Two additions to the moss flora of the South Shetland Islands in the maritime Antarctic

Tortella fragilis (Drumm.) Limpr. (Pottiaceae) and Bryum nivale Müll. Hal. (Bryaceae) are recorded for the first time from the South Shetland Islands in the northern maritime Antarctic. They were discovered in the Admiralty Bay area on King George Island, the largest island of this archipelago. The two species are briefly characterized morphologically, their habitats are described, and their distribution in the Antarctic is mapped. Discovery of these species has increased the documented moss flora of King George Island to 67 species, strengthening it in the leading position among individual areas with the richest diversity of moss flora in Antarctica. Likewise, T. fragilis and B. nivale represent remarkable additions to the moss flora of the South Shetland Islands, which currently consists of 92 species and one variety, making this archipelago by far the richest bryofloristically amongst large geographic regions of the Antarctic. Comparison of recent (2018) and old (1985) photographs revealed a significant retreat of glacial cover and suggests that the collection site was likely opened for colonization only within the last several decades. The record of T. fragilis is biogeographically relevant, and constitutes an intermediate site between the species’ occurrences in the Antarctic Peninsula and southern South America. The present record of B. nivale is the fourth discovery of the species worldwide, which may be helpful for the future designation of the distribution of this extremely rare species.


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In February 2018 we carried out field work on King George Island, which primarily aimed to collect material for phylogeographical investigations on Antarctic endemic moss species. In the Admiralty Bay area, we focused, among others, on the isolated and poorly accessible cliff of Klekowski Crag. Our sampling effort resulted in the discovery of two species new to the island's moss flora, namely Tortella fragilis (Drumm.) Limpr. (Pottiaceae) and Bryum nivale Müll. Hal. (Bryaceae). In this article, the records of these two very rare species are described and discussed in the context of the diversity, taxonomy, and biogeography of the Antarctic moss flora.

Material and methods
The specimens were collected on Klekowski Crag in February 2018 during fieldwork on King George Island. The voucher collections are housed in the bryophyte herbarium in the W. Szafer Institute of Botany, Polish Academy of Sciences in Kraków (KRAM). Mosses were identified by routine microscopic and laboratory techniques. The specimens were carefully compared with those collected in the Antarctic and outside this continent. The current general topographical and glaciological context of the sampling site was compared with that reported over 30 years ago (approximately the time of earlier bryological fieldwork conducted in this area) based on photographs taken in 2018 and 1985 (Fig. 1). Distribution maps of species records in the Antarctic were also prepared.

Results
Klekowski Crag is a typical, highly-isolated terrestrial oasis in Admiralty Bay. Its southern part is almost entirely glaciated, with the exception of the summit ridge, whereas the northern side is mostly exposed, forming a steep cliff up to 200 m high, which in the summit part contains large expanses of stable rocks that change into extensive scree of weathered basalt rubble. Bryophytes mainly cover the faces of stable rocks and large boulders, and often grow in moist rock fissures and on moraines in the front of the glacier. When comparing the photographs of this area taken in 1985 and in 2018, some changes are clearly visible, indicating in particular significant retreat of the Lange Glacier ( Fig. 1). This results in wider contact of this outcrop with the waters of Admiralty Bay, and a larger area of exposed land in the frontal area of the crag. The glacial cover of its higher slopes in the prospected eastern part seems to have undergone less pronounced changes.
The populations of mosses described in this article were discovered in the central part of the rocky slope facing the sea, in the direct vicinity of a characteristic convex rock formation (Fig. 1B). Based on a rough visual reconstruction, this steep, rocky outcrop appears to have been ice-free to some extent 33 years ago, while the screes above it were mostly covered by either permanent or seasonal snow layer (Fig. 1A). Based on the available large-scale images, it is not possible to unambiguously confirm whether the sites explored in 2018 were also exposed during earlier bryological studies. The two new species records are presented in detail and discussed below.

Tortella fragilis
This species was found in the upper part of a rock ledge at the base of a sea-facing cliff. The population was very sparse, and the moss formed a loose tuft of less than 1 cm 2 , which was growing on a pocket of soil within a rocky rubble. The only associated species was Distichium capillaceum (Hedw.) Bruch & Schimp. This T. fragilis habitat is consistent with those in other localities of the species in Antarctica [4].
The plants of T. fragilis from King George Island match other collections of this species from the Antarctic. Like elsewhere in this region, these plants are sterile but commonly produce vegetative propagules formed by caducous, thickened apices of young leaves. In Antarctica, such deciduous leaf apices are known only in Tortella alpicola Dixon and Syntrichia sarconeurum Ochyra & R. H. Zander; thus, T. fragilis is likely to be confused with these species. However, in the former, the propagules are segmented as a series of barrel-shaped constrictions, which fracture into several pieces, whilst in T. fragilis, they are a single solid unit. Syntrichia sarconeurum propagules also form a single unit; however, this species is distinct from both species of Tortella (Müll. Hal.) Limpr. by possessing the hyaline basal leaf cells that change gradually into chlorophyllose cells along an ill-defined junction line at approximately the same level across the lamina, or sometimes lower at the leaf margins than at the costa. In contrast, the hyaline basal cells in Tortella species extend up the leaf margins, forming a V-shaped basal region, which sharply demarcates from the upper chlorophyllose cells along the abrupt junction line.
A characteristic feature of T. fragilis is bistratose distal laminal cells. However, in the Antarctic specimens, they vary from being partially bistratose to entirely unistratose throughout, and such phenotypes are also represented by specimens from King George Island. Nevertheless, because the leaves are rigid and the margins in the leaf subula are distinctly bordered by smooth and pellucid cells, these plants are included in T. fragilis. Bistratosity of the laminal cells, often coupled with a salient costa and thickened, fleshy marginal limbidia in many moss species, especially aquatic species, are often considered as a structural adaptation to swiftly flowing water [15,16]. However, molecular data have shown that, for example, the plants once described as Sciaromium lacustre Herzog & P. Rich. [17] and characterized by variously polystratose distal laminal cells do not differ genetically from the plants known as Drepanocladus longifolius (Mitt.) Paris [18].
Hence, Antarctic populations of T. fragilis are ideal for genetic investigations, which should resolve their taxonomic status and provide further insight into the significance of the differences in laminal cell stratosity as a taxonomic character. Tortella fragilis is a strict bipolar species, i.e., without intermediate localities in the tropical zone. It is widely distributed in the Southern Hemisphere but scattered in Lesotho in Southern Africa [19], in the South Island [20] and on the Campbell Islands [21] in New Zealand, in Tierra del Fuego [22], and on subantarctic South Georgia [23] and Îles Kerguelen [24]. In the Antarctic, T. fragilis has previously only been reported from the Antarctic Peninsula region where it occurs on the western coast, ranging from the Danco Coast to the Alexander Island, and on the eastern coast, from James Ross Island to the Wilkins Coast [4,25] (Fig. 2). The discovery of this species on King George Island reported here is new to the South Shetland Islands, and the first report in the peri-Antarctic archipelagoes. It may be considered a "geographic link" between the Antarctic Peninsula and southern South American populations of T. fragilis.

Bryum nivale
This species was recorded on a border of a rock ledge at the base of the Klekowski Crag cliff. It was found in a sheltered site on a pocket of wet soil in a rock crevice where it formed a small (ca. 2 cm 2 ) pure tuft. The only other moss growing on this site was Pohlia cruda (Hedw.) Lindb., which formed loose patches.
Species of the genus Bryum Hedw. are prominent in the impoverished Antarctic moss flora, both in terms of their frequency and cover. However, like elsewhere, their identification is problematic, because most populations are notoriously sterile and sporophyte characters are usually critical for accurate species determination. To date, seven Bryum species are known to occur in Antarctica [4,25], and B. nivale is the rarest species of the genus in this biome, as it has only been collected once on Alexander Island. This species has deeply concave, broadly ovate to rounded leaves, which are broadly acute and obtuse to shortly apiculate. The leaves are indistinctly bordered, and the laminal cells are elongaterhomboidal distally and rectangular below, widened and never red-tinged at the base. Bryum nivale remains insufficiently known taxonomically, mostly owing to its sterility and scarcity of material, although it is very distinct gametophytically from all other congeners in the austral polar regions. For a long time, this species was only known from the type collection from Bio-Bio Region of central Chile [26]. Later, it was discovered on Marion Island in the Subantarctic from whence it was first reported as Bryum amblyolepis Cardot [27] and from Alexander Island in the Antarctic [4,25]. The present record is the fourth discovery of this species (Fig. 3). Bryum nivale warrants special attention; careful searching during field work should contribute further specimens to allow better understanding and circumscription of this species. The known geographical range makes it difficult to designate the pattern of B. nivale distribution. Until the species is found in more localities, it can be tentatively defined as a south-temperate Afro-American species deeply penetrating into the Antarctic. This type of distribution is demonstrated by a large number of mosses, primarily tropical lowland, montane, and altimontane species [28,29]; however, it also includes a relatively small group of south-temperate cool-adapted moss species [30][31][32].

Discussion
Tortella fragilis and Bryum nivale are remarkable additions to the moss flora of King George Island (the South Shetland Islands). Until recently, the moss flora of this island consisted of 65 species, representing the richest local diversity of moss flora in the Antarctic. The present discoveries further increase the moss flora of this island to 67 species. The small Signy Island, part of the South Orkney Islands, has the second richest diversity of moss flora, with 59 species. The next two areas with the richest diversity of moss flora are two further islands of the South Shetland Islands archipelago, namely Deception and Livingston islands, which host 56 species each.
Tortella fragilis and B. nivale represent important contributions to the moss flora of the South Shetland Islands. Ninety-two species and one variety have so far been reported from this archipelago, making it the richest bryofloristically region in the entire Antarctic. The much smaller South Orkney Islands archipelago has the second richest moss flora, which, however, consists of only 59 species. Notably, the flora of the Antarctic Peninsula, which is a much larger territory than the South Shetland Islands, consists of only 67 species and two varieties.
In the case of new moss records in the Antarctic and subantarctic islands, a question remains on the origin of such new localities. It is unclear whether the small populations of the two species reported here were found in the newly open ground or if the location was ice-free in 1980. Analysis of available general photographic documentation ( Fig. 1) does not allow a clear-cut conclusion, although at least part of the area explored in 2018 was open during previous investigations in 1980s. Tortella fragilis and Bryum nivale could have been easily overlooked during earlier studies considering the small populations of the two species and complicated microtopography of the area. Nevertheless, the gradual emergence of the site seems to be of recent origin. In the 1985 image, only a small part of the rock was ice-free, and it is likely that the whole area was glaciated within the last century. Considering the hypothesis that these species were recently established, it remains unclear whether there was local dispersal from other, yet unknown, populations within King George Island, or whether the populations were established via aerial long-distance transport of propagules from remote areas. Population genetic tools have the potential to discern long-term isolation from recent dispersal processes [33,34], and molecular analyses of Antarctic populations of these species may provide further information.
There has been speculation regarding the origin of the moss flora of Antarctica. It has been accepted that the moss flora generally established following the Holocene migration of species via aerial long-distance dispersal [35]. Unfortunately, paleobotanical data remain scarce for the Antarctic and subantarctic islands [36][37][38][39][40], which prevents the detailed reconstruction of Quaternary glacial history and development of flora and vegetation cover after the Last Glacial Maximum. However, there is strong indirect evidence that some moss taxa are pre-Pleistocene survivors that outlived the glacial epoch in situ on ice-free nunataks and oases. The prime candidates for such survivors are endemic species that do not appear to have close relatives outside the Antarctic; for example Andreaea depressinervis Cardot [4], Schistidium lewis-smithii [2], and S. deceptionensis Ochyra, Bedn.-Ochyra & R. I. L. Sm. [41]. It cannot be excluded that Tortella fragilis also belongs to this group, especially in the context of its morphological differences from extra-Antarctic plants. Phylogeographic studies using DNA markers may help to resolve such taxonomic and phytogeographical issues [18].