Melicope oppenheimeri, section Pelea (Rutaceae), a new species from West Maui, Hawaiian Islands: with notes on its ecology, conservation, and phylogenetic placement

Abstract Melicope oppenheimeri K.R. Wood, Appelhans & W.L. Wagner (section Pelea (A. Gray) Hook. f., Rutaceae), a rare endemic tree from West Maui, Hawaiian Islands, is described and illustrated with notes on its ecology, conservation, and phylogenetic placement. The new species differs from Hawaiian congeners by its carpels basally connate 1/5, narrowed into a strongly reflexed beak 10–15 mm long. It also differs in a combination of leaves with 7–10 pair of secondary veins; cymes to 3 cm long; peduncles 5–6.5 mm long; flowers perfect; capsules 4–9 × 40–52 mm; and a densely appressed short-sericeous ovary. Melicope oppenheimeri is known only from an isolated cliff-base plateau in upper Waihe‘e Valley, West Maui. Its discovery brings the number of recognized Melicope J.R. Forst. & G. Forst. species in the Hawaiian Islands to 49. A table is included indicating the conservation status of Hawaiian Melicope and Platydesma H. Mann., which is nested within Melicope sect. Pelea. Melicope oppenheimeri falls into the IUCN Critically Endangered (CR) Red List category.


Introduction
Melicope J.R. Forst. & G. Forst. is the largest genus of the Citrus family (Rutaceae) and consists of ca. 235 species of shrubs and trees (Hartley 2001, Appelhans et al. 2014a. Th e distribution of Melicope 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). Ongoing phylogenetic studies of Melicope and closely related genera indicate the need for revisionary work in this group with several of the related small genera belonging in Melicope in order for it to be monophyletic (Harbaugh et al. 2009, Appelhans et al. 2014b). In the most recent systematic revision by Hartley (2001) Melicope was subdivided into four sections: Lepta (Lour.) T.G. Hartley; Melicope; Pelea (A. Gray) Hook. f.; and Vitifl orae T.G. Hartley. Only section Lepta proved to be a monophyletic group in a recent molecular study (Appelhans et al. 2014b). Th e currently known 48 endemic Hawaiian species are all members of sect. Pelea, which consists of 85 species almost exclusively restricted to the Australasian-Outer Melanesian-Pacifi c region. Within sect. Pelea, only the Hawaiian group proved to be monophyletic (Appelhans et al. 2014c). Th e Hawaiian endemic species all have unifoliolate leaves; plants presumably hermaphroditic or dioecious; carpels that range from being basally connate to fully connate, and with variations in exocarp and endocarp that contrast from glabrous to pubescent. Hartley (2001) inferred that Melicope was present in eastern Gondwanaland before about 96 Ma and states that the Hawaiian species represent a radiation that most likely traces back to a single colonization of the archipelago by a species from sect. Pelea. While Hartley's age estimate of Melicope is doubtful since the oldest fossils of the whole family date to the Late Cretaceous (Knobloch andMai 1986, Gregor 1989) and molecular dating studies estimated its origin in the Oligocene or Miocene (Muellner et al. 2007, Appelhans et al. 2012, his suggestion for a single colonization of the Hawaiian archipelago was supported by molecular phylogenetic analyses (Harbaugh et al. 2009, Appelhans et al. 2014b. Th e most recent molecular phylogenetic studies also indicate that the Hawaiian genus Platydesma H. Mann is nested within Melicope sect. Pelea and that the seven known Marquesan Melicope endemics are a closely related group resultant from two independent colonization events from Hawaiian Melicope (Harbaugh et al. 2009, Appelhans et al. 2014c).

Methods
All measurements and descriptions were taken from dried herbarium specimens or from notes made in the fi eld and are presented in the descriptions as follows: length × width, followed by units of measurement (mm or cm). Diagnosis. Diff ers from Hawaiian congeners by its combination of leaves having 7-10 pair of secondary veins; cymes to 3 cm long; peduncles 5-6.5 mm long; fl owers perfect; carpels basally connate 1/5, narrowed into a strongly refl exed beak 10-15 mm long, capsules 4-9 × 40-52 mm; and ovary appressed densely short-sericeous.
Phenology. To date, Melicope oppenheimeri has been observed with fl ower buds in January and August, with fl owers at anthesis during September, and with fruit during January, February, May, August, September, and November.
Etymology. We are pleased to name this new species in honor of Hank Oppenheimer, botanist with the Maui Nui Plant Extinction Prevention Program, who collected the type specimen and has made many valuable contributions to the understanding and conservation of the Hawaiian fl ora.  Th e following couplets can be inserted into the existing key to Hawaiian Melicope (treated as Pelea) by Stone, Wagner, and Herbst (in Wagner et al. 1999, pp. 1179-1182 (59)  Superb examples of Metrosideros-Cheirodendron montane wet forest dominate above these cliff s in association with windswept wet shrublands and occasional bog communities in and around the locality known as Kaho'olewa Ridge (Wood 1997). At the base of the cliff s, which enclose the southern perimeter of the plateau lie heaps of basalt talus with accumulated substrates which are moderately deep in sections and appear to be fi ne textured brown silty clay.
Th e forests spreading below the plateau are composed of Metrosideros mixed lowland riparian vegetation, which are closed to open in canopy and dissected by deeply   (Wood 1997). Notable observations of native birds in the upper Waihe'e region include nesting seabird colonies of dark-rumped petrels (Pterodroma sandwichensis Ridgeway) along with native forest birds such as 'apapane (Himatione sanguinea Gmelin), and 'amakihi (Chlorodrepanis virens wilsoni Rothschild).
Phylogenetic placement. Melicope oppenheimeri, like all Hawaiian Melicope, falls into section Pelea, which has a distribution ranging from Taiwan, the Philippines, and Borneo eastward to the Hawaiian and Marquesas Islands, and south to New Caledonia. Only Melicope triphylla (Lam.) Merr. is distributed in the Southeast Asian areas mentioned above, and the remainder of sect. Pelea is restricted to New Guinea and Pa-cifi c archipelagos (Hartley 2001). Section Pelea proved to be polyphyletic in molecular phylogenetic analyses, and monophyly can be reached if the New Caledonian species are excluded and the Hawaiian endemic genus Platydesma is included in the section (Appelhans et al. 2014b). Hartley (2001, pp. 31, 139-140) stated that the Hawaiian species mostly resemble the New Caledonian species -especially M. vieillardii -based on several "primitive" characters including bisexual fl owers, persistent sepals and petals, apically acute staminal fi laments, basally connate carpels, glabrous endocarp, and Type A seed attachment, however, a close phylogenetic relationship of the Hawaiian and the New Caledonian species could not be verifi ed (Appelhans et al. 2014b). Th e Hawaiian species of Melicope have been treated under the genus Pelea by Wagner et al. (1990)  Th e closest relatives of M. oppenheimeri could not be determined due to the low genetic variation in the sampled nuclear and plastid markers. We are currently working on resolving phylogenetic relationships of Hawaiian Melicope using Next-generation sequencing.
Morphology and related taxa. Although beaked fruit have evolved in a few species of Melicope belonging to sections Melicope and Vitifl orae (Hartley 2001, p. 19), this character is unique to M. oppenheimeri within sect. Pelea ( Figure 1C, 5B). Beaked fruit have also evolved in Hawaiian Platydesma sect. Cornutia B.C. Stone, which is nested within Melicope sect. Pelea, but which is not an immediate relative of M. oppenheimeri.
Two other morphologically similar Hawaiian Melicope, also with carpels coherent at base include M. molokaiense  also diff ers with leaves having 10-20 pair of secondary veins; cymes ca. 6 cm long; and peduncles 7-38 mm long. Melicope oppenheimeri has leaves with 7-10 pair of secondary veins; cymes ca. 3 cm long; and peduncles 5-6.5 mm long.
Melicope species are generally either exclusively hermaphroditic or dioecious, yet there are a few recorded exceptions (Hartley 2001, p. 10). Although M. oppenheimeri is apparently hermaphroditic, we cannot make a defi nitive statement on the breeding system of this rare narrow endemic, having only six collections for study, and limited fl owering material.
Conservation status. Plant and animal endemics from isolated oceanic islands are often endangered or critically endangered (Kreft et al. 2008, Sakai et al. 2002. Th e ongoing decline of native pollinators (Kearns et al. 1998) and seed dispersers (Milberg and Tyrberg 1993), in combination with other primary extrinsic factors such as invasive non-native plants, predation by introduced vertebrates, loss and fragmentation of natural habitats, and devastation by severe storms, are leading to an increase in extinctions throughout the islands of Oceania (Sakai et al. 2002, Wood 2007, 2012, Kingsford et al. 2009). Other prominent factors such as strict habitat requirements, very low historic population densities and narrow geographic range increase the risk of extinction. (Sakai et al. 2002, Wood 2007, 2015. It is currently unclear how many of the estimated 10,000 native Hawaiian insect species have gone extinct, but at this point in time the Hawaiian Islands have lost 79 of its native bird species and are left with only 32 , Burney et al. 2001, Boyer 2008. Th e authors maintain a checklist of endemic Hawaiian vascular plant taxa that have no known wild individuals remaining. Of the estimated 1191 native vascular plant species in Hawai'i, 130 taxa are now presumed extinct. Evidently 41 of these possible extinctions have occurred in the Hawaiian lobeliads (Campanulaceae), a family renowned for their co-evolution with Hawai'i's unique forest birds, the honeycreepers, in the endemic subfamily Drepanidinae of the Fringillidae or fi nch family (Wood 2014(Wood , 2015. Th e Lamiaceae or mint family falls second in this severe category, with 22 species that are presumed extinct. With two-thirds of the surviving forest bird species in Hawai'i being critically endangered and a continued decline in native arthropods, there is grave concern for the endangered Hawaiian fl ora and for their unique insular relationships with biodiversity as a whole. Even today, little is known about the life cycles, breeding system variations, and habitat preferences found in the Hawaiian fl ora (Sakai et al. 2002, Wood 2015, but it is known that Melicope rely on insects for pollination and birds for dispersal (Hartley 2001). Within Hawaiian Melicope fi ve species are currently presumed extinct, 19 are federally listed as endangered, and with the inclusion of M. oppenheimeri, ten species fall into the Plant Extinction Prevention Program (PEPP) category, meaning there are 50 or fewer individuals remaining (see Table 1). Members of Hawaiian Rutaceae are currently in the process of being evaluated according to IUCN categories and criteria. IUCN Red List Category. When evaluated using the World Conservation Union (IUCN) criteria for endangerment (IUCN 2001), Melicope oppenheimeri 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 numbering system of criteria and subcriteria: CR B1 ab(i,ii,iii,v)+2ab(i,ii,iii,v); C2a(ii); D; which refl ects a severely limited Extent of Occurrence (EOO) and Area of Occupancy (AOO) of less than 1 km 2 and a wild population of only three individuals. It should be noted that seed collections of M. oppenheimeri have been made by Maui PEPP staff during routine monitoring and there is currently a single cultivated individual being grown at the Olinda Rare Plant Facility on East Maui. cal Botanical Garden, the U.S. Fish and Wildlife Service, Th e Hawai'i State Department of Land and Natural Resources, and the Plant Extinction Prevention Program of Hawai'i for their continued focus on conservation. We appreciate the eff orts of the Hawai'i State Division of Forestry and Wildlife and their Olinda Rare Plant Facility on East Maui, especially for the cultivation of Melicope oppenheimeri. Much gratitude to Alice Tangerini for the superb illustration, Timothy Flynn for assistance at the PTBG herbarium, and to Pedro Acevedo-Rodríguez and David Lorence for greatly improving this manuscript.