RESEARCH REPOSITORY

This is the author’s final version of the work, as accepted for publication following peer review but without the publisher’s layout or pagination.

The definitive version is available at:

https://doi.org/10.1016/j.jep.2018.04.040

Cunningham, A.B., Brinckmann, J.A., Kulloli, R.N. and Schippmann, U. (2018) Rising trade, declining stocks: The global gugul (Commiphora wightii) trade.

Journal of Ethnopharmacology

http://researchrepository.murdoch.edu.au/id/eprint/40905/

Copyright: © 2018 Elsevier B.V.

It is posted here for your personal use. No further distribution is permitted.

Author’s Accepted Manuscript

Rising trade, declining stocks: The global gugul(Commiphora wightii) trade

A.B. Cunningham, J.A. Brinckmann, R.N. Kulloli,U. Schippmann

PII: S0378-8741(17)34489-6DOI: https://doi.org/10.1016/j.jep.2018.04.040Reference: JEP11335

To appear in: Journal of Ethnopharmacology

Received date: 22 December 2017Revised date: 23 April 2018Accepted date: 27 April 2018

Cite this article as: A.B. Cunningham, J.A. Brinckmann, R.N. Kulloli and U.Schippmann, Rising trade, declining stocks: The global gugul (Commiphorawightii) trade, Journal of Ethnopharmacology,https://doi.org/10.1016/j.jep.2018.04.040

This is a PDF file of an unedited manuscript that has been accepted forpublication. As a service to our customers we are providing this early version ofthe manuscript. The manuscript will undergo copyediting, typesetting, andreview of the resulting galley proof before it is published in its final citable form.Please note that during the production process errors may be discovered whichcould affect the content, and all legal disclaimers that apply to the journal pertain.

www.elsevier.com/locate/jep

1

Rising trade, declining stocks: the global gugul (Commiphora wightii) trade

A.B. Cunninghama,b*, J.A. Brinckmannc, R. N. Kullolid, U. Schippmanne

aSchool of Life Sciences, University of KwaZulu-Natal, King Edward Avenue, Pietermaritzburg, 3209, South Africa; and b School of Veterinary and Life Sciences, Murdoch University, 90 South St., Murdoch WA 6150, Australia cTraditional Medicinals, 4515 Ross Road, Sebastopol, California 95472, USA d Botanical Survey of India, Arid Zone Regional Circle (AZRC), Jodhpur, Rajasthan-342014, India eBundesamt für Naturschutz (BfN), Konstantinstr. 110, Bonn 53179, Germany *Corresponding author. tonyc05@bigpond.net.au (A.B. Cunningham)

ABSTRACT

Ethnopharmacological relevance: Commiphora wightii is exploited in India and Pakistan for an oleo-resin (gum guggul) traditionally used in Ayurvedic, Siddha and Unani medical systems. Processed C. wightii oleo-resin products are exported from India to 42 countries, including re-export to Pakistan, for anti-inflammatory use and as an anti-inflammatory and an anti-obesity treatment considered to lower cholesterol and lipid levels. The C. wightii export trade has particular relevance to the European Union because Belgium, France, Germany, Hungary, Italy, the Netherlands, and United Kingdom are importing countries. Demand and prices for C. wightii oleo-resin are increasing and wild stocks of C. wightii are in decline. The overexploitation of C. wightii after tapping for its commercially valuable oleo-resin is not a new problem, however, but one that has existed for over 50 years. Lopping and chopping trees to extract C. wightii oleo-resin has had a devastating impact on C. wightii populations since the 1960’s. Aim of the study: The aim of this study was to review the sustainability of the global trade in C. wightii oleo-resin. This included reviewing studies on resin tapping methods and the impacts of wild harvest on C. wightii populations in India and Pakistan. Materials and Methods: Firstly, we reviewed studies on impacts of C. wightii oleo-resin harvest and on the policy responses taken in relation to harvest and trade in C. wightii oleo-resin. Secondly, we reviewed studies on C. wightii cultivation. Thirdly, global trade data for C. wightii were analyzed. Results and Conclusions: Destructive harvest to obtain the gum is the major threat facing this species. C. wightii populations are also fragmented by habitat loss through clearing for farming. Cutting and lopping in order to extract the medicinal gum are a major threat to C. wightii populations, as is poor recruitment due to grazing by livestock. As a result of over-exploitation, C. wightii oleo-resin production has declined in India. In Gujarat, a key production area, the decline over a 50-year period has been from 30 tonnes in 1963, to 2.42 tonnes in 1999 to 1.6 tonnes in 2013. Consequently, large quantities of C. wightii oleo-resin (around 505 tonnes/year) are imported into India from Pakistan. An estimated 193 tonnes/year of crude gum equivalent is exported from India in the form of processed products. With remaining populations in decline due to commercial exploitation for international trade, a range of policy options (such as CITES Appendix II listing) and practical conservation actions (such as cultivation) need to be considered. Abbreviations: AYUSH, Ministry of Ayurveda, Yoga & Naturopathy, Unani, Siddha & Homoeopathy; CAMP, Conservation Assessment and Management Plan process; CITES, Convention on International Trade in Endangered Species; CR, Critically Endangered; DD, Data Deficient; EU, European Union; E, Endangered; GRIN, Germplasm Resources Information Network; HS, Harmonized Commodity Description and Coding System; INR, Indian rupees; ITC, Indian Trade Classification; IUCN, International Union for Conservation of Nature; MT, metric tonnes; USDA, United States Department of Agriculture; VU, vulnerable. Keywords: Commiphora wightii, oleo-resin, guggul, harvesting impacts, CITES

1.0 Introduction Commiphora wightii (Burseraceae) is a multi-branched shrub growing to 2 - 3 m high with the papery bark typical of many Commiphora species. Commercial exploitation of the gum currently

2

takes place in Pakistan, mainly in Baluchistan and Sind, (Williams & Ahmad, 1999) but also in Khyber Pakhtunkhwa Province, Pakistan (Sher, et al., 2014) and in Gujarat and Rajasthan, India (Dixit & Rao, 2000; Kulloli & Kumar, 2013). Most gum harvest is from the wild, both for export and use in the Ayurvedic, Siddha and Unani systems of medicine (Chaudhary, 2012). In India, C. wightii oleo-resin (widely known as gum guggul or guggulu) is also used as incense in meditation and purification rituals, in perfumery, calico-printing, dyeing silk and cotton and as firewood (Reddy, et al., 2012). C. wightii oleo-resin is also reported in use as a substitute for African myrrh (C. africana) and as an adulterant of true myrrh (C. myrrha) (Tropicos.org. Missouri Botanical Garden, n.d.). Although new compounds continue to be found in C. wightii oleo-resins (Meselhy, 2003), the main commercial interest is in guggulsterones. These contain active ingredients used to treat arthritis, cancer and to reduce cholesterol and obesity (Antonio, et al., 1999; González-Castejón & Rodríguez-Casado, 2011; Sharma, et al., 2009). The main active ingredients are Z-guggulsterone and E-guggulsterone (González-Castejón & Rodríguez-Casado, 2011).

Overexploitation of C. wightii and tree death after intensive tapping for its commercially valuable oleo-resin is a challenge that has persisted for over 50 years. Tapping, lopping and chopping trees to extract C. wightii oleo-resin has had a devastating impact on C. wightii populations since the 1960’s. Atal et al. (1975), for example, recorded that a “large number of plants of C. mukul (= C. wightii) were present some 10 to 15 years ago in Rajasthan, but the number has come down considerably, largely due to the faulty techniques of tapping employed by the local inhabitants” (Atal, et al., 1975). Similarly, in Gujarat, the local Forest Department collected 30 tons of gum-resin in 1963, but in 1999 only 2.42 tons were collected (Dixit & Rao, 2000). Observations by many researchers, including by Atal et al. (1975), Dixit and Rao (2000), Soni (2010), Soni and Swarnkar (2006) indicate declining C. wightii stocks.

In India in 2002, C. wightii was classified as ‘Lower risk and conservation dependent (LRcd)’ [GES (Gujarat Ecological Society), MSU (Maharaja Sayajirao University) and GUIDE (Gujarat Institute of Desert Ecology), 2002] cited in (Rajendrakumar, 2013). Commiphora wightii populations are considered to have declined to less than 50% of their original size, leaving isolated sub-populations (Parmar, 2003). More recently, a conservation threat assessment by Reddy et al. (2012) suggested that this species is threatened across all of Rajasthan and Gujarat and should be considered endangered (Reddy, et al., 2012). The Government of India now includes C. wightii under their Rare, Endangered, Threatened (RET) category of species (Samantaray, et al., 2011) and in Rajasthan there is a ban on tapping of C. wightii trees (Samanta & Mandal, 2014). It is not surprising, therefore, that in March 2015, the Government of India expressed concerns about difficulties the Ayurvedic medicine industry is experiencing procuring C. wightii (Naik, 2015). Internationally, although initially considered Data Deficient (DD) on the IUCN Red List, it has recently been changed to Critically Endangered (CE) (Ved, et al., 2015). With demand and prices for gum guggul increasing and wild stocks of C. wightii in decline, the aim of this study was to review the extent of international trade in C. wightii oleo-resins, current conservation measures and the evidence for criteria for inclusion on CITES Appendix II based on Art. IV 2(a) of the Convention on International Trade in Endangered Species (CITES).

2.0 Materials and methods

Firstly, to get clarity on the trade assessment, we accessed all available published information on the taxonomy and trade names for C. wightii. Secondly, trade data for C. wightii was analysed using a range of sources. Trade from Gujarat (2008-2013) was from Yogi et al. (2014). International trade data was derived from the Govt. of India Department of Commerce EXPORT IMPORT DATA BANK (Version 7.2 – TRADESTAT) and the India-based Zauba import-export trade database, which relies on actual shipment documents (Zauba Technologies & Data Services Pvt. Ltd., n.d.). Using the harmonized system (HS) tariff codes (HS Codes) was complicated by two factors. Firstly, that a variety of HS Codes are used by Indian

3

exporters for various articles of commerce that contain C. wightii (= C. mukul) in various forms. For this reason, as Table 7 shows, the Indian Trade Classification (ITC) definitions are provided as well as the actual shipment descriptions that were used by the exporters, as these show the second challenge, namely that incorrect HS Codes are often used by exporters.

Thirdly, we reviewed published information on C. wightii ecology and population biology, oleo-resin yields and on the impacts of “gum guggul” harvest on C. wightii populations from across the geographic range of this species.

3.0 Results

3.1 Scientific name and synonyms

Correct species classification is at the basis of correct labelling of herbal ingredients and herbal products. The taxonomy of the source of gum guggul is particularly confused, possibly due to the taxonomic confusion pervasive across the genus Commiphora. For example, Balsamodendron mukul Hook. ex Stocks (1849), renamed as Commiphora roxburghii by Santapau in 1964 (Bhandari, 1964; Kulloli & Kumar, 2014a) and corrected to Commiphora wightii (Arn.) Band. by Bhandari (1964) (The Plant List, 2013; USDA, ARS, National Genetic Resources Program, n.d.). The current accepted name of the source of gum guggul is Commiphora wightii (Arn.) Bhandari (The Plant List, 2013). Widely recognized synonyms for C. wightii are Balsamodendron mukul Hook. ex Stocks (1849), Balsamodendron wightii Arn. and Commiphora mukul (Hook ex. Stocks) (Gardner & McGuffin, 2013; USDA, ARS, National Genetic Resources Program, n.d.). Yet The Plant List (2017) also considers C. mukul (Hook ex. Stocks) as an accepted name, contradicting other sources. Consequently, Commiphora mukul (Hook. ex Stocks) Engl., continues to be used in authoritative pharmacological publications (for example, González-Castejón and Rodriguez-Casado, 2011). 3.2 Common names including trade names Hindi: Gogil, Gugal, Guggul, Mukul, Ranghanturb, Bol, Hirabol; Sanskrit: Bhavabhishtha, Bhutahara, Bolah, Devadhupa, Deveshta, Dhurta, Divya, Durga, Guggalu, Jatala, Jatayu, Kalaniriyasa, Kaushika, Kumbha, Kumlhi, Kumbholu, KumbholuKhalaka, Kunti, Pavandvishta, Pura, Puta, Rakshoha, Rasagandhah, Sarvasaha, Shambhava, Shiva, Uddipta, Ulukhalaka, Usha, Vayughna; Tamil: Gukkal, Gukkulu, Mai shakshi , Vellaippapolam; Telugu: Gugul, Mabisaksh, Maisakshi, Balimtra-Polam; Kannada: Bola; Malayalam: Narumpasamaram, Narumpasa; Marathi: Guggala, Gulag; Gujarati: Gugal, Gugali, Gugar, Guggul, Mukul, Ranghanturb; Bengali: Gugal, Guggul, Mukul, Ranghanturb; English: Indian bdellium, Gum guggul, Mukul myrrh tree; Arabic: Mogla, Moql, Mokhil, Aphalatana; Persian: Baijahundana; Sinhalese: Rata – dummula (Sharma & Kumar, 2012; Lal & Kasera, 2010; Bedevian, 1994; Kapoor, 1990; Bhatt, et al., 1989; Sharma, et al., 1983; Atal, et al., 1975; Patil, et al., 1972; Nadkarni, 1954).

3.3 Geographic distribution C. wightii occurs in Pakistan (Karachi, Sind and Baluchistan) and India (Rajasthan, Gujarat, Haryana, Maharashtra and Madhya Pradesh) (Rajendrakumar, 2013; India Biodiversity Portal, 2015). Reports of C. wightii in North Karnataka in the old floras are not supported by proper specimens (D.K. Ved., pers. comm., 2015). In addition, the occurrence of C. wightii in Oman by Mosti et al. (2012) needs confirmation. In India, C. wightii is reported from five of India’s 15 agro-climatic zones; Gujarat Plains and Hill Region, Western Dry Region (Rajasthan), Eastern Plateau and Hill Region (Madhya Pradesh), Central Plateau and Hill Region (Madhya Pradesh and Rajasthan), and Western Plateau and Hill Region (Maharashtra and Madhya Pradesh) (National Medicinal Plants Board, n.d.). In their recent review, Kulloli & Kumar (2013) have summarized the information on the distribution of C. wightii in India, where C. wightii occurs in arid regions of Gujarat and Rajasthan including foothills of the Aravalli ranges and the Thar Desert. According to Soni (2010), “biodiversity hot-spots” for C. wightii are near Jaipur and Ajmer, the Indian Thar desert (Udaipur, Banswara, Dungarpur, Pratapgarh and Chittorgarh). In India, Kulloli et. al. (2013a) have mapped the

4

distribution and density of C. wightii in each district of the Rajasthan state. C. wightii occurs in arid and semi-arid woodlands, particularly on hills or slopes at the base of mountains to a region of flat land, commonly in Euphorbia scrub (Champion & Seth, 1968; Kulloli & Kumar, 2013). Studies by Kulloli et al. (2013a) also showed that natural populations of C. wightii preferred hills and piedmonts at 94% sites and pediment plains at 6% sites. Its habitat had sandy and sandy loamy soils. Most common associates included Prosopis juliflora, Euphorbia caducifolia, Boswellia serrata, Wrightia tinctoria, Grewia tenax, Acacia senegal, Calotropis procera, Butea monosperma, Dichrostachys cinerea, Anogeissus pendula, Rhus mysorensis and Maytenus emarginata (Kulloli, et al., 2013a). 3.4 Reproductive biology and population densities

Relatively little is known about the reproductive biology, seed dispersal and seedling establishment of C. wightii (Kulloli & Kumar, 2013). What we do know is that in wild C. wightii populations, reproduction is primarily from seed. However, fruit yields and seed set are considered to be very low in natural conditions. In terms of its reproductive biology, C. wightii is a sporophytic apomict showing nucellar polyembryony (Gupta, et al., 1998). Despite the fact that C. wightii produces morphologically normal pollen and pistils, Gupta et al. (1996) have shown that C. wightii is non-pseudogamous (i.e., apomixis is independent of pollination stimulus). Seed germination experiments based on seed color and size of seeds revealed that a black large seed gives more germination (18 %) as compared to other seed morphs (Kulloli, et al., 2013b).

The total population size of C. wightii is unknown. In the Kachchh area of Gujarat, India, Dixit & Rao (2000) assessed C. wightii density in 286 circular 0.1 ha plots and found C. wightii in 125 plots (43.7%) with an average density of about 49 plants per ha. The highest C. wightii densities were in undulating (41.2%) and hilly (23.5%) terrain. Joshi et al. (2012) found an even higher density of C. wightii in the Kachchh area in their survey of the Tapkeshwari Hill ranges (75.84 plants per ha). In Rajasthan, C. wightii density varied from 2 - 14 plants per ha in protected sites and 2 - 8 plants per ha in unprotected sites. In protected sites its canopy cover and plant height were also more than that in disturbed sites. Though it was co-dominant at all the sites, its dominance improved in protection while it declined in open conditions (Kulloli, et al., 2013a). No quantitative studies are known from Pakistan.

3.5 Threats and population trends

Destructive harvest to obtain the gum is the major threat facing this species. C. wightii oleo-resin is important in international trade, but is being extracted using unsustainable methods (Fig. 1C). For example, the application of ethephon on tapping cuts to increase guggul gum certainly increased gum production, but in the long-term this kills C. wightii plants (Soni, 2010).

5

Fig. 1. A. Typical growth form of Commiphora wightii B. Natural gum exudate from branches. C. Destructive tapping showing exposed wood surrounded by exudate. D. Raw guggul gum resin in a local market in Rajasthan. E. Experimental tapping to quantify gum yield from C. wightii.

In a study in North Gujarat, India, Rajendrakumar (2013) quantified C. wightii distribution along 123 belt transects and assessed which impacts threatened this species. Cutting and lopping in order to extract the medicinal gum were the major threat to C. wightii populations. Poor recruitment due to grazing is also a threat (Dixit & Rao, 2000). In common with several other Commiphora and Boswellia species, tapping of resin from C. wightii takes place in the dry season and stops when the rain arrives. Krishna-Murthy & Shiva (1977) suggest that this is because wet season resin yields are low and the resin is washed away from the stem (Krishna-Murthy & Shiva, 1977). In India, steam

6

distillation technology has caused a shift from commercial resin tapping to intensive lopping of branches. Destructive harvest methods, possibly combined with infection by the bacterium Xanthomonas axonopodis pv. commiphorae (Samanta & Mandal, 2014) have had a devastating impact on C. wightii populations (Kulloli & Kumar, 2013). Although many researchers cite the observation of Atal et al. (1975) that “a healthy mature tree yields 250 to 500 g of dry resin in one collecting season”, Samanta & Mandal (2014) have quantified oleo-resin yields in relation to C. wightii tree diameter (Fig. 2) as well as oleo-resin production according to different seasons. In their study, Samanta & Mandal (2014) found that C. wightii trees tapped in September produced the highest gum (49.4 ±t14.4 g per tree), whereas oleo-resin production was lowest in May (3.1 ±40.6 g per tree). Arya et al. (2011) suggested that C. wightii plants treated with ethephon dose 200 - 225 mg in the month of March helps in plant survival in arid conditions even after gum tapping (Arya, et al., 2011).

Fig. 2. A. The relationship between oleo-resin tapping success and infection rate by the bacterium Xanthomonas axonopodis pv. commiphorae and B. The correlation between C. wightii tree diameter and oleo-resin yield (redrawn from Samanta and Mandal, 2014).

3.6 Utilization and trade 3.6.1 National and cross-border trade In the 1970’s, Atal et al. (1975) noted that the Bhuj market in Gujarat, India, “meets practically the entire demand of the country. Bombay, Delhi, Calcutta and Amritsar are the important centres to which Guggul is exported from the Bhuj market” and that C. wightii oleo-resin was also sold from the Beawar and Balotra markets in Rajasthan to other markets in India. Today, the government of Rajasthan has banned the tapping of C. wightii trees (Samanta & Mandal, 2014). The main national supply source within India is from Gujarat, where the product is marketed through State controlled Gujarat State Forest Development Corporation Ltd (GFDCL) (Mandal, et al., 2011). Table 1 shows the trend of annual quantities for the five-year period of years 2008 - 2009 through 2012 - 2013 (Yogi, et al., 2014).

Table 1 Collection of guggul gum in Gujarat (from Yogi et. al., 2014) State Agricultural year (Apr-Mar) / Quantity C. wightii oleo-resin collected (tonnes)

2008-09 2009-10 2010-11 2011-12 2012-13 Gujarat 9.9 tonnes 6.4 tonnes 2.9 tonnes 3.3 tonnes 1.6 tonnes

Large quantities of C. wightii oleo-resin are also imported into India from Pakistan. At present, due to shortages of C. wightii oleo-resin in India caused by over-exploitation, there is a major cross-

7

border trade in C. wightii oleo-resin guggul from the Baluchistan province of Pakistan to India (Mandal, et al., 2011).

In one of the few assessments of the domestic trade in C. wightii oleo-resin in India, it was shown that in 2000 the largest quantity was sold in Mumbai market (100-500 tonnes), followed by Bangalore (100-125 tonnes), Shivpuri (100-120 tonnes) and then the Delhi market (50-100 tonnes) (Subrat, et al., 2002). Anotherstudy on the medicinal plants trade in India (Ved & Goraya, 2008) identified C. wightii oleo-resin one of the high volume trade products and estimated the total industrial demand of Indian herbal industries as 500 to 1000 tonnes per year for C. wightii oleo-resin, with a price range of 140 - 160 Indian rupees (INR) per kg (2006 - 2007). Ved & Goraya (2008) also reported that more than 90% of this demand is being met through imports from Pakistan. Precisely quantifying the level of international trade is not possible due to the absence of a specific HS Code for C. wightii, the rampant use of incorrect general HS Codes, and the unknown quantities used as components of Ayurvedic medicine complex formulations and multi-herb products. However, with the knowledge that India has export restrictions in place for wild C. wightii of Indian origin and that Pakistan has become the primary supplier to India, determining the quantity that India imports from Pakistan can provide an estimation of most export trade. It is, however, not known whether Pakistan exports guggul gum in significant quantities to countries other than India. Because India’s domestic collection levels are very low (Table 1) it can be assumed that India’s exports of C. wightii are comprised, for the most part, of Pakistan origin material. The India-based Zauba import-export trade database, which relies on actual shipment documents, reveals that India imports C. wightii oleo-resin only from Pakistan (but under several different mostly incorrect HS Codes). Table 2 quantifies India’s 2014 imports of C. wightii oleo-resin at 504.6 tonnes, entirely from Pakistan, which corroborates the Ved & Goraya's (2008) conclusion the Indian herbal industry demand is at least 500 tonnes annually with most of this imported from Pakistan.

Table 2 India 2014 imports of guggal

HS Code Description Origin Country

Port of Discharge

Quantity (kg)

Value (INR)

12119049 Herbs – Guggal (each bag NT WT. 50~65 kg)

Pakistan Nhava Sheva Sea

34,300 1,360,233

12119099 Guggal (Commiphora mukul) Pakistan Nhava Sheva Sea

32,540 2,013,855

13019029 Guggal Pakistan Nhava Sheva Sea

59,950 3,096,736

13019031 Pakistan Gum Guggal Part of Plants Pakistan Chennai Sea 2,100 1,213,788

13019039 Guggal (Commiphora wightii (Arn.)/mukul)

Pakistan Nhava Sheva Sea and Tughlakabad

325,055 13,828,697.33

13019049 Guggal Pakistan Nhava Sheva Sea

50,640 3,458,651

India 2014 imports 504,585 24,971,960.33

Source: Zauba Technologies & Data Services Pvt Ltd., 2015

Table 3 provides estimated apparent consumption in India of 286.155 tonnes based on 2014 imports from Pakistan, 2013 collection in Gujarat, and 2014 Indian exports. The calculation does not take into account quantities from controlled cultivation in India. Table 3 Apparent consumption of guggul gum in India Source: Elaboration on data presented in Tables 1 to 6

Collection in Gujarat 1.6 tonnes Imported from Pakistan 504.585 tonnes Exported by India – gum resin 27.504 tonnes

8

Exported by India- extracts [27.504 tonnes] 192.526 tonnes (estimated crude gum equivalent based on average DER of 7:1 (w/w)

Apparent consumption (not including significant unknown quantities used domestically as component of Ayurveda Siddha, and Unani formulations and products)

286.155 tonnes

Domestic consumption of C. wightii oleo-resin in Pakistan was estimated at 18.5 tonnes in 1978 (Williams & Ahmad, 1999), up to between 25 – 50 tonnes in 2000 (Sheikh, et al., 2000). Recent export trade data now shows Pakistan exporting over 500 tonnes to India in 2014 (see Table 2). Commiphora wightii oleo-resin is used domestically for medicinal purposes, but exploitation for export from Pakistan and India and the international export trade is also significant.

There is insufficient data available to quantify the level of illegal trade, which still needs clarification for both Pakistan and India. Ahmed et al. (2013) reported on governmental enforcement against illegal tapping of C. wightii in the Nagarparkar Hills of Tharparkar, Pakistan, but no information on the specific regulations were cited. In India, the export of C. wightii oleo-resin, its derivatives and extracts, if obtained from wild populations, has been banned since 1994 (Ministry of Commerce, Government of India, 1994). Despite this, it is possible that export of wild-collected C. wightii products of Indian origin may still be continuing. Although not specific to C. wightii, the extent of illegal wild collection and illegal export trade in India is reportedly high (Subrat, et al., 2002).

3.6.2 International export trade

Indian extraction houses and contract packagers process and value-add to C. wightii oleo-resin produced nationally or imported from Pakistan. This is then exported in the forms of bulk extracts as well as finished products in dosage form (capsules, tablets). Table 4 shows India’s 2014 exports (mainly with incorrect HS Codes used) of C. wightii oleo-resin.

Table 4 India 2014 exports of guggal/guggul/guggulu Source: Zauba Technologies & Data Services Pvt Ltd.

HS Code Description Destination Quantity

(kg) Value (INR)

12119091 Herbs: Commiphora mukul (gum) Hungary 6 10,570

12119099 Commiphora mukul France, Kuwait 700 1,120,731

13019039 Crude herbs, Guggal, Commiphora mukul

Germany, Pakistan, Nepal

6,450 768,159

13019042 Guggal (Balsamodendron mukul) UAE 1500 88,370

13021918 Guggul powder (Ayurvedic herbal powders)

Romania 130 88,920

13021990 Ayurvedic herbal powder: Guggul Romania 305 223,862

14049090 Herbal items: Guggal powder UK 29 49,206

30049079 Guggul powder Romania 15 7,182

33079090 Guggul for prayer South Africa 60 21,187

38256100 Certified organic guggulu powder Germany 30 26,702

2014 GUGGUL GUM EXPORTS: 9,225 2,404,889

Table 5 shows that 2014 exports of various C. wightii oleo-resin extracts amounted to 27.502 tonnes. “Guggul native extract” has an approximate 9:1 drug-to-extract ratio (DER) (United States Pharmacopeial Convention, 2015) but there are also commercial extracts that are normalized or standardized down to an approximate 5:1 DER. Using an average of 7:1 (w/w),

9

the 27.502 tonnes of exported extracts would be approximately equivalent to 192,526 kg crude gum resin.

Table 5 India 2014 exports of guggul extracts Source: Zauba Technologies & Data Services Pvt Ltd.

HS Code Description Destination Quantity

(kg) Value (INR)

09109990 Guggul Extract 2.5% guggulsterones

Canada 15 31,135

13019039 Guggul gum extracts France, US, Indonesia, 4,158 12,638,411

13021911 Certified organic guggul extract, 2.5-3% guggulsterones

US 1 4,429

13021918 Commiphora extract (Guggul)

Spain, US 100 267,118

13021919 Indian origin guggul powder extract, 2.5% guggulsterone

US 50 206,251

13021919

Guggul extracts (Commiphora mukul); various different strengths and standardizations

US, Canada, Singapore, Italy, New Zealand, France, Costa Rica, Japan, Brazil, Netherlands, Malaysia, Slovakia, Finland, Germany, Indonesia, South Africa, Spain, Austria, Czech Republic, Netherlands

22,500 48,407,499

13021920 Certified organic guggul extract 3% guggulsterones Z&E

US 250 968,083

13021990 Guggul (Commiphora mukul) gum resin extract 3~5 : 1 (w/w)

Netherlands, Japan, UK, Romania, US 331 938,240

13023900 Guggul (Commiphora mukul) extract, 2.5% guggulsterones

Malaysia, Croatia 35 128,663

33012941 Certified organic Guggul extract

US 25 85,026

33019090 Guggulu CO2 extract US 26 113,238

33049190 Alcohol-free guggul (Commiphora mukul) perfumery compound

Czech Republic, Saudi Arabia 13 39,312

2014 GUGGUL EXTRACT EXPORTS:

27,504 63,827,405

Table 6 shows the export quantities of complex mixtures or formulations and products that contain guggul as one component. For these goods, the quantity of guggul cannot be quantified as the amounts used in the formulations are not known and the export units are, for example, quantified by pieces (PCS), bottles (BTL), packages (PAC), numbers (NOS), and boxes (BOX).

Table 6 India 2014 exports of formulations/products that contain guggul Source: Zauba Technologies & Data Services Pvt Ltd.

HS Code Description Destination Unit Quantity Value (INR)

10

12119099

Bulk certified organic medicinal herb mixes containing guggul with other herbs

USA, UK, Canada, Netherlands KG 2163 8,509,344

12119099

Herbal extracts & formulations containing guggul with other herbs (capsules or tablets)

Macedonia BTL 660 240,977

12119099 Shuddha Guggulu (C. mukul) 500 mg capsules

Germany PCS 22,000 73,810

20098990 Herbal products containing guggul

Canada, USA PCS 2950 185,472

21069099 Herbal products containing guggul

USA, Canada, France, Netherlands, UK, Sweden

BTL,CTN, NOS, PCS

4,635 693,894

30033900 Herbal products containing guggul

USA, Hungary, Ukraine, Bulgaria, Netherlands, Australia,

PCS, PAC 3914 1,050,415

30039011 Ayurvedic medicines containing guggul

Nepal, Finland, Germany, Kyrgyzstan, Lithuania, Kenya, Denmark, USA, Mauritius, Netherlands, New Zealand, Malta, Romania, Philippines, Singapore, Peru

NOS, PCS BTL, BOX

61,114 4,489,426

30039090 Herbal products containing guggul

Czech Republic, Peru, Mauritius, Singapore, Russia,

PCS, NOS 403 26,217

30044090 Ayurvedic medicines containing guggul

Tanzania, Malaysia PAC 1809 90,578

30045090 Lookman-E-Hayat Tel (97% sesame oil, 3% guggul)

South Africa, Zambia NOS 186 8,419

30049011

Ayurvedic medicines containing guggul (capsules, tablets, churnam)

Nepal, Sri Lanka, USA, UK, Malaysia, New Zealand, Mauritius, Guatemala, Romania, Malta, Poland, Latvia, Bulgaria, Russia, Finland, Netherlands, Belgium, Kazakhstan, France, Czech Republic, Canada, Kuwait, Fiji, Seychelles, Singapore,

BTL,CTN, NOS, PCS TBS,BOX, PAC,

178,600 16,929,804

30049029 Ayurvedic medicines containing guggul

USA, South Africa, Australia, New Zealand

PCS, NOS 4,160 255,553

30049099 Ayurvedic herbal preparations containing guggul

Belgium, Bulgaria, USA, Ghana, Mauritius, Tanzania, Zambia, New Zealand, Ukraine,

PCS, NOS PAC

5,880 799,810

33049910 Guggulu Vati Dietary Supplement

France NOS 10 2,957

33049990 Dietary Supplements

USA, Mauritius, Afghanistan, Canada

PCS 2406 219,108

11

containing guggul

33051090 Shuddha Guggulu capsules (60S)

Malaysia NOS 50 3,065

33073090 Food supplements containing guggul (capseuls)

Malaysia NOS 50 3,065

33074100 Incense containing guggul

Nepal, Mauritius, Canada, Trinidad & Tobago, UK, Australia

DOZ, PCS, CTN, KG,

1,832 340,073

33074900 Incense containing guggul

Nepal, Netherlands, USA, PAC, PCS, KG

1846 168,908

33079090 Herbal products that contain guggul

Czech Republic PCS 54 6,416

Table 7 shows the various HS Codes used by Indian exporters in 2014 for various articles of commerce that contain C. wightii (C. mukul) in various forms. The Indian Trade Classification (ITC) definitions are provided as well as the actual shipment descriptions that were used by the exporters, which clearly illustrates that incorrect HS Codes are often used by exporters.

Table 7 HS Codes used in 2014 for shipments exported by Indian companies described as containing C. mukul, C. wightii, guggal, guggul, or guggulu

Sources: (1) Govt. of India Department of Commerce EXPORT IMPORT DATA BANK Version 7.2 – TRADESTAT; and (2) Zauba Technologies & Data Services Pvt Ltd: https://www.zauba.com/

HS Code ITC Definition of HS Code Actual Shipment Description(s) from Zauba.com

Main Destination(s)

12119091 Chirata (Swertia chirayita) HERBS: COMMIPHORA MUKUL (GUM)

Hungary

12119099

Other plants and parts of plants used in perfumery, pharmacy, insecticidal / fungicidal purposes, fresh or dried

100% ORGANIC MEDICINAL HERBS & SPICES: 100% ORGANIC GUGGAL (KAISHORE GUGGULU) POWDER

USA

100% ORGANIC MEDICINAL HERBS: 100% ORGANIC GUGGAL (COMMIPHORA MUKUL) WHOLE

UK

100% ORGANIC MEDICINAL HERBS: SIMHANAD GUGGAL

UK

HERBAL EXTRACTS & FORMULATION: KANCHNAAR GUGGUL

Macedonia

INDIAN HERB: COMMIPHORA MUKUL

Kuwait

ORGANIC MEDICINAL HERBS: 100% ORGANIC THRIPHALA GUGGULU (COMMIPHORA MUKUL)

Canada

13019039 Other natural gum resins

COMMIPHORA MUKUL Germany COMMIPHORA MUKUL EXTRACT (GUGGUL GUM)

France

CRUDE HERBS: GUGGAL Pakistan POWDERED HERBAL EXTRACTS: GUGGUL EXTRACT (2.5% Guggulsterones)

Indonesia, USA

12

13019042 Oleoresins of fruits GUGGAL/BALASA MODERAN UAE

13021918 Gamboge gum-resin (Garcinia hanburyi) extract

COMMIPHORA EXTRACT (GUGGUL)

Spain

GUGGUL POWDER (AYURVEDIC HERBAL POWDERS)

Romania

13021919 Other extracts HERBAL EXTRACT: COMMIPHORA MUKUL EXTRACT

Brazil, Canada, Czech Republic, France, Germany, Italy, Japan, Netherlands, New Zealand, Singapore, Slovakia, South Africa, Spain, UK, USA

13021920 Cashew (Anacardium occidentale) Shell Liquid (CNSL)

HERBAL EXTRACT: Organic Guggul extract (3% Guggulsterones)

USA

13021990 Other extracts, derived from vegetable products

AYURVEDIC HERBAL POWDER: GUGGUL POWDER

Romania

GUGGUL EXTRACT 4:1 (5-10% GUGGULSTERONES)

UK

COMMIPHORA MUKUL DRY EXTRACT (GUGGUL)

USA

13023900

Other mucilages and thickeners, whether or not modified, derived from vegetable products

COMMIPHORA MUKUL (DP) (GUGGUL E&Z)

Malaysia

14049090 Other vegetable materials not elsewhere specified (nes)

HERBAL ITEMS: GUGGAL POWDER

UK

20098990 Other fruit juice HERBAL PRODUCTS: GOKSHRADI GUGGUL

Canada, USA

21069099 Other food preparations, not elsewhere specified (nes)

FOOD SUPPLEMENT: KACHANA GUGGAL 60 Tablets

Sweden

HERBAL SUPPLEMENT: (POWDER) GUGGUL POWDER. COMMIPHORA MUKUL POWDER

Canada, France, Netherlands, USA

POWDERED HERBS & MASSAGE OIL, PURE GUGGUL POWDER

USA

30033900

Other medicaments containing hormones or other product of heading 2937 excluding antibiotics

HERBAL PRODUCT: GUGGUL CAPSULE or GUGGUL CHURNA

Australia, Bulgaria, Hungary, Netherlands, Peru, Ukraine, USA

30039011 Medicaments of Ayurvedic System, not put up in measured doses or packed for retail sale

Ayurvedic Guggul (Capsules or Tablets)

Australia, Denmark, Finland, Kenya, Lithuania, Malta, Nepal, Netherlands, New Zealand, Philippines, Singapore, USA

30039090 Other medicaments not put up in measured doses or in packing for retail

TRIFLA GUGGULU Russia

30044090 Formulations of other vegetable alkaloids and its derivatives

MEDICINES: ZANDU KISHORE GUGGUL (AYURVEDIC) or SHUDDHA GUGGULU Capsules

Malaysia, Tanzania

30049011 Medicaments of Ayurvedic System, put up in measured

Ayurvedic Medicines: Guggul (Capsules or Tablets)

Bulgaria, Canada, Finland, Latvia, Kazakhstan,

13

doses or packed for retail sale / Commiphora wightii (Shuddha Guggulu) Capsules

Malaysia, Nepal, Netherlands, Poland, Sri Lanka, Russia, UK, USA

30049029 Other anthelmintic drugs, antiamoebic and other antiprotozoal / antifungal drugs

AYURVEDIC MEDICINES: YOGARAJ GUGGUL (ZAN) TABLETS

New Zealand, South Africa

30049099 Other medicines put up for retail sale, not elsewhere specified (nes)

PROCESSED INDIAN HERBS AS HERBALS SUPPLEMENTS: KISHORE GUGGUL SPL TABLETS

Belgium

AYURVEDIC HERBAL PREPARATION: TRIPHLA GUGGUL

Ghana

HERBAL SUPPLEMENT: GUGGUL COMMIPHORA MUKUL TABLET

USA

PHARMA PRODUCT: SHUDDHA GUGGULU CAPSULE

Tanzania

33019090

Other concentrates of essential oils in fats, fixed oils, waxes or the like, Terpenic byproducts of deterpenation of essential oils, aqueous distillates and aqueous solutions of essential oils

GUGGULU CO2 EXTRACT USA

33049190 Other (beauty, make-up or skincare) powders, whether or not compressed

HERBALS PRODUCT ITEMS: GUGGUL (COMMPHURA MUKUL)

Czech Republic

PERFUMERY COMPOUND FREE FROM ALCOHOL: MUBARAK (GUGGAL) FOR BUKHUR

Saudi Arabia

33049910 Face creams (excluding turmeric)

HERBAL SUPPLEMENT: GUGGUL VATI

France

33049990 Other beauty or make-up preparations and preparations for the care of the skin

HERBAL DIETARY SUPPLEMENT: PUNERNAVADI GUGGULU 90 VEGETARIAN CAPSULES

USA

33074100 “AGARBATTI" and other odoriferous preparations which operate by burning

GUGGAL (50 GM PKT) Australia, Canada, Nepal, USA

33074900 Other odoriferous preparations used for deodorizing room (excluding agarbatti)

PUJA GUGGAL (for burning) USA HERBAL PRODUCTS: HIMALAYA SUDDHA GUGGUL TABLETS

Czech Republic

4.0 Discussion

Wild harvest is the main source of C. wightii oleo-resin and destructive tapping and oleo-resin extraction methods have had a devastating effect on wild C. wightii populations. Consequently, C. wightii oleo-resin production has declined in India over a 50 year period. Clearly, a range of strategies is required to manage wild C. wightii populations. These range from a ban on tapping C. wightii in Rajasthan (Samanta & Mandal, 2014) to community-based conservation in both India (Soni, 2010) and Pakistan (Ahmed, et al., 2013) and more formal in situ and ex situ conservation initiatives.

14

4.1 Commerce, conservation and conflicting approaches

It is clear from our review that while the Government of India has tried to ban C. wightii exports, the problem has shifted on to neighbouring Pakistan where wild stocks are also over-exploited for export on C. wightii oleo-resins to India. Over twenty years ago, the Ministry of Commerce, Government of India banned the export of C. wightii oleo-resin, its derivatives and extracts if obtained from the wild (Ministry of Commerce, Government of India, 1994), placing it on the ‘negative list’ for exports (Ministry of Commerce, Government of India, 2005). At the same time, Schedule I of India’s Import Policy states that the import of crude drugs, including guggulu (C. wightii oleo-resin), that are needed for the manufacture of Ayurvedic or Unani medicine, is permitted freely (Ministry of Commerce & Industry, Government of India, 2012). Goods on the ‘negative list’ for export such as C. wightii oleo-resin may be imported for value-adding and re-export. There is no evidence of a similar export ban in Pakistan for C. wightii obtained from the wild. In India, the main national supply of C. wightii oleo-resin is from the State of Gujarat, with marketing through state-controlled Gujarat State Forest Development Corporation Ltd (GFDCL) (Mandal, et al., 2011).

Due to over-exploitation, C. wightii is one of the top 40 conservation priority species in India (Bhattacharyya, et al., 2006) and India is no longer self-sufficient in C. wightii oleo-resin. The situation in Gujarat illustrates this point. In 1963, the local Forest Department collected 30 tons of gum-resin, with only 2.42 tons were collected in 1999 (Dixit & Rao, 2000), with just to 1.6 tonnes collected in Gujarat in 2013 (Yogi, et al., 2014). Over this same period, demand has increased. The global increase in obesity levels (Ng, et al., 2014), including a rapid rise in Asia (Ramachandran & Snehalatha, 2010) may be one driver of increased demand, due to use of guggulsterone containing products from C. wightii to treat obesity and high levels of blood cholesterol (González-Castejón & Rodríguez-Casado, 2011). Whatever the drivers of demand, declining national C. wightii populations stocks means that India is reliant on importing C. wightii oleo-resin from neighbouring Pakistan. Based on our analyses of trade data, India imported nearly 505 tonnes of Pakistan, while producing a fraction of this (Table 3). Based on the same set of trade data from Tables 2-7, India exports more C. wightii oleo-resin that it produces, particularly as extracts, which based on an average drug-to-extract ratio (DER) of 7:1 (w/w), would equate to an estimated crude C. wightii oleo-resin equivalent of 192.5 tonnes. An additional 27.5 tonnes are exported as unprocessed (“crude”) C. wightii oleo-resin. National consumption of C. wightii oleo-resin is high in India. Even if the presumably large quantities used domestically in Ayurvedic, Siddha and Unani formulations and products are excluded, as these are very difficult to quantify, we estimate that C. wightii oleo-resin consumption is at least 286.2 tonnes per year (Table 3).

Risks associated with unsustainable harvest and declining production are not just an environmental conservation issue. It is not uncommon for substitution to take place, with decline in active ingredients at best and potential associated health risks in a worst-case situation. Adulteration with resins from other species and “look-alike” problems are common. For example, a study on frankincense (gum olibanum) samples collected from markets in China showed that out of 50 commercial samples, 27 were official frankincense and 23 were fake (Zhong, et al., 2012). We are not aware of any similar comparative studies on what is being sold as C. wightii oleo-resin or extracts, but suggest there is a need for these comparative analyses.

4.2 What role is cultivation playing in C. wightii conservation?

There are some major initiatives to plant C. wightii using cuttings taken from wild trees in India and Pakistan. Some cultivation initiatives in India date back over 40 years. In Rajasthan, for example, the Regional Research Ayurveda Institute, Jaipur, started a Guggul Herbal Farm at Mangliawas (Ajmer) (Bhatt & Dixit, 1974). More recently, the Rajasthan government has started a project that aims to have 1,700 ha of C. wightii under cultivation, aiming to raise about 500,000 C. wightii saplings for distribution to nurseries in 32 districts in Rajasthan. And in the Kuchchh area

15

of Gujarat, the Indian National Medicinal Plants Board (New Delhi) initiated a C. wightii cultivation project in 500 to 800 ha area (Kulhari, et al., 2014). In India, the Central Institute of Medicinal and Aromatic Plants (CIMAP) has also developed a cultivar named ‘marusudha’ (National Medicinal Plants Board, 2008). In view of better vigor and survival in native sites in western Rajasthan’s bioclimatic conditions, ex-situ and in-situ conservation are likely to be more successful in the districts of Jaisalmer, Barmer, Jalore and Jodhpur than in other areas (Kulloli, et al., 2013a). Using Ecological Niche Modelling (MAXENT Algorithm), Kulloli & Kumar (2014b) have determined the best potential areas for the reintroduction of C. wightii (Kulloli & Kumar, 2014b).

Proliferation using tissue culture has also been demonstrated. Kulhari et al. (2014) also recommend ex situ conservation strategies, including micro-propagation of genotypes with high guggulsterone levels. Ex-situ and in-situ conservation of C. wightii has been recommended for specific locations in Barmer, Jaisalmer and Jodhpur of Rajasthan, India (Kulloli, et al., 2013a). This is also supported by higher amount of E and Z guggulsterone in plants from Bikaner and Jodhpur (247 - 257 µ/g) in arid western Rajasthan compared to those from southwest Rajasthan (135 - 166 µ/g) (Kulhari et. al, 2012). C. wightii in the Jaisalmer, Barmer and Jodhpur area have more E and Z guggulsterones, a desirable trait in this species (Kulloli, et al., 2013a) as these are potent active ingredients in C. wightii oleo-resin (Meselhy, 2003). For its ex-situ conservation, the density of trees in plantations should preferably be kept low (100 - 400/ha). Since it is open to invasion by shrubby weeds like Prosopis juliflora (Dixit & Rao, 2000) regular monitoring of weedy species is essential so as to check their spread through removal, if required (Kulloli, et al., 2013a). A recent study by Kulloli et al. (2015) was carried out to investigate appropriate season and treatments for C. wightii production from cuttings. In Rajasthan, India, for example 3,500 three-month old plantlets (each about 30 cm tall) were then transferred and planted in the Aravali hills at a site near Gulta (Jaipur district) with the help of local communities (Soni, 2010). Planting has also been implemented on a similar scale in Pakistan, with similar sized 4,250 rooted cutting planted in rangeland sites in Sind with the participation of local people and community-based “Green Guard’s” (Ahmed, et al., 2013). We support these developments and recommend the establishment of value chains that provide options for added values of cultivated material. Although experimental cultivation using cuttings in some locations (such as Madhya Pradesh), this is hampered by termite attack on the cuttings (A.B-C, personal observation, 2008). Challenges facing planting from cuttings need to be addressed if a shift from wild harvest to cultivation is to occur in the future.

4.3 Community-based management and planting of C. wightii

Achieving successful, community-based forest management is challenging anywhere and South Asia is no exception. Joint Forest Management (JFM) in India is a good example, where despite decades of donor support, conflicts still occur (Ballabh, et al., 2012). Despite this, community-based forest management still holds promise (Conroy, et al., 2002). In Rajasthan, India, the focus of community-based conservation work is through the “Guggal Bachao Abhiyan” (Save Guggal Movement) that includes conservation education and a planting programme. Similarly in Pakistan, planting of C. wightii has been implemented, with similar sized 4,250 rooted cutting planted in rangeland sites in Sind with the participation of local people and community-based “Green Guard’s” (Ahmed, et al., 2013). In common with any conservation, strong tenure over land and resources, avoidance of “elite capture” and adequate returns to local communities all play a key role. According to Kulhari et al. (2014), the National Herbal Farm Mangliawas, Ajmer, Rajasthan have tried to conserve C. wightii but despite this, “are not satisfactory in view of the increasing demand of the raw drugs and to cope up with the rapid denudation of the forests and depletion of the species”. So if cultivation is to meet market demand, then it has to successfully expand to avoid a situation where demand exceeds supply.

16

5.0 Conclusions

India exports more C. wightii oleo-resin that it produces, particularly as extracts. In essence, a long history of over-exploitation in India coupled to a ban exports from India has transferred the problem to Pakistan, with gum gugul imports from Pakistan to India now filling the supply gap. Improved monitoring of international trade on a species basis can be a useful conservation tool and will overcome the current difficulties in trade data analysis. But encourage the current shift to cultivated sources of supply, it would also be useful to develop traceable supply chains for C. wightii oleo-resin from cultivated stocks, so that producers are not disadvantaged by CITES App. II monitoring requirements for wild harvested C. wightii oleo-resins. Based on the evidence presented in this review, it is suggested that C. wightii fulfills the criteria for inclusion on CITES Appendix II based on Art. IV 2(a). Wild C. wightii populations have been fragmented by habitat loss through clearing for farming. Remaining populations are in decline due to destructive commercial exploitation for the international oleo-resin trade (Parmar, 2003; Rajendrakumar, 2013; Reddy, et al., 2012). Over a decade ago, Parmar (2003) considered that the wild C. wightii population in India had declined to less than 50% of its original size, leaving isolated subpopulations (Parmar, 2003). More recently, in a CAMP (Conservation Assessment and Management Plan) report (September 2007) for Rajasthan, C. wightii was assessed as Critically Endangered for the state of Rajasthan (with an estimated decline of more than 80% in its wild populations over a three generation time period i.e. 50 - 60 years) (D.K. Ved., pers. comm., 2015). Over-exploitation is compounded by poor seed set, very poor seed germination (5%) with arid conditions often resulting in recruitment failure in wild populations. Young plants are rarely seen under the adult plants (Yadav, et al. 1999, cited by Kulloli & Kumar, 2013, and Reddy, et al., 2012), not only due to low germination rates, but also due to grazing by livestock (Dixit & Rao, 2000). In March 2015, the Government of India’s Minister of State, Ministry of Ayurveda, Yoga & Naturopathy, Unani, Siddha & Homoeopathy (AYUSH), expressed concerns about C. wightii (Naik, 2015). In addition, the status of C. wightii has been changed from Data Deficient (DD) to Critically Endangered (CE) on the IUCN Red List (Ved, et al., 2015). Rising scarcity of C. wightii oleo-resin is the likely cause of increasing oleo-resin prices, with over 95% of India’s 500 - 600 tons/year industrial requirement for C. wightii oleo-resin being imported into India from Pakistan (Planning Commission, 2000).

Acknowledgements

Support from the Bundesamt für Naturschutz (BfN) that enabled us to review the conservation and trade situation facing C. wightii with regard to possible CITES Appendix II listing based on Art. IV 2(a) is gratefully acknowledged. RNK would also like to thank his research supervisor, Dr. Suresh Kumar for his support.

Authors contributions

A. B (Tony) Cunningham, Josef Brinckmann and Uwe Schippmann planned the review, which was written by Tony Cunningham and Josef Brinckmann, with Ravikiran Kulloli adding to the review on the basis on his fieldwork on C. wightii in India. Trade data were collected by Josef Brinckmann. The photographs in Figure 1 were taken by Ravikiran Kulloli.

References

Ahmed, A. et al., 2013. Combating Desertification Effects by Participatory Action and In-situ Conservation of Commiphora wightii: An Endangered Medicinal Shrub in Nagarparkar Hills of Tharparkar, Pakistan. Advances inEnvironmental Biology, 7(13), pp. 4039-4045.

17

Antonio, J. et al., 1999. Effects of a standardized guggulsterone phosphate supplement on body composition in overweight adults: A pilot study. Current Therapeutic Research, 60(5), pp. 220-227.

Arya, R., Nirwan, B. & Meena, K., 2011. Ethephon based gum tapping technique for sustainable gum harvesting from Guggul (Commiphora wightii (Arn.) Bhandari) in arid Rajasthan. Gandhinaga, s.n.

Atal, C., Gupta, O. & Afaq, S., 1975. Commiphora mukul: source of guggal in Indian systems of medicine. Economic Botany, 29(3), pp. 209-218.

Ballabh, V., Balooni, K. & Dave, S., 2012. Why local resources management institutions decline: A comparative analysis of Van (Forest) Panchayats and Forest Protection Committees in India. World Development, 30(12), pp. 2153-2167.

Bedevian, A., 1994. Illustrated Polyglottic Dictionary of Plant Names. Cairo: Medbouly Library.

Bhandari, M., 1964. Notes on Indian desert plants 4 - new names and combinations. Bulletin of the Botanical Survey of India, Volume 6, pp. 327-328.

Bhattacharyya, R., Bhattacharya, S. & Chaudhuri, S., 2006. Conservation and documentation of the medicinal plant resources of India. Biodiversity and Conservation, 15(8), p. 2705–2717.

Bhatt, G. & Dixit, R., 1974. A preliminary study on extensive cultivation of guggul at Mangliawas herbal farm, Ajmer, Rajasthan. Journal of Research in Indian Medicine, 9(4), pp. 51-58.

Bhatt, J., Nair, M. & Ram, H., 1989. Enhancement of oleo-gum resin production in C. wightii by improved tapping technique. Current Science, 58(7), pp. 349-357.

Champion, H. & Seth, S., 1968. A revised survey of the forest types of India, Delhi: Government of India.

Chaudhary, G., 2012. Pharmacological properties of Commiphora wightii Arn. Bhandari - an overview. International Journal of Pharmacy and Pharmaceutical Sciences, 4(3), pp. 73-75.

Conroy, C., Mishra, A. & Rai, A., 2002. Learning from self-initiated community forest management in Orissa, India.. 4(3), pp. 227-237.

Dixit, A. & Rao, S., 2000. Observation on distribution and habitat characteristics of Gugal (Commiphora wightii) in the arid region of Kachchh, Gujarat, India. Tropical Ecology, 41(1), pp. 81-88.

Gardner, Z. & McGuffin, M., 2013. American Herbal Products Association’s Botanical Safety Handbook, Second Edition. Boca Raton(Florida): CRC Press.

González-Castejón, M. & Rodríguez-Casado, A., 2011. Dietary Phytochemicals and Their Potential Effects on Obesity: A Review. Pharmacological Research, Volume 64, pp. 438-455.

18

Gupta, P., Shivanna, K. & Mohan Ram, H., 1996. Apomixis and Polyembryony in the Guggul Plant, Commiphora wightii. Annals of Botany, Volume 78, pp. 67-72.

Gupta, P., Shivanna, K. & Mohan Ram, H., 1998. Pollen-pistil Interaction in a Non-pseudogamous Apomict, Commiphora wightii. Annals of Botany, 81(5), pp. 589-594.

India Biodiversity Portal, 2015. Commiphora wightii (Arn.) Bhandari. [Online] Available at: http://indiabiodiversity.org/species/show/226901 [Accessed 2015].

Joshi, P., Joshi, E. & Jain, B., 2012. Ecology and conservation of threatened plants in Tapkeshwari Hill ranges in the Kachchh Island, Gujarat, India. Journal of Threatened Taxa, 4(2), pp. 2390-2397.

Kapoor, L., 1990. Handbook of Ayurvedic Medicinal Plants. Boca Raton: CRC Press.

Krishna-Murthy, T. & Shiva, M., 1977. Salai Guggul from Boswellia serrata Roxb.-its Exploitation and Utilization. The Indian Forester, 103(7), pp. 466-474.

Kulhari, A. et al., 2012. Problems, progress and future prospects of improvement of Commiphora wightii (Arn.) Bhandari, an endangered herbal magic, through modern biotechnological tools: a review. Genetic Resources and Crop Evolution, 59(6), pp. 1223-1254.

Kulhari, A. et al., 2014. Survey, Collection and Conservation of Commiphora wightii (ARN.) Bhandari-an Important Medicinal Plant Heading towards Extinction. Indian Forester, 140(12), pp. 1171-1183.

Kulloli, R. & Kumar, S., 2013. Commiphora wightii (Arnott) Bhandari: A threatened plant of conservation concern. Journal of Medicinal Plants Research, 7(28), pp. 2043-2052.

Kulloli, R. & Kumar, S., 2014a. Commiphora wightii (Arnott.) Bhandari in the Indian Desert: Biology, Distribution and Threat Status. In: D. Nandwani, ed. Sustainable Development and Biodiversity - Issues, Technology and Innovation. s.l.:Springer International Publishing, pp. pp 301-313.

Kulloli, R. & Kumar, S., 2014b. Comparison of Bioclimatic, NDVI and Elevation variables in assessing extent of Commiphora wightii (Arnt.) Bhand. The International Archives of the Photogrammetry, Remote Sensing and Spatial Information Sciences, Volume XL-8, pp. 589-595.

Kulloli, R., Kumar, S. & Jindal, S., 2013b. Ex-situ Conservation of an Arid Threatened Species Commiphora wightii (Arnt.) Bhand. Through Seeds. Journal of Tropical Forestry, 29(6), pp. 15-22.

Kulloli, R. et al., 2013a. Distribution of Commiphora wightii in Rajasthan with Special Emphasis on Its Conservation Planning in Arid Areas. Vegetos, 26(SP), pp. 113-120.

Lal, H. & Kasera, P., 2010. Status and distribution range of guggal: a critically endangered medicinal plant from the Indian Thar Desert. Science & Culture, 76(11–12), p. 531–533.

19

Mandal, K., Samanta, J., Maiti, S. & Kamboj, R., 2011. Myths and facts of guggal gum tapping. The Indian Forester, 137(11), p. 1346–1347.

Meselhy, M., 2003. Inhibition of LPS-induced NO production by the oleogum resin of Commiphora wightii and its constituents. Phytochemistry, 62(2), pp. 213-218.

Ministry of Commerce & Industry, Government of India, 2012. ITC (HS), 2012, Schedule 1 – Import Policy. [Online] Available at: http://dgft.gov.in/Exim/2000/NOT/itc(hs)/ch12.pdf [Accessed 29 August 2015].

Ministry of Commerce, Government of India, 1994. PUBLIC NOTICE No. 47 (PN)/92-97. New Delhi: Ministry of Commerce.

Ministry of Commerce, Government of India, 2005. PUBLIC NOTICE NO. 47 (RE-2005) /2004-2009. [Online] Available at: http://dgft.gov.in/exim/2000/pn/pn05%5Cpn4705.htm [Accessed 29 August 2015].

Mosti, S., Raffaelli, M. & Tardelli, M., 2012. to the Flora of Central-Southern Dhofar (Sultanate of Oman). Webbia, 67(1), pp. 65-91.

Nadkarni, K., 1954. Indian Materia Medica. Bombay: Popular Prakashan.

Naik, S., 2015. Availability of Medicinal and Aromatic Plants/Herbs, New Delhi: Press Information Bureau.

National Medicinal Plants Board, 2008. Agro-techniques of selected medicinal plants. New Delhi: The Energy and Resources Institute Press.

National Medicinal Plants Board, n.d. Agro Climatic Zones. [Online] Available at: http://www.nmpb.nic.in/searchdetails.php?lid=311&skey=agro [Accessed 28 August 2015].

Ng, M. et al., 2014. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the Global Burden of Disease Study 2013. The Lancet, 384(9945), pp. 766 - 781.

Parmar, P., 2003. Loss of Commiphora wightii (Arn.) Bhandari in Indian Desert. Bulletin of the Botanical Survey of India, Volume 45, pp. 77-90.

Patil, V., Nayek, U. & Dev, S., 1972. Chemistry of Ayurvedic crude drugs. I. Guggulu (resin from Commiphora mukul). 1. Steroidal constituents. Tetrahedron, 28(2), pp. 2341-2352.

Planning Commission, 2000. Report of Task Force on Conservation and Sustainable use of Medicinal Plants, New Delhi: Planning Commnission, Government of India.

Rabinowitz, D., Cairns, S. & Dillon, T., 1986. Seven forms of rarity and their frequency in flora of the British Isles. In: M. Soule, ed. Conservation Biology, the Science and Scarcity of Diversity. Sunderland, Massachusetts: Sinauer, p. 182–204.

20

Rajendrakumar, S., 2013. Distribution and abundance of Commiphora wightii (Arn) Bhandari, in the forest of north Gujarat region (NGR), Gujarat, India. Indian Journal of Plant Sciences, 2(1), pp. 43-51.

Ramachandran, A. & Snehalatha, C., 2010. Rising Burden of Obesity in Asia. Journal of Obesity, Volume 2010, Article ID 868573, 8 pages.

Reddy, C. et al., 2012. Conservation threat assessment of Commiphora wightii (Arn.) Bhandari—an economically important species. Taiwania, 57(3), pp. 288-293.

Samanta, J. & Mandal, K., 2014. Scientific analysis of indigenous techniques for guggal (Commiphora wightii) tapping in India. Journal of Forestry Research, 25(3), p. 695−700.

Samanta, J. & Mandal, K., 2014. Scientific analysis of indigenous techniques for guggal (Commiphora wightii) tapping in India. Journal of Forestry Research, 25(3), p. 695−700.

Samantaray, S., Bishoyi, A., Geetha, K. & Satyabrata, M., 2011. Assessment of genetic diversity using RAPD and ISSR markers in guggul (Commiphora wightii). Journal of Medicinal and Aromatic Plants.

Sharma, B. et al., 2009. Effects of guggulsterone isolated from Commiphora mukul in high fat diet induced diabetic rats. Food Chem Toxicol, 47(10), pp. 2631-2639.

Sharma, S. et al., 1983. A clinical assessment of Commiphora mukul (juggulu) and Inula racemosa (pushkarmoola) for the treatment of coronary heart disease (hridroga). Journal of the National Integrated Medical Association, 25(12), pp. 384-393.

Sharma, S. & Kumar, A., 2012. Traditional uses of herbal medicinal plants of Rajasthan: Guggal. International Journal of Life Sciences and Pharma Reserch, 2(4), pp. 77-82.

Sheikh, A. et al., 2000. Pakistan - First National Report on the Implementation of the Convention on Biological Diversity, s.l.: United Nations, FAO, UNEP, UNESCO.

Sher, H., Aldosari, A., Ali, A. & de Boer, H., 2014. Economic benefits of high value medicinal plants to Pakistani communities: an analysis of current practice and potential. Journal of Ethnobiology and Ethnomedicine, 10(71).

Soni, V., 2010. Conservation of Commiphora wightii an endangered medicinal shrub, through propagation planting, and education awareness program in the Aravali Hills of Rajasthan, India. Conservation Evidence, Volume 7, pp. 27-31.

Soni, V. & Swarnkar, P. L., 2006. Commiphora wightii. An important medicinal plant species. Medicinal Plant Conservation, Volume 12, pp. 40-42.

Subrat, N., Iyer, M. & Prasad, R., 2002. The ayurvedic medicine industry: Current status and sustainability, New Delhi: Ecotech Services (India) Private Ltd..

The Plant List, 2013. Commiphora wightii (Arn.) Bhandari. [Online] Available at: http://www.theplantlist.org/tpl1.1/record/kew-2733729 [Accessed 24 August 2015].

21

Tropicos.org. Missouri Botanical Garden, n.d. Commiphora wightii (Arn.) Bhandari. [Online] Available at: http://www.tropicos.org/Name/50313440?projectid=32 [Accessed 28 August 2015].

United States Pharmacopeial Convention, 2015. United States Pharmacopeia, Thirty-Eighth Revision. 38 ed. Rockville(Maryland): United States Pharmacopeial Convention.

USDA, ARS, National Genetic Resources Program, n.d. Commiphora wightii (Arn.) Bhandari. [Online] Available at: http://www.ars-grin.gov/cgi-bin/npgs/html/taxon.pl?406462 [Accessed 24 August 2015].

Ved, D. & Goraya, G., 2008. Demand and Supply of Medicinal Plants in India. Dehra Dun: Bishen Singh Mahendra Pal Singh.

Ved, D., Saha, D., Ravikumar, K. & Haridasan, K., 2015. Commiphora wightii. [Online] Available at: http://www.iucnredlist.org/details/full/31231/0 [Accessed 26 July 2015].

Williams, J. & Ahmad, Z., 1999. Priorities for Medicinal Plants Research and Development in Pakistan, New Delhi: International Development Research Centre.

Yogi, R., Bhattacharya, A. & Jaiswal, A., 2014. Lac, Plant Resins and Gums Statistics at a Glance 2013. Bulletin (Technical) No. 06/2014, Namkum, Ranchi: ICAR-Indian Institute of Natural Resins and Gums.

Zauba Technologies & Data Services Pvt. Ltd., n.d. Search Import Export Data of India. [Online] Available at: https://www.zauba.com/.[Accessed 19 8 2015].

Zhong, M., Rao, W. & Xiao, C., 2012. Study on determination methods and investigate on the commercial samples for Olibanum. The Chinese Journal of Modern Applied Pharmacy, Issue 5, pp. 409-414.