Two new species and two new records of Artabotrys (Annonaceae) from Thailand

Abstract Two new species of Artabotrys are described from Thailand. Artabotrys tanaosriensis J.Chen, Chalermglin & R.M.K.Saunders, sp. nov., is similar to A. oblanceolatus Craib but differs in its symmetrical, cuneate or decurrent leaf base, externally distinct outer petal blades and claws, deltoid and undulate outer petal blades, rhomboid and undulate inner petal blades and shorter, subsessile and slightly beaked monocarps. Artabotrys spathulatus J.Chen, Chalermglin & R.M.K.Saunders, sp. nov., is most similar to A. tanaosriensis but differs in having flat outer petal blades, broadly rhomboid outer petal claws, broadly spathulate and strongly concave inner petal blades and strongly beaked monocarps. Two new records for the Flora of Thailand are furthermore reported here: A. punctulatus C.Y.Wu ex S.H.Yuan and A. byrsophyllus I.M.Turner & Utteridge, which were previously confused with A. aeneus Ast and A. grandifolius King, respectively. A key to Artabotrys species indigenous to Thailand is provided here.


Introduction
Artabotrys R.Br. is one of the largest palaeotropical genera in the Annonaceae, with ca. 105 species (Guo et al. 2017). The majority of the species occur in Asia, with only ca. 30 species in Africa (Mabberley 2008). Artabotrys species are woody climbers that are unique among climbing members of the Annonaceae in possessing specialised and persistent inflorescence hooks (Fig. 2B, D) to assist climbing; these hooks are derived from peduncles and bear flowers and fruits (Posluszny and Fisher 2000). Although these inflorescence hooks allow easy recognition of the genus, identification at the species level is often challenging (Turner 2009;Turner and Utteridge 2015). The leaf lamina is often decurrent to the petiole and the midrib is often raised on the adaxial surface of leaves. The inflorescences often bear several to many flowers, but are singleflowered in some species.
The underlying floral Bauplan of Artabotrys species is rather uniform, with the exception of two African species, viz. A. thomsonii Oliv. (Le Thomas 1969) and A. brachypetalus Benth. (Robson 1960), which have been shown to be early divergent lineages in molecular phylogenetic reconstructions (Chen et al. unpubl.). Individual flowers possess one whorl of three sepals and two whorls of three petals each, with the sepals much smaller than the petals and with the two petal whorls subequal. Each petal has a distinct upper laminar blade and a basal concave claw, usually with a constriction at the junction between the two regions (Figs 1A,B,2B,D). The inner petals are basally connivent, forming a dome that covers the reproductive organs, with three lateral apertures at the base of the dome, enabling pollinator access. The three inner petals abscise as a single unit after anthesis. The flowers are hermaphroditic, with numerous stamens and carpels. Each carpel contains two ovules with basal placentation. The fruits are apocarpous, with "monocarps" (derived from individual carpels after fertilisation) that are usually sessile or borne on very short stipes; the generic name is derived in part from the Greek word "botrys", which alludes to its grape-like fruits.
Although Artabotrys is comparatively well-studied in Thailand, many names have been misapplied and several taxonomic and nomenclatural misunderstandings persist. Craib (1925) Craib andA. venustus King. Chalermglin (2001, 2005) published a photographic guide to Thai Annonaceae that included 10 species, viz. "A. burmanicus" (a misapplied name), "A. grandifolius" (a misapplied name: see new records for Thailand below) A. harmandii, A. hexapetalus, "A. oblanceolatus" (a misapplied name), A. siamensis, A. spinosus, A. suaveolens, A. vanprukii and an unnamed species (which represents "true" A. oblanceolatus). More recently, Thongpairoj (2008)  Ridl." (a misapplied name, for which the name A. oxycarpus should be applied: Thongpairoj 2008) and A. sumatranus Miq. Several species cited by these authors do not occur naturally in Thailand: A. hexapetalus is widely cultivated in Thailand but is likely to be of South Indian or Sri Lankan origin, for example; and Craib (1925) recorded A. scortechinii from Langkawi, an island that was previously under Siamese rule but now part of Peninsular Malaysia. No specimens of A. scortechinii from Thailand or Langkawi have been seen; A. scortechinii is likely to be endemic to Peninsular Malaysia and Singapore (Chen et al. in press). Additionally, three other species (A. lowianus, A. sumatranus and A. vanprukii) are poorly known owing to the absence of flowers and/or fruits in the type specimens, limited available material to assess variation and the problematic treatment of these taxa by previous authors. It is beyond the scope of this paper to clarify these taxonomic problems, however.
Examination of herbarium specimens and fieldwork in Thailand has revealed two new Artabotrys species, which are formally described here. In addition, two new records for Thailand are reported and past taxonomic errors rectified. A total of 15 species are recognised (excluding the aforementioned problematic taxa) and a key to the native species of Artabotrys in Thailand is provided.

Materials and methods
The material studied comprises herbarium specimens of Artabotrys species from Thailand and neighbouring regions from the following herbaria: A, E, KUFF, KUN, L, NY, QBG, SING and US; high-resolution digital images of specimens (especially types) from JSTOR Global Plants (https://plants.jstor.org/) and other virtual herbarium websites; as well as fresh material collected during fieldwork in Thailand. Species delimitation was based on discontinuities (gaps) in morphological variation. The morphological gap is an indirect assessment of the underlying reproductive isolation because the lack of gene flow prevents two lineages from homogenising (Coyne and Orr 2004;Rieseberg et al. 2006). Morphological measurements were taken from dried herbarium specimens unless otherwise stated.
Phenology. Flowering specimens collected in February and August; fruiting specimens collected in October.
Distribution and habitat. So far only known from Thailand (Fig. 5), but possibly also occurring in the adjacent Tanintharyi National Park in Myanmar. Inhabits tropical rain forests on lateritic soil; 150-1000 m elev.
Etymology. The specific epithet alludes to "Tanao Sri", the Thai name of the Bilauktaung subrange of the Tenasserim Range where this species occurs.
Local name.
Phenology. Flowering and fruiting specimens collected in March. Distribution and habitat. So far only known from Thailand (Fig. 5). Inhabits tropical rain forests at the base of limestone hills; ca. 100 m elev.
Etymology. The specific epithet reflects the morphology of the inner petals.

Local name.
Karawek Phruksa Sawan. Notes. The fruit and seeds are only known from fresh material and have not been preserved due to fungal infection.
The distinction between A. spathulatus and A. tanaosriensis is corroborated by unpublished phylogenetic analysis of combined chloroplast (matK, ndhF, psbA-trnH, trnL-F) and nuclear (AP3,carboxymethylenebutenolidase,GI,HMGS,LFY,mag1,ncpGS,NIA,PhyA,RPB2) DNA sequence data, which retrieved A. spathulatus as sister to A. uniflorus, with A. tanaosriensis sister to A. suaveolens (J. Chen et al. unpublished data). Notes. The name A. grandifolius is misapplied by Chalermglin (2001), Thongpairoj (2008, as "A. grandiflorus") and Insura (2009), for which the name A. byrsophyllus  should be applied; A. grandifolius sensu King is restricted to Peninsular Malaysia. Artabotrys byrsophyllus can be distinguished from A. grandifolius by reference to its leathery leaves, reticulate tertiary leaf venation that is indistinct on both surfaces, shorter petals (outer petals 13-16 mm vs. ca. 21 mm; blade of inner petals ca. 8 mm vs. 16-17 mm) and subsessile monocarps with marked apiculum. Notes. Specimens of this species were mistakenly recognised as a new species ("A. sp. 5 (Kao Yai)") by Thongpairoj (2008) and misidentified as "A. aereus" by Insura (2009). Artabotrys punctulatus can be distinguished from A. aeneus (which is only known from Vietnam) by its chartaceous leaves, sparsely pubescent (vs. densely villose) flowering pedicels, sepals and petals, smaller sepals and its elongated, raised rim between the claw and blade on the adaxial surface of the inner petals.

Artabotrys punctulatus C.Y.Wu ex S.H.Yuan
Key to the native Artabotrys species in Thailand  Turner and Utteridge (2015). Localities of A. punctulatus in Yunnan were retrieved from georeferenced herbarium records in GBIF (https://www.gbif.org/).