American Journal of Botany 89(11): 1682–1696. 2002.

THE PHYLOGENY AND A NEW CLASSIFICATION OF THE

GINGERS (ZINGIBERACEAE): EVIDENCE FROM
MOLECULAR DATA1

W. JOHN KRESS,2,5 LINDA M. PRINCE,2,4 AND KYLE J. WILLIAMS3

2
Botany, MRC-166, United States National Herbarium, National Museum of Natural History, Smithsonian Institution, P.O. Box
37012, Washington, D.C. 20013-7012 USA; 3Department of Biology, Duke University, Durham, North Carolina 27708 USA

The pantropical Zingiberaceae is the largest family in the order Zingiberales with 53 genera and over 1200 species. Classifications
of the family first proposed in 1889 and refined by others since that time recognize four tribes (Globbeae, Hedychieae, Alpinieae, and
Zingibereae) based on morphological features, such as number of locules and placentation in the ovary, development of staminodia,
modifications of the fertile anther, and rhizome-shoot-leaf orientation. New phylogenetic analyses based on DNA sequences of the
nuclear internal transcribed spacer (ITS) and plastid matK regions suggest that at least some of these morphological traits are homo-
plasious and three of the tribes are paraphyletic. The African genus Siphonochilus and Bornean genus Tamijia are basal clades. The
former Alpinieae and Hedychieae for the most part are monophyletic taxa with the Globbeae and Zingibereae included within the
latter. The results of these phylogenetic investigations are used to propose a new classification of the Zingiberaceae that recognizes
four subfamilies and four tribes: Siphonochiloideae (Siphonochileae), Tamijioideae (Tamijieae), Alpinioideae (Alpinieae, Riedelieae),
and Zingiberoideae (Zingibereae, Globbeae). Morphological features congruent with this classification and the taxonomic status of
various monotypic genera are discussed.

Key words: classification; gingers; ITS; matK; phylogeny; tropical; Zingiberaceae; Zingiberales.

The primarily tropical Zingiberales are phylogenetically em-
bedded within the derived eumonocots (Arecales, Commelin-
ales, Poales) and include many conspicuous taxa, such as the
bananas (Musaceae), birds of paradise (Strelitziaceae), heli-
conias (Heliconiaceae), and gingers (Zingiberaceae). With 53
genera and over 1200 species, the Zingiberaceae is the largest
of the eight families of the order (Kress, 1990). In earlier clas-
sifications (e.g., Petersen, 1889; Schumann, 1904) the family
Costaceae (Fig. 1) was included in the Zingiberaceae, but with
a number of distinctive characters (e.g., lack of aromatic oils,
branched aerial stems, and spiral monostichous phyllotaxy;
Specht et al., 2001) it is now accepted as the sister clade to
the gingers (Kress, 1990, 1995; Kress et al., 2001). The Zin-
giberaceae is distributed pantropically with one genus (Re-
nealmia) found in the Neotropics, four genera (Aframomum,
Aulotandra, Siphonochilus, and Renealmia) found in Africa,
and the rest of the genera distributed in east Asia and the
Pacific Islands. The family is still poorly known taxonomically
with many species (Theilade and Mood, 1997; Sakai and Na-
gamasu, 1998; Poulsen, Mood, and Ibrahim, 1999; Williams,
Kress, and Thet Tun, 2002) and even genera (Newman, 1995;
Mood and Larsen, 1997; Larsen and Mood, 1998; Sakai and
1
Manuscript received 15 February 2002; revision accepted 3 May 2002.
The authors thank Ray Baker, Josef Bogner, Mike Bordelon, Alan Carle,
Mark Collins, David Harris, Yin Yin Kyi, Kai Larsen, Qing-Jun Li, Jing-Ping
Liao, Ida Lopez, Paul Manos, John Mood, Mark Newman, Chatchai Ngam-
riabsakul, Dan Nicolson, David Orr, Louise Pedersen, Kai Rangsiruji, Shoko
Sakai, Henk van der Werf, Tom Wood, Qi-Gen Wu, and Yong-Mei Xia for
discussion, assistance, and tissue samples that made this investigation possi-
ble. The comments of two anonymous reviewers significantly improved the
manuscript. This work was funded by the Smithsonian Scholarly Studies Pro-
gram, the Biotic Surveys and Inventories Program of the National Museum
of Natural History, and the A.W. Mellon Training Grant for Plant Systematics
to Duke University.
4
Current address: Rancho Santa Ana Botanic Garden, 1500 North College
Avenue, Claremont, California 91711-3157 USA.
5
Author for reprint requests (phone: 202-357-2534; FAX: 202-786-2563;
e-mail: kress.john@nmnh.si.edu).
1682
Nagamasu, 2000; Kress and Larsen, 2001; Larsen and Jenjit-
tikul, 2001) newly described in the last several years.
The currently accepted classification of the Zingiberaceae
(Petersen, 1889; Schumann, 1904; Holttum, 1950; Burtt and
Smith, 1972; Larsen et al., 1998) includes four tribes (Hedy-
chieae: 22 genera, Figs. 2–3; Alpinieae: 25 genera, Fig. 4;
Zingibereae: one genus, Fig. 5; and Globbeae: four genera,
Fig. 6) and is based on both vegetative and floral character-
istics (Table 1). Although a number of morphological features
have been used to distinguish the four tribes, in most cases
the defining characters are either not unique to any one tribe
or are not universal for all taxa within any tribe (Table 1). For
example, the plane of distichy of the leaves is perpendicular
to the rhizome in the Alpinieae (except in the genera Rhyn-
chanthus and Pommereschea) and is parallel to the rhizome in
the other three tribes (except for Siliquamomum in the Hedy-
chieae). Similarly, the ovary is unilocular in all members of
the Globbeae, but trilocular in the other three tribes with some
exceptions, e.g., unilocular in Tamijia and partially unilocular
in Caulokaempferia, Paracautleya, Scaphochlamys, Siphono-
chilus, and Riedelia (Larsen et al., 1998; Sakai and Nagamasu,
2000). The lateral staminodes are well developed in Hedy-
chieae, Globbeae, and Zingibereae (Figs. 2–3, 5–7) and gen-
erally absent in the Alpinieae (Fig. 4; but all five staminodes
are absent in Rhynchanthus). The fusion of the lateral stami-
nodes to the central labellum (Fig. 7) in Siphonochilus (He-
dychieae; Fig. 2) and Zingiber (Zingibereae; Fig. 5) has now
been reported in the narrow endemic Tamijia (Alpinieae) from
Borneo (Sakai and Nagamasu, 2000). Most of the characters
that are used to define the tribes are often inconsistent and
variable.
The circumscription of various genera of the Zingiberaceae
has also been debated by investigators (e.g., Etlingera: Burtt
and Smith, 1986; Curcumorpha: Larsen, 1997; Paramomum:
Wu, 1997), and a consensus has not been reached on the actual
number of genera in the family. Nearly one-quarter of the gen-
October 2002] KRESS ET AL.—PHYLOGENY OF THE GINGERS 1683

Figs. 1–6. Representatives of the major groups of the family Zingiberaceae and the sister family Costaceae. 1. Costaceae (Monocostus). 2. Hedychieae
(Siphonochilus). 3. Hedychieae (Hedychium). 4. Alpinieae (Alpinia). 5. Zingibereae (Zingiber). 6. Globbeae (Mantisia).

era in the Zingiberaceae are monospecific, but no criteria for
the recognition of these species at the generic level have been
established. One important question in the classification of the
family is how to determine the taxonomic status of these often
morphologically very distinctive monospecific genera.
Recently several papers have used molecular data to explore
the phylogenetic relationships within the family Zingiberaceae
(Searle and Hedderson, 2000; Wood, Whitten, and Williams,
2000) as well as within several genera (Hedychium: Wood,
Whitten, and Williams, 2000; Alpinia: Rangsiruji, Newman,
and Cronk, 2000a, b; Roscoea: Ngamriabsakul, Newman, and
Cronk, 2000; Aframomum: Harris et al., 2000). These analyses
have succeeded in clarifying the patterns of evolutionary re-
lationships to varying degrees, but in general have been lim-
ited in breadth of taxon sampling as well as resolution.
Our goal in the present study is to use molecular sequence
data to generate hypotheses on the phylogenetic relationships
among the genera of the Zingiberaceae in order to evaluate
past classifications of the family, to identify morphological
features that characterize the various clades detected by the
molecular analyses, to evaluate the status of monotypic genera
where possible, and to construct a new phylogenetic classifi-
cation of the family.
MATERIALS AND METHODS
Taxa—We sampled 104 species in 41 genera representing all four tribes of
the Zingiberaceae (http://ajbsupp.botany.org/v89/). In the larger genera (e.g.,
Alpinia, Curcuma, Hedychium, Globba, Zingiber) several species representing
infrageneric morphological diversity were included. Unfortunately, for several
important genera (e.g., Elettaria, Geocharis, Geostachys) we either did not
have adequate tissue samples or we were not able to amplify DNA. We also
lacked adequate samples of a number of rare monospecific genera (e.g., Lep-
tosolena, Parakaempferia, Paracautleya, Nanochilus, and Cyphostigma).
Outgroup—We initially used representative taxa of the seven other families
of the Zingiberales as outgroups in our molecular analyses (http://ajbsupp.
botany.org/v89/). However, because of the difficulty of aligning the sequences
of the internal transcribed spacer (ITS) loci and matK-trnK flanking intergenic
spacer regions in these other families with our ingroup taxa, we first conducted
more focused analyses of the coding region of matK, which is easier to align
 1684

TABLE 1. Characteristics and genera of the previously recognized tribes of the Zingiberaceae (after Schumann, 1904; Holttum, 1950; Burtt and Smith, 1972; Larsen et al., 1998).
Authorities follow Reveal (2002).

Tribes
Character Alpinieae A. Rich. (1841) Hedychieae Horan. (1862) Globbeae Meisn. (1842) Zingibereae Meisn. (1842)

1) Plane of distichy of leaves perpendicular to rhizome parallel to rhizome parallel to rhizome parallel to rhizome
2) Lateral staminodes small or absent, never petaloid petaloid, free from labellum petaloid, free from labellum and petaloid, fused to labellum
sometimes connate to filament
3) Labellum not connate to filament not connate to filament connate to filament in slender tube not connate to filament
4) Stamen medium length short length long with arching filament anther crest elongated and wrapped
around style
5) Ovary 3-locular (sometimes incom- 3-locular (sometimes incom- 1-locular 3-locular
pletely so) pletely so)
6) Placentation axial or free central axial, basal, or free columnar parietal axial
7) Style not exserted beyond anther not exserted beyond anther not exserted beyond anther sacs exserted beyond anther sacs
sacs sacs
8) Stigma expanded expanded not expanded not expanded
9) Placement of generaa Aframomum (50) Boesenbergia (60) Globba (100) Zingiber (100)
Alpinia (225) Camptandra (4) Hemiorchis (3)
Amomum (150) Caulokaempferia (10) Mantisia (4)
Aulotandra (6) Cautleya (2) Gagnepainia (3)
Burbidgea (8) Cornukaempferia (2)
Cyphostigma (1) Curcuma (50)
AMERICAN JOURNAL

Elettaria (6) Curcumorpha (1)

OF

Elettariopsis (10) Distichochlamys (3)

Etlingera (70) Haniffia (2)
Geocharis (7) Haplochorema (4)
Geostachys (18) Hedychium (50)
Hornstedtia (50) Hitchenia (3)
BOTANY

Leptosolena (1) Kaempferia (40)

Nanochilus (1) Laosanthus (1)
Paramomum (1) Paracautleya (1)
Plagiostachys (20) Parakaempferia (1)
Pleuranthodium (25) Pyrgophyllum (1)
Pommereschea (2) Roscoea (17)
Renealmia (75) Scaphochlamys (30)
Rhynchanthus (6) Siliquamomum (1)
Riedelia (60) Siphonochilus (15)
Siamanthus (1) Smithatris (2)
Stadiochilus (1) Stahlianthus (7)
Tamijia (1)
Vanoverberghia (1)
a Placement according to references cited above. Number of species follows each genus.
[Vol. 89
October 2002] KRESS ET AL.—PHYLOGENY OF THE GINGERS
Fig. 7. Floral diagram of the Zingiberaceae with perianth whorls, fertile
stamen, lateral staminodes, and labellum indicated. (Not drawn to scale; based
on Kress, 1990.)
among all of the families. Our results provide strong support for the placement
of the African genus Siphonochilus as the basal lineage to the remaining
Zingiberaceae. In addition, all of the other members of the Zingiberaceae we
sequenced except Siphonochilus share a 12-base deletion at the 39-end of
matK; this deletion is absent in all other Zingiberales. We interpret this de-
letion as a synapomorphy of the Zingiberaceae excluding Siphonochilus,
which retains this 12-base sequence as a symplesiomorphy with the rest of
the Zingiberales. We therefore used Siphonochilus as the outgroup for the rest
of the Zingiberaceae in the subsequent analyses of the complete ITS and matK
regions in order to facilitate sequence alignment within the family and provide
maximum resolution among genera.
Molecular methods—Total genomic DNAs were extracted using a minor
modification of the Doyle and Doyle (1987) hexadecyltrimethylammonium
bromide (CTAB) method. The aqueous phase was extracted with 24 parts
chloroform : 1 part isoamyl alcohol. DNA was resuspended in tris and eth-
ylenediaminetetraacetic acid (TE) buffer following isopropyl alcohol precip-
itation. Amplification of ITS was accomplished using ITS4 and ITS5 primers
(White et al., 1990). The chloroplast matK region was amplified with trnK1F
(Manos and Steele, 1997) and trnK2R (Steele and Vilgalys, 1994). All am-
plifications used Gibco BRL Taq DNA polymerase (Carlsbad, California,
USA) according to the manufacturer’s directions with annealing temperatures
of 54–588C. Amplified products were purified using the polyethylene glycol
8000 (PEG) precipitation protocol (Johnson and Soltis, 1995) with the prod-
ucts sequenced directly using automated sequencing methodology of the ABI
Prismy Big Dye Terminator Cycle Sequencing Ready Reaction Kit (Foster
City, California, USA). Sequencing primers included the amplification primers
plus ITS2 (White et al., 1990) and ITS3G (59-GCA TCG ATG AAG AAC
GTA GT-39; K. J. Williams) for the ITS region. Zingiberales-specific internal
sequencing primers were designed by L. M. Prince for the matK region in-
cluding mSP2F (59-TGG GTT AGA GAC GAA TGT GT-39), mIF (59-GTT
CAG TAC TTG TGA AAC GTT-39), m5Fa (59-CTC TAT GGG TCT TCA
AGG AT-39), m8Fa (59-TAC TTC GAC TTT CCT GTG CC-39), mSP2R (59-
TTT AAC GTC TAA TTA GAT CGG-39), mIR (59-CGT TTC ACA AGT
ACT GAA CTA-39), m5R (59-AGG ATC CTT GAA AAT CCA TAG A-39),
and m8R (59-AGC ACA AGA AAG TCG AAG-39). Primers m5Fa, m8Fa,
and m8R are modifications or complements of the primers of Steele and Vil-
galys (1994). Products were cleaned in Sephadex G-50 (fine) Centri-Sep spin
columns (Princeton Separations P/N 901, Adelphia, New Jersey, USA), dried
1685
under vacuum, and run on an ABI 377 Automated Sequencer (Applied Bio-
systems, Foster City, California, USA) at the Smithsonian Institution’s Lab-
oratory for Molecular Systematics. Raw sequences were assembled and edited
using Sequencher 3.1.1 (Gene Codes Corporation, Ann Arbor, Michigan,
USA) and manually aligned in Se-Al 2.0a3 (Rambaut, 2000). Results of ex-
ploratory analyses (not shown) that excluded difficult-to-align regions (104
base pairs [bp] in ITS and 254 bp in matK) produced topologies very similar
to those including the entire alignment. For this reason, we are presenting
here only results from analyses of the full data set.
Phylogenetic analyses—Maximum parsimony analyses of the ITS and
matK sequence data were conducted using PAUP*4.0 (Swofford, 1998) with
unweighted characters and 500 random-sequence-addition replicates, saving
all shortest trees under tree bisection-reconnection (TBR) branch swapping,
STEEPEST DESCENT off, MULTREES on, COLLAPSE branches if maxi-
mum length is zero. Multiple random-sequence additions were chosen to min-
imize the likelihood of being trapped on any particular tree island (Maddison,
1991). Bootstrap analyses (Felsenstein, 1985; Mort et al., 2000) were con-
ducted using PAUP*4.0 with ten random addition replicates, TBR branch
swapping, for 100 bootstrap replicates. Bootstrap support was categorized as
strong (.85%), moderate (70–85%), weak (50–70%), or poor (,50%). The
data sets for each gene region were analyzed separately and then, following
the total evidence approach for multiple data sets (de Queiroz, Donoghue, and
Kim, 1995; Nixon and Carpenter, 1996), we combined the sequence data. For
the combined analysis, all 104 species were included, although six species
(Caulokaempferia coenobialis, Curcuma aeruginosa, Distichochlamys citrea,
Kaempferia parviflora, K. pulchra, and Zingiber corallinum; http://ajbsupp.
botany.org/v89/) lacked sequence data for either ITS or matK.
RESULTS
Internal transcribed spacer—The ITS-1 had a total aligned
length of 277 bp (unaligned sequences ranged from 206 to
247 bp) with a mean guanine-cytosine (GC) content of
54.06%; the 5.8S region had an aligned length of 165 bp
(range of 163–165 bp) and a GC content of 51.18%; and the
ITS-2 aligned length was 372 bp (range of 242–292 bp) with
a GC content of 59.53%.
The analysis of the ITS sequence data resulted in 48 equally
parsimonious nearly fully resolved trees of 1603 steps (number
of parsimony-informative characters 5 323; consistency index
[CI] 5 0.366; retention index [RI] 5 0.724; rescaled consis-
tency index [RC] 5 0.265; Fig. 8). Tamijia is strongly sup-
ported (bootstrap value 5 90%) as a stem lineage one node
above Siphonochilus. The remaining taxa comprise two major
monophyletic lineages: one includes most of the Alpinieae
(bootstrap value 5 86%) and the other includes the Hedy-
chieae plus the Globbeae and Zingibereae, although bootstrap
support for the latter clade is weak (bootstrap value 5 52%).
Within the Alpinieae clade, Pleuranthodium 1 Riedelia 1
Burbidgea 1 Siamanthus are strongly supported as a mono-
phyletic group (bootstrap value 5 98%). Among the larger
genera, Aframomum and Renealmia are strongly supported as
monophyletic. However, several genera are not monophyletic:
Alpinia, with four nonmonophyletic groups of species referred
to as Alpinia I (A. conchigera and A. galanga), Alpinia II (A.
elegans, A. luteocarpa, and A. vittata), Alpinia III (A. ble-
pharocalyx, A. intermedia, A. pumila, A. calcarata, A. offici-
narum, and A. foxworthyi), and Alpinia IV (A. carolinensis);
Amomum, with two groups of species referred to as Amomum
I (A. glabrum and A. longipetiolatum) and Amomum II (A.
villosum and A. sp.); and Etlingera, with two groups of species
referred to as Etlingera I (E. elatior and E. yunnanensis) and
Etlingera II (E. littoralis).
1686 AMERICAN JOURNAL OF BOTANY [Vol. 89

Fig. 8. One of the 48 equally parsimonious trees of the Zingiberaceae in the analysis of the ITS sequence data (length 5 1603; consistency index 5 0.366
excluding uninformative characters; retention index 5 0.724; and rescaled consistency index 5 0.265) showing branch lengths (above the line) and bootstrap
values (below the line if $50%; values for branches within genera are excluded). Asterisks indicate nodes that collapse in the strict consensus tree. Polyphyletic
species groups in the genera Alpinia (Alp), Amomum (Amo), Etlingera (Etl), and Curcuma (Cur) are indicated.
October 2002] KRESS ET AL.—PHYLOGENY OF THE GINGERS
Within the Hedychieae clade the Globbeae are monophyletic
and sister to the remaining taxa, but with poor bootstrap sup-
port (,50%). Globba 1 Mantisia and Hemiorchis 1 Gag-
nepainia are strongly supported as sister genera (bootstrap val-
ue 5 100%). The Zingibereae (the genus Zingiber) are placed
as a crown clade within the Hedychieae. Although the topol-
ogy within this clade is fully resolved there is only poor sup-
port for all nodes connecting more than four genera. Most
branches on the tree are short. A clade including Stahlianthus,
Hitchenia, Smithatris, and Curcuma is strongly supported
(bootstrap value 5 98%), and the latter genus is paraphyletic
with three groups of species referred to as Curcuma I (C. com-
osa, C. aeruginosa, and C. roscoeana), Curcuma II (C. tho-
relii), and Curcuma III (C. bicolor and C. sp.). Boesenbergia
is also paraphyletic with two groups of species referred to as
Boesenbergia I (B. pulcherrima) and Boesenbergia II (B. ro-
tunda). All of the remaining genera in the Hedychieae are
strongly supported as monophyletic. Pommereschea and Rhyn-
chanthus of the Alpinieae are embedded within the Hedy-
chieae clade and Siliquamomum of the traditional Hedychieae
is placed with other Alpinieae.
matK—The 59 trnK-matK intergenic spacer region had a
total aligned length of 1101 bp (unaligned sequences ranged
from 767 to 884 bp) with a mean GC content of 30.01%; the
matK coding region had an aligned length of 1641 bp (range
of 1542–1572 bp) and a GC content of 29.69%; and the matK-
39 trnK intergenic spacer region aligned length was 507 bp
(range of 279–316 bp) with a GC content of 29.98%.
The analysis of the matK region (coding and noncoding)
resulted in more than 40 000 equally parsimonious trees (at
which point the analysis was stopped) of 1104 steps (number
of parsimony-informative characters 5 482; CI 5 0.630; RI
5 0.893; RC 5 0.562; Fig. 9). A strict consensus of these
shortest trees (Fig. 9) provides strong support (bootstrap values
.99%) for the same two major clades as defined by the ITS
data (the traditional Alpinieae and the traditional Hedychieae
plus Globbeae and Zingibereae), but does not resolve the po-
sition of the genus Tamijia with respect to these two clades.
There is little resolution among genera in the latter clade.
Globba 1 Mantisia and Hemiorchis 1 Gagnepainia are
strongly supported as sister genera (bootstrap values 5 100%),
but there is only poor support for uniting these four genera of
the traditional Globbeae into a single clade. The paraphyletic
nature of Globba with Mantisia is strongly supported. As in
the ITS tree, a ‘‘Curcuma clade,’’ including Hitchenia, Stah-
lianthus, Smithatris, and a paraphyletic Curcuma, is moder-
ately supported (bootstrap value 5 74%). The matK data
weakly support (bootstrap value 5 54%) a ‘‘Kaempferia
clade’’ consisting of Zingiber, Boesenbergia, Curcumorpha,
Kaempferia, Scaphochlamys, Distichochlamys, Cornukaemp-
feria, and Haniffia.
Within the Alpinieae, four major clades are resolved. Sia-
manthus and Siliquamomum are weakly supported as sister
genera (bootstrap value 5 53%), but unresolved with the other
Alpinieae. Pleuranthodium 1 Riedelia 1 Burbidgea are
strongly supported as a clade (bootstrap value 5 96%; here-
after referred to as the ‘‘Riedelia clade’’), but likewise unre-
solved in the Alpinieae. Among the remaining Alpinieae, two
primary and almost fully resolved clades are strongly sup-
ported (bootstrap value $87%). Renealmia 1 Aframomum 1
Elettariopsis 1 Paramomum 1 Amomum I 1 Alpinia I form
one monophyletic group (hereafter referred to as the ‘‘Re-
1687
nealmia clade’’) and Alpinia II 1 Vanoverberghia 1 Etlingera
I 1 Hornstedtia 1 Etlingera II 1 Amomum II 1 Alpinia III
1 Plagiostachys form the second (hereafter referred to as the
‘‘Etlingera clade’’). As in the ITS results, Pommereschea and
Rhynchanthus of the Alpinieae are embedded within the He-
dychieae, and Siliquamomum of the Hedychieae is placed
within the Alpinieae.
Combined data set—The analysis of the combined ITS and
matK sequence data resulted in 980 equally parsimonious trees
of 2647 steps (number of parsimony-informative characters 5
806; CI 5 0.450; RI 5 0.805; RC 5 0.362; Figs. 10–11). A
strict consensus of these 980 shortest trees (Figs. 10–11) pro-
vides strong support (bootstrap values .99%) for the two ma-
jor clades identified by the ITS and matK data analyzed sep-
arately: (1) the Hedychieae, Globbeae, and Zingibereae, and
(2) the traditional Alpinieae. Pommereschea and Rhynchan-
thus are embedded within the former, and Siliquamomum is
placed in the latter. Tamijia is strongly supported (bootstrap
value 5 100%) as sister to these two major clades. There is
only weak resolution and support among genera in the He-
dychieae clade, except for Globba 1 Mantisia, Hemiorchis 1
Gagnepainia, Cautleya 1 Roscoea, and Distichochlamys 1
Scaphochlamys (bootstrap values 5 95–100%). The Curcuma
clade, including Hitchenia, Stahlianthus, Smithatris, and a par-
aphyletic Curcuma, is strongly supported (bootstrap value 5
100%), whereas the Kaempferia clade is weakly supported
(bootstrap value 5 54%).
Excluding Tamijia, three of the four major clades in Alpi-
nieae are resolved as in the matK analysis. Siliquamomum is
unresolved and Siamanthus is strongly supported (bootstrap
value 5 88%) as part of the Riedelia clade (bootstrap value
5 100%). The remaining Alpinieae are moderately supported
as a monophyletic group (bootstrap value 5 85%) with strong
support for the Renealmia clade and Etlingera clade (bootstrap
values 5 86 and 91%, respectively) within it.
DISCUSSION
Molecular evidence and the current classification—The
two molecular data sets used in our analysis of the evolution-
ary relationships of the genera in the Zingiberaceae resulted
in generally congruent and compatible trees. The ITS sequence
data produced an almost fully resolved tree, but in general
lacked even moderate bootstrap support for many of the main
clades, especially among the Hedychieae-Globbeae-Zingiber-
eae taxa. The phylogenetic analysis of the matK coding and
noncoding regions resulted in stronger bootstrap support for
relationships among the genera of the Alpinieae, but support
within the Hedychieae was weak. The combined data sets pro-
duced a more fully resolved tree with strong support for many,
but not all, groups of genera.
The taxonomic concepts of earlier workers (e.g., Schumann,
1904; Holttum, 1950; Burtt and Smith, 1972; Larsen et al.,
1998) on the classification of the Zingiberaceae are partially
congruent with the results of our phylogenetic analyses of mo-
lecular sequence data. Members of the two largest tribes, Al-
pinieae and Hedychieae, for the most part form well-supported
monophyletic groups with the major rearrangements being the
basal position of Siphonochilus and Tamijia in the family, the
inclusion of Pommereschea and Rhynchanthus in the Hedy-
chieae clade, and the position of Siliquamomum in the Alpin-
ieae clade. We have confirmed that the former Globbeae are
1688 AMERICAN JOURNAL OF BOTANY [Vol. 89

Fig. 9. One of over 40 000 equally parsimonious trees of the Zingiberaceae in the analysis of the matK region (coding and noncoding) sequence data (length
5 1104; consistency index 5 0.630 excluding uninformative characters; retention index 5 0.893; and rescaled consistency index 5 0.562) showing branch
lengths (above the line) and bootstrap values (below the line if $50%; values for branches within genera are excluded). Asterisks indicate nodes that collapse
in the strict consensus tree. Polyphyletic species groups in the genera Alpinia (Alp), Amomum (Amo), Etlingera (Etl), and Curcuma (Cur) are indicated.
October 2002] KRESS ET AL.—PHYLOGENY OF THE GINGERS 1689

Fig. 10. One of 980 equally parsimonious trees of the Zingiberaceae in the analysis of the combined ITS and matK region sequence data (length 5 2647;
consistency index 5 0.450 excluding uninformative characters; retention index 5 0.805; and rescaled consistency index 5 0.362) showing branch lengths
(above the line) and bootstrap values (below the line if $50%; values for branches within genera are excluded). Asterisks indicate nodes that collapse in the
strict consensus tree. Polyphyletic species groups in the genera Alpinia (Alp), Amomum (Amo), Etlingera (Etl), and Curcuma (Cur) are indicated.
1690 AMERICAN JOURNAL OF BOTANY [Vol. 89

Fig. 11. One of 980 equally parsimonious trees of the combined analysis of the Zingiberaceae in which monophyletic genera have been collapsed into a
single branch for clarity. Branch lengths (above the line) and bootstrap values (below the line if $50%) are shown for clades encompassing two or more genera.
Asterisks indicate nodes that collapse in the strict consensus tree. Subfamilies and tribes of the new classification of the family are indicated (see Fig. 10 and
Tables 2–4).
October 2002] KRESS ET AL.—PHYLOGENY OF THE GINGERS
closely allied with the Hedychieae, but we have not resolved
whether the four genera of this tribe constitute a monophyletic
or paraphyletic group. It is clear that the genus Zingiber is a
derived taxon within the Hedychieae and should not be rec-
ognized at the tribal level.
Our results provide some insight into the long-standing tax-
onomic problems that have been encountered in some of the
largest genera of the family, e.g., Alpinia, Amomum, Etlingera,
Curcuma, and Globba. Even though we only included a mod-
est sampling of each genus in our analysis, the polyphyletic
status of each of these five genera is clear. Other large genera
such as Hedychium, Kaempferia, Zingiber, Aframomum, and
Renealmia are strongly supported as monophyletic.
The present study is the most exhaustive investigation to
date of the evolutionary relationships within the family Zin-
giberaceae. Searle and Hedderson (2000) analyzed the rela-
tionships among 12 genera (including Siphonochilus) in the
traditional Hedychieae plus Zingiber and five genera of the
Alpinieae using ITS sequence data; Globba was used to root
the tree. Their results were congruent with our analyses in
uniting 11 of the 12 genera of the Hedychieae in a single clade
and recognizing a ‘‘Kaempferia group’’ consisting of Kaemp-
feria, Boesenbergia, Zingiber, Cornukaempferia, Scaphochla-
mys, and Distichochlamys. However, only weak jackknife sup-
port was present for any branches connecting more than two
genera. They also noted that Siphonochilus occupied an iso-
lated position exterior to the Hedychieae and sister to the tra-
ditional Alpinieae. This position sister to the Alpineae was
clearly an anomaly resulting from selection of Globba as the
outgroup in their study. Wood, Whitten, and Williams (2000)
focused on the genus Hedychium in their analysis and included
17 other genera primarily in the traditional Hedychieae. Their
results were similar to Searle and Hedderson’s in defining a
Kaempferia group (without Scaphochlamys, but with Zingiber)
and placing Siphonochilus near Alpinia. As resolved by our
data, the analysis by Wood, Whitten, and Williams provided
support for a Curcuma clade (including the genera Curcuma,
Hitchenia, and Stahlianthus) and the position of Pommeres-
chea and Rhynchanthus in the Hedychieae.
The investigations by Rangsiruji, Newman, and Cronk
(2000a, b) and Harris et al. (2000) concentrated on the tradi-
tional Alpinieae, especially infrageneric relationships within
Alpinia and Aframomum, respectively, using ITS sequence
data and included several additional genera as outgroups. Our
analyses confirmed the close relationship of Pleuranthodium
and Burbidgea, the polyphyly of Amomum, and the monophy-
ly of Aframomum as shown in their studies. Rangsiruji, New-
man, and Cronk suggested that Alpinia may be paraphyletic
with Renealmia, but because of their limited outgroup selec-
tion they did not have sufficient data to support any major
taxonomic changes in these taxa (see discussion below under
Alpinioideae).
A new classification of the Zingiberaceae—Although some
congruence exists between the former classifications of the
Zingiberaceae and our current phylogenetic results (Fig. 11),
we believe that a revised classification is needed that better
represents the new data on evolutionary relationships. We ac-
cept that our results do not fully resolve all of the relationships
among genera, that some major clades have only weak boot-
strap support, that some ambiguity still exists in the placement
of certain genera, and that several critical large genera have
now been shown to be polyphyletic. Nonetheless, based on the
1691
TABLE 2. A key to the subfamilies and tribes of a new Linnaean clas-
sification of the Zingiberaceae (see Figs. 10 and 11 and Table 4).
Authorities follow Reveal (2002).
1. Plane of distichy of leaves perpendicular to rhizome.
2. Lateral staminodes well developed and fused to labellum. (Sta-
minodia laterales bene evoluta et ad labellum conjuncta.)
3. Plants evergreen with fibrous rhizomes; ovary unilocular with
parietal placentation. (Plantae sempervirens rhizomatibus fibro-
sis; ovarium uniloculare placentatio parietalis.) . . . . Tamijioideae
W. J. Kress, subfam. nov. et Tamijieae W. J. Kress, tribus nov.
3. Plants with seasonal dormancy period and fleshy rhizomes;
ovary trilocular with axial placentation. (Plantae dormientes
seasonaliter et rhizomatibus carnosis; ovarium triloculare pla-
centatio axilis.) . . . . Siphonochiloideae W. J. Kress, subfam. nov.
et Siphonochileae W. J. Kress, tribus nov.
2. Lateral staminodes reduced or absent. (Staminodia laterales re-
ducta vel absens.) . . . . . . . . . . . . . . . . . . . . . . . . . . Alpiniodeae Link (1829)
4. Extrafloral nectaries present on leaf blades; fruits silique-like
opening by longitudinal slits. (Laminae foliorum nectariis ex-
trafloralibus; fructibus similibus siliquarum, a rimis longitu-
dinalibus aperiens.) . . . . . . . . . Riedelieae W. J. Kress, tribus nov.
4. Extrafloral nectaries absent; fruits fleshy or indehiscent.
(Nectariis extrafloralibus absens; fructibus carnosis vel
indehiscentibus.) . . . . . . . . . . . . . . . . . . . . . Alpinieae A. Rich. (1841)
1. Plane of distichy of leaves parallel to rhizome . . Zingiberoideae Haask.
(1844)
5. Ovary trilocular with axial, basal or free columnar placentation;
labellum usually not connate to the filament . . . . . Zingibereae Meisn.
(1842)
5. Ovary unilocular with parietal placentation; labellum often con-
nate to filament in a slender tube . . . . . . . . . Globbeae Meisn. (1842)
results of our analyses that do have strong support, we propose
a realignment of the genera of the Zingiberaceae into four
subfamilies (Tables 2–4): the Siphonochiloideae (the genus Si-
phonochilus only), the Tamijioideae (the single genus Tami-
jia), the Alpinioideae (most of the former Alpinieae), and the
Zingiberoideae (including the former tribes Hedychieae, Zin-
gibereae, and Globbeae).
Within the Alpinioideae, we recognize the two main clades
as tribes Alpinieae and Riedelieae; the placement of Siliqua-
momum is equivocal and requires further study (Fig. 11). The
polyphyletic nature of three of the major genera in the Alpi-
nieae (Alpinia, Amomum, and Etlingera) prevents us from for-
mally recognizing the Renealmia clade and the Etlingera clade
at this time, even though each clade has strong bootstrap sup-
port. Within the Zingiberoideae we recognize two tribes to
distinguish most of the old Hedychieae (here called the Zin-
gibereae) from the Globbeae (Fig. 11). Although strong mo-
lecular support is lacking for either tribe within the Zingiber-
oideae, we believe that it is better to recognize the Zingibereae
and to retain the Globbeae until more evidence is accumulated.
We also refrain from formally recognizing either the Kaemp-
feria clade or the Curcuma clade at this time. We have not
been able to place the genus Caulokaempferia into either tribe
with any degree of certainty. A forthcoming investigation of
the Globbeae and related taxa will address some of these issues
in more depth (K. J. Williams, W. J. Kress, and P. S. Manos,
unpublished data). The relationships among the genera are dis-
cussed below within the framework of this revised classifica-
tion.
Basal lineages—The strong support from the coding region
of matK for the position of Siphonochilus as the basal lineage
in the family was at first surprising. The subsequent discovery
1692 AMERICAN JOURNAL OF BOTANY [Vol. 89

TABLE 4. Characteristics of the subfamilies and tribes of the new classification of the Zingiberaceae presented here (Burtt, 1972; Burtt and Smith, 1972; Larsen et al., 1998; Sakai and

sometimes connate to

globbose and dehiscent

TABLE 3. Placement of genera in the new classification of the family

connate to filament in
Zingiberaceae. (Asterisks indicate taxa not sampled in the molec-

short to long, some-

petaloid, free from
parallel to rhizome
ular phylogenetic analyses; these genera are tentatively placed

spurred or absent
dormancy period
Zingiberoideae:

labellum and

times arching
based on morphological features.)

slender tube
Globbeae

filament
Subfamily Subfamily Subfamily Subfamily

1-locular
Siphonochiloideae Tamijioideae Alpinioideae Zingiberoideae

parietal
W. J. Kress W. J. Kress Link Haask.

absent
fleshy
Tribe Tribe Tribe Tribe
Siphonochileae Tamijieae Alpinieae Zingibereae Meisn.
W. J. Kress W. J. Kress A. Rich.

Nagamasu, 2000; W. J. Kress, personal observation). Some nondiagnostic features are included as a reference to the previous classification (see Table 1).

wrapped around style

not connate to filament
Siphonochilus Tamijia Aframomum Boesenbergia

well-developed and
petaloid, free from or

3-locular (sometimes

axial, basal, or free

fleshy and dehiscent

Alpinia Camptandra

fused to labellum

absent, petaloid, or

incompletely so)
parallel to rhizome
Amomum Cautleya

dormancy period
Zingiberoideae:
Zingibereae
*Aulotandra Cornukaempferia

short to long
*Cyphostigma Curcuma

columnar
*Elettaria Curcumorpha
Elettariopsis Distichochlamys

absent
fleshy
Etlingera Haniffia
*Geocharis *Haplochorema
*Geostachys Hedychium
Hornstedtia Hitchenia

not connate to filament

small or absent, never
*Leptosolena Kaempferia

indehiscent or fleshy
medium, sometimes

axial or free central

Paramomum *Laosanthus

petaloid or absent
perpendicular to
Plagiostachys *Nanochilus

Alpinioideae:
Alpinieae
Renealmia *Paracautleya
Vanoverberghia *Parakaempferia

rhizome

petaloid

arching
evergreen
Pommereschea

3-locular
fibrous
Tribe Pyrgophyllum

absent
Subfamilies and Tribes
Riedelieae Rhynchanthus
W. J. Kress Roscoea
Burbidgea Scaphochlamys

silique-like, opening by
Pleuranthodium Smithatris

not connate to filament

small or absent, never
present on leaf blades
Riedelia *Stadiochilus

longitudinal slits
Siamanthus Stahlianthus

petaloid or absent
Zingiber perpendicular to

axial or parietal
Alpinioideae:

1- or 3-locular
Riedelieae

Incertae Sedis
Siliquamomum Tribe
rhizome

petaloid
evergreen

Globbeae Meisn.

medium
fibrous

Gagnepainia
Globba
Hemiorchis
Mantisia not connate to filament

Incertae Sedis
petaloid, fused to

Caulokaempferia
perpendicular to
Tamijioideae:
Tamijieae

labellum
rhizome
evergreen

unknown
1-locular
petaloid

parietal
of a 12-base insertion at the 39 end of matK that this genus
fibrous

absent

short

shares with all other Zingiberales, but not the rest of the Zin-
giberaceae, provided unequivocal support for this basal place-
ment. Our morphological interpretation of this topology is that
not connate to filament

the partial to almost complete fusion of the lateral staminodes

3-locular (sometimes

to the large labellum in Siphonochilus is a plesiomorphic char-

incompletely so)
petaloid, fused to
Siphonochiloideae:

perpendicular to
dormancy period

acter of the basal Zingiberaceae shared with the sister family

Siphonochileae

Costaceae (Figs. 1–2, 7). The recent discovery of the mono-

labellum

typic genus Tamijia, a narrow endemic from northern Borneo

rhizome

petaloid

(Sakai and Nagamasu, 2000), is equally interesting. Although

absent

fleshy
fleshy

short

axial

the inflorescence structure and vegetative morphology are un-

like Siphonochilus, Tamijia shares the same fusion of the lat-
eral staminodes and labellum, and some relationship between
4) Extrafloral nectaries
3) Plane of distichy of

the two genera was suggested by Sakai and Nagamasu (2000).

5) Lateral staminodes

The independent results of our molecular analysis place Tam-

ijia as sister to the remaining Zingiberaceae, excluding the
10) Placentation
Character

8) Anther crest
1) Seasonality

basal Siphonochilus, and confirm that this floral character is a

2) Rhizomes

6) Labellum

11) Capsule
7) Filament

feature shared with the sister taxa of the Costaceae. Because

9) Ovary
leaves

of the distinctness of these two genera in the family and their

basal positions, we have chosen to recognize each genus as a
subfamily of the Zingiberaceae, the Siphonochiloideae and the
October 2002] KRESS ET AL.—PHYLOGENY OF THE GINGERS
Tamijioideae, to indicate their phylogenetic position in the
Zingiberaceae (Tables 2–4).
Alpinioideae—The former tribe Alpinieae and new subfam-
ily Alpinioideae are defined by a number of features (Tables
1, 2, 4). The most conspicuous floral feature is the great re-
duction or absence of the two lateral staminodes (Figs. 4, 7).
These staminodes represent two modified stamens of the outer
staminal whorl of the Zingiberaceae floral plan; the third mem-
ber of this whorl is absent. The ‘‘labellum,’’ which is nearly
ubiquitous in the family, is a petaloid structure formed by the
fusion of the two lateral sterile stamens of the inner staminal
whorl; the median member of this whorl is the single tetras-
porangiate fertile stamen. The lateral staminodes are also ab-
sent in the genera Rhynchanthus and Pommereschea, usually
placed in the traditional Alpinieae. However, in these two gen-
era the labellum is also reduced or absent and our molecular
results place them within the new Zingiberoideae. These two
genera are clear examples of independent reductions in lateral
staminodes in the family.
The second apomorphy of the Alpinioideae is the perpen-
dicular orientation of the plane of distichy of the shoots with
respect to the direction of growth of the rhizome (Burtt, 1972).
This character is present in all of the genera formerly placed
in the Alpinieae, except for Rhynchanthus and Pommereschea
in which the orientation is parallel. In accordance with the
suggestions of others (e.g., K. Larsen [AAU], T. Wood
[FLAS], and M. Newman [E], personal communication;
Smith, 1980), these two genera should be included in the Zin-
giberoideae. Sakai and Nagamasu (2000) assigned their new
genus Tamijia to the Alpinieae based on the perpendicular
shoot orientation, but recognized that their genus was some-
what anomalous in this tribe. Indeed, according to our molec-
ular results, Tamijia deserves recognition as a separate sub-
family altogether.
Within the subfamily Alpinioideae are two major groups of
genera, here recognized as tribes Alpinieae and Riedelieae (Ta-
bles 2–4). The first tribe contains the majority of genera in the
subfamily and includes taxa distributed in Asia, Africa, and
the Americas. The taxa in the Alpinieae fall into two main
subclades, the Renealmia clade and the Etlingera clade, each
of which is supported by strong bootstrap values. However,
three of the largest genera in this tribe, Etlingera, Amomum,
and Alpinia, are polyphyletic, and the latter two have species
in both the Renealmia clade and the Etlingera clade. Because
our sampling of Etlingera was modest (three species) we sug-
gest that taxon sampling be increased before any firm conclu-
sions be drawn about the status of this genus. However, it is
clear from this investigation as well as others (Harris et al.,
2000; Rangsiruji, Newman, and Cronk, 2000b) that major ad-
ditional taxonomic studies and realignments are necessary in
both Alpinia and Amomum. In Renealmia, the one genus in
the Alpinioideae that is distributed across continents, our lim-
ited sampling of six species provided good support for a dis-
tinct African clade and a tropical American clade (Figs. 8–10).
For Alpinia the results of our analysis identified four sepa-
rate groups (Alpinia I–IV) in the 12 species we sampled. Each
of these four groups corresponds to one of the clades recog-
nized in the molecular analysis of Rangsiruji, Newman, and
Cronk (2000b) and, as in their analysis, our results do not
support the classification of Alpinia proposed by Smith
(1990a). Alpinia galanga and A. conchigera (Alpinia I; part
of the A. galanga clade of Rangsiruji, Newman, and Cronk)
1693
are placed in two separate sections of subgenus Alpinia by
Smith, but here form a strongly supported clade basal to the
other members of the Renealmia clade (Aframomum, Reneal-
mia, Amomum I, Elettariopsis, and Paramomum; including Af-
rican, Asian, and American species). The rest of Alpinia is
scattered in the Etlingera clade. Alpinia II (A. elegans, A. lu-
teocarpa, and A. vittata; part of the A. eubractea clade of
Rangsiruji, Newman, and Cronk) includes the genus Vanov-
erberghia (from the Philippines and Taiwan) and is allied with
the polyphyletic Etlingera, Hornstedtia, and Amomum II (all
Asian). Alpinia III (six species included in four of Rangsiruji,
Newman, and Cronk’s clades) is united with the genus Pla-
giostachys whereas Alpinia IV (single species A. carolinensis
in Rangsiruji, Newman, and Cronk’s A. carolinensis clade) is
unresolved with Alpinia II and III. A more extensive analysis
of Alpinia is in progress (A.-Z. Liu and W. J. Kress, unpub-
lished data).
Taxonomic matters are made worse by the polyphyletic na-
ture of the genus Amomum. Although we only sampled four
species in this genus, these four species form two separate
lineages: one within the Renealmia clade as sister to the genus
Elettariopsis, which has a striking similarity in floral structure
and is often difficult to distinguish from Amomum (Holttum,
1950; Kiew, 1982), and the other in the Etlingera clade, which
is strongly supported to include a species of Etlingera. The
polyphyly of Amomum was also suggested by Harris et al.
(2000) in their investigation of the molecular systematics of
the genus Aframomum. In a separate analysis of over 30 spe-
cies of Amomum using ITS and matK sequence data, we have
identified four separate lineages of Amomum scattered among
the other genera of the Alpinieae (Y.-M. Xia, W. J. Kress, and
L. M. Prince, unpublished data). Needless to say, the generic
boundaries and definitions of all the taxa in this tribe require
more extensive and careful molecular and morphological study
before a new classification can be proposed. For this reason
we have chosen not to give formal taxonomic status to either
the Renealmia clade or the Etlingera clade, even though strong
molecular support exists for both lineages.
The Riedelieae (Tables 2–4) include four genera united by
both molecular and morphological characters: Burbidgea (Bor-
neo), Pleuranthodium (primarily New Guinea and Bismarck
Archipelago), Riedelia (New Guinea), and Siamanthus (Thai-
land). The affinities of these four genera are indicated by their
common possession of long, slender silique-like capsules that
open by longitudinal slits to the base (Smith, 1972, 1990b;
Larsen and Mood, 1998). Larsen and Mood (1998) also point-
ed out that the close relationship of at least three of these
genera (Burbidgea, Riedelia, and Siamanthus) is suggested by
unique ‘‘nectary pits’’ on the dorsal midrib of the leaf blade.
We have now confirmed the presence of these extrafloral nec-
taries in Pleuranthodium as well (W. J. Kress and M. Borde-
lon, unpublished data). These vegetative and reproductive
characters taken together make the Riedelieae a readily rec-
ognizable tribe in the Alpinioideae.
The long silique-like fruits of Siliquamomum (Southern Chi-
na and Vietnam) are similar to the fruits found in the Riede-
lieae, but the presence of a well-developed labellum and lateral
staminodes as well as the absence of the extrafloral nectaries
on the leaf midribs separate this genus from other members
of that tribe. The placement of Siliquamomum in either the
Riedelieae or the Alpinieae is unresolved by our molecular
analysis. For these reasons we prefer to place this genus as
1694 AMERICAN JOURNAL
incertae sedis until further evidence confirms its position in
the Alpinioideae.
Within the Alpinioideae, we included in our molecular anal-
ysis four of the six monospecific genera. Cyphostigma pul-
chellum (Thw.) Benth., restricted in distribution to Sri Lanka,
is poorly known (Dassanayake, 1983), and no tissue was avail-
able for our investigation. Leptosolena haenkei Presl, endemic
to the lower slopes of Mt. Pinatubo in Northern Luzon, Phil-
ippines, has not been collected since it was described in the
early 1900s and is presumed extinct (Madulid, 1996). Based
on morphological features we have tentatively placed these
small genera (along with the African Aulotandra and Asian
Geocharis and Geostachys) in the Alpinieae. Vanoverberghia,
also from the Philippines, was only known from a single spe-
cies, V. sepulchrei Merr., until a second species, V. sasakiana
H. Funak. & H. Ohashi, was described from the Lanyu Islands
southeast of Taiwan (Funakoshi and Ohashi, 2000). Merrill
(1912), in his original description of the genus, compared it
to Riedelia, but also recognized its affinity to Alpinia as did
Smith (1990a). Our results show that this genus is a member
of the Alpinia II clade that includes other species from the
Philippines (e.g., A. elegans and A. luteocarpa). As noted
above, a phylogenetic and taxonomic revision of Alpinia and
its closely related genera, including Vanoverberghia and Pla-
giostachys, is needed.
The monotypic Paramomum, endemic to Yunnan, China,
was recently moved by Wu (1997) into the genus Amomum.
In the original description of Paramomum, Tong (1985) com-
pared it to Costus because of its supposed spiral phyllotaxy.
Our molecular results place this genus as sister to Elettariopsis
in a clade with species of Amomum I, thus supporting its sep-
aration from Amomum and clear distance from Costus. The
monotypic and distinct nature of the remaining two genera in
the Alpinioideae, Siliquamomum and Siamanthus, is also sup-
ported here by the long branch lengths and isolated positions
of these taxa in or near the Riedelieae.
Zingiberoideae—Our subfamily Zingiberoideae contains
the remaining genera in the family, which were formerly
placed within the three tribes Zingibereae, Hedychieae, and
Globbeae (Table 3). The most recognizable floral features of
this subfamily are the conspicuous and often well-developed
lateral staminodes (Figs. 3, 5, 6) that are generally absent in
the Alpinioideae (Tables 2, 4). These lateral staminodes are
fused to the corolla tube and free from the labellum in most
of the former Hedychieae, whereas they are fused to the la-
bellum in the genus Zingiber (former Zingibereae; Fig. 5) and
connate to the filament in Globba and Mantisia (part of the
former Globbeae; Fig. 6). In a few genera the lateral stami-
nodes and/or the labellum are reduced or absent (Rhynchan-
thus, Pommereschea, Nanochilus, Stadiochilus, Laosanthus,
Hedychium horsfieldii, and H. bordelonianum; Smith, 1980;
Newman, 1990; Larsen and Jenjittikul, 2001; Williams, Kress,
and Thet Tun, 2002). Hence, the presence of well-developed
lateral staminodes is a feature not shared by all members of
the Zingiberoideae as recognized here.
The most prominent vegetative feature that is universal in
this subfamily is the parallel orientation of the plane of disti-
chy of the leafy shoots with respect to the rhizome (perpen-
dicular orientation in all other Zingiberaceae). As pointed out
earlier, this character was the basis for some authors to suggest
that genera such as Rhynchanthus and Pommereschea with
parallel orientation were not properly placed in the Alpinieae
OF BOTANY [Vol. 89
(Burtt, 1972; Smith, 1980; Wood, Whitten, and Williams,
2000). A second vegetative trait that characterizes the Zingi-
beroideae (and Siphonochilus), briefly discussed by Wood,
Whitten, and Williams (2000), is the capacity for members of
this subfamily to go into dormancy during the dry season in
monsoonal climates. Unlike the Alpinioideae and Tamijioi-
deae, in which individuals are evergreen throughout the year,
the Zingiberoideae, including taxa of the former Hedychieae,
Globbeae, and Zingibereae, have a forced dormancy period
during which all aboveground parts are shed and the plant
overwinters as a thick, often fleshy underground rhizome
(sometimes with starch-filled roots or tubers). Either just prior
to or at the earliest sign of the wet season, individuals will
break dormancy with either vegetative shoots or reproductive
shoots (e.g., Hemiorchis, Gagnepainia, Mantisia, some
kaempferias and many curcumas). However, some species in
the Zingiberoideae can also be evergreen in the wet forest
habitats where they occur (e.g., some globbas, zingibers, and
hedychiums), but these same species can be forced into dor-
mancy under stress or in greenhouse environments (M. Bor-
delon [US] and T. Wood [FLAS], personal communication).
These latter taxa may be descendents of ancestors from mon-
soonal climates that have secondarily colonized evergreen hab-
itats. As far as we know, members of Alpinioideae cannot be
forced into dormancy, possess tough fibrous rather than fleshy
rhizomes, and are always evergreen in their natural habitats.
Within the Zingiberoideae, we have chosen, for historical
consistency, to recognize two tribes even though our molecular
data do not provide strong support for these clades (Tables 2–
4). The Zingibereae include most of the former Hedychieae as
well as the genus Zingiber. All members of this tribe possess
a trilocular ovary, which in some genera may be incompletely
closed towards the apex (e.g., Scaphochlamys and Paracau-
tleya), and axial or rarely basal placentation. Within the Zin-
gibereae several groups of genera are supported by varying
bootstrap values. A Kaempferia clade, including Haniffia, Zin-
giber, Kaempferia, Distichochlamys, Scaphochlamys, Boesen-
bergia, Curcumorpha, and Cornukaempferia (and probably
Haplochorema and Parakaempferia not included in our anal-
ysis) is only weakly supported here, but has also been recog-
nized by others (Newman, 1995; Searle and Hedderson, 2000;
Wood, Whitten, and Williams, 2000). These taxa lack the dis-
tinctive pseudostem (except for Zingiber and Haniffia) found
in other members of the subfamily. Although it has been sug-
gested that the genus Cornukaempferia is allied with either
Kaempferia (Mood and Larsen, 1997) or Zingiber (Searle and
Hedderson, 2000; Wood, Whitten, and Williams, 2000), our
results do not support either of these hypotheses and resolution
among the genera of the Kaempferia clade is generally low.
The close relationship between Distichochlamys and Sca-
phochlamys as well as their generic boundaries have been rec-
ognized (Newman, 1995). However, the taxonomic position of
Curcumorpha and Boesenbergia requires some discussion.
Boesenbergia is a genus of about 60 species found throughout
tropical Asia, including India, Myanmar, Thailand, Malaysia,
and Borneo (Sirirugsa, 1992), and is distinguished by its two-
ranked inflorescence bracts, saccate labellum, and phenologi-
cal pattern of flowers opening from the apex toward the base
(Smith, 1987). Curcumorpha longiflora was described as a
monotypic genus from northeastern India (now known to also
occur in Myanmar and Thailand) distinctive in its radical in-
florescences with spirally arranged bracts and the presence of
a staminodial cup (Rao and Verma, 1971). Larsen (1997)
October 2002] KRESS ET AL.—PHYLOGENY OF THE GINGERS
placed Curcumorpha into Boesenbergia stating that the char-
acters cited by the original authors did not sufficiently distin-
guish it from that genus. Our results suggest that Boesenbergia
itself may be polyphyletic with one group of species (here
represented by B. pulcherrima) allied to Curcumorpha. This
taxonomic complex is yet another example of the problems
that exist in defining clear generic boundaries in the Zingi-
beraceae.
The Curcuma clade has strong bootstrap support and in-
cludes Curcuma, Stahlianthus, Hitchenia, and Smithatris,
which share cone-like inflorescences of few-flowered, con-
gested bracts (although much reduced in Stahlianthus). Cur-
cuma, with about 50 species, has been circumscribed by its
‘‘pouched’’ inflorescence bracts and versatile, usually spurred
anthers. However, these features are neither unique nor uni-
versal in the genus, and our results along with those of others
(Wood, Whitten, and Williams, 2000) strongly suggest that
Curcuma is paraphyletic with Hitchenia and Stahlianthus, and
maybe Smithatris. Expanded taxon sampling within these gen-
era is necessary to realign species and distinguish boundaries
among the taxa (T. Rehse, W. J. Kress, and P. S. Manos, un-
published data). Rather than accepting an enlarged concept of
Curcuma to include these associated genera, the strong support
of several clades within the Curcuma complex may necessitate
the splitting up of Curcuma into several smaller genera.
Among the remaining genera in the Zingibereae two pri-
marily Himalayan clades have strong support: the Roscoea 1
Cautleya clade in the western end of the range from Kashmir
to southwestern China and the Pommereschea 1 Rhynchan-
thus clade in the eastern end straddling the borders of Yunnan,
Myanmar, and Thailand. Both of these clades have moderate
to strong support and at least in the ITS analysis form a weakly
supported Himalayan alliance of four genera. The placement
of Hedychium (a large, strongly supported monophyletic ge-
nus), the monotypic Pyrgophyllum endemic to southwestern
China, and the few-species Camptandra from the lowland wet
forests of Thailand and Malaysia is still unresolved, although
the latter two genera are allied with the Curcuma clade in the
ITS analysis.
The four genera in the traditionally recognized Globbeae
(Tables 2–4; Fig. 6) are united by several morphological char-
acters, such as the unilocular ovary with parietal placentation
(convergent with Tamijia) and the long-arching filament to
which the labellum and/or lateral staminodes are fused (in
Globba and Mantisia only). Our molecular analysis strongly
places the four genera of the Globbeae within the Zingibero-
ideae, but only weakly outside the taxa comprising the Zin-
gibereae (see discussion below on Caulokaempferia). A num-
ber of vegetative and floral characters unite Globba with Man-
tisia and Hemiorchis with Gagnepainia, a result that is strong-
ly supported by both the ITS and matK sequence data as well.
Our analysis shows that the Indo-Burmese Mantisia is sister
to an Indo-Burmese clade of Globba suggesting that the latter
genus is paraphyletic; the relationships within this clade are
currently under investigation (K. J. Williams, W. J. Kress, and
P. S. Manos, unpublished data). Our ITS data provide only
weak support to unite the four genera, and the combined anal-
ysis does not resolve this relationship. However, a more com-
prehensively sampled data set (K. J. Williams, W. J. Kress,
and P. S. Manos, unpublished data) suggests that the tribe, as
traditionally recognized, is in fact monophyletic. Because of
this additional evidence and in the interest of maintaining sta-
bility with past classifications we advocate retaining the Glob-
1695
beae as earlier recognized until forthcoming evidence proves
otherwise.
Caulokaempferia, first included within the genus Kaempferia,
was subsequently recognized as distinct by Larsen (1964). Its
possible relationship to both Camptandra and Boesenbergia have
been noted (Larsen and Smith, 1972). Our results to not closely
ally Caulokaempferia to any of the above three genera, and the
combined analyses of the two molecular data sets leaves the
placement of the genus within the Zingiberoideae unresolved
with respect to the Zingibereae and the Globbeae. We therefore
at present recognize Caulokaempferia as incertae sedis within the
Zingiberoideae in our revised classification.
We have been able to address the phylogenetic placement
and distinctiveness of a number of the monotypic genera with-
in the Zingiberoideae. Taxa such as Haniffia, Cornukaempfer-
ia, and Pyrgophyllum are characterized by relatively long
branch lengths in the combined analyses (32–41 bp), while
others, such as Curcumorpha, Hitchenia, Stahlianthus, and
Smithatris, are less distinct (9–20 bp). As exploration of new
habitats in Southeast Asia increases, additional species are be-
ing found in many genera that were previously only known
from a single species (e.g., Curcumorpha, Cornukaempferia,
Haniffia, Distichochlamys, and Smithatris). In addition, several
monotypic genera such as Nanochilus, Paracautleya, Parak-
aempferia, Laosanthus, and Stadiochilus are yet to be sampled
for inclusion in molecular investigations. We have tentatively
placed these genera in the Zingibereae based on their mor-
phology alone. A more thorough sampling and expanded phy-
logenetic analyses should provide additional answers to the
status of the many small genera in the family.
Future directions—We recommend that more species of the
large paraphyletic genera Curcuma, Alpinia, Amomum, and Etlin-
gera be added to future molecular analyses to better delimit ge-
neric boundaries in these taxa and their allied genera. Taxa from
important, but undersampled, genera such as Hornstedtia, Aulo-
tandra, Elettaria, Geocharis, Geostachys, Riedelia, Burbidgea,
and Scaphochlamys should be included in future investigations.
We are especially interested in the placement and taxonomic sta-
tus of the remaining monotypic genera (Stadiochilus, Nanochilus,
Cyphostigma, Laosanthus, Paracautleya, Parakaempferia, and
Leptosolena), some of which are exceedingly rare and may be
extinct in the wild. We plan to continue our taxon sampling
throughout the family with the hopes of recognizing appropriate
monophyletic genera and eventually proposing a more detailed
classification of the Zingiberaceae. We are also currently utilizing
our phylogenetic results to investigate patterns of biogeographic
history and character evolution in this interesting and diverse
pantropical family.
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