Revision of Cyrtandra (Gesneriaceae) in the Marquesas Islands

Abstract During the preparation of the Vascular Flora of the Marquesas Islands three new species of Cyrtandra (Gesneriaceae) have come to light and are described herein: C. uapouensis W. L. Wagner & Lorence, C. uahukaensis W. L. Wagner & Lorence, and C. kenwoodii W. L. Wagner & A. J. Wagner. Amended descriptions of the eight previously described Marquesan species are also provided as well as a key to the species. With the description of these the new species Cyrtandra in the Marquesas Islands consists of 11 species, six of which have been included in recent molecular phylogenetic studies of Pacific Cyrtandra, and appear to have arisen from one original introduction. If the other five species are members of this Marquesas clade then Cyrtandra would represent the largest lineage of Marquesas vascular plants. Psychotria is largest genus in the Marquesas Islands with 13 species, but is thought to consist of three separate lineages.


Introduction
Cyrtandra J.R. Forster & G.Forster (Gesneriaceae) is a genus of about 650 species with a paleotropical distribution from Southeast Asia and throughout the Pacifi c islands (Atkins et al. in press). Cyrtandra represents approximately 15-20% of the species within the family Gesneriaceae, and is a major component of the Old World members of the family, which are members of subfamily Cyrtandroideae Endlicher (Burtt and Wiehler 1995). Th e greatest concentration of species is in the Malesian region where 450 to 600 species occur (Atkins et al. in press). Cyrtandra species form a conspicuous component of the understory in forests across this vast region. Although the genus is readily dispersed, occurring on virtually all archipelagoes across the Pacifi c islands to the remote Hawaiian Islands, most species are local endemics, with distributions on one island or occasionally on several within a single archipelago. Recent phylogenetic studies of Cyrtandra (Burtt 2001;Cronk et al. 2005;Clark et al. 2008Clark et al. , 2009) support a Southeast Asian origin of the genus, with subsequent dispersal and diversifi cation throughout the Pacifi c. Th ese studies identify a single strongly supported Pacifi c oceanic island clade that dates back ±22 million years (Clark et al. 2009). Brown (1935) described the fi rst species of Cyrtandra from the Marquesas Islands in his Gesneriaceae treatment for the Flora of Southeastern Polynesia . In the treatment he recognized four species ( C. feaniana, C. ootensis, C. nukuhivensis, and C. toviana ), all currently recognized here, but both C. ootensis and C. nukuhivensis with modifi ed delimitations. Brown also described a fi fth species, C. jonesii , but placed it in a new genus, Cyrtandroidea , which he erroneously believed to be a member of the Campanulaceae. He mentioned the stamens and style as features that place this plant with otherwise clear features of a Cyrtandra in the Campanulaceae. Gillett (1973) provided an updated revision of the Marquesas species as part of a reconsideration of the south Pacifi c species. He recognized the same fi ve species as Brown and made the combination for Cyrtandroidea jonesii to bring it properly into the genus as Cytrandra jonesii . Fosberg and Sachet (1981) in their revision of Marquesan Cyrtandra maintained all fi ve species. Th ey also added three more species revealed by then recent collecting ( C. tahuatensis, C. revoluta ) and by a new interpretation of collections from Nuku Hiva considered by Gillett to represent C. jonesii (now C. thibaultii ) . Collecting in the Marquesas Islands intensifi ed greatly with the initiation of the current Vascular Flora of the Marquesas Islands project under the direction of Warren L. Wagner and David H. Lorence (Lorence and Wagner 2011;Wagner and Lorence 1997) resulting in discovery of two additional species ( C. uahukaensis, C. kenwoodii ) and a reinterpretation of C. nukuhivensis to exclude the Ua Pou populations as C. uapouensis , bringing the total to 11 species in the Marquesas Islands (Table 1).
Th e Marquesas Island species form a weakly supported clade in the recent maximum likelihood molecular analyses (Clark et al. 2009) with six of the 11 species sampled. Figure 1 presents a portion of the overall tree with the Marquesas species and the sister group to them from Clark et al. (2009). Th e Marquesas species are divided into two major strongly supported clades with one outlier, C. kenwoodii from Ua Pou, that is unplaced in a polytomy with the other two clades. Th e two primary clades in the molecular analysis are corroborated by morphology: species with calyx divided nearly to the base forming one clade (with all three species sampled, C. feaniana, C. ootensis, and C. tahuatensis ), and the species with plicate calyx, which are divided less than ¾ of their length forming the second clade (with only C. jonesii and C. thibaultii sampled). Within the divided calyx clade there are three samples of C. tahuatensis . Th ey do not form a clade but rather the two samples from Tahuata form a clade sister to a polytomy of the Fatu Hiva sample and the single samples of the other two species. Several of the unique Marquesas species were not included, especially the peltate-leaved C. toviana and the revolute-leaved C. revoluta , in the analyses so that a conclusion of a single introduction for all of the species cannot be substantiated until there has been further sampling and perhaps more variable sequence data added since support for some parts of the clade are not robust (Clark et al. 2009). Th e plicate calyx clade occurs on the older islands of the Northern Marquesas group (Nuku Hiva, Ua Huka, and Ua Pou) while the divided calyx clade occurs primarily on the younger islands of the southern group (Hiva Oa, Tahuata, and Fatu Hiva)(see Fig. 2 for Map of the the Marquesas Islands) . Th ere are a few collections of the divided calyx clade from the older islands, all of which were collected by the Pacifi c Entomological Survey in 1929-1930. If the  locality information on the labels of these collections is correct, the species of the divided calyx clade appear to no longer occur on the older islands. When evaluated using the IUCN Red list categories and criteria for threatened species version 3.1 (IUCN 2001, see also http://www.iucnredlist.org/static/categories_cri-teria_3_1), all 11 of the Marquesan species of Cyrtandra fall into the Endangered (EN) or Critically Endangered (CR) categories, which designate species facing the highest risk of extinction in the wild. Marquesan species of Cyrtandra meet the IUCN criteria by having known ranges less than 100 km 2 , an area of occupancy of less than 10 km 2 , and continuing decline in the quality of habitat across the Marquesas Islands (Florence and Lorence 1997;Mueller-Dombois and Fosberg 1998;Meyer and Salvat 2009). All measurements given herein are taken from dried herbarium specimens, although certain features such as shapes were supplemented with information from alcohol-preserved fl owers and fruits, fi eld notes, and color slides or digital photos. Measurements are presented in the descriptions as follows: length × width, followed by units of measurement (mm or cm). Specimens from the following herbaria were studied: AD, BISH, BKL, CBG, CHR, E, HAST, K, L, MO, MPU, NSW, NY, P, PAP, PTBG, S, UC, US, and WU). Many of the Marquesas Cyrtandra species are very narrowly distributed so distribution maps would not be especially useful so we provide here ( Fig. 2) a map of the Marquesas Islands to show the islands and their relationship to one another.
Distribution. Marquesas Islands, endemic to Ua Huka, scattered in Hitikau area to Vaikivi summit and drainage, from 500 to 870 m. One collection (Mumford & Adamson 561, BISH) made in 1929 is from Nuku Hiva, but it is possible that the locality on the label is incorrect and the plant was actually collected on Ua Huka, where Adamson was for four days in October 1929 (N. Evenhuis, pers. comm. May 2013).
Conservation Status. IUCN Red List Category: Endangered EN B1ab (i,ii,iii) + 2 ab (i,ii,iii). B2: total area of occupancy less than 5000 km 2 (ca. 445 km 2 ). B1a, severely fragmented; B1b (i-iii), habitat continuing decline inferred. Th e suitable habitat for Cyrtandra thibaultii on Nuku Hiva (ca. 340 km 2 ) and Ua Pou (ca. 105 km 2 ), is restricted to mountain slopes and summits, indicated as an endangered environment that is threatened by human activity (deforestation and fi re), feral animals, and invasive plants, reducing the extent of the forest (Florence and Lorence 1997;Mueller-Dombois and Fosberg 1998;Meyer and Salvat 2009  Discussion. Th e sample used (Wood 10428) in the molecular study by Clark et al. (2009) was identifi ed as C. nukuhivensis , but during this taxonomic revision it was re-identifi ed as the closely related C. thilbaultii . Description. Shrubs 1-2 m tall; stems apparently few. Leaves opposite, borne on upper 2-5 nodes, broadly elliptic, 18-26 × 7-10 cm, lower surface densely ferruginous appressed pubescent, upper surface glabrate, irregularly dentate, the teeth variable in size, petiole 5 -6.5 cm, ferruginous appressed to spreading pubescent. Flowers in cymes arising in the upper leaf axils, apparently 1-3 fl owered, peduncle 0-2 mm, ca. 1-2 mm in diameter, pedicels up to 6 mm; calyx cylindrical-ellipsoid, white, plicate; corolla much longer than calyx; style up to 10 mm, fl ower parts otherwise unknown. Partly mature berries up to 14 mm long.
Etymology. Th e specifi c epithet refers to the island of Ua Huka where the only known populations occur.
Conservation status. IUCN Red List Category: Critically Endangered CR B2a + 2b (i, ii, iii). B2: total area of occupancy less than 10 km 2 (ca. 5 km 2 ). B2a, a single population known; b (i-iii), habitat continuing decline inferred. Th e suitable habitat for Cyrtandra uahukaensis on Ua Huka (ca. 83 km 2 ) is indicated as an endangered environment, threatened feral animals, and invasive plants, reducing the extent of the forest (Florence and Discussion. Little is known about this species as it has been collected only four times. None of the collections were preserved with any fl owers, only young fruit. Cyrtandra uahukaensis is characterized by the densely pubescent leaves and condensed infl orescences. It grows in the same area as C. jonesii and appears to be closely related.
Ecology. Cyrtandra uapouensis is known only in Metrosideros collina -Weinmannia marquesana wet forest with diverse fern understory and other shrubs and trees such as species of Cheirodendron, Coprosma, Crossostylis, Ilex, Melicope, and Xylosma .
Etymology. Th e specifi c epithet refers to the island of Ua Pou where the only known populations occur.
Conservation status. IUCN Red List Category: Critically Endangered CR B2a + 2b (i, ii, iii). B2: total area of occupancy less than 10 km 2 (ca. 5 km 2 ). B2a, a single population known; b (i-iii), habitat continuing decline inferred. Th e suitable habitat for Cyrtandra uapouensis on Ua Pou (ca. 105 km 2 ) is indicated as an endangered environment, threatened feral animals and invasive plants, reducing the extent of the forest (Florence Mueller-Dombois and Fosberg 1998;Meyer and Salvat 2009) Discussion. Gillett (1973) included the only known specimen of Cyrtandra uapouensis at that time ( Quayle 1151 ) within his delimitation of C. nukuhivensis ; populations from Ua Pou are here separated based on its occurrence on a diff erent island and its consistently larger leaves. Cyrtandra uapouensis grows sympatrically with C. kenwoodii, and there are several collections (cited in hybrid section) that are morphologically intermediate between them that appear to represent hybrids. Th e fact that C. kenwoodii forms a separate branch in the phylogenetic analyses (Clark et al. 2009; fi g. 1) from both the divided calyx group and the plicate calyx group suggests that perhaps this hybridization has impacted the genome of C. kenwoodii or that the species is of hybrid origin. Description. Shrubs 0.2-1 m. Leaves opposite, clustered on upper 2-5 nodes, brittle, elliptic to elliptic-oblanceolate, 4-7.6 × 1.0-2.1 cm, upper surface glossy, green, glabrous, lower surface pale green, glabrous, margins irregularly and inconspicuously serrulate, apex acuminate, base attenuate, petioles 0.2-1.6 cm long. Flowers in loose, open cymes 3-6 cm long, arising in the upper leaf axils, cymes 1-3 fl owered, peduncles 15-40 mm long, ca. 1-1.5 mm in diameter, pedicels 10-18 mm, bracts lanceolate, ca. 6-8 mm; calyx funnelform, white, ca. 11-15 mm long, lobes 5-9 mm long, subequal, glabrous, deciduous after anthesis; corolla white, funnelform, tube ca. 24-26 mm long, lobes ca. 6-8 mm long. Immature berry 15 mm long.

Cyrtandra kenwoodii
Distribution. Marquesas Islands, rare, endemic to high ridges of Ua Pou, from Oave and Matahenua to Teavahaakiti,Tekahuipu,and Tekohepu, Ecology. Cyrtandra kenwoodii is known only in cloud-swept summits with Metrosideros collina shrubland with other shurbs and small trees such as Apetahia, Freycinetia, and Hibiscus .
Etymology. Th is new species is named for Kenneth R. Wood, who fi rst collected it and who has contributed greatly to our knowledge of the fl ora of the Marquesas and the Hawaiian Islands through his collections and fi eld observations. Conservation status. IUCN Red List Category: Critically Endangered EN B2a + B2b(i-iii). B2: total area of occupancy less than 10 km 2 (ca. 5 km 2 ). B2a, a single population known; b (i-iii), habitat continuing decline inferred. Th e suitable habitat for Cyrtandra kenwoodii on Ua Pou (ca. 105 km 2 ) is indicated as an endangered environ- Discussion. Th e sample of Cyrtandra kenwoodii used ( Wood & Perlman 10804 ) in the molecular study by Clark et al. (2009) was identifi ed as C. feaniana , prior to realization that the diminutive plants from Ua Pou represented an undescribed species. Th e molecular data show that C. kenwoodii is in a polytomy along with the two primary clades of Marquesan species, but is grouped here with the plicate species as it has the calyx only divided about half way to the base, but is not plicate as far as is known. Description. Shrub 1.5-3 m; stems glabrous or with a few scattered hairs when young. Leaves opposite, lanceolate to elliptic, 2.5-19 × 1.3-7.2 cm, glabrous, margins crenulateserrulate, apex acute or acuminate, base cuneate, petioles 1-5 cm. Flowers 1-3 in cymes arising in the leaf axils, usually somewhat shorter than the leaves, glabrous or with scattered hairs, peduncles 10-45 mm long, ca. 0.5-1.5 mm in diameter, pedicels 18-35 mm long, bracts inconspicuous, narrowly lanceolate or triangular, 1-5 mm long, deciduous; calyx usually white, occasionally greenish white, 10-24 mm, divided nearly to the base, lobes lanceolate, tardily deciduous; corolla white, glabrous externally, tube 18-23 mm long, the lobes subequal, broadly obovate, 10-12 mm long; ovary narrowly ovoid, glabrous, style ca. 7 mm long, minutely puberulent. Berries pale orange, ca. 15 mm long, narrowly ovoid, glabrous.
Distribution. Marquesas Islands, occurring on Hiva Oa and Tahuata, and known from a few collections made in 1922 on Nuku Hiva and Ua Huka, from 700 to 1100 m.
Ecology. Cyrtandra feaniana is known from ridges and summit areas of montane wet forest dominated by Metrosideros collina and other shrubs and trees such as Weinmannia marquesana forest with diverse fern understory and other shrubs and trees such as species of Coprosma, Crossostylis, Freycinetia, Ilex, Melicope, Polyscias, Psychotria , and Xylosma .
Conservation status. IUCN Red List Category: Endangered EN B1ab (i,ii,iii) + 2ab (i,ii,iii). B2: total area of occupancy less than 5000 km 2 (ca. 799 km 2 ). B1a, severely fragmented; B1b (i-iii), habitat continuing decline inferred. Th e suitable habitat for Cyrtandra feaniana on Nuku Hiva (ca. 340 km 2 ), Ua Huka (ca. 83 km 2 ), Hiva Oa (ca. 315 km 2 ), and Tahuata (ca. 61 km 2 ) is restricted to mountain slopes and summits, indicated as an endangered environment that is threatened by human activity (deforestation and fi re), feral animals, and invasive plants, reducing the extent of the forest (Florence and Lorence 1997;Mueller-Dombois and Fosberg 1998;Meyer and Salvat 2009   Discussion. Cyrtandra feaniana along with the closely related C. ootensis are the most commonly occurring species of Cyrtandra in the Marquesas Islands. In addition C. feaniana has the widest distribution, along with C. ootensis , occurring on four islands, although seemingly rare on Nuku Hiva and Ua Huka and has not been collected on either island since 1922. Specimens with more than a few hairs on various parts of the plant are here identifi ed as C. ootensis . Th is includes all of the specimens from Fatu Hiva that are nearly glabrous, but have much larger leaves like other populations of C. ootensis . Alternatively, it is possible that these glabrate Fatu Hiva populations represent hybrids or hybrid derivatives between C. feaniana and C. ootensis . Th is hypothesized hydridization if correct would require the colonization of Fatu Hiva by C. feaniana followed by hybridization with C. ootensis to produce the glabrate larger-leaved plants. Description. Shrub to 1-4 m tall; stems ferruginous pubescent. Leaves opposite, densely ferruginous pubescent, elliptic to broadly elliptic, 12-22 × 5-9.5 cm, apex acuminate, base attenuate, margins serrate, petioles 2-5 cm long. Flowers 1-3 in cymes to 20 cm, peduncles 6-8.5 cm long, ca. 2-3 mm in diameter, pedicels 20-35 mm, bracts ca. 4 mm; calyx green, 12-20 mm, divided almost to base, densely ferruginous pubescent deciduous; corolla ca. 25 mm long, tube cylindrical, 18-20 mm long, lobes suborbicular; ovary ca. 8-14 mm, densely pilose, style 4-5 mm, densely pilose. Immature fruit narrowly ovoid, ca. 15 mm long, densely pubescent.
Ecology. Cyrtandra tahuatensis is known from ridges and summit areas in wet forest and shrubland with shrubs and trees such as species of Coprosma, Crossostylis, Freycinetia, Ilex, Melicope, Metrosideros, Polyscias, and Weinmannia .
Distribution. In the Marquesas known only from the type collections on Fatu Hiva at 830 m.
Ecology. Th e type was collected on a cliff face, but the specifi c ecology of Cyrtandra revoluta is unknown.
Conservation status. IUCN Red List Category: Critically Endangered CR B2a + 2b (i, ii, iii). B1, total extent of occurrence less than 100 km 2 (ca. 85 km 2 ), a,b, known from a single location; B2a, estimated area of occupancy estimated to be less than 10 km 2 [one collection known]; B2b (i-iii), habitat continuing decline inferred. Th e estimated area of occupancy for Cyrtandra revoluta on Fatu Hiva (less than 10 km 2 ) is indicated as an endangered environment, threatened by human activity (deforestation and fi re), feral animals, and invasive plant species, reducing the extent of the forest (Florence and Lorence 1997;Mueller-Dombois and Fosberg 1998;Meyer and Salvat 2009).
Distribution. Marquesas Islands, very rare or perhaps extinct, endemic to Toovii Plateau, Nuku Hiva, ca. 800-900 m. It is known from three collections collected in 1844, 1922, and the most recent in 1982.
Ecology. Cyrtandra toviana is known only in Metrosideros collina woodland. Conservation status. IUCN Red List Categories: Critically Endangered CR B2a + 2b (i, ii, iii). B1, extent of occurrence estimated to be less than 100 km 2 ; B2, area of occupancy estimated to be less than 10 km 2 (ca. 9 km 2 ), and B2a, a single population known; b (i-iii), habitat continuing decline inferred. Th e suitable habitat for Cyrtandra toviana on Nuku Hiva (ca. 340 km 2 ) is indicated as an endangered environment, threatened by human activity (deforestation), feral animals, and invasive plants, reducing the extent of the forest (Florence and Lorence 1997;Mueller-Dombois and Fosberg 1998;Meyer and Salvat 2009 Discussion. Cyrtandra toviana is unique within Marquesan Cyrtandra with its peltate leaves and small campanulate calyx. In fact, it could well represent a separate introduction of the genus to the Marquesas Islands.