Ramulariopsis Speg., Pseudovularia Speg., Didymariopsis speg. and Ramulaspera holci-lanati (Cav.) Lindau

October 1972

Vol. 59, Part 2 Trans. Br. mycol. Soc. 59 (2), 185-191 (1972) Printed in Great Britain

RAMULARIOPSIS SPEG., PSEUDOVULARIA SPEG., DIDYMARIOPSIS SPEG. AND RAMULASPERA HOLCI-LANATI (CAV.) LINDAU By F. C. DEIGHTON Commonwealth Mycological Institute, Kew (With Plate 29 and 2 Text-figures) The material of the types of the three monotypic genera, Ramulariopsis, Pseudooularia and Didymariopsis, in Herb. LPS show that Ramulariopsis can be considered a well-characterized and distinct genus, while Pseudouularia is not distinguishable from Ramularia Unger, and Didymariopsis is a synonym of Colletotrichum Corda. There being no character by which Ramulaspera holci-lanati can be distinguished generically from several species (including the type) of Ramularia, the new combination Ramularia holci-lanati (Cav.) Deighton is proposed.

Spegazzini, An. Mus. naco Hist. nat. B. Aires ~O, 421 (1910). Spegazzini described the characters of this genus as: 'hyphae hyalinae nodoso-articulatae dichotomice V. alterne ramosae; articuli facile soluti apice infero attenuato-truncati, supero breviter capitato-bilobi, in conidiis sensim transeuntes; conidia cylindracea, 1 -septata non catenulata concoloria ' . In his description of the type (and only) species he said: 'articuli hypharum continui (25-30 P,=5 p,), lobulorum apicalium altero integro altero minute bidentato; conidia quandoque leniter fusoidea quandoque vix subclavulata utrinque plus minusve acutiuscule rotundata (20-50 p, =5-7 p,), primo continua dein 1, rarius 2, - septata, ad septa non V. obsoletissime constricta, recta v. parum inaequilateralia hyalina laevia ', Type (and only) species; R. cnidoscoli Speg. The material (LPS) of the two syntypes of R. cnidoscoli was examined, and it is considered that Spegazzini's description and his interpretation of the characters of this fungus need modification. The following is an amended description of the species. RAMULARIOPS1S

RAMULARIOPS1S CNIDOSCOLI

20, 422 (1910).

(Fig.

Spegazzini, An. Mus. naco Hist. nat. B. Aires

1)

Leaf spot merely a diffuse pale discoloration of affected areas, with indefinite margin. Caespituli hypophyllous, aggregated along the veins of the leaf or over orbicular areas, slightly yellowish. Mycelium internal, copious; hyphae almost colourless, branched, septate, r-5-3 p,m wide. Stromata up to 65 p,m wide and 40 p,m high, developing in the spongy mesophyll (probably at least at first substomatal), developing a slight Vol. 59, Part 12

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Fig.

I.

Ramulariopsis lIIIidoscoli. Conidiophores and conidia, from LPS 12851, lectotype.

yellowish-brown colour with age, numerous and densely aggregated, finally becoming contiguous, composed of dense aggregations of mycelial hyphae and bursting through the epidermis (probably at first through the stomata) and developing into dense fascicles of numerous conidiophores. Conidiophores colourless, erect, thin-walled, smooth, simple or occasionally

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once branched towards the base (the branch being about as long as the main limb), rarely with a very short lateral branch, distantly septate (rather more closely septate in the fertile apical portion, up to at least 170 pm long, 2'S-3 pm wide near the base, 3·S-6·S pm wide in the distal portion, bearing a terminal conidial scar or group of scars and single scars or groups of scars on short lateral protrusions which arise from the upper nodes just below the septa. Conidia colourless, thin-walled, smooth, subcylindric or subfusiform, mostly straight, occasionally slightly curved or irregular, catenulate, sometimes in branched chains, the terminal conidia broadly obtuse at the apex, 0-4 septate, not or only very slightly constricted at the septa, IS-60 pm long, 4'S-6 pm wide. The scars on the conidia and on the conidiophores are slightly but distinctly thickened, only very slightly prominent, I -2 pm diam. On leaves of Cnidoscolus cnicodendron Griseb. and C. vitifolius PoW in Argentina. It will be seen that what Spegazzini considered to be dichotomously or alternately branched 'hyphae' (i.e. conidiophores) with segments readily separating are here regarded as conidiophores producing conidia in branched chains in the same manner as those of Ramularia and Cladosporium, in which genera the conidia often remain attached to one another and to the conidiophores for a considerable time: a phenomenon more easily observed in fresh specimens. In Ramularia a single conidium or a single conidial chain (simple or branched) is produced terminally on the conidiophore and the old conidial scar becomes displaced to a lateral position as a result of the sympodial proliferation of the conidiophore. In Ramulariopsis, however, after the first terminal conidium or conidial chain has been produced, a second or even a third is produced from a point close to the first one, so that eventually a small crowded group of old conidial scars is to be seen on the now somewhat swollen apex of the conidiophore. Further conidia are produced later from one or more intercalary lateral protuberances some distance below the apex of the conidiophore, and these intercalary protuberances may bear more than one conidium and become nodose. Somewhat the same characters are to be seen in Fulvia Ciferri in which, however, the lateral protuberances at the nodes of the conidiophores sometimes proliferate into short branches and the conidiophores and conidia are distinctly olivaceous in colour. The definition of Ramulariopsis is therefore amended. Speg, char. emend. A Ramularia Unger differt conidiis in gregibus parvis ad apicem et ad nodos intercalares conidiophororum effectis. RAMULARIOPSIS

Specimens examined. On Cnidoscolus cnicodendron, Salta, Oran, Argentina, iv. 1905, C. Spegazzini, LPS 12850, syntype (slide, 1M19II81). On Cnidoscolus vitifolius, Jujuy, Ledesma, Argentina, iv. 1905, C. Spegazzini, LPS 12851, syntype and lectotype (slides, 1M1 91182). (LPS 12850 is rather poor material and LPS 12851 is better designated the lectotype.)

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DIDYMARIOPSIS Spegazzini, An. Mus. naco Hist. nat. B. Aires 20,424 (1910).

Spegazzini described this genus briefly: 'Est Didymaria hyphis olivaceis conidiisque hyalinis donata.' The type (and only) species, D. cuphaeicola Speg., was figured and described on the same page as follows: 'acervuli saepius epiphylli penicilliformes, ex hyphis tenuibus (100-200 p=6 p) fuligineis apice subhyalinis laxeque denticulatis efformati; conidia saepius cylindracea rarius subclavulata utrinque rotundata (14-20 P=5-6 p) primo continua dein medio 1 -septata non constricta hyalina, aerogene solitaria'. The material of the type species (on leaves of Cuphaea mesostemon Koehne, near Metan, Salta, Argentina, vi. 1905, C. Spegazzini, LPS 12761: slides, IMI 9II80) was examined by my colleague Dr B. C. Sutton who identified it as the conidial (Colletotrichum) state of Glomerella cingulata (Stonem.) Spauld. & Schrenk. The type material bears a plentiful growth of the fungus which is undoubtedly the one that Spegazzini described. The genus Didymariopsis Speg. is therefore a synonym of Colletotrichum Corda. PSEUDOVULARIA

Spegazzini, An. Mus. naco Hist. nat. B. Aires 20, 418 (1910).

Spegazzini's brief description of this genus was: 'Est Ovularia conidiis globosis pleurogenis et acrogenis donata.' The type (and only) species, P. trifolii Speg., was figured and described as follows: 'Maculae suborbiculares indeterminatae 3-5 mm. diam. centro subcinerascentes, ambitu subrufescentes. Hyphae caespitulorum erectiusculae superne acuminatae inferne non incrassatae (500-700=5-7 p) continuae V. r-g-septatae hyalinae, in parte dimidia superne sigmoideoflexuosae ad angulos vix denticulatae; conidia sursum rotundata deorsum minute papillata (7-10 p diam.) laevia punctulato-nubilosa.' The figure (500-7°0 pm) given in the published description as the length of the conidiophores is obviously a typographic error. On the packet of the type collection (a photograph of which is here reproduced as Plate 29) Spegazzini's measurements at the side of his figure of a conidiophore fascicle are 50-100 x 5-7 p. The type material (LPS), which was in very poor condition, was unfortunately lost in the post when it was returned but a slide showing the one complete, though rather collapsed conidiophore 85 pm long (depicted here in Fig. 2), the bases of the other conidiophores in the fascicle and a number of conidia, was later sent to LPS together with a photograph of the type packet with Spegazzini's drawings. A pencilled note, signed Sarasola, inside the type packet stated that conidiophores were not seen but the spores are similar to those of Ovularia viciae in form and dimensions. Material of Ovularia viciae (Frank) Sacco (== Ramularia viciae Frank) has not been available to me: its conidia are said to be 10·5 x 7.8 usn. Ovularia sphaeroidea (Sacc.) Sacco (== Ramularia sphaeroidea Sacc.) has subglobose conidia, 8-10 pm diam, which are very minutely rough-walled though not quite as closely verruculose as in Pseudovularia trifolii. Similar minutely rough-walled conidia are to be found in Ramularia pusilla Ung. (the type species of Ramularia) and in Ramulaspera

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/

)0

o

00

o o

B

o

A

lOpm

Fig. 2. A, Ramularia argentinensis, six conidia and a collapsed conidiophore, from LPS 12946, the type of Pseudooularia trifolii. B, C, R. holci-lanati; B, four conidia from the type (K); C, three conidia and a conidiophore from IMI 136573 (New Zealand specimen).

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holci-lanati (Cav.) Lindau. There seems to be no reason to separate Pseudovularia Speg. from Ramularia Unger, to which genus its type species (which is only known from the type collection) is therefore transferred with a new name, R. argentinensis, since there is already Ramularia trifolii J aap, which is very different. The following description is based on Spegazzini's description and an examination of the type material. Ramularia argentinensis Deighton, nom.nov. (Fig. 2A, PI. 29)

== Pseudooularia trifolii Spegazzini, An. Mus. naco Hist. nat. B. Aires 20, 418 (1910); non Ramularia trifolii Jaap, Verh. bot. Ver. Provo Brandenb, 52, Abh.: I I (1910). Leafspots suborbicular, 3-5 mm diam, without definite margin, becoming greyish in the centre and somewhat reddish at the edge. Conidiophores hypophyllous, emerging through the stomata in dense fascicles of 24 or more from a colourless stroma which appears to be about 40 p,m wide. Conidiophores colourless, smooth, erect, thin-walled, continuous or with a few distant septa not readily visible, substraight but slightly angled at the old conidial scars, 50-100 p,m long, 2'5-5 p,m (mostly 4'5 p,m) wide though Spegazzini says 5-7 p,m wide. Old conidial scars conspicuously thickened and slightly prominent, about I p,m diam. Conidia colourless, subglobose or broadly ellipsoid, with a conspicuously thickened and slightly prominent convex hilum about I p,m diam, continuous, very minutely and closely rough-walled, 7-1 I x 6'5-8'5 p,m. On leaves of Trifolium pretense Linn. in Argentina. Specimen examined. On Trifolium "platense' [pratensc], Lezama, Argentina, 2. xi. 1904, C. Spegazzini, LPS 12946, type (slide, 1M192834).

Ramularia holci-lanati (Cav.) Deighton, comb.nov. (Fig. 2B, C) == Ovularia holci-lanati Cavara, Fungi Longobardiae exsiccati 144 (1893). == Ramulaspera holci-lanati (Cav.) Lindau, Rabenhorst's Kryptogamen-Flora, 2 Aufl., I Bd, 8 Abt.: 260 (1905)'

Stroma absent. Conidiophores few to a fascicle, emerging through the stoma in a single row and not breaking the stoma, colourless, smooth, thin-walled, erect, substraight but sometimes slightly angled at the old conidial scars, simple or occasionally sparingly branched, 1-2 septate (sometimes continuous above a septum situated about 10 p,m from the base), up to 235 p,m long, up to 4'25 p,m wide at the base, varying from 3 to 3'5 p,m wide throughout most of the length and diminishing to about 2'5 p,m wide towards the apex. Conidia colourless, obovoid or (less commonly) ellipsoid, usually continuous, though Latch (1964) says in some lesions up to 10 % r-septate, with a thin and minutely and closely verruculose wall and a conspicuously thickened hilum, 13-27 x 5-11'5 p,m. Causing a leaf spot on Holcus lanatus Linn. in Europe and New Zealand. R. holci-lanati has been well illustrated by Griffiths (1957) and by Latch (1964), and was also figured by Cavara (1893) who, however, depicted the

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conidial wall much more coarsely verrucose than it actually is and also confused the base with the apex of the conidia. The following measurements have been given by different authors: conidiophores 170 x 21"m (Cavara), 80-100 x 21"m (Griffiths), 70-235 x 2'3-3 p,m (Latch); conidia 16-22 x 6-10 p,m (Cavara), 16-27 x 6-10 p,m (Lindau), 13-22 x 5-1 I I"m with a mean of 17.6 x 7·61"m (Griffiths), 14.8-24 x 8'3-1 1'5 p,m with a mean of 19'5 x 9'7 I"m (Latch). As Griffiths (195 I) has remarked, several collections of Ramularia pusilla Unger (== Ovularia pusilla (Ung.) Sacco & D. Sacc.), the type species of Ramularia Unger, bear conidia with minutely roughened walls much like those of R. holci-lanati and, as has already been mentioned, like those of R. argentinensis. There seems to be no reason why R. holci-lanati should not be included in the genus Ramularia. Specimens examined: on Holcus lanatus. Italy: S. Pietro in Verzolo near Pavia, summer, F. Cavara, Fungi Longobardiae exsiccati 144, type (K ex BM: slide, IMI 149145). New Zealand: Palmerston North, 25. xi. 1968, G. C. M. Latch (IMI 136573: specimen and culture).

I wish to thank Professor ]. C. Lindquist (LPS) and Dr R. W. G. Dennis (K) for allowing me to examine specimens in their keeping and Dr G. C. M. Latch for the specimen and culture of R. holci-lanati from New Zealand. I am also grateful to Dr B. C. Sutton for allowing me to incorporate in this paper his notes on Didymariopsis, and to Mr D. W. Fry for the photograph reproduced as a Plate. REFERENCES

CAVARA, F. (1893). Fungi Longobardiae exsiccati siveMycetum specimina in Longobardia collect«, exsiccata et speciebus novis vel criticis, iconibus illustrata, Pugillus III, no. 144, Ticini. GRIFFITHS, E. (1957). Occurrence of Ramulaspera holci-lanati in Britain. Transactions oj th8 British Mycological Society 40, 232-236. LATCH, G.C.M. (1964). Ramulariapusilla Ung, and Ramulaspera holci-lanati (Cav.) Lind. in New Zealand. New Zealand Journal of Agricultural Research 7, 405-416. LINDAU, G. (1905)' Fungi imperfecti,Ryphomycetes (I Halfte). Rabenhorst's KryptogamenFlora von Deutschland, Oesterreich und tier Sduoeiz, 2 Auflage, I Band, 8 Abteilung. Leipzig. SPEGAZZINI, C. (1910). Mycetes argentinenses. Anales delMuseo nacional deHistoria natural de Buenos Aires20,329-467. EXPLANATION OF PLATE

29

Photograph of Spegazzini's pencil drawing and notes on the packet of the type specimen of Pseudouularia trifolii (LPS).

(Accepted for publication 20 December 197 I)