Keratinophilic Fungi Associated with Free-Living Mammals and Birds

93 Keratinophilic fungi associated with free-living mammals and birds

Z. Hubalek

Institute of Vertebrate Biology, Academy of Sciences, Valtice, Czech Republic

Summary A concise list of records of keratinophilic fungi mainly isolated from hair [in mammals] or feathers [in birds] of asymptomatic animals or from their nests is given. Their frequency of occurrence and different ecological aspects of the association of keratinophilic fungi with wild vertebrates are also discussed. Key words Keratinophilic fungi, Mammals, Birds

‘Keratinophilic’ (i.e., often occurring on keratinous In the following concise list of records of KF spe- substrates) and ‘keratinolytic’ (keratin-decomposing) cies, the isolates were obtained from hair (in mammals) or fungi should be differentiated. Some keratinophilic fungi feathers (in birds) of asymptomatic animals, unless other- namely do not digest keratin and live off components wise indicated. The paragraph ‘Ref.’ (References) lists other than the keratin of the keratinous structures [1-4]. In published records and the ‘Coll.’ (Collections) additional this review, only the keratinolytic fungi (KF) are treated. KF strains deposited in culture collections, which were Non-keratinolytic keratinophilic fungi found on wild ver- isolated from wild vertebrates. tebrates range among members of the genera, e.g., Amauroascus albicans (Apinis) von Arx Acremonium, Alternaria, Arcuadendron, Chaetomium, Syn. Arachniotus albicans Apinis. Chrysosporium (C. luteum, C. merdarium, C. olivaceum, Ref. Rodents (Microtus arvalis, Apodemus flavico- C. pruinosum, C. inops), Cladosporium, Curvularia, llis, A. agrarius, A. sylvaticus) in Czechland and Geomyces (G. pannorus), Gliomastix, Gymnascella (syn. Yugoslavia [12]. Bird feathers, nests (Tyto alba, Passer Arachniotus; G. aurantiaca, G. citrina, G. dankaliensis, domesticus, P. montanus) and pellets (Asio otus, Merops G. hyalinospora, G. marginospora, G. nodulosa), apiaster) in England, Czechland and Yugoslavia [13-15]. Gymnoascus (G. reessii), Myxotrichum, Pseudogymno- Aphanoascus durus (Zukal) Cano et Guarro ascus, Scopulariopsis or Sepedonium. Many of them are Syn. Gymnoascus durus Zukal, Keratinophyton cellulolytic. durum (Zukal) Currah. Only free-living homoiotherm (endotherm) verte- Coll. UAMH 3671: hedgehog, Ivory Coast brates including, e.g., feral pigeons, have been involved in (M. P. English). this survey, whereas domestic animals, captive wild ani- Aphanoascus fulvescens (Cooke) Apinis mals, and those living in zoological gardens or farms have Syn. Anixiopsis stercoraria (Hansen) Hansen, been omitted. A. fulvescens (Cooke) de Vries. Occasional skin lesions in mammals including Species of keratinolytic fungi associated man. Ref. Mammals (Erinaceus europaeus, Sorex ara- with wild vertebrates neus, Neomys anomalus, Clethrionomys glareolus, Microtus arvalis, M. subterraneus, Apodemus agrarius, Teleomorph genera of KF associated with free- A. flavicollis, A. sylvaticus, Tatera indica, Millardia mel- living mammals or birds are classified in two families of tada, Oryctolagus cuniculus, Dama dama, Sus scrofa - the ascomycetaceous Onygenales: Arthrodermataceae lesions) in India, Czechland, Slovakia, Yugoslavia, (Arthroderma, Ctenomyces) and Onygenaceae Denmark, Belgium and France [12,16-20]. Birds (Amauroascus, Aphanoascus, Apinisia, Auxarthron, (A. anser, Anasplatyrhynchos, Fulica atra, Phasianus col- Oncocladium, Onygena, Shanorella, Uncinocarpus). chicus, Tringa glareola, Tyto alba, Ficedula hypoleuca, Anamorphs involve Arthrographis, Chrysosporium, Phylloscopus collybita, Panurus biarmicus, Turdus meru- Malbranchea, Microsporum, Trichophyton, Monodictys la, Phoenicurus ochruros, S. serinus, Emberiza schoeni- and Myriodontium [5-11]. clus, Passer domesticus, P. montanus, Corvus monedula, P. pica) and their nests (Podiceps cristatus, P. nigricollis, P. ruficollis, Ixobrychus minutus, Aythya fuligula, Larus ridibundus, Columba livia, Streptopelia decaocto, Tyto alba, Anthus trivialis, Motacilla alba, Ficedula albicollis, P. collybita, Acrocephalus arundinaceus, Turdus philome- Corresponding address: los, T. merula, Lanius collurio, Parus major, P. ater, Dr. Z. Hubalek Laboratory of Medical Zoology Hirundo rustica, Delichon urbica, R. riparia, Carduelis Institute of Vertebrate Biology, chloris, Fringilla coelebs, P. montanus, Sturnus vulgaris) Academy of Sciences, Klasterni 2, CZ-69142 Valtice, Czech Republic in England, Czechland, Yugoslavia and Denmark Fax: +420 627 352387 [14,15,17,21-25]. Bird pellets (Bubo virginianus, Tyto E-mail: [email protected] alba, Asio otus, Falco tinnunculus, Merops apiaster) in ©2000 Revista Iberoamericana de Micología England, Czechland,Yugoslavia, Denmark and Canada Apdo. 699, E-48080 Bilbao (Spain) [9,14,15,17, 26,27]. 94

Aphanoascus keratinophilus Punsola et Cano Arthroderma benhamiae Ajello et Cheng Anam. Chrysosporium keratinophilum (Frey) Anam. Trichophyton mentagrophytes (Robin) Carmichael. Blanchard. Three anamorph varieties of this zoophilic der- Ref. Mammals (Crocidura russula, Sorex sp., matophyte are associated with free-living vertebrates: Talpa europaea, Clethrionomys glareolus, Microtus arva- T. m. var. mentagrophytes; lis, Apodemus flavicollis, A. sylvaticus, Tatera indica, T. m. var. quinckeanum (agent of classical mouse Rattus rattus, R. norvegicus, Mus platythrix, Funambulus favus); palmarum, Bandicota indica, Oryctolagus cuniculus) in T. m. var. erinacei (= T. proliferans English et Germany, Czechland, Slovakia, Yugoslavia, India, Stockdale). Nigeria and France [12,16,19,20,28,29]. Birds (Anas T. m. mentagrophytes is an important zoophilic platyrhynchos, Aythya fuligula, Larus argentatus, dermatophyte transmissible to humans principally from Lagopus lagopus, Phasianus colchicus, Dendrocopos mammals, especially rodents [39-44], but also kangaroos major, Columba livia, Galerida cristata, Sylvia curruca, [45,46]. Wild rodents are reservoirs for T. mentagrophytes Phylloscopus collybita, P. trochilus, Acrocephalus scirpa- in agroecosystems. ceus, Turdus philomelos, T. merula, Parus major, Passer Ref. Mammals (Erinaceus europaeus - lesions, domesticus, P. montanus, C. carduelis, S. serinus, Sturnus Talpa europaea, Sorex araneus, Ondatra zibethicus - vulgaris, Corvus monedula, P. pica) and their nests lesions, Myocastor coypus - lesions, Arvicola terrestris, (P. puffinus, Streptopelia decaocto, Tyto alba, D. major, Microtus agrestis, M. arvalis, M. oeconomus - lesions, G. cristata, Hirundo rustica, Delichon urbica, R. riparia, M. pennsylvanicus, Clethrionomys glareolus, C. rutilus, Motacilla cinerea, Muscicapa striata, Ficedula albicollis, Apodemus flavicollis, A. sylvaticus, A. agrarius, Sylvia atricapilla, P. collybita, T. merula, Prunella modu- Peromyscus gossypinus, P. polionotus, P. maniculatus, laris, Phoenicurus ochruros, Lanius collurio, P. major, Dipodomys ordii, Rattus norvegicus, R. rattus, R. exulans, P. ater, Sitta europaea, Carduelis chloris, C. cannabina, Funambulus palmarum, Mus musculus, Meriones ery- S. serinus, Fringilla coelebs, P. domesticus, P. montanus, throurus, Sigmodon hispidus, Hystrix africaeaustralis, S. vulgaris, C. monedula) in England, Czechland, Sciurus carolinensis, S. vulgaris - lesions, Lepus europa- Yugoslavia, Russia and France [14,15,21,24,25,30-33]. eus - lesions, L. americanus - lesions, Sus scrofa, Cervus Bird pellets (Falco tinnunculus, Asio otus, Merops apias- elaphus, Odocoileus virginianus, Capra ibex, B. bison, ter) in England, Czechland and Yugoslavia [14,15,27]. Canis lupus, C. latrans, Procyon lotor - lesions, M. me- Aphanoascus reticulisporus (Routien) Hubalek phitis, Mustela nigripes, Taxidea taxus, V. vulpes, Syn. Anixiopsis reticulispora Routien. M. meles, Macropus major, Wallabia spp., Trichosurus Anam. Chrysosporium sp. vulpecula, Didelphis marsupialis, D. virginianus, Ref. Rodents (Apodemus flavicollis), Yugoslavia Glossophaga soricina, Pteronotus psilotus) in USA, [12]. Birds (Passer domesticus, Corvus monedula) and Australia, New Zealand, Egypt, Africa, Azerbaijan, their nests (Carduelis cannabina, C. monedula) in Romania, Slovakia, England, Russia, Germany, Italy, Czechland, Yugoslavia and India [14,15,34]. France, Austria, Croatia, Poland, India, Nigeria, Columbia Aphanoascus terreus (Randhawa et Sandhu) [20,25,28,29,35,36,41,42,44-77]. Birds (Tympanuchus Apinis phasianellus - favus, Fulica atra, Sylvia curruca, Syn. Keratinophyton terreum Randhawa et Emberiza schoeniclus), USA and Czechland [25,64,78]. Sandhu. Coll. UAMH 3490: Passer montanus nest, Bzenec, Anam. Chrysosporium indicum (Randhawa et Czechland, 1971 (Z. Hubalek 909A). 552A: an abandoned Sandhu) Garg. (and by rodents visited) nest of Anas strepera near Ref. Mammals (Suncus murinus, Neomys anoma- Pohorelice, Czechland, 1970 (Z. Hubalek, confirmed by lus, Apodemus agrarius, A. flavicollis, A. sylvaticus, Mus L. Sigler). platythrix, M. musculus, Tatera indica, Rattus rattus, T. m. quinckeanum (Zopf) Smith et Austwick cau- R. norvegicus, Cricetomys gambianus, Funambulus pal- ses favus in mice, less often in fox, squirrel, domestic marum, Cervus elaphus, V. vulpes) in Romania, Germany, mammals (e.g., cat) and humans. Wild mice have been India, Czechland, Yugoslavia, Nigeria [12,16,25,29, described as a cause of human favus in, e.g., Australia, 35,36]. Birds (Cygnus olor, A. anser, Fulica atra, Hungary, Yugoslavia and Russia [54,61,79-81]. Phasianus colchicus, Tringa glareola, Larus ridibundus, Ref. Isolated from wild rodents during epizootics Streptopelia turtur, Upupa epops, Parus major, C. coc- of favus in Hungary [80] and S. Australia [79]. cothraustes, Passer domesticus, P. montanus), their nests T. m. erinacei (Smith et Marples) Padhye et (Podiceps nigricollis, Ixobrychus minutus, Anas strepera, Carmichael causes skin disease in hedgehogs (England, Falco tinnunculus, F. atra, V. vanellus, L. ridibundus, France, Israel, New Zealand), transmissible to humans Tyto alba, Hirundo rustica, Turdus philomelos, T. merula, [63,82-84]. Carduelis chloris, P. montanus, Emberiza citrinella) and Ref. Mammals (Erinaceus europaeus - skin lesions pellets (Asio otus) in Czechland, Yugoslavia and India on the head especially on ear lobes, E. albiventris, rarely [14,15,24,34,37]. in Apodemus sylvaticus, Microtus agrestis, Mus musculus Coll. UAMH 2557: Milvus migrans, Queensland, and Rattus norvegicus) in New Zealand, England, Austria, 1965 (R.G. Rees H427), UAMH 3226: dead bird, Italy, Israel and Kenya [56,63,67,74,85-93]. Also in hiber- California, 1969 (J. W. Carmichael). nating hedgehogs and their nests in England [94]. Two of Apinisia queenslandica Apinis et Rees eight marked wild E. europaeus become infected (presu- Syn. Chrysosporium articulatum Sharapov. mably through bodily contact) in Bushy Park (London) Ref. Passer domesticus, India [38]. during the study period of about 15 months [90]. Coll. UAMH 4320: Sicista betulina, Novosibirsk, Generally, 20-25% of E. europaeus are infected in Russia, 1974 (V. M. Sharapov VKM-F2116) = CBS 662. England. Pathogenicity of the fungus for hedgehog is low, 78. UAMH 4709: Apodemus agrarius, Novosibirsk, but the infection usually persists throughout life. Russia, 1974 (V. M. Sharapov VKM-F2117) = CBS 663. Arthroderma borellii (Moraes, Padhye et Ajello) 78. Padhye, Weitzman, McGinnis et Ajello Keratinolytic fungi in wild vertebrates Hubalek Z 95

Syn. Nannizzia borellii Moraes, Padhye et Ajello. Pseudocheirus laniginosus) in Scotland, Australia, Anam. Microsporum amazonicum Moraes, Borelli Yugoslavia, Czechland and France [12,20,103,108]. Birds et Feo. (Climacteris leucophaea, Phasianus colchicus, Parus Ref. Rodents (Oryzomys sp., Proechimys cayen- major, Passer domesticus), their nests (Prunella modula- nensis) in Brazil [95-96]. ris, Turdus merula) and pellets (Asio otus) in England, Arthroderma cajetani (Ajello) Weitzman, Australia, Czechland, Yugoslavia and India [14,15,30, McGinnis, Padhye et Ajello 34,106]. Syn. Nannizzia cajetani Ajello. Arthroderma curreyi Berkeley Anam. Microsporum cookei Ajello. Probably iden- Ref. Mammals (Oryctolagus cuniculus burrows tical [97] is A. racemosum (Rush-Munro, Smith et Borelli) and hair, Erinaceus europaeus, Sorex araneus, Neomys Weitzman, McGinnis, Padhye et Ajello [basionym anomalus, N. fodiens, Crocidura suaveolens, C. russula, Nannizzia racemosa Rush-Munro, Smith et Borelli, anam. Talpa europaea, Clethrionomys glareolus, Microtus arva- Microsporum racemosum Borellii]. lis, M. subterraneus, Apodemus flavicollis, A. sylvaticus, Ref. Mammals (Erinaceus europaeus, Sorex ara- A. agrarius, Rattus rattus, R. norvegicus, R. assimilis, neus, Neotoma floridana, Microtus arvalis, Clethrionomys R. conatus, R. lutreolus, Melomys cervinipes, M. lutillus, glareolus, Apodemus flavicollis, A. sylvaticus, A. agra- Hydromys chrysogaster, Uromys caudimaculatus, rius, A. microps, Peromyscus gossypinus, P. polionotus, Isoodon macrourus, Trichosurus caninus, Perameles P. nuttalli, Mus musculus, Sigmodon hispidus, nasuta, D. dama, Rhinolophus ferrumequinum) in Great Reithrodontomys humulis, Rattus rattus, R. norvegicus, Britain, Australia, Yugoslavia, Czechland, Denmark, R. assimilis, R. lutreolus, Melomys cervinipes, Sciurus France [12,17,20,56,64,103,108]. Birds (Phasianus col- vulgaris, Sylvilagus floridanus, Oryctolagus cuniculus, chicus, P. perdix, Alectura lathami, Monarcha trivirgata, Didelphis marsupialis, Isoodon macrourus, Trichosurus Pitta versicolor, Colluricincla megarhyncha, Psophodes vulpecula, Perameles nasuta, Macropus major, olivaceus, Tringa glareola, Scolopax rusticola, Larus ridi- Pseudocheirus laniginosus, Aepyprymnus rufescens, bundus, Tyto alba, Columba livia, R. riparia, Motacilla M. mephitis, Procyon lotor, M. meles) in USA, New alba, Acrocephalus palustris, A. scirpaceus, A. schoeno- Zealand, Czechland, Slovakia, Yugoslavia, Romania, baenus, Sylvia communis, Phylloscopus collybita, Turdus Germany, England, France, Italy, Venezuela, Brazil and merula, T. philomelos, T. iliacus, Erithacus rubecula, Australia [12,19,28,35,41,51,52,57,63,64,67,69,72,100- Luscinia megarhynchos, Prunella modularis, T. troglody- 105]. Birds (Anas acuta, A. platyrhynchos, A. crecca, tes, Parus major, P. caeruleus, Panurus biarmicus, Sitta Aythya ferina, Fulica atra, Sterna hirundo, Larus argen- europaea, C. coccothraustes, Carduelis cannabina, tatus, Alectura lathami, Columbiformes, Cuculiformes, C. spinus, Fringilla coelebs, Passer domesticus, P. monta- Turdus merula, Parus major, C. coccothrauastes, Passer nus, Sturnus vulgaris, Corvus corone, C. monedula, montanus, Sturnus vulgaris, Emberiza schoeniclus, other P. pica, Garrulus glandarius, Emberiza citrinella, Passeriformes) and their nests (Delichon urbica, P. major, E. schoeniclus), their nests (Anas platyrhynchos, A. stre- Corvus monedula) in Australia, England, Czechland and pera, P. colchicus, Fulica atra, L. ridibundus, Hirundo Russia [14,15,21,31,32,106]. rustica, R. riparia, Muscicapa striata, Ficedula albicollis, Coll. UAMH 3282: ‘rat’, Mysore, India, 1969 = T. merula, T. philomelos, P. major, S. europaea, CDC B359. P. domesticus, P. montanus) and pellets (Asio otus) in Arthroderma ciferrii Varsavsky et Ajello England, Australia, Czechland, Yugoslavia, Denmark, Anam. Chrysosporium georgii (Varsavsky et Italy and France [13-15,17,21,24,25,30,31,33,67,106, Ajello) van Oorschot. 109,110]. Syn. Trichophyton georgiae Varsavsky et Ajello. Arthroderma flavescens Rees Ref. Mammals (Clethrionomys glareolus, Anam. Trichophyton flavescens Padhye et Apodemus flavicollis, A. sylvaticus, Oryctolagus Carmichael. cuniculus) in Yugoslavia, Czechland, Austria and France Ref. Birds (Trichoglossus moluccanus, Halcyon [12,20,74]. Birds (Columba livia, Merops apiaster, sancta) in Queensland [106,111]. Dendrocopos major, R. riparia, Acrocephalus scirpaceus, Arthroderma fulvum (Stockdale) Weitzman, Turdus merula, Aegithalos caudatus, Parus cyanus, McGinnis, Padhye et Ajello P. major, P. caeruleus, P. palustris, Passer domesticus, Syn. Nannizzia fulva Stockdale. P. montanus, Sturnus vulgaris, Corvus frugilegus, Anam. Microsporum fulvum Uriburu, closely rela- Carduelis cannabina), their nests (Anas platyrhynchos, ted to M. gypseum (Microsporum gypseum complex) Hirundo rustica, Delichon urbica, R. riparia, Muscicapa [112] and usually not differentiated in ecological studies. striata, P. phoenicurus, Parus ater, Sitta europaea, See Arthroderma gypseum. P. domesticus, P. montanus, Sturnus vulgaris) and pellets Arthroderma gloriae Ajello (Asio otus) in Czechland, Yugoslavia, Russia and France Anam. Trichophyton gloriae Ajello. [14,15,22-25, 32,33,107]. Ref. Mustela frenata,USA [64]. Coll. UAMH 1677: hedgehog (M. J. Marples). Arthroderma grubyi (Georg, Ajello, Friedman et UAMH 2535: Didelphis marsupialis, Georgia, USA, 1958 Brinkman) Ajello, Weitzman, McGinnis et Padhye (S. McKeever) = ATCC 44005. UAMH 2560: Rattus assi- Syn. Nannizzia grubyia Georg, Ajello, Friedman et milis, Queensland, 1965 (R. G. Rees H432). UAMH 4016: Brinkman. wild mouse 1976 (L. Kapica 11). Anam. Microsporum vanbreuseghemii Georg, Arthroderma cuniculi Dawson Ajello, Friedman et Brinkman. Possibly identical to Ref. Mammals (Oryctolagus cuniculus burrows M. gallinae (Megnin) Grigorakis [97]. Occasional infec- and hair, Neomys anomalus, Crocidura russula, tions in dog, cat and man. Clethrionomys glareolus, Microtus arvalis, Apodemus fla- Ref. Mammals (Ratufa indica, stray Felis catus, vicollis, A. sylvaticus, Rattus norvegicus, R. assimilis, Sciurus vulgaris) in India, Italy and Czechland Melomys cervinipes, M. lutillus, Hydromys chrysogaster, [64,113,114]. Uromys caudimaculatus, Isoodon macrourus, Trichosurus Arthroderma gypseum (Nannizzi) Weitzman, vulpecula, Perameles nasuta, Schoinobates volans, McGinnis, Padhye et Ajello, and 96

Arthroderma incurvatum (Stockdale) Weitzman, Coll. UAMH 2783: Thomomys talpoides burrow, McGinnis, Padhye et Ajello Edmonton, 1967 (D. Remington). Syn. Nannizzia gypsea (Nannizzi) Stockdale, and Arthroderma obtusum (Dawson et Gentles) N. incurvata Stockdale, respectively. Weitzman, McGinnis, Padhye et Ajello Anam. Microsporum gypseum (Bodin) Guiart et Syn. Nannizzia obtusa Dawson et Gentles. Grigorakis. Anam. Microsporum nanum Fuentes. A zoophilic In ecological studies, these two teleomorph species dermatophyte, causing skin disease in pig, man, and wild (and A. fulvum), i. e. the Microsporum gypseum anamorph monkeys (in Africa). complex, are usually not differentiated. Microsporum gyp- Ref. A wild mouse in Germany [28]. seum is a typical geophilic dermatophyte, causing infre- Arthroderma otae (Hasegawa et Usui) McGinnis, quent skin infections in mammals including man and in Weitzman, Padhye et Ajello domestic and caged birds. Syn. Nannizzia otae Hasegawa et Usui. Ref. Mammals (Erinaceaus europaeus, Sorex ara- Anam. Microsporum canis Bodin. A zoophilic der- neus, Crocidura leucodon, Suncus murinus, matophyte, often detected in domestic or stray cats and Clethrionomys glareolus, Microtus arvalis, M. subterra- dogs, but very rarely in free-living wild mammals. neus, Apodemus flavicollis, A. sylvaticus, Peromyscus Ref. Mammals (Urocyon cinereoargentatus, Rattus gossypinus, P. polionotus, Sigmodon hispidus, rattus, R. norvegicus, Mus musculus), USA and Italy Reithrodontomys humulis, Mus platythrix, M. musculus, [64,66,67]. Rattus norvegicus, R. rattus, R. assimilis, Melomys luti- Arthroderma persicolor (Stockdale) Weitzman, llus, Arvicanthis niloticus, Tatera indica, Meriones McGinnis, Padhye et Ajello hurriane, Sciurus carolinensis, Lepus europaeus, Syn. Nannizzia persicolor Stockdale. Oryctolagus cuniculus, D. dama, Rupicapra rupicapra - Anam. Microsporum persicolor (Sabouraud) lesions, Isoodon macrourus, Didelphis marsupialis, Guiart et Grigorakis. A zoophilic species, transmissions Procyon lotor, M. mephitis, Macropus major, Wallabia from rodents to man were described [122]. rufogrisea) in USA, Czechland, Egypt, England, Slovakia, Ref. Mammals (Neomys anomalus, Sorex araneus, Germany, Australia, Romania, Philippines, Italy, France, Clethrionomys glareolus, C. gapperi, Microtus arvalis, India and Nigeria [16,19,28,29,36,41,46,50-53,55,64,66, M. agrestis, M. oeconomus, Apodemus sylvaticus, A. flavi- 67,69,71,72,100,103,115-120]. Birds (Apteryx australis, collis, Peromyscus maniculatus, C. cricetus, Eliomys Alectura lathami, Trichoglossus chlorolepidotus, other quercinus, Pipistrellus pipistrellus), with occasional skin Psittaciformes, Passer domesticus, P. montanus, Garrulus lesions in Clethrionomys and Microtus voles, in England, glandarius), their nests (Turdus merula, T. philomelos, France, Canada, Yugoslavia, Austria, Italy, Czechland and Carduelis cannabina) and pellets (Corvus frugilegus) in Slovakia [12,20,60,67,68,72-74,104,116,117,122-129]. England, Australia, Czechland and New Zealand Birds (Acrocephalus scirpaceus, A. schoenobaenus) in [14,15,30,31,63,106]. Czechland [25]. Arthroderma insingulare Padhye et Carmichael Coll. UAMH 2557: fork-tailed kite, Australia Anam. Trichophyton terrestre Durie et Frey (often (R. G. Rees H427). red-pigmented strains). See also Arthroderma quadrifi- Arthroderma quadrifidum Dawson et Gentles dum. Anam. Trichophyton terrestre Durie et Frey. Syn. Ref. Birds (Aythya fuligula, A. apus, Hirundo rus- T. thuringiense Koch. Red-pigmented isolates of T. terres- tica, R. riparia, Phylloscopus collybita, Locustella lusci- tre might be mildly pathogenic for small mammals [56]. nioides, Acrocephalus arundinaceus, A. schoenobaenus, Ref. Mammals (Erinaceus europaeus, Sorex ara- S. serinus, Passer domesticus), Czechland [25]. neus, S. alpinus, Neomys fodiens, N. anomalus, Crocidura Coll. UAMH 3431: rodent, Czechland, 1967 suaveolens, C. leucodon, C. russula, Talpa europaea, (M. Otcenasek, ‘T. terrestre - red’) = CDC X-751. Ondatra zibethicus, Clethrionomys glareolus, Microtus Arthroderma lenticularum Pore, Tsao et Plunkett arvalis, M. agrestis, M. subterraneus, M. pennsylvanicus, Anam. Trichophyton terrestre Durie et Frey. See M. ochrogaster, Apodemus flavicollis, A. sylvaticus, also A. quadrifidum. A. agrarius, Peromyscus maniculatus, P. polionotus, Ref. Small mammals (Neomys anomalus, Onychomys leucogaster, Dipodomys ordii, Erethizon dor- Crocidura suaveolens, Apodemus flavicollis) in satum, Micromys minutus, Mus musculus, Rattus norvegi- Yugoslavia and Czechland [12]. Birds (A. apus, cus, R. rattus, R. assimilis, Sciurus niger, Lepus Acrocephalus arundinaceus, A. scirpaceus, A. schoeno- europaeus, L. americanus, O. cuniculus, Capreolus baenus, Sylvia curruca, Phylloscopus collybita, Lanius capreolus, Cervus elaphus, D. dama, Odocoileus virginia- collurio, Parus major, P. caeruleus, Passer domesticus, nus, O. hemionus, Antilocapra americana, Canis latrans, P. montanus, Emberiza citrinella), Czechland and Vulpes fulva, V. vulpes, Mustela vison, Taxidea taxus, Yugoslavia [14,15,25}. M. meles, P. putorius, Trichosurus vulpecula) in New Arthroderma melis Krivanec, Janeckova et Zealand, Great Britain, Czechland, Romania, Russia, Otcenasek. Germany, Australia, USA, Italy, France, Slovakia, Anam. Trichophyton melis Krivanec, Janeckova et Yugoslavia, Denmark, Austria and Poland Otcenasek. [12,17,19,20,28,35,36,41,56,61,63,64,66-70,72,74,76,85, Ref. Burrows with nests of M. meles and V. vulpes, 100,103,108,115,119,130]. Birds (Anas platyrhynchos, Czechland [121]. A. acuta, A. strepera, A. querquedula, A. crecca, Arthroderma multifidum Dawson A. clypeata, Aythya ferina, A. nyroca, A. fuligula, Mergus Ref. Lagomorphs (Oryctolagus cuniculus hair and albellus, Falco tinnunculus, Fulica atra, C. coturnix, burrows) in Scotland and France [20,108], and rodent L. lagopus, Phasianus colchicus, Larus argentatus, Tyto nests in Slovakia [19]. Birds (Rallus aquaticus, Riparia alba, Merops apiaster, Columba livia, Dendrocopos riparia, Motacilla flava, Sylvia borin, Acrocephalus scir- major, R. riparia, Motacilla flava, M. citreola, Locustella paceus, A. schoenobaenus, Passer domesticus, P. monta- naevia, Acrocephalus scirpaceus, A. schoenobaenus, nus, Corvus monedula) and their nests (Delichon urbica, Phylloscopus collybita, Saxicola torquata, Turdus merula, R. riparia, P. montanus), Czechland and Yugoslavia T. philomelos, Erithacus rubecula, Luscinia megarhyn- [14,15,25,31]. Keratinolytic fungi in wild vertebrates Hubalek Z 97 chos, Phoenicurus ochruros, Lanius collurio, Aegithalos Syn. Oidiodendron kalrai Tewari et Macpherson. caudatus, Parus major, P. caeruleus, P. palustris, P. cya- Onychomycosis and skin lesions in humans sporadically. nus, Carduelis cannabina, C. carduelis, C. chloris, Coll. UAMH 4164, 4165: Setonyx brachyurus S. serinus, Passer domesticus, P. montanus, Sturnus vul- (wallaby) hair, W. Australia, 1978 (R. McAleer). garis, Corvus corone, C. monedula, C. frugilegus, P. pica, Auxarthron umbrinum (Boudier) Orr et Plunkett Emberiza citrinella), their nests (Ixobrychus minutus, Syn. Myxotrichum brunneum Rostrup, Auxarthron A. fuligula, P. colchicus, Hirundo rustica, R. riparia, brunneum (Rostrup) Orr et Kuehn. Sylvia atricapilla, P. collybita, T. philomelos, T. merula, Anam. Malbranchea albolutea Sigler et Prunella modularis, E. rubecula, L. collurio, P. major, Carmichael. P. palustris, Sitta europaea, Fringilla coelebs, C. chloris, Ref. Mammals (Erinaceus europaeus, Apodemus C. cannabina, P. domesticus, P. montanus, S. vulgaris, sylvaticus, Rattus rattus, R. norvegicus, Cricetomys gam- E. citrinella) and pellets (Falco tinnunculus, Asio otus) in bianus) in Denmark, Macedonia, Bosnia and Nigeria England, Czechland, Yugoslavia, Russia and France [12,17,29]. Birds (Phasianus colchicus, Passer domesti- [14,15,21-25,27,30-33,109,110,130]. cus) and their nests (R. riparia, Turdus merula) in Arthroderma simii Stockdale, Mackenzie et Czechland and Denmark [14,15,17]. Austwick Coll. UAMH 161, 162: Neotoma micropus (lungs), Anam. Trichophyton simii (Pinoy) Stockdale, Texas, 1949 (C. W. Emmons A4718 & A 4966). UAMH Mackenzie et Austwick. 1587: Thomomys burrow, California, 1961 (O. A. Plunkett Ringworm in primates including man, dog and 350). UAMH 4434: badger burrow soil, Queensland, 1981 fowls (India, Africa, Brazil). Relatively often in animal (L. Sigler). hair and poultry feathers but not yet reported from wild Auxarthron zuffianum (Morini) Orr et Kuehn birds. Syn. Gymnoascus zuffianus Morini. Ref. Mammals (Papio papio, Suncus murinus, Ref. Mammals (Thomomys burrow, Tatera indica, Tatera indica, R. rattus, Mus platythrix, Funambulus pal- Mus platythrix, Meriones hurrianae, Clethrionomys marum, Bandicota indica, Nesokia indica, Millardia mel- glareolus, Microtus arvalis, Apodemus flavicollis, A. syl- tada, Meriones hurriane) in Guinea and India vaticus, A. agrarius) in USA, India, Yugoslavia and [16,131,132]. Also reported from an asymptomatic Czechland [5,12,16]. Bird pellets (Merops apiaster), Microtus arvalis in E. Bohemia, Czechland but mating Yugoslavia [14,15]. studies of the isolate with A. simii were unsuccessful Chrysosporium evolceanui (Randhawa et Sandhu) [114]. Garg Arthroderma tuberculatum Kuehn Ref. Mammals (Neomys anomalus, Crocidura leu- Rare human infections have been described. codon, Apodemus flavicollis, A. sylvaticus, A. agrarius, Ref. Mammals (Rattus rattus, Dipodomys ordii, Glis glis, other rodents) in Australia, Germany, Melomys cervinipes, Isoodon macrourus, Macropus Yugoslavia and Czechland [12,26,36,103]. Birds (Turdus major, Pseudocheirus laniginosus) in Australia and USA merula, Passer domesticus, Sturnus vulgaris, Corvus [64,70,103]. Birds (Alectura lathami, Trichoglossus chlo- monedula) and their nests (Delichon urbica, Turdus philo- rolepidotus, other Psittaciformes, Dendrocopos major, melos, Carduelis chloris, C. monedula) in Czechland, A. apus, Hirundo rustica, R. riparia, Acrocephalus scirpa- Yugoslavia and India [14,15,25,34]. ceus, A. schoenobaenus, Phylloscopus collybita, Remiz Coll. UAMH 1361: Apodemus sp., England pendulinus, Turdus americanus, Paras major, Aegithalos (M. J. Marples E32). UAMH 2554: Tyto alba, caudatus, Passer domesticus, P. montanus, Sturnus vulga- Queensland, 1965 (R.G. Rees H201). UAMH 2555: ris, Emberiza citrinella), their nests (Tyto alba, Delichon Ocyphaps lophotes (crested pigeon), Queensland, 1965 urbica, R. riparia, Ficedula albicollis, P. phoenicurus, (R. G. Rees H440). UAMH 2556: Phalacrocorax, Parus palustris, Sturnus vulgaris, P. montanus) and owl Queensland, 1964 (R.G. Rees H239). UAMH 2770: rab- pellets in USA, Australia, Czechland, Yugoslavia, Russia bit, Alberta, 1967 (D. Remington). and India [14,15,23-25,32,34,37,106,133]. Chrysosporium lobatum Scharapov Arthroderma uncinatum Dawson et Gentles Coll. UAMH 4321: mouse hair, Rostov, Russia, Anam. Trichophyton (Keratinomyces) ajelloi 1969 (V. M. Sharapov VKM-F2120) = CBS 666.78. (Vanbreuseghem) Ajello. UAMH 3434: Passer domesticus feathers, Valtice, A typical geophilic dermatophyte, causing rare Czechland, 1970 (Z. Hubalek) = G. F. Orr O-3278 = CBS skin infections in mammals including man. 276.77. Ref. Mammals (Erinaceus europaeus, Talpa euro- Chrysosporium lucknowense Garg paea, Clethrionomys glareolus, Microtus arvalis, Ref. Rodents (Apodemus flavicollis, A. agrarius) in M. pennsylvanicus, M. subterraneus, Apodemus flavico- Yugoslavia and Czechland [12]. llis, A. sylvaticus, A. agrarius, Mus musculus, Rattus rat- Birds (Anas sp., Psittacula krameri, Phasianus col- tus, R. norvegicus, Sciurus vulgaris, Lepus eropaeus, chicus, Parus major, Passer domesticus) in Czechland Oryctolagus cuniculus, Trichosurus vulpecula, D. dama, and India [14,15,38]. B. bison) in New Zealand, Australia, Czechland, Scotland, Coll. CBS 251.72: feather, California, 1972 England, Slovakia, Germany, USA, Romania, France, (G.F. Orr). Yugoslavia, Italy and Poland [12,17,19,20,28,36,41, Chrysosporium mephiticum Sigler 60,63,64,67,69,72,76,98-100,103,105,108,115,124,134]. Coll. UAMH 791: feathers, California (G. F. Orr Birds (Phasianus colchicus, Passer domesticus), their O-564). UAMH 2559: Haliastur sphenurus, Queensland, nests (Delichon urbica, Muscicapa striata, Erithacus 1965 (R. G. Rees H428). rubecula, Prunella modularis, Turdus merula, T. philome- Chrysosporium tropicum Carmichael los, Carduelis chloris, C. cannabina, Passer montanus) in Teleom. Aphanoascus sp. [8]. England, Czechland, Yugoslavia and Japan [14,15,21, Ref. Mammals (Sorex araneus, Neomys anomalus, 30,31,135]. Crocidura suaveolens, Suncus murinus, Clethrionomys Arthrographis kalrae (Tewari et Macpherson) glareolus, Microtus arvalis, Apodemus flavicollis, A. syl- Sigler et Carmichael vaticus, A. agrarius, Mus musculus, M. platythrix, 98

Oryzomys sp. , Tatera indica, Rattus norvegicus, R. rattus, Microsporum ripariae Hubalek et Rush-Munro Funambulus palmarum, Bandicota indica, Nesokia indica, Teleom. Arthroderma sp. The species is related to, Millardia meltada, Cricetomys gambianus, Meriones but different from, Microsporum fulvum [97]. hurriane, Oryctolagus cuniculus) in Australia, Brazil, Ref. Feathers and nests of Riparia riparia in India, Yugoslavia, Czechland, Slovakia, Nigeria and Czechland [14,15,139]. France [12,16,19,20,29,95,103]. Birds (Anas platyrhyn- Monodictys levis (Wiltshire) Hughes chos, A. acuta, A. strepera, A. crecca, A querquedula, Ref. Falco tinnunculus pellets, England [27]. A. clypeata, Aythya ferina, A. fuligula, Mergus albellus, Myriodontium keratinophilum Samson et Fulica atra, Chlidonias nigra, C. coturnix, Phasianus col- Polonelli chicus, Columba livia, Athene noctua, Upupa epops, Coll. IMI 235783: Sorex araneus, England, 1979 Dendrocopos major, Motacilla flava, Locustella naevia, (A. Wright 528/78). UAMH 3435: Phasianus colchicus Acrocephalus schoenobaenus, Phylloscopus collybita, feathers, Valtice, Czechland, 1970 (Z. Hubalek) = Luscinia svecica, Turdus merula, Erithacus rubecula, G. F. Orr O-3297. Luscinia megarhynchos, Phoenicurus ochruros, Lanius Oncocladium flavum Wallroth collurio, Remiz pendulinus, Parus major, P. caeruleus, Syn. Actinodendron verticillatum (Smith) Orr et C. carduelis, C. cannabina, S. serinus, Passer domesticus, Kuehn, Gymnoascus verticillatus Smith. P. montanus, Sturnus vulgaris, Corvus corone, C. mone- Anam. Malbranchea flava Sigler et Carmichael. dula, C. splendens, P. pica, Emberiza schoeniclus), their Ref. Insectivores (Neomys anomalus) in Bosnia nests (Podiceps ruficollis, Ixobrychus minutus, Larus ridi- [12]. Birds (e.g., Falco berigora) in England and bundus, Streptopelia decaocto, Tyto alba, A. apus, Australia [13,106]. Ficedula albicollis, Acrocephalus scirpaceus, T. philome- Onygena equina (Wildenow) Persoon los, T. merula, P. major, P. ater, C. cannabina, C. chloris, Coll. DAOM 124593: owl pellet, Australia. Wat- Fringilla coelebs, P. montanus, S. vulgaris) and pellets 38: owl pellet, England (R. Watling). (Falco tinnunculus - as Aleurisma sp., Asio otus, Merops Onygena piligena (Schumacher) Fries apiaster) in England, Czechland, Yugoslavia, Russia and Syn. Onygena corvina Albertini et Schweinitz. India [14,15,23-25,27,31,32,34,37,38]. Ref. Rodents (Apodemus sylvaticus), Yugoslavia Ctenomyces serratus Eidam [12]. Pellets of birds of prey (Asio otus, other owl species, Ref. Mammals (Macropus major, Neomys anoma- Falco tinnunculus) in Czechland, Japan and England lus, Tatera indica, Mus platythrix, Meriones hurrianae, [27,140,141]. rodent nests) in Australia, Germany, India, Yugoslavia, Coll. 604: crow remains, Belgium. UAMH 3795: Czechland and Slovakia [16,12,19,28]. Birds (Anser bird remains = CBS 152. 73. DAOM 48905: feather, anser, Anas clypeata, P. perdix, Phasianus colchicus, British Columbia. MICH: mouse remains, Michigan Francolinus pondicerianus, Coturnix spp., Galloperdix (Smith). FH 7320: owl casting, USA (Thaxter). spadicea, Alectura lathami, V. vanellus, Merops apiaster, Shanorella spirotricha Benjamin Upupa epops, Acrocephalus scirpaceus, Turdus merula, Ref. Birds (a crow, and Monarcha trivirgatus), Carduelis cannabina, C. spinus, S. serinus, Passer domes- USA and Australia [13,106]. ticus, Sturnus vulgaris, Corvus monedula), their nests Coll. UAMH 3116: owl pellet, Utah, 1963 (P. puffinus, Anas platyrhynchos, Aythya ferina, P. colchi- (R. K. Benjamin RSA 1424). RSA 1517: owl pellet, cus, Larus ridibundus, Columba livia, Delichon urbica, California [9]. T. philomelos, T. merula, C. carduelis, C. chloris, C. can- Trichophyton phaseoliforme Borelli et Feo nabina, S. serinus, Fringilla coelebs, P. domesticus, Ref. Rodents (Proechimys cayennensis, Heteromys P. montanus, C. monedula) and pellets (Asio otus, anomalus, Rattus rattus) in Venezuela [142]. M. apiaster) in England, Czechland, Yugoslavia, India Trichophyton verrucosum Bodin and Australia [13-15,21,23-25,30,37,67,106,109,110,136]. Only sporadic records of this important zoophilic Malbranchea arcuata Sigler et Carmichael dermatophyte are known in wild mammals but virtually Ref. Rodents (Apodemus flavicollis, A. sylvaticus) never in birds. Sparrows (Passer spp.) have been suspec- in Macedonia and Bosnia [12]. ted to carry the fungus from farm to farm. Coll. UAMH 3844, 3845: Merops apiaster pellets Ref. Mammals (Odocoileus hemionus, Talpa euro- in a nest, Pesirevo, S. R. Macedonia, 1968 (Z. Hubalek paea - lesions, M. musculus - lesions, Apodemus sylvati- 232B & 236A). UAMH 3842: Corvus monedula feathers, cus) in USA, Germany, Czechland, Australia and Poland S. R. Macedonia, 1968 (Z. Hubalek 153A). [75,76,119,143,144]. Malbranchea fulva Sigler et Carmichael Uncinocarpus reesii Sigler et Orr References: Passer domesticus, India [34]. Anam. Malbranchea sp. Malbranchea pulchella Saccardo et Penzig Ref. Rodents (Rattus rattus), Australia [103]. Birds Ref. Rodents (Apodemus flavicollis) in Yugoslavia (Streptopelia decaocto, Parus major, Passer domesticus, [12]. Birds (Passer domesticus), their nests (Sturnus vul- Corvus monedula, P. pica) and their nests (Columba livia, garis) and pellets (Corvus frugilegus) in Czechland and Delichon urbica, Carduelis cannabina, C. monedula) in India [14,15,34,37]. Yugoslavia and Czechland, as Auxarthron sp. [14,15]. Microsporum gallinae (Megnin) Grigorakis Coll. UAMH 4689: Hirundo rustica nest, Russia Syn. Trichophyton gallinae (Megnin) Silva et (V. M. Sharapov) = CBS 668.78. Benham. Uncinocarpus uncinatus (Eidam) Currah Teleom. Arthroderma sp. Very closely related or Syn. Myxotrichum (Gymnoascus) uncinatum identical is Arthroderma grubyi [97]. (Eidam) Schroeter. A zoophilic dermatophyte causing favus in poultry, Coll. RSA 425: owl pellet, California [9]. but only rarely reported in wild birds, primates including man, domestic mammals and not at all in wild mammals. Ref. Favus in four wild P. perdix, Germany [137], and in a Lyrurus tetrix, Finland [138]. Keratinolytic fungi in wild vertebrates Hubalek Z 99

Ecological aspects of the association of Mammals vs. birds Rees [103,106] compared the frequency of occu- keratinophilic fungi with wild rrence of keratinophilic fungi between wild mammals and vertebrates birds in Australia. Mammals were more often contamina- ted (21%) than birds (4%). However, only a few species Frequency of fungal species (A. cajetani, A. cuniculi, A. gypseum) were significantly The list presents a total of 52 species of KF. Table more common in mammals, while A. tuberculatum was 1 summarizes published reports of KF isolated from free- more frequent in birds, and C. serratus was especially living mammals, birds, and their nests or pellets. There is numerous in gallinaceous birds. Hubalek et al. [12] found a certain bias in the records since about 7,000 of the mam- that the proportion of KF isolated was the same between mals were examined selectively for the presence only of wild mammals and birds caught in Czechland and pathogenic dermatophytes (especially T. mentagrophytes), Yugoslavia, i. e., 18% of the total fungi. However, some and non-pathogenic KF isolates were discarded. It is the- genera (Auxarthron, Malbranchea, Uncinocarpus) and refore not surprising that A. benhamiae is (together with species (A. curreyi, C. evolceanui, C. tropicum, M. arcua- A. quadrifidum) the most frequent species reported. Other ta) were more frequent in mammals whereas other fungi KF species very often found in wild vertebrates include in birds (Aphanoascus, Ctenomyces, Microsporum). (in the decreasing order of frequency) A. curreyi, C. tropi- Table 1 gives some idea of the distribution of KF between cum, A. cajetani, A. uncinatum, C. serratus, A. ciferrii, wild mammals and birds. KF species more frequently A. gypseum + incurvatum (M. gypseum complex), A. kera- reported in mammals than in birds have been A. benha- tinophilus, A. fulvescens, A. terreus and A. tuberculatum. miae, A. borellii, A. cajetani, A. gypseum, A. otae, A. persicolor, A. simii, A. uncinatum, A. umbrinum, Table 1. Reported isolations of individual species of KF from wild mammals A. zuffianum, T. phaseoliforme and T. verrucosum. On the and birds ______other hand, KF species relatively more often reported in wild birds than in mammals have been A. fulvescens, Mammals Birds ______A. keratinophilus, A. reticulisporus, A. terreus, A. ciferrii, Hair Nests, Feathers Nests, A. curreyi, A. insingulare, A. lenticularum, A. tubercula- burrows pellets ______tum, C. evolceanui, C. lucknowense, C. tropicum, C. serratus, M. fulva, M. pulchella, M. gallinae, M. ripa- Total examined: 25,838 137 4,155 804 ______riae, O. piligena, S. spirotricha and U. reesii. Amauroascus albicans 6- 19 Aphanoascus durus 1- -- Host species A. fulvescens 43 1 49 139 A. keratinophilus 90 1 57 93 Pugh [30,109,110,136] and Pugh & Evans [21] A. reticulisporus 1-922 observed affinity of A. curreyi to blackbirds and other A. terreus 67 - 119 36 Turdus spp., and that of C. serratus to galliform species, Apinisia queenslandica 2- 4- Arthroderma benhamiae: especially to the partridge. Pugh & Evans [145] further T. m. mentagrophytes 1257 - 5 2 observed that feather fats of different bird species (black- T. m. quinckeanum >10 - - - T. m. erinacei 182 14 - - bird, pheasant, pigeon) influence in diverse ways (i.e. sti- Arthroderma borellii 8- -- mulate, inhibit, or do not affect) the growth of some KF in A. cajetani 299 4 39 4 A. ciferrii 67 - 106 97 vitro. For instance, A. curreyi was stimulated with feather A. cuniculi 53 13 33 11 fat obtained from blackbirds or pheasants but slightly A. curreyi 216 2 289 64 inhibited with that from pigeons; A. uncinatum was mar- A. flavescens -- 2- A. gloriae 1- -- kedly stimulated by pheasant, and inhibited by pigeon, A. grubyi 3- -- feather fat. However, Hubalek [14] isolated A. curreyi A. gypseum, incurvatum, fulvum (M. gypseum complex) 207 1 28 11 quite frequently not only from Turdidae but also from A. insingulare 1-18- birds of some other avian families, notably gulls and A. lenticularum 4-24- A. melis -2 -- wetland birds. T. m. erinacei and T. terrestre ‘red’ are A. multifidum 610149 species closely associated with hedgehog, in fact its ‘skin A. obtusum 1- -- residents’ [56]. Affinities of A. persicolor to C. glareolus A. otae 5- -- A. persicolor 472 2 3 - and of T. m. mentagrophytes to A. sylvaticus have been A. quadrifidum 981 3 259 231 repeatedly ascertained in Europe [20,72,73,124-126]. A. simii 99 - - - A. tuberculatum 10 - 136 45 A. keratinophilus, A. curreyi and A. cuniculi have occu- A. uncinatum 103 7 9 182 rred more often on C. glareolus than on A. sylvaticus [20]. Arthrographis kalrae 1- -- Auxarthron umbrinum 17 2 3 2 A significant association between A. simii and Tatera A. zuffianum 12 1 - 3 indica was observed in India [16]. Interestingly, M. ripa- Chrysosporium evolceanui 23 - 28 5 riae has only been isolated from sand martins, and not C. lobatum 1- 1- C. lucknowense 3- 8- from other avian species [14,15,139]. A. ciferrii was the C. mephiticum -- 2- dominant species in sparrows (Passer spp.), while A. ful- C. tropicum 142 1 322 60 Ctenomyces serratus 73 1 160 56 vescens, A. keratinophilus and C. tropicum were distribu- Malbranchea arcuata 4- 11 ted relatively equally among bird species [146]. However, M. fulva --11- M. pulchella 1-112 A. ciferrii was also recovered very often from feathers of Microsporum gallinae -- 5- rooks [32]. M. ripariae -- 32 Monodictys levis -- -2 Myriodontum keratinophilum 1- 1- Host population density Oncocladium flavum 1- 3- Morris & English [89] found a greater frequency of Onygena equina -- -2 O. piligena 2- 45 T. m. erinacei in hedgehogs in New Zealand (47%) than Shanorella spirotricha -- 22 in Great Britain (20%) and ascribed it to the higher popu- Trichophyton phaseoliforme 10 - - - T. verrucosum 6- -- lation density of hedgehog in New Zealand compared to Uncinocarpus reesii 1-136 that in U. K. U. uncinatus -- -1 ______100

Host age and sex open landscape [15]. Also Humpolickova & Otcenacek Morris & English [89] recovered T. m. erinacei [25] isolated KF less frequently from birds living in more often from male and adult hedgehogs than from woods than those occurring in other habitats in Czechland. female and juvenile animals. Mariat et al. [72] isolated A. persicolor and T. mentagrophytes more frequently from Contact with the soil male than female rodents. Humpolickova & Otcenasek Vertebrates with frequent contact with the soil [25] found KF more frequently in adult birds than in the generally harbour more KF than those without it juveniles, and in males more than in females. Sarangi & [32,34,37]. Most importantly, virtually no KF were detec- Ghosh [34] observed a higher frequency of A. terreus, ted in 313 bats (Chiroptera) examined [67,106]. A. fulves- A. reticulisporus and C. tropicum in male than in female cens, A. ciferrii, A. cuniculi, A. multifidum, house sparrows, and in young than in adults; only C. evol- A. quadrifidum, A. tuberculatum, C. evolceanui and ceanui was more frequent in adults than in juvenile birds. C. serratus were significantly more often recorded in birds with frequent (active) contact with the soil, whereas Feathers/hair vs. nests only A. curreyi predominated in birds without pronounced A few KF (A. curreyi, A. quadrifidum) occurred contact with the soil [15]. more frequently on feathers than in nests of birds whereas some other species (A. fulvescens, A. uncinatum) were Seasonal distribution more frequent in nests than in the plumage [15]. Table 1 The minimum occurrence of most fungi is gene- indicates A. fulvescens, A. keratinophilus, A. ciferrii, rally in summer, whereas the peaks are often observed in A. multifidum, A. quadrifidum, A. uncinatum and U. reesii autumn, and spring or winter in the temperate climatic as KF relatively more frequent in bird nests than on fea- zone. In India, most KF were isolated from house spa- thers. rrows during the monsoon period, while the minimum was detected in summer [34]. Pesterev & Stadukhin [77] reco- Geographic area vered T. m. mentagrophytes from small mammals more Certain differences in keratinophilic mycoflora of frequently in April and October than in other months. wild vertebrates have been found between certain areas Buchvald et al. [69] isolated A. quadrifidum and A. unci- [103,124]. For instance, A. simii occurs enzootically in natum from Microtus arvalis in Slovakia more frequently restricted areas of India [16]. Chabasse et al. [20] obser- in September than in May. A similar result was obtained ved a different frequency of KF on small mammals within [20] with A. quadrifidum on rabbit in France. Otcenasek three geographic areas in France. Climatic and mesocli- (pers. comm.) found a peak of the occurrence of kerati- matic conditions (e.g., coastal vs. continental areas) may nophilic fungi (mainly A. quadrifidum) on small mammals play a role [34]. in autumn (October-November) and a minimum in summer in S. Moravia; the same situation was found in birds’ Habitat nests [147]. Arthroderma spp. (A. ciferrii, A. quadrifidum, Many mycologists observed different frequencies A. tuberculatum) were most frequent in house sparrows in of KF on wild vertebrates in various habitats [124]. winter and spring, whereas Aphanoascus fulvescens see- Water vs. terrestrial habitats med to prevail in late summer and winter, and C. tropicum A. keratinophilus, A. cajetani, A. ciferrii, A. cuni- and C. serratus in summer [23]. In the nests of tree spa- culi, A. multifidum, A. quadrifidum, A. tuberculatum, rrows, the summer and winter peaks were also observed A. uncinatum, Auxarthron spp., C. evolceanui, C. tropi- for A. fulvescens, and spring and/or autumn peak for cum, C. serratus and M. ripariae were isolated more fre- A. keratinophilus, A. quadrifidum, A. tuberculatum, quently from terrestrial birds than from waterbirds. On the A. ciferrii, C. serratus, A. curreyi, A. terreus and C. tropi- other hand, A. fulvescens and A. terreus were more fre- cum [147]. quent in waterbirds than in terrestrial birds [14,15]. Humidity Urban, rural and exoanthropic habitats Pugh & Evans [21] isolated most KF from avian No significant differences in KF on small mam- nests with a water content below 20%, but Hubalek et al. mals were detected between urban and rural habitats in [146], Hubalek [24,151] and Hubalek & Balat [147] Germany [28]. On the other hand, Morris & English [89] recorded KF more often in nests with >15% of water, and recovered T. m. erinacei more often from hedgehogs in markedly hygrophilic (hygrotolerant) spp. were A. kerati- urban (17%) than in rural (9%) habitats, and as many as nophilus, A. fulvescens and A. terreus. Covered avian 47% of hedgehogs were infected in Bushy Park, London. nests (i.e. those in hollows, nests boxes, buildings) Also Pesterev & Stadukhin [77] isolated T. m. menta- obviously provide better conditions for KF than open grophytes significantly more frequently from small mam- nests [31]. A. keratinophilus, A. cajetani, A. ciferrii, mals in man-inhabited areas than in exoanthropic habitats. A. cuniculi, A. multifidum, A. quadrifidum, A. tubercula- Hubalek [15] recovered A. quadrifidum, C. tropicum and tum, C. evolceanui, C. tropicum, C. serratus and M. ripa- C. serratus more frequently in synanthropic birds whereas riae all prevailed in birds nesting in hollows or in A. terreus prevailed in exoanthropic ones. Sharapov & well-covered nests lined mainly with keratinous material Kuzmina [32] isolated more KF from birds living in intra- whereas only A. terreus and A. curreyi were more fre- villan habitats than from those in woodland and moorland. quent in birds breeding in open nests [14,15,107]. Also KF have been more often recovered from synanthropic Humpolickova & Otcenasek [25] found that the nests in mammals and birds than from exoanthropic animals holes harbour KF more frequently than those on the [32,37,77,103,106]. In Italy, M. canis was isolated from ground and on trees. synanthropic rodents but not from exoanthropic animals [67]. Acidity The influence of pH on the distribution of KF in Woodland vs. openland habitats birds’ nests was ascertained by Pugh [30] and Pugh & A. curreyi was significantly more frequent in forest Evans [21] who found A. uncinatum and C. serratus to be birds whereas A. tuberculatum prevailed in the birds of an acidophilic (acidotolerant) and an alkalophilic (alkalo- Keratinolytic fungi in wild vertebrates Hubalek Z 101 tolerant) species, respectively, while A. quadrifidum pre- brates. The host and/or substrate preference has allowed a ferred neutral to alkaline conditions. A. keratinophilus and simple classification of the pathogenic KF (dermatophy- A. fulvescens are alkalotolerant, they occur significantly tes) into three ecological groups: anthropophilic, zoophi- more often in bird nests under neutral or alkaline condi- lic, and geophilic species [149]. A more detailed tions with pH>6.5, whereas A. uncinatum and A. curreyi ecological classification of the dermatophytes has been are acidophilic (acidotolerant) species [146-148]. A. unci- suggested [150]. The virulence of keratinolytic fungal pa- natum only occurs infrequently in bird nests and even less thogens, associated with wild mammals and birds, varies so on birds and mammals in contrast to the soil; on the widely from opportunistic agents causing dermatomycosis other hand, it is very common in arable and acid soils (skin, hair or nail disease) only rarely (e.g., T. ajelloi, [31,106,145]. The pH value of feathers fluctuated between A. tuberculatum, M. cookei, A. fulvescens) to those more 4.4 and 6.8 (mean 5.7) in house sparrow during the year; virulent (e.g., M. gypseum) and up to obligate pathogens in the breeding season, the range was 6.1 to 6.8 [23]; Pugh (e.g., T. mentagrophytes, T. verrucosum, M. gallinae). [30] recorded pH 5.5-7.3 (range) and 6.5 (mean) of feat- Zoophilic (and geophilic) dermatophytes associa- hers from various birds. There are no data about pH ted with wild vertebrates (and their prevalent wild or stray values of the hair of wild mammals. hosts in parentheses) are T. mentagrophytes var. mentagrophytes (rodent), T. m. var. quinckeanum (mouse), T. m. Substrate var. erinacei (hedgehog), T. verrucosum, T. simii (mon- The composition (keratin, plant material, etc.) of key, fowl), M. canis (cat, dog), M. gypseum (rodent), birds’ nests was found to be an important factor in the dis- M. persicolor (vole), M. gallinae (fowl). Human ring- tribution of KF [146,147], as well as the breeding stage, worm is contractable from wild rodents (T. m. menta- i.e., the presence of eggs, young or abandoning the nest grophytes and var. quinckeanum, M. persicolor), after fledging. For instance, A. keratinophilus occurs more hedgehog (T. m. var. erinacei), stray cats or dogs frequently in deserted and older nests than in those inhabi- (M. canis, M. persicolor) and monkeys (T. simii). ted by birds, and C. serratus has a higher affinity to feat- It is important that pathogenic but also saprophytic hers than to hair in the nest lining [146]. KF may be carried on birds’ feathers or mammals’ fur over long distances. For instance, A. fulvescens, A. tuberculatum and M. ripariae were isolated from the plumage Pathogenic keratinophilic fungi in wild of a number of migratory birds [14,15]. This is significant homoiothermous vertebrates not only epizootiologically, but also evolutionary, for genetic mixing of fungal populations in diverse parts of A majority of species of the ecological group of the world. keratin decomposing fungi are true saprophytes but some species are potentially pathogenic for homoiotherm verte-

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