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Phylogeny and Systematics of Kewa (Kewaceae)
Author(s): Mats Thulin, Anders Larsson, Erika J. Edwards and Abigail J. Moore
Source: Systematic Botany, 43(3):689-700.
Published By: The American Society of Plant Taxonomists
URL: http://www.bioone.org/doi/full/10.1600/036364418X697409
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Systematic Botany (2018), 43(3): pp. 689–700
© Copyright 2018 by the American Society of Plant Taxonomists
DOI 10.1600/036364418X697409
Date of publication August 10, 2018
Phylogeny and Systematics of Kewa (Kewaceae)
Mats Thulin,
1,6
Anders Larsson,
2
Erika J. Edwards,
3,4
and Abigail J. Moore
3,5
1
Systematic Biology, Department of Organismal Biology, EBC, Uppsala University, Norbyv¨agen 18D, 752 36
Uppsala, Sweden; mats.thulin@ebc.uu.se
2
NBIS, SciLifeLab, Uppsala University, Box 596, 751 24 Uppsala, Sweden; anders@ormbunkar.se
3
Department of Ecology and Evolutionary Biology, Brown University, 80 Waterman Street, Box G-W,
Providence, Rhode Island 02912, USA
4
Department of Ecology and Evolutionary Biology, Yale University, P.O. Box 208105, New Haven,
Connecticut 06520, USA; erika.edwards@yale.edu
5
Department of Microbiology and Plant Biology and Oklahoma Biological Survey, University of Oklahoma,
770 Van Vleet Oval, Norman, Oklahoma 73019, USA; abigail.j.moore@ou.edu
6
Author for correspondence (mats.thulin@ebc.uu.se)
Communicating Editor: Chuck Bell
Abstract—The genus Kewa in the monogeneric family Kewaceae (Caryophyllales) is revised. Six species are recognized, K. acida on St. Helena, K.
angrae-pequenae in Namibia and South Africa, K. arenicola (incl. K. trachysperma) in South Africa, K. bowkeriana (incl. K. suffruticosa) widespread in
eastern and southern Africa and in Madagascar, K. caespitosa in Angola and Namibia, and K. salsoloides in Namibia, Botswana, and South Africa. Kewa
is morphologically distinctive, notably by its simple perianth where the two outer perianth-segments are more or less sepaloid and the three inner
ones more or less petaloid, and by its indumentum of short glandular hairs, often with prominent, persistent, wart-like bases. All species have an acid
taste, apparently due to the presence of oxalic acid. All names are typified, including one lectotype designated here. An identification key and
distribution maps for all species are provided. The phylogeny of Kewa is reconstructed based on plastid trnK-matK and rbcL and nuclear ITS
sequences. Kewa is strongly supported and the included species have strong to no support, whereas the relationships between the species are mostly
unsupported. The phylogeny is da ted and the estimated age of the Ke wa stem clade is (37.5–)45.0(–57.0) million years and of thecrown clade (3.0–)3.9(–7.4)
million years. The age of the crown clade would also be the estimated date when K. acida on the approximately 14 million years old St. Helena
diverged from its potential sister group on the African continent, and would coincide with the earliest possible date for the introduction of the
ancestor of K. acida to St. Helena.
Keywords—Caryophyllales, Hypertelis, molecular dating, St. Helena, taxonomy, typification.
The number of recognized families of flowering plants has in
the last decades usually been just over 400, the recent classi-
fication of the Angiosperm Phylogeny Group (2016), APG IV,
for example, having 416. New families of flowering plants are
still occasionally proposed, mostly for small, odd genera,
where new evidence has shown them to be previously mis-
placed. Recent examples in Caryophyllales are Microtea Sw.
with nine species in tropical America, previously placed in
Amaranthaceae or Phytolaccaceae, but now in Microteaceae
(Sch¨aferhoff et al. 2009), and Corbichonia Scop. with two species
in Africa and Asia, previously mostly placed in Molluginaceae
or Lophiocarpaceae, but now in Corbichoniaceae (Thulin et al.
2016).
Kewa Christenh. in Kewaceae (Christenhusz et al. 2014) is an
example of a new genus placed in a new family, an extremely
unusual situation. The species involved have long been treated as
members of the genus Hypertelis E.Mey. ex Fenzl in Mollugi-
naceae. This genus was found to be non-monophyletic (Christin
et al. 2011), with part of it (H. spergulacea E.Mey. ex Fenzl, the
type) belonging to Molluginaceae, and another part (H. bow-
keriana Sond. and H. salsoloides (Burch.) Adamson) being sister
to a large clade including, among others, the well-established
families Aizoaceae and Nyctaginaceae. Hypertelis bowkeriana, H.
salsoloides and their relatives were placed in Kewa by Chris-
tenhusz et al. (2014), whereas H. spergulacea and its relatives were
treated in a modified Hypertelis by Thulin et al. (2016).
The taxonomy of Kewa with eight recognized species pro-
posed by Christenhusz et al. (2014) is entirely based on the
treatment of Hypertelis by Adamson (1957). However,
Christenhusz et al. (2014) have missed, for example, that since
then Jeffrey (1961) has treated Hypertelis suffruticosa (Baker)
Adamson ([Kewa suffruticosa (Baker) Christenh.) from
Madagascar as a synonym of H. bowkeriana.
Here we present a phylogeny of the core Caryophyllales
based on plastid trnK-matK and rbcL and nuclear ITS sequence
data and with a much expanded sampling of Kewa compared
to previous studies and including K. acida (Hook.f.) Christenh.,
endemic to St. Helena. The phylogeny is dated to enable us to
put an age to the stem and crown clades of Kewa, and to give an
age estimate of its dispersal to St. Helena. We also propose a
revised classification of Kewa and Kewaceae, including a more
detailed morphological characterization of the family, typifi-
cations of all names, descriptions of all recognized taxa, a new
key to the species, as well as distribution maps for all species.
Materials and Methods
Taxon Sampling—The sampling included representatives of nearly all
families within the core Caryophyllales, and is essentially the same as that
in Thulin et al. (2016: Fig. 1), except for the sampling of Kewaceae that is
expanded to include 14 accessions representing all six species of Kewa
recognized here (see under Taxonomy). In total, 78 accessions from 65
species were included in the analyses (Appendix 1), and 24 sequences were
newly generated for this study.
Data Availability—Alignments, tree files, and supplemental figures
are all available from the Dryad Digital Repository (Thulin et al. 2018).
DNA Extraction, Amplification, and Sequencing—Dried leaf material
from herbarium specimens was used for DNA extraction. Samples were
extracted using the FastDNA SPIN kit (MP Biomedicals, LLC, Santa Ana,
California) following manufacturer’s protocol except that two elution steps
were generally used, with 50 ml of DES each time to maximize yield.
The nuclear ribosomal internal transcribed spacer (ITS) and chloroplast
trnK-matK regions were amplified using PCR. The primers ITS4 and ITS5
(White et al. 1990) were used to amplify the ITS region, whereas for the trnK-
matK region various combinations of the forward primers trnKmatK_For H,
M, G, and K and the reverse primers trnKmatK_Rev B, C, E, and I, all from
Christin et al. (2011), except for trnKmatK_M (50-ACTATGTATCATTGGT-
TAAGC-30), were used. The same PCR protocol was used for both regions, in
25 ml reactions including 1 unit GoTaq (Promega Corporation, Madison,
Wisconsin), 5 3GoTaq Reaction Buffer (Promega), 0.5 mM MgCl
2
,0.15mM
689
each dNTP (New England Biolabs, Inc.,Ipswich, Massachusetts), 0.2 mMeach
primer, and approximately 0.6 ng extracted DNA. The following PCR pro-
gram was used: initial denaturation of 3 min at 94°C; 37 cycles of 1 min
denaturation at 94°C, 30 s annealing at 48°C (for ITS) or 51°C (for trnK-matK),
60 to 150 s extension at 72°C, and final extension of 10 min at 72°C.
The PCR products were cleaned with the Exo-SAP PCR Product Pre-
Sequencing Kit (USB Corporation, Cleveland, Ohio). Cleaned PCR prod-
ucts were sequenced at the Rhode Island Genomics and Sequencing Center
with either a 3130XL Genetic Analyzer or a 3500XL Genetic Analyzer
(Applied Biosystems, Life Technologies, Inc., Grand Island, New York).
Fig. 1. Dated phylogeny. Maximum clade credibility chronogram from BEAST analysis of the combined core Caryophyllales dataset. Branch labels
show Bayesian posterior probabilities from the BEAST analysis and the MrBayes analysis (the latter included only when they differ from the BEAST
analysis), and values from 1000 bootstrap replicates with RAxML. Posterior probabilities of 1.0 and bootstrap values of 100 are replaced by asterisks,
whereas posterior probabilities less than 0.95 and bootstrap values less than 70 are replaced by dashes. When more than one accession per species was
included, the locality after the name corresponds to those in Appendix 1. Members of Kewa are shown in bold. SAfr 5South Africa.
SYSTEMATIC BOTANY [Volume 43690
The same primers were used for PCR and sequencing, with additional
internal primers being used to sequence samples for which trnK-matK
could be amplified as a single fragment. Chromatograms were edited and
contigs were constructed using ChromasPro v. 1.7.5 (Technelysium Pty.
Ltd., Tewantin, Queensland, Australia).
Sequence Alignment, Phylogenetic Analyses, and Divergence Time
Estimation—Sequences were aligned using MAFFT v. 7.271 (Katoh and
Standley 2013) and alignments were checked by eye and manually adjusted
in AliView v. 1.18.1 (Larsson 2014). Maximum likelihood bootstrap ana-
lyses were performed using RAxML-HPC-PTHREADS-AVX v. 8.2.4
(Stamatakis 2014). A first analysis was made using trnK-matK and rbcL
sequences and with Simmondsia as outgroup in agreement with Thulin et al.
(2016). As ITS sequences were not possible to align across this group of
taxa, a second analysis of ITS sequences from Kewa and with Corbichonia
and Lophiocarpus as outgroups was made. In the trnK-matK/rbcL tree
(Supplemental Fig. S1) all species except K. bowkeriana (samples from
Namibia and South Africa) were monophyletic, whereas in the ITS tree
(Supplemental Fig. S2) K. bowkeriana (samples from Namibia, South Africa
and Madagascar) was monophyletic, but K. salsoloides was paraphyletic
with respect to K. caespitosa. As otherwise no strong conflicts between the
topologies of the trnK-matK/rbcL (Fig. S1) and ITS (Fig. S2) analyses could
be detected, the two datasets were concatenated and analyzed together. For
each analysis, a search for the best tree was combined with 1000 bootstrap
pseudoreplicates. Models of nucleotide substitution were chosen according
to the corrected Akaike information criterion (AICc) as implemented with
PartitionFinder v. 2.1.1 (Lanfear et al. 2016). The optimal model for ITS was
GTR 1G and for trnK-matK and rbcL GTR 1I1G. Due to limitations in
RAxML, only one model can be used in a partitioned dataset and
GTRGAMMA was selected for all partitions.
Bayesian inference tree searches were performed with MrBayes v. 3.2.1
(Ronquist et al. 2012). For the combined dataset we did two runs of four
chains each (one cold and three heated), for 10 million generations. For this
analysis, each locus was assigned a separate partition with model sub-
stitution parameters unlinked, and branch lengths linked. Substitution
models were selected with PartitionFinder as described for RAxML above.
The posterior was sampled every 1000 generations. Inspection of log-files
in Tracer v. 1.5 (Rambaut and Drummond 2009) revealed that all the runs
converged within the first two million generations. We excluded the first
two million generations (20%) of each run as burn-in before summarizing
the posterior.
Divergence times for the stem and crown clade of Kewa were estimated
using BEAST v. 1.8.4 (Drummond et al. 2012). Due to the paucity of
Caryophyllales fossils, we used a combination of primary and secondary
calibration points in our dating analyses. For our two secondary calibration
points, we used two normally distributed age priors: 51.9 million years
(Ma) (with a standard deviation of 10%) assigned to the node between
Molluginaceae and the Portulacinae clade, based on Christin et al. (2011),
and 25 Ma (with a standard deviation of 10%) assigned to the node between
Opuntia Mill. and Pereskia aculeata Mill., based on Arakaki et al. (2011). In
addition, a minimum age constraint of 60 Ma was assigned to the node
between Dianthus L. and Spinacia L., based on the fossil pollen Chenopo-
dipollis multiplex (Weyland & Pflug) Krutzsch (Nichols and Traverse 1971).
This primary calibration point was modeled as a gamma-shaped distri-
bution (shape 51.5, scale 55, offset 560). The analyses were performed
with a lognormal, uncorrelated clock model with a birth-death tree prior.
Priors were set to default values except for the previously described node
ages. GTR 1G and GTR 1I1G nucleotide substitution models as in the
MrBayes analysis were used. We ran the analysis three times for 100 million
generations and sampled the posterior every 1000 generations. Visual
inspection in Tracer v. 1.5 (Rambaut and Drummond 2009) revealed that all
runs converged within 10 million generations. Therefore, the first 10
million generations (10%) of each run were removed as burn-in before we
combined the runs with LogCombiner v. 1.8.0 (Rambaut and Drummond
2013a). Finally, we summarized the tree samples with TreeAnnotator v.
1.8.0 (Rambaut and Drummond 2013b).
Results
Combined Core Caryophyllales Dataset—The dated phy-
logeny based on the combination of trnK-matK, rbcL, and ITS
data is shown in Fig. 1 (maximum likelihood (ML) and
Bayesian inference trees showing branch lengths are in Figs.
S3 and S4, respectively). Corbichonia (Corbichoniaceae) and
Lophiocarpus (Lophiocarpaceae) together are strongly sup-
ported as sister to a clade with members of Kewaceae (Kewa),
Barbeuiaceae (Barbeuia), Gisekiaceae (Gisekia), Aizoaceae (Conicosia,
Galenia, Gibbaeum, Mesembryanthemum, Sesuvium, Tetragonia),
Phytolaccaceae (Phytolacca), Sarcobataceae (Sarcobatus), Petiver-
iaceae (Petiveria, Rivina), and Nyctaginaceae (Bougainvillea, Guapira,
Mirabilis).
Kewa is strongly supported, and within the genus, the two
samples of K. acida come out together with strong support, as
do the two samples of K. angrae-pequenae and the two samples
of K. caespitosa. The four samples of K. bowkeriana form an
unsupported clade in the ML and MrBayes analyses, but in the
BEAST analysis (Fig. 1), this clade is well supported. Within K.
bowkeriana, the two samples from Namibia form a strongly
supported pair in all analyses, as do the two samples from
South Africa (KwaZulu-Natal) and Madagascar. Kewa salso-
loides, represented by three samples, is recovered as mono-
phyletic, but without support in the BEAST analysis (Fig. 1).
However, in the ML and MrBayes analyses K. salsoloides is
paraphyletic with respect to K. caespitosa. The relationships
between the species are mostly unsupported, notably K. acida
on St. Helena is sister to the rest of the species in the BEAST
analysis, but without support, whereas ML and MrBayes
retrieve a basal polytomy within the genus. Kewa angrae-
pequenae is well supported as sister to K. salsoloides and K.
caespitosa together in all three analyses.
Divergence Time Estimates—The divergence time estimates
resulted in an age of (37.5–)45.0(–57.0) Ma for the Kewa stem
clade and (3.0–)3.9(–7.4) Ma for the Kewa crown clade (Fig. S5).
The age of the Kewa crown clade would also be the estimated
date when the stem clade of K. acida diverged from its potential
sister group on the African continent, and thus a potential
maximum age of when K. acida colonized St. Helena. Within
Kewa, the crown clade of the widespread K. bowkeriana has an
estimated age of (1.5–)1.8(–4.5) Ma, whereas the crown clades
of the narrowly distributed K. acida, K. angrae-pequenae, and K.
caespitosa, as well as the fairly widespread K. salsoloides, are
much younger.
Discussion
The topology of the tree based on the core Caryophyllales
dataset (Fig. 1) essentially agrees with the results of Thulin
et al. (2016), the main difference being the increased sampling
of members of Kewa.Kewa is strongly supported, comprising
all the samples of the included species: K. acida, K. angrae-pequenae,
K. arenicola, K. bowkeriana, K. caespitosa, and K. salsoloides.The
narrowly distributed species K. acida, K. angrae-pequenae,andK.
caespitosa are strongly supported, whereas the more widespread
and variable K. bowkeriana and K. salsoloides are unsupported or, in
thecaseofK. bowkeriana, supported only in BEAST.
Within K. bowkeriana, the samples from South Africa
(KwaZulu-Natal) and Madagascar come out together with
strong support, as do the two samples from Namibia. While all
samples of K. bowkeriana came out together in the ITS tree, the
South African sample was separated from the Namibian
samples with the trnK-matK sequences (trnK-matK sequences
could not be obtained for the Madagascar sample). The syn-
onymization of Hypertelis suffruticosa ([K. suffruticosa from
Madagascar with the continental African H. bowkeriana ([K.
bowkeriana) by Jeffrey (1961) therefore is corroborated.
Kewa angrae-pequenae is well supported as sister to K. sal-
soloides and K. caespitosa together. This clade also has some
morphological support as the three species included differ
from other species of Kewa by having mostly pink (versus
THULIN ET AL.: PHYLOGENY AND SYSTEMATICS OF KEWA 6912018]
mostly white) flowers. The species pair K. salsoloides and K.
caespitosa also has good support, although K. salsoloides is
recovered as paraphyletic with respect to K. caespitosa in two of
the analyses (and in the ITS, but not the chloroplast tree).
Otherwise, the relationships between the species are un-
supported. The sister group relationship between K. acida on
St. Helena and the rest of the species recovered in the BEAST
analysis, albeit without support, indicates that the estimated
age of the Kewa crown clade, (3.0–)3.9(–7.4) Ma, would also
coincide with the earliest possible date for the introduction of
the ancestor of K. acida to St. Helena. This inference is further
supported by Kewa outgroups also being distributed on the
African mainland, strongly suggesting that stem lineage Kewa
resided in mainland Africa, and the St. Helena disjunction is
due to a single, long distance dispersal from Africa to
St. Helena.
The volcanic St. Helena emerged from the sea approxi-
mately 14 MYA (Cresswell 2016). The island is extremely
remote, the nearest land being the Ascension Island, about
1100 km towards northwest. The distance to Africa, the nearest
continent, is about 1900 km, and to South America about
2700 km.
The early colonization of the remote and inhospitable St.
Helena by plants must have been a very slow process (Ashmole
and Ashmole 2000; Lambdon 2012). A late Miocene deposit on
St. Helena with spores and pollen about 9 Ma revealed an island
dominated by ferns and lycopods (Muir and Baker 1968), but
some angiosperms were also present, notably the genus Tro-
chetiopsis (Malvaceae), with three species recorded on the island
(Cronk 1990), two of which are still extant (Lambdon 2012).
According to Lambdon (2012), 45 endemic species of vas-
cular plants can be recognized on St. Helena today and the
native flora includes between 31 and 43 further species, three
of which are now extinct. Many of the endemics, particularly in
the dry zone at lower altitudes, have their closest relatives in
southern Africa, and were assumed to be of a more recent
origin than the endemics of the wet zone (Cronk 2000). In any
case, their ancestors must have arrived in St. Helena by long
distance dispersal during the 14 Ma that the island has existed.
Kewa acida, the ancestor of which is estimated to have diverged
from its African relatives (3.0–)3.9(–7.4) MYA, does not appear
to be particularly recent, although it is confined to the dry
zone. Other endemics on St. Helena that have been dated are
Phylica polifolia (Vahl) Pillans (Rhamnaceae), a shrub or small
tree that seems to be a recent result of a radiation that started
about 2 MYA (Richardson et al. 2001), and the extinct endemic
genus Nesiota Hook.f. (Rhamnaceae), with the single arbo-
rescent species N. elliptica (Roxb.) Hook.f., the ancestor of
which was estimated to have diverged from its sister, Tri-
chocephalus stipularis (L.) Brogn. from the Western Cape of
South Africa, about 12 MYA (Richardson et al. 2001).
Taxonomic Treatment
KEWACEAE Christenh., Phytotaxa 181: 240. 2014. TYPE:Kewa
Christenh.
Family of a single genus.
KEWA Christenh., Phytotaxa 181: 240. 2014. TYPE:Kewa salso-
loides (Burch.) Christenh.
Annual or perennial glaucous herbs, subshrubs or dwarf
shrubs, glabrous or with minute glandular hairs, each borne at
the tip of cone-shaped outgrowths of the mesophyll that re-
main as sometimes prominent warts, particularly on pedun-
cles, pedicels, and outside of the perianth. Leaves alternate or
subopposite, often crowded and with axillary short-shoots,
sessile, with an acid taste apparently due to presence of oxalic
acid; stipules persistent, membranous, entire to denticulate,
with lower part adnate to the leaf-base and forming a 6
amplexicaul sheath; leaf-blades linear to narrowly obovate in
outline, succulent, almost terete, with a 6distinct groove on
the underside, entire. Inflorescences terminal, often becoming
seemingly axillary, pedunculate, umbel-like cymes, with 1–
many pedicellate flowers, each flower with a bract and 2
bracteoles at base of pedicels; bracts and bracteoles mem-
branous, entire to denticulate; pedicels often 6deflexed.
Flowers chasmogamous or sometimes cleistogamous; peri-
anth of 5 free unequal segments, with quincuncial aestivation
in bud; segments with median part greenish, 6rounded on the
back, membranous margins narrow in 2 outer 6elliptic and
sepaloid segments, widened and 6conspicuous in 3 inner 6
broadly obovate and petaloid, pink or white ones. Stamens
3–15, when 5 alternate with the perianth segments, the fila-
ments linear, slightly united at the base; anthers basifixed,
dehiscing by longitudinal slits. Disk absent. Ovary superior,
syncarpous, of (3–)5 carpels, (3–)5-locular, with numerous
axile ovules; stigmas (3–)5, spreading to 6appressed to top of
ovary. Capsule ovoid-elliptic to subglobose, surrounded by
perianth, thin-walled, loculicidally dehiscent, the central axis
remaining in the middle after dehiscence. Seeds pear- to
comma-shaped in outline, smooth to tuberculate, brownish-
black, with a minute strophiole; embryo straight. Chromo-
some number n58 (reported only for Kewa bowkeriana).
Figures 2, 3.
Distribution—Six species in southern and eastern Africa,
Madagascar, and St. Helena (Fig. 4).
General Remarks—As in many other members of Car-
yophyllales, the flowers of Kewa possess a simple perianth
with five, free, quincuncially arranged perianth-segments.
However, in Kewa the two outer perianth-segments are
more or less sepaloid, whereas the three inner ones are more or
less petaloid (Figs. 2, 3). This differentiation within the peri-
anth is most obvious in the more large-flowered species, such
as the white-flowered K. acida (Christenhusz et al. 2017) and
the pink-flowered K. salsoloides, whereas it is somewhat less
prominent in, for example, K. bowkeriana, a species with more
inconspicuous and sometimes even cleistogamous flowers.
The perianth parts of “Hypertelis”have been said to be
chimeric (Brockington et al. 2009), i.e. each perianth part
would be partly sepaloid and partly petaloid. This may be true
for H. spergulacea, where all perianth parts are more or less
equal, petaloid above and sepaloid below, but not for the
differentiated perianth of Kewa. The differentiation among the
perianth-segments within a simple 5-merous perianth as seen
in Kewa indeed seems to be unique in Caryophyllales and
perhaps in flowering plants in general.
AnotherpeculiarfeatureofKewaceaeistheindu-
mentum. It consists of short glandular hairs, which may
have a many-celled thickened and often more or less
conical wart-like base of mesophyll covered by elongate
epidermis cells (Fig. 3D). These warts or “glands”occur on
both vegetative parts and on the perianth, but in varying
amountsandsizesinthedifferent species. When situated
on pedicels or perianths they tend to become reddish-
brown in colour and can be very prominent (Fig. 3A),
SYSTEMATIC BOTANY [Volume 43692
remaining long after the ephemeral top part has fallen off.
The function of these warts is unknown and no similar
structures seem to be known in related families.
Many families within Caryophyllales are characterized by
having a blue/red pigmentation of betalains rather than the
ubiquitous anthocyanins in other flowering plants, and
according to Brockington et al. (2015) a single origin of the
betalain pigmentation is most likely. Reversals from betalains
to anthocyanins have occurred within the betalain-producing
clade a few times, one example being Kewaceae in which the
occurrence of anthocyanins was confirmed in K. salsoloides by
Thulin et al. (2016).
Fig. 2. Kewa salsoloides. A. Habit. B. Leaf with stipules. C. Portion of underside of leaf, showing groove. D. Inflorescence. E. Flower. F. Sepaloid perianth-
segment. G. Petaloid perianth-segment. H. Stamen. I. Ovary and styles. J. Cross-section of ovary. K. Capsule. L. Seed. Scale bars: A 510 mm; B, D 55 mm; C,
E–K51 mm; L 50.5 mm. Drawn from Thulin et al. 11956 by Margaret Tebbs.
THULIN ET AL.: PHYLOGENY AND SYSTEMATICS OF KEWA 6932018]
In the protologue of Kewa acida (as Pharnaceum acidum),
Hooker (1867) mentioned the acid taste of the plant and its use
as a salad plant on St. Helena, and Melliss s. n. (K), a specimen
of K. acida, has a note saying that the succulent leaves of this
plant have “the acid flavour of Oxalis.”This acid taste, ap-
parently due to the presence of oxalic acid (H. El-Seedi
unpubl.), is common to all species of Kewa and is an excel-
lent field character for the group (M. Thulin pers. comm.). The
acid taste has also been noted by various other collectors (e.g.
in K. salsoloides,Hanekom 2155, K), and is reflected in the
vernacular name “braksuring”(brak is brackish and suring
sorrel in Afrikaans).
Key to the Species of
Kewa
1. Perianth-segments 7 mm or more long. . ...................................................................................1.K. acida
1. Perianth-segments up to 5 mm long. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Stamens 12–15...............................................................................................................3
3. Leaves 6narrowly obovate in outline, 6–15 32–4 mm; inflorescences 1–3-flowered, smooth or sparsely warty. . . . . . . . . . . . . . . . . . . . . . . . . . . .
..........................................................................................................2.K. angrae-pequenae
3. Leaves linear to narrowly oblanceolate in outline, 5–40 31–3 mm; inflorescences 3–10-flowered, with many prominent warts on peduncles, pedicels,
and outside of perianth. . . . .......................................................................................6.K. salsoloides
2. Stamens 3–9...................................................................................................................4
4. Leaves 0.5–1 mm wide; peduncles, pedicels, and outside of perianth mostly with prominent warts; stamens 5. ...............4.K. bowkeriana
4. Leaves 1–2.5 mm wide; peduncles, pedicels, and outside of perianth mostly smooth and without prominent warts; stamens 3–9...............5
5. Plant annual; perianth-segments 2–3 mm long; stamens 3–5; seeds almost smooth to distinctly tuberculate. . . . . . . . . . . . . . . . . . . 3. K. arenicola
5. Plant perennial; perianth-segments 3–5 mm long; stamens 5–9; seeds smooth. ..........................................5.K. caespitosa
1. KEWA ACIDA (Hook.f.) Christenh., Phytotaxa 181: 241.
2014. Pharnaceum acidum Hook.f., Ic. Pl. 11: 26, t. 1035.
1867. Hypertelis acida (Hook.f.) K. M ¨ull., Bot. Jahrb. Syst.
42, Beih. 97: 62. 1908. TYPE:ST. HELENA. Sandy Bay,
Burchell 113 (lectotype: K! barcode K000232014, desig-
nated by Adamson, J. S. Afr. Bot. 24: 57. 1957).
Note on Typification—Cronk (2000) designated Burchell
113 in K as lectotype and this typification was also cited by
Christenhusz et al. (2017). However, already Adamson (1957)
cited the Burchell specimen at K as “Type”, and this is here
regarded as the first lectotypification in accordance with ICBN,
Art. 9.8 (McNeill et al. 2012).
Annual to short-lived perennial herb or subshrub, up to
40 cm tall, ascending, glabrous. Leaves linear to narrowly
oblanceolate, 20–60(–80) 31.5–6 mm. Inflorescences with
peduncles 5–16 cm long, 2–15-flowered; pedicels 6–30 mm
long. Flowers with perianth-segments 7–12 mm long,
spreading to somewhat deflexed at anthesis, the petaloid
segments white. Stamens ca. 15, ca. 4 mm long; anthers
0.7–0.8 mm long. Ovary 5-locular; stigmas 5, ca. 1.5 mm long,
6spreading and curved. Capsule 7–8 mm long. Seeds ca.
0.6 mm long, obscurely tuberculate. Figure 3B.
Distribution—Kewa acida is endemic to St. Helena (Fig. 4A),
where it is confined to the southern coastal fringe (Lambdon
2012).
Habitat—Stony or rocky hillsides or cliffs; near sea level to
500 m.
Notes—Kewa acida is the species with the largest flowers in
the genus (Fig. 3B). According to Lambdon (2012) plants in
Fig. 3. A. Kewa salsoloides, inflorescence, from Klein Aus, Namibia. B. Kewa acida, inflorescence, from St. Helena. C. Kewa bowkeriana, inflorescence, from
Madagascar (progeny of Thulin & Razafindraibe 11819 cultivated in Uppsala). D. Kewa bowkeriana, glandular hair with wart-like base (plant origin as in C).
Photos by M. Thulin (A), Phil Lambdon (B), Magnus Lid ´en (C), and Allison Perrigo (D).
SYSTEMATIC BOTANY [Volume 43694
drier locations near sea level tend to be annual, whereas at
higher locations affected by mist they tend to perennate.
Representative Specimens Examined—St. Helena. In valley near Sandy
Bay, Jan 1954, Kerr 3 (BM); Long Range, 21 Feb 2009, Herian et al. ECS18 (K).
2. KEWA ANGRAE-PEQUENAE (Friedrich) Christenh.,
Phytotaxa 181: 241. 2014. Hypertelis angrae-pequenae
Friedrich, Mitt. Bot. Staatssamml. M¨unchen 2: 62. 1955.
TYPE: NAMIBIA. L¨uderitz Distr., road to Aussensee, 24
May 1950, Kinges 2799 (holotype: M barcode M0107809
[digital image!]; isotypes: M barcode M0107810 [digital
image!], PRE barcode PRE0404567 [digital image!]).
Subshrub or shrublet, up to 30 cm tall, ascending, gla-
brous or sometimes with scattered glandular hairs that
Fig. 4. Distributions of species of Kewa.A.K. acida (triangle), K. bowkeriana (circles). B. K. salsoloides.C.K. angrae-pequenae (triangles), K. arenicola (squares),
K. caespitosa (circles).
THULIN ET AL.: PHYLOGENY AND SYSTEMATICS OF KEWA 6952018]
remain as prominent 6reddish-brown warts at least on
pedicels. Leaves 6narrowly obovate, 6–15 32–4 mm, obtuse
to acute at the apex. Inflorescences on peduncles 1–2(–3) cm
long, 1–3-flowered; pedicels 5–10(–20) mm long. Flowers
with perianth-segments 4–4.5 mm long, 6deflexed at anth-
esis, the petaloid ones white to pink. Stamens 12–15, ca.
2.5 mm long; anthers ca. 0.8 mm long. Ovary 5-locular; stigmas 5,
ca.0.8mmlong.Capsuleca.4mmlong.Seeds0.7–0.8 mm long,
smooth.
Distribution—Kewa angrae-pequenae is distributed in coastal
regions of south-western Namibia and adjacent parts of north-
western South Africa (Fig. 4C).
Habitat—Confined to sandy or stony ground; near sea
level.
Notes—Kewa angrae-pequenae agrees with K. salsoloides by
having flowers with 12–15 stamens and perianth-lobes that are
more or less deflexed at anthesis. It differs in its short and wide
leaves, in its 1–3 (versus 3–10)-flowered inflorescences with
short peduncles, and in its often smooth (versus always warty)
pedicels and perianth. Warts on pedicels and perianth seem
never to occur in plants from the northern part of the range
(Namibia), but are mostly prominent in plants from South
Africa.
Representative Specimens Examined—Namibia.—KARAS:L¨uderitz,
near Fjord, 26.70313S, 15.08909E, 20 Apr 2013, Thulin & Larsson 11968 (UPS,
WIND); L ¨uderitz peninsula, kleiner Bogenfels to Essy Bay, 26.72232°S,
15.08922°E, 6 Oct 2006, Kolberg & Tholkes 2062 (K, WIND); Oranjemund,
Yacht Basin area, [28.61667°S, 16.43333°E], 17 Feb 1991, Ward 11126 (K,
WIND). South Africa.—NORTHERN CAPE: Port Nolloth, Holgat, Sep 1929,
Schlechter 10902 (K).—WESTERN CAPE: Rob Eiland beach N of Olifants River
mouth, 16 Aug 1978, Roux & Ramsey 70 (K).
3. KEWA ARENICOLA (Sond.) Christenh., Phytotaxa 181:
241. 2014. Hypertelis arenicola Sond. in Harv. & Sond., Fl.
Cap. 1: 145. 1860. TYPE:SOUTH AFRICA. Western Cape,
Green Point, Zeyher 619 (lectotype: S no. S05–4763!,
designated by Adamson, J. S. Afr. Bot. 24: 58. 1957; iso-
lectotypes: BM! barcode BM000902639, BOL barcode
BOL128290 [digital image!], K! barcode K000232006, PRE
barcode PRE0404565–0 [digital image!], SAM barcode
SAM0036904–0 [digital image!], TCD barcode TCD0002765
[digital image!]).
5Hypertelis trachysperma Adamson, J. S. Afr. Bot. 12: 35. 1946.
Kewa trachysperma (Adamson) Christenh., Phytotaxa 181: 241.
2014. TYPE:SOUTH AFRICA.WesternCape,ZeekoeVlei,22Apr
1946, Walgate 687 (holotype: BOL barcode BOL128291 [digital
image!]; isotypes: NBG barcode NBG0021524–0[digital
image!], SAM barcode SAM0057871–0 [digital image!],
SAM barcode SAM0074853–0 [digital image!]).
Note on Typification—Adamson (1957) cited Zeyher 619 in
Sas“type”of Hypertelis arenicola. The specimen in S here cited
as lectotype has the number 619, but the name of the collector is
given as “Dr Pappe.”However, it is well known that Pappe
sometimes changed the names of collectors in this way (Gunn
and Codd 1981).
Annual herb, with prostrate to ascending stems up to 15 cm
long, glabrous. Leaves linear to narrowly oblanceolate, 5–45 3
1–1.5 mm, glabrous, obtuse to acute at the apex. Inflorescences
on peduncles 0–4 cm long, 1–6-flowered; pedicels 2–10 mm
long. Flowers with perianth-segments 2–3 mm long, spreading
at anthesis, the petaloid segments pink to whitish. Stamens
3–5, ca. 1.5 mm long; anthers ca. 0.4 mm long. Ovary 3–5-
locular; stigmas 3–5, ca. 0.4 mm long. Capsule 2–3 mm long.
Seeds ca. 0.6 mm long, almost smooth to distinctly tuberculate
throughout or with tubercles close to hilar end only.
Distribution—Kewa arenicola is known from the Northern,
Western, and Eastern Cape Provinces in South Africa (Fig. 4C).
Habitat—On open muddy or sandy ground, mostly in
seasonally wet depressions; near sea level to 630 m.
Notes—Adamson recognized Hypertelis trachysperma as
distinct from H. arenicola on the basis of peduncles shorter (versus
longer) than leaves, five (versus three) stamens, and tuberculate
(versus smooth) seeds (Adamson et al. 1946; Adamson 1957).
These characters were also used by Christenhusz et al. (2014) to
separate these species (as Kewa trachysperma and K. arenicola).
However, the lectotype of K. arenicola clearly has tuberculate
seeds and this character therefore cannot be used for species
distinction in the way proposed by these authors. Some col-
lections of K. arenicola in the wider sense taken here indeed have
almost smooth seeds, but there is apparently sometimes vari-
ation within populations. For example, Hafstr¨
om s. n. (S), cited as
Hypertelis arenicola by Adamson (1957) consists of five in-
dividuals with tuberculate seeds and one with almost smooth
seeds. Furthermore, tubercles are also present to various extents
even in seeds that are almost smooth, particularly near the hilar
end of the seeds. As for peduncles, there seems to be no cor-
relation between peduncle length and seed ornamentation, and
the number of stamens may vary from three to five within a
single population, such as the tuberculate-seeded Helme 6500,
where flowers with three, four, or five stamens were recorded.
The gynoecium in K. arenicola is 3-, 4- or 5-merous and may
vary within populations and even within a single plant, such
as in one of the individuals of Acock 3916 (S). In all other species
of Kewa the gynoecium is consistently 5-merous.
Acocks 19199, the only collection seen from Northern Cape,
consists of plants with particularly short peduncles, varying
from 0 to just a few mm. A photograph of a plant from N of
Nieuwoudtville, also in Northern Cape, communicated by
Nick Helme, also shows very short or non-existing peduncles,
indicating a geographically correlated variation in this respect.
Representative Specimens Examined—South Africa.—NORTHERN CAPE:
Calvinia, Lokenburg, 16 Mar 1957, Acocks 19199 (K).—WESTERN CAPE:
Paarden Island, 22 Dec 1934, Acock 3916 (S); Cape Point Nature Reserve,
0.6 km N Olifantsbos Bay, [34.25069°S, 18.38153°E], 11 Feb 2010, Helme
6500 (NBG).—EASTERN CAPE: Uitenhage, near Redhouse, Aug 1912, Paterson
2219 (K).
4. KEWA BOWKERIANA (Sond.) Christenh., Phytotaxa 181:
241. 2014. Hypertelis bowkeriana Sond. in Harv. & Sond., Fl.
Cap. 1: 145. 1860. TYPE:SOUTH AFRICA, Cape Province,
Albany, Bowker s. n. (holotype: K! barcode K000232011;
isotype: S! no. S05–5021).
5Pharnaceum suffruticosum Baker, J. Linn. Soc. Bot. 20: 151.
1883, nom. illeg. (non Pallas, Reise Russ. Reich. 3: 716.
1776). Hypertelis suffruticosa Adamson, J. S. Afr. Bot. 24: 55.
1957. Kewa suffruticosa (Adamson) Christenh., Phytotaxa
141: 241. 2014. TYPE:MADAGASCAR. Ambongo, 16 Feb 1841,
Pervill´e 647 (holotype: K! barcode K000232013; isotypes: P!
barcodes P04999563, P04999566).
5Mollugo suffruticosa Peter, Abh. Ges. Wiss. G ¨ottingen, n.f.
13(2): 54. 1928. TYPE:TANZANIA. Pare Distr., NW of Buiko
toards Hedaru, 10–11 Jun 1926, Peter 41190 (holotype: B
barcode B100159478 [digital image!]).
5Mollugo suffruticosa Peter forma annua Peter, Fl. Deutsch Ost-
Afr. 2(2): 29. 1932. TYPE:TANZANIA. Lushoto Distr., Lake
Manga, Peter 10864 (holotype: B, destr.).
SYSTEMATIC BOTANY [Volume 43696
Perennial herb or subshrub, up to 30 cm tall, sometimes
forming carpets by means of prostrate stems and ascend-
ing branches, with scattered glandular hairs that often re-
main as prominent 6reddish-brown warts, particularly on
pedicels and outside of perianth. Leaves linear, 10–75 3
0.5–1 mm, obtuse to subacute at the apex. Inflorescences
with peduncles 3–10 cm long, 2–8-flowered; pedicels 2–10
(–20) mm long. Flowers chasmogamous or sometimes
cleistogamous; perianth-segments 3–4mmlong,erector
spreading, rarely becoming deflexed at anthesis, the pet-
aloid segments white or sometimes pink or with pink tips.
Stamens 5, 2–3mmlong;anthers0.4–0.6 mm long. Ovary
5-locular; stigmas 5, ca. 0.5 mm long, spreading and curved
or 6appressed to top of ovary. Capsule 3.5–5mmlong.
Seeds 0.5–0.6 mm long, smooth. Chromosome number n58
(Ratter 1968). Figure 3C, D.
Distribution—Kewa bowkeriana is the most widespread
species in the genus and has been recorded from Ethiopia,
Kenya, Tanzania, Zimbabwe, Mozambique, Swaziland, Bot-
swana, Namibia, South Africa, and Madagascar (Fig. 4A). The
distribution is not continuous, but shows marked disjunctions
between the arid areas in eastern and southern Africa and
between southern (Toliara) and northwestern Madagascar
(Mahajanga). The species is well established and widespread
in Toliara, whereas only two collections seem to have been
made in Mahajanga, Pervill´e 647 (type of Pharnaceum suf-
fruticosum) from 1841 and Perrier de la Bˆathie 1659 from 1903. It
is quite possible that the Mahajanga population reached
Madagascar from East Africa and the Toliara population from
southern Africa.
Habitat—In open situations, mostly on sandy or gravelly,
saline ground, such as in salt pan depressions and at margins
of mangroves; near sea level to 1850 m.
Notes—Kewa bowkeriana is well supported as mono-
phyletic only in the BEAST analysis, whereas it forms an
unsupported clade in the ML and MrBayes analyses (Fig. 1).
The species (with samples from Namibia, South Africa and
Madagascar) is also supported as monophyletic in the ITS
tree (Fig. S2). However, in all combined analyses (Fig. 1), the
two samples from Namibia form a strongly supported pair,
as do the two samples from South Africa (KwaZulu-Natal)
and Madagascar.
This molecular differentiation within K. bowkeriana is not,
as far as we have been able to detect, correlated with any
corresponding morphological differentiation. Instead, K.
bowkeriana is relatively uniform over its large and disjunct
area of distribution. It differs from all the other species in the
genus by its very narrow, only 0.5–1 mm wide, leaves. It
agrees with K. salsoloides in usually having warts on pedicels
and outside of the perianth (Fig. 3C, D, but differs from this
species, apart from leaf width, by having flowers with 5
(versus 12–15) stamens and usually white (versus pink)
petaloid perianth-segments (Fig. 3C). The perianth-segments
are mostly erect or spreading in K. bowkeriana (Fig. 3C), but
they may occasionally be more or less deflexed at anthesis as
in K. salsoloides.
Christenhusz et al. (2014) separated K. salsoloides from K.
bowkeriana (and from all other species of Kewa except K. acida)
by its warty (versus smooth) peduncles, pedicels, and peri-
anth. This is a mistake repeated from Adamson (1957). Warts
in the inflorescence region are normal in K. bowkeriana and are
sometimes present also in K. caespitosa and K. angrae-pequenae.
Representative Specimens Examined—Ethiopia.—SIDAMO:ElSod,
[4.2°N, 38.38333°E], 15 Nov 1952, Gillett 14270 (K). Kenya.—LAIKIPIA DISTR.:
67 km N of Rumuruti on Maralal road, [0.7°N, 36.61667°E], 14 Nov 1977,
Carter & Stannard 370 (K).—LAMU DISTR.: 2 km SE of Kibauni, N of Kipini, 4
Mar 1977, Hooper & Townsend 1186 (K). Tanzania.—MBULU/SINGIDA DISTR.:
Yaida valley, Endashi, 19 Jan 1970, Richards 25187 (K).—LUSHOTO DISTR.:
Lake Manka, Jun 1967, Procter 3679 (K). Zimbabwe.—GWANDA DISTR.: near
Sundowner Hotel, Gwanda, 26 Mar 1959, Drummond 6038 (K).—MATOBO
DISTR.: 12 km SE of Figtree on Matopos road, 29 Jan 1974, Mavi 1495 (K).
Mozambique.—GAZA: Massingir Distr., 1 km W of Zulo, 7 Dec 1981, White
46 (K).—MAPUTO: Moamba, 15 km on road to Chinhanguanine, 31 Oct 1980,
de Konig & Nuvunga 8589 (K). Botswana.—NGAMILAND: near Tsau, 18 Mar
1961, Richards 14775 (K).—SOUTHEAST: Gaberones Dam, 25 Aug 1966, Gillett
17470 (K). Namibia.—OTJOZONDJUPA: Okahandja, 10 Aug 1934, Dinter 7789
(WIND).—KHOMAS: Windhoek, Avis Dam, 22.57790°S, 17.12539°E, 9 Apr
2013, Thulin & Larsson 11945 (UPS, WIND). South Africa.—LIMPOPO:24km
W of Pietersburg, 27 Jan 1962, van Vuuren 1366 (K).—KWAZULU-NATAL:
Lower Tugela valley below Maqumbi, 28 Feb 1963, Edwards 3054 (K); E of
Ingwavuma, 27.06338°S, 32.18979°E, 5 Apr 2013, Thulin et al. 11943 (NU,
UPS).—EASTERN CAPE: 35 km from Grahamstown on Cradock road, Sep
1929, Dyer 2109 (K). Madagascar.—MAHAJANGA: near Soalala (Ambongo),
Oct 1903, Perrier de la Bˆathie 1659 (P).—TOLIARA:NWofCapSainte-Marie
towards Lavanono, 8 Mar 1955, Humbert & Capuron 29333 (G, HBG, K, MO,
P, TAN, WAG); E of Amboasary, 7 km after turning to Tsimelahy,24.9721°S,
46.6189°E, 9 Apr 2010, Thulin & Razafindraibe 11819 (TAN, UPS).
5. KEWA CAESPITOSA (Friedrich) Christenh., Phytotaxa
181: 241. 2014. Hypertelis caespitosa Friedrich, Mitt.
Bot. Staatssamml. M ¨unchen 2: 64. 1955. TYPE:NAMIBIA.
Swakopmund –Cap Cross, 14 Mar 1935, Dinter 8471
(holotype: M barcode M0107811 [digital image!]; isotypes:
BM! barcode BM000902641, BOL barcode BOL128289
[digital image!], K! barcode K000232010, P! barcode
P00461734, PRE barcode PRE0404566–0 [digital image!],
S! no. S-G-7085).
5Pharnaceum salsoloides Burch. var. mossamedensis Welw. ex
Hiern, Cat. Afr. Pl. Welw. 1: 418. 1898. Hypertelis salsoloides
(Burch.) Adamson var. mossamedensis (Welw. ex Hiern)
Gonç., Consp. Fl. Angol. 4: 321. 1970. TYPE:ANGOLA.
Mossamedes, near the town of Mossamedes, Jul 1859,
Welwitsch 2381 (lectotype: BM! barcode BM000902642,
designated by Gonçalves (1970: 321); isolectotypes:
COI barcode COI00070557 [digital image!], K!, LISU
barcode LISU214655 [digital image!], LISU barcode
LISU214656 [digital image!], M barcode M0107812
[digital image!]).
Note on Typification—Gonçalves (1970) cited Welwitsch
2381 in BM as “hol´otipo”of Pharnaceum salsoloides var. mos-
samedensis. This statement is here regarded as a lectotypifi-
cation in accordance with ICBN, Art. 9.8 (McNeill et al. 2012).
Perennial herb or subshrub, up to 15 cm tall, usually with
many decumbent to ascending stems, glabrous or sometimes
with a few scattered glandular hairs that remain as prominent
6reddish-brown warts on pedicels and outside of perianth.
Leaves linear to narrowly oblanceolate 5–30 31–2.5 mm,
obtuse to subacute at the apex. Inflorescences with peduncles
1–7 cm long, 2–8-flowered; pedicels 4–18 mm long. Perianth-
segments 3–5 mm long, 6deflexed at anthesis, the petaloid
segments pink. Stamens 5–9, 2–3 mm long; anthers 0.4–0.6 mm
long. Ovary 5-locular; stigmas 5, 0.5–0.8 mm long, 6spreading
and curved. Capsule ca. 4 mm long. Seeds ca. 0.6 mm long,
smooth.
Distribution—Kewa caespitosa is distributed in coastal re-
gions of southwestern Angola and west-central Namibia (Fig.
4C).
Habitat—In open situations on sandy or stony ground; near
sea level to 150 m.
THULIN ET AL.: PHYLOGENY AND SYSTEMATICS OF KEWA 6972018]
Notes—Kewa caespitosa is close to K. salsoloides from which it
differs mainly in the fewer stamens (5–9 versus 12–15) and by
mostly lacking warts on pedicels and perianth. In a large
population in Namibia studied in 2013 (Thulin et al. 11949) the
number of stamens was found to vary continuously from 5 to 9
in different plants, and sometimes the stamen number varied
within individuals. Warts on pedicels were mostly lacking, but
varied in some plants from few to several. A similar variation
was reported by Hiern (1898) from Angola in the protologue of
Pharnaceum salsoloides var. mossamedensis. Typical K. salsoloides
is not known from Angola, but in Namibia K. salsoloides and K.
caespitosa may grow in close proximity but, as far as known,
without any intergradation. Species rank for these two taxa
therefore seems appropriate, although they are not clearly
separated in the molecular analyses.
Representative Specimens Examined—Angola.—NAMIB: Pinda, R.
Coroca, 24 May 1937, Exell & Mendonça 2195 (BM); near Farol, 27 Dec 1955,
Torre 8324 (BM). Namibia.—ERONGO: just N of Wlotzkasbaken, 22.38825°S,
14.44137°E, 10 Apr 2013, Thulin et al. 11949 (UPS, WIND); ca. 8 km E of
Wlotzkasbaken, 25 Jun 2006, 22.38506°S, 14.52678°E, 25 Jun 2006, Kolberg &
Tholkes 2018 (K, WIND).
6. KEWA SALSOLOIDES (Burch.) Christenh., Phytotaxa 181:
241. 2014. Pharnaceum salsoloides Burch., Trav. Int. S. Afr. 1:
286. 1822. Hypertelis salsoloides (Burch.) Adamson in J. S.
Afr. Bot. 24: 52. 1957. TYPE:SOUTH AFRICA. Calvinia, be-
tween Zak R. and Kopjesfontein, Sep 1811, Burchell 1508
(holotype: K! barcode K000232012).
Pharnaceum verrucosum Eckl. & Zeyh., Enum. Pl. Afr. Austral.
2: 286. 1836. Hypertelis verrucosa (Eckl. & Zeyh.) Fenzl,
Ann. Wiener Mus. Naturgesch. 2: 262. 1839. TYPE:SOUTH
AFRICA.“ad flumen Gauritzrivier”,Ecklon & Zeyher 1826
(lectotype: S! no. S05–4626, designated here; isolectotypes:
C barcode C10000084 [digital image!], TCD barcode
TCD0002801 [digital image!], W barcode W0009847
[digital image!], W barcode W0009848 [digital image!]).
Hypertelis verrucosa (Eckl. & Zeyh.) Fenzl var. laevigata Sond. in
Harv. & Sond., Fl. Cap. 1: 144. 1860. TYPE:SOUTH AFRICA.
Sondagʼs rivier, Dr`ege s. n. (not located).
Note on Typification—Adamson (1957: 52) cited Zeyher 615
in S as “type”of Pharnaceum verrucosum. However, the only
collection cited in the protologue is Ecklon & Zeyher 1826,
thus Adamson’s action cannot be regarded as a valid
lectotypification.
Perennial herb or subshrub, up to 40 cm tall, ascending, with
glandular hairs that remain as prominent 6reddish-brown
warts, particularly on peduncles, pedicels, and outside of
perianth. Leaves linear to narrowly oblanceolate, 5–40 3
1–3 mm, obtuse to acute at the apex. Inflorescences with pe-
duncles 1–15 cm long, 3–10-flowered; pedicels 6–30(–40) mm
long. Flowers with perianth-segments 3–5 mm long, 6de-
flexed at anthesis, the petaloid segments pink. Stamens 12–15,
2–4 mm long; anthers 0.6–1 mm long. Ovary 5-locular; stigmas
5, 0.6–1.5 mm long, 6spreading and curved. Capsule 4–6mm
long. Seeds 0.6–0.8 mm long, smooth. Figures 2, 3A.
Distribution—Kewa salsoloides is known with certainty only
from Namibia, southern Botswana, and South Africa (Fig. 4B).
Records of Hypertelis salsoloides var. mossamendensis from
Mozambique in Gonçalves (1978) refer to material of K.
bowkeriana. Adamson (1957) previously recorded H. salsoloides
from Botswana (Bechuanaland), but the cited specimen, van
Son s. n. from near Gaberones, is K. bowkeriana. Adamson
(1957) also mentioned unspecified occurrences of H. salsoloides
in Zimbabwe and indeed one of two specimens of the col-
lection Rogers 5520 (K) from “Salisbury”is this species (the
other one being K. bowkeriana). As all other material of Kewa
seen from Zimbabwe, including the area around Salisbury
(now Harare), represents K. bowkeriana, this particular speci-
men is almost certainly mislabeled.
Habitat—In open situations, mostly on sandy or gravelly
saline ground, often in seasonally wet depressions; near sea
level to 1700 m.
Notes—Kewa salsoloides is a variable species that can be
recognized by its 3–10-flowered inflorescences with conspic-
uous warts on pedicels and outside of perianth, and by its pink
flowers with more or less deflexed perianth-lobes and 12–15
stamens. For differences from K. angrae-pequenae, K. bowkeriana
and K. caespitosa, see under these species.
Representative Specimens Examined—Namibia.—OTJOZONDJUPA:
Gross Barmen, 22.11332°S, 16.74573°E, 14 Apr 2013, Thulin et al. 11956
(UPS, WIND).—KARAS: Klein Aus, 26.65948°S, 16.23516°E, 18 Apr 2013,
Thulin & Larsson 11963 (UPS, WIND). Botswana.—KGALAGADI: Mabuase-
hube pan, 12 Mar 1976, Vahrmeijer 3071 (K, WIND). South Africa.—
NORTHERN CAPE: Farm Klein Pella between Springputs and Grootberg,
15 May 2000, Snijman 1744 (K).—WESTERN CAPE: near Robertson, 11 Jun
1955, van Niekerk 375 (K).—EASTERN CAPE: Toekomst, Somerset East,
Sundayʼs R. valley, 5 Nov 1930, Long 219 (K).—FREE STATE:39kmfrom
Philippolis on road to Luckhoff, Farm Swartfontein, 1 Mar 1981, Herman
456 (K).
Acknowledgments
We are indebted to the curators of BM, K, NBG, P, S, UPS, and WIND for
putting herbarium material and/or images at our disposal. MT and AL
acknowledge the Ministry of Environment and Tourism in Namibia for
collecting permits, and the National Botanical Research Institute and
the National Herbarium for use of facilities and logistical support; in
KwaZulu-Natal the Ezemvelo KZN Wildlife Permits Office and the
Bews herbarium are acknowledged. Particular thanks to Leevi
Nanyeni, Marianne Hochobes, and Quanita Daniels for company in the
field in Namibia, and to Douglas Stone for company in KwaZulu-Natal.
We are grateful to Margaret Tebbs for the drawing in Fig. 2, to Phil
LambdonforthephotographinFig.3BandforleafsamplesofKewa
acida,toMagnusLid´en for the photograph in Fig. 3C, to Allison Perrigo
for assistance with the photograph in Fig. 3D, to Pascal-Antoine
Christin for providing the sequence of Kewa bowkeriana from Mada-
gascar, and to two anonymous reviewers for helpful comments. The
research is based in part upon work conducted using the Rhode Island
Genomics and Sequencing Center which is supported in part by the
National Science Foundation under EPSCoR Grants Nos. 0554548 and
EPS-1004057.
Author Contributions
MT did the taxonomic work and drafted the paper, AJM did the lab-
work, AL did the phylogenetic analyses, and all authors took part in the
interpretation of the data and the final preparation of the manuscript.
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Appendix 1. Taxa sampled for the phylogenetic analyses with voucher
information and GenBank accession numbers. Accessions are grouped by
family, with Kewaceae first. Information is listed as follows: species name
and author(s), country and number (if there is more than one accession of
the species from that country), collector and number (with herbarium
acronym in parentheses), GenBank numbers for trnK-matK,rbcL, and ITS,
when available. Sequences generated for this study are marked with an
asterisk. A dash indicates a missing sequence.
Kewaceae: Kewa acida (Hook.f.) Christenh., St. Helena 1 (Lotʼs Wife),
Lambdon s. n. (UPS, photo), MH019260*, —, MH018120*; St. Helena 2
(Horseʼs Head), Lambdon s. n. (UPS, photo), MH019262*, —, MH018122*.
Kewa angrae-pequenae (Friedrich) Christenh., Namibia 1, Thulin & Larsson
11967 (UPS), MH019258*, —, MH018117*; Namibia 2, Thulin & Larsson
11968 (UPS), MH019259*, —, MH018118*. Kewa arenicola (Sond.)
Christenh., South Africa, Helme 6500 (NBG), —,—, MH018127*. Kewa
bowkeriana (Sond.) Christenh., Namibia 1, Giess 171 (NY), FN825761,
FN824476, —; Namibia 2, Thulin & Larsson 11945 (UPS), MH019263*, —,
MH018123*; South Africa, KwaZulu-Natal, Thulin et al. 11943 (UPS),
MH019261*, —, MH018121*; Madagascar, Thulin & Razafindraibe 11819
(UPS), —,—, MH018126*. Kewa caespitosa (Friedrich) Christenh.,
Namibia 1, Thulin et al. 11948 (UPS), MH019264*, —, MH018124*; Namibia
2, Thulin et al. 11949 (UPS), MH019265*, —, MH018125*. Kewa salsoloides
(Burch.) Christenh., South Africa, Ogburn 143 (BRU), FN825762.1,
FN824478.1, —; Namibia 1, Thulin et al. 11956 (UPS), MH019266*, —,
MH018128*; Namibia 2, Thulin & Larsson 11963 (UPS), MH019257*, —,
MH018116*. Aizoaceae: Conicosia pugioniformis (L.) N.E.Br., South
Africa, Klak 1570 (BOL-matK only), KF132628.1, JQ412345, —.Galenia
africana L., JQ024963.1, JQ025048, —.Gibbaeum heathii (N.E.Br.) L.Bolus,
South Africa, Klak 1125 (BOL), KF132691.1, —,—.Mesembryanthemum
crystallinum L., HM850877.1, HM850175, —.Sesuvium portulacastrum
(L.) L., KC185420.1, FN868308, —.Tetragonia tetragonoides (Pall.) Kuntze,
HM850882.1, HM850395, —.Amaranthaceae: Spinacia turkestanica Iljin,
Fuentes 181 (B), HE855620.1, —,—.Anacampserotaceae: Anacampseros
kurtzii Bacigalupo, Leuenberger & Eggli 4217 (ZSS-matK only), DQ855853.1,
—,—.Barbeuiaceae: Barbeuia madagascariensis Steud., AY042552.1,
GQ497673, —.Basellaceae: Basella alba L., JQ844148.1, M62564, —.
Cactaceae: Opuntia phaeacantha Engelm., FN997327.1, —,—.Pereskia
aculeata Mill., HM041757.1, AY875229, —.Caryophyllacae: Dianthus
laingsburgensis S.S.Hooper, GU441169.1, —,—.Corbichoniaceae: Cor-
bichonia decumbens (Forssk.) Exell, Botswana, Aye 1074 (NY), FN825760,
FN824475, —; South Africa, KwaZulu-Natal, Thulin et al. 11942 (UPS),
KT950946, —, MH018119*. Didiereaceae: Alluaudia dumosa (Drake)
Drake, Madagascar, Stone s. n., HQ620839.1, —,—.Gisekiaceae: Gisekia
africana (Lour.) Kuntze, Namibia, Thulin et al. 11955 (UPS), KT950945, —,
—.Halophytaceae: Halophytum ameghinoi Speg., Chase 1753 (K-rbcL
only), AY514852.1, AJ403024, —.Limeaceae: Limeum aethiopicum Burm.f.,
THULIN ET AL.: PHYLOGENY AND SYSTEMATICS OF KEWA 6992018]
Namibia, Thulin & Larsson 11957 (UPS), KT950934, —,—.Limeum dinteri
G.Schellenb., Namibia, Thulin & Larsson 11959 (UPS), KT950935, —,—.
Lophiocarpaceae: Lophiocarpus polystachyus Turcz., Namibia 1, De
Winter 3156 (K), AY042611, —,—; Namibia 2, Karas Region, Thulin &
Larsson 11958 (UPS), KT950947, —, MH018129*. Macarthuriaceae: Mac-
arthuria australis H¨ugel ex Endl., Australia, Lepschi & Brims 1943 (G),
FN825765.1, FN824479.1, —.Molluginaceae: Adenogramma glomerata (L.f.)
Druce, South Africa 2, Fries 25-9-20 (NY), FN825687.1, FN824406, —.Ade-
nogramma mollugo Rchb., South Africa, Pillans 10526 (NY), FN825690,
FN824409, —.Coelanthum semiquinquefidum (Hook.) Druce, South Africa,
Wright 1853 (NY), FN825759, FN824411, —.Glinus lotoides L., USA, Errter
8854 (NY), FN825692, —,—.Glinus oppositifolius (L.) Aug.DC., Taiwan,
Huang & Huang 14175 (NY), FN825695, FN824415, —.Glinus setiflorus
Forssk., Kenya, Burney & al. T46 (NY), FN825698, FN824418, —.Hypertelis
cerviana (L.) Thulin, Namibia, Thulin et al. 11954 (UPS), KT950944, —,—.
Hypertelis fragilis (Wawra) Thulin, Angola, Ward & Ward 79 (K), FN825724,
FN824442, —.Hypertelis spergulacea E.Mey. ex Fenzl, Namibia 1, Thulin &
Larsson 11960 (UPS), KT950931, —,—; Namibia 2, Thulin & Larsson 11962
(UPS),KT950932, —,—; Namibia 3, Giess etal. 5366 (K), F N825700, FN824420 ,
—; South Africa, Acocks 19256 (K), FN825701, FN824421, —.Hypertelis
umbellata (Forssk.) Thulin, Ethiopia, Thulin et al. 11211 (UPS), FN825713,
FN824433, —.Mollugo brasiliensis Thulin & Harley, Brazil, Guedes et al.
PCD5162 (K), KT950938, —,—.Mollugo disticha (L.) Ser., Sri Lanka,
Lundqvist 11379 (UPS), KT950942, —,—.Mollugo ulei (Pilger) Thulin, Brazil,
Harvey 19007 (SPF), FN825699, F N824419, —.Mollugo verticillata L., USA,
Sage & Sage8-2007 (TRT),FN825740, FN824459, —.Paramollugo angustifolia
(M.G.Gilbert & Thulin) Thulin, Somalia, Thulin et al. 7606 (UPS), FN825702,
—,—.Paramollugo decandra (Scott Elliot) Thulin, Madagascar, Croat 30852
(K), FN825718, FN824437, —.Paramollugo nudicaulis (Lam.) Thulin,
Somalia, Thulin & Bashir Mohamed 6759 (UPS), FN825730, F N824448, —.
Pharnaceum elongatum (DC.) Adamson, South Africa, Ogburn 153 (BRU),
FN825746, FN824464, —.Pharnaceum lanuginosum J.C.Manning & Gold-
blatt, South Africa, Ogburn 161 (BRU), FN825752, FN824469, —.Pharnaceum
lineare L.f., South Africa, Helme 5887 (NBG), KT950943, —,—.Pharnaceum
reflexum Eckl. & Zeyh., South Africa, Taylor 1162 (NY), FN825751, —,—.
Polpoda capensis C.Presl, South Africa, Acocks 17405 (CANB), FN825753,
FN824470, —.Psammotropha obovata Adamson, South Africa, Hilliard &
Burtt 7045 (K), FN825754, FN824471, —.Psammotropha quadrangularis
Fenzl, South Africa, Ogburn 160 (BRU), FN825755, FN824472, —.Suessen-
guthiella scleranthoides (Sond.) Friedrich, Namibia, Thulin & Larsson 11964
(UPS), KT950936, —,—.Trigastrotheca molluginea F.Muell., Australia,
Telford 11746 (CANB), FN825725, FN824443, —.Trigastrotheca stricta (L.)
Thulin, Australia, Lazarides & Adams 326 (CANB), FN825736, FN824454, —.
Montiaceae: Lewisia longipetala (Piper) S.Clay, Edwards 141 (BRU-matK
only), HQ620876.1, —,—.Nyctaginaceae: Bougainvillea glabra Choisy,
JQ844141.1, M88340, —.Guapira discolor (Spreng.) Little, KJ522684.1,
KJ522686, —.Mirabilis jalapa L., FN868307.1, HM850179, —.Petiveriaceae:
Petiveria alliacea L., GQ429080.1, AJ402987, —.Rivina humilis L.,
AY514850.1, M62569, —.Phytolaccaceae: Phytolacca americana L., Qiu
94109 (IND-matK only), DQ401362.1, HM850257, —.Portulacaceae: Portu-
laca amilis Speg., Ogburn 11 (BRU-matK only), HQ620886.1, —,—.Sarco-
bataceae: Sarcobatus vermiculatus (Hook.) Torr., AY042652.1, AF132088, —.
Simmondsiaceae: Simmondsia chinensis (Link) C.K.Schneid., AF204863.1,
AF093732, —.Stegnospermataceae: Stegnosperma halimifolium Benth.,
HQ878442.1, M62571, —.Talinaceae: Talinum fruticosum (L.) Juss., Ferguson
848 (ZSS-matK only), DQ855844.1, KJ380905, —.
SYSTEMATIC BOTANY [Volume 43700
