A contribution to the systematics of Xylopia (Annonaceae) in Southeast Asia

TL;DR: 23 Xylopia species in the Sundaic region of Southeast Asia are recognised, and evidence that additional collecting and taxonomic analysis in the region is needed is provided.

Abstract: Herbarium and field study of Xylopia L. (Annonaceae) for the Flora of Peninsular Malaysia and the Flora of Thailand projects has clarified regional diversity patterns within this ecologically significant lowland rainforest genus. Two species groups represented within Southeast Asian floras are delineated, one centred on Xylopia ferruginea (Hook.f. & Thomson) Baill. and the other on Xylopia malayana Hook.f. & Thomson. In the Xylopia ferruginea group, a new species, Xylopia erythrodactyla D.M.Johnson & N.A.Murray, is distinguished from X. ferruginea, and a new combination, Xylopia sumatrana (Miq.) D.M.Johnson & N.A.Murray, is proposed, based on an earlier name for the species currently known as Xylopia stenopetala Oliv. In the Xylopia malayana group, review of the species Xylopia elliptica Maingay ex Hook.f. & Thomson resulted in the recognition of three additional species: Xylopia platycarpa D.M.Johnson & N.A.Murray, from southern Thailand and northwestern Peninsular Malaysia, Xylopia ngii D.M.Johnson & N.A.Murray, from Peninsular Malaysia, Sumatra and Borneo, and Xylopia heterotricha D.M.Johnson & N.A.Murray, from Sumatra and Borneo. The taxon Xylopia malayana Hook.f. & Thomson var. obscura Kochummen is placed in synonymy under Xylopia elliptica sensu stricto. Xylopia fusca Maingay ex Hook.f. & Thomson var. sessiliflora Kochummen & Whitmore is distinguished from Xylopia fusca, and raised to species status as Xylopia sessiliflora (Kochummen & Whitmore) D.M.Johnson & N.A.Murray. We recognise 23 Xylopia species in the Sundaic region of Southeast Asia, and provide evidence that additional collecting and taxonomic analysis in the region is needed.

Summary

Introduction

• The Annonaceae, a flowering plant family of 2500 species, including the economically important soursop, custard apple and ylang-ylang, is widespread across the tropics.
• Corlett & Turner (1997) determined that Annonaceae ranked fourth in species-richness among flowering plant families in Singapore; Appanah et al. (1993) found that Annonaceae ranked first in species diversity among lianas of Malaysian forests.
• A full treatment, including keys and distribution maps, is forthcoming.
• Conservation assessments using IUCN (2012) criteria are not included in this account as more data are required for these than the authors currently have available.

Xylopia ferruginea group

• The Xylopia ferruginea group is characterised by stilt roots, relatively long (5-19 mm) flower pedicels, a flat receptacle lacking a staminal cone (Fig. 2K ), flat narrowly oblong stamens with a tongue-shaped apex to the anther connective (Fig. 2J ), stigmas studded with small papillae (Fig. 2I ), and rugose seeds (Fig. 2C-D ).
• Seeds in a single row, parallel to long axis of monocarp, 6-12 per monocarp, 7.2-8.8 mm long, 5.5-5.6 mm wide, 4.7-5.1 mm thick, ellipsoid, elliptic in cross section, dark brown, rugose, flattened or a little concave at micropylar end, rounded at chalazal end, raphe and antiraphe distinctly raised; aril and aril plate absent.
• The bulk of the Sarawak and Brunei collections have come from either lowland peat swamp forest or heath forest (terminology following Saw, 2010) .
• These features are frequent in Sumatran specimens of Xylopia ferruginea s.s., which in general have larger and broader leaves than those of Peninsular Malaysian and Bornean plants, as well as a tendency toward a subcordate rather than truncate leaf base.
• The leaves are retuse at the apex and broadly cuneate and decurrent at the base.

Xylopia malayana group

• Species of the Xylopia malayana group are distinctive and well circumscribed with the exception of X. elliptica and X. malayana.
• The protologue, reproduced verbatim below, shows that the diagnosis emphasised the glabrous branches, the small elliptic, obtuse, membranous, glabrous leaves and the solitary flowers: 14.
• X. elliptica, Maingay mss.; branches glabrous, leaves small elliptic obtuse membranous glabrous, tip rounded, nerves faint reticulate, flowers small solitary erect pubescent, sepals subacute united to the middle, ovaries 1-3.
• Ridley (1922) subsequently maintained King's concept of the species intact.

Xylopia platycarpa

• Restricted to a small area of southern Thailand and northwestern Peninsular Malaysia.
• All localities are in lowland evergreen forest.
• Flowers in July and August, fruit collected in July.

Local name. Kerangi lotong (Kedah: Awang 42444).

• The species is named for its unusually flattened and beanlike monocarps.
• Twigs dark brown to brownish grey, eventually lenticellate, glabrous or finely but sparsely pubescent and soon glabrate; double-branching occasional.
• Material of this species is usually identified in herbarium collections as Xylopia malayana, but X. ngii differs consistently from that species in its smaller (2-2.9 mm long) sepals sparsely covered with pale brown pubescence and the longer (13.5-34.2 mm) and narrower (1-1.6 mm wide at the midpoint) outer petals.

Distribution

• The leaf blades are relatively small and oblong, often with a blotchy mottled appearance to the adaxial leaf blade surface when dried.
• Malaysia, Negeri Sembilan, Kuala Pilah, Pasoh F.R., Compt, also known as -TYPE.
• To confuse things further, this specimen was identified in turn as both Xylopia elliptica and X. malayana in the same publication by Corner (1978) .

Conclusion

• Six species are widespread across the Malay Peninsula, Sumatra and Borneo: Xylopia caudata Wall. ex Hook.f. & Thomson, X. ferruginea, X. fusca, X. malayana, X. ngii and X. sumatrana.
• Two species are shared between the Malay Peninsula and Borneo: Xylopia erythrodactyla and X. magna.
• Several species are large trees more than 40 meters in height, and this, coupled with sparseness of individuals in populations, may cause them to be overlooked.
• This explanation accords well with the extraordinary diversity of the genus found at sites such as the Pasoh Reserve, where in 2014 the authors verified the occurrence of seven Xylopia species in or near the Pasoh permanent 50-hectare research plot (Manokaran et al., 1992) .
• The authors results make clear, however, that further collecting and taxonomic analysis of the Malay Peninsula flora is still critically needed.

Full text

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Gardens’ Bulletin Singapore 67(2): 361–386. 2015
doi: 10.3850/S2382581215000307
A contribution to the systematics of Xylopia
(Annonaceae) in Southeast Asia
D.M. Johnson & N.A. Murray
Department of Botany & Microbiology, Ohio Wesleyan University
Delaware, OH 43015 USA
dmjohnso@owu.edu
namurray@owu.edu
ABSTRACT. Herbarium and eld study of Xylopia L. (Annonaceae) for the Flora of Peninsular
Malaysia and the Flora of Thailand projects has claried regional diversity patterns within
this ecologically signicant lowland rainforest genus. Two species groups represented within
Southeast Asian oras are delineated, one centred on Xylopia ferruginea (Hook.f. & Thomson)
Baill. and the other on Xylopia malayana Hook.f. & Thomson. In the Xylopia ferruginea group,
a new species, Xylopia erythrodactyla D.M.Johnson & N.A.Murray, is distinguished from X.
ferruginea, and a new combination, Xylopia sumatrana (Miq.) D.M.Johnson & N.A.Murray,
is proposed, based on an earlier name for the species currently known as Xylopia stenopetala
Oliv. In the Xylopia malayana group, review of the species Xylopia elliptica Maingay ex
Hook.f. & Thomson resulted in the recognition of three additional species: Xylopia platycarpa
D.M.Johnson & N.A.Murray, from southern Thailand and northwestern Peninsular Malaysia,
Xylopia ngii D.M.Johnson & N.A.Murray, from Peninsular Malaysia, Sumatra and Borneo,
and Xylopia heterotricha D.M.Johnson & N.A.Murray, from Sumatra and Borneo. The taxon
Xylopia malayana Hook.f. & Thomson var. obscura Kochummen is placed in synonymy under
Xylopia elliptica sensu stricto. Xylopia fusca Maingay ex Hook.f. & Thomson var. sessiliora
Kochummen & Whitmore is distinguished from Xylopia fusca, and raised to species status as
Xylopia sessiliora (Kochummen & Whitmore) D.M.Johnson & N.A.Murray. We recognise 23
Xylopia species in the Sundaic region of Southeast Asia, and provide evidence that additional
collecting and taxonomic analysis in the region is needed.
Keywords. Annonaceae, biogeography, Borneo, Malay Peninsula, Sumatra, Sundaland,
Thailand, Xylopia
Introduction
The Annonaceae, a owering plant family of 2500 species, including the economically
important soursop, custard apple and ylang-ylang, is widespread across the tropics.
The family is most diverse, and ecologically most signicant, in tropical Asia, where
it is represented by c. 40 genera and 800 species. In southeastern Asia it is one of
the dominant families in lowland wet forests. Corlett & Turner (1997) determined
that Annonaceae ranked fourth in species-richness among owering plant families
in Singapore; Appanah et al. (1993) found that Annonaceae ranked rst in species
diversity among lianas of Malaysian forests. In long-term ecological plots in Southeast

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Gard. Bull. Singapore 67(2) 2015
Asia Annonaceae usually rank among the top ten tree families in both number of
individuals and number of species, though not in basal area (see examples in Losos &
Leigh, 2004).
The genus Xylopia L., the only pantropical genus in the family, comprises
180–200 species of trees and shrubs worldwide. The highest concentration of species
in Southeast Asia occurs in the Sundaic region extending from the Kra Isthmus in
southern Thailand to Wallace’s Line, a region of high diversity for many plant taxa.
Xylopias are distinctive among the Annonaceae in their cone-shaped buds, elongate,
aromatic owers, and dehiscent fruits with seeds bearing arils or eshy seed coats. In
West Africa the peppery fruits of Xylopia aethiopica (Dunal) A.Rich. have long been
used as a spice (Dunal, 1817; Burkill, 1985) and are sold commercially. Despite its
signicance, the genus has never been monographed.
In preparing keys and descriptions of the genus Xylopia (Annonaceae) for the
Flora of Peninsular Malaysia and Flora of Thailand projects we had the opportunity to
study material in herbaria with important holdings for the region as well as to observe
several species in the eld. At the beginning of our study 13 Xylopia taxa were known
from Peninsular Malaysia, Singapore and Thailand combined (Sinclair, 1953, 1955;
Kochummen et al., 1970; Kochummen, 1972a, 1972b; Chalermglin, 2001; Gardner et
al., 2015).
Analysis of morphological and preliminary molecular data (Stull et al., 2011;
Thomas et al., 2015; Stull et al., in prep.) has shown that the Southeast Asian species of
Xylopia fall into two groups, one including Xylopia ferruginea (Hook.f. & Thomson)
Baill. and a second including Xylopia malayana Hook.f. & Thomson, each with
their respective allies. Our study revealed a much greater diversity of species than
previously recognised in both groups. To document this diversity, and reconcile it with
the previously existing taxonomy and nomenclature for the genus, the following paper
is presented. A full treatment, including keys and distribution maps, is forthcoming.
Conservation assessments using IUCN (2012) criteria are not included in
this account as more data are required for these than we currently have available.
Although historical EOOs and AOOs can be calculated, we are conscious that many of
the collections have been made in lowland forest areas that have suffered from rapid
deforestation. In these cases the Population Reduction (A) criterion would be more
appropriate, as has been used for many dipterocarp species (IUCN, 2014), but again
we would require more on-the-ground knowledge than we currently have.
Xylopia ferruginea group
The Xylopia ferruginea group is characterised by stilt roots, relatively long (5–19
mm) ower pedicels, a at receptacle lacking a staminal cone (Fig. 2K), at narrowly
oblong stamens with a tongue-shaped apex to the anther connective (Fig. 2J), stigmas
studded with small papillae (Fig. 2I), and rugose seeds (Fig. 2C–D). In addition, most
species of the Xylopia ferruginea group have relatively numerous (up to 20) linear and
somewhat torulose monocarps.

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Xylopia in Southeast Asia
Study of the group resulted in demarcation of a new species, and recognition of
an earlier name for an existing species.
Xylopia erythrodactyla D.M.Johnson & N.A.Murray, sp. nov.
Species resembling Xylopia ferruginea in the rusty pubescence of the leaves and
owers and the long narrow monocarps, but differing consistently in the more densely
pubescent and thicker leaves, thicker pedicels (1.3–2.5 mm), longer sepals (4.8–7.9
mm), broader outer petals (3–3.7 mm wide at the midpoint) and narrowly oblong and
weakly torulose monocarps 7.5–10.7 cm long and 0.6–1.1 cm wide. In contrast, in
Xylopia ferruginea the pedicels are 1–1.3 mm thick, the sepals are 3–5.5 mm long, the
outer petals are 2–2.2 mm wide at the midpoint, and the monocarps are linear, strongly
torulose, 6.2–11.6 cm long and 0.4–0.6 cm wide. – TYPE: Malaysia, Sarawak, Teluk
Bandung, Santubong, 1st Division, 18 September 1984 (fr), Awa & Ismawi S.47080
(holotype KEP; isotypes ASU, K, L, SAR). (Fig. 1, 2)
Tree up to 30 m tall, dbh up to 75 cm, bole smooth with stilt roots at the base;
secondary branches drooping. Bark smooth, light brown, brown tinged with red,
brick-red, or orange, very nely ssured. Twigs light grey to brown, eventually
dark grey, densely ferruginous-pubescent/velutinous, eventually glabrate. Leaf with
larger blades 12.4–26 cm long, 3.9–7 cm wide, subcoriaceous to coriaceous, strongly
discolorous, oblanceolate, oblong-oblanceolate, or narrowly elliptic, base rounded to
cuneate and short-decurrent, apex short-acuminate, the acumen 2–7 mm long, glabrous
adaxially, densely ferruginous-pubescent, the pubescence especially pronounced
along the midrib, secondary veins, and larger higher-order veins abaxially; midrib
impressed adaxially, raised abaxially; secondary veins 11–14 per side, diverging at
50–60° from the midrib, brochidodromous, these and higher-order veins indistinct
adaxially, strongly raised abaxially; petiole 5–12 mm long, deeply canaliculate
(margins nearly meeting), pubescent. Inorescences axillary or from axils of fallen
leaves, 1–3-owered, densely ferruginous-pubescent; peduncles 1–2 per axil, 2 mm
long; pedicels 2 per peduncle, 7–14 mm long, 1.6–2.5 mm thick; bract 1, attached
⅓–½ distance from base of pedicel, 2.9–3 mm long, ovate, apex acute to obtuse; buds
linear-lanceolate, sometimes somewhat falciform and slightly twisted, apex obtuse.
Sepals ⅛–¼-connate, 4–7.9 mm long, 4–5.3 mm wide, coriaceous, broadly ovate to
triangular, apex acute to acuminate, occasionally obtuse, pubescent along margins
and at apex adaxially, ferruginous-pubescent abaxially. Petals pale yellow to white
in vivo; outer petals curving outward at anthesis, 38–45 mm long, 4–5.3 mm wide at
base, 3–3.7 mm wide at midpoint, linear-lanceolate, obtuse, densely grey-puberulent
adaxially, densely ferruginous-pubescent abaxially; inner petals erect at anthesis, 32–
40 mm long, c. 3.5 mm wide at base, c. 1.3 mm wide at midpoint, linear, densely
grey-puberulent on both surfaces except for glabrous concave base. Stamens up to
77, 2.7–3.5 mm long, narrowly oblong, often setose along edges of anther locules,
apex of connective 0.4–0.6 mm long, oblong, densely long-papillate, lament 0.3–0.5
mm long, glabrous; staminal cone absent; outer staminodes c. 18, c. 2.7 mm long,

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Gard. Bull. Singapore 67(2) 2015
Fig. 1. Xylopia erythrodactyla D.M.Johnson & N.A.Murray. A. Two leaves, abaxial view. B.
Flower bud and abaxial view of monocarp, the latter showing beginning dehiscence with single
seed visible. C. Single monocarp in lateral view, resting on adaxial surface of a leaf.
(Photos: N.A. Murray)
oblanceolate, at, apex obtuse. Carpels 16–20; ovaries 1.5–2.5 mm long, narrowly
oblong, densely ferruginous-pubescent with hairs obscuring lower portion of stigmas;
stigmas loosely connivent, c. 2.2 mm long, dark, with a few scattered hairs and
studded with amber-coloured papillae. Torus at, c. 3.4 mm in diameter. Pedicel of
fruit 11–20 mm long, 4–7 mm thick, pubescent; torus of fruit c. 8 mm high, 9–14
mm in diam., depressed-globose, sparsely pubescent to glabrate. Monocarps red with
brown tomentum in vivo, up to 20 per fruit, 5.5–10.7 cm long, 0.6–1.1 cm wide and
thick, linear to narrowly oblong, weakly torulose, terete in cross-section, apex rostrate,
the beak 2.5–9 mm long, base contracted into a stipe 8–10 mm long, 3.5–4 mm thick,
longitudinally wrinkled, ferruginous-pubescent to glabrate; pericarp 1.7 mm thick.
Seeds in a single row, parallel to long axis of monocarp, 6–12 per monocarp, 7.2–8.8
mm long, 5.5–5.6 mm wide, 4.7–5.1 mm thick, ellipsoid, elliptic in cross section, dark
brown, rugose, attened or a little concave at micropylar end, rounded at chalazal end,
raphe and antiraphe distinctly raised; aril and aril plate absent.
Distribution. Occurs in Terengganu in northeastern Peninsular Malaysia, and on the
northern coast of the island of Borneo in Sarawak (East Malaysia) and in Brunei.
Considering its restricted habitat and the pace of development in Sarawak, this species

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Fig. 2. Xylopia erythrodactyla D.M.Johnson & N.A.Murray. A. Habit. B. Inorescence with
ower buds, side view. C. Seed, view of micropylar end. D. Seed, side view. E. Fruit. F.
Outer petal, adaxial view. G. Inner petal, adaxial view. H. Stigma apex. I. Carpel. J. Stamen.
K. Close-up of ower with petals and stamens removed, to show sepals, carpels and torus.
L. Schematic side view of ower at anthesis, one outer petal removed. Drawn by Kate Ball
from (A) Awa & Ismawi S.47080, ASU; (B) Sibat ak Luang S.24502, L; (C–E) Chew & Kiah
SFN.40982, A; (F, G, K) Zehnder S.16803, A; (H–J) Rogstad 704, A; and (L) eld sketch.