|Magicicada sp. infected with Massospora cicadina. Note the spore mass that has replaced the abdomen of the cicada.|
Massospora cicadina is a fungal pathogen that infects 13 and 17 year periodical cicadas in two stages resulting in the formation of a conidial pustule that erupts from the cicadas abdomen, leading to infertility and eventual death. Currently, the fungus is not known to occur on any other host.
M. cicadina was first observed by Leidy in 1850 but was not described until 1879 by Charles Horton Peck. Peck placed the fungus among the class Coniomycetes, but in 1888 Thaxter and Forbes placed it instead in Entomophthoraceae. It wasn't until 1921 that the pathogen's microscopic characteristics were thoroughly studied by Speare, who found that conidia germinate quickly when placed in a nutrient substance.
M. cicadina infects the genus Magicicada, which consists of 13 and 17-year periodical cicadas. Magicicada spends most of its life underground feeding on xylem fluids of tree roots, and emerge from underground every 13 or 17 years. While their lifestyle lasts such a long period, adult periodical cicadas are only active for 4 to 6 weeks during which they deposit their eggs on tree roots. Females attract males for mating through flicking their wings, while males produce a mating call. When depositing eggs, the female cicada will cut a V-shaped cut into a tree root's bark and can deposit up to 600 or more eggs.
Spores of M. cicadina are capable of germinating and infecting cicadas at as little as one year but may remain dormant for either 13 or 17 years before becoming active. This is a synchronous cycle that corresponds with the periods between cicada emergences. M. cicadina is thought to be the only known pathogen that coincides with cicada life cycle, and because of this it is considered to have the longest life cycle of any fungus. M. cicadina resting spores however do not require a dormancy between cicada emergences. Resting spores are capable of germinating and infecting periodical cicadas after less than a year from their introduction into the soil. Cicadas first become infected by fungal spores as the nymphs dig tunnels to the surface days before their emergence from the soil as adults.
There are two infectious forms of M. cicadina a cicada can become infected with, called Stage I and Stage II, each producing different spores. While the mycelial development of M. cicadina spores in its cicada host have not been studied thoroughly, they are thought to have similar developmental stages to other Entomophthoromycotina fungal species.
During Stage I infection, the mycelium of M. cicadina gives rise to hyphal bodies that form into binucleate condidiosphores, forming a honeycomb-like septum across the cicada's body cavity. The vegetative growth of M. cicadina is restricted to the softer tissues in the posterior segments of the cicada, resulting in the progressive sloughing off of these posterior abdominal segments as they rot away. The fungus that sprouts as a pustule from the abdominal region of the cicada is endogenous in origin and consists of a granular conidial mass. There is no difference found in the time it takes for the cicada's abdominal segments to fall off between male and female cicadas. While the sloughing off of these segments causes female and male sterility, it does not kill the cicada immediately, allowing it to fly and walk around as usual, spreading the spores to other healthy individuals. This infection process is unique to M. cicadina.
The spores produced during Stage II infection are resting spores that also develop from hyphal bodies. However the hyphal bodies during this stage are tetranucleate and longer than those of stage I spores. Instead of forming special cavities, resting spores are distributed evenly throughout its host's body cavity.
Stage I Infection
Initial infection takes place while cicada nymphs dig their way to the surface of the soil. Stage I infected cicadas produce haploid conidiospores, forming the asexual conidial stage of the fungus. Spores produced by Stage I infected cicadas are capable of infecting other adult cicadas. There is no difference found between the proportion of male to female nymphs being infected by spores in this stage. In the early stages of infection during Stage I, the infection is completely concealed inside the abdomen of the cicada. However near the death of the host, the rear segments of the abdomen fall off, revealing a white, chalky mass of the fungus, which actively produces and forcibly discharges spores. Because of this method spreading of Stage I spores, cicadas infected with M. cicadina have been commonly referred to as "flying salt shakers of death". Stage I infected cicadas are observed to spend more time walking around and dragging their abdomen to aid in the spreading of condidiospores for further infection of other cicadas. This is a behavioral change thought to be the result of a fungal extended phenotype, the physical inflictions of the infected cicadas, or the general phenology of cicada life cycles. Stage I infected males respond to mating calls of both males and females and attract healthy males through flicking their wings, a behavior only observed in healthy females. This altered behavior aids cicadas in the conidial stage of M. cicadina with infecting healthy cicadas. Stage I infected males also tolerate mounting from courting males, suggesting that M. cicadina alters insect sexual behavior to increase infection rates.
Stage II Infection
Cicadas that come into contact with an infected adult cicada contract Stage II infection. During Stage II infection, the fungus produces a different kind of spore, which have thick, ornamented walls and are not directly infective to adult cicadas. Instead, these spores lie dormant in soil and will infect the next generation of cicadas during their next 13 or 17 year emergence from the soil. The fungus renders both males and females sterile, though the insect may remain alive and mobile while discharging spores. Infected cicadas display some normal behavior such as sexual responsiveness, and even copulation between infected and healthy cicadas has been observed. As cicada males form large chorus centers during mating, the infection rate of males with the resting spore stage is typically higher than infected females at this stage. Conidia that fill the abdomens of infected males at this stage also alter the pitch of their mating call, resulting in them sounding smaller than they actually are to females, which may also contribute to the prevalence of higher infection rates in males than in females.
Species of the genus Massospora are believed to be found in all habitats of their host species, which includes large temperate ranges in the Southern and Northern hemispheres.
The density of cicadas over one 17-year cicada emergence period was found in one study to have dropped by one half due to infections from the fungus, while the amount of infected cicadas producing resting spores increased by 9-fold. This suggests that the fungus can be utilized as a control agent in decreasing the significant damage cicadas impose on tree roots they lay their eggs on during their periodical emergences. Studies of M. cicadina and its host can also provide insights into biological clocks and environmental signaling due to their synchronous life cycles.
Similar Host-parasite Systems
Other parasites that specifically hijack host sexual behaviors include the cicada Okanagana rimosa of the Tibicininae subfamily. These parasites also produce condidiospores during infection in mechanisms similar to Stage I infections in M. cicadina.
- Edward., Steinhaus (2014). Insect Pathology V2 An Advanced Treatise. Elsevier Science. ISBN 9780323143172. OCLC 1044715985.
- Duke, L.; Steinkraus, D.C; English, J.E; Smith, K.G (2002-05-01). "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:10.1016/S0022-2011(02)00040-X. ISSN 0022-2011. PMID 12234535.
- Cooley, John R.; Marshall, David C.; Hill, Kathy B. R. (2018-01-23). "A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada)". Scientific Reports. 8 (1): 1432. doi:10.1038/s41598-018-19813-0. ISSN 2045-2322. PMC 5780379. PMID 29362478.
- "Flying salt shakers of death :Cornell Mushroom Blog". blog.mycology.cornell.edu. Retrieved 2018-10-23.
- Speare, A. T. (1921). "Massospora cicadina Peck: A Fungous Parasite of the Periodical Cicada". Mycologia. 13 (2): 72–82. doi:10.2307/3753297. JSTOR 3753297.
- White, Joann; Lloyd, Monte (1983-08-01). "A Pathogenic Fungus, Massospora cicadina Peck (Entomophthorales), in Emerging Nymphs of Periodical Cicadas1 (Homoptera: Cicadidae)". Environmental Entomology. 12 (4): 1245–1252. doi:10.1093/ee/12.4.1245. ISSN 1938-2936.
- A specialized fungal parasite ( Massospora cicadina ) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada )
- Infectivity of resting spores of Massospora cicadina (Entomophthorales: Entomophthoraceae), an entomopathogenic fungus of periodical cicadas (Magicicada spp.) (Homoptera: Cicadidae)
- The Ecology, Behavior and Evolution of Periodical Cicadas
- Periodical Cicadas
- Flying Salt Shakers of Death, an article about Massospora species on the Cornell Mushroom Blog.