CRYPTOGAMIE

Mycologie

ANCIENNE REVUE DE MYCOLOGIE

Fondée par R. Heim en 1936

Directeur de la publication : Dr. Hélène Bischler-Causse

Rédaction : Dr. Bruno Dennetière

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BUREAU DE RÉDACTION

Écologie et Phytopathologie : G. Durrieu (Laboratoire Botanique et Forestier, 39 Allées Jules

Guesdes, F-31062 Toulouse Cedex) — Systématique : P. Joly (Laboratoire de Cryptogamie,

Muséum National d'Histoire Naturelle, 12 rue Buffon, F-75005 Paris) — Physiologie : G.

Manachére (Laboratoire de Mycologie, Université de Lyon 1, 43 bd du 11 Novembre 1918,

F-69622 Villeurbanne Cedex) — Cytologie : D. Zickler (Laboratoire de Génétique, Université

Paris Sud, Centre d'Orsay, Bât. 400, F-91405 Orsay) — Autres spécialités : M.F. Roquebert (Labo-

ratoire de Cryptogamie, Muséum National d'Histoire Naturelle, 12 rue Buffon, F-75005 Paris).

COMITÉ DE LECTURE

J. Boidin (Lyon), J. Chevaugeon (Orsay), J. Fayret (Toulouse), W. Gams (Baarn), G.L. Hennebert

(Louvain-la-Neuve), Ch. Montant (Toulouse), Cl. Moreau (Brest), D.N. Pegler (Kew), B. Sutton

(Kew), G. Turian (Genéve).

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TARIFS DES ABONNEMENTS Tome 17, 1996

CRYPTOGAMIE comprend trois sections : Algologie, Bryologie-Lichénologie, Mycologie.

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CRYPTOGAMIE, Mycologie est indexé par Biological Abstracts, Current Contents, Geo Abstracts,

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Illustration de couverture : Clavaria vermicularis Scop., dessin de R. Heim.

Source : MNHN, Paris

YPTOGAMIE

MYCOLOGIE

TOME 17 FASCICULE 34 1996

CONTENTS

ALTÉS A., MORENO G. & WRIGHT J. E. — New data on Tulostoma subsqua-

mosit (GASTETOMY CELLS) oce D ee. 230891 139

MANDEEL Q. A. — Survey of Fusarium species in an arid environment of

Bahrain. IV — Prevalence of Fusarium species in various soil groups

using severalisclation techniques а eta yee 149

JOB D. — Environmental growth requirements for submerged cultures of the

ectomyccorhizal fungus Cenococcum geophilum Fr..................... 165

GHERBAWY Y. A. M. H. — Keratinolytic and keratinophilic fungi of swamp’s

soil and air in Qena city and their response to garlic extract and onion

oitreatmenis. ecce e LE UT

Bibliography S ол, TO mM MN.

Bibliothèque Centrale Muséum

ШШШ.

3 3001 00226845 5

Source : ММНМ, Paris

NOTE DE LA RÉDACTION

Nous prions nos abonnées, nos lecteurs et les auteurs de bien vouloir nous

excuser pour les retards de publication qu’a subi CRYPTOGAMIE-MYCOLOGIE au

cours de l’année 1996.

En août de cette année, la rédaction a en effet été détruite lors d’un incendie au

Laboratoire de Cryptogamie du Muséum National d'Histoire Naturelle. Ce sinistre a

entrainé la destruction de notre fascicule 3 en préparation, ainsi que les manuscrits soumis,

l'ensemble de la correspondance et les bases de données.

Il est possible que certains auteurs ayant soumis leur manuscrit avant cette date

soient sans réponse de la rédaction. Nous leur suggérons dans ce cas de prendre contact le

plus rapidement possible.

La parution de CRYPTOGAMIE-M YCOLOGIE reprendra son rythme habi-

tuel dès le mois de mars 1997.

Vous renouvelant nos excuses les plus sincères, nous vous présentons nos

meilleurs vœux pour l’année 1997.

The editorial board request subscribers, readers and authors to accept their

sincere apologies for the publication delay endured in 1996 by the journal

CRYPTOGAMIE-MYCOLOGIE.

In fact, in this year august summer month, the editorial room was completely

destroyed by a fire that occurred at the Laboratoire de Cryptogamie, Muséum National

d'Histoire Naturelle. The sinister resulted in the complete deterioration of the fascicle

under preparation (vol. 17, no. 3), copies of submitted manuscripts, the journal archives

and important data bases.

Some authors have submitted manuscripts before this date. Few might have not

receive any reply relating to the fate of notes presented. These persons are urgently

requested to contact the managing editor as soon as possible.

The publication of CRYPTOGAMIE-MYCOLOGIE will resume its normal

course starting from march 1997.

The editorial board would appreciate interested persons do accept his most

sincere regrets and is pleased to present you his warmest greetings for the ongoing 1997

year.

Source : MNHN, Paris

Cryptogamie, Mycol. 1996, 17 (3-4) : 139-148 139

NEW DATA ON TULOSTOMA SUBSQUAMOSUM

(GASTEROMYCETES)

ALBERTO ALTES *, GABRIEL MORENO * & JORGE E. WRIGHT **

* Dpto. Biologia Vegetal, Universidad de Alcala, 28871 Alcala de Henares, Madrid, Spain.

** Dpto. Ciencias Biológicas, Facultad de Ciencias Exactas y Naturales,

Universidad de Buenos Aires, 1428 Buenos Aires, Argentina.

ABSTRACT — The presence of. Tulostoma subsquamosum has been confirmed in Spain and by

extension throughout Europe. Only a reduced number of records of this species were made in India,

Pakistan and Argentina. A macroscopic and microscopic study of Spanish collections was carried out

and compared with T. subsquamosum and T. melanocyclum holotypes. The most important features

are illustrated by microphotographs and scanning electron microscopy.

KEY WORDS: chorology, taxonomy, Tulostoma melanocyclum, T. subsquamosum.

Since Long & Ahmad (1947) first described Tulostoma subsquamosum Long &

S. Ahmad from material collected in India, very few references have been added for this

species. Wright (1987) considered it a critical taxon and gave two more records: the first

one from Pakistan (not far from the type locality) and the second from Argentina that

notably expanded its distribution area. Later, Calonge & Wright (1989) recorded its

presence in Spain with some doubts due to the great macroscopic similarity observed

between their material and 7: melanocyclum Bresadola. We have no further knowledge

about any additional record of T. subsquamosum. For this reason, it is believed that

material collected and studied by us during the last years in Spain, the macro- and

microscopic features of which fits fairly well with those of the 7: subsquamosum holotype,

are especially interesting. Thus, we can confirm the presence of this fungus in Spain (and

therefore in Europe), which not only extends notably its distribution area, but also

contributes to a better knowledge of this critical taxon.

MATERIALS AND METHODS

The collections studied are from the herbaria of the following institutions:

University of Alcalá de Henares, Madrid, Spain (AH); Real Jardín Botánico of Madrid.

Spain (MA-Fungi); University of Buenos Aires, Argentina (BAFC); Royal Botanic

Gardens, Kew, Surrey, England (K).

Source : MNHN, Paris

140 A. ALTES, G. MORENO & JE. WRIGHT

The colour of the gleba has been determined by comparison with the Natural

Colour Guide of Locquin (1975), with the corresponding code in parentheses. Photo-

graphs, both of light microscope (LM) and scanning electron microscope (SEM), were

made according to Moreno et al. (1995).

DESCRIPTION

Tulostoma subsquamosum Long & S.Ahmad, Farlowia 3:241, 1947.

Figs. 1-12,17-24

Material studied. SPAIN: Almeria: Sierra de Maria, 26-X11-1987, J.A.Oria de Rueda, MA-Fungi

20304. Cádiz: Grazalema, IV-1987, PThompson, MA-Fungi 20250 (as T. melanocyclum).

Madrid: Meco, 26-Х1-1989, A.Bernao, AH 13579. Navarra: Alsasua, 1-V-1973, E.Arrondo,

MA-Fungi 20290 (as T. melanocyclum) (doubtful). Toledo: km 41 ctra, Arganda-Mora de

Toledo, 28-IV-1986, C.Gómez, MA-Fungi 16316 (аз T. melanocyclum). Valencia: El Saler,

23-XI-1989, A,Burguete, AH 12449. Zaragoza: Bujaraloz, 4-X-1991, A.Altés et al, AH

13826 and 13827; ibidem, 17-11-1995, K.Kreisel er al., AH 18421; ibidem, 31-X-95, G.Mo-

reno & A.Altés, AH 19020, 19021, 19022, 19023, 19024 y 19025; Pina de Ebro, 9-XI1-1989,

J. Blasco, MA-Fungi 32137 (as T. melanocyclum). INDIA: Gurdaspur, Jaggatpur, УШ-1938,

S.Ahmad 258 (BAFC) HOLOTYPE. ARGENTINA: Chaco, Avia Teray, УП-1930, A.Cas-

tellanos, BAFC 29454 (ex ВА 1245)

Material studied of other species. ITALIA: “In glavrosis prope Tridentum", 1902, G.Bresadola, K,

HOLOTYPE of T. melanocyclum.

Spanish material of this species (16 collections) exhibits the following features:

Basidiocarps 15-49 mm long, more frequent length 20-40 mm. Spore-sac 7-12,5 mm diam,

globose to subglobose. Mouth tubular, more or less developed, normally small (0,3-1 mm

diam) when compared with the spore-sac size, peristome concolorous with the endoperi-

dium. Exoperidium seemingly granulose, more or less persistent, mixed with sand or soil

particles, even though it tends to form a thin membrane in contact with the endoperidium,

which in most basidiocarps persists as white patches. Endoperidium with numerous

remains of exoperidium, though in naked zones it appears smooth and dirty white to pale

ochre colored. Gleba ferrugineous (rubeus A3f). Stipe 10-43 x 1-4 mm, cylindrical, rather

straight, typically covered with dark brown scales, somewhat striate in the upper third,

with a slightly wider bulbous base and often covered with mycelial remains.

Basidiospores 4,5-6(-6,5) um diam, globose to subglobose, pale yellow, notably

verrucose. Under SEM a more or less dense net of irregular crests with reticulate to

subreticulate appearance can be observed (Figs. 17-21). Capillitium 3,5-11 рт diam, thick

walled, often with a continuous lumen, branched, pale yellow, very to not at all broadened

at the frequent septa which sometimes are ochraceous. Exoperidium formed by 4-8 um

diam, tortuose, thick-walled, branched, subhyaline to pale yellow hyphae, usually not

broadened at the colourless septa, mixed with other thin walled and very frequently

septate hyphae. The latter being easily disjointable and giving rise to cells with very diverse

shapes and sizes (Fig. 23), similar to the sphaerocysts of exoperidium of T. squamosum

Gmelin:Pers. (Moreno et al., 1992). Endoperidium formed by hyphae similar to those of

capillitium, 3-5 ит diam, compactly interwoven, thick walled, usually with a continuous

lumen, branched, subhyaline, more or less broadened (up to 9 um diam) at the usually pale

ochre septa.

Source : MNHN, Paris

NEW DATA ON TULOSTOMA SUBSQUAMOSUM 141

REMARKS

The holotype collection of 7: subsquamosum actually consists of spore sacs and

fragments of stipes belonging to three basidiocarps (Fig 1), although Long & Ahmad

(1947) cited four specimens in the mentioned collection. The features we can observe in

this material agree fairly well with the given description and show no differences when

compared with those of the Spanish material. The presence of sphaerocyst-like cells in the

exoperidium of the holotype is remarkable. This character had not been underlined until

now in this species, and also not observed in the other studied material. Accordingly, it

should be stressed that the presence of these sphaerocysts is not always simple to check

This difficulty may be due to the poor state of conservation of the exoperidium or to the

fact that specimens were collected a long time after their complete development: further-

more the great quantity of sand and soil particles mixed with the exoperidium are very

difficult to eliminate. Nevertheless, by choosing carefully the material it is possible to

observe these cells in the white patches remaining on the endoperidium. So far, little

attention was paid to the microscopy of the exoperidium and the endoperidium; however,

it appears to be an interesting character within a genus not exhibiting so much good

taxonomic features. This is the case in T. squamosum (Moreno et al., 1992) and T.

cyclophorum Lloyd (Wright, 1987; Moreno et al., 1990), as well as in T. subsquamosum. We

think it is necessary to pay more attention to these structures in any future taxonomic

studies on the genus Tulostoma.

Another especially important feature in this species is the spore ornamentation.

It consists of diversely sized and shaped crests, which form a more or less tangled usually

rather dense subreticule as shown by SEM (Figs. 2,3,17-22). Sometimes this net is looser

and reminds of the typical spore ornamentation of 7: fimbriatum Fr. However, confusion

between both species is to be excluded since the latter has a fibrillose-fimbriate mouth and

a clearly hyphal exoperidium. The sample MA-Fungi 20290 is the only one that shows a

different spore ornamentation, not subreticulate but consisting of short crests with more

or less conical spines. However, its other characters agree with T. subsquamosum, in

particular the presence of sphaerocysts in the exoperidium (Fig. 23). For this reason we

maintain this collection for the moment in 7; subsquamosum.

The presence of a stipe almost completely covered with dark brown scales, a

more or less developed tubular mouth, and a peristome concolorous with the endoperi-

dium, are other important data to characterize this taxon.

T. squamosum shares many of the indicated features and is very similar to 7:

subsquamosum. The latter also has a tubular mouth, a stipe covered with dark brown

scales, and spores notably ornamented under LM.

Therefore, it is not surprising that S. Ahmad had previously misinterpreted the

holotype of T. subsquamosum as T. squamosum, even less if we realize that its distribution

was at that time exclusively European. But later, when Long and S. Ahmad compared their

material with typical specimens of T. squamosum from Hungary and France, they did not

doubt that both species were different (Long & Ahmad, 1947). The basic differences

between both species are that T. squamosum has much larger scales on the stipe, an

exoperidium that tends to remain as circular patches over the endoperidium, and a

different spore ornamentation with conical spines formed by several apically fused ele-

ments. However, as mentioned before, 7: squamosum also has sphaerocysts in the exope-

ridium, and the spore ornamentation sometimes appears not so different from that of T.

subsquamosum under SEM. These data strengthen the relation of similarity between both

Source : MNHN, Paris

142 A. ALTÉS, G. MORENO & JE. WRIGHT

species. Even so, excepting a few problematic cases, we believe that it should not be too

difficult to distinguish both taxa.

In the specific case of Spain, and focusing on the material studied, T. subsqua-

mosum has been repeatedly mistaken for T. melanocyclum. However, examination of

holotype of the latter disclose enough differences between the two species. The macrosco-

pic aspects of 7: melanocyclum (Fig. 13) and T. brumale are almost identical, with gracile

habit, small sporal sac (usually not larger than 10 mm diam), tubular mouth (7: melano-

cyclum: Fig 14), reddish brown peristome, stipe with rather small scales, and mycelial

remains at the bulbous base, but 7: melanocyclum has a hyphal exoperidium and usually a

darker stipe than 7: brumale. SEM reveals the spore ornamentation consisting of conical

spines formed by several apical united elements (Figs. 15,16), a feature shared with 7:

squamosum, the capillitium slightly broadened at the septa, and the lack of sphaerocysts in

the exoperidium.

All Spanish samples so far referred to 7: melanocyclum have features not fitting

with the concept of this taxon and so have to be excluded from this species. This implies the

elimination of 7: melanocyclum from the Spanish Tulostoma catalogue, not discarding its

future incorporation, The revision of these samples, and others mentioned before,

confirms the presence of 7: subsquamosum in Spain and Europe, but also reveals its good

representation in this country. For the same reasons that 7; subsquamosum has been

confused with 7: melanocyclum in Spain we suspect that this also happened in other areas,

especially in Mediterranean countries. Thus it would be opportunate to restudy all the

material cited under 7: melanocyclum originating from that area.

Futhermore, examination of a specimen from Argentina allows us to confirm

the presence of 7: subsquamosum in the Southamerican subcontinent where so far only

one reference was known (Wright, 1987). Even though the features of this collection agree

with the given description, we must remark that the corresponding spores are slightly

smaller and that their ornamentation is not so prominent (Fig. 22). On the other hand, the

presence of sphaerocysts in its exoperidium is specially notable (Fig. 24).

ACKNOWLEDGMENTS

We wish to express our gratitude to the curators of the herbaria BAFC, K and

MA-Fungi for the loan of material used in this study. The collaboration of J.A.Perez and

A.Priego with the SEM has been fundamental. This project was partly supported by the

Programa de Cooperación con Iberoamérica, Ministerio de Educación y Ciencia, Spain.

REFERENCES

CALONGE ЕО. & WRIGHT J.E., 1989 — El género Tulostoma Pers.:Pers, (Gasteromycetes) en

España. Boletín de la sociedad micológica de Madrid 13: 119-137.

LOCQUIN M.V., 1975 — Natural Color Guide. Publ. by the author, Sens, France. 12 pl.

LONG W.H. & AHMAD S., 1947 — The genus Tylostoma in India. Farlowia 3: 225-267

MORENO G., ALTÉS A. & AYALA N., 1990 — Tulostoma cyclophorum Lloyd (Gasteromycetes,

Basidiomycotina) nuevo para España peninsular. Anales del instituto de biología de la

universidad nacional de México, serie botánica 60: 21-25.

Source - MNHN. Paris

NEW DATA ON TULOSTOMA SUBSQUAMOSUM 143

MORENO G., ALTÉS A., OCHOA C. & WRIGHT J.E., 1995 — Contribution to the study of the

Tulostomataceae in Baja California, Mexico. I. Mycologia 87: 96-120.

MORENO G., ALTES A. & WRIGHT J.E., 1992 — Tulostoma squamosum, T.verrucosum and

T.mussooriense are the same species. Mycotaxon 43: 61-68.

WRIGHT J.E., 1987 — The genus Tulostoma (Gasteromycetes). A world monograph. J.Cramer,

Berlin, Stuttgart, Germany. 338 pp., 50 pl.

Source : MNHN, Paris

144 A. ALTES, С. MORENO & ЈЕ. WRIGHT

FIGS. 1-3. — Tulostoma subsquamosum, S. Ahmad 258 (BAFC), holotype. 1. Basidiocarps showing

the tubular mouth. 2, 3. SEM micrographs of spore ornamentation. Scale bars: FIG. 1 =

5 mm, FIGS. 2, 3 = 1 um.

Source : MNHN. Paris

NEW DATA ON TULOSTOMA SUBSQUAMOSUM 145

ЈЕ 258 ли ДЕ

| ў

Tue бума Subay amesun dos

ез ы quate.

Aevi 1432

FIGS, 4-12. — Tulostoma subsquamosum, S. Ahmad 258 (BAFC), holotype. 4. Original label from

5. Ahmad herbarium. 5-7. Light micrographs of capillitium septa. 8-12. Groups of

sphaerocysts from the exoperidium. Scale bar = 10 um

Source : MNHN. Paris

146 A. ALTES, С. MORENO & JE. WRIGHT

FIGS. 13-16. — Tulostoma melanocyclum, K, holotype. 13. Basidiocarps. 14. Detail of a spore-sac

showing the tubular mouth and the dark peristome. 15, 16. SEM micrographs of spore

ornamentation. Scale bars: FIGS. 13, 14 = 5 mm, FIGS. 15, 16 = 1 um

Source : MNHN. Paris

NEW DATA ON TULOSTOMA SUBSQUAMOSUM 147

FIGS. 17-22. — Tulostoma subsquamosum, SEM micrographs of spore ornamentation. 17. AH

13826. 18. AH 13827. 19, AH 12449. 20. MA-Fungi 16316. 21. MA-Fungi 20304. 22.

BAFC 29454. Scale bars = 1 um.

Source : MNHN. Paris

148 A. ALTES, G. MORENO 4 ЈЕ. WRIGHT

FIGS. 23, 24. — Tulostoma subsquamosum, light micrographs of sphaerocysts from the exoperidium.

23. MA-Fungi 20290. 24. BAFC 29454. Scale bar = 10 um.

Source : MNHN, Paris

Cryptogamie, Mycol. 1996, 17 (3-4) : 149-163 149

SURVEY OF FUSARIUM SPECIES

IN AN ARID ENVIRONMENT OF BAHRAIN.

IV. PREVALENCE OF FUSARIUM SPECIES

IN VARIOUS SOIL GROUPS USING

SEVERAL ISOLATION TECHNIQUES

QAHER A. MANDEEL

Department of Biology, College of Science, University of Bahrain,

РО. Box 32038, Isa Town, State of Bahrain

ABSTRACT — Three isolation techniques, namely soil dilution, soil plating and soil baiting were

used to recover six Fusarium species from various soil groups in the arid environment of Bahrain. A

total of 428 isolates were recovered using the above techniques. Soil samples analyzed were generally

poor in organic matter, slightly alkaline, highly saline and low in total soluble salts. Maximum isolate

recovery and species spectrum were mainly recorded from soils of regosols, characterized by low

salinity levels (660 uS cm”). Of species encountered, Fusarium solani, Е equiseti and Е compactum

were dominant and frequent in all soil groups. Species prevalence, distribution and total isolate s were

greatly influenced by soil salinity, which counteracted other soil parameters. The soil dilution plate

yielded the highest population level and species diversity from regosol soils, Significant interaction

occurred between the applied technique and species recovery, as determined by chi-square analysis.

Results obtained are in favour of the use of multi-isolation techniques and media approach for

comparing survey studies of soil-borne Fusaria from noncultivated desert environment.

KEY WORDS — Arid environment, Fusarium, isolation techniques, soil group, survey.

INTRODUCTION

Bahrain is a small island nation in the Arabian Gulf consisting of an archipelago

of 33 islands; these are situated 25 Km off the eastern coast of the Saudia Arabian

Peninsula with а total area of about 695 Km? (Fig. 1). According to Doornkamp et al.

(1980), the main island of Bahrain can be divided into five major physiographic zones:

coastal lowlands, backslopes, escarpment, interior basin and central plateau and jebels.

Most soils are saline, calcareous, gypsiferous and coarse in texture, and as such are closely

related both geologically and climatologically to the Arabian Peninsula. Also as in other

arid environments, soils are generally of low fertility being poor in organic matter content

(<0.05-1.51%.) and nutrient level. The water-holding capacity is low and available mois-

ture about 2.6 %. Microbial tolerance to such an extreme ecosystem also characterized by

high temperatures is critical for their survival.

Source : MNHN, Paris

150 ОА. MANDEEL

The genus Fusarium is one of the most common member of soil-biotic micro-

flora (Burgess, 1981; Stoner, 1981). Geographic distribution of Fusaria in various ecolo-

gical zones are well documented (Burgess et al., 1988; Kommedhal et al., 1988; Marasas et

al., 1988; Jeschke et al., 1990; Burgess & Summerell, 1992; Sanglang et al., 1995). However,

the majority of surveys on Fusarium diversity have focused on cultivated soils and there

have been few studies on noncultivated ones (Booth, 1977). This situation gives the

impression the genus is rare in nature or ecologically unimportant in noncultivuted soils,

despite the fact that known Fusaria have been reported from all types of soils (Stoner,

1981).

Noncultivated soils and habitats of Fusaria include forests, scrub communities,

savannahs, prairies, pastures and other grasslands, deserts, swamps, littorial and coastal

zones. Mandeel er al. (1995) and Abbas & Mandeel (1995) recently reported on the

occurrence of Fusarium species in the arid deserts of Bahrain. Diversity and abundance

were correlated to soil factors such as organic matter and salinity (Moubasher & Al-Subai,

1987; Khodair et al., 1991) rather than with climatological conditions (Burgess ef al.,

1988). However, no information is available on the abundance and distribution of Fusaria

in soil groups of arid deserts. Data on population dynamics, species variability,

species inter-and intra-relationships and mechanisms of existence under extreme and

stressful environments could provide a better understanding on the native fungus ecosys-

tem.

The purpose of this study is to survey the abundance and distribution of Fusaria

in various noncultivated soil groups of Bahrain arid desert and compare the effect of three

isolation techniques on their recovery.

MATERIALS AND METHODS

Climate

Bahrain, like mainland Arabia, falls in the North African-Euroasian climate

province. The main island has a typical Saharo-Arabian climate, characterized by hot,

humid summers and mild winters with low annual rainfall. Average monthly rainfall and

temperature in the main island is illustrated in Fig 2. According to climate norms obtained

from the Civil Aviation Directorate (Bahrain, 1990 -1996), the mean annual temperature is

17.3° C, with a recorded June maximum of 47.5° C and a January minimum of 2.8? C.

Total annual rainfall range between 0 to 17 mm. The wettest month is January with up to

17 mm, while May to October is have very low rainfall of less than 0.05 mm.

Soils

According to Doornkamp et al. (1980) and Abbas & El Oglah (1992), soils of

Bahrain island are formed from Holocene and Pleistocene sedimentary rocks; they could

be divided into five major groups (Fig. 1):

(1) Cultivated solonchak: this group is located on the northern coastal lowlands extending

from Jurdab in the east, through the coastal area of Tubli Bay, Manama, Diraz, Sar,

Hamalah, to Dar Kulaib in the west. Soils are composed of loamy, sandy and clay

subgroups. Normally they are characterized by. having a high water table. They are usually

cultivated with the main crops being date palm and tomatoes.

Source : MNHN, Paris

|: ooh.

s Коњ

Cutvoted Solonchok

П nr

Regosols

lock dominoled oros

Row minerols

ИСТУ

Huwar

Islands:

BAHRAIN

v SUE

ARABIA

Figure 1. Location map of Bahrain representing the soil groups (extracted from Abbas & El-Oqlah,

1992) where collection of soil samples were made

Source : ММНМ, Paris

152 ОА. MANDEEL

(2) Natural solonchak: this group of soils is found between the interior of the northern

coastal lowlands and the base of the backslopes, extending from Sanad in the east,

through northern Aali, Karzakan and Хаад, to the Al-Mumatalah in the south-west.

Here soils contain gypsiferous solonchak and sabkha subgroups. Natural solonchak soils

are usually quartz-gypsiferous sands, salt pans and marine mudflats; they too are charac-

terized by having a high water table.

(3) Regosols: this group of soils is mainly an almost continuous strip in the coastal areas.

Itis also found between coastal lowlands and backslopes. Two sub-groups are recognized:

aeolian sands and recent beach deposits. They are mainly in the form of stable sands, dune

sands and beach sands.

(4) Raw mineral soils: raw mineral soils are found in the backslope zone, the escarpment,

and in the north-eastern part of the central basin. Three subgroups are recognized: soils of

the interior basin, soil detrital fans and stone pavement soils. These soils are usually loamy,

sandy or gravely.

(5) Rock dominant areas: these are restricted to the central part of the island. Such areas

constitute all the central plateau, some of the basin, the escarpment and some parts of the

northern and southern backslopes.

Soil sampling procedures and analysis

Soil samples were collected from five locations, namely As-Sehla, Zaalaq,

Duraz, Awali and Sakhir, adequately representing the five soil groups. All locations are

within the central and southern part of the main island (Fig. 1). Sampling sites and

physiographic zone, soil type, dominant plant communities and respective soil chemical

analysis data are listed in Tablel. Each soil group was sampled once during two winter

seasons: January 1995 and January 1996.

For each soil group, four composite soil samples, 2 Kg each, were collected, some

20-30 m apart. Each sample consisted of about 10 subsamples (200g), taken with a clean

hand-trowel, approximately 4 m apart and from the upper 15 cm of the soil profile.

Subsamples were combined, placed in paper bags, labeled, air-dried and stored at 5° С

until processed, within one week (Burgess & Summerell, 1992). Although samples were all

taken from all soil groups dominated by natural vegetation, care was taken to collect them

away from plant canopies or roots to avoid a rhizosphere effect.

For the assays, composite soil samples were thoroughly hand-mixed in plastic

bags under sterile conditions and divided in two parts. The first was stored at 5° C, the

second was used for chemical analyses. Soil pH and electrical conductivity (uS ст!) were

determined in a 1:5 soil:water extract using a JENWAY Water Analyser (Model PW1).

Organic matter content (%) was determined by ashing 100 g of air-dried soil in a furnace

at 600° C for 1 hr and estmiating difference in weight. Total soluble salts (TSS) were

measured by mixing 20 g with 100 ml distilled water, filtering and evaporating the filtrate

at 105° C. The dry residue was then weighed and the TSS calculated. Table 1 presents the

average values of three soil replicates,

Isolation

The second part of the sample was further air-dried, homogenized, crushed to a

fine powder when necessary and passed through a 0.5 mm soil screen to remove root

fragments and other debris (Kreutzer, 1972). Three techniques were used to isolate

Source - MNHN, Paris

153

OCCURENCE OF FUSARIUM SPP. IN BAHRAIN

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Source : ММНМ. Paris

154 Q.A. MANDEEL

—e-Temp. DRY РЕКЮО А МЕТ PERIODa

rainfall

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Figure 2. Average monthly rainfall and temperature in Bahrain

Fusarium species from these composite soil samples: soil dilution, direct soil plating and

the baiting technique on selective media.

In the dilution plate method, ten grams of soil are suspended in 90 ml sterile

distilled water and thoroughly mixed for 5 min. Soil suspension is allowed to settle for 30

sec and a | ml aliquot of the 1:10 dilution is then dispensed uniformly over the surface of

six replicate plates per selected medium. Preliminary studies indicated this dilution ratio

was the most suitable for samples taken from the various soil groups (15-20 Fusarium

colonies/plate).

The direct plating technique was modified from McMullen & Stack (1982). For

each composite sample 0.05 g was evenly distributed over the surface of a solidified

medium. This weight of soil gave similar numbers of Fusarium colonies per plate as before

(Kreutzer, 1972).

For the baiting technique, young stems and leaves of bean (Phaseolus vulgaris)

were removed, washed thoroughly in sterilized distilled water, damp dried and then cut

into | mm pieces. Plant parts were mixed whilst still moist and placed in glass Petri dishes

before being autoclaved at 120? C for 15 min; these were then air-dried for 4 hrs. A

previously sieved sample from each soil group was hand-mixed with the autoclaved plant

parts at a 10:1 ratio. Moisture content of the mixed sample was adjusted to 15 % (w/w) and

placed in 1 1 Erlenmeyer flasks. The latter were shaken trice weekly and incubated for 21

days at room temperature under continuous cool white lights. Mixed soil samples were

then air-dried and again sieved as previously described. Material retained on the 0.5 mm

soil screen was further washed Гог 20 min under tap water (Burgess et al., 1988). Washed

particles were then plotted dry for 48 hrs and 0.05g of dried material (for each composite

soil) was uniformly sprinkled over the surface of a selected media in six replicates. The

Source : MNHN, Paris

OCCURENCE OF FUSARIUM SPP. IN BAHRAIN 155

sieved soil of each soil group was treated using the dilution plate technique as previously

described.

Isolation plates were incubated at 22 + 2° C for 10 days under a 12 hr photope-

riod using cool white fluorescent lights (Burgess & Summerell, 1992). Developing colonies

on each medium that were putative Fusarium species were transferred individually to

standard 2% acidified potato dextrose agar medium (APDA) and incubated as described

above.

Media used for isolation

The following media were used: Oxoid commercial acidified potato dextrose

agar as a nutrient rich medium, Komada selective medium, Nash-Snyder or peptone

PCNB agar and selective Fusarium agar. All media were autoclaved (15 min at 120° C) and

allowed to cool to 45° C before addition of antibiotics, adjustment of pH or addition of

heat-labile ingredients. Fifteen ml of each medium were added to Petri dishes stored in the

refrigerator for at least five days before use.

For identification purposes three additional media were used: synthetic nutrient

agar, potato sucrose agar and 2% water agar.

Identification

Single spore or hyphal tip cultures of representative Fusarium species were

prepared and maintained on PDA under the incubating conditions described above for

seven days, Identifications were made according to Brayford (1993).

Data analyses

To quantify fungal abundance and distribution among soil groups and accor-

ding to the isolation technique, relative densities were determined. The relative density (70)

of a species is defined as the number of its isolates divided by the total number of Fusarium

isolates.

To estimate the recovery of Fusarium species according to the isolation techni-

ques from each soil type, percentage recoveries were determined. Percentage recovery is

defined as the number of Fusarium species recovered from each soil type, divided by the

total number of fungi recovered from the same type.

Chi-square tests were used to test homogeneity in contingency tables prepared

using frequencies of occurrence, measure the independence of species recovery by each

isolation technique among soil types.

RESULTS

Habitats sampling and soil analyses

Characteristics of the sampling sites and data from soil analyses are listed in

Table1. Samples collected mainly from the central-southern part of the main island Fig.1)

represent the five major soil group types. Sampling sites located in the physiographic zone

of coastal lowlands and the plant cover were mainly dominated by salt tolerant plants, e.g.

Zygophyllum qatarense and Heliotropium crispum (Abbas & El-Oglah, 1992).

Data extracted from the analyses of the several soil types proved to vary

Source - MNHN. Paris

156 Q.A. MANDEEL

considerably (Table 1). The highest pH value (8.5) was recorded in natural solonchak soil

and the lowest pH (7.7) in soils of cultivated solonchak and raw mineral ones. Electrical

conductivity (salinity) fluctuated greatly ranging from as low as 660 u S cm’! in regosols to

as high as 15930 uS cm’! in cultivated solonchak. The highest total soluble salts were

recorded in solonchak soils (6.7%), whereas the lowest was found in raw mineral and

rock-dominated areas (1.12%). Organic matter content varied from 18.34% in cultivated

solonchak to 1.04% in regosols. Texture of the collected soil samples proved to be

generally sandy to sandy loam and gravely.

Fusarium species prevalence and distribution

Six Fusarium species were isolated from the various soil groups. These are listed

according to their sections following Brayford (1993): Fusarium solani (Mart.) Sacc.

(sections Martiella and Ventricosum), Е sambucinum Fuckel (section Discolor), Е com-

pactum (Wollenw.) Gordon and Е equiseti (Corda) Sacc. sensu Gordon (section Gibbo-

sum), Е chlamydosporum Wollenw.& Reinking and Е sporotrichioides Sherb. (section

Arthrosporiella). The recovery of Fusarium species from soil groups considered using

different media selective for the genus and three different isolation techniques, are shown

in Tables 2 & 3. In general, highest species recovery was from samples from regosols (6

species), followed by natural solonchak (4 species), raw mineral and rock dominated ones

(3 species). No Fusarium was recovered from cultivated solonchak samples.

The highest average number of isolates was also obtained from regosols (122) as

compared to other soil groups. However the mean percentage recovery of Fusarium

Soil Group*

Fusarium spp. cs NS R RM RD RD%**

Е. solani 23 з 28.26

(1) (3) (1) 10.2

F. compactum 25 2 29.34

(23) 46.93

Е. sambucinum 8 8.7

F. equiseti 22 3 27.17

(19) 38.77

F. chlamydosporum 4 4.34

(2) 4.08

F. sporotrichioides 2 247

Total number of fungi 10 2 326 17 126

* Soil groups are :

RM-Raw Mineral Soils; RD-Rock Dominated Areas.

**Relative Density Values.

CS- Cultivated Solonchak; NS-Natural Solonchak; R-Regosols;

Table 2. Occurrence of Fusarium species in various soil groups during January 1995 and 1996, isolated

using the soil dilution plate method and direct soil plating. Soil plating values are shown between

parentheses.

Source : MNHN. Paris

OCCURENCE OF FUSARIUM SPP. IN BAHRAIN 157

species and respective isolates, in relation to the average total number of other fungi, was

highest in natural solonchak composite samples (85.71%), followed by raw minerals

(41.6%) and regosols (30.9%) while being lowest in soils of rock dominated area (8.27%).

The average relative density of Fusarium taxa among the several soil types ranged from

37.74 to 2.17% for Е solani and F. sporotrichioides, respectively (Tables 2 & 3).

Effect of the isolation technique on the recovery of Fusarium species

Three techniques were used to compare species recovery from treated soil groups

(Tables 2 & 3). A total of 428 Fusarium strains were recovered using the soil dilution, soil

baiting and direct soil plating techniques. Now recovery of Fusarium isolates proved to be

highest in the case of regosols using the dilution plate technique (84 isolates), followed by

the soil baiting technique (direct soil plating: 65 isolates). Also and except for raw mineral

soils, maximum isolate recovery was obtained by direct soil plating as compared to soil

dilution using the baiting technique (Table 3). But species diversity varied considerably

among soil groups and isolation techniques with some taxa not being recovered from

certain soils. The three most frequent Fusaria observed were Е solani, Е compactum and

Е equiseti. The number of species recovered by soil dilution proved to be greater in the

case of regosols in comparison to other soil groups or the two other techniques (Tables 2

& 3).

The highest frequency of occurrence was displayed by Е compactum and F.

equiseti following the soil-baiting technique (80%); F solani stands after when applying

Isolation Technique**

Soil Dilution Soil Plating Soil Baiting

_Taxon Dilution Plate

F. solani 4.64 12.24 38.14 3.51

F. compactum 0.02 5.85 15.67 4.14

F. sambucinum 2599778 0.91 2.39 3.02

F. equiseti 0.21 3.89 9.28 1.54

F. chlamydosporum 5.78 2.56 1.75 227

F. sporotrichioides 5.94 0.22 0.58 0.75

~ Data represent Chi-square statistic at 748.43 (15 df)

** See the Material and Methods section for details on isolation techniques.

*** Values in italics represent source of significant contribution to the chi-squar value.

Table 3. Occurrence of Fusarium species in various soil groups during January 1995 and 1996, isolated

using the soil baiting method and plated by soil dilution plate method and direct soil plating. Soil

plating values are shown between parentheses.

Source - MNHN. Paris

158 ОА. MANDEEL

Soil Group *

Fusarium зрр. cs NS R RM RD RD%**

F. solani 61 36 2 79.2

(37) (8) (9) 33:33

Е. compactum 3 1 8 9.6

(12) (15) (22) (11) 37.03

F. equiseti 2 2 10 E 112

(16) (13) (09 (D 29.62

Total number of fungi 30 40 510 221 297

* Soil groups are : CS- Cultivated Solonchak; NS-Natural Solonchak; R-Regosols;

RM-Raw Mineral Soils; RD=Rock Dominated Areas.

**Relative Density Values.

Table 4. Contingency table* for Fusarium species by isolation technique interactions among all soil

groups.

Frequency of Occurrence (*)

100

F. solani

F. compactum

F. sambucinum

F. equiseti

F. chlamydosporum

Е. sporotrichioides

Dilution Plating Baiting Total

Isolation Technique

Figure 3. Frequency of occurrence (%) of Fusarium species using various isolation techniques.

Source : MNHN, Paris

OCCURENCE OF FUSARIUM SPP. IN BAHRAIN 159

either the soil plating or the soil baiting techniques (60%) (Fig. 3). The frequency of

occurrence of other Fusaria ranged from 0-40%, The Fusarium solani exhibits the highest

total frequency (70%) while Е sambucinum and Е sporotrichioides displays the lowest

ones(10%). Fusaria sampled from the different soil types were not recovered independently

of the isolation technique applied. Interaction between species and techniques among soil

groups proved to be highly significant, as determined by the chi-square contingency table

at P = 0.05 (Table 4). A greater than expected recovery of Е sambucinum and Е solani

occurred using the soil dilution and the soil plating techniques, respectively. For the soil

baiting method (using the soil dilution one), recovery of Е solani, Е compactum and F.

equiseti was greater than expected. Similar significant chi-square values were obtained in

the contingency table using relative density figures.

DISCUSSION

All Fusaria isolated during this study were recorded earlier in cultivated and

noncultivated habitats of Bahrain with the exception of Е sporotrichioides (Mandeel &

Abbas, 1994; Mandeel et al., 1995; Abbas & Mandeel, 1995). In this and in previous

studies, the three most frequently recovered species were Е solani, Е compactum and F.

equiseti (Fig. 3). These taxa were also reported from desert and saline soils of related

Arabian peninsula countries (Mazen et al., 1980; Abdel-Kader et al., 1983; Moustafa &

Khosrawi, 1983; Abdel-Hafez et al., 1990; Hashem, 1995). Similar findings were noted

from other deserts of the world: French Sahara (Nicot, 1960); Sonaran desert (Ranzoni,

1968); Nevada desert (Durrell & Shields (1960) and in desert soils of Wadi Bir-El-Ain,

Eastern desert of Egypt (Moubasher er al., 1985).

The above Fusaria are typically soil-borne fungi persisting in soil in the absence

of suitable substrate as dormant chlamydospores (Nash et al., 1961), as resistant hyphae

(Nyvall & Kommedahl, 1968) or as conidia in the case of plant residues (Kreutzer, 1972).

In terms of host specificity, these Fusaria range from highly competitive saprophytes able

to interact with other soil microflora (Nyvall & Kommedhal, 1970) to specialized forms

attacking several plant families where they induce considerable economic losses (Burgess,

1981). Nutritionally, they are active under a broad range of substrates with mutation being

quite frequent within populations to adapt to specific requirements (Toussoun & Nelson,

1975). Also once they are established within a soil niche or as plant pathogens, they are

difficult to eliminate.

Species spectrum and numbers can be related to variations in climatic conditions

on a large geographical scale basis (Burgess et al., 1988; Kommedahl et а1.,1988, Jeschke ег

al., 1990; Burgess & Summerelle, 1992; Sanglang et al., 1995). In this repect, Е solani, F.

compactum and Е equiseti are cosmopolitan in distribution, adapted to a wide range ОГ

environmental conditions and habitats, in particular habitats of arid and semi arid

regions. Other species (Е sambucinum and Е sporotrichioides) with specific climatic

requirements are restricted to cold temperate and alpine soils; they thus occur in low

frequencies in zones unfavorable for their survival. By analogy, the former category may be

classified as soil-inhabitants and the latter as soil-transients. However, on a narrow

geographical scale basis, Fusarium recovery and distribution is also largely influenced by

soil factors. Thus, the highest species diversity and isolate recovery occurred in the case of

гевозо (Tables 2 & 3), probably due to their low salinity levels (660 uScmr!), as compared

to other soil types. Similar findings were reported elsewhere (Khodair ег al., 1991; Abbas

& Mandeel, 1995).

Source : MNHN, Paris

160 ОА. MANDEEL

Although it is difficult to relate variations in Fusarium population and spectra to

a specific soil factor, the exerted effect of high salinity levels counteracted richness in

organic matter as a food source and thus greatly reduced Fusarium recovery from the same

soils (Table 1). Therefore, Fusarium were not recovered from soil types rich in organic

matter, such as cultivated solanchak (18.34%) having a high total soluble salts (6.7%),

presumably because of their high electrical conductivity: 15930 uS cm" (Tables 1, 2 & 3).

Recovery of Fusarium species increased in soils of raw minerals characterized by low

salinity levels, low to moderate organic matter content and soluble salts, followed by

natural solonchak soils. Similar observations were also reported by Abdel Fattah et al.,

(1977) from salt marsh soils. Variations in pH does not seem to affect species prevalence

and density except possibly in the extremes (Mandeel & Abbas, 1994).

Low recovery levels and limited species variability was found in noncultivated

soil types as compared to cultivated soils (Mandeel er a/; 1995). This is in agreement with

other findings (Nash & Christou, 1965). Stoner (1981) stated however that "since the roles

of these fungi (Fusarium) are not restricted to parasitism and disease and can involve

nutrient cycling and other functions in noncultivated soils, it is conceivable that large

populations are not a prerequisite to significant ecological impact”.

In noncultivated hot desert ecosystem, where Fusarium species are present at

discrete locations in low frequencies and in various forms, it becomes essential to use many

isolation techniques to adequately demonstrate species abundance and distribution (Sto-

ner, 1981; McMullen & Stack, 1982). Based on modes of persistence in soil, isolation

technique can greatly affect rate of recovery of individual members within the genus.

Because soils in Bahrain are formed from Holocene and Pleistocene sedimentary rocks

that are saline and generally poor in organic matter (Table 1), isolation methods applied

here aimed to isolate species from these groups of soils. The soil dilution technique

decreases soil salinity by 1075 and favours the isolation of species sporulating profusely or

which are basically chlamydopores formers (Burgess & Summerell, 1992). Although the

technique has some limitations, it reflects the general distribuiton trends associated with

microbial activity and nutrient cycling processes, especially in stressful environments such

as deserts (Mandeel et a/., 1995). For fast growing species persisting in soils as mycelium or

by adherence to humus or mineral particles, the soil plating technique is appropriate. The

baiting procedure was designed to recover competitive saprophytes by the addition of an

organic substrate. In the present work, highest species diversity and density were found

with the soil dilution method from samples of regosals as compared to the other methods

(Tables 1 & 2).

Although certain species were not recovered by one or the other technique, it is

difficult to assess whether recovery of an individual species was favoured or inhibited by

the isolation technique. In addition, Sanglang eż al. (1995) indicate that inability to recover

aspecies from a particular soil in a climatic region do not imply the fungus is totally absent

even when present at low frequencies, given the nature of the isolation technique used.

Therefore, for quantitative and qualitative comparisons of soil Fusarial, several techni-

ques must be used to avoid any possible bias in the survey results (Burgess, 1981;

MeMullen & Stack, 1982).

Analysis of the relationships between species recovery and isolation technique as

determined by chi-square tests revealed significant interactions (Table 4). These suggest

some techniques allow a greater recovery of Fusarium species from the different soil

groups. On the whole, soil dilution or plating using the baiting technique yielded higher

isolate numbers for Е solani, Е compactum and Е equesiti from all soil groups as

compared to other techniques (Tables 1, 2).

Source : MNHN. Paris

OCCURENCE OF FUSARIUM SPP. IN BAHRAIN 161

Mandeel er al. (1995) compared several media for Fusarium recovery from

cultivated and noncultivated habitats of Bahrain. They concluded that standardization of

isolation media greatly minimizes variations within population types. This is particularly

important when comparing surveys from arid habitats. Ideally, more than one technique

and media should be used for recovery of soil-borne Fusarium species.

Several investigators did not disclose significant differences in the density or

diversity of Fusarium species isolated by soil dilution, soil plating or debris plating

techniques (McMullen & Stack 1982). But when comparisons were made for soils of

different altitudes, the diversity of Fusarium species was found to be greater when using the

debris plating technique rather than the soil dilution plating (Jeschke ег al., 1990). In the

present study, use of the soil dilution technique gave a recovery of Fusarium species by

lowering salinity levels (Table 1).

The results of the present work show that observed spectra and densities of

Fusarium species are low when compared to data for cultivated soils. Also predominant

species appear better adapted to extreme environment and have broader nutrient require-

ments; such accounts for their higher frequency when compared to other species. Further,

since each isolation technique and medium used is somewhat selective, it is difficult to

recover all species by one technique and one medium. It is therfore important to use a

combination of various isolation methods and media to obtain good estimates of a

populations density and the diversity of species within the genus in case of soil surveys.

ACKNOWLEDGMENTS

The author wish to thank Dr. С. Hoad for reviewing the present document and

Mrs. Fatema Abdul Rahim for typing the manuscript.

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Source : MNHN, Paris

OCCURENCE OF FUSARIUM SPP. IN BAHRAIN 163

NYVALL В. Е & KOMMEDAHL T, 1970 - Saprophytism and survival of Fusarium moniliforme

in corn stalks, Phytopathology 60 : 1233-1235.

RANZONI F. V., 1968 — Fungi isolated in culture from soils of the Sonoran Desert. Mycologia 60

356-371.

SANGLANG A. E., BURGESS L. W., BACKHOUSE D. B., DUFF J. & WURST M., 1995 —

Mycogeography of Fusarium species in soils from tropical, arid and Mediterranean

regions of Australia. Mycological research 99 : 523-528.

STONER M. F, 1981 — Ecology of Fusarium in noncultivated soils. In: Nelson P.E., Toussoun Т.А.

& Cook R.J. (ed.), Fusarium, Diseases, Biology, and Taxonomy. Pennsylvania State Uni-

versity Press: University Park, Pennsylvania, U.S.A., pp.276-286.

TOUSSOUN T. A. & NELSON P. E. 1975 — Variation and speciation in the fusaria. Annual review

of phytopathology 13 : 71-82.

Source : ММНМ. Paris

ааа меа

Поя à

Cryptogamie, Mycol. 1996, 17 (3-4) : 165-171 165

ENVIRONMENTAL GROWTH REQUIREMENTS FOR

SUBMERGED CULTURES OF THE ECTOMYCORRHIZAL

FUNGUS CENOCOCCUM GEOPHILUM Fr.

Daniel JOB

Laboratoire de Microbiologie, Université de Neuchâtel,

Chantemerle 22, CH — 2007, Neuchâtel, Suis

ABSTRACT — The ability of Cenococcum geophilum to produce an enlarged biomass of submerged

mycelial condensations under different culture conditions was evaluated. Best production (mycelial

dry weight 11,15 mg/ml) occurred in 101 flasks of glucose di-ammonium tartrate casein medium (pH

5.8) flushed with 90 1 / hour of sterile air and inoculated with 5% w-w of fresh mycelium with

incubation in the light (100 lux) during 28 days at 25° С.

RESUME — La capacité de Cenococcum geophilum à produire une biomasse considérable de

mycélium submergé dans différentes conditions de culture a été testée. Le meilleur rendement (poids

sec de mycélium 11,15 mg/ml) a été obtenu dans des flacons de 10 litres, contenant un milieu glucose,

di-ammonium tartrate et caséine (pH 5.8), dans lesquels 90 litres d'air stérile sont injectés par heure.

Ces flacons sont inoculés avec 5% poids/poids de mycélium frais et incubés 28 jours sous éclairage

(100 lux) à 25° C.

INTRODUCTION

Ectomycorrhizal fungi occur in nearly all soils on earth and form a symbiotic

relationship with roots of most terrestrial plants.

Mycorrhizal fungi are known to benefit plant growth in several ways as nutrient

uptake (Harley & Smith, 1983) and in pathways involving phosphorus nutrition (Morton

et al., 1990). These fungi increase plant tolerance to a number of stressors or activate

transport of water to the roots (Parke et al., 1983). In addition, soil or seedling inoculation

with ectomycorrhizal fungi make possible the introduction of tree plants in areas which

would not otherwise support their growth (Harvey, 1991).

The first step in an artificial inoculation program requires the development of

appropriate iinocula. There is a diversity of sources of mycorrhizal inocula and few patent

applications have been made with most involving particular growth substrates (Menge ег

al., 1978; Marx et al., 1981; Baltruschat & Dehne, 1985; Wood et al., 1985).

In a previous paper (Job & Aragno, 1992) we investigated nutritional growth

requeriments of Cenoccum geophilum in submerged cultures. This fungus has been fre-

quently reported in ectomycorrhizal associations with several economically important

tree families (Heslin & Douglas, 1986; Danielson & Pruden, 1989).

Source - ММНМ, Paris

166 D. JOB

In the present work, we investigated the ability of this taxon to produce large

amounts of mycelial pellets under а range of different cultural conditions. We can thus

propose an optimized culture environment with the final objective of producing sufficient

quantity of inocula for large-scale forest application.

MATERIALS AND METHODS

Strain

Experiments were conducted with strain XO1-20) supplied by Vitroculture SA.,

Porrentruy, Switzerland; isolation locality is Birmensdorf, Zurich.

Preparation of mycelial inoculum

Cultures of Cenoccum geophilum were grown in Gd-ATC (glucose

di-ammonium tartrate casein medium: Job & Aragno, 1992) at 25° C. After an incubation

period of 21 days in dark conditions, mycelial pellets were aseptically homogenized and

used as inocula for all experiments.

Culture media

The selected strain was grown in Gd-ATC. For each test, five 10 1 flasks

containing 7 | of sterile medium (sterilized 90 min at 121° C) were used.

At the end of the incubation period (28 days), mycelial pellets were washed and

dried. Fungal biomass is expressed as mg dry weight/ ml culture medium with given values

being means of five replicates.

Temperature and light intensity

Flasks (pH 5) inoculated with 3% of inoculum were incubated 28 days (air

flushing 60 I/h) at 15, 25 or 30° C and 100, 200, 300 lux 12 hs/day or in complete darkness.

Air flushing

Flasks (pH 5) inoculated with 3% of inoculum were flushed with 10, 30, 60, 90

and 120 l/h sterile air and incubated 28 days at 25° C under 100 lux at 12 hs/day.

Flasks inoculated with 3 % of inoculum, flushed with 90 W/h sterile air, with pH

adjusted (0.1 M HCl or NaOH) to 2.2, 3.4, 4.6, 5.8 and 7.0 were incubated 28 days at 25° C

and under 100 lux at 12 hs/day.

Size of inoculum

Flasks (pH 5.8) were inoculated with 7 differents levels of inocula (1%, 2%, 3%,

4%, 5%, 7.5% and 10% w-w) and then incubated 28 days at 25° C, under 100 lux at 12

hs/day and flushed with 90 ИВ sterile air.

Source - ММНМ, Paris

SUBMERGED CULTURES OF CENOCOCCUM GEOPHILUM 167

LUX

ше 0 100 200 300

15 2.12 +/- 0.12 4.15 +/- 0.17 428 +/- 0.26 431 +/- 021

25 3.96 +/- 0.21 6.60 +/- 0.27 6.53 +/- 0.35 6.27 +/- 0.40

30 412 +- 014 | 627 +/- 0.19 6.61 +/- 038 6.07 +/- 0.35

Table 1. — Mycelial dry weight (mg/ml) of Cenococcum geophilum (mean of

the different conditions of light and temperature tested

replicates) obtained in

Tableau 1. — Poids sec du mycelium de Cenococcum geophilum (moyenne de 5 expériences) obtenu

dans différentes conditions de lumière et températures.

| Жш

10 30 60 90 120, и

Fig. 1: Mycelial biomass (mg dry weigt/ml) obtained after 28 days, in Gd-ATC medium with different

air flush (/h)

Fig. 1: Biomasse du mycélium (mg poids sec/ml) produite après 28 jours, dans un milieu Gd-ATC avec

différent pompage d'air stérile (Vh)

mg/ml

MNHN, Pai

168 D. JOB

mg/ml

22 3.4 4.6 5.8 7 pH

Fig. 2: Mycelial biomass (mg dry weigt/ml) obtained after 28 da

in Gd-ATC medium with different

Fig. 2: Biomasse du mycélium (mg poids sec/ml) produite aprés 28 jours, dans un milieu Gd-ATC avec

différent pH

RESULTS

Table I shows yields as mycelium dry weight mg/ml culture medium obtained

under different conditions of light and temperature.

Both temperature and light are important for the mycelial growth of filamentous

fungi. Present data indicate dark conditions were unsuitable for growth of Сепоссит

geophilum. Indeed, table I shows, that a maximum growth at 25 or 30° C was obtained only

under light conditions. However no significant yield increment was obtained with increase

in light ntensity from 100 to 300 lux.

Figures 1, 2 and 3 relate mycelial growth to the amount of air flushing, inoculum

size or to pH.

We observed, (figure 1) that a flush of 90 liters of sterile air per hour was the

optimum to support best mycelial growth. A decrease of this flush considerabily reduced

mycelial yield and at a flush of 10 I/hs the fungus failed to grow vigorusly.

A similar result appear from figures 2 or 3. A neutral pH or a too acid value (2.2

or 3.4) affected fungal yield production of C. geophilum. An inoculum level of 5% w-w

proved to be the optimum to support a good mycelial growth. A decrease in the amount of

the inoculum also negatively affected fungal production.

Source : MNHN, Paris

SUBMERGED CULTURES OF CENOCOCCUM GEOPHILUM 169

Beside, figure 4 compares growth curves of C. geophilum developing in a stan-

dard media for ectomycorrhizal fungi as Melin-Norkans’ modified medium: MMN (Job

et Aragno, 1992) and in an optimized medium for C. geophilum (Gd-ATC, pH 5) in

standard culture conditions (Job et Aragno, op.cit) with growth data of the same fungus in

Gd-ATC medium at pH 5.8 but inoculated with 5% of mycelia and incubated in the

optimized conditions (25° 00 lux 12 hs/day and flushed with 90 1 sterile air /hs).

mg/ml

al 2 3 4 5 7.5 10

Fig. 3: Mycelial biomass (mg dry weigt/ml) obtained after 28 days, in Gd-ATC medium inoculated

with 7 differents levels of inoculum.

Fig, 3: Biomasse du mycélium (mg poids sec/ml) produite aprés 28 jours, dans un milieu Gd-ATC

inoculé avec 7 différentes quantites d'inoculum

Beside, figure 4 compares growth curves of C. geophilum developing in a stan-

dard media for ectomycorrhizal fungi as Melin-Norkans' modified medium: MMN (Job

et Aragno, 1992) and in an optimized medium for C. geophilum (Gd-ATC, pH 5) in

standard culture conditions (Job et Aragno, op.cit) with growth data of the same fungus in

Gd-ATC medium at pH 5.8 but inoculated with 5% of mycelia and incubated in the

DISCUSSION

Ectomycorrhizal fungi exhibit a wide range of pH tolerance (pH 3.0-7.0).

However, in vitro, pH affects the growth in culture of several ectomycorrhizal fugi

(Suvercha et al. 1991)

MNHN, Paris

170 D. JOB

mg/ml

12 =

10 jé

Е 3

8 medium

7 А — Gd-ATC opt

6 --- Gd-ATC

5 ] ---- MMN

4 -—

5 L

78 14 24 28

days

Fig. 4: Growth curves of Cenococcum geophilum (mg dry weight/ml) in two media for ectomycorrhizal

fungi (MMN and Gd-ATC) in standard conditions and in the Gd-ATC in the optimized conditions

Fig. 4: Courbes de croissance de Cenococcum geophilum (mg poids sec/ml) dans deux milieux pour

champignons ectomycorrhiziques (МММ et Gd-ATC) en conditiones standard et dans le milieu

Gd-ATC en conditions optimales.

Our work showed that different values of temperature and pH exerted significant

effects on the mycelial growth of C. geophilum. We found that the temperature and pH

required for optimum growth in vitro of C. geophilum were similar to those required for

other fungi (Song et al. 1987). However, in comparison to other ectomycorrhizal fungi, C.

geophilum, requires a relatively high light level for optimum submerged mycelial conden-

sations growth.

We also observed the increment of growth of this fungus when we increased the

air flush, showing that mycelium growth used oxygen and an adequate supply of this is an

essential requirement throughout the fermentation cycle. One of the advantages of the air

flush design here introduced, was the use of a sparger which admits a stream of small air

bubbles resulting in a more effective aeration and smaller pellets as compared to pellets

obtained using mechanical agitation (Job et Aragno, 1992).

Therefore, a well-balanced aeration and agitation system is necessary, due to the

partialy contradictory requirements of filamentous fungi: the necessity of high oxygen

tension and a high sensitivity against mechanical stress (figure 1 shows that a very high

flush decreased the mycelial growth).

Contrary to the general idea that ectomycorrhizal fungi grow very slowly in

Source : ММНМ, Paris

SUBMERGED CULTURES OF CENOCOCCUM GEOPHILUM 171

liquid media (Chapman et al., 1990) our results stress that optimization of the culture

medium and environmental conditions, allows fast growth developing a marked biomass

in submerged cultures. Such is indicated by the high biomass yield developed by Сепосос-

сит geophilum to levels approximatring yields developed by several saprophytic fungi

(Song et al., 19 87).

ACKNOWLEDGEMENTS

The authors wish to thank Vitroculture S.A. and CERS (projet nj1404) for their

financial support.

REFERENCES

BALTRUSCHAT H. & DEHNE H-W, 1985 - Culture substrate for inoculation of plants with

mycorrhiza fungi consisting of and adsorbent e.g. vermiculite for pumice in which mycorrhiza-

infected plants have been grown. German patent 3416315.

CHAPMAN W.K., BERCH S.M. & BALLARD T.M., 1990 — In vitro growth of ectomycorrhizal

fungi on dilute agar. Mycologia 2: 526-527.

DANIELSON R.M. & PRUDEN M., 1989 — The ectomycorrhizal status of urban Spruce. Myco-

logia 82: 335-341.

HARLEY J.L. & SMITH S.H., 1983 — Mycorrhizal symbiosis. Academic, San Diego, California

HARVEY L.M., 1991 — Cultivation techniques for the production of ectomycorrhizal fungi

Biotechnology advances 9: 13-29.

HESLIN M.C. & DOUGLAS G.C., 1986 — Synthesis of Poplar mycorrhizas. Transaction broteria

mycological society 86: 117-122.

JOB D. & ARAGNO M., 1992 — Nutritional growth requeriments for submerged cultures of the

ectomycorrhizal fungi Сепососсит geophilum. Cryptogamie, Mycologie 13 (2): 19-85

MARX D.H., RUEHLE J.L., KENNEY D.S., CORDELL C.E., RIFFLE J.W., MOLINA R.J.,

PAWUK W.H., NAVRATIL S., TINUS R.W. & GOODWIN O., 1982 — Commercial

vegetative inoculum of Pisolithus tinctorius and inoculation techniques for development of

ectomycorrhizae on container-grown tree seedlings. Forest science 28: 373-400.

MENGE J.A., LABANAUSKAS C.K., JOHNSON E.L.V. & PLATT R.G., 1978 — Partial substi-

tution of mycorrhizal fungi for phosphorus fertilization in the greenhouse culture of

citrus. Soil science society american 42: 926-932.

MORTON J.B., YARGER JE. & WRIGHT S.F., 1990 — Soil solution P concentrations necessary

for nodulation and nitrogen fixation in mycorrhizal and non-micorrhizal red clover. Soil

biology and biochemistry 22: 127-

PARKE L.J., LINDERMAN R.G. & BLACK C.H., 1983 — The role of ectomycorrhizas in drought

tolerance of Douglas-fir seedling. New phytologist 95: 83-95.

SONG C.H., CHO K.Y. & NAIR N.G., 1987 — А synthetic mediumfor the production of submerged

cultures of Lentinus edodes. Mycologia 19: 866-876.

SUVERCHA K., MUKERII С. & ARORA D.K., 1971. Ectomycorrhiza.in Handbook of Applied

Mycology Vol 1: 187-216. Marcel Dekker, Inc, Ney York.

WOOD Т., BIERMANN B. & GRAINGER H., 1985 — Improved production of axenic vesicular-

arbuscular mycorrhizal fungi using porous substrates inoculated with root inoculum. U.S.

patent 755493.

Source : MNHN, Paris

Source : ММНМ. Paris

Cryptogamie, Mycol. 1996, 17 (3-4) : 173-185 173

KERATINOLYTIC AND KERATINOPHILIC

FUNGI OF SWAMP'S SOIL AND AIR IN QENA CITY

AND THEIR RESPONSE TO GARLIC EXTRACT

AND ONION OIL TREATMENTS

Y. A. M. H. Gherbawy

Botany Department, Faculty of Science, South Valley University, Qena, Egypt

ABSTRACT — 48 species and one variety belonging to 25 genera were recorded from 50 soil samples

and from the atmosphere of a swamp in the city of Qena using the hair baiting technique at 28° C.

Twenty taxa were dermatophytes or closely related fungi. Most common and frequent species of this

group were Aphanoascus fulvescens, Aph. terreus and Aphanoascus sp. (anamorph: Chrysosporium

tropicum) and Chrysosporium xerophilum. Sixty-eight isolates were tested for their ability to grow on

hair-sand medium. Most strains tested (73.5 %) had moderate growth rate. All keratinophilic fungi

identified in the present investigation were sensitive to garlic extract and onion oil.

KEY WORDS: Air-spora, antifungal, garlic extract, keratinolytic and keratinophilic,onion oil

INTRODUCTION

Soil rich in keratinic residues constitute a permanent or an occasional reservoir

for dermatophytes, keratinolytic and keratinophilic fungi and is thus a potential source of

infection for man and animals. Several investigations have been carried on the presence of

these fungi in soil and in air in many countries all over the world (Papavassilion &

Bartzokas, 1975; Alteras & Lehrer, 1977; Acosta & Roberstad, 1979; Della-France &

Caretta, 1984; Chabasse, 1988). However, in Arab countries few such surveys were made

(Amer et al., 1975; Jana et al., 1979; Youssef et al., 1980, 1989; Abdel-Fattah ег al., 1982:

Abdel-Mallek et al., 1989; Abdel-Hafez et al., 1989, 1991; Karam El-Din et al., 1990;

Moubasher et al., 1990; El-Said, 1993, 1994; El-Maghraby, 1994).

The distinction between keratinophilic and keratinolytic fungi is based on the

proposals of Majchrowicz & Dominik (1969) and Dominik et al.(1973), later on adopted

by Filipello Marchisio & Luppi Mosca (1980, 1982). Keratinolytic species are defined as

those fungi able to directly destroy keratin, while keratinophilic taxa are only liable to use

materials naturally associated with keratin or resulting from its breakdown. The kerati-

nolytic activity of dermatophytes using guinea-pig hair as a test substrate was measured by

Yu et al. (1968).

Garlic ( Allium sativum L.) extract and onion oil have a long history of reputed

value and actual use for their medicinal, antimicrobial and pesticidal properties (Amon-

Source : MNHN, Paris

174 Y.A.M.H. GHERBAWY

Каг & Banerji, 1971; Shekhawat & Prasada, 1971; Fliermans, 1973; Appleton & Tansey,

1975; Tansey & Appleton, 1975; Moore & Atkins, 1977; Lewis et al.,1977; Deshmukh,

1984; Yoshida et al., 1987; Gherbawy, 1989; Singh et al. 1990; Zohari et al., 1992).

The present investigation aimed to study composition and frequency of occur-

rence of keratinophilic fungi in swamp’s soil and air in the city of Qena and their

keratinolytic activity. Also, a preliminary study on the antifungal effect of garlic extract

and onion oil on isolated keratinophilic taxa was conducted.

MATERIALS AND METHODS

Fifty soil samples were collected from different swamp localities in Qena,

according to the method described by Johson er al. (1959). Soil samples were analysed

chemically for the estimation of total soluble salts and organic matter. A pH-meter

(WGPYE model 290) was used for the determination of soil pH.

Isolation of keratinophilic fungi from soil samples

The hair baiting technique was employed as recommended by Vanbreuseghem

(1952) and as employed by Abdel-Fattah ег al.(1982): 100 g of soil were put in a sterile

plate and a sufficient quantity of sterile distilled water was added and mixed thoroughly to

bring about 20-25 % moisture content. Pieces of sterile horse hairs were sprinkled on the

surface of moistened soil. Two plates were used for each sample; plates were incubated at

28° C for 6-8 weeks and soil in plates was remoistened whenever necessary Moulds

appearing on the baits were transferred to the surface of Sabouraud dextrose agar medium

(Moss & McQuown, 1969) supplemented with 20 unit/ml of sodium penicillin, 40 u g/ml

of dihydrostreptomycin and 0.05 % cycloheximide (Actidione “R“). Before adding to the

agar, the frist two antibiotics were dissolved separately in sterile distilled water while the

third was dissolved in methanol. Plates were incubated at 28° C for 3-4 weeks and

developing colonies identified. Frequency of occurrence as percentage of samples and

relative important value (RIV) were calculated for each species (Shearer & Webster, 1985;

Ali-Shtayeh & Asa'd Al-Sheikh, 1988).

Estimation of airborne fungi

Plates (9 cm diam.) containing each 100g soil were moistened with distilled water

to about 25-30 %. Horse hair fragments were scattered on the soil surface. Plates were then

autoclaved (three times) at 121? C for 30 min. Sterile plate was exposed for 1 h to the

atmosphere of swamp; the process was repeated at 50 different sites. Exposed plates were

incubated at 28° C for 10-12 weeks and remoistened whenever necessary. Five hair

fragments/replicate were then inoculated on plates containing Sabouraud dextrose agar

medium, incubated at 28* C for 3-4 weeks and colonies developing from these hair

fragments were then identified. Frequency of occurrence as percentage of samples and

relative important value (RIV) was calculated for each species (Shearer & Webster, 1985;

Ali — Shtayeh & Asa'd Al — Sheikh, 1988).

Source : MNHN, Paris

KERATINOPHILIC FUNGI OF SWAMP'S SOIL AND AIR 175

Keratinolytic activity

Sixty-eight isolates of keratinophilic fungi were recoverd during the current

study; these were used for keratinolysis tests following the English method (1976). Hair-

sand cultures were made by scattering 1 cm long pieces of autoclaved hair over the surface

of 9 cm Petri dishes containing moist twice-autoclaved sand from the mangrove; plates

were inoculated with a 5 ml aqueous spore suspension of each fungus.The hair of fair

horse was used in all experments. After an incubation period of 20 days at room

temperature, the amount of fungal growth and sporulation was rated: + for weak growth,

+ + for moderate growth, + + + for heavy sporing and spreading cultures.

Test for the antifungal activities of some natural products

Twenty fungal isolates of keratinophilic fungi recovered in the present investi-

gation were used to study the antifungal effect of garlic extract and onion oil

Garlic (Allium sativum L.) extract

20 g of garlic bulbuls free of scaly le vere washed several times with sterile

distilled water, Bulbuls were homogenised in a sterile blender in 100 ml ethanol (70 %); the

mixture was then completed to 200 ml with distilled water to obtain a 10 % garlic extract.

The latter was then added to the autoclaved medium (Sabouraud liquid medium) at 3

concentrations: 1000, 2000 and 3000 ppm; a garlic free extract medium was used as

control.

Cultures were incubated at 28° C for 15 days.

Onion (Allium cepa L.) oil

Onion oil obtained from El-Nasr Company originates from dehydrating agricul-

tural products (A.R.E.). The oil was added to the medium (except for the control) to give

concentrations of 100, 200 and 300 ppm. Cultures were incubated at 28° C for 15 days.

RESULTS AND DISCUSSION

Soil samples

The organic matter content and total soluble salts in tested soil samples fluctua-

ted between 3.5-8.4 and 0.5-4.1 %, respectivily. All soil samples proved to be alkaline: pH

= 7.4-8.5.

Forty-one keratinophilic and cycloheximide resistant species were collected

from 50 swamp soil samples baited with horse hair fragments at 28° C.

Aphanoascus (teleomorph of Chrysosporium) was the most common genus,

occurring in 86 % of the samples and had RIV of 119.7. It was represented by 3 species: À.

fulvescens, A. terreus (anamorph: Chrysosporium indicum) and Aphanoascus sp. (Chrys

porium tropicum). They were present in 60 %, 24 % and 30 % of tested soil samples and

developed RIV values of 73.3, 32.4 and 40.5, respectivily. Aphanoascus fulvescens is known

to induce skin infections (Rippon et al., 1970; Albala er al., 1982). The above fungi were

previously isolated from soil but with different fequencies in many parts of the world

Source - MNHN., Pans

УА М.Н. GHERBAWY

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Source - MNHN, Paris

178 Y.A.M.H. GHERBAWY

(Piotelli & Caretta, 1974; Mostafa, 1977; Todaro, 1978; Jana et al. 1979; Sur & Ghosh,

1980; Abdel-Fattah er a/,. 1982; Calvo et al., 1984; Filipello Marchisio, 1986; Chabasse.,

1988; Abdel-Hafez ег al., 1991; El-Said, 1993).

The anamorphic genus Chrysosporium was the second most frequent entity; it

was encountered in 40 % of samples analyzed and had RIV of 54.7. For this genus six

species were identifed with C. xerophilum (28 %) being the most common one. The remai-

ning five taxa were rarely recovered; these were C. asperatum (4 %), C. carmichaelii (10 94),

C. lucknowense (4%), C. pannicola (6 %) and C. pruinosum (2%). All these species were

isolated from the soil samples of Oman by El-Said, (1993); there they developed from 6,

12, 10, 10 and 10 %, soil samples respectively. In Egypt, C. asperatum and C. pannicola were

isolated from Egyptian soils by Abdel-Hafez et al. (1989, 1991). Filipello Marchisio (1986)

isolated C. pannicola (3.5 %) and C. xerophilum (7.0 %) from children's sandpits in Italy.

Arthroderma occupied the third place with respect to number of cases of

isolation of recorded genera; it was recovered from 28 % of samples examined and had

RIV of 37.4. Four species were isolated; these are А. ciferii (teleomorph of Chrysosporium

georgii), A. cuniculi, A. curreyi and A. lenticulare (Trichophyton terrestre). In Italy, Filipello

Marchisio (1986) isolated 4. cuniculi and A. curreyi from children's sandpits. In Oman

El-Said (1993) isolated all above Arthroderma from soil samples.

Aspergillus (3 species + 1 variety) occupied the fourth place and was encounte-

red in 26 % of the soil samples. Among observed Aspergilli, most commonly collected

were A. flavus and A. terreus. The remaining taxa were scarcely recovered; these were 4

flavus var. columnaris, A. fumigatus and A. niger. Aspergillosis due to A. fumigatus and А

flavus has a cosmopolitan distribution (Frey et al., 1979). Khallil & Abdel-Sater (1991)

isolated А. flavus, A. fumigatus, A. niger and A. terreus from mangrove soils of the

Egyptian Red Sea Coast. Most of the above Aspergilli were previously encountered, but

with different incidence from various types of soil from many parts of the world (Sunda-

ram, 1987; Abdel-Hafez er al., 1989; El-Said, 1993, 1994).

‘hophyton developed from 16 % of collected samples. It was represented by

Tajelloi and T. mentagrophytes. These two species have a wide distribution and аге

recovered from different substrates (Todaro, 1978; Filipello Marchisio, 1986; Abdel —

Hafez er al., 1989; El-Said, 1994). The above two species were found as saprophytes in man

and animals, but also have been recognised as causal agents of tinea, onychomycosis and

ringworms (Frey et al., 1979).

Microsporum gypseum was observed on only 14 % of the samples. Abdel-Fattah

et al. (1982) isolated M. gypseum from Egyptian soils where it was encountered in 8.5, 2.9

and 7.1 % of soils baited with human hair, animal hair and feathers, respectively. This

species is cosmopolitan and it is encountered in different geographic zones (Stepanish-

cheva, 1965; Belukha & Lukyanova, 1969; Padhye et al., 1967; Meinhof & Grabowski,

1972; Alilous & Asgar, 1973; Abdel-Hafez et al., 1989). The fungus was reported from skin

lesions, feather and pellets of free-living birds, hairs and skin of monkeys, dogs, mice, rats

and other small mammals. It was also recognised as the causal agent of dermatomycosis in

cattle and in man from different parts of the world (Domsch et al., 1980).

The remaining 13 genera and 15 species recorded were recovered in rare fre-

qeuncies (Tab. 1).

Airborne fungi

The concentrations and the composition of air-spora trapped at 1.5 m above

ground level are showen in Table (1).

Source : MNHN, Paris

KERATINOPHILIC FUNGI OF SWAMP'S SOIL AND AIR 179

Twenty-nine species and 1 variety belonging to 15 genera were recovered from

the swamp atmosphere using hair baiting technique at 28° C.

Aphanoascus, a genus closely related to dermatophytes, was common in the air;

it emerged in 90 % of exposed samples. Aphanoascus also comprised 31.3 % of total fungal

catches and had RIV of 121.3. Three species were identified: А. fulvescens, A. terreus and

Aphanoascus sp. These occurred in 60 %, 42 % and 52 % of exposures; they comprise

11.2%, 9.5 % and 10.3 % of total fungi and had RIVs of 71.2, 51.2 and 62.3, respectively.

Aphanoascus terreus and Aphanoascus sp. were recovered previously from the air of Hibis

Temple at El-Kharga Oasis in Egypt: there they emerged in 25 % and 33 % of exposures

and matched 3.1 % and 16.1 % of total fungi, respectively (Ismail, 1990). Other fungi

closely related to dermatophytes were also isolated but with different incidences: Apinisia

queenslandica, Chrysosporium asperatum, C. pruinosum, C. xerophilum, Microsporum

gypseum, Myceliophthora vellerea, Trichophyton equinum and T. mentagrophytes. Few

numbers of keratinophilic fungi has been encountered previously from the air in other

parts of the world (Papavassilion & Bartzokas, 1975; Alteras & Lehrer, 1977; Acosta &

Roberstad, 1979; Patil & Kulkarni, 1981; Della-France & Caretta, 1984; Moubasher et al.,

1990; El-Maghraby, 1994).

Several moulds were also isolated from the swamp atmosphere using horse hair

fragments as bait; these include members of the genera Alternaria (1 species), Aspergillus

(5 + 1 variety), Cladosporium (2), Cochliobolus (1), Cunninghamella (1), Mycosphaerella

(1), Penicillium (5), Scopulariopsis (1) and Syncephalastrum (1). For these genera most

commonly encountered species were: Alternaria alternata, Aspergillus flavus, A. fumigatus,

A. niger, A. sydowii, Cladosporium cladosporioides, Cochliobolus spicifer, Cunninghamella

echinulata, Mycosphaerella tassiana, Penicillium chrysogenum, P. corylophilum, P. funicu-

losum, Scopulariopsis brevicaulis and Syncephalastrum racemosum. These findings are

almost in agreement with those reported by El- hraby (1994) during a study on the

atmosphere of some schools at Hurghada City; this author also reported that several of

the above taxa were then most commonly encountered on goat hair baits lying on

Sabouraud dextrose agar. Several of the previous taxa are known to be allerginic (Plu-

tarco, 1958; Masatomo et al., 1991), or causing asthma (Beaumont et al, 1985), able to

develop ocular infection (Sehgal et al., 1981), hyper-sensitivity pneumonities and pulmo-

nary infections (Treger et al., 1985; Arianayagam et al., 1986).

Keratinolytic activity

Table (2) indicate that isolates of different or the same species have variable

growth. Most of the isolates (50) showed а resonable rate (++) of growth. Ten isolates gave

higher rates (+++) with abundant vegetative growth. Some isolates have keratin-

degrading enzyme(s), but they differ in their capabilities for the production of these

enzymes. Peyton et al. (1986) recorded a significant keratinolytic activity of M. canis and

M. gypseum. Filipello Marchisio (1986) reported that members of Microsporum, Tricho-

phyton, Mariannea, Aphanoascus, Chrysosporium, Malbranchea and Geomyces were the

most active keratinolysis. In Egypt, Mahmood (1990) reported that 7: mentagrophytes was

able to grow actively on horse hairs.

Source : MNHN, Paris

180 Y.A.M.H. GHERBAWY

Rate of growth

Fungal isolates ip ++ +++

Aphanoascus. fulvescens (10) -

A.terreus (6) 2

Aphanoascus sp. (8) 3

Apinisia queenslandica (1) -

Arthroderma.ciferrii (2) E

A.cuniculi (4) 1

A. curreyi (6) 2

A.lenticulare (1) -

Chrysosporium asperatum (1) -

C. carmichaelii (4) -

C.lucknowense (1) -

С. pannicola (2) -

С. pruinosum (1) -

С. xerophilum (8) 2

Microsporum вурзеит (5) -

Myceliophthora vellerea (1) -

Trichophyton ajelloi (1) -

T. equinum (2) 1

T. mentagrophytes (3) -

T. rubrum (1) - -

Total (68) 8 50. 10

Percentage (100) 11.8 735 14.7

* The number between parentheses indicate the number of isolates tested.+,

indicates weak growth; + +, indicates moderate growth; + + +, indicates

abundant growth.

кшк O OV Ea EO pa ds кә ORO OR А

Table 2 : growth of fungal isolates on hair- sand medium.

Effect of garlic extract and onion oil on isolated keratinophilic fungi.

Garlic extract

All tested fungi were sensitive to garlic extract. Mycelial dry weight of Apha-

noascus fulvescens, A. terreus, Apinisia queenslandica, Arthroderma ciferrii, A. cuniculi, A.

curreyi, Chrysosporium asperatum, C. carmichaelii, C. lucknowense, C. pannicola, C. priu-

nosum, Microsporum gypseum, Trichophyton ajelloi and T. mentagrophytes was signifi-

cantly reduced by the three tested concentrations. Mycelial dry weight of Aphanoascus sp.,

Arthroderma lenticulare, Chrysosporium xerophilum and Trichophyton equinum signifi-

cantly depressed by 2000 and 3000 ppm, whereas that of 7; rubrum was decreased by the

3000 ppm only ( Table 3).

Source : MNHN, Paris

KERATINOPHILIC FUNGI OF SWAMP'S SOIL AND AIR 181

Garlic Extract Onion Oil

Species L M H L M H

ыы шшш (4000ppm) | 100 200 400

| Aphanoascus. fulvescens 0* | 758 33* 15*

A. ferreus p и 12* |82 62* 20*

Aphanoascus sp. 86 74* 68* 192 81* 70*

Apinisia queenslandica 71" 62* ок 187 63* 22*

Arthroderma.ciferrii 53* 42* ок | 66* 54* 0*

А. cuniculi 62* 35* 12% me 42* 13*

A. curreyi 50* 0* ок |65* 41* 0*

A.lenticulare 85 73* 25* |92 87 62*

Chrysosporium asperatum | 72* 60* 45% |84 63“ 23"

C. carmichaelii 69* 71“ 63* | 73* 39* 10*

C.lucknowense 76* 53* 25* |86 65* 18*

C. pannicola 68* 32* o* |75* 52* о,

С. pruinosum 65* 43* 0* |70* 35* ок

С. xerophilum 85 70* 35* |90 84 60*

Microsporum gypseum 51* 48% 25+ |85 65* 22*

Myceliophthora vellerea 95 84 7* |97 90 85

Trichophyton ajelloi 77* 72* 33* |86 66* 24*

T. equinum 83 75 55 89 72“ 65*

T. mentagrophytes 59* 10* o* |40* oF о,

T. rubrum 92 80* 69% |75* 60* 12*

* Means significant difference comparable with the control.

Table 3 : Effect of various concentrations of garlic extract and onion oil on the mycelial dry weight

(calculated as percentage of the control) of the test fungi

Appleton & Tansey (1975) reported that Epidermophyton floccosum. Microspo-

rum canis, M.gypseum, Trichophyton mentagrophy tes, T. rubrum and Scopulariopsis brevi-

caulis do not grow in a concentration of 5.10 garlic extract. Prasad et al. (1982) observed

that the topical application of the crude extract of garlic at a 1/10 concentration in distilled

water could combat rabbit dermatophytosis induced by Microsporium canis without

causing any apparent side effects.

Onion oil

The three levels of onion oil inhibited mycelial growth of Aphanoascus fulves-

cens, Arthroderma ciferii, A. cuniculi, A. curreyi, Chrysosporium carmichaelii, C. pannicola,

A. purinosum, Trichophyton mentagrophytes and T. rubrum. Mycelial growth of Ap/ianoas-

cus terreus, Aphanoascus sp., Apinisia queenslandica, Chrysosporium asperatum, C. luck-

nowense, Microsporum gypseum, Trichophyton ajelloi and T. equinum was significantly

retarded by medium and high doses. However, Arthroderma lenticulare and Chrysosporium

xerophilum were significantly retarded by high doses only. On the other hand Myce-

liophthora vellerea was not significantly affected by any level of onion oil (Table 4).

Shekhawat & Prasada (1971) reported that boiled water extracts of onion caused

inhibition to growth of Alternaria tenuis, Helminthosprum sp.and Curvularia penniseta.

More recently Zohari et al. (1992) noticed that onion oil (at 200 ppm) completely inhibited

growth of Microsporum canis, M. gypseum and Trichophyton simii, while Chrysosporium

Source : MNHN, Paris

182 Y.A.M.H. GHERBAWY

queenslandicum and Trichophyton mentagrophytes were completely inhibited by a 500 ppm

content.

ACKNOWLEDGEMENTS.

The author is deeply indebted to Prof Dr. S. 1. 1. Abdel-Hafez professor of

Mycology, Assiut University, Egypt for valuable advices and to Dr. A.M. El-Araby for

continuous encouragements.

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TREGER T. R., VISSCHER D. W., BARTLETT M. S. & SMITH J. W., 1985 -Dignosis of

pulmonary infection caused by Aspergillus. Usefulness of respiratory cultures. Journal of

infectious deseases 152: 572-576.

TODARO Е, 1978 — Polluting agent of beaches. Notes 11. Results of screening in 10 localities on the

shore north of Messina (Italy). Nuovi annali dOigiene e microbiologia 29: 491-498.

VANBREUSEGBEM R., 1952 — Biological technique for the isolation of dermatophytes from soil.

Annales de la Société belge de médecine tropicale 32: 173

YOSEIEDA S., KASUGA S., HAYASFU N., USHROGUSTH T., NUTSURA H. & NAKA-

САМА S., 1987 — Antifungal activity of ajoene derived from garlic. Applied and environ-

mental microbiology 53: 615-617.

YOUSSEF Y. A., KARAM EL-DIN A. A. & MOHAMED А.,1989 — Survey of soil from human

pathogenic fungi from Ismailia Governorate. Egypt. 1. Isolation of keratinophilic fungi.

Mans. Sci. Bull. 16 (2): 153-163

YOUSSEF К. h. A., YOUSSEF Y. A. & YOUSSEF Н. H., 1980 — Fungi and thermophilic

actinomycetes in the air of the Cancer Institute hospital. Ain Shams scientific bulletin 22

(AB): 75-88

YU R. J, HLTRMON S. R. & BLANK Е, 1968 — Isolation and purification of extracellular

keratinase of T. mentagrophytes. Journal of bacteriology 96: 1435-1436.

ZOHARI A. A., KHAYRIA M. ABD AWAD & SABAH M. S., 1992 — Antibacterial,

antidermatophytic and antitoxigenic activities of onion (Allium cepa L.) oil. Second

Regional Mycological Conference RMC2 1 7-10 October, 1992, Abstract 94-95, University

of Al — Azhar, Cairo, Egypt.

Source : ММНМ, Paris

Source : MNHN. Paris

Cryptogamie, Mycol. 1996, 17 (3-4) : 187-188 187

ANALYSES BIBLIOGRAPHIQUES

BRAUN U. : The Powdery Mildews (Erysiphales) of Europe. Gustav Fischer Verlag, Jena,

Stuttgart, New York, 337 рр., 112 figures, 1995. ISBN 3-334-60994-4. Prix 98 DM.

L'ordre des Erysiphales rassemble les agents des oidiums ou blancs des végétaux, en anglais

powdery mildews’.

Ces parasites obligatoires se recensent sur plus d'un millier d'espèces végétales et provo-

quent des maladies souvent économiquement très importantes, telles que Poidium de la vigne, dû à

Uncinula necator. Le terme oidium dérive du genre Oidium proposé par Link en 1809, bien que la

description originale ne concernait aucun agent pathogene de ce groupe.

L'ouvrage sur les Erysiphales de l'Europe est une suite logique de l'importante monogra-

phie mondiale des Erysiphacées, proposée une dizaine d'années auparavant par le méme auteur. La

différence fondamentale entre ces deux traités est que le premier concerne exclusivement les plantes-

hótes européennes. Ce nouveau document reproduit donc, en partie, le contenu de cette monographie.

Toutefois, comme le souligne l'auteur, des données supplémentaires y ont été integrées, Elles concer-

nent surtout la diversité des plantes-hótes et leur répartition géographique. Ces informations repré-

sentent sans conteste : un apport interéssant à notre connaissance de la biodiversité de ce groupe. Plus

important, cet ouvrage devrait servir de stimulant pour des études floristiques élargies sur les

Erysiphales, en particulier, dans les pays européens pour lesquels les données disponibles sont trés

réduites.

Les premiers chapitres représentent un rappel des structures mycéliennes spécifiques des

Erysiphales et de leur téléomorphes ainsi que des critères majeurs utilisés dans la taxonomie de ce

groupe. L'auteur traite ensuite la biologie des Erysiphales, l'influence des facteurs externes sur leur

développement, la distribution géographique et les spectres des plantes-hótes. La position des

Erysiphales dans la classification générale des champignons est également abordée. A cet égard,

l'auteur favorise l'hypothése du maintien de cet ensemble dans une méme famille, les Erysiphaceae ; il

rejete donc la proposition de faire éclater ce groupe en trois familles, sur la base de différences

morphologiques mineures.

Aprés une analyse a un niveau global des particularités du groupe, la partie centrale de

l'ouvrage traite de la taxonomie des douze genres erysiphaléens. Cette partie propose une clef des

genres traités, suivie d'une clef des espéces considérées, regroupées par plante-hóte ; cette derniere

représente une excellente synthèse des informations d'ordre taxonomique et son utilisation s'avère

trés aisée.

Le reste de l'ouvrage est consacré à la desription des genres et des espèces affines. Ces

descriptions sont toujours accompagnées d'une synonymie compléte, des références bibliographiques

les plus importantes, des illustrations, des détails des exsiccata examinés, des cai ctéres morphologi-

ques, d'une fiche signalétique du spécimen type, enfin, des informations sur la distribution en Europe.

Ces parties descriptives sont identiques à celles publiées dans la monographie précédente. Ceci

explique la présence à la fin de certaines descriptions, d'un paragraphe intitulé énotes' et dans lequel

l'auteur développe des idées critiques résultant des travaux entretemps réalisés sur la systématique de

ces champignons. Le texte des paragraphes descriptifs est très soigné, concis et relativement clair.

Les derniers chapitres de l'ouvrage traitent successivement des anamorphes, des anamor-

phes de position incertaine et des espèces douteuses ou à exclure. La bibliographie est importante mais

ne parait pas exhaustive. Elle est suivie par un chapitre d'illustrations qui comportant soixante pages ;

ce sont surtout d'excellents dessins au trait. Le livre se termine par un index des plantes-hôtes et un

index des noms scientifiques des champignons considéré:

La présentation de cet ouvrage a regu un soin particulier. Le texte est reproduit sur deux

Source : MNHN, Paris

188 ANALYSES BIBLIOGRAPHIQUES

colonnes, ce qui permet une lecture aisée. On peut regretter que l'aire de répartition de chaque espèce

n'ait pas fait l'objet d'un regroupement sur une base géographique, plutót que sur les zones de culture

des plantes-hótes, comme ce fut le cas dans la monographie précédente. Ceci aurait permis un

repérage plus facile d'une information particulière. Le choix d'un second type de caractère pour ces

distributions aurait conduit à un gain de place assez appréciable.

En conclusion, il ne fait aucun doute que ce document de base sur ces pathogènes à

importance économique marquée, sera trés favorablement acceuilli par toutes les personnes interés-

sées par les aspects fondamentaux et appliqués des oidiums : mycologues, phytopathologistes,

horticulteurs, agriculteurs, agronomes et également des botanistes.

Jean Mouchacca

TAN C. S. Н, HOEKSTRA E. S. & SAMSON В. A. : Fungi that cause superficial

mycoses. ISBN 90-70351-23-4. Centraalbureau voor Schimmelcultures (P. O. Box 273,

3740 AG Baarn, Pays-Bas), en collaboration avec le Dr. Paul Janssen Medical Institute.

(Turnehoutseweg 30, B-2340 Beerse, Belgique), 108 pp, 1994.

Comme spécifié dans le titre, cet ouvrage traite exclusivement des champignons, au sens

large du terme, responsables de mycoses superficielles chez l'homme. Il est surtout destiné à un public

médical ou paramédical ayant des notions limité en mycologie. Son édition est le fruit d'une

collaboration fructeuse entre cet important centre de recherches néerlandais en mycologie qu'est le

CBS et l'institut Paul Janssen à vocation plus médicale.

C'est essentiellement un document descriptif technique de haut niveau, des pathogènes

responsables des mycoses superficielles les plus répandues. Son édition vient appuyer le cours de

mycologie médicale destiné au dermatologistes, délivré par les deux établissements,

Les champignons responsables des mycoses superficielles rassemblent tout d'abord, les vrais

dermatophytes appartenant aux genres Trichophyton, Microsporum et Epidermophyton. Sont égale-

ment traitées les dermatomycoses générées par quelques levures et champignons, surtout ceux réputés

keratinolytiques. Une troisième partie est consacrée au groupe des champignons saprophytes com-

puns, couramment isolés de nos jours, de peau, ongles ou cheveux déteriorés. Ces derniers rassem.

blent des levures et des champignons filamenteux non responsables de vrais dermatomycoses, mais

dont l'identification est indispensable afin d'exclure leur pathogénicité

Aprés une bréve introduction, on trouve quelques conseils sur les techniques d’échantillon-

nage des structures fongiques, les méthodes d'examen directe du matériel échantillonné et les

techniques de culture des pathogènes au laboratoire. La classification des champignons est abordée

avec l'appui de nombreux documents iconographiques. Pour chaque agent pathogène considéré, une

fiche descriptive fournit des informations sur la morphologie des cultures en bo "te de pétri, les

Structures mycéliennes et sporales et la distribution géographique, Chaque fiche est accompagnée de

dessins au trait et d'une page complète de photos en noir et blanc, illustrant l'aspect des colonies et les

Structures mycéliennes.

Cet ouvrage de format A4 est abondamment illustré de planches de photos, en noir et blanc,

d'une excellente qualité de reproduction. Les photos de microscopie photonique ou de balayage sont

très nettes et devraient permettre une comparaison rapide avec un matériel d'étude. Une petite série de

planches en couleur rassemblent des reproductions des colonies des vrais dermatophytes, son objectif.

étant de permettre une identification rapide par simple comparaison. Il reste à féliciter les trois

auteurs pour l'effort nécessaire à l'édition de cet ouvrage dont la diffusion dans le monde médical est

assurée par avance.

Jean Mouchacca

Source - MNHN, pod

Cryptogamie, Mycol. 1996, 17 (3-4) : 189-190

TABLE DU TOME 17

ALBERTO E. — voir MORENO G.

ALTÉS A., MORENO G. & WRIGHT J. E. — New data on Tulostoma Ri Дад (Gas-

derómycetes) eec acer oe ens АД. D

BETTUCHI L. — voir CORREA A.

BOUTEVILLE R. J. — voir NEZZAR-HOCINE H.

BUYCK B. — voir VERBEKEN A

CHEVALIER G. voir NEZZAR-HOCINE H

CORREA A., ROQUEBERT M. F. & BETTUCHI L. — Trichorzianins activity on mycelial

growth of Sclerotium cepivorum under laboratory conditions in vitro ............

DURRIEU G. — Invasion de Microsphaeria vanbruntiana var. sambuci-racemosae para-

site de Sambucus racemosa en France et en Espagne ....................... ~

EL-SAÍD A. H. M. — Isolation of fungi from human hair samples collected in El-Bahrin

and the antifungal activity of various shampoos ..…..................... ,

ERBAWY Y. A. M. H. — Keratinolytic and keratinophilic fungi of swamp's soil and air

in Qena city and their response to garlic extract and onion oil treatments .......

GRACIA E., ILLANA C. & MORENO С. — Enteridium rubiginosum sp. nov., а new

Myxomycetes from $райп............. Mu NE M ЕЧ ы

HALLI-HARGAS R. — voir NEZZAR-HOCINE H.

HASAN H. A. H. Destruction of aflatoxin Bl on sorghum grain with acids, salts and

ammonia derivatives . . AP NA M reso RL 5

ILLANA C. — voir GRACIA E.

JOB D. — Environmental growth requirements for submerged cultures of the ecto

myccorhizal fungus Сепососсит geophilum Fr...

LANQUETIN P. — voir LEGER J. C.

LEGER J. C. & LANQUETIN P. — Contribution à l'étude des caractéres culturaux chez

les Hymenochaetaceae (Basidiomycotina) он

189

139

173

129

165

105

Source : MNHN, Paris

190 TABLE DU TOME 17

MANDEEL Q. A. — Survey of Fusarium species in an arid environment of Bahrain.

IV — Prevalence of Fusarium species in various soil groups using several isolation

techniques. . ..... 149

MORELET M. & SIGAUD P. — Observations on a poplar leaf infection occuring in

north-east China : the grey spot disease ......................... п

MORENO С. — voir GRACIA Е.

MORENO С. — voir ALTES A.

MORENO G. & ALBERTO E. — Agaricales sensu lato de Argentina 1............. жа

NEZZAR-HOCINE H., BOUTEVILLE К. J., HALLI-HARGAS К. & CHEVALIER С.

La macroflore fongique de Cedrus atlantica (Endl.) Manetti ex Carrière. I — Inven-

taire des espèces d'une cédraie du massif du Djurjura (Algérie) et connaissances

acvtuelles sur les champignons des cédraies ................................. 85

OLUFOLAJI D. В. — Effects of some fungicides on germination, growth and sporulation

of Curvularia cymbopogonis ................ ER UAE MAN MN 7

RAYNAL С. — Présence en France de Claviceps paspali Stev. et Hall sur Paspalum disti-

chum L. et de Vergotisme correspondant sur le bétail... ..................... 21

ROQUEBERT M. Е — voir CORREA A.

SIGAUD P. — voir MORELET M

VERBEKEN A., BUYCK B & WALLEYN R. — Lentinus clitocyboides Hennings is

а Russula..

WALLEYN R. — voir VERBEKEN A.

WRIGHT J. E. — voir ALTÉS A.

Analyses bibliographiques . . е хе ы EE вар, ЕКО 187.

пына ы auteurs TL е ра ри ии 57

Source : MNHN. Paris

Commission paritaire 16-1-1986 - N° 58611 - Dépôt légal 1“ trimestre 1997 - Imprimerie Е Paillart

"Sortie des presses le 21 février 1997 - Imprimé en France

Éditeur : A.D.A.C. (Association des Amis des Cryptogames)

Président : D. Lamy; Secrétaire : B. Dennétiére

Trésorier : E. Bury: Directeur de la publication : H. Causse

Source : MNHN. Paris

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Biosystema 1 - Introduction à la systématique zoologique - (Concepts. Principes, Méthodes) par

L. Matile, P. Tassy & D. Goujet. 1987.

Biosystema 2 - Systématique Cladistique - Quelques textes fondamentaux. Glossaire. Traduction

et adaptation de D. Goujet, L. Matile, P. Janvier & J.P. Hugot. 1988

Biosystema 3 - La systématique et l'évolution de Lamarck aux théoriciens modernes, par

S. Lovtrup. 1988.

Biosystema 4 - L'analyse cladistique: probléme et solutions heuristiques informatisées, par

M. d'Udekem-Gevers. 1990.

Biosystema 5 - Les introuvables de J.B. Lamarck- Discours d'ouverture du cours de zoologie et

articles du Dictionnaire d'Histoire naturelle. Edition préparée par D. Goujet. 1990.

Biosystema 6 - Systématique et Ecologie, par R. Barbault, Cl. Combes, F. Renaud, N. Le Brun

& A. Dubois. Edition coordonnée par J.P. Hugot. 1991.

Biosystema 7 - Systématique et Biogéographie Historique. Textes historiques et

méthodologiques. Traduction et adaptation de P. Janvier, L. Matile & Th. Bourgoin.

1991.

Biosystema 8 - Systématique et Société. Edition coordonnée par С. Pasteur. 1993.

Biosystema 9 - Les Monocotylédones, par J. Mathez. 1993.

Biosystema 10 - Systématique botanique : problèmes actuels. Edition coordonnée par O. Poncy.

1993.

Biosystema 11 - Systématique et Phylogénie: modèles d'évolution biologique. Edition

coordonnée par P. Tassy et H. Lelièvre. 1994.

Biosystema 12 - Phylsyst: logiciel de reconstruction phylogénétique, par 1. Bichindaritz,

5. Potter & В. Sigwalt +. 1994

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Biosystema 14 - Systématique et Informatique. Edition coordonnée par J. Lebbe, en préparation.

Le Conseil de la SFS. ХП 1995

Source : MNHN, Paris