Cordyceps Blog

References for an article entitled: "2011 - The Year Cordyceps Mushroomed in the Media Landscape, but did not thrive in Tibet" to be published in Fungi

Sources:
Evans, H.E., Elliot, S.L, and D.P. Hughes 2011. Hidden diversity behind the Zombie-Ant fungus Ophiocordyceps unilateralis: Four new species described from Carpenter ants in Minas Gerais, Brazil. PloS One Vol 4.5, p. 598 – 602. link

Giove, Candice 2011. New Yorkers paying $800 an ounce for worms that promise sexual prowess. NY Post, Jan 16. link

Halpern, Georges 2007. Healing Mushrooms – Effective treatment for today’s illnesses, Square One Publishers. link

Hansen, Eric. 2011 The Killing Fields - The skyrocketing market value of yarchagumba, a rare fungus prized as an aphrodisiac, has led to turf wars—and possibly murder. Outside Magazine, Sept. link

Hoover, K., M. Grove, M. Gardner, D.P. Hughes, J. McNeil and J. Slavicek. 2011. A gene for an extended phenotype. Science 333: 1401. (PDF)

Huffington Post 2011 a. New Zombie-Creating Fungi Discovered (BBC VIDEO) Mar. 2. link

Huffington Post 2011 b. Caterpillar Fungus Transforms Tibet With Huge Cash Influx. Oct 10.  link

Hughes, D.P., Andersen, S. Hywel-Jones, N.L. , Himaman, W., Bilen, J and J.J. Boomsma 2011. Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection BMC Ecology 2011, 11:13. (PDF)

Hughes D.P., Wappler, T, & C. C. Labandeira  2010. Ancient death-grip leaf scars reveal ant fungal parasitism Biology Letters, 18th August. (PDF) [many more of Hughes’ papers are available at his webpages]

James, Jamie 2010. Nepal's Aphrodisiac War. Men's Journal 137, May. link

Jolly, Joanna 2011. Yarsagumba: Curse of Himalayan Annapurna region. BBC News, Katmandu, Jan 4. link

Matsuyama, Kanoko 2011. Himalayan Fungus Aids Mitsubishi Tanabe Sales With Multiple Sclerosis Drug. Bloomberg, Feb. link

National Geographic Daily News 2011. Photos: "Zombie" Ants Found With New Mind-Control Fungi, Text Matt Kaplan, Mar 3.  link

National Geographic Radio Weekend 2011. Feature on Cordyceps - Boyd Matson interviews Daniel Winkler, Apr. 16. link

Paterson, R. M. 2008, Cordyceps - A traditional Chinese medicine and another fungal therapeutic biofactory? Phytochemistry 69: 1469–1495. link

Rundle, Michael 2011. Zombie Animals: Fungi, Insects And Parasites That Resemble The Walking Dead. Huffington Post UK, Mar 10. link

Science Daily 2009. European Evolutionary Biologists Rally behind Richard Dawkins' Extended Phenotype. Jan 19, link

Silverman, Lauren 2011. Caterpillar Fungus: The Viagra Of The Himalayas. NPR, Oct. 9.

Stone Marcia 2011. Parasite gene makes caterpillars do bidding. Decode Science Blog.link

Winkler, Daniel 2008. The Mushrooming Fungi Market in Tibet - Exemplified by Cordyceps sinensis and Tricholoma matsutake’, in The Shadow of the Leaping Dragon: Demography, Development, and the Environment in Tibetan Areas. Journal of the International Association of Tibetan Studies 4.  link

Wong YY, Moon A, Duffin R, Barthet-Barateig A, Meijer HA, Clemens MJ, de Moor CH. 2010. Cordycepin Inhibits Protein Synthesis and Cell Adhesion through Effects on Signal Transduction. Journal of Biological Chemistry 285.4: 2610–2621. link

Zimmer 2011. More eldritch ant horror. Discover Magazine Blogs, May 9. link

Two news bits regarding insects and Cordyceps related fungi came to my attention today.
First piece of research is on ant behavior and what seems like their vaccination program against Metarhizium anisopliae, a Cordyceps anamorph that is a pathogenic fungus. The second article reports on the hope of using the same Metarhizium to fight ticks in in New England, the vector for the spread of Lyme's disease. 
Metarhizium anisopliae use as a insecticide is not a new approach. It was first used over 130 years ago. In 1879 Elie Metchnikoff used it in experimental tests to control the wheat grain beetle, Anisoplia austriaca. It was later used to control the sugar beet curculio, Cleonus punctiventris (for more details see MBCN). In recent years the use of Metarhizium anisopliae is being researched to control the spread of malaria by infecting the African mosquito Anopheles gambiae.

1. A German/Austrian researcher team published an article entitled "Social Transfer of Pathogenic Fungus Promotes Active Immunisation in Ant Colonies"

in PloS Biology describing what looks like Lasius ants vaccinating each other against theCordyceps anamorph Metarhizium anisopliae, which is a serious entomopathogene. 

Author Summary 
Close social contact facilitates pathogen transmission in societies, often causing epidemics. In contrast to this, we show that limited transmission of a fungal pathogen in ant colonies can be beneficial for the host, because it promotes “social immunisation” of healthy group members. We found that ants exposed to the fungus are heavily groomed by their healthy nestmates. Grooming removes a significant number of fungal conidiospores from the body surface of exposed ants and reduces their risk of falling sick. At the same time, previously healthy nestmates are themselves exposed to a small number of conidiospores, triggering low-level infections. These micro-infections are not deadly, but result in upregulated expression of a specific set of immune genes and pathogen-specific protective immune stimulation. Pathogen transfer by social interactions is therefore the underlying mechanism of social immunisation against fungal infections in ant societies. There is a similarity between such natural social immunisation and human efforts to induce immunity against deadly diseases, such as smallpox. Before vaccination with dead or attenuated strains was invented, immunity in human societies was induced by actively transferring low-level infections (“variolation”), just like in ants.

Citation: Konrad M, Vyleta ML, Theis FJ, Stock M, Tragust S, et al. (2012) Social Transfer of Pathogenic Fungus Promotes Active Immunisation in Ant Colonies. PLoS Biol 10(4): e1001300. doi:10.1371/journal.pbio.1001300

2. Scientists find fungus that kills Lyme disease-carrying ticks

  http://bangordailynews.com/2012/03/04/health/scientists-find-fungus-that-kills-lyme-disease-carrying-ticks/

Here a collection of the best Cordyceps photos I took during our Mushroaming Bolivia's Amazon Rain Forest Tour, January 20 through February 2, 2012. Unless otherwise specified the fungi were found between 250 to 400m a.s.l. All specimens have been deposited in the National Herbarium in La Paz, Bolivia.  Note all these fruiting bodies are growing post-mortem out of the parasitized insects.
Link to the 2014 Mushroaming Cordyceps Expedition to Tibet

Cordyceps acridophila 

3) On of my favorite specimens was this oldish 8 cm sphinxoid moth digested by a Cordyceps. It is an Akanthomyces species (Tatiana suggests A. pistilariformis), an anamorphic fungus related to Cordyceps. Anamorphic means this fungus does not reproduce sexually with spores, but produces conidia, which have the same DNA as the fungus. It already has shed all its conidia, which grow on the antenna-like structures, called conidiophores. Check out Isaria tenuipes below, that gives you an idea how many conidia can be grown by an anamorph. The fungus affixed the moth to the leaf so it can keep this great perch to disperse its "spores" successfully. Madidi National Park, Bolivia.

 

Isaria tenuipes

4) An Isaria tenuipes Peck, another Cordyceps-anamorph growing out of a Pupa of Noctunidae found in the hollow of a very decayed tree trunk.
Fruiting body height 5cm. Chalalan, Madidi National Park, Bolivia.


5) Another Isaria tenuipes with tons of conidia or conidiospores. The attic greek root of the term conidia means dust. Isaria is a cosmopolitan species. I am not sure if the infected insect was very hairy or some other organism is responsible for all the brittles. Chalalan, MadidiNational Park, Bolivia.

 

Ophiocordyceps australis

6) A red fruiting Ophiocordyceps australis fruiting from an ant between Xylaria fruiting bodies. At first I was just trying to get a picture of the Xylaria then I saw the Cordyceps. Key for finding Cordyceps is slowing down and looking carefully. Best substrate are decaying tree trunks, but many other locations are sites Cordyceps will direct its prey to before killing it and digesting it. Chalalan, Madidi National Park, Bolivia.


7) A transect of the head of an Ophiocordyceps australis reveals seed-like structures, which are the perithecia containing the asci-sacs in which the spores are produced. Size of the head is about 8 mm. Chalalan, Madidi National Park, Bolivia.
 

Ophiocordyceps australis 

8) Ophiocordyceps australis growing out of an ant.
Cerro Brujo, Rurrenabaque, Bolivia

 

Metacordyceps martialis? and Ophiocordyceps australis 

9) A late stage Metacordyceps, probably Metacordyceps martialis laying next to Ophiocordyceps australis. 
Found by Brendan O'Brian at Cerro Brujo, Rurrenabaque, Bolivia

Metacordyceps sp.?

10) A much fresher specimen, probably a Metacordyceps. The fruiting bodies are growing out of a coleopteran larva (length ca 6 cm).
Cerro Brujo, Rurrenabaque, Bolivia

The enlarged fruiting body 
10a) The yellow area in the center of the stromata contains mature perithecia. The darkish spots are the ostioles, the opening of the perithecium through which the spores are released. The top white part is not fully differentiated yet and still growing. When maturing it will turn yellow too and develop the pimpled surface due to growth of the perithecia.



11) Probably a Hirsutella, a Cordyceps anamorph. As typical for an anamorph this specimen is lacking a well-defined "head". Hirsutella-species will depend on the digested insect.  Found by Colden McClurg at Cerro Brujo, Rurrenabaque, Bolivia. Identified by Tatiana Sanjuan.



12) Ophiocordyceps kniphofiodes var. ponerinae jutting out of a dead trunk. Ponerinae refers to the group of ants this Ophiocordyceps attacks. I love the orange-black contrast. The orange is the fertile tissue. Identified by Tatiana Sanjuan. Chalalan, Madidi National Park, Bolivia.


12a) Here the same Ophiocordyceps kniphofiodes var. ponerinae with its victim or host, whichever perspective one takes, a Ponerinae ant dug out of the rotten wood. Unfortunately my camera was fogged-up that morning. Photographing in the rain forest, even when it does not rain is a real challenge. My flash stopped working for 5 days, but once out of the humidity it came back to life, go figure! Chalalan, Madidi National Park, Bolivia.



13) A similar looking Cordyceps we encountered in Coroico in the Yungas, the cloud forest belt in around 1500 m asl. Found by Nicole Cook.
If the host is a Megaloptera larvae, which it seems to be, then this would be the newly described Ophiocordyceps tiputini, according to Tatiana Sanjuan. 

14) Another ant-parasitizing Ophiocordyceps kniphofioides var. ponerinae. This stroma is not fully matured yet.
Found by Brendan O'Brien at Cerro Brujo, Rurrenabaque, Bolivia.


15) A brightly red fruiting Cordyceps growing out of some insect protein. Trying to figure out what it could be,  I came up with Cordyceps pruinosa due to color and perithecia shape and alignment. However, so far this species is not described from the neotropics, but known from East Asia. Tatiana Sanjuan informed me that she found many specimen of C. pruinosa in the Amazon and depending on the host it could be C. caloceroides (parasitizing on Theraphosidae / tarantula) or C. pruinosa (parasitizing eggs of Acrididae / grasshoppers). Furthermore she sugests that with application of KOH these fungi turn purple. Found by Pat Hill in Chalalan, Madidi National Park, Bolivia.


15a) Partly extracted from the log, the kink in one of the stromata was caused when it hit the tough bark and changed direction to find its way out.


15b) What color, what beautiful structure! Chalalan, Madidi National Park, Bolivia.




16) Fruiting bodies growing out of a mesh of palm roots. I waited for three days to unearth the host insect in hope the fungus would further mature. Unfortunately digging down to the host insect was impossible. It was all totally intertwined palm roots looking absolutely identical to the black lower part of the stromata and before I got to any insect I had already broken off or sliced off the fungal tissue from its elusive base. Last straw was when I cut my finger. Should have brought a big saw! Chalalan, Madidi National Park, Bolivia.


16a) Transect of the Cordyceps shown above. The perithecia are not fully developed yet. Larry Evans tried to find spores under the microscope, but to no avail.

 

Torrubiella sp.

17) A Salticidae spider fully enmeshed in fungal tissue by a Torrubiella species. Size is about 3 cm across. Found by Colden McClurg near Caquihuara Macaw Cliff, Madidi National Park, Bolivia.


17a) Looking at the top of the former spider. The ring-like structure and the round knobs inside the ring are packed with perithecia<radeditorformatted_1> of the Torrubiella fungus.


Link to the 2014 Mushroaming Cordyceps Expedition to East Tibet

Recently I came across a few new scientific publications on Cordyceps. Here is a short overview.

I was glad to see a new article by Yao et al. on the distribution area of Ophiocordyceps sinensis by a group of China-based researchers. The authors claim to having traveled the distribution area extensively, besides sifting through a lot of mostly Chinese sources to outline the current distribution. It does not really contain much new information regarding the extent of the distribution area beyond what my distribution maps (Winkler 2008 & 2009) already are showing. However, most interesting I find their on-site verification of the lowest altitude of caterpillar fungus distribution just around 3000m and debunking older claims of sites in the low 2000m.  Also the highest distribution of around 5000m is confirmed. Here a quote: " The lowest altitude recorded was 3,087 m with supporting collections [..] made in Xiaojin County, Sichuan Province. It is conceivable that 3,000 m is in general the reliable lowest altitude for the distribution of O. sinensis. The highest altitude was recorded as 5,048 m [..] collected in Nagqu County, Tibet." And of course I should mention that they collected lot of herbaria samples. 
However, Yao et al. claim to have published first records for twelve counties in Tibet AR previously not published does not really hold up. Several of these counties were already reported as Cordyceps sourcing area in the Atlas of Tibet AR (1996) I used as one of my sources for compiling the first Cordyceps distribution map I published in 2005 (Winkler 2005). Anyways, overall it was very helpful that a lot of Chinese language sources were scanned and a bunch of bad sources that reported Ophiocordyceps sinensis to grow outside of its distribution area were debunked.

Another paper authored by a team from researchers in Hong Kong describes microscopy techniques to verify Ophiocordyceps sinensis authenticity. Furthermore the team analyzed over 50 O. sinensis products on the market , the majority being the natural product, but the samples included also pills and clear counterfits. Not surprisingly there was not only caterpillar fungus in many products....

Very interesting from a taxonomic point is an article on Metacordyceps taxonomy by Kepler et al. 2011. So far Metocordyceps was only described from East Asia, but now it is apparent that it is also distributed in the Neotropics. Already in February 2011 I found Metacordyceps in Ecuador's Amazon Rain forest, but back then it was not published yet as distributed in the Americas. 
A picture of a Metacordyceps is posted below.

A medical article comparing Ophiocordyceps sinensis with Cyclosporin by Ding et al. 2011, a Chinese team of doctors from Xian was published and concluding that the Cs and cyclosporin recipients did not show significantly different outcome, but Cs recipients had less complications, if I understand the abstract correctly and it gets more techincal quickly.


Sources:
Atlas of AR [Xizang Zizhiqu Dituce] (1996). Zhongguo Ditu Chubanshe Chuban (China Cartographic Publishing House), Beijing, 1-167. (in Chinese)

Au D, Wang L, Yang D, Mok DK, Chan AS, Xu H. 2011. Application of microscopy in authentication of valuable Chinese medicine I--Cordyceps sinensis, its counterfeits, and related products. Microsc Res Tech. 75.1:54-64. pdf

Ding C, Tian PX, Xue W, Ding X, Yan H, Pan X, Feng X, Xiang H, Hou J, Tian X. 2011. Efficacy ofCordyceps sinensis in long term treatment of renal transplant patients. In: Front Biosci (Elite Ed). 2011 1.3:301-7. www.ncbi.nlm.nih.gov/pubmed/21196310

Kepler RM, Sung GH, Ban S, Nakagiri A, Chen MJ, Huang B, Li Z, Spatafora JW. 2012. New teleomorph combinations in the entomopathogenic genus Metacordyceps. Mycologia 104(1):182-97.

Winkler, D. 2005. Yartsa Gunbu - Cordyceps sinensis. Economy, Ethno-mycology & Ecology of a Fungus Endemic to the Tibetan Plateau. 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. link

Winkler, D. 2008. Yartsa Gunbu (Cordyceps sinensis) and the Fungal Commodification of the Rural Economy in Tibet AR. Economic Botany 63.2: 291-306. pdf

Yi Li, Xiao-Liang Wang, Lei Jiao, Yi Jiang, Hui Li, Si-Ping Jiang, Ngarong Lhosum Tseiring,
Shen-Zhan Fu, Cai-Hong Dong, Yu Zhan, and Yi-Jian Yao 2011. A Survey of the Geographic Distribution of Ophiocordyceps sinensis. Journal of Microbiology 49.6, pp. 913-919. pdf