Integrating ethnobiological knowledge into biodiversity conservation in the Eastern Himalayas

Biocultural knowledge provides valuable insight into ecological processes, and can guide conservation practitioners in local contexts. In many regions, however, such knowledge is underutilized due to its often-fragmented record in disparate sources. In this article, we review and apply ethnobiological knowledge to biodiversity conservation in the Eastern Himalayas. Using Sikkim, India as a case study, we: (i) traced the history and trends of ethnobiological documentation; (ii) identified priority species and habitat types; and, (iii) analyzed within and among community differences pertaining to species use and management. Our results revealed that Sikkim is a biocultural hotspot, where six ethnic communities and 1128 species engage in biocultural relationships. Since the mid-1800s, the number of ethnobiological publications from Sikkim has exponentially increased; however, our results also indicate that much of this knowledge is both unwritten and partitioned within an aging, gendered, and caste or ethnic group-specific stratum of society. Reviewed species were primarily wild or wild cultivated, native to subtropical and temperate forests, and pend IUCN Red List of Threatened Species assessment. Our results demonstrate the value of engaging local knowledge holders as active participants in conservation, and suggest the need for further ethnobiological research in the Eastern Himalayas. Our interdisciplinary approach, which included rank indices and geospatial modelling, can help integrate diverse datasets into evidence-based policy. Electronic supplementary material The online version of this article (doi:10.1186/s13002-017-0148-9) contains supplementary material, which is available to authorized users.


Background
Conservation practitioners have historically considered the role of human communities only or primarily in terms of the threats that extractive and transformative activities pose on the environment [1][2][3]. As a theoretical consequence, people-free or 'fortress conservation' strategies have become the dominant means of protecting 'natural' systems from anthropogenic influence [4,5]. However, over the past twodecades, a paradigm shift among conservationists has challenged this convention [6][7][8]. Termed biocultural approaches to conservation [9], recent programs have integrated the innovations, practices, and worldviews of Indigenous and local communities into policies addressing the rapid attrition of Earth's biological and cultural diversity, hereafter termed biocultural diversity [9][10][11][12].
Thematically, biocultural approaches to conservation emphasize the dynamic, multi-scalar feedback loops that link social and ecological processes [9]. They synthesize biodiversity science and ethnographic fieldwork to discern processes that shape extant Earth systems [13]. In doing so, they help deconstruct the dualism separating 'nature' from society, and place local people back in parks as conservation agents [14][15][16]. Worldwide, such projects have had a variety of reported successes, including heightened spiritual connection and increased environmental literacy [16,17]. However, debates continue as to the verity of reported claims and the extent to which conservation programs should serve human welfare [9].
'Landscape' initiatives in the Eastern Himalayas evidence the successful utilization of biocultural principles for conservation purposes [18]. In 1997, an International Centre for Integrated Mountain Development (ICI-MOD)-led collective petitioned for the designation of Mt. Khangchendzonga as a dynamic complex of socio-ecological interaction [19,20]-a biocultural hotspot. The transboundary Khangchendzonga Landscape (KL) is situated within the Himalayan Biodiversity Hotspot [21,22], and includes Bhutan, India, and Nepal. It incorporates 7.2-million people belonging to diverse ethnic communities, including Indigenous groups like the Lepchas of Sikkim and Darjeeling, the Lhop (Doya) of Amu Mo Chhu Valley, and Walungpas of Walangchung Gola of Taplejung [22]. Because of this complexity, biocultural approaches to conservation facilitated environmental management in the KL. Co-management, communitybased conservation, and integrated conservation and development, for example, have empowered Indigenous and local peoples through non-government organizations (NGOs), and promoted international cooperation along sensitive geopolitical boundaries [21][22][23][24].
Since its original delineation, the India-led Khangchendzonga Landscape Conservation and Development Initiative and Feasibility Assessment has committed 14,061 km 2 of land, with a population of 6,325,457 people, into KL conservation policies [25]. KL-India's network is comprised of 16 protected areas (PAs), including a biosphere reserve (n = 1), national parks (n = 4), and national wildlife sanctuaries (n = 11). Within the Indian landscape, the Government of Sikkim's (GoS) efforts in the Khangchendzonga Biosphere Reserve (KBR) are perhaps the greatest testament to claims regarding efficacy of biocultural principles for achieving local and international conservation objectives. Sikkim occupies a 7096-km 2 zone of the Indian Eastern Himalayas, and has 37% of its total area, excluding transition zones of the KBR, designated for conservation purposes. The Khangchendzonga National Park (KNP) encompasses over 80% of all protected lands in Sikkim (Table 1); six additional sanctuaries can be found within the borders of these PAs [25]. For maintaining tribal sanctity and for cultural conservation purposes, the GoS demarcated Dzongu Territory for the exclusive use of the Indigenous Lepcha people [26]. On 17 July 2016, the KNP was inscribed India's first mixed-criteria UNESCO World Heritage Site based on the region's biocultural heritage.
Traditional and community knowledge buttresses conservation policies in Sikkim and is heralded for its adaptive capacity. However, at the same time, Sikkim's biocultural heritage is threatened by 'modernizing' forces associated with globalization and rapid climatic change. As noted in the Sikkim Biodiversity Action Plan, the state lacks formalized and collated records of its biodiversity, which extends into ethnobiological documentation [27]. Even among existing studies, including ethnobiological datasets, records are strictly qualitative, and exist as repetitive, fragmentary notes that lack a consolidated attempt for strengthening policy [28,29]. Mobilizing this knowledge and associated datasets into environmental management programs remains a challenge.
In this review, we explore the application of ethnobiological knowledge for biodiversity conservation in Sikkim. Specifically, we ask: (i) What is the spatio-temporal pattern of ethnobiological knowledge documentation?; (ii) How is ethnobiological knowledge partitioned within and among ethnic communities?; (iii) What species are priority targets for conservation, and are these species found within protected areas? In asking these questions, we hope to reframe discourses that focus on the Eastern Himalayas as only or primarily a reservoir of biological and genetic diversity. To our knowledge, our manuscript serves as the first ethnobiological review of the Sikkim Eastern Himalayas.

The Sikkim Eastern Himalayas
Sikkim is divided into four districts, and situated between Bhutan, Nepal, the Tibetan Autonomous Region of China (TARC), and the Indian State of West Bengal. In the 17th Century, Lepcha Fig. 3 for geographical location of detailed PAs multi-directional process of change resulted in Sikkim's protectorate status and eventual integration into India as its 22nd state in 1975 [30]. Prior to integration, major socioecological changes followed contact with the British East India Company in the mid-1880s. During this period, Nepali migration, here a generic term that includes many castes and ethnicities, was incentivized to promote colonial agricultural development in the Eastern Himalayas [31]. These progressive changes resulted in a rich admixture of ethnobiological traditions from the Greater Himalayas. Demographic records from Sikkim have varied in quality since the first census in 1891; notwithstanding, Sikkim's population appears to have increased from 30,458 to 607,688 people between 1891 and 2011 [32,33]. The Anthropological Survey of India identified 25 ethnic communities in the state during its first ethnographic survey between 1988 and 1990 [34]. These communities are generally grouped as: (i) Bhutias (Lhopos, including Denjongpas, Lachenpas, and Lachungpas) and Lepchas, the autochthons of Sikkim who represent less than 20% of the total population; (ii) People of Nepalese origin, mainly Limbus and Rais, who began migrating to Sikkim from the 1870s and represent more than 75% of the population; and, (iii) People from the plains of India, including Bengalis, Biharis, and Marwaris [35]. In June 1978, Lepcha, Bhutia, Chumbipa, Dopthapa, Drokpa, Kagate, Sherpa, Tibetan, Tromopa, and Yolmo communities were recognized as Scheduled Tribes in Sikkim; the Kami, Damai, Lobar, Majhi and Sarki were classified as Scheduled Castes. The Government of India considers some 'Nepali' identifying or identified groups in Sikkim as 'backward castes': Gurung, Magar, Newars, Limbu/Subba, Rai, Sunwar, and Tamang. Bengali, Bihari, Deswali, Marwari, and Punjabi -identifying communities, all recent migrants who are diverse both within and among respective communities, are well-established in modern Sikkim [36]. In total, our study recognizes 32 ethnic communities, 17 languages, and 9 religions in Sikkim [34,[36][37][38].
Sikkim's landscape is a well-recognized biodiversity hotspot, with habitat types broadly categorized into six categories that are correlated elevation (  [39]. Diverse assemblages of human communities living within and (re)producing these ecosystems have facilitated the region's rich, biocultural heritage.

Data collection and standardization
From October 2015 through February 2016, we conducted a systematic review of publically available and accessible literature pertaining to ethnobiological knowledge in the Sikkim Eastern Himalayas. For this study, we defined ethnobiological knowledge as traditional and community knowledge-Indigenous and non-Indigenous-related to socio-ecological interactions between identified or identifiable taxa and the people of Sikkim. Using search terms Darjeeling/Kalimpong/Sikkim/Eastern Himalaya AND Ethno/Indigenous/Traditional, we searched four digital databases: (i) ENVIS [40]; (ii) Google Scholar; (iii) NELUMBO [41]; and, (iv) Project Muse [42]. We included Darjeeling and Kalimpong (West Bengal, India) as place-based keywords due to their historical association with the Kingdom of Sikkim. After analysis, we omitted data published in the ENVIS Medicinal Plants of Sikkim database due to its primary reference of non-Sikkimese user groups and medical traditions. We then conducted archival research at six institutions in Gangtok, Sikkim using the same criteria: (i) The Botanical Survey of India; (ii) The G. B. Pant National Institute of Himalayan Environment and Sustainable Development, Sikkim Unit; (iii) The Namgyal Institute of Tibetology; (iv) Home Department, Government of Sikkim Central Library; (v) Sikkim University Central Library; and, (vii) Sikkim State Bioinformatics Institute. Once collected, each source was reviewed for the following subsets of data: study site name, including the names of sacred landscapes, cities, villages, panchyats, samitis, blocks, districts, and subdivisions; bio-physical characteristics of site-specific studies; publication date; Indigenous and local castes, clans, and groups surveyed; and, species diversity. These sources are provided as an additional file [see Additional file 1].
We transcribed species data from each reviewed record into a working database [see Additional file 2]. After all sources were reviewed, we then standardized species to current taxonomic designations using international databases and field guides [43][44][45][46][47][48]. Concurrently, we tabulated the relative citation frequency for each species, and partitioned uses into one of 19 accepted categories (Table 2) [49,50]. Relative citation frequency was calculated by dividing each citation value by the value of the most frequently cited species [see Additional file 2]. Regarding ecological data, we detailed Sikkim-specific altitudinal range data when possible [51][52][53][54][55][56][57][58]; data from the region were used as a proxy in the absence of Sikkim-specific records [45][46][47][59][60][61]. Finally, we collected the following data: the conservation status of species from the IUCN Red List of Threatened Species [62] and Government of Sikkim [63]; and, naturalization, cultivation, or domestication status [47,64]. Our study assumes that the number of use categories reported for a given species corresponds with the amount of attention it receives from communities in Sikkim. It is important to note that the number of uses might not correspond to current and active applications of those uses.

Data analysis
We geo-referenced reported study sites and conducted spatio-temporal analyses of reviewed data in ArcGIS [11,65,66]. Specifically, we performed the following assessments: (i) identification of administrative districts with the highest representation of ethnobiological records; (ii) temporal analysis of ethnobiological knowledge documentation; and, (iii) identification of surveyed communities and their knowledge documentation through time.
We calculated two conservation ranks for reviewed species based on accepted methods for categorical data (Tables 3 & 4): Harvest Rank (HR) and Sensitivity Rank (SR) (see [67,68]). From this point, however, we could not carry out further statistics as our rank assignation was based on qualitative criteria in which numerical ranks represent other categories rather than quantities. The HR value incorporated harvest and provenance data ( Table 4): wild and native (WN) = 5; wild-cultivated and native (WCN) = 4; wild and non-native (WNN) = 3; wild-cultivated and nonnative (CNN) = 2; and cultivated (C) = 1 [60,67,69]. We believe that wild and native species are of higher conservation priority because on their provenance in the Sikkim   [60,63]. Using matrix criteria to account for these attributes, we scored SR in a decreasing order to 8-1 (Table 4) [69]. We also calculated a relative citation frequency (CF), or the number of reviewed citations for species e divided by the maximum number of citations for n surveyed species. These data are provided as an additional file [see Additional file 2]. We hope these ranks, although qualitative, serve as platform for future analyses that integrate social and natural science data with community knowledge to indicate priority targets for biodiversity conservation.
Using the altitudinal range of each reviewed species, we modeled biocultural hotspots in Sikkim using a standard methodology at 100 m altitudinal resolution ( Fig. 2) (see [70]). Here, we aimed to project a qualitative map that identified priority regions for biodiversity conservation based on the altitudinal range of reviewed species. We acknowledge that modeling procedures often account for GIS-based, site-specific occurrences and bioclimatic variables associated with specific species [70,71]. However, such data from Sikkim is only available in heterogeneous, fragmented forms that are geographically biased or incorrect. Moreover, Sikkim's topography, which averages 40°s lope, and altitudinal variation, ranging from 284 m to 8586 m, generate a plethora of unpredictable microhabitat and microclimatic conditions that: influence species distributions; limit the practicality of field surveys; and, bias conventional modeling procedures [72]. Therefore, in the absence of data, our model engages altitudinal distribution data as the sole proxy for various methodologies [73].

Spatio-temporal analysis
Our review resulted in 176 ethnobiological records from the Sikkim Eastern Himalayas [see Additional file 1]. These records include 42 site-specific surveys, 18 of which were multi-site studies (total geo-referenced locations: 119), 94 contained methodological or instructional content on species use, 15 contained folk tales or cultural information beyond medical or material utility, and ten were biodiversity-related records with ethnobiological footnotes (Fig. 1). Based on site-specific records, North District received the greatest survey effort (37%) followed by West District (33%), East District (16%), and South District (14%). North District's survey effort was driven by studies in Dzongu Territory (North District), a once-royal land plot now reserved for certain Lepcha families. The average survey altitude across sitespecific records was 1775 m ASL (+/-712 m SD).
Our temporal analysis revealed that biocultural records were first published during the East India Company's expansion across the Indian Subcontinent during the 1840s [74][75][76]. Our review specifies that Sir Archibald Campbell, the first British political officer to Sikkim and Darjeeling, authored the first ethnobotanical vignettes from Sikkim as they relate to Lepcha communities [74]. Concurrently, Sir Joseph Dalton Hooker, a British doctor and an esteemed naturalist, reflected upon the region's biocultural heritage in his two-volume Himalayan Journals published 1854. For much of the mid-19th Century, naturalist records were the primary sources of biocultural anecdotes, particularly as they relate to Rhododendron spp. (see [21]). We identified no biocultural records dating one century after Hooker's Journals. A few generalist surveys were conducted during the mid-20th Century in what was termed the Sikkim and Darjeeling Hills [77,78]. Approximately 14% of all ethnobiological records from Sikkim were published between 1854 and 1990, none of which detailed specific study sites (Fig. 2). The late 20th Century saw an exponential increase in these studies across Sikkim, particularly regarding medicinal plant species. Place and district-specific studies revealed that the earliest documentation began in West District, and moved toward North District during the second decade of the 21st Century (Fig. 1). Approximately, 87% of all reviewed biocultural studies were published between 1990 and 2016, with a significant increase in publication rate during the first decade of the 21st Century (r = 0.863; P < 0.001).

Surveyed ethnic communities
Six of 32 identified ethnic communities in Sikkim have written ethnobiological records: Bhutia, Lepcha, Limbu, Nepali, Sherpa, and Tibetan communities. However, most reviewed records were not ethnic-group specific and  [45,79]. Allium sikkimense, Mahonia sikkimensis, Rhododendron sikkimensis, and Swertia pedicellata. The taxonomic designations for these and many of our reported species, however, are pending official revision. In Animalia, fish were the most represented Chordates (37), followed by Mammals (22), Birds (12) and Amphibians (3) [see Additional file 2]. Three invertebrates were cited, two of which were in the Apidae. In Fungae, Basidiomycetes accounted for 77% of reviewed species (44), with approximately 85% of the remaining 13 Ascomycetes being Lichens.

Biocultural hotspots
Our map illustrates areas that have the greatest potential richness of species with biocultural records, termed biocultural hotspots, based on the elevational range of species (Fig. 3). Grid cell values range 7 (low) to 619 (high) species and are presented at 100-m elevational resolution. The highest grid-cell values were located outside of PAs. Richness of culturally important species was highest in subtropical zones across kingdoms, with a sharp decline toward alpine regions.

Discussion
Our review indicates that Sikkim has a rich biocultural heritage that includes knowledge pertaining to over 1100 species Disease and health-related categories were based on criteria outlined by the World Health Organization [61] of animals, fungi, and plants. Local people not only know about the useful properties of these species, but also the community ecology and life histories of diverse organisms [80]. These aspects of ethnobiological knowledge, which encompass abundance, distribution, and phenology, significantly influence community management practices and can therefore benefit conservation planning in Sikkim [29,79]. For instance, in previous studies, Lepcha communities were engaged by government researchers to understand the population status of under-surveyed bird species; local communities were found to provide "data" at the accuracy needed to make management decisions [81,82]. Our reviewed records also implied that faith traditions and community taboos sustain many ethnobiological relationships in Sikkim, and cultivate a sense of stewardship toward critical habitat [35,[83][84][85][86]. We conclude that targeting biocultural knowledge systems, including gaps in ethnobiological research, is a practical way to incorporate local peoples-their knowledge, land, and participation-into multi-scalar conservation directives in the Eastern Himalayas.
Our analyses illuminated the dynamic nature of ethnobiological knowledge, and evidenced its ongoing construction amidst changing socio-ecological conditions. We traced a dramatic increase in ethnobiological records published since the 1950s, with a significant spike in the mid-1990s. This trend appears correlated with both the relaxation of permit restrictions into Sikkim, and the 1993 initiation of the Convention on Biological Diversity (CBD) following the Earth Summit in Rio de Janeiro in 1992. The CBD obliged signatory polities, including India, to acknowledge and preserve biocultural knowledge as an adaptive resource for conservation initiatives, record and disseminate biocultural knowledge for practical applications, and ensure equitable benefits arising from biocultural knowledge (reviewed by [21]). Our assessment highlighted, however, a stark difference in ethnobiological knowledge within and among ethnic communities. Intra-cultural differences compounded overall knowledge diversity based on age, gender, occupation, and individual strategies and interests [26]. These factors were not quantitatively justified in any of our reviewed studies. The paucity of records from 26 identified ethnic communities further indicates that much of Sikkim's biocultural heritage remains as unwritten, oral traditions situated within a gendered, caste-specific, and aging stratum of society. In the future, we suggest that researchers begin addressing these gaps through collaborations with nomadic or semi-nomadic peoples at high altitudes, including Bhutia, Chumbipa, Dopthapa, Drokpa, Kagate, Sherpa, Tromopa and Yolmo communities. High-altitude zones are particularly sensitive to climatic changes that may alter community assemblages, ecological processes, and, as an extension, historical ways of relating to the environment [85,87,88]. With the participation of these groups, conservationists can craft more holistic and culturally appropriate strategies for both restoration and conservation in the Eastern Himalayas.
As previously alluded to, older members of rural communities were the primary user group of reviewed species, namely for medicine. Knowledge of species use, practice, and folklore was reported to decrease in recent generations, as much of the knowledge was documented from collaborators between 50 and 70 years of age [26,29]. Today, younger generations migrate to urban centers where they are neither exposed to local species nor the traditions that surround them. Both imposed legal structures in the early 21st Century and market liberalization in the mid-1990s have further complicated knowledge transmission and species use, resulting in the attrition of ethnobiological knowledge in Sikkim. For instance, between the 1970s and 1990s, the Sikkim Forest, Environment and Wildlife Management Department permitted commercial exploitation of medicinal plants, including from PAs. However, as of 2001, the government implemented a 5-year ban on medicinal plant collection via Order No. 13/F/Env&W. This order received a 5-year extension in 2006, and will likely be ratified again in the future. Moreover, local access to state healthcare providers and allopathic medicine has reduced local dependency on wild animals, fungi, and plants as medicine.
Incentivizing and/or commercializing the cultivation of edible and medicinal plants and fungi within agroforestry systems may reduce pressure on wild populations and create habitat corridors for threatened species [29,107]. To date, most conservation efforts in Sikkim have been directed toward the nominal designation of PAs at mid and high altitudes. Military encampments and agricultural landscapes surround these PAs. Moreover, traditional doctors, spiritual healers, and rural villagers still harvest and collect many reviewed species from these areas despite legal restrictions [104,[108][109][110][111][112]. Conservationists can begin addressing these pressures, without marginalizing local communities, by promoting cooperative agroforestry programs along PA borders. Recent reviews, for example, have suggested integrating edible and medicinal plant cultivation into existing Nepalese Paperbush (Edgeworthia gardneri; Thymelaeaceae) or Black Cardamom (Amomum subulatum; Zingiberaceae) agroforestry systems which already yield high profits [29,113,114]. As noted by Charnley et al. [115], such programs must do more than identify the "right" or best model for knowledge application and sharing, and must address existing societal factors that may hinder program implementation or undermine community structures. Organizational frameworks could, therefore, draw upon pre-existing dzumsa and dwichi committee structures in Sikkim, which have legacies of conservation impact [116,117]. Any cooperative, however, must ensure that agroforestry systems produce marketable amounts of edibles that can either be preserved or transported to market before spoilage (as reviewed by [29,116]). Our conservation rank system and additional files is useful for identifying target species based on criteria of interest, including medicinal use, altitudinal range, and population status [see Additional files 1, 2 and 3].
Incorporating ethnobiological knowledge into biodiversity conservation is a meaningful way to empower local communities to both monitor and preserve species of biocultural importance [9,11,116]. Based on our review, communities have obvious incentive to conserve biodiversity for cultural purposes and practical use. However, our results suggest a literature bias toward medicinal plants, and a paucity of records from the kingdoms Animalia and Fungae. To hone the applicability of our biocultural hotspot concept, we recommend that researchers incorporate new criteria, including species-specific ranges and habitat information, into our model structure. Moreover, we suggest that researchers document ethnobiological relationships that extend beyond medicinal uses of species to include living oral traditions, folklore, art, etc. By combining ethnobiological surveys with biodiversity science, particularly the gaps noted in recent reviews [21,29], conservationists can better understand the socio-ecological dynamics shaping modern Sikkim.

Conclusion
We collated and applied ethnobiological knowledge to promote biodiversity conservation in the Eastern Himalayas. We began with a spatio-temporal review of biocultural records from Sikkim, India to understand: (i) patterns in biocultural knowledge documentation; (ii) the diversity of species with biocultural records; and (iii) the partitioning of biocultural knowledge within and among ethnic communities. We then galvanized these records into two conservation indices and a biocultural hotspot model that indicate conservation priorities in Sikkim.