Boletín Micológico Vol. 11 (1-2) : 41-50 1996

COPROPHILOUS FUNGI FROM CONFINED DEERS IN PAVIA (LOMBARDIA, ITALY)

(Hongos coprófilos en ciervos confinados en Pavia (Lombardia, Italia)

Giuseppe Caretta* & Edoardo Piontelli** *Istituto di Micologia Medica, Universitá di Pavia Via S.Epifanio 14,

27100 Pavia (Italia). * * Universidad de Valparaiso, Escuela de Medicina, Cátedra de Micología Casilla 92 V, Valparaíso (Chile).

Key words: Coprophilous fungi, deer, Zygomyeetes, Aseomyeetes ,I/yphomyeetes. Palabras clave: Hongos coprófilos, ciervo, Zygomyeetes, Aseomyeetes, I/yphomyeetes.

SUMMARY

Eighteen samples of fresh dungs were collected in spring time in arder to eslablish the presence of copro­philousfungi in a grol/pof deersconfined ina private park located near Pavia (Lombardia, Italy). A total of 40 genera and 5 7 species distributed in: 65 Zygomyeetes, 56 Aseomyeetes, 100 H.. .. phomyeetes and 2 Basidiomyeetes (11 = 223) was detected.

Dominant species were: Mueor hiemalis, Gra­phium penicillioides, Fusarium verticillioides, Mueor raeemosus, Saeeobolus versieolor, Chaetomium bostryehodes and Doratomyees eolumnaris.

It is also noted the diversity and density of some species in this kind of dungs and new records of some Aseomyeetes in this geographic area, such as: Aseodes­mis sphaerospora, Coprotus diseulus, Sphaerodes fimieola, Zopfiel/a leueotrieha, Kernia nitida and Thele-

bolus erustaeeus are also mentioned.

INTRODUCTION

Coprophilous fungi play several roles in soil and grassland ecosystem, specially in the decomposition and núneralizationofherbivore feces (Angel & Wicklow,1975). The quantification, distribution and the structure of coprophilous community are related to different physiolo­gical, ecological and biogeographical features which are closely linked to the kind and composition of the substra­tum as well as to the surrounding terrestrial habitat (Sinh & Webster, 1973 ; Safar & Cooke, 1988 a,b; Kuthubutheen & Webster, 1986)

The complexity of fecal-substrata is similar to soil sytems and exhibits a high degree.of spatial and temporary

RESUMEN

Con el fin de determinar la presencia de hongos coprófilos en un grupo de cien'os confinados en un parque privado en las cercanías de Pavia (Lombardía, Italia), se colectaron I8 muestras de excrementosfi·escos en un período primaveral.

Se detectaron un total de 40 génerosy 57 especies distribuidas en: 65 Zygomyeetes, 56 Aseomyeetes, 100 H..vphomyeetes y 2 Basidiomyeetes (n=223).

Las especies dominantes fueron Mueor hiemalis, Graphium penicillioides, Fusarium vertieillioides, Mu­eor raeemosus, Saeeobolus versieolor, Chaetomium hostryehodes y Doratomyees eolumnaris.

Se comenta la diversidad y densidad de algunas especies en este tipo de excrementos y se mencionan nuevos recod de algunos Aseomyeetes en ésta área geográfica, tales cOlllo:Aseodesmis sphaerospora, Coprotus diseulus, Sphaerodes fimieola, Zopfiella

leueotrieha, Kernia nitida y Thelebolus erustaeeus.

heterogeneity in biotic andabiotic components, thus making difficult to measure in situ (Miller, 1995). Moreover, changes in species composition during succession affect measurementoffungal diversity (Wicklow & Moore, 1974, Kuthubutheen & Webster, 1986).

Italian contributions to the occurrenceand distribu­tion of coprophilous fungi in animal dung remain scarse andlimited tocertaingroupofanimals. Data covering this country are still rare and referred to the mycota of rabbit dung from Piemonte(Vesco daletal ., 1967)and thefungal population colonizing the horse, goat and sheep dung in Lombardia (Caretta et al., 1994).

41

Coprophilollsfimgi in dllngfro/ll confined deers - G.Caretta & E.Piontelli

The present survey was therefore undertaken to acquire further taxonomic informations about the occur­rence and diversity of coprophilous fungi from Roe deer dung confined to a same kind 9ffood in a 3.000 m2 park located in thesuburbsofPavia (Lombardia). Anecological event which we considered interesting beca use of the unfrecuent association of this animals with a purely antropophilic habitat.

MATERIAL S AND METHODS

The dungs of 18 deers were collected in 1995 in the private park of S. Martino Siccomario a suburb ofPavia. Samples were collected in spring . These animals had been fed with hay, grass and cereal s, in particular maize, all year long.

Eighteen samples of fresh dung were singly col­lected in sterile containers in different park areas. Each sample wasdivided intothree subsamplesofapproximately equal size, and placed on moist blotting-paper in indivi­dual sterilePetri dishes.

Samples were incubated for 60 days at room te m­perature (19-22 oC) and daily exposed 10 natural Iight. Substratum moisture was maintained by periodic additions of sterile destilled water for up to 30 days.

Dung was inspected for fungal fructífications at regular intervals during this incubation periodo

Isolations were usually attempted in 2 media, PDA and agar with decoction ofthe same deer feces . Moreover in most cases macroscopic and microscopic observations were carried out directIy in living material ofthe dung.

No attempt was made to count the total number of colonies of each species in a single Petri dish. Species occurring more than once over the three replica te dishes were counted as one occurrence. Portions of dung samples and slides of sorne fungal species are retainedat the Insti­tute of Medical Mycology of Pavia . . The microscopic preparation of fungi were mounted in cotton-blue and lactophenol or simply lactophenol.

RESULTS AND DISCUSSION

A total of 223 isolates representative of : 65 Zygomycetes, 56 Ascomycetes, 100 lIyphomycetes and two Basidiomycetes was obtained from 18 deer fecal samples. Fiftysix species belonging to 41 genera were recorded (Table. 1). The dominant species occurring over 50 % in 18 samples, were Chaetomium hostrychotles, Doratomyc;es columnaris, Fusarium .vertidllioides, Graphium penidllioides , Mucor hiemalis, M. racemo­sus and Saccoholus versicolor (Table. 1, Figure A).

42

Frequent species occurring between 30- 49 % were Botryotrichum piluliferllm, Piptocephalis lepidula, Scopulariopsis hrevicaulis, S. hrumptii, Sordaria fimi­cola and Penidllium spp. (Table. 1).

The rare species isolates only once (8%), represented several groups offungi mostIy cosmopolitan coprophilousAscomycetes(1O/18), which arecommon in differentkinds of feces collected from herbiverous animals such as : Ascoholus perplexans, Ascodesmis sphaeros­pora, Chaetomium glohosum,Ch.murorum,Ch.pilu­liferum, Coprotus discu/us, Podospora minig/utinans, Sphaerodes fimicola, Sporormiella minima, and Zopfiella leucotricha. (Table. 1). Their scarce propagules density in Petri dishes, may not reflecttheir occurrence in the habitat and this may be due to the kind of food ea ten by these animals (pellets), a slower time offructification, a cIear interspecific competition between the fecal micro­biota (bacteria and fungí), or to the conditions ofincubations (Wicklow&Moore, 1974; Safar&Cooke, 1988b).

The total number of species developing on these fe­ces was higher than in other study in the same geographical locality with different types of dung (Caretta et al, 1994)

Most ofthe fungal groups exhibited fructifications usually abollt the 5 (Zygomycetes) to 10-25 days (Asco­Deuteromycetes and Basidiomycetes). Later on (30-60 days), only a few of them (Asco and Deuteromycetes) appeared when the moisture of the substratum fell due to the fact that the Petri dishes were not added sterile water. Main taxa were sorne ; Penidllium spp., Coprotus discu­lus, Kernia nitida; Theleholus crustaceus, Doratomyces stemonitis and Scopulariopsis brevicaulis. However many ofthem made their appearance from 10 to 20 days. This coincides with the influence ofthe activity ofwater in the sllccession of coprophilóus fungi described by Kuthubutheen & Webster (1986).

The mucoraceous and H.vphomycetes species are common of herbivore excrements of most animals, and may also occur on other types of decaying organic matter.

The presence of sorne of these fungi in deer dung, can be probably attributed to their ability to colonize the maize stored, one of the ingredients in the food for deers.

M.hiemalis the most dominant fungi isolated, is common in di1Jerent herbivorous feces (Harper & Webster, 1964, Dal Yesco et al, 1967), usually appear after 3-5 days incubation with their parasites, specially Chaetocladium brefeldii and in our case with Piptocephalis /epidula . It is also oue of the most comni.on and representative soil fun­gi and its competi tive ability, especiaIly in agricultural soil, is dlle to the fact that they genninate and grow rapidly when stimulated by soluble nutrients, being even able to excIude Trichoderma harziallum from specific habitat (Wardle et al. , 1993). Y ét as Shearer (1995), sta tes it this situations is surprising beca use the M u corales are considet:ed r- selected ill1d poor coinpetitors. The scarse presence of T. harzia-

.¡:.. w

Table 1. Relative frecuency of total coprophilous fungi on fecal deer substrata

TAXA Number ofsamples 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18

Acremonium sp. + + Acremonium strictum W.Gams + Alternaria sp. + Ascobolus furfuraceus Pers & Hook + + A. perplexans Massee & Sal. + Ascodesmis sphaerospora Obrist + Aspergillus c/avatus Desmaz. + + + Botryotrichum piluliferum Sacc. & March + + + + + + Chaetocladium brefeldii v.Tiegh & Le Mond + + + + Chaetomium bostrychodes Zopf + + + + + + + + + + + Cglobosum Kunze + C murorum Corda + Cpiluliferum Daniels + Cladorrhinum foecundissimum Sacc.&March + + Coprinus sp. + + Coprotus disculus Kimbr.,Luck-Allen & Cain + Doratomyces columnaris Swart + + + + + + + + + + + D.stemonitis (Pers:Fr.) Morton & Smith + + + Fusarium verticillioides (Sacc.) Nirenb. + + + + + + + + + + + + + + F.solani (Mart.) Sacc. + + Fusarium sp. + + Gilmaniella humicola Barron + Gliocladium roseum Bainier + + Graphium penicillioides Corda + + + + + + + + + + + + + + + G.putredinis (Corda) Hughes + Iodophanus carneus (Pers.) Korf + + Kernia nUida (Sacc.) Nieuwl. + + Mortierella reticulata Y.Tiegh.& Le Mond + Mucor bainieri Mehrotra & Baijal + + + + + M hiemalis Wehmer + + + + + + + + + + + + + + + + + Mplumbeus Bonord + + + +

n

2 1 1 2 1 1 3 6 4 11 1 1 1 2 2 1 11 3 14 2 2 1 2 15 1 2 2 1 5 17 4

%

0,89 0,44 0,44 0,89 0,44 0,44 .

1,341

2,69 I

1,79 4;93 0,44 0,44 0,44 0,89 0,89 0,44 4,93 1,34 6,27 0,89 0,89 0,44 0,89 6,72 0,44 0,89 0,89 0,44 2,24 7,62 1,79

r . {5'

~ :,-

~ '" ':::,

~. s· §­~ ~ 9 '" " <:)

.s, ::s ~ ~ '" -. '"

a (¡

'" ª " P.<>

~ '" E:=:

t Table 1. (Continuation)

TAXA N umber of samples 1 2 3 4 5 6 7 8 9

M.racemosus Fresen. + + + + + + + + Oedocephalum glomerulosum (Buill.)Sacc. Penicillium spp. + + + + Phycomyces blakesleanus Burgeff Pilobolus kleinii V.Tieghem Piptocephalis lepidula (Marchal) Benjamin + + Podospora miniglutinans Mirza &Cain P.setosa (Wint.) Niessl. + Rhizopus stolonifer (Ehremb.:Fr.) Vuill . Sllccobolus citrinus Boudier &Torrend + + + S. versicolor (P.Karst.) P.Karst. + + + + + + + Scopulariopsis brevicaulis (Sacc.) Bain. + + + + S.brumptii Salvanet-Duval + + + Sepedonium hialinospinosum Matsushima + SOrllllriafimicola (Rob.)Cesati & De Notaris + + Sphllerodes fimicolll (Hans.) Cannon &,Hawksw. + Sporormiellll minima(Auersw) Ahmed & Cain Stilbellll erytrocephlllll (Ditmar) Lindau Syncephlllis cornu V.Tiegh.& Le Monn. + S.reflexll v.Tiegh. + Thamnidium elegans Link + Thelebolus crustllceus (Fuckel) Kimbr. Trichoderma hllrzillnum Rifai + + Trichurus spiralis Hasselbr. Volutella ciliatll Alb. & Schw. ex Fr. Zopfiella leucotrichll (Speg.) Malloch & Cain

-~- - -- . _- -

10 11 12 13 14 15 16 17 18

+ + + + + + + +

.+ + + + + +

+ + + + + +

+ + +

+ + + + + + + +

+ + + + + + +

+ + + + + +

+ + + +

+ +

+ + + + + +

+ + +

+

n

14 2 7 1 2 7 1 3 1 4 14 8 6 3 6 1 1 3 2 2 5 2 2 2 1 1

%

6,27 0,89 3,13 0,44 0,89 3,13 0,44 1,34 0,44 1,79 6,27 3,58 2,69 1,34 2,69 0,44 0,44 1,34 0,89 0,89 2,24 0,89 0,89 0,89 0,44 0,44 --

:;

ª' ~ ';-> ~ 8 .s, ~ "'-~ ~

Q \;'l «l ~ Ro M

~ ¡¡; E=::

Coprophilolls jimgi in dllng from conjined deers - G.Caretla & E.Piontelli

num, a species which is assumed to be not coprophilous can be explained by its appearance in the surrounding soil.

Dung is thusa mechanism for thedispersionofsome soil fungi, Iike F. verticillioides (=F. moniliforme) , one of the most prevalent field fungi occurring in a great variety of plant hosts. Their frequency in dung can be explained because itis oneofthe organisms associated with corn-based feeds and by the ability to adapt easily to this new ecological niche.

Fusarium verticillioides , anamorph of Gibberella moniliformis, was found on horse dung (PionteIli et al. , 1981) and on cow dung (Dominik & Majchrowicz, 1970). It has been suspected of being involved in human and animal diseases and has been shown to be toxic for a varie­tyof experimental animals. (Kriek et al. , 1981 a, b). The new groupof mycotoxins, calIed fumonisins, was characterized in 1988 by Bezuidenhout et al.

Doratomyces coLumnaris, has been isolated by Swart (1967) on dung pelIets of ha res colIected in the MelvilIe Koppies Nature Reserve in Johannesburg. The main characteristic features on which the specific epithet isbased, uponarethevery short synnema tapped by a smaIl almostflat head, from which the conidia arise in a column.

D. columnaris in our study was the species occur­ring with significantly higher frecuency. In a previous study, this species was found on horse dung colIected in the province of Pavia, Lombardia (Caretta et al. , 1994).

Among the synnematous fungi , Graphium peni­cillioides is another significant fungal species restricted to deer dung. Graphium species are commonly found on woody substrata or plantdebris andanimaldung. Theyare frequentIy found as anamorphs of Ascomycetes, Ophios­toma, PetrieLLa, Petriellidium. G. pellicillioides was reported byEIIis (1971), on woodofPopulus; thehostof this species is Zea.

Scopulariopsis species, anamorphs of Microascus, are commonly found on aH types of decaying organic materials; they are quite frequentIy isolated from soils.

The species most frequently found on animal dung (ping, monkey, camel, horse, goat, cow and sheep) was S. brevicaulis (Udagawa & Takada, 1971 ; Dominik & Majchrowicz 1970, PiontelIi et el. , 1981; CareUa et al. , 1994 ).It is a celIulol)1ic and proteolytic fungus associated sometime in hunlans onychomycosis, ulcerating granuloma and chronic granulomatous inflammation of tendon sheaths and muscJe (Emmons et al., 1977). S. brevicaulis has the ability to attack arsenic compounds with the production of volatile gas identified as trime-thylarsine (ChalIenger, 1954).

Among the Ascomycetes on deer dung only sorne species were predominant: C. bostrychodes, SaccoboLus versicoLor and S. citrinus.

Chaetomium bostrychodes was present in abundance in a relatively high number of deer dung. This

species has a cosmopolitan distribution with the principal substrata being dung, seeds, soil or animal hairs .

This fungus is able to decompose ceIlulose ( Vesco dal et al., 1967) and is of interest because of mycotoxin production.

Larvae of the sciarid fly LicoreLLa maLi avoided ascomata of Ch. bostrychodes that had growth on rabblt dung, but consumed the fmit bodies of other coexisting coprophilous fungi (Helsel & Wicklow, 1978). The presen­ce of larvae of L. mali in rabbit dung decreased the number of sporulating species ofcoprophilousfungi, and increased the relative abundance of Ch. bostrychodes (Wicklow & Yocom, 1982). For Wicklow (1979,1988), Ch. bostry­choides has effective mechanical and chemical defenses against fungus feeding arthropods; this fact is related to the toxicity of Chaetoinium metabolites as chaetomin, chaetocins, chaetoglobosins and other metabolites (Uda­gawa et al., 1979, Udagawa, 1984).

Saccobolus versicolor is the most variable species of the genus Saccobolus (Brummelen, 1967). Apart from the variation in the shape and stmcture ofthe fmit -bodies, there is a considerable variation in pigmentation of these, ones the size of the ascospores and the variation of the episporium. For Brummelen (1967), it is impossible to distinguish moreor lessconstant forms within the species.

With regard to other fungal taxa found on the deer dung, sorne are known only or prevalently from dung as OedoceplzaLum glomerulosum, Stilbella erytroce­plzala or Sy"ceplzalis cornu (Jeffries & Kirk, 1976), others are interesting speciesasMortierellareticulataandPhyco­myces blakesleanus. These rarely colIected fungi teII us Iittle about their habitat, but sometimes from these few findings, valuable ecological data can be extracted.

Another interesting species recorded on deer dWlg and native of Europe, was Z.leucotricha (= Tipterospora leucotricJza (Speg) Lundq.). OriginalIy this fungus was colIected by Spegazzini (1878) on roUen branches of Sambucus nigra from Conegliano, Venezia, Italy and named SON/aria leucotricJra. AII the synonyms species examined by Lundqvist (1969), were found on various herbaceous material and seeds. On dung this species was not known. A synopsis of the genus Zopfiella and generic delimitation of Zopfiella, Podospora and Tripterospora was proposed by Guarro et al. , 1991.

Many of coprophilous fungi found in the present study, were Iisted by various autIlOrsondeer dung and the feces of other animals (Lundqvist, 1972; Richardson, 1972; Parker, 1979; BelI, 1983).

BeIl & Mahoney (1995), have observed that the dung from domesticated animals that receive regular intestinal drenches to rid them of internal parasites, shows a disappointing lack of fungi growing on it.

Most fungi occurring on deer dung are anamorphs

45

Coprophi/olls fitngi in dllng ¡'-Olll confined deers - G.Caretta & E.Piontelli

of Ascom..vcota, particulary of genera belonging to the formerly so called"Discom..vcetes " and to the "Pyre­nom..vcetes", someof which arecoprophilous and typical components of the fungal succession on dung (Seifert et al., 1983).

Despite the complexity of the fungal population within alimentary canalon deer, the gross composition of the mycota of a particular animals is remarkably stable in

their eco tope and tends to be characteristic for these animals. The main differences in fungal composition from animal to animal is diflicult to be related to a specific cause, but it is mainly influenced to the kind of food, like grasses, forages and grains, the size of animal, the geographic locali­zation, and interspecific competitive interactions by COI11-pounds which inhibit or stil11ulate the growth of SOl11e fungi and other biotic and abiotic factors.

Figure A. Frequency (%) of dominant species isolated in deer dung

20

15

10

5

o

1.- JJfucor hiemalis 2.- Graplzium pellici/lioides 3.- Fusarium verticillioides 4.- Mucor racemoslls 5.- Saccohollls versicolor 6.- Cnaetomillm bostrychodes 7.- Doratomyces colll"maris

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46

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Coprophilolls jimgi in dllng fi'OIll conjined deers - G.Caretla & EPiontelli

Figures. 1. Thelebolus crustaceus, ascus and ascospores (Bar =50¡tm). 2. Ascodesmis sphaerospora, ascus and mature ascospores (Bar=20¡tm). 3. Piptocephalis lepidula, dichotomously branchedsporangiosphore andconidia (Bar=8¡tm). 4. Syncephalis cornu, terminal swelling merosporangia and conidia (Bar= 1 O¡tm). 5.Syncephalis rejlexa, merosporangia and conidia (Bar = IO¡tl1l). 6. Cladorrhinumfoecundissimum, conidiogenouscell andconidia(Bar=lO¡tl1l) . 7-8. Mortie­rella reticulata, sporangiophoresandconidia (Bar=20¡tm). 9. Sepedonium hialinospinosum, conidia (Bar=1O¡tm).10. Kernia nitida, ascomata and circinate hair (Bar= 50¡t). 11. Saccobolus citrinus, ascospore clusters (Bar=lO¡tm). 12. Saccobolus depauperatus, ascospore clusters (Bar =lO¡tm). 13. Ascobolus perplexans,ascospores with a loose episporium (Bar =lO¡tm). 14. Zopfiella leucotricha, bicellular ascospores and hialine hairs ofthe upper part ofthe ascomata (Bar =5¡tm). J5.Coprotus disculus, ascus and young ascospores (Bar =lO¡tm). 16. Sphaerodesfimicola, reticulate ascospores (Bar=lO¡tm).

47

Coprophilolls fimgi in dllng frOIll confined deers - G.Carella & E.Piontelli

48

Coprophilo/ls fimgi in d/lng FOIll conjined deers - G.Caretta & E.Piontelli

49

Coprophi/olls fimgi in dllng ji-OJ/l conlmed deers - G. Caretta & E. Piontelli

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50

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