Studies in Austral Bryaceae (Bryopsida). III. A Preliminary Account with Keys to Rosulabryum J.R. Spence in Chile

Abstract A preliminary study of the genus Rosulabryum J.R. Spence in Chile is presented, with brief species descriptions, notes on ecology and distributions, and a taxonomic key. The following 12 species are confirmed with vouchered specimens; Rosulabryumandicola (Hook.) Ochyra, Rosulabryumbillarderii (Schwägr.) J.R. Spence, Rosulabryumcampylothecium (Taylor) J.R. Spence, Rosulabryumcapillare (Hedw.) J.R. Spence, Rosulabryumcoloratum (Müll. Hal.) J.R. Spence, Rosulabryumdensifolium (Brid.) Ochyra, Rosulabryumlongidens (Thér.) J.R. Spence, Rosulabryummacrophyllum (Cardot & Broth.) Ochyra, Rosulabryumperlimbatum (Cardot) Ochyra, Rosulabryumpuconense (Herzog & Thér.) J.R. Spence, Rosulabryumrubens (Mitt.) J.R. Spence, and Rosulabryumtorquescens (Bruch ex De Not.) J.R. Spence. Rosulabryumcanariense (Brid.) Ochyra is tentatively excluded as the Chilean material can be referred to R.coloratum. Similarly, Rosulabryumviridescens (Welw. & Duby) Ochyra is tentatively excluded since the Chilean plants do not match the African type, but instead appear to be atypical plants of R.campylothecium.


Introduction
With a known moss flora of more than 900 species, Chile has a rich but incompletely documented bryoflora (Müller 2009). Recent studies involving herbarium collections and field work (Larraín 2016;Ireland et al. 2017;Drapela and Larraín 2020;Larraín et al. 2020) suggest that many more species will be discovered. The country has a great diversity of climates, geological substrates, and vegetation communities, ranging from tropical arid deserts in the north, montane and alpine climates along the Andean Mountain chain, Mediterranean-climate regions in the center of the country, to temperate and subantarctic forests and moorlands in the south.
The Bryaceae is a large world-wide family that occurs in a wide variety of habitats and climates and can represent as much as 10% of the species richness in local and regional moss floras. Chile has an extremely rich and incompletely known Bryaceae flora, with an estimated 85 species, based on revisions and recent collecting (Ochi 1980(Ochi , 1982Müller 2009;Ireland et al. 2017;Spence 2020a). These field studies have also revealed species that appear to be new to science, mostly in the genera Gemmabryum J.R. Spence & H.P. Ramsay, Ochiobryum J.R. Spence & H.P. Ramsay, and Plagiobryoides J.R. Spence.
One of the most easily recognized and common genera is Rosulabryum J.R. Spence, which is well represented in the southern hemisphere. The genus currently consists of ca. 75 described species (J. Spence unpublished data), with 12 well documented species in Chile. However, much of the country remains under collected, especially in the north and in the Andes, thus it is likely that additional species will be found with more intensive field work. Of particular note is the presence of a diverse montane Rosulabryum flora in the northern and central Andes which may extend southward into the Chilean Andes.
Rosulabryum occurs in a clade with Brachymenium Schwägr. sect. Brachymenium, sister to a clade consisting of Plagiobryum Lindb., Plagiobryoides J.R. Spence and Ptychostomum Hornsch. (Pedersen et al. 2006). The molecular studies that include more than one species in the genus include Cox and Hedderson (2003), Pedersen et al. (2003) and Pedersen et al. (2006). These studies show a well-supported Rosulabryum clade using several different species. However, the relationships and phylogenetic position of the Rosulabryum and the related Ptychostomum clades remain unresolved at this time.

Method and materials
Collections were obtained from various herbaria, primarily CONC, MO and NY. Additional field work in the Tierra del Fuego region of Chile (Magellanes Province) has been completed and collections are currently being studied in the author's personal herbaria. Much of the recent floristic work has been done in the southern regions of Bío Bío, Aisén and Magallanes (e.g., Larraín 2016;Ireland et al. 2017;Drapela and Larraín 2020;Spence 2020a;unpublished data). Nomenclature for the species documented in this study follows Spence (2020b). This study is a preliminary treatment of the genus for Chile to help guide identification of collections and field work.

Results
Of the 12 species documented in this study, their distributions include four main elements, 1) widespread temperate, 2) southern temperate, 3) subantarctic/Nothofagus, and 4) Neotropical montane. The widespread element includes R. capillare, R. rubens and R. torquescens. Southern temperate species include R. billarderii, R. campylothecium, and R. macrophyllum, with the first two extending to Australasia. The subantarctic element is represented by R. perlimbatum, which extends to southern New Zealand. The Neotropical montane element includes R. andicola and R. densifolium. An endemic element may also exist, as currently R. longidens and R. puconense are endemic to Chile, with potentially one record of the former reported from Argentina which needs to be verified. Rosulabryum coloratum has an anomalous distribution, as it occurs in montane regions of Bolivia as well as lower elevations of south-central Chile. In general, these distributions conform at least in part to well documented and similar distributions among the vascular plant flora of Chile (Moreira-Muñoz 2011). Overall, the diversity of Rosulabryum in Chile is similar to that in other well studied regions, including Australasia (14 spp.) and North America (16 spp.), but appears to be more diverse than the western Palearctic (8 spp.).
Rosulabryum is characterized by a combination of predominantly gametophyte characters, including mostly rosulate habit to sometimes evenly foliate stems, ovate to obovate or spathulate leaves, a well-developed limbidium, serrulate, serrate or denticulate distal leaf margins, costa with well-developed stereid band, nodding capsule, well-developed peristome with appendiculate cilia, small spores, rhizoidal tubers, and filiform gemmae in the leaf axils (Mohamed 1979;Spence 1996). In terms of gametophyte morphology, Rosulabryum is most similar to Rhodobryum. Rhodobryum differs in producing distinctive stolons, a weakly developed to nearly absent stereid band in the costa, and a lack of rhizoidal tubers and leaf axil gemmae. Both genera often have polysetose perichaetia, but this feature is much more common in Rhodobryum. In addition, the chromosomes of Rhodobryum are significantly different in structure not only from Rosulabryum but the rest of the family (cf. Ramsay and Spence 1996).  Ireland & G. Bellolio 35234, 21 Nov. 2002 (MO).

Rosulabryum billarderii (Schwägr.) J.R. Spence
Remarks. The common widespread species of large Rosulabryum from central Chile south to Aisén. The species is also found in Argentina, the Falkland Islands, Australia, New Zealand and Macquarie Island (Spence and Ramsay 2019). In the Magellanes Region it is largely replaced by R. perlimbatum. The species occurs in a variety of forested and semi-open habitats, often in shade on mesic to damp soil banks, fallen logs, tree stumps and soil-covered ledges. It is characterized by dioicous sexual condition, strongly rosulate stems, large leaves that are irregularly contorted when dry, a costa excurrent into a short awn, a strong limbidium, serrate leaf margins, and brown to red-brown rhizoidal tubers (Illustrations:

Remarks. A common temperate species in the central and south regions of Chile from
Coquimbo Region to at least the Los Lagos Region but absent from colder subantarctic climates. It also occurs in Australia and New Zealand (Spence and Ramsay 2019). The species is found on exposed to partially shaded damp to drying soil, sand, and rock ledges, often in open woodlands or on cliffs and outcrops. The species is characterized by dioicous sexual condition, medium-sized imbricate golden to yellow-green strongly concave leaves, a costa excurrent in a long often denticulate awn, a weak or nearly absent limbidium distally, serrate distal leaf margins, and the absence of rhizoidal tubers

Remarks.
A worldwide temperate species found in a wide variety of habitats, but most often on damp shaded soil or fallen logs and tree stumps. Its distribution in Chile remains poorly understood but it is common in the more temperate southern regions such as Bío Bío (Ireland et al. 2017). It is characterized by dioicous sexual condition, rosulate stems, small obovate leaves that are spirally twisted around the stem when dry, a costa excurrent into a medium to long awn, moderately well-developed limbidium, serrate distal leaf margins, and small brown rhizoidal tubers (Illustrations: Syed 1973 Ireland & G. Bellolio 33903, 23 Nov. 2001 (MO): Region VIII, Bío Bío Province, Saltillo del Itata, small falls on Itata River, 37°04'S 72°09'W, ca. 210 m, on brick wall beside poplar trees by river, R.R. Ireland & G. Bellolio 34950, 28 Oct. 2002 (MO).

Remarks.
A relatively uncommon species found principally in semi-arid regions in the central and northern regions of Chile and adjacent areas of Bolivia, found on sandy soil or soil over rock, often near streams. The species is characterized by its dioicous sexual condition, evenly foliate stems, large narrowly ovate leaves that are spirally twisted around the stem when dry, a weak limbidium distally, and brown to red-brown rhizoidal tubers. Ochi (1980) had synonymized it with R. canariense but it is treated here as a good species (see below under R. canariense). (Illustration : Ochi 1980: 148, as Bryum canariense).

Remarks.
A robust species distributed throughout the Neotropics, primarily along the mountain chains from Mexico south to Chile, and throughout the Andes (Ochi 1980). It is common at higher elevations, often above 3000 m, but can also occur in the lowlands, and is found along streams and in wetland areas on wet soil or rock. The species is characterized by its dioicous sexual condition, long evenly foliate stems with large narrowly ovate leaves, a costa excurrent into a medium to long awn, strong limbidium, sharply serrate to denticulate distal leaf margins, with the teeth often double, and brown to red-brown rhizoidal tubers (Ochi 1967: 30, as Bryum densifolium).

Remarks.
A common species in the central regions of Chile, from the Bío Bío north to at least Coquimbo, usually on tree trunks and larger branches, stumps and fallen trees in forests, occasionally on soil. The species is characterized by dioicous sexual condition, small leaves, rosulate fertile stems, with numerous rosulate to evenly foliate innovations with leaves spirally twisted around the stem when dry, strong excurrent costa in medium to long awn which is sometimes red, brown to red-brown filiform gemmae in the leaf axils of sterile shoots, and small red to red-brown rhizoidal tubers. Ochi (1982) synonymized this with the Neotropical R. pseudocapillare (Besch.) Ochyra, but R. longidens is quite distinct from that species. The single report from Argentina (Ochi 1982;as R. pseudocapillare) needs to be re-examined as it may be a different species, thus R. longidens may be a Chilean endemic. It is the only epiphytic species in the genus in Chile. There are no known illustrations of this species.

Rosulabryum macrophyllum (Cardot & Broth.) Ochyra
Remarks. An uncommon species of moist to wet soil in the subantarctic moorlands and Nothofagus forests in southern Chile, reaching north to the Aisén Region (Ochi 1982;Larraín 2016)). The species is characterized by dioicous sexual condition, rosulate stems, large ovate leaves that are ±imbricate when dry, costa excurrent into a short awn, a fairly well developed limbidium, finely serrulate distal leaf margins, and brown to red-brown rhizoidal tubers. The species is also known from the Falkland Islands and Argentina (Illustrations: Ochi 1967: 33, as Bryum macrophyllum).

Rosulabryum perlimbatum (Cardot) Ochyra
Remarks. A common and widespread species of the subantarctic forests and moorlands of the Magallanes and Aisén Regions on damp to wet soil, fallen logs, and tree stumps (Ochi 1982). Reports from further north are likely misidentifications and are either R. andicola or R. billarderii. This is a robust species with dioicous sexual condi-tion, rosulate stems, sometimes with 2+ interrupted clumps along stems, large leaves that are contorted to somewhat imbricate when dry, serrulate distal leaf margins, an extremely wide limbidium of 4+ rows distally, and brown to red-brown rhizoidal tubers. The wide limbidium often gives the leaves a white-margined appearance. The species is also found in Argentina, the Falkland Islands, and extreme southern New Zealand (Illustrations: Mohamed 1979: 422, as Bryum perlimbatum;Fife 2015: 87, as R. perlimbatum).

Rosulabryum puconense (Herzog & Thér.) J.R. Spence
Remarks. This species was synonymized under R. capillare by Ochi (1980). However, it differs in significant ways. It is characterized by small rosulate to evenly foliate stems, small leaves that are somewhat imbricate to irregularly contorted when dry, costa excurrent in a short awn, a weak to sometimes absent limbidium, and smooth to finely serrulate distal leaf margins. Perhaps most striking are its sexual condition and rhizoidal tubers. Most collections are synoicous, but some are single-sex and thus would be considered dioicous. The species likely has the same sexual systems as R. torquescens and can be described as polyoicous. The rhizoidal tubers are similar to those produced by R. rubens, with often protuberant cell walls, but they are much larger. Some tubers are up to 600 µm across, with colors varying from red-brown to red or orange. R. puconense seems to have a preference for mesic to dry soil under shrubs and is especially common along the coasts from central Chile south to the Tierra del Fuego region. Although currently a Chilean endemic, it may ultimately be found in southern Argentina. There are no known illustrations of this species.

Remarks.
A rare species generally found in disturbed habitats, especially on disturbed soil and concrete, and possibly introduced from the northern hemisphere. There is only one record from Chile in disturbed habitats in the capitol Santiago (Ochi and Mahu 1988, at HO, not seen!). It is characterized by its dioicous sexual condition, rosulate to somewhat evenly foliate stems, small leaves that are irregularly contorted when dry, costa excurrent into a medium-length awn, a narrow but usually distinct limbidium, and serrulate distal leaf margins. The plants are often reddish-tinged. The rhizoidal tubers are diagnostic; predominantly red, with strongly protuberant cell walls, from 100-280 µm in diameter, often arising from lower leaf axils or at the base of the stem on short rhizoids. The species has a scattered world-wide temperate distribution (Illustrations: Crundwell and Nyholm 1964: 630, as Bryum rubens;Lüth 2019: 938 as Ptychostomum rubens; Holyoak 2021: 232, as P. rubens).

Remarks.
A widespread warm temperate to subtropical species in the northern hemisphere, Africa, Australasia and South America (Spence and Ramsay 2019). Although there are few collections from Chile, the species is likely to be common in the Mediterranean-climate regions of the country as far south as Los Lagos. It is found on soil, soil over rock and occasionally wood, including burnt wood, generally in exposed areas, often along road cuts. It is characterized by synoicous or rarely autoicous sexual condition, rosulate stems, medium-sized leaves that are irregularly contorted when dry, a costa excurrent in a medium to long awn, strong limbidium, serrate distal leaf margins, and scarlet, bright red to orange rhizoidal tubers (Illustrations: Syed 1973, 308 as Bryum torquescens; Spence and Ramsay 2006: 347, as R. torquescens;Hallingbäck et al. 2008: 350, as B. torquescens;Lüth 2019: 939 as Ptychostomum torquescens; Holyoak 2021: 257, as P. torquescens).

Excluded species
Rosulabryum canariense (Brid.) Ochyra. Ochi (1980) placed R. coloratum into synonymy under this species. Here they are treated as specifically distinct (see above under R. coloratum). True R. canariense is autoicous or synoicous, has interrupted rosulate tufts along the stem, irregularly contorted obovate leaves, and bright red, scarlet or orange rhizoidal tubers. I have not seen any material from Chile in collections examined in this study with these characters, thus it is tentatively excluded from South America, but is retained in the key pending additional field work. It is a northern hemisphere Mediterranean-climate species, also reported from South Africa, although the plants there are somewhat distinct from northern hemisphere plants.
Rosulabryum viridescens (Welw. & Duby) Ochyra. Ochi (1977) reported this species based on the type of Bryum hamatum Dusén, an illegitimate name as there was no formal description. More recently, I have identified several collections from the Bío Bío Region as this species. However, having recently obtained material of R. viridescens from South Africa, it is clear that the South American material is not that species (cf. Magill 1987). Most of the recently named collections are atypical specimens of R. campylothecium, while the B. hamatum type may be an aberrant form of R. macrophyllum or R. perlimbatum characterized by imbricate ovate leaves. Thus R. viridescens in tentatively excluded from Chile and South America, although it is retained in the key.