T h e early stages of mycelial development in cicadas infected by M.
cicadina have not yet been satisfactorily observed, although cytologically it is known that the fungus in common with other species of Entomoph
thora has coenocytic hyphae with large conspicuous nuclei.
Following advanced disintegration of the insect tissue, the mycelium usually becomes septate, forming cells with two or, rarely, three nuclei.
Eventually the cells separate and r o u n d u p to form hyphal bodies.
These give rise to short, unbranched, binucleate conidiophores that form hymenium-like layers a r o u n d cavities of various sizes; thus producing a honeycomb effect throughout the insect's segments (Goldstein, 1929).
O n the free end of each conidiophore which projects into the cavity, a single conidium is formed, into which the entire contents of the conidio
phore flows. T h e emptied conidiophore then shrinks or collapses and is finally crushed as other turgid hyphae give rise to additional conidio
phores within the cavity or form new chambers.
At maturity the endogenous conidia lie free in groups or clusters within the global pockets, b u t are not exposed until the body segments of the host disintegrate or rot away.
T h e hyphal bodies that give rise to resting spores are, according to Goldstein (1929), tetranucleate and considerably longer than those that form conidiophores. H e could find n o direct evidence that they were formed by fusion of two smaller hyphal cells, b u t considered, together with Speare (1921), that the hyphal bodies merely represent longer frag
ments of mycelium with four, instead of two, nuclei. T h e resting spores which are formed by a process of b u d d i n g are, therefore, azygospores b u t are thought by Goldstein to be a type of chlamydospore. T h e rest
ing spores are not formed within special cavities, b u t lie rather evenly distributed throughout the insect's body cavity.
Speare (1921) reported that conidia were never as a b u n d a n t as rest
ing spores and that b o t h types of reproductive bodies did not occur simultaneously or consecutively in the same individual. According to him the conidia appeared exclusively in the early part of the season in which the cicada was in flight, while the resting spores developed toward the end of the same period.
2. Disease Signs and Symptoms
Insects attacked by this fungus present a remarkable appearance. T h e vegetative growth of the fungus is confined to the softer tissues in the posterior segments of the body of the host. As each successive segment of the body becomes filled with the fungus spores, the chitinous b a n d about the segment is broken apart by the pressure of the swelling mass of fungus hyphae and breaks away, exposing a creamy white mass of spores which soon become dry and brittle. T h e exposed spores may then crumble or break away in a single piece. T h e abdominal segments slough off successively, finally leaving the insects flying about with thorax and head only. T h i s unusual condition must make it one of the more easily recognized diseases of insects (Speare, 1921; Goldstein, 1929).
3. Pathogenicity
T h e r e are some contradictory reports on the importance of M.
cicadina in the n a t u r a l control of the 17-year cicada. Speare (1921) ob
served that infection is confined largely to spent males, thus indicating that the organism may not be of great economic importance. Goldstein (1929), however, found the fungus in both males and females; in fact most of her specimens containing resting spores were females whose bodies still contained m a n y eggs. Such a situation would enhance the importance of this organism from an economic viewpoint (Steinhaus, 1949). Pending m u c h m o r e information on this host-parasite relation
ship, it is impossible to assess the importance of this organism in the control of M. septendecim.
4. Dissemination
Since the conidia of Massospora are formed within the insect body, their dissemination takes place in a different m a n n e r from that of Entomophthora. T h e continued mobility of the host assists in spreading the conidia in two ways. W h e n the intersegmental m e m b r a n e has been destroyed, the activity of the insect helps to detach the most posterior abdominal segment, thus liberating the conidia. I n addition, continued movement of the insect as successive segments are severed results in a better dispersal of the disease.
T h i s rather peculiar habit of growth may also serve as a source of infection d u r i n g the subterranean portion of the insects' developmental cycle, when there is n o opportunity for the discharge of conidia into the o p e n air. It is also known that the conidia, with heavy warted walls, are capable of surviving in the soil for a considerable period of time. Hence, it is quite possible, following infection d u r i n g their u n d e r g r o u n d ex
istence, that many insects may perish below g r o u n d or soon after emerg
ing. Those that escape may eventually develop the disease d u r i n g their aerial existence through contamination with " a i r b o r n e " spores a n d / o r through contact with infected insects while o n the ground.
ACKNOWLEDGMENTS
T h e writer wishes to express his thanks to Dr. T . C. L o u g h h e e d for constructive criticism in the preparation of this manuscript; to Miss Doreen Archibald, for as
sistance in m u c h of the work; and to Mrs. Μ. N . Reynolds and her staff, Main Library, Canada Department of Agriculture, Ottawa, for providing many of the references cited.
T h e writer is also indebted to Mr. D. C Anderson for the photographs.
APPENDIX I
A n index of the various entomogenous formsß described and named in the genus Entomophthora^ (— Empusa) w i t h important taxonomic references.
E. acaricida Petch (Petch, 1940*,« 1942) E. acaridis Petch (Petch, 1944*) E. americana T h a x t e r (Thaxter, 1888*) E. anglica Petch (Petch, 1944*)
E. anisopliae Metchnikoff (Saccardo, 1891) E. anticae Reichhardt (Mitchell, 1919)
6 T h e list is thought to be complete; the author, therefore, w o u l d appreciate having his attention drawn to any omissions.
7 O w i n g to the fact that different authors have allocated identical species to different genera, the 104 k n o w n (species) epithets appear in the 134 combinations
cited by MacLeod (1956).
8 A n asterisk denotes the reference in which the species was originally described and named.
Ε. aphidis Hoffman (Thaxter, 1888; Petch, 1937, 1939)
E. brahminae Bose and Mehta (Bose and Mehta, 1953*) E. bullata T h a x t e r ined. (Povah, 1935*; Petch, 1939) E. calliphorae Giard (Giard, 1879*; Thaxter, 1888) E. calopteni Bessey (Bessey, 1883*; Thaxter, 1888) E. caroliniana T h a x t e r (Thaxter, 1888*)
E. carpentieri Giard (Giard, 1888*; Petch, 1944)
E. chromaphidis Burger and Swain (Burger and Swain, 1918*) Ε cimbicis Bubäk (Bubäk, 1906*; Petch, 1944)
E. cleoni (Wize) Bubäk (Bubäk, 1916) Ε. coleopterorum Petch (Petch, 1932*, 1944) E. colorata Sorokin (Thaxter, 1888; Saccardo, 1891) E. conglomerata Sorokin (Thaxter, 1888)
E. conica Nowakowski (Thaxter, 1888)
E. coronata Costantin (Costantin, 1897*; Harris, 1948) E. creatonotus Yen (Yen, 1962*)
E. culicis Braun (Braun, 1855*; Thaxter, 1888) Ε. curvispora Nowakowski (Thaxter, 1888) E. cyrtoneurae Giard (Giard, 1888*) E. delphacis Hori (Esaki et al., 1937)
E. delpiniana Cavara (Cavara, 1899b*) E. ferruginea Phillips (Thaxter, 1888; Petch, 1937) E. forficulae Giard (Giard, 1889*)
E. grylli Fresenius (Fresenius, 1856*; Thaxter, 1888) Ε. henrici Molliard (Molliard, 1918*)
E. hylemyiae Lakon (Lakon, 1935*)
E. ignobilis Hall and D u n n (Hall and D u n n , 1957b*) E. jaapiana Bubäk (Bubäk, 1916*; Saccardo, 1926) Ε. jassi Cohn (Thaxter, 1888)
Ε. kansana Hutchinson (Hutchinson, 1961; 1962*) E. lageniformis T h a x t e r (Thaxter, 1888*)
Ε. lampyridarum T h a x t e r (Thaxter, 1888*; Petch, 1944) E. lauxaniae Bubäk (Bubäk, 1906; Petch, 1932)
E. lecanii Zimmermann (Zimmermann, 1901*) Ε. macrospora (printer's error, Thaxter, 1888) E. megasperma Cohn (Cohn, 1875*; Giard, 1888) Ε. montana T h a x t e r (Thaxter, 1888*)
E. muscae Cohn (Cohn, 1855*)
Ε. muscarina (printer's error, Thaxter, 1888) E. muscivora Schroeter (Thaxter, 1888) E. nebriae Raunkiaer (Raunkiaer, 1892*)
E. obscura Hall and D u n n (Hall and D u n n , 1957b*) E. occidentalis T h a x t e r (Thaxter, 1888*; Petch, 1944) E. ovispora Nowakowski (Thaxter, 1888)
E. packyrrhinae Arthur (Müller-Kögler, 1957) Ε. papillata T h a x t e r (Thaxter, 1888*) E. pelliculosa Sorokin (Thaxter, 1888)
E. phalangicida Lagerheim (Lagerheim, 1898*) Ε. phryganeae Sorokin (Thaxter, 1888)
E. phytonomi Arthur (Arthur, 1886; Thaxter, 1888)
E. planchoniana Cornu (Cornu, 1873*; Thaxter, 1888; Petch, 1937) E. plusiae Giard (Saccardo, 1891)
E. pooreana Smith (Smith, 1900*) E. pseudococci Speare (Speare, 1912*) E. punctata Garbowski (Garbowski, 1927*) E. pyralidarum Petch (Petch, 1937*) E. radicans Brefeld (Thaxter, 1888) E. reticulata Petch (Petch, 1939*) E. rhizospora T h a x t e r (Thaxter, 1888*)
E. richten (Bresadola and Staritz) Bubäk (Bubäk, 1916) Ε. ritnosa Sorokin (Giard, 1888)
E. saccharina Giard (Saccardo, 1891) E. scatophagae Giard (Giard, 1888*) E. sciarae Olive (Olive, 1906*)
E. sepulchralis T h a x t e r (Thaxter, 1888*)
E. sphaerosperma Fresenius (Fresenius, 1856*; Thaxter, 1888) Ε. sphaerosperma Fresenius cicadelliphaga T u r i a n (Turian, 1957*) E. sphaerosperma Fresenius elateridiphaga T u r i a n (Turian, 1957*) E. staritzii (Bresadola and Staritz) Bubäk (Bubäk, 1916*) Ε. syrphi Giard (Giard, 1888*)
E. telaria Giard (Giard, 1888*)
E. tenthredinis Fresenius (Thaxter, 1888; Petch, 1944) E. tipulae Fresenius (Thaxter, 1888)
E. thaxteriana Petch (Petch, 1937*)
E. uvella Krassilstschik (Thaxter, 1888; Saccardo, 1891) E. variabilis T h a x t e r (Thaxter, 1888*)
E. virescens T h a x t e r (Thaxter, 1888*)
E. virulenta Hall and D u n n (Hall and D u n n , 1957b*) E. zabrii Rozsypal (Rozsypal, 1951*)
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