Ophiocordyceps sinensis

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Ophiocordyceps sinensis
Cordyceps sinensis.jpg
Ophiocordyceps sinensis (left) growing out of the head of a dead caterpillar
Scientific classification
Kingdom: Fungi
Division: Ascomycota
Class: Sordariomycetes
Order: Hypocreales
Family: Ophiocordycipitaceae
Genus: Ophiocordyceps
Species: O. sinensis
Binomial name
Ophiocordyceps sinensis
(Berk.) G.H.Sung, J.M.Sung, Hywel-Jones & Spatafora (2007)
Synonyms[1]

Sphaeria sinensis Berk. (1843)
Cordyceps sinensis (Berk.) Sacc. (1878)

Ophiocordyceps sinensis is a fungus that parasitizes larvae of ghost moths and produces a fruiting body valued as a herbal remedy. The fungus germinates in the living larva, kills and mummifies it, and then the stalk-like fruiting body emerges from the corpse. It is known in English colloquially as caterpillar fungus, or by its more prominent foreign names (see below): Yartsa Gunbu (Tibetan: དབྱར་རྩྭ་དགུན་འབུ་Wylie: dbyar rtswa dgun 'bu, literally "winter worm, summer grass"), or Dōng chóng xià cǎo (Chinese: 冬虫夏草). Of the various entomopathogenic fungi, Ophiocordyceps sinensis is one that has been used for at least 2000 years[2] for its reputed abilities to treat many diseases related to lungs, kidney, and erectile dysfunction. This fungus is not yet cultivated commercially,[3] despite the fact that several fermentable strains of Ophiocordyceps sinensis have been isolated by Chinese scientists.[4] Overharvesting and over exploitation have led to the classification of O. sinensis as an endangered species in China.[5] Additional research needs to be carried out in order to understand its morphology and growth habit for conservation and optimum utilization.

The moths in which O. sinensis grows are ambiguously referred to as "ghost moth", which identifies either a single species or the genus Thitarodes, and the species parasitized by O. sinensis may be one of several Thitarodes that live on the Tibetan Plateau (Tibet, Qinghai, West-Sichuan, SW-Gansu & NW Yunnan), and the Himalayas (India, Nepal, Bhutan).

O. sinensis is known in the West as a medicinal mushroom, and its use has a long history in Traditional Chinese medicine as well as Traditional Tibetan medicine.[6] The hand-collected fungus-caterpillar combination is valued by herbalists and as a status symbol;[7] it is used as an aphrodisiac and treatment for ailments such as fatigue and cancer, although such use is mainly based on traditional Chinese medicine and anecdote.

Taxonomic History/ Systematics[edit]

Caterpillars with emerging Ophiocordyceps sinensis

Morphological Features[edit]

Similar to other Cordyceps species, O. sinensis consists of two parts, a fungal endosclerotium (caterpillar) and stroma.[2] The stroma is the upper fungal part and is dark brown or black, but can be a yellow color when fresh and, longer than the caterpillar itself, usually 4–10 cm. It grows singly from the larval head, and is clavate, sublanceolate or fusiform and distinct from the stipe.[8] The stipe is slender, glabrous, and longitudinally furrowed or ridged. The fertile part of the stroma is the head. The head is granular due to the ostioles of the embedded perithecia.[2] The perithecia are ordinally arranged and ovoid [8] The asci are cylindrical or slightly tapering at both ends, and may be straight or curved, with a capitate and hemispheroid apex and may be two to four spored.[2] Similarly, ascospores are hyaline, filiform, multiseptate at a length of 5-12 um and subattenuated on both sides.[8] Perithecial, ascus and ascospore characters in the fruiting bodies are the key identification characteristics of O. sinensis. Ophiocordyceps (Petch) Kobayasi species produce whole ascospores and do not separate into part spores which is different from other Cordyceps species, which produce either immersed or superficial perithecia perpendicular to stromal surface and the ascospores at maturity are disarticulated into part spores.[9] Generally Cordyceps species possess brightly colored and fleshy stromata, but O. sinensis had dark pigments and tough to pliant stromata, a typical characteristic feature of most of the Ophiocordyceps species.[3]

Important developments in Classification[edit]

The species was first described scientifically by Miles Berkeley in 1843 as Sphaeria sinensis;[10] Pier Andrea Saccardo transferred the species to the genus Cordyceps in 1878.[11] The scientific name's etymology is from the Latin cord "club", ceps "head", and sinensis "from China". The fungus was known as Cordyceps sinensis until 2007, when molecular analysis was used to emend the classification of the Cordycipitaceae and the Clavicipitaceae, resulting in the naming of a new family Ophiocordycipitaceae and the transfer of several Cordyceps species to Ophiocordyceps.[9] Based on a molecular phylogenetic study, Sung et al. (2007) separated the megagenus Cordyceps into four genera as it was polyphyletic, viz. Cordyceps (40 spp.), Ophiocordyceps (146 spp.), Metacordyceps (6 spp.) and Elaphocordyceps (21 spp.), while the remaining 175 spp. were left in Cordyceps. As a result, C. sinensis was transferred to Ophiocordyceps, hence renamed as O. sinensis.[2]

Common Names[edit]

In Tibetan it is known as དབྱར་རྩྭ་དགུན་འབུ་ (Wylie: dbyar rtswa dgun 'buZYPY: yartsa gunbu, "summer grass winter bug"), which is the source of the Nepali यार्शागुम्बा, yarshagumba, yarchagumba or yarsagumba. The transliteration in Bhutan is Yartsa Guenboob. It is known as keera jhar, keeda jadi, keeda ghas or 'ghaas fafoond in Nepali. Its name in Chinese Dōng chóng xià cǎo (冬蟲夏草) means "winter worm, summer grass" (i.e., "worm in the winter, [turns to] plant in the summer"). The Chinese name is a literal translation of the original Tibetan name, which was first recorded in the 15th Century by the Tibetan doctor Zurkhar Namnyi Dorje. In colloquial Tibetan Yartsa gunbu is often shortened to simply "bu" or "yartsa".

In traditional Chinese medicine, its name is often abbreviated as chong cao (蟲草 "insect plant"), a name that also applies to other Cordyceps species, such as C. militaris. In Japanese, it is known by the Japanese reading of the characters for the Chinese name, tōchūkasō (冬虫夏草?).

Strangely, sometimes in Chinese English language texts Cordyceps sinensis is referred to as aweto [Hill H. Art. XXXVI: The Vegetable Caterpillar (Cordiceps robertsii). Transactions and Proceedings of the Royal Society of New Zealand 1868-1961. Vol 34, 1901;396-401], which is the Māori name for Cordyceps robertsii, a species from New Zealand.

The English term "vegetable caterpillar" is a misnomer, as no plant is involved. "Caterpillar fungus" is a preferable term.

Nomenclature of the anamorph[edit]

Since the 1980s, 22 species in 13 genera have been attributed to the anamorph of O. sinensis. Of the 22 species, Cephalosporium acreomonium is the zygomycetous species of Umbelopsis, Chrysosporium sinense has very low similarity in RAPD polymorphism, hence it is not the anamorph. Likewise, Cephalosporium dongchongxiacae, C. sp. sensu, Hirsutella sinensis and H. hepiali and Synnematium sinnense are synonymous and only H. sinensis is only validly published in articles. Cephalosporium sinensis possibly might be synonymous to H. sinensis but there is lack of valid information. Isaria farinose is combined to Paecilomyces farinosus and is not the anamorph. Several species like Isaria sp. Verticella sp. Scydalium sp. Stachybotrys sp. were identified only up to generic level, and thus it is dubious that they are anamorph. Mortierella hepiali is discarded as anamorph as it belongs to Zygomycota. Paecilomyces sinensis and Sporothrix insectorum are discarded based on the molecular evidence. P. lingi appeared only in one article and thus is discarded due to incomplete information. Tolypocladium sinense, P. hepiali, and Scydalium hepiali, have no valid information and thus are not considered as anamorph to Ophiocordyceps sinensis. V. sinensis is not considered anamorph as there is no valid published information. Similarly, Metarhizium anisopliae is not considered anamorph as it has widely distributed host range, and is not restricted only in high altitude.[12] Thus Hirsutella sinensis is considered the validly published anamorph of O. sinensis. Cordyceps nepalensis and C. multiaxialis which had similar morphological characteristics to C. sinensis, also had almost identical or identical ITS sequences and its presumed anamorph, H. sinensis. This also confirms H. sinensis to be anamorph of O. sinensis and suggests C. nepalensis and C. multiaxialis are synonyms.[13] Evidence based on microcyclic conidiation from ascospores and molecular studies [2] support H. sinensis as the anamorph of the caterpillar fungus, O. sinensis.

Ecology[edit]

The caterpillars prone to infection by O. sinensis generally live 6 inches (15,25 cm) underground [4] in alpine grass and shrub-lands on the Tibetan Plateau and the Himalayas at an altitude between 3,000 and 5,000 m (9,800 and 16,400 ft). The fungus is reported from the northern range of Nepal, Bhutan, and also from the northern states of India, apart from northern Yunnan, eastern Qinghai, eastern Tibet, western Sichuan, southwestern Gansu provinces.[4] The fungus consumes its host from inside out as they hibernate in alpine meadows. Usually the larvae are more vulnerable after shedding their skin, during late summer. The fungal fruiting body disperses spores which infect the caterpillar. The infected larvae tend to remain vertical to the soil surface with their heads up. The fungus then germinates in the living larva, kills and mummifies it, and then the stalk-like fruiting body emerges from the head and the fungus finally emerges from the soil by early spring.[14] Fifty-seven taxa from seven genera (1 Bipectilus, 1 Endoclita, 1 Gazoryctra, 12 Hepialus, 2 Magnificus, 3 Pharmacis, and 37 Thitarodes [3]) are recognized as potential hosts of O. sinensis.

Reproduction biology[edit]

Ophiocordyceps sinensis has both teleomorphic and anamorphic phases. Spending up to five years underground before pupating, the Thitarodes caterpillar is attacked while feeding on roots. It is not certain how the fungus infects the caterpillar; possibly by ingestion of a fungal spore or by the fungus mycelium invading the insect through one of the insect's breathing pores. The dark brown to black fruiting body (or mushroom) emerges from the ground in spring or early summer, the long, usually columnar fruiting body reaches 5–15 cm above the surface and releases spores.

In late autumn, chemicals on the skin of the caterpillar interact with the fungal spores and release the fungal mycelia, which then infects the caterpillar.[4] After invading a host larva, the fungus ramifies throughout the host and eventually kills it. Gradually the host larvae become rigid due to the production of fungal sclerotia. Fungal sclerotia are multihyphal structures that can remain dormant and then germinate to produce spores. After over-wintering, the fungus ruptures the host body, forming a sexual sporulating structure (a perithecial stroma) from the larval head in summer that is connected to the sclerotia (dead larva) below ground and grows upward to emerge from the soil.[15] The slow growing O. sinensis grows at a comparatively low temperature, i.e., below 21oC. Temperature requirements and growth rates are crucial factors that identify O. sinensis from other similar fungi.[3]

Use in medicine[edit]

It is used as a reputed curative to many diseases, anti- aging,[16] hypoglycemic,[17] aphrodisiac and also treatment against cancer. Ophiocordyceps sinensis serves against kidney and lung problems and stimulates the immune system; it is used for treatment of fatigue, night sweating, respiratory disease, hyperglycemia, hyperlipidemia, asthenia after severe illness, arrhythmias and other heart diseases and liver disease.[4]

Research is carried out worldwide to ascertain its medical effects.

Traditional Asian medicines[edit]

Weighing the precious Caterpillar fungus in Yushu, Southern Qinghai, China[18]

Medicinal use of the caterpillar fungus apparently originated in Tibet and Nepal. So far the oldest known text documenting its use was written in the late fourteen hundreds by the Tibetan doctor Zurkhar Nyamnyi Dorje (Wylie: Zur mkhar mnyam nyid rdo rje)[1439-1475]) in his text: Man ngag bye ba ring bsrel ("Instructions on a Myriad of Medicines"). A translation is available at Winkler.[19]

The first mention of Ophiocordyceps sinensis in traditional Chinese Medicine was in Wang Ang’s 1694 compendium of materia medica, Ben Cao Bei Yao.[20] In the 18th Century it was listed in Wu Yiluo's Ben cao cong xin ("New compilation of materia medica").[21] No sources have been published to uphold widespread claims of "thousands of years of use in Chinese medicine" or use of "chong cao since the 7th Century Tang Dynasty in China". The ethno-mycological knowledge on caterpillar fungus among the Nepalese people is documented by Devkota(2006) The entire fungus-caterpillar combination is hand-collected for medicinal use.

The fungus is a medicinal mushroom which is highly prized by practitioners of Tibetan medicine, Chinese medicine and traditional Folk medicines, in which it is used as an aphrodisiac and as a treatment for a variety of ailments from fatigue to cancer. In Chinese medicine it is regarded as having an excellent balance of yin and yang as it is apparently both animal and vegetable. Assays have found that Ophiocordyceps species produce many pharmacologically active substances. They are now cultivated on an industrial scale for their medicinal value. However, no one has succeeded so far in rearing the fungus by infecting cultivated caterpillars;[3] all products derived from cultured Ophiocordyceps are derived from mycelia grown on grains or in liquids.

According to Bensky et al. (2004), laboratory-grown C. sinensis mycelia have similar clinical efficacy and less associated toxicity. He notes a toxicity case of constipation, abdominal distension, and decreased peristalsis, two cases of irregular menstruation, and one case report of amenorrhea following ingestion of tablets or capsules containing C. sinensis. In Chinese medicine C. sinensis is considered sweet and warm, entering the lung and kidney channels; the typical dosage is 3–9 grams.[22]

Cordycepin, a compound isolated from the "Caterpillar fungus".

Introduction to the Western world[edit]

Ophiocordyceps sinensis

The Western world was largely unaware of Ophiocordyceps prior to 1993. The fungus dramatically caught the world's eye due to the performance of three female Chinese athletes, Wang Junxia, Qu Yunxia, and Zhang Linli. These athletes broke five world records for 1,500, 3,000 and 10,000 meter dashes at the National Games in Beijing, China. The number of new world records set at a single track event attracted much attention and suspicion. Following the races, the women were expected by some to fail drug tests for anabolic steroids. However, the athletes' tests revealed no illegal substances, and coach Ma Junren told the reporters that the runners were taking Ophiocordyceps sinensis and turtle blood at his request. However for the 2000 Sydney Olympics, Ma Junren withdrew some of his athletes at the last minute. It was speculated that a new doping test would have revealed illegal substances, thus half a dozen Chinese field and track athletes were left at home.

Economics and impact[edit]

Many shops in downtown Lanzhou advertise Dōng chóng xià cǎo (冬虫夏草) among other local specialties.

In rural Tibet, yartsa gunbu has become the most important source of cash income. The fungi contributed 40% of the annual cash income to local households and 8.5% to the GDP in 2004. Prices have increased continuously, especially since the late 1990s. In 2008, one kilogram traded for US$3,000 (lowest quality) to over US$18,000 (best quality, largest larvae). The annual production on the Tibetan Plateau was estimated in 2009 at 80–175 tons.[23] The Himalayan Ophiocordyceps production might not exceed a few tons.

In 2004 the value of a kilogram of caterpillars was estimated at about 30,000 to 60,000 Nepali rupees in Nepal, and about Rs 100,000 in India.[24] In 2011 the value of a kilogram of caterpillars was estimated at about 350,000 to 450,000 Nepali rupees in Nepal. A 2012 BBC article indicated that in north Indian villages a single fungus was worth Rs 150 (about £2 or $3), which is more than the daily wage of a manual laborer.[25]

According to Daniel Winkler, the price of Ophiocordyceps sinensis has risen dramatically on the Tibetan Plateau, basically 900% between 1998 and 2008, an annual average of over 20% (after inflation). However, the value of big sized caterpillar fungus has increased more dramatically than smaller size Cordyceps, regarded as lower quality.[20]

Year  % Price Increase Price/kg (Yuan)
1980s 1,800
1997 467% (incl. inflation) 8,400
2004 429% (incl. inflation) 36,000
2005 10,000–60,000
2013 125,000–500,000

Because of its high value, inter-village conflicts over access to its grassland habitats has become a headache for the local governing bodies and in several cases people were killed. In November 2011, a court in Nepal convicted 19 villagers over the murder of a group of farmers during a fight over the prized aphrodisiac fungus. Seven farmers were killed in the remote northern district of Manang in June 2009 after going to forage for Yarchagumba. [26]

Its value gave it a role in the Nepalese Civil War, as the Nepalese Maoists and government forces fought for control of the lucrative export trade during the June–July harvest season.[27] Collecting yarchagumba in Nepal had only been legalised in 2001, and now demand is highest in countries such as China, Thailand, Vietnam, Korea and Japan. By 2002, the herb was valued at R 105,000 ($1,435) per kilogram, allowing the government to charge a royalty of R 20,000 ($280) per kilogram.

The search for Ophiocordyceps sinensis is often perceived to pose a threat to the environment of the Tibetan Plateau where it grows. While it has been collected for centuries and is still common in such areas, current collection rates are much higher than in historical times.

Ophiocordyceps producers like to perpetuate the story that unscrupulous harvesters insert twigs into the ascocarps of wild C. sinensis to increase their weight and therefore the price paid. A tiny twig is only used when the ascocarp is broken from the caterpillar, and has nothing to do with artificially increasing weight. Supposedly, at some point in the past, someone inserted lead wires with which to increase weight; however, each year hundreds of millions of specimens are harvested and this appears to have been a one-time occurrence.[citation needed]

Cultivated C. sinensis mycelium is an alternative to wild-harvested C. sinensis, and producers claim it may offer improved consistency. Artificial culture of C. sinensis is typically by growth of pure mycelia in liquid culture (in China) or on grains (in the West). The first time in Vietnam, Prof. Aca. Dr. Dai Duy Ban together with scientists and DAIBIO Company and DAIBIO Great Traditional Medicine Family Clinic discovered the Cordyceps sinensis as Isaria cerambycidae N.SP. to develop Fermentation DAIBIO Cordyceps Sinensis.[28] Ascocarps are not produced through in vitro cultivation.

References[edit]

  1. ^ "Ophiocordyceps sinensis (Berk.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora 2007". MycoBank. International Mycological Association. Retrieved 2011-07-19. 
  2. ^ a b c d e f Shrestha, B., Weimin, Z., Yongjie, Z., & Xingzhong, L. (2010). What is the Chinese caterpillar fungus Ophiocordyceps sinensis (Ophiocordycipitaceae)?. Mycology: An International Journal On Fungal Biology, 1(4), 228-236. doi:10.1080/21501203.2010.536791.
  3. ^ a b c d e Hsieh, C., et al., A Systematic Review of the Mysterious Caterpillar Fungus Ophiocordyceps sinensis in Dong-ChongXiaCao and Related Bioactive Ingredients. Vol. 3. 2013. 16-32.
  4. ^ a b c d e Zhu JS, Halpem GM, Jones K. 1998. The scientific rediscovery of an ancient Chinese herbal medicince: Cordyceps sinensis. I. J Alt Complem Med 4:289-303.
  5. ^ Xiao-Liang, W., & Yi-Jian, Y. (2011). Host insect species of Ophiocordyceps sinensis: a review. Zookeys, 12743-59. doi:10.3897/zookeys.127.802
  6. ^ Halpern, Miller (2002). Medicinal Mushrooms. New York, New York: M. Evans and Company, Inc. pp. 64–65. ISBN 0-87131-981-0 
  7. ^ http://www.npr.org/2011/10/09/141164173/caterpillar-fungus-the-viagra-of-the-himalayas
  8. ^ a b c Sung, G. H., et al. (2007). "A multi-gene phylogeny of Clavicipitaceae (Ascomycota, Fungi): identification of localized incongruence using a combinational bootstrap approach." Molecular Phylogenetics and Evolution 44(3): 1204-1223.
  9. ^ a b Sung GH, Hywel-Jones NL, Sung JM, Luangsa-Ard JJ, Shrestha B, Spatafora JW. (2007). "Phylogenetic classification of Cordyceps and the clavicipitaceous fungi". Studies in Mycology 57: 5–59. doi:10.3114/sim.2007.57.01. PMC 2104736. PMID 18490993. 
  10. ^ Berkeley MJ. (1843). "On some entomogenous Sphaeriae". London Journal of Botany 2: 205–11. 
  11. ^ Saccardo PA. (1878). "Enumeratio Pyrenomycetum Hypocreaceorum hucusque cognitorum systemate carpologico dispositorum" (PDF). Michelia (in Latin) 1 (3): 277–325. 
  12. ^ Jiang, Y. Y., & Yao, Y. J. (n.d). Names related to Cordyceps sinensis anamorph. Mycotaxon, 84245-254.
  13. ^ Liu, Z., Liang, Z., Liu, A., Yao, Y., Hyde, K. D., & Yu, Z. (n.d). Molecular evidence for teleomorph-anamorph connections in Cordyceps based on ITS-5.8S rDNA sequences. Mycological Research, 106(9), 1100-1108.
  14. ^ Stone, R. (2008). Last Stand for the Body Snatcher of the Himalayas?. Science, (5905), 1182. doi:10.2307/20145300
  15. ^ Xing, X. K., & Guo, S. X. (2008). The Structure and Histochemistry of Sclerotia of Ophiocordyceps sinensis. Mycologia, (4), 616. doi:10.2307/20444986.
  16. ^ Ji DB, Ye J, Li CL, Wang YH, Zhao J, Cai SQ (2009) Antiaging effect of Cordyceps sinensis extract. Phytotherapy Research 23 (1): 116-122. Doi: 10.1002/ptr.2576
  17. ^ Zhang GQ, Huang YD, Bian Y, Wong JH, Ng TB, Wang HX (2006) Hypoglycemic activity of the fungus Cordyceps militaris, Cordyceps sinensis, Tricholoma mongolicum and Omphalia lapidescens in streptozotocin-induced diabetic rats. Applied Microbiology and Biotechnology 72 (6): 1152-1156. Doi: 10.1007/s00253-006-0411-9.
  18. ^ http://tibetwebdigest.com/why-are-people-fighting-over-caterpillar-fungus/
  19. ^ Winkler D. (2008). "The mushrooming fungi market in Tibet exemplified by Cordyceps sinensis and Tricholoma matsutake". Journal of the International Association of Tibetan Studies. In: In the Shadow of the Leaping Dragon: Demography, Development, and the Environment in Tibetan Areas (4). 
  20. ^ a b Winkler D. (2008). "Yartsa Gunbu (Cordyceps sinensis) and the fungal commodification of the rural economy in Tibet AR". Economic Botany 62 (3): 291–305. doi:10.1007/s12231-008-9038-3. 
  21. ^ Wu Y (1757). "Ben cao cong xin" - "New compilation of materia medica" (in Chinese). 
  22. ^ Bensky D, Gamble A, Clavey S, Stöger E, Bensky L. Lai (2004). Materia Medica: Chinese Herbal Medicine (3rd ed.). Seattle, Washington: Eastland Press. ISBN 978-0-939616-42-8. 
  23. ^ Winkler, D. (2009). "Caterpillar Fungus (Ophiocordyceps sinensis) Production and Sustainability on the Tibetan Plateau and in the Himalayas". Asian Medicine 5 (2): 291. doi:10.1163/157342109X568829.  edit
  24. ^ Sharma S. (2004). "Trade of Cordyceps sinensis from high altitudes of the Indian Himalaya: Conservation and biotechnological priorities" (PDF). Current Science 86 (12): 1614–9. 
  25. ^ Jeffrey, Craig (2012-07-07). "The 'Viagra' transforming local economies in India". BBC News. Retrieved July 9, 2012. 
  26. ^ Staff (14 November 2011) 'Himalayan viagra': Six men get life for Nepal murders BBC News Asia, Retrieved 9 July 2012
  27. ^ Baral N, Heinen JT. (2005). "The Maoist people's war and conservation in Nepal". Politics and the Life Sciences 24 (1): 2–11. doi:10.2990/1471-5457(2005)24[2:TMPWAC]2.0.CO;2. 
  28. ^ DAIBIO Cordyceps Sinensis in Vietnam


Further reading[edit]

  • Winkler, D. 2005. Yartsa Gunbu - Cordyceps sinensis. Economy, Ecology & Ethno-mycology of a Fungus Endemic to the Tibetan Plateau. In: A.BOESI & F. CARDI (eds.). Wildlife and plants in traditional and modern Tibet: Conceptions, Exploitation and Conservation. Memorie della Società Italiana di Scienze Naturali e del Museo Civico di Storia Naturale di Milano, Vol. 33.1:69–85.
  • Zhang Y., Zhang S., Wang M., Bai F. & Liu X. (2010). "High Diversity of the Fungal Community Structure in Naturally-Occurring Ophiocordyceps sinensis". PLoS ONE 5(12): e15570. doi:10.1371/journal.pone.0015570.

External links[edit]