of
OERG lemma seems most resemble those of S;>o-
examined. Their presence on the C. cyperoides to
is
(Tateoka al, 1959: b,64)
probably symplesiomorphic, given the near univer- robolus vaginiflorus et fig.
and and Pappophorum elegaris (Tateoka et al, 1959: fig.
sal occurrence of silica bodies in grass leaves,
lemma homologous b,155). also somewhat resembles a microhair re-
that the is transformationally to It
however, ported by Peterson (1989: 2,d) for two species
the Testing for parallel loss or gain, fig.
leaf.
approach (Snow, of Muhlenbergia, Tlie swelling distal to the base of
require a cladistic in prep.).
will
was ab-
Pscimmagroslis
The lack of microhairs the microhairs in (Fig. 65)
Bicellular microhairs.
elsewhere Eleusininae.
sent in
Lept
decipiens) not unequivocal evidence (or their ab- Although not identified as such, an enneapogo-
is
sence, since a single microhair was often all diat noid microhair was recently shown for the arundi-
Pentameris distichophylla (Barker,
was three or more specimens of a given noid species
visible for
1993: The recognition of three mor-
taxon. Microhairs were not restricted to certain por- fig. l,c).
microhairs admittedly rep-
when were usu- phological categories of
lemma, infrequent,
tions of the but,
which can misguide
found near the apex. In some taxa, such as resents typological thinking,
ally
(Mayr,
they extend onto the awn. Given a sim{)le the understanding of biological reality
Lintonia,
would Thus, when making preliminary hypotheses
presence or absence, microhairs probably ])e 1982).
of phylogenetic value In Eleusininae. How- of homology (de Pinna, 1991), one might consider
little
whether "enneapogonoid" microhairs of Cla-
two features of microhairs suggest their utility the
ever,
and Psammagrostis wiseana are
Amarasinghe and doraphis cyperoides
as systematic markers. First,
occurring
Watson demonstrated that ten chloridoid
(1988)
genera, including Leptochloa, have partitioning whether the relative elongation of the basal cell is
been
having
More- a "character" the elongation
membranes in the basal cell of the microhair. itself,
enneapogonoid
membranes were limited the subfamily achieved independently from the
over, the to
&
morphologies of micro-
Chloridoideae (Amarasinghe Watson, 1988: 307), type. Overall, the distinct
Of the genera they surveyed in Eleusininae, Era- hairs in Eleusininae and their tendency to be re-
and lacked the stricted generically together suggest their potential
Pogonarthria, Triraphis
grostis,
membranes. The use of partitioning membranes as value as indicators of phylogenetic relationships.
The and
characterization interpreta-
marker subfamily Papillae.
a potential phylogenetic in the
were confounded by several
mcrits further investigation over a wider range of tion of papillae initially