Stinkhorns: Fungi No One Can Love?

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"If you are able to give, the Friends of GMNH is still one of the most important funding resources that our Georgia Museum of Natural History has these days. In the absence of our fundraising gatherings, your donations and memberships are important to us and we will be eager to get back to regular activities when it is safe to do so."

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This post first appeared in the weekly Newsletter of the Friends of GMNH and appears here courtesy of Dr. Robert Wyatt.

Stinkhorns: Fungi No One Can Love?

by Dr. Robert Wyatt

Those of us with broad interests in natural history enjoyed a stellar year for fungi in the late summer and fall of 2020.  Unusually high rainfall coupled with prolonged warm temperatures brought forth a diverse array of mycological wonders.  In my yard perhaps the most intriguing of these were the stinkhorns (Phallales), which first announced their presence to me via their putrid smell, reminiscent of decaying flesh.  And then I spied the horn, which, as the Latin name implies, looks very much like a phallus.  They certainly deserve their common name!

Phallus ravenellii with large and small flies feeding on the gleba

These interlopers arrived in mid-October but stayed around, appearing sporadically depending on weather conditions, until December.  The first wave was the largest, with perhaps as many as 100, spread across several clusters, suddenly springing up from coarse mulch applied earlier in the summer along our driveway.  Ann and I quickly identified this distinctive species as Phallus ravenellii, named "in honor" of Henry William Ravenel, a South Carolina planter and botanist who described many new species of fungi and flowering plants.  [I use quotation marks because one might wonder exactly how pleased Ravenel was to receive the dubious distinction of having a stinkhorn dubbed "Ravenel's Phallus."]
 

One of the largest clusters of Phallus ravenellii

 

In any case, this mushroom is hard to miss, reaching a height of 10 cm or more with a white, spongy stem that is hollow and a cap covered with a gray-green gelatinous gleba in which the spores are embedded.  These above ground structures last only a day or two, but more may emerge from "eggs" located just below the surface.

"Egg" of Phallus ravenellii and American carrion beetle

 

The elevation of the stalk occurs surprisingly rapidly (see time-lapse film at this link).  Every time I checked these 'shrooms, they were covered with small to large flies including fruit flies (Drosophilidae), fungus gnats (Mycetophilidae), and house flies (Muscidae) apparently enjoying the banquet of bad-smelling, but presumably tasty and nourishing, slime . Harder to see because of their ability to disappear very quickly were green and black beetles that proved to be American Carrion Beetles (Necrophila americana), which normally feed on dead and decaying animal flesh.

Necrophila americana American carrion beetle

At first I thought the flies and beetles might be dupes of the stinkhorn -- tricked into visiting by the distinctive odor and picking up and transporting spores inadvertently on their legs and bodies.  But they were regularly present and lingered as long as slime was available.  Apparently, the gleba is highly nutritious, and the spores and slime are purposely ingested by insects, which carry relatively few spores on the outside of their bodies (Tuno, 1998).  This intrepid Japanese researcher examined hundreds of fly rectums and found, on average, drosophilids harbored 35,000 to 240,000 spores, whereas muscids contained 1,680,000!  And germination of these spores was > 90%.  This would seem to answer a question posed by Roy (1994), who wondered if the attraction of flying insects was really advantageous to stinkhorns.  The latter are not pathogenic and therefore differ from the rust and smut fungi whose spores are delivered by confused flies to infect flowers of the plants she studied.  It seems likely that these insects defecate spores in areas conducive for growth of stinkhorns, spore germination is enhanced (or at least not diminished) after passage through fly digestive tracts, and spores may grow better in the nitrogen-enhanced environment that fly feces provide.
There is a further wrinkle to this story.  Recently, Teichert et al. (2012) discovered a bizarre understory tree in Brazilian rainforest that they argue is pollinated by certain nitulid and scarab beetles that ordinarily disperse spores of stinkhorns.  The odor chemistry of the foul-smelling flowers of Dugetia cadaverica (Annonaceae) involves molecules typically associated with the smells of carcasses and cheese and which are chemically similar to the characteristic earthy odors of fungi.  They conclude that this plant deceives the beetles using visual cues, such as flowers produced at ground level that resemble mushrooms, as well as olfactory ones.  [I am not making this up!]
Here are a couple more links:  (https://www.mushroomexpert.com/phallaceae.html) and (https://www.walterreeves.com/landscaping/stinkhorn-mushroom-identification-and-control/).
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Dr. Robert Wyatt obtained his bachelor's degree from the University of North Carolina at Chapel Hill and his doctorate from Duke University, both in Botany. He taught for two years at Texas A&M University before joining the faculty at the University of Georgia, where he was a Professor of Botany and Ecology for more than 20 years. From 1999 to 2005 Dr. Wyatt was the Executive Director of the Highlands Biological Station, an interinstitutional center of the University of North Carolina. He has won numerous awards for teaching and research, including a Guggenheim Fellowship that enabled him to produce a book entitled Ecology and Evolution of Plant Reproduction. He has trained more than 40 graduate students, received millions of dollars in research grants, and published more than 160 scientific papers.