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Three fungi on leaves of Vitis
[ 223 ]
Trans. Br . mycol, Soc. 67 (2) 223-232 (1976)
Printed in Great Britain
THREE FUNGI ON LEAVES OF VITIS By F. C. DEIGHTON Lately Commonwealth Mycological Institute, K eui" Three species of Hyphomycetes parasitizing leaves of Vitis spp. are described: Phaeoramularia dissiliens (Duby) comb .nov. (Torula dissiliens Duby, more commonly known as Cercospora roessleri (Catt .) Sacc.); Phaeoramularia heterospora (Ell. & Gall.) comb.nov. (Septosporium heterosporum Ell. & Gall.); and Asperisporium minutulum (Sacc.) comb .nov. (Fusicladium minutulum Sacc.). There has been considerable confusion over the identity of these three species, as is shown by the synonymy and in the misidentifications cited. There has also been some confusion with a fourth species on leaves of Vitis, Asperisporium vitiphyllum (Speschnew) Deighton in Sutton (1975) and even with Pseudocercospora vitis (Lev.) Speg. An examination of numerous specimens shows that Ph. dissiliens is a somewhat variable species, and the species described from Israel (Cercospora leoni, C. corynelioides and C. judaica), which seem to be known only from their type collections, are considered to be mere variants of Ph . dissiliens. Ph. heterospora and Asperisporium minutulum seem often to have been confused, probably because of the similarity in ornamentation of their mature conidia.
Phaeoramularia dissiliens (Duby) comb.nov. (Figs. 1-4). Torula dissiliens Duby, M em. Soc. Physique Geneue 7 (1) : 215 (1836) . Septocylindrium dissiliens (Duby) Sacc., Mycotheca veneta 583 (1876), and M ichelia 1 (1) : 89 (1877). Cladosporium riissleri Cattaneo, Balm Com. agrar. Voghera 13 (13-14): 263 (1876). Cercospora riissleri (Catt.) Sacc., Michelia 2 (6): 128 (1880). Ragnhildiana rosleri (Catt.) Vassiljevskiy in Vassiljevskiy & Karakulin, Fungi imperfecti parasitici, Pars I Hyphomycetes: 375 (1937). Septosporium fuckelii Thiim., Ost. bot. Z. 27: 137 ( 1877). Cercospora fuckelii (T hiim.) Jaczewski, Gribnya parazitnya bolezni vinogradnoi lozy (Parasitic fungal diseases of grape vine], ed. 2: 81 (1906) (as ' Cercospora fuckelii Sacc.') . Isariopsis fuckellii (Thiim.) du Plessis, Fmg. S. Afr. 17: 62 (1942), misapplied name. 1< Present address: Discher's Pond, Great Gransden, Sandy, Beds.
roesleri forma fuckelii (Thum.) Elenkin, Bal. Rast. (Morbi Plant.) 4 (4- 5) : 68
Cercospora
(19 09). Cladosporium pestis Thiim., Ost. bot. Z. 27 : 12 (1877). Cercospora leoni Siivulescu & Rayss, Revue Path. ueg. Ent, agric. Fr. 22: 223 (1935), and Annis Cryptog. exot. 8: 68 (1935). Cercospora corynelioides Siivulescu & Rayss, Revue Path. ueg: Ent. agric . Fr. 22: 223 (1935), and Annls Cryptog. exot. 8 : 67 (1935). Cercospora j udaica Rayss, Palest. J . Bot. Jerusalem Ser. 3 : 41 ( 1943)· ?Septocylindrium virens Sacc., Nuovo G. bot. ital. 8 : 186 (1876).
The variously published spellings of the epithet originally published as "rossleri' are given above. The epithet was derived from the name of the collector, Rossler, and is more correctly spelled , roessleri ' . Disease symptoms very variable. Most commonly the fungus causes small indefinite yellowish discoloured areas on the upper leaf surface while on corresponding areas on the lower surface appear olivaceous (often dark olivaceous) caespituli forming dense effuse patches, usually numerous and each up to 3 mm wide, sometimes confluent and in severe infections covering large areas of the leaf. Sometimes definite, irregularly orbicular, dark brown spots up to 1 em diam, later becoming greyish in the centre, appear among the yellow discoloured areas. Sometimes large paler or darker brown spots only are produced and these may be numerous on a leaf : sporulation is more or less confined to these spots and may also occur on the upper surface of older spots. This variation in symptoms may occur on the same variety of grape in the same locality, as is to be seen in the specimens from Tandoiarn, Pakistan. M ycelium internal: hyphae colourless, 2-3 Ilm wide. Stroma substornatal, composed of almost colourless hyphae: stroma of variable size, in IMI 83452 8-2
224
Threefungi on leaves of Vitis
Fig. 1. Phaeoramularia dissiliens. Conidiophores and conidia. From Duby's specimen, RabenhorstWinter, F. sur. 2878 (Herb . K), authentic for and possibly the type of the name Torula dissiliens.
F. C. Deighton
225
10 pm
. .
"-
Fig. 2 . Phaeoramularia dissiliens. Conidiophores and conidia. (A) From Rossler's specimen, Thumen, F. ausrr. 1261 (Herb. K), syntype of Cladosporium roessleri; (B) from Passerini's specimen, Rabenhorst, F. eur. 1874 (Herb . K) as Torula dissiliens.
226
Three fungi on leaves of Vitis
A
I Opm
Fig. 3. Phaeoramularia dissiliens. Conidiophores and conidia. (A) From the type of Cercospora leoni; (B) from the type of Cercospora judaica.
F. C. Deighton
227
l
, I
I
c L..--....J 10 pm
A
Fig. 4. Phaeoramularia dissiliens. Conidiophores and conidia. (A) From 1M1 83452 from Pakistan; (B) from 1M1 87726 from Cyprus; (C) from Fuckel's F. Then. 2240 (Herb. K), type of SeptospoTium fuckelii; (D) from the type of Cercospora corynelioides (Herb. BUCA), showing four conidiophores from the same fascicle.
228
Three fungi on leaves of Vitis
about 30 pm wide and :25 pm high. Conidiophores usually numerous (50 or more) but sometimes fewer in a divergent fascicle, varying from pale to deep olivaceous, more or less straight, usually simple but occasionally branched, not geniculate, septate (but often continuous above a basal septum when short), smooth or sometimes minutely roughwalled about the apex, 25-90 flm long (sometimes slightly longer), 3-6'5 pm wide. Conidial scars conspicuously thickened, 1-2 pm diam, the old scars usually lying more or less flat against the side of the conid iophore. Conidia pale to moderate olivaceous , mostly subcylindric, occasionally slightly obclavate, catenulate, often in branched chains, the terminal ones broadly rounded at the apex, usually smooth but sometimes minutely rough-walled all over or in part, usually straight but occasionally slightly curved, 0- to 7-septate, most commonly 3-septate but sometimes mostly r-septate, with additional secondary septa being laid down after the first few have been formed, usually not constricted but occasionally slightly constricted at some or all of the septa, 16-84 x 3'5-8 pm. The scar at the apex of some catenate conidia may be as much as :2 '5 lim diam. The width of the conidia varies in different collections. In the type of Torula dissiliens (99973) they are 3'5-6'5 pm wide ; in the type of Clad osporium riissleri (100931) they are 4-5 '5 pm wide; in the type of Cercospora Leoni they are 5-6'5 pm wide; in the type of C. judaica they are 5-8 flm wide. Other collections show conidia 4-7 pm wide. On leaves of grapevine (Vitis vimfera L.) in Switzerland, Germany, France, Austria, Italy, Malta, Cyprus, Israel, Iran, Yemen, Pakistan and doubtless in territories between. Now uncommon in Europe as a result of the use offungicidal sprays. Savulescu & Rayss gave the measurements of Cercospora leoni as: conidiophores 15-35 x 4-6 um ; conidia at first o-septate, later 1- or z-septate, rarely 3-septate, 18-40 x 6'5-7 pm. My measurements of the type were: conidiophores up to 25 lim long, 3-5'5 pm wide, usually bearing only a terminal scar, rarely with 2 such scars, 0- to r-septate above a basal septum; conidia mostly 0- to i-septate, sometimes with a second and very rarely with a third very thin secondary septum, 24-38 '5 x 5-6'5 lim. They described C. corynelioides as having conidiophores 30-110 x 4-6 pm and conidia 3- to 5-septate, 30-48 x 4-7 lim. The type shows conidiophores very variable in length, breadth, depth of colour and septation, even in the same fascicle, and conid ia mostly 0- to 3-sept ate , I have no doubt that C. cory nelioides, like C. leoni and C. judaica, is only a variant of Phaeoramularia
dissiliens. Ph. dissiliens grows easily in culture. Cultures
from 1MI 83452 from Pakistan sporulated abundantly within a week, without ultraviolet illumination , on potato dextrose agar and oth er commonly used media, forming small dense orbicular dark brown colonies 2-3 mm diam after 15 days. After a month the colonies were about 15 mm diam and somewhat radially plicate. The conidia remained attached to each other in long, usually unbranched, chains . Saccardo's figure of Septocylindrium virens, Fungi italici no. 73 (1877), shows a fungus very similar to the one he illustrated (Fungi italici no . 74) as S, dissiliens but with narrower conidia (0-3 but mostly 3 septate, 15 x 3 pm). Saccardo did not figure conidiophores for either species. The type of S. virens was said to be Saccardo, Mycotheca veneta no. :284 on rotten leaves and stems of Vitis vinifera from Selva (Treviso) Sept. 1873. There are two packets of Saccardo, Mycotheca veneta 284 in Herb. K (one ex BM), both from Selva (Treviso) but collected Sept. 1874 (not 1873). The printed label reads' Saccardo Mycotheca Veneta 284. Cladosporium vi tis (Lev.) Sacco Septon ema vitis Lev. non Sacco Mycol. veneto 176 (ubi S eptocylindrium virens Sacco spec.nov.)Cladosporium ampelinum Pass. Erb. Critt. ital. Ser. H 595.' Both specimens in Herb. K are Pseudocercospora vitis (Lev.) Speg, and no other fungus is present. I therefore do not know Septocylindrium virens apart from Saccardo 's figure and description but am inclined to agree with Pirotta (1879: 212-213) that it is probably only a variant of S. dissiliens (i.e. Pha eoramularia dissiliens) though I have not seen any specimen of this species with conidia only 15 x 3 p m when mature. The type of S eptocylindrium virens var, onopordi Saccardo (1886), in Herb. PAD, growing on rotten stem of Onopordon , is not a Phaeoramularia and does not look much like Saccardo's figure of S .virens. Isariopsis fu ckelii is a misapplied name: the fungus described and figured by du Plessis is Pseudocercospora vitis. Spe cimens examined Specimens in Herb. K. Switzerland: Canton Waadt [Vaud), leg. Duby, Rabenhorst-Winter, Fungi eur. 2878 sub nom. Torula dissiliens and authentic for and possibly the type of that name (slide 1M1 99973). Germany: autumn, Fuckel's fungi rhenani 2240 sub nom, 'Sphaerella vitis, fungus conidiophorus', type of S eptosporium fu ckelii (slide 1MI 100930). Austria: near Klosterneuburg, aut. 1874. leg. Rossler, Thiimen, Fungi austriaci 1261 sub nom. 'Sphaerella vitis Fuckel, fungus conidiophorus', syntype of Cladosporium rossleri (slide1M1 100931); Klosterneuburg, aut. 1876, leg. Thurnen, Thumen, Mycoth. univ. 671, type of
F. C. Deighton Cladosporium pestis (slide IMI 15574). Italy: near Parma, autumn 1873, G. Passerini, Rabenhorst, Fungi eur. 1874 sub nom. Torula dissiliens (slide IMl 99974)
and Herb . Berk. 1879 no. 2 (slide IMI 99998) which is probably part of the same collection; Vittorio (Treviso ), Oct. 1875, Sac cardo, Mycorh. ven eta 583, sub nom. Septo cylindrium dissiliens (slide IMI 99975). Spe cimen in Herb. BUCA. Israel: Malia, 1 July 1935, J. de Leon, Mycofiora Palastinica, Tr. Sdoulescu & T . Rayss 35, type of Cercospora corynelioides (slide IMI 191833). Specimens in Herb. PAD. France: Rouen, aut . 1879, leg. Malbranche, slide only sub nom. Cercospora rsssleri (drawing IMI 101591). Switzerland: Ollen, Canton Vaud, Aug. 1894, J. Dufour, sub nom. Septocyl indrium dissiliens (slide IMl 101593). Specimens in Herb. 1M1 (IM I numbers in parentheses). Israel: Malia, 29 May 1935, J. De Leon, type of Cercospora leoni (82178): Bath Yam, 5 Oct. 1946, T. Rayss, type of Cercospora judaica (82179). Germany: Tarnsel, 25 Oct. 1903, P. Vogel, sub nom. Cercospora oiticola (8593). Malta: Selrnun, 30 May 1957, B. E. J. Wheeler (70172b), slide made by Wheeler in Malta, but no material of this fungus found on the herbarium specimen Wheeler 224. Cyprus: cornm. 17 Oct. 1928, H. M. Morris (8586); near Nisou, 13 Aug. 1931, R. M. Nattrass 85 (8587); Meneon , 10 Sept. 1956, G . P. Georghiou A-1i7 (69177); N icosia, 18 July 1961, A. Papasolomontos (87726). Iran : Rezaieh, Aug. 1955, Maleki (71323), and 29 Aug. 1955, Sharif & Mamootchehri (68709). Yemen: comm. 2"5 Dec. 1971, I. F. Gamal El Din (163385). Pakistan : Mirpur Khas, 15 July 1959, S. A. Khan (89435 b); Tandojam, 23 Oct. 1959, S. A. Khan (79797a), 7 July 1960, S. A. Khan (83455), 4 Nov. 1960, S. A. Khan (83452), 16 Oct. 1962, S. A. Khan (98256 and 98277), and 3 Jan. 1969, S. A. Khan (137422 and 137423); Bhawalpur, 20 Oct. 1960, A. Ghafoor & Mustafa (84863), and 10 Oct. 1961, A. Ghafoor (94 170b).
Phaeoramularia heterospora (Ell. & Gall .) comb.nov. (Fig. 5). Septosporium heterosporum Ellis & Galloway, J. Mycol. 5: 67 (1889)· Stigmina vitis Dearness & Bartholomew, Mycologia 21: 328 (1929). Leaf spots suborbicular with irregular margin, up to 5 rom wide, brown becoming greyish in the centre; sometimes (on V. giradiana ) merely indefinite brownish areas. Caespituli hypophyllous, dark olivaceous, punctiform and densely distributed over the spot. Mycelium internal: hyphae almost colourless, about 2'5 pm wide. Stroma substomatal , up to So pm wide and 30 pm high, consisting of a basal weft of almost colourless hyphae from which arise numerous closely packed, unbranched, assurgent, paralJel hyphae which become pale olivac eous just before emergence through the stoma above which they develop into the conidiophores, Conidiophores numerous in a dense slightly
229
divergent fascicle, simple, often only up to 25 lim long, moderate olivaceous, 1- to z-septate and bearing only a terminal conidial scar, but sometim es up to 65 pm long, 4- to 5-septate, dark olivaceous and bearing several old conidial scars, smooth or sometimes very slightly asperulate towards the apex, 5-6'5 I'm wide. Old conidial scars lying flat against the side of the conidiophore, slightly prominent, 1'S-2Ilm diam. Conidia at first ellipsoid to subcylindric, 0-4 septate, not constricted or con stricted at the median (primary) septum, moderate olivaceous, smooth or minutely verruculose (the roughness scarcely visible), later becoming deeper in colour and finally dark olivaceou s, stout walled, coarsely verrucose or rugose, with up to 5 primary transverse septa and 1-3 secondary transverse septa and sometimes also with a few secondary longitudinal septa, strongly constricted at the primary septa and sometimes at some of the secondary septa, 18-57 pm long, mostly 5-16 pm wide but sometimes up to 20 pm wide . The dark exospore of the older conidia becomes fissured, the segments being arranged sometimes in broken longitudinal stripes but in the olde st con id ia in an irregular more or less honeycomb pattern. The conidia are catenate, often slightly papillate at the base, the terminal ones broadly rounded at the apex. The conidiophores in most of the collections seen are short and bear a single terminal conidial scar , rarely 2 scars. In the type of Stigmina vitis, sim ilar short conidiophores occur but many are much longer, darker in colour, more septate, and bear several conidial scars . In the specimen from Israel, only a few conidiophores are short, most being sim ilar to the longer ones on the type of S. uitis. In this collection from Israel, the conidia are more frequently catenate than in other collections , and the fissuring of the exospore on the older conidia is in a pattern of broken longitudinal stripes (similar to the pattern on some of the conidia of Californian specimens), but no very rugose and irregular conidia were seen . Pycnidia (presumably spermogonia), up to 75 lim diam, ar e plentiful on the leaves of the type of Septosporium heterosporum and of IMI 8588 from Israel.
Specimens examined Specimen ill H erb. (Ellis collections). On V itis californica. Near Orange, Calif., U.S.A., F. L. Scribner, type of S eptosporium heterosporum (slide IMI 129292). Sp ecimen ill H erb. DAOM. On Vitis giradiana. Riverside, Calif., U .S.A., 9 Aug. 1924, E. Bartholomew 8886, type of Stig mina Vilis (slide IMI 96376). Specimens in H erb. 1M!. On Viris californica. Colton, Calif., U.S .A., Sept. 1926, E. Bartholomew, Petrak's
nv
23°
Three fungi on leaves of Vitis
c
....·. e"_' O
L-.-J I Op m
Fig. 5. Phaeoramularia heterospora. Conidiophores and conidia. (A) From IMI 32750; (B) from the type of Septosporium heterosporum (Herb. NY); (C) from the type of Stigmina vitis (Herb. DAOM), showing a long conidiophore. Mycoth. univ. 1394 and a second packet ex herb. Petrak (1MI 32750). On Vitis giradiana. Glendale, Calif., U.S.A., 8 Dec. 1929, O. A. Plunkett (Southern Californian fungi), sub nom. Stigmina vitis (lMI 154559). On Vitis vinifera. Near Haifa, Israel, 11 Apr. 1929, I. Reichert (IMI 8588).
Asperisporium minutulum (Sacc.) comb.nov, (Fig. 6).
Fusicladium minutulum Sacc., Nuovo G. bot. ita!., ser. 2, 27: 85 (1920). Leaf spots irregularly orbicular with indefinite margin, sometimes rather yellowish brown with a
deeper brown margin but usually dark brown, mostly up to 6 mm but sometimes almost 1 em wide. Caespituli hypophyllous, dark brown, punctiform, densely distributed over the spot. Mycelium internal: hyphae almost colourless, 1'5-2'5 pm wide, becoming up to 3 pm wide in the substomatal cavity. Stroma substomatal, consisting of a basal weft up to 10 pm deep of almost colourless hyphae from which arise numerous assurgent, closely packed, parallel, unbranched, very pale olivaceous, septate hyphae, 3-4 pm wide, which are, in fact, the conidiophores each of which terminates in a conidiogenous cell which is the
F. C. Deighton
I
~ ··
8 . .
10 ,um
Fig. 6. Asperisporium minutulum. Conidiophores and conidia. (A) From the type of Fusicladium minutulum (Herb. PAD); (B) an abnormal three-celled conidium, from Calif. fungi 291 (Herb. NY). only part that shows above the epidermis. Conidiaphores very numerous in a dense fascicle which eventually ruptures the stoma, the fascicles discrete but sometimes contiguous. Conidiogenous cells moderately deep olivaceous, continuous, sometimes slightly verruculose about the apex, 12-22 pm long, mostly slightly clavate, 5'56·5 pm wide (sometimes as narrow as 5 pm and sometimes as wide as 8 pm) towards the apex and 4-5"5 pm wide at the base, but sometimes subcylindric and only 3·S/jm wide. Conidial scars conspicuous, slightly prominent, 1'5-2 Ijm diam. Conidia variable in shape, mostly broadly ellipsoid, r-septate, strongly constricted at the septum,
moderately deep olivaceous and coarsely verrucose, the thick outer verrucose wall-layer showing reticulate fissures, often 2- to 3-septate with similar wall sculpturing, sometimes 0- to z-septate, pale olivaceous, relatively minutely verrucose and not reticulate, and occasionally 1- to 3-septate, pale olivaceous and smooth, broadly rounded at both ends, 11-19 (rarely up to 2s),um long, 7'5-9'5 (rarely 10'5-12 or as little as 5'5) ,urn wide. The individual cells of more strongly constricted conidia may separate easily in microscopic mounts. In some of the darker rugose conidia, longitudinal septa may be laid down in one or more of the cells, and sometimes a conidium is seen with one
Three fungi on leaves of Vitis (presumably basal) cell and a pair of partially separated upper cells. Hilum thickened, prominent and sometimes on a small papilla, often excentric. The conidia are not catenulate. Saccardo says, in the type description, 'caespitulis saepius hypophyllis'. I found no epiphyllous conidiophores on the type or on any of the other specimens examined. Saccardo gives the following measurements: conidiophores 18 x 5-6 pm; conidia r-septate, constricted, 16-17 x 11-12 flm, rarely up to 20-22 X 11-12 flm and z-septate, Conidia are plentiful in the ample type material, and in the other collections examined, but I found most were somewhat narrower than 11-12 flm. In sections of the leaf spots, immersed globose bodies up to 50 flm diam are to be seen, with a wall of brown cells one cell thick and colourless contents, which may be developing spermogonia. These bodies are sometimes discrete from the conidiophore fascicles but are sometimes contiguous and in mycelial connexion with them. Indications were seen in one such body of the presence of immature rod-shaped spermatia. Specimens examined
Economic fungi 8) (slide IMI 129289); Klamath river at Walker, Calif., 15 Sept. 1934, L. C. Wheeler 3258 (slide IMI 129290); Maacama Creek, Sonoma Co., Calif., 20 Aug. 1930, H. E. & S. T. Parks (Californian fungi distr. by Herb. Univ. Calif. 291) (slide IMI 129291) 'rarely collected but ranges throughout the Coast Range'. Specimen in Herb. 1M1 (ex Herb. WSP). On Vitis sp. At Bridge over East Fork of Illinois river, Near Kerby, Josephine Co., Ore., 25 Aug. 1932, H. E. Parks, WSP 44235 (IMI 129872). Specimen in Herb. E. On Vitis californica. Pine Grove, Amador Co., Calif., July 1893, Geo. Hansen, Flora of the Sequoia gigantea region no. 1235, sub nom. Cladosporium pygmaeum E. & E. (a name never published) (slide IMI 112142).
For making available specimens in their keeping I wish to thank the curators of the mycological collections in the following herbaria: BUCA, DAOM, E, K, NY and PAD. The late Prof. T. Rayss kindly deposited in Herb. IMI portions of the type collections of Cercospora leoni and C. judaica. REFERENCES
Specimen in Herb. PAD. On Vitis californica. Grant's Pass, Ore., 2 Sept. 1916, James R. Weir 10050, type (slide IMI 129533). Specimens in Herb. NY (sub nom. Septosporium heterosporum Ell. & Gall.). On Vitis californica. Suisun, Calif., 3 Aug. 1888, F. S. Earle (Seymour & Earle,
PIROTTA, R. (1879). I funghi parassiti dei vitigni, Archo Lab. Bot. Critt, R. Univ. Pavia 2-3, 131-225. SACCARDO, P. A. (1886). Sylloge fungorum 4, 226. Padua. SUTTON, B. C. (1975). Coelomycetes. V. Coryneum. Mycological Papers 138, 1-224.
(Accepted for publication 9 December 1975)
Trans. Br . mycol, Soc. 67 (2) 223-232 (1976)
Printed in Great Britain
THREE FUNGI ON LEAVES OF VITIS By F. C. DEIGHTON Lately Commonwealth Mycological Institute, K eui" Three species of Hyphomycetes parasitizing leaves of Vitis spp. are described: Phaeoramularia dissiliens (Duby) comb .nov. (Torula dissiliens Duby, more commonly known as Cercospora roessleri (Catt .) Sacc.); Phaeoramularia heterospora (Ell. & Gall.) comb.nov. (Septosporium heterosporum Ell. & Gall.); and Asperisporium minutulum (Sacc.) comb .nov. (Fusicladium minutulum Sacc.). There has been considerable confusion over the identity of these three species, as is shown by the synonymy and in the misidentifications cited. There has also been some confusion with a fourth species on leaves of Vitis, Asperisporium vitiphyllum (Speschnew) Deighton in Sutton (1975) and even with Pseudocercospora vitis (Lev.) Speg. An examination of numerous specimens shows that Ph. dissiliens is a somewhat variable species, and the species described from Israel (Cercospora leoni, C. corynelioides and C. judaica), which seem to be known only from their type collections, are considered to be mere variants of Ph . dissiliens. Ph. heterospora and Asperisporium minutulum seem often to have been confused, probably because of the similarity in ornamentation of their mature conidia.
Phaeoramularia dissiliens (Duby) comb.nov. (Figs. 1-4). Torula dissiliens Duby, M em. Soc. Physique Geneue 7 (1) : 215 (1836) . Septocylindrium dissiliens (Duby) Sacc., Mycotheca veneta 583 (1876), and M ichelia 1 (1) : 89 (1877). Cladosporium riissleri Cattaneo, Balm Com. agrar. Voghera 13 (13-14): 263 (1876). Cercospora riissleri (Catt.) Sacc., Michelia 2 (6): 128 (1880). Ragnhildiana rosleri (Catt.) Vassiljevskiy in Vassiljevskiy & Karakulin, Fungi imperfecti parasitici, Pars I Hyphomycetes: 375 (1937). Septosporium fuckelii Thiim., Ost. bot. Z. 27: 137 ( 1877). Cercospora fuckelii (T hiim.) Jaczewski, Gribnya parazitnya bolezni vinogradnoi lozy (Parasitic fungal diseases of grape vine], ed. 2: 81 (1906) (as ' Cercospora fuckelii Sacc.') . Isariopsis fuckellii (Thiim.) du Plessis, Fmg. S. Afr. 17: 62 (1942), misapplied name. 1< Present address: Discher's Pond, Great Gransden, Sandy, Beds.
roesleri forma fuckelii (Thum.) Elenkin, Bal. Rast. (Morbi Plant.) 4 (4- 5) : 68
Cercospora
(19 09). Cladosporium pestis Thiim., Ost. bot. Z. 27 : 12 (1877). Cercospora leoni Siivulescu & Rayss, Revue Path. ueg. Ent, agric. Fr. 22: 223 (1935), and Annis Cryptog. exot. 8: 68 (1935). Cercospora corynelioides Siivulescu & Rayss, Revue Path. ueg: Ent. agric . Fr. 22: 223 (1935), and Annls Cryptog. exot. 8 : 67 (1935). Cercospora j udaica Rayss, Palest. J . Bot. Jerusalem Ser. 3 : 41 ( 1943)· ?Septocylindrium virens Sacc., Nuovo G. bot. ital. 8 : 186 (1876).
The variously published spellings of the epithet originally published as "rossleri' are given above. The epithet was derived from the name of the collector, Rossler, and is more correctly spelled , roessleri ' . Disease symptoms very variable. Most commonly the fungus causes small indefinite yellowish discoloured areas on the upper leaf surface while on corresponding areas on the lower surface appear olivaceous (often dark olivaceous) caespituli forming dense effuse patches, usually numerous and each up to 3 mm wide, sometimes confluent and in severe infections covering large areas of the leaf. Sometimes definite, irregularly orbicular, dark brown spots up to 1 em diam, later becoming greyish in the centre, appear among the yellow discoloured areas. Sometimes large paler or darker brown spots only are produced and these may be numerous on a leaf : sporulation is more or less confined to these spots and may also occur on the upper surface of older spots. This variation in symptoms may occur on the same variety of grape in the same locality, as is to be seen in the specimens from Tandoiarn, Pakistan. M ycelium internal: hyphae colourless, 2-3 Ilm wide. Stroma substornatal, composed of almost colourless hyphae: stroma of variable size, in IMI 83452 8-2
224
Threefungi on leaves of Vitis
Fig. 1. Phaeoramularia dissiliens. Conidiophores and conidia. From Duby's specimen, RabenhorstWinter, F. sur. 2878 (Herb . K), authentic for and possibly the type of the name Torula dissiliens.
F. C. Deighton
225
10 pm
. .
"-
Fig. 2 . Phaeoramularia dissiliens. Conidiophores and conidia. (A) From Rossler's specimen, Thumen, F. ausrr. 1261 (Herb. K), syntype of Cladosporium roessleri; (B) from Passerini's specimen, Rabenhorst, F. eur. 1874 (Herb . K) as Torula dissiliens.
226
Three fungi on leaves of Vitis
A
I Opm
Fig. 3. Phaeoramularia dissiliens. Conidiophores and conidia. (A) From the type of Cercospora leoni; (B) from the type of Cercospora judaica.
F. C. Deighton
227
l
, I
I
c L..--....J 10 pm
A
Fig. 4. Phaeoramularia dissiliens. Conidiophores and conidia. (A) From 1M1 83452 from Pakistan; (B) from 1M1 87726 from Cyprus; (C) from Fuckel's F. Then. 2240 (Herb. K), type of SeptospoTium fuckelii; (D) from the type of Cercospora corynelioides (Herb. BUCA), showing four conidiophores from the same fascicle.
228
Three fungi on leaves of Vitis
about 30 pm wide and :25 pm high. Conidiophores usually numerous (50 or more) but sometimes fewer in a divergent fascicle, varying from pale to deep olivaceous, more or less straight, usually simple but occasionally branched, not geniculate, septate (but often continuous above a basal septum when short), smooth or sometimes minutely roughwalled about the apex, 25-90 flm long (sometimes slightly longer), 3-6'5 pm wide. Conidial scars conspicuously thickened, 1-2 pm diam, the old scars usually lying more or less flat against the side of the conid iophore. Conidia pale to moderate olivaceous , mostly subcylindric, occasionally slightly obclavate, catenulate, often in branched chains, the terminal ones broadly rounded at the apex, usually smooth but sometimes minutely rough-walled all over or in part, usually straight but occasionally slightly curved, 0- to 7-septate, most commonly 3-septate but sometimes mostly r-septate, with additional secondary septa being laid down after the first few have been formed, usually not constricted but occasionally slightly constricted at some or all of the septa, 16-84 x 3'5-8 pm. The scar at the apex of some catenate conidia may be as much as :2 '5 lim diam. The width of the conidia varies in different collections. In the type of Torula dissiliens (99973) they are 3'5-6'5 pm wide ; in the type of Clad osporium riissleri (100931) they are 4-5 '5 pm wide; in the type of Cercospora Leoni they are 5-6'5 pm wide; in the type of C. judaica they are 5-8 flm wide. Other collections show conidia 4-7 pm wide. On leaves of grapevine (Vitis vimfera L.) in Switzerland, Germany, France, Austria, Italy, Malta, Cyprus, Israel, Iran, Yemen, Pakistan and doubtless in territories between. Now uncommon in Europe as a result of the use offungicidal sprays. Savulescu & Rayss gave the measurements of Cercospora leoni as: conidiophores 15-35 x 4-6 um ; conidia at first o-septate, later 1- or z-septate, rarely 3-septate, 18-40 x 6'5-7 pm. My measurements of the type were: conidiophores up to 25 lim long, 3-5'5 pm wide, usually bearing only a terminal scar, rarely with 2 such scars, 0- to r-septate above a basal septum; conidia mostly 0- to i-septate, sometimes with a second and very rarely with a third very thin secondary septum, 24-38 '5 x 5-6'5 lim. They described C. corynelioides as having conidiophores 30-110 x 4-6 pm and conidia 3- to 5-septate, 30-48 x 4-7 lim. The type shows conidiophores very variable in length, breadth, depth of colour and septation, even in the same fascicle, and conid ia mostly 0- to 3-sept ate , I have no doubt that C. cory nelioides, like C. leoni and C. judaica, is only a variant of Phaeoramularia
dissiliens. Ph. dissiliens grows easily in culture. Cultures
from 1MI 83452 from Pakistan sporulated abundantly within a week, without ultraviolet illumination , on potato dextrose agar and oth er commonly used media, forming small dense orbicular dark brown colonies 2-3 mm diam after 15 days. After a month the colonies were about 15 mm diam and somewhat radially plicate. The conidia remained attached to each other in long, usually unbranched, chains . Saccardo's figure of Septocylindrium virens, Fungi italici no. 73 (1877), shows a fungus very similar to the one he illustrated (Fungi italici no . 74) as S, dissiliens but with narrower conidia (0-3 but mostly 3 septate, 15 x 3 pm). Saccardo did not figure conidiophores for either species. The type of S. virens was said to be Saccardo, Mycotheca veneta no. :284 on rotten leaves and stems of Vitis vinifera from Selva (Treviso) Sept. 1873. There are two packets of Saccardo, Mycotheca veneta 284 in Herb. K (one ex BM), both from Selva (Treviso) but collected Sept. 1874 (not 1873). The printed label reads' Saccardo Mycotheca Veneta 284. Cladosporium vi tis (Lev.) Sacco Septon ema vitis Lev. non Sacco Mycol. veneto 176 (ubi S eptocylindrium virens Sacco spec.nov.)Cladosporium ampelinum Pass. Erb. Critt. ital. Ser. H 595.' Both specimens in Herb. K are Pseudocercospora vitis (Lev.) Speg, and no other fungus is present. I therefore do not know Septocylindrium virens apart from Saccardo 's figure and description but am inclined to agree with Pirotta (1879: 212-213) that it is probably only a variant of S. dissiliens (i.e. Pha eoramularia dissiliens) though I have not seen any specimen of this species with conidia only 15 x 3 p m when mature. The type of S eptocylindrium virens var, onopordi Saccardo (1886), in Herb. PAD, growing on rotten stem of Onopordon , is not a Phaeoramularia and does not look much like Saccardo's figure of S .virens. Isariopsis fu ckelii is a misapplied name: the fungus described and figured by du Plessis is Pseudocercospora vitis. Spe cimens examined Specimens in Herb. K. Switzerland: Canton Waadt [Vaud), leg. Duby, Rabenhorst-Winter, Fungi eur. 2878 sub nom. Torula dissiliens and authentic for and possibly the type of that name (slide 1M1 99973). Germany: autumn, Fuckel's fungi rhenani 2240 sub nom, 'Sphaerella vitis, fungus conidiophorus', type of S eptosporium fu ckelii (slide 1MI 100930). Austria: near Klosterneuburg, aut. 1874. leg. Rossler, Thiimen, Fungi austriaci 1261 sub nom. 'Sphaerella vitis Fuckel, fungus conidiophorus', syntype of Cladosporium rossleri (slide1M1 100931); Klosterneuburg, aut. 1876, leg. Thurnen, Thumen, Mycoth. univ. 671, type of
F. C. Deighton Cladosporium pestis (slide IMI 15574). Italy: near Parma, autumn 1873, G. Passerini, Rabenhorst, Fungi eur. 1874 sub nom. Torula dissiliens (slide IMl 99974)
and Herb . Berk. 1879 no. 2 (slide IMI 99998) which is probably part of the same collection; Vittorio (Treviso ), Oct. 1875, Sac cardo, Mycorh. ven eta 583, sub nom. Septo cylindrium dissiliens (slide IMI 99975). Spe cimen in Herb. BUCA. Israel: Malia, 1 July 1935, J. de Leon, Mycofiora Palastinica, Tr. Sdoulescu & T . Rayss 35, type of Cercospora corynelioides (slide IMI 191833). Specimens in Herb. PAD. France: Rouen, aut . 1879, leg. Malbranche, slide only sub nom. Cercospora rsssleri (drawing IMI 101591). Switzerland: Ollen, Canton Vaud, Aug. 1894, J. Dufour, sub nom. Septocyl indrium dissiliens (slide IMl 101593). Specimens in Herb. 1M1 (IM I numbers in parentheses). Israel: Malia, 29 May 1935, J. De Leon, type of Cercospora leoni (82178): Bath Yam, 5 Oct. 1946, T. Rayss, type of Cercospora judaica (82179). Germany: Tarnsel, 25 Oct. 1903, P. Vogel, sub nom. Cercospora oiticola (8593). Malta: Selrnun, 30 May 1957, B. E. J. Wheeler (70172b), slide made by Wheeler in Malta, but no material of this fungus found on the herbarium specimen Wheeler 224. Cyprus: cornm. 17 Oct. 1928, H. M. Morris (8586); near Nisou, 13 Aug. 1931, R. M. Nattrass 85 (8587); Meneon , 10 Sept. 1956, G . P. Georghiou A-1i7 (69177); N icosia, 18 July 1961, A. Papasolomontos (87726). Iran : Rezaieh, Aug. 1955, Maleki (71323), and 29 Aug. 1955, Sharif & Mamootchehri (68709). Yemen: comm. 2"5 Dec. 1971, I. F. Gamal El Din (163385). Pakistan : Mirpur Khas, 15 July 1959, S. A. Khan (89435 b); Tandojam, 23 Oct. 1959, S. A. Khan (79797a), 7 July 1960, S. A. Khan (83455), 4 Nov. 1960, S. A. Khan (83452), 16 Oct. 1962, S. A. Khan (98256 and 98277), and 3 Jan. 1969, S. A. Khan (137422 and 137423); Bhawalpur, 20 Oct. 1960, A. Ghafoor & Mustafa (84863), and 10 Oct. 1961, A. Ghafoor (94 170b).
Phaeoramularia heterospora (Ell. & Gall .) comb.nov. (Fig. 5). Septosporium heterosporum Ellis & Galloway, J. Mycol. 5: 67 (1889)· Stigmina vitis Dearness & Bartholomew, Mycologia 21: 328 (1929). Leaf spots suborbicular with irregular margin, up to 5 rom wide, brown becoming greyish in the centre; sometimes (on V. giradiana ) merely indefinite brownish areas. Caespituli hypophyllous, dark olivaceous, punctiform and densely distributed over the spot. Mycelium internal: hyphae almost colourless, about 2'5 pm wide. Stroma substomatal , up to So pm wide and 30 pm high, consisting of a basal weft of almost colourless hyphae from which arise numerous closely packed, unbranched, assurgent, paralJel hyphae which become pale olivac eous just before emergence through the stoma above which they develop into the conidiophores, Conidiophores numerous in a dense slightly
229
divergent fascicle, simple, often only up to 25 lim long, moderate olivaceous, 1- to z-septate and bearing only a terminal conidial scar, but sometim es up to 65 pm long, 4- to 5-septate, dark olivaceous and bearing several old conidial scars, smooth or sometimes very slightly asperulate towards the apex, 5-6'5 I'm wide. Old conidial scars lying flat against the side of the conidiophore, slightly prominent, 1'S-2Ilm diam. Conidia at first ellipsoid to subcylindric, 0-4 septate, not constricted or con stricted at the median (primary) septum, moderate olivaceous, smooth or minutely verruculose (the roughness scarcely visible), later becoming deeper in colour and finally dark olivaceou s, stout walled, coarsely verrucose or rugose, with up to 5 primary transverse septa and 1-3 secondary transverse septa and sometimes also with a few secondary longitudinal septa, strongly constricted at the primary septa and sometimes at some of the secondary septa, 18-57 pm long, mostly 5-16 pm wide but sometimes up to 20 pm wide . The dark exospore of the older conidia becomes fissured, the segments being arranged sometimes in broken longitudinal stripes but in the olde st con id ia in an irregular more or less honeycomb pattern. The conidia are catenate, often slightly papillate at the base, the terminal ones broadly rounded at the apex. The conidiophores in most of the collections seen are short and bear a single terminal conidial scar , rarely 2 scars. In the type of Stigmina vitis, sim ilar short conidiophores occur but many are much longer, darker in colour, more septate, and bear several conidial scars . In the specimen from Israel, only a few conidiophores are short, most being sim ilar to the longer ones on the type of S. uitis. In this collection from Israel, the conidia are more frequently catenate than in other collections , and the fissuring of the exospore on the older conidia is in a pattern of broken longitudinal stripes (similar to the pattern on some of the conidia of Californian specimens), but no very rugose and irregular conidia were seen . Pycnidia (presumably spermogonia), up to 75 lim diam, ar e plentiful on the leaves of the type of Septosporium heterosporum and of IMI 8588 from Israel.
Specimens examined Specimen ill H erb. (Ellis collections). On V itis californica. Near Orange, Calif., U.S.A., F. L. Scribner, type of S eptosporium heterosporum (slide IMI 129292). Sp ecimen ill H erb. DAOM. On Vitis giradiana. Riverside, Calif., U .S.A., 9 Aug. 1924, E. Bartholomew 8886, type of Stig mina Vilis (slide IMI 96376). Specimens in H erb. 1M!. On Viris californica. Colton, Calif., U.S .A., Sept. 1926, E. Bartholomew, Petrak's
nv
23°
Three fungi on leaves of Vitis
c
....·. e"_' O
L-.-J I Op m
Fig. 5. Phaeoramularia heterospora. Conidiophores and conidia. (A) From IMI 32750; (B) from the type of Septosporium heterosporum (Herb. NY); (C) from the type of Stigmina vitis (Herb. DAOM), showing a long conidiophore. Mycoth. univ. 1394 and a second packet ex herb. Petrak (1MI 32750). On Vitis giradiana. Glendale, Calif., U.S.A., 8 Dec. 1929, O. A. Plunkett (Southern Californian fungi), sub nom. Stigmina vitis (lMI 154559). On Vitis vinifera. Near Haifa, Israel, 11 Apr. 1929, I. Reichert (IMI 8588).
Asperisporium minutulum (Sacc.) comb.nov, (Fig. 6).
Fusicladium minutulum Sacc., Nuovo G. bot. ita!., ser. 2, 27: 85 (1920). Leaf spots irregularly orbicular with indefinite margin, sometimes rather yellowish brown with a
deeper brown margin but usually dark brown, mostly up to 6 mm but sometimes almost 1 em wide. Caespituli hypophyllous, dark brown, punctiform, densely distributed over the spot. Mycelium internal: hyphae almost colourless, 1'5-2'5 pm wide, becoming up to 3 pm wide in the substomatal cavity. Stroma substomatal, consisting of a basal weft up to 10 pm deep of almost colourless hyphae from which arise numerous assurgent, closely packed, parallel, unbranched, very pale olivaceous, septate hyphae, 3-4 pm wide, which are, in fact, the conidiophores each of which terminates in a conidiogenous cell which is the
F. C. Deighton
I
~ ··
8 . .
10 ,um
Fig. 6. Asperisporium minutulum. Conidiophores and conidia. (A) From the type of Fusicladium minutulum (Herb. PAD); (B) an abnormal three-celled conidium, from Calif. fungi 291 (Herb. NY). only part that shows above the epidermis. Conidiaphores very numerous in a dense fascicle which eventually ruptures the stoma, the fascicles discrete but sometimes contiguous. Conidiogenous cells moderately deep olivaceous, continuous, sometimes slightly verruculose about the apex, 12-22 pm long, mostly slightly clavate, 5'56·5 pm wide (sometimes as narrow as 5 pm and sometimes as wide as 8 pm) towards the apex and 4-5"5 pm wide at the base, but sometimes subcylindric and only 3·S/jm wide. Conidial scars conspicuous, slightly prominent, 1'5-2 Ijm diam. Conidia variable in shape, mostly broadly ellipsoid, r-septate, strongly constricted at the septum,
moderately deep olivaceous and coarsely verrucose, the thick outer verrucose wall-layer showing reticulate fissures, often 2- to 3-septate with similar wall sculpturing, sometimes 0- to z-septate, pale olivaceous, relatively minutely verrucose and not reticulate, and occasionally 1- to 3-septate, pale olivaceous and smooth, broadly rounded at both ends, 11-19 (rarely up to 2s),um long, 7'5-9'5 (rarely 10'5-12 or as little as 5'5) ,urn wide. The individual cells of more strongly constricted conidia may separate easily in microscopic mounts. In some of the darker rugose conidia, longitudinal septa may be laid down in one or more of the cells, and sometimes a conidium is seen with one
Three fungi on leaves of Vitis (presumably basal) cell and a pair of partially separated upper cells. Hilum thickened, prominent and sometimes on a small papilla, often excentric. The conidia are not catenulate. Saccardo says, in the type description, 'caespitulis saepius hypophyllis'. I found no epiphyllous conidiophores on the type or on any of the other specimens examined. Saccardo gives the following measurements: conidiophores 18 x 5-6 pm; conidia r-septate, constricted, 16-17 x 11-12 flm, rarely up to 20-22 X 11-12 flm and z-septate, Conidia are plentiful in the ample type material, and in the other collections examined, but I found most were somewhat narrower than 11-12 flm. In sections of the leaf spots, immersed globose bodies up to 50 flm diam are to be seen, with a wall of brown cells one cell thick and colourless contents, which may be developing spermogonia. These bodies are sometimes discrete from the conidiophore fascicles but are sometimes contiguous and in mycelial connexion with them. Indications were seen in one such body of the presence of immature rod-shaped spermatia. Specimens examined
Economic fungi 8) (slide IMI 129289); Klamath river at Walker, Calif., 15 Sept. 1934, L. C. Wheeler 3258 (slide IMI 129290); Maacama Creek, Sonoma Co., Calif., 20 Aug. 1930, H. E. & S. T. Parks (Californian fungi distr. by Herb. Univ. Calif. 291) (slide IMI 129291) 'rarely collected but ranges throughout the Coast Range'. Specimen in Herb. 1M1 (ex Herb. WSP). On Vitis sp. At Bridge over East Fork of Illinois river, Near Kerby, Josephine Co., Ore., 25 Aug. 1932, H. E. Parks, WSP 44235 (IMI 129872). Specimen in Herb. E. On Vitis californica. Pine Grove, Amador Co., Calif., July 1893, Geo. Hansen, Flora of the Sequoia gigantea region no. 1235, sub nom. Cladosporium pygmaeum E. & E. (a name never published) (slide IMI 112142).
For making available specimens in their keeping I wish to thank the curators of the mycological collections in the following herbaria: BUCA, DAOM, E, K, NY and PAD. The late Prof. T. Rayss kindly deposited in Herb. IMI portions of the type collections of Cercospora leoni and C. judaica. REFERENCES
Specimen in Herb. PAD. On Vitis californica. Grant's Pass, Ore., 2 Sept. 1916, James R. Weir 10050, type (slide IMI 129533). Specimens in Herb. NY (sub nom. Septosporium heterosporum Ell. & Gall.). On Vitis californica. Suisun, Calif., 3 Aug. 1888, F. S. Earle (Seymour & Earle,
PIROTTA, R. (1879). I funghi parassiti dei vitigni, Archo Lab. Bot. Critt, R. Univ. Pavia 2-3, 131-225. SACCARDO, P. A. (1886). Sylloge fungorum 4, 226. Padua. SUTTON, B. C. (1975). Coelomycetes. V. Coryneum. Mycological Papers 138, 1-224.
(Accepted for publication 9 December 1975)