Codonoboea (Gesneriaceae) in Terengganu, Peninsular Malaysia, including three new species

Abstract Of the 92 Codonoboea species that occur in Peninsular Malaysia, 20 are recorded from the state of Terengganu, of which 9 are endemic to Terengganu including three new species, C. norakhirrudiniana Kiew, C. rheophytica Kiew and C. sallehuddiniana C.L.Lim, that are here described and illustrated. A key and checklist to all the Terengganu species are provided. The majority of species grow in lowland rain forest, amongst which C. densifolia and C. rheophytica are rheophytic. Only four grow in montane forest. The flora of Terengganu is still incompletely known, especially in the northern part of the state and in mountainous areas and so, with botanical exploration, more new species can be expected in this speciose genus.


Introduction
The centre of diversity of the genus Codonoboea (Gesneriaceae) is Peninsular Malaysia from where at least 92 species of the 140 named species are known (Lim and Kiew 2014). However, while the west coast of Peninsular Malaysia is relatively well-collected and from where 35 species were described , the east coast is comparatively poorly known with, for example, prior to this study, just six described from Terengganu. The total now stands at 20 species.  ganu. Codonoboea anthonyi and C. leiophylla, first described from Terengganu, have since been found in SE Kelantan.
Three new species are described here. There are undoubtedly more species that await discovery as many areas remain to be explored. Besides a checklist for Terengganu Codonoboea, a key is provided to facilitate their identification.

Materials and methods
Specimens, including type specimens of Peninsular Malaysian Codonoboea species in the herbaria at BM, K, KEP, KLU, SING and UKMB (acronyms follow Thiers 2019), were examined. All specimens cited were seen by the authors. Literature relevant to the region (West Malesia and Thailand) was consulted. Conventional methods employed in herbarium taxonomy were applied in this study. All measurements were taken from dried herbarium specimens. The spelling of localities follows Hamidah et al. (2011).
It grows in the Tembat Forest Reserve. In 2010, the KEP botany team carried out an intensive collecting programme in the area that was designated for clear-felling for the extension to the Kenyir Hydroelectric Dam in an effort to provide a permanent record of this little known forest. As a result, several new species were discovered, such as two species of Codonoboea, C. norakhirrudiniana and C. tembatensis (Kiew, 2014). Although both these species were quite common and widespread within the Tembat Forest Reserve, they have not been found in other forests in Terengganu. The Tembat Forest Reserve has since been clear-felled for the extension to the Kenyir Hydroelectric Dam. The current status of their populations is not known but, because of their restricted distributions, there is the possibility that the widespread clear-felling will ultimately result in their extinction.
Distribution. Endemic in Terengganu, Dungun District, Rasau Kerteh Forest Reserve, known only from the type.
Ecology. Rheophyte clinging onto rock surface along river in regenerated lowland dipterocarp forest at 54 m altitude. Etymology.
Greek -rheo, pertaining to flowing water. The rheophytic habit is very unusual in Codonoboea species.

Notes. Although
Codonoboea species are common on rocks close to streams and on river banks, very few, notably C. densifolia, C. salicina and this new species, grow within the flood zone and are true rheophytes. All three have the typical habit of rheophytes, wiry stem and exceptionally narrow leaves, although C. densifolia and C. salicina are not obligate rheophytes, since they also grow on steep banks in forest.
Its flower characters place it within the Heteroboea group of species. Other species in this group are large, robust herbs with large, broad leaves quite unlike those of C. rheophytica. Molecular analysis confirms that it (labelled as Codonoboea sp. nov. 2) falls within this group (Lim and Kiew 2014). Diagnosis. In its habit (stem unbranched, woody, 10-25 cm long, 3-6 mm thick) and its petiolate, narrowly lanceolate or slightly oblanceolate lamina 9-20 cm long with many, deeply impressed veins and a serrate margin with teeth 3-5 × 1.2-2 mm, Codonoboea sallehuddiniana resembles C. breviflora (Ridl.) Kiew but it is different in its dichasium with two short branches and flowers in pairs (C. breviflora has a one-flowered inflorescence), its large foliose bracts 11-12 mm long (not linear and 5-10 mm long), its rosy purple, narrow corolla 15-16 mm long (not shorter, campanulate, pale purple to white corolla and 10-14 mm long) and shorter fruits 3-3.5 cm long (not 3-5.5 cm long).
Distribution. Endemic in Dungun District (Jerangau FR, Pasir Raja FR and Sungai Loh) Notes. The inflorescence of Codonoboea sallehuddiniana is unusual for the genus. The basic inflorescence in Codonoboea is a pair-flowered cyme that may be reduced to a single flower (as in C. breviflora) or be branched once (a dichasial pair-flowered cyme) or many times to form a thyrse. In C. sallehuddiniana, the dichasium has two short branches and, on these, are pairs of short-stalked flowers each subtended by a large foliose bract that decreases in size towards the apex. The flowers are all positioned in the same direction. The particularly long, narrow corolla tube that scarcely dilates and has prominent hairs in the mouth is unusual in Codonoboea.

Habitat
In Terengganu, most Codonoboea species have been collected from lowland dipterocarp forest below 250 m elevation in the foothills of the Terengganu Range. Few are found at higher elevations, namely C. codonion (to 550 m), C. puncticulata (924 m) and, from Gunung (Mount) Padang (at 1,040 m), C. padangensis and C. grandifolia. However, this is likely an artefact of collecting because very few mountain peaks in Terengganu have been explored botanically. Many species are associated with steep earth slopes, either in forest or on river banks or on rocks but two, C. densifolia and C. rheophytica, with characteristic narrow leaves, are rheophytes that live on rocks in the flood zone in streams.
No species is recorded from the Marang or Kuala Nerus Districts. This is probably because they are coastal districts and, as yet, no species has been collected from kapur forest nor from tropical heath forest, nor from streams and rivers with tidal influence.
Codonoboea species are all obligate shade plants that grow in conditions of high humidity. In Terengganu, they are particularly vulnerable because most grow in forest below 250 m elevation and it is this land that is most vulnerable to land use changes. Populations are eliminated by clear-felling forests for palm oil plantations and infrastructure development such as road building or constructing hydroelectric dams. No Codonoboea species is weedy and able to adapt to conditions when the tree canopy is opened up from logging or clear-felling (Kiew 2009).

Distribution
Comparison of species per district illustrates that the northern districts of Besut and Setiu, each with six Codonoboea species, are poorer in species compared with 11-12 species recorded for the Dungun, Kemaman and Hulu Terengganu districts. This, however, is likely due to under-collecting; the northern districts are still poorly known. Within the limitation that many areas have still to be explored, particularly in the north and at high elevations, several patterns of distribution can be identified amongst the more widespread species.
Apart from the widespread species (C. quinquevulnera, C. platypus and C. rugosa), the Terengganu flora does not share any species with the Main Range or the west coast states (Table 1). Codonoboea rugosa is confined to the northern states and its distribution extends into Thailand. On the east coast, it appears to replace C. crinita (Jack) C.L.Lim that is common on the west coast, particularly in the hills. Excluding these widespread species, four species (C. atrosanguinea, C. anthonyi, C. leiophylla and C. salicinoides) are shared with Kelantan, four with Pahang (C. atrosanguinea, C. codonion, C. grandifolia and C. salicinoides) and two with Johor (C. densifolia and C. puncticulata). The last two species are much more common in Johor and reach their northern limit in southern Terengganu.

Endemism
Nationally, the level of endemism in Codonoboea (as Didymocarpus) is high, 94% (Kiew 1991b) and many species are site endemics. Of the 20 species in Terengganu, only three have distributions extending beyond Peninsular Malaysia. Codonoboea puncticulata was recorded from Singapore but that population is now extinct; C. platypus is known from Sumatra and Borneo; and C. platypus and C. rugosa from Peninsular Thailand. Of the nine species endemic to Terengganu (Table 2), C. padangensis and C. rheophytica are each at present known from a single population and C. miniata, C. norakhirrudiniana and C. tembatensis from restricted areas.

Codonoboea anthonyi (Kiew) C.L.Lim
In Kiew & Lim, Gard. Bull. Sing. 62 (2011) 256. Basionym: Didymocarpus anthonyi Kiew, Gard. Bull. Sing. 44 (1992 24. Homotypic synonym: Henckelia anthonyi (Kiew) A. Weber, Beitr. Biol. Pflanzen 70 (1998)  Note. In Terengganu known only from one old 1904 collection, Rostados s.n., that  described as Paraboea caerulea. It is a very distinct narrow-leaved species not likely to be confused with any other species. It is not known if the ongoing tin-mining in 1904 destroyed its habitat, which would explain why it has not been collected since. Rheophytes are particularly vulnerable to habitat disturbance that would cause increased silt disposition, destruction of river banks or the opening of the canopy. It is likely, therefore, that the Bkt. Bandi population has been eliminated. However, it is common in Johor (Kiew, 1987).
Ecology. Lower montane forest at 1100-1220 m elevation, in shade on very steep earth slopes.
Note. It is a striking species with particularly large leaves and flowers. It only grows on steep earth slopes and appears to be rare and local.