Three new alien Chenopodiaceae species in the flora of Russia

1 Moscow State University, Leninskiye Gory, 1/12, Moscow, 119234, Russian Federation 2 Tomsk State University, Lenina Pr., 36, Tomsk, 634050, Russian Federation 3 Komarov Botanical Institute RAS, Prof. Popova St., 2, St. Petersburg, 197376, Russian Federation 4 Perkalsky Dendrological Park of the Komarov Botanical Institute RAS, Pyatigorsk, Stavropol Territory, 357506, Russian Federation 5 E-mail: suchor@mail.ru; ORCID iD: https://orcid.org/0000-0003-2220-826X 6 ORCID iD: https://orcid.org/0000-0003-4833-5953 7 ORCID iD: https://orcid.org/0000-0001-9954-2181 8 ORCID iD: https://orcid.org/0000-0002-5158-3096 * Corresponding author


Introduction
The Chenopodiaceae clade is recognized as a part of Amaranthaceae Juss. s. l. after extensive molecular studies (e. g., Cuénoud et al., 2002, Kadereit et al., 2003Brockington et al., 2009). The members of this clade play an important role in steppe, desert, and coastal vegetation types or are noxious weeds in temperate regions (e. g., Korovin, 1934;Danin, 1983;Australian vegetation, 1994;Busso, Bonvissuto, 2009). In Russia, the number of Chenopodiaceae species can provisionally be estimated as 180 (133 species in European Russia: Sukhorukov, 2014), but some difficult genera like Corispermum L. and Chenopodium L. have not been properly revised yet in the Asiatic part.
There are many articles reporting new alien Chenopodiaceae in different provinces of Russia. Such translocations are occurring from natural vegetation types to the north suffering habitat changes. In almost all cases, the species originate in the same continent (intracontinental introduction). The Central Asian species Atriplex laevis C. A. Mey., Axyris amaranthoides L., Corispermum declinatum Stephan ex Iljin, Salsola collina Pall., and Teloxys aristata (L.) Moq. are the most frequent invaders in different parts of European Russia (Sukhorukov, 2014) being synanthropic components of the flora. These examples do not include Chenopodiaceae crossing between continents. However, the vegetation in many subtropical regions is already facing a problem with naturalization of some Chenopodiaceae, especially Chenopodioideae from Australia, e. g. Atriplex inflata F. Muell., A. nummularia Lindl., A. suberecta Verdoorn to North and South Africa and South America (Maire, 1962;Germishuizen, Meyer, 2003;Brignone et al., 2016;APD, 2019) and Dysphania pumilio (R. Br.) Mosyakin et Clemants to Africa, South Europe, and the Americas (Uotila, Raus, Kalheber in Greuter, Raus, 2001 [with references therein]; Iamonico, 2011;USDA, NRCS, 2021;Uotila et al., 2021). The present article provides new information about the recent intercontinental introduction of three species of Chenopo-diaceae in different parts of Russia.

Material and Methods
The first author Alexander Sukhorukov (AS) has observed many native and alien Chenopodiaceae in different parts of the world, especially in European Russia (1997+), the Nepal Himalaya (2005)(2006)(2007)(2008)(2009)(2010)(2011)(2012)(2013)(2014)(2015), and African countries (2009+). The morphological evaluation of the three species under consideration has also been provided by AS. The continuous field investigations were carried out in North-West Russia (the Leningrad Region) by Elena Glazkova (1993+) who also paid special attention to alien species during field trips to the North Caucasus (2005) and the Far East (the Kuril Islands) (2019). Dmitry Shilnikov (DS) carried out the field studies in the North Caucasus (1999+) covered the Krasnodar Territory, Stavropol Territory, the Republics of Adygeya, Karachayevo-Circassian, Kabardino-Balkarian, North Ossetia -Alania, Daghestan (Russia) as well as Azerbaijan. Some other territories of Russia were also visited by DS. The identification of Chenopodiastrum simplex collected by E. Glazkova was also confirmed by the phylogenetic analysis that will be reported in another paper (Uotila et al., in prep.).
Morphology. For a detailed description see Basset, Crompton (1982, as Chenopodium gigantospermum). Related to Chenopodiastrum hybridum (L.) S. Fuentes, Uotila et Borsch and C. badachschanicum (Tzvelev) S. Fuentes, Uotila et Borsch. From the first species, C. simplex is easily differentiated by the loose pericarp and rugose seeds (C. hybridum has adherent pericarp and foveolate seeds). Both C. simplex and C. badachschanicum possess the same carpological characters mentioned above. However, the leaves demonstrate some differences: they are ovate in outline, dentate or with attenuate lobes in C. simplex and usually triangular in C. badachschanicum.
To check the relationships in Chenopodiastrum and reveal the taxonomic status of a sample collected in the Leningrad Region, we conducted a more detailed phylogenetic analysis of the genus compared with the previous molecular trees (Fuentes-Bazan et al., 2012). The results presented in Uotila et al. (in prep.) revealed that the sample from Russia falls within one subclade with another sample of C. simplex taken from North America.
Habitat. Not mentioned on the label, but the specimen seems to have been collected in a ruderal site.
General distribution. Australia; as alien in W and C Europe, South America, southern Africa. Sukhorukov A. P. Three new alien Chenopodiaceae species in the flora of Russia  Morphology. The description of this species is available, e. g., in Wilson (1984) and Sukhorukov (2014). Compared to Dysphania from Africa and Asia (see detailed investigations of Uotila, 2013;Sukhorukov, 2014;Sukhorukov, Kushunina, 2014;Sukhorukov et al., 2019;Uotila et al., 2021), this species has white (not green) incurved perianth segments and other reproductive characters. Compared with D. carinata, D. pumilio has slightly keeled (nor carinate or cristate), glabrous or slightly hairy perianth segments.
Habitat. A small population (10 m 2 ) was found near a private house in a disturbed habitat, together with Polygonum arenastrum Boreau, Poa pratensis L., Plantago major L., and Taraxacum officinale F. H. Wigg.
General distribution. Australia; as alien and naturalized in N and S America, N, S and E Africa, South Europe, East Asia.

Discussion
The introduction with subsequent naturalization of alien species and possible transformation of natural and secondary habitats is one of the biggest problems in the biological sciences (Didham et al., 2005;Traveset, Richardson, 2006;Pyšek et al., 2017;Russell et al., 2017). In the Chenopodiaceae clade (Amaranthaceae s. l.), some species, especially from Chenopodioideae, are widespread weeds in temperate regions of Eurasia, as well as being alien    son, 1984). A large number of Eurasian Chenopodiaceae with further naturalization were discovered in temperate South and North America (e. g., Aellen, 1929;Zappettini, 1953;Clemants, Mosyakin, 2003;Brignone et al., 2016;Jocou et al., 2020;Brignone, Denham, 2021). Similarly, many Australian and American Chenopodiaceae, especially different Chenopodium taxa (recently considered within the genera Chenopodium s. str., Blitum, Lipandra and Oxybasis: Fuentes-Bazan et al., 2012), were discovered in Europe especially in the first half of the 20 th century, mostly brought with wool and other goods (Aellen, 1929;Uotila, 2001). Here we pay special attention to the distribution of Chenopodiastrum simplex, Dysphania carinata and D. pumilio outside their natural range, with further categorization of their possible alien status.
Chenopodiastrum simplex is native to North America and seems to be a rare casual alien species in Europe known in Fennoscandia mostly from the first half of the 20 th century (Uotila, 2001). However, examination of herbarium collections in Vienna (W) by the first author (AS) showed the presence of plants with the same leaf and fruit/seed characters in Austria. According to GBIF (2019+), the species is also known from Germany, the Netherlands and Spain, but the corresponding records have not been checked by us. To date, the recent distribution of C. simplex in Europe requires further study. The report of C. simplex in Siberia (Lomonosova, 1992, as Chenopodium hybridum subsp. gigantospermum) is erroneous and a corresponding specimen belongs to C. badachschanicum (Tzvelev) S. Fuentes, Uotila et Borsch, a species widely distributed in Central Asia, South Siberia, the Himalaya and Tibet (Uotila et al., in prep.). Both species are morphologically similar, and the exact identification may be verified by phylogenetic analysis. 82 Sukhorukov A. P. Three new alien Chenopodiaceae species in the flora of Russia  Chenopodiastrum simplex seems to be a recent immigrant to the remote Moschny Island, since it was not found during previous expeditions to the islands of the Eastern Gulf of Finland (Glazkova, 2001). Although only one exemplar of C. simplex was found in August 2017, and it was not possible to visit this island later, the population may not be extinct owing to ability of many annual Chenopodioideae including Chenopodiastrum to form a viable soil seed bank for at least several years in conjunction with the carpological characteristics (different thickness of the seed-coat testa resulting in the heterospermous seeds) and physiological dormancy (Sukhorukov, Zhang, 2013;Sukhorukov, 2014, with references therein). The introduction of C. simplex may be connected with crop import. Similarly, C. simplex was brought into Fennoscandia as a rare casual species with North American grain and soybeans (Uotila, 2001). The current status of C. simplex in Russia can be described as 'casual alien', as for some other rare exotic Chenopodiaceae in the Leningrad Region, e. g. Beta maritima L. and Atriplex oblongifolia Waldst. et Kit. found on the islands of the Gulf of Finland earlier (Glazkova, 2006;Sukhorukov, Uotila, 2007).
The native distribution area of Dysphania carinata covers the easternmost part of Australia including Queensland, New South Wales and Victoria (Wilson, 1984). As an alien plant, it clearly prefers areas with arid climate, e. g., Namibia, where it mostly occupies dried-up river beds and can be considered as naturalized species (AS, pers. obs. in 2017(AS, pers. obs. in -2018. In South Africa, it has been found in many regions (Germishuizen, Meyer, 2003). The records in other semi-arid and arid regions of Africa are still scattered (Brenan, 1954(Brenan, , 1988; APD, 2019; AS, pers. obs. and a specimen [MW] collected in Tanzania in 2020). Dysphania carinata seems to be introduced in Europe in the late 19 th century with Australian wool (Aellen, 1929, as Chenopodium carinatum) and it is also reported in some parts of West, Central and North Europe (Uotila, 2011) andWest Asia (Al-Turki, Ghafoor, 1996, as Chenopodium carinatum). However, this name is frequently misapplied to the closely related D. pumilio in many floras and checklists of Europe, another alien on the continent (Chytry, 1993). For this reason, the naturalization status of D. carinata has not been properly assessed, the records have not been mapped 84 Sukhorukov A. P. Three new alien Chenopodiaceae species in the flora of Russia (Jalas, Suominen, 1980), and the species considered to be a casual alien (Uotila, 2011;Sukhorukov, 2014). In East Asia, it is reported from Japan (GBIF, 2019+), but at least some records refer to D. pumilio (Flora-Kanagawa Association, 2018;A. Sukhorukov, re-identifications in different herbaria). The reverse misidentification occurred in Ignatov (1988), when a specimen of D. carinata from the Primorye Territory of Russia was erroneously identified as D. pumilio. Thus, we exclude D. pumilio from the flora of the Russian Far East. Based on the scattered records of D. carinata in Eurasia, its naturalization in the Russian Far East seems to be impossible due to unsuitable climatic conditions (e. g., high precipitation, low winter temperatures).
Dysphania pumilio occurs as a native species mostly in southern Australia (Wilson, 1984) with further spreading as an alien into many subtropical regions of southern, central and eastern Africa (Brenan, 1954;Germishuizen, Meyer, 2003;Sukhorukov et al., 2016), Japan (Flora-Kanagawa Association, 2018), North and South America (Gleason, 1952 as Chenopodium pumilio;Clemants, Mosyakin, 2003;Funez et al. 2017;Brignone, 2020). At present, it is considered to be an invasive plant in North America (CABI, 2021). Knowledge of the occurrence and status of D. pumilio in Europe has changed dramatically. In the beginning of the 20 th century this species had not yet been noticed (Aellen, 1929) owing to confusion with D. carinata (re-identifications of the late P. Aellen and A. Sukhorukov in 2019, G!), but several decades later, it was being reported as an alien species in West and Central Europe (Aellen, 1961;Jalas, Suominen, 1980). The first collections from Central Europe are dated in 1870s (Aellen, 1961). Lhotská, Hejný (1979) reported the presence of a viable seed bank based on observations in the Czech Republic as well as different dispersal characteristics facilitating the naturalization of D. pumilio in Central Europe. To date, the alien status of D. pumilio has been changed to 'naturalized alien' in Central, South and East Europe (Ukraine) (Uotila, 2011). The recent detailed investigations confirm its naturalized and invasive status in at least some countries of South Europe, namely in Spain (Castroviejo, 1990;Uotila, 2011), Italy (Iamonico, 2011), andSerbia (Bogosavljević, Zlatković, 2017) being found in various disturbed habitats. According to observations by the first author (AS), D. pumilio is common in Barcelona (Spain) and Lisbon (Portugal) growing in asphalt cracks and sandy areas. First records of the species as a casual alien are known from Bulgaria (Grozeva, 2007) and Belarus (Dzhus, 2011). Based on the literature data and our own observations, D. pumilio is able to naturalize in the countries with subtropical and warm temperate climate, and therefore further records of the species in Russia are expected in the North Caucasus and in the arid regions of European Russia.

Conclusion
The three species reported here have different alien status in the secondary distribution areas, and we assume their different naturalization status in Russia. Dysphania pumilio could potentially become a successful invader in ruderal sites in the southern part of European Russia and the North Caucasus.

Acknowledgments
The research of A. Sukhorukov was carried out in accordance with the scientific programe 121032500084-6 of the Department of Higher Plants (Lomonosov Moscow State University). The study of E. Glazkova and V. Shvanova was carried out within the framework of the research project no. АААА-А 19-119031290052-1 (Vascular plants of Eurasia: systematics, flora, plant resources) of the Komarov Botanical Institute, RAS. The field investigations of E. Glazkova on Moschny Island in 2017 were supported by the Complex Expedition "Gogland" of the Russian Geographical Society, and she thanks the organizers and all participants of the expedition. We thank Geoffrey Harper for the proofread of the paper and Maria Kushunina for help in preparation of the final maps. We are also indebted to Pertti Uotila who paid our attention to an unusual specimen of Chenopodiastrum from Moschny Island. We also thank Marina Legchenko (LE) and Nina Stepanova (MHA) for the scanned images of Chenopodiastrum simplex and Dysphania carinata, respectively.