Cicada STDs, Suicidal Crickets, and the Truth About Flamingos

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In the summer of 2016, billions of periodical cicadas of the Magicicada genus appeared in the northeastern United States, erupting from the land after nearly two decades of maturing underground. As usual, they would proceed to spend the subsequent five to six weeks of their remaining lives foraging for food and having sex, calling out to mates by flicking their wings, generating distinct mating songs. Nature was taking its course—including the butt-eating, sexually-transmissible fungal pathogen, Massospora cicadina.

Periodical cicadas are first infected by Massospora as nymphs—the “adolescent” stage of insects that undergo metamorphosis—where the spores germinate and remain dormant until their cicada hosts emerge from the soil in the summer (Duke, Steinkraus, English, & Smith, 2002). Once above ground, the spores undergo massive growth within their hosts’ abdomens, consuming their organs in the process. As the fungus grows to capacity and its host is drawing closer to its unfortunate end, the hard exoskeletal panels encasing the abdomen is shed, revealing a white plug-like structure underneath—a giant mass of Massospora spores (Kasson et al., 2018). This “plug” allows the infected host to rain down Massospora over the soil as it flies through the air, sowing the seeds of death (well, spores of death) for the next generation of cicadas that will emerge after 13-17 years underground.

And if this phenomenon wasn’t strange enough by itself, these “flying saltshakers of death” are also hopped up on quite a variety of drugs, specifically amphetamines and psychoactive hallucinogenics produced by the fungus to control the host’s behavior (Kasson et al., 2018). While the drugs potentially explain why the cicadas seem to be totally fine despite having an entire third of their bodies consumed by a pathogenic fungus, they seem to also have another unexpected side effect: hypersexuality in males (Kasson et al., 2018). Horny and pumped with behavior-altering drugs, infected males go out into the world trying to mate with anything they can find, even other males, attracting them by mimicking female mating signals. These cicadas cannot truly mate—their genitals have either been consumed by Massospora or sloughed off with the rest of their bodies—but the physical contact during the act allow the spores to potentially find new hosts.

Pretty terrible end of the stick for the cicada, but c’est la vie.

Now, in case you’re sitting there wondering why I’m rambling about cicada STDs, here’s the point: “mind-controlling”—or, more accurately, behavior-altering—parasites are a fascinating, terrifying, and often morbidly entertaining existence in nature that is unapologetically absurd and brutal in how it sustains itself. Massospora cicadina is only one of the countless number of obligate parasites—parasites that depend on a host to complete its lifecycle—that upon infection can chemically manipulate a host organism to do its bidding. Unable to reach maturity or reproduce on its own, they evolved the ability to transmit themselves into host organisms, a crucial development for the survival and reproductive success of the humble parasite. As a result, they have developed intricate and shockingly complex evolutionary strategies in order to end up in the perfect host.

At the most fundamental level, the goal of a parasite is to get from Point A to Point B. Some species—such as our dear friend, Massospora cicadina, or the infamous zombie ant fungus, Ophiocordyceps unilateralis—are perfectly happy spending the rest of their days feeding off and reproducing within a single organism, releasing their spores out into the world once they’re done with it.

Other parasites are not so easily satisfied; rather than simply moving from A to B, their journey involves jumping from A to B to C, to perhaps even a D, going from host to host until they reach their desired environment or “final host”.

A fascinating example of this is a class of parasitic tapeworms known as Cestoda that frequently infect Artemia parthenogenetica, or brine shrimp (you might recognize them as thoses painfully underwhelming sea monkeys that were all the rage in the 50s). Brine shrimp contain a specific type of organic pigment called a carotenoid, which they get from consuming a type of algae that naturally produce carotenoids. Carotenoids are responsible for the orange and red coloration of fruits and vegetables such as carrots, pumpkins, strawberries, etc. When infected with cestodes, the brine shrimp begin to swim closer to the surface and to each other, increasing their exposure to ultraviolet light; this activates the “photoreceptive functions” of the carotenoids within the brine shrimp, causing them to exhibit red pigmentation (Sánchez, Georgiev, & Greene, 2007).

So why go through all this trouble to expose their hosts to predators? The answer is flamingos. Cestodes alter the pigmentation and behavior of their brine shrimp hosts to make them more vulnerable to predation by flamingos, opening up a direct pipeline to their desired destination: their guts. For these cestodes, the flamingo gut is the ideal environment for sexual reproduction, and the eventual final host.

But what if there is no final host? What if the parasite is only fixing to get from one place to another? Paragordius tricuspidatus, or the horsehair worm is one such parasite. Rather than using its host organism as a baby-making factory or an all-you-can-eat buffet, it uses its host as a means of transportation, “controlling” its mind to seek out water. When Paragoridius infects its insect host, the cricket Nemobius sylvestris—dubbed the “kamikaze cricket” for reasons you will see in a bit—it sets off a series of biochemical changes in the cricket’s brain to alter its behavior, leading it to commit “suicide” by jumping into bodies of water such as swimming pools or streams (Thomas et al., 2003). Once in the water, the worms—who have been steadily growing within the cricket’s body up until this point—exit the insect’s carcass and immediately begin mating. From then on, the worms are free-living in the water and no longer require a throwaway host to meet an untimely end.

From mind-altering cicada STDs to suicidal cricket worms, parasitism is a vicious cycle of consumption, behavioral manipulation, and truly miserable deaths. On the surface it seems like such an ugly thing—inherently predatory, macabre, and completely unforgiving—but the truth is, they only take as much as they give. Do you recall the suicidal crickets from before? The discarded cricket carcasses eventually end up as food for fish and other aquatic animals living in the bodies of water they drowned in (Sato et al., 2011). Parasites do give back—perhaps not to their hosts, but certainly back to their ecosystems.

Parasites are a living, breathing testament to the tenacity and adaptivity of nature. These organisms cannot think; their cognitive capabilities are primitive at best, and some don’t even possess brains or nervous systems. There is no “master plan,” no strategical meeting; it’s all the result of over millions of  years of evolution, millions of years of living and mating and dying, all of this culminating in the hope that perhaps, perhaps this species might carry on. The sheer complexity of a process that too many perceive as random trial and error (it’s not; evolution is directional and by no means random or left to chance) can regulate an entire sector of life that we as humans fail to even notice until it’s gone. It’s frightening and awe-inspiring, oft overlooked and completely humbling; this is the magic—or, the science—behind crazy, stranger-than-fiction behavior of parasites.


Resources:

Boyce, G., Gluck-Thaler, E., Slot, J. C., Stajich, J. E., Davis, W. J., James, T. Y., . . . Kasson, M. T. (2018). Discovery of psychoactive plant and mushroom alkaloids in ancient fungal cicada pathogens. bioRxiv. doi:10.1101/375105

Duke, L., Steinkraus, D. C., English, J. E., & Smith, K. G. (2002). Infectivity of resting spores of Massospora cicadina (Entomophthorales: Entomophthoraceae), an entomopathogenic fungus of periodical cicadas (Magicicada spp.) (Homoptera: Cicadidae). Journal of Invertebrate Pathology, 80(1), 1-6. doi:https://doi.org/10.1016/S0022-2011(02)00040-X

Libersat, F., Kaiser, M., & Emanuel, S. (2018). Mind Control: How Parasites Manipulate Cognitive Functions in Their Insect Hosts. Frontiers in Psychology, 9(572). doi:10.3389/fpsyg.2018.00572

Sánchez, M. I., Georgiev, B. B., & Green, A. J. (2007). Avian cestodes affect the behaviour of their intermediate host Artemia parthenogenetica: An experimental study. Behavioural Processes, 74(3), 293-299. doi:https://doi.org/10.1016/j.beproc.2006.11.002

Sato, T., Watanabe, K., Kanaiwa, M., Niizuma, Y., Harada, Y., & Lafferty, K. D. (2011). Nematomorph parasites drive energy flow through a riparian ecosystem. Ecology, 92(1), 201-207.

Thomas, F., Ulitsky, P., Augier, R., Dusticier, N., Samuel, D., Strambi, C., . . . Cayre, M. (2003). Biochemical and histological changes in the brain of the cricket Nemobius sylvestris infected by the manipulative parasite Paragordius tricuspidatus (Nematomorpha). International Journal for Parasitology, 33(4), 435-443. doi:https://doi.org/10.1016/S0020-7519(03)00014-6