An overview of the alien flora of the Yamal-Nenets Autonomous Area (Russia)

From eight years, 2012–2019, of field research, critical work in herbariums and literature reviews, we have established and identified as alien in the Yamal-Nenets Autonomous Area (YaNAA) a list of 216 vascular plant species from 144 genera and 35 families. The set of the ten richest families, by the number of species, alters in that the alien flora includes such families as Fabaceae, Polygonaceae and Chenopodiaceae, whereas the Cyperaceae, Salicaceae and Juncaceae families are absent from it. The richest by the number of species genus in the alien flora of the YaNAA is Chenopodium. We have classified the non-native species by the degree of naturalization, means of introduction and frequency of occurrence. We considered all alien species as kenophytes. For some arrival into the region can be traced back to 17 century, but most of them appeared at, or since, the end of 20 century or later. We distinguished three groups according to the naturalization degree: ephemerophytes (70%), kolonophytes (15%), and epekophytes (15%). Life history strategies and growth forms of the alien species differ from the native ones, with absolute dominance of herbaceous forms and a high proportion of annuals among them. By means of introduction, xenophytes prevail (82%), the remainder being number of ergasiophytes and xenoergasiophytes.


Introduction
Yamal-Nenets Autonomous Area (YaNAA) is one of the primary regions in Russia for gas and oil production. Industrial development, and the associated expansion of transport infrastructure in this region, has significantly transformed the environment and in particular facilitated the migration of non-native species into the local flora. Immigrant alien species first appear at and then spread along the roadsides and road pads, railway pads, ruderal sites, around airports and railway stations; also at river's alluvium. The results of the invasion of aggressive alien species can be catastrophic for native ecosystems, while on the other hand the appearance of new species is an enrichment of local floras, which, in the West Siberian North, are normally very species poor. Monitoring of alien species should become a part of future regional floristic studies.
There is significant information in the literature about the diversity of vascular plants in the YaNAA, including non-published herbarium collections (Pismarkina 2014a). "Flora of Western Siberia" (Krylov 1927(Krylov -1964, "The Arctic Flora of the USSR" (Tolmachev 1960(Tolmachev -1987 and "Flora of Siberia" (Krasnoborov et al. 1987(Krasnoborov et al. -1997Malyschev et al. 2003) are the most valuable sources, though even in such fundamental works information about alien species is minimal. In "Conspectus florae Sibiriae" (Baikov 2005) and "Conspectus florae Rossiae Asiaticae" (Baikov 2012), mainly based on the material from "Flora of Siberia", there is very limited information about the distribution of species within the individual administrative units. Books summarizing the results of the inventory and analysis of the flora of several regions within the YaNAA were devoted to the Polar Urals (Knyazev et al. 2006), the Yamal Peninsula (Rebristaya 2013), the Upper Taz State Reserve (Neshataev et al. 2002) and the floodplain of the Taz River (Titov and Potokin 2001). However, these also provide little information about non-native species. The most useful information about the synanthropic component of flora was found in the monograph of Dorogostayskaya (1972) and papers by Trotsenko (1990), Vilchek and Kuznetsov (1996), Ishbirdin et al. (1996) and Khozyainova (2007). Although much floristic information has been achieved for more than a century, summary publication about the flora of the YaNAA is still absent. The totality of nonnative species that has entered the region has not been a subject of any special investigation.

Methods
The YaNAA is situated in the North of West Siberia. The northernmost point of the YaNAA lies at approximately 73°20′N and the southernmost at 62°N. The region stretches throughout the three bioclimatic zones: tundra (including Arctic tundra, Northern and Southern Hypoarctic tundra subzones), forest-tundra and taiga (including northern and middle taiga subzones) (Larin 2004).
The high latitude location of the YaNAA, its remoteness from warm air and water masses and the plain topography determine its sharply continental climate. Winters last almost eight months with minimum temperatures as low as -59°C. Summers though short and cool may have some days, in the southern part of the region, with temperatures as high as +30-34°С. Summer isotherms follow latitudinal direction and change from a mean July temperature of +4°С in the north to +16°С in the south. Winter isotherms have meridional direction and the mean January temperature changes from -22°С in the western part of the region to -27°С in the eastern part (Larin 2004). Permafrost underlain the terrain.
As "alien" (synonyms: exotic, introduced, non-native, non-indigenous, adventive) we consider species, which appearance in the study region was not connected with natural flora genesis, but is the result of human economic activity, primarily anthropogenic disturbance of plant and soil cover. The absence of natural predators (phytophagous insects and pathogens) often enables exotic species (Tuganaev and Puzyrev 1988;Burda 1991).
While working with literature and herbarium specimens we took into account information about the presence of the species in natural or anthropogenic habitats within YaNAA borders and adressed the following questions: 1) Is the presence of a species in any specific locality connected with any anthropogenic activity?
2) Is the species adventive throughout the whole YaNAA territory?
If the species is native in one part of the region, and in another part, usually northwards, it is obviously adventive, we did not include it in the alien fraction. To evaluate the modern range of the species of the regional flora, along with literature, we used also internet resources (Afonin et al. 2008;GBIF 2020aGBIF , 2020bGBIF , 2020cPismarkina 2018Pismarkina -2019. For the analysis of the alien flora by the degree of naturalization and the means of introduction, we used the classification by F.G. Schroeder (Schroeder 1969;Ignatov et al. 1990).
For the analysis of alien flora by the species occurrence frequency, we used the following scale: -solitary: species found in one locality in the YaNAA; -very rarely: species found in 2-5 locаlities; -rarely: species found in 6-10 localities; -often: species is known from 11-15 localities; -commonly: species found in 16 or more localities.
Our field work in the YaNAA in 2012-2019 is reported in a number of publications (Byalt et al. 2017(Byalt et al. , 2020Egorov 2019a, 2019b;Pismarkina 2014aPismarkina , 2014bPismarkina , 2019Pismarkina and Khitun 2019;Bystrushkin 2019, 2020;. Our data, critical check of the herbaria specimens in the mentioned above herbariums (LE, MW, SVER, TK) and literature references, followed by nomenclature control according to the website "Plants of the World Online" (POWO 2019), allow us to present a list of 216 species from 144 genera and 35 families in the alien fraction of the regional flora of the YaNAA. Previously, we wrote about 190 alien species (Pismarkina et al. 2018), an additional 26 species appeared due to new findings, new identifications and re-identifications of herbaria specimens. In 2019-2020, we reviewed the list of the alien species and only information that was confirmed by a possession of a herbaria specimen was used. Therefore, species known in the YaNAA only from literature reference were not included in our list.

Results
The alien species portion contributes only 20.3% of total regional flora. There are several reasons for such a low proportion, compared to regions that lie further south: 1) Geographical position in the north of West Siberia. Here, not only naturalization, but even encroachment of new species (mainly originated from more southern regions), is difficult due to the climatic and biological barriers; 2) Relative "youth" of synanthropic component of regional flora; 3) The limited number of publications devoted to adventive plants since the work of Dorogostayskaya (1972).

Frequency of occurrence and degree of naturalization
The majority of the alien species were found in the YaNAA one to five times (i.e., "solitary" or "very rarely"), there are 87 and 80 species respectively in these categories, and thus 77.3% of the alien species we found. Thirty species we categorized as occurring "rarely" (13.9%). Species recorded as "often" and "commonly" (11 and 8 species respectively) contributed only 8.9% of the alien flora.
Extensive introduction of alien species to the north of West Siberia started concurrently with the migration of people from European Russia (17 th century onwards), but it became more intensive during the period of gas and oil exploration and industrial development. Therefore, all non-native species in the flora of YaNAA are kenophytes, including the oldest grains and the weeds accompanying them, which in European part of Russia and in the south of Siberia are considered as archaeophytes (e.g., Hordeum vulgare L., Chenopodium album L., Triticum aestivum L., Chenopodium rubrum L., Centaurea cyanus L.).
There are 16 ephemerophytes with the frequency of occurrence "rarely" in this Only two ephemerophytes occur "often", Brassica rapa L. and Dactylis glomerata L., they are both used in lawn and arable field grass mixtures and therefore are repeatedly introduced into the region.
Epekophytes are a group of species that spread through human-made habitats. None of 33 species classified as epekophytes in the YaNAA belonged to the occurrence frequency group "solitary". Nine epekophytes occur "very rarely": Anthyllis vulneraria L., Carum carvi L., Lactuca tatarica (L.) C.A. Mey., Sisymbrium loeselii L., Silene tatarica (L.) Pers., Chenopodium acerifolium Andrz., L., Persicaria maculosa (L.) S.F. Gray, Convolvulus arvensis L., Linaria vulgaris Mill. Species in this group behave differently. Thus, Anthyllis vulneraria and Persicaria maculosa, were found in 2013 and 2014, and they still grow at those same sites but they did not spread to other sites in the region, whereas all other species expanded during the later years of our study to the new settlements. For example, Sisymbrium loeselii was first recorded in Noyabrsk in 2013, in 2017 we observed it in many places in Novy Urengoi, and in 2019in abandoned lawns and wastelands in Nadym.
The higher the degree of naturalization, the fewer species achieve it. Long-term observations are necessary to distinguish kolonophytes and ephemerophytes. In contrast to Mayorov et al. (2012), we do not consider all introduced rhizomatous species as kolonophytes. Among the perennial rhizomatous plants, we classified as kolonophytes only those species, that at the time of observation had formed spacious populations and were flowering or fruiting. These are, for example, Galium album Mill., Pedicularis sibirica Vved., Urtica angustifolia Fisch. ex Hornem., Alopecurus arundinaceus Poir., Elymus sibiricus L., Lolium pratense, L. perenne L., Phleum pratense L., Typha angustifolia L., T. latifolia L. Taking into account big annual variation in mean temperatures during the vegetation season in the Russian Far North, even such species can die off before managing to form stable autogenous populations.
Epekophytes are clearly distinct in the YaNAA. They are not a transitional group from kolonophytes to agriophytes, when former kolonophytes start successfully spread out, but have not yet manage to encroach new habitats. In this region, as a rule, epekophytes have the highest degree of naturalization among the alien species. We explain this by the specifics of the native ecosystems (taiga, forest-tundra, tundra), which provide harsh phytocoenotic and edaphic barriers to the introduced species. Thick moss and lichen cover; the high acidity, hydrological and thermal regimes of the soil, combine to prevent the settlement of non-native plants. Therefore, exotic plants spread only through anthropogenic habitats. Exceptions do occur such as our 2016 observation of Hordeum jubatum in the dry pine forest and Matricaria discoidea on the river alluvium in taiga, but such observations are solitary.

Life history strategies and growth forms of alien species
The non-native flora differs from the indigenous by absolute dominance of herbaceous forms and by the very high proportion of annuals among them. Annuals represent almost 41% (88 species) of the alien flora. Other short living plants are less numerous: biennials (15 species, 7.0%); annuals/biennials (9 species, 4.2%); plants, which complete their life cycle in various time, depending on conditions their life span can vary from 1 or 2 years to several years (9 species, 4.2%). However, perennial herbs (91 species, 42.1%) are the largest group, as they are in the indigenous flora. There are only four species of shrubs (1.2 %) in the non-native flora. Mayorov et al. (2012) reported similar proportions for the alien flora of Moscow city and the Moscow region. It is likely, that the selection of growth forms and life history strategies of alien species is similarly throughout the temperate zone.
Species with different life history strategies exhibit different levels of ability to naturalize. Among annuals, we found 76 ephemerophytes, one kolonophyte and 11 epekophytes. Among biennials, there were 11 ephemerophytes, one kolonophyte and three epekophytes. Perennials were represented by 51 ephemerophytes, 24 kolonophytes and 16 epekophytes. Among species where their life span can vary between biennial or perennial, there are two ephemerophytes and one kolonophyte. Among those species, which can be either annuals or biennials, there are seven ephemerophytes and two epekophytes. Among the plants, which can live 1 to 2 or several years, there are three ephemerophytes, two kolonophytes and one epekophyte. All shrubs (Cytisus ruthenicus, Rosa glabrifolia, Rubus idaeus and Sorbaria sorbifolia) we classified as kolonophytes. Distribution of the species with different degrees of naturalization among the groups with different life history strategies is shown on Fig. 3. The proportion of ephemerophytes is the largest among annuals -85.2%, decreasing among the plants with longer life spans. The reason is the inability of annuals and biennials to sustain vegetative reproduction, which decreases their chance to form autogenous populations in the environments of middle and northern taiga with severe continental climate.

Means of introduction
By means of introduction, xenophytes, i.e., unintentionally introduced species, absolutely prevail (177 species, 81.9% of non-indigenous flora). There are also several (15 species, 6.7%) ergasiophytes, i.e., species escaping from cultivation: A special group in the flora of the YaNAA is formed by species which distribution ranges lie within the territory of the YaNAA and "alien" they are only outside those ranges. These are the following species Inula britannica L., Erysimum cheiranthoides L., Erysimum odoratum Ehrh., Silene vulgaris (Moench) Garcke, Lathyrus pratensis L., Fragaria vesca L., Potentilla norvegica L., Galium verum L., Allium schoenoprasum L., A. strictum Schrad., Lemna trisulca L., Beckmannia eruciformis (L.) Host, Calamagrostis epigeios (L.) Roth, Phalaris arundinacea L., Phragmites australis (Cav.) Trin. ex Steud., Poa annua L. and P. sublanata Reverd. In the south and southeast of YaNAA, within the middle taiga subzone, in the Ob River valley, these species grow in the forest and meadow habitats. In the middle and northern part of the region, including peninsulas, they are anthropochores spreading via disturbed sites in settlements and along the roads. We did not include these species in the alien flora.

Conclusion
After appearing in new localities, alien species gradually adapt to their new environments. In the Western Siberian Arctic and Subarctic, it is still too early to speak about phytopollution and bioinvasions but the monitoring of alien species is a matter of necessity. In the Subarctic towns, there are certain positive effects of non-indigenous species in that they make the urban environment more diverse. Among introduced species, there are ornamental, medicinal, fodder plants and food plants. We did not observe spreading of alien species via slightly disturbed natural habitats comparable with such dissemination in more southerly regions. Regarding non-native species becoming detrimentally invasive, we feel that there is currently no imminent or significant threat.