Journal of Threatened Taxa | www.threatenedtaxa.org | 26 June 2022 | 14(6): 21239–21245

ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print)

https://doi.org/10.11609/jott.5977.14.6.21239-21245

#5977 | Received 10 April 2020 | Final received 15 May 2022 | Finally accepted 21 May 2022

Taxonomy and threat assessment of Lagotis kunawurensis Rupr. (Plantaginaceae), an endemic medicinal plant species of the Himalaya, India

Aijaz Hassan Ganie ¹, Tariq Ahmad Butt ², Anzar Ahmad Khuroo ³, Nazima Rasool ⁴,

Rameez Ahmad ⁵, Syed Basharat ⁶ & Zafar A. Reshi ⁷

^1,4 Department of Botany, Kargil Campus, University of Kashmir, Ladakh 194105, India.

^2,6 Regional Research Institute of Unani Medicine, Srinagar, Jammu & Kashmir 190006, India.

^3,5 Centre for Biodiversity & Taxonomy, Department of Botany, University of Kashmir, Srinagar, Jammu & Kashmir 190006, India.

⁷ Department of Botany, University of Kashmir, Srinagar, Jammu & Kashmir 190006, India.

¹ aijazku@gmail.com (corresponding author), ² smpusrinagar@gmail.com, ³ anzarak@gmail.com, ⁴ rasoolnazima@gmail.com, ⁵ rameezkhuroo929@gmail.com, ⁶ basharat=basharat@gmail.com, ⁷ zreshi@gmail.com

Editor: Anonymity requested. Date of publication: 26 June 2022 (online & print)

Citation: Ganie, A.H., T.A. Butt, A.A. Khuroo, N. Rasool, R. Ahmad, S. Basharat & Z.A. Reshi (2022). Taxonomy and threat assessment of Lagotis kunawurensis Rupr. (Plantaginaceae), an endemic medicinal plant species of the Himalaya, India. Journal of Threatened Taxa 14(6): 21239–21245. https://doi.org/10.11609/jott.5977.14.6.21239-21245

Copyright: © Ganie et al. 2022. Creative Commons Attribution 4.0 International License. JoTT allows unrestricted use, reproduction, and distribution of this article in any medium by providing adequate credit to the author(s) and the source of publication.

Funding: The work has not been funded by any agency.

Competing interests: The authors declare no competing interests.

Author details: Aijaz Hassan Ganie is working as Assistant Professor at Department of Botany Kargil Campus. Tariq Ahmad Butt is working as research officer at Regional Research Institute of Unani Medicine. Anzar Ahmad Khuroo is senior Assiatant Professor at Centre for Biodiversity & Taxonomy, Department of Botany, University of Kashmir. Nazima Rasool is working as Assistant Professor at Department of Botany Kargil Campus, Rameez Ahmad is research scholar at Department of Botany, University of Kashmir. Syed Basharat is technical officer at Regional Research Institute of Unani Medicine. Zafar A Reshi is Professor at Department of Botany, University of Kashmir.

Author contributions: AHG, TAB and AAK conceived the project idea; AHG, TAB, NR and SB collected the data. AHG, AAK, RA and ZAR analyzed and compiled the data; AHG and AAK wrote the manuscript, while all other authors provided editorial advices and contributed to finalize the manuscript.

Acknowledgements: The authors are thankful to the director general CCRUM New Delhi, in-charge RRIUM Srinagar and head, Department of Botany, University of Kashmir, Srinagar for providing the necessary facilities. The supporting staff members at RRIUM and CBT, Department of Botany, University of Kashmir are also acknowledged for their kind help during the course of the present study.

Abstract: Lagotis kunawurensis Rupr. (Plantaginaceae), a rare plant species endemic to the Himalaya, is reported here after a gap of 50 years from Ladakh. This species has often been taxonomically misidentified and confused with Picrorhiza kurroa, an important medicinal plant of the Himalaya. The present study clarifies the taxonomy of L. kunawurensis by providing description and photo illustrations of diagnostic characters which will aid its proper field identification. Furthermore, the threat assessment of L. kunawurensis using the IUCN Red List of Threatened Species has been conducted based on the available occurrence records, and the species currently falls under the ‘Near Threatened’ category. This species is used for medicinal purposes by locals in the study area. As the species is simultaneously experiencing various kinds of threats and the known distribution range is relatively smaller, it is right time to develop conservation strategies for the sustainable utilization of this endemic medicinal plant species of the Himalaya.

Keywords: Biogeography, conservation, Ladakh, medicinal plant, Picrorhiza kurroa, status, uses.

INTRODUCTION

Plants are crucial for the existence of life (Isbell et al. 2011). However, in recent times, plants are subjected to various threats such as habitat loss, over-exploitation, pollution, illicit trade (Tali et al. 2014; Ganie et al. 2019), and increasing stresses associated with climate change (Urban 2015; Hamid et al. 2020). These anthropogenic pressures on plant diversity are predicted to push Earth beyond the tipping points (Steffen et al. 2015; Bachman et al. 2017). In response to such grave concerns, the Target 2 of Convention on Biological Diversity (CBD) has called for assessment of threat status at regional, national, and global level to identify plant species which need immediate conservation. Empirical evaluation of threat status of biodiversity has emerged as an area of immediate research focus (Agnihotri et al. 2107; Tali et al. 2018; Ganie et al. 2019). Designation of current threat status of a species is crucial in assessing the risk of extinction, development of conservation policy, and drawing public attention towards these species, as well as their declining habitats (Burton 2003; Tali et al. 2018; Ganie et al. 2019).

The Himalaya, one of the global biodiversity hotspots, harbors about 10,000 plant species of which >3,100 are endemic to the region (Chitale et al. 2014). The Indian Himalayan region is rich in biodiversity, including prized medicinal plants (Tali et al. 2019; Dar & Khuroo 2020; Ganie et al. 2020). The genus Lagotis J. Gaertn. (Family: Plantaginaceae) has several species endemic to the Himalayan region (Stewart 1972; Lu 1992; Li et al. 2014). Four species of Lagotis have been recorded from the Himalaya (Stewart 1972) and two: L. cashmeriana (Royle) Rupr. and L. kunawurensis Rupr. are narrow endemic to the region. Stewart (1972) has recorded L. kunawurensis from Ladakh, Trans-Himalayan region in India; however, since then no other researcher (Kachroo et al. 1977; Polunin & Stainton 1984; Klimeš & Dickoré 2006; Behera et al. 2014) has reported this species from Ladakh. Recently, while carrying out botanical surveys to document the flora of Ladakh, specimens of a typical Lagotis species were collected from Sapi La, Kargil (Ladakh). After critical study of its morphological features, the species was identified as Lagotis kunawurensis Rupr. (Stewart 1972; Polunin & Stainton 1984). The later researchers, most likely, have taxonomically confused L. kunawurensis with Picrorhiza kurroa, another important medicinal plant of the Himalaya (Lagotis kunawurensis- efloraindia https://sites.google.com/site/efloraofindia/species/mz/p/plantaginaceae/lagotis/lagotiskunawurensis).

In an era of biodiversity crisis, the correct taxonomic identification and scientific information on the occurrence and population status of endemic species is urgently needed to undertake threat assessment, and thereafter develop appropriate conservation strategies (Chitale et al. 2104; Tali et al. 2018; Khuroo et al. 2020). In the backdrop of L. kunawurensis being a narrow endemic species, the present study aimed to resolve its taxonomic confusion and also for the first time undertake an empirical assessment of its threat status across the Himalaya based on IUCN Red List criteria (IUCN 2012).

MATERIALS AND METHODS

Study area

The Himalaya, covering an area of about 329,109.22 km², is located between 25.065–35.082 °N & 73.013–97.041 °E, along the northern boundary of India (Chitale et al. 2014). The climate is sub-alpine-temperate in western Himalaya, while it is sub-tropical to temperate in eastern Himalaya; whereas annual temperature and precipitation is on average 5 °C and 1,200 mm in western Himalaya, it is 10 °C and 3,500 mm in eastern Himalaya, respectively. The wide elevation gradient in the Himalaya ranging from 500–8,800 m results in a variety of ecosystems within short distances, from alluvial grasslands and subtropical broadleaf forests along the foothills to temperate broadleaf forests in the mid-hills, mixed conifer and conifer forests in the higher hills, and alpine meadows above the treeline (Chitale et al. 2014).

The Trans-Himalayan region of Ladakh, the collection site of the present study, is located at the northwestern boundary of India between 21.095–37.083 °N & 72.066–78.041 °E. This region possesses a wide altitudinal gradient, land with diverse geological formations, resulting in the rich diversity of alpine and cold-desert flora (Nüsser & Dickorè 2002). The collection site namely, Sapi La is located in district Kargil of Ladakh at an altitude of 4,375 m, at 34.036 °N & 76.019 °E, and situated about 70 km towards the southwestern side of Kargil township.

Taxonomy

Standard herbarium methods (Bridson & Forman 1992) were used during collection, processing and preparation of the herbarium specimens. Voucher specimens have been deposited at the University of Kashmir Herbarium (KASH). Besides, an ethno-botanical survey was conducted in the study area to document the traditional use of this plant species. The survey usually started with the interview of elderly and experienced members, locally known as ‘Amchi’ to collect information regarding medicinal uses of this plant species.

Record of operative threats

The operative threats (both direct and indirect) to plant species and their habitats were assessed during different seasons of the year at regular intervals of time following Ganie et al. (2019).

Threat assessment

Occurrence records for Lagotis kunawurensis were obtained from the Global Biodiversity Information Facility database (GBIF 2018) using the ‘gbif’ function from the ‘dismo’ package (https://CRAN.R-project.org/package=dismo) (Hijmans et al. 2017) and supplemented with the occurrence records from India Biodiversity Portal (IBP 2018), herbarium records (BSD, KASH) and field surveys.

Adopting the IUCN Red List Categories and Criteria, version 3.1 (IUCN 2012), we assessed the current threat status of the species based on the Criterion B; it takes into account the geographic range size as well as evidence of diminishing or fragmenting populations (Gaston & Fuller 2009; Cosiaux et al. 2018). The Criterion B is appropriate for assigning conservation status even when data is scarce and the geographic distribution of a species is known from only a few georeferenced herbarium records (Cosiaux et al. 2018). We used the ConR package (https://CRAN.R-project.org/package=ConR) (Dauby et al. 2017) implemented in R software (https://www.R-project.org/; R Core Team 2018) to calculate extent of occurrence (EOO) and area of occupancy (AOO) based on the occurrence records of the species. EOO was calculated by constructing a minimum convex polygon around all the known occurrences while AOO was estimated as the sum of occupied cells after superimposing the grid with cells of desired size (Dauby et al. 2017; Cosiaux et al. 2018; Lughadha et al. 2018). During the present study, the minimum AOO was estimated based on a standard grid cell of size 2 x 2 km (IUCN 2017). In addition, we also calculated the number of ‘locations’, as defined by IUCN (2017), with respect to the various types of threats, so that a single ‘location’ may involve more than one adjacent sub-populations.

RESULTS

Taxonomic description

Lagotis kunawurensis Rupr., Sert. Tianschan. 64 1869.

Synonyms: Gymnandra kunawurensis Royle ex Benth., Scroph. ind. 47, 1835.

Lagotis glauca var. kunawurensis (Royle) Hook. f., Fl. Brit. Ind. 5, 569, 1885

Plant herbaceous up to 23 cm tall; roots many, fibrous; basal leaves obovate-oblanceolate, with cuneate leaf base, dentate-denticulate margin and acute-rounded leaf apex, 6-8 cm long and 1.5–2.2 cm broad, petiolate, petiole creamy with reddish tinge, 6–8 cm in length; stem leaves ovate, sessile, 2–3 cm long and 1–1.5 cm broad; inflorescence spike, flowers pale mauve or blue, numerous; calyx spathe-like; corolla tube slender, zygomorphic, bracts numerous, overlapping; stamens 2, filament as long as corolla or shorter; anthers reniform, black in colour; ovary 2 locular, superior; stigma capitate, bilobed (Image 1).

Specimens examined: India, Ladakh, Kargil: Sapi La, 03 August 2017, Tariq, Aijaz, & Khuroo 1000129; 23 July 2019, Aijaz & Nazima 110991 (KASH); Himachal Pradesh, Lahaul: Rohtang pass, 04 August 1994, Murti & Singh 102923 (BSD).

Identification aid: In western Himalaya, there is a confusion regarding the identification between Lagotis kunawurensis and Picrorhiza kurroa (https://sites.google.com/site/efloraofindia/species/mz/p/plantaginaceae/lagotis/lagotiskunawurensis), therefore the comparison of the diagnostic characters between these two species is provided to facilitate their correct taxonomic identification (Table 1).

Flowering period: July–August.

Ecological note: The species grows in the cold desert alpine areas which experience high speed winds and also prone to landslides. Also, the species is over-exploited for local use by herbal healers and whole plant along with roots is extracted. During the present study, the species was recorded only at one site (i.e., Sapi La) in the entire Ladakh region. The number of mature individuals at the collection site was about 250 individuals, thus represented by a small population size.

Distribution

Global: Pakistan (Deosai, Baltistan); India (Drass, Rusi La, Sapi La and Zanskar in Ladakh, Jhow, Kunawur, Phalloot in Himachal Pradesh, Uttarakhand, and Sikkim); Nepal (Mechi, Gandaki Zone, Sagarmatha Zone, Koshi Zone, Thorung La, Manang, Karnali. Suli Gad); Bhutan (Catalogue of life-https://www.catalogueoflife.org)

During the present study, the plant species was collected from Sapi La (4370 m.; 34.036 °N and 76.019 °E), in Kargil district of Ladakh, India (Figure 1).

Ethno-medicinal uses

The plant species, in particular roots, are used against abdomen cramps, inflammation, and brown phlegm. The plant is also used as liver tonic and to treat different types of fevers in the collection site of the present study.

Threat status

Empirical evaluation of the threat status revealed that the extent of occurrence (EOO) and area of occupancy (AOO) for L. kunawurensis is 2,78,896 km² and 88 km² respectively (Figure 1). Furthermore, the species is recorded from 24 unique localities, representing a total of 19 sub-populations from 20 different locations (sensu IUCN 2012) which are more than 10 locations that represent the upper most limits for the ‘Vulnerable’ (VU) category under sub-criterion ‘a’. Therefore, L. kunawurensis is assigned under IUCN category of Near Threatened (NT) according to criterion B.

DISCUSSION

After Stewart (1972), Lagotis kunawurensis has not been reported from the Ladakh region (Kachroo et al. 1977; Polunin & Stainton, 1984; Klimeš & Dickoré, 2006; Behera et al. 2014), therefore the authenticity of its presence in this region was doubtful. However, the present study clearly demonstrates distribution of L. kunawurensis in the region. The species has been confused with similar-looking Picrorhiza kurroa, another important medicinal plant that grows in Ladakh. A detailed taxonomic description and photo illustrations of diagnostic characters, as worked out in the present study, will facilitate its easier field identification, which is crucial for its conservation and sustainable use.

The present study has revealed that L. kunawurensis is currently Near Threatened (NT). Being narrow endemic to the Himalaya, rare distribution at high altitudes and smaller population size in the region makes the species highly vulnerable to contemporary land-use and climate changes (Rana et al. 2017). Ladakh region is recently experiencing climate change, which can impact both floral and faunal diversity of the region (Barrett & Bosek 2018). As L. kunawurensis is a narrow endemic species, thus considered more prone to extinction due to changing climate (Muthumperumal et al. 2020). In Ladakh, the species is mostly extracted by ‘Amchis’ (local herbal healers) for preparation of traditional medicine. Overexploitation for local use poses a serious threat to valuable wild medicinal plant species, and in turn endangers their habitats as well (Ganie et al. 2019). The medicinally important plant species is overharvested, in most cases illegally, from their wild habitats for trade in the national and international markets. This poses one of the biggest threats to the plant species (Ganie & Tali 2013). Worryingly, the species is extracted as a whole along with roots, that hinders its sexual (seeds) and/or asexual (rootstock) reproduction and which in turn results in reduction of population size and distribution (Tali et al. 2014). The species grows in landslide prone areas in the study area. Landslides are one of the major factors of habitat fragmentation (Dar & Naqshi 2002) and also play a major role in making the plant species vulnerable to local extirpation (Ganie et al. 2019). The landslides can lead to the competitive advantage for growth of other ruderal species due to changes brought in physico-chemical properties of the soil, which in turn can render the natural habitat of endemic species unfavorable, and lead to their population decline (Tali et al. 2014; Ganie et al. 2019). If these threats continue to operate unchecked, the species is highly susceptible to become threatened in near future. To focus conservation action at a regional scale, it becomes necessary to prioritize these species in their natural distributional range (Nori et al. 2016).

Therefore, in an era of rapid land-use change and climate crisis, the results from present study have wide relevance in devising successful conservation strategies for this endemic species in high-altitude habitats of the Himalaya. Looking ahead, the present study can serve as an early warning for undertaking urgent efforts to conserve this important endemic medicinal plant species.

Table 1. Comparison of diagnostic characters between Lagotis kunawurensis and Picrorhiza kurroa.

Diagnostic characters	Species
	Lagotis kunawurensis	Picrorhiza kurroa
Leaf a. Type b. Shape	Both basal and stem leaves present Basal leaves obovate-oblanceolate Stem leaves ovate, sessile	Only stem leaves present Absent Stem leaves spathulate to narrow elliptical with winged leaf stalk
Inflorescence a. Type b. Size	Spike Up to 15–20 cm long	Cylindrical head Up to 10 cm long
Flower a. Colour b. Stamens	Pale mauve or blue Short, not exerted	Purplish-blue Long, exerted

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REFRENCES

Agnihotri, P., T. Husain, P.A. Shirke, O.P. Sidhu, H. Singh, V. Dixit, A.A. Khuroo, D.V Amla & C.S. Nautiyal (2017). Climate Change-driven Shifts in Elevation and Ecophysiological Traits of Himalayan Plants during the Past Century. Current Science 112(3): 595–601.

Bachman, S.P., E.M.N. Lughadha & M.C. Rivers (2017). Quantifying progress toward a conservation assessment for all plants. Conservation Biology 32(3): 516–524

Barrett, K & K. Bosak (2018). The Role of Place in Adapting to Climate Change: A Case Study from Ladakh, Western Himalayas. Sustainability 10(4): 898. https://doi.org/10.3390/su10040898

Behera, M.D., S. Martin & P.S. Roy (2014). Biodiversity of Kargil Cold Desert in Ladakh Himalaya, pp. 253–274. In: Nakano S., T. Yahara, T. Nakashizuka (eds.). Integrative Observation and Assessment, Ecological Research Monograph. Springer, Japan, xv+431 pp. https://doi.org/10.1007/978-4-431-54783-9

Bridson, D. & L. Forman (1998). The herbarium handbook, 3^rd ed. Kew, Royal Botanic Gardens, London, 320 pp.

Burton, J.A. (2003). The context of red data books, with a complete bibliography of the IUCN publications 291–300. In: De Iongh, H., O.S. B´anki, W. Bergmans, M.J. Van derWerff ten Bosch (eds). The Harmonization of Red Lists for Threatened Species in Europe. The Netherlands Commission for International Nature Protection, Leiden, 332 pp.

Catalogue of life. https://www.catalogueoflife.org. Accessed on 10 April 2020.

Chitale, V.S., M.D. Behera & P.S. Roy (2014). Future of Endemic Flora of Biodiversity Hotspots in India. PloS ONE 9(12): e115264. https://doi.org/10.1371/journal.pone.0115264

Cosiaux, A., L.M. Gardiner, F.W. Stauffer, S.P. Bachman, B. Sonké, W.J Baker & T.L.P. Couvreur (2018). Low extinction risk for an important plant resource: conservation assessments of continental African palms (Arecaceae/Palmae). Biological Conservation 221: 323–33.

Dar, G.H. & A.A. Khuroo (2020). Biodiversity of the Himalaya: Jammu and Kashmir State. Springer Nature, Singapore, 1,100 pp.

Dar, G.H. & A.R. Naqshi (2002). Plant resources of Kashmir: Diversity, utilizationand conservation, pp. 109–122. In: Pandit, A.K. (Ed.). Natural resources of Western Himalaya, Valley Book House, Srinagar, Kashmir.

Dauby, G., T. Stévart, V. Droissart, A. Cosiaux, V. Deblauwe, M. Simo-Droissart, M.S.M. Sosef, P.P.I.I. Lowry, G.E. Schatz, R.E. Gereau & T.L.P. Couvreur (2017). ConR: An R package to assist large-scale multispecies preliminary conservation assessments using distribution data. Ecology and Evolution 7: 11292–11303. https://CRAN.R-project.org/package=ConR

Efloraindia https://sites.google.com/site/efloraofindia/species/mz/p/plantaginaceae/lagotis/lagotiskunawurensis. Accessed on 10 April 2020.

Ganie, A.H & B.A. Tali (2013). Vanishing medicinal plants of Kashmir Himalaya. India’s endangered. (Available online). http://indiasendangered.com/vanishing-medicinal-plants-of-kashmir-himalaya/.

Ganie, A.H., B.A. Tali, A.A. Khuroo, Z.A. Reshi & I.A. Nawchoo (2019). Impact assessment of anthropogenic threats to high-valued medicinal plants of Kashmir Himalaya, India. Journal of Nature Conservation 50: 125715. https://doi.org/10.1016/j.jnc.2019.125715

Ganie, A.H., B.A. Tali, A.A. Khuroo, I.A. Nawchoo, Z.A. Reshi & G.H. Dar (2020). Diversity in medicinal and aromatic flora of the Kashmir Himalaya, pp. 545–564. In: Dar G. & Khuroo A. (eds). Biodiversity of the Himalaya: Jammu and Kashmir State. Springer, Singapore, xxiii+1,100 pp.

Gaston, K.J. & R.A. Fuller. (2009). The sizes of species’ geographic ranges. Journal of Applied Ecology 46: 1–9.

GBIF (2018). Global Biodiversity Information Facility database. https://www.gbif.org/ Accessed 21 March 2020.

Hamid, M., A.A Khuroo, A.H. Malik, R. Ahmad, C.P. Singh, J. Dolezal & S.M. Haq (2020). Early evidence of shifts in alpine summit vegetation: A case study from Kashmir Himalaya. Frontiers in Plant Science 11: 421.

Hijmans, R.J., S. Phillips, J. Leathwick & J. Elith (2017). dismo: Species Distribution Modeling. R package version 1.1-4. https://CRAN.R-project.org/package=dismo

IBP (2018). India Biodiversity Portal. https://indiabiodiversity.org/. Accessed 21 March 2020.

Isbell, F., V. Calcagno, A. Hector, J. Connolly, W.S. Harpole, P.B. Reich, M. Scherer-Lorenzen, B. Schmid, D. Tilman, J. van Ruijven, A. Weigelt, B.J. Wilsey, E.S. Zavaleta & M. Loreau (2011). High plant diversity is needed to maintain ecosystem services. Nature 477: 199–202. https://doi.org/10.1038/nature10282

IUCN (2012). IUCN Red List Categories and Criteria: Version 3.1. 2^nd edition. IUCN Species Survival Commission, Gland, Switzerland and Cambridge, UK, 32 pp. 

IUCN (2017). Guidelines for Using the IUCN Red List Categories and Criteria. Version 13.http://www.iucnredlist.org/documents/RedListGuidelines.pdf

Kachroo, P., B.L. Sapru & U. Dhar (1977). Flora of Ladakh. An Ecological and Taxonomical Appraisal. Bishen Singh Mahender Pal Singh, Dehra Dun, 172 pp.

Khuroo, A.A., G. Mehraj, I. Muzafar, I. Rashid & G.H. Dar (2020). Biodiversity conservation in Jammu and Kashmir state: current status and future challenges, pp. 1049–1076. In: Dar H.S. & A.A Khuroo (eds). Biodiversity of the Himalaya: Jammu and Kashmir State. Springer, Singapore, xxiii+1,100 pp.

Klimeš, L. & W.B. Dickoré (2006). Flora of Ladakh (Jammu and Kashmir, India)-a preliminary checklist. http://www.butbn.cas.cz/klimes. Accessed 3 February 2020.

Li, G.D., C. Kim, H.G. Zha & Z. Zhou (2014). Molecular phylogeny and biogeography of the arctic-alpine genus Lagotis (Plantaginaceae). Taxon 63(1): 103–115.

Lu, X.F. (1992). A study of Lagotis Gaertn. (Scrophulariaceae) in the Qinghai-Tibet Plateau. Acta Biologica Plateau Sin 11: 187–198.

Lughadha, N.E., B.E. Walker, C. Canteiro, H. Chadburn, A.P. Davis, S. Hargreaves, E.J. Lucas, A. Schuiteman, E. Williams, S.P. Bachman, D. Baines, A. Barker, A.P. Budden, J. Carretero, J.J. Clarkson, A. Roberts & M.C. Rivers (2018). The use and misuse of herbarium specimens in evaluating plant extinction risks. Philosophical Transactions of the Royal Society B 374(1763): 20170402. https://doi.org/10.1098/rstb.2017.0402

Muthumperumal, C., P. Balasubramanian & L. Rasingam (2020). An assessment of the conservation status of a presumed extinct tree species Wendlandia angustifolia Wight ex. Hook.f. in southern Western Ghats, India. Journal of Threatened Taxa 12(4): 15468–15474. https://doi.org/10.11609/jott.5148.12.4.15468-15474

Nori, J., R. Torres, J.N. Lescano, J.M. Cordier, E. Maria, M.E. Periago & D. Baldo (2016). Protected areas and spatial conservation priorities for endemic vertebrates of the Gran Chaco, one of the most threatened ecoregions of the world. Diversity and Distributions 22(12): 1212–1219.

Nüsser, M. & W.B. Dickorè (2002). A tangle in the triangle: Vegetation map of the Eastern Hindukush (Chitral, northern Pakistan). Erdkundle 56(1): 37–59

Polunin, O & A. Stainton (1984). Flowers of the Himalaya. Oxford University Press, Delhi, 295 pp.

R Core Team (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

Rana, S.K., H.K. Rana & S.K. Ghimire, K.K. Srestha & S. Ranjitkar (2017). Predicting the impact of climate change on the distribution of two threatened Himalayan medicinal plants of Liliaceae in Nepal. Journal of Mountain Science 14(3): 558–570.

Steffen, W., W. Broadgate, L. Deutsch, O. Gaffney & C. Ludwig (2015). The trajectory of the Anthropocene: the great acceleration. The Anthropocene Review 2: 81–98.

Stewart, R.R. (1972). Flora of West Pakistan: An annonated catalogue of the vascular plants of West Pakistan and Kashmir. Fakhri Press, Karachi, Pakistan, 450 pp.

Tali, B.A., A.A. Khuroo, I.A. Nawchoo & A.H. Ganie (2018). Prioritizing conservation of medicinal flora in the Himalayan biodiversity hotspot: An integrated ecological and socio-economic approach. Environmental Conservation 46(2): 147–154. https://doi.org/10.1017/S0376892918000425

Tali, B.A., A.H. Ganie, I.A. Nawchoo, A.A. Wani & Z.A. Reshi (2014). Assessment of threat status of selected endemic medicinal plants using IUCN regional guidelines: A case study from Kashmir Himalaya. Journal for Nature Conservation 23: 80–89.

Tali, B.A., A.A. Khuroo, A.H. Ganie & A.A. Nawchoo (2019). Diversity, distribution and traditional uses of medicinal plants in Jammu and Kashmir (J&K) state of Indian Himalayas. Journal of Herbal Medicine 17: 100280. https://doi.org/10.1016/j.hermed.2019.100280

Urban, M.C. (2015). Accelerating extinction risk from climate change. Science 348: 571–573.