1. On certain species of Mucor with a key to all accepted species

M. A. A. SCHIPPER
Centraalbureau voor Schimmelcultures, Baarn.

 

Summary

Treated are all species of Mucor known in culture and not discussed in three earlier papers (Schipper, 1973, 1975, 1976). Described are 21 species and varieties, four of which are new taxa (Mucor amphibiorum, M. tuberculisporus, M. variosporus, M. zychae var. linnemanniae) and one is validated (M. prayagensis). The rather unusual results of interspecific contrasts in the described taxa are discussed in connection with literature data. A key is given to all accepted Mucor species, varieties and formae; 49 taxa are considered.

 

Introduction

In this last of a series of four papers dealing with the genus Mucor, the taxa not considered earlier are discussed. In the previous papers (Schipper, 1973, 1975, 1976) the species belonging to more or less natural groups have been described. In the first paper Mucor hiemalis and its relatives were treated, in the second M. mucedo, M. flavus and some similar taxa and in the third M. circinelloides, M. racemosus and related species. The species to be treated below have only few characters in common.
All strains under study grow and sporulate well at 25°C. Temperatures below 15°C are often rather unfavourable for the development, at 5°C no growth is observed in the great majority of the studied species. Few grow and sporulate at 37°C and 40°C; 45°C is over the maximum for all. Most of the species are indifferent or nearly so to increased sugar concentration (4% beerwort agar/4% beerwortagar + 20% saccharose).
Colonies are composed of one region of fruiting only. Sporangiophores are unbranched or, infrequently, once branched and tend to collapse rather soon, with the exception of M. indicus, which forms repeatedly branched sporangiophores.
Borne erect, the young sporangiophore may recurve during the development of the sporangium, straightening after its maturation (Fig. 1b). The curvature of the young sporangiophore appears to be independent of light and gravity: simultaneous cultures grown in continuous darkness, in light 12/12 h and upside down with or without bottom light, all showed the same type of recurvature. A few species with [p. 2] this character, may show some short, slender, permanently recurved branches bearing sporangiola in ageing cultures (Fig. 1a). This feature might indicate a rather close relationship to Backusella Hesseltine & Ellis. [p. 3]

 fig. 1

Fig. 1
a. permanently recurved branch bearing sporangiola in ageing culture (Mucor recurvus var. indica); b. transitory recurvature of young sporangiophore (Mucor recurvus var. recurvus); c. repeatedly sympodial short circinate branches which each bear a small, sterile sporangium (Mucor odoratus); d. repeatedly sympodial short sterile branches (Mucor falcatus).

A rather unusual branching pattern results when the main stalk of the sporangiophore bends aside in a young stage, remaining short and sterile, and subsequently the first lateral branch takes its place. The new main stalk may grow tall, bearing a sporangium, or the branching is repeated in the same way (Fig. 1d). Occasionally the sporangiophore consists of repeatedly sympodial, short, circinate branches which each usually bear a small and mostly sterile sporangium (Fig. 1c) and a long top branch with a fertile sporangium. Sporangiophores may be borne in small groups on a common base.
Sporangia usually turn from glistening-moist into vitreous in appearance; the mature sporangia vary from pale yellowish to golden yellow or yellowish brown, except in the dark coloured M. mousanensis and M. ucrainicus. Conical columellae can be found in most of the species, either as the principal form or as a secondary form; often the columellae have golden yellow, yellowish-brown or brown contents. The sporangiospores have yellowish to bright yellow, granular contents, either diffuse or concentrated in the centre.
Although the species have above features more or less in common, they do not form a clearly delimited group. Some subgroups may, however, be distinguished. Mucor tuberculisporus, M. oblongiellipticus, M. recurvus and M. variabilis all have conical columellae with coloured contents and a fringe of needle-shaped spines at the base. Transitory recurvature of the sporangiophores is common feature in M. tuberculisporus, M. oblongiellipticus and M. recurvus. Ellipsoidal sporangiospores with yellow granular contents are produced in M. oblongiellipticus, M. recurvus and M. variabilis,
Since only a single strain or a limited number of strains are known for most of the species discussed below, specific variability could not be determined. With this limitation in mind, reserve was practised to avoid probably hasty conclusions concerning synonymy.

 

Descriptions 

1. Mucor guilliermondii Nadson & Philippov - Fig. 2

Mucor guilliermondii Nadson & Phillipov - Revue gén. Bot 37: 450. 1925.

The following description is of CBS 174.27, on beerwort agar at 20°C in daylight.
Colony up to 15 mm in height, radial growth 40 mm in 5 days, white, Pale Gull Gray, with pale yellowish reverse, slightly aromatic; sporangiophores up to 7 µm in diam, erect or transistorily recurved when young, soon collapsing, unbranched, rarely with a lateral branch; sporangia hyaline with a touch of yellowish-brown, vitreous in aspect, occasionally up to 60 µm in diam, but mostly much smaller, with deliquescent, transparent walls; columellae elongated-conical, few ellipsoidal to globose, up to 25 x 13 µm, mostly much smaller, hyaline, with extremely small collars or none; sporangiospores in young cultures ellipsoidal, 4.4-5.4 x 1.7-2 µm, hyaline, usually [p. 4] with a droplet at each end, in ageing cultures reniform, triangular and larger ellipsoidal sporangiospores up to 8 x 2.7 µm are also present; substrate mycelium up to 25 µm in diam, filled with droplets, chlamydospores occur; zygospores unknown.
Influence of temperature: at 37°C. no growth; at 30 - 10°C growth at sporulation; at 5°C no growth.
Influence of light: insignificant.
Influence of medium: on beerwort agar + 20% saccharose good growth and sporulation, young sporangiophores recurved. On all media tested, including horse-dung, the columellae kept their conical shape.

 fig. 2

Fig. 2
Mucor guilliermondii, CBS 174.27
a. columellae; b. sporangiospores


Material examined

CBS 174.27 (-), type strain.


Discussion

Zycha (1935) treated Mucor guilliermondii as a synonym of M. subtilissimus Oudem. The almost obclavate columellae in M. guilliermondii (Fig. 2b), however, are hard to reconcile with the columellae in M. subtilissimus, which were described by Oudemans (1898) as being globose. Otherwise the neotype of Mucor subtilissimus, CBS 735.70, is very similar to CBS 174.27.

 

2. Mucor subtilissimus Oudem. - Fig. 3

Mucor subtilissimus Oudem. - Ned. Kruidk. Archf 3: 463. 1898.

The following description is of CBS 735.70 on beerwort agar at 20°C in daylight.
Colony up to 24 mm in height, radial growth 90 mm in 5 days, Pale Gull Gray, with pale yellowish reverse, slightly aromatic; sporangiophores up to 10 µm in diam, constricted next to young sporangia, infrequently swollen, sparsely branched, limp [p. 5] and soon collapsing, sometimes giving rise to peripherial sporangial colonies, with slightly incrusted walls, pallid mouse grey; sporangia hyaline or with a yellowish tinge and vitreous in aspect, globose to slightly flattened, up to 70 µm in diam, with transparent diffluent walls; columellae globose to subglobose, up to 33 µm in diam, infrequently ellipsoidal up to 42 x 35 µm, with small collars; sporangiospores ellipsoidal, mostly 5.4 x 2.5 µm (4-8 x 2-3.5 µm), usually with a granule at each end; substrate hyphae irregular in width, up to 30 µm, filled with droplets, chlamydospores may occur; zygospores unknown.

 fig. 3

Fig. 3
Mucor subtilissimus, CBS 735.70
a. columellae; b. sporangiospores

Influence of temperature: at 37°C no growth; at 30-10°C growth and sporulation, though slow at 10°C; at 5°C no growth.
Influence of light: insignificant.


Material examined

CBS 735.70 (-) = NRRL 1909, neotype, isolated from soil, Wisconsin, USA.


Discussion

Oudeman's original strain is lost. Schipper (1973) regarded the species as doubtful because of the absence of either authentic material or a culture fully fitting the original description. Since the characters in Oudeman's description are rather close to those of CBS 735.70, the discrepancies in size range possibly being due to the influence of environmental conditions, the strain CBS 735.70 is proposed here as neotype of Mucor subtilissimus. [p. 6]

 

3. Mucor bacilliformis Hesseltine - Fig. 4

Mucor bacilliformis Hesseltine - Mycologia 46: 360. 1954.

The following description is of CBS 251.53, on beerwort agar at 20°C, in daylight.
Colony up to 16 mm in height, radial growth 70 mm in 5 days, Pale Smoke Gray, with slightly yellowish reverse, faintly aromatic; sporangiophores up to 8 µm in diam, unbranched at first, then tardily branched in a sympodial fashion, branches with wide bases (Fig. 4b); sporangia pale yellowish tan, vitreous in aspect, up to 50 µm in diam, with slightly translucent, deliquescent walls; columellae applanate, globose or broadly ellipsoidal, up to 30 µm in diam but mostly much smaller, rarely larger, collar poorly defined or absent; sporangiospores bacilliform, usually slightly recurved to reniform, 4-4.7 x 1-1.3 (6.5 x 1.6) µm, with a granule at each end; substrate hyphae growing deep down into the agar, giant cells filled with droplets and up to 60 µm in diam, chlamydospores and oidia present; zygospores homothallic, formed at a short distance above the substrate on zygophores which are shorter than the sporangiophores, black, globose or nearly so, roughened by broad projections which are often brushlike in outline, up to 80 x 77 µm and infrequently double azygospores occur; suspensors straight, equal or nearly so, enlarging toward the zygospores.
Influence of temperature: at 30°C no growth; at 25-10°C growth and sporulation, both sexual and asexual, but at 10°C development is very slow; at 5 °C extremely slow growth, no sporulation.
Influence of light: Cultures grown in light produced abundant sporangia and few zygospores; simultaneous cultures grown in darkness produced abundant zygospores and few sporangia. Cultures grown at 25°C in light produced incompletely developed zygospores, in darkness at 25°C zygospores were better developed; at 20-17°C no influence of light on maturation of zygospores was observed. [p. 7]

 fig. 4

Fig. 4
Mucor bacilliformis, CBS 251.53
a. columellae; b. sporangiospores; c. zygospore between suspensors.


Material examined

CBS 251.53, type strain.
CBS 573.70, received from H. Naganishi (Naganishi et al., 1969).


Discussion

Compared with the type strain, CBS 573.70 is more vigorous in radial growth and zygospore production. Giant cells are rarely found. The sporangiospores are usually straight and 3.3-4 x 1 (5 x 1.3) µm in size. Zygospores formed near the substrate are up to 105 x 95 µm, while higher in the aerial mycelium small zygospores of 30 x 25 µm are found.

 

4. Mucor microsporus Namyslowski - Fig. 5

Mucor microsporus Namyslowski - Bull. int. Acad. Sci. Lett. Cracovie, sér. B. Sci. nat. p. 517. 1910.
Mucor cylindrosporus Ling - Revue gén. Bot. 42: 731. 1930.

The following description is of CBS 204.28, on beerwort agar at 20°C in daylight.
Colony usually 3-4 mm in height, though occasionally up to 23 mm, radial growth 55 mm in 9 days, Pale Pinkish Buff, slightly odorous; marginal colonies occur; sporangiophores up to 10 (-15) µm in diam, unbranched, with slightly roughened walls, mouse grey; aberrations that occur in the sporangiophore are torsion, irregular width, swelling and/or constriction next to the columella; sporangia yellowish-hyaline when young, later yellowish-brown and vitreous in aspect or, infrequently, [p. 8] sand colour and powdery in aspect, up to 80 (-100) µm in diam, with slightly trans-parent, incrusted diffluent walls; columellae obovoid to ellipsoidal, infrequently tending to pyriform, the smallest globose, up to 70 x 55 (80 x 65) µm, with yellowish or reddish-brown contents, each with a small collar or just a line of attachment; sporangiospores cylindrical-ellipsoidal, 3.4-5.4 x 2-3 µm; zygospores unknown.
Influence of temperature: at 30°C no growth; at 25-5°C growth and sporulation, rate of development decreasing with lower temperatures, extremely slow at 5°C.
Influence of light: insignificant.
Influence of medium: colonies grow more rapidly on beerwort agar than on PCA, YEA, hay infusion agar, 2% beerwort agar or beerwort agar + 20% saccharose. Swelling of the sporangiophores seemed to be stimulated by increased sugar content of the medium.

 fig. 5

Fig. 5
Mucor microsporus, CBS 204.28
a. columellae; b. sporangiospores.


Material examined

CBS 204.28, type strain of M. cylindrosporus.
CBS 245.35, received from H. Zycha, isolated from soil, Bockstein, Salzburg (Zycha, 1935).


Discussion

Radial growth of CBS 204.28 is slow and few marginal colonies occur, whereas growth of CBS 245.35 is even slower and consequently sporangial colonies are more abundant. The sporangiospores in CBS 245.35 are mostly 3 x 2.5 µm.
When Dyr (1940) described Mucor bohemicus, he regarded it to be quite close to M. microsporus. The description is rather brief, without illustrations. As no type strain is available, its position is uncertain.

 

5. Mucor indicus Lendner - Fig. 6

Mucor indicus Lendner - Bull. Soc. bot. Genève 21: 258. 1930.

Misapplied name:
Mucor rouxii (Calmette) Wehmer sensu Wehmer - Zentbl. Bakt. ParasitKde. Abt. 2, 6: 364. 1900 = Mucor rouxianus (Calmette) Wehmer - Zentbl. Bakt. ParasitKde, Abt. 2, 6: 357. 1900 (name change; incidentally mentioned).

The following description is of CBS 226.29, on beerwort agar at 20°C in daylight.
Colony up to 10 mm in height, Warm Buff to Antimony Yellow, with Buff Yellow to Apricot Yellow reverse, aromatic; sporangiophores up to 14 µm in diam, repeatedly branched sympodially with long branches, with or without yellowish-brown contents; sporangia at first golden yellow, later with a brownish, vitreous aspect, up to 75 µm in diam, av. 40-50 µm in diam, with diffluent, transparent walls; columellae [p. 9] applanate, subglobose, rarely elongated, up to 56 x 53 µm, pallid mouse grey, infrequently with reddish-brown contents, collars small or just a line of attachment; sporangiospores subglobose to cylindrical-ellipsoidal, 5.4-5.7 x 4.4. µm, with granular contents; zygospores (CBS 226.29 (+) x CBS 422.71 (-), on beerwort agar, at 25°C) in the aerial mycelium, most abundant in the underportion of the colony, black, globose to slightly compressed, up to 100 µm in diam (including rather pointed stellate projections up to 10 (-14) µm in length), single or double azygospores may occur; suspensors unequal, one very short, the other swollen but constricted adjacent to the zygospore, up to 35 µm in diam, with reddish-brown contents.

 fig. 6

Fig. 6
Mucor indicus, CBS 226.29
a. sporangiophore; b. columellae; c. sporangiospores.

Influence of temperature: at 45°C no growth; at 40°C growth, no sporulation; between 37-25°C good growth and sporulation, optimal at 30°C; at 20°C growth, rather poor sporulation; between 15-10°C slow growth, no sporulation; at 5°C no growth. At 30°C (in light), the colony colour is Avellaneous to Deep Olive-Buff and abundant repeatedly branched sporangiophores are produced, sporangiospores are ellipsoidal to cylindrical-ellipsoidal, 5.4-6.4 x 3.8-4.8 µm, av. 5.4 x 4 µm.
Influence of light: cultures grown in darkness at 20°C are Light Buff in colour (production of yellow pigment being considerably reduced) and produce sterile mycelium; sporangiophores unbranched or branched once or twice, sometimes with swellings (failed sporangial development); columellae globose to applanate, up to 35 (-45) µm in diam; sporangiospores ellipsoidal to globose; chlamydospores abundant in substrate hyphae. [p. 10]


Material examined

CBS 120.08 (+), received as M. rouxii, most probably from C. Wehmer.
CBS 226.29 (+), type strain.
CBS 480.70B (+) = ATCC 4855 and CBS 480.70C (+) = ATCC 4857, received as M. rouxii, originating from Blakeslee's collection sub C 1067 and C 980 respectively.
CBS 422.71 (-), isolated from Pachyrhizus erosus by I. Gandjar. Indonesia.
CBS 423.71 (-), isolated from dustheap by I. Gandjar, Indonesia.
CBS 424.71 (-), isolated from decaying peanut by I. Gandjar, Indonesia.


Discussion

The type strain of Mucor indicus, CBS 226.29. was studied under various environmental conditions. Grown at temperatures below 20°C, sporulation was poor; it then resembled CBS 120.08 by producing few unbranched or weakly branched sporangiophores, some abortive sporangia and much sterile mycelium. At higher temperatures CBS 226.29 sporulated much more profusely than CBS 120.08, and sporangiophores were repeatedly branched.
Wehmer (1900) claimed to have verified the identity of his strain by comparing it to Calmette's (1892) Amylomyces rouxii and thus considered A. rouxii Calmette to be a species of Mucor. Calmette's strain is now lost. Ellis et al. (1976) indicated CBS 438.76 as neotype of Amylomyces rouxii; this strain differs conspicuously from CBS 120.08 and it cannot be classified in Mucor. Consequently the name Mucor rouxii (Calmette) Wehmer is no longer available for the species represented by CBS 120.08. In view of the above, CBS 120.08 is considered to be a poorly developed strain of Mucor indicus.
CBS 128.08 was sent to A.F. Blakeslee in 1928, and to several other workers. CBS 120.08, 480.70B and 480.70C are much alike and they are possibly subcultures of a single isolate. The colonies are yellowish under all conditions; few, unbranched or weakly branched sporangiophores and much sterile mycelium were produced. CBS 120.08 does not survive a year's storage at 5°C. CBS 422.71, 423.71 and 424.71 produce well developed colonies at 20°C and at 15°C sporulation is poor. These strains produce abundant chlamydospores in sporangiophores and substrate hyphae. All strains studied produced zygospores in matings with 226.29 (+) or CBS 422.71 (-), on beerwort agar at 25°C.
Occasionally strains of M. indicus and M. circinelloides are rather similar. A second region of profusely branched short sporangiophores was never observed in M. indicus, whereas it is often present in M. circinelloides. Globose columellae predominate in M. indicus, obovoid ones being rare, whereas in M. circinelloides obovoid columellae are most common. Mucor indicus shows good growth and sporulation at 37°C, whereas M. circinelloides is extremely poor at that temperature. According to Naganishi & Hirahara (1966), M. indicus requires vitamin B1, while M. circinelloides does not. [p. 11]

 

6. Mucor variosporus Schipper, nom. nov. - Fig. 7

Mucor luteus Linnemann var. indica Baijal & Mehrotra - Sydowia 19: 206. 1965: non Mucor indicus Lendner - Bull. Soc. bot. Geneve 21: 258. 1930.

The following description is of CBS 837.70, on beerwort agar at 20°C in daylight.
Colony up to 20 (-30) mm in height, Cream Buff to Chamois, with Buff-Yellow reverse, slightly aromatic; sporangiophores up to 14 (-23) µm in diam, erect, later collapsing, sometimes giving rise to peripheral sporangial colonies, unbranched or once branched, with or without yellowish to reddish-brown contents; sporangia yellow, vitreous in aspect, up to 150 µm in diam, with deliquescent, transparent, slightly encrusted walls; columellae ellipsoidal-obovoid or globose, up to 72 x 60 µm or 70 µm in diam, with or without yellowish-brown contents, collars poorly defined or absent; sporangiospores variable in shape and size, oblong ellipsoidal, ellipsoidal, planoconvex, a few globose, 5.5-13.5 x 3.5-8 µm, rarely larger, pale yellowish and with granular contents; substrate hyphae with yellowish contents; giant cells up to 60 µm in diam may occur; zygospores unknown.

 fig. 7

Fig. 7
Mucor variosporus, CBS 837.70
a. columellae; b. sporangiospores. [p. 12].

Influence of temperature: at 37°C no growth; at 30-15°C growth and sporulation, optimal at 30°C, rather poor sporulation at 15°C; at 10°C growth, no sporulation; at 5°C no growth. One-year storage at 5°C proved to be undesirable.
Influence of light: cultures grown in darkness are slightly paler and inclined to produce sterile mycelium.


Material examined

CBS 837.70 (-), type strain.


Discussion

CBS 837.70 differs from M. hiemalis Wehmer f. luteus (Linnemann) Schipper in many respects. Under standard conditions, the type strain of the latter produces sporangia up to 70 µm in diam, globose columellae and narrow-ellipsoidal sporangiospores 3.3-9.5 x 1.4-4 µm. Furthermore, between 25 and 5°C sporulating colonies are produced, at 30°C growth is stunted and no sporulation occurs.

 

7. Mucor inaequisporus Dade - Fig. 8

Mucor inaequisporus Dade - Trans Br. mycol. Soc. 21: 25. 1937.
Mucor inaequisporus Dade f. kaki Naganishi & Hirahara - Essays and Studies, Hiroshima Jogakuin College 16: 117. 1966.

The following description is of CBS 255.36, on beerwort agar at 20°C in daylight.
Colony up to 30 mm in height, Light Cadmium to Aniline Yellow with Apricot Yellow reverse, aromatic, slightly folded substrate; sporangiophores up to 18 (-30) µm in diam, with quite broad short bases, unbranched, though sympodial branches may occur, with or without yellowish contents, with slightly encrusted pallid mouse grey walls, in ageing cultures several septa may be found; sporangial development only starts after rather considerable elongation of the young sporangiophore, collapsing sporangiophores may give rise to sporangial colonies; sporangia golden yellow at first, later orange-brown, vitreous in aspect, up to 150 (-175) µm in diam, with transparent diffluent walls, occasionally sporangiospores may germinate within the sporangium; columellae obovoid-pyriform or subglobose, the smaller ones infrequently conical to applanate, up to 83 x 75 µm, pallid mouse grey, with or without reddish-brown contents and with small collars; sporangiospores extremely variable in size and shape, the smaller ones ellipsoidal, approx. 5-7 x 3-4 µm, the larger ones ellipsoidal to globose, yellowish, up to 30 x 23 µm or 12-18 µm in diam, with granular contents; zygospores (CBS 255.36 (-) x CBS 496.66 (+) on beerwort agar at 25°C) in the aerial mycelium, most abundant in the lower part of the colony, [p. 13] black, globose to slightly compressed, up to 80 x 75 (100 x 85) µm, projections up to 3(-5) µm in length included; suspensors unequal, one very short, the other swollen but constricted next to the zygospore, up to 35 µm in diam, with reddish-brown contents.
Influence of temperature: at 37-30°C no growth; at 25-10°C growth and sporulation, but at 10°C abnormal; at 5°C no growth. A one year storage at 5°C is unsuitable.
Influence of light: cultures grown in darkness are Chamois, tinged orange and inclined to produce sterile mycelium.

 fig. 8

Fig. 8
Mucor inaequisporus, CBS 255.36
a. columellae; b. sporangiospores.


Material examined

CBS 255.36 (-), type strain of M. inaequisporus.
CBS 351.50 (-), strain 5/50 KB. Boedijn and J. Reitsma (Boedijn, 1958).
CBS 496.66 (+) and CBS 497.66 (-) received as M. inaequisporus f. kaki from H. Naganishi (Hirahara & Naganishi, 1965; Naganishi & Hirahara, 1966).


Discussion

The following deviations from the above described pattern were observed: the height of the colony may vary from 10 to 30 (-40) mm; CBS 351.50, 496.66 and 497.66 are Avellaneous; a folded substrate was only seen in CBS 255.36; sporangial [p. 14] formation may start on rather short sporangiophores; CBS 496.66 and 497.66 have pale brown sporangia; if CBS 496.66 is grown in darkness (20°C) some sporangia are powdery in aspect; in CBS 351.50, 496.66 and 497.66 columellae have a truncate base; in CBS 496.66 sporangiospores are rather small; CBS 496.66 and 497.66 grow and sporulate at 30°C, of the 4 strains only CBS 351.50 survives one year storage at 5°C; in CBS 351.50, 496.66 and 497.66 colonies grown in darkness are only slightly paler than those grown in daylight.
The studied strains produce zygospores in matings with CBS 496.66 (+) or CBS 497.66 (-), the chosen tester pair, on beerwort agar at 25°C.

 

8. Mucor amphibiorum Schipper, sp. nov. - Fig. 9

Coloniae in agaro maltoso 20°C dilute brunneo-griseae; sporangiophora ad 20 µm lata, plerumque simplicia: sporangia fusca, ad 100 µm diam; columellae ellipsoideae, ad 60 x 50 µm, collari exiguo circumdatae; sporangiosporae globosae, 3.4-5.4 µm diam; zygosporae atra, protuberantiis stellaribus obtectae, ad 70 µm diam. Crescit et sporulat temperaturis inter 10 et 30°C.
Typus: CBS 763.74, isolatus ex organis internis amphibiorum ex Australia.

 fig. 9

Fig. 9
Mucor amphibiorum, CBS 763.74
a. sporangiophore; b. columellae; c. sporangiospores; d. zygospores between suspensors (CBS 763.74 x 185.77).

The following description is of CBS 763.74, on beerwort agar at 20°C in daylight.
Colony up to 25 mm in height, Pale Smoke Gray, with pale yellowish reverse, slightly aromatic; sporangiophores up to 20 µm in width, unbranched, rarely sympodially [p. 15] branched, weak and soon drooping; sporangial development only starts after rather considerable elongation of the young sporangiophore; sporangia pale yellowish at first, then dark brown, vitreous is aspect, up to 75 (-100) µm in diam, slightly flattened; columellae cylindrical-ellipsoidal, sometimes tending to pyriform, the smaller ones infrequently conical, up to 60 x 50 µm, rarely larger, pallid mouse grey. with or without yellowish contents and with small collars; sporangiospores globose, 3.4-5.4 µm in diam, with slightly granular contents; zygospores (CBS 763.74 (+) x CBS 185.77 (-) on beerwort agar at 25°C) in the aerial mycelium, most abundant in the lower part of the colony, black, globose to slightly compressed, up to 70 x 60 µm, stellate projections up to 7 µm in length included; suspensors with yellowish contents, unequal: one very short, the other swollen but constricted next to the zygospore.
Influence of temperature: at 37°C no growth; at 30-10°C growth and sporulation, rate of development decreasing with a drop in temperature, extremely slow at 10°C; at 5°C no or negligable growth.
Influence of light: colonies grown in darkness are Pale Gull Gray; sporangiophores with several septa, infrequently with chlamydospores, present; sporangia blackish-brown.
Influence of medium: as cultures grown on beerwort agar show rather slow radial growth and often sporulate poorly, the strain was grown on a variety of other media. Beerwort agar proved to be more suitable than Ypps, PDA, cornmeal or cherry agar; Czapek agar was unsuitable.


Material examined

CBS 763.74 (+), CBS 764.74 (+), CBS 765.74 (+) and CBS 766.74 (+), received from H. J. Scholer sub M 239, M 240, M 241, M 243, isolated from Amphibians, imported from Australia by one and the same animal dealer (Frank et al.. 1974).
CBS 185.77 (-), received from H. J. Scholer sub D4135 = W. Frank 760'565 = U. Roester 8626, isolated from a diseased Poison Arrow Frog (Dendrobates spec.), recently imported from Central America.


Discussion

In CBS 185.77 sporangia are almost black and slightly powdery in aspect; sporangiospores rarely over 4.5 µm in diam.
The available (+) strains produced zygospores in matings with the only (-) strain on beerwort agar at 25°C. The chosen testerpair is: CBS 763.74 (+) and CBS 185.77 (-). [p. 16]

 

9. Mucor prayagensis B. S. Mehrotra & Nand ex Schipper, sp. nov. - Fig. 10

Mucor prayagensis B. S. Mehrotra & Nand in B. S. Mehrotra - Final techn. Rep.. p. 31. 1976 (without Latin diagnosis).

Coloniae in agaro maltose 20°C griseo-albae: sporangiophora ad 15 µm lata, plerumque simplicia; sporangia flavida, ad 75 µm diam, paries deliquescens et transparens: columellae subglobosae ad applanatae, ad 39 x 43 µm , collari minutissimo vel nullo circumdatae: sporangiosporae ellipsoideae, 7-15.5 x 4.0-6.8 µm; zygosporae ignotae. Crescit et sporulat temperaturis inter 10 et 40°C.
Typus: CBS 816.70, isolatus e terra, Bogana prope Ghazipur in India, a B. S. Mehrotra & Nand (1967).

The following description is of CBS 816.70, on beerwort agar at 20°C in daylight.
Colony up to 17 mm in height, greyish white to Pale Smoke Gray, reverse slightly yellowish, radial growth rather slow; sporangiophores up to 10 (-15) µm in width, erect, later collapsing and thus initiating sporangial colonies around the periphery of the parent colony, usually unbranched, sporangia yellowish, vitreous in aspect, up to 60 (-75) µm in diam, with deliquescent, transparent walls; columellae subglobose to applanate, up to 39 x 43 µm , with or without yellowish-brown contents; collars minuscule or absent; sporangiospores variable in shape, ellipsoidal or flattened at one side (7-) 9.5-12.3 (-515-5) x 4-5.4 (-6.8) µm, greyish, with granular contents; substrate hyphae with yellowish-brown contents: zygospores unknown.
Influence of temperature: at 40-10°C growth and sporulation; at 30°C colony tending to appricot yellow, reverse yolk yellow, at 25°C sporangia golden yellow to brownish-yellow; at 15-10°C slow to very slow development; at 5°C no growth.
Influence of light: insignificant.
Influence of medium: on beerwort agar + 20% saccharose good growth and sporulation were observed.

 fig. 10

Fig. 10
Mucor prayagensis, CBS 816.70
a. columellae; b. sporangiospores. [p. 17].


Material examined

CBS 816.70 (+), type strain.

 

10. Mucor variabilis Sarbhoy - Fig. 11

Mucor variabilis Sarbhoy - Trans. Br. mycol. Soc. 48: 559. 1965.

The following description is of CBS 564.66, on beerwort agar at 20°C in daylight.
Colony up to 20 mm in height, Light Ochraceous-Buff, with Antimony Yellow reverse; sporangiophores up to 14 (-20) µm in diam, unbranched, rarely sympodially [p. 18] branched, with or without yellowish-brown contents; sporangia yellowish, vitreous in aspect, up to 100 (-125) µm in diam, with encrusted, deliquescent walls; columellae applanate conical or cylindrical, up to 70 x 75 (85 x 100) µm, with or without reddish-brown contents, with small collars mainly consisting of short, needle-shaped crystals; sporangiospores ellipsoidal, (9.1-) 10.8-15.2 (-18.9) x (6.4-) 7.1-9.1 (-10.8) µm, yellowish or with golden yellow droplets in the centre; substrate hyphae irregular in diam, locally swollen up to 50 µm, filled with droplets.
Influence of temperature: at 40-15°C growth and sporulation, though at 40 and 37°C several sporangiospores are subglobose or bizarre in shape and at 15°C development is retarded; at 10°C no growth.
Influence of light: cultures grown in darkness are slightly paler and their development is slightly retarded.

 fig. 11

Fig. 11
Mucor variabilis, CBS 564.66
a. columellae; b. sporangiospores.


Material examined

CBS 564.66 (-), type strain.

 

11. Mucor recurvus Butler var. recurvus - Fig. 12, 13, 1b

(?) Mucor aromatices Povah - Bull. Torrey bot. Club 44. 296. 1917.
Mucor recurvus Butler - Mycologia 44: 561. 1952.

The following description is of CBS 318.52, on beerwort agar at 20°C in daylight.
Colony rather loose, up to 40 mm in height, Pinkish Buff to Light Pinkish Cinnamon, with apricot yellow reverse, aromatic; sporangiophores up to 18 µm in diam, transitorily recurved, soon collapsing, unbranched, infrequently sympodially branched, with or without yellow contents; sporangia golden yellow, vitreous in aspect, up to 125 µm in diam, with finely echinulate, deliquescent, transparent walls; columellae applanate, conical, cylindrical, up to 70 x 60 µm, rarely larger, with or with-out yellowish- or reddish-brown contents, with small collars mainly composed of needle-shaped crystals; sporangiospores ellipsoidal, sometimes flattened at one side, (12.2-) 15.2-20.9 (-27) x (5.4-) 6.4-8.4 (-11) µm, with yellow, granular contents; substrate hyphae up to 40 µm in diam, partially filled with yellow droplets; zygospores (CBS 196.71 (-) x CBS 195.71 (+) on PDA at 25°C) mainly produced in the upper portion of the colony, sometimes in a ladder-like fashion, globose, compressed between suspensors, up to 160 x 125 µm, roughened by projections up to 11 µm in length, glossy black; suspensors rather equal, straight, up to 40 µm in diam, elongatedly conical, tapering towards the zygophores, one or rarely both with golden yellow contents; zygospores up to 18 µm in diam, mouse-grey, the part adjacent to the suspensor may show yellow-orange colouring, with slightly encrusted walls.[p. 19]

 fig. 12

Fig. 12
Mucor recurvus var. recurvus, CBS 318.52
a. columellae; b. sporangiospores: CBS 992.70; c. columellae; d. sporangiospores.

Influence of temperature: at 45°C no development; at 40-10°C growth and sporulation; at 30-25°C optimal development, at 10°C very slow; at 5°C no development. At higher temperatures the pigmentation is slightly more marked. At 40 and 37°C repeated sympodial branching may occur: short branches with small, often sterile sporangia and a long apical branch with a fertile sporangium.
Influence of light: cultures grown in darkness are greyish-white with a slight yellowish tinge. The sporangiophores are very sensitive to daylight; illuminated from one [p. 20] side only, their position is almost horizontal, which seems to stimulate branching. Influence of medium: on beerwortagar + 40% saccharose and on Czapek agar good growth and sporulation.

 fig. 13

Fig. 13
Mucor recurvus var. recurvus, CBS 196.71
a. sporangiospores; CBS 317.15; b. sporangiospores; c. young zygospore between suspensors (CBS 195.71 x 196.71).


Material examined

Herbarium specimen
Povah no. 24 (MICH.), type of M. aromaticus, dried culture on bread.

Living strains
CBS 318.52 (+), type strain of M. recurvus.
CBS 317.52 (+), received from M. Blinc, Ljubljana, Yugoslavia, sub no. 9, isolated from decaying wood. Macedonia.
CBS 673.75 (-), received from W. A. Shipton sub R-34, isolated from soil, Douglas, Townsville, Australia.
CBS 992.70 (-) = NRRL 1711, received as M. aromaticus (Ellis & Hesseltine, 1969).
CBS 195.71 (+), CBS 196.71 (-), one sporangium isolates from a zygospores-producing culture, received as (?) M. aromaticus from Chiu-Yuan Chien, isolated from wild rat dung in Athens, Georgia, USA. [p. 21]


Discussion

The first descriptions of Mucor aromaticus and M. recurvus show similarity. Judging from Povah's (1917) illustrations, M. aromaticus might also be closely related to M. flavus Bain. No authentic living culture of M. aromaticus is known to exist. The available herbarium material, Povah no. 24 (Mich.), does not make it possible to reconstruct its morphology.
For comparison with the herbarium specimen, the strains under consideration, and also CBS 234.35 and CBS 126.70 of M. flavus were grown on bread and left to dry at room-temperature for 6 months. The six strains of M. recurvus were much lighter in colour than Povah's specimen, the two M. flavus strains produced darker (Buckthorn Brown) colonies. The specified odour ('somewhat like camphor and celluloid', Povah, 1917) was lacking in all. The colour of the sporangia in Povah's specimen resembled that in the M. recurvus strains, whereas that of M. flavus sporangia was much darker. The sporangiospores were similar in all the bread-cultures. The shape of the columellae in Povah's specimen could not be determined with certainty, but was described as being subglobose to oval or nearly pyriform. Synonymy of Mucor aromaticus and M. recurvus is uncertain, M. recurvus is definitely different from M. flavus (Schipper, 1975).
The strains vary in colony height, intensity of colour, width of the sporangiophores (up to 24 µm), size of the sporangia (up to 200 µm in diam) and accordingly of the columellae, size of the sporangiospores (up to 30 x 10 µm) and the maximum diameter of substrate hyphae (up to 65 µm). The strains CBS 992.70, 195.71 and 196.71 are of the larger forms.
Only the type strain developed well at 40-37°C. Each of the strains in study showed good growth and sporulation on beerwort agar + 40% saccharose; on Czapek agar CBS 318.52, 317.52 and 673.75 developed well. In CBS 992.70, 195.71 and 196.71 substrate hyphae spread rapidly, producing only a small number of scattered sporangiophores.
CBS 195.71 (+) and CBS 196.71 (-) are the only satisfactory mating partners among the available strains. All other (+) and (-) contrasts yielded only a few, rather small zygospores. Second most succesful in the series was the mating CBS 318.52 (+) x CBS 196.71 (-).

 

12. Mucor recurvus Butler var. indica Baijal & B.S. Mehrotra - Fig. 14, 1a

Mucor recurvus Butler var. indica Baijal & B. S. Mehrotra - Sydowia 19: 207. 1965.

The following description is of CBS 786.70 on beerwort agar at 20°C in daylight.
Colony up to 30 mm in height, Pinkish Buff with apricot yellow reverse, aromatic; sporangiophores up to 17 µm in diam, transitorily recurved, later collapsing, unbranched or infrequently branched, in ageing cultures some repeatedly branched, short, recurved side-branches bearing sporangiola are present; sporangia golden yellow, vitreous in aspect, up to 125 µm in diam but mostly smaller, with encrusted [p. 22] deliquescent walls, sporangiola 20 µm and more in diam, with persistent transparent, spiny walls; columellae applanate, conical to cylindrical, up to 55 x 54 (62 x 58) µm, with reddish-yellow contents and with small collars mainly consisting of needle-shaped crystals; sporangiospores ellipsoidal, (13.8-) 15.5-18 (-22.3) x (8.4-) 10.4-10.8 (11.1) µm, with yellow, granular contents; substrate hyphae locally swollen, filled with droplets.
Influence of temperature: at 45°C no growth; at 40-10°C growth and sporulation, at 30-20°C optimal development; at 10°C extremely slow. At higher temperatures the pigmentation is slightly intensified.
Influence of light: cultures grown in darkness greyish with a yellowish tinge; re-curved side-branches with sporangiola rather common.
Influence of medium: on beet-wort agar + 40% saccharose good growth and sporulation; on Czapek agar development is only slightly weaker.

 fig. 14

Fig. 14
Mucor recurvus var, indica, CBS 786.70
a. columellae; b. sporangiospores.


Material examined

CBS 786.70 (-) = MX-47, type strain.


Discussion

The production of both sporangia and sporangiola is characteristic for the genus Backusella. In Mucor recurvus var. indica sporangiola occur only rarely in ageing cultures. [p. 23]

 

13. Mucor tuberculisporus Schipper sp. nov. - Fig. 15

Misapplied name:
Mucor heterosporus Fischer sensu Baijal & Mehrotra - Sydowia 19: 210. 1965.

Coloniae in agaro maltoso 20°C dilute olivaceo-griseae. Sporangiophora ad 18 µm lata, primum curvata, deinde recta, simplicia vel modice ramosa. Sporangia dilute brunnea, ad 125 µm diam; in culturis vetustis sporangiola raro adsunt. Columellae applanatae ad conicae, ad 63 x 55 µm. Sporangiosporae irregulariter polyhedricae, protrusionibus rotundatis ornatae, 10-12 µm diam.
Typus CBS 562.66, isolatus e terra, prope Shillong in India, a U. Baijal et B.S. Mehrotra, 1965, velut Mucor heterosporus.

The following description is of CBS 562.66, on beerwort agar at 20°C in daylight.
Colony up to 25 (-40) mm in height, Pale Olive-Gray with very slightly yellowish reverse; sporangiophores up to 18 µm in diam, transitorily recurved, soon collapsing, unbranched or weakly sympodially branched, in ageing cultures short, slender, permanently recurved branches infrequently present, occasionally repeatedly sympodially branched bearing sporangiola; sporangia brownish, moist to vitreous in aspect, up to 125 (-150) µm in diam but mostly smaller, with encrusted, deliquescent walls; sporangiola 15 µm or more in diam with persistent, transparent, spiny walls; columellae applanate to conical, up to 63 x 55 (93 x 83) µm, pallid mouse-grey or with brownish contents, with small, spiny collars; sporangiospores irregularly polyhedral with rounded protrusions, 10-12 µm in diam, yellowish; substrate hyphae filled with droplets, zygospores unknown.

 fig. 15

Fig. 15
Mucor tuberculisporus, CBS 562.66
a. sporangiophore; b. columellae; c. sporangiospores. [p. 24].

Influence of temperature: at 37°C no growth; at 30°C poor growth; at 25-5°C growth and sporulation, at 25-20°C optimal development, at 5°C very slow. At 5°C repeatedly sympodial short branches develop with small, often sterile sporangia and a long apical branch with a fertile sporangium.
Influence of light: insignificant.
Influence of medium: on beerwort agar + 20% saccharose at 20°C the sporangiospores were subglobose, 10.8-13.5 µm in diam, the walls slightly rough in appearance, on beerwort agar + 40% saccharose the sporangiospores were subglobose, with rather smooth walls; on beerwort agar + 60% saccharose the sporangiospores were subglobose, smooth (Plate 1). On Czapek agar growth and sporulation, but weaker than on beerwort agar.


Material examined

CBS 562.66 (-) = MX-25, type strain, received as M. heterosporus.
CBS 570.70 (-), received from H. Naganishi (Naganishi et al., 1969) as M. heterosporus.

 plate 1

Plate 1
Mucor tuberculisporus, CBS 562.66
a-d. sporangiospores: a. on beerwortagar; b. on beerwortagar + 20% saccharose; c. on beerwortagar + 40% saccharose; d. on beerwortagar + 60% saccharose (x 1000)


Discussion

No type material of Mucor heterosporus Fischer is known. Linnemann (1936) identified one of her own isolates, CBS 240.35, as M. heterosporus, but this culture proved to be a strain of M. circinelloides (Schipper, 1976). Baijal & Mehrotra (1965) claimed to have refound M. heterosporus with their isolate MX-25 (= CBS 562.66) but this strain deviates from Fischer's (1892) diagnosis in several ways: Fischer described botryosely branched sporangiophores, ellipsoidal or ovoidal columellae and smooth, 4-15 µm in diam, sporangiospores which are mostly irregularly rounded or slightly angular, but are occasionally shaped in a bizarre manner. The bizarre spores mentioned by Fischer are probably not diagnostic, since large, irregularly shaped, [p. 25] presumably unfinished 'spores' are not unusual in Mucor colonies grown under unfavourable conditions or in degenerating strains. The identity of M. heterosporus Fischer consequently remains uncertain. Zycha & al. (1969) combined the characters given by both Linnemann (1936) and by Baijal & Mehrotra (1965) to 'characterize' M. heterosporus, though the data apply to quite different species.

 

14. Mucor oblongiellipticus Naganishi, Hirahara & Seshita ex Pidoplichko & Milko - Fig. 16

Mucor oblongiellipticus Naganishi, Hirahara & Seshita - Bull. Hiroshima Jogakuin Coll. 19: 52. 1969 (without Latin diagnosis); ex Pidoplichko & Milko - Atlas mucoral' nykh gribov Kiev p. 81. 1971.

 fig. 16

Fig. 16
Mucor oblongiellipticus, CBS 568.70
a. columellae; b. sporangiospores

The following description is of CBS 568.70, on beerwort agar at 20°C in daylight.
Colony up to 50 mm in height, Pinkish Buff to Cinnamon-Buff, with pale yellowish [p. 26] reverse, aromatic; sporangiophores up to 38 µm in diam, transitorily recurved, unbranched or branched at the base, with slightly encrusted walls, with or without reddish brown or bright yellow contents, phototropic; sporangia golden yellow, up to 300 (375) µm in diam, vitreous in aspect, with encrusted deliquescent transparent walls; columellae elongated applanate to conical or subglobose to ellipsoidal, up to 133 x 115 µm , with or without yellowish- or reddish-brown contents, with small collars consisting of needle-shaped crystals; sporangiospores oblongly ellipsoidal, in young cultures rather uniform, (21.6) 39.2-40.5 x (8.1) 14.9-15.5 µm, in ageing cultures smaller spores (14 x 5 µm and up) may be found, yellowish or with yellow granules concentrated in the center; substrate hyphae growing deep down into the medium, with giant-cells up to 155 µm in diam and with brownish contents.
Influence of temperature: at 37°C no growth; at 30-10°C growth and sporulation; at 5°C growth, no sporulation. At 30°C the sporangiospores are globose to broadly ellipsoidal, 30 x 18 - 20 µm; at 15°C and 10°C development is rather slow and a few sporangiophores are scattered throughout the colony.
Influence of light: colonies grown in darkness are much paler than those grown in light; branching of the sporangiophores only infrequently occuring.


Material examined

CBS 568.70, type strain.

 

15. Mucor oblongisporus Naumov sensu Naganishi, Hirahara & Joshita - Fig. 17

Mucor oblongisporus Naumov - Mater. Mikol. Fitopat. Ross 1: 11. 1915; sensu Naganishi, Hirahara & Joshita - Bull. Hiroshima Jogakuin Coll. 19: 55. 1969.

The following description is of CBS 569.70, on beerwort agar at 20°C in daylight.
Colony loose, up to 34 mm in height, Pale Smoke Gray; sporangiophores firm, up to 40 (-50) µm in diam, with a wider base and a slight constriction next to the sporangium, unbranched, infrequently with a short, recurved branch, bearing a sterile sporangium, with slightly encrusted walls, small droplets often occuring on the surface; sporangial development starts only after a rather considerable elongation of the young sporangiophore, then the sporangiophore recurves, straightening after maturation of the sporangium; the rare branching of the sporangiophore may start before or after the formation of a sporangium on the main axis; sporangia pale yellowish (sand colour), moist to slightly powdery in aspect, up to 250 µm in diam, infrequently larger, with finely echinulate, slightly transparent walls; columellae ellipsoidal to pyriform, the smallest conical, up to 110 x 75 µm , with or without brownish contents, collars mainly consisting of needle-shaped crystals approx. 10 µm in length; sporangiospores ellipsoidal, sometimes slightly flattened at one side, 11.5-16.2 x [p. 27] 6.8-8.4 µm, with greyish-yellow, cloudy to granular contents; substrate hyphae growing rather deep down into the agar, clearly visible between sporangiophores, irregular in width, filled with droplets.
Influence of temperature: at 37°C no growth; at 30°C poor development; at 25-10°C growth and sporulation; at 5°C slow, poor development.
Influence of light: insignificant.
Influence of medium: on Czapek agar growth and sporulation, but rather poor.

 fig. 17

Fig. 17
Mucor oblongisporus, CBS 569.70
a. young sporangiophore; b. columellae; c. sporangiospores


Material examined

CBS 569.70 = KN 451 = IFO 7058, neotype strain. [p. 28]


Discussion

No original material of Mucor oblongisporus is known to exist. The strain CBS 569.70, indicated as neotype by Naganishi et al. (1969), differs from Naumov's (1915) original description, in which the following key-features were mentioned: sporangiophores 20-35 µm in diam, weakly branched; sporangia (90) 100-120 (-150) µm in diam; columellae 72-90 x 60-80 µm, often covered with some sporangiospores due to a slimy substance mixed with the sporangiospores. Naumov (1915) did not mention a transitory curvature of the sporangiophores, and either the presence of needle-shaped crystals on the sporangial wall. Consequently Naumov's specimen might have been Mucor flavus (Schipper, 1975).
Apart from the transitory recurvature of the sporangiophores, the conical shape of the smallest columellae, collars that consist mainly of needle-shaped spines and the poor development at 5°C, the strain CBS 569.70 is in many aspects nearer to M. mucedo than to the species described in this paper. Like M. mucedo, it forms firm, erect sporangiophores, covered with small droplets, bearing large sporangia that are glistening-moist to slightly powdery in aspect, with columellae ellipsoidal to pyriform and sporangiospores with cloudy-granular contents.

 

16. Mucor mousanensis Baijal & B. S. Mehrotra - Fig. 18

Mucor mousanensis Baijal & B. S. Mehrotra - Sydowia 19: 205. 1965.

The following description is of CBS 999.70, on beerwort agar at 20°C in daylight.
Colony up to 5 mm in height, radial growth 50 mm in 4 days, 75-80 mm in 6 days, zonate, the central part with mature sporangia and Deep Mouse Gray, the margin with immature sporangia and Deep Olive Buff, Chamois reverse, slightly aromatic; sporangiophores up to 15 (-20) µm in width, usually unbranched, with slightly roughened walls, mouse-grey to brownish; sporangia at first bright yellow, later bluish black to black, globose to dorsiventrally flattened, up to 120 µm in diam, with bluish, echinulate, persistent walls; short sporangiophores with yellowish-brown sporangia are interspersed among the tall sporangiophores; columellae applanate elongated conical or ellipsoidal, up to 70 x 50 µm , mouse-grey or brownish, with collars varying from large to small; sporangiospores ellipsoidal, 6-8 x 4.4-5.1 µm, greyish; zygospores unknown.
Influence of temperature: at 37°C no growth, at 30-15°C growth and sporulation, at 20-15°C rather slow, at 10°C growth restricted, or no growth, no sporulation; at 5°C no growth.
Influence of light: cultures grown in darkness do not show any zonation.
Influence of medium: colonies on PDA are looser than those on beerwort agar.
Colonies on cherry agar are restricted and surrounded by sporangial colonies. [p. 29]

 fig. 18

Fig. 18
Mucor mousanensis, CBS 999.70
a. columellae; b. sporangiospores; c. columellae: CBS 721.76


Material examined

CBS 999.70 (+) = MX-14, type strain.
CBS 721.76 (+), received from G. L. Benny sub nr. 103, isolated from dung of Rattus norvegensis, Taichung area, Taiwan.
CBS 531.77 (+), received from P. C. Misra, sub PCM 603, isolated from mouse dung, Gorakhpur, India.


Discussion

CBS 721.76 differs from the type strain by having colonies up to 30 mm in height; sporangia at first pallid yellowish, later becoming black; sporangiophores mostly 6.8 x 4 µm (5.5-6.8 x 3-4 µm).
[p. 30]

 

17. Mucor ucrainicus Milko - Fig. 19

Mucor ucrainicus Milko in Pidoplichko & Milko - Atlas Mucoral'nykh gribov p. 62. 1971.

The following description is of CBS 221.71, on beerwort agar at 20°C in daylight.
Colony up to 50 mm in height, radial growth 50 mm in 4 days, 70-80 mm in 6 days, zonate, Pale Olive-Gray to Pallid Mouse Gray, with slightly yellowish reverse; sporangiophores up to 20 (-25) µm in width, though usually narrower below the columella, and wider at the base, erect, later collapsing, marginal colonies may occur, usually unbranched though ramification of the basal part of the sporangiophore may occur and in ageing cultures short secondary branches may be formed, sporangiophore walls are slightly roughened, brownish-purple; sporangia at first whitish, changing to purplish and then either pale yellowish-brown and vitreous in aspect or dark grey and powdery in aspect, up to 150 (-175) µm in diam, with slightly transparent walls, with needle-shaped crystals 5-7 µm in length; tall sporangiophores are interspersed with short sporangiophores with small sporangia; columellae elongated conical to ellipsoidal, large columellae tending to campanulate, small columellae applanate-conical, up to 120 x 87 µm, but mostly much smaller, with or without brownish, granular contents and with short collars, mainly consisting of needle-shaped crystals; sporangiospores ellipsoidal, rather uniform, mostly 7 x 4 µm (4.4-8.1 x 2.7-4.7 µm), greyish; zygospores unknown.
Influence of temperature: at 30°C no growth; at 25-5°C growth and sporulation, though slow at 10-5°C.
Influence of light: cultures grown in darkness do not show any zonation.

 fig. 19

Fig. 19
Mucor ucrainicus, CBS 221.71
a. columellae; b. sporangiospores. [p. 31].


Material examined

CBS 221.71 (-) = BKM F 1440, type strain.


Discussion

Mucor ucrainicus may be synonymous with M. mousanensis, mainly differing in colour of sporangia and columellae. However, considering the small number of available strains any conclusion about synonymy seems premature.

 

18. Mucor zychae Baijal & B. S. Mehrotra var. zychae - Fig. 20

Mucor zychae Baijal & B. S. Mehrotra - Sydowia 19: 204. 1965.

The following description is of CBS 416.67, on beerwort agar at 20°C in daylight.
Colony up to 5 (-10) mm in height, radial growth 55 mm in 7 days, zonate, Pale Olive-Gray, with slightly yellowish reverse; sporangiophores up to 7 µm in diam, at first erect but soon drooping, unbranched; sporangia hyaline with a yellowish tinge, vitreous in aspect, up to 60 (-75) µm in diam, with slightly incrusted, transparent, deliquescent walls; columellae subglobose to conical, up to 28 x 21 (32 x 36) µm, [p. 32] with or without pale yellowish contents, with or without small collars; sporangiospores ellipsoidal, (9.5-) 13.5-23 x (7.2-) 10.1-13.5 µm, with granular contents, pale yellowish-grey; substrate hyphae with swollen regions and globose giant-cells up to 60-70 µm in diam, filled with droplets.
Influence of temperature: at 37°C poor growth and sporulation; at 30-20°C growth and sporulation; at 15°C very poor growth, no sporulation. At all temperatures growth was slower and sporulation poorer than in other Mucor species.
Influence of light: colonies grown in darkness lacked zonation, sporulation was slightly poorer.
Influence of medium: general development is better on beerwort agar than on PDA or cornmeal agar.

 fig. 20

Fig. 20
Mucor zychae var. zychae, CBS 416.76
a. columellae; b. sporangiospores; c. giant-cell.


Material examined

CBS 416.67. type strain, from manured soil. India.

 

19. Mucor zychae Baijal & B. S. Mehrotra var. linnemanniae Schipper var. nov. - Fig. 21

Mucor disperses Hagem var. megalospora Linnemann Beitrag zu einer Flora der Mucorineae Marburgs, p. 184. 1936 (without Latin diagnosis).

A var. zychae differt sporangiosporis globosis neque ellipsoideis.
Typus: CBS 233.35, isolatus ex dejectis compositis in Germania a G. Linnemann. 1934.

The following description is of CBS 233.35, on beerwort agar at 20°C in daylight.
Colony up to 3 (-5) mm in height, radial growth 60 mm in 7 days, zonate, Pale Olive-Buff, with slightly yellow reverse; sporangiophores up to 8 µm in diam, at first erect, later drooping, usually unbranched, infrequently sympodially branched; sporangia hyaline with a yellowish tinge, vitreous in aspect, up to 60 (-75) µm in diam, with deliquescent walls; columellae subglobose, applanate or conical, up to 28 x 25 µm, rarely larger, with or without small collars; sporangiospores globose, subglobose, (11-) 14-18 (-24) µm in diam, with granular contents, pale yellowish; substrate hyphae with swollen regions and globose giant-cells up to 80 µm in diam, filled with droplets.
Influence of temperature: at 30°C only submerged mycelium; at 25-10°C growth and sporulation; at 5°C very slow growth and sporulation. At all temperatures growth was slower, and sporulation poorer than in most other Mucor species.
Influence of light: cultures grown in darkness lacked zonation, sporulation was slightly poorer. [p. 33]

 fig. 21

Fig. 21
Mucor zychae var. linnemanniae, CBS 233.35
a. columellae; b. sporangiospores; c. giant-cell.


Material examined

CBS 233.35, type strain of M. dispersus var. megalospora. isolated from compost, Marburg, F.R.G.
CBS 389.35, received as M. dispersus var. megalospora from H. Zycha, most probably a subculture of CBS 233.35.
CBS 785.70 = IMI 89318, received as M. dispersus, originating from C.T. Ingold.


Discussion

Mucor dispersus var. megalospora differs from Backusella lamprospora (Lendner) Benny & Benjamin = M. dispersus in the absence of sporangiola, a characteristic of Backusella. Furthermore, in Backusella lamprospora the sporangiophores are recurved when young, short branches and short sympodially branched sporangiophores bearing sporangiola only are formed near the substrate, and the sporangiospores are 8-13 µm in diam.
CBS 233.35 differs from the typical variety of M. zychae by producing globose instead of ellipsoidal sporangiospores; furthermore the latter shows good growth and sporulation at 30°C, but no growth below 15°C. [p. 34]
While validating the taxon, the epithet 'megalospora' was not adopted since the sporangiospores are of the same size as in var. zychae.
The influence of cultural conditions on sporangiospore size was studied by Williams (1959). The strain CBS 785.70 was probably used in these experiments. Illumination, temperature, pH and sugar content of the medium were found to affect the spore size. In the present study, the number and size of giant-cells, were found to vary as a result of different cultural conditions.

 

20. Mucor odoratus Treschow - Fig. 22 and Fig. 1e

Mucor odoratus Treschow - Bot. Tidsskr. 45: 148. 1941.
(?) Mucor rufescens Fischer - Rabenh. Krypt. Fl. Pilze IV, Aufl. 2, p. 192. 1892.

 fig. 22

Fig. 22. Mucor odoratus, columellae and sporangiospores
a. CBS 130.41; b. CBS 120.71

The following description is of CBS 130.41, on beerwort agar at 20°C in daylight.
Colony up to 1 mm in height, Olive-Buff to Deep Olive-Buff, with yellowish reverse, aromatic; sporangiophores up to 15 µm in diam, borne solitarily or in small [p. 35] groups on a common base, unbranched or branched with repeatedly sympodial, short circinate branches, usually bearing small, mostly sterile, sporangia and a long apical branch with a fertile sporangium, with or without yellow contents; sporangia golden yellow, vitreous in aspect, up to 75 (-100) µm in diam, with encrusted deliquescent, transparent walls; columellae applanate to slightly conical or subglobose, up to 32 x 32 (45 x 46) µm, with or without yellowish-brown contents, with small collars; sporangiospores ellipsoidal or plano-convexly ellipsoidal (7.8-) 9.5-17.5 (21.6) x (3.7-) 4-9.8 (-13.5) µm, with granular contents, yellowish, agglutinate; zygospores unknown.
Influence of temperature: at 40 and 37°C slow submerged growth, no sporulation; at 30-10°C growth and sporulation; at 5°C hardly any growth. Optimal development at 30-25°C; at lower temperatures occurence of recurved sporangiophores in young cultures is more frequent than at higher temperatures.
Influence of light: colonies grown in darkness are paler and sporulation is retarded.
Influence of medium: on beerwort agar + 20% saccharose at 20°C pigmentation is more marked, sporulation more abundant and the sporangiospores larger (11.8-25.6 x 6.7-14.8 µm).


Material examined

CBS 130.41, type strain of M. odoratus.
CBS 179.76A, 179.76B, 179.76C, 179.76D, 179.76E, five isolates from one sample of cow dung, F.R.G.
CBS 572.70, received as M. rufescens from H. Naganishi (Naganishi et aI., 1969).
CBS 120.71, received from C. Y. Chien, sub nr. 612, isolated from horse dung, Georgia, U.S.A.
CBS 201.71, isolated from horse dung, Netherlands.


Discussion

Though the original descriptions of M. rufescens and of M. odoratus show much similarity and M. rufescens was described first, the name M. odoratus is preferred because the type strain of this species is available. Each of the strains studied deviates from Fischer's (1892) diagnosis of M. rufescens by the production of shorter sporangiophores, smaller sporangia and probably by weaker pigmentation. The peculiar branching pattern on the lower portion of the sporangiophore was not described by Fischer (1892), nor by Treschow (1941). Mehrotra (1967) noticed this type of branching in his strain MX-41 of M. odoratus, as did Chien (pers. commun., 1971) in CBS 120.71.
Slight variations are found in height of the colony (1-7 mm), colour, the rate of sporulation (which is never very abundant), the intensity of odour, the maximum size of the sporangia (75-100 µm) and the average size of the sporangiospores. [p. 36]

 

21. Mucor falcatus Schipper - Fig. 23, Fig. 1d

Mucor falcatus Schipper - Antonie van Leeuwenhoek 33: 195. 1967.

Misapplied name:
Mucor strictus Hagem sensu Zycha - Krypt. Fl. Mark. Brandenb. 6a, Pilze II, p. 80. 1935.

 fig. 23

Fig. 23
Mucor falcatus, CBS 251.35
a. young sporangiophores; b. columellae; c. sporangiospores.

The following description is of CBS 251.35, on beerwort agar at 20°C in daylight. [p. 37]
Colony up to 8 mm in height, radial growth 60 mm in 7 days, greyish-white with a slightly yellowish tinge, with pallidly yellowish reverse, slightly aromatic; sporangiophores up to 18 µm in diam, readily collapsing, once or repeatedly sympodially branched, the main stalk soon bending aside and remaining short and sterile, the first branch taking its place, either growing tall and bearing a sporangium or the branching is repeated in the same way; sporangia yellowish to brownish, vitreous in aspect, up to 100 (-130) µm in diam, with encrusted, deliquescent walls; columellae conical or cylindrical, up to 60 x 55 µm, with or without yellowish-brown contents, with small collars; sporangiospores mainly globose, some ellipsoidal and/or deformed, 5.5-10 µm in diam, with granular contents, pallidly yellowish.
Influence of temperature: at 37°C no growth; at 30°C growth, no sporulation: at 25-10°C growth and sporulation, at 10°C series of very short, sterile branches are produced.
Influence of light: insignificant.
Influence of medium: on beerwort agar + 20% saccharose good growth, intensified pigmentation, poor sporulation.


Material examined

CBS 251.35 (+), type strain of M. falcatus, received from G. Linnemann as M. strictus, isolated from honey comb.
CBS 252.35 (+), received from H. Zycha as M. strictus, isolated from rabbit droppings.


Discussion

Zycha (1935) reported that in an unpublished study of Burkert in 1923 on Mucor strictus sensu Zycha zygospores were described as being very dark, up to 136 x 150 µm, dioecious and borne on special zygophores 9-25 µm in diam. Since Burkert's strains are no longer available and both strains CBS 251.35 and 252.35 turned out to be of the same mating reaction type, zygospores could not be studied.

 

22. Mucor azygosporus R. K. Benjamin - Fig. 24

Mucor azygosporus R. K. Benjamin in Benjamin & B. S. Mehrotra - Aliso 5: 240. 1963.

The following description is of CBS 292.63, on beerwort agar at 20°C in daylight.
Colony up to 16 mm in height, radial growth 30 mm in 5 days, 50-60 mm in 7 days, composed of tall sporangiophores and short azygophores; colony colour variegated, parts of the colony with mainly sporangia Ochraceous-Orange to Ochraceous-Salmon, parts with sporangia and azygospores Ochraceous-Tawny, while the lower portion where the azygospores are formed is sepia, reverse Ochraceous-Orange; sporangiophores [p. 38] weak and soon limp, up to 10 (-15) µm in diam, unbranched, mouse-greyish, with or without red-brown contents, phototropic; sporangial development initiating on the sporangiophores when these are about half their final height; sporangia orange to golden yellow, up to 100 (-150) µm in diam, vitrous in aspect, with encrusted, slightly transparent, deliquescent walls; columellae subglobose, infrequently applanate, up to 70 µm in diam, with golden yellow to reddish-brown contents and mouse-greyish walls, collars small; sporangiospores globose, broadly ellipsoidal, 6.7-9.5 x 5.4-8.1 (12.2 x 7.1) µm, with granular contents, yellowish to yellowish-orange, small granules may adhere to the surface of the spores; substrate hyphae up to 35 µm in diam, with bright orange-yellow contents, forming numerous oidia; azygospores, arising terminally on azygophores, subglobose, up to 125 x 115 µm, black, roughened by projections up to 8 µm in length; azygophores up to 14 µm in diam, widening to 35 µm at the juncture with the azygospore, the clavate part with reddish-brown contents.

 fig. 24

Fig. 24
Mucor azygosporus, CBS 292.63
a. columellae; b. sporangiospores; c. young azygospore.

Influence of temperature: at 40°C no growth; at 37°C growth, but mainly submerged, no sporulation; at 30-15°C growth and sporulation, slowing down with decrease of temperature; at 10°C growth insignificant or none. A years storage at 5°C undesirable.
Influence of light: in darkness the production of azygospores precedes the production of sporangia; in light sporangia are produced first, and outnumber the azygospores. [p. 39]


Material examined

CBS 292.63, type strain.

 

23. Mucor sinensis Milko & Beljakova - Fig. 25

Mucor sinensis Milko & Beljakova in Pidoplichko & Milko - Atlas mucoral'nykh gribov, p. 53. 1971.

 fig. 25

Fig. 25
Mucor sinensis, CBS 204.74
a. columellae; b. sporangiospores; c. chlamydospores.

The following description is of CBS 204.74, on beerwort agar at 20°C in daylight.
Colony up to 25 mm in height, radial growth 85 mm in 4 days, greyish white to Pale Smoke Gray, with pale yellowish reverse, slightly odorous; sporangiophores up to 10 (-14) µm in width, limp and soon collapsing, initiating sporangial colonies, usually unbranched though some branches may occur, with slightly roughened [p. 40] walls and numerous chlamydospores (causing split sporangiophores); sporangia pale yellowish-brown and vitreous in aspect, or sand-colour, mat glittering and powdery in aspect, globose to slightly dorsiventrally flattened, up to 70 (-100) µm in diam, with transparent, slightly incrusted walls; columellae ellipsoidal, cylindrical, elongated conical, conical infrequently slightly irregular in outline, up to 42 x 35 µm, rarely larger, with or without brownish contents; each collar, if present, is just a line of attachment; sporangiospores globose, subglobose, broadly ellipsoidal or irregular in shape, 5.4-12.2 x 4-10.8 µm, mixed with some larger, globose sporangiospores up to 16.2 µm in diam, with greyish, granular contents, zygospores unknown.
Influence of temperature: at 37°C no growth; at 30°C stunted growth, abnormal; at 25-5°C growth and sporulation, rate of development slowing down with de-crease of temperature.
Influence of light: insignificant.


Material examined

CBS 204.74 = BKM F-638, type strain.

 

Mating experiments

General remarks

In the present revision of the genus Mucor, species circumscriptions are based on general morphology as well as on the ability of heterothallic strains to produce zygospores. The presence of true zygospores in matings of similar strains is considered to be proof that these strains belong to the same species. Incomplete conjugation or non appearance of any visible reaction, however, does not necessarily provide evidence to the contrary.
Zygospores are not always clearly distinguishable from parthenospores. The term 'true zygospore' therefore demands some stipulation.
Surveying the major processes involved in sexual reproduction in Mucorales, formation of a true zygospore as a result of (+) and (-) interaction includes the following: zygophore production, zygophore fusion, gametangium formation, lysis of fusion wall and plasmogamy, zygospore development (Gooday, 1973). In incomplete conjugation lysis of the fusion wall does not occur. In practice, however, it is not easy to prove or disprove the dissolution of the fusion wall using the light microscope and secondary indicative characters are needed. Zygospore germination should be allotted the most importance. Unfortunately zygospores are difficult to germinate and there is a considerable time lapse between production and germination and again between germination and mating ability of the progeny (Gauger, 1965, 1977). Another possible way of establishing their genuineness is abundance: if a line of zygospore-like bodies is present within a few days after mating, one can be fairly certain that the majority of these are true zygospores, though occasionally mixed with some parthenospores. [p. 41]
Parthenospores develop from a single gametangium, thus being supported by a single suspensor. The other 'suspensor' may either wither, remain transparent, or develop into more or less rounded structure, not closely adnate to the spore (Blakeslee et al., 1921; Ling, 1930). Parthenospores are similar to the zygospores, though usually somewhat smaller and often slightly irregular in outline.
A second 'suspensor' is not always present but initiation of (pro)gametangia is dependant on the (one time) stimulus of a compatible zygophore (parthenospore = azygospore).
The interaction of (+) and (-) strains of widely different morphological taxa may infrequently result in some parthenospores, together with conjugations that failed at an earlier stage (progametangia, gametangia). Stages of the morphogenesis of induced azygospores in Gilbertella persicaria (Eddy) Hesseltine (+) by imperfect hybridization with Rhizopus stolonifer (Ehrenb. ex Fr.) Lind (-) were clearly shown in S.E.M. and T.E.M. micrographs by O'Donnell & al. (1977). Callen (1940) probably also obtained parthenospores in contrasts of Rhizopus sexualis (Smith) Callen with Rh. stolonifer, Mucor hiemalis Wehmer and Absidia cylindrospora Hagem. He described them as hybrid zygospores, but the small and unusual shape of the 'suspensor' of the Rh. stolonifer partner and the Rh. sexualis-type of exosporium pattern of the 'zygospores' in Rh. sexualis x M. hiemalis, suggest the presence of parthenospores rather than zygospores.
In interspecific matings, parthenospores may be found in addition to incomplete conjugations in matings of (+) and (-) strains which differ in physiology but are morphologically similar, and may also occur next to zygospores in fully compatible partners.
Only suitable partners of a single species are able to produce zygospores readily; actual zygospore production is dependent on many external and internal conditions, most of which are not yet fully understood. In mating partners isolated together, fertility is often stronger than in separately isolated strains; inability to complete an initiated sexual reaction not being unusual in the latter. Havens (1976) found that in Mucor hiemalis the average mating potency is high in groups of isolates which are electrophoretically similar, independant of morphological variance. In a number of Mucor species zygospores are still unknown; in others the available (+) and (-) strains seem unsuited and produce only a few zygospores on mating.

Results (click on table) 

fig. 1 Table 1

Interfertility tests of species of similar morphology, made in search of possible relationships or unknown mating reaction types, had formerly been a routine giving rather predictable results. However, the results proved to be confusing in the present investigation. Zygospore-like bodies were found in several of the interspecific contrasts, often of species widely different in general morphology. Therefore it was deemed desirable to investigate all possible combinations, including (+) and (-) strains of the related Backusella circina and B. lamprospora, on beerwort agar at 25°C (Table 1) and partly at 21 and 27°C.
Compatible mating partners of Mucor amphibiorum, M. indicus and M. recurvus were available; no distinct mating reaction was observed in M. microsporus, M. oblongiellipticus, [p. 42] [p. 43] [p. 44] M. odoratus or M. sinensis; each of the remaining species proved to be represented by only one mating reaction type.
The frequently encountered, confusing, zygospore-like bodies mentioned above were often rather pale, small, sometimes slightly misshapen and appeared rather late in comparison to most intraspecific Mucor matings. They were never really abundant and were generally produced inside a wall of touching interwoven hyphae and incomplete conjugations. Observation in situ was usually not possible and slide preparation was handicapped by the adjacent hyphal growth.
Some contrasts of type strains of species differing in general morphology, produced apparently true zygospores between two seemingly active suspensors (see below: Example A).

 

Table 2. Data of Mucor prayagensis, M. indicus, M. inaequisporus andM. variosporus.

M. prayagensis

M. indicus

M. inaequisporus

M. variosporus

sporangiophores

unbranched, up to 10(-15) µm in diam

repeatedly branched up to 14 µm in diam

unbranched, up to 18 (-30) µm in diam

unbranched. up to 14 (-23) µm in diam

sporangia

yellowish, vitreous, up to 60 (-75) µm in diam, walls transparent

brownish, vitreous, up to 80 µm mostly 40-50 µm in diam. walls transparent

brownish, vitreous, up to 150 (-175) µm in diam, walls transparent

yellow, vitreous, up to 150 µm in diam. walls transparent

columellae

subglobose applanate, up to 39 x 43 µm

subglobose applanate, up to 50 x 53 µm, mostly smaller

obovoid-pyriform up to 83 x 75 µm

ellipsoidal-obovoidal up to 72 x 60 µm

sporangiospores

9.5-12.3 x
4-5.4 µm

5.4-5.7 x 4.4 µm

5.7 x 3-4 µm and 12-18 µm in diam and up to
30 x 23 µm

5.5-13.5 x
3.5-8 µm

zygospores

(one strain only)

black, 80 (-100) µm in diam. stellate

black, 80 (-100) µm in diam. stellate

(one strain only)

suspensors

 

unequal: one very short, the other swollen (up to 35 µm) and then constricted, both with yellow contents

unequal: one very short, the other swollen (up to 35 µm) and then constricted, both with yellow contents

 

good growth and sporulation at:

40-20 (-15°) C

37-20° C

30-15° C

30-20 (-15°) C

source:

soil, India

226.29: probably soil, India,
423.71: dust-heap, Indonesia

496.66: persimmon, Japan 497.66

rotten Ficus fruit, India

[p. 45]

To exemplify, two sets of matings will be discussed and illustrated in detail and furthermore, an illustrative separate contrast will be presented. Example A concerns strains which mainly act within a defined group of species. Examples B and C concern strains in which mating-reactions were observed throughout almost the whole range of interspecific contrasts.

Example A: matings of Mucor inaequisporus, M. indicus, M. variosporus and M. prayagensis (Table 1). A survey of morphological data of the species concerned is given in Table 2.

In Mucor indicus, the mating of CBS 226.29 (+) x CBS 423.71 (-) yielded zygospores after 2 days on beerwort agar at 25°C (Fig. 26a). The mating testers in M. inaequisporus CBS 496.66 (+) and CBS 497.66 (-) did so after 3 days (Fig. 26b).
M. indicus x M. inaequisporus. From CBS 226.29 (+) x CBS 497.66 (-) progametangia were formed in a broad band after 2 days, in 3 days gametangia were observed, some of which developed into greyish zygospore-like bodies, up to 45 µm in diam, with unequal suspensors which both had yellowish contents (Fig. 26c). CBS 423.71 (-) x CBS 496.66 (+) yielded after 3 days a rather large number of dark brown zygospore-like bodies, up to 70 µm in diam, with unequal suspensors which both had yellowish or brownish contents (Fig. 26d).
M. prayagensis x M. indicus. CBS 816.70 (+) x CBS 423.71 (-) produced a small number of blackish brown zygospore-like structures, up to 60 µm in diam.
M. prayagensis x M. inaequisporus. From CBS 816.70 (+) x CBS 497.66 (-) progametangia and gametangia occurred after 2 days; on the third day the fusion wall of some gametangia showed bulging, an indication of incompatibility (Ling, 1930). The zygospore-like structures which formed later were black, app. 35 µm, rarely up to 85 µm in diam, with often one large, or several smaller globules inside (another sign of incompleteness), with unequal suspensors of which the larger had yellowish contents (Fig. 26e).
M. variosporus x M. indicus. CBS 837.70 (-) x CBS 226.29 (+) showed young zygospore-like bodies in 3 days that appeared mature after 4 days and were black, up to 80 µm in diam, with unequal suspensors which both had yellowish contents; only a few incomplete conjugations were observed at that period (Fig. 26f).
M. variosporus x M. inaequisporus. From CBS 837.70 (-) x CBS 496.66 (+) blackish brown zygospore-like bodies were obtained in 4 days, up to 75 (-90) µm in diam, with globules inside and unequal suspensors of which the larger had coloured contents (Fig. 26g).
M. variosporus x M. prayagensis. CBS 837.70 (-) x CBS 816.70 (+) yielded abundant incomplete conjugations and a small number of zygospore-like bodies which were reddish brown or pale yellowish brown (even after 3 weeks of interaction), up to 65 (-75) µm in diam, contained some globules, and never showed more than one apparently normal suspensor.
Mucor indicus, M. inaequisporus and M. variosporus, rather different in morphology, seem to produce true zygospores with each other. Germination tests to establish the true nature of these structures would be very desirable. [p. 46]

 fig. 26

Fig. 26 a-b Stages in the conjugation of the testerpairs
a. Mucor indicus; b. Mucor inaequisporus. c-d. Stages in the conjugation of Mucor indicus x M. inaequisporus; c. CBS 226.29 (+) x CBS 497.66 (H; d. CBS 423.71 H) x CBS 496.66 (+). e. Stages in the conjugation of Mucor prayagensis CBS 816.70 (+) x M. inaequisporus, CBS 497.66 (-). f. Stages in the conjugation of Mucor variosporus CBS 837.70 (-) x M. indicus, CBS 226.29 (+); g. Stages in the conjugation of Mucor variosporus CBS 837.70 (-) x M. inaequisporus, CBS 496.66 (+) [p. 47].

 fig. 27

Fig. 27
Stages in the conjugation of Backusella circina x Mucor prayagensis
a. CBS 129.70 (+) x CBS 816.70 (+); b. CBS 322.69 (-) x CBS 816.70 (+) [p. 48]

Example B: Matings of CBS 763.74; 764.74; 765.74; 766.74, Mucor amphibiorum, which probably originate from one source (Frank et al., 1974) and which each have a (+) reaction.
On beerwort agar at 25°C the tester pair of M. amphibiorum, CBS 763.74 (+) x CBS 185.77 (-), produce black zygospores, up to 70 µm in diam, between unequal suspensors with yellowish contents; incompleted conjugations are rare.
Contrasts of M. amphibiorum (+) with (-) strains of M. guilliermondii, M. tuberculisporus, M. inaequisporus, M. indicus, M. oblongisporus, M. recurvus, M. recurvus var. indicus, M. ucranicus, M. variabilis, M. variosporus, Backusella circina and B. lamprospora each yielded a rather small number of zygospore-like bodies inside a wall of touching interwoven hyphae and incomplete conjugations; the bodies were dark brown, up to approx. 50 µm in diam, sometimes mis-shapen and/or containing globules; the suspensors were unequal, the larger being coloured.
The above data on Mucor amphibiorum, CBS 763.74 etc., and also Backusella circina, CBS 322.69, like Blakeslee & Cartledge's (1927) 'Mucor H', show that the degree of imperfect hybridization and the taxonomic relationship are unconnected.

Example C: Another 'strong' partner in several interspecific contrasts is Backusella circina, CBS 322.69 (-). Successive phases of incomplete conjugation between B. circina and Mucor prayagensis (+) are illustrated in Fig. 27.

 

Key to the accepted species of mucor

All species described in Studies in Mycology 4(I), 10(II), 12(III) and in the present paper (IV) are keyed out below.
Characters are based on live strains, generally grown on beerwort agar at 20°C; in some cases simultaneous cultures at 5°, 37° and 40°C or on acid beerwort agar/cherry agar are necessary; for explanation of used terms see also Schipper (1975).

1a.

Tallest sporangiophores usually repeatedly sympodially branched; sporangia usually less than 100 µm in diameter; zygospores or azygospores, when present, reddish brown to dark brown

2

1b.

Tallest sporangiophores unbranched or weakly sympodially branched or at least some sporangia with a diameter of more than 100 µm; zygospores or azygospores, when present, dark brown to black

14

 

 

 

2a.

Growth and sporulation at 37°C, growth at 40°C

M. indicus

2b.

Poor or no growth at 37°C, no growth at 40°C

3

 

 

 

3a.

Reddish brown azygospores borne terminally and subterminally on branched azygophores present in monosporangial cultures

M. bainieri (III: 17)

3b.

Reddish brown azygospores on branched azygophores absent in monosporangial cultures

4

 

 

 

4a.

Sporangiospores ellipsoidal (L/B 1.3-1.6) or (sub)globose and approx. 4-6 µm in diam, smooth; chlamydospores in sporangiophores uncommon

5

 

[p. 49]

 

4b.

Sporangiospores broadly ellipsoidal (L/B I.15-1.3) or (sub)globose and up to 8-10 µm in diam, smooth or verrucose; chlamydospores in sporangiophores abundant or rare

10

 

 

 

5a.

Colonies low, velvety; recurved sporangiophores absent

6

5b.

Colonies otherwise; recurved sporangiophores present or absent

7

 

 

 

6a.

Sporangia blackish, with though, persistent walls; columellae applanate; sporangiophores with swollen regions

M. ramosissimus
(III: 15)

6b.

Sporangia greyish-brown, with diffluent walls: colmellae mostly subglobose; sporangiophores of regular width

M. zonatus (III: 19)

 

 

 

7a. 

Colonies greyish; sporangiophores up to 7 (-10) µm in diam; sporangia blackish

8

7b.

Colonies brownish; sporangiophores up to 14 (-17) µm in diam; sporangia brownish to brownish grey, rarely dark brown

9

 

 

 

8a.

Sporangiospores subglobose

M. circinelloides f. janssenii (III: 13)

8b.

Sporangiospores ellipsoidal

M. circinelloides f. griseo-cyanus (III: 12)

 

 

 

9a. 

Colmellae globose

M. circinelloides f. lusitanicus (III: 9)

9b.

Columellae obovoidal

M. circinelloides f. circinelloides (III: 5)

 

 

 

10a. 

Sporangiophores repeatedly branched in a sympodial fashion, with long branches originating just below the preceding sporangium and at acute angles (except occasionally at the top)

M. fuscus (III: 30)

10b.

Sporangiophores branched in a mixed sympodial and monopodial fashion, not as described above

11

 

 

 

11a. 

Columellae usually with apical projections; sporangiospores (sub)globose, brownish, punctate; chlamydospores in sporangiophores rare

M. plumbeus (III: 26)

11b.

Columellae usually smooth; sporangiospores subglobose or broadly ellipsoidal, greyish, generally smooth; chlamydospores in sporangiophores usually abundant

11

 

 

 

12a.

Sporangiospores mainly subglobose

M. racemosus f. sphaerosporus
(III: 23)

12b.

Sporangiospores broadly ellipsoidal

13

 

 

 

13a.

Columellae obovoidal to broadly pyriform, often 50 µm and more in height; monopodial branches short

M. racemosus f. racemosus (III: 20)

13b.

Columellae subglobose, obovoidal or ellipsoidal, mostly 20 µm or less in height, rarely up to 40 µm; monopodial branches long

M. racemosus f. chibinensis (III: 24)

 

 

 

14a. 

Tall sporangiophores slightly sympodially branched, branches occurring rather late; sporangia with a diameter of less than 80 µm, sporangiospores ellipsoidal

15

14b.

Tall sporangiophores unbranched except for an infrequent single sympodial branch or at least some sporangia with a diameter of more than 80 µm or sporangiospores not ellipsoidal

19

 

 

 

15a.

Zygospores present in monosporangial cultures

M. genevensis (I: 34)

15b.

Zygospores absent in monosporangial cultures

16

 

 

 

16a.

Branches arising just below the blackish-brown sporangia, often swollen at the base; columellae globose; sporangiospores cylindrical

M hiemalis f. silvaticus (I: 31)

 

[p. 50]

 

16b.

Branches arising at a longer distance below the yellowish to dark-brown sporangia

17

 

 

 

17a.

Sporangia yellowish; columellae globose; sporangiospores narrow ellipsoidal

M. hiemalis f. luteus (I: 33)

17b.

Sporangia brownish to dark brown; columellae globose and ellipsoidal; sporangiospores ellipsoidal to cylindrical-ellipsoidal

18

 

 

 

18a.

Sporangiospores mainly cylindrical-ellipsoidal

M. hiemalis f. corticolus (I: 31)

18b.

Sporangiospores ellipsoidal, sometimes flattened at one side

M. hiemalis f. hiemalis (I: 26)

 

 

 

19a. 

Young sporangiophores erect

20

19b.

Young sporangiophores transitorily recurved

45

 

 

 

20a.

Tall sporangiophores sympodially branched

22

20b.

Tall sporangiophores unbranched or infrequently with a single branch

21

 

 

 

21a.

Sporangia often more than 150 µm in diam

26

21b.

Sporangia usually not exceeding 150 µm in diam

29

 

 

 

22a. 

Colonies approx. 1 mm in height; at least some sporangia over 100 µm in diam and having persistent walls; sporangiospores approx. 8 x 6 µm

M. aligarensis (II: 18)

22b.

Colonies more than 1 mm in height

23

 

 

 

23a.

Sporangiophores of two types: tall and short, sympodially branched; sporangia on tall sporangiophores with deliquescent walls, sporangia on short sporangiophores with persistent walls; sporangiospores ellipsoidal mostly 7 x 4 µm

M. saturninus (II: 16)

23b.

Sporangiophores either of one type only or of two types; sporangiospores ellipsoidal over 7 µm in length or subglobose

24

 

 

 

24a.

Sporangiospores ellipsoidal

M. flavus (II: 26)

24b.

Sporangiospores globose or subglobose

25

 

 

 

25a.

Sporangiospores globose or subglobose 4-5 µm in diam

M. minutus (II: 24)

25b.

Sporangiospores globose or subglobose when grown at 20°C, ellipsoidal when grown at 5°C

M. strictus (II: 23)

 

 

 

26a. 

Columellae ovoidal or conical

27

26b.

Columellae obovoidal, ellipsoidal or pyriform

28

 

 

 

27a.

Mature sporangia dorsiventrally flattened, often 400 µm and over in diam; sporangiospores 25 µm and over in average length

M. plasmaticus
(II: 19)

27b.

Mature sporangia slightly dorsiventrally flattened, rarely exceeding 200 µm in diam: sporangiospores usually 7.5-10 µm in length; psychrophilic: poor sporulation at 20°C; slow superficial growth at all temperatures

M. psychrophilus
(II: 21)

 

 

 

28a.

Sporangiospores usually ellipsoidal, up to 10 µm in length; rapid growth on cherry agar or acid beerwort agar

M. piriformis (II: 13)

28b.

Sporangiospores typically cylindrical-ellipsoidal, often over 10 µm in length; restricted growth on cherry agar or acid beerwort agar

M. mucedo (II: 8)

 

 

 

29a. 

Zygospores or azygospores present in monosporangial cultures

30

29b.

Zygospores or azygospores absent in monosporangial cultures

31

 

[p. 51]

 

30a.

Sporangiospores bacilliform

M. bacilliformis

30b.

Sporangiospores globose or broadly ellipsoidal

M. azygosporus

 

 

 

31a.

Sporangiospores ellipsoidal or cylindrical-ellipsoidal, 8 µm or less in length

32

31b.

Sporangiospores ellipsoidal, over I2 µm in length and/or globose

36

 

 

 

32a.

Sporangiospores narrow ellipsoidal, with a granule (globule) at each end

33

32b.

Sporangiospores ellipsoidal, without granules at the ends

34

 

 

 

33a.

Columellae mostly obclavate

M. guilliermondii

33b.

Columellae globose to subglobose

M. subtilissimus

 

 

 

34a. 

Sporangia less than 100 µm in diam

M. microsporus

34b.

Sporangia over 100 µm in diam present

35

 

 

 

35a.

Colony very dark grey; sporangia bluish-black; columellae mouse-grey or brownish

M. mousanensis

35b.

Colony grey; sporangia pale brown or dark grey; columellae hyaline, with or without brownish contents

M. ucrainicus

 

 

 

36a. 

Sporangia 75 µm or less in diam

37

36b.

Sporangia often 100 µm or more in diam

42

 

 

 

37a.

Sporangia up to 75 µm in diam; sporangiophores often 15 µm or more in width

38

37b.

Sporangia not exceeding 60 µm in diam; sporangiophores not exceeding 10 µm in width

39

 

 

 

38a.

Sporangiospores globose, 3.5-5.5 µm in diam, non-agglutinate

M. amphibiorum

38b.

Sporangiospores ellipsoidal or planoconvex-ellipsoidal, up to approx. 18 x 10 µm, agglutinate

M. odoratus

 

 

 

39a.

Sporangiophores 8 µm or less in width; globose giant cells present

40

39b.

Sporangiophores up to 10 (-15) µm in width; giant cells absent

41

 

 

 

40a.

Sporangiospores ellipsoidal

M. zychae var. zychae

40b.

Sporangiospores (sub)globose

M. zychae var. linnemanniae

 

 

 

41a. 

Sporangiospores ellipsoidal or flattened at one side

M. prayagensis

41b.

Sporangiospores (sub)globose

M. sinensis

 

 

 

42a. 

Sporangiospores extremely variable in shape and size: ellipsoidal, less than 10 µm in length, mixed with much larger, ellipsoidal to globose sporangiospores up to 30 µm in length

M. inaequisporus

42b.

Sporangiospores less variable, either ellipsoidal or (sub)globose

43

 

 

 

43a.

Sporangiospores (sub)globose; sporangiophores with a sterile, sickleshaped branch at the base

M. falcatus

43b.

Sporangiospores ellipsoidal; sporangiophores unbranched

44

 

 

 

44a.

Columellae ellipsoid-obovoidal or globose; no growth at 37°C

M. variosporus

44b.

Columellae applanate to elongated applanate or conical; growth at 37°C

M. variabilis

 

 

 

45a. 

Sporangia up to 250 µm or more in diam

46

45b.

Sporangia 200 µm or less in diam

47

 

 

 

46a.

Sporangiospores oblong-ellipsoidal, up to 40 µm in length

M. oblongiellipticus

46b.

Sporangiospores ellipsoidal, 16 µm or less in length

M. oblongisporus

 

[p. 52]

 

47a. 

Sporangia 60 µm or less in diam

M. guilliermondii

47b.

Sporangia up to 125 µm and over in diam

48

 

 

 

48a.

Sporangiospores irregularly polyhedral

M. tuberculisporus

48b.

Sporangiospores ellipsoidal or oblong-ellipsoidal

49

 

 

 

49a.

Sporangiola absent

M. recurvus var. recurvus

49b.

A few short, permanently recurved branches bearing sporangiola with persistent spiny walls present in ageing cultures

M. recurvus var. indica

[p. 53]


 

2. On the genera Rhizomucor and Parasitella

M. A. A. SCHIPPER
Centraalbureau voor Schimmelcultures, Baarn.

 

Summary

The genus Rhizomucor is reintroduced for the 3 thermophilic species, Rhizomucor pusillus, Rh. miehei and Rh. tauricus. The genus is distinct from Mucor by the formation of stolons and rhizoids and by its temperature requirements. The genus Parasitella is accepted for the single species, Parasitella parasitica.

 

Introduction

The accepted species of the genus Rhizomucor were originally described as Mucor pusillus, M. miehei and M. tauricus, although their stolons and rhizoids are generically distinct.
The monotypic genus, Parasitella, differs from Mucor by its parasitic behaviour, by the origin of the sporangiophores and, furthermore, by its zygosporic stage.

 

Rhizomucor (Lucet & Cost.) Wehmer ex Vuill.

Mucor Mich. ex Fr. sect. Rhizomucor Lucet & Cost. - C.r. hebd. Séanc. Acad. Sei., Paris 129: 1033. 1899 = Mucor Mich. ex Fr. subg. Rhizomucor (Lucet & Cost.) Sacc. & Syd. in Sacc. - Syll. Fung. 16: 385. 1902 = Rhizomucor (Lucet & Cost.) Wehmer in Lafar - Handb. Techn. Mykol. 4: 459. 1907 (incidentally mentioned): ex Vuill. - Champ. paras. myc. homme p. 14. 1931.

Thermophilic; sporangiophores originating from aerial mycelium, either from short aerial hyphae or from distinct stolons, both with simple or weakly branched rhizoids; sporangiophores branched, each branch bearing a multispored terminal sporangium; sporangia borne in an upright position, globose, dark (coloured), distinctly columellate, non-apophysate; sporangiospores subglobose, zygospores globose, covered with blunt projections, and formed in the aerial mycelium between non-ornamented, isogamous opposite suspensors. [p. 54]

Type species: Mucor (Rhizomucor) parasiticus Lucet & Cost. = Rh. pusillus (Lindt) Schipper.


Discussion

Lucet & Costantin's (1899) recognition of Rhizomucor as a taxon was accepted as a separate genus by Wehmer (in Lafar, 1907), Vuillemin (1931) and by Hesseltine & Ellis (1973). However, Lendner (1908), Naumov (1915) and Pidoplichko & Milko (1971) regarded Rhizomucor as synonymous to the genus Rhizopus Ehrenb. Naumov (1935, 1939) considered it to have a doubtful position, being related to either Rhizopus, Lichtheimia Vuill. (= Absidia van Tieghem) or Mucor.
The genus is close to Actinomucor in which rhizoids and stolons are also not very pronounced and sporangiophores and sporangia have a similar structure. However, Actinomucor is not thermophilic, has hyaline sporangia, and is not known to have zygospores.
Rhizomucor differs from Mucor by having stolons and rhizoids, from Rhizopus by the repeatedly branched sporangiophores and the absence of apophyses and from Absidia in having globose sporangia, and the absence of apophyses.
The thermophilic nature of species classified in Rhizomucor has always been recognized and investigated though not used for the delimitation of the group. Lindt (1886), Miehe (1907) and Lucet & Costantin (1900, 1901) noted optimal development of their strains at approx. 37-40°C, and growth from 22-24°C to over 50°C. These temperature requirements are unknown in Mucor.

 

Key to the species

Characters are based on strains grown on beerwort agar (or SMA) at 36°C.

1a.

Poor growth, hardly any sporulation; sporangiophores up to 35 µm in width

Rh. tauricus

1b.

Good growth and sporulation; sporangiophores up to 15 µm in width

2

 

 

 

2a.

Zygospores absent in monosporangial cultures

Rh. pusillus

2b.

Zygospores present in monosporangial cultures

3

 

 

 

3a.

Zygospores more than 50 µm in diam

Rh. pusillus

3b.

Zygospores less than 50 µm in diam

Rh. miehei

 

24. Rhizomucor pusillus (Lindt) Schipper, comb. nov. - Figs. 28, 29

Mucor pusillus Lindt - Arch. exp. Path. Pharmak. 21: 272. 1886 (basionym,).
(?) Mucor septatus Bezold in Siebenmann - Schimmelmyc. menschl. Ohres p. 97. 1889 = Rhizomucor septatus (Bezold) Lucet & Cost. - Archs Parasit. 4: 362. 1901.
Mucor (sect. Rhizomucor) parasiticus Lucet & Cost. - C.r. hebd. Séanc. Acad. Sei., Paris 129: 1033. 1899 = Rhizopus parasiticus (Lucet & Cost.) Lendner - Matér. Fiore Cryptog. Suisse 3: 115. 1908.
(?) Mucor muriperda Sacc. & Sinigaglia in Sacc. - Annls mycol. 11: 321. 1913 = Thieghemella muriperda (Sacc. & Sinigaglia) Naumov - Opredelitel' Mukorovykh (Mucorales) p. 84. 1935. [p. 55]
Mucor buntingii Lendner - Bull. Soc. hot. Genève 21: 260. 1930.
Mucor hagemii Naumov - Opredelitel' Mukorovykh (Mucorales) p. 55. 1935 (without latin diagnosis).

The following description is of CBS 354.68, on beerwort agar at 36°C in darkness.
Colony 1 (-2) mm in height, Hair Brown; stolons up to 17 µm in diam, with roughened walls, brownish; rhizoids weakly developed, brownish; sporangiophores branching in a mixed monopodial-sympodial fashion, mostly subterminal, up to 11 (-15) µm in diam, brownish, with slightly encrusted walls; sporangia grey, glittering, up to 80 (-100) µm in diam, with encrusted walls which rupture at maturity; columellae obovoidal to slightly pyriform, up to 45 x 38 µm, rarely larger, light brown to [p. 56] mouse grey, smooth or with very small protrusions, collars poorly defined to none; sporangiospores subglobose, a few ellipsoidal, 3-4 µm in diam, rarely larger; zygospores (CBS 253.53 (+) x CBS 354.68 (-) on beerwort agar at 30°C) formed in the aerial mycelium, globose to slightly compressed, up to 70 x 63 µm, included blunt spines, dark brown to black, suspensors equal, elongated conical.
Influence of temperature: at 57 °C no growth; at 55°C slow growth, poor sporulation or none; at 50-24°C growth and sporulation: at 21°C extremely slow growth.
Influence of light: insignificant.
Influence of medium: the addition of 20-40% saccharose stimulated extension growth, provoked production of slightly larger sporangia on main stalks and of short, repeatedly sympodially branched subterminal branches, each bearing small sporangia. Colonies were less dense on Czapek agar (containing 30 gr saccharose/litre) than on beerwort agar. The absence or presence of thiamine (in SMA) did not influence development.

 fig. 28

Fig. 28
Rhizomucor pusillus, CBS 354.68
a. sporangiophores; b. columellae; c. sporangiospores; d. zygospore between suspensors; e. rhizoids.


Material examined

Heterothallic strains
CBS 231.29 (+), type strain of M. buntingii.
CBS 219.31 (+). received from E. A. R. F. Baudet, isolated from pig's kidney.
CBS 253.53 (+), received from J. A. von Arx. isolated from water. Wisconsin tank.
CBS 294.63 (+), received from C. L. Fergus, isolated from mushroom compost.
CBS 668.66 (+), isolated from Psittacus erythacus (parrot) lung.
CBS 183.67 (-), received sub 6; CBS 184.67 (+), received sub 8 (Cooney & Emerson. 1964).
CBS 354.68 (-), neotype strain of Rh. pusillus, isolated from cornmeal.
CBS 970.68 (+), received from G. L. Hennebert sub GLH 11292, isolated from seed-rice from China.
CBS 198.71A, isolated from cocoa.
CBS 198.71B (+), isolated from mustard.
CBS 198.71Cl (+), II (+), III (-). isolated from caraway seed,
and other strains e.g. isolated from pig's compost, salami, cole-seed and soil.

Homothallic strains
CBS 245.58, received sub BB325, LSH (Smith, 1957).
CBS 198.71 D, isolated from caraway seed,
and five other strains from unknown sources.


Discussion

 fig. 29

Fig. 29
Rhizomucor pusillus, CBS 245.58
a. sporangiophores; b. columellae; c. sporangiospores; d. zygospore between suspensors.

The strains studied showed slight variations in colony height (1 to 4 mm), in colony colour (Light Smoke Gray to Deep Grayish Olive or Hair Brown) and in the maximum diameter of the sporangia (approx. 80-100 pm). Though heterothallism is usual in Rhizomucor pusillus, some strains are homothallic, but morphologically identical, to the heterothallic strains (Fig. 29).
Miehe (1907) recognized the similarity between Mucor pusillus Lindt and Rhizomucor parasiticus, settling on the older name Mucor pusillus for his isolate. Vuillemin (1931) concluded that Rhizomucor parasiticus, Rh. septatus and Mucor pusillus were synonymous. Scholer (1970) also recognized the synonymy of Rh. parasiticus [p. 57] and M. pusillus, but did not re-introduce Rhizomucor in order to prevent confusion.
As no type material of the species is known, CBS 354.68 is here proposed as neotype for Rh. pusillus.
Ellis & Hesseltine (1966) identified the type material of Mucor muriperda as M. pusillus. The type strain of Mucor hagemii was a CBS strain received as M. pusillus from O. Hagem. This strain is now lost, but the slight differences between the original diagnosis of M. pusillus and Naumov's (1935) description of M. hagemii, lie well within the limits of specific variability.
Rhizomucor pusillus is a common causative agent of animal mycoses (Scholer, 1970). Artificially evoked mortal mycoses in rabbits were described as early as 1886 by Lindt. Scholer (1970) determined the pathogenicity of ten strains on mice; each strain evoked a strong reaction and caused macroscopical changes of the kidneys.

Mating experiments, - The strains CBS 253.53 (+) and CBS 354.68 (-) were chosen as tester pair. The mating reaction signs were determined by Schipper (1976) by means of contrasts with Absidia corymbifera CBS 271.65 (-), CBS 270.65 (+) and others.
Optimal mating results are obtained at 27-33 °C, on beerwort agar. Few zygospores are formed at 24°C and 36°C; no zygospores are produced at or above 40°C.
On beerwort agar, YpSs and YEA the production of zygospores was abundant.
The addition of 20-40% saccharose to beerwort agar was unfavourable for the production [p. 58]
of zygospores: on beerwort agar + 20% saccharose rather few zygospores were formed and on beerwort agar + 40% saccharose they were rare or absent.
The homothallic strain CBS 245.58 produced zygospores at temperatures between 24 and 36°C. The addition of saccharose to beerwort agar proved unfavourable for zygospore production, whereas darkness was stimulative. Absence of thiamin in SMA did not interfere with zygospore production.

 

25. Rhizomucor miehei (Cooney & Emerson) Schipper, comb. nov. - Fig. 30

Mucor miehei Cooney & Emerson - Thermophilic Fungi p. 26. 1964 (basionym).

 fig. 30

Fig. 30
Rhizomucor miehei, CBS 182.67
a. sporangiophores; b. rhizoids; c. columellae; d. sporangiospores; e. zygospores between suspensors [p. 59].

The following description is of CBS 182.67, on beerwort agar at 36°C in darkness.
Colony 1 mm in height, Deep Olive Gray; stolons up to 9 µm in diam with roughened walls; rhizoids weakly developed; sporangiophores sympodially branched, up to 7 µm in diam, with slightly encrusted, brownish walls; sporangia grey, glittering, up to 50 (-60) µm in diam, with encrusted walls which rupture at maturity; columellae obovoid to slightly pyriform, up to 28 x 25 µm, rarely larger, brownish to mouse grey, with small protrusions; collars poorly defined to none; sporangiospores subglobose, a few ellipsoidal, 3-4 µm in diam, rarely larger; zygospores (homothallic) formed in the aerial mycelium, globose to slightly compressed, up to 50 µm, but mostly approx. 35 µm in diam including stellate warts, reddish brown when young, then blackish brown; suspensors equal, elongated conical.
Influence of temperature (4 days): at 55-24°C growth, at 57 and 21°C negligible growth; at 50-24°C sporangial development, though weak at 50°C and rather slow at 27-24°C; at 40-27 (24)°C zygospore production, though rather slow at 27°C and a few zygospores were formed after 6 days at 24°C.
Influence of light: colonies grown in daylight are paler due to the smaller number of zygospores.
Influence of medium: the addition of 20-40% saccharose to beerwort agar had no appreciable effect on growth and sporangial development, but with 40% saccharose zygospores were absent. On Czapek agar (containing 30 gr saccharose/litre) colonies were noticeably less dense than on beerwort agar. An absence of thiamin (in SMA) resulted in scanty colonies without zygospores.


Material examined

CBS 370.65, deposited by Novo Industri A/S.
CBS 182.67, type strain.
CBS 429.70, received from A. E. Apinis sub BDUN 147, isolated from stored barley.
CBS 521.70, received from H. C. Evans sub XIV Leycett (Evans, 1971).
CBS 370.71, CBS 267.73, isolated from sputum.
and several strains sent by M. R. Tansey, isolated from Indiana soil, and two strains without data, received for identification.


Discussion

 The strains which were studied showed slight variation in colony colour (Light Neutral Gray to Neutral Gray or Deep Olive Gray) and sometimes sporangia up to 75 µm in diameter.
Cooney & Emerson (1964) considered their new species, Mucor miehei, to be distinguishable from M. pusillus on the basis of its homothallism. They classified all the homothallic strains in M. miehei and included CBS 245.58 (Smith's (1957) strain BB 325), a strain which is actually identical to M. pusillus (Schipper, 1969; Scholer 1970; Branner-Jørgensen & Ilum Nielsen, 1974). The present author considers the general morphology to be of most importance (see: Rhizomucor pusillus, homothallic strains). [p. 60]

 plate 2

Plate 2. Ornamentation of the outer zygospore wall
a. Rhizomucor pusillus; CBS 253.53 (+) x CBS 354.68 (-); b. Rh. pusillus, CBS 245.58; c. Rh.miehei, CBS 182.67. (scanning electron micrograph, x 4300). [p. 61].

Rh. pusillus produces small bunches of short subterminal branches on the main sporangiophores, while Rh. miehei shows a looser sympodial pattern with relatively longer side branches. In addition the sporangia and columellae of Rh. pusillus are usually larger than those of Rh. miehei. As branching pattern and sporangium size may vary they are probably unsuitable distinguishing specific features.
The zygosporic stages of Rhizomucor miehei and Rh. pusillus show marked differences in the colour of young zygospores, the size of mature zygospores and suspensors, and the markings on the outer zygospore wall (Plate 2).
In order to test the value of differences in zygospore-size (for the distinction of Rh. miehei and Rh. pusillus), the diameter of the largest zygospores were determined in each of the available strains of Rh. miehei, in all possible mating combinations of fourteen (+) and seven (-) strains of Rh. pusillus, and the available homothallic strains of Rh. pusillus, The measurements presented below were taken after 3 days on beerwort agar at 30°C. (Fig. 31). The poorest results shown for Rh. pusillus are from combinations in which CBS 294.63 (+) acted as a partner: in each of those matings only a few, small zygospores were formed. On account of these data the zygospore size is regarded as a key character in distinguishing Rh. miehei and (homothallic) Rh. Pusillus. Agamic strains of Rh. miehei were never encountered.
Cooney & Emerson (1964) characterized Rh. miehei and Rh. pusillus as having minimum growth temperatures of 25°C and 20°C respectively. These observations were confirmed by Scholer (1970) for a much larger number of strains, but in the present study temperature limits of both species were very close. The supposed higher maximum growth temperature of Rh. miehei (57°C) against that of Rh. pusillus (55 °C) (Cooney & Emerson, 1964) was not confirmed by Scholer (1970).
Growth in Rh. miehei is generally slower than in Rh. pusillus. The increases in colony diam within 24h, at the optimum temperature of 36°C, are given below. Rates are noted from the second day after inoculation to discount possible unequally delayed initiation.

 

beerwort agar

beerwort agar


 

 

+ 20% saccharose

CBS 354.68, Rh. pusillus

25-30 mm

35 mm *

CBS 245.58, Rh. pusillus (homothallic)

25-30 mm

35 mm *

CBS 182.67, Rh. miehei

20 mm

25 mm


* reaching edge of petri dish

Scholer & Müller (1966) tested Rh. pusillus and Rh. miehei strains on their ability to assimilate a number of carbon-sources. They found that Rh. pusillus grew very well with saccharose as the sole C-source, whereas Rh. miehei did not. Branner-Jørgensen & Ilum Nielsen (1974), however, did not find the difference in their strains to be significant.
Scholer & Müller (1966) found their 24 strains of Rh. pusillus to be thiamin-independent, whereas the 4 available strains of Rh. miehei showed thiamin-dependence. These results were confirmed in the present investigation for 23 heterothallic and 7 homothallic strains of Rh. pusillus and 17 strains of Rh. miehei.
Rhizomucor miehei produces a protease which is used to replace calf-rennet in cheese industry. Branner-Jørgensen & Ilum Nielsen (1974) reported the protease yield in heterothallic Rh. pusillus to be 1% and in homothallic Rh. pusillus to be 2-4% [p. 62] of the yield in Rh. miehei. The same investigators concluded that the coagulating enzyme of Rh. pusillus is different from that of Rh. miehei.
In immuno-electrophoretic studies of the proteins (Ilum Nielsen & Hansen, 1975) the homothallic strains of Rh. pusillus showed a closer relationship to heterothallic Rh. pusillus than to Rh. miehei.
Since mated strains of heterothallic Rh. pusillus were not included in the above studies, an eventual influence of ± interaction on metabolism is not known.
Scholer (1970) showed that Rh. miehei can evoke lethal mycosis in mice, causing macroscopical changes of the kidneys similar to those inflicted by Rh. pusillus.

 fig. 31

Fig. 31
Diameter of largest zygospores in single strains/matings.
Rhizomucor miehei; Rh. pusillus, matings; Rh. pusillus, homothallic.

 

26. Rhizomucor tauricus (Milko & Schkurenko) Schipper, comb. nov. - Fig. 32

Mucor tauricus Milko & Schkurenko - Nov. Sist. niz. Rast. 7: 139. 1970 (basionym).

The following description is of CBS 179.69, on beerwort agar + 20% saccharose at 36°C in darkness.
Colony less than 1 mm in height, Grayish Olive; stolons up to 20 µm in diam; rhizoids very weakly developed; sporangiophores either slender and up to 10 µm in [p. 63] diam, but more often swollen and up to 35 µm,  frequently gradually tapering towards the base or irregular in width, either unbranched or weakly branched with short subterminal branches or, rarely, repeatedly sympodially branched, wide sporangiophores sometimes showing additional dichotomously branched tips, sporangiophores either brownish or glassy-hyaline in appearance; sporangia grey, glittering, up to 125 µm in diam, with encrusted rupturing walls, occasionally sterile; columellae globose to obovoid, up to 70 x 60 µm (90 x 85 µm), light mouse grey or brownish, collars poorly defined or absent; sporangiospores subglobose, occasionally ellipsoidal, 3-4 µm in diam.

 fig. 32

Fig. 32
Rhizomucor tauricus, CBS 179.69
a. sporangiophores; b. columellae; c. sporangiospores [p. 64].

Influence of temperature: at 57°C no growth, at 55-24°C growth and sporulation, at 21°C extremely slow growth and no sporulation.
Influence of light: insignificant.
Influence of medium: the influence of saccharose-enrichment of beerwort agar on growth, expressed in colony diameter after 4 days at 36°C, is shown in Fig. 33. On beerwort agar colonies were dark brown, sporangiophores were only of the swollen type, all being irregular in width, sporangia were sterile. On beerwort agar with 20-80% saccharose colonies were grey, some sporangiophores were of the slender type and sporangia contained spores. Cultures on PDA (20 gr glucose/litre) sporulated better than those on beerwort agar. Cultures on SMA (40 gr glucose/litre), with or without thiamin, were very poor. The addition of saccharose to beerwort agar also effected a shift in the maximum growth temperature: on beerwort agar alone no growth was observed at 50°C, but on beerwort agar + 20% saccharose cultures still grew at 55°C.

 fig. 33

Fig. 33 Influence of saccharose enrichment of beerwort agar on radial growth of Rhizomucor tauricus, CBS 179.69.


Material examined

CBS 179.69(-) = BKM F 1379, type strain.


Discussion

Since cultures on beerwort agar were very poor, the description is based on a culture on beerwort agar + 20% saccharose. Milko & Schkurenko (1970) made their diagnosis using cultures on prune-agar, which seems to have the same influence on the fungus as beerwort agar. The authors mainly distinguished Rh. tauricus from Rh. pusillus and Rh. miehei by its swollen sporangiophores and by its lower temperature maximum of 47-49°C. On medium enriched with saccharose, however, Rh. tauricus and Rh. pusillus have the same (55 °C) maximum growth temperature. On beerwort agar with saccharose a low percentage of narrow sporangiophores occurred [p. 65] which resembled those in Rh. pusillus.
Since only one isolate of Rh. tauricus is available, it is difficult to decide whether it is a deviating strain of Rh. pusillus or a true species. Mating experiments of Rh. tauricus with Rh. pusillus are handicapped by the osmophilism of the first. Rhizomucor tauricus hardly grows on plain beerwort agar; both Rh. tauricus and Rh. pusillus grow well on beerwort agar + 20% saccharose, but zygospore production is greatly reduced in matings of Rh. pusillus on beerwort agar with increased sugar content. Even on this medium, however, zygospore-like bodies, with the same diameter (up to 80 µm), colour and ornamentation as those of Rh. pusillus, were obtained in 10 out of 14 contrasts of Rh. tauricus with Rh. pusillus (+) at 30°C. No evidence of conjugation was observed. In contrasts of Rh. tauricus with Absidia corymbifera, CBS 270.65 (+), on beerwort agar + 20% saccharose and on Y.E.A. at 30°C, no reaction was observed.

 

Parasitella Bain

Parasitella Bain - Bull. Soc. mycol. Fr. 19: 153. 1903.

Facultative gall-forming parasites of other Mucorales; in free living colonies sporangiophores originate from vertical growing tips of substrate hyphae, in parasitizing colonies sporangiophores are formed on aerial hyphae; sporangiophores hyaline, simple or branched, each branch bearing a multispored terminal sporangium; sporangia borne in an upright position; globose to subglobose, columellate, non-apophysate: sporangiospores ellipsoidal; zygospores globose, covered with blunt projections formed in the aerial mycelium between opposite isogamous suspensors, several suspensors having finger-like outgrowths.

Type species: Parasitella simplex Bain.


Discussion

Bainier (1903) erected the genus Parasitella to accomodate Mucor parasiticus Bain. (1884) which mainly differs from other Mucor spp. by its parasitic behaviour. Burgeff (1924) pointed out the unusual origin of the sporangiophores in pure culture and obtained the zygosporic stage, using the occurrence of outgrowths on the suspensors as a further criterion for the distinction of Parasitella from Mucor. Zycha (1935) Naumov (1939), Zycha et al. (1969) and others differentiated Parasitella from Mucor by its gall-forming parasitism and the appendaged suspensors.
Burgeff (1924) made careful observations of both the saprobic and parasitic development of the species from sporangiospores. The apparent tendency of the fungus to parasitize either (+) or (-) strains of heterothallic (Absidia) hosts and also the resemblance of the early stages in gall-development to imperfect conjugations, lead to a theory that parasitism might have developed by way of an imperfect sexual reaction. [p. 66]
Satina & Blakeslee (1926) confirmed a tendency for one mating type of the parasite to react preferentially with a single mating type of the host in two species of Absidia, but found no sex-limited relation between parasite and other hosts.
Burgeff (1924) obtained zygospores in matings of strains grown as parasites, whereas matings in pure culture failed. Satina & Blakeslee (1926) yielded zygospores in matings of pure cultures.

 

27. Parasitella parasitica (Bain.) Syd. - Fig. 34

Mucor parasiticus Bain. - Annls Sci. nat. Ser. 6, 19: 212. 1884 = Parasitella simplex Bain. - Bull. Soc. mycol. Fr. 19: 153. 1903 (name change) = Parasitella parasitica (Bain.) Syd. - Annls mycol. 1: 371. 1903.

The following description is of CBS 412.66 on beerwort agar at 20°C in daylight, after 6 days.
Colony up to 10 (15) mm in height, 25 mm in diam, white to Pale Smoke Gray with yellowish reverse; sporangiophores reach to the margin of the colony; sporangiophores up to 7 µm in diam, infrequently swollen, simple or once branched, soon collapsing and thus initiating sporangial colonies around the periphery of the parent colony; sporangia yellowish-hyaline, at first moist, later vitreous in aspect, up to 70 µm in diam, with transparent, diffluent walls; columellae applanate, globose to ellipsoidal, up to 30 µm in diam, with small collars or none; sporangiospores narrow ellipsoidal, sometimes flattened at one side, 4-8 x 2.5-3.5 µm; zygospores (CBS 412.66 (+) x CBS 208.28 (-) on beerwort agar at 20°C) in the aerial mycelium, reddish brown, up to 70 µm in diam, including stellate projections up to 8 µm in length; suspensors unequal, up to 40 µm in diam, with or without one to several finger-like outgrowths.
Influence of temperature: at 36°C restricted, stunted growth; at 30-15°C growth and sporulation, optimal at 25°C, at 10°C very slow growth, no sporulation; at 6°C no growth.
Influence of light: simultaneous cultures grown in darkness cover a larger area, sporangiophores do not always reach to the margin of the colony, and the colonies are surrounded by more numerous sporangial colonies.


Material examined

CBS 207.28 (+), CBS 208.21 (-), received from A. F. Blakeslee.
CBS 412.66 (+), neotype strain, received from J. E. Wright, originating from C. W. Hesseltine.
CBS 152.69 (+) = NRRL 1461, and CBS 153.69 (-) = NRRL 1459, which may be of the same origin. [p. 67]

 fig. 34

Fig. 34
Parasitella parasitica, CBS 412.66
a. sporangiophores; b. columellae; c. sporangiospores; CBS 207.28; d. columellae; e. sporangiospores; CBS 207.28 x 208.28; f. zygospore CBS 412.66 x Mucor hiemalis f. linens, CBS 243.35 (-); g. partenospore; h. galls.


Discussion

As no material of Bainier's specimen is available, the strain CBS 412.66 is here proposed as neotype of Parasitella parasitica,
The studied strains showed variations in growth rate (10-30 mm), in the maximum and minimum growth temperature and in the shape of the sporangiospores [p. 68] which were narrow ellipsoidal, ellipsoidal or cylindrical ellipsoidal, but varied with changes in environment (especially temperature).
Zycha (1935), Naumov (1939), Zycha et al. (1969), Hesseltine & Ellis (1973) considered P. parasitica to be similar to Mucor hiemalis. It differs, however, by the slower growth, whitish colonies and narrow sporangiophores, which originate from tips of substrate hyphae, and by reddish brown zygospores with often one appendaged suspensor.
In order to fully investigate the possibility of a close relationship to M. hiemalis, the available strains of Parasitella parasitica were contrasted with the Mucor hiemalis testerpairs chosen by Schipper (1973). In CBS 412.66 x M. hiemalis f. luteus, CBS 243.35 (-), zygospore-like bodies similar to Parasitella zygospores with only one suspensor, were repeatedly found (Fig. 34g), but formed rather late compared to intraspecific zygospores. None of the other contrasts with M. hiemalis showed any recognizable reactions. The induction of parthenospores in CBS 412.66 x CBS 243.35 (-) is here regarded as a confirmation of the strain designation by Burgeff (1924).
Grown with a suitable host (e.g. Rhizopus stolonifer), P. parasitica produces numerous narrow hyphae which contact the host mycelium, forming a crosswall near each tip. The tip cell then enlarges, the contact-wall is dissolved, outgrowths of the cell form a gall-like structure at the contact area and the adjacent part of the contacting hypha becomes a thick-walled cell in which nuclei of host and parasite are mixed (coenocecidia; Buhr, 1964).
Since the early stages in gall development closely resemble those in conjugation, determination of the mating reaction-type after incomplete conjugations with known (+) or (-) partners is problematic. Burgeff (1924) designated the strains (+) and (-) according to their tendency to parasitize Absidia-hosts of only one (opposite) sign. The induction of parthenospores in CBS 412.66 x CBS 243.35 (-) is here regarded as a confirmation of the strain designation by Burgeff.

 

Acknowledgements

The author wishes to express her sincere gratitude to Dr. J. A. von Arx, Dr. G. S. de Hoog and Miss C. van Oorschot M. Ph. for valuable criticism during the preparation of the manuscript. Many thanks are due to Miss L. van Dijk, Mrs. E. Hilhorst, Miss. I. ten Hoedt, Miss J. Pannebakker and Mrs. J. Willemstein for technical assistance, and to Dr. J. A. Stalpers for taking scanning electron micrographs. [p. 69]

 

References

Benny, G. L. & Benjamin, R. K., 1975 - Observations on Thamnidiaceae (Mucorales). New taxa, new combinations, and notes on selected species. - Aliso 8: 301-351.
Bainier, G., 1884 - Nouvelles Observations sur les Zygospores des Mucorinées.- Annls Sci. nat., Ser. 6, 19: 200-214.
Bainier, G., 1903 - Sur quelques espèces de Mucorinées nouvelles ou peu connues. - Bull. Soc. mycol. Fr. 19: 153-172.
Blakeslee, A. F, 1904 - Sexual reproduction in the Mucorineae. - Proc. Am. Acad. Arts Sci. 40: 205-319.
Blakeslee, A. F., 1906 - Zygospore germination in the Mucorineae. - Annls mycol. 4: 1-128.
Blakeslee, A. E & Cartledge, J. L., 1927 - Sexual dimorphism in Mucorales. II. Interspecific reactions. - Bot. Gaz. 84: 51-57.
Blakeslee, A. F., Cartledge, J. L. & Welch, D. S., 1921 - Sexual dimorphism in Cunninghamella. - Bot. Gaz. 72: 185-219.
Boedijn, K. B., 1958 - Notes on the Mucorales of Indonesia. - Sydowia 12: 321-362.
Branner-Jørgensen, S. & Ilum Nielsen, R., 1974 - Comparative enzyme patterns in Mucor miehei Cooney & Emerson and Mucor pusillus Lindt - 2nd int. Symp. Gen. industr. Micr., Sheffield.
Brefeld, O., 1872 - Botanische Untersuchungen über Schimmelpilze I. Zygomycetes. - Leipzig.
Buhr. H., 1964 - Bestimmungstabellen der Gallen (Zoo- und Phytocecidien) an Pflanzen Mittel- und Nordeuropas. Jena.
Burgeff, H., 1924 - Untersuchungen über Sexualität und Parasitismus bei Mucorineen I. - Bot. Abh. 4: 1-135.
Callen, E. O., 1940 - The Morphology, Cytology and Sexuality of the Homothallic Rhizopus sexualis (Smith) Callen. - Ann. Bot., N.S., 4: 791-818.
Calmette, A., 1892 - Contribution á l'etude des ferments de l'amidon; la levure chinoise. – Annls Inst. Pasteur, Paris 6: 604-620.
Cooney, D. G. & Emerson, R., 1964 - Thermophilic fungi. - San Francisco/London.
Cutter, V. M. jr., 1942 - Nuclear behaviour in the Mucorales I. The Mucor pattern. - Bull. Torrey bot. Club 69: 480-508.
Dyr, J., 1940 - Generis Mucor Mich. species duae novae. - Studia bot. cech. 3: 80.
Ellis, J. J & Hesseltine, C. W., 1966 - Species of Absidia with ovoid sporangiospores. II. Sabouraudia 5: 59-77.
Ellis, J. J. & Hesseltine, C. W., 1969 - Two new members of the Mucorales. - Mycologia 61: 863-872.
Ellis, J. J., Rhodes, L. J. & Hesseltine, C. W., 1976 - The genus Amylomyces. - Mycologia 68: 131-143.
Evans, H. C., 1971 - Thermophilous fungi of coal spoil tips. II Occurrence, distribution and temperature relationships. - Trans. Br. mycol. Soc. 57: 255-266.
Eijk, G. W. van, 1972 - Presence of carotenoids and ergosterol in Mucor azygospora and in Mucor inaequisporus. - Antonie van Leeuwenhoek 38: 163-167.
Fischer, A., 1892 - Phycomycetes. - Rabenhorst's Kryptogamenflora von Deutschland, Oesterreich und der Schweiz IV (Pilze). - Leipzig.
Frank, W., Roesler, U & Scholer, H. J, 1974 Sphaerulen-Bildung bei einer Mucor-Spezies in inneren Organen von Amphibien. Vorläufige Mitteilung. - Zentbl. Bakt. ParasitKde, Abt. I, 226: 405-417.
Gauger, W., 1965 - The germination of zygospores of Mucor hiemalis. - Mycologia 57: 634-641.
Gauger, W., 1977 - Meiotic Gene Segregation in Rhizopus stolonifer. - J. gen. Microbol. 101: 211-217.
Gooday, G. W., 1973 - Differentiation in the Mucorales. - Symp. Soc. gen. Microbiol. 23: 269-294.
Hagem, O., 1910 - Neue Untersuchungen über norwegische Mucorineen. - Annls mycol. 8: 265-286.
Havens, P. L., 1976 - Comparative zone electrophoresis and mating experiments in the taxonomy of Mucor hiemalis. - Mycotaxon 4: 218-232.
Hesseltine, C. W., 1955 - Genera of Mucorales with notes on their synonymy. - Mycologica 47: 344-363. [p. 70]
Hesseltine, C. W. & Ellis, J J 1973 - Mucorales. - in: Ainsworth. G. C. & al. The Fungi, 4B: 187-217.
Hirahara, S. & Naganishi, H., 1965 - Microsporic observation on the growth of a Mucor species found in unripe persimmon (Diospyros kaki L). - Essays Stud. Fac. Hiroshima Jogakuin Coll. 15: 69-79.
Ilum Nielsen, R. & Hansen, S. A., 1975 - Mucor proteases and their application in taxonomy. - Fifth Linderstrøm-Lang Conference, Vejle.
Lendner, A., 1908 - Les Mucorinées de la Suisse. In: Matériaux pour la Flore Cryptogamique Suisse, vol. 3. - Berne.
Lindt. W., 1886 - Mittheilungen über einige neue pathogene Schimmelpilze. - Arch. exp. Path. Pharmak. 21: 269-298.
Ling Young, 1930 - Etude des phénomènes de la sexualité chez les Mucorinées. - Revue gén. Bot. 42: 567-768.
Linnemann, G., 1936 - Beitrag zu einer Flora der Mucorineae Marburgs. - Marburg.
Lucet, A. & Costantin, J., 1899 - Sur une nouvelle Mucorinée pathogène. - C. r. hebd. Sèanc. Acad. Sci., Paris 129: 1031-1034.
Lucet, A. & Costantin, J, 1900 - Rhizomucor parasiticus. Espèce pathogène de l'homme. - Revue gén. Bot. 12: 81-98.
Lacet, A. & Costantin, J., 1901 - Contribution à l'etude des Mucorinées pathogènes. - Archs Parasit. 4: 362-408.
Mehrotra, B. S., 1967 - Final Technical Report (grant U. S. P1 480 funds in India, Project UR-A7 - (10-9)). May 25. 1967.
Miehe, H., 1907 - Die Selbsterhitzung des Heus. - Jena.
Milko, A. A. & Schkurenko, V. A., 1970 - De specie nova e genere Mucor notula. - Nov. Sist. niz. Rast. 7. 139-141.
Naganishi, H. & Hirahara, S., 1966 - On a Mucor sp. found in fallen unripe persimmon. - Essays Stud. Fac. Hiroshima Jogakuin Coll. 16: 109-120.
Naganishi, H. & Hirahara, S., 1968 - A new species Mucor pseudolamprosporus belonging to the Sphaerosporus section. - Essays Stud. Fac. Hiroshima Jogakuin Coll. 18: 167-172.
Naganishi, H., Hirahara, S. & Seshita, Y., 1969 - Rare Mucor species in Japan. - Bull. Hiroshima Jogakuin Coll. 19: 49-77
Naumov, N. A., 1915 - Tabelitsy delja opredelenyja predstaviteleni Mucoraceae - Petrograd. Naumov, N. A., 1915 - Petersburger Pilze. - Mater. Mikol. Fitopat. Ross. 4: 6-34.
Naumov, N. A., 1935 - Opredelitel'Mukorovykh (Mucorales), Ed. 2. - Moscow (in Russian):1939 - Clès des Mucorinées (Mucorales). Paris. (in French).
O'Donnell, K. L., Ellis, J. J. & Hesseltine, C. W., 1977 Morphogenesis of azygospores induced in Gilbertella persicaria (+) by imperfect hybridization with Rhizopus stolonifer (-). - Can. J. Bot. 55: 2721-2727.
Oudemans, C. A. J. A., 1898 - Contribution à la Flora Mycologique des Pays-Bas XVI. - Ned. Kruidk. Archf.. Sér 3, 1: 430-535.
Pidoplichko, N. M. & Milko, A. A., 1971 - Atlas mucoral'nykh gribov. - Kiev.
Povah, A. H. W., 1917 - A critical study of certain species of Mucor. - Bull. Torrey bot. Club 44: 287-310.
Saccardo, P. A. & Sydow, P., 1902 - in: Saccardo, P. A., Sylloge Fung. 16. - Patavii.
Satina, S. & Blakeslee, A. F., 1926 - The Mucor parasite Parasitella in relation to sex. - Proc. natn. Acad. Sci. U.S.A. 12: 202-207.
Schipper, M. A. A., 1967 - Mucor strictus Hagem, a psychrophilic fungus, and Mucor falcatus, sp. n. - Antonie van Leeuwenhoek 33: 189-195.
Schipper, M. A. A., 1969 - Zygosporic stages in heterothallic Mucor. - Antonie van Leeuwen-hoek 35: 189-208.
Schipper, M. A. A., 1973 - A study on variability in Mucor hiemalis and related species. - Stud. Mycol. 4: 1-40.
Schipper, M. A. A., 1975 - On Mucor mucedo, Mucor flavus and related species. - Stud. Mycol. 10: 1-33.
Schipper, M. A. A., 1976 - Induced azygospore formation in Mucor (Rhizomucor) pusillus by Absidia corymbifera. - Antonie van Leeuwenhoek 42: 141-144.
Schipper, M. A. A., 1976 - On Mucor circinelloides, Mucor racemosus and related species. - Stud. Mycol. 12: 1-40. [p. 71]
Scholer, H. J., 1970 - Mucormykosen bei Mensch und Tier. Taxonomie der Erreger. Chemotherapie im Tierexperiment und in der Klinik. - Habilitationsschrift, Basel.
Scholer, H. J. & Muller, E., 1966 - Beziehungen zwischen biochemischer Leistung und Morphologie bei Pilzen aus der Familie der Mucoraceen. - Path. Microbiol. 29: 730-741.
Smith, G., 1957 - Some new and interesting species of microfungi. - Trans. Br. mycol. Soc. 40: 481-488.
Tode, H. J, 1790 - Fungi Mecklenb. sel. 1. - Lüneburg.
Vuillemin, P., 1931 - Les Champignons parasites et les mycoses de l' homme. - Paris.
Wehmer, C., 1907 - Mucoraceen gärungen, Morphologie und Systematik der Mucoraceen. - In: F. Lafar, Handbuch der technischen Mykologie 4: 455-506. Jena.
Williams, C. N., 1959 - Spore size in relation to culture conditions. – Trans. Br. mycol. Soc. 42: 213-222.
Zycha, H., 1935 - Pilze II. Mucorineae. - Kryptogamenflora der Mark Brandenburg 6a. Leipzig.
Zycha, H., Siepmann, R. & Linnemann, G., 1969 - Mucorales. Eine Beschreibung aller Gattungen und Arten dieser Pilzgruppe. - Lehre.