Revision of endemic Marquesas Islands Bidens (Asteraceae, Coreopsideae)

Abstract During the preparation of the Vascular Flora of the Marquesas Islands four new species of Bidens (Coreopsideae, Asteraceae) have come to light and are described herein: Bidens woodii W.L. Wagner, J.R. Clark & Lorence, sp. nov. from Ua Pou, and Bidens microcephala W.L. Wagner, J.R. Clark & Lorence sp. nov., Bidens evapelliana W.L. Wagner, J.R. Clark & Lorence, sp. nov., and Bidens wichmanii W.L. Wagner, J.R. Clark & Lorence, sp. nov. from the undercollected island of Fatu Hiva. In addition to these new species, we recognize the following six species of Bidens previously described from the Marquesas Islands: Bidens beckiana (F. Br.) Sherff (Eiao and Hatutaa), Bidens bipontina Sherff and Bidens cordifolia Sch. Bip. (both in Nuku Hiva), Bidens henryi Sherff (Hiva Oa, Tahuata), Bidens uapensis (F. Br.) Sherff (Ua Pou), and Bidens polycephala Sch. Bip. (Nuku Hiva, Ua Huku, Hiva Oa, Tahuata, and Mohotani). Two names are reduced to synonymy under Bidens polycephala: Bidens collina Degener & Sherff, syn. nov. and Bidens jardinii Sch. Bip., syn. nov. Bidens polycephala has the widest distribution of the Marquesan species on five of the islands and exhibits considerable variation.


Introduction
Th e Flora of the Marquesas Islands project is a collaborative program, primarily between the Smithsonian Institution and the National Tropical Botanical Garden, intended to further knowledge of the fl ora of this remote archipelago. In 1997 the fi rst publications of new species and revisions of genera with more than one endemic species were initiated (Florence and Lorence 1997;Wagner and Lorence 1997). Since that time a series of publications has enumerated and revised a number of genera (for summary see Lorence and Wagner 2011). After the 2011 issue in PhytoKeys there were only two major groups in the Marquesas Islands fl ora for which revisions had not been completed. Th e fi rst, Cyrtandra J. R. Forst. & G.Forst. (Gesneriaceae), is now complete with 11 species . Th e present revision of the Marquesas species of Bidens L. completes the precursor publications required to fi nalize the data in the online Flora of the Marquesas Islands website (Wagner and Lorence 2002 and onward; http://botany.si.edu/pacifi cislandbiodiversity/marquesasfl ora/index.htm). Th e new species described in these precursor publications have increased the known native fl ora in the Marquesas Islands by about 25%.
Th e genus Bidens is the largest genus of the tribe Coreopsideae with 150-235 species (Sherff 1937;Strother and Weedon 2006); most research on various groups within the genus suggest numbers at the lower end of the range are probably more accurate (e. g. Ganders and Nagata 1990). Th e genus has had a long, complex taxonomic history summarized by Sherff (1937) in his revision of the genus. Sherff 's revision remains the only modern study of the entire genus as presently delimited in which he treated 235 species, many with one to several varieties. Most of the species occur in the Americas and Africa, while Sherff (1937) accepted 59 species in the Hawaiian Islands and southeastern Polynesia, but our current estimate is there are about 40 species. Th ere are only a few indigenous species in Europe and northern Asia. Th e taxonomy of the genus remains confused despite a growing number of individual groups within the genus having been the subject of detailed studies (Ganders et al. 2000). Species of related genera such as Coreocarpus Benth., Coreopsis L., Cosmos Cav., Dahlia Cav., and Th elesperma Less. have had a tangled history with Bidens, and it has been one of the most diffi cult to defi ne. Relationships among the 20+ genera within the tribe Coreopsideae are poorly understood, but recent phylogenetic studies using molecular data as well as morphological and anatomical traits are helping to resolve monophyletic groups within the tribe and the relationships among them (Ganders et al. 2000;Kimball and Crawford 2004;Crawford et al. 2009;Knope et al. 2012;Funk et al. unpubl.). Th ese recent molecular phylogenies have also indicated that some Coreopsideae genera are not monophyletic, especially in the broadly sampled (multiple species in 19 genera) study by Kimball and Crawford (2004). Th ese studies have resolved a number of well-supported lineages; however, the two largest genera, Bidens and Coreopsis, were determined to be non-monophyletic in their present delimitation. One alternative at this stage of the phylogenetic understanding of the various clades is that a broadly circumscribed genus Bidens (or Coreopsis), inclusive of much of the tribe, would be the best taxonomic solution to the problem. Th e alternative would be to segregate out numerous relatively small genera refl ecting morphologically identifi able monophyletic groups. If this latter course were to be followed for the Pacifi c species, which are in a clade containing B. pilosa L. and other New World species, the correct generic name would seem to be the obscure name Kerneria Moench.
In the Marquesas Islands Schultz (1856) described four species, B. cordifolia, B. jardinii, B. polycephala, and B. serrulata, in his enumeration of plants collected by Jardin. Bidens jardinii is here considered to be a synonym of B. polycephala, and B. serrulata is a homonym. Sherff as part of his overall multiyear eff orts to study the genus provided B. serrulata with the new name, B. bipontina. Forest Brown (1935) described two additional species in the genus Campylotheca Cassini, C. beckiana and C. uapensis. Th ese were transferred later to Bidens by Sherff , who also described three additional species himself, B. henryi, B. collina, and B. ahnnei (the latter two here considered synonyms of B. polycephala). Additional names in Bidens from the Marquesas are Bidens hivoana Degener & Sherff (1934), described from the island of Hiva Oa, and Bidens teikiteetinii Florence and Stuessy (1988). With subsequent study both have been transferred to Oparanthus (Shannon and Wagner 1997). To the previously described six species we here add four species from two underexplored islands: B. woodii, from the summit of Ua Pou, and B. microcephala, B. evapelliana, and B. wichmanii from Fatu Hiva (Table 1). We have arranged the species in the taxonomic section according to an unpublished phylogeny by Funk et al. See Fig. 1 for map of the Marquesas Islands showing the geographic relationships among the islands.
When evaluated using the IUCN criteria for endangerment (IUCN 2001, see also www.iucnredlist.org/info/categories_criteria2001), most of the Marquesan species of Bidens 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 Bidens meet these 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.
Due to the small areas involved on oceanic islands, many single island endemics have a geographic range of less than 100 km² and some less than 10 km². Th erefore they will fall automatically into the Critically Endangered (CR), Endangered (EN), or Vulnerable (VU) category, or in other words into extremely high (CR) to lower (VU) risk of extinction categories despite the fact that they may have relatively small natural Table 1. Island distribution of Marquesas species of Bidens. Islands arranged from oldest to youngest.

Species / Island Eiao Hatutaa Nuku Hiva Ua Huka Ua Pou Hiva Oa Tahuata Fatu Hiva
ranges and may be relatively common locally with healthy, regenerating populations. Some will fall into the Data Defi cient (DD) category, simply because we know so little about their actual population size, status, and range. Although the IUCN evaluations are not ideally suited for islands, for the sake of consistency we use them herein for Marquesas Bidens and where appropriate have added qualifying comments under Conservation Status for species that seem extremely at risk and those that are more common.
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 meas-  Specimens from the following herbaria were studied: AD, BISH,  BKL, BR, CBG, CHR, F, K, L, MO, MPU, NSW, NY, P, PAP, PTBG, OS, TEX, UBC, US, and WU. We have examined all collections cited except for the four types of the Schultz (1856) names for which we studied images of them sent by P. Lowrey.
Habitat. Bidens henryi is known from ridges and summit areas in montane wet shrubland or low forest with Metrosideros collina (J.R. Forst. & G. Forst.) A. Gray and Weinmannia marquesana F. Br. with fern understory along with other shrubs and trees such as species of Cheirodendron, Coprosma, Crossostylis, Cyrtandra, and Myrsine.
Conservation status. Proposed IUCN Red List Category Endangered (EN), criteria B2b i-iii): B2, total area of occupancy less than 500 km² (ca. 50 km²); b (iiii), habitat continuing decline inferred. Th e suitable habitat for Bidens polycephla on Nuku Huka (ca. 340 km²), Ua Huka (ca. 83 km²), and Tahuata (ca. 61 km²) is indicated as an endangered environment, threatened by human activity (deforestation), feral animals, and invasive plants, thus reducing the extent of the forest. However, B. polycephala has been observed to be locally common in some areas with considerable regeneration, and alternatively it might be considered Near Th reatened (  Discussion. Bidens polycephala is the most variable of the Marquesan Bidens, and is also the most widespread, occurring on four islands. It is similar to Bidens henryi but diff ers in having much shorter involucral bracts and in the large but variable number of heads among individuals, and it occupies drier and lower elevation habitats. Some of the collections of this species from Nuku Hiva seem to grade toward B. bipontina as they have more caudate leaf apices and longer rays (e.g.,  Description. Erect, suff rutescent perennial herbs 0.6-3 m tall. Leaves simple, 4.5-12 cm long including petiole, blades lanceolate to lanceolate-elliptic, 3-8.5 × 1-4 cm, mostly glabrous, except for a tuft of hairs on lower surface at base, margins serrulate to serrate, apex acuminate to occasionally acute. Heads 3-12(-16), in diff use cymes, terminating main stem and lateral branches, 2-8 mm in diameter excluding rays, peduncles 0.4-7 cm long, stout; outer involucral bracts 1.5-8 mm long, well differentiated from inner bracts, margins ciliate, inner bracts often with a tuft of hairs at apex; ray fl orets 5-11 per head, sterile, rays yellow, 7-15 × 1.5-5 mm; disk fl orets ca. 23-25, perfect. Achenes gray or black, straight, 3-5 × 0.5 mm, tipped, margin setose; pappus of 2 irregularly antrorse barbed awns.
Habitat. On sea cliff s in mixture of native shrub and trees and alien vegetation, with native species such as Dodonaea viscosa Jacq., Hibiscus tiliaceus, Pisonia grandis R. Etymology. Th e specifi c epithet refers to the extremely small heads, probably the smallest in the genus.
Conservation status. Proposed IUCN Red List Category Critically Endangered (CR), criteria B1ab, B2a,b (i-iii): B1, total extent of occurrence less than 100 km² (ca. 85 km²), a, severely fragmented and b, continuing habitat decline inferred; B2a, estimated area of occupancy estimated to be less than 10 km²; B2b (i-iii), habitat continuing decline inferred. Th e estimated area of occupancy for B. microcephala on Fatu Hiva (ca. 85 km²) is indicated as an endangered environment, threatened by human activity (deforestation and fi re), feral animals, and invasive plant species, thus reducing the extent of the suitable habitat. It is still locally common and regenerating on some cliff areas inaccessible to goats, however, so VU might be an alternative category (Butaud, pers. comm. 2014). , this reduction is even more extreme; fl ower heads in these specimens contain consistently fewer than 4 fl orets each, often only two or even occasionally one. Th ese latter specimens also universally exhibit entire to subentire leaf margins and might represent yet another evolutionary lineage worthy of formal recognition (e.g., in Lorence 7823, specimen from cultivated plant grown from seed from Perlman 14996).  Description. Erect, suff rutescent perennial herbs 0.5-1 m tall. Leaves simple, 5-7 cm long including petiole, petiole stout, blades thick and coriaceous, ovate to broadly ovate, 3-4.5 × 1.8-2.5 cm, glabrous, the veins on lower surface conspicuously raised, margins serrate, apex short-acuminate. Heads 1-2, in compact cymes terminating main stem and lateral branches, 4-5 mm in diameter excluding rays, peduncles ca. 2 cm long, stout, glabrous; outer involucral bracts ca. 3-4 mm long, broad, well diff erentiated from inner bracts; inner bracts dark purple, erose and with a few short hairs; ray fl orets ca. 6-8, sterile, rays yellow, obovate, 10-12 × 4-7 mm, apices often bi-or tri-lobed; disk fl orets ca. 30-34, perfect, corollas yellow; pappus absent. Achenes not seen. Distribution. Marquesas Islands, Ua Pou, known only from the type on the summit crest around Oave and the nearby peak of Matahenua, ca. 920 m.

Bidens woodii
Habitat. Occurs in low shrubland of Metrosideros collina with Dicranopteris linearis on the windswept and cloud-shrouded summit area.
Etymology. Th is new species is named for Kenneth R. Wood, who made the only known collection of it and who has contributed greatly to our knowledge of the fl ora of the Marquesas and Hawaii through his collections, excellent photography, and fi eld observations. Conservation status. IUCN Red List Category Endangered (EN), criteria B2a, B2b i-iii: B2, total area of occupancy less than 500 km² (c. 50 km²); B2a, fragmented populations; b (i-iii), habitat continuing decline inferred. Th e suitable habitat for Bidens woodii on Ua Pou (c. 105 km²) is indicated as an endangered environment, threatened by human activity (deforestation, fi re), feral animals, and invasive plants, thus reducing the extent of the suitable habitat.
Distribution. Marquesas Islands, occurring only in a relative small area of the Toovii Plateau on Nuku Hiva, from 750-1130 m.
Habitat. Bidens cordifolia is known from montane wet shrubland or low forest with Metrosideros collina and Weinmannia marquesana with fern understory along with other shrubs and trees such as species of Coprosma, Crossostylis, Cyrtandra, Dicranopteris, Geniostoma, and Myrsine.
Conservation status. Proposed IUCN Red List Category Critically Endangered (CR), criteria B1ab, B2a,b (i-iii): B1, total extent of occurrence less than 100 km² (less than 10 km²); a,b, known from a single location; B2a, area of occupancy estimated to be less than 10 km²; B2b (i-iii), habitat continuing decline inferred. Th e suitable habitat for Bidens cordifolia on Nuku Huka (ca. 340 km²) is indicated as an endangered environment, threatened by human activity (deforestation, fi re), feral animals (goats), and invasive plants, thus reducing the extent of the forest. Discussion. Bidens cordifolia is one of the least known species of Bidens in the Marquesas Islands. We have seen only two collections we refer to this species as well as images taken by Jean-François Butaud in 2008 and 2009 of additional populations. In addition to these collections and observations this species was only known from the type and a collection made in 1840 (Barclay 3213, BM) as cited by Sherff (1937 Description. Erect subshrubs 0.7-1.3 m tall. Leaves simple, 1.5-9.5 cm long including petiole, blades narrowly ovate or lanceolate, 1-7 × 0.8-4 cm, glabrous or pubescent toward the base and in a line along the petiole, margins serrulate, apex acuminate. Heads (1-)3(-4), in diff use cymes terminating main stem and lateral branches, 5-15 mm in diameter excluding rays, peduncles 1.5-11.8 cm long, glabrous; outer involucral bracts 4-9 mm long, broad and tapering somewhat at the base, apex sometimes erose, inner bracts sometimes erose at apex; ray fl orets 5-11, sterile, rays yellow, 9-15 × 2-3 mm wide, apex entire or divided into 2-3 acute to rounded lobes; disk fl orets ca. 30-34, perfect, corollas yellow. Achenes gray, straight or slightly curved, 8-10 × 1 mm, conspicuously setose; pappus of 2 antrorse barbed awns.
Habitat. Bidens beckiana is scattered to locally common on steep slopes and ridges, ravines, or cliff s, from mesic to xeric shrublands and grasslands with Dinebra xerophila, Waltheria indica L., Cordia lutea Lam., Dodonaea viscosa, and Th espesia populnea (L.) Sol. ex Corrêa. Judging from the number of collections B. beckiana appears to be more common on Hatutaa than Eiao, which has populations of feral sheep, pigs, cats, and rats.
Conservation status. Endangered (EN), criteria B2b (i-iii): B2, total area of occupancy less than 500 km² (ca. 47 km²); b (i-iii), habitat quality continuing decline inferred. Th e suitable habitat for Bidens beckiana on Eiao (40 km²) and Hatutaa (7 km²) is indicated as an endangered environment, threatened by feral animals, and invasive plants, thus reducing the extent of the suitable habitat. Discussion. Bidens beckiana is characterized by having outer and inner involucral bracts that are scarcely diff erentiated from the pales, and very broad outer bracts that are usually somewhat constricted at the base.

Putative hybrid Bidens bipontina × Bidens polycephala
We have examined two gatherings from Nuku Hiva in Tapueahu Valley NW of Toovii that may represent hybrids. One of them (Butaud 2587) was collected in a small population of ca. 10 similar individuals (Butaud, pers. comm.), and could represent either hybrid individuals or less likely an undescribed taxon. A second gathering (Perlman & Wood 15021) seems to represent a mixed collection of one parent (B. bipontina, all but one of the specimens) and a putative hybrid (one specimen at US). Th ese plants were growing with or fairly close to populations of B. bipontina, which occurs in the valley, and B. polycephala, which occurs in nearby areas, but has not been collected specifi cally near these putative hybrids. More information is needed to make an informed interpretation. Th ese collections diff er from both putative parents in having almost exclusively trifoliolate leaves, relatively small heads 1-3 mm in diameter excluding rays, glabrate, but with scattered hairs on margins of bracts, upper surfaces and in axils, outer involucral bracts ca. 2 mm long, linear, sparsely ciliate, ray fl orets 2-4 per head, rays 4-8 mm long, and achenes ca. 3 mm. Th e Butaud collection was included in a recent molecular phylogenetic study of Pacifi c Bidens (Funk et al. unpubl.), and it is placed in a small clade consisting of B. bipontina and B. cordifolia, but is not identical to either.

Acknowledgments
We are grateful to the Bishop Museum Herbarium (BISH) for access to and loans of their collections. Ray Fosberg made his notes for a revision he preparing of Marquesas Bidens available to Wagner that were useful in our analyses leading the revision presented here. In addition to the collections, images and observations made by two of the authors (W.L. Wagner and D.H. Lorence), the observations and descriptions were made possible by fi eld observations, photos, and specimens provided by Ken Wood and Steve Perlman (National Tropical Botanical Garden) as part of the "Vascular Flora of the Marquesas Islands" project, which was supported by a generous private donation to the National Tropical Botanical Garden. We are grateful to the Délégation à la Recherche (Papeete, Tahiti), the Musée de Tahiti et des Iles, and the Service du Développement Rural for logistic support, the Délégation for permission to collect in the Marquesas, and the Délégation and the Haut-Commissariat de la République en Polynésie française for permission to conduct research. Th e illustrations were skillfully drawn by Alice Tangerini (Smithsonian Institution). We appreciate the download and edits by Nancy Khan of the specimens examined from the Marquesas database as well as an overall edit of the manuscript. We also appreciate the helpful comments, images, and insights on Marquesas Bidens by Jean-François Butaud and helpful comments from Jacques Florence. P. Lowrey provided images of the Paris types of the names described by Schultz. We appreciate the useful review comments by Mesfi n Tadesse. Th e contribution by W.L. Wagner to this study was partially supported by the Smithsonian Research Opportunities Fund and the National Tropical Botanical Garden McBryde Endowment for Hawaiian and Pacifi c Botany.