Melicope stonei, section Pelea (Rutaceae), a new species from Kaua‘i, Hawaiian Islands: with notes on its distribution, ecology, conservation status, and phylogenetic placement

Abstract Melicope stonei K.R. Wood, Appelhans & W.L. Wagner (section Pelea, Rutaceae), a new endemic tree species from Kaua‘i, Hawaiian Islands, is described and illustrated with notes on its distribution, ecology, conservation status, and phylogenetic placement. The new species differs from its Hawaiian congeners by its unique combination of distinct carpels and ramiflorous inflorescences arising on stems below the leaves; plants monoecious; leaf blades (5–)8–30 × (4–)6–11 cm, with abaxial surface densely tomentose, especially along midribs; and very long petioles of up to 9 cm. Since its discovery in 1988, 94 individuals have been documented and are confined to a 1.5 km2 region of unique high canopy mesic forest. Melicope stonei represents a new Critically Endangered (CR) single island endemic species on Kaua‘i.


Introduction
The genus Melicope J.R. Forst. & G. Forst. consists of ca. 235 species of shrubs and trees with a distribution that ranges from the Malagasy and Indo-Himalayan regions in the east to the Hawaiian and Marquesan Islands in the west and from Nepal, southern China, Taiwan and the Japanese Ogasawara Islands in the north to New Zealand and Australia in the south (Hartley 2001, Appelhans et al. 2014a, Wood et al. 2016a. With the inclusion of Melicope stonei K.R. Wood, Appelhans & W.L. Wagner, the total number of recognized Melicope reported for the Hawaiian Islands totals 50 endemic species, making Melicope the most species-rich radiation of woody plants throughout the archipelago (Hillebrand 1888, Hartley and Stone 1989, Wagner et al. 1999, Wood et al. 2016a. Molecular phylogenetic studies indicate that the Hawaiian species arose from a single introduction, and that the Hawaiian genus Platydesma H. Mann is nested within Melicope section Pelea (A. Gray) Hook. f. as sister to the Hawaiian species of Melicope (Harbaugh et al. 2009, Appelhans et al. 2014b. To preserve the monophyly of Melicope sect. Pelea, Platydesma must be merged with Melicope and when those new combinations are validly published, Hawaiian Melicope will then be increased by an additional four species. In the most current systematic revision by Hartley (2001) Melicope was subdivided into four sections: Lepta (Lour.) T.G. Hartley; Melicope; Pelea; and Vitiflorae T.G. Hartley. Only sect. Lepta proved to be a monophyletic group in a recent molecular study (Appelhans et al. 2014b). All Hawaiian species of Melicope are members of sect. Pelea, which consists of 86 species almost exclusively restricted to Melanesia and the Pacific region. Pelea previously was recognized at the genus rank with the Hawaiian species subdivided into four sections in the revision by Stone (1969): Apocarpa B.C. Stone; Cubicarpa B.C. Stone; Megacarpa B.C. Stone; and Pelea (Wagner et al. 1999). The classification needs to be revised since the sectional classification of Hartley (2001) would require the Hawaiian groups to be treated as subsections if it is appropriate to continue recognizing them at all. Within these four Hawaiian groups only the Hawaiian Pelea group proved to be monophyletic (Appelhans et al. 2014c).
Phenology. Melicope stonei has been observed with flower buds in January, May, and September, and with both flower and fruit during January, February, and July.

Etymology.
We are pleased to name Melicope stonei in honor of Benjamin Clemens Masterman Stone, British-American botanist, born in Shanghai, China in1933 and passed in 1994 while working at the Philippine National Museum on the Flora of the Philippines Project. He contributed over 300 publications to science during his career, including taxonomic monographs of Hawaiian Pelea (Stone 1969) and Platydesma (Stone 1962). For all his contributions, especially his keen insights into Hawaiian Melicope, we gratefully extend him due recognition.  Threats to Melicope stonei include habitat degradation by introduced pigs (Sus scrofa L.) and mule deer (Odocoileus hemionus Rafinesque), predation of seeds by rats (Rattus rattus L. and R. exulans Peale), environmental events such as hurricanes, fire (mostly by humans), and competition with invasive non-native plant species, including Adiantum hispidulum Sw. Tryon (Cyatheaceae) all of which possess the ability to spread rapidly and cover effectively large areas (Smith 1985).
Conservation status. IUCN Red List Category. When evaluated using the World Conservation Union (IUCN) criteria for endangerment (IUCN 2001), Melicope stonei falls into the Critically Endangered (CR) category, which designates this species as facing a very high risk of extinction in the wild. Our formal evaluation can be summarized by the following IUCN hierarchical alphanumeric ranking system of criteria and subcriteria: CR B1ab(i,ii,iii,iv,v)+2ab(i,ii,iii,iv,v); C2a(i); which reflects a severely limited Extent of Occurrence (EOO) and Area of Occupancy (AOO) of less than 1.5 km 2 and a wild population of less than 100 individuals with all facing a continuing decline in their area of extent and quality of habitat (see Distribution, ecology, and threats). Seeds from several individuals of M. stonei have been collected and submitted to the NTBG Horticultural Department for cultivation.
Morphology, related taxa, and phylogenetic placement. Melicope stonei stands apart from all other described Hawaiian Melicope species by its combination of being large monoecious trees up to 12 m tall with distinct carpels and short-villous ramiflorous inflorescences. There are three other Hawaiian species that usually have ramiflorous cymes arising on stems below the leaves, Stone, also from Kaua'i. The latter two differ with carpels connate and leaves glabrous or with some hairs on midrib (Wagner et al. 1999), and the former, M. ovata, lacks the short-villous peduncles, pedicels, sepals, and petals found on M. stonei. Morphologically, these species have little else in common with M. stonei.
Four specimens of Melicope stonei (Wagner & Wood 6891;Wood 7696;Wood & Aguraiuja 7697;Wood, Query & Kirkpatrick 15101) have been included in phylogenetic analyses of Hawaiian Melicope (Harbaugh et al. 2009;Appelhans et al. 2014b,c) and they all represent paratypes of this new species. The specimens were labeled as M. knudsenii in these studies according to their original conferred determination. Phylogenetic analyses showed that the former section Apocarpa is paraphyletic with respect to the former section Pelea (unpublished results) and that M. stonei forms a clade with the "Apocarpa" species M. adscendens and M. ovata (Fig. 4). The monophyly of this clade is supported by posterior probability (1.00pp) and bootstrap (98bs) values and the three species, of which three to four specimens have been sampled, were resolved as monophyletic entities (Appelhans et al. 2014c;Fig. 4 (Appelhans et al. 2014c;Fig. 4) do not have clear morphological similarities with the new species. While M. stonei is a tall tree, M. adscendens is a sprawling shrub and M. ovata is a shrub or small tree with sprawling branches. Melicope adscendens has considerably smaller leaves 1.5-6.5 × 1-4 cm and does not have a densely tomentose abaxial leaf surface, being minutely puberulent, becoming glabrate (as compared to M. stonei with leaves (5-)8-30 × (4-)6-11 cm with densely tomentose abaxial leaf surface). Melicope ovata has sepals glabrous or sparsely minutely ciliate externally, and petals glabrous externally (Wagner et al. 1999), (as compared to M. stonei with sepals and petals densely short-villous externally).
Morphologically, Melicope stonei is most similar to M. barbigera and the Kaua'i population of M. knudsenii (see above). Melicope knudsenii has been shown to be polyphyletic and the Maui form does not belong to this group (Appelhans et al. 2014c;Fig. 4). As a result, a future publication is now in preparation which will resurrect the Maui form (i.e., M. multiflora Rock) as a species distinct from the Kaua`i M. knudsenii. While M. barbigera and the Kaua'i form of M. knudsenii are resolved as immediate sisters in the phylogenetic analyses, M. stonei is not closely related to them and belongs to another clade of the paraphyletic Apocarpa group (Appelhans et al. 2014c;Fig. 4). It should be noted that the variable abaxial midrib pubescence of M. stonei ranging from villous on the sides to uniform pubescence (Fig. 2E-F) could represent natural