152

FUNGAL PATHOGENS OF SPIDERSHe EVANS

CAB International Institute of Biological Control , Silwood Park, As cot,Berk s SL5 7PY, UK

AND R A SAMSONCentraalbureau voor Schimmelcultures, P.O . Box 2 73 , 3740 AG Baarn,

The Netherlands

This article deals exclusively with thosefung i which are proven or purportedpathogens of spiders (Aranea e,Arachnida). They are usually includedw ithin the umbrella terms of entomo-genous or entomopathogenic fungi(Evans, 1982; Samson et 01. , 1987), sincethey share a similar morphology andbiology with some groups of insectpathogens. Purists may argue for moreprecise teminology, such as araneo-genous or araneopathogenic fungi , tor eadily identify the pathogen-hostassociations involved. Indeed, many ofthe mycologists mentioned in the follow-in g pages have been guilty of confusingspiders with insects in their publicationsand all , including the present authors,have paid sparse attention to determin-ing the spider hosts attacked by thesefun gi. In part, this has undoubtedly beendue to a dearth of arachnologists whoseservices can be called upon to give apositive indentification. This poor inter-disciplinary collaboration is evidencedby the absence of any reference to fun galpathogens in published works on thebiology of spiders, even when naturalenemies are discussed (Foelix, 1982;Nentwig, 1986).

There is abundant cir cumstantialevidence, both from field obs ervationsand from analogy with closely-related in-sect fung i, to support the statement thatmost, if not all, of the fungi includedhere, can be implicated directly in spidermortality. The cuticle of spiders is essen-tially similar in composition to that of in-sects (Foelix, 1982). Nevertheless, thehard exo cuticle, characteristi c of ins ectexoskeleton , is not present in the ab-dominal region (opisthosoma) of spiders.Physically, therefore, the opisthosomamust be considerably easier for fung al

spore penetration th an th e remammgspider exoskeleton, or compared to thatof insects. Invariabl y, th is is the part ofthe spider which first becomes mummi-fied and which later bears most of th eexternal fungal mycelium and fructifica-tions. It is suggested th at the majority offungal infections take place through thespider abdom en , involving bothmechanical and enzymatic penetration,and that the fungus once inside thehaemocoele enters a yeast phase whichsubsequently produces a toxin lethal tothe spider host. A review of fungalpathogenesis in insects can be found inSamson et 01. (1987) . There is no reasonto believe that the process is significantlydifferent in spiders.

The following is an account of thehistory, ta xonomy and ecology of thefungal pathogens of spiders : the first ofits kind, although a few papers relatingspecifically to descriptions of fungi onspiders have been published (Mains,1950, 1954; Kobayasi & Shimizu, 1976).It is not intended to be a comprehensivereview. The list of references has beenpruned as far as possible, withouthindering the more committed readerfrom gaining a ccess to the 60-70specialist taxonomy references con-sulted during the preparation of thisarticle.

HI STOR Y

That spiders are subject to lethal fungalinfections has been known for some con-siderable time. Gray (1858) describedseveral entomopathogenic fungal speciesand indicated that both the adult and eggstages may be attacked . According toPetch (1932), th e first illustration of afungus on a sp ider host was by Ditmar

in 1817 . This is reproduced in Gray'spublication and the same species (Akan-thomyces aranearum, see Fig . 7) wasredescribed by Cooke (1892), in hismasterly treatise on entomogenousfungi. For a more detailed insight intothe subject, however, we are indebted tothe industriousness of T Petch who nam-ed and described a large number of fungifrom spider hosts. E B Mains made ashorter but no less effective contributionto our knowledge of these specialised

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153(Basidiomycotina) att ackin g or activelyparasitising spiders. There are recordsof such fungi, someti mes with araneo-genous epithets, on spider hosts in themycological lit erature but these appearto be either secondary colonisers ofspider cadavers or hyperparasitic onobligate fungal pathogens. The Ento-mophthorales , for example, are com-monly reported on most groups of ter-restrial arthropods but, seemingly, havenever been described from spiders. In-deed, the true pathogens are restrictedto members of the Clavicipitales, andtheir hyphomycete anamorphs, whichhave de veloped mechanisms enablingthem to invade, kill and colonise both in-sect and spider hosts . Some genera andspecies occur only on sp iders whilstothers are less sel ective in their hostrange. The following genera have beenrecorded on spiders and are either con-sistently or uniquely associated withthese hosts:

Ascomycotina, Clavicipitales

Cordyceps (Fr .) Link (Figs . 3-4)At least eight species have been confirm-ed on spiders (Kobayasi, 1941, 1982 ;Kobayasi & Shimizu, 1976, 1983 ; Mains,1954).

Fi g. 1. Fungal genera on spiders. (AJ Hirsu-telIa; (BJHymenostilbe; (C) A kanthomyces : (DJCl athroconium ; (EJ Gihellula ; (F)

Granulomanus . (Bar = 10um).

fungi, whilst Y Kobayasi, has had a longassociation with fungal pathogens ofspiders which began more than 40 yearsago with his classic monograph (Koba-yasi, 1941) and has continued virtuallyto the present day (Kobayasi & Shimizu,1983) . Recent observations made by uson material collected in tropicalecosystems over the past 15 years, in-dicate that there are many species, andpossibly genera, still to be described andeven more awaiting discovery.

TAXONOMY

Significantly, perhaps, there are noknown representatives of the lower fungi(Mastigomycotina) or the higher fungi

Torrubiella Baud. (Figs. 2D , 5)Twenty-seven species hav e been describ-ed from spider hosts (Koba yasi , 1982;Kobayasi & Shimizu, 1983).

Deuteromycotina, Hyphomycetes

Akanthomyces Leb . (Figs. lC, 7)Three species reported so far fromspiders; both Cord ycep s and Torrubiellateleomorphs have been proposed for twoof these species (Samson & Evans, 1974).

Clathroconium Samson & Evans (Fig. ID)Monotypic genus, only on spiders;telemorph unknown (Samson & Evans,1982).

Engyodontium de Hoog (Fig. 2C)Three species on spiders; Torrubiellateleomorph reported (Gams et al. , 1984).

154

Fig. 3. Cordyceps caloceroides on Mugale spider, Brazil. Fig. 4. C. cylindrica on trapdoor spiderhidden in tunnel nest. Brazil. Fig. 5. Perithecia of Torrubie11a sp. on small salticid spider, noteorange ostioles emerging from yellow mycelial weft around perithecia, Ecuador. Fig. 6. Close-up

of ostiolar region with emergent capitate asci.

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Fig. 7. Akanthomyces aranearum, Ecuador. Fig. 8. Hymenostilbe sp. on salticid spider, Brazil.Fig. 9. Granulomanus synanamorph of Gibellula sp., Sulawesi. Fig. 10. VerticiIIium anamorph

from ascospore culture of Cordyceps caloceroides, Brazil.

156

Cibellula Cav. (Figs. lE, 11-17)Four species validated, genus confinedto spider hosts (petch, 1932; Mains, 1950;Samson & Evans, 1973; Kobayasi, 1982;Kobayasi & Shimizu, 1983). Synana-morph: Cranulomanus de Hoog & Sam-son (Fig. IF).

Hirsutella Pat. (Fig. lA)One authenticated species (Evans & Sam-son, 1982) but Kobayasi & Shimizu (1976)mention a Hirsutella anamorph whendescribing a new Cordyceps taxon fromspiders.

Hymenostilbe Petch (Fig. IB)Two species reported to attack spiders;teleomorph connection unproven (Sam-son & Evans, 1975).

Fig. 2. Fungal genera on spiders. (A)Nomuraea; (8) PaeciJornyces; (C) Engyodon-tium; (D) Torrubiella (ex M E 8oudier, 1885).

Nomuraea Maubl. (Fig. 2A)One species only but common on spiders(Kobayasi, 1941; Samson, 1974); Cor-dyceps teleomorph now confirmed(Evans, 1982).

Paecilomyces Bain. (Fig. 2B)Two species associated with spiders(Samson, 1974); teleomorph probably inthe genus Cordyceps.

Verticillium Nees per Link (Fig. 10)Two species recorded on spider hosts(Cams, 1971), but several of thearaneogenous Cordyceps species havebeen shown to produce Verticilliumanamorphs in culture (pers. obs.).

It is surprising that some of theplurivorous, cosmopolitan insectpathogens, such as Beauveria bassiana(Bals.) Vuill. and Metarhiziumanisopliae(Metsch.) Sorok., are not morecommon on spider hosts. The completeabsence of any spider pathogen in theEntomophthorales is intriguing.

In the genus TorrubieIIa, the promi-nent perithecia develop directly on thespider cadaver, typically on the abdomenand buried to some extent in a dense, fre-quently brightly-coloured mycelium. Asin most of the fungi included here, themycelium also extends onto the substratehelping to fix the spider in position. Theperithecia in the genus Cordycepsdevelop on aerial structures (stromata).The associated anamorph can occurdirectly on the mycelium or on syn-nemata of varying complexity.

ECOLOGY

Most of the fungal-infested spiderspecimens examined by the authors havebeen from subtropical and tropical forestecosystems and this reflects the richnessof these habitats as sources of entomo-pathogenic Clavicipitales (Evans, 1982).The diseased spider hosts are usuallyfound on the undersides of lower storeyshrubs and herbs, but occasionally ontree boles. Most are free-living adultspiders (possibly Salticidae), althoughclutches of eggs and smaller spiders, en-cased in tough silken threads or bags, arealso subject to attack. The larger forms(Mygalidae) occur in the leaf litter orburied in the soil in their silk-lined tun-nels. There is evidence that tropical orb-weaving spiders of the genera Argiopeand Nephila (Araneidae) are also infectedby pathogenic fungi, especially byNomuraea atypicola (Yasuda) Samson,dying in their webs or nearby on abnor-mal reduced webs (W Nentwig, pers.cornm.), The latter fungus has an in-teresting host range since it is also

prevalent on large trapdoor spiders inJapan (Kobayasi, 1941), producingelaborate synnemata on the subterra-nean hosts. Synnematal function in N.atypicola is clear cut. In Gibelluia it maybe two-fold: improving dispersal efficien-cy by lifting the conidiophores into amore exposed position, thereby takingadvantage of any air movement; aug-menting sporulation capacity, particular-lyon small spiders, by increasing thespore-bearing area through complexbranching. The apparent success ofGibellula as a spider pathogen may alsobe due to its ability to diversify itsresources. The Granulomanussynanamorph could be directed at poten-tial spider hosts coming into physicalcontact with the infected cadaver, ratherthan for aerial dispersal. However,movement of inoculum within theecosystem is a speculative subject sincewe have no information on how andwhen the various types of spidersbecome infected.

Evans (1974) regularly recorded en-tomopathogenic fungi on spiders inforest habitats in Ghana. Six collectingsites (20m') were sampled monthly overa one-year period and, after ants and coc-cids, spiders were found to be the groupof arthropods most affected by fungalpathogens. Over 150 specimens, repre-senting 15 species in 10 genera, were col-lected. Samson & Evans (1973) alsorecorded high levels of spider mortalityin Ghanaian cocoa farms, collecting 82specimens of Gibelluia pulchra(Sacc.)Cav. from 10 sample trees. Petch (1932)reported the same fungus as common atlower (tropical) altitudes in Sri Lanka.Another species of Gibellula, as yetundescribed, was collected in epizooticproportions over several years inEcuadorian cocoa farms. A more recentsurvey was carried out in a monsoonforest habitat in the Far East (Sulawesi,Indonesia) and, out of a total of 690fungal-infected arthropods, gatheredduring a three-week visit, 137 werespider hosts, or approximately 20% ofthe collection. Members of the genusGibellula were especially wellrepresented and this island seems to be

157a centre of diversity of these specialisedspider pathogens (H C Evans, Unpubl.).Although it has not been possible toquantify the data further, spider popula-tions are at a low level in most undisturb-ed tropical forests . It is concluded,therefore, that fungal pathogens con-stitute a significant spider mortality fac-tor in such ecosystems. This is not to saythat such fungi are rare or absent inother, less humid, temperate regions.Leatherdale (1958), for example, lists 13species of fungal pathogens on spidersin the UK. The predominantly temperateAsian collections of Kobayasi (1982) andKobayasi & Shimizu (1983), furthermoretestify to their ubiquitousness.

It is now becoming increasingly ap-parent that spiders are an importantcomponent in the biological control ofpest insects. Are fungal pathogens ofspiders, therefore, a negative componentin terms of pest control? Severalarguments for and against can be put for-ward. Spiders do prey on pests and, con-sequently, any mortality factor ofarachnids must be looked upon asdetrimental to the crop and hence toman. Nevertheless, spiders are alsonatural enemies of beneficial insects andcan destroy large numbers of insectpredators. Moreover, they also competewith the latter for prey. Whichever argu-ment is valid, and it could be either giventhe complexity of tropical cropecosystems, the status of fungalpathogens should be carefully evaluatedin any modelling of spider populationdynamics.

There seems to be no better way of en-ding this article than by drawing uponthe still relevant remarks from one of theearliest reviews on en to mapathogenicfungi: "It is hoped, in conclusion, thatthese pages may awaken some curiosi-ty, if not interest, in favour of thesesingular productions, and thus lead tofurther inquiry as to the species of in-sects that unfortunately become thebases of the fungoid parasites" (Gray,1858).

We would like to thank Dr C Prior forpermission to use Fig . 11 and Ms GGodwin for photographic assistance.

158

Figs. 11-17. Variations on a theme - the genus Gibellula. Fig. 11. Gibellula leiopus, sugarcanespider, Trinidad. Figs. 12-17. Undescribed Gibellula spp. on small, free-living salticid spiders

from tropical forests.

159REFERENCES

COOKE, M C (1892). Vegetable Wasps andPlant Worms. London: Society for Pro-moting Christian Knowledge, 364 pp.

EVANS, H C (1974). Natural control of arthro-pods, with special reference to ants [Fermi-cidae], by fungi in the tropical high forestof Ghana. Journal of Applied Ecology 11,37-49.

EVANS, H C (1982). Entomogenous fungi intropical forest ecosystems: an appraisal.Ecological Entomology 7, 47-60.

EVANS. H C & SAMSON, R A (1982). Entorno-genous fungi from the Galapagos Islands.Canadian Journal of Botany 60, 2325-2333.

FOELlx, R F (1982). Biology of Spiders. Cam-bridge, Massachusetts: Harvard UniversityPress, 306 pp.

GAMS. W (1971). Cephalosporium-urtige,SchimmelpiIze (Hyphomycetes). Stuttgart: GFischer, 262 pp.

GAMS, W, HOOG, C S DE, SAMSON, R A &EVANS, H C (1984). The hyphomycete genusEngyodontium a link between VerticiIliumand Aphanocladium. Persoonia 12, 135-147.

GRAY, R C (1858). Notices of Insects that areKnown to Form the Bases of FungoidParasites. London: Privately Printed, 22 pp.

KOBAYASI, Y (1941). The genus Cordyceps andits allies. Science Reports of the TokyoBunrika Daiguku 5, 53-260.

KOBAYASI, Y (1982). Keys to the taxa of thegenera Cordyceps and TorrubieIIa. Transac-tions of the Mycological Society of Japan 23,329-364.

KOBAYASI, Y & SHIMIZU, D (1976). Somespecies of Cordyceps and its allies onspiders. Kew BuIIetin 31, 557-566.

KOBAYASI, Y & SHIMIZU, D (1983). Iconography

of Vegetable Wasps and Plant Worms. Osaka,Japan: Hoikusha Publ. Co., 280 pp.

LEATHERDALE, D (1958). A host catalogue ofBritish entomogenous fungi. The Entomo-logist's Monthly Magazine 64, 108-110.

MAINS, E B (1950). The genus GibeIIula onspiders in North America. Mycologia 42,306-321.

MAINS, E B (1954). Species of Cordyceps onspiders. BuIIetin of the Torrey Botanical Club81, 492-500.

NENTWIG, W (Ed.) (1986). Ecophysiology ofSpiders. Berlin: Springer-Verlag, 430 pp.

PETCH, T (1932). Gibellula. AnnalesMycologici 30, 386-393.

SAMSON, R A (1974). PaeciIomyces and someallied Hyphomycetes. Studies in Mycology6,119 pp.

SAMSON R A & EVANS, H C (1973). Notes onentomogenous fungi from Ghana. I. Thegenera GibeIIula and PseudogibeIIula. ActaBotanica Neerlandica 22, 522-528.

SAMSON, R A & EVANS, H C (1974). Notes onentomogenous fungi from Ghana. II. Thegenus Akanthomyces. Acta BotanicaNeerlandica 23, 28-35.

SAMSON, R A & EVANS, H C (1975). Notes onentomogenous fungi from Ghana. III. Thegenus HymenostiIbe. Proceedings of theKoninkIijke Nederlandse Akademie vanWetenschappen, Amsterdam 78, 73-80.

SAMSON, R A & EVANS, H C (1982).Clathroconium, a new helicosporoushyphomycete genus from spiders. CanadianJournal of Botany 60, 1577-1580.

SAMSON, R A, EVANS, H C & LATGE, J P (1987).An Atlas of Entomopathogenic Fungi. Berlin:Springer-Verlag (In Press).

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