(Ces.) Wils. and Related Species

Delevopment of Fructificationsin Colletotrichum Graminicola (Ces.) Wils. and Related Species

byB. C. Sutton

Reprinted fromCanadian Journal of Botany

Volume 44 (1966)

887

DEVELOPMENT OF FRUCTIFICATIONS INCOLLETOTRICHUM GRAMINICOLA (CES.) WILS.

AND RELATED SPECIES'

B. C. SUTTON2Department of Forestry of Canada, Forest Research Laboratory, Winnipeg, Manitoba

Received March 14, 1966

AbstractThe development of fructifications in Colletotrichum graminicola (Ces.) Wils.

is compared with that of other Colletotrichum species occurring naturally ongraminicolous and non-graminicolous hosts. Two types are distinguished: (a) thepulvinate in which the outer epidermal wall and cuticle are ruptured at the sametime by the developing conidiophores, setae, and stromatic tissue, and (b) thehypostromatic in which the outer epidermal wall is penetrated by fine hyphaefrom the epidermal stroma, the cuticle being ruptured separately by the setaeand conidiophores. Colletotrichum graminicola on a wide range of graminicoloushosts exhibits only the pulvinate type, but other Colletotrichum species developin either way depending on the nature of the substrate and the strain of fungusinvolved. The generic separation of C. graminicola from other species by thiscriterion is not accepted.

RésuméL'auteur compare le developpement des sporanges chez Colletotrichum gra-

minicola (Ces.) celui d'autres Colletotricha qui ont pour hetes naturelsdes plantes graminees ou autres. Deux processus s'observent: (a) celui du spo-range pulvine ou la membrane epidermique externe et la cuticule sent rompuesen meme temps par les conidiophores sous-jacents, les poils et par le tissu stroma-tique ; et (b) celui de type hypostromatique oh la membrane epidermique externeest attaquee par les hyphes fins qui proviennent des stroma epidermiques; la cuti-cule est rompue separement par les poils et les conidiophores. Le premier proces-sus a ete observe, b. l'exclusion de l'autre, chez Colletotrichum graminicola surune grande variete d'hOtes-gramines. Par centre, les sporanges d'autres Colleto-tricha se developpent d'apres les deux manieres, selon la nature du lit ou de lalignee. L'auteur n'accepte pas ces caracteres comme generiques at considere queC. graminicola doit titre garde dans le genre Colletotrichum.

IntroductionForm genera of the Fungi Imperfecti have been assigned to orders and

families on the basis of major differences in the type of fructification on which,or in which, conidia are formed.

Much of the confusion surrounding the taxonomy of Colletotrichum Cordaand Vermicularia Tode is directly due to excessive emphasis being placed oncharacters of the fructifications. Colletotrichum has been placed in the Melan-coniales (Saccardo 1884), the Acervulales (Potebnia 1910), and the Stroma-taceae (Hanel 1923), and Vermicularia in the Gymnomycetes (Fuckel 1869),the Sphaeropsidales (Saccardo 1884), the Pseudopycnidiales (Potebnia1910), the Tuberculariaceae (Hohnel 1923), and the Melanconiales (Grove1937). Archer (1926) and Duke (1928) assigned both genera to the Melan-coniales and showed that there is no reasonable basis for keeping them apart.

'Part of a thesis presented to the University of London, England, in partial fulfilment ofthe requirements for the degree of Doctor of Philosophy.

'Formerly assistant mycologist at the Commonwealth Mycological Institute, Ferry Lane,Kew, Surrey, England.

Canadian Journal of Botany. Volume 44 (1966)

888 CANADIAN JOURNAL OF BOTANY. VOL. 44, 1966

Attempts to evolve a more satisfactory means of separating form-generaand taxa above the generic level in the Fungi buperfecti originated with thework of Costantin (1888), but it was Archer (1926), working with pycnidialand acervular fungi in culture, who questioned the reliability of using grossfeatures of the fructifications in the taxonomy of these particular groups.Mason (1937) suggested that too much emphasis had been placed on pycnidia,acervuli, and sporodochia in current classification, and interpreted them allas forms of a fungal stroma.

Vassiljevsky and Karakulin (1950) suggested that the development of thefructification in Colletotrichum graminicola (Ces.) Wils. differed fundamentallyfrom that in other members of the genus and proposed adopting DicladiumCes. for this species. They tentatively assigned C. falcatum Went to the samegenus. This type of development in which setae and conidiophores are initiatedbetween the cuticle and the outer epidermal wall was first described for C.falcatum by Edgerton and Carvajal (1944).

The problem of defining generic limits in the Colletotrichum complex ofgenera necessitates a consideration of conidium morphology, conidiophoredevelopment, presence and distribution, or absence, of setae, and type offructification. The purpose of the work described here was to determine anydifferences in fructification development for straight- and falcate-sporedColletotrichum species on graminicolous hosts that might be useful taxonomiccriteria at the generic level, and to examine the generic concepts advancedby Vassiljevsky and Karakulin for C. graminicola in relation to the range ofgeneric criteria available for defining Colletotrichum.

Reference to material examined during this study is made by citing acces-sion numbers of the IM I herbarium.

HistoricalA brief account of the taxonomic and nomenclatural history of C. gramini-

cola and related fungi is essential to place in perspective the generic reorgani-zation suggested by Vassiljevsky and Karakulin.

Vermicularia Tode (1790) was described with three species, but since thestarting point for Fungi Caeteri is 1 Jan. 1821 (Fries 1821), the validatingauthority for Vermicularia is Fries (1825). It was overlooked by Duke (1928)that Vermicularia Tode ex Fries is a later homonym of Vermicularia Meunch,1802 (Verbenaceae), and until such time as the starting point is changed to anearlier date than 1802, Vermicularia Tode ex Fries must be regarded asillegitimate.

Colletothrichum was originally described by Corda (1831-32) with a singlespecies but he later changed the name to Colletotrichum (Corda 1837). Therelationship between Vermicularia and Colletotrichum has been obscured bythe original diagnosis of Vermicularia, which by modern standards, is quiteinadequate. Duke (1928) studied this particular aspect and concluded thatColletotrichum and Vermicularia are not distinct. However, Grove (1937),Vassiljevsky and Karakulin (1950), and Negru (1960) maintained the separa-tion of the two genera.

Dicladium Cesati (1852) was based on a single species, D. graminicola

SUTTON: FRUITING OF COLLETOTRICHUM 889

Cesati, described from Echinochloa crus-galli (L.) Beauv. and Zea mays L.The name was transferred to Vermicularia by Westendorp (1861) becauseof the falcate conidia and setose fructifications. Saccardo (1886) placed thefungus in Steirochaete Braun & Casp. but noted that it may be a Colletotrichum.By 1900 several similar falcate-spored species from Gramineae had beendescribed in Vermicularia and Colletotrichum, including C. falcatum on sugar-cane.

Ellisiella Sacc. (1880), described with the single species E. caudata Sacc.from Sorghum nutantis, was referred by Peck (1885) to Colletotrichum, butthe formal combination was not made.

In general studies on these genera, Marchionatto (1947) adopted Colleto-trichum for straight-spored species with subepidermal acervuli and Vermicu-laria for species with straight spores formed in pseudopycnidia. The falcate-spored species were at first referred to Ellisiella Sacc. but after studying theoriginal description of this genus he preferred to place them in ColletotrichopsisBubak. Wollenweber and Hochapfel (1949) preferred to adopt Vermiculariafor the falcate-spored species. The conclusions of all these workers were notbased on type studies. Despite this, Muntafiola (1952) followed Marchionatto'ssuggestion and transferred Dicladium graminicola Ces. to Colletotrichopsis.The issue was further complicated by Camara (1949), who included Ellisiellacaudata Sacc. (as E. caudata (Peck) Sacc.), the monotype species of Ellisiella,in his newly erected genus Ellisiellina Camara. Batista (1956) eventuallyselected E. caudata as the lectotype species of Ellisiellina and then createdfurther confusion by transferring to it the names of some species formerlyplaced in Colletotrichum and Vermicularia. Since Ellisiellina Camara is basedon the same type species as Ellisiella Sacc. it automatically becomes an obli-gate synonym of the earlier described name. The genus Ellisiella, althoughmonotypic when originally erected by Saccardo, was provided with a 'newlectotype' species (E. hydrangeae Camara) by Batista (1956). Thus reconsti-tuted, it should be known as Ellisiella Batista (1956), which is a later homonymof Ellisiella Saccardo (1880), and therefore illegitimate. Following Marchion-atto and Muntatiola, Batista removed to Colletotrichopsis the species formerlyplaced in Ellisiella Saccardo. This genus was considered by Arx (1957a) tobe inseparable from Colletotrichum. The position concerning Ellisiella issummarized as follows:

Ellisiella Sacc. (1880)Type species: E. caudata Sacc.Ellisiellina Camara (1949), obligate synonym of Ellisiella Sacc.Original species: E. biciliata Camara, E. caudata (Sacc.) Camara (as

' (Peck) Camara')Lectotype species: E. caudata (Sacc.) Camara selected by Batista (1956).

Ellisiella Batista (1956) (as `Sacc. emend. nobis'), later homonym of El-lisiella Sacc.Type species: E. hydrangeae Camara and da Luz

Shear and Wood (1913) established a firm experimental basis to the modernconcept of Colletotrichum when a large number of species previously differ-entiated by slight and inconsistent morphological characters and the supposed


fixity of very narrow host ranges, were relegated to synonymy with C. gloeo-sporioides (Penz.) Sacc. Although his conclusions were based solely upon theexamination of herbarium material, Wilson (1914) adopted a similar procedurewith Dicladium graminicola. He transferred the name to Colletotrichum andreduced 10 more to synonymy. C. falcatum and Ellisiella caudata were notincluded. Boning and Wallner (1936) extended Wilson's synonymy butmaintained C. falcatum as distinct. Vassiljevsky and Karakulin (1950) revertedto the original name Dicladium graminicola on the basis of a specific type offructification development but Arx (1957b) reappraised Colletotrichum andproposed a broad concept of the species. He also adopted Glomerella tucu-manensis (Speg.) Arx and Muller (previously described as the perfect state ofC. falcatum, the red rot pathogen) for all falcate-spored graminicolous Col-letotrichum species. C. graminicola was newly described as the conidial state ofG. tucumanensis, and C. falcatum, E. caudata, and C. zeae Lobik were includedin a synonymy of 36 names. Until the work of Vassiljevsky and Karakulinmost of the taxonomic complications concerning Colletotrichum involvedconidium shape and the distribution of setae in fructifications. The intro-duction of developmental concepts of the fructification and the subsequentnomenclatural changes have not clarified the position. Although Arx hasadopted a modern broad concept of Colletotrichum, the narrower views ofVassiljevsky and Karakulin have not been examined in detail.

ObservationsPulvinate Development

As a typical example of pulvinate development, C. lindemuthianum (Sacc.& Magn.) Bri. and Cay. on pods of Glycine max (L.) Merr. (IMI 93255b) isdescribed. The immersed mycelium was composed of hyaline to subhyaline,branched, septate, smooth-walled hyphae, 1.5-2.5 ,a wide. Hyphae were intra-cellular, and extensively penetrated the necrotic pod tissue. They were denselyaggregated into a pseudoparenchymatic stroma in the epidermal cells and oneor two rows of parenchyma below the region in which fructifications were tobe formed. Early in development of the fructifications, the lateral epidermalwalls were ruptured near the junction withh the outer epidermal walls followedby a simultaneous break in the outer epidermal wall and cuticle. As setae,conidiophores, and hyphal pseudoparenchyma were produced, the cuticleand outer epidermal wall were pushed aside (Fig. 2). Essentially the same typeof formation was described for this species by Barrus (1921). Young stages indevelopment were more easily observed in C. lebbeck (Syd.) Petrak on podsof Albizia lebbeck (L.) Benth. (IMI 93032). Immersed hyphae were largelyaggregated in the epidermis and diffusely ramified in the deeper tissues.

FIG. 1. Colletotrichum lebbeck on Albizia lebbeck IMI 93032. Pulvinate development;outer epidermal wall and cuticle elevated but not ruptured. 260X

FIG. 2. Colletotrichum lindemuthianum on Glycine max IMI 93255b. Pulvinate devel-opment; ruptured cuticle and outer epidermal wall. 420X

FIG. 3. Colletotrichum capsici on Ananas comosus IMI 63262. Hypostromatic develop-ment; conidiophores and setae formed between outer epidermal wall and cuticle. 825 X

FIG. 4. Colletotrichum agaves on Sansevieria sp. IMI 948886. Pulvinate development;epidermis ruptured between the lateral and inner walls. 120X

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Conidiophores and setae were formed in the epidermal cells after the lateralwalls had been broken near the junction with the outer epidermal walls andthe latter became elevated after inception of conidium formation (Fig. 1).Finally, the outer epidermal wall and cuticle were ruptured simultaneously.Failure of the fungus to rupture the outer epidermal wall early in develop-ment may be due to some extent to the width of the wall which averaged 6 Ain thickness. Almost the same method of development occurred in C. capsici(Syd.) Butl. and Bisby on pods of Capsicum annuum L. (IMI 93451) wheremore extensive formation of pseudoparenchyma occurred after rupture of theepidermis and cuticle. Conidiophores and setae were produced after ruptureof the epidermis and cuticle whereas in C. lebbeck they were formed withinthe epidermis before emergence. In these particular collections of C. lebbeckand C. capsici, the outer epidermal walls were appreciably thicker than thoseof Glycine max but this had no effect on the basic type of development.

The epidermal structure of Sansevieria sp. had no effect on egress by C. agavesCay. (IMI 94888b). The outer epidermal cell walls averaged 17 inin thick-ness. The lateral walls were thickened near the junction with the outer wallbut tapered towards the inner epidermal wall which was 3 A thick. As theaggregation of hyphae in the epidermis and immediate three to four layers ofparenchyma increased in size, the epidermis was ruptured at the weak junctionbetween the lateral and inner walls (Fig. 4). This was concomitant with therupture of the outer wall and cuticle as conidium formation began.

One collection of C. dematium (Pers. ex Fr.) Fr. on Bromus sp. (IM I 98131)developed in precisely the same way as collections of the same species on non-graminicolous hosts. Immersed hyphae were intracellular and densely aggre-gated into a pseudoparenchymatic stroma in the epidermal cells and theimmediate palisade tissue beneath the developing fructification. The outerepidermal wall and cuticle were ruptured after the breaking of the lateralthin epidermal walls. Similarly a single collection of C. gloeosporioides onseeds of Sorghum vulgare Pers. (IMI 73667a) was pulvinate. The immersedhyphae were intracellular and concentrated in the four outer cell layers ofthe testa. Stages in formation of the fructifications were identical with othercollections of the species on several different hosts.

The pulvinate type of development has been reported for most of theColletotrichum species, and has been confirmed in this study for the followingspecies in addition to those mentioned elsewhere in this paper.

C. acaciae Gutner, C. brachytrichum Delacr., C. circinans (Berk.) Vogl.,C. coccodes (Wallr.) Hughes, C. higginsianum Sacc., C. lagenarium (Pass.)Ell. & Halst., C. lini (Westd.) Tochinai, C. musae (Berk. & Curt.) Arx, C.trichellum (Fr. ex Fr.) Duke, and C. trifolii Bain and Essary.

F IG. 5. Colletotrichum graminicola on Zea mays IMI 84301. Hypostromatic develop-ment; initial stages in elevation of cuticle. 1050 X

FIG. 6. Colletotrichum gloeosporioides on Cortaderia sp. IMI 95720. Hypostromaticdevelopment; stroma formed after egress. 325 X

F IG. 7. Colletotrichum dematium on Calamagrostis sp. IMI 102150b. Hypostromaticdevelopment from sclerotium. 550 X

FIG. 8. Colletotrichum graminicola on Sorghum vulgare IMI 67789b. Hypostromaticdevelopment; minute hyphae penetrating outer epidermal wall. 1400 X


Hypostromatic DevelopmentTo illustrate the basic features of this method, the fructifications of the

*lectotype collection of Dicladium graminicola Ces. ( = Colletotrichum gra-minicola (Ces.) Wils.) on Zea sp. are described.

The collection consisted of a dried culm mounted with a reproduction ofthe original description. No necrotic symptoms were associated with thefructifications which were sparse, lenticular, vein-limited, 200-400 X 100 A.

A few dark brown, rigid, thick-walled setae with irregular bulbous baseswere present but most were broken near the base. Undamaged setae weretapered towards lighter acute apices, 1- to 6-septate and 150 ,u long by 7wide at the base. No intact conidia were found. Wilson (1914) also examinedsome of Cesati's material and stated "conidia were the same as for Colleto-trichum cereale" and gave the average size as 20 X 4 A. Setae were described as115 bt long.

Sections 5-10 u thick showed extensive intracellular penetration of theepidermal cells, parenchymatic fiber cells, and unthickened parenchyma.Hyphae were more abundant in the epidermis, and lateral development inthis layer was in excess of that in the deeper parenchymatic fiber tissue. Im-mersed hyphae were subhyaline to mid brown, smooth-walled, septate,branched, 3.5-7 diam. Small penetration hyphae measuring 0.5-0.75 tdiam. were produced from the vegetative mycelium in the epidermal cells.They penetrated the outer epidermal wall subsequently to form conidiophoresand setae between this wall and the cuticle. Between the outer epidermalwall and the cuticle the penetration hyphae enlarged to produce setal andconidiophore initials. The cuticle ruptured as setae and conidiophores in-creased in size and finally it curled back towards the host surface. Collectionsof C. graminicola on seeds of Zea mays (IMI 84301) (Fig. 5) and leaves ofSorghum vulgare (IMI 67789b) (Fig. 8) showed early stages of developmentparticularly well.

This method was described by Edgerton and Carvajal (1944) for C. falcatum,by Vassiljevsky and Karakulin (1950) for D. graminicola, and by Saccas (1954)for C. graminicola. The latter species is figured as completely superficial innatural infections by Arx (1957b), Chowdhury (1936), and Muntanola (1952).

In the present study, collections of C. graminicola on leaves, seeds, and culmsof Zea mays (14 collections) and Sorghum spp. (43 collections) revealed nosignificant difference in development for most of the specimens but two ex-ceptions were found. The fructifications in a sample of C. graminicola onsenescent leaves of Zea mays (IMI 59856b) were produced in the most parthypostromatically. Fructifications were also formed in association withstomata. Guard cells, adjacent epidermal cells, surrounding parenchyma, andthe substomatal chambers became fully penetrated by hyphae. The sub-stomatal mycelium grew through the stomatal opening to form superficialconidiophores and setae. The development of a superficial stroma sometimes

* D. graminicola Ces. was originally described from Echinochloa crus-galli and Zea mays.Material borrowed from Herb. B (Berlin) and labelled Dicladium graminicola, Italy, V. Cesati,1852 was submitted to Dr. C. R. Metcalfe, Jodrell Laboratory, R. B. G., Kew for host deter-mination. He reported as follows: "In all probability this is Zea, but the material is too scrappyto be absolutely certain. The epidermal structure agrees reasonably well with Zea, but un-fortunately the epidermis of Zea is somewhat variable which makes identification difficult!"

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occurred with a mat of hyphae extending over the stomatal opening. A singlecollection of C. graminicola on culms of Zea mays (IMI 38604b) showed stagesin fructification development which were similar to those described for thelectotype of C. graminicola. However, the epidermis and parenchyma wereparticularly thick-walled and during development of the fructification theseelements became disorganized and separated from one another. Excessivesuperficial vegetative growth and complete loss of the cuticle were associatedwith such disorganization. The fructification finally appeared similar to asuperficial sporodochium.

Most collections of C. falcatum on sugarcane developed in a manner com-parable to that for C. graminicola but one sample on a culm of Saccharumofficinarum L. (IMI 75930) showed almost constant association of fructifica-tions with thin-walled epidermal cells. Most epidermal cells were stronglythickened with small reduced lumina but approximately 20% had thinnerlateral and outer walls. Although development was again hypostromatic,more fructifications were produced from the thin-walled epidermal cells andsuperficial vegetative growth often occurred after egress in these cases. Hoof(1949) illustrated a fungus on Sorghum vulgare, which he named C. falcatum,as developing in both a pulvinate and hypostromatic manner. No attemptwas made to correlate the type of development to the structure of the epider-mis of the host.

Hypostromatic development has been confirmed in collections of C. gram-inicola on the following additional graminicolous hosts: Andropogon hirtusL., A. sp., Arundinella sp., Avena sativa L., Axonopus compressus (Swartz)Beauv., A. sp., Chasmopodium sp., Chloris gayana Kunth., Cortaderia selloana(Schult.) Aschers & Graebn., Cynodon dactylon (L.) Pers., Digitaria spp.,Echinochloa crus-galli, Hierochloa sp., Hyparrhenia spp., Paspalum dilatatumPoir., P. platense Spreng., Pennisetum clandestinum Hochst. ex Chior., P.purpureum Schumach., Phacelurus sp., Phleum pratense L., Poa annua L.,Rottboellia exaltata L., Sorghum halepense (L.) Pers., S. sudanense Stapf, S.spp., and Sporobolus sp.

Hypostromatic development is not restricted to C. graminicola. Severalcollections of C. dematium (Pers. ex Fr.) Grove, a species readily separablefrom C. graminicola by spore shape and size, were found to show the same typeof development on graminicolous substrates. These included collections onLolium perenne L. (IMI 98132) , Calamagrostis epigeios (L.) Roth. (IMI 21050) ,C. neglecta (Ehrh.) Gaertn., Mey. & Schreb. (IMI 60849), C. sp. (IMI 102150b),Andropogon sp. (IMI 98553b), Setaria sp. (IMI 98926b), and Poa annua(IMI 93035). On Lolium perenne, fructifications were formed in a hypostro-matic manner not only from sclerotia but also from aggregations of hyphae inthe epidermis. Similarly on Calamagrostis sp. the conidiophores and setae wereseated directly on the outer epidermal wall and originated from thick-walleddark brown sclerotioid hyphal cells in the epidermis (Fig. 7). On Poa annuasome superficial vegetative growth occurred after penetration of the outerepidermal wall to produce a pulvinate stroma up to 35 p in depth. Conidio-phores and setae were formed on the external face of the stroma. In one collec-tion of C. gloeosporioides on Cortaderia sp. (IMI 95720) extraepidermal vegeta-tive growth following hypostromatic development did occur (Fig. 6) but was


not as marked as in C. dematium on Poa annua. It is also pertinent to notethat a collection of C. capsici (Syd.) Butl. & Bisby on Ananas comosus (L.)Merr. (Bromeliaceae) (IMI 63262) developed in the same way as C. gramini-cola (Fig. 3). This was the only sample found in which hypostromatic develop-ment occurred in a Colletotrichum species infecting a non-graminicolous host.An identical method of development has been described for Annellolaciniadinemasporioides Sutton on Ananas spp. (Sutton 1964).

In the genus Ellisiella, which differs from Colletotrichum in having conidiawith a single apical appendage, four collections on graminicolous substrateswere examined: on Cymbopogon sp. (IMI 79777), Imperata arundinaceaCyrillo (IMI 24908), I. cylindrica (L.) Beauv. (IMI 51304), and Sacciolepisindica (L.) Chase (IMI 38874). In all collections the type of developmentwas identical with that described for C. graminicola. There was a minimalamount of extraepidermal vegetative development in some collections butin no case was the epidermis disorganized.

ConclusionsA broad concept of Colletotrichum has been adopted. Within the generic

limits defined by Arx (1957b) there are two distinct ways in which Colleto-trichum fructifications may develop.

The first type of development is termed pulvinate (Ainsworth and Bisby1961) and implies the rupture of the host cells by mechanical force. In mostspecies the lateral epidermal walls are ruptured by the developing mycelium.Cuticle and outer epidermal wall are broken simultaneously as the emergentconidiophores, setae, and vegetative cells increase in size. Conidiophores andsetae may be initiated before, during, or after the outer layers of host cellsare broken. This depends to some extent on the amount of stromatic tissueproduced under the particular environmental conditions. The second methodis termed hypostromatic, a term coined here to describe the position of thevegetative stroma in relation to the outer epidermal wall. It implies that thefungus either possesses the necessary enzyme system for degradation of specificregions of the outer epidermal wall (Wood 1960) or emerges solely by mechani-cal force in a similar way to the process of penetration and ingress showngenerally by most pathogens. It is typical of C. graminicola, C. falcatum, andmore rarely of some Colletotrichum species, occurring on graminicolous hosts.Small hyphal threads from the intraepidermal stroma penetrate the outerepidermal wall to form the setal and conidiophore initials between the walland the cuticle. The latter is ruptured separately by the subsequent enlarge-ment of setae and conidiophores. Vegetative development sometimes occursafter egress to produce a reduced type of stroma but this is infrequent. Fungishowing this tendency are still considered in this group if the outer epidermalwall is penetrated separately by fine hyphae. Finally the cuticle may becompletely sloughed-off leaving an apparently superficial fructification.Some earlier workers thus included C. graminicola (as Dicladium graminicola)with Ellisiella in the Hyphomycetes.

If the hypostromatic type of development were rigidly restricted to C.graminicola on one hand and the rest of the Colletotrichum species on theother, there would be some justification for supporting the generic separation

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suggested by Vassiljevsky and Karakulin (1950). However, if this systemwere to be followed literally, it would be necessary to remove to Dicladiumnot only C. graminicola but some falcate and straight-spored hypostromaticstrains of species which are normally pulvinate on other hosts. These arestrains which only differ from the 'normal' strains in the type of fructificationdevelopment. There is no difference in the characteristic shape of conidia insuch species on graminicolous hosts and no difference in method of conidiumformation. Observations do not support this separation. Hypostromaticdevelopment has been found not only in C. graminicola and C. falcatum butin C. dematium on five different graminicolous substrates and C. gloeosporioideson a single graminicolous substrate. The latter two species are pulvinate ontheir normal non-graminicolous hosts and it is interesting to note here thatthey were found to develop in their normal pulvinate manner in collectionson two graminicolous hosts. C. gloeosporioides and C. dematium are readilyseparable from C. falcatum and C. graminicola by spore shape and size so thepossibility of misidentification may be excluded. Another interesting exampleof hypostromatic development was the egress of C. capsici on leaves of Ananascomosus (Bromeliaceae). C. capsici is normally pulvinate on a wide range ofdicotyledonous hosts. This species developed in the same way as A nnellolaciniadinemasporioides on the same substrate. Both were comparable with thesamples of C. graminicola studied. Similarly the Ellisiella species which wereexamined, all on graminicolous substrates, produced hypostromatic fructi-fications.

Although there have been reports of C. graminicola from non-graminicoloushosts (Seymour 1929; Tiffany and Gilman 1954; Anonymous 1960), examplesof differences in development of fructifications have not been found in theliterature. Such identifications have not been subsequently confirmed andmust remain in doubt (Sutton 1962; Zwillenberg 1959), but a study of thedevelopment of fructifications in C. graminicola on non-graminicolous sub-strates, if the host range indeed extends beyond the Gramineae, would assistin clarifying developmental concepts.

Factors governing the egress of Colletotrichum species include the mechanicalforce the fungus can exert, the range of enzymes available for degradingbarriers to egress, and the ratio of pectin to cellulose in the outer epidermalwall and cuticle of the host (Wood 1960). The possibility that the width of theouter epidermal wall may provide an indirect structural limitation on theability of some strains or species to develop in a pulvinate manner was notexamined fully. From the different species and substrates studied no satis-factory conclusions could be drawn. Hypostromatic development occurredon hosts with outer epidermal walls varying from 0.7 to 5.0 p in thicknessand pulvinate development with walls from 1.5 to 20 A in the thickness. Ifhypostromatic development was merely a response by the fungus to a struc-tural limitation on egress by the host one would expect hypostromatic devel-opment to occur when the outer epidermal wall is particularly thick. However,this did not consistently occur.

In the light of such evidence it is preferable to consider both types of devel-opment as functions of the fungus—host relationship, the final method ofdevelopment being dependent on the strain of fungus involved and the nature


of the host. Since there are no major differences in conidium morphology,phialidic type of conidiophore development, and distribution of setae, thetwo types of development, shown by C. graminicola on one hand and the restof the C. species on the other, cannot be used for generic separation in the waythat Vassiljevsky and Karakulin suggest. Therefore Dicladium is consideredsynonymous with Colletotrichum.

In any system of classification Ellisiella Sacc. must be placed close toColletotrichum graminicola and C. falcatum because apart from the strikingsimilarity in fructification development there are no differences in conidiumand conidiophore ontogeny or in presence and distribution of setae. Ellisiellais for the present kept apart from Colletotrichum because of the difference inconidium morphology but until Ellisiella species are studied in culture theseparation of this genus from Colletotrichum must be tentative.

AcknowledgmentsThe author is grateful to Dr. J. Kohlmeyer for permitting him to examine

material in his keeping at Herb. B, to Dr. D. G. M. Muller and Mrs. P.Hackett for providing translations of foreign texts, to Mr. E. R. Raynerfor preparing the plates, and to the CM I staff for their interest and helpduring the progress of this study.

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(Ces.) Wils. and Related Species

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