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Taxonomic Status of the Genera Sorosporella and Syngliocladium Associated with Grasshoppers and Locusts (Orthoptera: Acridoidea) in Africa

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Taxonomic Status of the Genera Sorosporella and Syngliocladium Associated with Grasshoppers and Locusts (Orthoptera: Acridoidea) in Africa Mycol. Res. 106 (6): 737–744 (June 2002). # The British Mycological Society 737 DOI: 10.1017\S0953756202006056 Printed in the United Kingdom. Taxonomic status of the genera Sorosporella and Syngliocladium associated with grasshoppers and locusts (Orthoptera: Acridoidea) in Africa Harry C. EVANS* and Paresh A. SHAH† CABI Bioscience UK Centre, Silwood Park, Ascot, Berks. SL5 7TA, UK. E-mail: h.evans!cabi.org Received 2 September 2001; accepted 28 April 2002. The occurrence of disease outbreaks associated with the genus Sorosporella on grasshoppers and locusts (Orthoptera: Acridoidea) in Africa is reported. Infected hosts, representing ten genera within five acridoid subfamilies, are characterized by red, thick-walled chlamydospores which completely fill the cadaver. On selective media, the chlamydospores, up to seven-years-old, germinated to produce a Syngliocladium anamorph which is considered to be undescribed. The new species Syngliocladium acridiorum is described and two varieties are delimited: var. acridiorum, on various grasshopper and locust genera from the Sahelian region of West Africa; and, var. madagascariensis, on the Madagascan migratory locust. The ecology of these insect-fungal associations is discussed. Sorosporella is treated as a synonym of Syngliocladium. INTRODUCTION synanamorph, Syngliocladium Petch. Subsequently, Hodge, Humber & Wozniak (1998) described two Between 1990 and 1993, surveys for mycopathogens of Syngliocladium species from the USA and emended the orthopteran pests were conducted in Africa and Asia as generic diagnosis, which also included Sorosporella as a part of a multinational, collaborative project for the chlamydosporic synanamorph. biological control of grasshoppers and locusts of the Based on these recent developments, the taxonomic family Acridoidea or Acrididae (Kooyman & Shah status of the collections on African locusts and 1992). These include some of the world’s most grasshoppers is re-assessed and the ecological impli- destructive agricultural pests, with the most damaging, cations are discussed. the plague or migratory species, collectively being referred to as locusts. During the early surveys in Mali, grasshopper MATERIALS AND METHODS cadavers were collected with characteristic red, dry and The techniques employed for the survey and collection powdery infections. The causal agent of the disease of diseased orthopterans have been described earlier outbreak on nymphs of Kraussaria angulifera was (Kooyman & Shah 1992, Shah et al. 1997). identified as belonging to the genus Sorosporella, Isolations were made either by aseptically removing typified by brightly coloured or pigmented chlamydo- chlamydospore masses from host cadavers and spores (Samson, Evans & Latge 1988), and an associated streaking them onto agar media or by shaking the conidial state was isolated in culture (Shah 1993). cadavers directly over the exposed agar plates con- Subsequent surveys in West Africa revealed the same taining: mealworm agar (MWA; Samson & Evans fungus on a number of other acridoid genera (Shah et 1974); potato carrot agar (PCA) amended with cyclo- al. 1994, Shah, Kooyman & Paraı$ so 1997). Parallel heximide; or, a selective medium (VMA) for detecting surveys in Madagascar showed a similar disease on the Verticillium chlamydospores in soil (Christen 1982). African migratory locust which also produced a conidial Subcultures were maintained on PCA, MWA and anamorph in vitro (Welling et al. 1995). Shah & Evans Molisch’s agar (MOA) (Speare 1920), at 25 mC, with a (1997) briefly reported on these findings and expressed 12 h black light cycle. reservations about the taxonomic status of the genus Sorosporella and its associated but poorly defined ECOLOGY Infected orthopterans, characterized by red-coloured, * Corresponding author. mummified cadavers, were collected in the West African † Current address: Plant & Invertebrate Ecology Division, IACR- Rothamsted, Harpenden, Herts AL5 2JQ, UK. countries of Benin, Chad, Niger and Mali (Figs 1, 2), as Sorosporella and Syngliocladium on grasshoppers and locusts 738 Figs 1–6. Syngliocladium acridiorum on African grasshoppers and locusts. Figs 1–2. S. acridiorum var. acridiorum on nymphs of Kraussaria angulifera from Mali (IMI 386212). Note brittle condition of the cadavers, in which the appendages and sclerites are frequently missing exposing the red, powdery masses of chlamydospores. Bar l 10 mm and 5 mm respectively. Fig. 3. Area of collection in south-west Madagascar of locusts infected with S. acridiorum var. madagascariensis. Arrow shows a band of hoppers or nymphs migrating across the savannah. Figs 4–5. S. acridiorum var. madagascariensis (IMI 386216) in situ on adults of Locusta migratoria capito. Cadavers occur directly on the soil surface and slowly disintegrate to liberate irregular masses of chlamydospores (arrowed). Bar l 10 mm. Fig. 6. S. acridiorum var. madagascariensis in vitro, isolated from chlamydospores of IMI 386216; seven-month-old culture on MWA showing white, convoluted stromatic colony producing abundant synnematal initials and mature synnemata (arrowed). Bar l 15 mm. H. C. Evans and P. A. Shah 739 Table 1. Hosts of Syngliocladium acridiorum var. acridiorum diseased grasshopper specimens examined from West recorded from grasshoppers and locusts in West Africa, 1990–93. Africa and Madagascar, showed any external fungal Acridoidea Benin Chad Mali Niger structures and it would appear that the only spore type produced on the host in the field is the endogenous, Acrididae resting or chlamydospore stage, assignable to the genus Oedopodinae Sorosporella. Plating of the chlamydospores, from Acrotylus blondeli" jj Gastrimargus africanus africanus j specimens collected up to seven-years previously and Oedaleus nigerensis j stored at 20–23 m, resulted in the production of slow- Oedaleus senegalensis# j growing colonies bearing conidiogenous structures as Cyrtacanthacridinae described and illustrated by Speare (1920) and Pendland Anacridium m melanorhodon# . j & Boucias (1987) for a Syngliocladium synanamorph Kraussaria angulifera" jj Ornithacris cavroisi j associated with Sorosporella infections of moths (Lepi- Cantontopinae doptera: Noctuidae) and mole crickets (Orthoptera: Diablocatantops axillaris" jj Gryllotalpidae) respectively. Hemiacridinae Hieroglyphus daganensis" jj Pyrgomorphidae (syn. Pyrgomorphinae)* TAXONOMY Pyrgomorpha cognata species jjjj complex Morphologically, the West African isolates can be distinguished from previously described Syngliocladium " Species of slight or occasional economic importance. # Aggregating grasshopper or locust species of great economic species (Hodge et al. 1998), and from the Madagascan importance. isolates. However, because of the overall similarities of * Recognised as a subfamily by Johnston (1956), but as a separate the pathogens associated with acridoid hosts, separation family by Dirsh (1965). at the varietal level is recommended. The new species, Syngliocladium acridiorum is therefore proposed with well as from the island of Madagascar (Figs 3–5). These two varieties. represented ten different genera within five subfamilies of Acridoidea (Table 1). The African migratory locust occurs as two distinct subspecies but, significantly, no (a) infections were recorded on the mainland type, Locusta ( f ) migratoria migratorioides which is endemic to the Niger floodplain. In contrast, the only collections of the pathogens from Madagascar were made from the 50ím subspecies unique to the island, L. m. capito. Infected locusts were found in the south-west region from (g) 1992–93 (Welling et al. 1995), and again in 1997 (H. C. (b) Evans, unpubl.; Sakahara, April 1997), where this species is a major pest of annual crops. In the Sahelian region of West Africa, Oedaleus senegalensis (Senegalese 10ím grasshopper) is now the principal pest of rain-fed cereal (i) crops, whilst several of the other aggregating species, (h) such as Hieroglyphus daganensis (rice locust), (c) Anacridium melanorhodon (tree locust) and Kraussaria (e) angulifera have also attained pest status in recent years (k) (Jago 1990). Field symptoms have been described and illustrated 10ím in detail for disease outbreaks on West African (h) grasshoppers (Shah & Evans 1997). Typically, the (d) cadavers are found attached to the lower vegetation in the early stages but, later, these often fall to the soil. ( j) However, the locust cadavers in Madagascar always occurred on the soil surface in various stages of degradation (Figs 4–5). There was no evidence of the summit disease behaviour, so symptomatic of acridoids Fig. 7. Syngliocladium acridiorum. (a–e) var. acridiorum (IMI 386212). (a) Chlamydospores aggregated into discrete balls or infected with Entomophaga grylli (Fresen.) Batko sclerotia; (b) chlamydospores; (c) conidiophores; (d) macr- (Samson et al. 1988). Weathering of the cadavers results oconidia; (e) microconidia. (f–k) var. madagascariensis (IMI in the brick-red chlamydospore masses (Fig. 5), or 386215): (f) chlamydospores, aggregation or agglutination; aggregations (Speare 1920), or agglutinations (Welling (g) chlamydospores; (h) conidiophores; (i) macroconidia; (j) et al. 1995), being exposed and released onto the microconidia; (k) macroconidia producing microconidia vegetation and soil. None of the many hundreds of directly. Bars l 10 µm. Sorosporella and Syngliocladium on grasshoppers and locusts 740 Fig 8–13. Syngliocladium acridiorum var. acridiorum (IMI 386212). Fig. 8. Synnemata produced on PCA after 10 weeks. Bar l 1n5 mm. Fig. 9. Conidiophores
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