Systematics and rarity of Australia's tassel-ferns (Lycopodiaceae : Lycopodiophyta)

Tassel-ferns belong to the Lycopodiaceae, a globally distributed family of homosporous, seedles vascular plants including species that exhibit diverse shoot forms relating to their varied habitats. Hypotheses regarding the generic placement and relationships of tassel-ferns have been unstable due to a paucity of morphological characters for systematic analysis which contrasted with relationships uncovered in the first molecular phylogeny of the group. This study investigates the monophyly, placement and global diversification of tassel-ferns (hitherto genus Huperzia Bernh.) using mixed-model Bayesian inference phylogenetic analysis of DNA-sequences from five chloroplast loci in combination with 70 non-molecular characters derived from a large global collection of plants grown under controlled conditions. The phylogenetic hypotheses generated from these analyses support the monophyly of Lycopodiaceae its subfamilies Lycopodioideae and Huperzioideae. These subfamilies exhibit significant synapomorphies that are associated with their differing habits and life-history strategies. The Lycopodioideae are anisotomously branching plants that spread laterally over the terrestrial habitat, contrasting with the Huperzioideae which are isotomously branching plants that have a tufted and generally localised habit. These features are corroborated by anatomical synapomorphies such as stem stele type and microscopic synapomorphies such as spore type and gametophyte types. Within the Huperzioideae are three general morphological and anatomical groups: Phylloglossum drummondii Kunze which is the only wholly deciduous Lycopodiaceae that regenerates from underground tubers, fir-moss type Huperzia s.l. which are disperse by detachable bulbils and tassel-fern type Huperzia s.l. which disperse primarily by spores or via layering of fertile shoot tips. The monophyly of the genus Huperzia s.l. is poorly supported and in several analyses it is rendered paraphyletic with the morphologically divergent Phylloglossum drummondii Kunze being embedded between within it. Based on molecular data, the genus Huperzia s.l. contains a clearly divergent well-supported fir-moss clade and tassel-fern clade. Both are corroborated by morphological synapomorphies that can be identified in the field. Based on the relationships between these major clades, a recommendation is made to continue to recognise the genus Phylloglossum Kunze and to restrict the genus Huperzia Bernh to the fir-moss clade and to recognise a third genus, Phlegmariurus Holub, for the species rich tassel-fern clade. Phlegmariurus (tassel-ferns) are predominantly epiphytic and epilithic tropical plants. They form tufted pendulous shoots and exhibit varied specializations related to the epiphytic habit including re-oriented lycophylls, succulence, glaucousness and multibranched strobili. New combinations with the genus Phlegmariurus Holub are proposed for the Australian tassel-fern species H. carinata (Desv. ex Poir.) Trevis., H. dalhousieana (Spring) Trevis., H. filiformis (Sw.) Holub, H. lockyeri (D.L. Jones & B. Gray) Holub, H. marsupiiformis (D.L. Jones & B. Gray) Holub, H. phlegmaria (L) Rothm., H. phlegmarioides (Gaudich.) Rothm., H.prolifera (Blume) Trevis., H. squarrosa (G. Forst.) Trevis. and H. varia (Brown) Trevis. In contrast, Huperzia s.s. (fir-mosses) are terrestrial, temperate and predominantly northern hemisphere plants and only one species, H. australiana (Herter) Holub, is confirmed as occurring in Australia. The Australian tassel-ferns P. carinatus (Desv. ex Poir.) Ching, P. dalhousianus (Spring) A.R.Field comb. nov., P. filiformis (Sw.) W.H.Wagner, P. lockyeri (D.Jones & B.Gray) A.R.Field comb. nov., P. marsupiiformis (D.Jones & B.Gray) A.R.Field comb. nov. and P. phlegmarioides (Gaudich.) A.R.Field comb. nov. are monophyletic. Based on an examination of their type materials, no recommendations are made to change their species nomenclature. The species hitherto recognised as H. prolifera (Blume) Trevis. has been misidentified in Australia and a new name, P. tetrastichoides (A.R.Field & Bostock) A.R.Field comb. nov. was introduced for this species in Australia. The remaining two Australian species P. phlegmaria s.l. (Rothm.) T.Sen & U.Sen, and P. squarrosus (G.Forst.) Á. Löve & D. Löve, were not monophyletic. The current dataset renders P. squarrosus paraphyletic, indicating that it requires taxonomic review at a global scale. The Australian population appears to be conspecific with the type of P. squarrosus (G.Forst.) Á. Löve & D. Löve, and no changes to the species nomenclature of Australian plants it recommended at this stage. The widespread and variable P. phlegmaria s.l. is polyphyletic. Morphologically distinct species from outside Australia are inserted within it and not all plants recognised as P. phlegmaria s.l. belong to the same clade. In Australia, a classification based on monophyletic taxa is obtained if three species are recognised, P. longibracteatus (Domin) A.R.Field comb. nov., P. ledermannii (Herter) A.R.Field comb. nov. and P. cf. phlegmaria sp. nov. A.R.Field. These three species are identified by differences in their stem structure, lignification and pigmentation; the arrangement, shape and colour of their sporophylls and the phyllotaxy, size and shape of their lycophylls. They occur in sympatry at numerous localities in northern Queensland and no intergrades were observed. Based on the strict sense interpretation of this species presented here, P. phlegmaria (L.) T.Sen & U.Sen, the type of which comes from India, is restricted to India and Asia and Malesia. Overall, the level of tassel-fern endemism in Australia and its relationships with overseas floras was typical of the Palaeotropical region. The Australian tassel-fern flora includes long branch species with no close relatives, endemic species of southern origin, endemic species of Malesian origin and non-endemic species belonging to derived clades that are widespread across the Palaeotropics. The blue-tassel-fern H. dalhousieana is the most phylogenetically distinct tassel-fern species indigenous to Australia, having no close relatives as well as exhibiting multiple autapomorphies. Following re-appraisal of species diversity in tassel-ferns, this study investigated the rarity of the species identified as occurring in Australia. Tropical Australian tassel-ferns can be assigned to four rarity groups. One species is of least concern, being uncommon but widespread in many habitats, three are vulnerable, being confined to specific habitats over two regions, five are endangered, being scarce, altitudinally restricted and occurring in one region only, and one species, P. dalhousieanus, is critically endangered, being extremely scarce in rare and widely scattered specialised habitats. It is proposed that the critically endangered P. dalhousieanus is naturally rare because it is an obligate niche-specialist associated with a small proportion of the epiphytic nestfern Platycerium hillii T. Moore that expresses a particular degenerate life-stage. Populations of P. dalhousieanus are declining rapidly and unless a management plan is developed and implemented, P. dalhousieanus will most probably become extinct in Australia in the near future