Bot. Rev. (2009) 75:52–66
DOI 10.1007/s12229-008-9018-4
What is a Genus in Cypereae: Phylogeny, Character
Homology Assessment and Generic
Circumscription in Cypereae
A. Muthama Muasya1,2,6 & Alexander Vrijdaghs2 &
David A. Simpson3 & Mark W. Chase3 &
Paul Goetghebeur4 & Erik Smets2,5
1
Botany Department, University of Cape Town, Rondebosch 7700, South Africa
Laboratory of Plant Systematics, K.U. Leuven, Kasteelpark Arenberg 31, BE-3001 Leuven, Belgium
3
Royal Botanic Gardens Kew, Richmond Surrey TW9 3DS, UK
4
Department of Biology, Ghent University, K.L. Ledegancksraat 35, B-9000 Ghent, Belgium
5
National Herbarium of the Netherlands, P. O. Box 9514, NL-2300 RA Leiden, Netherlands
6
Author for Correspondence; e-mail: muthama.muasya@uct.ac.za
Published online: 6 December 2008
# The Author(s) 2008. This article is published with open access at Springerlink.com
2
Abstract Using a DNA-based tree as the framework, the homology of key
taxonomic characters in tribe Cypereae (900 species in 19 genera, the largest of
which is Cyperus) is assessed and revisit the question of generic circumscription.
Plastid DNA (rbcL gene, rps16 intron, trnL intron and trnL-F intergenic spacer)
sequence matrix for 50 species in 19 genera of Cypereae is analysed using the
maximum parsimony algorithm of PAUP. Two major groups are observed: the
Ficinia and Cyperus clades. The Ficinia clade includes taxa with a center of
diversity in the Cape Floristic Region of South Africa. These are predominantly
perennial herbs (with exception of Isolepis, which is predominantly annual) having
non-Kranz (C3) anatomy and spirally arranged glumes. Species of the Cyperus clade
have a predominatly distichous glume arrangement and Kranz anatomy which is
either absent (C3) or present (C4). Cyperus is the core genus in the Cyperus clade, in
which 13 additional segregate genera are embedded. These segregate genera differ
from typical Cyperus in one or more of a few gross morphological characters. There
are no unambiguous characters separating C3 and C4 Cyperus species. The
circumscription of Cypereae is broadened to include all taxa with a Cyperus-type
embryo and perianth segments. Three taxa possessing perianth segments, namely
Hellmuthia membranacea, Scirpus falsus and S. ficinioides, are supported to be
closer to Cyperus than to Scirpus.
Keywords Cyperus Clade . Ficinia Clade . Life Forms . Hypogynous Scales .
Gynophore . Kranz Anatomy . Inflorescence Morphology . Elongation of Filaments .
Dispersal Unit . Nutlet Orientation
What is a genus in Cypereae
53
Introduction
Taxa included in tribe Cypereae are annual or perennial herbs that vary in stature
from minute to 5 m tall. Leaves generally have well-developed blades, but are
reduced to lobes in some species; there also may be a ligule. Inflorescences are
capitate or anthelate. They all have hermaphrodite, trimerous flowers, with each
subtended by a papery glume. Glumes are spirally or distichously arranged in the
spikelets, apart from some reduced species in which the arrangement is obscure.
Generic classification in tribe Cypereae and subfamily Cyperoideae dates back to
Linneaus (1753), who described the genera Scirpus and Cyperus to include all
species of Cyperaceae with bisexual flowers, and distinguished by the spiral versus
distichous glume arrangement in Scirpus and Cyperus respectively. The broad
circumscription of Scirpus, based on common and widespread characters, resulted in
a heterogeneous assemblage which was treated by subsequent workers as one genus
(e.g. Boeckeler, 1870; Clarke, 1894, 1898, 1902; Hitchcock et al., 1969) or split into
a number of smaller genera (e.g. Brown, 1810; Raynal 1973; Wilson, 1981;
Goetghebeur, 1998).
Classification of genera into tribes in Cyperoideae has differed widely among
authors, depending on which character(s) were emphasized. Therefore, there is a
need to revise generic and tribal circumscriptions and especially incorporate new
evidence from morphology and DNA sequence data.
Taxonomic History of Tribe Cypereae
Tribal concepts in Cyperoideae have varied over the years. A large number of
legitimate tribal names have been published in Cyperoideae, including Cypereae,
Scirpeae, Fuireneae, Ficinieae, Schoenoplecteae, Abildgaardieae, Lipocarpheae, and
Eleocharideae (Goetghebeur, 1985). Cypereae and Scirpeae have been the most
frequently used tribal names (e.g. Haines & Lye, 1983; Bruhl, 1995; Goetghebeur,
1998). The main difference has traditionally been that Scirpeae have spirally
arranged glumes whereas in Cypereae glumes are two-ranked (e.g. Lye, 1971).
However, this tribal classification has resulted in genera such as Oxycaryum and
Isolepis being classified in Scirpeae even though these genera show closer affinity to
Cyperus, as pointed out by Raynal (1973).
Embryological data (e.g. Van der Veken, 1965; Haines & Lye, 1971, 1976, 1983;
Raynal, 1973, 1977; Wilson, 1981; Goetghebeur, 1996, 1998; Bruhl, 1995) have
contributed significantly to generic and tribal circumscription in Cyperoideae.
Heterogeneous Scirpus sensu lato has embryo types characteristic of Cyperus,
Carex, Bulbostylis, Fimbristylis, Schoenus and Schoenoplectus, whereas Cyperus
has mainly the Cyperus-type embryo. Based on the interpretation that several genera
could have the same type of embryo but a single genus should have only a single
type of embryo, Scirpus sensu lato was split into several genera. Currently
(Geotghebeur, 1998), tribes in Cyperoideae are classified to include genera sharing
a single embryo type. For example, Cypereae have the Cyperus-type embryo and the
similar Ficinia-type, whereas Scirpeae sensu stricto have only the Fimbristylis-type
embryo.
54
A.M. Muasya, et al.
Two recent classifications of Cyperoideae, based predominantly on morphological
data, have differed in placement of genera in Cypereae. Goetghebeur (1998) classified
all taxa characterised by Cyperus-type embryo in Cypereae, whereas Bruhl (1995)
placed genera having spiral glume arrangement (i.e. Isolepis, Ficinia, Desmoschoenus, Scirpoides, Kyllingiella, Oxycaryum) in Scirpeae. Hellmuthia, bearing spirally
arranged glumes but having an additional pair of scales in flowers subtended by the
most proximal glumes, was placed in Scirpeae by Bruhl (1995) but in Chrysitricheae
by Goetghebeur (1998). Bruhl (1995) did not recognise the tribes Eleocharideae and
Fuireneae (sensu Goetghebeur, 1998), but included these taxa in Scirpeae.
Phylogeny, Character Homology Assessment and Generic Circumscription
Phylogenetic Relationship Based on Molecular Data
Over the last ten years, molecular systematic data have been used in the classification of
ranks above family (e.g. APG, 2003) and in supraqeneric classification within
Cyperaceae (Muasya et al., 1998, 2000a; Simpson et al., 2007). Studies on Cyperoideae
have targeted phylogenetic relationships in Scirpeae (Muasya et al., 2000b, Dhooge
et al., 2003) and Abildgaardieae (Ghamkhar et al., 2007), and focussed on genera
Eleocharis (Roalson & Friar, 2000; Yano et al., 2004), Isolepis (Muasya et al., 2001a),
Cyperus sensu lato (Muasya et al., 2002) and Schoenoplectus (Yano & Hoshino, 2005).
Total DNA was extracted from leaves or culms collected in the field or from
herbarium specimens (Table 1). DNA extraction, amplification and sequencing were
performed according to published procedures (e.g. Muasya et al., 2001a, 2002), and
the resulting sequences aligned manually. We present and discuss here results of a
maximum parsimony analysis of representatives of 18 of the 19 genera in Cypereae
recognised by us; no material of the monotypic genus Ascopholis was available. The
DNA data matrix (rbcL gene, rps16 intron, trnL intron and trnL-F intergenic spacer)
comprises 3,721 characters among which 625 are potentially parsimony-informative.
The matrix was analysed using the heuristic algorithm in PAUP* (Swofford, 2002),
random addition for 10,000 replicates with tree-bisection-reconnection (TBR).
Bootstrap analysis was performed for 1,000 replicates under maximum parsimony
criterion (random taxon addition, twin replicates, TBR).
The strict consensus tree generated from the maximum parsimony analysis is
presented in Fig. 1, with the bootstrap values for the various branches mapped.
Cypereae are resolved into the Cyperus and Ficinia clades. The Ficinia clade
comprises Scirpoides, Hellmuthia, Isolepis, Ficinia, Desmoschoenus and two Scirpus
species (S. falsus and S. ficinioides). The Cyperus clade has Cyperus sensu stricto as
the core genus, in which the thirteen derived genera (Alinula, Androtrichum,
Ascolepis, Courtoisina, Kyllinga, Kyllingiella, Lipocarpha, Oxycaryum, Pycreus,
Queenslandiella, Remirea, Sphaerocyperus, and Volkiella) are embedded.
Assessment of Morphological Character Homology
Using the DNA phylogenetic framework (Fig. 1), we evaluate the homology of key
morphological characters used in classification of the Cypereae. The morphological
What is a genus in Cypereae
55
Table 1 List of Taxa Sampled with Vouchers and Genbank Accession Numbers
Taxon
Voucher
GenBank accession numbers
rbcL
Cyperoideae Suess.
Abildgaardieae Lye
Abildgaardia ovata
(Burm. f.) Kral
Fimbristylis dichotoma (L.)
Vahl
Cypereae Dumort.
Alinula lipocarphoides
(Kük.) J. Raynal
Alinula paradoxa Goetgh. &
Vorster
Androtrichum giganteum
(Kunth) H. Pfeiff.
Androtrichum trigynum
(Spreng.) H. Pfeiff.
Ascolepis capensis (Kunth)
Ridl.
Ascolepis protea Welw.
Courtoisina assimilis
(Steud.) Maquet
Cyperus compressus L.
Cyperus cuspidatus Kunth
Kenya: Muasya et al. 684
(EA, K)
Kenya: Muasya 1006
(EA, K)
rps16
trnL-F OR
intron/spacer
Y12985
AJ295754
Y13008
AJ295755
Kenya: Muasya: 2592 (EA)
–
–
EF178608
Tanzania: Faden et al.
96/29 (K)
Argentina: Tressens et al.
4292 (K)
Argentina: Goetghebeur
4764 (GENT)
Kenya: Muasya 1009
(EA, K)
Congo: Fay 2700 (K)
Tanzania: Faden et al.
96/119 (K)
Thailand: Muasya 1375 (K)
Thailand: Muasya 1374 (K)
AJ278290 –
AJ295756
EF178546
–
EF178547
–
Cyperus involucratus Rottb. Madagascar: Kew Acc.
6136603
Cyperus laevigatus L.
Kenya: Muasya 1041 (EA)
Cyperus longus L.
Europe: Chase 2276 (K)
Cyperus papyrus L.
Chad: Hepper 4213 (K)
Cyperus pulchellus R. Br.
Thailand: Muasya 1377 (K)
Cyperus pygmaeus Rottb.
Kenya: Muasya 1133 (K)
Desmoschoenus spiralis
New Zealand: Ford 44/94
Hook. f.
(NU)
Ficinia bergiana Kunth
S. Africa: Muasya 2337 (BOL)
Ficinia distans C. B. Clarke S. Africa: Muasya 2283 (BOL)
Ficinia esterhuyseniae
S. Africa: Muasya 2312 (BOL)
Muasya
Tanzania: Faden et al.
Ficinia gracilis Schrad.
96/433 (K)
Ficinia nodosa (Rottb.)
Australia: Stind 21216 (K)
Goetgh., Muasya & D. A.
Simpson
Ficinia rigida Levyns
S. Africa: Muasya 2319 (K)
Ficinia trichodes (Schrad.) S. Africa: Muasya 2328 (K)
Benth. & Hook. f.
Ficinia radiata (L. f.) Kunth S. Africa: Muasya 2310 (K)
Hellmuthia membranacea
S. Africa: Weerderman et al.
(Thunb.) R. W. Haines &
269 (K); Muasya 1145 (K)
Lye
BRITAIN: Muasya 1058 (K)
Isolepis cernua (Vahl)
Roem. & Schult. var.
cernua
Isolepis fluitans (L.) R. Br. Kenya: Muasya 1057 (K)
Y13003
AF449518
AJ295757
Y13002
AY40590
–
AY449519
–
AY040595
AF449506 AF449521
AF449508 AF449523
Y12967
AF445920
AF449555/–
AF449557/
AF449569
AJ295758
Y13017
Y13015
Y12966
AY40591
AJ404698
AJ404701
AF449527
AF449528
AF449531
–
AF449534
–
AY040596
AY040598
AJ295759
AY040599
AJ295760
AJ295753
EF200588 EF078974
EF178548
EF178549 EF078975
EF178593
EF178594
EF178590
EF178550
EF178534
Y12984
EF174386
AJ295793
EF178557 EF174387
EF178558 EF174388
EF178602
EF178603
EF200589 EF078976
Y13000
EF174389
–
AJ295815
Y13014
AF449538
AJ295775
Y12961
EF174390
AJ295780
56
A.M. Muasya, et al.
Table 1 (continued)
Taxon
Isolepis hystrix (Thunb.)
Nees
Isolepis levynsiana Muasya
& D. A. Simpson
Isolepis marginata (Thunb.)
A. Dietr.
Isolepis setacea (L.) R. Br.
Isolepis tenuissima (Nees)
Kunth
Isolepis venustula Kunth
Kyllinga appendiculata K.
Schum.
Kyllinga brevifolia Rottb.
Kyllinga bulbosa P. Beauv.
Kyllingiella microcephala
(Steud.) R. W. Haines &
Lye
Kyllingiella polyphylla (A.
Rich.) Lye
Lipocarpha hemisphaerica
(Roth.) Goetgh.
Lipocarpha nana (A. Rich.)
J.Raynal
Oxycaryum cubense (Poepp.
& Kunth) E.Palla
Pycreus flavescens (L.)
Rchb.
Pycreus nuerensis (Boeck.)
S.S.Hooper
Queenslandiella hyalina
(Vahl) Ballard
Remirea maritima Aubl.
Scirpoides holoschoenus
(L.) Soják
Scirpoides thunbergii
(Schrad.) Soják
Scirpus falsus C. B. Clarke
Voucher
GenBank accession numbers
rbcL
rps16
trnL-F OR
intron/spacer
S. Africa: Muasya 1150 (K)
AJ404711
-
AJ295785
S. Africa: Muasya 1151 (K)
AF449514 AF449514
Australia: Coveny et al.
17452 (K)
Kenya: Muasya 1059 (K)
S. Africa: Muasya 2369 (K)
AJ404714 EF174391
AF449563/
AF449575
AJ295790
Y12962
EF174392
AY725947 -
AJ295799
–
S. Africa: Muasya 1189 (K)
Kenya: Muasya 1050 (EA, K)
AJ404724 Y13007
AF449542
AJ295804
AJ295761
Australia: Coveny et al.
17459 (K)
Kenya: Muasya 1020 (EA, K)
Zimbabwe: Muasya et al.
1118 (K)
AF449515 AF449543
AF449564/
AF449576
AY040601
AJ295807
Y12979
AF449544
AY040592 AF449540
Tanzania: Wingfield 497 (K) Y13013
AF449541
AJ295515
Thailand: Muasya 1217 (K)
AF449516 AF449546
Kenya: Muasya 972
(EA, K)
ZAMBIA: Richards
13318 (K)
Kenya: Muasya 1022 (EA, K)
Y12990
AF449545
AF449565/
AF449577
AJ295762
Y13006
–
AY040602
Y13005
AF449547
AJ295763
Tanzania: Muasya 940
(EA, K)
Kenya: Mwachala 296 (EA)
Y13004
AF449549
AY040603
AY725953 –
–
Tanzania: Faden et al.
96/48 (K)
S. Africa: Acocks s.n. (K)
AY040593 AF449550
AY040604
Y12994
AY344153
AJ295811
S. Africa: Muasya 1205 (K)
AJ404727 AF449551
AJ295812
EF178559 EF174393
–
EF178560 EF174394
–
AJ404699 AF449552
AJ295764
EF178561 –
–
Y13011
–
AJ295768
Y12953
–
AJ295765
S. Africa: Hilliard 13609
(GENT)
Scirpus ficinioides Kunth
S. Africa: Hilliard 16095
(GENT)
Sphaerocyperus erinaceus
Tanzania: Faden et al. 96/338
(Ridl.) Lye
(K)
Volkiella disticha Merxm. & Namibia: Muller et al.
4245 (K)
Czech
Eleocharideae Goetgh.
Eleocharis marginulata
Kenya: Muasya 1039 (EA, K)
Steud.
Fuireneae Reichenb. ex Fenzl
Actinoscirpus grossus (L. f.) Malaysia: Simpson 2660 (K)
Goetgh. & D. A. Simpson
What is a genus in Cypereae
57
Table 1 (continued)
Taxon
Bolboschoenus maritimus
(L.) Palla
Bolboschoenus nobilis
(Ridl.) Goetgh. & D. A.
Simpson
Fuirena sp.
Voucher
GenBank accession numbers
rbcL
rps16
trnL-F OR
intron/spacer
Botswana: Smith 2452 (K)
Y12996
–
AJ295767
S. Africa: Leistner 144 (K)
Y12995
–
–
Y12970
–
–
Brazil: Thomas et al. 10404
(NY)
Isolepis humillima (Benth.) Australia: Thomas et al. 622
K. L. Wilson
(BRI)
Schoenoplectiella articulata Tanzania: Muasya 947
(L.) Lye
(EA, K)
Schoenoplectus corymbosus Kenya: Muasya 1004 (EA)
(Roth ex Roem. & Schult.)
J. Raynal
Schoenoplectus lacustris (L.) Britain: Muasya 1043 (K)
Palla
Schoenoplectus litoralis
Hong Kong: Shaw 883 (K)
(Schrad.) Palla
Scirpeae Kunth ex Dumort.
Eriophorum vaginatum L.
Poland: Beyer et al. 2 (K)
Eriophorum viridicarinatum USA: Boufford 23053 (WS)
(Engl.) Fern.
Scirpus ancistrochaetus
USA: Nacsi 7544 (DOV)
Schuyler
Scirpus sylvaticus L.
HBUG/86–0541 (GENT)
Mapanioideae C. B. Clarke
Hypolytreae Presl ex Fenzl
Hypolytrum nemorum (Vahl) Malaysia: Simpson 1379 (K)
Spreng.
Mapania cuspidata (Miq.)
Brunei: Marsh 4 (K)
Uittien
AJ404728 AF449539
AJ295784
Y12987
–
–
EF178570 –
EF178607
Y12943
AJ295809
AF449554
EF178571 –
–
Y12951
U49230
AJ295769
–
AF449553
–
EF178578 EF174395
–
EF178586 EF174396
–
Y12958
AY344142
AJ295816
Y12955
DQ058318
AJ295817
Classification following interpretation of current data and Goetghebeur (1998)
characters are manually plotted on the DNA topology, majority of characters can be
unambiguously reconstructed on the phylogeny. Ascopholis, a monotypic genus
restricted to India (Goetghebeur, 1998), has not been included in this study due to
unavailability of material. Generic status of Ascopholis is not accepted by all, and it
has been suggested to be conspecific to the widespread Cyperus mollipes (C. B.
Clarke) K. Schum (Govaerts et al., 2007).
Mature Embryo Morphology
Cypereae are characterised by the presence of a Cyperus-type embryo (Van der
Veken, 1965; Haines & Lye, 1971, 1976; Raynal 1973; Wilson, 1981; Goetghebeur,
1985). In the Ficinia clade, species of Ficinia have a Ficinia-type embryo which is
similar to Cyperus-type, but Isolepis, Hellmuthia and Scirpoides have a typical
Cyperus-type embryo (Van der Veken, 1965; Haines & Lye, 1971). The embryo type
58
A.M. Muasya, et al.
Fig. 1 Maximum parsimony
strict consensus tree of Cypereae
based on heuristic analysis of
plastid DNA sequence data.
Cyperus and Ficinia clades
are marked by black and grey
bars respectively. Bootstrap
support values shown as *for
50–74%, ** for 75–89% and
*** for 90–100%
in Scirpus falsus and S. ficinioides has not been studied, mainly because mature
nutlets were not available.
Concepts of mature embryo morphological states are subject to individual
interpretation of homology, and it may be difficult to distinguish similar embryo
types in some cases. For example, Isolepis humillima, placed in Isolepis due to the
presence of spiral glume arrangement, has been interpreted as having an embryo
similar to Scirpoides (Wilson, 1981). The phylogenetic position of this taxon in
molecular analyses is within Schoenoplectus subgen. Actaeogeton, a group
possessing a Schoenoplectus-type embryo. The mature embryo in Cypereae is less
complex when compared to state is the sister tribe Fuireneae (Schoenoplectus type),
hence our study does not support Juguet's contention (as reported in Raynal, 1973)
that the embryogeny of Cypereae is very evolved compared to the rest of the family.
What is a genus in Cypereae
59
Table 2 Summary of Some of the Diagnostic Characters of the Genera in Cypereae
Genus (total/
studied species)
Habit
Floret
no.
Glume
Dispersal
arrangement unit
Nutlet
orientation
Alinula (4/2)
Androtrichum (2/2)
Annual
Perennial
One
Many
Distichous
Distichous
Dorsiventral C4
Dorsiventral C3
Ascolepis (20/2)
Annual/
perennial
Perennial
Annual
Annual/
perennial
Perennial
Perennial
One
Distichous
Ascopholis (1/0)
Courtoisina (2/1)
Cyperus (550/7)
One
Distichous
Many
Distichous
1-Many Distichous/
spiral
Desmoschoenus (1/1)
Many
Spiral
Ficinia (60/8)
Many
Distichous/
spiral
Hellmuthia (1/1)
Perennial
Many
Spiral
Isolepis (70/9)
Annual
Many
Distichous/
(perennial)
spiral
Kyllinga (60/2)
Perennial
Many
Distichous
(annual)
Kyllingiella (4/2)
Perennial
Many
Spiral
Lipocarpha (35/2)
Annual/
One
Distichous
perennial
Oxycaryum (1/1)
Annual
Many
Spiral
(perennial)
Pycreus (100/2)
Annual/
Many
Distichous
perennial
Queenslandiella (1/1) Annual
Many
Distichous
Remirea (1/1)
Perennial
One
Distichous
Scirpoides (5/2)
Perennial
Many
Spiral
Scirpus spp. (3/2;
Perennial
Many
Spiral
Southern Africa)
Sphaerocyperus (1/1) Perennial
One
Distichous
Volkiella (1/1)
Annual
One
Distichous
Nutlet
Nutlet &
filaments
Spikelet/
nutlet
Spikelet
Spikelet
Spikelet/
nutlet
Nutlet
Nutlet
Photosynthetic
type
Dorsiventral C4
Dorsiventral C4
Dorsiventral C3
Dorsiventral C3 & C4
Dorsiventral C3
Dorsiventral C3
Nutlet
Nutlet
Dorsiventral C3
Dorsiventral C3
Spikelet
Lateral
Nutlet
Spikelet
Dorsiventral C3
Dorsiventral C4
Nutlet
Dorsiventral C3
Nutlet
Lateral
C4
Spikelet
Spikelet
Nutlet
Nutlet
Lateral
Dorsiventral
Dorsiventral
Dorsiventral
C4
C4
C3
?
Spikelet
Spikelet
Dorsiventral C4
Dorsiventral C4
C4
Classification following interpretation of current data and Goetghebeur (1998).
Annual Versus Perennial Life Form
Annual and perennial growth forms are observed among members of tribe Cypereae
(Haines & Lye, 1983; Goetghebeur, 1998; Table 2). In the Ficinia clade, an annual
life form has evolved only in Isolepis (which also has some perennial species)
whereas all other taxa are perennial. In the Cyperus clade, an annual life form is
exclusively found in Courtoisina, Queenslandiella and Alinula; a predominantly
perennial life form is observed in Oxycaryum, Kyllingiella, Remirea, Sphaerocyperus,
Kyllinga and Ascolepis); while both annual and perennial life forms are recorded in
Cyperus sensu stricto, Pycreus and Lipocarpha.
Glume Arrangement
Spiral glume arrangement is a plesiomorphic state in Cyperoideae (Muasya et al.,
2001b). In Cypereae (Table 2), the Ficinia clade has predominantly a spiral glume
60
A.M. Muasya, et al.
arrangement, except in few species of Ficinia (e.g. F. distans and F. angustifolia) and
Isolepis (I. levynsiana and I. venustula). In the Cyperus clade, distichous glume
arrangement is usual especially in Androtrichum, Cyperus sensu stricto, Courtoisina,
Pycreus, Kyllinga, Queenslandiella, Sphaerocyperus, Remirea, and Volkiella. Oxycaryum,
Kyllingiella and Alinula have a spiral glume arrangement, while the spikelet is too
reduced in Ascolepis and Lipocarpha for interpretation of glume arrangement
(Goetghebeur, 1998). Distichous glume arrangement has evolved more than once
in Cypereae, occurring in both the Ficinia and Cyperus clades, and is therefore not
unique in Cyperus sensu stricto. The unreliability of distichous arrangement as a
diagnostic character has been previously shown (e.g. Raynal, 1973), and evident
from our study where taxa with the Cyperus-like distichous glume arrangement
(e.g. Isolepis levynsiana) are resolved in the Ficinia clade.
Hypogynous Scales
Hypogynous scales, a character considered plesiomorphic in Cyperoideae, are found
in Scirpeae, Fuireneae, Eleocharideae, Dulichieae, and Schoeneae but are absent
from Abildgaardieae and Cypereae (Goetghebeur, 1998). Scirpus falsus and S.
ficinioides, resolved in Cypereae in molecular phylogenetic analyses (Fig. 1), have
bristle-like perianth segments. Similar perianth segments, some well developed
and others rudimentary, have been observed in Ficinia material (Muasya et al.,
unpublished results).
Some florets in Hellmuthia have two scales, which have been suggested to be
homologous to scales in Mapanioideae (Haines & Lye, 1976; Goetghebeur, 1998).
Recent floral ontogenetic studies (Vrijdaghs et al., 2006) have revealed an adaxially
situated third scale in some proximal flowers in spikelets of Hellmuthia, and these
are interpreted to be perianth segments and not glumes of reduced florets as in
Mapanioideae. Hellmuthia is resolved in the DNA phylogeny among the Ficinia
clade and closely related to Scirpus falsus and S. ficinioides.
Gynophores
The gynophore in Cypereae, formed by the development of the hypogynous stalk, is
characterised by a lobed cup that envelops the basal part of the nutlet (Vrijdaghs
et al., 2005). This structure is absent from the rest of Cyperoideae except for Ficinia,
in which variation is observed in size and shape of the gynophore. However, some
Ficinia species lack a gynophore, while on the other hand some Isolepis species (e.g.
I. marginata) have a rudimentary gynophore (Clarke, 1898; Levyns, 1950; Muasya
et al., 2000c, 2001a). A gynophore is present in Alinula lipocarphoides, a taxon
previously described in Ficinia and later transferred to Alinula (Kükenthal, 1936;
Raynal, 1977), here resolved in the Cyperus clade as sister to Lipocarpha.
Kranz Anatomy
As in most angiosperms families, the plesiomorphic photosynthetic system in most
of Cyperaceae is C3 type. Multiple origins of Kranz anatomy are recorded in several
lineages including Rhynchospora, Eleocharis, Fimbristylis and Cyperus (Raynal,
What is a genus in Cypereae
61
1973; Estelita, 1993; Goetghebeur, 1998; Soros & Bruhl, 2000; Muasya et al., 2002;
Bruhl & Wilson, 2007). Among Cypereae, Kranz anatomy has evolved once among
Cyperus clade and is recorded in Fig. 1 between Cyperus cuspidatus to Alinula
lipocarphoides. Bruhl & Wilson (2007) erroneously reported Volkiella to be C3,
while in the supporting references they show isotopic carbon reading (−13.6) which
is typical for C4.
Samples of Alinula paradoxa and Lipocarpha rehmannii, reported to be C3
(Stock et al., 2004), might have been based on wrongly identified material,
especially since there are four other records as C4 for L. rehmannii (Bruhl and
Wilson, 2007), and recent carbon isotope studies have confirmed other samples of
these taxa to be C4 (Muasya, unpublished results).
Inflorescence Morphology
Inflorescence morphology varies greatly in Cypereae. The basic inflorescence has
spikelets in a panicle (Raynal, 1971), which is often modified into an anthela or
contracted into a capitate head, spike or reduced to a single spikelet (Goetghebeur,
1998). In Cyperus, C3 taxa tend to have the spikelets arranged in digitate clusters,
which is one of the few morphological characters to distinguish the C3 and C4 taxa
(which are usually spicately arranged), apart from those species that have the
inflorescence reduced to a head (Goetghebeur, 1998). Kükenthal (1935–1936) used
this (only partly correctly) to subdivide his subgenus ‘Eu-cyperus’, while Raynal
(1973) also noted this (as not being a simple dividing character) particularly in
discussing the origins of the ‘Mariscus’ group of species.
Spikelets in a majority of Cypereae have many flowers. Several genera (e.g.
Lipocarpha, Ascolepis, Alinula) have pseudo-spikelets, in which spikelets are
reduced to single flowers (glumes lost) arranged in cones, each single-flower
spikelet subtended by a glume-like bract. The resulting cone resembles a spikelet
(Haines & Lye, 1983; Goetghebeur & Vorster, 1988) hence the use of the term
‘pseudo-spikelet’.
Elongation of Filaments
Stamen filaments in most members of Cyperoideae are nearly as long as the glumes
and inconspicuous after anthesis. Androtrichum trigynum and A. giganteum have
filaments strongly elongating after anthesis, giving the inflorescence a cotton-like
look. Such elongation of filaments is not observed in any other species in
Cyperoideae.
Dispersal unit
Nutlets (also called achenes by some authors, e.g. Goetghebeur, 1998) in members
of Cypereae are dispersed singly or together with elongated filaments, one to a few
glumes, or parts of the spikelet axis, or even as complete spikelets (Kükenthal,
1935–1936; Raynal, 1973; Haines & Lye, 1983; Goetghebeur, 1998; Table 2).
Courtoisina, Queenslandiella, Kyllinga, Remirea, Sphaerocyperus, Lipocarpha, and
Ascolepis have spikelets dispersing as intact units, whereas all taxa in the Ficinia
62
A.M. Muasya, et al.
clade, Kyllingiella, Pycreus, Oxycaryum, and Remirea have nutlets dispersed singly.
Cyperus has nutlets dispersed either singly or as whole spikelets or variants thereof
(notably in Cyperus odoratus).
Nutlet Orientation
Two kinds of nutlet orientation are observed in Cypereae (Table 2). Dorsiventral
nutlet orientation is the most common and plesiomorphic state (Kükenthal, 1935–
1936; Goetghebeur, 1998; Muasya et al., 2001b). Within Cypereae and Cyperaceae,
species with distigmatic styles and dorsiventrally compressed nutlets are observed.
Only the genera Kyllinga, Pycreus, and Queenslandiella have lateral nutlet
orientation with distigmatic styles and laterally compressed nutlets.
Generic Circumscription
Cypereae are defined here as including all taxa sharing the Cyperus-type of embryo.
We expand the tribal circumscription to include characters states such as the
occasional presence of floral scales and bristle-like perianth segments, observed in
the Ficinia clade.
The Ficinia Clade
Taxa in this clade have a predominantly spiral glume arrangement, but note the
presence of distichous glume arrangement in Ficinia and Isolepis. All the genera
share ficinioid morphology, e.g. tufted perennials, spiral glume arrangement, and
have a center of diversity in the Cape floristic region of South Africa (Goetghebeur,
1998; Archer, 1998; Muasya & Simpson, 2002; Muasya, 2005). The individual
genera are diagnosed by a combination of several characters (Table 2), the most
notable being the presence of a gynophore and ligule in Ficinia (including
Desmoschoenus), presence of two or three scales in the lower florets in Hellmuthia,
and perennial growth form and spiral glume arrangement in Scirpoides, whereas
Isolepis includes predominantly annual species with a spiral glume arrangement.
Two annual species (Isolepis leucoloma and I. levynsiana) with distichous glumes
previously described in Cyperus have been transferred to Isolepis, based on
morphological and molecular data (Archer, 1998; Muasya et al., 2006, 2007).
There is overlap in generic limits between Isolepis and Ficinia as presently
recognised, whereas Desmoschoenus is embedded in Ficinia (Fig. 1). An annual
species with rudimentary gynophore described as Isolepis (I. marginata) is resolved
in DNA analysis as more closely related to Ficinia. Desmoschoenus and Sickmannia
(Ficinia radiata), taxa with a gynophore but with additional unique features, have
been recognised as distinct from Ficinia. Phylogenetic results presented here (Fig. 1)
show that these taxa are embedded in Ficinia, and should be recognized as members
of Ficinia. Sickmannia has already been recognised as Ficinia (F. radiata) in recent
treatments (Goetghebeur, 1998; Archer, 2000), whereas Desmoschoenus spiralis, a
New Zealand endemic growing in the same coastal habitat as Ficinia nodosa, has no
name in Ficinia. More studies are in progress to resolve relationships in the Ficinia
clade.
What is a genus in Cypereae
63
Two of the Scirpus species, S. falsus and S. ficinioides from southern Africa, have
the gross morphology of the Ficinia clade, including perennial habit, scapose culms,
pseudolateral inflorescences, and spiral glumes. Presence of perianth segments has
been used to include these taxa in Scirpus (e.g. Kunth, 1837; Clarke, 1898; GordonGray, 1995) even though typical Scirpus has paniculate inflorescences and nodded
culms. So far no embryo studies have been done on these taxa, and attempts to
locate appropriate material have not been successful as the taxa rarely produce
mature nutlets. Phylogenetic studies resolve these taxa as sister to Hellmuthia
(Fig. 1), a pattern that suggests evolution from a southern African ancestor, unlike
Scirpus, which is Holarctic. A new genus should be erected to include these two
taxa, and more studies are in progress to formalise the recognition of this genus.
The Cyperus Clade
Genera in the Cyperus clade are circumscribed by a combination of morphological
characters including spikelet morphology, unit of dispersal, and nutlet orientation
(Table 2). Although these genera can be grouped into C3 and C4 anatomical types,
there are few observable gross morphological characters to separate the species of
Cyperus sensu stricto with the two kinds of anatomy.
Among C3 genera, Androtrichum is diagnosed by the presence of elongated
stamen filaments that are persistent and dispersed with the nutlets. However, the two
taxa, A. giganteum and A. trigynum, are not sister (Fig. 1) and their shared character
state, presence of elongated filaments, may be a parallel adaptation to dispersal in
swampy coastal dunes. Kyllingiella and Oxycaryum, previously classified in
Scirpeae (e.g. Bruhl, 1995), have a spiral glume arrangement unlike C3 species of
Cyperus sensu stricto, which have a distichous glume arrangement (Lye, 1971;
Haines & Lye, 1978). Courtoisina has similar morphology to C3 species of Cyperus,
but the whole spikelet is dispersed intact.
The C4 genera include a number that are monotypic or with few species (i.e.
Queenslandiella, Sphaerocyperus, Remirea, Volkiella, and Alinula), which are
separated from the larger genera by a combination of characters. Among the clearly
recognizable larger genera are Kyllinga, and Pycreus (together with monotypic
Queenslandiella), which have laterally flattened nutlets. Alinula, Volkiella, Ascolepis,
and Lipocarpha have highly reduced spikelets. The C4 species of Cyperus sensu
stricto have spikelets comprising more than one floret and dorsiventrally compressed
nutlets.
There are differences in opinion on whether to recognise Cyperus sensu lato, in a
very broad sense with a number of subgenera (e.g. subgenus Kyllinga, and C3 and
C4 species of Cyperus sensu stricto in different subgenera; e.g. Kükenthal, 1935–
1936), or in a narrow sense with various segregate genera (with Cyperus sensu
stricto including C3 and C4 species; e.g. Goetghebeur, 1998). Our results show
Cyperus sensu stricto to be polyphyletic, and merging all the segregate taxa into
broadly circumscribed Cyperus sensu lato and recognizing various segregates as
subgenera would make a monophyletic entity. However, this option is not favored
because it would result in a big genus (c. 900 species) and reduce taxonomic clarity.
Other partial merging of the taxa into Cyperus, recognizing Oxycaryum, Kyllingiella,
Sphaerocyperus, Remirea, Lipocarpha, and Ascolepis as distinct, but treating
64
A.M. Muasya, et al.
Courtoisina, Kyllinga, Pycreus, Queenslandiella, and Alinula as subgenera of
Cyperus (e.g. Haines & Lye, 1983; Lye, 1997) is not supported by this study.
We follow Goetghebeur (1998) in recognizing Cyperus sensu stricto and
recognizing the segregate taxa at generic rank (Table 2) pending more intensive
phylogenetic studies to get a full resolution of their relationships.
Future Research
Molecular phylogenetic studies have focused more attention on the Ficinia clade
(38% sampling) and less on the Cyperus clade (5% sampling), yet Cyperus clade
exhibits wide morphological variation. With more intensive molecular phylogenetic
studies and more extensive sampling to include the complete diversity of growth
form and morphological types, we expect a better understanding of character
homology, which will allow better-informed decisions about generic limits.
Acknowledgements AMM acknowledges a visiting postdoctoral fellowship from the Belgian Fund for
Scientific Research-Flanders (FWO-Vlaanderen, G.0104.01N) and a grant from the K.U. Leuven (grant F/
02/052) during the period this paper was prepared.
Open Access This article is distributed under the terms of the Creative Commons Attribution
Noncommercial License which permits any noncommercial use, distribution, and reproduction in any
medium, provided the original author(s) and source are credited.
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