A new cryptically dioecious species of bush tomato (Solanum) from the Northern Territory, Australia

Abstract A new species of dioecious Solanum from the Australian “Dioicum Complex” of Solanum subgenus Leptostemonum is described. Solanum cowiei Martine sp. nov., is allied with other members of this problematic lineage, but differs in its slender leaves, limited armature and diminutive habit. The species was first segregated by botanists at the Northern Territory Herbarium as Solanum sp. Litchfield (I.D. Cowie 1428); and specimens representing this species have also been referred to by Symon as Solanum sp. Fitzmaurice River. Collections suggest that this is an endemic of the sub-arid tropical zone of the Northern Territory. SEM images support initial assumptions that the new species is cryptically dioecious via production of inaperturate pollen grains in morphologically hermaphrodite flowers.


Introduction
More than three decades ago the late David Symon published the fi rst comprehensive monograph of Solanum in Australia (1980), a collection of species descriptions for 125 native and exotic solanums including fourteen species newly described by the author. Symon (1980) included a set of 18 native Australian "spiny solanums" of Solanum subgenus Leptostemonum within his interpretation of Solanum section Melongena , thus allying them with the cultivated eggplant ( Solanum melongena ). All nine morphologi-cally androdioecious spiny solanums known in Australia at that time were included in this group. Th ese nine species were later confi rmed by Anderson and Symon (1989) to be cryptically dioecious, with morphologically hermaphrodite fl owers producing pollen without pores (inaperturate) -thus rendering the fl owers (and the plants that bear them) functionally female. Th e remaining Australian native species included in Solanum section Melongena sensu Symon are andromonoecious, and were assumed to represent the ancestral condition from which cryptic dioecy arose in the group (Symon 1980, Anderson andSymon 1989) -fi rst by a separation of male and hermaphrodite fl owers and then a loss of pollen apertures (Martine and Anderson 2007).
Research using molecular phylogenetics approaches , Martine et al. 2009 found that the Australian Solanum section Melongena sensu Symon is not a monophyletic group, but appeared to support the evolutionary pathway from andromonoecy to dioecy in Australian Solanum . Th ese studies also identifi ed two clades of dioecious species, 1) the "Kakadu Clade" of Th e Northern Territory, consisting of Solanum asymmetriphyllum and S . sejunctum , a species described in 2006 (Brennan et al. 2006) and 2) the "Dioicum Complex," a group of 8-9 described species and several geographic variants/forms with its center of diversity in the Kimberley region of Western Australia, a few species extending into the Northern Territory and one species ranging as far as Queensland.
Th e Dioicum Complex, in particular, is a taxonomically challenging group, as acknowledged by Symon (1980) and confi rmed by phylogenetic studies , Bohs et al. 2007, Martine et al. 2009). While the clade is well supported, the relationships among the included taxa are diffi cult to resolve and species boundaries are sometimes blurry -especially in the fi eld. Still, collections and observations made over the last decade by C.T. Martine (CTM) and others (e.g. Barrett 2013) have begun to not only clarify relationships of the Dioicum Complex, but should allow for the formal description of previously unnamed taxa -including the one described herein.
In 2009, CTM followed up on collections by local botanists (including K. Brennan, I. Cowie, D. Lewis, and J. Westaway) of a taxon that had been segregated in the Northern Territory Herbarium as Solanum sp. Litchfi eld ( I.D. Cowie 1428 ). New fi eld collections from Litchfi eld National Park by CTM and colleagues were then used for molecular work (Martine et al. 2011) inferring that Solanum sp. Litchfi eld was closely allied with S. dioicum and a member of the "Dioicum Complex" sensu Martine et al. (2006). Unfortunately, few collections had been made of this taxon that included reproductive elements and fi eld surveys made in April-May 2009 and May 2013 located no individuals in fl ower or fruit. However, multiple new reproductive collections (and some older collections now recognized as this taxon) were deposited/fi led at DNA between 2009 and the present day, thus allowing for a species description to now be completed.
Among the specimens now annotated as Solanum sp. Litchfi eld is a sheet that had been in an indet. folder until recently. Th is specimen, Barritt 1396 , of a staminate plant in fl ower, was identifi ed by the collector as Solanum dioicum . During a visit to the Northern Territory Herbarium in 2004, Symon encountered the specimen, annotated it as Solanum sp. Fitzmaurice River, and recorded a page of notes on the morphological characteristics setting this taxon apart from others. Th ose notes, left in the specimen folder, are here incorporated and used, in part, to describe Solanum cowiei -a posthumous contribution described further in Martine (2013). Description. Clonal, erect subshrub to 80 cm. Single woody stems 4-5 mm diameter from slender, scarcely-rooted underground stolons, splitting at ca. 40 cm into 2-6 branches. Overall plant aspect yellow-green to gray-green (becoming slightly redtinged), with older stems eventually woody and gray. Stems with short, dense indumentum of stellate trichomes. Prickles straight, even throughout or slightly widened at base, fi ne, 5-12mm long, scattered or absent on stems, rarely dense, tending to be absent on woody growth, except near base. Leaves 4-9 cm × 5-10 (-22) mm (largest on newer resprout growth), alternate, linear -lanceolate; margins entire to wavy or rarely lobed; the base tapering to a short petiole 1-1.5 mm long, apex acute; dark green above, slightly lighter beneath, both sides slightly scabrous with short, dense trichomes; trichomes mostly short stalked, porrect-stellate with short central ray. Flowers borne on new growth. Male infl orescence a cyme to at least 6 cm long with 9-12 fl owers that are shed successively, only 1-2 fl owers open at a time; pedicel 5-7 mm, unarmed; calyx 7 mm long with or without a few prickles towards the base, the lobes ending with a slender fi liform acumen ca. 3 mm long; petals 5, fused; corolla 1 cm long, purple, broadly stellate to rotate, acumens 0.5 mm; stamens 5, anthers 2-5 mm long, oblong-lanceolate to somewhat tapered, poricidal, fi laments 2 mm; in a loose anther cone; ovary, style, and stigma vestigial and not exserted beyond the stamens. Morphologically hermaphrodite fl owers solitary, functionally female with anthers producing inaperturate pollen (Fig. 1F). Female fl ower on short pedicel; calyx ca. 5 mm, densely armed with long, straight prickles and stellate trichomes; lobes 6 mm, unequal and linear, prickly; corolla ca. 2 cm diameter, 2 cm long, stellate-funnelform, purple; acumens ca. 2 mm; ovary glabrous, 1 mm diameter at anthesis; style erect, 10 mm (including stigmatic surfaces); bifi d stigmas 1.5 mm long; stamens of same proportions as in staminate fl owers. Peduncle 1.5 cm long, 1.5 mm diameter, sparsely armed with small prickles to 2 mm long. Fruit a green berry 1.2-1.5 cm diameter, globular, drying to black-green and apparently detaching and falling from calyx. Fruiting calyx 2 cm wide, 1.5 cm long, densely armed along sutures, prickles widened (0.5-1 mm) at base and 5-7 mm long, tapering to long fi ne tip; calyx short stellate-pubescent, more so on sutures and around bases of prickles; calyx lobes extending to slender fi liform acumen 5-7 mm long, covered in fi ne stellate trichomes at tip of each lobe; expanding and surrounding fruit except for ca. 1.5 cm opening at mouth. Calyx retained on stem following fruit drop, at times remaining on plant into next season. Seeds 1.5-2 mm, brown, conspicuously and minutely reticulate.

Solanum cowiei
Distribution and ecology. Solanum cowiei is presently known from a handful of localities in the sub-arid tropical zone of the Northern Territory (a region known colloquially as the "Top End"), most of these habitats are classifi ed under the Tropical eucalypt woodlands/grasslands Major Vegetation Group (National Land and Water Resources 2002). Th e species is associated with low sandstone outcrops and open eucalypt woodlands, where it typically grows among small boulders or in sandy grassy areas between or around rock formations. Th e areas where S. cowiei has been collected are fi re-prone and burn at semi-regular intervals ( Fig. 2A, B), allowing for this taxon to compete eff ectively with species of lesser fi re tolerance. While the specifi c pollination biology is unknown, the fl owers are clearly buzz pollinated and are likely visited by bees in the genera Xylocopa and Amegilla , among others (Anderson and Symon 1988). Seed dispersal seems, by initial impressions, to be mechanical. Fruits appear to detach upon maturation, leaving the calyces behind on the plant.
Phenology. Most fl owering specimens have been collected from October-November and March-May, with fruiting specimens collected in Jan-Feb and May. Blooming appears to occur on new shoots soon after burns, as evidenced by dozens of male plants found to be in bud within weeks of managed burns set in the Lost City area of Litchfi eld National Park in late May, 2013.
Etymology. Solanum cowiei is named for Dr. Ian Cowie, Chief Botanist at the Northern Territory Herbarium (DNA) and one of the fi rst to recognize the distinct nature of the taxon.
Preliminary conservation status. Based on IUCN Red List Categories (IUCN 2011), S. cowiei is considered Data Defi cient (DD). Th e species is relatively widespread, occurring over a geographic range of over 800 km, but it has been collected in fewer than 10 localities. Th e small number of collections, coupled with the fact that populations outside of Litchfi eld National Park were only confi rmed within the last several years, suggest that the species is common in some localities but uncommon on the regional and global scales. Th e clonal nature of the species is worth considering, as "populations" of S. cowiei often appear to be large multi-stemmed genets connected by an underground network of stolons. Because the species is dioecious, individual genets cannot self-fertilize, leading to the potential for reproductively isolated clonal individuals. Further data are required before a certain conservation status can be determined. Key populations are protected in Litchfi eld, Limmen and Keep River National Parks and appear secure given current fi re management regimes. fi eld National Park, perhaps the most visited recreation area in the Northern Territory, three primary populations are on routes well travelled by day visitors and campers. Th e most collected population sits along the road to Florence Falls, with tour buses and cars passing on macadam nearly every day within 10 m of individual plants. Th anks to a series of biodiversity surveys undertaken by staff of the NT Herbarium over the last decade or so (e.g., Cowie et al. 2011, Lewis et al. 2010), the species is now known to have a broader distribution spanning from one side of the Top End from Limmen National Park near the Gulf of Carpenteria in the east to Keep River National Park and northward into the Macadam Range in the west. Across this range many characters remain constant, with leaf lobing (unlobed to slightly lobed) and density of prickles (absent to rarely dense) tending to vary the most.
Vigorous post-fi re regrowth has been noted in some areas of deep sand beneath open canopies, with one apparently clonal population in a ca. 20 × 20 m area around the Lost City consisting of ca. 40 ramets (Martine, Evans and Dugan pers. obs.). Resprout growth in this grouping was vigorous and well-armed (Fig. 2C), with numerous male fl ower buds produced on ramets 12-15 cm tall. While other species in this burn area had also begun to resprout, most had not yet developed fl ower buds -leading one to believe that the fl owers of S. cowiei , once opened, would face little local competition for pollinators. While fi re is thought to infl uence the life histories of other species in the Dioicum Complex (Symon 1980), little data exist on its direct eff ects on recruitment patterns.
Previous molecular work (Martine et al. 2011) reveals that Solanum cowiei is a lineage within the Dioicum Complex -but its relationship to other species in the complex remains unresolved pending continued work in the group (CTM, in progress). Based on morphology, the species appears closely allied to S. dioicum and S. carduiforme , the latter species also collected during the Limmen and Keep River surveys. On sight, it diff ers most from S. carduiforme in its leaf shape, lobing, and overall growth form. Th e leaves of S. carduiforme are wider (5 cm across), "long-triangular" in shape, with welldeveloped lobes. Compared to all other solanums in the complex, S. cowiei is rather slight of habit, rarely getting taller than knee height and having poorly developed branching. Aerial shoots, while becoming weakly woody, are much like temporary structures, dying back to the underground stolons during fi re or when outcompeted during gaps in the fi re cycle -only to spring back to life soon after fi res have burned.
In support of its disturbance-adapted nature, much of the biomass in populations of S. cowiei appears to be below-ground. Stolons function in vegetative reproduction (Fig. 2D), but are also likely important for short-term energy and water storage in the sandy soils inhabited by the species. Stolons unearthed in the fi eld snapped crisply and bore the smell of potato starch. Root systems extending from these stolons are coarse and poorly developed.
Th e link of this species to fi re may be the key determinant of the success of the species in individual sites. In unburned sites surveyed by the fi rst author in the Lost City area of Litchfi eld National Park (in 2009 and (Fig. 2A), individual plants were diffi cult to locate and devoid of reproductive structures. In recently burned areas (Fig. 2B) plants were locally abundant, with budding ramets emerging from the sand at high densities.
Th e designation of S. cowiei , along with the recent description of S. zoeae and allied unnamed variants in the Kimberley region (Barrett 2013), brings the count of cryptically dioecious Solanum taxa in Australia to 15. Th e preponderance of this unusual breeding system in this Australian lineage continues to generate questions regarding the evolution of the condition (e.g., Martine and Anderson 2007) and related ecological interactions (Dugan andMartine 2013, Martine andEvans 2013).
Th e poor resolution of the relationships among Australia's dioecious Solanum species is a function of both overlapping morphological characteristics (see Symon 1980) and general diffi culties in defi ning lower level relationships across all Old World "spiny solanums" (Bohs et al. 2007, Vorontsova et al. 2013. Further resolution of the relationships among Australian taxa will hopefully be achieved by combining greater sampling of populations (especially in the Kimberley) with Next Generation molecular techniques (C.T.Martine, studies in progress).