Four new species of Cyrtandra (Gesneriaceae) from the South Pacific islands of Fiji

Abstract During fieldwork in Fiji, four new species of Cyrtandra (Gesneriaceae) were discovered and are described herein: C. gregoryi M.A.Johnson, sp. nov., C. hispida M.A.Johnson, sp. nov., C. longifructosa M.A.Johnson, sp. nov., and C. waisaliensis M.A.Johnson, sp. nov. The addition of four new species brings the current number of Fijian Cyrtandra to 41 endemic species. Two of the four species are known from only a single locality, and all of the new species are likely endangered or critically endangered. Continued fieldwork in the islands of Fiji is warranted in order to better understand current species distributions and population demographics of Cyrtandra in this species-rich and still poorly explored region of the South Pacific.


Introduction
The Southeast Asian-Pacific genus Cyrtandra J.R. Forster & G. Forster (Gesneriaceae) comprises ca. 800 species, with centers of diversity in Borneo, New Guinea, the Philippines, and the Pacific islands (Atkins et al. 2013). Species of Cyrtandra are restricted to the understory of rainforests and exhibit high diversity in habit (shrubs, small trees, herbs, or vines), flower color (white, yellow, purple, pink, red), and fruit morphology (indehiscent capsules or berries). In the Pacific, Cyrtandra is one of the largest and most widely distributed genera of flowering plants, with ca. 175 species occurring across a region that extends from the Solomon Islands, east to the Marquesas, and north to the Hawaiian Islands. The vast majority of species are single island endemics, with the entire range of a species often being restricted to a single valley or mountain region.
Recent phylogenetic studies suggest that Cyrtandra evolved in Southeast Asia, followed by dispersal to the Pacific islands (Clark et al. 2008(Clark et al. , 2009Johnson et al. 2017), likely via frugivorous birds. The Pacific clade appears to have originated in Fiji ca. 9 mya, with subsequent founder events from Fiji to archipelagos both near (e.g., Samoa) and far (e.g., the Hawaiian Islands) resulting in the current distribution of Cyrtandra across the Pacific (Johnson et al. 2017). While Fiji hosts the second highest number of endemic Cyrtandra species in the Pacific (second only to the Hawaiian Islands, with 60 spp.), only limited research has been conducted on the genus in this diverse region. Gillett (1967) conducted the only thorough taxonomic review of Fijian Cyrtandra to date, with his treatment dividing 35 species among six informal groups. However, upon further study of Cyrtandra across the South Pacific, Gillett (1973) acknowledged that these groupings were largely inadequate and that a more accurate treatment of Fijian Cyrtandra would require considerably more fieldwork. Smith's treatment of Cyrtandra in the Flora of Fiji (1991) was largely drawn from Gillett (1967), although two species were restored from synonymy bringing the number of recognized species to 37.
Botanical explorations in Fiji from 1840-1953 resulted in the description of all 37 currently recognized species of Fijian Cyrtandra. Since the 1960s, relatively few collections of Fijian Cyrtandra have been made. In the 1970s, a number of new roads were built in Fiji to accommodate the expanding agricultural industry, vastly increasing accessibility into remote regions (e.g., central Vanua Levu, eastern Taveuni; Lin 2012). In 2014 and 2015, I was able to undertake extensive fieldwork across the four largest Fijian islands (Viti Levu, Vanua Levu, Taveuni, and Kadavu), focusing on regions that have been poorly explored in the past. This work resulted in the discovery of four new species that are here described and illustrated.

Methods
Diagnoses of the new species are based on morphological traits and DNA sequence variation in a phylogenetic context. Morphological measurements were taken from live plants in the field, as many characters essential to Cyrtandra identification are lost upon drying (particularly floral characters). Information was also taken from liquid fixativepreserved flowers and fruit, as well as from digital photographs. To ensure accurate identification, comparisons were made with all existing species descriptions (Gillett 1967, Smith 1991 as well as with herbarium specimens housed at BISH, GH, K, NY, PTBG, RSA, SUVA, UC, and US. Samples of all four new species were included in a recent molecular phylogeny of the Pacific clade of Cyrtandra, which is based on five loci and a dense taxon sampling of 121 species (including 30 Fijian species; Johnson et al. 2017). This study provided the information necessary to identify the closest relatives of each of the new species based on shared phylogenetic history. Conservation status was assessed in accordance with IUCN Red List Category criteria (IUCN Standards and Petitions Subcommittee 2016).
Phenology. Individuals of this species were in flower when collected in August and November, with fruits likely becoming mature ca. 5-6 months later.
Etymology. I am pleased to name this new species after my husband, Gregory Hora, to whom I am most grateful for his assistance in collecting this and other species across Fiji. Phylogenetic placement. A recent phylogenetic study by Johnson et al. (2017) placed Cyrtandra gregoryi sister to C. ciliata with strong support (Fig. 4). Cyrtandra ciliata is endemic to the Fijian islands of Vanua Levu, Taveuni, and Koro from 300-1100 m elevation. These species share a cymose inflorescence and glabrous to glabrate leaves. The key provided in the taxonomic treatment by Gillett (1967) would place C. gregoryi in species Group 5 based on the branching cyme inflorescence, non-woody inflorescence axis, deciduous calyx, styles and/or stamens being exserted from the corolla tube, and stamens 8-12 mm long.
Conservation status. Proposed IUCN Red List Category: Endangered (EN) based on an estimated area of occupancy of < 500 km 2 (criterion B2), known to exist at no more than five locations (B2a), inferred decline in area of occupancy (B2bii), decline in area, extent, and/or quality of habitat (B2biii), decline in number of mature individuals (B2bv), and population size estimated to number fewer than 250 mature individuals (D).
Although Bouma National Heritage Park protects ca. 15,000 hectares of intact rainforest on eastern Taveuni, indigenous Fijians are permitted to clear land near villages for agriculture. As a result, large areas of coastal forest are increasingly being cleared for dalo (taro, Colocasia esculenta (L.) Schott) and yaqona (kava, Piper methysticum L.f.), the two main export crops of Taveuni. Given that C. gregoryi appears to be restricted to low-elevation forests, it is highly likely that individuals of this species were extirpated during clearing for human settlements and agriculture. Invasive plants are also a major threat to native plants in the area; mile-a-minute vine (kudzu, Pueraria lobata (Willd.) Ohwi) may be particularly problematic as it rapidly grows over trees and shrubs and can Notes. Eight individuals of C. gregoryi were recorded during field surveys along the Lavena coastal trail, with all of these being reproductive. Additional field surveys in the area are likely to reveal more individuals. No other Cyrtandra species were observed growing sympatrically with C. gregoryi in the Lavena region, although C. tempestii Horne ex. C.B. Clarke was collected 0.64 km to the SE. An additional collection was made of a single individual of C. gregoryi near the Tavoro Falls in Bouma National Heritage Park, an area that also hosts C. ciliata. Diagnosis. Cyrtandra hispida is morphologically similar to C. waisaliensis sp. nov., but differs in its axillary cyme inflorescence of 2-4 flowers (vs. cauliflorous cyme inflorescence of 2-8 flowers), green bracts and bracteoles 5-9 mm long (vs. white bracts and bracteoles 3-10 mm long), calyx pale green and 29-31 mm long (vs. calyx white and 23-37 mm long), corolla tube 31-34 mm long (vs. corolla tube 23-27 mm long), and staminodes 2 (vs. staminodes 3).
Etymology. This species is named for the stiff trichomes that cover the stems, leaves, and inflorescences.
Phylogenetic placement. A recent phylogenetic study by Johnson et al. (2017) placed Cyrtandra hispida in a weakly supported clade with four other species (C. cephalophora Gillespie, C. waisaliensis sp. nov., C. dolichocarpa A. Gray, C. longifructosa sp. nov.) that are recorded from the Fijian Islands of Viti Levu (C. cephalophora) and/or Vanua Levu (C. cephalophora, C. waisaliensis, C. dolichocarpa, C. longifructosa) (Fig.  4). Within this clade, C. hispida is most similar morphologically to C. waisaliensis (sp. nov., described below). Both species have large bilabiate corollas, persistent cylindrical calyces, ovate to obovate leaves, and a dense indument of long stiff trichomes covering the stems, leaves, and inflorescences. Additional sampling of species and of nuclear genic regions may be required to confidently place C. hispida with its closest relatives.
The key provided in the taxonomic treatment by Gillett (1967) would place C. hispida in species Group 2 based on the branching cyme inflorescence and the persistent calyx.
Conservation status. Proposed IUCN Red List Category: Endangered (EN) based on an estimated area of occupancy of < 500 km 2 (criterion B2), known to exist at no more than five locations (B2a), projected decline in extent of occurrence (B2bi), area of occupancy (B2bii), and area, extent, and/or quality of habitat (B2biii). Although the two areas where this species has been collected are within the Taveuni Forest Reserve, the forest above Somosomo Village is currently being cleared for a hydropower dam (M. Johnson, pers. obs.). Additional threats include mining for gold and copper, invasion by plant species such as Clidemia hirta (L.) D. Don (Koster's curse; M. Johnson, pers. obs), and damage from tropical cyclones. Further surveys are needed in the upland forests of Taveuni (which remain relatively unexplored, exceptions being the area surrounding Lake Tagimoucia and the road to Des Voeux Peak) to determine the extent of occurrence and population demographics of C. hispida.
Additional specimens examined. FIJI. Taveuni Notes. Cyrtandra hispida was observed to grow sympatrically with three species on Des Voeux Peak (C. leucantha A.C. Sm., C. ciliata, and Cyrtandra sp.) and three species in the mountains above Somosomo (C. leucantha, C. ciliata, C. taviunensis Gillespie). Several individuals were observed that appeared to be of hybrid origin in these populations, with the widespread and common C. ciliata inferred as one of the parents based on similar floral morphology. While the observation of ongoing hybridization in these populations suggests the possibility of C. hispida being of hybrid origin, none of the sympatric species have morphological characters similar to C. hispida. Furthermore, C. hispida is placed in a clade of species that are endemic to the neighboring islands of Vanua Levu and Viti Levu, and does not appear to be closely related to species endemic to Taveuni. Diagnosis. This species is closely related to C. dolichocarpa (Fig. 8), but differs in its glabrous elliptic-ovate leaves (vs. moderately pubescent lanceolate-ovate leaves), blades up to 22 × 9 cm (vs. blades up to 17 × 7 cm), petioles 3-9 cm long (vs. petioles 1-4 cm long), deciduous lanceolate bracts (vs. persistent ovate bracts), peduncles 2-4 mm long (vs. 5-10 mm long), pedicels 11-18 mm long (vs. 21-27 mm long), deciduous beaked calyx (vs. persistent cylindrical calyx), and corolla tube 23-29 mm long (vs. corolla tube 36-55 mm long).
Phenology. Individuals of this species had flowers, immature fruits, and mature fruits when collected in July.
Etymology. Named for the elongate cylindrical fruits, one of the diagnostic characteristics of this species.
Phylogenetic placement. The phylogenetic study by Johnson et al. (2017) placed Cyrtandra longifructosa as sister to C. dolichocarpa (endemic to Vanua Levu and Rabi, Fiji) with strong support (Fig. 4). These species both have large bilabiate corollas and elongate cylindrical berries. The key provided in the taxonomic treatment by Gillett (1967) would place C. longifructosa in species Group 3 based on the branching cyme inflorescence, non-woody inflorescence axis, deciduous calyx, inserted anthers and styles, and calyx lobes about the same length as the calyx tube.
Conservation status. Proposed IUCN Red List Category: Critically Endangered (CR): based on an estimated area of occupancy of < 10 km 2 (criterion B2), known to exist only at a single location (B2a), projected decline in extent of occurrence (B2bi), area of occupancy (B2bii), and area, extent, and/or quality of habitat (B2biii). This species is only known from one locality in the central mountains of Vanua Levu, warranting additional surveys in areas of Vanua Levu with intact rainforest (e.g., Waisali, the Natewa Peninsula) to determine the full extent of occurrence and population demographics of C. longifructosa. Regions with suitable rainforest habitat on Vanua Levu are threatened by logging, mining for bauxite and gold, invasive plant species such as Clidemia hirta (Koster's curse; M. Johnson, pers. obs.), and tropical cyclones. Notes. The population of C. longifructosa was observed to contain ca. 20 individuals, many of which were reproductive. No other Cyrtandra species were observed growing in the immediate vicinity, although the closely related species C. dolichocarpa, C. waisaliensis, and C. cephalophora were all collected 2.25 km W of the C. longifructosa population described here. Diagnosis. The new species is closely related to C. dolichocarpa and C. longifructosa (Fig. 8), but differs in its dense bristly pubescence on the young stems, leaves, petioles, and inflorescences (vs. moderate appressed pubescence on C. dolichocarpa; vs. glabrous on C. longifructosa), cauliflorous inflorescences (vs. axillary inflorescences in both C. dolichocarpa and C. longifructosa), persistent foliaceous ovate white bracts to 10 mm long (vs. non-foliaceous green bracts to 5 mm long in C. dolichocarpa; vs. deciduous non-foliaceous lanceolate green bracts to 8 mm long in C. longifructosa), and multiple persistent foliaceous white bracteoles (vs. single deciduous non-foliaceous green bracteoles in C. dolichocarpa; vs. bracteoles absent in C. longifructosa).
Distribution and ecology. Cyrtandra waisaliensis is known only from one population in the Waisali Forest Reserve on Vanua Levu, Fiji at 300-360 m elevation, occurring in the dense forest understory alongside a creek (Fig. 9).
Phenology. Flowers and immature fruits were observed in July, with fruits likely becoming mature ca. 5-6 months later (December-January).
Etymology. The new species is named after the area of Vanua Levu where it was collected, Waisali Forest Reserve.
Phylogenetic placement. A recent phylogenetic study by Johnson et al. (2017) supported the placement of Cyrtandra waisaliensis as sister to C. longifructosa (endemic to Vanua Levu) and C. dolichocarpa (endemic to Vanua Levu and Rabi; Fig. 4). These species all have large bilabiate corollas, and both C. dolichocarpa and C. longifructosa have elongate cylindrical white fruits. However, C. waisaliensis is also morphologically similar to C. hispida; these species share bilabiate corollas, persistent cylindrical caly-ces, and a dense indument of stiff uniseriate trichomes. Cyrtandra hispida is currently placed in a polytomy with C. cephalophora and the clade comprising C. waisaliensis, C. longifructosa, and C. dolichocarpa. The key provided in the taxonomic treatment by Gillett (1967) would place C. waisaliensis in species Group 2, based on the branching cyme inflorescence and the persistent calyx.
Conservation status. Proposed IUCN Red List Category: Critically Endangered (CR) based on an estimated area of occupancy of < 10 km 2 (criterion B2), known to exist at only a single location (B2a), projected decline in extent of occurrence (B2bi), area of occupancy (B2bii), and area, extent, and/or quality of habitat (B2biii). This species is only known from one locality in the central mountains of Vanua Levu, warranting additional surveys in areas of Vanua Levu with intact rainforest (e.g., Waisali, the Natewa Peninsula) to determine the full extent of occurrence and population demographics of C. waisaliensis. Regions with suitable rainforest habitat on Vanua Levu are threatened by logging, mining for bauxite and gold, invasive plant species such as Notes. The observed population of C. waisaliensis was comprised of ca. 20 individuals, many of which were reproductive. A single individual appeared to be of hybrid origin, with the putative parents being C. waisaliensis and C. cephalophora based on morphological characters intermediate between these two species.

Conclusions
The recognition of C. gregoryi, C. hispida, C. longifructosa, and C. waisaliensis brings the new total of Fijian Cyrtandra species to 41. The four new species of Cyrtandra described here demonstrate that the islands of Fiji remain poorly explored botanically, at least in some regions. Of the 28 Fijian Cyrtandra species collected during field expeditions in 2014 and 2015, four of these were new to science. An additional four Cyrtandra species could not be keyed out to any of the existing species due to a lack of reproductive material. However, with further field study it is possible that these, along with other future collections, may be identified as new species.
being an excellent field assistant and for providing endless encouragement and moral support. This work would not have been possible without the kind peoples of Fiji, who offered their assistance, expertise and hospitality. The following herbaria graciously allowed the use of their collections for study: BISH, GH, K, NY, RSA, SUVA, UC, US, and WU. John Game provided collection information and photographs of Cyrtandra gregoryi for study. Funding for this project was provided by the following: Rancho Santa