﻿Revised checklist of endemic vascular plants of Kazakhstan

﻿Abstract We compiled a checklist of endemic vascular plants occurring in Kazakhstan, employing an exhaustive examination of literature sources, herbarium collections, databases and field observations. Our study reveals that 451 taxa can be considered endemic to Kazakhstan, constituting 7.97% of the total vascular plant diversity in the country. These endemic taxa, originating from 139 genera and 34 families, predominantly thrive in the southern regions of Kazakhstan, specifically in the mountain ridges of the Kazakh part of the Tian Shan, including Karatau (123 taxa), Dzungarian Alatau (80 taxa) and Trans-Ili and Kungey Alatau (50 taxa). Notably, 107 endemic species are granted legal protection. Detailed information regarding life form, life cycle, conservation status and geographical distribution across floristic regions was meticulously compiled for each endemic taxon. Of the six groups of life forms, herbs include the highest part of endemic taxa (367 taxa), followed by dwarf semishrubs (25 taxa), shrubs (23 taxa), subshrubs (20 taxa), undershrubs (13 taxa) and trees (3 taxa). The observed life cycles are perennials (408 taxa), annuals (33 taxa) and biennials (10 taxa). This paper serves as a fundamental groundwork for prospective investigations aimed at assessing population sizes and hotspots of plant endemism throughout Kazakhstan, crucial for determining conservation status of endemic plants.


Introduction
Endemic plants hold particular importance in studying the history of flora and vegetation of diverse geographical regions, since they represent an important element of biodiversity and serve as vital benchmarks for identifying areas of high biodiversity value.In recent years, much attention has been paid to the study of endemic plants, as evidenced by a large number of scientific publications (Tojibaev et al. 2020a;Baasanmunkh et al. 2022;Erst et al. 2022;Chung et al. 2023;Villaseñor et al. 2023).
Kazakhstan occupies a central position within Eurasia and holds a notable distinction of being the ninth largest country globally, with 2,724,900 km 2 of land area.The territory of Kazakhstan is characterised by a remarkable ecological heterogeneity (Abdulina 1999;Akzhigitova et al. 2003), marked by prominent zonal boundaries, notably the demarcation between the cold-temperate and temperate regions of Northern Eurasia and the Irano-Turanian warm region with the Mediterranean-like type of climate, the latter encompassing the southern part of Kazakhstan.
The remarkable diversity of natural conditions in Kazakhstan contributes to the exceptional richness of its flora, its notable originality and a significant number of endemic plant species in Kazakhstan.According to the latest inventory, 5,658 vascular plant species, representing 159 families and 1,067 genera, occur in the country (Abdulina 1999).
The investigation of endemic plant species, which represent a vital and highly vulnerable component of biodiversity, has garnered significant attention in numerous countries.The number of endemic plants in the countries neighbouring Kazakhstan varies, with China exhibiting the highest number of endemic species at 14,939 (Huang et al. 2011).There are over 2,700 endemic taxa in Russia (Kamelin and Budantsev 2019), Mongolia has 102 taxa (Baasanmunkh et al. 2022), Kyrgyzstan has 393 taxa (Lazkov and Sultanova 2014) and Uzbekistan has 378 taxa (Sennikov et al. 2016).Based on a comprehensive review of the "Flora of Kazakhstan" (Pavlov 1956(Pavlov -1966)), Goloskokov (1969) counted 760 endemic species from 199 genera and 47 families in Kazakhstan.Otherwise, various sources estimated the presence of 709 to 823 species of endemic plants in Kazakhstan (Pavlov 1956(Pavlov -1966;;Bykov 1966;Goloskokov 1969;Baitenov 2001;Gemedjieva et al. 2010).
The available information regarding the composition of endemic plant species in Kazakhstan, as documented in the "Flora of Kazakhstan" (Pavlov 1956(Pavlov -1966) ) and other related sources (Bykov 1966;Goloskokov 1969), is largely outdated.Since then, numerous species previously classified as endemic have been discovered beyond the borders of Kazakhstan or reduced to synonyms.In addition, in the last 10 years alone, more than 25 species of endemic plants have been described as new to science from the territory of Kazakhstan, for example: six species of Tulipa (T.annae J.de Groot & Zonn, T. auliekolica Perezhogin, T. dianaeverettiae J.  (Pimenov and Kljuykov 2014) and Nitraria iliensis Banaev & Tomoshevich (Banaev et al. 2023).
Consequently, the current knowledge regarding the species diversity of endemic plants in Kazakhstan remains poorly available.In order to address this knowledge gap, our research endeavour aimed to compile the checklist of endemic vascular plants in Kazakhstan, based on an extensive analysis of literary sources, comprehensive revision of herbarium collections and data from field observations.
Within the scope of this investigation, we provide a list and an analysis of national endemic vascular plants growing strictly within Kazakhstan (see Appendix 1).This study considers two taxonomic levels of endemic plants: species and subspecies; taxa with a rank lower than subspecies were not considered.Additionally, we present a separate list encompassing sub-endemic taxa (see Suppl.material 1).In this paper, sub-endemics refer to taxa that were formerly considered endemics, but subsequently found in a neighbouring country or countries, based on published literature or herbarium material.In addition, we present a list of former endemics of Kazakhstan reclassified as synonyms of taxa with broader geographical distributions (see Suppl.material 2).
The distribution of each endemic taxon in Kazakhstan is given according to the floristic division of the country (Pavlov 1956).This division partitions Kazakhstan's territory into 29 distinct floristic regions and seven subregions (Fig. 1).
The systematic order and taxonomic position of the families are based on the classification of angiosperms by APG IV (2016).The names of the accept-ed genera and species are mostly in accordance with Plants of the World Online (POWO 2023), with corrections according to recently-published taxonomic revisions.The authorship of species, genera and families has been critically cross-checked against the information provided in the International Plant Names Index (IPNI 2023).

Results
Based on a rigorous revision of endemic vascular plants in Kazakhstan, a total of 451 taxa have been identified as endemic to the country (Appendix 1), which account for 7.97% of the total number (5,658 species) of vascular plants in Kazakhstan (Abdulina 1999) 22taxa from 1 genus), Liliaceae Juss.(18 taxa from 3 genera), Rosaceae Juss.(17 taxa from 7 genera), Poaceae Barnhart (15 taxa from 8 genera) and Amaranthaceae Juss.(14 taxa from 10 genera) (Fig. 2A).The remaining 23 families are represented by one to 10 species each.
Genera with the greatest number of endemic taxa are as follows: Astragalus L. with 46 taxa, Oxytropis DC. with 22 taxa, Allium L. with 21 taxa, Taraxacum F.H.Wigg.with 20 taxa, Jurinea Cass.with 20 taxa, Tulipa L. with 13 taxa, Lappula Moench with 11 taxa, Artemisia L. with nine taxa, Zygophyllum L. with nine taxa and Phlomoides Moench with nine taxa.The remaining genera are represented by one to seven taxa (Fig. 2B).
Amongst all endemic plants in Kazakhstan, 107 species, constituting 23.7% of the overall number of endemic taxa, are presently under the state-level legal protection (Baitulin 2014).
According to the results of our research, 341 taxa previously considered endemics are recognised as sub-endemics of Kazakhstan (see Suppl.material 1) because they were found in the neighbouring countries.The largest number of plants previously considered endemic to Kazakhstan was found in China -152 taxa, Kyrgyzstan -138 taxa, Uzbekistan -71 taxa, Russia -59 taxa, Mongolia -59 taxa, Tajikistan -31 taxa, Turkmenistan -19 taxa.The total of 169 former endemic taxa of Kazakhstan were synonymised to taxa with wider distribution ranges (see Suppl.material 2).

Discussion
Based on our critical evaluation of vascular plants of Kazakhstan, 451 taxa are identified as endemic to the country (Appendix 1).This figure corresponds to  55-63% of the previously-reported numbers, i.e. 709-823 species (Pavlov 1956(Pavlov -1966;;Bykov 1966;Goloskokov 1969;Baitenov 2001;Gemedjieva et al. 2010).The substantial difference in the number of endemic taxa compared to earlier publications is due to their reliance on outdated information solely derived from the nine-volume edition of the Flora of Kazakhstan (Pavlov 1956(Pavlov -1966)).Our review reveals that 341 taxa previously considered endemics are to be treated as sub-endemics of Kazakhstan (see Suppl.material 1), whereas 169 former endemic taxa were synonymised to taxa with wider distribution ranges (see Suppl.material 2).For example, two most recent publications removed two endemic taxa from Kazakhstan: Allium valentinae Pavlov was found in Kyrgyzstan (Sennikov and Lazkov 2023), whereas the generic status of Pseudomarrubium was rejected (Zhao et al. 2023).Such examples provide evidence of ongoing taxonomic and floristic studies that are constantly shaping the list of endemic plants of Kazakhstan.Despite the extensive territory and diverse natural conditions of Kazakhstan, the occurrence of endemic taxa appears highly uneven in the country.The largest number of endemic plants is concentrated in mountainous areas, specifically in the southern and south-eastern parts of Kazakhstan, within the following floristic regions: Karatau (123 taxa), followed by the Dzungarian Alatau (80 taxa) and Trans-Ili Kungey Alatau (50 taxa).These results fully align with the analysis presented by Gemedjieva et al. (2010), who examined the distributions of endemic plants in Kazakhstan, despite their use of outdated taxonomic and distributional data.The distribution pattern of endemic taxa across the territory of Kazakhstan supports the assertion made by Körner (2002) that mountain systems serve as biodiversity and endemism hotspots due to the compression of distinct climatic zones over varying altitudes.According to the latest global analysis of seed plant endemism, the territory of Kazakhstan is assigned to the centre of neo-endemism (Cai et al. 2023).The mountainous regions of Tian Shan in the south and the Altai Mountains in eastern Kazakhstan appear to have favoured this, because the mountainous regions exhibit a great diversity in their plant lineages and, therefore, contribute to high levels of neo-endemism.
The distribution of endemic plants in Kazakhstan is presumably influenced by the geological and climatic history of the territory.Past climate change and geological history help to explain how diversification and relictualisation shape the distribution of neo-and paleoendemism and simultaneously phylogenetic endemism worldwide (Cai et al. 2023).The influence of geological history on speciation, differentiation, migration and extinction of species has been highlighted by many scientists (Takhtajan 1969;Raven and Axelrod 1974;Latham and Ricklefs 1993;Axelrod et al. 1996;Huang et al. 2011).A prime example illustrating this phenomenon is the endemic taxa richness in the ancient Karatau Mountains (123 taxa), located at the westernmost limit of the Tian Shan.The Karatau Mountains possess a complex geological composition, characterised by the presence of the oldest Precambrian shale formations in Central Asia, as well as the Lower Paleozoic formations consisting of metamorphosed limestones and shales, overlain by a quartzite stratum (Kamelin 1990).An important factor in the distribution of endemic plants is long-term climatic stability.Central Asia is known for the presence of ancient plant lineages which survived there due to the continuous history of suitable climatic conditions (e.g. in Lactuca s.l.: Kilian et al. (2017)).The influence of geological and climatic history on the distribution of endemic plants in Kazakhstan requires additional research, given the poorly-studied bedrock types in Central Asia.
In the flora of Kazakhstan, herbs include most of the endemic taxa.The life forms of plants reflect their adaptability to environmental conditions and form the units of ecological classification, grouping plants with similar adaptive structures (Aipeisova 2009).According to Yurtsev (1976) and Rabotnov (1978), studies of life forms contribute to the understanding of species biology and their roles within ecosystems.The diversity of life forms represents a cumulative effect of long-term evolutionary processes responding to gradual changes in regional ecological conditions (Keller 1938;Shennikov 1950;Serebryakov 1964).
Amongst endemic plants of Kazakhstan, perennials (408 taxa) are most numerous.A global analysis of the distribution of plant life cycles around the world has shown that annual plants predominate in hot and arid conditions, especially during the long dry season (Poppenwimer et al. 2022).The number of annuals and biennials in Kazakhstan is 43 taxa or 9% of the total number of endemic plants of Kazakhstan.The distribution of endemic annuals over the territory of Kazakhstan is relatively uniform.The greatest number of annuals is noted in Western Upland (7 taxa), Zaysan (6 taxa) and Karatau (6 taxa).Amongst the families, the greatest number of annual endemic taxa is registered in Boraginaceae Juss.(17 taxa), Brassicaceae Burnett (8 taxa) and Amaranthaceae Juss.(6 taxa); in other families, 1-3 taxa are registered.
Given that numerous endemic plant species have restricted distributions, which makes them more prone to extinction (Myers et al. 2000;Pitman and Jørgensen 2002), it is crucial to emphasise the assessment and protection of such species (Baasanmunkh et al. 2022).Amongst 451 endemic taxa of Kazakhstan, 107 species are currently under state protection.We consider it necessary to further re-assess the status of protection of endemic plants of Kazakhstan using IUCN criteria.
During the critical examination of endemic plants in Kazakhstan, we found that some endemic plants were inaccurately attributed to other countries in the Plants of the World Online (POWO 2023).For instance, Arthrophytum subulifolium Schrenk and Atriplex iljinii Aellen, according to POWO, are supposedly present in Turkmenistan.However, Arthrophytum subulifolium Schrenk exclusively grows in a narrow region of the Chu-Ili Range in Kazakhstan (Osmanali et al. 2019), while Atriplex iljinii is solely found in the Mangistau, Aktobe and Kyzylorda Regions of Kazakhstan (Suchorukow 2007).Stipa argillosa Kotukhov and Thalictrum bykovii Kotukhov, along with Gagea azutavica Kotukhov, are incorrectly recorded in POWO as species native to the Altai Republic in the Russian Federation, whereas these species were described from East Kazakhstan (Kotukhov 1989(Kotukhov , 1990(Kotukhov , 1998)).

Conclusions
This checklist includes all strictly endemic plants of Kazakhstan, consisting of 451 taxa (species or subspecies) belonging to 139 genera and 34 families.The largest number of endemic taxa is concentrated in mountainous areas, specifically in the southern and south-eastern parts of Kazakhstan.
This paper serves as a fundamental groundwork for prospective investigations aimed at assessing population sizes and numbers of endemic taxa throughout Kazakhstan, crucial for determining their conservation status.Of course, this checklist of plant endemics of Kazakhstan is not final and will be revised in the future as a result of ongoing taxonomic and floristic studies.*Tulipa orthopoda Vved.listed in POWO is recognised as a synonym for Tulipa bifloriformis Vved., based on Christenhusz et al. (2013) and Everett (2013).This scientific paper also notes that the species status of Tulipa orthopoda should be warranted, based on differences in morphological characters and flowering period, but further fieldwork is required to establish the variability of T. bifloriformis in the wild.*Tulipa brachystemon Regel in POWO is recognised as a synonym for Tulipa tetraphylla Regel, also according to Christenhusz et al. (2013) and Everett (2013).However, Zonneveld (2009) (Kotukhov 1998).The Azutau Ridge borders the basin of Lake Markakol from the south and is entirely situated within the territory of Kazakhstan (Yegorina et al. 2003).*Thalictrum bykovii Kotukhov, as well as the previous species in POWO, is erroneously listed for the Altai Republic of the Russian Federation.This species was also described from the territory of East Kazakhstan.Type: Southern Altai, eastern spurs of Azutau Ridge, Mramornaya Mount, Middle belt, 900-1100 m above sea level, south-eastern slope, steppe shrub meadows, 14/06/1984, Yu.Kotukhov (LE).

Figure 2 .
Figure 2. The largest families by the number of endemic taxa (A).The largest genera by the number of endemic taxa (B).

Figure 3 .
Figure 3. Endemic taxa richness in the floristic regions of Kazakhstan (A).The number of endemic taxa in the floristic regions of Kazakhstan (B).