Infested by Caterpillar Fungus 2006

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Published in:  Mushroom - The Journal of Wild Mushrooming, Issue 89 Vol. 24.2, 2006, p.7-12.

Infested by the Caterpillar Fungus (Cordyceps sinensis)
A Tibetan once in a lifetime experience

Daniel Winkler

            For three days we had been driving on this muddy track known as the Sichuan-Tibet "Highway." Peaks of freshly snowcapped mountains were enshrouded by thick clouds, and heavy loads of rain were regularly released by the monsoon clouds, causing the already bad roads to disintegrate even further. The old Beijing-Jeep broke down frequently, one time stranding us in the middle of a flooded creek. Luckily we were able to locate a truck, which pulled us out, although not without exacting a small fortune from the Tibetan foresters whom I accompanied.
             At first I was annoyed when the car broke down or got stuck. Soon I discovered that it was a great chance to explore the surroundings. In Bachen County I observed a Tibetan man very slowly walking along a green hillside while staring at the ground, paying little attention to his herd of yaks. Suddenly the nomad started digging. Thinking he might be digging medicinal plants I got curious. I rushed up the slope, but had to slow down quickly. Although I had been in Tibet for a week, hiking uphill at 14,500 feet gave me good insight into how old age will feel. My rest gave me the chance to marvel at crimson Incarvilleas, purple Pedicularis and bright yellow Himalayan poppies.
Seemingly, the nomad had dug up two roots. When he realized that I was interested in his find, he proudly showed them to me. I never had seen such a life form before and had no idea what it was. It definitely wasn't a type of plant. Yet out of its head, just above its eyes, grew a long brown stalk, my Tibetan co-worker, Pema Gyatso, called `grass'. He explained that I had seen my first Yartsa gunbu, which means "summer grass-winter worm" in Tibetan. It turned out Pema knew quite a bit about it, having collected them to help augment his family's meager income. "Bu" (worm), as he called it for short, start growing a grass above ground when spring comes to the grasslands and can be found for about a month. Tibetan herders collect them all over the grasslands and export them down to China, where they are known in Traditional Chinese Medicine as "Dong chong xia cao" ("Chongcao" for short), which is a literal translation of the Tibetan.
Back home in July 1997, I learned that the ghost moth caterpillar had been infested by the ascomycete, Cordyceps sinensis, an entomophagous (insect-eating) or entomogenous (insect-originating) flask fungus in the Clavicipitaceae.  The best known member of this family is Claviceps purpurea, wheat ergot, infamous for causing ergotism, a.k.a. St. Anthony's fire, with symptoms of vomiting, diarrhoea, hallucinations, and possibly lethal gangrene and famous for providing lysergic acid. And while consuming Cordyceps sinensis will not provide any of ergot's symptoms, eating a caterpillar fungus specimen might well cause disgusted retching in some faint western souls, due to a lack of culinary appreciation of insect delicacies.
However, it is not only innocent ghost moths who become infested by Cordyceps, for apparently I too suffered an infestation. I won't claim that it is onlyCordyceps that forces me to return to Tibet again and again, as it forces the moribund caterpillar to move to the place of its last rest, but my curiosity got seriously stoked. There seems to be no end to discovery when looking into such an elusive and complex - bordering on esoteric - organism endemic to one of the world's most remote areas.
As it turns out, the sprout that grows out of the caterpillar is the ascomycete's stroma, the fruiting body that is covered with spore-producing cells (asci) on its upper end. Upping the ante, each spore divides itself into 60 fertile propagules, an adaptation to increase the odds of the fungal "spore" actually making contact with its host larva.
"Host" might be too innocuous a term to describe this abusive and fatal relationship. For once the guest has made itself comfortable, having entered through orifices or attached itself to the outside, it starts feeding on the host. At first the "guest" dines respectfully on non-vital organs. As a last rite of their union, Cordyceps sinensis apparently makes the larva crawl into a position ideal for fungal spore dispersal - essentially taking the host on one last outing before immobilizing it for good. Infected larvae will wait out the harsh but arid Tibetan winter close to the surface, while the less fungally `accommodating' larvae will hibernate deep down in the roots of Polygonum knotweed, Kobresia sedges or Astragalus milk-vetch, to mention a few of its favourite fodder plants.
            Safely rooted, a healthy caterpillar might hibernate, daydreaming about metamorphosing into a beautiful moth fluttering for a mere few days above flower-studded meadows in hopes of scenting out a mate willing to engage in the eternal dance of genders, after three to five years spent mostly as a lowly larva.
However, by the time spring kicks in, a fungally compromised larva is not much of an insect anymore. Although its remaining exoskeleton gives the illusion of a continued caterpillar existence, by then it functions solely as a fungal fodder fridge, ready to be completely raided when warmer temperatures allow the fungus to complete its hostile takeover. Once the fungus has replaced the complete interior of the larvae with its thread-like hyphae, it will grow its sporocarp - what Tibetans call a blade of "grass" - right out of the caterpillar's fontanel.
The fruiting body will grow up 5-15cm above the ground in order to have its propagules dispersed by the wind to land on yet another larva of the 30 or so species of ghost moth (Thitarodes, formerly Hepialus) endemic to the Tibetan Plateau. The distribution of Cordyceps sinensis is thus completely dependent on the occurrence of the ghost moths. Both organisms are endemic to grassland ecosystems of the Tibetan Plateau and adjacent areas, between altitudes of 3000m to 5000m [9,000 to 16,500 ft], usually within a range of 500m [1,500 ft] around the potential tree line.
After my first encounter, I kept running into Cordyceps while consulting western non-governmental organisations (NGO) on reforestation, non-timber forest products and rural income generation in Tibetan areas. Leaving my guesthouse one morning in Lithang, in May 1999, I had to literally watch my steps. Sidewalks, and even some sections of side streets, were covered with patches of thousands of caterpillar fungi spread out for drying. You definitely wouldn't want to step on them, since they lose a lot of value if the sporocarp breaks off the caterpillar.
There was a lot of money lying on the ground. In 1999, one specimen fetched anywhere from Yuan 1 to 5 (¥8.2=$1), the bigger the better. In 2004, a large specimen fetched up to ¥10, prices having been driven up by a widespread assumption that Chongcao would help against SARS. Often there were several pounds of Bu spread out on the ground, with one pound consisting of 200 to 2000 fungi. (Weight depends partly on size, but mostly on moisture content.) DuringYartsa Gunbu season the main street in Lithang is hustling and bustling with deals, sellers mingling with buyers flashing their scales. Nomads and farmers arrive hourly from the hinterland, selling off their harvest, be it a handful from a day of searching or bagfuls from weeks of collecting with the entire family. The scene is male-dominated, but there are a few women, attracting mostly women sellers. Middlemen buy up the Yartsa Gunbu and pass it on to big buyers, many of them representatives of phytopharma companies in Chinese coastal areas. Millions of Yuan are exchanged for Bu. These are substantial amounts when you take into account that the annual rural income is below ¥1000 ($122).
In general Tibetans live off their land by farming the lower elevations and by herding yak, dzo (yak-cow hybrids), sheep and goat. Basically all of the Tibetan Plateau is grazed, except the most arid north-eastern high altitude desert of the Changtang. Traditionally in Tibet animals don't get fenced in, only areas that should not be grazed like fields or orchards are fenced in. However, China's Central government is trying hard to overcome "backward" herding practices and is forcing fences onto nomads. The justification is that with clear ownership comes responsibility and overgrazing will be minimized. However, it is also just a new disguise for a century old conflict between nomadic and settled societies. This perspective is openly confirmed by official pronouncements like the one from the late 1990s when a high government official proclaimed that there would be no nomads in China after the year 2000.
In 2005 this is not the case, but often fencing comes with detrimental environmental results and economically devastating costs for families. But there are also winners; if you have good connections you will be able to secure good pastures with access to drinking water. What is really odd is that when I was working on reforestation there was no support from any government agency for fencing to keep out animals when seedlings were very susceptible to damage from livestock. Go figure.
Part of the rational behind the pasture reforms is that although these ancient practices have successfully sustained households for millennia, they contribute very little to the cash income of families. Herding isn't a big money maker, since most Tibetans don't like to sell off their animals for slaughter. Buddhist ethics respect all life as sacred, which does not stop nomads and farmers from taking lives to feed their families, but often prevents them from selling off their animals to make extra cash. Also nomads like to hold onto their animals to increase their herd size in the case that a bad winter strikes and kills off a lot of the animals. Cash is made by selling wool and hides, but mostly by selling butter or extra meat. Growing grains beyond subsistence is also not very interesting, since grain prices are kept artificially low in China.
Thus, the essential bit of cash income to get by in a more and more commercialized world is made over proportionally from non-farming/herding activities such as seasonally contracted labor, i.e. back braking road work at meager ¥20 to ¥30 ($2.40-$3.60) per day. Seedling planting is more attractive, but forestry work is usually reserved for Han Chinese government employees imported from the lowlands. When we tried to integrate local Tibetans in reforestation work, we offered ¥40 per day to make it more attractive since planting season overlaps with Bu collection season since both seedlings and fungi feed off of moisture being released by the thawing of the ground.
More important than contracted labor and surely more popular and reliable is the collection of herbs and hunting of mushrooms and wildlife products, traditional activities for subsistence and trade for many centuries. Tibetans collected medicinal plants for export to China to trade for tea and luxury items like silks and brocade. Wildlife products are pursued by only a few renegades targeting male musk deer for their glands that fetch an astronomical ¥1500 to ¥ 3000; black bears for their precious gall bladder; or red or white-lipped deer antlers, a popular remedy in Traditional Chinese Medicine just as locally grown yak penis. More commonly Tibetans go after herbs and mushrooms, which are technically known as non-timber forest products (NTFP) or to coin an equivalently "slick" term better suited for the Tibetan Plateau conditions "non-livestock grassland products" (NLGP). NTFP are nowadays dominated by matsutake (Tricholoma matsutake) widely collected for fresh export to Japan since the 1990s, but other edible fungi such as morels, chanterelles and boletes are also catching on as export goodies. The most commonly collected herbs are bulbs of fritillary (Fritillaria, TCM: Bei mu), and roots of rhubarb (Rheum, Da huang), Saussurea plants (Xue hua) and milk fetch (Astragalus, Huang qi). All in all, Tibetan and Chinese Medicines use hundreds of medicinal plants growing in Tibet.
It is interesting to note that Yartsa Gunbu is mostly collected by Tibetan nomads and farmers who still make their living in traditional ways, although there used to be a traditional taboo placed on digging Bu and other medicinal plant roots as well as gold. Namkhai Norbu, a Tibetan scholar and Lama wrote in his book "Journey among the Tibetan Nomads" based on his travels in the late 1950s: "Rigya, the general laws that govern relations with the environment", forbid the digging of Bu, since it is regarded as a treasure of "the earth spirits". Digging Yartsa Gunbu provokes these earth spirits who will strike the offender, his family and clan with sickness and punish his livestock with ill health.
This Tibetan belief regarding the earth spirits probably predates Buddhist thought. However, in Lithang and most other places this belief is not practiced anymore. It might be due to a loss of these traditions or different local traditions. It is very plausible that the taboo has been lost in Lithang. I could imagine that Tibetans observed first Chinese and then some Tibetan collectors digging without suffering direct ill effects. Thus, the taboo might have been lost. Supporting this idea is the fact that in the Golok area Yartsa Gunbu was not really exploited by Tibetans until after large-scale exploitation was started after the Chinese took control in the 1950s. Before the take-over Golokpas were famous for keeping all outsiders, Chinese or Western, out of their territory, thus very successfully protecting their traditions, while Lithang was much earlier impacted by Chinese imperial policy. Lithang had a small Chinese garrison since 1720, but direct Chinese control was not imposed until 1906, when General Zhao Erfeng's armies quelled the 1905 rebellion in Kham against Chinese rule.

One night I found myself in the home of a Lithang party official. His house was selected since it was a beautiful traditional Tibetan house. His no less beautiful daughter and her friend had been hired by the County government as the official hostesses, a completely honorable function. After a welcome song (apparently a Tibetan melody recycled with Mandarin lyrics), I was served an opulent meal with all Tibetan specialities: deep-fried Tibetan bread, momos (noodle dumplings), dried yak meat ("please cut yourself a piece out of the hind leg"), and, for dessert, troma (or droma, tiny silverweed tubers [Potentilla anserina] with sweet potato taste floating in only slightly rancid melted butter). All this was accompanied by plenty of drink, and it was there I ran unexpectedly into caterpillar fungus again.
            I had yet to learn to resist the pressure to drink heavily at these functions. This particular evening turned out to culminate in imbibing barley schnapps enhanced by a floating caterpillar. I felt brave enough simply drinking the Bu-infused booze, but I really started sweating and squirming (a bit like a bu worm myself) as I was offered that thing to eat. All eyes were fixed on the guest of honor, while my eyes were fixed on that alcohol- marinated caterpillar. I tried to insist that this was too much of an honor and the generous host should enjoy this delicacy, but there was no way out. Finally I closed my eyes, invoked the benefits of all the schnapps that permeated my digestive system (as well as the worm) and put it in my mouth. Unfortunately the caterpillar fungus was too big to swallow and I had to chew it.
It turns out Cordyceps sinensis has a pleasant fungal flavour. But maybe that's how larvae taste in the first place?
In April 2004, I found myself crawling on all fours over the slightly moist ground inhaling the aromatic smell of the small-leafed rhododendron and the fungal breath of soil awoken by spring. The pleasant warmth radiating from the strong subtropical sun was cancelled out by a cold wind blowing down from the snow-covered jagged peaks surrounding us. However, the sunlight was supposed to be a major help in spotting the tiny stromata, the fruiting bodies of the Caterpillar fungus, which emerge with the first green sprouts of sedges in an otherwise brownish landscape. Sonam Doden, a Tibetan butter dealer from Dardsemdo (Chinese: Kangding, formerly Tatsienlu), who agreed to take my friend Sherab Gyaltsen and me on a Yartsa Gunbu hunt, told me that the shadow of the tiny fungus would help me to tell the stroma apart from all the other little brown objects that carpet the ground in early spring, such as rhody twigs and withered stems of edelweiss and asters. Finding the elusive stroma by its shadow sounded a bit better than the Tibetan folklore that the caterpillar fungus can be best spotted on a windless day, since only a plant with an insect as its root would tremble slightly.
We had been crawling around for over an hour now at 4,500m [14,000 ft] and had not found a single Bu.  At least this mode of movement did not cause any altitude-induced shortage of breath. Scanning the ground so closely, I was reminded of the vegetation studies I had done in the early 90s in East Tibet, and in the absence of the fungus my mind kept itself busy by babbling names of plants I thought I recognised, such as Kobresia pygmaea sedges, Notholirion bulbiferum lilies, and Meconopsis horridula blue poppies. Luckily, not far above us a Tibetan family had interrupted their beautiful singing, breaking out a few times into excited screaming. Apparently they were sharing their joy when finding some Bu. Their success told me, it should be only a question of time until we stumbled upon the elusive Yartsa Gunbu too.

I marvelled at all the small azaleas that blanketed the slopes. All were about half a meter tall, kept in check by browsing livestock. I recalled the beauty of these shrubs in late May. Once I drove by when all the surrounding slopes were ablaze in bluish purple from their tiny flowers. Set on fire, my chain of thoughts went on, probably all these slopes had been burned before to create good pastures. Uncountable slopes where dark spruce-fir forests or evergreen oak-spruce forests had grown were replaced by pastures and shrub lands owing to centuries of grazing and slope burning. This must have substantially extended the habitat of the caterpillar fungus in Tibet. The yak and its herders as the best friends of Cordyceps sinensis? Interesting idea.
Suddenly I realized I was looking at a minuscule brown straight protuberance between tufts of grey grass. And it had its own shadow! But it did not move. Could this be it? Was this the needle in the haystack? Sonam and Sherab were sure it was Yartsa Gunbu. I got out my Swiss knife and was ready to dig it up. Wait a minute, Daniel, I told myself; first you have to document it. Get out the camera. I had come half way around the world to find some Cordyceps sinensisgrowing in the wild after years of collecting info and data, especially on its importance for Tibetan nomads and farmers. Seven years after I first encountered it in Bachen, I was finally looking at a stroma pushing its way up from the soil.
Digging out the caterpillar fungus, I first used my knife to cut the turf. Kobresia sedges have very dense root systems. Often Tibetans cut the turf into bricks and build walls out of it, definitely a form of ancient green construction. Most of the biomass of Kobresia is concentrated underground, a great strategy to protect itself from extreme weather and widespread intense grazing. The "host" of Cordyceps, the ghost moth larva, feeds off these sedges, which make up most of the grasslands of the Tibetan Plateau, over which I was crawling like a larva myself. Once I had carefully removed the humus-rich topsoil and tough roots of the sedges from the front side of the fungally transformed worm, I started carefully to peel back a thin layer of mycelium that encapsulated the insect part of the whole Yartsa Gunbu. Finally, the larva showed its yellowish body so I could take a photo of the whole organism in situ. (photo on your left)
We continued our search but found only two more Bu within the next few hours.  Around noon, in typical Tibetan hospitality, the fungus foraying family invited us to join their picnic. They had brewed a pot of tea, although to my tongue its taste did not invoke any memories of tea. It is better described as a kind of broth, since lots of salt and butter, most of the time rancid, is added. But a cup of soup is just the right thing on a cool spring day up in the mountains, even if it tastes rancid. This is the unique taste one has to accept to find culinary contentment in Tibet.
I had my teacup with me. Every Tibetan always brings his own bowl with him wherever he goes, since it is also needed for eating "tsampa," roasted barley flour mixed into the tea, Tibetan's daily staple. Mixing tsampa into tea is a challenging exercise that takes practice and refined finger coordination. First, one has to guess the right amount of flour and, second, the flour gets mixed into the greasy tea with your index and middle fingers. Watching a Tibetan mixing tsampa it seems very simple, even gracious and clean. Actually, clean is a misnomer for two reasons-first, I was using my dirty fingers after digging larvae and, second, the procedure is rather messy for the underskilled. I have developed an approach to minimize the mess: I do the first mixing with my knife. Yes, in this instance the blade I had just used to cut turf.
In the end the batter is supposed to turn into a kneadable mass. A Tibetan friend told me how he had been admonished as a child for not cleaning his bowl properly with the words "every dog is able to keep its bowl cleaner than you," which makes perfect sense when considering that the bowl is licked clean after use, then dried with the sleeve of one's coat. Along with the tea we were offered bread and a tasty string cheese. I felt regret that I only had some roasted almonds to share.
Chatting about our Bu hunt, we found out that the family was also disappointed with their meagre harvest. Sherab speculated that there might be so few specimens because the area was well searched. This was a plausible explanation as evidenced by the multitude of colorful dots in the brown landscape moving steadily but trance-like in slow motion searching all over on this Saturday in late April. Also, it was the very first week of the season. When I looked closely at the dug specimen, it was apparent that the spore producing asci had not fully developed yet. This is bad news for Cordyceps. In an ideal world Cordyceps sporocarps should not be picked until after the first week or two, when they would have released their spores to guarantee sustainability of collection. However, no such regulations are formulated anywhere yet, and so far Cordyceps seems not highly endangered, a promising fact for a very precious organism collected intensely for centuries in Tibet.
At this point it might be time to explain what all this fuss is about. This funky fungus, besides its larva-fixated feeding fancy, is a highly sought-after medicinal mushroom in the two ancient systems of medicine in Tibet and China. While there are plenty of fungi to go around for the 6 million Tibetans living right among it, the demand of 1.5 billion Han Chinese is a market force of a completely different dimension. The western market so far is relying on lab grown mycelia, since most westerners don't encounter enough social pressure to eat larvae.
In Tibet, the use of Cordyceps sinensis was traced back by Dr. Yonten Gyatso to documents of the 14th century, where it is mentioned in the Tibetan medicine text "Instructions on a Myriad of Medicines" by Nyamnyi Dorje [b.1439-d.1475]. Some Tibetan doctors recognize Cordyceps under a different name in an 11th century text, but other Tibetan doctors insist it is clearly a lizard, not a fungus that the ancient "Blue Beryl" folio is referring to. In Tibetan Medicine,Yartsa Gunbu is placed in the category of "medicinal essences" (Tsi Man), which includes several tonics. It is used as a tonic for general strengthening, boosting the immune system and increasing virility, and is prescribed for kidney and heart problems. It is also used for treatment of hepatitis B. Unlike in China, where patients consume the whole fungus, in Tibetan medicine it is mostly prescribed in formulated composite remedies, which contain a variety of ingredients to balance each other, thus optimizing their efficiency and minimizing side effects. [Tibetan medicine was formalized between the 8th and 11th Century. It absorbed a lot of knowledge from the Indian Ayuvedic system, but also integrated classical Greek elements, which arrived in Tibet via pre-Islamic Persia, Bactria and other long lost cultures].
In Traditional Chinese Medicine Cordyceps sinensis is regarded as a powerful remedy for asthma and TB, and thus was rumored to help against SARS. However, its main lure is its tonic function, to speed up convalescence, prevent sickness, and boost the immune system and vitality. Of course, anything that boosts vitality will boost libido as well, which in turn attracts the segment of consumers with the most disposable income, namely men over forty. Many Tibetans perceive the Cordyceps' Viagra-like function as the main reason why the Chinese are paying a fortune for these caterpillars. When I asked some Tibetan men in Lithang if they use some of the Bu they gather, I was answered with laughter. "We don't need to take that!"
Regardless of how the Tibetological discussion plays out regarding the first written reference to Yartsa Gunbu, currently the oldest Chinese reference to "dong chong xia cao"-the Chinese translation of the Tibetan name "winter worm-summer grass"-is from 1757 by Wu Yiluo, but it was clearly used before that date in China. In 1736 the French Jesuit Du Halde, residing at the imperial palace, described how the court physician treated him successfully with the "Hia Tsao Tong Tchong". Du Halde mentions the fact that it is hard to "procure" and that its value is four times its weight in silver.
There are other Chongcao species used in Traditional Chinese Medicine, such as the brightly orange fruiting Cordyceps militaris. This entomogenous fungus grows all over North America and Eurasia and is also widely cultivated. I came across a zip-lock bag full of it in the office of a Chinese ecology professor, who swore that it had helped him to overcome his late afternoon exhaustion.
There are a multitude of studies demonstrating the medicinal potential of Cordycepin and other active components in Cordyceps sinensis. Results include lower bad HDL cholesterol, improved blood circulation, and better utilization of oxygen in the body. In 1993, the latter was brought to the attention of the western world during the track and field world championships in Stuttgart, Germany, when to everyone's surprise Chinese runners won several long distance races. This success raised eyebrows, and the coach partially attributed it to the fact that he had integrated Cordyceps sinensis in the athletes' diet, which is not restricted as a performance-enhancing substance. This success, which was not repeated at the next world championships, is still being used to advertiseCordyceps' capacity to enhance stamina. If I had true myco-vision I would insist that it is no coincidence that a stamina-enhancing mushroom - our term "stamina" referring to the threads of life spun by the divine Fates - is made of thread-like hyphae spun by the fungus, but I don't really need to spin this thread too much, since the story of the fungus itself suffices.

Daniel Winkler started out mushroom hunting in the Bavarian Alps at age three. Trained as a geographer and ecologist, he works as researcher and NGO consultant on environmental issues of the Tibetan Plateau and Himalayas. He has published on forest ecology, forestry, traditional land-use practices, and medicinal plants and fungi. Daniel also guides mushroom and botanical tours in Tibet and gives presentations on Tibet and also mushrooms. He lives in Kirkland, WA and has been a member of the Puget Sound Mycological Society since 1996.
Last edited Thu, 09/06/2012 - 12:25