Solanum lagoense (Solanaceae, Geminata clade), a new species from Lagoa Santa, Minas Gerais State, Brazil

Abstract A new species of Solanum (Solanaceae) from the Geminata clade is described for the Brazilian flora. Solanum lagoense Stehmann is only known from Lapinha, a rocky massif located in the Lagoa Santa karst region of Minas Gerais State. The flora of this area, including Solanaceae, was studied in detail in the second half of the 19th century by the Danish botanist Eugene Warming. The species differs from other members of the Geminata clade in Brazil in its geminate leaves of different sizes, simple multicellular trichomes present on the new growth and young stems, short extra-axillary inflorescences with few (1-3) flowers, and its stellate corollas with cucullate and strongly reflexed lobes. Here we present a description, taxonomic comments and a preliminary assessment of conservation status of this critically endangered species.


Introduction
Solanum L. (Solanaceae) is one of the ten largest genera of fl owering plants, with 1,250-1,700 species distributed on all continents except Antarctica, but with its highest species diversity in the Neotropics (Frodin 2004;Nee 1999). Among the Solanaceae, Solanum is morphologically easy to recognize by its combination of anthers opening by apical pores and a usually evenly 5-lobed calyx. Th is combination of traits is not shared with any other genera in the family (Hunziker 2001). Important crops are found in the genus, such as potato (S. tuberosum L.), tomato (S. lycopersicum L.) and eggplant (S. melongena L.) that are widely cultivated around the world and contribute to the economies of many countries (Hawkes 1999).
Approximately 272 species of Solanum occur in the Brazilian fl ora, of which 131 are endemic to the country . Th e highest species richness and endemism are found in the Atlantic rain forest, a biome recognized as a biodiversity hotspot at a global level (Mittermeier et al. 2004). Th e Atlantic forest originally consisted of an almost continuous strip of land of variable width along the Brazilian coast. Today, this huge forest is represented by remnants and biologically impoverished fragments representing less than 12% of its original cover (Ribeiro et al. 2009). Despite this, several new species in Solanum have been described from the Atlantic forest in recent years (Giacomin et al. 2013;Giacomin and Stehmann 2014;Knapp et al. 2015), indicating that the inventory of the Brazilian fl ora is far from completion (Sobral and Stehmann 2009).
With more than 11,000 species of angiosperms, Minas Gerais State has been recognized as the richest in Brazil (Forzza et al. 2010;Forzza et al. 2012). Th is fl oristic richness is associated with the diversity of environments found in Minas Gerais: Atlantic rain forest, Cerrado (savanna-like vegetation), and Caatinga (dry and open thorn scrub). Transition areas between these main vegetation types, mainly those associated with the Espinhaço range, have received special attention since the 19th century, when European naturalists such as Auguste Saint-Hilaire, Carl F. Martius, George Langsdorff , and others travelled in the inner part of the country, describing its fl ora. Some of these botanists were based in Minas Gerais for long periods of time and explored particular areas in depth; these include the Swede Anders F. Regnell working in Caldas (Concha-Quezada 2011;Dahlgren 1962) and the Dane Eugene Warming in Lagoa Santa (Warming 1908).
Lagoa Santa is a karstic (limestone) region of the Serra de Espinhaço long known for its important paleontological and archeological sites (Berbert-Born 2002). Th e fi rst scientist to explore its countless caves was the Danish paleontologist Peter Wilhelm Lund (1801-1880), who found many exemplars of the Brazilian megafauna and human fossils. Th e botanist Johannes Eugenius Bülow Warming (1841Warming ( -1924 was Lund's secretary between 1863 and 1866. He collected and took to Europe over 3,000 dried plant specimens. Th ese, in addition to the more than 700 herbarium sheets donated by Lund, are today held in the herbarium of the Natural History Museum in Copenhagen (Gomes 2006). Many of these specimens are nomenclatural types and were cited in the Flora Brasilensis (Martius 1846). Warming distributed herbarium material to many specialists in Europe (Warming 1908). Th e Solanaceae were worked on by W. P. Hiern who described seven new species and two varieties of Solanum (Hiern 1876).
As part of a larger project following Warming's footsteps, we searched for species with few records and nomenclatural type populations in the same places where Warming collected in Lagoa Santa. During the development of this project, samples of an unusual species of Solanum from the Geminata clade were collected. Th is group is well studied and the Brazilian species of the group have recently been revised (Knapp et al. 2015). We compared our specimens with the others described for the clade and with Warming's collections kept in the Copenhagen herbarium (C) and other herbaria of the world. We could not match it with any known species and therefore recognize it as new, and describe it here.
We collected in Lagoa Santa from December 2014 to March 2015, and focused our eff orts on the areas surrounding the rocky massifs such as Lapinha, Sumidouro, and Morro do Baú. Th ese localities present unique environmental conditions due to higher degrees of shade that lead to higher humidity and temperature stability, thus contributing to diff erent species compositions than the surrounding savanna matrix (cerrado). Description. Shrub to 1.5 m, rhizomatous, with clonal reproduction; young stems terete, but slightly angled, glabrous or pilose with simple, uniseriate, and recurved trichomes, each with 8-15 cells; new growth always pilose, with stem obviously angled; bark of older stems brown, slightly winged from the leaf bases. Sympodial units difoliate, geminate, the leaves of a pair diff ering in size, but not usually in shape. Leaves simple; major leaves 5.6-12.4 cm long, 2.2-4.7 cm wide, elliptic, membranous, glabrous on both surfaces, the abaxial surface olivaceous to moss green, the adaxial surface dark green; major veins 7-9 pairs, drying somewhat darker than the lamina and slightly sunken on the adaxial surface, somewhat prominent and lighter on abaxial surface; base attenuate, sometimes slightly asymmetric; margins entire, slightly revolute; apex acute, the tip somewhat blunt; petiole 0.6-1.0 cm long, glabrous; minor leaves 1.6-2.9 cm long, 0.9-1.7 cm wide, differing from major leaves only in size and in having a shorter petiole. Infl orescences 0.2-2 cm long, extra-axillary, arising below the nodes, unbranched, with 1-3 fl owers, glabrous; peduncle ca. 3 mm; pedicels 1.4-1.5 cm long, ca. 0.3 mm in diameter, slender, abruptly swollen at the apex, spreading or pendant at anthesis, glabrous, articulated at the base; pedicel scars spaced 0.5-2 mm apart. Buds globose, the corolla strongly exserted from the calyx tube before anthesis. Flowers 5-merous, all perfect. Calyx with the tube ca. 1.0 mm long, broadly conical, the lobes 1.0-1.2 mm long, ca. 1.3 wide, triangular or obtuse, strongly refl exed at anthesis, glabrous adaxially, minutely papillate abaxially, the papillae denser at the tips. Corolla ca. 1.0 cm in diameter, white, stellate, lobed 2/3 of the way to the base, the lobes 1-nerved, ca. 4-5.2 mm long, ca. 2.4-3.6 mm wide, ovate, spreading at anthesis, glabrous, minutely papillate on the margins and the apex, the tips cucullate. Stamens ca. 3.5 mm long; fi lament tube ca. 0.7 mm long, the free portion of the fi laments ca. 0.3 mm long, glabrous; anthers 2.4-2.5 mm long, ellipsoid to slightly obovate, ca. 0.7 mm wide at the base, ca. 0.9 mm wide at the apex, yellow, poricidal at the tips, the pores large and introrse, lengthening to slits with age. Ovary glabrous; style 5-6 mm long, glabrous; stigma not expanded, blunt, the surface minutely papillate. Fruit a subglobose berry, slightly depressed, 1.2-1.3 cm long, 1.3-1.5 cm in diameter, green, darker toward the pedicel, the pericarp not markedly shiny, thick, the mesocarp not juicy; fruiting pedicels 1.7-2.2 cm long, less than 1 mm in diameter at the base, ca. 2 mm in diameter at the apex, gradually expanded to the apex, pendant and hidden under the foliage; fruiting calyx lobes somewhat hyaline, not markedly expanding in fruit, but clearly recurved. Seeds 15-30 per berry, fl attened, ellipsoid to irregularly ellipsoid or sometimes ovate-reniform, 3.2-4.0 mm long, 2.8-3.1 mm wide, dark brown, vernicose, with pale incrassate margins, the seed coat obscurely foveolate.

Solanum lagoense
Distribution. Known only from the type locality at the Gruta da Lapinha, Lagoa Santa, Minas Gerais, in southeastern Brazil.   Ecology. Solanum lagoense grows on well-drained soils in the understory of the seasonal forest (Floresta Estacional Semidecidual) that covers the entrance of caves as well as the canyons and blind valleys associated with the carbonatic rocky massifs of Lagoa Santa. Th is specifi c habitat is very stable with respect to temperature and humidity throughout the year, in comparison with Cerrado, the typical vegetation matrix in the region. An extensive subterranean system of rhizomes connects individuals in the populations we have sampled ( Figure 1B), indicating that this species is capable of vegetative reproduction. We observed no bees visiting the fl owers. Th e green fruits, hanging and hidden under the foliage, suggest dispersal by bats that inhabit the caves, but the natural history of this species is in need of detailed study.

Specimens examined (paratypes). BRAZIL. Minas
Phenology. Flowering specimens were collected in January, occasionally in March, while fruiting material was seen in January, February, and March.
Etymology. Th e name refers to Lagoa Santa, a Brazilian locality where two important Danish researchers, Peter Lund and Eugene Warming, worked in the mid 19th century. Warming started his botanical career here studying the Cerrado fl ora and its ecological relationships. Nowadays he is recognized as one of the Fathers of Ecology.
Preliminary conservation status (IUCN 2014). Critically Endangered (CR) B1, 2 a, b(ii, iii, iv). Th is species is known from a single locality, the Gruta da Lapinha, included in the Parque Estadual do Sumidouro, a protected area that encompasses 52 caves. Th ere is an increasing human pressure in its microhabitat near the base of the limestone walls, where many climbing routes are in constant use. Th e limestone outcrops have being mined for decades, drastically reducing the habitat of this species. Th e surrounding landscape is changing very quickly with the growth of the municipality of Lagoa Santa, infl uenced by the Vector North project that fostered the expansion of the metropolitan region of Belo Horizonte, the capital of the state (Auler and Piló 2015). All of these threats support an assessment of Critically Endangered. Eff orts to locate new populations in the conservation unit, as well as in similar habitats associated with caves outside it are needed.
Notes. Solanum lagoense is a small shrub with entirely glabrous leaves, short infl orescences, few small fl owers, and green fruits that are hidden below the foliage. Th ese characters are common in species belonging to Geminata clade, a group that is highly diverse in the Atlantic forest (Knapp 2002;Knapp et al. 2015). Solanum lagoense is similar to S. restingae, S. amorimii and S. psilophyllum Stehmann & Giacomin due to its glabrous and geminate, but not dimorphic leaves. Th e latter three species are distinguished by their glabrous stems, even on the new growth, and short fruiting pedicels (up to 1.5 cm long), whereas S. lagoense has clearly pilose young stems and longer fruiting pedicels. Solanum restingae is endemic to Bahia and Espírito Santo states and has a strongly winged stem and basally attenuate leaves. Solanum amorimii grows in southern Bahia, but also in far northeastern Minas Gerais; its stem is not winged, the leaves are somewhat auriculate at the base. Despite its occurrence in the region of the Serra do Cipó and the Iron Quadrangle relatively close to Lagoa Santa, S. psilophyllum has longer petioles (>1.5 cm) and leaves (>10 cm) and more fl owers per infl orescence (5-8).
Other species belonging to the Geminata clade recorded in the southern part of Espinhaço mountains in Minas Gerais are S. verticillatum Knapp & Stehmann, S. gnaphalocarpon Vell., S. intermedium Sendtn., and S. warmingii Hiern, the last three collected by Warming in Lagoa Santa and cited or described by Hiern (1877). It is noteworthy that after Warming's intensive collecting eff orts in Lagoa Santa (1863-1866), including the Lapinha and Sumidouro limestone outcrops, few new species have been described in the last decades. Th is can be due to Warming's extensive collecting or to the fact that few researchers have been collected recently in the area. Most collecting eff orts in the southern Espinhaço chain have been concentrated in rocky quartzite fi elds (campos rupestres) found in high altitude areas (above 900 m) that houses one of the richest fl oras of the Neotropical region, almost half of the species endemic (Echternacht et al. 2011;Giulietti and Pirani 1997).
At fi rst glance, S. lagoense also resembles species belonging to Solanum inornatum clade, but the trichomes, leaf arrangement, and number of seeds are quite distinct. While S. inornatum group shows trichomes with few cells (up to 4), geminate leaves diff ering in form, and translucent fruits with few seeds (up to 10) , S. lagoense has multicellular soft trichomes, with more than eight cells, geminate leaves equal in form and hard, green berries with more than 15 seeds per fruit.
Th e clonal reproduction in S. lagoense is noteworthy. All individuals of the population studied have horizontal rhizomes below the leaf litter, linking all the plants together, similar to other members of the Geminata clade such as S. arboreum of northern South America (Knapp 2002) and S. psilophyllum of the southern Espinhaço range in Minas Gerais. In Solanaceae, vegetative reproduction is common in the tuberbearing potatoes (Hawkes 1990;Spooner et al. 2014), and has also been reported in weedy species of the Leptostemonum clade growing in open places or forest margins such as Solanum viarum Dunal, S. palinacanthum Dunal, Solanum guaraniticum A. St.-Hil., and S. paniculatum L., all common species of southeastern Brazil (Mentz and Oliveira 2004). It appears clonal reproduction is widespread across Solanum, and it has been reported in the Cyphomandra, Morelloid, Dulcamaroid, and Brevantherum clades (Giacomin and Stehmann 2014;Vallejo-Marí n and O'Brien 2007). Th e extent of this habit and reproductive mode is not well-documented in Neotropical solanums largely because the underground parts are rarely collected or even observed in these woody plants (see Knapp 2002).
Lagoa Santa is considered an example of a well-catalogued site. Warming compiled a thorough collection listing 2,593 plant species (Warming 1908). Our discovery of this new species in Lagoa Santa strengthens the claim for more fl oristic and taxonomic inventories in Brazil, not only in poorly collected areas such as Amazonia (Sousa-Baena et al. 2014), but also in "well-studied" areas. In-depth fl oristic inventories in places with diffi cult access or with distinct and poorly documented microclimatic conditions, have often resulted in discoveries of new rare and endemic species, even in what appear to be well-catalogued sites.