A new species of Cyanea (Campanulaceae, Lobelioideae), from the Ko‘olau Mountains of O‘ahu, Hawaiian Islands

Abstract Cyanea konahuanuiensis Sporck-Koehler, M. Waite, A.M. Williams, sp. nov., a recently documented, narrowly endemic species from the Hawaiian Island of O‘ahu, is described and illustrated with photographs from the field. The closest likely relatives to the species, current conservation needs, and management future are discussed. It is currently known from 20 mature plants from two subpopulations and is restricted to a drainage below the Kōnāhua-nui summit (K1), the highest summit of the Ko‘olau Mountains, located on Windward O‘ahu. It differs from all other Cyanea species by its combination of densely pubescent leaves, petioles, and flowers; sparsely pubescent to glabrous stems, long calyx lobes, and staminal column being adnate to the corolla.


Introduction
Th e Campanulaceae is a large, diverse, and cosmopolitan plant family with representatives inhabiting a wide range of ecosystems including tropical, subtropical, temperate, and even frigid zones with exceptional diversifi cation in South Africa and Hawai'i (Lammers 2007). One of the most exceptional adaptive radiation events known in the family is the monophyletic lobeliod group in Hawai'i (Givnish et al. 2008). Th e Hawaiian lobelioids are a group of woody eudicots comprised of six genera, Brighamia A. Gray, Clermontia Gaudich., Cyanea Gaudich., Delissea Gaudich., Lobelia L., and Trematolobelia A. Zahlbr. Together they account for roughly ten percent of Hawaiian angiosperm diversity (Wagner et al. 1999(Wagner et al. , 2005 with a total of 128 taxa, 78 of which are currently recognized as Th reatened and Endangered (T&E; USFWS http://www.fws.gov/endangered/).Th e lobelioids in Hawai'i represent the largest adaptive radiation from a single colonization event known from any plant group restricted to an oceanic island chain (Oppenheimer andLorence 2012, Givnish et al. 2008). According to the most current treatment of the Hawaiian Lobelioids (Lammers 2007), Cyanea (including the merger of the genus Rollandia) is the most species-rich genus in the radiation, comprised of 79 currently recognized species (54 T&E). A possible explanation for the impressive speciation in this genus is that the fl eshy fruits are poorly distributed by Hawai'i's native forest birds, which do not typically travel long distances, leading to parallel speciation events on multiple islands (Givnish 2008). Cyanea occurs in mesic to wet forests across the Hawaiian archipelago and includes many taxa with restricted distributions, most of which are single island endemics.
In September 2012, the Kōnāhua-nui summit area of the Ko'olau Mountains on the island of O'ahu was surveyed ( Figure 1). Th e target species was Cyanea humboldtiana (Gaudich.) Lammers, Givnish & Sytsma, a species federally listed as Endangered, and endemic to the Ko'olau Mountains. It was hoped to locate additional individuals to monitor and manage as a part of species recovery eff orts. We summited K1 (the highest of the two peaks of Kōnāhua-nui) and descended into a stream drainage and once near the bottom of the gulch, directly adjacent to the stream, several plants were discovered of a Cyanea with hairy leaves and petioles, glabrous stems, and long, hairy calyx lobes. Th ere were no fl owers present on the plants and only one immature infructescence. Th e specifi c taxon could not be confi rmed in the fi eld and it was decided to take photos and collect a dropped and decaying leaf for further investigation.
Preliminary research in the following weeks consisted of examining the plants using photos and the one fallen, partially decayed leaf collected from the fi eld. After reviewing the current treatments of Cyanea, sharing the photos with local experts, and looking at specimens at the Bishop Museum, it was concluded that the species in question was most likely undescribed. To be certain, fertile specimen was required.
Th ereafter, trips to the remote population were made every two to three months. Th ese subsequent expeditions surveyed the surrounding area and revealed the presence of additional individuals. In June 2013, an automated game camera was installed connected to cellular phone service that transmitted a photo of one of the plants three times per 24 hour period ( Figure 2). Th is camera allowed us to monitor the fl ower development and visit the plants again when we were certain the fl owers would be fully mature.
In addition, type specimens of all of the Hawaiian Lobeliads were examined in the Herbarium Pacifi cum of the Bernice Pauahi Bishop Museum (BISH) collection, with special attention given to Clermontia, Cyanea, Delissea, and the formerly recognized generic group, Rollandia Gaudich. None of the Hawaiian Campanulaceae was a match to the Cyanea under study.
Th ere are several species that share some characteristics with C. konahuanuiensis including: Cyanea crispa Gaudich., Cyanea calycina Gaudich., Cyanea humboldtiana Gaudich., and Cyanea pilosa A. Gray (Table 1). For example, C. crispa, C. calycina, and C. humboldtiana all share a staminal column that is adnate to the corolla tube, similar overall stature and leaf shape, presence of some leaf pubescence (though not to the same degree as C. konahuanuiensis), and similar number of fl owers in each infl orescence (C. konahuanuiensis also shares the characteristic of pendant infl orescences but to a lesser degree than C. humboldtiana). However, they all diff er in the degree of leaf pubescence (C. konahuanuiensis being signifi cantly more hairy), calyx lobe length, and corolla surface characteristics.  Th e Hawai'i Island endemic C. pilosa shares a comparable leaf shape and is similarly pubescent (though dissection scope inspection revealed that hair structure diff ers) to C. konahuanuiensis, but the latter lacks hairy stems and has more abundant hair on both leaf surfaces. Also, fl ower color and calyx lobe length diff er radically, C. pilosa usually having white fl owers and much shorter calyx lobes (2-5 mm long) and C. konahuanuiensis having brilliant purple fl owers. Lastly, unlike C. konahuanuiensis, the staminal column of C. pilosa is not adnate to the corolla tube (Figures 3,4,5,6,7,8 and Table 1).
Because so few individuals of C. konahuanuiensis are known, collections were limited to two fertile vouchers, each including one infl orescence and two leaves. Flowers were also collected from three individual plants and preserved in alcohol for precise fl oral analysis (see Specimens Examined section). In order to ensure limited damage to the population and to further conserve the species, detailed measurements were taken of fi ve, reproductively mature and fl owering, live plants in the wild for most of the descriptive information in this paper. For corolla tube lobe length and width, surface characteristics, and anther length and surface characteristic data from the preserved fl owers were utilized. Seed data are taken from living material deposited at the University of Hawai'i Harold L. Lyon Arboretum micropropagation facility. Selected measurements from the dried holotype specimen are included parenthetically in the description.  (Figure 9).
Distribution  Don, Hedychium gardnerianum Sheppard ex Ker Gawl., Rubus rosifolius Sm., and Setaria palmifolia (J. König) Stapf. Bryophyte species are prevalent and include Distichophyllum freycinetii (Schwägr.) Mitt., Plagiochila difl exa Mont. & Gottsche, and species of Bazzania S. Gray. Th e native arthropod, Megalagrion oahuense Blackburn (a Hawaiian endemic damselfl y) has been observed on C. konahuanuiensis. Soil is of basaltic origin and typical of wet forest sites on O'ahu and the average annual rainfall is approximately 2600 mm (Giambelluca et al. 2013). Th e plants occupy a gulch both at the base and middle of relatively steep slopes which results in direct sunlight exposure occurring for a few hours close to midday and varying seasonally. Plants occur on both northwest and south facing slopes of the gulch, mostly along the banks of intermittent streams, but can also be found several meters from the stream with no apparent preference. Small stem fragments that are detached from plant have been observed to take root, forming new clones.
Phenology. Cyanea konahuanuiensis has been observed fl owering from June-August with fruit developing from August-October. All observed fruits have aborted, been eaten, or decomposed before maturity. Th e lifespan and time to maturity of the species is unknown. Immature, nearly aborted fruits have been collected when all others had aborted. Fruits have been submitted to the Lyon Arboretum Micropropaga- tion lab where some of the seeds have germinated and it is interesting to note that the seedlings have densely pubescent leaves (Figure 3).
Etymology. Th e specifi c name pays homage to the twin-peaked (946 m and 960 m) Kōnāhua-nui Pu'u (summit), the tallest peaks in the Ko'olau Mountain range on windward (east) O'ahu. Lit. Large fat innards (Pukui et al. 1974), + Latin suffi x -ensis, indicating a place of origin or belonging. "In one story a giant threw his great testicles (Kona hua nui) at a woman who escaped him." (Pukui et al. 1974). Kōnāhuanui has signifi cance not only because it is the highest peak in the Ko'olau Range, but because the summit area is a largely intact native ecosystem in relative close proximity to Honolulu, the largest city in the State of Hawai'i. To our knowledge, there has never before been a plant species named after this beautiful and biologically important locality. After seeking counsel with Hawaiian cultural practitioners Kaua Neumann and Kīhei Nahale-a (pers. comm. 2014), it is proposed to give the species a Hawaiian name of Hāhā mili'ohu, meaning "Th e Cyanea that is caressed by the mist".
Conservation. Cyanea konahuanuiensis is a critically imperiled species (see Conservation status below) due to its low population numbers and exceptionally narrow endemism. Some of the conservation obstacles to overcome include probable loss of most, if not all, of its native avian pollinators and dispersers, and suspected herbivory by introduced taxa such as rats, terrestrial gastropod mollusks (slugs), and feral pigs (Sus scrofa). Invasive plant species are becoming increasingly common even in relatively hard to access sites along and near mountain summits in Hawai'i. Species such as Ageratina adenophora, Clidemia hirta, Erigeron karvinskianus, Hedychium gardnerianum, Rubus rosifolius and Setaria palmifolia are competing with C. konahuanuiensis and other native species for space and resources. It is conceivable that stochastic events such as landslides, hurricanes, and fl ash-fl ooding could obliterate the majority or all of the currently known plants with a single event. Approximately 20 mature plants and several immature plants have been observed in total. Plants that were observed ranged from seedlings to reproductively mature individuals. Seedlings are scarce, however, which suggests that the population may be declining.
Th e Hawai'i DLNR, Division of Forestry and Wildlife (DOFAW) has largely funded this research by providing staff time to further investigate this species. Th e Hawai'i Plant Extinction Prevention (PEP) Program focuses on conserving and restoring plants with less than 50 known wild individuals. Because C. konahuanuiensis falls within that threshold, O'ahu PEP is working closely with DOFAW staff to protect this critically rare taxon. Th e fi rst goal of the PEP Program is to secure seeds or propagules from each individual mature plant for ex situ germplasm banking. Th e long-term goal for the PEP Program and DOFAW will be to collaborate in the eff ort to grow and out- plant nursery stock into appropriate restoration sites. Currently there are no protected (fenced) areas in similar habitat with comparable elevation, rainfall, humidity, and species composition on O'ahu. Our recommendation is that additional fenced outplanting sites be established in appropriate areas of the Ko'olau Mountains in order to establish multiple populations of this species. Th e authors emphasize the importance of prioritizing staff time to carry out further vegetation surveys in areas that have not been explored in recent history as this exciting new fi nd shows that even seemingly well botanized areas in Hawai'i may yet yield new discoveries.
In October 2013, immature fruits from two plants were collected and have since germinated at the UH Harold L. Lyon Arboretum after being directly sown on an agar medium. Th is is valuable information since at this time all observed fruits seem to be aborting prior to maturity. We recommend collecting immature fruit (or mature fruit if possible) from all reproductive individuals during future fruiting seasons in order to secure genetic representation from all reproductively mature individuals in ex situ collections. Th e use of cellular phone-connected game cameras is recommended for monitoring of rare plants in remote locations. Th is novel use of game camera technology saved time and resources, optimizing the timing of visits and increasing the likelihood of making successful and representative observations required for the species description and fruit collections. Th is rapidly improving technology could have many positive impacts on monitoring rare plants for fl ower development, fruit development, herbivory impacts, and the eff ects of various seasonal events. Discussion. For over a century the taxa that currently comprise the genus Cyanea were recognized as two separate genera, Cyanea and Rollandia. Th e genus Rollandia was distinguished from Cyanea based on the single character of staminal column adnation to corolla in the former (Gaudichaud-Beaupré 1844; Hillebrand 1888 ;Lammers 1990;Rock 1919). Phylogenetic investigations of molecular data revealed that the taxa of Rollandia are embedded within the genus Cyanea (Lammers, 1993). Together with two species of Cyanea (C. acuminata and C. grimesiana), they form a clade referred to as the "acuminata clade" (Givnish et al. 1995). Cyanea konahuanuiensis most likely  belongs in this clade based on the staminal column being adnate to the corolla tube. It is noteworthy to mention that C. konahuanuiensis shares close geographic proximity to several taxa of the acuminata clade. Eight out of the nine previously recognized Rollandia taxa from this clade are endemic to O'ahu (the ninth taxon, C. parvifolia C. N. Forbes is only known from the type specimen collected on Kaua'i) and six out of those eight are even more restricted, occurring only in the Ko'olau Range. Of those six, one taxon (C. humboldtiana) is known to occur on the summit ridges near C. konahuanuiensis.

Key to species
Th ere is currently no published taxonomic key for Cyanea that includes the merger of the Rollandia clade. Th e following couplets can be inserted into the most recent revision of Rollandia (Lammers 1990in Wagner et al. 1990) to separate C. konahuanuiensis from C. humboldtiana.

Conservation status
Using the IUCN Red List criteria (IUCN 2012), Cyanea konahuanuiensis falls into the Critically Endangered (CR) category, a rank given to species facing the highest threat of extinction in the wild, fi tting the following criteria defi ned by IUCN Red List: B1) Extent of occurrence estimated to be < 100 km 2 and D) number of mature individuals < 50. Th is species is currently known from only one population in two sub-gulches of a single stream drainage. It is our recommendation that C. konahuanuiensis be evaluated by the United States Fish and Wildlife Service to be added as a Candidate for listing as Endangered under the Endangered Species Act of 1973. A recovery plan should be written and implemented.
Matthew J. Keir, Timothy I. Kroessig, Joel Q. C. Lau, Cliff ord W. Morden, Kīhei Nahale-a, Kaua Neumann, Douglas O. Okamoto, Hank L. Oppenheimer, Richard J. Pender, Tom A. Ranker, Lara S. Reynolds, and Lauren A. Weisenberger for botanical expertise, assistance, encouragement, and thought-provoking discussions. Th ank you to Yoshiko Akashi for making the species distribution map and thanks to Chris A. Johns for making a special trip to take descriptive photos. We thank Barbara H. Kennedy, the collection manager of the Bernice P. Bishop Museum herbarium (BISH) for access to specimens and assistance with preparing the Type specimens for this study and we thank the Lyon Arboretum for assistance with managing propagules that were obtained during the course of this study. Th is manuscript was greatly improved by suggestions from David H. Lorence (PTBG) who also provided encouragement and mentorship throughout the process from investigating the plants to writing the paper. Vicki A. Funk and Warren L. Wagner (US) are thanked for valuable suggestions on the manuscript.