Abstract
The insect-pathogenic fungus Ophiocordyceps sinensis (better known as Cordyceps sinensis) is harvested over much of the Himalayan plateau as a highly prized remedy in traditional Oriental medicine. Over the past 10 years its financial value has increased dramatically, with collectors paid as much as US $12,500 kg−1 for top-quality material. This is causing significant distortion to local economies, and there is widespread concern that the current rate of collection is unsustainable. This paper introduces the fungus and its insect hosts, documents some of the biological and social constraints to achieving sustainability, describes the socioeconomic climate within which harvest and sale occurs in Bhutan, and details the measures put in place by the Royal Government of Bhutan to promote wise management of this valuable natural resource.
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Introduction
Ophiocordyceps sinensis (better known as Cordyceps sinensis or by its Tibetan name yartsa gunbu) is one of the most highly prized and expensive natural products used in traditional Oriental medicine. It is used as a remedy for a wide range of conditions, especially to aid in building strength and recovery from illness. Several factors over the past 10 years and more have combined to increase demand, including widespread publicity surrounding its use by record-breaking Chinese athletes, health concerns caused by the SARS and bird flu outbreaks in S and SE Asia, and increasing affluence in China, its principal market. In Bhutan O. sinensis was placed on Schedule 1 of the Forest and Nature Conservation Act and its harvest was illegal until 2004 (apart from a small pilot scheme in Lunana from 2002), when a limited collection regime was introduced. Sustainability of its harvest cannot be assured without a full understanding of the fungus, its insect hosts and their inter-relationships, and a monitoring programme to establish baseline population densities. This paper describes the first stages in these processes.
The fungus
Ophiocordyceps sinensis (Fig. 1) is a fungal parasite of larvae (caterpillars) belonging to the ghost moth genus Thitarodes (Hepialidae, Lepidoptera). It has a wide but patchy distribution in montane grasslands of the Tibetan plateau, being recorded from Bhutan (Namgyel and Tshitila 2003), China (Tibet (** fruit-bodies on stroma surface; b stroma of O. sinensis dug out of the ground at Namna, showing stroma develo** from larval cadaver; c stromata of the forest ecotype (O. sinensis?) from the Bumthang Valley, north central Bhutan. Note remains of the cocoon surrounding the larval cadavers, which is cleaned off before sale
The species was first described by Berkeley (1843) as Sphaeria sinensis, from material sent to the UK from markets in Guangdong (Pegler et al. 1994). For many years, it has been referred to as Cordyceps sinensis following its transfer by Saccardo (1878), but recent molecular phylogenetic studies (Sung et al. 2007) have shown that Cordyceps as recognized at that time was polyphyletic, and that C. sinensis is not congeneric with the type species C. militaris. Transfer of the species to Ophiocordyceps, within the newly recognized family Ophiocordycipitaceae was therefore recommended.
There have been some studies that conclude that the Himalayan Cordyceps associated with ghost moths comprise a species aggregate rather than a single species. Zang and Kinjo (1998) list seven species of Cordyceps parasitic on hepialid larvae in the Himalayan region. The diagnostic characteristics cited were based on morphological examination, and it is probable that some at least of these taxa are based on minor morphological traits of limited phylogenetic significance. Following studies of RAPDs by Chen et al. (1999), preliminary molecular studies based on ITS analysis (Stensrud et al. 2007) indicated that several distinct clades may exist within O. sinensis, and the authors speculated that these might represent cryptic species. Our own studies on Ophiocordyceps associated with ghost moth larvae in Bhutan have not yet identified clearly distinct taxa based on morphological analysis, with the exception of a coniferous forest-inhabiting ecotype with unusually large stromata that may be conspecific with collections from China from similar habitats. These have been assigned (almost certainly incorrectly) to the European/Mediterranean species C. gracilis by Zang and Kinjo (1998). A molecular analysis of representative collections from each region of northern Bhutan is under way.
Ophiocordyceps sinensis has an anamorph (asexual stage) referable to Hirsutella, with ascospores germinating directly to produce conidiogenous cells and conidia that probably act as the infective propagules; this has been demonstrated in related species (Hywel-Jones unpublished observation). Despite claims to the contrary (e.g. Pegler et al. 1994; Li et al. 1999) the ascospores of Ophiocordyceps species are aseptate and do not fragment following dispersal in common with true Cordyceps species (Sung et al. 2007). Anamorph-teleomorph connections for this species are highly confused, with no fewer than 22 anamorph names linked to the sexual stage (Jiang and Yao 2002). Many of these are erroneous, and some are likely to have led to the use of misidentified strains in commercial preparations. Misidentifications can also be demonstrated in public sequence databases (Stensrud et al. 2007), some of which are likely to be the result of sequencing rapidly growing contaminating fungi rather than the genuine species. The genuine anamorph of O. sinensis grows very slowly in standard culture conditions, taking 1–2 months to grow to 2–3 mm diameter on standard media (e.g. Potato Dextrose Agar) at 15–20°C (Hywel-Jones unpublished observation).
