Author’s note: This blog post is rated not safe for lunch. Actually, it’s rated not safe for breakfast, lunch, dinner, or teatime. I debated whether I should even write it it’s so revolting but a friend who reports for KUNC convinced me I should. So … blame public radio.

The opening line of a new paper in Scientific Reports reads, “Parasites and their hosts cohabit the same body, but they have strongly divergent interests in how to make use of it,” – to which I instantly thought, “like any married couple in a car”.

Only in this case, one spouse is actively trying to kill the other.

Such is the case for the fungus Massospora cicadina and its hapless victim, the periodical cicada (Magicicada sp.). North Americans have a love-hate (some would say hate-hate) relationship with this plump insect, which has a bizarre habit of emerging en masse every 13 or 17 years to eat, mate, and drive area humans to distraction with their shrill, 100-decibel screeching. What can you do? If life gives you cicadas, make cicada ice cream.

When I was about seven or eight a brood emerged around us in northern Kentucky. I had endless fun plucking the adults off their perches by pinching their wings – they were docile like cows, so you could walk right up to them – and studying the fat, red-eyed insects. I do not recall seeing any that were horrifically maimed. But as it turns out, there is one parasite that has adapted to the periodical cicada life cycle, waiting patiently in the soil for 13 or 17 years for their victims to emerge. This is Massospora cicadina, and it makes its own version of cicada ice cream.

Cicada nymphs live underground for those 13 or 17 years, sucking the juices from plant roots. When the magic moment comes and they burrow to the surface, some of them come into contact with spores of the fungus. About two to five percent of them end up infected.

After finding its way inside its shiny new cicada, the fungus makes itself right at home by multiplying mercilessly into thousands of white, powdery spores. These spores are conidia, asexually-produced reproductive cells, and are termed a Stage I infection. These spores are infectious to other adult cicadas.

Cicadas infected by conidia experience a similar infection, termed Stage II, that results in sexually-produced spores. These spores are meant to find their way to the soil, where they can withstand more than a dozen years of environmental abuse as they await their next meal.

Cicadas infected by either kind of spore acquire an abdomen swollen with chalky white spores, ultimately causing both their reproductive equipment and several terminal segments of their body to fall off, leaving a gruesome open wound.

Of course, being cicadas, not only do they not grasp the horror of their situation, they have no idea they are infected or that they can infect other cicadas. So they also go on doing all the normal things cicadas do during their month topside. All the things.

Which produced this horrifying sentence, brought to you verbatim from the esteemed pages Nature’s own Scientific Reports, “…[T]hus, it is relatively common to find a healthy cicada with its genitalia plunged into the abdominal spore mass of an infected partner or to see healthy cicadas attached to fragments of abdomen or terminalia that have torn free from infected partners during attempted copulation.”

Oh god.

"Uninfected male Magicicada septendecim (left) with genitalia torn from a female infected by Stage I of Massospora cicadina (right)." Credit: Fig. 2 Cooley et al. 2018

Mating isn't the only thing infected cicadas do, of course. Cicadas infected by Stage I spores tend to drag their gaping abdomens behind them, leaving a trail of spores, not unlike (and I’m just not going to hold back today) a dog dealing with infected anal sacs. Cicadas infected with Stage II spores also do this, but “spend relatively more time than Stage I cicadas flying and visibly spewing spores from their damaged abdomens.” Remember, the goal of Stage II spores is not to find another host, but to end up in soil likely to be home to baby cicadas.

But it gets worse. Because Massospora decided that all this just wasn’t quite evil enough. It really needed to up the ante. So, as the scientists reveal in their graphic new paper, males who are infected with Stage I spores will respond to the mating calls of other males by flicking their wings – something only healthy, receptive females usually do. And, cicadas being cicadas, you can guess the result.

Thus, males are more likely to become infected than females because they will mate with infected females but also with infected males. But what if this was just a side effect of infection? What if something about having your entire abdomen filled with evil fungal spawn had some sort of generic feminizing effect?

The scientists thought about this possibility. But only males infected with Stage I spores flick their wings in response to male calls. Stage II infected males do not. If male wing-flicking was simply a side effect of being infected by Massospora, we would expect both types of infected males to behave this way. So it seems likely the behavior is an active fungal stratagem to improve its reproductive potential. There may be two organisms living in the cicada's body, but only one them has their hands on the wheel, and it's not the cicada.

Massosspora has also been shown to manipulate the sexual behavior of at least one other non-periodical cicada, and more examples in other species are suspected. So, the authors conclude, to the general phenomenon of zombie insects whose behavior is manipulated by parasitic fungi (a large category mycologists refer to as entomophthoralean fungi), we may now add fungi that mess with insect bedroom behavior. As they say, all is fair in love and war. This is both.

Reference

John R. Cooley, David C. Marshall, Kathy B. R. Hill. A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada). Scientific Reports, 2018; 8 (1) DOI: 10.1038/s41598-018-19813-0