Artabotrys angustipetalus (Annonaceae), a new species from Thailand, including a plastid phylogeny and character evolutionary analyses of thorn occurrence in Artabotrys

Abstract

Artabotrys R. Br. is one of the larger genera of Annonaceae with over 100 species distributed throughout the palaeotropics plus northern Australia. Although the genus is morphologically very well circumscribed, species delimitation is quite problematic owing to overlapping morphological characteristics. In Thailand, 20 species of
Artabotrys have been reported, including A. multiflorus C. E. C. Fisch. Detailed comparisons with the type specimen from Myanmar revealed that A. multiflorus occurring in Kanchanaburi Province of Thailand represents a new species herein described as A. angustipetalus Photikwan & Chaowasku. The new species differs from A. multiflorus by having fewer flowers per hook, linear (vs oblong to oblong-lanceolate) petals, acute (vs obtuse) petal apex, longer and narrower petals and fewer carpels per flower. A multi-locus plastid phylogeny including an accession of A. angustipetalus and 30 accessions of other species of Artabotrys has been reconstructed. The results uncover a well-supported clade consisting of thorn-bearing species of Artabotrys, with A. angustipetalus recovered outside this clade. To understand the evolution of thorns in Artabotrys, ancestral character-state reconstructions were carried out; this trait
is inferred to have evolved only once in Artabotrys. The benefits of thorns in Artabotrys species are discussed and
hypothesized.

Full text

Artabotrys angustipetalus (Annonaceae), a new species
from Thailand, including a plastid phylogeny and
character evolutionary analyses of thorn occurrence in
Artabotrys
Authors: Photikwan, Ekkaphon, Damthongdee, Anissara, Jongsook,
Hathaichanok, and Chaowasku, Tanawat
Source: Willdenowia, 51(1) : 69-82
Published By: Botanic Garden and Botanical Museum Berlin (BGBM)
URL: https://doi.org/10.3372/wi.51.51106
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Willdenowia
Annals of the Botanic Garden and Botanical Museum Berlin
EKKAPHON PHOTIKWAN1,2, ANISSARA DAMTHONGDEE1, HATHAICHANOK JONGSOOK1,3 & TANAWAT
CHAOWASKU1,4*
Artabotrys angustipetalus (Annonaceae), a new species from Thailand, including a plas-
tid phylogeny and character evolutionary analyses of thorn occurrence in Artabotrys
Version of record first published online on 23 March 2021 ahead of inclusion in April 2021 issue.
Abstract: Artabotrys R. Br. is one of the larger genera of Annonaceae with over 100 species distributed throughout
the palaeotropics plus northern Australia. Although the genus is morphologically very well circumscribed, species
delimitation is quite problematic owing to overlapping morphological characteristics. In Thailand, 20 species of
Arta botrys have been reported, including A. multiflorus C. E. C. Fisch. Detailed comparisons with the type specimen
from Myanmar revealed that A. multiflorus occurring in Kanchanaburi Province of Thailand represents a new species
herein described as A. angustipetalus Photikwan & Chaowasku. The new species diers from A. multiflorus by hav-
ing fewer flowers per hook, linear (vs oblong to oblong-lanceolate) petals, acute (vs obtuse) petal apex, longer and
narrower petals and fewer carpels per flower. A multi-locus plastid phylogeny including an accession of A. angusti-
petalus and 30 accessions of other species of Artabotrys has been reconstructed. The results uncover a well-supported
clade consisting of thorn-bearing species of Artabotrys, with A. angustipetalus recovered outside this clade. To
understand the evolution of thorns in Artabotrys, ancestral character-state reconstructions were carried out; this trait
is inferred to have evolved only once in Artabotrys. The benefits of thorns in Artabotrys species are discussed and
hypothesized.
Key words: Annonaceae, Artabotrys, evolution, new species, systematics, taxonomy, Thailand, thorns, Xylopieae
Article history: Received 18 May 2020; peer-review completed 20 August 2020; received in revised form 21 Sep-
tember 2020; accepted for publication 12 October 2020.
Citation: Photikwan E., Damthongdee A., Jongsook H. & Chaowasku T. 2021: Artabotrys angustipetalus (Annona-
ceae), a new species from Thailand, including a plastid phylogeny and character evolutionary analyses of thorn
occurrence in Artabotrys. – Willdenowia 51: 69 – 82. doi: https://doi.org/10.3372/wi.51.51106
Introduction
Artabotrys is one of the larger genera of Annonaceae,
a pantropical family of flowering plants consisting of
c. 2430 species (Couvreur & al. 2019) in 108 genera
(Guo & al. 2017; Chaowasku & al. 2018a, 2018b; Xue
& al. 2018; note that Friesodielsia Steenis and Scheero-
mitra Diels are synonymous, see Saunders & al. 2020;
and Melodorum Lour. has been synonymized with Uva-
ria L., see Turner 2018). Artabotrys, with over 100 spe-
cies distributed in tropical forests of Africa-Madagascar,
Asia, New Guinea and Australia, has been classified in
the tribe Xylopieae of the subfamily Annonoideae (Cha-
trou & al. 2012). Artabotrys is mainly characterized by
(1) hooked peduncles and inflorescence axes, (2) inner
petals that are generally constricted over the reproductive
1 Herbarium, Division of Plant Science and Technology, Department of Biology, Faculty of Science, Chiang Mai University, 239
Huay Kaew Rd., Chiang Mai 50200, Thailand.
2 M.Sc. Program in Teaching Biology, Graduate School and Faculty of Science, Chiang Mai University, 239 Huay Kaew Rd.,
Chiang Mai 50200, Thailand.
3 Current address: Rubber Standard Development Group, Rubber Division, Department of Agriculture, 50 Phahonyothin Rd.,
Bangkok 10900, Thailand.
4 Research Center in Bioresources for Agriculture, Industry, and Medicine, Chiang Mai University, 239 Huay Kaew Rd., Chiang
Mai 50200, Thailand; *e-mail: tanawat.chaowasku@cmu.ac.th (author for correspondence).
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70 Photikwan & al.: Artabotrys angustipetalus from Thailand, thorn occurrence in Artabotrys
organs, (3) biovulate carpels, with basal placentation and
(4) sessile to shortly stipitate monocarps (Keßler 1993;
Chen & al. 2018; Chen & Eiadthong 2020). Species of
Artabotrys develop a climbing habit with the help of
hooked peduncles and inflorescence axes, but sometimes
appear as straggling shrubs (e.g. in A. spinosus Craib;
Chalermglin 2001; personal observations). Moreover,
some species even possess thorns, a rare character in An-
nonaceae; these thorns are generally observable on the
lower part of plants (Posluszny & Fisher 2000; Chalerm-
glin 2001; Fisher & al. 2002; personal observations).
The genus has been inferred to have originated in Africa
and subsequently dispersed to Madagascar and to Asia-
Australasia (Chen & al. 2019). The latter dispersal event
has been inferred to have occurred during the Middle Mi-
ocene via overland migration across Arabia. The major-
ity of species diversity is in Asia-Australasia instead of
Africa-Madagascar, with c. 75 species vs c. 30 species,
respectively (Chen & al. 2018).
Although, as a genus, Artabotrys is easily recogniz-
able, species delimitation and identification are somewhat
problematic (e.g. Turner 2009; Turner & Utteridge 2015;
Chen & al. 2018). In Thailand, there are 20 species of
Artabotrys reported, two of which have recently been
described (Chen & Eiadthong 2020). However, based on
personal observations, identification of some specimens is
still unsatisfactory due to the morphological heterogene-
ity of certain species, e.g. A. harmandii Finet & Gagnep.,
A. siamensis Miq. and A. spinosus. In the course of iden-
tifying specimens for the inclusion in a molecular phy-
logeny in order to solve some species complexes in Thai
Artabotrys as part of the first author’s M.Sc. study, we
came across specimens from southwestern Thailand iden-
tified as A. multiflorus C. E. C. Fisch. These collections do
not match the type specimen of A. multiflorus well. There-
fore, in this study, we re-assess the taxonomic status of
such specimens by detailed morphological comparisons.
A multi-locus plastid phylogeny is also reconstructed,
incorporating, among others, an accession of A. cf. mul-
tiflorus and multiple accessions of the above-mentioned
three species. In addition, as mentioned earlier, certain
species of Arta botrys exhibit thorns, a feature that is ex-
ceptional in the family. Several questions regarding this
remarkable trait arise, e.g. did it evolve only once? Con-
sequently, character evolutionary analyses are performed
to shed light on the evolution of thorns in Artabotrys, with
discussion on their putative advantages.
Material and methods
Phylogenetic reconstructions
The ingroup consisted of Xylopieae: 31 accessions of
Artabotrys and two species of Xylopia L. On the basis
of plastid DNA data, both genera have been consistently
retrieved as sister genera with strong support (e.g. Cha-
trou & al. 2012; Guo & al. 2017), although this relation-
ship was not supported based on some nuclear DNA data
(Couvreur & al. 2019). Outgroups were members of Du-
guetieae (a species of Letestudoxa Pellegr. plus a species
of Pseudartabotrys Pellegr.). Six plastid DNA regions
(matK, ndhF and rbcL exons; trnL intron; psbA-trnH and
trnL-trnF intergenic spacers) were included. Sequences
of 18 accessions were newly generated in the present
study. Appendix 1 shows voucher information and Gen-
Bank accession numbers.
DNA extraction, amplification and sequencing, in-
cluding primer sequences, used in the present study fol-
lowed Chaowasku & al. (2018a, 2018b, 2020). Sequences
obtained were edited using the Staden package (Staden &
al. 2000) and then aligned using the Multiple Sequence
Comparison by Log-Expectation (MUSCLE; Edgar
2004) implemented in MEGA7 (Kumar & al. 2016). The
alignments were subsequently checked manually and ad-
justed where necessary based on the similarity criterion
(Simmons 2004). In some accessions there was an inver-
sion of 15-stretch nucleotides in the psbA-trnH intergen-
ic spacer and this was complementarily reversed to be
alignable to the remaining sequences, following Pirie &
al. (2006). In total, 5484 nucleotide characters were in-
cluded. Indel characters were not included because only
a few non-autapomorphic indel structures were present.
Alignments are available in the Supplemental content on-
line (https://doi.org/10.3372/wi.51.51106).
Parsimony analysis was performed in TNT version
1.5 (Golobo & Catalano 2016). All characters were
equally weighted and unordered. Incongruence among
regions was assessed by analysing each region indi-
vidually to see if there was any significant topological
conflict (e.g. Wiens 1998). Multiple most parsimonious
trees were generated by a heuristic search of the com-
bined data, with 9000 replicates of random sequence ad-
dition, saving 10 trees per replicate, and using the tree
bisection and reconnection (TBR) branch-swapping al-
gorithm. Clade support was assessed by symmetric re-
sampling (SR; Golobo & al. 2003). A default change
probability was used. Two hundred thousand replicates
were run, each with four replicates of random sequence
addition, saving four trees per replicate. A clade with SR
≥ 85 %, 70 – 84 %, or 50 – 69 % was considered strongly,
moderately, or weakly supported, respectively. Maxi-
mum likelihood analysis was carried out in IQ-TREE
version 1.6.10 (Nguyen & al. 2015) under partition mod-
els (Chernomor & al. 2016) implemented with the “-spp”
command, whereas Bayesian Markov chain Monte Carlo
(MCMC; Yang & Rannala 1997) phylogenetic analysis
was accomplished in MrBayes version 3.2.6 (Ronquist
& al. 2012). Both analyses were run via the CIPRES
Science Gateway version 3.3 (Miller & al. 2010). The
data matrix was divided into five partitions based on the
identity of DNA regions (the trnL intron and the adjacent
trnL-trnF intergenic spacer were combined as a single
partition). The most appropriate model of sequence evo-
lution for each DNA partition was chosen by the Akaike
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71Willdenowia 51 – 2021
Information Criterion (AIC; Akaike 1974) scores, using
FindModel (http://www.hiv.lanl.gov/content/sequence
/findmodel/findmodel.html; Posada & Crandall 1998).
The General Time Reversible (GTR; Tavaré 1986) nu-
cleotide substitution model was selected for one parti-
tion (matK), whereas GTR with a gamma distribution
for among-site rate variation (G) was selected for two
partitions (ndhF and psbA-trnH). The Hasegawa-Kishi-
no-Yano (HKY; Hasegawa & al. 1985) substitution mod-
el was selected for one partition (trnLF [= trnL intron +
trnL-trnF intergenic spacer]), while HKY with G was
selected for the remaining partition (rbcL). Clade sup-
port in the maximum likelihood analysis was measured
by a non-parametric bootstrap resampling (BS; Felsen-
stein 1985) with 2000 replicates. Similar to the dier-
entiation of the SR values in the parsimony analysis, a
clade with BS ≥ 85 %, 70 – 84 %, or 50 – 69 % was con-
sidered strongly, moderately, or weakly supported, re-
spectively. In the Bayesian analysis, four independent
analyses, each using four MCMC chains, were simul-
taneously run; each run was set for 10 million genera-
tions. The default prior settings were used except for the
prior parameter of rate multiplier (“ratepr” [=variable]).
The temperature parameter was set to 0.08. Trees and
all parameter values were sampled every 1000th genera-
tion. Convergence was assessed by checking the stand-
ard deviation of split frequencies of the runs with values
<0.01 interpreted as indicative of a good convergence
and by checking for adequate eective sample sizes
(ESS > 200) using Tracer version 1.6 (Rambaut & al.
2013). The first 25 % of all trees sampled were discarded
as burn-in and the 50 % majority-rule consensus tree was
created from the remaining trees. A clade with poste-
rior probabilities (PP) ≥ 0.95, 0.9 – 0.94, or 0.5 – 0.89 was
considered strongly supported, weakly supported, or un-
supported, respectively.
Ancestral character-state reconstructions of thorn oc-
currence in Artabotrys
The presence/absence of thorns in all accessions includ-
ed was surveyed from literature (Blume 1830; Bentham
1861; Oliver 1868; Hooker & Thomson 1872; King
1892; Diels 1915, 1931; Pellegrin 1920; Craib 1925;
Le Thomas 1969; Posluszny & Fisher 2000; Chalerm-
glin 2001; Nurainas 2004; Jessup 2007; Li & al. 2011;
Chen & Eiadthong 2020), from specimen labels and/or
from personal observations in the field. Ten thousand
post burn-in trees (2500 from each run) from the Baye-
sian analysis were used as input trees for parsimony
and maximum likelihood ancestral character-state re-
constructions in Mesquite version 3.6 (Maddison &
Maddison 2018). Character state changes were treated
as unordered. The “Mk1” model was adopted for the
maximum likelihood ancestral character-state recon-
structions, with default model settings. The “trace over
trees” option was chosen and reconstructions across
the input trees were summarized at each node of the
Bayesian 50 % majority-rule consensus tree using the
“uniquely best state” option.
Morphology
The morphological data of Artabotrys multiflorus for
comparison were derived from Fischer (1937) and study
of the type specimen. Two gatherings of A. cf. multiflorus
from southwestern Thailand (Keßler PK 3227 [B, BKF,
CMUB, L] and Aongyong 16 [CMUB]) were studied
morphologically (herbarium codes according to Index
herbariorum; http://sweetgum.nybg.org/science/ih/).
Aongyong 16 is a voucher for molecular phylogenetic
analyses and, although sterile, can be identified as the
same taxon as Keßler PK 3227 because both gatherings
have coriaceous leaves and both were collected ± 3 km
apart at the same elevation. The indumentum terminol-
ogy used followed Hewson (1988). The abbreviation “c.”
(circa) was added when there was a single observation/
measurement. The term “almost glabrous” means “with
fewer than ten hairs”.
Results
The parsimony analysis resulted in 21 most parsimo-
nious trees with 759 steps. The consistency and reten-
tion indices (CI and RI) were both 0.89. There was no
strong topological conflict (SR ≥ 85 %) in the analyses
of each plastid region. The ingroup monophyly was
maximally supported as shown in Fig. 1. Artabotrys and
Xylopia were each recovered as a maximally supported
sister clades. In the former genus, a maximally sup-
ported clade composed of two accessions of A. thom-
sonii Oliv., both from Africa, was retrieved as the sister
group of a large maximally supported clade consisting
of the remaining accessions of Artabotrys. In this large
clade, there were two strongly supported sister clades:
a clade of A. pierreanus Engl. & Diels and A. stolzii
Diels (PP 1, BS 87 %, SR 91 %), both from Africa, and
a clade containing the rest of the genus from Asia-Aus-
tralasia (PP 1, BS 99 %, SR 99 %). The relationships in
this Asian-Australasian clade were largely unresolved.
There was a moderately to strongly supported clade
(PP 1, BS 80 %, SR 81 %) comprising thorn-bearing
species: A. carnosipetalus Jessup, A. harmandii (four
accessions), A. hexapetalus (L. f.) Bhandari (two acces-
sions), A. oblanceolatus Craib, A. siamensis (two ac-
cessions) and A. spinosus (four accessions). There were
two strongly supported clades of A. harmandii (A. har-
mandii-1 + A. harmandii-2 [PP 1, BS 98 %, SR 98 %]
and A. harmandii-3 + A. harmandii-4 [PP 1, BS 94 %,
SR 96 %]) and of A. spinosus (A. spinosus-1 from Mun
River + A. spinosus-2 from Chi River [PP 1, BS 99 %,
SR 99 %] and A. spinosus-3 + A. spinosus-4 [PP 1, BS
100 %, SR 99 %], both from the Mekong River). The two
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72 Photikwan & al.: Artabotrys angustipetalus from Thailand, thorn occurrence in Artabotrys
clades of A. harmandii did not show sister relationships,
nor did the two clades of A. spinosus. Two accessions
of A. siamensis also did not form a clade. Outside the
thorn-bearing clade, A. cf. multiflorus was retrieved as
the sister group of a strongly supported clade (PP 1, BS
100 %, SR 99 %) composed of A. uniflorus (Gri.) Craib
and Artabotrys sp. 1 THA with weak to strong support
(PP 1, BS 60 %, SR 59 %).
In Artabotrys, the occurrence of thorns was inferred
to have evolved once in the thorn-bearing clade (Fig. 2).
The character state “thorns present” was reconstructed at
the crown node of the thorn-bearing clade in all 10 000
Fig. 1. Phylogram from Bayesian inference, showing relationships within Artabotrys. Bayesian posterior probabilities (PP), maxi-
mum likelihood bootstrap values (BS) and parsimony symmetric resampling values (SR) are indicated: PP/BS/SR. ** = BS and/or
SR < 50 %. Scale bar unit = substitutions per site. AUST. = Australasia.
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73Willdenowia 51 – 2021
Letestudoxa bella
Pseudartabotrys letestui
Artabotrys harmandii-3
Artabotrys harmandii-4
Artabotrys siamensis-1
Artabotrys harmandii-1
Artabotrys harmandii-2
Artabotrys siamensis-2
Artabotrys carnosipetalus
Artabotrys hexapetalus-1
Artabotrys hexapetalus-2
Artabotrys spinosus-1
Artabotrys spinosus-2
Artabotrys spinosus-3
Artabotrys spinosus-4
Arabotrys oblanceolatus
Artabotrys longipetalus-1
Artabotrys longipetalus-2
Artabotrys cf. multiflorus = Artabotrys angustipetalus sp. nov.
Artabotrys sp. 1 THA
Artabotrys uniflorus
Artabotrys punctulatus
Artabotrys blumei
Artabotrys suaveolens
Artabotrys gracilis
Artabotrys sp. 2 SUM
Artabotrys crassifolius
Artabotrys longistigmatus
Artabotrys sp. 3 PNG
Artabotrys pierreanus
Artabotrys stolzii
Artabotrys thomsonii-1
Artabotrys thomsonii-2
Xylopia maccreae
Xylopia vielana
Thorns Absent
Thorns Present
Node Absent
Equivocal
Parsimony: Thorns Present = 10000 Trees
Maximum Likelihood: Thorns Present = 9833 Trees; Equivocal = 167 Trees
THORN-BEARING
AT CROWN NODE OF THORN-BEARING CLADE:
Fig. 2. Maximum likelihood and parsimony ancestral character-state reconstructions of thorn occurrence in Artabotrys across
10 000 post burn-in trees from Bayesian phylogenetic inference shown on Bayesian 50 % majority-rule consensus tree.
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74 Photikwan & al.: Artabotrys angustipetalus from Thailand, thorn occurrence in Artabotrys
input trees under the parsimony criterion. Under the max-
imum likelihood approach it was reconstructed in 9833
trees, while the remaining 167 trees were equivocally re-
constructed.
Discussion
A new species of Artabotrys from Thailand
Artabotrys cf. multiflorus is somewhat poorly supported
as the sister species of a strongly supported clade com-
posed of A. uniflorus and Artabotrys sp. 1 THA (Fig. 1).
However, A. uniflorus and Artabotrys sp. 1 THA possess
only one flower per hook with rather thick and fleshy pet-
als (personal observations), whereas each hook of A. cf.
multiflorus bears more or less five flowers exhibiting thin
and rather chartaceous petals (Fig. 3). Upon a closer com-
parison with the type specimen (Fig. 4) and protologue
(Fischer 1937) of A. multiflorus, A. cf. multiflorus diers
in several respects (Table 1), i.e. number of flowers per
hook (Fig. 3, 4), petal shape, length, width and apex (Fig.
4, 5A, 5B) and number of carpels per flower. In addition,
the elevation where A. cf. multiflorus (c.510 m) and A.
multiflorus (c. 914 m) occur is also considerably dier-
ent. The exact locality of A. multiflorus cannot be traced,
but it is expected to be somewhere in the Burmese Dawna
range (Fischer 1937 [as “Dawnas”]), northwest of the lo-
cality of A. cf. multiflorus (Kanchanaburi Province, Thai-
land). On the basis of these dierences, A. cf. multiflorus
is described here as new to science. As a consequence,
A. multiflorus is most likely to be absent from the flora
of Thailand.
Artabotrys angustipetalus Photikwan & Chaowasku, sp.
nov. – Fig. 3, 5.
Holotype: Thailand, Kanchanaburi Province, Thung Yai
Naresuan Wildlife Sanctuary, 17 Feb 2002 [in flower],
Keßler PK 3227 (BKF! [SN144809]; isotypes: B!, BKF!,
CMUB!, L! [L.1749583, L.1749584]).
Diagnosis — Artabotrys angustipetalus is morphologi-
cally close to A. multiflorus C. E. C. Fisch. The former
diers primarily from the latter by having more or less
five flowers (vs > 12) per hook, linear (vs oblong to
oblong-lanceolate) petals, acute (vs obtuse) petal apex,
longer and narrower petals and fewer carpels per flower.
Description — Woody climbers to 30 m long,
c.10cm in diam.; young twigs almost glabrous;
petiole 4 – 7mm long, grooved on upper surface,
almost glabrous on both surfaces; leaf blade
coriaceous, 10.7 – 14.2 × 4.8 – 7.7 cm, elliptic,
sometimes ± obovate, glabrous on both surfaces
including secondary veins, apex cuspidate-
acute, base cuneate; midrib slightly raised and
glabrous on upper surface, raised and glabrous
on lower surface; secondary veins 10 – 12 per
side, angle with midrib 65° – 80° (at middle part of leaf
blade). Inflorescences terminal developing to ± leaf-
opposed; flowering peduncle and inflorescence axis
hook-shaped, first curve 17 – 27mm long, 3 – 4mm wide
(at midpoint of curve), second curve 7 – 10 mm long,
2 – 2.3mm wide (at midpoint of curve), both curves pu-
berulous with appressed hairs, bearing ± 5 flowers per
hook, divided into 1 or 2 fascicles, with several bracts
at base of each fascicle, ± ovate; flowering pedicel
12 – 18mm long, puberulous with appressed hairs. Se-
pals free, 2 – 2.5 × 2 – 2.5mm, broadly ovate, apex acute-
acuminate, sometimes slightly obtuse, outside and mar-
gin puberulous with appressed hairs, inside glabrous.
Outer petals 29 – 30 × c.3mm, linear, apex acute, divid-
ed into a blade and a claw, claw c.3.8mm long, upper
rim of claw slightly raised and curved, outside of outer
petals puberulous with appressed hairs on blade, more
densely so on claw, margin puberulous with appressed
to erect hairs, inside puberulous with appressed hairs
on blade, claw glabrous, but upper rim of claw tomen-
tose with erect hairs; inner petals 30 – 31 × 2 – 2.5 mm,
linear, apex acute, divided into a blade and a claw, claw
c.3.5mm long, upper rim of claw distinctly raised and
curved, covering stamens and carpels, outside of inner
petals puberulous with appressed hairs on blade, but to-
mentose with erect hairs on claw (c. ⅔ of claw length
from upper rim), remaining area of claw puberulous
with appressed hairs, margin puberulous with appressed
to erect hairs, inside puberulous with appressed hairs on
blade, claw glabrous, but upper rim of claw tomentose
with erect hairs. Torus c. 1 × 2 mm, slightly elevated,
apex flat-topped, tomentose-villous with erect hairs
on areas unoccupied by stamens and carpels. Stamens
25 – 32 per flower, 1.1 – 1.2 mm long, connective apex
± truncate, covering thecae. Carpels 7 or 8 per flower,
1.1 – 1.4 mm long; stigmas terete and curved; ovaries
glabrous; ovules 2 per ovary, basal. Fruit unknown.
Phenology — Flowering material collected in February.
Distribution and ecology — Kanchanaburi Province, SW
Thailand; occurring in primary evergreen forests at an el-
evation of c.510m.
Field notes — Bark blackish; flowers with very sweet
fruity smell, petals greenish yellow.
Table 1. Main morphological dierences between Artabotrys angusti-
petalus and A. multiflorus.
Feature A. angustipetalus A. multiflorus
Number of flowers per hook ± 5 > 12
Petal shape linear oblong to oblong-
lanceolate
Petal apex acute obtuse
Petal length (mm) 29 – 31 18 – 25
Petal width (mm) 2 – 3 6 – 9
Number of carpels per flower 7 or 8 12 – 21
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75Willdenowia 51 – 2021
Fig. 3. Holotype of Artabotrys angustipetalus Photikwan & Chaowasku – Keßler PK 3227 (BKF [SN144809]).
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76 Photikwan & al.: Artabotrys angustipetalus from Thailand, thorn occurrence in Artabotrys
Fig. 4. Isotype of Artabotrys multiflorus C. E. C. Fisch. – Parkinson 5220 (E [E00393106]).
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77Willdenowia 51 – 2021
Conservation status — DD (Data Deficient) according
to IUCN (2012) because this species is known from only
two collections. Further explorations are required before
an assessment can be made.
Additional specimen examined (paratype) — T:
Kanchanaburi Province, Thongphaphum District, Phuye,
without date [sterile], Aongyong 16 (CMUB).
Evolution of thorns in Artabotrys
The occurrence of thorns in Annonaceae is exceptional.
Besides certain species of Artabotrys, thorns are also
present in a few species of Anno-
na L. (H. Rainer, personal com-
munication; e.g. A. spinescens
Mart., personal observations on
a specimen at P [P01984538]),
which belongs to the tribe An-
noneae of the subfamily Anno-
noideae (Chatrou & al. 2012).
Based on the ancestral character-
state reconstructions of thorn
occurrence in Artabotrys, this
trait is inferred to have evolved
only once as a synapomorphy of
the thorn-bearing clade (Fig. 2),
which is equivalent to clade D2
in Chen & al. (2019). Three spe-
cies of Artabotrys that are absent
in our analyses, A. brevipes Craib,
A. manoranjanii M. V. Ramana &
al. and A. pleurocarpus Maingay
ex Hook. f. & Thomson, also pos-
sess thorns according to Insura
(2009), Ramana & al. (2016) and
personal observations. Accord-
ing to Insura (2009), at least one
additional species, A. vanprukii
Craib, endemic to Thailand, also
exhibits thorns. The synapomor-
phic thorn occurrence is system-
atically powerful in elucidating
coarse phylogenetic placements
of Asian-Australasian species
of Artabotrys, i.e. species with
thorns are (or will be) members of
the thorn-bearing clade, whereas
those without thorns are (or will
be) recovered outside the thorn-
bearing clade. This is clearly ex-
emplified in the new species A.
angustipetalus, which does not
possess thorns and has been re-
covered outside the thorn-bearing
clade (Fig. 1, 2). Observations
in living plants reveal that thorns
generally emerge in pairs and are generally found along
the lower part of stems (Fig. 6A). In some species, e.g.
A. spinosus, these thorns can appear on the upper part
of stems as well, even on young orthotropic branches
(personal observations). According to Posluszny & Fish-
er (2000), these thorns represent plagiotropic branches
that do not develop further. We have observed the devel-
opment of thorns in a sapling and noticed that a thorn
emerged rather soon, i.e. as a second plagiotropic branch
at a height of only c. 25 cm (Fig. 6B). One of the pos-
sible functions of thorns is herbivore protection, espe-
cially from larger vertebrate animals (Grubb 1992; Ronel
& Lev-Yadun 2012; Nascimento & al. 2020). Addi-
Fig. 5. Flowering organs of Artabotrys angustipetalus. – A: abaxial side of outer petal
(left), adaxial side of outer petal (right); B: abaxial side of inner petal (left), adaxial side of
inner petal (right); C: adaxial side of outer petal claw; D: adaxial side of inner petal claw;
E: adaxial side of stamen (left), abaxial side of stamen (right); F: view from above showing
sepals; G: carpel.
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78 Photikwan & al.: Artabotrys angustipetalus from Thailand, thorn occurrence in Artabotrys
tionally, as demonstrated by Fisher & al. (2002), light
plays an important role for thorn development in A.
hexapetalus, i.e. the more shaded the areas, the more
thorns are developed. It seems that there is more driv-
ing force for plants in shaded areas to grow orthotropic
branches up above to reach light and find support from
other plants. Therefore, the growth of the less necessary
plagiotropic branches is possibly minimized by develop-
ing more thorns instead. The orthotropic branches of the
thorn-bearing species of Artabotrys can grow very fast
and at some point after they reach other plants, fewer
thorns but more plagiotropic branches with hooks are
developed (personal observations). Regarding thorns in
a few species of Annona, mentioned above, further on-
togenetic study is indispensable to ascertain if they are
homologous with thorns in Artabotrys species because
the branching architecture of Annona is distichous,
without the distinction between orthotropic and plagio-
tropic branches, whereas the branching architecture of
Artabotrys is spiral, with the distinction between ortho-
tropic and plagiotropic branches (Johnson 2003).
Three species in the thorn-bearing clade, Artabotrys
harmandii, A. siamensis and A. spinosus, each appear to
be non-monophyletic (Fig. 1). There are some morpho-
logical dierences (e.g. leaf and/or petal shape) between
two lineages/clades of each species; however, we believe
that more resolved phylogenetic hypotheses incorporat-
ing more DNA sequences, particularly nuclear DNA
markers via baiting (e.g. Couvreur & al. 2019; Brée & al.
2020), are required before any solid taxonomic conclu-
sion on these species can be drawn.
Acknowledgements
We are grateful to the curators of the herbaria B, BKF,
CMUB, E, L and P for the material studied. Kithisak
Aongyong, Vittaya Kaewjaroay, Aimorn Rodphitak and
Saksan Kaitongsuk provided useful material for molecu-
lar phylogenetic analyses. Torsakul Nawanin scanned the
holotype of Artabotrys angustipetalus. The first author is
indebted to the scholarship project for the promotion of
science and mathematics talented teachers (PSMT) for
supporting the M.Sc. study at Chiang Mai University.
The last author thanks the Thailand Science Research and
Innovation (TSRI) for the research grant. Partial financial
support for this study was from Chiang Mai University.
Heimo Rainer is kindly thanked for providing the infor-
mation on Annona species having thorns. Thomas Cou-
vreur and an anonymous reviewer considerably improved
an earlier draft of this article.
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81Willdenowia 51 – 2021
Appendix 1
Specimens for molecular phylogenetic analyses and their GenBank accession numbers. Unavailable sequences are denoted with —, whereas newly generated sequences are denoted with **.
Taxon Accession Country Collector and number
(herbarium)
matK ndhF psbA-trnH rbcL trnLF
Artabotrys angustipetalus
Photikwan & Chaowasku
A. cf. multiflorus = A.
angustipetalus sp. nov.
Thailand Aongyong 16 (CMUB) MW057941** MW057959** MW057977** MW057995** MW058013**
Artabotrys blumei Hook. f.
& Thomson
Hong Kong Thomas 11-544 (HKU) KM924839 KM924869 KM924970 KM924909 KM924937
Artabotrys carnosipetalus
Jessup
Australia Sankowsky 3196 (BRI) KM924835 KM924865 KM924966 KM924905 KM924933
Artabotrys crassifolius
Hook. f. & Thomson
Malaysia Teo 843 (L) KM924836 KM924866 KM924967 KM924906 KM924934
Artabotrys gracilis King Indonesia Puglisi 262 (HKU) KM924837 KM924867 KM924968 KM924907 KM924935
Artabotrys harmandii
Finet & Gagnep.
A. harmandii-1 Thailand Rodphitak 1 (CMUB) MW057953** MW057971** MW057989** MW058007** MW058025**
Artabotrys harmandii A. harmandii-2 Thailand Keßler & al. 3213 (L) KM924838 KM924868 KM924969 KM924908 KM924936
Artabotrys harmandii A. harmandii-3 Thailand Chaowasku 81 (CMUB) MW057938** MW057956** MW057974** MW057992** MW058010**
Artabotrys harmandii A. harmandii-4 Thailand Chaowasku 193 (CMUB) MW057946** MW057964** MW057982** MW058000** MW058018**
Artabotrys hexapetalus
(L. f.) Bhandari
A. hexapetalus-1 Thailand Chaowasku 194 (CMUB) MW057939** MW057957** MW057975** MW057993** MW058011**
Artabotrys hexapetalus A. hexapetalus-2 cultivated Anon. s.n. [Utrecht Botanic
Garden, 94GR01614] (U)
AY238962 — — AY238953 —
Artabotrys hexapetalus A. hexapetalus-2 India Chatrou 470 (U) — EF179284 AY841429 — EF179317
Artabotrys longipetalus
Junhao Chen & Eiadthong
A. longipetalus-1 Thailand Aongyong 17 (CMUB) MW057940** MW057958** MW057976** MW057994** MW058012**
Artabotrys longipetalus A. longipetalus-2 Thailand Aongyong 18 (CMUB) MW057950** MW057968** MW057986** MW058004** MW058022**
Artabotrys longistigmatus
Nurainas
Indonesia Puglisi 194 (HKU) KM924840 KM924870 KM924971 KM924910 KM924938
Artabotrys oblanceolatus
Craib
Thailand Chaowasku 195 (CMUB) MW057943** MW057961** MW057979** MW057997** MW058015**
Artabotrys pierreanus
Engl. & Diels
Gabon Wieringa 6132 (WAG) KM924843 KM924874 KM924975 KM924913 KM924942
Artabotrys punctulatus
C. Y. Wu
Thailand Chaowasku 196 (CMUB) MW057955** MW057973** MW057991** MW058009** MW058027**
Artabotrys siamensis Miq. A. siamensis-1 Thailand Damthongdee AD 3 (BKF) MW057948** MW057966** MW057984** MW058002** MW058020**
Artabotrys siamensis A. siamensis-2 Thailand Kaitongsuk SK 226 (BKF) MW057954** MW057972** MW057990** MW058008** MW058026**
(continued on next page)
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82 Photikwan & al.: Artabotrys angustipetalus from Thailand, thorn occurrence in Artabotrys
Taxon Accession Country Collector and number
(herbarium)
matK ndhF psbA-trnH rbcL trnLF
Artabotrys spinosus Craib A. spinosus-1
MUN RIV.
Thailand Chaowasku 197 (CMUB) MW057947** MW057965** MW057983** MW058001** MW058019**
Artabotrys spinosus A. spinosus-2
CHI RIV.
Thailand Chaowasku 198 (CMUB) MW057945** MW057963** MW057981** MW057999** MW058017**
Artabotrys spinosus A. spinosus-3
MEKONG RIV.
Thailand Chaowasku 199 (CMUB) MW057944** MW057962** MW057980** MW057998** MW058016**
Artabotrys spinosus A. spinosus-4
MEKONG RIV.
Thailand Chaowasku 200 (CMUB) MW057952** MW057970** MW057988** MW058006** MW058024**
Artabotrys stolzii Diels Tanzania Couvreur 72 (WAG) KM924846 KM924877 KM924978 KM924916 KM924945
Artabotrys suaveolens
(Blume) Blume
Thailand Chaowasku 201 (CMUB) MW057942** MW057960** MW057978** MW057996** MW058014**
Artabotrys thomsonii Oliv. A. thomsonii-1 Gabon Wieringa 4018 (WAG) DQ125052 EF179285 DQ125118 AY841599 AY841676
Artabotrys thomsonii A. thomsonii-2 Central
African
Republic
Harris 4533 (E) KM924847 KM924878 KM924979 KM924917 KM924946
Artabotrys uniflorus
(Gri.) Craib
Thailand Kaewjaroay 1 (CMUB) MW057951** MW057969** MW057987** MW058005** MW058023**
Artabotrys sp. 1 A. sp. 1 THA Thailand Damthongdee AD 9 (BKF) MW057949** MW057967** MW057985** MW058003** MW058021**
Artabotrys sp. 2 A. sp. 2 SUM Indonesia Puglisi 164 (HKU) KM924845 KM924876 KM924977 KM924915 KM924944
Artabotrys sp. 3 A. sp. 3 PNG Papua New
Guinea
BRC & Weiblen
WP5B1081 (BRC)
KM924844 KM924875 KM924976 KM924914 KM924943
Letestudoxa bella Pellegr. Gabon Wieringa 2797 (WAG) DQ125059 EF179302 DQ125128 AY841629 AY841707
Pseudartabotrys letestui
Pellegr.
Gabon Wieringa 3273 (WAG) DQ125061 EF179307 DQ125131 AY841650 AY841728
Xylopia maccreae
(F. Muell.) L. S. Sm.
Australia Sankowsky 3148 (BRI) KM924860 KM924900 KM924998 KM924928 KM924961
Xylopia vielana Pierre Thailand Chalermglin 530725 (HKU) KM924863 KM924903 KM925001 KM924931 KM924964
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