Plant Syst. Evol. 246: 89–107 (2004)
DOI 10.1007/s00606-004-0128-0
Carex, subgenus Carex (Cyperaceae) – A phylogenetic approach
using ITS sequences
M. Hendrichs, F. Oberwinkler, D. Begerow, and R. Bauer
Universität Tübingen, Botanisches Institut, Lehrstuhl Spezielle Botanik und Mykologie,
Tübingen, Germany
Received August 6, 2003; accepted December 5, 2003
Published online: March 26, 2004
Ó Springer-Verlag 2004
Abstract. To evaluate the sectional classification in
Carex, subgenus Carex, the ITS region of 117
species belonging to 32 sections was analyzed with
Neighbor Joining (NJ) and Markov chain Monte
Carlo (MCMC) methods. In our analyses (1)
species of subgenus Indocarex appear as a statistically well supported group within subgenus Carex.
(2) The representatives of sections Vesicariae,
Hirtae, Pseudocypereae, Ceratocystis, Spirostachyae, Bicolores, Paniceae, Trachychlaenae, Scirpinae,
Atratae and Albae group in statistically supported
clades with higher support in MCMC than in NJ.
(3) C. rariflora clusters with representatives of
section Limosae, however only weakly supported.
(4) Taxa of section Phacocystis are divided in two
statistically supported subclusters that are closely
related to a core group of section Hymenochlaenae.
(5) Species of sections Montanae, Pachystylae,
Digitatae, Phacocystis, Rhomboidales, Careyanae
and Frigidae are segregated into two or more
clusters each. (6) Five species of section Frigidae
cluster together, whereas the seven others are in
scattered positions. Based on these results, delimitation of sections is discussed.
Key words: Bayesian analysis, Carex, ITS, molecular
phylogeny, systematics.
The genus Carex L. is widespread mainly in
the northern hemisphere with approximately
2000 species (Reznicek 1990). In a worldwide
taxonomic survey of the genus Kükenthal
(1909) confirmed the subdivision of the genus
Carex into the subgenera (Eu-)Carex, Indocarex, Vignea and Primocarex. Subgenus Carex
comprises some three quarters of the species
(Kükenthal 1909, Mackenzie 1931–1935,
Chater 1980, Ball 1990). They have a worldwide distribution, with most of them occuring
in the northern hemisphere. The inclusion of
subgenus Indocarex, often assumed as not
clearly separable from subgenus Carex (Koyama 1962, Reznicek 1990), would considerably
enlarge the geographic distribution of subgenus Carex to the subtropics and tropics of East
Asia and Central America. Kükenthal (1909)
distinguished 48 sections and subsections
within subgenus Carex. Since then, many
additional species have been described but no
new classification on a worldwide scale has
been proposed.
Recent molecular phylogenetic studies in
Cyperaceae using the rbcL gene (Muasya
et al. 1998), chloroplast DNA sequences
(Yen and Olmstead 2000), and ITS data
(Roalson et al. 2001, Starr et al. 1999,
Waterway and Olmstead 1998) have given
new insight in the relationships between the
90
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
genera of Cariceae. Mainly species of section
Acrocystis have been analyzed by Roalson
et al. (2001). That study focused on the
North American species and has shown the
potential of the ITS region for phylogenetic
interpretations on sectional level. We studied
62 species mainly from northern Europe;
furthermore, sequences of 55 species derived
from GenBank were included in this work
(see Table 1). Thus, our molecular analyses
comprise 117 species of 32 sections in total.
Section delimitations will be discussed in
detail and compared with the classical
concept proposed by Kükenthal (1909).
Materials and methods
Plant collection and DNA extraction. The analyzed
Carex species are listed in Table 1. Assignment of
sections and subsections corresponds mainly to
the concept of Kükenthal (1909). Total genomic
DNA was isolated from fresh or dried leaf tissue
either by crushing the plant material in liquid
nitrogen or by shaking the samples for 3 min at
30 Hz (Mixer Mill MM 300, Retsch, Haan,
Germany). DNeasy Plant Mini Kit (Qiagen,
Hilden, Germany) was used following the manufacturer’s protocol.
PCR and sequencing. The ITS region (about
700 bp) localized between the 18S and the 28S
rRNA genes, was amplified with the primer pair
ITSL (Hsiao et al. 1995) or ITS5, respectively, and
ITS4 (White et al. 1990). Amplification parameters
were as described in Starr et al. (1999). We adjusted
the annealing temperature to 54 °C for ITS5 and
51 °C for ITSL, the annealing time to 55 s, and the
extension time to 3 min. The product was purified
with QIAquick PCR Purification Kit (Qiagen,
Hilden, Germany). The dsDNA obtained was
sequenced directly on both strands using the ABI
PRISM Big DyeTM Terminator Cycle Sequencing
Ready Reaction Kit (PE Applied Biosystems) on
an automated sequencer (ABI 373A, PE Applied
Biosystems). The sequences of both strands were
combined and proof read with SequencherTM 4.1
software (Gene Codes Corp., Michigan).
All sequences reported in this study have been
deposited in GenBank (see Table 1).
The alignment contained 638 nucleotide sites.
After removing ambiguously aligned positions
(221–237, 416–436, 588–595), 592 sites remained
for analyses with 246 variable sites (ITS1: 141, 5.8S:
6, ITS2: 99). The ingroup alone contained 238
variable sites. The alignment is available upon
request.
Phylogenetic analysis. DNA sequences were
aligned using Clustal X (Jeanmougin et al. 1998).
Some manual corrections were done in Se-Al
v2.0a7b (Rambaut 2001) to improve ambiguously
aligned positions.
The likelihood ratio test as implemented in
Modeltest 3.0 (Posada and Crandall 1998) selected
GTR + I + G (Swofford et al. 1996) as DNA
substitution model (details below).
A Bayesian method of phylogenetic inference
using a Metropolis-coupled Markov chain Monte
Carlo (MCMC) approach was carried out as
implemented in the program MrBayes (Huelsenbeck
and Ronquist 2001) with GTR + I + G as substitution model. Four incrementally heated simultaneous Monte Carlo Markov chains were run over
2 000 000 generations. Trees were sampled every
100th generation, resulting in an overall sampling of
20 000 trees. To obtain estimates for the a posteriori
probabilities, a 50% majority rule consensus tree
was computed from the trees sampled after the
process had reached stationarity (burnin ¼ 2000).
This Bayesian approach of phylogenetic analysis
was repeated eight times, always using random
starting trees and random starting values for the
model parameters to test the reproducibility of
the results. Branch lengths were estimated under the
maximum likelihood criterion and the same substitution model in PAUP 4.0b10 (Swofford 2002).
Neighbor joining analysis (Saitou and Nei 1987)
was done with PAUP 4.0b10 (Swofford 2002) using
genetic distances according to GTR + I + G as
substitution model with the following settings:
base frequencies A ¼ 0.154109, C ¼ 0.307645,
G ¼ 0.366090, T ¼ 0.172156; rate matrix AC ¼
1.11373, AG ¼ 3.97984, AT ¼ 0.93190, CG ¼
0.32777, CT ¼ 6.41726, GT ¼ 1.00000; proportion
of invariant nucleotide sites ¼ 0.495368 and gamma
distribution shape parameter ¼ 0.729428. Support
for internal nodes was estimated by 1000 neighbor
joining bootstrap replicates under the same model
settings.
The unrooted phylograms from neighbor joining and MCMC analyses were rooted with three
Carex species of subgenus Vignea that clustered
together with high bootstrap support.
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
91
Table 1. Species analyzed in this study
Species
C.
C.
C.
C.
C.
C.
C.
C.
acuta L.
acutiformis Ehrh.a
acutiformisb
alba Scop.
alma Bailey
angarae Steud.
angustata Boott
antoniensis A. Chev.
C. aquatilis Wahlenb.a
C. aquatilisb
C. atrata L.
C. atrofusca Schkuhr
C. aurea Nutt.
C. austroalpina Becherer
C. bella Bailey
C. bicolor All.
C. bigelowii
Torr. ex Schwein.
C. brachystachys Schrank
(& Moll)
C. brevicollis DC.
C. brunnea Thunb.
C. buxbaumii Wahlenb.
C. canescens L.
C. capillaris L.
Chromos.
no. (2n)b
(Phacocystis Dumort.)
Paludosae Fries
USSR, Siberia
78
Germany, FO 7501
USSR, Kazakh SSR
54
Switzerland, HMH 2857
USA, California
USSR, Magadan Oblast
66, 68
USA, Idaho
Cape Verde Islands,
Santo Antao
72, 74, 76, Canada, Salt Plains,
79–80, 84
TUB
Finland, HeRB 4634
54
Sweden, HMH 2758
36, 38, 40 Sweden, HMH 2652
AF284992
AY278300
AF284993
AY278259
AF285025
AF284980
AF285015
AF285041
52
40
USA, California
Italy, HeRB 4252
AF285062
AY278276
40
50, 52
USA, New Mexico
Switzerland, FO 11601
AF284966
AY278283
68, 70, 71
Finland, HeRB 4626
AY278303
40
AY278277
54
Spain, Pyrenees,
HeRB 5336
USSR, Moldavian SSR
China, Guizhou
Germany, HMH 1896
USSR, Siberia
Sweden, HMH 2651
AF285011
AF285003
AY278262
AF284990
AY278256
44, 64?
USA, Vermont
AF285058
28
52, 54, 56
Canada, Quebec
USA, Oregon
USA, Texas
AF284976
AF284965
AF285029
48
48, 50, 52
Germany, HeRB 2761
USA, North Carolina
Germany, WM 364
AY278307
AF285035
AY278267
68?, 70–72, Germany, HMH 1854
74
Mexico, Chiapas
54
Canada, British
Columbia
74, 76
Germany, HeRB 4177
AY278312
Albae Asch. & Graebn.
Multiflorae Kunth
Atratae Kunth
(Phacocystis Dumort.)
(Pseudocypereae Tuck.)
(Phacocystis Dumort.)
Atratae Kunth
Frigidae Fries,
Fuliginosae Tuck.
(Bicolores Tuck.)
Frigidae Fries,
Ferrugineae Tuck.
Atratae Kunth
Acutae Fries,
Bicolores Tuck.
(Phacocystis Dumort.)
C. distans L.
Frigidae Fries,
Curvicolles Kük.
Rhomboidales Kük.
(Graciles Tuck.)
Atratae Kunth
Canescentes Fries
(Capillares Asch. &
Graebner)
Hymenochlaenae Drejer,
Longirostres Kük.
Montanae Fries
(Digitatae Fries)
Hymenochlaenae Drejer,
Debiles Carey
(Ceratocystis Dumort.)
Careyanae Tuck.
Digitatae Fries,
Eu-Digitatae Kük.
Spirostachyae Drejer
C. donnell-smithii Bailey
C. eburnea Boott
Fecundae Kük.
Albae Asch. & Graebn.
C. elata All.
(Phacocystis Dumort.)
C. castanea Wahlenb.
C. communis Bailey
C. concinnoides Mack.
C. debilis Michx.
C. demissa Hornem.
C. digitalis Willd.
C. digitata L.
Locality/Voucherc
Section and
subsectiona
56
62
74, 106
GenBank
accession no.
AY278302
AY278301
AY278263
AY278313
AF285005
AF285000
AY278255
92
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
Table 1 (continued)
Species
Section and
subsectiona
Chromos.
no. (2n)b
Locality/Voucherc
GenBank
accession no.
C. eleusinoides Turcz.
(Phacocystis Dumort.)
ca. 60, 84
AF285006
C. ericetorum Pollich
C. exsiccata Bailey
Montanae Fries
Physocarpae Drejer,
Vesicariae Tuck.
Spirostachyae Drejer
Paniceae Tuck.
Frigidae Fries,
Ferrugineae Tuck.
Indicae Tuck.,
Gracilirostres Kük.
Frigidae Fries,
Ferrugineae Tuck.
Trachychlaenae Drejer
(Ceratocystis Dumort.)
Frigidae Fries,
Fuliginosae Tuck.
Frigidae Fries,
Fuliginosae Tuck.
Scirpinae Tuck.
Pachystylae Kük.
Hymenochlaenae Drejer,
Gracillimae Carey
Pachystylae Kük.
Hirtae Tuck.
Trachychlaenae Drejer
30
40
USSR, Buryatskaya
ASSR
Germany, HeRB 3929
Canada, British
Columbia
Germany, HeRB 1557
USSR, Magadan Oblast
France, HMH 2082
AY278311
AF285016
AY278275
44, 48
China, Sichuan
AF284981
34
Germany, HMH 1180
AY278279
76, 90?
60, 62
56
Germany, HMH 2993
AY278274
Germany, HMH 1869
AY278310
Switzerland HeRB 6360 AY278291
40
Sweden, HMH 2729
58
USA, California
AF285027
USSR, Magadan Oblast AF285049
USA, Vermont
AF285054
C. extensa Good.
C. falcata Turcz.
C. ferruginea Scop.
C. filicina Nees
C. firma Host
C. flacca Schreb.
C. flava L.
C. frigida All.
C. fuliginosa Schkuhr
C. gigas (Holm) Mack.
C. globularis L.
C. gracillima Schwein.
C. grioletii Roemer
C. hirta L.
C. hispida Willd. ex
Schkuhr
C. hostiana DC.
C. humilis Leysser
C. kitaibeliana Degen
ex Becherer
C. lanceolata Boott
C. lasiocarpa Ehrh.
C. laxiflora Lam.
C. lemmonii Boott
C. lepidocarpa Tausch
C. leucodonta Holm
C. limosa L.
C. liparocarpos Gaudin
C. lupulina Muehlenb.
ex Willd.
C. lurida Wahlenb.
60
50, 52, 54
AY278281
AF285055
AY278254
48
USSR, SFSR, Sochi
112, (114?) Germany, HMH 513
42
Italy, FO 9266
AF285048
AY278296
AY278272
(Ceratocystis Dumort.)
Digitatae Fries,
Eu-Digitatae Kük.
(Frigidae Fries)
56
36
France, HMH 2140
Germany, WM 360
AY278309
AY278260
36
Bosnia, FO 16810
AY278258
Digitatae Fries,
Eu-Digitatae Kük.
Hirtae Tuck.
68–80
Japan, Kanagawa Pref. AF285009
(56?), 76,
77
40?
Sweden, HMH 2788
AY278297
64
38
56
USA, Texas
USA, California
Germany, HeRB 1511
USA, Arizona
Austria, FO 21960
Italy, HeRB 4258
USA, Texas
AF284964
AF284971
AY278293
AF284973
AY278298
AY278261
AF284963
64, 66
USA, North Carolina
AF284962
Careyanae Tuck.
(Ferrugineae Tuck.)
(Ceratocystis Dumort.)
Montanae Fries
Limosae Tuck.
Lamprochlaenae Drejer
Physocarpae Drejer,
Lupulinae Tuck.
Physocarpae Drejer,
Tentaculatae Tuck.
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
93
Table 1 (continued)
Species
Section and
subsectiona
Frigidae Fries,
Fuliginosae Tuck.
C. mairii Cosson & Germ. Spirostachyae Drejer
C. mandshurica Meinsh.
Pachystylae Kük.
Chromos.
no. (2n)b
C. luzulina Olney
C. microdonta Torr.
& Hook.
C. mira Kük.
C. montana L.
C. mucronata All.
C. nigra (L.) Reich.
ssp. juncella
C. norvegica Retz.
ssp. media
C. olbiensis Jordan
C. ornithopoda Willd.
Locality/Voucherc
GenBank
accession no.
AY278252
(Granulares O. Lang)
64
USA, Washington,
FO 30632
France, FO 9499b
Korea, Kangwon
Province
USA, Texas
Frigidae Fries,
Mucronatae Nyman
Montanae Fries
Frigidae Fries,
Mucronatae Nyman
(Phacocystis Dumort.)
42
Korea, Kangwon Prov. AF285046
38
36
Germany, HMH 1421
Italy, HMH 2240
AY278271
AY278257
84
Germany, FO 29072
AY278304
Atratae Kunth
56
Switzerland, HMH 3004 AY278264
46
54
Italy, FO 9331
Germany, HMH 2964
AY278282
AY278269
54, 56
Austria, HeRB 6362
AY278268
Careyanae Tuck.
Digitatae Fries,
Eu-Digitatae Kük.
C. ornithopodioides Hausm. Digitatae Fries,
Eu-Digitatae Kük.
C. otrubae Podp.
Stenorhynchae Holm
C. oxyandra Kudo
(Montanae Fries)
C. pallescens L.
Pachystylae Kük.
C. panicea L.
Paniceae Tuck.
C. parviflora Host
Atratae Kunth
C. paupercula Michx.
(Limosae Tuck.)
C. pedunculata Muehlenb. Digitatae Fries,
Eu-Digitatae Kük.
C. pellita Willd.
Hirtae Tuck.
C. pennsylvanica Lam.
Montanae Fries
C. picta Steud.
Digitatae Fries,
Eu-Digitatae Kük.
C. pilosa Scop.
Rhomboidales Kük.
C. pilulifera L.
Montanae Fries
C. polystachya Swartz
Indicae Tuck.,
ex Wahlenb.
Turgidulae Kük
C. prasina Wahlenb.
Hymenochlaenae Drejer,
Gracillimae Carey
C. pseudocyperus L.
Pseudocypereae Tuck.
C. rariflora (Wahlenb.) Sm. Limosae Tuck.
C. raynoldsii Dew.
Atratae Kunth
C. rossii Boott
Montanae Fries
C. rostrata Stokes
Physocarpae Drejer,
Vesicariae Tuck.
C. rugosperma Mack.
Montanae Fries
68, 70
AY278253
AF285045
AF285052
USSR, Crimea
18, 20, 24 Japan
64, 66, 70? France, HMH 2105
32
Germany, HMH 1779
54
Switzerland, HeRB 6361
58, 60
Finland, HeRB 4652
26
USA, Michigan
AF284996
AF285061
AY278299
AY278284
AY278265
AY278292
AF284969
78, 81, 82
36
32
USA, California
USA, Michigan
USA, Alabama
AF285031
AF284977
AF285020
44
18
Germany, HeRB 4598
AY278286
Denmark, HMH 1934
AY278280
Brazil, Federal District AF285014
USA, North Carolina
AF285043
66
52, 54
58
36
60?, 76
Germany, HMH 2991
Norway, HeRB 6359
USA, Idaho, FO 30938
USA, Oregon
Germany, HMH 1827
AY278295
AY278305
AY278266
AF284972
AY278294
32?
USA, Pennsylvania
AF284978
94
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
Table 1 (continued)
Species
Section and
subsectiona
Chromos.
no. (2n)b
Locality/Voucherc
GenBank
accession no.
C. saxatilis L.
Physocarpae Drejer,
Vesicariae Tuck.
(Phacocystis Dumort.)
Scirpinae Tuck.
80
Sweden, HMH 2574
AY278288
62, 64, 68
USA, California
USA, Utah
AF285037
AF285050
(Phacocystis Dumort.)
72, 76, 80
USA, Oregon
AF285059
Germany, HMH 1156
AY278278
Italy, FO 32901
USA, California
Germany, WM 2015
AY278273
AF285040
AY278306
58
66
Germany, HMH 1777
USSR, Kazakhstan
USA, Wyoming
Germany, HMH 2253
AY278287
AF285047
AF285051
AY278270
60
USSR, Siberia
AF285042
30, 32
82, 86
Sweden, HMH 2684
Germany, HMH 1782
AY278285
AY278289
ca. 72
Canada, NWT, TUB
AY278308
Switzerland, HMH 1856 AY278290
Japan, Shizuoka Pref. AF285023
C. schottii Dew.
C. scirpoidea Michx.
ssp. scirpoidea
C. scopulorum Holm
var. bracteosa
C. sempervirens Vill.
C. serrulata Biv.
C. spissa Bailey
C. sylvatica Huds.
C.
C.
C.
C.
tomentosa L.a
tomentosab
torreyi Tuck.
umbrosa Hosta
C. umbrosab ssp.
sabynensis
C. vaginata Tausch
C. vesicaria L.
C. viridula Michx.a
C. viridulab
C. wahuensis C. A. Mey.
ssp. robusta
C. whitneyi Olney
C. wiluica Meinsh. ex
Maack
Frigidae Fries,
30, 32, 34
Ferrugineae Tuck.
(Trachychlaenae Drejer)
Trachychlaenae Drejer
Hymenochlaenae Drejer, 58
Longirostres Kük.
Pachystylae Kük.
48
Pachystylae Kük.
Mitratae Kük.,
Eu-Mitratae Kük.
Paniceae Tuck.
Physocarpae Drejer,
Vesicariae Tuck.
(Ceratocystis Dumort.)
Rhomboidales Kük.
48?
62
Hymenochlaenae Drejer,
Pubescentes Kük.
(Phacocystis Dumort.)
ca. 50
USA, Nevada
AF285053
USSR, Siberia
AF285010
Origin of sequence: Roalson et al. 2001
Sections and subsections mainly follow the concept of Kükenthal (1909); others in brackets
b
Chromosome counts compiled from original literature (Cayouette and Morisset 1986; Crins and Ball
1988; Davies 1956; Dietrich 1964, 1967, 1972; Dunlop 1997; Dunlop and Crow 1999; Faulkner 1972, 1973;
Favarger 1965; Halkka et al. 1992; Heilborn 1922, 1924, 1928, 1939; Jörgensen et al. 1958; Kjellqvist and
Löve 1963; Löve and Löve 1981, 1982; Löve et al. 1957; Löve and Solbrig 1964; Luceño 1993; Martens
1939; McClintock and Waterway 1994; Moore and Calder 1964; Murı́n and Májovsky 1976; Naczi 1999;
Nishikawa et al. 1984; Reese 1953; Schmid 1983; Standley 1985; Tanaka 1942a, 1942b, 1949; Wahl 1940;
Whitkus 1981) or fide Chater (1980), Roalson et al. (2001) and FNA (2002)
c
Acronyms of herbaria and collections: HeRB: R. Berndt (private collection); HMH: M. Hendrichs
(private collection) FO: F. Oberwinkler (private collection); WM: W. Maier (private collection); TUB:
Herbarium Tubingense
a
Results
The different runs of the performed Bayesian
phylogenetic analysis yielded consistent
results. Stationarity of the Markov chains
was reached after approximately 200 000 generations of trees, i.e. after 2000 trees had been
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
sampled. Thus, we discarded the first 2000
trees and included 18 000 sampled trees in
the 50% majority rule consensus tree of each
run. One of these is given in Fig. 1. The
phylogram obtained by the NJ analysis is
shown in Fig. 2.
Our analyses include 117 species belonging
to 32 sections in subgenus Carex (see Table 1),
in which the sections Capillares, Graciles,
Granulares, Fecundae, Lamprochlaenae, Mitratae and Paludosae, are represented by one
species only. In general, the tree topology of
the MCMC analysis correlates with that of the
NJ analysis (compare Fig. 1 with Fig. 2).
Rooted with three species of subgenus
Vignea, the members of subgenus Carex
appear as a highly supported lineage. Furthermore, in both analyses the supported sectional
clusters contain the same representatives.
Thus, in both analyses the representatives of
subgenus Indocarex appear as a statistically
well supported group within subgenus Carex.
The representatives of sections Vesicariae,
Hirtae, Pseudocypereae, Ceratocystis, Spirostachyae, Bicolores, Paniceae, Trachychlaenae,
Scirpinae, Atratae and Albae form statistically
supported clades. C. rariflora clusters together
with the other representatives of section Limosae, however only weakly supported. In general, statistical support for these groups is
higher in the MCMC topology than in the NJ
topology. In both analyses the representatives
of sections Montanae, Pachystylae, Digitatae,
Phacocystis, Rhomboidales, Careyanae and
Frigidae fall into two or more clusters. Furthermore, in both analyses five species of
section Frigidae cluster together paraphyletically, referred to as section Ferrugineae in our
dendrograms. Seven other representatives of
section Frigidae included in our analyses are
scattered throughout the trees. In both analyses the representatives of section Phacocystis
fall into two statistically supported subclusters.
They are closely related to a core group of
section Hymenochlaenae.
While the ITS region is useful in defining sections within subgenus Carex, this
region does not provide enough phylogenetic
95
information to fully resolve relationships
among sections in subgenus Carex.
A tendency towards lower chromosome
numbers in more derived groups (Roalson
et al. 2001) is not supported by our analyses
(see below). Chromosome numbers of the
species studied are listed in Table 1, giving
the chromosome counts available in literature.
Discussion
The discussion of the sections mainly follows
their order of appearance in Fig. 1.
Section Vesicariae is represented in our
analyses by four species. The three-stigmatic
C. vesicaria and C. rostrata are very common
in Central Europe. Both are adapted to wet
habitats, the latter probably with a preference
to acid soil conditions. C. saxatilis, very
common in Northern European tundra vegetation, usually has two stigmas, rarely three.
These taxa cluster together with the threestigmatic C. exsiccata, which is adapted to the
same wet and marshy habitats in pacific North
America. Species delimitation causes considerable difficulties in this group. C. saxatilis was
treated as a subspecies of C. vesicaria by
Kükenthal (1909), but was also regarded as a
distinct species (e.g. Mackenzie 1931–1935,
Chater 1980, Reznicek and Ford 2002). C.
exsiccata was interpreted as variety of C.
vesicaria by several authors (e.g. Boott 1867,
Kükenthal 1909) but also as a separate species
(e.g. Bailey 1889, Mackenzie 1931–1935, Reznicek and Ford 2002). Our ITS data can
contribute to the understanding of the species
concept by basepair(bp)-differences. C. vesicaria and C. rostrata differ in three bp over the
total length of 638 bp, the difference between
C. vesicaria and C. saxatilis is only one bp. C.
exsiccata differs from C. vesicaria and C.
rostrata in four bp. Therefore it can be
concluded that C. exsiccata is separate from
C. vesicaria as well as C. rostrata. A very close
relationship of C. saxatilis and C. vesicaria has
to be assumed, although our specimens are
morphologically easily distinguishable: C.
saxatilis has more compact and very dark
96
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
C. saxatilis
C. exsiccata
C. vesicaria
C. rostrata
84
63
C. pellita
C. lasiocarpa
C. lupulina
C. lurida
100 C. pseudocyperus
84
C. antoniensis
100
C. paupercula
76
C. limosa
54
C. rariflora
C. donnell-smithii
52
C. prasina
100 C. aquatilis b
C. aquatilisa
64 87
C. angustata
C. schottii
98
C. elata
C. bigelowii
51
C. scopulorum
92
C. debilis
75
C. gracillima
86
81
C. castanea
C. whitneyi
C. nigra
86
C. acuta
C. wiluica
99
C. eleusinoides
C. atrata
89
C. norvegica
98
C. angarae
C. parviflora
100
C. raynoldsii
89
C. bella
C. buxbaumii
C. filicina
67
78
62
100
95
C. eburnea
C. humilis
C. lanceolata
C. communis
95
C. leucodonta
C. pilulifera
C. oxyandra
C. rossii
80
100
80
79
100
69
C. tomentosaa
C. tomentosab
85
C. hispida
98
Phacocystis 2
Atratae
Bicolores
C. laxiflora
Paniceae
Trachychlaenae
100
82
Ferrugineae
100
98
C. globularis
100
100
95
100
C. digitalis
C. microdonta
C. acutiformis a
C. acutiformis b
C. pallescens
C. torreyi
C. pedunculata
C. picta
C. ericetorum
C. viridulab
80 C. lepidocarpa
C. demissa
99
C. viridulaa
C. flava
C. hostiana
Granulares
Paludosae
"Digitatae 3"
Ceratocystis
C. sylvatica
C. umbrosa a
C. umbrosab
C. mandshurica
C. wahuensis
Mitratae
95
100
Graciles
"Montanae 3"
C. vaginata
C. falcata
C. panicea
C. pilosa
C. mucronata
INDOCAREX
C. polystachya
C. olbiensis
100
100
Hymenochlaenae
C. aurea
C. bicolor
C. spissa
C. serrulata
C. flacca
C. grioletii
100
C. ferruginea
C. austroalpina
C. brachystachys
C. sempervirens
C. firma
100
54
96
Phacocystis 1
100
92
88
Fecundae
Albae
"Digitatae 2"
100
77
67
Lupulinae
Pseudocypereae
Limosae
C. brunnea
C. alba
99
100
Hirtae
97
96
78
100
C. hirta
100
100
90
Vesicariae
62
82
C. distans
C. mairii
C. digitata
100
C. ornithopoda
C. ornithopodioides
C. brevicollis
C. fuliginosa
C. atrofusca
100
C. montana
C. mira
100
C. pennsylvanica
C. rugosperma
C. luzulina
C. lemmonii
100
C. gigas
C. scirpoidea
C. capillaris
C. kitaibeliana
C. liparocarpos
C. concinnoides
C. frigida
C. extensa
Spirostachyae
73
59
54
74
100
100
0.005 substitutions/site
Digitatae 1
Montanae 1+"2"
Scirpinae
Capillares
Lamprochlaenae
C. alma
C. canescens
C. otrubae
VIGNEA
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
pistillate spikes, is normally smaller, and has
mostly two stigmas. Many potential hybrids
between C. vesicaria and C. saxatilis have been
reported (Chater 1980; Ford et al. 1993, Cayouette and Catling 1992), named as C. grahamii
Boott on the British Isles, C. stenolepis Less. in
Southern Scandinavia and C. mainensis Porter
ex Britton in North America. They all share the
same ecology of wet and marshy, more calcareous grounds. As was shown for the shortbeaked taxa of section Vesicariae, including
C. saxatilis, allele frequencies of isozymes can
contribute to the problem of species delimitation (Ford et al. 1991).
The representatives of section Hirtae, C.
hirta, C. lasiocarpa and C. pellita, are related to
the former section. The American C. pellita is
more closely related to the European C. hirta
than to C. lasiocarpa from Sweden. This result
is not congruent with the chromosome counts
giving the maximal count in the whole genus
Carex of 2n ¼ 112 (Heilborn 1924, Davies
1956, Dietrich 1972) for the type species C.
hirta (Egorova 1971). A significantly lower
chromosome number is reported for the
American C. pellita (Löve and Löve 1981,
McClintock and Waterway 1994, Wahl 1940),
and exactly the half number for C. lasiocarpa.
(Reese 1953, McClintock and Waterway 1994).
As was shown in section Capillares (Löve et al.
1957) the differentiation of chromosomes in
classes based on length can give useful information to derivation, even if the simple chromosome count seems to be confusing.
The close affinity of section Lupulinae to
Vesicariae has never been doubted. Kükenthal
regarded both sections as subsections within
the section Physocarpae (Kükenthal 1909);
97
Mackenzie (1931–1935) also points out a close
relationship. Our data support the separation
of section Lupulinae (e.g. Mackenzie 1931–
1935, Fernald 1950) with C. lupulina and also
C. lurida included.
The two analyzed species of section
Pseudocypereae, C. pseudocyperus collected in
Germany and C. antoniensis from the Cape
Verde Islands, share identical ITS sequence. A
closer affinity of sections Vesicariae and Lupulinae and section Pseudocypereae is supported
by NJ analysis, corresponding with the classical concept (Kükenthal 1909, Mackenzie
1931–1935).
A closer relationship of sections Vesicariae,
Lupulinae, Hirtae and Pseudocypereae is indicated by our analyses (a posteriori probability
100%, bootstrap value 56%). This was suggested by various authors (e.g. Mackenzie
1931–1935, Reznicek 1990) mainly due to the
persistent style in most species. It is also
supported by anatomical data of transverse
sections of leafs and culms (Shepherd 1976)
and by hybridization patterns. The hybrids of
C. vesicaria and C. rostrata with C. pseudocyperus are common in Europe, the hybrids with
C. lasiocarpa and C. hirta are rarely found
(Kükenthal 1909, Chater 1980). From North
America a hybrid between C. lurida and C.
rostrata is known (Cayouette and Catling
1992). These frequent hybridizations result
from the highly similar ecological preferences
of wet to marshy and usually calcareous
habitats of all species within this group.
Section Limosae is a morphologically very
homogeneous section of small species with
characteristic pale-brown sheaths and a dense
yellowish indumentum on the roots. These
b
Fig. 1. Bayesian inference of phylogenetic relationships within the subgenus Carex. Metropolis-coupled
Markov chain Monte Carlo analysis of an alignment of nuclear sequences from the ITS region using the general
time reversible model of DNA substitution with gamma distributed substitution rates, estimation of invariant
sites, random starting trees, and random starting parameter values. Majority rule consensus tree from 18 000
trees that were sampled after the process had reached stationarity. The topology was rooted with Carex alma,
C. canescens and C. otrubae (subgenus Vignea). The numbers on branches are estimates of a posteriori
probabilities. Branch lengths were estimated using Maximum Likelihood settings and are scaled in terms of
expected numbers of nucleotide substitutions per site. The sectional concept applied mainly corresponds to
Kükenthal (1909) and Chater (1980). In section Hymenochlaenae only the core group is indicated
98
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
76 C. saxatilis
69
C. vesicaria
Vesicariae
C. exsiccata
59 50 C. rostrata
85
C. lupulina
Lupulinae
Pseudocypereae
C. lurida
55
93 C. pseudocyperus
C. antoniensis
C. hirta
C. pellita
C. lasiocarpa
C. paupercula
C. limosa
C. rariflora
C. donnell-smithii
C. prasina
54
C. pallescens
C. torreyi
C. acutiformisa
100
C. acutiformis b
C. globularis
70
C. pedunculata
C. picta
C. lepidocarpa
C. viridula a
85
C. demissa
79
C. viridula b
98
C. flava
C. hostiana
C. sylvatica
C. frigida
C. capillaris
C. extensa
64
71
C. distans
C. mairii
83 C. aquatilis b
53
C. aquatilisa
65 C. angustata
68
C. schottii
71
C. elata
C. bigelowii
C. scopulorum
83
72 C. nigra
C. wiluica
92 C. acuta
58
C. eleusinoides
66
C. debilis
C. gracillima
C. whitneyi
59
C. castanea
56
C. digitata
C. ornithopodioides
100
C. ornithopoda
100 C. aurea
C. bicolor
C. olbiensis
68
78
Hirtae
88
Limosae
Fecundae
Paludosae
"Digitatae 3"
Ceratocystis
Capillares
Spirostachyae
Phacocystis
Hymenochlaenae
Digitatae 1
Bicolores
C. laxiflora
76
93
89 C. vaginata
Paniceae
C. falcata
C. panicea
C. pilosa
C. tomentosa a
C. tomentosa b
96
C. pennsylvanica
C. rugosperma
C. ericetorum
C. digitalis
98
98
"Montanae 2"
C. microdonta
90
0.005 substitutions/site
100
C. mucronata
C. luzulina
C. lemmonii
C. atrofusca
C. fuliginosa
C. brevicollis
55
C. montana
C. mira
C. concinnoides
75 C. umbrosab
C. mandshurica
63
94 C. umbrosa a
C. wahuensis
96 C. hispida
72
C. spissa
97
C. serrulata
C. flacca
C. grioletii
99
C. ferruginea
86
C. austroalpina
C. brachystachys
98
C. sempervirens
C. firma
C. kitaibeliana
C. pilulifera
C. rossii
56
C. oxyandra
C. communis
64
C. leucodonta
C. liparocarpos
100
C. gigas
C. scirpoidea
C. norvegica
C. parviflora
C. angarae
C. buxbaumii
C. raynoldsii
86
51
C. bella
C. atrata
99 C. humilis
C. lanceolata
82 C. alba
74
C. eburnea
C. brunnea
95
C. filicina
C. polystachya
97
C. alma
C. canescens
C. otrubae
Granulares
Montanae 1
Mitratae
Trachychlaenae
Ferrugineae
"Montanae 3"
Lamprochlaenae
Scirpinae
Atratae
"Digitatae 2"
Albae
Graciles
Indicae (INDOCAREX)
VIGNEA
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
species share similar ecological preferences of
very wet and open peat. In our analyses C.
paupercula and C. limosa cluster together with
good support. C. rariflora, morphologically
and ecologically very similar to the latter
species, is in most analyses connected to
section Limosae but never with good support.
According to our data, section Limosae is not
closely related to section Atratae, as was
proposed by Crins (1990) on morphological
grounds.
C. donnell-smithii is the only representative
of section Fecundae in our analysis. The
position in the phylograms, indicated by NJ
and MCMC analysis, has to be verified by
additional sampling, including taxa from Central and South America.
C. prasina has been included in section
Hymenochlaenae (Kükenthal 1909) and was
considered closely related to C. gracillima
(Kükenthal 1909, Mackenzie 1931–1935). Our
molecular data do not support this interpretation.
Section Phacocystis comprises distigmatic
species within subgenus Carex. The species are
adapted to marshy and wet habitats and
usually grow in populations with high numbers
of individuals mainly in the northern temperate hemisphere. Kükenthal (1909) divided the
section in seven subsections, Mackenzie (1931–
1935) accepted six of them. Species delimitation is difficult in this section (Hjelmqvist and
Nyholm 1947; Sylvén 1963; Hylander 1966;
Faulkner 1972, 1973; Cayouette and Morisset
1986). For many species a hybrid origin was
presumed with the hybrids even staying fertile
(Lepage 1956, Dutilly et al. 1958, Faulkner
1973, Cayouette and Morisset 1985, Cayouette
and Catling 1992).
The eleven species of section Phacocystis,
analyzed in this study, form two well
99
supported sister clades. A first group comprises C. aquatilis, C. angustata, C. schottii,
C. elata, closely related to C. bigelowii and
C. scopulorum as members of Kükenthal’s
(1909) subsection Rigidae. The second group
contains C. eleusinoides as sister group of
C. acuta, C. wiluica, and C. nigra. An adequate
phylogenetic treatment of this section would
require worldwide sampling. Only in case of
C. angustata and C. schottii the geographical
distribution correlates strictly with the molecular grouping. For C. aquatilis we compared a
Canadian and a European specimen. Their ITS
sequences differ in only 1 bp – this similarity
again proves the wide distribution ranges of
northern hemispheric species. Our results for
section Phacocystis support the subsectional
grouping of the taxa proposed by Faulkner
(1973) on the basis of hybridization experiments. However, the groups proposed by
Standley (Standley 1987, 1989, 1990) after
clustering analysis of different anatomical
characters and cytological data are not fully
supported.
The former subsection Bicolores, comprising distigmatic species, was often treated
as a section of its own (e.g. Tuckerman 1843,
Mackenzie 1931–1935, Ball 2002a). This
separation is supported by our data (see
below).
Section Hymenochlaenae clusters together
with the two Phacocystis-groups in both analyses. This species-rich section is traditionally
divided into four groups for North America
(Mackenzie 1931–1935, Waterway 2002) or in
six subsections by Kükenthal (1909). We
studied eight species and found a core
group including the North American species C. debilis, C. gracillima, C. castanea,
and C. whitneyi. Another American species,
C. prasina, is not closely related to this clade
b
Fig. 2. ITS phylogram of the subgenus Carex obtained by neighbor joining analysis using the GTR+I+G
substitution model. The topology was rooted with Carex alma, C. canescens and C. otrubae (subgenus Vignea).
Percentage bootstrap values of 1 000 replicates are given at each furcation. Values smaller than 50% are not
shown. Branch lengths are scaled in terms of expected numbers of nucleotide substitutions per site. The
sectional concept applied mainly corresponds to Kükenthal (1909) and Chater (1980), respectively. In section
Hymenochlaenae only the core group is indicated
100
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
(Roalson et al. 2001). The treatment of
C. whitney in section Longicaules (comp.
Mackenzie 1931–1935, Egorova 1999, Mastrogiuseppe 2002) is not supported by ITS data.
Unexpectedly, C. sylvatica and C. capillaris
neither cluster together nor with any other
member of section Hymenochlaenae. This is in
contrast to the broad sectional concept of
Kükenthal (1909), who treated C. capillaris in
subsection Capillares. Later authors (e.g. Mackenzie 1931–1935, Egorova 1999, Ball 2002b)
separated both on sectional rank, which is
supported by molecular data. Thus, our
molecular data support the interpretation that
section Hymenochlaenae sensu Drejer (1844) is
heterogeneous as was proposed earlier considering morphological data (e.g. Ascherson and
Graebner 1902–1904, Mackenzie 1931–1935),
and recently by phylogenetic hypotheses based
on ITS and cpDNA sequences (Waterway
and Olmstead 1998, Roalson et al. 2001).
Chromosome counts were not applicable for a
better resolution of the species-rich Hymenochlaenae (Heilborn 1924, Davies 1956, Löve et al.
1957, Moore and Calder 1964, Dietrich 1972).
The seven species of the homogeneous
section Atratae included in our analyses form
a well supported clade in both analyses. The
section is well characterized by mostly bisexual
terminal spikes and the dark-colored scales
and perigynia. In the MCMC analysis,
C. atrata is closely connected to C. norvegica
and C. angarae. These two species differ in
5 bp in our alignment. C. parviflora, found
in Switzerland, seems closely related to
C. raynoldsii from Idaho and C. bella from
New Mexico. C. buxbaumii clusters within
section Atratae but has no closer relationship
to any species in the analyses. It also differs
considerably
in
chromosome
number
(Heilborn 1924, Löve and Löve 1981; compare
Table 1).
The two members of subgenus Indocarex
integrated in our analyses, C. polystachya and
C. filicina of section Indicae, cluster together
with high support. The Chinese C. brunnea, as
the only member of distigmatic section Graciles, clusters together with section Indicae
(Fig. 1) or section Albae (Fig. 2) respectively
(comp. Roalson et al. 2001). To clarify the
position of section Indicae, sampling of other
species of subgenus Indocarex and of Asian
species of related sections is required.
The two members of section Albae, C. alba
and C. eburnea, cluster together with high
support in all analyses. Kükenthal (1909)
considered these taxa to be identical, however
they can be easily separated by seven different
bp in ITS sequences.
MCMC analysis reveals high support for a
close relationship of section Indicae, subgenus
Indocarex, to section Albae. Thus, subgenus
Indocarex cannot be separated from subgenus
Carex as a subgenus of its own (e.g. Raymond
1959, Koyama 1962), as was shown previously
by Starr et al. (1999) and Roalson et al. (2001)
and is supported by chloroplast DNA data
(Yen and Olmstead 2000).
Section Digitatae is divided into three
distinct groups in the ITS hypotheses. The
European species C. digitata, C. ornithopoda,
and C. ornithopodioides strongly cluster together (Digitatae 1) underlining morphological
similarities. A second clade (‘‘Digitatae 2’’)
combines C. humilis with C. lanceolata, again
with high support. The sequence of Japanese
C. lanceolata is with 1 bp difference nearly
identical to C. humilis.
In some analyses the American C. concinnoides, characterized by a square achene and
four stigmas per pistil, groups with the European Digitatae 1, but without sufficient support.
C. pedunculata clusters together with the
dioecious C. picta in both analyses (‘‘Digitatae
3’’; a posteriori probability 100%, bootstrap
value 72%). Traditionally, C. picta was placed
in section Pictae, subgenus Primocarex.
Kükenthal (1909) already gives a hint to the
closer relationship of C. picta and C. pedunculata by referring to C. baltzellii as a member of
section Digitatae: ‘‘Species subgeneris Eucarex
ab hac derivata est C. Baltzellii Chapm.’’
(Kükenthal 1909, p. 82). This was followed
by later authors (e.g. Mackenzie 1931–1935,
Martens 1939, Ball 2002c) and can be
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
confirmed by molecular data (comp. Roalson
et al. 2001). Chromosome numbers of C. picta
(2n ¼ 32) (Löve and Löve 1981) and C. pedunculata (2n ¼ 26) (Löve and Löve 1981) are
low compared to the zygotic numbers of other
species of section Digitatae. Chromosome
numbers of C. digitata (Davies 1956), C.
ornithopoda and C. ornithopodioides are very
similar to each other with an average diploid
number of 52 (Heilborn 1924, Dietrich 1972).
Chromosome numbers in ‘‘Digitatae 2’’ differ
very much: C. humilis with zygotic number of
36 (Tanaka 1942b, Dietrich 1972, Murı́n and
Májovsky 1976) and C. lanceolata with a range
of counts from 68 to 80 (in Roalson et al.
2001).
Section Montanae appears non-monophyletic, too (Fig. 1). One group, designated
‘‘Montanae 3’’ comprises C. communis and C.
leucodonta together with C. rossii, C. pilulifera
and C. oxyranda. A second group (‘‘Montanae
2’’), not closely related to the first one, consists
of C. pennsylvanica, C. rugosperma and C.
ericetorum. The latter species does not cluster
in this group in MCMC analysis, though in
both groups European specimens are mixed
together with North American or Asian species. Thus, a geographical separation is not
supported. The namegiving C. montana (Montanae 1) clusters together with C. mira, and
appears on a common branch with the former
group in MCMC analysis. C. mira, integrated
in section Frigidae by Kükenthal (1909), was
classified as a member of section Montanae by
Ohwi (1936), which is verified by our molecular data. The non-monophyletic nature of
section Montanae recently was explained in
great detail by Roalson et al. (2001) and is
therefore not discussed here.
Two species of distigmatic section Bicolores
were studied in our analysis: C. bicolor collected in Switzerland and C. aurea from
California. Tuckerman (1843) separated section Bicolores from section Phacocystis
(Kükenthal 1909). C. eleusinoides, ascribed to
section Bicolores by Kükenthal (1909), was
treated as member of section Phacocystis by
Ohwi (1936), which is supported by our data.
101
Mackenzie (1931–1935) accepted this classification because of special characteristics of
perigynia and distribution of sexes in the
spikes. The ITS sequences of C. bicolor and
C. aurea differ only in 1 bp. Also chromosome
numbers are apparently identical (Davies 1956,
Dietrich 1972, Faulkner 1972, Löve and Löve
1981). A larger sampling, including Californian species C. hassei and C. garberi, is
required to clarify species delimitation of C.
aurea and C. bicolor.
In our phylograms two species of section
Careyanae, C. laxiflora from Texas and C.
olbiensis from Italy cluster between section
Bicolores and Paniceae. Another species, C.
digitalis, traditionally classified in section
Careyanae, clusters with C. microdonta, the
only representative of section Granulares integrated in our analyses. A close relationship of
section Careyanae and section Paniceae was
often postulated in previous studies based on
identical morphological characters, like perigynium structure and sheathing lowest bract
(e.g. Carey 1848, Kükenthal 1909, Mackenzie
1931–1935, Koyama 1962). Based on foliar
flavonoids, Manhart (1986) demonstrated that
the North American species of the broadly
defined section Careyanae can be separated in
two subgroups. This was supported by detailed
investigations in macro- and micromorphology (Bryson 1980, Naczi 1997) and by molecular data (Starr et al. 1999).
Section Paniceae forms a well supported
clade in NJ analysis (Fig. 2). The Russian C.
falcata is closely related to C. vaginata from
Swedish Lappland. The difference of only one
bp in ITS sequences raises the question how
to distinguish these species. In contrast, C.
panicea is well distinguished from C. vaginata
in its ITS sequence by 11 bp exchanges. The
chromosome number of the species within
this section is 2n ¼ 32 (Heilborn 1922, 1924;
Dietrich 1972; Löve and Löve 1981). The
close relationship of section Bicolores
and section Panicea was already proposed
by Kükenthal (1909) and Mackenzie
(1931–1935) and is supported by our molecular data.
102
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
Traditionally, C. pilosa is considered to
belong to section Rhomboidales. In our phylograms the latter species always clusters within
section Paniceae. Two other species of section
Rhomboidales, C. brevicollis and C. wahuensis,
do not cluster with C. pilosa in both molecular
trees. In the MCMC analysis, Carex wahuensis
is well supported in a cluster together with C.
umbrosa and C. mandshurica. There is no
support for the position of C. brevicollis.
Additional sampling in this section with many
species in East Asia is urgently required for
critically reviewing Koyamas (1962) enlarged
sectional concept.
The two specimens of C. tomentosa from
Germany and Kazakhstan differ in only 1 bp
in the ITS sequence. Their position in the tree
is discussed below together with other members of section Pachystylae.
The analyzed species of section Trachychlaenae cluster together in both molecular
trees. C. flacca is the most common sedge in
Central Europe lacking clearcut ecological or
altitudinal preferences. A mediterranean taxon, C. serrulata, has been classified as subspecies by Kükenthal (1909). The cytological
similarities (Heilborn 1924, Davies 1956,
Kjellqvist and Löve 1963, Dietrich 1972, Löve
and Löve 1981) are underlined by our ITS data
with only 1 bp difference within a total of
638 bp. The Mediterranean C. hispida is a
sister taxon of C. spissa from California. The
separation of these two species in section
Hispidae, as proposed by Mackenzie (1931–
1935), is at least not contrary to the molecular
result. In both analyses, C. grioletii, a species
of the heterogeneous section Pachystylae,
clusters close to section Trachychlaenae.
Molecular phylograms reveal the section
Frigidae to be non-monopyhletic. The species
ascribed to subsection Ferrugineae by Kükenthal (1909) cluster in two closely related groups
together with section Trachychlaenae in both
analyses. A first group comprises C. ferruginea,
C. austroalpina, and C. brachystachys. These
species are characterized by perigynia with
prominent nerves and anthers with only
slightly serrated terminal tips. The diploid
chromosome number is 40 (Dietrich 1967).
The second group of Ferrugineae, including
C. sempervirens and C. firma, can be characterized morphologically by a perigynium surface without conspicuous nerves and anthers
terminating with a strongly serrated crown-like
structure (Dietrich 1967). These morphological
features and identical chromosome sets
(2n ¼ 36) are shared by C. kitaibeliana and
C. mucronata (Dietrich 1967). C. kitaibeliana
clusters together with the Ferrugineae group in
the NJ tree, but without support. In the
MCMC phylogram, C. kitaibeliana appears
as an isolated taxon within Carex. In both
molecular trees, C. mucronata clusters together
with C. digitalis and C. microdonta, however
only weakly supported.
Species included in section Frigidae
subsection Fuliginosae by Kükenthal (1909),
C. fuliginosa, C. luzulina, C. atrofusca, and
C. frigida, are scattered in both trees without
any supported position. Only the American
species C. luzulina clusters together with
C. lemmonii, with significant support, as discussed below. However, they are not closely
associated to the core group of this section,
which consists only of European species.
C. fuliginosa grows in tussocks, but resembles
morphologically C. atrata, which forms longcreeping rootstocks. Both share bisexual
terminal spikes with female flowers inserted
above basal male flowers. In both trees there is
no closer connection to section Atratae.
C. atrofusca was often doubted to be a
member of section Frigidae (e.g. Christ 1885,
Dietrich 1967). Dietrich (1967) suggested a
closer relationship to section Atrata. In our
analyses, however, the position of C. atrofusca
is not resolved at all.
Also C. frigida, distinguished by bidentate
beak and a chromosome number of 2n ¼ 56
(Davies 1956, Dietrich 1967), does not appear
within the core group of section Frigidae.
The next cluster in the MCMC tree comprises three species of section Pachystylae,
C. pallescens, C. torreyi and C. globularis,
surprisingly clustering always together with
C. acutiformis as the only representative of
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
section Paludosae. C. tomentosa, another member of section Pachystylae in the traditional
classification, does not cluster together with
this group. Its unsupported position in the NJ
tree is close to section Paniceae. This position
is confirmed by the MCMC analysis. The two
other members of section Pachystylae treated
in our analysis, C. mandshurica and C. grioletii,
do not appear within the core group.
C. mandshurica is grouped with C. umbrosa
in both the NJ and MCMC tree, and
C. grioletii is close to section Trachychlaenae
in both trees. Nevertheless, section Pachystylae
sensu Kükenthal (1909) is proven to be
non-monophyletic by our analyses.
Section Ceratocystis forms an optimally
supported cluster in all analyses, with C. flava
and C. hostiana connected to a core group
comprising C. viridula, C. lepidocarpa and
C. demissa. ITS sequences allow to distinguish
C. flava from C. hostiana and the complex of
taxa grouped around C. viridula. This corresponds with chromosome numbers, i.e. an
aneuploid series from the diploid numbers 56
for C. hostiana (Davies 1956, Heilborn 1924)
to 60 for C. flava (Heilborn 1939, Crins and
Ball 1988, Halkka et al. 1992) and 2n ¼ 68, 70
within a group including C. demissa and
C. lepidocarpa (Heilborn 1928, Dietrich 1964,
Halkka et al. 1992). Our data support the proposal of Schmid (1983) to rank C. lepidocarpa
and C. demissa as subspecies of C. viridula.
Crins and Ball (1989) accepted this taxonomy
for the American species. The C. flava complex
is one of the most difficult and actually wellstudied groups (Schmid 1981, 1982, 1983,
1986; Crins and Ball 1988, 1989; Crins 1990;
Bruederle and Jensen 1991; Halkka et al. 1992;
Pykälä and Toivonen 1994; Hedrén and
Prentice 1996). Therefore, we included
sequences of five additional specimens of the
C. flava agg. in our analyses. However, since
ITS sequences yielded no apparent resolution
these data are not presented. Analysis of a
more variable region may probably supply
better results.
The grouping of C. sylvatica with section
Ceratocystis in both analyses underlines the
103
revealed heterogeneity of section Hymenochlaenae.
C. umbrosa is the only species of section
Mitratae in our analyses. The specimen from
Siberia, identified as subspecies sabynensis by
Murray et al. (in Roalson et al. 2001) clusters
closer to C. mandshurica than to C. umbrosa
from Germany (Fig. 2). In contrast to Kükenthal (1909), who accepted only subspecies
rank, Ohwi (1936) separated C. sabynensis as
a distinct species, which is supported by NJ
analysis.
Three species of section Spirostachyae form
a well supported cluster. C. extensa and C.
distans are closely related and always grouped
together with C. mairii. Section Spirostachyae
has often been united with section Ceratocystis
to one section Extensae Fries (e.g. Fries 1835,
Drejer 1844, Bailey 1889, Holm 1903,
Mackenzie 1931–1935, Kreczetovicz 1935).
The separation into two sections was
favored by patterns of flavonoid compounds
(Harborne 1971), by character compatibility
analyses and multivariate statistical analyses of
morphological data (Crins and Ball 1988). It is
also in agreement with our molecular data.
C. lemmonii and C. luzulina both belong to a
small group of species endemic to the mountains of western North America. C. lemmonii
was included by Kükenthal (1909) in section
Spirostachyae, but considered as a member of
section Frigidae by Mackenzie (1931–1935).
Interestingly, it clusters together with C. luzulina of section Frigidae, but shows no close
relationship to the core group of the section.
Accordingly, it would be at least not contrary to
our molecular results, to restrict section Spirostachyae and also subsection Ferrugineae of
section Frigidae to European species.
The dioecious section Scirpinae was included in subgenus Primocarex by some authors
(e.g Kükenthal 1909, Chater 1980), but also
transferred to subgenus Carex (e.g. Bailey 1889,
Mackenzie 1931–1935) based on recent support
by molecular phylograms (Roalson et al. 2001).
C. gigas and C. scirpoidea, two morphologically
and cytologically slightly different American
species (Löve and Solbrig 1964, Dunlop 1997,
104
M. Hendrichs et al.: Carex, subgenus Carex (Cyperaceae)
Dunlop and Crow 1999) cluster together with
statistical support. However, connections to
any other section are not resolved.
C. liparocarpos, the only species of section
Lamprochlaenae in our study, is placed in an
isolated position in the MCMC tree.
In summary, the ITS region does not
provide enough phylogenetic information to
fully resolve the relationships between sections
within subgenus Carex. Nevertheless, conclusions on some major affinities within adequately sampled sections and about defining
these sections can be inferred. Certainly, a
comprehensive interpretation of sectional limits within subgenus Carex requires additional
data and therefore no taxonomic conclusions
are drawn in this study.
The authors thank R. Berndt for the loan of
specimens, W. Maier for the loan of specimens and
helpful discussion, M. Weiß and M. Göker for
assistance in phylogenetic analyses, an anonymous
reviewer for valuable comments and the Deutsche
Forschungsgemeinschaft for financial support. This
paper is partial fulfillment of the requirements for a
PhD degree for MH, University of Tübingen.
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Address of the authors: M. Hendrichs (e-mail:
mh@uni-tuebingen.de), F. Oberwinkler, D. Begerow and R. Bauer, Universität Tübingen, Botanisches Institut, Lehrstuhl Spezielle Botanik und
Mykologie, Auf der Morgenstelle 1, D-72076
Tübingen, Germany.