A sticky and heavily armed new species of Solanum (Solanumsubg.Leptostemonum, Solanaceae) from eastern Brazil

Abstract We describe a new species of spiny Solanum (Solanumsubg.Leptostemonum), endemic to the Brazilian Atlantic Forest and associated with granitic outcrops (inselbergs or sugar loaf mountains). Solanumkollastrum Gouvêa & Giacomin, sp. nov. is morphologically similar to the poorly known S.sublentum Hiern, but is a heavily armed, much more robust plant with stellate-glandular indumentum. Together with S.sublentum, it is morphologically related to some species of Solanum such as S.hexandrum Vell., S.robustum H.Wendl., and S.stagnale Moric. that share strongly accrescent calyces, large leaves with the bases decurrent on to the petiole, pendent simple inflorescences and large, robust flowers. The new species is restricted to a few known populations in southern Bahia and north-eastern Minas Gerais states and conservation efforts are needed.


Introduction
Solanum L., with about 1,400 species, is the most species-rich genus of the economically important Solanaceae family, in addition to being amongst the largest genera of flowering plants (Frodin 2004;Hawkes 1999). The distribution range of Solanum is proportional to its species richness: species belonging to the genus occur in all continents but Antarctica, with the highest diversity being found in tropical and subtropical regions of South America (Knapp 2002;Dupin et al. 2016). Phylogenetic studies have recovered the major lineages within Solanum, with the prickly species that possess stellate trichomes composing the largest of them, a monophyletic group known as the Leptostemonum clade or Solanum subg. Leptostemonum Bitter (Bohs 2005, Levin et al. 2006, Weese and Bohs 2007, Särkinen et al. 2013). The 'spiny solanums', as the group is informally named, comprises two major groups: the Old World lineage, which is particularly diversified in Australia, eastern Africa (incl. Madagascar) and tropical Asia and the highly diverse New World grade, that includes some Torva and Lasiocarpa clade representatives native to both the New and Old Worlds (Stern et al. 2011;Vorontsova et al. 2013;Aubriot et al. 2016).
Brazil, especially the eastern portion of its territory, is one of the primary centres of diversity and endemism for both non-spiny (Knapp 2002) and spiny solanums (Whalen 1984) in the New World. With approximately 110 species of spiny solanums (Agra 2007;BFG 2015) and 10 of the 13 New World lineages recovered in Stern et al. (2011), the Brazilian Solanum flora is exceedingly diverse. Ongoing efforts to document and describe the diversity of Solanum in the country through modern taxonomy and intensive fieldwork efforts (i.e. Flora do Brasil 2020 project; http://floradobrasil. jbrj.gov.br/, also see BFG 2015) have shed light on the taxonomy of endemic groups (e.g. Asterophorum clade, Gouvêa and Stehmann in press.;Inornatum clade, Giacomin 2015) and led to the discovery of various undescribed species (e.g. Giacomin and Stehmann 2014;Knapp et al. 2015;Gouvêa and Stehmann 2016;Agra and Stehmann 2016). Here we describe a new species of spiny Solanum from the states of Bahia and Minas Gerais associated with granitic outcrops (inselbergs), a poorly sampled environment with a high degree of endemism in many plant groups (Martinelli 2007, Porembski 2007, de Paula et al. 2017.

Material and methods
For the present study, specimens from the following herbaria were examined: ALCB, BHCB, CEPEC, FURB, HUEFS, MBM, MBML, NY, RB, RFFP and UFP (acronyms from Index Herbariorum; http://sweetgum.nybg.org/science/ih). Expeditions to the areas where the new species occurs were carried out in June 2014, September 2015 and June 2018. During these expeditions, in addition to herbarium collections, juvenile plants were also collected in situ and cultivated at the Museu de História Natural e Jardim Botânico da Universidade Federal de Minas Gerais to obtain further information about plant development and morphology. Measurements of reproductive characters were performed in both dry and fresh or fixed (70% alcohol) material. Terminology used to describe the overall morphology and indumentum follows Radford et al. (1976), but trichome typology was based on Roe (1972) and Mentz et al. (2000). Conservation status was assessed using the IUCN Red List Categories and Criteria (IUCN 2017) and for that, estimates of extent of occurrence (EOO) and area of occupancy (AOO) were calculated using the GeoCat tool (www.geocat.kew.org; Bachman et al. 2011) with the cell size of 2 km 2 for AOO. The criteria used for species delimitation is based on the morphological cluster species concept (Mallet 1995 Diagnosis. Differs from S. sublentum Hiern in its tomentose young stems, petioles and inflorescence axis with the indumentum composed of long-stalked (up to 1 cm) stellate-glandular trichomes with all rays glandular (versus pubescent-glandular indumentum composed of persistent simple glandular and persistent to early deciduous sessile to short-stalked stellate trichomes with only the midpoint glandular), in its straight stem prickles up to 17 mm long (versus recurved to oblique stem prickles up to 6 mm long) and in its large mature leaves 20.5-42 cm long and 20-38 cm wide (versus mature leaves 5.7-17 cm long and 3.8-14 cm wide).
Description. Shrubs up to 3.5 m, erect, moderately branched. Young stems terete, densely tomentose with hyaline to ochraceous stellate-glandular trichomes, these sessile to long-stalked with multiseriate stalks up to 1 cm long, multiangulate, the rays 5-20, 2-3-celled, unequal in length, all or almost all with a capitate glandular distal cell, the midpoint 2-3-celled, equal to or twice the length of the longest ray, the distal cell glandular; stems densely armed with prickles up to 17 mm long and to 2.3 mm wide at the base, straight, slightly flattened, stramineous to yellowish at base, becoming ferruginous towards the apex, pubescent with stellate trichomes like those of the stems and some small, stalked, uniseriate glandular trichomes at the base; bark of older stems greyish dark brown. Sympodial units difoliate to plurifoliate, the leaves not geminate, the leaves arranged in a 2/5 phyllotaxic spiral. Leaves simple, lobed, 20.5-42 cm long, 20-38 cm wide, the blade broadly elliptic to broadly ovate, membranous, discolorous, green adaxially and whitish light green abaxially when fresh, becoming dark green adaxially and light green to pale brown abaxially when dried; adaxial surface densely stellateglandular tomentose but always visible, with multiangulate trichomes, these short-to long-stalked, with multiseriate stalks 3-4 cells wide, up to 1 mm long, the rays 4-11, 1-celled, all eglandular or with one or more glandular ones (then 2-3-celled), unequal in length, the midpoints 2-3-celled, usually longer than the rays, mixed with smaller porrect to antrorse, usually eglandular stellate trichomes, these sessile to short-stalked (stalks to 0.1 mm long), the rays 2-5, 1-celled and minute, inconspicuous, unbranched, subsessile uniseriate glandular trichomes; the abaxial surface densely stellate-glandular tomentose, the epidermis barely visible, with trichomes like those of the adaxial surface, but more densely distributed; sparsely to moderately armed along the midrib and the primary veins of both surfaces with straight, laterally compressed prickles reaching up to 10 mm long and to 1.3 mm wide at the base adaxially, up to 17.5 mm long and to 1.8 mm wide at the base abaxially; primary veins 5-7 pairs; base cordate, the two major basal lobes obtuse to rounded, 2.5-7 cm long at the longest point, often overlapping each other over the petiole, not decurrent on to the petiole; margins with the lateral lobes 1.5-4.8 cm long, 4-9 cm wide at base, acute or less often obtuse or rounded at the apex, both basal and lateral lobes sometimes with small secondary lobes; apex acute; petiole 4.5-19.5 cm, densely tomentose with trichomes like those of the stem, armed. Inflorescence a scorpioid cyme, usually unbranched, rarely forked or trifurcate, internodal or subopposite the leaves, the axis densely glandular tomentose with trichomes like those of the stem, but these hyaline to ochraceous, armed; peduncles 2.6-6 cm long, the rachis 4.3-11 cm long, with 11-35 flowers, with up to 3 open at the same time; pedicel insertions generally unequally spaced, adjacent to spaced 2.3 cm apart; pedicels 4.8-18 mm long in open flowers, straight, articulated at base, armed, densely tomentose with trichomes like those of the stem, but with the epidermis and trichomes often purple-coloured. Flowers 5-merous, the plants andromonoecious, producing hermaphroditic flowers (long-styled) and functionally male short-styled flowers, which vary in proportion (number of long-vs short-styled flowers) between inflorescences. Calyx somewhat urceolate, inflated, foliaceous, purple (mainly along the margins and apex of the calyx lobes) to green, armed, densely tomentose with the epidermis barely to not visible basally, becoming gradually more visible towards the apex of the lobes, with trichomes like those of the stem but these sometimes purple and with some eglan- Figure 1. Line drawing of Solanum kollastrum. A habit with notably dense prickles, leaves lacking secondary lobes and internodal inflorescences B detail of the prickly inflorescence with a hermaphrodite flower at anthesis C detail of a dissected flower D detail of the fruits enclosed by the strongly accrescent fruiting calyces (with the uppermost fruiting calyx opened to expose the fruit) from Gouvêa 102 (BHCB). dular rays; base rounded, markedly plicate on the fusion line at the base of the adjacent sepals, these basally concave, the calyx tube 4.5-8.2 mm long, 9.4-15.2 mm in diameter at the point with the largest diameter, the lobes 7.5-15.6 mm long, 6-9 mm wide at the base, triangular, the margins plane to strongly undulate and revolute, the apices acute to caudate. Corolla 2.3-3.9 cm in diameter, purple to lilac or bluish-lilac, stellate, lobed 2/5 to 1/2 of its length, interpetalar tissue absent, the tube 1.1-2.2 cm long, the lobes 10.9-15 mm long, 8.8-13.4 mm wide, deltate to triangular, the margins straight Figure 2. Solanum kollastrum. A plant habit B detail of stem prickles C young inflorescence (upper right corner: detail of a more developed inflorescence) D flowering calyx E a short-styled and a long-styled flower displaying the extremes of variation of corolla size and colour found in the species (here exhibited by flowers of the same inflorescence); also note the various degrees of anther curvature and location of the apical pores compared with the images F and G F long-styled flower (hermaphroditic) with extrorse pores and slightly outwardly curved apices G short-styled flower (functionally male) with extrorse pores and markedly outwardly curved apices H infructescence with details of the strongly accrescent fruiting calyces (one of which was dissected to show the fruit) and the mature fruit colour (left side: details of fruit shape; right side: detail of a dissected fruit showing the four locules, placentation, seed colour and shape). Scale bars: 1.2 m (A); 3 cm (B, C, H); 1.5 cm (D, F, G); 1.8 cm (E). Photographs by Y.F. Gouvêa. to slightly convex at base, the apex acute, apiculate or not, stellate-glandular tomentose abaxially with trichomes like those of the leaves, almost glabrous adaxially with trichomes sparsely distributed along the veins and near the apex. Stamens equal; filament tube 1-2.1 mm long; free portion of the filaments 1.3-2.9 mm long, glabrous; anthers 7.5-10 mm long, 2.8-4.3 mm wide, 2.4-2.9 mm thick at the widest point, slightly gibbous, broadly lanceolate, narrowed towards the apex, sagittate at base, connivent, with the pores directed to apex and slightly extrorse, the epidermis papillose, slightly swollen dorsally. Ovary conical to somewhat cupuliform, 4-lobed, 4-locular, densely stellate-glandular tomentose at the apex, becoming glabrous with age, the trichomes 2-7-rayed, stellate, sessile, with a 2-4-celled, eglandular or glandular midpoint longer than the 1-celled rays; style 13.7-15.9 mm long in long-styled flowers, 1.2-3.7 mm long in short-styled flowers, cylindrical, glabrous; stigma globose to clavate, up to 1.4 mm long in long-styled flowers, papillose, green when fresh. Infructescence axis up to 29 cm long. Fruit a widely depressed ovoid to obloid berry, 11.4-20 mm long, 12-22.5 mm wide, the pericarp smooth, pale green to white, with scattered stellate trichomes at the apex; fruiting pedicels 1.4-2.2 cm long, armed; fruiting calyx strongly accrescent, completely covering the fruit in all stages of development, the tube 16-20.4 mm long and 19-34 mm in diameter at the widest point, the lobes 11-21.8 long, 13.7-19 mm   (Fig. 4). The known S. kollastrum habitats vary from environments subject to periods of drought (e.g. the edge of small seasonal semi-deciduous forest fragments or vegetation islands on inselbergs) to constantly wetter environments, at the edge of the aforementioned coastal forests, where the climate is under a strong oceanic influence. Its observed elevational range is from sea level to about 900 m. Field observations as well as its anther morphology (i.e. poricidal dehiscence and the anthers' robustness) suggest that its primary pollinators are medium-to large-sized bees (e.g. genus Ptiloglossa) with buzzing behaviour (Michener 1962, Buchmann 1983. Solanum kollastrum fruits hang outside (below) the foliage on long inflorescence axes and are enclosed until their maturity by an inflated Physalis-like calyx. This, along with the persistent green to white epicarp colour, the fleshy mesocarp, the numerous relatively small seeds and the release of a mild sweetish scent at fruit maturity are characteristics associated with fruits eaten by bats (Van der Pijl 1972, Cooper et al. 1986, Charles-Dominique and Cockle 2001. Actually, several studies have shown the importance of the fruits of Solanum species in bat diets (Marinho-Filho 1991, Passos et al. 2003, Zanon and dos Reis 2007, Mello et al. 2008a) and the role of bats as dispersal agents for Solanum species (Uieda and Vasconcellos-Neto 1985, Iudica and Bonaccorso 1997, Galindo-Gonzáles et al. 2000, Mello et al. 2008b). Many other Solanum species also present such features (e.g. those here considered morphologically related to S. kollastrum; see discussion). However, species-level studies on pollination or fruit dispersal of Brazilian Solanum species are virtually non-existent, although being fundamental to confirm and better understand the interactions between these species and their pollinators and dispersal agents.
Phenology. Flowering specimens were found from April to November, when immature fruits were also observed, indicating that Solanum kollastrum may bloom throughout most of the year. Specimens with mature fruits were observed at the end of June.
Etymology. The epithet kollastrum is derived from the Greek words for glue (κόλλα) and star (άστρον), referring to the notable stellate-glandular trichomes observed on the younger stems, petioles and inflorescence axis of this species.
Preliminary conservation status. Endangered (EN) B2 a, b (ii, iii, iv); Extent of Occurrence (EOO) 32,626 km 2 (NT); Area of Occupancy (AOO) 20 km 2 (EN). Despite the relatively large EOO (>20,000 km 2 ) of S. kollastrum, its small AOO (<500 km 2 ), the few and disjunct collections, all outside protected areas and the vulnerability of its habitats, lead us to suggest it should be attributed an Endangered status (IUCN 2017).

Discussion
Solanum kollastrum is morphologically related to a group of species endemic to the south-eastern Brazilian Atlantic Forest that share strongly accrescent fruiting calyces, large leaves with decurrent bases and large, robust flowers (see Fig. 2). This unnamed group appears to include five known species (i.e. S. hexandrum Vell., S. kollastrum, S. robustum H.Wendl., S. stagnale Moric., and S. sublentum). Of these, three species (S. hexandrum, S. robustum and S. stagnale) were sampled in the molecular phylogeny of Stern et al. (2011), forming a moderately supported clade sister to the clade that includes species traditionally placed in Solanum section Erythrotrichum A.Child. Although Stern et al. (2011) included both of these groups in the Erythrotrichum clade, the lineage containing S. kollastrum and related species may deserve recognition as a separate clade, emphasising its morphological, ecological and geographical distinctive nature.
Amongst the species in this group, only S. kollastrum and S. sublentum have glandular trichomes on the entire plant (see Fig. 3) and cordate leaf bases. Decurrent leaf bases of S. kollastrum are only seen in the first leaves of the seedlings, with the subsequent leaves gradually changing shape to become cordate and non-decurrent. In contrast, the leaf bases in S. hexandrum, S. robustum and S. stagnale remain decurrent throughout the plants' life, varying in shape from attenuate to truncate. Solanum kollastrum most closely resembles S. sublentum, of which it can be readily distinguished by the robust long-stalked (up to 1 cm) stellate-glandular trichomes with all rays having a glandular distal cell (some rays may lose the glandular cell through breakage or by the disruption of the gland wall) composing the indumentum of its young stems, petioles and inflorescence axis (see Fig. 3A; trichomes in S. sublentum are mostly simple). The shape and length of its stem prickles and the robustness of its leaves also are useful for the distinction between these species (see diagnosis for more details). Although easily differentiated, Solanum kollastrum and S. sublentum have very similar floral morphologies, sharing well-developed calyces that are strongly accrescent in fruits, showy purple to lilac corollas and robust anthers (see Fig. 2). Their leaves also resemble each other: both are lobed (with secondary lobes or not), elliptic to ovate (or broadly ovate in S. kollastrum) and have cordate bases (varying from truncate to cordate or sagitate in S. sublentum). In addition, the glandular nature of their trichomes, although they differ in type, is also a common character to both species. In the field, S. kollastrum has notably larger leaves than those of S. sublentum, however, usually only the apices of the branches are collected, with the fully developed leaves not represented in herbarium material, so this character is often not apparent from herbarium specimens. The diameter of the stems at the middle portion of the internode between the two youngest mature leaves is, in most cases, an additional distinguishing character between these species (0.9-3 mm in S. sublentum and 3.8-6.6 mm in S. kollastrum). Despite the fact that S. kollastrum and S. sublentum occur in similar environmental conditions (associated with outcrops or at edges of lowland forests, see Fig. 5), they have not been observed in sympatry.
The size and colour of the S. kollastrum corollas, the shape of its anthers and density and shape of its stem prickles are quite variable. The corollas of the examined specimens vary from 2.3 to 3.9 cm in diameter and from purple to bluish-lilac, with flowers exhibiting sometimes the extremes of variation of these characters in the same inflorescence (see Fig. 2E). The anther shape and the position of the apical pores also varies considerably; the anthers of plants from the type locality are straight (typical) with slightly extrorse apical pores, while those of plants from the coastal region have apices with varying degrees of curvature outwards from the cone, with pores markedly extrorse (see Figs 2E-G). Despite the observed variability, apically curved anthers are only found in S. kollastrum when compared to morphologically similar species. This distinct anther morphology may reflect differences in the plant-pollinator interaction, being an interesting issue for further investigation. The length of trichome rays and midpoints is also variable; plants collected in Caatiba, Bahia, have stem, petiole and inflorescence axis trichomes with rays and midpoints much longer than those specimens from other localities.
Plants growing in open restinga vegetation sites exhibit distinct architecture. These plants are lower and wider in their overall appearance due to the branching near the base of the major stem, with which the first order branches form angles close to 90° (see Fig. 5C). Plants from other habitats are more erect and become taller, with the first order branches forming angles close to 45° (habit with Y-shaped overall appearance; see Figs 5B, 5D and 2A). Differences in density and shape of the stem prickles between populations from inland and coastal areas is also observed, with the coastal populations possessing moderately distributed stem prickles with slightly broader bases, rather than the densely distributed narrowly based needle-like prickles of inland populations.
The discovery of S. kollastrum, a robust and conspicuous plant growing at the roadsides in regions close to large urban centres, highlights how insufficiently known the Brazilian flora is, even at present, and how urgent the need is to describe, study and conserve the country's plant diversity. Thus, we hope that this discovery encourages the study on the most diverse aspects of this species' biology.