New species and new records of Artabotrys (Annonaceae) from peninsular Thailand

Abstract Two new species of Artabotrys (Annonaceae) are described from peninsular Thailand. Artabotrys longipetalus J.Chen & Eiadthong, sp. nov., is unique among Artabotrys species in Thailand in having linear petals, relatively long flower pedicels and sessile monocarps. Artabotrys insurae J.Chen & Eiadthong, sp. nov., resembles Artabotrys uniflorus (Griff.) Craib, but can be distinguished by its oblique leaf base, flat petal blades, apiculate anther connective apex and the presence of a monocarp stipe. In addition, two new records for the Flora of Thailand are reported, viz. Artabotrys crassifolius Hook.f. & Thomson and Artabotrys pleurocarpus Maingay ex Hook.f. & Thomson; both species are so far only known from peninsular Thailand. A key to the 20 species of Artabotrys in Thailand is provided.


Introduction
Artabotrys R.Br. (Annonaceae) is a palaeotropical genus of woody climbers that inhabits tropical rain forests and seasonally dry forests. The genus comprises over 100 species, with the majority occurring in Asia, ca. 30 species in Africa, and one species in Northern Australia (Chen et al. 2018). The presence of specialised inflorescence hooks that assist climbing distinguishes Artabotrys from other Annonaceae climbers. A recent molecular phylogenetic study (Chen et al. 2019) revealed that the genus consists of an early-divergent grade (EDG) of two African species, and a main Artabotrys clade (MAC) comprising an Asian clade sister to an African clade. Artabotrys possess trimerous flowers, with a whorl of sepals and two whorls of petals. The outer and inner petals are generally similar in size whereas the sepals are much smaller than the petals. MAC species are characterised by petals with a distinct upper blade and a basal concave claw, and an elaborate rim between the inner petal blade and claw which enables the inner petals to cohere tightly over the reproductive organs (Chen et al. 2020). Conversely, EDG species lack a projecting rim on the inner petals, with one species (A. brachypetalus Benth.) entirely lacking the distinction between petal blade and claw (Chen et al. 2020). The flowers of Artabotrys are hermaphroditic, with many stamens and few to many unfused carpels. Each carpel has two ovules on a basal placenta. After fertilisation, these carpels develop into free monocarps that are sessile or borne on short stipes.
Herbarium specimens are easily assigned to Artabotrys if the diagnostic inflorescence hooks are present. The inflorescence is sometimes only slightly recurved, however; in rare cases, it does not manifest as a hook (Fig. 1A). The inflorescence hook is peculiar with regard to its morphology and ontogeny, which are discussed in great detail in Posluszny and Fisher (2000). The hook formation involves successive development of two hook leaves (hook leaf 1, HL 1 followed by hook leaf 2, HL 2 ), flattening and curving of the inflorescence away from the main shoot, and curving of the inflorescence back towards the main shoot. Uneven tissue expansion displaces HL 1 to the distal position and HL 2 to the proximal position (figs 23, 24 in Posluszny and Fisher 2000). The floral bud in the axil of HL 2 is in fact the original apical meristem. The definition of the peduncle, which is usually the distance between the first-formed lower bract and the twig, is contentious in Artabotrys because the first-formed bract (HL 1 ) is not in the lowest (proximal) position. Here, we regard the entire hook (curved axis from HL 1 to twig) as the peduncle but it should be noted that its morphology is highly variable within a species, becoming woody as it clasps onto a twig or not manifest as a hook at all as mentioned earlier. Further higher-order branching of the hook inflorescence may occur, resulting in the formation of lateral branches, which are defined as the axes between the hook and the base of the last pedicel (Fig. 1B). The inflorescence lateral branches may be condensed (Fig. 1A, 2F) or elongate (Fig. 1B). Although the genus is easily recognised, identification at the species level is not as straightforward. Petal morphology is sometimes useful (especially for fresh material), but a suite of more subtle characters are often needed for the identification of herbarium specimens. The characters of taxonomic utility in Artabotrys include indumentum on lower leaf surface (erect vs. appressed), leaf base (cuneate vs. decurrent on petiole vs. rounded vs. oblique), pedicel length, sepal size, petal size and shape, anther connective apex (apiculate vs. truncate), number of carpels per flower, number of monocarps per fruit, monocarp apex, monocarp stipe length and monocarp size.
Although Thailand is considered to be well known botanically, there remains an upward trend in the number of plant species described from Thailand (Middleton et al. 2019). This is also the case for Annonaceae, particularly in peninsular Thailand where new Annonaceae species are continuously added to the baseline of 39 species listed in Craib (1925). Over the past five years, for instance, an Alphonsea species (Turner and
The conservation status of the new species was assessed using the criteria stipulated in the IUCN Red List (IUCN 2012). The extent of occurrence (EOO) and area of occupancy (AOO) of each new species were calculated with the default 2 km 2 grid using GeoCAT (Bachman et al. 2011; http://geocat.kew.org). The abbreviations used in the conservation assessments follow IUCN (2012).
Phenology. Flowering specimens collected in February and August; fruiting specimens collected in May.
Distribution and habitat. So far only known from peninsular Thailand (Fig. 6). It occurs in lowland rain forests at elevation 100-730 m, in both undisturbed and partially disturbed sites, sometimes along ridges.
Etymology. The specific epithet reflects the long petals of this species.
Phenology. Flowering and fruiting specimens collected in August and September. Fruiting specimens also collected in February and June.
Distribution and habitat. So far only known from peninsular Thailand (Fig. 6). It occurs in lowland moist and dry forests, secondary forests and forest edges at elevation 80-200 m.
Etymology. The specific epithet was given in honour of Mr Tawee Insura, whose prolific collection of Artabotrys specimens during his MSc study led to the discovery of several new species and new records for Thailand.
Preliminary conservation status. Artabotrys insurae is estimated to have an EOO of 15,994 km 2 and an AOO of 20 km 2 . This species largely occurs within various Wildlife Sanctuaries, which constitute Protected Areas in Thailand. A population exists in a remnant forest adjacent to Khao Le Buddhist Temple in Songkhla; such vegetation is regarded as sacrosanct and hence would likely remain undisturbed. We suggest a status of Vulnerable [VU D2] for this species because its restricted AOO makes it susceptible to future threats such as climate change. Notes. This species is most similar to A. uniflorus from peninsular Thailand (Chumphon, Ranong, Phang-Nga and Surat Thani) in having erect-pubescent lower leaf surfaces, 1-flowered (rarely 2-flowered) inflorescences, caudate to acuminate leaf apex and relatively narrow monocarps (10-15 mm wide). Its distribution overlaps with A. uniflorus in Surat Thani. Artabotrys siamensis Miq. from Northern, Northeastern, Eastern and Southwestern Thailand is also similar in having erect-pubescent lower leaf surfaces, but is distinct due to its coriaceous leaves, cuneate leaf base, thicker petals, numerous carpels (25-29 per flower), numerous monocarps (up to 22 per fruit) and broader monocarps (15-20 mm wide). Notes. This species was hitherto known from Malacca, Kedah and Perak in Peninsular Malaysia (Sinclair 1955). Specimens of A. pleurocarpus from peninsular Thailand were formerly misidentified as A. kurzii Hook.f. & Thomson or identified to genus level; they were only recently re-identified during our preparation of the Artabotrys treatment for the Flora of Thailand. The specimens from peninsular Thailand and Peninsular Malaysia closely match one another in leaf and fruit morphology and there can be no doubt that they are conspecific. Therefore, this represents the first record of A. pleurocarpus in Thailand. Artabotrys pleurocarpus is distinct among the Thai species on account of its fruit morphology, with relatively few monocarps (up to 9 per fruit) that are prominently beaked (2-3 mm long), quite large (22-30 mm long, 15-20 mm wide) and borne on a long stipe (7-10 mm long). The fruits therefore superficially resemble those of Polyalthia species, but specimens can be easily assigned to Artabotrys if the inflorescence/infructescence hook is present. Although A. kurzii from Myanmar (Pegu) was previously confused with A. pleurocarpus, it bears little resemblance to A. pleurocarpus, differing in its obovate (vs. oblong-lanceolate to oblong-elliptic) leaves, mucronate (vs. caudate to acuminate) leaf apex and short petioles (1-2 mm long vs. 4-6 mm long).  (1955)). Notes. The protologue for A. crassifolius cites a specimen from Martaban in Myanmar. In addition, a regional checklist (Kress et al. 2003) and a forest flora (Kurz 1877) indicate the presence of this species in Tenasserim (Taninthayi), Myanmar. However, Turner (2015) was unable to trace the syntype or any other specimen of this species from Myanmar; our attempts to trace those specimens were likewise in vain. The occurrence of A. crassifolius in Myanmar therefore requires future verification. Artabotrys crassifolius can be distinguished from other species in Thailand as its young twigs, flower pedicels and lower surface of sepals have a dense covering of long appressed hairs that is visible with the naked eye. In Thailand, this species is currently known from a single gathering from Trang, which exhibits the unique indumentum mentioned earlier and has monocarps with shape and size matching A. crassifolius. The specimens of this gathering were previously filed as 'Artabotrys indet' and only recently identified for the Flora of Thailand project. Outside of Thailand, A. crassifolius is widespread in Peninsular Malaysia but restricted to the Central Catchment Nature Reserve and Bukit Timah Nature Reserve in Singapore.