Nomuraea viridulus, a new entomogenous fungus from Taiwan

Mycological Society of America

Nomuraea viridulus, a New Entomogenous Fungus from Taiwan

Author(s): S. S. Tzean, L. S. Hsieh, J. L. Chen, W. J. Wu

Source: Mycologia, Vol. 84, No. 5 (Sep. - Oct., 1992), pp. 781-786

Published by: Mycological Society of America

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Mycologia.

BRIEF ARTICLES

Mycologia, 84(5), 1992, pp. 781-786.

© 1992, by The New York Botanical Garden, Bronx, NY 10458-5126

NOMURAEA VIRIDULUS, A NEW ENTOMOGENOUS FUNGUS

FROM TAIWAN

S. S. TZEAN,1 L. S. HSIEH, J. L. CHEN, AND W. J. Wu

Department of Plant Pathology and Entomology, National Taiwan University, Taipei, Taiwan, 10617 Republic of China

The genus Nomuraea erected by Kish, Samson and Allen (1974) was characterized by the for- mation of mono- or synnematous conidiophores bearing verticils of metulae and phialides in com- pact clusters encircling the stalk mostly below the septa; phialides usually in whorls, broadly cylindrical or sometimes with a swollen base, neck very short or absent; and conidia green to slightly purple in mass (Samson, 1974). Samson (1974) recognized two species, N. rileyi (Farlow) Samson and N. atypicola (Yasuda) Samson; in both species the teleomorphic state remains un- known. N. rileyi was entomopathogenic with a potential for biocontrol of insect pests, particu- larly lepidopterans (Ignoffo et al., 1976; Ignoffo and Garcia, 1985, 1989), whereas N. atypicola was a spider parasite, common in gardens and roadsides in Japan (Samson, 1974). Hocking (1977) described a new species, N. anemonoides Hocking from Australian soil, which contrasts with the previously described Nomuraea species by its synnematous rugulose conidophores bear- ing irregular verticils of phialides alone or metu- lae and phialides at most septa along the whole length of the conidiophore, and also by globose, ellipsoidal, or ellipso-pedunculate conidia. N. anemonoides, although probably a saprophyte, can be lethal to lepidopteran larvae when ex- posed at high dosage (Ignoffo and Garcia, 1989). In the course of a study of entomogenous fungi from Taiwan, on many occasions a distinctive fungus was found frequently on cicada (Cryp- totympana facialis Walker) cadavers. The spe- cific fungus turned out to be a Nomuraea sp. but produced huge greenish, cylindrical, slightly curved or allantoid conidia, which can be readily

' Corresponding author: S. S. Tzean, Department of Plant Pathology and Entomology, National Taiwan University, Taipei, Taiwan, 10617 R.O.C.

distinguished from known Nomuraea spp. and thus it is described as new. Illustrations and di- agnosis were based on cultures on malt-extract agar (MEA) and on cicadas as well. Color no- menclature for colonies, mycelia and conidia was adapted from the color standard of Kornerup and Wanscher (1978). Preparation of microscopic structures for scanning electron microscopy fol- lowed previously described methods (Tzean and Estey, 1978).

Nomuraea viridulus Tzean, Hsieh, Chen et Wu,

sp. nov. FIGS. 1-10

Coloniae in maltis extractis agaribus ad 25 C in 14 diebus, crescentes, lente attingentes 1.5-2.3 cm dia- metro, centrales velutinae, zonatae, fairnosae, prae- sertim distinctae ubi sporulae graves, cinerascentes vi- rides, ad obscure virides, margine floccosae albae. Reversum centrum luteolum ad luteolum brunneum, subcentrum ad marginem obscure viride ad incolorem. Odor diffusis. Pigmentum demptum exsudatum li- quidum. Synnemata absens. Mycelium ramosum sep- tatum, laevis paries, album 2.5-3.8 Atm latum. Coni- diophorum ascendens mazime saepe ab aerio, subinde ab superficie laevis paries, hyalinum, longitudine usque ad 210 ,im, verticillatum, ramosum vel phialis vel saepe cum irrequlari subterminali, laterali vel infero plano ramoso, 1-2 vel in verticillato orienti prope septum; rami late clavati, clavati vel cylindrici 11.7-31.6 x 2.6-3.8 Atm; phiales adpressae 3-8 per ramum vel su- binde solitariae portatae directae in conidophoris, ova- lis-cylindrica, ellipsoideae. Collum absens vel vix man- ifestum 5.3-9.2 x 3.3-4.6 ,um. Conidia catenulata non septata, laevis-paries, cylindrica, ellipsoidea, plerum- que leviter curva vel allantoidea, separata extrema ali- quando apiculata, solitaria, cinerascentia, lutea, in massis obscure cinerascentia viridia ad perviridia 14.4- 19.4 x 3.8-4.4 Atm. Chlamydospora absens. In insecti hospete, mycelium primum album, floccosum, tegens sutura, invicem ad viride caesiam ad pallidum viride, velutinum, in aetate, cinerascens viride ad hebetem viridem cum gravi sporulato, ramosum. Phiales et co- nidia plus minusve pinguia, sed breve qum illa in cul- tura; constitantia 4-12, phiales per ramum, ramus ori- ens non limitatus ab septo, subinde proliferatus novus 781

MYCOLOGIA

Go

FIG. 1. Nomuraea viridulus. Characteristics of co- nidiophores, metulae, phialides and conidia in culture media (MEA).

ramus. Conidiophora subliliter aspra ad aspros paries. Synnemata et chlamydospora absens.

HOLOTYPUS: in Cryptotympanafacialis Walker, Ho- moptera, Hsintien, Taipei, Taiwan, R.O.C., 22 June 1989, PPH14; ISOTYPUS IMI.

Colonies on MEA growing slowly, at 25 C in 14 days, 1.5-2.3 cm diam, zonate, velutinous to farinose, greyish green to dull green (26D-E4-5, 27D-E4-6), margin floccose, white. Reverse cen- ter yellowish to yellowish brown (5C-F4-6), sub- central to margin dull green (26-27D-E3-4) to colorless. Odor and diffuse pigment lacking. Ex- udate clear colorless. Synnemata absent. Myce- lium branched, septate, smooth-walled, hyaline, 2.5-3.8 ,um wide. Conidiophores ascending most

commonly from aerial, occasionally from surface

or submerged hyphae, septate, straight or sinu- ous, smooth-walled, hyaline, up to 210 ,um in length, 3.1-5 ,um wide, bearing divergent, ter- minal, verticillate metulae or phialides, or with

FIG. 2. Nomuraea viridulus. Characteristics of co- nidiophores, metulae, phialides, and conidia on cicada, Cryptotympana facialis Walker. Note that the coni- diogenous structures and conidia are usually shorter and broader than those on culture media.

irregularly subterminal lateral or lower levels metulae, one to two or in whorl arising near sep- ta; metulae broadly clavate, or cylindrical, 11.7- 31.6 x 2.6-3.8 ,tm; phialides appressed three to eight per metulae, or occasionally sessile and solitary borne directly on the conidiophores, oval-cylindrical, ellipsoidal, neck absent or bare- ly perceptible, 5.3-9.2 x 3.3-4.6 Am. Conidia catenulate, nonseptate, smooth-walled, cylindri- cal, ellipsoidal, usually slightly curved or allan- toid, sometimes apiculate, greyish yellow, in mass dull greyish green to dark green, 14.4-19.4 x 3.8-4.4 Atm. Chlamydospores absent. Under scanning electron microscopy, phialides and co- nidia usually covered with a layer of mucilage. On insect hosts, mycelium initially white, floc- cose, covering the sutures, turning vivid blue (22A8) to light green (27D-E4-5), velutinous, in age greyish green to dull green, with heavy spor- ulation, metulae, phialides and conidia usually broader and shorter than those in culture media; 4-12 phialides per metulae, growing along the 782

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FIGs. 3-6. The characteristics of habitat, colony, conidiophores, conidiogenous cells and conidia of Nomuraea viridulus. 3. Naturally infested cicada, Crypt otympana facialis, body juncture overlaid with velutinous mycelium and dull-green conidia. 4. Colony on MEA at 25 C in 14 days without illumination. 5. Conidiophore bearing terminal verticillate phialides and subterminal or lateral metulae and verticillate phialides, metulae sometimes arising near septa. 6. Conidia cylindrical, ellipsoidal, some slightly curved or allantoid. Bars = _10,Mm.

MYCOLOGIA

FIGS. 7-10. Scanning electron micrographs of the sporulating structures and conidia of Nomuraea viridulus. 7. Phialides verticillate or solitary (arrow) borne on metulae or ascending directly from the fertile hyphae. 8. Phialides neck absent or barely perceptible, apex truncate (arrow), or somewhat thickened in conidiogenesis (arrow). 9. Conidia catenulate, schizolytic (right arrow), phialides oval-cylindrical, covered with distinct mucilage (left arrow). 10. Conidia cylindrical, some curved, apiculate (upper arrow), some with mucilage (lower arrow).

Bars = 5 um.

whole length of the conidiophores at random not restricted at septa, occasionally metulae prolif- erating; conidiophores finely roughened to roughened. Synnemata and chlamydospores ab- sent.

SPECIMEN EXAMINED. _{On Cryptotympanafacialis, Ho}

44, Hsintien, Taipei, Taiwan, R.O.C. 22 June, 1989, HOLOTYPE PPH 14 (dried culture) and extype PPH 14E (living culture), deposited in the Department

of Plant Pathology and Entomology, National Taiwan University, Taipei, Taiwan. PPH14E was also depos- ited in the Culture Collection and Research Center (CCRC 32589), Hsinchu, Taiwan. ISOTYPES NY, IMI. Other specimen examined, exclusively on cicada, Ho 1, Furong, Taipei, 13 July 1988; Ho 5, Chingmeei, Taipei, 17 Aug. 1988; Ho 7, Sirting Park, Pingtung, 10 Sept. 1988; Homoptera, Ho 49, Full-Moon Mt., Tao- yuen, 16 July 1989; Ho 57, Fushan, Taipei, 9 Aug. 1989; Ho 51, Botanical Garden, Taipei, 29 July 1989; 784

BRIEF ARTICLES Ho 68, Paoming Temple, Keelung, 25 Aug. 1989; Ho

72, Nanjen Mt., Pingtung, 24 Sept. 1989.

Nomuraea viridulus has been encountered on cicada cadavers on many occasions during a 2 year survey from Taiwan. This fact indicates its common occurrence and suggests that it has been overlooked in the past. The distinguishing char- acteristics of N. viridulus consist of erect or flex- uous conidiophores bearing irregular verticils of phialides alone, or metulae and phialides, along their whole length randomly and not restricted at septa, appressed whorls of phialides, phialides without collula and huge cylindrical, ellipsoidal, usually slightly curved or allantoid conidia. The characteristics of metulae and phialides of N. viridulus show close resemblence to N. rileyi and N. atypicola; however, the former's phialides and metulae are apparently longer and broader than the latter's. Also there is a striking difference in size and shape of conidia between them (Samson, 1974) making the distinction easy. Though the irregular verticils of phialides alone, or metulae and phialides, along the whole length of conid- iophores of N. viridulus are similar to N. ane- monoides, between them a conspicuous distinc- tion exists not only in size of metulae and phialides but also in size and shape of conidia, and they can be differentiated from each other (Hocking, 1977). For comparison all the cur- rently known Nomuraea species with their key microscopic traits were tabulated (TABLE I). In other aspects, N. viridulus also shows some sim- ilarity to several species of Paecilomyces and Metarhizium (Samson, 1974; Tulloch, 1976). However, in most species of Paecilomyces col- onies are never true green, have thinner hyphae and smaller conidiogenous structures, with flask- shaped phialides in divergent clusters and ta- pering abruptly into a long thin neck (Samson, 1974; Brown and Smith, 1957). While in Metar- hizium, conidiophores are variable in length, usually much shorter than in Nomuraea, with apical loosely penicillate or verticillate branches, each branch bearing two to five metulae and phialides, metulae clavate, phialides elongate cy- lindrical, with central constriction, and in most species conidiophores usually are aggregated into sporodochia, with stromatic base, and conidia laterally adhering together to form a prismatic column (Samson, 1974). These traits aid in sep- aration of Paecilomyces and Metarhizium from N. viridulus despite similarity in microscopic fea- tures in one way or another.

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MYCOLOGIA MYCOLOGIA Inasmuch as N. viridulus is widespread, adapts

and survives well in nature as is evident from a 2 year survey, it might be capable of initiation of an epizootic in certain insect pests. Such po- tential for biocontrol merit further exploration, particularly in pathogenicity and host specificity in light of the past records (Samson et al., 1988; Ignoffo et al., 1976).

The research was supported by grants from the Na- tional Science Council (NSC-80-0409-B002-49) and Council of Agriculture, Executive Yuan [79-Lung- Chien-7-1-Liang 51(27)], R.O.C. The authors are in- debted to Drs. R. D. Goos, C. J. K. Wang, W. H. Ko, H. C. Evans and L. Sigler for reviewing the manuscript, invaluable comments and assistance; to Dr. J. C. Liao for preparation of the Latin diagnosis; to Mr. Y. C. Shiao for technical assistance.

Key Words: entomogenous fungi, Hyphomycetes, No- muraea, taxonomy

LITERATURE CITED

Brown, A. H. S., and G. Smith. 1957. The genus

Paecilomyces Bainier and its perfect stage Bys- sochlamys Westling. Trans. Brit. Mycol. Soc. 40:

17-89.

Hocking, A. D. 1977. Nomuraea anemonoides sp. Inasmuch as N. viridulus is widespread, adapts and survives well in nature as is evident from a 2 year survey, it might be capable of initiation of an epizootic in certain insect pests. Such po- tential for biocontrol merit further exploration, particularly in pathogenicity and host specificity in light of the past records (Samson et al., 1988; Ignoffo et al., 1976).

The research was supported by grants from the Na- tional Science Council (NSC-80-0409-B002-49) and Council of Agriculture, Executive Yuan [79-Lung- Chien-7-1-Liang 51(27)], R.O.C. The authors are in- debted to Drs. R. D. Goos, C. J. K. Wang, W. H. Ko, H. C. Evans and L. Sigler for reviewing the manuscript, invaluable comments and assistance; to Dr. J. C. Liao for preparation of the Latin diagnosis; to Mr. Y. C. Shiao for technical assistance.

Key Words: entomogenous fungi, Hyphomycetes, No- muraea, taxonomy

LITERATURE CITED

Brown, A. H. S., and G. Smith. 1957. The genus

Paecilomyces Bainier and its perfect stage Bys- sochlamys Westling. Trans. Brit. Mycol. Soc. 40:

17-89.

Hocking, A. D. 1977. Nomuraea anemonoides sp.

nov. from Australian soil. Trans. Brit. Mycol. Soc. 69: 511-513.

Ignoffo, C. M., and C. Garcia. 1985. Host spectrum

and relative virulence of an Ecuadoran and a Mis- sissippian biotype of Nomuraea rileyi. J. Invert. Pathol. 45: 346-352.

, and . 1989. Relative virulence of No- muraea spp. (N. rileyi, N. atypicola, N. anemono- dies) originally isolated from an insect, a spider, and soil. J. Invert. Pathol. 54: 373-378.

, N. L. Marston, D. L. Hostetter, and B. Puttler.

1976. Natural and induced epizootics of Nomu- raea rileyi in soybean caterpillars. J. Invert. Pathol. 27: 191-198.

Kish, L. P., R. A. Samson, and G. E. Allen. 1974.

The genus Nomuraea Maublanc. J. Invert. Pathol. 24: 154-158.

Kornerup, A., and J. H. Wanscher. 1978. Methuen

handbook of colour. Eyre Methuen Ltd., London, United Kingdom. 252 pp.

Samson, R. A. 1974. Paecilomyces and some allied HIyphomycetes. Stud. Mycol. 6: 1-119.

, and H. C. Evans, and J. P. Latge. 1988. Atlas

of entomopathogenic fungi. Springer-Verlag, New York. 187 pp.

Tulloch, M. 1976. The genus Metarhizium. Trans. Brit. Mycol. Soc. 63: 407-411.

Tzean, S. S., and R. H . Estey. 1978. Schizophyllum commune Fr. as a destructive mycoparasite. Can-

ad. J. Microbiol. 24: 780-784.

nov. from Australian soil. Trans. Brit. Mycol. Soc. 69: 511-513.

Ignoffo, C. M., and C. Garcia. 1985. Host spectrum

and relative virulence of an Ecuadoran and a Mis- sissippian biotype of Nomuraea rileyi. J. Invert. Pathol. 45: 346-352.

, and . 1989. Relative virulence of No- muraea spp. (N. rileyi, N. atypicola, N. anemono- dies) originally isolated from an insect, a spider, and soil. J. Invert. Pathol. 54: 373-378.

, N. L. Marston, D. L. Hostetter, and B. Puttler.

1976. Natural and induced epizootics of Nomu- raea rileyi in soybean caterpillars. J. Invert. Pathol. 27: 191-198.

Kish, L. P., R. A. Samson, and G. E. Allen. 1974.

The genus Nomuraea Maublanc. J. Invert. Pathol. 24: 154-158.

Kornerup, A., and J. H. Wanscher. 1978. Methuen

handbook of colour. Eyre Methuen Ltd., London, United Kingdom. 252 pp.

Samson, R. A. 1974. Paecilomyces and some allied HIyphomycetes. Stud. Mycol. 6: 1-119.

, and H. C. Evans, and J. P. Latge. 1988. Atlas

of entomopathogenic fungi. Springer-Verlag, New York. 187 pp.

Tulloch, M. 1976. The genus Metarhizium. Trans. Brit. Mycol. Soc. 63: 407-411.

Tzean, S. S., and R. H . Estey. 1978. Schizophyllum commune Fr. as a destructive mycoparasite. Can-

ad. J. Microbiol. 24: 780-784.

Mycologia, 84(5), 1992, pp. 786-790.

© 1992, by The New York Botanical Garden, Bronx, NY 10458-5126

STEPHANOCYSTS AS NEMATODE-TRAPPING

AND INFECTING

PROPAGULES

J. Y. LIOU AND S. S. TZEAN1

Department of Plant Pathology and Entomology, National Taiwan University, Taipei, Taiwan, 10617, Republic of China

Mycologia, 84(5), 1992, pp. 786-790.

© 1992, by The New York Botanical Garden, Bronx, NY 10458-5126

STEPHANOCYSTS AS NEMATODE-TRAPPING

AND INFECTING

PROPAGULES

J. Y. LIOU AND S. S. TZEAN1

Department of Plant Pathology and Entomology, National Taiwan University, Taipei, Taiwan, 10617, Republic of China

The term stephanocysts was coined by Boidin (1950) to describe a unique structure present in the context of the hymenium of a specific group of resupinate Basidiomycetes, especially in the genus Hyphoderma. Stephanocysts are bicelled, consisting of a cup-like basal cell and a terminal globose cell. At the juncture of the two cells, a row of spines surrounds the circumference. Boi-

din (1950) claimed that these spines arise from

the upper cell, but this opinion has not been The term stephanocysts was coined by Boidin (1950) to describe a unique structure present in the context of the hymenium of a specific group of resupinate Basidiomycetes, especially in the genus Hyphoderma. Stephanocysts are bicelled, consisting of a cup-like basal cell and a terminal globose cell. At the juncture of the two cells, a row of spines surrounds the circumference. Boi-

din (1950) claimed that these spines arise from

the upper cell, but this opinion has not been Corresponding author.

Corresponding author.

confirmed by later workers (Burdsall, 1969; Hal- lenberg, 1990). The circumscription for the stephanocysts has been further broadened to in- clude a reduced, one-celled type discovered in H. puberum (Fr.: Fr.) Wallr. (Boidin, 1958). The reduced stephanocyst consists of a swollen cell arising directly from the hyphal elements, which is surrounded by spines at the circumference and resembles the upper globose cell of the other form (Boidin, 1958; Burdsall, 1969). Additional atyp- ical stephanocysts were found in H. comptum (Jack.) Jiulich (Jiilich, 1976), H. echinocystis Er- confirmed by later workers (Burdsall, 1969; Hal- lenberg, 1990). The circumscription for the stephanocysts has been further broadened to in- clude a reduced, one-celled type discovered in H. puberum (Fr.: Fr.) Wallr. (Boidin, 1958). The reduced stephanocyst consists of a swollen cell arising directly from the hyphal elements, which is surrounded by spines at the circumference and resembles the upper globose cell of the other form (Boidin, 1958; Burdsall, 1969). Additional atyp- ical stephanocysts were found in H. comptum (Jack.) Jiulich (Jiilich, 1976), H. echinocystis Er- 786