Fungus infections

Fungus infection
Massospora cicadina infection.

Periodical cicadas are subject to infection by the specialized fungal parasite Massospora cicadina Peck (Speare 1919, Marlatt 1923). Infection follows a predictable phenology. Early in a periodical cicada emergence “Stage I”, infected cicadas produce conidia capable of infecting other adult cicadas (Speare 1921, Soper 1974, Soper et al. 1976). Later in the emergence “Stage II” cicadas infected by conidiospores produce resting spores that complete the fungal life cycle by infecting the next generation of cicada nymphs that will emerge from the soil 13 or 17 years later (Soper et al. 1976, Duke et al. 2002).

The most amazing thing about the fungus? It turns infected cicadas into “zombie insects” that disperse more fungus by causing males infected with Stage I to produce wing-flick signals as if they were females– making them highly attractive to cicadas of both sexes (Cooley et al. 2018)! This example is unusual in the “zombie insect” literature in that infected cicadas are co-opted to become active spore dispersers while they are still alive; many similar host-parasite systems accomplish dispersal only once the host is dead. Furthermore, Massospora also produces powerful psychoactive chemicals whose function is not well understood (Boyce et al. 2019).

This video describes the fungus life cycle and how it turns cicadas into “zombie insects.”

 

Literature

Alexander, R. D. 1967. Acoustical communication in arthropods. Annual Review Of Entomology 12:495-526.

Boyce, G. R., E. Gluck-Thaler, J. C. Slot, J. E. Stajich, W. J. Davis, T. Y. James, J. R. Cooley, D. G. Panaccione, J. Eilenberg, H. H. De Fine Licht, A. M. Macias, M. C. Berger, K. L. Wickert, C. M. Stauder, E. J. Spahr, M. D. Maust, A. M. Metheny, C. Simon, G. Kritsky, K. T. Hodge, R. A. Humber, T. Gullion, D. P. G. Short, T. Kijimoto, D. Mozgai, N. Arguedas, and M. T. Kasson. 2019. Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying cicada pathogens. Fungal Ecology 41: 147-164.

Cantrall, I. J. 1937. Notes on the infection of the seventeen-year cicada, Magicicada septendecim (Linn.) by the fungus Massospora cicadina Peck. Bulletin of the Brooklyn Entomological Society 32:120-121.

Cooley, J. R. 1999. Sexual behavior in North American cicadas of the genera Magicicada and Okanagana. Ph.D. The University of Michigan, Ann Arbor.

Cooley, J. R., Marshall, D. C., & Hill, K. B. R. 2018. A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada). Scientific Reports, 8(1): 1432.

Duke, L., D. C. Steinkraus, J. E. English, and K. G. Smith. 2002. Infectivity of resting spores of Massospora cicadina (Entomophthorales : Entomophthoraceae), an entomopathogenic fungus of periodical cicadas (Magicicada spp.) (Homoptera : Cicadidae). Journal Of Invertebrate Pathology 80:1-6.

Dunning, D., J. Byers, and C. Zanger. 1979. Courtship in two species of periodical cicada, Magicicada septendecim and Magicicada cassini. Animal Behaviour 27:1073-1090.

Lloyd, M., J. A. White, and N. Stanton. 1982. Dispersal of fungus-infected cicadas to new habitat. Environmental Entomology 11:852-858.

Lovett, B., A. Macias, J. E. Stajich, J. Cooley, J. Eilenberg, H. H. d. F. Licht, and M. T. Kasson. 2020. Behavioral betrayal: How select fungal parasites enlist living insects to do their bidding. PLOS Pathogens (In Press).

Marlatt, C. L. 1923. The Periodical Cicada. United States Department of Agriculture, Bureau of Entomology Bulletin 71:1-183.

Soper, R. 1963. Massospora levispora, a new species of fungus pathogenic to the cicada Okanagana rimosa. Canadian Journal of Botany 41:875-878.

Soper, R. 1974. The genus Massospora entomopathogenic for cicadas. Part I. Taxonomy of the genus. Mycotaxon:13-40.

Soper, R., A. J. Delyzer, and L. F. R. Smith. 1976. The genus Massospora entomopathogenic for cicadas. Part II. Biology of Massospora levispora and its host Okanagana rimosa, with notes on Massospora cicadina on the periodical cicadas. Annals Of The Entomological Society Of America 69:89-95.

Speare, A. T. 1919. The Fungus Parasite of the Periodical Cicada. Science 50:116-117.

Speare, A. T. 1921. Massospora cicadina Peck, a fungous parasite of the periodical cicada. Mycologia 13:72-82.

White, J., P. Ganter, R. McFarland, N. Stanton, and M. LLoyd. 1983. Spontaneous, field-tested and tethered flight in healthy and infected Magicicada septendecim L. Oecologia 57:281-286.

White, J., and M. Lloyd. 1983. A pathogenic fungus, Massospora cicadina Peck (Entomophthorales) in emerging nymphs of periodical cicadas (Homoptera: Cicadidae). Environmental Entomology 12:1245-1252.