New and resurrected Hawaiian species of pilo (Coprosma, Rubiaceae) from the island of Maui

Abstract Two species of Coprosma (Rubiaceae) J.R.Forst. & G.Forst. are described from the island of Maui of the Hawaiian Archipelago. A newly described taxon, Coprosma cordicarpa J.Cantley, Sporck-Koehler, & M.Chau, sp. nov. is locally common in medium to high elevation dry forests and shrublands of leeward East Maui. The second taxon is resurrected from the synonymy of Coprosma foliosa A.Gray as Coprosma stephanocarpa Hillebr. and occurs in mesic to wet rainforests of both East and West Maui. Both taxa are segregated from Coprosma foliosa, with which they share similar morphological characters. A conspicuous and persistent calyx of the fruit and various floral characters most easily differentiate both taxa from other Hawaiian taxa. The newly described Coprosma cordicarpa is further distinguished from Coprosma stephanocarpa by a central constriction of the fruit with a depressed apex, which gives it a characteristic heart shape. Furthermore, the taxa are largely separated phenologically, ecologically, and geographically. Descriptions, conservation status, and specimens examined for the new species are included.


Introduction
Th ere are more than 110 species in the genus Coprosma J.R. Forst. & G.Forst., which consists of species that are predominantly dioecious and wind pollinated. Species range in habit from trailing woody plants to large trees and produce many various colored fruits (e.g. black, blue, orange, red, yellow, and translucent), which are most often twoseeded drupes. Th e genus is Oceanic in distribution with a primary center of diversity in New Zealand (ca. 55 spp.: Glenny et al. 2010), and secondary centers of diversity in the Hawaiian Islands (13 spp.: Wagner et al. 1999), New Guinea (15 spp.: Garner 2002, Australia (8 spp.: Th ompson 2010) and the Marquesas Islands (6 spp.: Wagner and Lorence 2011). Elsewhere, species are scattered widely across many islands and archipelagos of the Pacifi c Ocean from Borneo to the Juan Fernández Islands, but each island or archipelago has only one or two endemic species. Cantley et al. (2014) indicate from their molecular phylogeny that the Hawaiian Islands were colonized by Coprosma during two independent colonization events: once for the black-fruited C. ernodeoides, and secondly for all orange-fruited species. Th e orangefruited Hawaiian Coprosma taxa-known locally as pilo in the Hawaiian languagewere determined to be most closely related to the six Marquesan species and one (of two) species from Rapa Iti of the Austral Islands. Together, these taxa (from the Hawaiian Islands, Marquesas Islands, and Rapa Iti) were found to be more closely related to taxa in New Zealand than to other species on islands elsewhere in the Pacifi c where Coprosma taxa occur (i.e. Austral Is., Cook Is., Fiji, Kermadec Is., Lord Howe I., Norfolk I., Pitcairn I., Samoa, Society Is., and Vanuatu). Cantley et al. (2014) also determined that Hawaiian taxa were not closely related to Australian or Malesian taxa. Within the Hawaiian Islands, Coprosma taxa occur on all major islands except for Ni'ihau and Kaho'olawe. All taxa are endemic to the archipelago, but some maintain distributions across multiple islands. Th e intra-archipelago relationships among these taxa are not known. No resolution among Hawaiian taxa was recovered by Cantley et al. (2014), which they suggest is because the colonization event to the Hawaiian Islands by the orange-fruited Coprosma ancestor occurred after the emergence of Kaua'i (≈5 Ma). Th erefore, few detectable genetic mutations have since accumulated, which made it diffi cult to resolve recently diverged evolutionary relationships from the methodology that was used.
Species belonging to the genus Coprosma were fi rst formally described in the Hawaiian Islands by Asa Gray in 1858 from material gathered by Nelson on Cook's last voyage to the islands, and by Menzies during Vancouver's voyage (Gray 1858). Th e descriptions of the taxa were brief, but included seven from the Hawaiian Islands. Following this, a number of individuals described additional taxa including: Wawra (1872), Hillebrand (1888), Heller (1896), Léveillé (1911), Rock (1913), and Oliver (1935, 1942. No new species of Coprosma have been described from the Hawaiian Islands since Oliver (1942). Only one comprehensive monograph of the genus was published (Oliver 1935), and therein was provided a thorough discussion of Hawaiian taxa, which highlighted Oliver's dissatisfaction with attempting to fully delineate them with limited material, and without fi eld observations. Th e most recent taxonomic treatment including all Ha-waiian Coprosma taxa was by Wagner et al. (1999). In this treatment, six species and all varieties were sunk into synonymy. Th e resulting treatment details 13 endemic Hawaiian species in total from what was previously more than 20 taxa. Many taxa in Wagner (1999) are described as having a wide range of morphological diversity-such as for C. foliosa A.Gray, C. ochracea W. Oliver, and C. pubens A.Gray. Th ese species occur across multiple islands, whereas single island endemic taxa have much better defi ned morphologies (ex. C. ellpitica W. Oliver of Kaua'i or C. longifolia A. Gray of O'ahu). In some cases, Wagner et al. (1999) note at the end of the taxonomic descriptions that various Hawaiian Coprosma taxa are in need of fi eldwork in order to better understand precise relationships and probable segregate taxa. In the fi eld, Hawaiian Coprosma are notoriously diffi cult to quickly distinguish from one another as diagnostic characters among taxa are minute, and boundaries among species are not always clearly defi ned. Further complicating proper identifi cation is that taxa are often found growing sympatrically, and are thought to hybridize occasionally. Without knowledge of variant morphologies of populations on diff erent islands, it is often diffi cult to accurately identify a particular taxon in the fi eld, even with the most current key to species (J. Cantley, pers. obs.).
Such is the case for currently described C. foliosa, which is a widespread taxon occurring on islands of Kaua'i, O'ahu, Moloka'i, Maui, and Lana'i (Wagner 1999). It is eff ectively replaced on Hawai'i Island by the morphologically similar C. menziesii A.Gray. Coprosma foliosa was fi rst described by Gray (1858), as a shrub with glabrous lanceolate to oblanceolate leaves and obovate to globose fruit with a naked apex. Following this, Hillebrand (1888) described a similar species, C. stephanocarpa Hillebr. from Moloka'i, Maui, and Kaua'i, indicating the species had-as the name suggestsa fruit with a persistent calyx on the apex that is connate, forming a crown-like structure. Th e Kaua'i specimens considered to represent C. stephanocarpa were recognized by Gray (1858) as C. pubens A.Gray var. kauensis A.Gray, and later were elevated to species level by Heller (1896). Hillebrand (1888) indicated the fruit of C. stephanocarpa was globose or obovate with a depressed apex becoming bisulcate, and crowned by the spreading discreet calyx lobes. Rock (1913) then described C. vontempskyi Rock from rainforests above Olinda, Maui, which shared similar morphological characters of Hillebrand's C. stephanocarpa, yet he made no mention of C. stephanocarpa in his description. Oliver (1935) recognized this oversight by Rock and sank C. vontempskyi into C. stephanocarpa as he deemed them indistinguishable. Oliver revised the description of C. stephanocarpa and restricted the fruit morphology to a "drupe [that is] ovoid… [and] crowned by the persistent calyx, 5-6 mm long." However, the new restricted description of C. stephanocarpa failed to the mention Hillebrand's fruit characters describing the fruit as sometimes "obovate with a depressed apex, becoming bisulcate." Th e bisulcate character was never again noted in further Hawaiian Coprosma taxonomic descriptions, including in Wagner et al. (1999) where C. stephanocarpa (plus C. fauriei H. Lév. and C. skottsbergiana W. Oliver) was offi cially lumped into C. foliosa. Oliver (1935) notes that his descriptions of C. stephanocarpa were not fully satisfying to him as he felt unable to disentangle the diverse series, subspecies, forms, and potential hybrids of C. stephanocarpa, particularly on East Maui, with only limited material, which was provided to him from his collaborator Harold St. John at the Bishop Museum in Honolulu.
Th e (re)discovery of bisulcate fruit with a depressed apex and a persistent crownlike calyx from a locally common Coprosma taxon in the Kanaio Natural Area Reserve on leeward East Maui, plus the diffi culty in keying these individuals to the species level, prompted this detailed investigation by the authors. Th e investigation included in-depth herbarium research, as well as fi eldwork to validate fi ndings and to assess the taxon's abundance and distribution on Maui. Th is paper recognizes one new distinct species, C. cordicarpa, and unexpectedly confi rms the need to resurrect C. stephanocarpa from synonymy. Both taxa are segregated from C. foliosa using morphological, ecological, phenological, and geographical lines of evidence. Th is study, plus a concurrent study of a new taxon from Kaua'i (D. Lorence, pers. comm.), increases the total number of endemic Coprosma species in the Hawaiian Islands to 16.

Methods
All measurements given herein are taken from dried herbarium specimens. Field observations were performed in September 2013, September 2014, and May 2015 to assess abundance and to take fi eld notes and digital photos. Seeds of C. cordicarpa were collected from two populations at Kanaio Natural Area Reserve and Auwahi totaling 609 seeds from 32 individual plants. All seeds were deposited for long-term germplasm storage at the Seed Conservation Laboratory at Lyon Arboretum. Measurements are presented in the descriptions as follows: length, then width, each followed by units of measurement (mm or cm). More than 80 specimens (including type specimens) from the BISH herbarium were studied and measured. Validations were also garnered from PTBG specimens. Th e area of occupancy (distribution) for each species was calculated using herbarium collection data and fi eld observations. Th e conservation status is proposed following the IUCN Red List Category criteria (IUCN 2001; www.iucnredlist. org/info/categories_criteria2001). A fi le including measurements and notes taken from herbaria specimens is provided as supplemental data (See Suppl. material 1: Coprosma Morphology Data Matrix).
Phenology. Flowering specimens were collected from August to September except for one individual in March. Field observations of September 2013 and 2014 found that most individuals of the population at Kanaio Natural Area Reserve and Auwahi were fruiting, and only few fl owering. Fruiting specimens were collected across many months, but it is unknown how long fruits were mature on individuals prior to collection.
Distribution. Known only from southern, leeward slopes of East Maui (  vaded habitats with Cenchrus clandestinus. It occurs primarily in open habitat receiving direct sunlight, but was observed in gulches and high elevation forests along the Kaupō Gap Trail (Seana Walsh, pers. comm.). Th e rainfall in the distribution of C. cordicarpa varies from 700 to 1900 mm annually with the highest rainfall occurring from December to January (Giambelluca et al. 2013). Flowering occurs during the dry season, and fruits appear to mature shortly preceding the wettest months, which may represent a germination strategy for this dry habitat taxon.
Etymology. Th e specifi c epithet refers to the heart-shaped fruit, which is a product of the central constriction of the fruit and depressed apex. Th is character is unique among Hawaiian Coprosma taxa.

Coprosma stephanocarpa Hillebr.
Phenology. Most fl owering specimens were collected from December to February and a lesser number from July to August. Specimens from Lihau (West Maui) are only known to fl ower in July. No individuals were fruiting or fl owering in late September 2014 in Makawao Forest Reserve, but immature fruits and fl owers were observed in May 2015. Most fruiting specimens occurred in July, but collections were made across many months.
Distribution. Known from East and West Maui, but apparently more prevalent on East Maui. Th e taxon occurs from approximately 975m to 1700m elevation. On East Maui, it is known from mesic sites from Kīpahulu Valley to Olinda. Collections on West Maui are collected from Lihau and Honokawai.
Ecology. Found in mesic to wet forests and shrublands with both native and non-native plant communities. Occurs primarily as an understory shrub to small tree. Th e rainfall varies dramatically across its distribution and precise collection localities should be geo-referenced to provide an accurate range of precipitation requirements for this taxon's distribution.
Etymology. Th e specifi c epithet refers to the persistent calyx on the fruit apex that looks like a crown (crown in Greek = stephanos) due to its persistence, connation, and irregular dentations. Discussion. When numerous collections of Coprosma foliosa from Maui were run through the most current key to Hawaiian Coprosma (Wagner et al. 1999), it was clear that at least two taxa subsumed under that species merited taxonomic recognition. Both taxa failed to key out, and specimens did not closely match the taxonomic description of C. foliosa or any other species. After multiple fi eld visits, herbarium specimen measurements, and an in-depth literature review, it was concluded that the two C. foliosa segregates, C. cordicarpa and C. stephanocarpa, maintain rather consistent morphologies on leeward East Maui (C. cordicarpa) and mesic areas of East and West Maui (C. stephanocarpa). Th ey can easily be segregated from the variable C. foliosa s.l. found on other islands and eff ectively replace C. foliosa s.l. on East Maui, although at least one form of C. foliosa s.l. is still found on West Maui. Coprosma cordicarpa is most easily distinguished from C. foliosa s.l. by its heart-shaped fruit characters, which include a depressed apex crowned by a persistent connate calyx and the tendency to become bisulcate, particularly when dry. Male individuals of C. cordicarpa are easily diff erentiated as the calyx is nearly double in size (2-4 mm) than that of C. foliosa s.l. (0.25-2 mm), and C. stephanocarpa (0.25-2 mm). Th e male calyx ontogeny of C. cordicarpa is quite striking; the irregularly toothed calyx initially appears to be completely connate (or nearly so) when in bud, but due to expansion of the growing corolla, the calyx is mechanically split (often in two locations) becoming deeply incised, and then brown callus tissue forms. Ecologically, C. cordicarpa is found in a unique habitat niche (dry forest/shrubland) compared to C. foliosa s.l. and C. stephanocarpa. Th e niche requirements of C. cordicarpa should be studied in more detail, but it is clear that the areas where it occurs receive much less precipitation than C. stephanocarpa habitat, which include mesic to wet locations of East and West Maui.
Phenological observations suggest that C. cordicarpa and C. stephanocarpa have different fl owering periods that are primarily non-overlapping. Coprosma cordicarpa has a primary fl owering period in late summer (August to September). Th e fl owering period of C. stephanocarpa is primarily the winter (December to February), with a less pronounced period of fl owering from July to August. Scant information about Hawaiian Coprosma phenology has been published, but C. ochracea and C. rhynchocarpa from Hawai'i Island have a peak fl owering period during early spring months (March to May; Lamoureux 1973), which is diff erent from the summer fl owering C. cordicarpa, and winter fl owering C. stephanocarpa. Phenological diff erences among the evolution of Lord Howe Island species of Coprosma have proven to be evolutionarily signifi cant (Papadopolos et al. 2011), and a similar case could also be true for Hawaiian taxa. However, it should be noted that while most, if not all, taxa of Hawaiian Coprosma have a primary robust fl owering period each year, a small percentage of individuals in any population can occasionally be sporadically fl owering across many diff erent months (J. Cantley, pers. obs.). Th e stochasticity of fl owering times could help explain the presence of occasional hybrids that are thought to exist among many sympatrically occurring Coprosma taxa in Hawai'i.
Th e taxonomic boundaries between Coprosma stephanocarpa and C. foliosa s.l. are less easily defi ned, especially from populations of C. foliosa s.l. occurring on the islands of Moloka'i and Lana'i. However, C. stephanocarpa is here restricted to Maui only, as taxa elsewhere appear to maintain consistent morphological diff erences. On Moloka'i, at least two morphotypes of C. foliosa s.l. exist that are similar to C. stephanocarpa. One of these taxa has smaller fruits that are globose with a naked apex, smaller fl oral characters, and smaller leaves in general, but other vegetative characters (e.g. stipule size & pubescence) are similar to C. stephanocarpa. Th e second Moloka'i C. foliosa s.l. morphotype has broad stipules that are more or less glabrous and ellipsoid to globose fruits with a small persistent crown that is not longer than 0.75 mm in length. Concerning Lana'i specimens, few collections have been made, but these agree in morphology with the former described small-fruited, small-leaved Moloka'i taxon, although much less morphological variation was noted. Fieldwork is needed on both islands to better understand these taxa and their relationship with C. stephanocarpa.
Conclusions. Th e recognition of C. cordicarpa and C. stephanocarpa brings the total number of Coprosma species described in the Hawaiian Islands to 15. A concurrent study of material collected on Kaua'i will increase the total number of taxa described to 16 (D. Lorence, pers. comm.). Ongoing investigation of the C. foliosa s.l. complex on Maui and other islands (Kaua'i, O'ahu, Moloka'i, and Lana'i) is currently being pursued by the authors. Preliminary investigation suggests that perhaps morphology is correlated with geographical location, which may support the need for resurrection of other currently synonymized or novel taxa not discussed in this paper. Moreover, detailed investigations of other currently valid taxa, such as the variable C. pubens and C. ochracea, could reveal cryptic taxa by understanding their diversity in better detail at the population level. Ultimately, it is suggested that a molecular study be undertaken to help shed light on the interesting evolutionary patterns of speciation for this dynamic genus in the Hawaiian Islands.