Saussurea species in Indian Himalayan Region : diversity , distribution and indigenous uses

In spite of the high economic value of the Saussurea species in the Indian Himalayan Region (IHR), the potential of most of the species is yet to be investigated. Therefore, an attempt has been made to study the diversity, distribution, habitat preference, nativity, endemism, status and indigenous uses of Saussurea species in the IHR. A total of 62 species were recorded from the IHR; of these, 37 species were native to the Himalayan region, 8 were endemic and 21 were near endemic to the IHR. Twenty-seven of the 28 species that were known to have indigenous uses also had medicinal value and are used for the treatment of various diseases/ailments. Many species, e.g., S. affinis (Ganga Mula*), S. auriculata (Pachak Kut), S. bracteata (Prerak Mul), S. costus (Kuth), S. gossypiphora (Kasturi Kamal) and S. obvallata (Brahm Kamal), have multiple uses. The genus showed high habitat specificity in that 16 species were recorded to be restricted to one or two habitats only. As many as 44 species were identified as rare in the study region. Considering the high industrial demand for raw materials and the endangered status of S. costus, S. gossypiphora, S. obvallata and S. simpsoniana (Fen Kamal), these species should be prioritized for conservation (in situ and ex situ) throughout the IHR. Population assessment of the rare-endangered, native, endemic and economically important species using standard ecological methods has been suggested for the quantification of the existing stock of these species in their natural habitats. Further, phytochemical investigations for the identification of active ingredients are suggested. Propagation and cultivation techniques are lacking for most of the species of Saussurea except for S. costus, S. obvallata and S. medusa (Snow Lotus). Furthermore, the native communities need to be sensitized to the sustainable use and conservation value of the species in this genus. *Local names given in parentheses throughout are in the Pahari language, spoken by native communities in the Himalayan region. Introduction It is well known that the Indian Himalayan Region (IHR) has a great range of plant diversity. The region alone supports about 18,440 species of plants (Angiosperms: 8,000 spp., Gymnosperm: 44 spp., Pteridophytes: 600 spp., Bryophytes: 1,736 spp., Lichens: 1,159 spp. and Fungi: 6,900 spp.). According to Samant et al., out of the total species of vascular plants, 1,748 species are medicinal. Asteraceae is the fourth largest family of vascular plants, comprising over 30,000 species (1,100 genera), and is distributed almost worldwide. In India, the family is estimated to have about 900 species under 167 genera. Plants of the family are perennial and most species are herbaceous in nature, with trees and shrubs representing only about 2% of the total. Saussurea is named after Horace Benedict de Saussure (1740-1799), a Swiss philosopher. It is an important genus of the family comprising an estimated 410 species, native to cool temperate and arctic regions of Asia, Europe, and North America, with the highest diversity in alpine habitats in the Himalayas and Central Asia. Of the estimated species, 61 are found in India. The genus is quite varied and is well known to have medicinal, religious and other economic values, i.e. food, flavoring material, rubber, oil, insecticides, dye, ornamental value, etc. Plants of the Saussurea genus range in height from the 5-10 cm tall dwarf alpine species to tall, thistle-like plants up to 3 m tall. The leaves are produced in a dense basal rosette, and spiral up the flowering stem. The flowers form in a dense head of small capitula, often completely surrounded in dense white to purple woolly hairs; the individual florets are also white to purple. The woolly hairs in high altitude species of the family are the densest, and aid in thermoregulation of the flowers, minimizing frost damage at night, and also preventing ultraviolet light damage from the intense high altitude sunlight. S. costus (Kuth, Figure 1A), native to the Himalayan Region, is one of the most commercially viable species of this genus and is in high demand for treating many diseases like bronchial asthma, rheumatism, cholera, jaundice, leprosy, etc. Besides this species, S. gossypiphora (Kasturi Kamal, Figure 1B) and S. obvallata (Brahm Kamal, Figure 1C) are very popular for medicinal and religious purposes in the IHR. A review of literature reveals that the information available for a few species of Saussurea in the region is fragmentary. To our knowledge, there is hardly any documentation available which contains comprehensive information on the diversity, distribution, habitat preference, nativity, endemism, status and indigenous uses of the species of Saussurea in the IHR. In view of the economic importance of the genus for the inhabitants of the region, this study was undertaken to: i) examine the diversity, distribution pattern and indigenous uses of the species of Saussurea in the IHR; ii) assess and analyze species for their habitat preference, nativity, endemism and status; and iii) suggest appropriate strategies for the conservation management of the


Introduction
It is well known that the Indian Himalayan Region (IHR) has a great range of plant diversity.The region alone supports about 18,440 species of plants (Angiosperms: 8,000 spp., Gymnosperm: 44 spp., Pteridophytes: 600 spp., Bryophytes: 1,736 spp., Lichens: 1,159 spp.and Fungi: 6,900 spp.). 1 According to Samant et al., 2 out of the total species of vascular plants, 1,748 species are medicinal.Asteraceae is the fourth largest family of vascular plants, comprising over 30,000 species (1,100 genera), and is distributed almost worldwide.In India, the family is estimated to have about 900 species under 167 genera. 3,4Plants of the family are perennial and most species are herbaceous in nature, with trees and shrubs representing only about 2% of the total.
Saussurea is named after Horace Benedict de Saussure (1740-1799), a Swiss philosopher.It is an important genus of the family comprising an estimated 410 species, native to cool temperate and arctic regions of Asia, Europe, and North America, with the highest diversity in alpine habitats in the Himalayas and Central Asia.Of the estimated species, 61 are found in India. 3,5,6The genus is quite varied and is well known to have medicinal, religious and other economic values, i.e. food, flavoring material, rubber, oil, insecticides, dye, ornamental value, etc.
Plants of the Saussurea genus range in height from the 5-10 cm tall dwarf alpine species to tall, thistle-like plants up to 3 m tall.The leaves are produced in a dense basal rosette, and spiral up the flowering stem.The flowers form in a dense head of small capitula, often completely surrounded in dense white to purple woolly hairs; the individual florets are also white to purple.The woolly hairs in high altitude species of the family are the densest, and aid in thermoregulation of the flowers, minimizing frost damage at night, and also preventing ultraviolet light damage from the intense high altitude sunlight. 7. costus (Kuth, Figure 1A), native to the Himalayan Region, 2 is one of the most commercially viable species of this genus and is in high demand for treating many diseases like bronchial asthma, rheumatism, cholera, jaundice, leprosy, etc. 8 Besides this species, S. gossypiphora (Kasturi Kamal, Figure 1B) and S. obvallata (Brahm Kamal, Figure 1C) are very popular for medicinal and religious purposes in the IHR.A review of literature reveals that the information available for a few species of Saussurea in the region is fragmentary.
To our knowledge, there is hardly any documentation available which contains comprehensive information on the diversity, distribution, habitat preference, nativity, endemism, status and indigenous uses of the species of Saussurea in the IHR.In view of the economic importance of the genus for the inhabitants of the region, this study was undertaken to: i) examine the diversity, distribution pattern and indigenous uses of the species of Saussurea in the IHR; ii) assess and analyze species for their habitat preference, nativity, endemism and status; and iii) suggest appropriate strategies for the conservation management of the species.the distribution range of the species. 2,27The species restricted to the IHR have been considered as endemic whereas those with extended distribution to neighboring countries/states have been considered as near endemic.IUCN status of the species was determined based on occurrence of the species in natural habitats.

Diversity, distribution and habitat preference
In the present study, 62 species of Saussurea were recorded from the IHR.All the species were herbaceous in nature and distributed between 550 m and 5,700 m.The greatest species diversity (33 spp.) was recorded in the zone between 3,500 m and 5,000 m (Figure 2).This high species diversity may be due to varied soil, climate and geography of the zone, which gives rise to many micro and macro habitats. 22he Northeast region of the Himalayas, particularly Sikkim, contains the greatest number of species of Saussurea (32 spp.), which is among the dominant plant genera in the state. 43n the present study, Saussurea was found within 15 habitats: shady/moist, alpine meadows/slopes, shrubberies, open grassy slope, shady rock/boulders, roadside/waste places, cultivated area/agricultural lands, dry places, rocky slopes, snowline/glacier slopes, forest, riverine, alpine screes, flooded areas and saline alkali lands (Table 1).Maximum species diversity was in alpine meadows/slopes (55 spp.), followed by shady/moist places (32 spp.), alpine screes (24 spp.) and forest (23 spp.) habitats.Sixteen species were restricted to one or two habitats only.

Native and endemic species
Of the total Saussurea species identified, 37 species were determined to be native to the Himalayan region and the remaining 25 species were non-native (Table 1).Among the native species, 8 species (S. atkinsoni, S. ceratocarpa, S. clarkei, S. costus, S. laneana, S. obscura, S. pantlingiana and S. sudhanshui) were endemic to the IHR, while 21 other species (S. abnormis, S. albescens, S. andersonii, S. andryaloides, S. auriculata, S. candol-leana, S. conica, S. gilesii, S. graminifolia, S. heteromalla (Kaliziri, Figure 1D), S. jacea, S. nimborum, S. nishiokae, S. piptathera, S. polystichoides, S. roylei, S. sughoo, S. taraxacifolia, S. thomsonii, S. tridactyla and S. yakla) had extended distribution to neighboring countries like Pakistan, Afghanistan, Bhutan, Tibet and Nepal, and were thus identified as near endemic.Endemic and habitat-specific species are generally considered more prone to extinction than widespread habitat generalists.Among the dominant high altitude genera in the Himalaya, Saussurea is the second largest genus with a preponderance of endemic species (35 spp.), 44 suggesting that there is great value in conservation management of the species in this genus.

Indigenous uses
Proper documentation and compilation of indigenous knowledge of a species helps to identify the potential and conservation value of the species and the document can be used as a tool to transfer this knowledge from genera-    In the present study, of the total species examined, indigenous uses of 28 species were known, and of these, 27 species had medicinal value or are used for the treatment of various diseases and ailments (Table 1).Six species (S. affinis, S. auriculata, S. bracteata, S. costus, S. gossypiphora and S. obvallata) are used as medicine, food, fodder, fuel, and for ornamental and religious purposes.Among the various parts, i.e. leaves, stem, flowers, seeds, aerial parts, roots, etc. of the plants used for curing diseases, roots are the most often cited.All parts of the plant of S. ceratocarpa, S. costus, S. graminifolia, S. medusa, S. obvallata and S. roylei are said to be used for medicinal purposes.
Among the species of Saussurea, S. costus is the most commercially viable species.Its medicinal properties are well documented in traditional Chinese medicine, the Tibetan system of medicine, and ayurvedic medicine.Out of the 175 formulations reported in The Handbook of Traditional Tibetan Drugs, this species is one of the main ingredients in 71 formulations. 45The roots of S. costus have a strong and sweet aromatic odor with a bitter taste, and are used as an antiseptic and in controling bronchial asthma, particularly of the vagotonic type. 8reparations made from this species are also reported to cure various diseases and conditions including dysentery, rheumatism, bronchitis, cholera, jaundice, ulcers, skin diseases, stomachache, gas, toothache, cough, cold, fever, edema, bruises and cuts. 8The oil extracted from the roots is known as Costus Oil, which is used in high-grade perfumes and in the preparation of hair oil.Costus Oil is also said to be effective in the treatment of leprosy.In the Himalayan states of India, the roots are used as insecticide to protect shawls and woollen fabrics, and as incense.In the Lahaul and Spiti districts of Himachal Pradesh, dried leaves of Kuth are smoked as tobacco and  upper parts of its plants are used as fuel and fodder. 8,42The roots of S. auriculata can be substituted for the roots of S. costus. 8esides S. costus, S. obvallata and S. gossypiphora are other high value species used not only for medicine, but also highly valued for religious purposes. 8,46These species are offered for worship at hill shrines and used to guard against evil spirits.The former, known as 'Brahma Kamal' has been designated the state flower for Uttarakhand.It is offered to the goddess 'Nanda Devi' and other deities on auspicious days.Some species such as S. bracteata, S. gnaphaloides, S. costus, S. obvallata and S. taraxacifolia are used as the main ingredients in the 'Amchi' Medical System, a traditional system of Tibetan medicine. 47Besides indigenous uses, the roots of S. costus, S. gossypiphora and S. simpsoniana yield an essential oil which has been sold for a premium in making high-grade perfume, various medicines and insecticides.

IUCN status
Habitat specificity, population size, distribution range and anthropogenic pressure play an important role in identifying the status of the species. 48Being habitat specific and distributed in a narrow geographical range, most high altitudinal species of Saussurea in the Himalayas are in need of some sort of protection (conservation). 49f the total species identified in the present study, 44 were identified as rare, 2 species, S. costus and S. gossypiphora, as critically endangered, and 2 species, S. obvallata and S. simpsoniana, as endangered, due to heavy pressure on these species.Other species were identified as occasional, uncommon and common in the study region (Figure 3).Population assessment using standard ecological methods is suggested for actual quantification of existing stock of the rare and threatened species in natural habitats.
S. costus has been in high demand in the pharmaceutical industry, but during the last decade the species has been even more popularized due to its threatened status globally.Due to high market demand and uncontrolled exploitation of the species, it was reported to be extinct in many pockets in the wild. 4To meet the market demand and conserve the species, commercial cultivation of S. costus was taken up in the neighboring villages of the habitats in Kashmir, and subsequently it was initiated in high altitude areas of neighboring states such as Himachal Pradesh and Uttarakhand.Being an endemic species to the Himalayas, the distribution of S. costus is quite restricted to an extremely narrow geographical range. 50ue to great demand for raw material from these plants, most of the natural populations of the species are either under destructive har-vesting or have been extirpated.Consequently, this invaluable species has been declared endangered 51,52 and is listed in Appendix I of CITES (Convention of International Trade in Endangered Species of Wild Fauna and Flora).The species is also included in the negative list of exports of the Ministry of Commerce, Government of India and in the 'Schedule VI' of the Wildlife Protection Act of India.Also, trade of the species is strictly prohibited under the Foreign Trade Development Act-1992.This species is being cultivated commercially in the cold desert of Lahaul Valley, but owing to the fluctuating and low market prices of raw material, the cultivation is restricted to a few villages. 42esides S. costus, many other species of Saussurea are categorized under rare and threatened.Apart from the restricted distribution, the harvesting of whole plants of most of the species of Saussurea is one of the reasons for their threatened status (harvesting of plant parts which permit regeneration or re-growth is a less damaging mode of use).Incidentally, S. ceratocarpa, S. graminifolia, S. medusa, S. obvallata and S. roylei are the prominent species whose whole plant is used for medicine and thus, these species are more prone to extinction and need immediate conservation.Law and Salick 53 revealed that the plants of S. laniceps (found in the Himalayan region), being larger in size, are easier to find and moreover, the whole plant of this species is harvested just before seed set.Therefore, early or untimely collection of the plants may also be one of the threats to the species.

Review of propagation and cultivation
The review of literature indicates that the propagation (conventional and in vitro) and cultivation techniques are lacking for most of the species of Saussurea excluding S. costus, 28,34 S. obvallata 35,36 and S. medusa. 37,38Cultivation of S. costus in the Cold Desert of the Lahaul valley was initiated during the 1920s, and at present the species is being cultivated commercially. 8,42mall scale cultivation of the species by some tribal communities has also been reported from the Nanda Devi Biosphere Reserve (2000-3500 m) of the Uttarakhand. 39In S. laniceps, due to its high medicinal and edible value and rarity, efforts are being made in Tibet towards its conservation and cultivation. 40nformation on the propagation and cultivation of some species of Saussurea is available at the Rock Garden Plant Database website. 41

Conclusions
The present study provides comprehensive information on the diversity, distribution, habitat preference, nativity, endemism and status of 62 species of Saussurea in the IHR.Among these, indigenous uses of 28 species are known in the region.The genus Saussurea shows high habitat specificity as 16 species were recorded to be restricted to one or two habitats only.A few of the species are known for their economic value and, therefore, other species should also be investigated for their economic importance.S. affinis, S. auriculata, S. bracteata, S. costus, S. gossypiphora and S. obvallata were recorded as multipurpose species, used as medicine, food, fodder, fuel, and for ornamental and religious purposes.Considering the high industrial demand for raw material and the endangered status of S. costus, S. gossypiphora, S. obvallata and S. simpsoniana, these 4 species should be priorities for conservation (in situ and ex situ) throughout the IHR.Population assessment of the native, endemic and rare/endangered species using standard ecological methods has been suggested for the quantification of the While exploring the floristic diversity of the West Himalayas between 1993 and 2003 and the North-West Himalayas between 2004 and 2006, we recorded observations on distribution, altitudinal range, habit and habitat of the Saussurea species.Knowledge of indigenous uses was gathered through interviews with local inhabitants.This was augmented by an extensive survey of literature on the species of Saussurea occurring in the IHR. 2,6-25Determination of nativity, endemism and IUCN status of the species N o n -c o m m e r c i a l u s e o n l y

Figure 2
Figure 2. Distribution of Saussurea species at different altitudinal ranges tion to generation.Therefore, the documentation of indigenous uses is essential for defining priorities for conservation of the species.Recorded information on the economic value of the species of Saussurea is very fragmentary.

Table 1 . Continued from previous page. Taxa LN/VN Altitudinal Habitat(s) Nativity Distribution Status Indigenous uses range (m)
Occ Amchi use its leaves and flowers in Mongolia, Russia (Siberia), liver, throat and heart troubles.Tajikistan NE Afghanistan, It is also used in mental disorder.N Pakistan, India (Jammu & Kashmir, Ladakh, Thang Lang La) S. glanduligera Schi.-Bip.irregular menses, semina/vaginal discharge, excessive bleeding from the womb and pain at the waist due to a loss of renal potency.

Table 1 . Continued from previous page. Taxa LN/VN Altitudinal Habitat(s) Nativity Distribution Status Indigenous uses range (m)
China China, India (Kashmir), Rare The whole herb is used in traditional Mongolia Nepal, E Tibet, N Pakistan, Chinese and Tibetan medicine for the treatment of headache, high blood pressure and to regulate menstrual cycles and treat menstrual problems.Also used as tonic for weakness and remedy for arthritis.**S.nimborum W.W. Sm.Reg Himal Indian Himalaya (Sikkim) Rare -S.obvallata (DC.)Edgew.Brahm Kamal, 3000-4800 2,3,5,9,10,13 Reg Himal Myanmar, Bhutan, India EN The flowers, rhizome and leaves are Kanwal, Birm (Uttar Pradesh, Chamoli used for various traditional, Kanwal Garhwal, Hemkund, religious, medicinal and ornamental Kashmir, Sikkim), E Tibet, purposes.The roots are applied to Nepal, Pakistan bruises, boils, wounds and cuts and used as a nerve tonic and powerful antiseptic.It is used in several Tibetan medicines and in the treatment of paralysis of the limbs and cerebral ischemia.medicine.It has a bitter taste and a Himachal Pradesh, Kashmir), cooling potency.Antidote, anti-Nepal inflammatory, emollient, hemostatic and vasoconstrictor, it is used in the treatment of wounds, excessive bleeding and meat poisoning.A paste of the plant is used as poultice to relieve aching joints.Continued next page