Entomophthora echinospora (Phycomycetes: Entomophthoraceae), a fungus pathogenic on the neotropical cicada, Procollina biolleyi (Homoptera: Cicadidae)

JOURNAL

OF INVERTEBR.4TE

Entomophthora a Fungus

PATHOLOGY

21, 37-90

(1973)

echinospora (Phycomycetes: Pathogenic on the Neotropical biolleyi

DAVID

(Homoptera:

TTRRELL

/meet Pathology Et~uironment

Research Canada,

AND

Entomophthoraceae), Cicada, Procollina

Cicadidae)

DOKALD

Itwtitufe,’ Srtult Ste.

i\l.

RIACLEOD

Cuudiro~ Forestry Service, Jlarie, On tcuio, Canada

En~omophthorcz echinasporn (Phycomycetes: Entomophthoraccac) as a major pathogen of the neotropical cicada Proco&u biollevi Mortality levels in teneral adults ranged from 40 to 705% during erlosion at Rajo la Hondura. Costa Rica. in 1971.

INTRODUCTION

During field investigations of the ecology of the neotropical cicada Procollina biolleyi at Bajo la Hondura, Costa Rica, in the summer of 1971, many teneral adults were observed to be killed by an entomogenous fungus. Subsequent examination showed t’he fungus to be Entomophthora echinospora, a species originally described by Thaxter (1888) from adults of the fly Sapyo?nyzn longipennis and known only from dipt’eran species. This is the first recorded account of an Edomophthora species on cicadas; previous records of phycomycete fungi attacking cicadas have involved species of the closely related genus Massospora (Soper, 1963). Est,imates of the incidence of mortality to the host were also determined. OBSERVATIOSS

The infection of P. biolleyi by E. echinospora was discovered during early July, ’ Contribut,ion

No.

228 from

this

Institute.

s7 Copyright

0

19’73

by

.kademic

Press,

Inr.

has (Homoptera: the peak

been

identified Cicadidae). period of adult

1971, at Bajo la Hondura, a montane, tropical, wet forest locality (SO@1000 m elev.) in the San Jose Province of C’osta Rica. Sampling of nymphal skins of P. biolleyi had been started during late June along the northern slope of a steep ravine covered with primary-growth and late sccondarygrowth forest. Judging from the numbers of nymphal skins collected and the abundance of singing males, this cicada wa.~ very abundant at this locality through July and August, presumably a peak period of adult emergence for this species. During the survey, many dead teneral adult cicadas were observed attached to the understory p1ant.s by copious fungal outgrowths. Systematic collection of infected teneral adults, healthy tenerals, and nymphal skins along four arbitrarily established transects in the forest understory in #July and early August, 1971, permit’ted the crude estimation of the percentage of infection of the fungus in the emerging cicada population. Such data are of particular in-

ss

YOUKG,

TYRRELL,

terest with respect to proposed furt,her study of the population biology of P. biol/,eyi and other species of neotropical cicadas. Description

of the Infection

Adults of P. biolleyi have a mean body length of 26.7 AZ 2.2 mm (N = 57) and a maximal mean thoracic width of 13.4 * 1.8 mm (N = 46). Therefore, being relatively large insects, thcac cicadas provide an CXtensivc microhabitat for potential infection b\: pathogenic fungus such as E. echinosporn. Infected individuals were readily ohserved at, a distance by the translucent reddish-brown hue assumed by the otherwise t,ransparent wings when coated with both conidia and extensive filamentous hyphal outgrowths from the head and thorax. Hyphac associated with the ventral portions of the thorax, including the legs, cause t,he dead adult to adhere to understory plants, in the clinging position assumed very shortly after cclosion (Fig. 1). Despite intensive searches on the forest floor xnd understory plants, infected dead uneclosecl nymphs were not found; with t
of the Fungus

Figs. 2, 3, and 4 depict the resting spores and conidia of E. echinospora as taken from a single adult male of P. biolleyi. Thaxter (1888) reported that the conidin are usually nearly symmetrical, measuring 20-25 X lo-14 pm in size. The conidia taken from P. biolleyi were 17.5-26.5 (mean of 21.96 r+ 1.98) X 10-18.5 (mean

AKD

MACLEOD

of 12.84 2 1.54) ~111, differing very little from Thaxter’s measurements. The spherical sesting spores (Fig. 3) were 35.0-47.5 pm in diameter (mean of 40.31 t 5.07 pm with epispore; 33.0 f 3.55 pm without epispore), while Thaxter (1888) reported ihat they range from 30 to 40 pm in diamctcr. Thus, it appears that the resting spores of E. echinospora from P. biolleyi are slightly larger than those measured by Thaxter. The cicada examined, as mcntioncd above, bore both coniclia and resting sporeti. Conidin were trapped on the underside of the wings after ejection by conidiophores on t.hc dorsal surface of the insect, while a small number of reddish-brown resting sports were found on t,hc ventral surface of the insect. X11 resting spores bore a mycclial appcnclagc (Figs. 2, 3). Incidence

of Mortality

in P. biolleyi

Pathogenic attack by E. echinospora in the population of P. biolleyi at Bajo la Hondura was consistently high during July and August, 1971 (Table I). We have noktl that between 40 and 70% of the tenTABLE

1

OF TICNERIL ADI:LT IL~ORT,\I,ITT I~RSULTING FIKM INFECTION BY Entomophthora cchinospora IN .\ POPCL~LTION OF 'LWK NEOTiWPlC:iL Crc.w:\, Procollina hidc~i .\‘I’ B.\Jo I,.\ Han-nrrn.\, Cow.\ R1c.i __~NO. infected Perwnt No. of dead mortalit) nymphal teneral due to ljate skins! adults* fungus -I___~ *June 26, 1971 42 I .-I :jx. 1 ,July 10 x3 41 49.4 July 17 126 7:3 -57 9 July 2.3 1o.i .5x .j.i 2 August .i 102 70 6X.7 August 12 03 52 5.5 !I .4ugust 27 31 A’2.0 50 __. .- -____ (L Total number of skins collcctcd from four transects of equal length (ahout 13 m) estahlished in primary-growth forest understory. b Collected along the same four transects used to rollrrt nymphal skins. ESTIM.ITI:S

ENTOMOPHITHORA

ECHINOSPORA

ss

1. Teneral Procollina biollrlyi killed by Entomophthora~rchinosporcc plant. FIG. 2. Resting spores of E. echinospora. x500. FIG. 3. Resting spore of IS. echinospora. Note mycelial appendage. X 1000. FIG. 4. Conidia of E. echinospora X 1000. FIG.

and

attached

to

understory

era1 adults are killed by this fungus, and it is clear that this fungus acts as a successful pathogen in the cicada population. It is possible that some infected teneral adults had fallen off understory plants in response to wind, rainfall, etc., although few or none were actually found on the ground. Nymphal skins are more securely fastened to branches and leaves of understory plants and are more difficult ta dislodge. Thus,

it is conceivable that mortality rates due to pathogenic attack may in fact be higher. However, we have no data on the incidence of attack by predators and parasites other than E. echinospora, factors which would have the opposite effect on our estimates. DISCUSSION Fungi attacking adult cicada populations have been previously reported. Cantrall

90

YOUNG,

TYRRELL,

(1937) noted substantial levels of infection by Massospora cicadina in populations of the North American periodical cicada, Magicicada septemdecim, and subsequently (Lloyd and Dybas, 1966) this infection was considered to be a possible means of regulating cicada numbers. Ciferri et al. (1957) identified 111.spinosa as a pathogen of Fidicina viridis and F. mannifera, and Soper (1963) has found M. Zevispora to be an important pathogen of the cicada Okanagana rimosa. In general, however, fungus infection of cicadas has been considered to be of incidental mortality. Katsura and Johnson (1937) and Katsura (1938) noted that the fungus Metarrhizium anisopliae attacks and kills mature (final instar) nymphs of periodical cicadas, and this fungus is also known from at least 75 other North American insects (DeBach and Schlinger, 1964). Incidental levels of attack by fungi of the genus Cordyceps have been noted for some Japanese cicadas (Kobayasi, 1939, 1941). In the present case, however, mortality resulting from the pathogenic attack was of substantial magnitude during the peak period of adult eclosion. Such high levels would point to the fungus being an important factor in the control of population levels of P. biolleyi at this location. Elucidation of the full cycle of infection must await further field studies. Investigations on the life cycle of M. septendecim and M. cassini (Lloyd and Dybas, 1966) and 0. rimosa, (Soper, unpubl.) have revealed that mature nymphs of these species construct their emergence holes several days before the actual date of eclosion. If P. biolleyi nymphs follow the same pattern of behavior, we may suppose that infection of the nymphs occurs from some reservoir of infection in the forest floor at the time they construct their emergence holes. Subsequent development of the fungus then occurs while the nymph remains in the ground, and results in death of the insect during cclosion.

AND MACLEOD

This reservoir may be replenished by the resting spores formed on infected nymphs, but it is not known whether the conidia produced infect mature cicada nymphs or adult cicadas. Answers to these questions will provide valuable information on the epizootiology of this interesting genus of fungal pathogens. ACKNOWLEDGMENTS This work was supported in part by College Science Improvement Grant CY-4711, awarded to Lawrence University. Research farilities in Costa Rica were generously provided by the Central American Field Studies Programme of the Associated Colleges of the Midwest. The cicada was identified by Dr. T. E. Moore, University of Michigan, and the technical assistance of Patrick Eagan (Lawrence) and Mrs. Mary Welton (I.P.R.I.) is also gratefully acknowledged. REFERENCES I. J. 1937. Notes on the infection of Seventeen-Year Cicada, Magicicada septendecim(Linn.), by the fungus, Massosporn cicadina Peck. Bull. Brooklyn Entomol. Sot., 32, 120-121. CIFERRI, R., MACHADO, A. A., AND VITAL, A. F. 1957. A new species of the genus Massospora with an Allomyces species. Atti (Pavia), 14, 15-22. DEBACH, P., AXD SCHLINGER, E. I. 1964. Biological cont.rol of insect pests and weeds. Reinhold, New York. KATSURA, S. K. 1938. Inoculation of young cicada nymphs with spores of green muscardine disraw. J. Econ. Entomol., 31, 124-125. K.4~s~n.4, S. Ii., AXD Jo~rn-SON, A. G. 1937. The green muscardinc fungus on the periodical cicada. Science, 86, 128. KOBAYASI, Y. 1939. On the genus Cordyceps and its allies on Cicadidae from Japan. BUZZ. Biogeogr. Sot. Jap., 9, 145-176. KOBAYASI, Y. 1941. The genus Cordyceps and its allics. Tokyo Bwwika Daigaku, Sect. B, 84, 53-260. LLOYD, M., AND DYBAS, H. S. 1966. The periodical cicada problem. I. Population ecology. Ewolulion, 20, 133-149. SOPER, R. S. 1963. Massospora levisporn, a new species of fungus pathogenic to the cicada, CANTRALL,

Okanagana

rimosa.

Can.

J. Bot.,

41, 87.5878.

R. 1888. The Entomophthoraceae of the United States. Mem. Boston Sot. Nat. Hist., 4, 133-201,

THAXTER,