Alien flora of Uttarakhand, western Himalaya: a comprehensive review

: Alien plant species have captured attention of the scientific community, ecologists, and environmentalists throughout the world. Like other regions, the Himalayan region is also grappling with the disrupting impacts of plant invasions. Based on an extensive review of studies conducted on alien plant species in the Indian Himalayan region, we report 728 alien plant species belonging to 450 genera under 108 families in the state of Uttarakhand, which represents 15% of the state’s flora. Fabaceae (89 species under 49 genera) followed by Asteraceae (63 species under 43 genera) and Poaceae (50 species under 35 genera) were the most diverse families amid alien species. Eucalyptus (15 species) followed by Ipomoea and Euphorbia (12 species each) and Pinus (11 species) were the most diverse genera. The maximum numbers of aliens (mostly herbs) in the state were introduced from America, followed by Europe. Owing to relatively high number of alien plant species in Uttarakhand, it is submitted that serious ecological and socio-economic consequences are likely to escalate in the future.

For Focus, Scope, Aims, and Policies, visit https://threatenedtaxa.org/index.php/JoTT/aims_scopeFor Article Submission Guidelines, visit https://threatenedtaxa.org/index.php/JoTT/about/submissionsFor Policies against Scientific Misconduct, visit https://threatenedtaxa.org/index.php/JoTT/policies_variousINTRODUCTION Non-native species or alien species have captured attention of the scientific community, ecologists, and environmentalists.It was once considered that alien plants will not spread in high mountains, but ongoing processes of economic development such as transboundary trade and migration have altered the situation (Khuroo et al. 2007).Recent studies have reported that increasing global trade and climate change will drastically affect the spread of non-native species (Khuroo et al. 2007;Bellard et al. 2018;Panda & Behera 2019;Tripathi et al. 2019) outside their native habitats.Several studies have attempted to investigate the impact of climate change on the spread of invasive alien species (IAs) using predictive modelling (Wasowicz et al. 2013;Chakraborty et al. 2018;Wan & Wang 2018;Mungi et al. 2020).According to Ahmad et al. (2019), approximately 65% of the total geographical area of India is prone to invasion by Parthenium hysterophorus, one of the world's worst weeds, with the western Himalaya being highly vulnerable under changing climate scenarios.Adhikari et al. (2015) identified invasion hotspots of alien species in India, and reported that most of the biodiversity hotspots, coastal regions and forest reserves are prone to plant invasion.Half of the total geographical area of India is vulnerable to invasion by alien plant species owing to favorable climatic conditions.Mungi et al. (2018) and Thapa et al. (2018) predicted that global climate change in the future will lead to expansion of invasive species in the western Himalaya.Weber & Li (2008) suggested that economic development is directly proportional to the rate of biological invasion.Also, it is observed that higher levels of imports and human development were responsible for the increase in the number of invasive species (Nunez & Pauchard 2009).Invasive species have high capacity to tolerate wide environmental conditions, high growth and dispersal rates along with short generation time, which resulted in their successful establishment (Lamsal 2018).Besides having aesthetic costs, such as change in land-use patterns, reduced crop production (Born et al. 2004), loss of native species, degradation of resources (Everard 2018), these invasive alien species incur huge economic costs.Further, the annual costs due to invasive alien species have been estimated to about US$137 billion in USA, US$14.5 billion in China (Weber & Li 2008), €12 billion in Europe, and £1.7 billion in Great Britain (Reshi & Khuroo 2012).Considering this in view, the documentation, identification, and economic evaluation of invasive alien species at the national level in general and at regional levels, specifically would be required.
The spread of IAs has raised significant concerns around the world; studies aimed at tracking and understanding the impact of alien flora have been undertaken in China (Liu et al. 2005;Weber & Li 2008;Qin et al. 2018;Yang et al. 2018b;Zhu et al. 2018), Japan (Enomoto 1999), Korea (Koh et al. 2000), Taiwan (Wu et al. 2004), and Singapore (Corlett 1988).India is also facing problems of alien plant invasion that are expected to exacerbate further.Once known for their harsh climate, diverse habitats, varied environmental conditions and limited accessibility, the Indian Himalayan region (IHR) is now at high risk due to human interventions, climate change and economic development (Yang et al. 2018a).Despite of rich floral diversity and vulnerability to changing scenario, minuscule efforts have been attempted to inventorize, predict and map the alien flora of IHR.Thus, documentation of the alien flora of the region is called for to develop management strategies.Although a handful of workers such as Pathak et al. (2019) have highlighted the need and importance of studies relating to alien plant invasion in IHR.Further, comprehensive studies on the alien floras exists for some parts of the IHR such as the Kashmir Himalaya (Khuroo et al. 2007;Dar et al. 2018;Haq et al. 2018;Mehraj et al. 2018a,b;Muzafar et al. 2019;Shaheen et al. 2019), Himachal Pradesh (Jaryan et al. 2013;Ahmad et al. 2018), Arunachal Pradesh (Kosaka et al. 2010), and its adjoining hilly regions of Assam (Barua et al. 2013), West Bengal (Maiti & Bakshi 1981), Manipur (Khomdram et al. 2011) and Tripura (Debnath et al. 2017;Debnath & Debnath 2017).Unfortunately, a detailed inventory of alien plants is still lacking for the state of Uttarakhand.As a Himalayan biodiversity hotspot, the mountainous state has been invaded by several alien plant species.Noteably, a few studies at regional level have been conducted such as Negi & Hajra (2007) listed 436 alien plant species of Doon valley, and Sekar et al. (2012) documented a total of 163 invasive alien plant species in Uttarakhand.In spite of the fact that only a small percentage of alien plants have the potential to become invasive, the damage they incur is irreparable.Thus, a detailed inventory documenting alien plants, including naturalized as well as invasives, for the entire Indian Himalayan region in general and the state of Uttarakhand specifically is not yet available.The objective of this communication is to present a checklist of alien plants for Uttarakhand, and highlight the significance of studies carried out on alien plant species in the Indian Himalayan region.

Study area
The state of Uttarakhand is largely mountainous and shares international boundaries with China in the north and Nepal in the east.With an area of 53,483 km 2 , the state lies between 30.0668 0 N & 79.0193 0 E. Nested in the western Himalaya, Uttarakhand varies greatly in terms of altitude, climate and topography.This variation has resulted in the successful establishment of diverse flora that comprises approximately 5,000 vascular plant species in the state (Rana & Rawat 2017) including alien plant species.According to Champion & Seth (1968) and India State of Forest Report (2019), the state comprises of eight forest types, viz., tropical moist deciduous, tropical dry deciduous, sub-tropical Himalayan pine forests, Himalayan moist temperate, Himalayan dry temperate, sub-alpine forests, moist alpine scrub, and dry alpine scrub.The elevation ranges between 210-7,817m with glaciers at the highest elevation to tropical forests at the lower elevations.The average annual precipitation ranges 1,000-2,500 mm (Kala 2014) and temperature ranges from sub-zero to 43 °C (India State of Forest Report 2009).

Data collection
An extensive review of existing information in the form of scientific research articles, online database, books, reports, and thesis dealing with alien plant research and inventories were examined.Indian herbaria such as the Botanical Survey of India (BSD), Dehradun, Forest Research Institute (DD), Dehradun and Wildlife Institute of India (WII), Dehradun were consulted to validate the species.The listing of alien plant species was enriched by collating information from existing flora and relevant scientific literature on the state, such as Hajra & Balodi (1995), Gaur (1999), Singh & Prakash (2002), Uniyal et al. (2007), Negi & Hajra (2007), Reddy (2008), Sekar et al. (2012), Jaryan et al. (2013), Sankaran & Suresh (2013), Rana & Rawat (2017), Inderjit et al. (2018), andPusalkar &Srivastava (2018) to name a few.Thus, the extensive review of these studies resulted in a master list comprising of the plant species which are alien to the state of Uttarakhand along with information on their nativity and life form.The authenticity of the plants occurring in the state and their growth form was also determined using regional floras or checklists such as Kanjilal (1928), Babu (1977), Osmaston (1994), Hajra & Balodi (1995), Gaur (1999), Singh & Prakash (2002), Uniyal et al. (2007), and Pusalkar & Srivastava (2018).Further, the plant names and family were rechecked using 'Plants of the World online (POWO)' (www.theplantsoftheworldonline.org.), the Plant List (www.theplantlist.org),and Tropicos (www.tropicos.org).Elimination of the synonyms was done to avoid the taxonomic inflation.The nativity of the plant species was established following POWO; International Plant Names Index (www.ipni.org),Khuroo et al. (2007), Negi & Hajra (2007), and Jaryan et al. (2012).The nativity of the species was further categorized at the continent level or geographical regions such as Africa, America (includes plant species occurring in Central or Tropical North and South America), North America (NAM), South America (SAM), Asia (excluding the Indian sub-continent, i.e., countries such as Bangladesh, Bhutan, India, Maldives, Nepal, Pakistan, and Sri Lanka), Australia, Europe, and Oceania.This resulted in the generation of a complete and updated list of the alien plant species that are reported in the state of Uttarakhand, located in the western Himalaya (Table 1).
With respect to nativity, America (plant species occurring in central or tropical, North, and South America) contributed the maximum (146 species), i.e., 20% of alien introductions in Uttarakhand, followed by Europe 104 species (14%), South America 91 species (13%), Asia (excluding the Indian sub-continent) 80 species (11%), North America 79 species (11%), and Africa 76 species (10%) (Table 3).The remaining 20% of the alien plant species were contributed by other continents or geographical regions.Noteably, majority of the herbs were introduced from America (Table 3).Interestingly, a few workers have provided an account on the status of naturalized and invasive alien plants in different regions of IHR, the details are provided in Table 4.

DISCUSSION
Uttarakhand harbours a rich diversity of natural resources.Several workers (Kala & Rawat 2004;Uniyal et al. 2007;Mathur & Joshi 2013;Rai et al. 2017) have explored the rich floral diversity of this Himalayan state.Several studies have estimated aliens in different regions of India, for instance, Nayar (1977) reported that 18% of the Indian flora comprise of alien plant species.Khuroo et al. (2007) reported a total of 571 alien plant species (29%) from the Kashmir Himalaya.Jaryan et al. (2013) estimated that almost 14% of the flora of Himachal Pradesh comprises of alien plant species.Inderjit et al. (2018) documented naturalized alien plant species in the Indian states and found 181 alien species that have naturalized in Uttarakhand.According to Dutta (2018), climate change accelerates alien species invasion whereby a number of non-invasive species may become invasive.Negi et al. (2019) reported that increased level of demographic transitions and climate change will further exaggerate the situation in IHR, thus enabling suitable conditions for the spread of invasive alien species.
Of 108 plant families reported, 20 families comprise more than 68% of the alien flora of the state.Sekar et al. (2012) also reported Fabaceae as the largest family in terms of IAs in Uttarakhand.Reddy (2008) reported that Asteraceae also contributed a major portion of exotics in India.Khuroo et al. (2007) and Jaryan et al. (2013) also reported the dominance of Asteraceae and Poaceae from the Himachal Pradesh and Kashmir Himalaya, respectively.Subsequently, Baard & Kraaij (2014) in South Africa and Shen et al. (2017) in Yunnan province of China reported dominance of Asteraceae followed by Fabaceae and Poaceae that accounts for majority of the alien flora.Categorization of the growth form showed the preponderance of herbs (46%) which may be associated with its short generation time, greater viability and the ability to tolerate wide environmental fluctuations.Interestingly, this is in agreement with the other studies (Khuroo et al. 2007;Reddy 2008;Sekar et al. 2012;Adhikhari et al. 2015;Rastogi et al. 2015;Inderjit et al. 2018) carried out in India as well as in the world (Baard & Kraaij 2014;Shen et al. 2017;Lee et al. 2018;Vinogradova et al. 2018).
A large number of aliens in Uttarakhand are reported from America, accounting for the majority of herbs.A majority of alien introductions in China (Weber et al. 2008) and India (35%) (Khuroo et al. 2012), specifically in Himachal Pradesh (23%) (Jaryan et al. 2013) are from South America, while Europe contributes the highest percentage (38%) of alien species in Kashmir (Khuroo et al. 2007).The prevalence of genera such as Eucalyptus, Ipomoea, Euphorbia, Pinus, Acacia, Juniperus, Amaranthus, Hibiscus, and Solanum is observed in Uttarakhand, which is in accordance with the studies carried out in India (Khuroo et al. 2012), Himachal Pradesh (Jaryan et al. 2013).A report of comparatively higher number of alien plant species (728) in Uttarakhand could be attributed due to higher species richness (ca.5,000) and lack of persuaded literature exclusively on alien plant species in other Himalayan states.

CONCLUSION
Biological invasions have been considered as the second largest threat to global biodiversity after habitat loss, and undoubtedly a huge number of species extinctions are associated with such invasions.Recognising the array of impacts that invasive alien species can have, one needs to reconsider the strategies that have been developed to deal with invasions.
Although, several international and regional programmes such as Global Invasive Species Programme, European Network of Invasive Species, Invasive Species Information Network and regional Eurasian networks have been initiated, little has been achieved in understanding and controlling plant invasions.Regional inventorization of alien flora is now considered a pre-requisite for gaining a better understanding and undertaking appropriate management practices.Also, modelling studies can 21550 J TT There is an urgent need to rectify such information gaps to pave the way forward for the correct compilation of regional databases that will in turn strengthen the scientific pool of knowledge and management practices.Uttarakhand is vulnerable to alien plants, and unfortunately the intensity of introductions is expected to escalate rapidly due to climate change and economic developments.

Figure 1 .
Figure 1.Life form categorization of alien plant species.

21529-21552 Alien flora of Uttarakhand Arora et al. 21542 J TT Name of the species Family Nativity Life form Reference Leonotis
nepetifolia (L.) R.Br.

Table 3 . Life form categorization of alien plant species in different continents or geographical regions.
Abbreviations used: Trop.A-Tropical America | NAM-North America | SAM-South America | AS-Asia | EU-Europe | AF-Africa | AU-Australia.

Table 4 . Details of the alien plant species reported in the India, Uttarakhand and its adjoining states/regions.
Despite a large number of studies undertaken to assess the alien flora of the country, it is submitted that correct identification and authentication of names of several unresolved or illegitimate species, for instance, names of alien plant species such as Adenostemma houstonianum, Anethum scandicina, Bignonia anguis-cati, Caesulia officinalis, Dombeya cayuseii, Hibiscus hawaii, Lagerstroemia floribunda, Luchea endopogon, Manihot tweediana, Oxalis dehradunensis, Oxalis richardiana, Peltophorum vogetianu, Persia owdenii, Phoenix senegalensis, Pterospermum semisagittatum, Roylea coccinea, Siegesbeckia marianum, Terminalia calamansanai, Terminalia oliveri, and Vigna faba reported by various workers need to be carried out.