Athyrium haleakalae (Athyriaceae), a new rheophytic fern species from East Maui, Hawaiian Islands: with notes on its distribution, ecology, and conservation status

Abstract Athyrium haleakalae K.R. Wood & W.L. Wagner (Athyriaceae), a small lithophytic fern from East Maui, Hawaiian Islands, is described and illustrated. Notes on its distribution, ecology, and conservation status are also presented. The new species appears to be an obligate rheophyte, preferring sites of fast moving water along concave walls of streams and waterfalls. Athyrium haleakalae differs from the only other known Hawaiian Athyrium, Athyrium microphyllum (Sm.) Alston, in having rhizomes 1–3 cm long and lanceolate blades 1- to 2-pinnate-pinnatifid, 3–8(–11) × 1–3(–4) cm, as compared to Athyrium microphyllum having rhizomes (10–)15–30 cm long and ovate to ovate-triangular blades 3-pinnate-pinnatifid to 4-pinnate, 30–82 × 20–50 cm.


Introduction
Athyrium Roth, in the family Athyriaceae Alston, is a genus composed of ca. 230 species of terrestrial or epilithic plants with mostly erect or occasionally creeping or ascending rhizomes. Primary centers of Athyrium diversity are found in the Sino-Himalayan region where ca. 91 species are recorded from Southwest China, Sichuan Basin, Tibet-Yunnan Plateau and Nepal (Kramer and Green 1990, Fraser-Jenkins 1997, Wang 1999, Mabberley 2008, Liu et al. 2009) and with secondary centers of diversity in the Western Pacifi c islands where ca. 54 species are known from the Japanese Archipelago, the Ryukyu Islands, Taiwan, and the Philippines (Salgado 1990, Kato 1995, Liu et al. 2009).
Concepts in the classifi cation of Athyrium continue to change and evolve with recent molecular phylogenetic studies (Smith et al. 2006, Christenhusz et al. 2011, Rothfels et al. 2012, Sundue and Rothfels 2014, PPG I 2016. Smith et al. (2006) published a revised fern classifi cation based on both morphological and molecular evidence placing Athyrium into Woodsiaceae (Diels) Herter, yet state that its placement was tentative and in need of a more refi ned analysis. Subsequently Christenhusz et al. (2011) placed Athyrium into Athyriaceae along with four other genera, namely Anisocampium C. Presl, Cornopteris Nakai, Deparia Hooker & Grev., and Diplazium Sw. Furthermore, they report the need for continued research, referring to the monophyly of Athyrium and Diplazium. In 2016 the Pteridophyte Phylogeny Group (PPG) published the most current understanding of lycophyte and fern phylogeny and in their community-derived classifi cation they limit Athyriaceae to three genera, namely Athyrium, Deparia, and Diplazium, with an estimated 650 species.
Th ere are nine other athyrioid fern species endemic to the Hawaiian Islands, namely Athyrium microphyllum (Sm.) Alston, Deparia cataracticola M. Kato (Palmer 2003, Vernon andRanker 2013). Th is recent discovery and present publication of Athyrium haleakalae K.R. Wood & W.L. Wagner brings the total number of Hawaiian Athyriaceae to ten, and represents the second Athyrium species in the archipelago.
Etymology  (Sakai et al. 2002). Estimates on the number of endemic fern and lycophyte taxa on Maui vary only slightly (Palmer 2003, Vernon andRanker 2013) and the present authors estimate there are 115, including fi ve single-island endemics. Athyrium haleakalae now represents the sixth single-island endemic fern or lycophyte taxon found on Maui. It is the tenth endemic athyrioid species in the Hawaiian Islands, and the second in that group that is restricted to a single island, the other being Deparia cataracticola M. Kato, of Kaua'i.
Since  bination of its small size, remoteness of preferred habitat, and the extreme physical geography of its surroundings can explain why A. haleakalae has been overlooked to date. Modern access by helicopter and careful fl oristic inventories around large waterfalls and rugged plunge pools have led to its recent discovery by botanists of the National Tropical Botanical Garden (NTBG), the Maui Nui Plant Extinction Prevention Program (PEPP), and Haleakalā National Park. It is believed that the extent of occurrence for A. haleakalae may be greater than the four drainages reported here, and further research into similar habitats along adjacent drainage basins could lead to the discovery of additional colonies.
Th e current distribution of Athyrium haleakalae has an elevational range of 1,161-1,326 m. Th e dominant plant community of those regions is a Metrosideros Banks ex Gaertn. (Myrtaceae)-Cheirodendron Nutt. ex Seem. (Araliaceae) montane wet forest. Large colonies of matting ferns such as Dicranopteris linearis (Brum. f.) Underw. and Diplopterygium pinnatum (Kunze) Nakai (both Gleicheniaceae) are associated with these forests, being especially expansive near forest borders where steep slopes drop down to deep dissecting streams. Observations to date indicate that Athyrium haleakalae is an obligate rheophyte which prefers concave moss-matted basalt walls along the waterline of perennial streams, forming colonies over wet basalt rock faces especially under and around the ledges of waterfalls and hollows of large plunge pools Conservation status. IUCN Red List Category. When evaluating the conservation status of Athyrium haleakalae utilizing the World Conservation Union (IUCN) criteria for endangerment (IUCN 2001), A. haleakalae falls into the Critically Endangered (CR) category, which designates this species as facing the highest risk of extinction in the wild. Our formal evaluation can be summarized by the following IUCN hierarchical alphanumeric coding system of criteria and subcriteria: CR B1ab(i,ii,iii,v)+2ab(i,ii, iii,v), which refl ects a wild population of ca. 300 individuals, an Extent of Occurrence (EOO) of 4.3 km 2 , and an Area of Occupancy (AOO) of less than 1 km 2 . Ecosystem trends on the mountain of Haleakalā also indicate that A. haleakalae is subject to an inferred decline in its area of occupancy, in addition to a decline in the extent and quality of its habitat and number of mature individuals. It should be noted that A. haleakalae is currently being cultivated by the Hawai'i State Division of Forestry and Wildlife at their Olinda Rare Plant Facility on East Maui.

Discussion
Athyrium microphyllum, previously thought to be the only member of the genus in the Hawaiian Islands, is widely distributed and endemic on all the major high islands, ranging from 500 to 2,320 m ( Figure 4B). Hawaiians called this species 'ākōlea and it is commonly found in native forest understory where it can occasionally become a co-dominant in healthy forests, especially just above the riparian edges of both mesic and wet forest habitats. Athyrium microphyllum is almost always terrestrial, averaging 50-100 cm tall, and having strait narrow rhizomes of up to 30 cm. Although A. microphyllum is occasionally lithophytic around streams, its large form eventually gets dislodged from the walls that enclose fast moving waters especially during fl ash fl oods.
Currently there are no extra-Hawaiian species of athyrioid ferns naturally occurring in the Hawaiian archipelago, although there are two historical introductions that have naturalized, namely Deparia petersenii (Kunze) M. Kato and Diplazium esculentum (Retz.) Sw. In our review, no previously described Athyrium was comparable to A. haleakalae, and with hopes for its conservation and habitat protection we report this newly discovered, critically endangered, narrow endemic rheophyte as the latest addition to the pteridophyte fl ora of the Hawaiian Islands.