A revision of the fern family Osmundaceae in Brazil

As part of floristic surveys in the Southern Cone of South America and the Flora do Brasil 2020 project, we present a revision of Osmundaceae in Brazil. Osmundaceae is represented by two genera ( Osmundastrum and Osmunda ) and three species. One of them, Osmunda piresii , is endemic to the savannas of Central Brazil, occurring in the states of Goiás, Minas Gerais


Introduction
The royal ferns (Osmundales) are the most ancient surviving lineage of leptosporangiate ferns (Bomfleur et al. 2017).The order comprises two families.One of them is the Guaireaceae, which became extinct during the Early Jurassic.The Guaireaceae has seven recognized species, and one of them, Guairea carnierii, has fossil records from the Rio Grande do Sul state in southern Brazil (Late Permian to Middle Triassic - Bomfleur et al. 2017).The other family is the Osmundaceae, with 18 extant species currently classified into six genera, as follows: Claytosmunda, Leptopteris, Osmunda, Osmundastrum, Plenasium, and Todea (PPG I 2016).This small group of ferns is remarkable in many respects.Its members represent the earliest lineage of all leptosporangiate ferns, with features that have been interpreted to be intermediate between eusporangiatae and leptosporangiatae (Bomfleur et al. 2015).The only extant family of this lineage, Osmundaceae, is characterized by unique and very distinctive rhizome anatomy (Hewitson 1962), with a two-layered cortex of stems and stipes, differentiated into inner, primarily parenchymatous cylinder, and outer sclerenchymatous cylinder.The stipes have a pair of stipular wings, and the tips of the stipe bundle are incurved, i.e., they are more or less horseshoeshaped.The peripheral xylem siphon is typically presented with leaf gaps (Bomfleur et al. 2017).The sporangia are arranged without a definite soral-type organization but with a rudimentary pathlike annulus, which is distinct from all other sporangia of leptosporangiate ferns (Gifford & Foster 1989).Phylogenetic studies have been carried out in the last 20 years and have supported the monophyly of the family and its current circumscription (Yatabe et al. 1999;Schuettpelz & Pryer, 2007;Metzgar et al. 2008).
Acta Botanica Brasilica, 2022, 36: e2020abb0537 Osmundaceae has a rich fossil record that can be traced back to the late Paleozoic.Fossils belonging to this family largely consist of permineralized stems (Gould 1970;Miller 1971), but compression-impression of fertile leaves have also been found (Naugolnykh 2002).Permineralized stems described as Palaeosmunda (Gould 1970) from the Upper Permian of Australia possess several characters with "osmundaceous" affinity, suggesting that the family probably arose in the Southern Hemisphere and subsequently dispersed from there (Skog 2001).Despite these Permian records, during the Mesozoic, Osmundaceae reached a more extensive distribution in both hemispheres, with a greater diversity of compressed and permineralized materials in the fossil record (Escapa & Cúneo 2012).
In Brazil, and South America more generally, extant representatives of Osmundaceae have been treated in regional floras (i.e., Capurro 1961Capurro , 1969;;Sehnem 1967;Charpin & Novara 1995;Tryon & Stolze 1990;Prado 2004;Arana & Ponce 2015;Kessler & Smith 2017) and catalogues (Hassler 1928;Capurro 1938;de la Sota & Ponce 2008;Sylvestre 2010).A list of lycophytes and ferns from Brazil was presented in the Catalog of Plants and Fungi of Brazil (Prado & Sylvestre 2010), where the family is represented by two genera and two species, as it does in the synthesis published by Prado et al. (2015).
Studies of herbarium specimens and fieldwork have shown that the Brazilian "osmundaceous" fern flora is overlooked.It is therefore necessary to update the taxonomy, nomenclature, and distribution of the extant representatives of these ferns in Brazil.Thus, the goal of the present study is to present a taxonomic revision of Osmundaceae in this country including an identification key, morphological descriptions, diagnostic illustrations, and ecological remarks for all species.

Materials and methods
This study was based on a critical review of relevant literature, morphological data gathered from living specimens during fieldwork, and an examination of collections housed at BHCB, HB, MBM, MBML, R, RB, RBR, RFA, SI, SF, and UFMT herbaria.We also analyzed specimens received on loan and/or electronic images from the following herbaria: ALCB, B, BR, CEPEC, CESJ, FR, FUEL, HUEG, HUFSJ, HURB, K, LE, LINN-HL, NY, P, PACA, S, SJRP, SP, SPF, UB, UCS, UEC, UPCB, and US (acronyms according to Thiers 2020, continuously updated).The complete list of examined exsiccates is provided List S1 in the supplementary material.We studied the original description and type specimens of all names cited for Brazil, and the relevant information referred to the distribution and habitat features.All taxa were arranged alphabetically, and author names were abbreviated according to the International Plant Names Index (IPNI).

Results and discussion
Osmundaceae is represented in Brazil by two genera, Osmunda and Osmundastrum, and three species, Osmunda piresii, O. spectabilis, and Osmundastrum cinnamomeum.The richest genus is Osmunda, with two species, one of them, Osmunda piresii, endemic to Brazil.
Osmundaceae occurs in all states of the country's Central West, Southeast, and South regions, as well as the state of Bahia in the Northeast.Although this is a family with a nearly cosmopolitan distribution and wide occurrence in the Neotropical region, it is practically absent in Brazil's North and Northeast regions (Fig. 1A).There are scattered records, which could not be checked due to the absence of images in virtual herbariums: one collected in Serra dos Carajás, Pará state (Dayle & Callejas 1803, IAN), identified only as Osmunda, and another one collected in the region of Matriz do Camaragibe, Alagoas state (Lyra 7894, TEPB), with no genus assigned.The species are found in the Atlantic Forest, Cerrado, Pampa, and Pantanal biomes.Remarkably, the family is absent in the Amazon and Caatinga biomes.
Terrestrial plants, with mostly unbranched, erect, or shortly creeping, ascending, sometimes treelike trunk, clothed in roots and persistent petioles, hairy at the apex.Rhizome anatomy distinctive, an ectophloic siphonostele (with a pith of parenchyma in center and phloem outside of vascular cylinder only), with a ring of discrete xylem strands, conduplicate or twice conduplicate in crosssection.Fronds 1-or 2-pinnate, bearing uniseriate hairs, these deciduous or persistent at axes, dimorphic or hemidimorphic; petiole caespitose, helicoidally arranged, with laterally winged stipules at bases, bearing mucilaginous hairs when young, with a single U-shaped vascular bundle; sclerenchyma strongly developed; base of lateral pinnae almost distinctly articulate or not; pinnule base auriculate or not; veins free, subpinnately furcate.Sporangia following veins or entirely covering strongly contracted fertile segments, not assembled in sori, sporangia with 128-512 spores, opening in an apical slit, annulus lateral; spores green, subglobose, trilete; gametophytes green, cordate, superficial.n = 22.
Six genera and about 18 species in temperate and tropical regions worldwide (PPG I 2016).Two genera and three species (one endemic) in Brazil.Terrestrial plants.Rhizome erect to shortly creeping, stout, woody, without scales.Fronds dimorphic or hemidimorphic with dimorphic pinnae; petioles arising as a crown at the apex of the rhizome, more or less hairy when young, base of petiole swollen and with lateral flaplike stipules; laminae 2-pinnate, fertile portions positioned apically, reduced to a midrib with almost no laminae present; pinnae not articulate to the rachis.Sporangia large, naked, with a small patch annulus.
Five species; distribution nearly worldwide across tropical and temperate regions, two species in East and Southeast Asia, one in Europe, and two species (and one hybrid) in the New World, both present (one endemic) in Brazil.Osmunda piresii differs from O. spectabilis in the number of pair of pinnae (2-4 pairs x 7-12 pairs), form of the segments (ovate to elliptic x oblong to elliptic), and sporangia distribution (interrupted x continuously distributed in fertile axes -Fig.3B).Osmunda piressi has terminal pinnulae proportionally larger than the lateral ones (Fig. 3A).
This species is endemic in the central part of Brazil, and it has been recorded in the states of Goiás, Mato Grosso, and Minas Gerais.It grows in wet fields, banks of streams This species has been classically treated as a synonym, variety, or subspecies of Osmunda regalis (Löve & Löve 1977;Smith 1981;Mickel & Beitel 1988;Tryon & Stolze 1989(1990);Palacios-Ríos 1990, 1995;Kessler & Smith 2017), a European species that does not occur in America (Arana & Ponce 2015;2016).
The species occurs throughout the New World, from Canada to Argentina and Uruguay.In Brazil, it occurs in Bahia, Distrito Federal, Espírito Santo, Goiás, Mato Grosso, Mato Grosso do Sul, Minas Gerais, Paraná, Rio de Janeiro, Rio Grande do Sul, Santa Catarina, and São Paulo.It can be found in the Cerrado and Atlantic Rainforest biomes, in ombrophilous or semideciduous seasonal forests, sandy coastal plains (restinga), and riverine forests.It grows in wet or marshy fields, streams, exposed hillsides, grasslands, and floodplains, in sunny or shaded places, from sea level to 1,700 m in elevation.
In the protologue of Osmunda gracilis, Link (1833) characterized the species mainly on the basis of the last segments ("pinnulae basis subauriculatae") and the overall reduced size of the specimen.After a morphological study of the holotype (Fig. 2B), we conclude that Osmunda gracilis was described using a specimen (collected in America meridionali?)under the morphological variation of Osmunda spectabilis and hence we propose synonymizing Osmunda gracilis under Osmunda spectabilis.Terrestrial plants, moderate-sized to large.Rhizome erect, stout, woody, without scales.Fronds dimorphic; petioles arising as a crown at apex of rhizome, ± hairy when young, base of petiole swollen and with lateral flaplike stipules; laminae pinnate-pinnatisect, fertile portions reduced to a midrib with almost no laminar tissue present; pinnae articulate to rachis.Sporangia large, naked, with a small patch annulus.
One species; nearly worldwide in tropical and temperate regions in Asia and the Americas.

Figure 4 .
Figure 4. Osmunda spectabilis Willd.A-General aspect of the fertile frond; B-Detail of fertile pinna, with sporangia completely covering the surface.Images: P. Labiak.