Serpocaulon demissum (Fée) D. Sanín, comb. nov. (Fig. 2, 3, 4, 5B–C, 6C–D, 7B).

Goniophlebium demissum Fée, Cryp. Vasc. Brésil 2: 63. 1872.

Polypodium catharinae var. rotundatum Christ, Bull. Herb. Boissier ser. 2, 2: 372 (1902).

Polypodium demissum (Fée) C. Chr. Index Fil. 325. 1906. Type:— BRAZIL. Rio de Janeiro: Jurujuba, Santa Cruz [Santa Cruz da Barra], 7 April 1872, A. Glaziou 5651 (lectotype P [P171187], here designated; isolectotypes P [P171187], P [P00624706], P [P00624705]).

Etymology: —The Latin epithet demissus means hanging down, related to the pendulous laminae.

Plants rupicolous (growing in leaf litter over rocks). Rhizomes 5−12 mm in diameter, short-creeping, light to dark brown, moderately pruinose. Scales dense along rhizomes, 4−9 × 2−3 mm, concolorous, light brown, lanceolate, subpeltate, insertion radially folding, patent, bases rounded, apices long-acuminate, caudate, with scattered pale marginal projections 1−2 mm long, especially at the base. Phyllopodia 1.0− 1.8 cm apart, 2−5 mm long. Fronds 19.2−62.0 cm long, erect. Petioles 6.5−29.0 cm, light brown, sinuate at the base, proximally and distally subterete. Laminae 12−34 × 4−14 cm, pinnatisect, lanceolate, truncate proximally, apex gradually reduced to a short-attenuate segment. Segments in 26−38 pairs, chartaceous, slightly revolute, proximal surcurrent and reflexed, medial decurrent, and apical pinnatisect, glabrous or sparsely pubescent with light brown to hyaline hairs, 3−18 cells long, catenate, strigose, scattered, mainly in axils of segments and rachis; scales bicolorous, dark brown at center, hyaline at margins, 1.0−3.2 × 0.15−0.24 mm, 10−26 × 2 cells wide, linear, subpeltate, sinuate, rounded and appressed at the base, each with a long-acuminate patent apex, dentate, mainly in axils of segments and rachis. Medial segments 2−6.5 × 0.4−0.9 cm. Veins forming 13−25 rows along and 1−2 rows of areoles between the costa and the margin of the segment, fertile veinlets usually inconspicuous. Sori in 6−23 × 1(rarely 2) rows per segment, not reaching apices of segments. Spores 52−56 × 30−35 µm, monolete, ellipsoid to plano-convex, with verrucate laesurae 23−29 µm long (Fig. 6C–D).

Distribution & habitat:— Serpocaulon demissum is endemic to the Brazilian inselbergs of the Atlantic Forest ecosystem (Fig. 1, 4), between [200] 560–1850 m, known from Bahia, Espírito Santo (Fig. 1), Minas Gerais, and Rio de Janeiro States.

Additional specimens examined:— BRAZIL. Bahia: Rio de Contas, Pico das Almas, vertente leste, vale acima da Fazenda Silvina, 1450 – 1500 m, 29 November 1988, R.M. Harley & B.L. Stannard 26677 (K); Rio de Contas, Pico das Almas, 25 km da cidade em direção ao Campo do Queiroz, 1850 m, 13º33’S, 41º57’W, 26 February 2006, F.B. Matos et al. 1049 (RB). Espírito Santo: Castelo, Parque Estadual de Forno Grande, Trilha para o Forninho, 1100 m, 20º30’58” S, 41º05’01” W, 12 February 2008, P.H. Labiak et al. 4566 (RB); Castelo, Parque Estadual de Forno Grande, 1300 m, 20º30’58” S, 41º05’20” W, 26 June 2008, A. Salino et al. 13607 (BHCB); Pancas, Pedra da Colina, 745 m, 19º13’52” S, 40º52’36” W, 11 March 2016, L.F.A. de Paula 894 (RB); Santa Maria do Jetibá, Garrafão, Pedra do Garrafão, 1081 m, 20º10’24.5” S, 40º55’06.8” W, 28 August 2009, A. Salino et al. 14539 (BHCB); Santa Maria do Jetibá, Pedra do Garrafão, depois da cultura do morango, 20º10’24.5” S, 40º55’06.6” W, 1079 m, 22 September 2018, D. Sanín et al. 7229 (BHCB, CESJ, F, HUA); Santa Teresa, Pedra da Onça, 1 February 2000, V. Demuner et al. 688 (BHCB). Minas Gerais: Dores de Guanhães, Serra do Caraça, 700 m, 19º04’14.3” S, 42º52’23.2” W, 15 August 2005, T.E. Almeida et al. 82 (BHCB); Teófilo Otoni, afloramento rochoso lado esquerdo da MG 418, cerca de 30 km norte Teófilo Otoni, em ilha de vegetação de afloramento granítico, 560 m, 17º51’22” S, 41º15’39” W, 27 January 2014, L.F.A. de Paula et al. 686 (BHCB); Teófilo Otoni, afloramento rochoso lado esquerdo da MG 418, cerca de 30 km norte Teófilo Otoni, em ilha de vegetação de afloramento granítico, 560 m, 17º51’22” S, 41º15’39” W, 16 April 2011, L.F.A. de Paula et al. 334 (BHCB); Teófilo Otoni Afloramento rochoso lado esquerdo da MG 418, cerca de 30 km norte de Teófilo, 560 m, 17º51’22” S, 41º15’39” W, 16 April 2011, L.F.A. de Paula et al. 336 (RB). Rio de Janeiro: Niterói, Parque Estadual da Serra da Tiririca, Pedra de Itacoatiara, 3 December 1994, M.G. Santos & F.C. Pinheiro 62 (RB); Niterói, Parque Estadual da Serra da Tiririca, Pedra de Itacoatiara, 20 March 1994, M.G. Santos & F.C. Pinheiro 51 (RB); Niterói, Morro do Tucum, Itacoatiara, 7 July 2012, L.P. Mauad 306 (BHCB, RB).

Discussion:— The distribution of Serpocaulon demissum is similar to described inselbergs endemics species: Mandevilla fistulosa Ferreira de Sales (2006: 115), M. grazielae Ferreira de Sales (2006: 117), and M. harleyi Ferreira de Sales (2006: 121), (Apocynaceae) (Ferreira de Sales et al. 2006), and Bradea borreroides (Oliveira & Sobrado (2016: 84) (Rubiaceae). Its altitudinal distribution is similar to Nanuza plicata Martius (1824: 16) Smith & Ayensu (1976: 38) (Velloziaceae), which colonizes rocky substrates from the seacoast to more than 1500 m.a.s.l. (Porembski & Barthlott 2000). Remarkably, this area corresponds to a recently recognized phytogeographical region for endemic bromeliads in the Atlantic Forest in Brazil (de Paula et al. 2016) from the states of Bahia to Rio de Janeiro.

Serpocaulon demissum was found at the margins of monocotyledonous mats containing principally species of Bromeliaceae and Velloziaceae. These mats are fundamental for providing establishment sites for other plant lifeforms (Porembski et al. 2000), because they accumulate organic matter between their roots (Porembski & Barthlott 2000).

Recent botanical exploration in the inselbergs localities of Linhares (Espírito Santo) and Teófilo Otoni (Minas Gerais), culminated in the description of two new endemic species of monocots (Viana & de Paula 2013, Gonçalves & de Paula 2016), and four eudicots (Ferreira de Sales et al. 2006, Oliveira & Sobrado 2016, Gouvêa et al. 2018). These discoveries show that these outcrop ecosystems are highly diverse, and still relatively unexplored (Giulietti & Pirani 1988, Porembski & Barthlott 2000, Porembski et al. 2000, de Paula et al. 2016, 2017).

Similar species and nomenclature:— Serpocaulon demissum resembles S. catharinae and S. vacillans (Table 1, Figs. 5−7), by sharing short-creeping rhizomes (except for S. vacillans, which has long-creeping rhizomes) and pinnatisect laminae with segments having predominantly one row of sori between the costae and the segment margins. It possesses moderately pruinose and rugose rhizomes as in S. catharinae and has sinuate petiole bases like S. vacillans.

Serpocaulon demissum differs from S. catharinae by having concolorous, larger (4−9 × 2−3 mm vs. 2.1−3.7(−7.9) × 0.4−1.9 mm) lanceolate rhizome scales (Fig. 5B and C), bullate at insertion, with scattered pale marginal prolongations of the margin cells 1−2 mm long, especially at the bases (Fig. 5C), petioles proximally sinuate (Fig. 3D), inconspicuous veinlets (Fig. 3I), and spore ornamentation lacking folded perine (Fig. 6C & D) (vs. bicolorous subulate rhizome scales (Fig. 5A) with dentate margins, straight petiole bases, conspicuous veinlets, and spore ornamentation with folded perine (Fig. 6A, B)).

From Serpocaulon vacillans, S. demissum differs by the superficially rupicolous rhizomes (Fig 3B, C), lanceolate rhizome scales (Fig. 5B), laminae glabrous or with sparse trichomes 3–18 cells long, scales distributed mainly in the axils of the segments, and spore ornamentation lacking folded perine (Fig. 6C & D) (vs. subterranean rhizomes, deltate to ovate-lanceolate rhizome scales (Fig. 5D), dense laminar pubescence with hairs 2–3 cells long, with scarce (if any) linear scales in the base of segments, and spore ornamentation with folded perine (Fig. 6 E & F)).

Hensen (1990) presented the name Goniophlebium demissum Fée as a new synonym for Polypodium catharinae. However, the author did not present information of the spores and the rhizome scales to support his conclusions. This information is presented here, and along with its distribution it is possible to recognize it as part of Serpocaulon ’s diversity.

Rhizome starch accumulation:— The presence of thick rhizomes supports that S. demissum developed a specialized system to store nutrients and water. Similar adaptations have been noted for several taxonomical groups in Brazilian inselbergs (Barthlott & Porembski 2000b, Conceiçao & Pirani 2005, Alves & Kolbek 2010, Porembski et al. 2000).

In a comparison with its relatives, all the species evaluated contain starch in their rhizome. However, S. demissum differs of S. catharinae because it presents starch in the whole rhizome (Fig. 7B) (vs. only around the vascular bundles (Fig. 7A)). It shares a similar starch distribution with S. vacillans but this species differs in the lack of a dense cuticle and lower amount of starch (Fig. 7C). Hovenkamp et al. (2016) evaluated the seasonal accumulation of starch in trophopods of the temperate fern Matteuccia struthiopteris (Linnaeus 1753: 1066) Todaro (1866: 235) (Onocleaceae) explained their results with the production of seasonal leaves, which was correlated with the temperate seasonality. We believe that the thick rhizomes of S. demissum similarly represents a functional trait that provides advantage in this harsh environment.

Conservation assessment:— Serpocaulon demissum is considered eligible for IUCN listing as Endangered (EN) (IUCN 2017) on the basis of its Area of Occupancy (AOO): 36 km 2, which is far less than the 500 km 2 as it is recommended by the Geospatial Conservation Assessment Tool (GeoCat) (Bachman et al. 2011). According to the World Database of Key Biodiversity Areas (http://www.keybiodiversityareas.org/home), the population from Castello locality is the only one in a protected area (Parque Estadual de Forno Grande, Espírito Santo State). The global population is at risk from human impacts such as granite mining in inselbergs, installation of telecommunication towers, the use of outcrops for cultivation, the invasion of exotic grasses, and tourism (Safford & Martinelli 2000, Viana & de Paula 2013, Gonçalves & de Paula 2016, de Paula et al. 2016, 2017, Oliveira & Sobrado 2016).

Studies on rock-dwelling populations of rock ferns (Schneller & Holderegger 1996, Vogel et al. 1999, Suter et al. 2000) attributed their population structure to multiple events of single-spore colonization via intra-gametophytic selfing, promoted by its long-distance dispersion capacity (Perrie & Brownsey 2007, De Groot et al. 2012, Bauret et al. 2017). In this context, the low gene flow registered between populations of angiosperms from different inselbergs (Barbará et al. 2007, Palma-Silva et al. 2011) pointed that each inselberg might host genetically isolated populations (de Paula et al. 2016, Hmeljievski et al. 2017). Stressing that those species are more susceptible of extinction by small alterations. Because of the small population size, severe fragmentation of the already isolated populations resulting from its rocky outcrop distribution, this species should be a priority candidate for conservation efforts.