Erratum to: Traditional use and management of NTFPs in Kangchenjunga Landscape: implications for conservation and livelihoods

Erratum In the original publication [1] the species name Kutki (Neopicrorhiza scrophulariiflora) is wrongly mentioned as CITES listed species. The correct version of the sentence in the second paragraph of “Threats and conservation challenges” can be found here: Illegal trade of NTFPs from the landscape often includes some of the CITES Appendix listed species such as Sunakhari (Orchids) and Lauth salla (Taxus wallichiana).


Background
Non-timber forest products (NTFPs) are the most important provisioning services people obtain from forest ecosystems [1]. The importance of NTFPs in rural livelihoods and forest conservation has been well recognized as they provide income generation opportunities to millions of people around the world [2][3][4][5], and they are also a major source of supplementary food, medicines, fibre, and construction materials [6,7]. In developing countries, biological resources obtained from forests, mostly NTFPs, may contribute as much as 20-25 % of income to rural people [7]. However, the economic potential of NTFPs is highly contextual and depends on a combined set of socio-cultural, ecological, geo-political, and economic conditions. Nevertheless, access to market/ commercialization of NTFPs and sustainable harvesting are two important aspects that need attention for sustainable development of the NTFP sector (also see [8]).
The ecological diversity of the Himalaya makes the area a habitat of a vast range of NTFPs. In the Himalayan region, harvesting NTFPs is a tradition that also contributes significantly to the local economy. Some NTFPs play an important role in traditional health care systems, while others have important cultural values and are sources of food and housing material [9][10][11]. Among all categories of NTFPs, medicinal plants have received much focus while the contribution of other categories of NTFPs has been overlooked. For example, the contribution of wild edible plants towards food security and income generation has been undervalued in Nepal [12].
Common threats to NTFPs in the Himalayan region include unsustainable harvesting and habitat loss due to land use change, deforestation and over-grazing [13,14]. Several other challenges have also been identified for sustainable management of NTFPs, such as policies that are ambiguous or poorly implemented due to the lack of resources, lack of comprehensive information on the ecology of the species and its socio-ecological impacts, and poor infrastructure for bioprospecting [15][16][17]. However, unsustainable harvesting is one of the major issues that affects ecological processes at many levels, from individual and population to community and ecosystem [2,18]. Commercialization of NTFPs is another important aspect involving different processes such as production, collection, processing, storage, transport, marketing, and sale. Marshall et al. [19] found that product marketing and sale were the most important of all factors that constrained overall success of NTFPs commercialization. However, Ghate et al. [20] found a clear relationship between the degree of proximity to the market and NTFP dependence; remote places with low market access had high NTFPs dependency.
The demand for NTFPs is increasing not only in local markets, but also in international markets. Therefore, some important steps to facilitate integration of NTFPs into the development agenda that benefits local communities include identifying potential species having trade value and conducting research on their ecology and sustainable harvest levels; conducting analyses on value chain and use patterns; and analyzing trends and challenges in marketing and management [21]. Here we focus on these aspects of NTFPs in the Kangchenjunga Landscape within the Eastern Himalaya [22] and explore the implications for conservation and livelihoods.

Study area
The Kangchenjunga Landscape is a transboundary landscape shared by Bhutan, India, and Nepal. It is one of the richest landscapes in the Hindu Kush Himalaya (HKH) in terms of cultural and biological diversity and forms part of the Himalaya Biodiversity Hotspot, one of 34 global Biodiversity Hotspots [23]. It extends over 25,000 sq. km within 26 0 21′40.49″ to 28 0 7′ 51.25″ North latitudes and 87 0 30′30.67″ to 90 0 24′31.18″ East longitudes (Fig. 1). The altitude in the landscape ranges from 50 masl in the south to 8,586 masl, the height of Mount Kangchenjunga-the world's third highest peak. Vegetation zones in the landscape is comprised of tropical, subtropical, temperate, subalpine, alpine, and nival.
The Kangchenjunga Landscape provides a range of ecosystem services that supports millions of people [24]. However, like many other landscapes worldwide, biodiversity and ecosystems within the landscape face threats mainly from anthropogenic pressures [25] and global climate change [26]. As a result, the people living in the landscape are economically, physically, and socially vulnerable [25,27].
Recognizing the global and regional significances and challenges that lie within this landscape, the Kangchenjunga Landscape Conservation and Development Initiative (KLCDI) has been initiated by the governments of Bhutan, India and Nepal to achieve biodiversity conservation and sustainable development by applying ecosystem approaches to transboundary landscape management [22]. One of these priority areas is sustainable utilization of NTFPs in the Kangchenjunga Landscape. Several species of high value NTFPs that are also threatened are found in the landscape such as Chiraito (Swertia chirayita), Panch aunle (Dactylorhiza hatagirea), Kutki (Neopicrorhiza scrophulariiflora), Laghupatra (Podophyllum hexandrum) and Lauth salla (Taxus wallichiana).

Data collection and analysis
We reviewed scientific studies published in journals and books on traditional uses of NTFPs in the Kangchenjunga Landscape. Various online databases were used (ISI Web of Science, Scopus, and Google Scholar) using specific search terms such as 'non-timber forest products' , 'medicinal plants' , 'wild edible plants' , and 'Kangchenjunga Landscape' , 'Nepal' , 'India' , 'Sikkim' , 'Darjeeling' , and 'Bhutan'. We also explored hard copies of relevant publications. We reviewed a total of 47 publications and one database to enumerate the NTFPs in the Kangchenjunga Landscape. The precision of species identification in this review was dependent on the original source. However, we verified currently accepted name(s) in online nomenclature sources (http://www. theplantlist.org and http://www.tropicos.org). Vernacular names when available have also been provided. A master list was produced providing Linnaean taxonomy, vernacular name(s), mode(s) of use, and reference(s) for each species (Table 1). We also collected trade data and reviewed policy documents on NTFPs of Bhutan, India and Nepal.

Pattern of publications
Majority of publications on NTFP were from India (60 %), while 34 % were from Nepal and 6 % from Bhutan. This is quite obvious as Darjeeling and the state of Sikkim in India make up a large part of the KL (56.3 %). The presence of two state level universities and research institutes has made significant contribution to the research in KL India [29]. Except for Bhutan, the species reported in this study were mostly documented through ethnobotanical studies conducted in different parts of the landscape. A few studies were focused on particular ethnic communities whereas most of the studies were on general ethnobotany of the region with mixed ethnic composition. Publication on NTFPs date back to 1988 in India while in Nepal and Bhutan it was started after 1996 (Fig. 2). However, majority of the publications (86 %) were published after 2000. All publications are qualitative in nature.

Frequency of NTFPs use
We reported on a total of 739 species of NTFPs used by the local people of Kangchenjunga Landscape. Of these, the highest number of NTFPs was documented from India (377 species), followed by Nepal (363) and Bhutan (245). These numbers, however, overlap in terms of distribution. The NTFPs used only in India were 185 species, while this number was 189 for Nepal and 166 for Bhutan.

Taxonomic diversity and growth habit
Angiosperms were predominant with 705 taxa belonging to 137 families followed by Gymnosperms (10) (14), Ericaceae (13), Rutaceae (13), and Liliaceae (11). NTFPs were distributed into different life forms, with herbs having the most species followed by trees and shrubs (Fig. 3). Pattern of NTFPs used according to different life forms was similar in Bhutan, India and Nepal. Such herbaceous species were mostly medicinal and their extensive use could be because they were frequently found in the forest, and it is believed that the more abundant a plant is the more medicinal virtues it may possess [30].

Major use categories
People from Kangchenjunga Landscape used NTFPs for 24 different purposes ( Table 2). A comparative analysis revealed that the highest number of use categories were reported from the Kangchenjunga Landscape region of India (20 categories) followed by Nepal (18) and Bhutan (14). Despite common occurrence of many species in India and Nepal, use pattern differed greatly in these two countries. Medicinal plants were among the main valuable NTFPs in the landscape. Of the total NTFPs, 334 species were used in traditional medicinal practice in India, whereas 297 species used in Nepal and 176 species used in Bhutan. A considerable number of species were also used as edibles as fruit, vegetables, and pickles in all three countries (Table 1 and Table 2). Fruit and shoots were the most frequently eaten parts.
The relatively higher number of diversity in wild edible NTFPs in Nepal could be because of higher diversity of ethnic groups living in the lowland Tarai to highland regions. There was a significant difference (χ2 = 35.06, df =64, α = 0.05 and 1-α = 83.67) in medicinal plants use pattern in major disease/ailment categories in India and Nepal. These results indicate differences between the traditions of NTFP use in different cultures of India and Nepal. Similar results were also obtained from East Timor [31]. NTFPs use varies from site to site because of the heterogeneity of the community and different traditional practices by ethnic groups [14].
Among 739 species used by the local people, most species were used for a single (550 species) purpose, while fewer were used for two (147) or multiple (42) purposes. Local people were well aware of collecting seasons, mode of collection, and frequency of collection of specific parts of plant species. Medicinal plants such as Heracleum nepalense is plucked on the first Tuesday after the Teej festival. This practice is known as 'Harlo'. The people believe that the medicinal plants plucked on that day are extremely effective and potent [32]. Similar practice of harvesting season can be found among the Amchis of the Himalaya where they believe that for better medicinal efficacy, specific parts of specific medicinal plants should be collected during specific seasons [33].

Ailments treated and preparation methods
The use of medicinal plant in treatment of particular ailment and the preparation method were not specified from Bhutan. In India and Nepal, a total of 27 major ailments were reportedly treated with medicinal plants with most species being used to treat multiple ailments (Table 3). Gastro-intestinal disorders; fever; cold, cough and sore throat; musculoskeletal disorders; injuries; dermatological infections; respiratory system disorders; nutritional disorders; and poisoning effects were treated with the highest diversity of medicinal plant species (Table 1 and Table 3). The high diversity of species use in gastro-intestinal disorders could be because of poor sanitation and drinking water quality in the Kangchenjunga Landscape as in many developing contries [34,35].
Mode of preparation included juice, paste, decoction, powder, infusion, and chewing raw plant parts (Fig. 4, Table 1). The majority of formulations were prepared as juice followed by paste and decoction. Proper selection of species, parts, as well as preparation and administration methods were very important in traditional health care systems.
Almost all plant parts were used to prepare different medicinal formulations: roots, rhizomes, tubers, bark, leaves, flowers, fruit, seeds, young shoots, whole plants, and gum and latex ( Table 1). The most frequently used plant parts were underground parts, followed by leaves, fruit, bark, whole plants, seeds and flowers (Fig. 5). Use of multiple plant parts was often documented ( Table 1). The preference for roots and rhizomes to prepare traditional remedies follows the scientific basis that roots generally contain high concentrations of bioactive compounds [36]. Such a trend is also reported from other studies from the Himalaya [35,37,38].

NTFPs trade and livelihoods potential
The role of NTFPs is particularly important in the Himalayan region where a large proportion of the rural population depends on them as a source of medicine, food, fibre, dye and other useful materials [39][40][41]. In the Kangchenjunga Landscape, many of the NTFPs are used for subsistence, while others are the main or only source of income generation. However, the role of nonmarketed NTFPs that were used for subsistence is largely ignorned when estimates are made of the economic importance of NTFPs to rural populations [42]. Understanding the economic value of non-marketed NTFPs helps to determine the true income of the gatherers and also helps ascertain the true value of the standing forest, leading to more rational decisions about its alternative uses [42].
Domestic as well as cross-border trade of NTFPs, both legally and illegally, is a historical practice in this region [43]. The traded NTFPs mostly include medicinal plants and to a lesser extent some wild edible plants and fibre yielding plants. The handmade paper from Argeli (Edgeworthia gardneri) is the only NTFPs that was sold after value addition in Nepal. Many of the species documented in this study possess high economic potential ( Table 4) and could thus supplement family income [44] while generating incentives for biodiversity conservation [45].
Commonly traded NTFPs from the Nepal part of the Kangchenjunga Landscape include medicinal plants such as Dactylorhiza hatagirea, Fritillaria cirrhosa, Neopicrorhiza scrophulariiflora, lichens, and Taxus wallichiana. Other important species under trade are Aconitum species, Valeriana jatamansi, Viscum album and Zanthoxylum species. Species such as Daphne bholua, Edgerworthia gardnerii, Rhododendron anthopogan, Rubia manjith, Swertia chirayita, Valeriana jatamansi, and Zanthoxylum species are traded in large volume following legal procedures. The collected plant materials are normally sold to middlepersons (local traders), with only a few collectors selling or exporting NTFPs directly in local and cross-border markets. The total amount of NTFPs traded from Nepal in the last five years was 2,029,960 kg and the amout of revenue generated was around US$ 76,066 (Fig. 6, Table 4). The lack of openly accessible information on traded species of NTFPs from Bhutan and India limited our ability to conduct a comparative analysis.
Despite the high potential for trade and livelihoods through NTFPs, local people in the Kangchenjunga Landscape are not able to adequately benefit from engaging in the NTFP sector. In most cases, collectors were not aware of the market price for their products and were compelled to sell based on the offers of the middlepersons [46]. Thus, ensuring that market information is available to local people is one of the challenges in the NTFP sector in the landscape. Moreover, traders reported several other issues including multiple taxation system, hurdles during transportation, and duration of transport permit.
As reported by Sundriyal and Sundriyal [47] from Sikkim within the Kangchenjunga Landscape, the sale of fruit provides minimum returns due to fairly low shelf life and market costs. Therefore, some value addition in the form of pickle, chutney, jam, jelly, etc. may increase fruit shelf-life and economic profit to local communities. This reflects a clear need to diversify the product base and to ensure that wild edible plants fetch higher prices [47]. There is also need for value addition for other NTFPs. Therefore, value addition at the local level is an essential part of NTFP trade. Untapped but potential species of NTFPs such as wild edible fruit and vegetables could be promoted in local markets. These could also be promoted for visitors in hotels and restaurants.
Another major problem in commercialization of NTFPs is the low volume in which they are collected and produced, in contrast to the large quantities that are required for the markets. This problem could be addressed by establishing cooperatives, and using these cooperatives for collective marketing which will ensure optimum benefits to collectors [48].

Threats and conservation challenges
Unustainable harvesting of NTFPs, mostly medicinal and edible plants, is the major threat to conservation and management of NTFPs in the Kangchenjunga Landscape [47,49]. Sustainable harvesting is essential for conservation of NTFPs, and in turn for ensuring the livelihoods of many rural peoples. Indeed, promotion of commercial extraction of NTFPs as a conservation strategy is based on the argument that forest conservation must be able to offer economic incentives to local peoples in order to counter the threat from destructive land uses such as logging and grazing. This strategy has gained wide acceptance as a conservation paradigm [2]. As indicated by Ticktin [2], despite growing concern over the conservation of these species, as well as their potential to enhance forest conservation and livelihoods, information on the ecological implications of harvest is not available in the Kangchenjunga Landscape.
Illegal trade of NTFPs from the landscape often includes some of the CITES Appendix listed species such as Sunakhari (Orchids), Kutki (Neopicrorhiza scrophulariiflora), and Lauth salla (Taxus wallichiana). The trade also includes some plant species under legal protection of the Government of Nepal like Orchids, Champ (Michelia champaca), Jhyau (Lichens), Jatamansi (Nardostachys grandiflora), and Sughandhawal (Valeriana jatamansi) [43]. These species are mostly traded to India via local collectors, whereas limited quantity of these items are exported to Tibet [50,51]. Conserving such species is challenging, yet illegal trade has  slightly decreased in the last decade due to effective conservation efforts of local organizations and increased cultivation practices in the landscape. Community forestry, which has restricted open access to NTFPs, and resource monitoring have also been effective in conserving NTFPs in recent years. In addition, availability of economically important NTFP species has currently declined due to deforestation and replacement with monoculture, use of pesticides and over harvesting [50]. Traditional knowledge on the use of NTFPs such as medicinal plants is also gradually declining due to socio-economic transformation in the Kangchenjunga Landscape [49,52,53].
Monitoring is one of the key components to promote the NTFP sector. Follow-up of rules, regulations and strategies related to NTFPs is necessary for contributing to changes in policy that are able to mainstream sustainable management of NTFPs with livelihoods improvement. Limited progress has been achieved in the Kangchenjunga Landscape in controling over-harvesting, enforcing effective harvesting regimes, and maintaining conducive and adaptive adminstrative processess. Recently adopted economic tools such as certification of sustainable harvests should also be applied as a means of ensuring that NTFPs collected sustainably can be identified as such by the consumers [54,55].
NTFPs reported from the Kangchenjunga Landscape also include many species under different threat categories as well as under priorities of the governments. For example, of the total 30 national priority herbs of Nepal, 26 are abundantly available in the Kangchenjunga Landscape, while all species prioritized for cultivation and research in Nepal are also reported from the Landscape [56]. Among these, Nardostachys grandiflora, Neopicrorhiza scrophulariiflora, Rauvolfia serpentina and Taxus wallichiana are the most threatened species. Therefore, the economic, socio-cultural and conservation values of these NTFPs are extremely high.

NTFP policy frameworks
A comparision of NTFP policy frameworks in the Kangchenjunga Landscape shows that Bhutan, India and Nepal have supportive policies for the NTFP sector, thereby providing enabling environments and support for NTFP programs and marketing [25]. As a result, many development agencies including national and international non-governmental organizations have placed emphasis on NTFPs in their programs. The collection, conservation and sustainable utilization of NTFPs in Bhutan is mostly  [57]. The Indian National Forest Policy (1988) makes a special mention of NTFPs emphasizing on protection, improvement and their enhanced production for generation of employment and income [58]. Likewise, in Nepal there are several sectoral as well as specific policy provisions for sustainable use and management of NTFPs [15,55]. The most comprehensive policy is the Herbs and Non-Timber Forest Product Development Policy 2004 [59]. The recent Nepal National Biodiversity Strategy and Action Plan 2014 and Forest Policy 2015 also emphasize sustainable use and management of NTFPs and critically provide special opportunity to support livelihoods of marginalized propoor and women through wise use of NTFP. Nevertheless, present policy formation, implementation and field reality reflects power structures and domination by certain stakeholders and interests [60].
Gender participation in policy formulation is also challenging. For example, 75 % of people collecting NTFPs in India were women and 100 % involved in NTFP processing were women, but their inclusion in Joint Forest Management committees was less than 10 % [61]. Similarly, in Nepal, although women contribute a large share of the labor for forest and biodiversity conservation in community forests, they represent only 22 % in the executive bodies of Community Forest User Groups [62]. Similar situation exists in Bhutan where the women's involvement is generally low in the designing, planning, and implementation of forestry policies, and there is limited understanding of the roles, knowledge, aspirations and contributions made by women towards NTFP management [63].
Considerable efforts have been made to develop the NTFP sector, but the contribution of NTFPs in national economies remains insignificant. As pointed by Shackleton and Pandey [21], the reason behind this is that their economic value remains invisible to external observers as most NTFPs are used for household purposes; production and harvest of NTFPs is a seasonal event, with their use or trade involving only small quantities; much of the NTFP trade is via informal and closed markets which are hard to enumerate; production and markets is dispersed; and their use is highest in rural areas, which are often remote and marginalised in terms of human resources and development policies.

Gaps on knowledge based conservation and management of NTFPs
Like in other parts of the Himalayas, there is still a severe paucity of in-depth field based information on the abundance, reproductive biology and ecological impacts of harvesting of NTFPs in the Kangchenjunga Landscape. There is no standard method available to estimate the economic contribution of NTFPs and their products. Research on the inventory, life history of NTFPs, and impact of harvesting on the ecosystem is a prerequiste for their sustainable management, yet very few such activities have been documented from the landscape [64]. Similarly, ecological impacts of NTFPs harvesting for domestic and commercial purposes must be estimated to ensure their sustainability and the implementation for effective conservation measures.
Market size, structure and value chain of NTFP species depend on the demand and supply characteristics of products and their beneficiaries in different areas. Understanding market information is important for value addition and in devising investment strategies [16] for NTFPs based products, their diversification, and related enterprises. At present, the majority of NTFPs from the Kangchenjunga Landscape are traded in the raw forms, and NTFP harvesters lack necessary support for market-based strategies from both private, as well as government sectors.
Indigenous knowledge and management systems have been recognized for contributing to sustainable use of NTFPs, and consequently they have secured legal rights to manage forest resources [55]. In the Kangchenjunga Landscape, indigenous knowledge on NTFP use is well documented, but indigenous management systems need to be assessed and used for sustainable management.

Conclusion
We documented NTFPs collected and used for various purposes by the local people of the Kangchenjunga Landscape. The diversity of NTFPs was highest in India, followed by Nepal and Bhutan. Though the landscape possesses many potential species for trade, their nominal contribution to local livelihoods was due to lack of value addition and commercialization. Unsustainable harvesting and lack of value addition and commercialization could be considered as major challenges for conservation and development of the NTFP sector in the landscape.
Tracing the trend of NTFP research and exploitation, it shows much focus on medicinal plants resulting in overharvesting of some highly potential medicinal plants, with   [65]. Highly potential NTFPs must be identified and grown for commercial cultivation and adopted in traditional agroforestry systems. This will reduce pressure on these species in their natural environments while providing economic benefits to poor farmers [47].
Conservation and development organizations, together with government agencies and private sectors, must provide technical and innovative inputs to add value to NTFP products. They must also facilitate community mobilization for assessment and identification of potential NTFPs. The latter role will be of significant importance considering the limited human and financial resources of government agencies in the Kangchenjunga Landscape. An integrated approach will promote sustainable use of NTFPs while contributing to income generation and livelihood improvement for local people. Transboundary landscape conservation programs will provide opportunities for transboundary cooperation through policy reforms, as well as providing opportunities to diversify livelihoods of forest dependent communities. However, marketing and commercialization of NTFPs can be successful only if the activity is transparent, equitable and sustainable, with important implications for poverty reduction and better resource management [20]. Increasing access to NTFP-selling outlets could be achieved through information dissemination, empowerment of collectors and establishment of linkages between collectors and traders [41]. The role of small and medium sized enterprises and cooperatives is extremely important to achieve sustainable management of NTFPs.