Reproductive and persistence strategy of the liverwort Arnellia fennica after the last glaciation in the area of disjunction in Central Europe (Polish Tatra Mountains, carpathians)

Abstract

The liverwort Arnellia fennica has a circumarctic distribution with disjunct and scarce localities in the Alps, Carpathians, and Pyrenees. Within the Carpathians, it is only known from the Tatra Mountains (in Poland), where so far only four occurrences have been documented in the forest belt of the limestone part of the Western Tatras. The species is considered a tertiary relict, which owes its survival during the last glaciation period to low-lying locations in areas not covered by ice. Previously, it has been demonstrated that this plant does not produce gemmae in the Tatra Mountains, nor does it reproduce sexually, hence it has not spread in this massif despite the high availability of potential habitats. These studies address the following questions: (1) why A. fennica, an arctic-alpine species, has only been found at low elevations in the Tatra Mountains so far, (2) what were the possibilities of its survival during the glaciation period as verified based on the latest paleoglaciological map, (3) how this species persists in the Tatras and why it remains a rare plant. As a result, nine additional new occurrences were found, bringing the total to 13 throughout the massif. Some of the sites were found in the high mountain area. For the first time, the production of gemmae in the Tatra population of A. fennica was observed and documented, along with the presence of male specimens of this dioecious species. Genetic studies have shown that individuals from all three groups of sites are genetically homogeneous, indicating a lack of sexual reproduction. The only way of dispersal for A. fennica in the Tatras is through propagule production. The uniqueness and specificity of these structures have been described, which differ significantly from the common model known in liverworts. The rarity of the species in the Tatra massif is attributed to the inefficient mode of vegetative reproduction and the absence of sexual reproduction. Paleoglaciological analysis of all montane sites (historical and new) of A. fennica showed that half were located in areas covered by glaciers. The hypothesis of this liverwort's survival during the glaciation period, at lower elevations, should be rejected. In light of the new data obtained, montane localities should be considered as secondary, which could have arisen after the glacier retreated only from high-mountain populations producing propagules transported downhill.

Keywords: Endangered species; Genetic variation; Limestone flora; Organellar genomes; Tertiary relicts.

Fig. 1

Object and area of study: (A) location of the Tatra Mountains on the map of Europe; (B) Arnellia fennica on limestone rocks in Kalacki Żleb gully (photo by P. Górski, June 22, 2019), (C) division of the Tatra Mountains: 1 - state border, 2- a rough range of sedimentary calciferous rocks located in the northern part of the massif, G - Mt Giewont, KW - Mt Kominiarski Wierch, O - Mt Osobitá.

Fig. 2

Distribution of Arnellia fennica in the Tatra Mountains: (A) new localities, numbers (1–9) denote the numbering of locations, see List of localities, (B) historical unconfirmed localities, (C) confirmed historical localities, (D) the collection sites for genetic analysis.

Fig. 3

The occurrence of arctic-alpine liverworts in 100-meter altitudinal belts on limestone substrate in the Polish Tatra Mountains (based on unpublished materials, P. Górski).

Fig. 4

Habitats of Arnellia fennica in the Western Tatras: (A,B) outcrops of limestone rocks in the upper part of Żleb Żeleźniak gully beneath the walls of Mt. Kominiarski Wierch (June 19, 2023); (C,D) a wide (unnamed) gully beneath the massif of Zawrat Kasprowy (July 15, 2023); the patch with A. fennica is marked with a red arrow (photo by P. Górski).

Fig. 5

Thread-like outhgrowths on the lower (abaxial) side of the leaf, at the apex of which gemmae are produced; the observed structures are marked with a red arrow, and the background of the image is a single-layered leaf (photo: P. Górski).

Fig. 6

Vegetative propagation of Arnellia fennica observed on shoots collected in the Tatra Mountains: (A) prepared whole leaf with gemmae developing on the abaxial side: a1 - basal part of the leaf with very intense production of propagules, a2 - gemmae detached from the leaf during specimen preparation, (B) gemmae (photo by P. Górski).

Fig. 7

Localities of Arnellia fennica on the paleoglaciological map of the Tatra Mountains (based on KML layer in GoogleEarth). Explanations: localities covered by glaciation − 1,3,4,7,9,11,12; sites outside the glacier-occupied area − 2,5,6,8,10,13; origin of sites (see List of localities): 1–9: Górski, Szczecińska, Sawicki (orig.), 10: I. Szyszyłowicz and J. Váňa^,, 11–13: J. Szweykowski and others.

Fig. 8

Chloroplast genome map of Arnellia fennica. Gray inner circle indicates GC content.

Fig. 9

Mitochondrial genome map of Arnellia fennica. Gray inner circle indicates GC content.

Fig. 10

The NOR region of Arnellia fennica - the intraindividula variable site (T-> C) is marked as yellow block.

Fig. 11

Phylogenetic relationships of leafy liverworts inferred from concentrated plastid (right) and mitochondrial dataset (left) using ML method. All clades are maximally supported unless indicated otherwise. Clade positions were optimized using cophylo function in the phylotools R package.