Massospora cicadina

Massospora cicadina is a fungal pathogen that infects only 13 and 17 year periodical cicadas. Infection results in a "plug" of spores that replaces the end of the cicada's abdomen while it is still alive, leading to infertility, disease transmission, and eventual death of the cicada.

Massospora cicadina
Magicicada sp. infected with Massospora cicadina. Note the spore mass that has replaced the abdomen of the cicada.
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Fungi
Division: Entomophthoromycota
Class: Entomophthoromycetes
Order: Entomophthorales
Family: Entomophthoraceae
Genus: Massospora
Species:
M. cicadina
Binomial name
Massospora cicadina
Cicada with extensive fungus on abdomen

Systematics

M. cicadina belongs to the phylum Zoopagomycota, subphylum Entomophthoromycota, and order Entomophthorales. About a dozen other species of Massospora are known, each of which attacks a specific species of cicada.

Discovery

In 1845, John H. B. Latrobe read a memoir of Benjamin Banneker at a meeting of the Maryland Historical Society. Latrobe reported that Banneker had in April 1800 described in his record book some of the characteristics of the periodical cicada, whose Brood X would soon begin emerging where he lived. In his description, Banneker wrote that the insects:

... begin to Sing or make a noise from first they come out of the Earth till they die. The hindermost part rots off, and it does not appear to be any pain to them, for they still continue on Singing till they die".[1]

In 1851, Joseph Leidy described and illustrated the fungus that had apparently caused the abdominal "rot" that Banneker had observed.[2][3][4] In 1879, Charles Horton Peck described the fungus and named it Massospora cicadina.[2][4][5] Peck placed the fungus among the class Coniomycetes, but in 1888 Thaxter and Forbes placed it instead in Entomophthoraceae. It was not until 1921 that the pathogen's microscopic characteristics were thoroughly studied by Speare,[6] who found that conidia germinate quickly when placed in a nutrient substance.[7]

Hosts

M. cicadina infects Magicicada species, which are 13 and 17-year periodical cicadas. Magicicada species spend most of their lives underground as nymphs, feeding on xylem fluids of tree roots.[8] They dig upwards through the soil to molt into adults and emerge above ground after 13 or 17 years. Adult periodical cicadas live only for 4 to 6 weeks, to mate and deposit their eggs. Females attract males for mating by flicking their wings, while males produce a mating call. After mating, female cicadas deposit up to 600 or more eggs in V-shaped cuts on tree twigs (usually 20 eggs at a time in each cut).[8]

Life cycle

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 synchronous cycle corresponds with local periods of cicada emergence. M. cicadina is thought to be the only pathogen that coincides with its host's 17-year life cycle; because of this it is considered to have the longest life cycle of any fungus.[9][10]

M. cicadina resting spores do not require a dormant period: They are capable of germinating and infecting periodical cicadas after less than a year from their introduction into soil. Cicadas are believed to become infected by fungal spores as the nymphs dig tunnels to the soil surface days before their emergence as adults.[10][11]

Infection

Stage I infection

Initial infection takes place while cicada nymphs dig their way to the surface of the soil before emerging as adults.[10][11] It is presumed that the emerging cicadas are infected by resting spores they encounter in the soil. In early stages of infection, hyphal bodies of the fungus are found in the host tissues. Later, Stage I infected adult cicadas produce haploid conidia, forming the asexual stage of the fungus.[9] Conidia produced by Stage I infected cicadas are capable of infecting other adult cicadas.

There is no difference between the proportion of male to female nymphs being infected by spores in this stage.[12] In the early stages of Stage I infection, the infection is completely concealed inside the abdomen of the cicada. Some time before the death of the host, the rear segments of the abdomen fall off, revealing a white, chalky mass or "plug" of the fungus, which produces spores. Because of this method of spreading of Stage I spores, cicadas infected with M. cicadina have been referred to as "flying salt shakers of death". Infected cicadas are infertile.

Stage I infected cicadas are observed to spend more time walking around and dragging their abdomen, which may aid in spreading conidia that infect other cicadas. This behavioral change is thought to be the result of a fungal extended phenotype, the physical afflictions of the infected cicadas, or the general phenology of cicada life cycles.[10] Progression in male and female cicadas is similar, including the time elapsed before the abdominal segments fall off.[12]

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 in infection of healthy cicadas.[10] Stage I infected males also tolerate mounting from courting males, suggesting that M. cicadina alters insect sexual behavior to increase infection rates.[9] The fruiting bodies of M. cicadina on Stage I infected adult cicadas possess a substituted amphetamine alkaloid, cathinone.[13]

Stage II infection

Cicadas that come into contact with conidia from an infected adult cicada contract Stage II infection. During Stage II infection, the fungus produces a different kind of spore: resting spores that have thick walls and are not directly infectious to adult cicadas. Instead, the resting spores lie dormant in soil and will infect the next generation of cicadas during their next 13 or 17 year emergence from the soil.[6]

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.[6] 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.[9] 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.[9]

Habitat

Species of the genus Massospora are found in the same habitats as their host cicadas, which includes large temperate ranges in the Southern and Northern hemispheres.

Potential applications

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 number of infected cicadas producing resting spores increased by 9-fold.[12] This suggests the fungus can be utilized as a control agent in decreasing the significant damage cicadas impose on young trees on which they lay their eggs.[11] Studies of M. cicadina and its hosts can also provide insights into biological clocks and environmental signaling due to their long, synchronous life cycles.

Similar host–parasite systems

References
  1. (1) Latrobe, John H. B., Esq. (1845). Memoir of Benjamin Banneker: Read before the Maryland Historical Society at the Monthly Meeting, May 1, 1845. Baltimore, Maryland: Printed by John D. Toy. p. 12. LCCN rc01003345. OCLC 85791076. Retrieved February 29, 2020 – via Internet Archive.{{cite book}}: CS1 maint: multiple names: authors list (link)
    (2) Barber, Janet E.; Nkwanta, Asamoah (2014). "Benjamin Banneker's Original Handwritten Document: Observations and Study of the Cicada". Journal of Humanistic Mathematics. 4 (1): 112–122. doi:10.5642/jhummath.201401.07. ISSN 2159-8118. OCLC 700943261. Archived from the original on August 27, 2014. Retrieved August 26, 2014. Page 115, Fig. 3: Image of page in Benjamin Banneker's Astronomical Journal, 1791-1806. Manuscript written by Benjamin Banneker (MS 2700). Special Collection. Maryland Historical Society, Baltimore, Maryland: "I like to forget that I inform to report that if their lives are Short they are merry, they begin to Sing or make a noise from first they come out of the Earth till they die. The hindermost part rots off, and it does not appear to be any pain to them, for they still continue on Singing till they die.".
  2. Kalfatovick, Martin R. (July 13, 2021). "Massospora cicadina" (Blog). Farewell to Brood X (2021) — See You in 2038!. Biodiversity Heritage Library. Archived from the original on August 28, 2021. Retrieved September 29, 2021.
  3. (1) Leidy, Joseph (1853). "Flora and Fauna Within Living Animals (accepted for publication: December 1851): Chapter III. Upon Pseudo-Entophyta, Etc.". Smithsonian Contributions to Knowledge. Vol. 5. Washington, D.C.: Smithsonian Institution. pp. 53–54. OCLC 609408263. Retrieved September 29, 2021 – via Biodiversity Heritage Library. In the spring of 1851, during the imago appearance of the seventeen-year locust, among myriads of the insect, several friends and myself found between 12 and 20 specimens, which, though living, had the posterior third of the abdominal contents converted into a dry, powdery, ochreous-yellow, compact mass of sporuloid bodies. The caudal appendages and posterior two or three abdominal rings covering the mass, were loose and easily detached, leaving the fungoid matter in the form of a cone, affixed by its base to the unaffected part of the abdomen of the insect
    (2) Leidy, Joseph (1853). "Plate X". Smithsonian Contributions to Knowledge (illustration). Vol. 5. Washington, D.C.: Smithsonian Institution. OCLC 609408263. Retrieved September 29, 2021 – via Biodiversity Heritage Library.
    (3) Leidy, Joseph (1853). "References to the plates and figures: Plate X". Smithsonian Contributions to Knowledge. Vol. 5. Washington, D.C.: Smithsonian Institution. p. 67. OCLC 609408263. Retrieved September 29, 2021 – via Biodiversity Heritage Library. Figs. 27, 28. Fungus mycelium, from the vagina of Cicada septendecim.
    Fig. 29. Spores from the same situation as Figs. 27, 28.
  4. Love, E.G. (April 1895). "Notes on the Seventeen Year Cicada, Cicada septendecim: The Cicada Fungus". Journal of the New-York Microscopical Society, Vol. 11, No. 2. New York: New York Microscopical Society. p. 42. OCLC 731007065. Retrieved September 28, 2021 – via Internet Archive. The Cicada Fungus.—A number of specimens, mostly males, were found which had been attacked by the fungus, Massospora cicadina. This fungus was first noticed, we believe, by the late Dr. Joseph Leidy, who in 1851 found from 12 to 20 specimens of C. septendecim "which though living had the posterior third of the abdominal contents converted into a dry powdery, ochreous yellow, compact mass of sporuloid bodies." Dr. Leidy also described and figured the fungus itself. This fungus was also described by Prof. Peck in 1870, who gave it the name it now bears.
    In the specimens which I found the entire abdominal cavity was tilled with a mass of spores, and the insects were still alive and able to "sing," although they were rather inactive. I did not find any portion of the fungus itself.
  5. Peck, Charles Horton (1879). "Report of the Botanist: Massopora, gen. nov: Massospora cicadina Pk.". Thirty-First Annual Report on the New York State Museum of Natural History by the Regents of the University of the State of New York. Albany, New York: Charles Van Benthuysen & Sons. p. 44. OCLC 939629305 – via Biodiversity Heritage Library. Spore mass occupying the abdominal cavity, whitish or pale cream-color, at length exposed by the falling away of the terminal rings of the abdomen; spores subglobose or broadly elliptical, granular within, sometimes containing one to three unequal nucleoli or oil globules, .00065′ — .00085′ in diameter.
  6. (1) Speare, A. T. (March 1921). "Massospora cicadina Peck: A Fungous Parasite of the Periodical Cicada". In Murrill, William Alphonso (ed.). Mycologia: Vol. 13, No. 2. Lancaster, Pennsylvania: New Era Printing Company. pp. 72–82. doi:10.1080/00275514.1921.12016863. ISSN 0027-5514. OCLC 1640733 – via Biodiversity Heritage Library.
    (2) Speare, A. T. (March 1921). "Plate 6: Massospora cicadina Peck". In Murrill, William Alphonso (ed.). Mycologia: Vol. 13, No. 2. (illustration). Lancaster, Pennsylvania: New Era Printing Company. ISSN 0027-5514. OCLC 1640733 – via Biodiversity Heritage Library.
  7. Steinhaus, Edward A. (2014). Insect Pathology: An Advanced Treatise. Vol. 2. New York: Academic Press. ISBN 9780323143172. OCLC 819403404.
  8. Williams, K S; Simon, C (1995). "The Ecology, Behavior, and Evolution of Periodical Cicadas". Annual Review of Entomology. 40 (1): 269–295. doi:10.1146/annurev.en.40.010195.001413. ISSN 0066-4170.
  9. Duke, L.; Steinkraus, D.C; English, J.E; Smith, K.G (May 1, 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:10.1016/S0022-2011(02)00040-X. ISSN 0022-2011. PMID 12234535.
  10. Cooley, John R.; Marshall, David C.; Hill, Kathy B. R. (January 23, 2018). "A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada)" (PDF). Scientific Reports. Springer Nature. 8 (1432): 1432. Bibcode:2018NatSR...8.1432C. doi:10.1038/s41598-018-19813-0. ISSN 2045-2322. PMC 5780379. PMID 29362478. Archived (PDF) from the original on August 30, 2021. Retrieved August 29, 2021.
  11. "Flying salt shakers of death :Cornell Mushroom Blog". blog.mycology.cornell.edu. Retrieved October 23, 2018.
  12. White, Joann; Lloyd, Monte (August 1, 1983). "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.
  13. Boyce, Greg R.; Gluck-Thaler, Emile; Slot, Jason C.; Stajich, Jason E.; Davis, William J.; James, Tim Y.; Cooley, John R.; Panaccione, Daniel G.; Eilenberg, Jørgen; De Fine Licht, Henrik H.; Macias, Angie M. (October 2019). "Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying cicada pathogens". Fungal Ecology. 41: 147–164. doi:10.1016/j.funeco.2019.06.002. PMC 6876628. PMID 31768192.
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