Nat. Nat. His t. Res., Vo l. 6 No. 1: 9ー 14 ， March 2000

Occurrence of Ammonia Fungi on the Forest Ground After Decomposition of a Dog Carcass

Toshimitsu Fukiharul), Koichi Osaku2), Kiyoshi Iguchi 3) and Masahiko Asada 1)

llNatural llNatural History Museum and Institute, Chiba 955-2 955-2 Aoba-cho, Chuo-ku, Chiba 260-8682, ]apan 21 2-84ー 2 Higashi-hatsuishi, Nagar巴 yama-shi ， Chiba 270ー0114 ， ]apan 31 Hiraoka Environmental Science Laboratory 8-8 8-8 Hosoyama, Asao・ ku ， Kawasaki-shi, Kanagawa 215-0001 , ]apan

Abstract Abstract Hebeloma vinosophyllum and Hebeloma spoliatum (Basidiomycota, Agaricales), which belong belong to the ammonia fungi , occurred on the ground in the close vicinity of a decompos 巴 d carcass carcass of a dog Canis familiaris in a forest dominated by Quercus serrata, Musashi-murayama city, Tokyo , centraI ]apan. This is the third record of ammonia fungi occurring at the site of a decomposed dog carcass.

Key words: ammonia fungi, Canis familiaris, dog carcass, Hebeloma spoliatum, Hebeloma vinosophyllum, Mammalia, Quercus serrata.

1992) defined “ ammonia Sagara (1975, Materials and Methods fungi" fungi" as “ a chemoecological group of fungi, which sequentially develop reproductive The study site was located in a forest at structures structures exclusively or relatively luxuriｭ Noyama-kita-koen, Musashi-murayama city, antly, on the soil after a sudden addition of Tokyo, at 35 0 46' N lat., 139 0 23' E long., apｭ ammonia, some other nitrogenous materials, proximately 150 m above sea level, about 1 which react as bases by themselves or on km distance from Lake Sayama_ The mean decomposition, or alkalis." Under natural air temperature is 14.1 0 C and annual precipiｭ conditions, the ammonia fungi have been tation is 1,631 mm (at Tachikawa city about reported reported to appear where the dead body of an 5 km away) and this area belongs to Camelｭ such as a dog (Sagara, 1976, 1984), cat lietea japonicae zone (Okutomi et al., 1987). (Sagara, 1976, 1981), snake (Hilton, 1978), The vegetation is dominated by Quercus serｭ rabbit rabbit (Takayama and Sagara, 1981) and rata Murray and mixed with deciduous and kangaroo (Miller and Hilton, 1986) was deｭ ever-green hardwoods σlex macropoda Miq., composed on the forest ground. Experimenｭ Clethra barvinervis Sieb. et Zucc., Eurya japonｭ tally, the ammonia fungi appear by th 巴 ica Thunb., Styrax jaρonicαSieb. et Zucc.) and sudden addition of a sufficient amount of conifer (Chamaecyρaris obtusa (Sieb. et Zucc.) urea on the forest ground (Sagara, 1975). End l.). More than 50 species of ammonia fungi were Fungi collected were dried at 60oC, and listed listed from Japan (Sagara, 1975, 1992; Fukiｭ observed microscopically. Anatomicalobserｭ haru and Hongo, 1995). In Sep t. 1996, baｭ vations and measurements were made on sidiocarps sidiocarps were observed in the close vicinity the preparations mounted in a 5% aqueous of of a decomposed body of an animal in a forest solution of KOH. The bones of the animal in in Tokyo, central Japan. In this paper, we collected were dried at 60oC, and anatomical report report the results of careful examination of observations and measurements were made. these these fungi and the anima l. Specimens of fungi and animal examined are deposited deposited at the Natural History Museum and Institute, Chiba (CBM).

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Results Results and Discussion 1. Hebeloma vinosophyllum Hongo (Figs. (Figs. 1 A, 2) Two fungal species were successively obｭ served served from 12 Sep t. to 27 S 巴 p t. 1996 in close This fungus is identif�d as Hebelomα vmos­ proximity to the decomposed animal carcass ophyllum Hongo from the following diagnosｭ (Fig. (Fig. lA , B). These fungi were id 巴 ntifìed as tic characters of this species (Hongo, 1965): Hebeloma vinosophyllum Hongo and H. spoｭ the tricholomatoid basidiocarp (F ig . 2A), corｭ liatwη(F r.) Kars t. (Basidiomycota, Agaricaｭ tinate partial veil, medium-sized (9.5-1 1. 0 x les). les). H. viη osophyllum was f�st observed on 6.0-6.5μm) densely verrucose amygdaliform 12 12 Sep t. On 23 Sept., H. vinosophyllum (Figs. basidiospores (Fig. 2C), and purple-brown 1 A, 2) and H. spoliatum (Figs. 1 B, 3) were both basidiospore-mass colo r. observed. observed. On 27 Sep t. only H. spoliatum was In the early stage of the study of ammonia observed. observed. The animal was id 巴 ntifìed as Canis fungi, this species was confused with Alniｭ familiaris familiaris Linnaeus. Discussion and notes on cola lα ctariolens Cl駑en輟n et Hongo. These morphology ，巴 cology and distribution are two species resemble each other in having provid 巴 d for these two fungi and the animal the same macroscopic characters of basidio carp, the same purple-brown basidiosporeｭ mass color and the sam 巴 microscopic characｭ ters ters of basidiospore. In addition, A. lactariｭ olens olens shows the sam 巴 behavior as an amｭ monia fungus (Fukiharu & Hongo, 1995). However, H. vinosophyllum (Fig. 2B) had the the glutinous upper layer of the pileipellis which distinguishes Hebeloma from Alnicolα (Sing巴 r ， 1986) . Hebeloma vinosophyllum was described as a new species without any description of beｭ havior havior that suggested it to b巴 an ammoma fungus (Hongo, 1965). Lat巴 r ， Sagara (1973) reported reported that the habitat of this species was closely closely r巴 lated with the decomposed animal matter such as the carcass or excremen t. He named th 巴 species a “ proteophilous fungus" (Sagara, 1973) and later reclassif�d it as an ammonia fungus (Sagara, 1975) 丘 vinoso­ phyllum has b 巴 en reported to occur at the site of of a decomposed dead body of a dog (Sagara, 1976), cat (Sagara, 1976, 1995) or rabbit (Sagara, 1981). This is the second report of this this fungus at the site of a decomposed dog carcass. carcass. In In natural conditions, H. vinosoPhyllum had been reported from Kyoto and Nagaoka-kyo cities, Kyoto Pref. in a Castanopsis forest Fig. Fig. 1. Ammonia fungi occurring at the site (Sagara, 1976, 1981); from Ootsu city, Shiga of of a decomposed carcass of a dog famil Canis ｭ Pref. Pref. in a mixed forest of and iaris. iaris. After decomposition of the dog carcass Castanoρ sis Quercus, and from Pinus forest (Hongo, 1965); in in a Quercus serrata dominaled forest , Noyama. kita-koen, Musashi-murayama city, Tokyo, 23 from Fujian, China in an ever-green mix 巴 d forest forest of Castα nopsis and Quercus (Hongo et Sept., 1996. A, Hebeloma vinosoρhyllum (CBMｭ FB 17141); B, Hebeloma spoliatum (CBM-FB al. , 1996) . In addition, by application of urea 17142) . Arrows show the bones of a dog to the soiJ in the fìeld , this fungus has been carcass. carcass. Scale bars: 2 cm. reported from Oita, Tottori, Kyoto and Shiga

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A

C 一一一

Fig. Fig. 2. Hebeloma vinosoρ hyllum. A , basidiocarps; B, anticl in al sect ion of th 巴 pileal surfac 巴; C, basidiospores. basidiospores. (A , dried material; B, C, mounted in 5% KOH so lution; AーC ， CBM.FB 17060). Scal 巴 bars: bars: A, 2 cm; B, 150μm ; C, 5μm

Japan in Chamaeｭ Pref . in western Castanopsis, 2. Hebeloma spoliatum (Fr.) Karst. cyparis, Cr:タρ tomeria ， Pinus, Quercus and Pleioｭ (Figs. (Figs. 1B, 3) blastus blastus vegetations (Sagara, 1975). By the same m 巴 thod ， this fungus has been reported This species is identified as Heb eloma spoliｭ from eastern Japan, from Nishi-nasuno, Toｭ atum (F r.) Kars t. sensu Hongo (Imazeki and chigi chigi Pref. in a mixed forest of Pinus and Hongo, 1987) from the following diagnostic Quercus Quercus (Suzuki, 1992); from M t. Kiyosumi, char acters of this spec ies (Imazeki and Chiba Pref. in a mixed forest of Quercus, Hongo, 1987): the tricholomatoid basidiocarp Abies, Pinus and Tsuga (Suzuki, 1992) ; from (Fig. 3A), a long rooting stipe (Fig. 1B) someｭ Abukuma Mountains, Fukushima Pre f. in a times present, brown sticky pileus, an evaｭ mixed forest of Castanopsis, Quercus and n escent cortinate partial veil present at the Abies Abies (Fukiharu, unpublished data). Biogeｭ very young stage (Fig. 3B) but lacking later ographically, the pres ent case fills th e blank (Fig.3C), medium-si zed (8.5-10.5x5.0-5.5 area area of its distribution record in th e central μm) densely verrucose amygdaliform basidｭ part part of Japan. H. vinosophyllum is known to iospore s (Fig. 3D) and pale brown spore-mass be a biotrophic (ectomycorrhizal) fungus colo r. (Sagara, 1995) . The vegetation data from the H ebe loma sρoliatum has been reported from present present case suggests an ectomycorrhiza l Europe (Bresadola, 1927-1933; Lange, 1935 - relationship relationship of H. vinosophyllum with the 1940; Bruchet, 1970) and from North Ameriｭ dominant tree speci 巴 s Quercus serratα， ca (Smith, 1938, 1984), but behavior specific Specimensexamined. Specimensexamined. Japan, Honshu, Tokyo, to ammonia fungi has not been known . Musashi-murayama city, Noyama-kita-koen, Sagara (1973) 白 rst reported that this species 150 m a.s.l., 12 Sep t. 1996 (CBM-FB 17060), (丘中 oliatum sensu Hongo) was closely relatｭ 23 Sep t. 1996 (CBM-FB 17141) . ed with decomposed animal matter and clas-

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A

Fig.3. Fig.3. Hebeloma spoliatum . A, matured basidiocarps ; B, C, young basidiocarps with cortinate veil at a very early stage (B) but disappearing soon (C); D, basidiospores. (A, B, C , dried material ; D, mounted in in 5% KOH solution; A, C, D, CBM-FB 17143; B, CBM-FB 17142). Scale bars : A, 2 cm ; B, 2 mm ; C, 1 cm; cm; D, 5μm . sified sified this species as “ an ammonia fungus" Musashi-murayama city, Noyama-kita-koen, (Sagara, 1975). In natural conditions, H. spoｭ 150 m a.s.l., 23 Sep t. 1996 (CBM-FB 17142), liatum liatum has been reported to occur at the site 27 Sep t. 1996 (CBM-FB 17143, 17149). of of decomposed animal matter, such as feces 3. 3. Canis familiaris Linnaeus of of cow, pig, fowl and human (Sagara, 1978a, (Figs. (Figs. 1, 4) 1995), human excrement night soil (Sagara, 1995), abandoned ( fiaviceps This animal was identified as a mammal le ω isii Cameron) nest (Sagara, 1979; Sagara Canidae since the bones had the following et et al. , 1985), moles (Mogera imaizumii Kuroda diagnostic characters of this family (Evans and M ω ogura ωogura Temminck) midden and Christensen, 1979). The wings of the (Sagara, 1978b, 1980, 1995, 1998), the shrew first cervical vertebrate (atlas) project from mole (Urotrichus talρoides tα， lpoides Temmiｭ the lateral masses (Fig. 4a), the cranial border nck) nck) midden (Sagara et al., 1981) and of scapula is arciform (Fig. 4b) and the cerviｭ dog (Nyctereutes ρ rocyonoides viverrinus Temｭ cal tubercle of trochanter major of femur is minck) midden (Sagara, 1995), from Hiroｭ projected (Fig. 4c, d) . Considering from the shima, Hyogo, Kyoto, Aichi and Niigata Pref. whole bone size, the shoulder height of this in in ]apan in Quercus, Pinus, Fagus dominated animal is estimated to be ca . 80 cm . The forests. forests. Sagara (1977) reported the first case natural mammal Canidae habitants in this of of this fungus from the site of a decomposed area are Canis familiaris Linnaeus, Nyctereusｭ dog carcass in Kyoto in a Castanopsis dominｭ tes procyonoides viverrinus Temminck and ated ated forest, and this is the second case. H. Vulpes vulpes Linnaeus of which C. familiaris spoliatum spoliatum is known to be a biotrophic (ecｭ is the only animal that has the shoulder tomycorrhizal) tomycorrhizal) (Sagara, 1995). The vegetaｭ height of this anima l. tion tion data from the present case suggest an The occurrence of ammonia fungi at the ectomycorrhizal ectomycorrhizal relationship of H. spoliatum site of a decomposed dog carcass was first with dominant tree sp 巴 cies Quercus serrata. reported from Kyoto, ]apan with the appearｭ Specimensexamined. Specimensexamined. ]apan, Honshu, Tokyo, ance of H. vinosophyllum (Sagara, 1976) and

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Fig. Fig. 4. The bone of a dog Canis familiaバs (CBM-ZZ 2676). a, The f�st cervical vertebrate (arrow shows the wing part); b, scapula (arrow shows the cranial border); c, femur; d, trochanter major (arrow (arrow shows the cervical tub erc ule). Scale bar: 20 cm

H. H. spoliatum (Sagara, 1977) from the same anatomy of the dog, 2nd ed. 1181 pp. W. B. plac巴 The second case was of Hebeloma syriｭ Saund 巴 rs Company, Philadelphia . ence ence Karsten found by D. P. Lewis “ around Fukiharu, T . and T. Hongo. 1995 . Ammonia fungi well-decayed corpses of dogs" in Texas, of Iriomote Island in the southern Ryukyus, North America (Sagara, 1984) . Thus, this is ]apan and new ammonia fungus, Hebeloma lu the third case to be reported. chuense. Mycoscience 36 ・ 53-58. Specimen examined. Japan, Honshu, Tokyo, Hilton, R. N. 1978. The ghoul fungus, Hebeloma sp Musashi-murayama city, Noyama-kita-koen, ined. Trans. Myco l. Soc . ]apan 19 : 418. 150 m a.s.l., 23 Sep t. 1996 (CBM-ZZ 2676). Hongo, T. 1965. Notes on ]apanese l arger fungi (l 7). ]. ]pn . Bo t. 40 (10) : 311-318. Acknowledgments Hongo, T., N. Kinjho, N . Taketomo, N. L. Huang, ]. We express our sincere thanks to Prof . N. L. Wu and ]. T. Lin. 1996 . Agarica l es in everｭ Sagara of Kyoto Un iv. for critical reading of green oak forests in East-Asia. Nippon Kingakuｭ this this manuscript and also to M r. T. Komiya of kai Kaiho 37: 63-64. (I n ]apanese) Natural History Museum and Institute, Chiba Imazeki, R. and T. Hongo (eds.). 1987. Colored for for advice on the mammal bone identif� illustrations of mushrooms of ]apan. Vo l. 1. 325 cation . pp . Ho iku sha Publishing, Osaka. (I n ]apanese w i th Latin name s and index) References Lange, ]. E. 1935 -1940 . F l ora Agaricina Danica. 5 Bresadola,]. 1927-1933. Ic onographia Mycologia. vols. Soc. Advan. Myco J. Denmark and Danish 26 26 vols . Soci. Bo t. It al. Mus. Civico di Storia Nat Bo t. Soc., Cop巴 nhagen. di di Tren to, Milano. Miller, O. K. ]r. and R. N . Hilton. 1986 . New and Bruchet, G. 1970. Contribution a l'岳 tud e du genre in teresting agarics from Western Australia . H e beloma (F r.) Kummer; partie sp馗iale. Bul J. Sydowia 39: 126-1 37. Soc. Soc. Linn. de Lyon 39(6}: 1 ー 131 Okutomi, K., S. Okuda, S. Tsuji and Y . Hoshino Evans, H. E. and G. C. Christensen. 1979. Miller 's 1 987. Vegetation of Tokyo . 249 pp. Tokyo-to,

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Tokyo. (In ]apan 巴 se with English summary) deposited burrows of Urotrichus talpoides (shrew Sagara. Sagara. N. 1973. Proteophilous fungi and f�eplace mole). Trans. Myco l. Soc. ]apan 22: 441-455. fungi fungi (a pr巴 liminary report). Trans. Myco l. Soc. Sagara. N.. Y. Kitamoto. R. Nishio and S. Yoshimi. ]apan 14: 41-46. 1985. Association of two Hebeloma species with Trans. Trans. Br. Sagara. Sagara. N. 1975. Ammonia fungi-a chemoecolog 田 decomposed nests of vespine . ical ical grouping of terrestrial fung i. Cont r. Bio l. Myco l. Soc. 84(2): 349-352. Lab. Lab. Kyoto Univ. 24: 205-276. Singer. R. 1986. The Agaricales in modern taxonｭ Sagara. Sagara. N. 1976. Presence of a buried mammalian omy. 4th ed. 981 pp. Koeltz Scientif� Books. carcass carcass indicated by the fungal fruiting bodies. Koenigstein. Nature 262: 816. Smith. A. H. 1938. New and unusual agarics from Sagara. Sagara. N. 1977. The fungi from the animal matter North Am 巴 rica 1. Mycologia 38: 20-4 l. decomposed place such as mammalian carcass Smith. A.I- I. 1984. Studies of species of Hebeloma and human feces. Nonezumi 139: 19-2 l. (In ]apｭ (F r.) Kummer from the Great Lakes Region of anes 巴) North America l. Sydowia 37 ・ 271-283. Sagara. Sagara. N. 1978a. Habitats of Hebeloma spoliatum Suzuki. A. 1992. Physiological characteristics of Trans. Trans. Myco l. Soc. ]apan 19: 90. (l n ]apanese) the ammonia fungi and their role in bioscience

Sagara. Sagara. N. 1978b. The occurrence of fungi in asso・ In Proc. Asian Myco l. Symp. Seoul. Korea. pp. ciation ciation with wood mouse nests. Trans. Myco l. 238-247. Soc. Soc. ]apan 19: 201-214. Takayama. S. and N. Sagara. 198 1. The occurrence Sagara. Sagara. N. 1979. A fungus occurred from abanｭ of Hebeloma vinosophyllum on soil after decomｭ doned nests of Vespula flaviceps lewisii. Insectarｭ position of the corpse of domestic rabbi t. Trans. ium 16: 212-215. (In ]apanese) Myco l. Soc. ]apan 22: 475-477. (In ]apanese) Sagara. Sagara. N. 1980. Not mouse but mole. Trans. (Accepted 23 February 2000) Myco l. Soc. ]apan 21: 519. Sagara. Sagara. N. 198 1. Occurrence of Laccaria proxima in 犬の死体分解跡における the the grave site of a ca t. Trans. Myco l. Soc. ]apan アンモニア菌の発生 22: 22: 271-275.

Sagara. Sagara. N. 1984. On "Corpse f�der". M cI lvainea 吹春俊光 1) ・大作晃一 2) ・井口 潔 3) •

6(2): 6(2): 7-9 浅田正彦 1) Sagara. Sagara. N. 1992. Experimental disturbances and epigeous epigeous fungi. In G. C. Carroll and D. T. Wick 1) 千葉県立中央博物館 low (eds.). The Fungal Community. 2nd ed.. pp. 干 260-8682 千葉市中央区青葉町 955-2 427-454. 427-454. Marcel Dekk 巴 r. New York 2) 干 270ー0114 千葉県流山市東初石 2-84-2 Sagara. Sagara. N. 1995. Association of ectomycorrhizal 円lt 団法人平岡環境科学研究所 fungi fungi with decomposed animal wastes in forest 干 215-0001 神奈川県川崎市麻生区細山 8-8 habitats: habitats: a cl 巴 aning Can.].symbiosis? Bo t. 73 (Supp l. 1): 1423-1433. アンモニア菌に属するアカヒダワカフサタケとアシ Sagara. Sagara. N. 1998. Methods for studying the nesting ナガヌメリ(担子菌綱，ハラタケ目)が，東京都内の ecology ecology of moles through observation of mush コナラが優占する林内でイヌの死体分解跡に発生し room fruiting. Honyurui Kagaku 38(2): 271-292. た.これまで何積かの動物の死体分解跡からアンモニ (In (In ]apanese with English abstract) ア菌が発生することは知られており，イヌの死体跡か Sagara. Sagara. N.. S. Honda. E. Kuroyanagi and S. Takaｭ ら発生が確認されたのは今回が 3 例目である. yama. 198 1. The occurrence of Hebeloma spoliｭ atum and Hebeloma radicosum on the dung-

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