A taxonomic revision of Melanoxerus (Rubiaceae), with descriptions of three new species of trees from Madagascar

Abstract Kainulainen, K. (2021). A taxonomic revision of Melanoxerus (Rubiaceae), with descriptions of three new species of trees from Madagascar. Candollea 76: 105–116. In English, English and French abstracts. This paper provides a taxonomic revision of Melanoxerus Kainul. & Bremer (Rubiaceae) – a genus of deciduous trees with eye-catching flowers and fruits that is endemic to Madagascar. Descriptions of three new species, Melanoxerus antsirananensis Kainul., Melanoxerus atropurpureus Kainul., and Melanoxerus maritimus Kainul. are presented along with distribution maps and a species identification key. The species distributions generally reflect the ecoregions of Madagascar, with Melanoxerus antsirananensis being found in the dry deciduous forests of the north; Melanoxerus atropurpureus in the inland dry deciduous forests of the west; Melanoxerus maritimus in dry deciduous forest on coastal sands; and Melanoxerus suavissimus (Homolle ex Cavaco) Kainul. & B. Bremer in the dry spiny thicket and succulent woodlands of the southwest.


Introduction
The genus Melanoxerus Kainul. & B. Bremer is part of the tribe Gardenieae in the flowering plant family Rubiaceae. It was segregated from Euclinia Salisb. based on the results of the molecular phylogenetic analyses by Kainulainen & Bremer (2014). Whereas Euclinia is restricted to central Africa, Melanoxerus is endemic to Madagascar, where it is widely distributed in the subarid to dry southern and western regions but also occurs in the dry to subhumid north. Melanoxerus is a genus of deciduous or semi-deciduous trees with smooth flaky bark and sympodial plagiotropic branches with terminally clustered leaves and scarious stipules covering the terminal buds. The flowers are showy and very fragrant, and the large fleshy fruits are lenticellate with conspicuous patterns. The genus can be further diagnosed in that leaves and flowers turn black when drying. It is readily distinct from the other genera of tribe Gardenieae in Madagascar, i.e., Catunaregam Wolf, Gardenia Ellis, and Hyperacanthus E. Mey. ex Bridson. Melanoxerus lacks the opposite-decussate spines of Catunaregam, the sheathing persistent stipules and resinous exudate of Gardenia, and the flowers and fruits are terminal, whereas in Hyperacanthus these appear axillary (Schatz, 2001;Madagascar Catalogue, 2021).
A taxonomic revision of Melanoxerus is warranted. Melanoxerus suavissimus (Homolle ex Cavaco) Kainul. & B. Bremer is currently the only recognized species in the genus. It was originally described by Cavaco (1967) as Gardenia suavissima Homolle ex Cavaco, but shortly thereafter transferred to Euclinia by Leroy (1974). In the protologue, Cavaco (1967) lists several paratypes from western Madagascar that do not correspond to the same species as the holotype from Ambovombe in southernmost Madagascar. The populations from northern Madagascar are also morphologically distinct. Since plants of Melanoxerus are deciduous and often flower before the leaves flush, specimens collected at different times of the year can be difficult to match up, and this may in part explain how the new species presented in this paper have escaped taxonomic attention in the past despite their eyecatching flowers and fruits. In this study I recognize a total number of four species in Madagascar, with M. antsirananensis Kainul., M. atropurpureus Kainul., and M. maritimus Kainul. being newly described.
The molecular phylogenetic study by Kainulainen & Bremer (2014) included samples from three of the four species recognized here, and their phylogenetic reconstruction from plastid DNA data indicates that Melanoxerus atropurpureus (as "sp. 2") and M. suavissimus are more closely related than either are to M. antsirananensis (as "sp. 1"). Melanoxerus maritimus was not included in that study. Kainulainen et al. (2017) estimated that the Melanoxerus clade diverged from an African ancestor around 9.4 Ma (with a 95 % highest posterior density interval of 6.6 -12.4 Ma), and that the crown age, and consequently the minimum age of the dispersal of this lineage from Africa to Madagascar, is 4.2 Ma (95 % HPD: 1.9 -6.9 Ma). Pollen dispersed in tetrads. Fruits fleshy-indehiscent, globose to ovoid, with a thick mesocarp and an exocarp covered with conspicuous lenticels. Seeds flattened, irregularly angled, horizontally inserted and immersed in soft pulp.
Distribution, habitat and ecology. -Melanoxerus is endemic to Madagascar and distributed across most of the southern and western regions (i.e. Anosy, Androy, Atsimo-Andrefana, Menabe, Melaky, Boeny, and Sofia Regions), as well as in northernmost Madagascar in the DIANA and SAVA Regions. Melanoxerus occurs in vegetation types ranging from subarid thickets to subhumid semi-deciduous forests, from sea level to about 800 m in elevation, and on various substrates from coastal sands to laterite, including skeletal soils in karstic limestone formations (tsingy). It is absent from the Central Highlands and the humid east coast. Although there are exceptions, in general the species distributions reflect the ecoregions of Madagascar (cf. Olson et al., 2001), with M. antsirananensis being found in the dry deciduous forests of the north; M. atropurpureus in the inland dry deciduous forests of the west; M. maritimus in dry deciduous forest on coastal sands; and M. suavissimus in the dry spiny thicket and succulent woodlands of the southwest (Fig. 1).
Little is known about the ecology of this genus, and no information on pollination or seed dispersal has been recorded for the specimens that I have examined. The flowers are large and ± fleshy, with funnelform to broadly urceolate corollas that are externally white (sometimes tinged purple or pale green) and internally purple or white with green, red, or purple markings. Pollen is usually deposited on the upper part of the style (secondary pollen presentation), which is club-shaped with longitudinal ridges. The flowers are strongly fragrant with a sweet smell like jasmine.
The fruits are large, indehiscent "berries" with a fleshy pulp and are most likely an adaptation to endozoochory. The seeds are presumably dispersed by lemurs, but it is possible that seed dispersal, at least in part, has relied on the recently extinct Malagasy megafauna, as has been suggested for Adansonia L. (Baum, 1995) -a genus which also has large indehiscent fruits, and a distribution in Madagascar that is similar to that of Melanoxerus. The leaves of Melanoxerus appear to be attractive to herbivores because in the specimens seen in this study the leaves are usually damaged. Although not documented, insects are probably responsible for part of the damages, although slugs (pers. obs.) and lemurs of the genus Propithecus (information on the label of Meyers & Boltz 110) have been observed feeding on leaves of M. antsirananensis.  (Fig. 2).
Phenology. -Flowering material has been collected from October to November and fruiting material from December to July.
Conservation status. -Melanoxerus atropurpureus has a wide distribution in western Madagascar and is known from several protected areas including Ankarafantsika, Bemaraha, and Namoroka. It can therefore be assigned a preliminary conservation status of "Least Concern" [LC] according the IUCN Red list Categories and Criteria (IUCN, 2012). However, it is not a commonly collected species, and more information is needed about its population size.
Notes. -The specimen Perrier de la Bâthie 1155A from the Ankara plateau is in poor shape but probably belongs to this species. In this species the exocarp of the fruit is often almost completely hidden by lenticels (Fig. 3F).
Distribution, habitat and ecology. -Melanoxerus maritimus is known from sea level to 30 m in elevation in coastal areas of the Boeny, Melaky, and Sofia Regions (Mahajanga Province) (Fig. 1). It grows in low canopy, dry deciduous forests on dunes and on edges of salt flats or mangroves.
Phenology. -Flowering material has been collected from June to November, and fruiting material from July to February.
Conservation status. -Melanoxerus maritimus is known from less than ten locations, (three of which are within the recently protected areas of Antrema, Bombetoka Belemboka, and Mandrozo), with an estimated area of occupancy (AOO) of less than 2000 km2. It appears restricted to littoral dry forest. This habitat is impacted for firewood or charcoal production (also noted on label of De Block & Rakotonasolo

806).
It is projected that the number of locations and the number of mature individuals continue to decline, and this species can therefore be assigned a preliminary conservation status of "Vulnerable" [VUB2ab(iii)] according to IUCN Red list Categories and Criteria (IUCN, 2012). However, more information is needed about the population size of this species.
Phenology. -Flowering specimens have been collected in (April) July to December, and fruiting specimens throughout the year.
Conservation status. -Melanoxerus suavissimus is widespread in south-western Madagascar and has been assigned an IUCN conservation status of "Least Concern" [LC] (IUCN, 2021).
Notes. -Since Cavaco's (1967) original description of Melanoxerus suavissimus (as Gardenia suavissima) included specimens of both M. atropurpureus and M. maritimus, an amended description is provided. This is the most widespread and the most commonly collected species. However, few collections have been made in from May to August (none from June), and presumably this species is usually leafless during that time. Melanoxerus suavissimus usually flowers at the same time or just before the new leaves flush (cf. Fig. 5A, D). Apparently, the juice of the fruits turns black and is used for making tattoos (Schatz, 2001). Information about of the use of Melanoxerus by local people is otherwise scant, although according to the label information on the specimen Ranaivojaona et al. 248, the fruits are edible.