NORDISK MYKOLOGISK TIDSSKRIFT BIND X HEFTE 1-2 KØBENHAVN 1972

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1 E A NORDISK MYKOLOGISK TIDSSKRIFT BIND X HEFTE 1-2 KØBENHAVN 1972

2 . 30 INDHOLD Side J. P. SKOU: Ascosphaerales o o o o o o 1 V. SMEDEGÅRD-PETERSEN and J. E. HERMANSEN : Leaf spot diseases on graminicolous species at a locality in Greenland 25 J. E. HERMANSEN and ARNE WIBERG: On the appearance of Erysiphe graminis f. sp. hordei and Puccinia hordei in the Faerces and the possible primary sources of inoculum 0 0 R. A. SINGH and M. S. PAVGI: Physiology of teliospore germination in Entyloma and Melanotaenium species M. P. HAWARE and M. S. PAVGI: Physiology of chlamydospore germination in Protomycopsis species o o o o o o o o o o o o o o o o o 43 N. FABRITIUS BUCHWALD: OTTO FRIDERICH MULLER und Boletus edulis als Speisepilz o o S. B. MATHUR and V. K. AGARWAL: A Pestoletia sp. causing fruit rot in apple o V. SMEDEGÅRD-PETERSEN: The perithecial and pycnidial stages of Pyrenophora teres and P. graminea in Denmark J. E. HERMANSEN: Successfullow temperature storage of conidia of Erysiphe graminis produced under dry conditions o o o o o 86 OVE ARBO HøEG og JOHAN LANGE: Om svampes kulturhistoriske rolle i Nordens middelalder 89 N. FABRITIUS BUCHWALD and PAUL NEERGAARD: A plea for the retention of Sclerotinia sclerotiorum as type species for the genus Sclerotinia o Notitser o o.. o o o o o o... o... o.. o.. o.. o" o o o o o o o o o.. o o o o o o o... o o o o o o. o 100 Ny Litteratur o o. o o o o o o o. o o. o' o,, o o o o o o o o o o o o o. 115 Meddelelser fra Foreningen til Svampekundskabens Fremme o o o o o o o o o 117 * REDAKTION: N. F. BUCHWALD J. KOCH * Udgivet af Foreningen til Svampekundskabens Fremme Trykningen afsluttet i januar 1973 Meddelelser rra JfOreningen til Svampekundskabens Fremme o o o o o o o o o o o o o 117 PDF scanning and OCR by the Danish Mycological Society REDAKTION: N. F. BUCHWALD J. KOCH

3 FRIESIA. Bind X. Hefte ASCOSPHAERA LES By J. P. SKOU Agricult ural R esear ch Department, Danish At om ic E nergy Commission Research Establishment Rise, DK-4000 Roskilde, Den mar k gro up. A BST RACT Cult ur es of the members of Ascosphaeraceae - the onl y family in Ascosphaerales under the series Plectomycet es - were compared and emended by adding new and hitherto undeseribed charact ers. as A. major comb. nov., and A. proliperda sp. nov. is erected. Neotypes from Ascosphaera. A. apis var. major is raised to a separate species Bettsia gen. nov. with the species B. alvei comb. nov. is separat ed sity of Copenhagen. Now and then diseases disturb the experiments (NØRGAARD HOLM & SKOU, in the press). In some of these cases NØRGAARD HOLM are designated for B. alvei and A. major. The new Ascosph aera species are found associated with the solitary bee, Megachile centuncularis. Experiments with pollinating bees, mainly Bombus LATR., Megachile LATR., and Osmia PANZ. species, have been carried out for several and Plant Breeding of t he Royal Veterinary and Agricultural Univer years by Sv. NØRGAARD HOLM at the Department of Crop Husbandry found cells of the leaf-cutting bee, Megachile centuncularis L., containing what he called 'gun powder' besides more or less mummified larvae and asked the present author what the reason might be (Fig. 1). The 'gun powder' was identified as ascomata of the genus Ascospha era OLIVE et SPILTOIR (SPILTOIR & OLIVE 1955). By comparing these ascomata to known species, new species and new characters were uncovered. Therefore it was found valuable to treat the whole FRI E l A X -1 - INTRODUCTION

4 - 2 - Fig. 1. Ascosphaera proliperda. The very first find, now des ginated a s the holotype of the species. The leaf-cuttings of the cell with the cocoon, the mummified larva of M eg a chile cen twnc u laris, and the ascomata of the fungus may be seen. - X 3. For the first time all members of Ascosphaeraceae were grown side by side. Results of the examinations and comparisons are presented below. TAXONOMY In the course of time several proposals have been made for the taxonomic position of these fungi, and the last word has possibly not been said yet. At first the fungi were placed in the Phycomycet es (MAASSEN 1916, VARITCHAK 1932, cf. further PROKSCHL 1953) ; then the opinion arose that the fungi might be transition forms between Phycomycetes and Ascomycetes (CLAUSSEN 1921, FITZPATRICK 1930, cf. further PROKSCHL 1953), while GAUMANN (1926) and VARITCHAK (1933) proposed placing them together with Protascales and Endomycetal es in the Hemiascomycetes (Hemiascomycetidae). The proof that the fungi are in faet Ascomycet es (VARITCHAK 1933) was definitely established by SPILTOIR (1955) who demonstrated binucleate ascogenous hyphae producing croziers, and the presence of 8-nucleate asci. These asci disintegrate soon, but groups of asci may develop a joint, exceedingly thin membrane (SPILTOIR 1955) so the mature ascospores occur in spore balls of varying size and number of spores, or they may be left free in the ascomata (author) (Figs. 4 and 9).

5 The fungi are heterothallic and sexually dirnorphic. When male and female mycelia are grown together, ascogonia with nutriocytes and one or more trichogynes are produced, the latter receiving protoplasmic material from papillae on the male mycelium (Fig. 2) ; cf. SPILTOIR (1955 ). Then the nutriocyte enlarges, and the density of its cont ent incr eases as t he ascogenous hyphae develo p and form aggregated bodies in the centre (Fig. 4) ( cf. BETTS 1912, Fig. 6), and as Fig. 2. A scosphaer a proliperda. An ascog onium with its trichogyne. - X 560. J* to dark brown and hard, but somewhat fragile. The sack-like membrane is filled with spore balls, and this show that this (1964) still uses 'synascus' and places the fungi close to Protomqces; cf. GXUMANN Such ascomata are cysts sensu stricto aiready used as the technical term by BETTS (1912) (Fig. 3). Later VARITCHAK (1933) proposed the name 'synascus', a term used en passant by VON BUREN (1915) for the spore mother cells of Protomuces, but there is no special reason for using this term in preference to that of BETTS. GXUMANN * ) ALEXOPOULOS (1962) incorrectly spelled the name A scosphaer i aceae. Outside Ascosphaeraceaer) OLIVE et SPILTOIR (SPILTOIR & OLIVE Fig. 3. A scosphaer a proliperda. Broken spo re cyst. ascoma is nothing but a cyst. - X 280. the asci and later the spores or spore balls develop. At the same time the nutriocyte exhausts of protoplasm and its cell wall chit iniz es, t ur ns olivaceous

6 ) this kind of ascomata is unkn own. Simplified to a single ascus the genus Eremascus EIDAM, which may contain more than 8 spores pro ascus, is brought to min d, but t his genus is without any kind of ascomata and it s sexual system simpler (HARROLD 1950) than that of Ascosphaeraceae. Actually, t he resemblance is obviously greater to Monascus VAN TIEGHEM of the Eurotiales which has a closely comparable sexual system (YOUNG 1931, SPILTOIR 1955), but with a cleistothecium vere (BUCHANAN 1910, COLE & KENDRICK 1968). SPIL TOIR (1955) and VON ARX (197 0) place the fungi in Eurotialee, but in the present author's opinion the difference is too great between the one-celled cysts developed from the multinucleate nutriocyte of the ascogonium and the mult icellu lar, pseudoparenchymatous peridium of t he cleistothecia with their hyphal investments most likely developed from haploid hyphae. Neither do the species of Ascosphaeraceae fit within the other orders of the series Plectomycet es (Gymnascales, Onygenal es and Microascales) cf. ALEXOPOULOS 1962, GAU MANN 1964, BOOTH 1966, AINSWORTH, JAMES & HAWKSWORTH 1971), but as it is more closely r elated he re than t o any other group of Ascomqcetes, the present author agr ees with GAUMANN (1964) in erecting the order Ascosphaerales with characters of the type family Ascosphaeraceae OLIVE et SPILTOIR (SPILTOIR & OLIVE 1955) emend. The placing of the or der close t o his Protomycetales (p. 107, 169) seems rather doubtful, and his use of 'synascus' and Synascomycete s is disadvantageous acc ording t o what is stated above ( et. GAUMANN 1964). D e s c r i p t i o n: In Ascosphaerales t he ascogonial nutriocyte containing t he ascogenous hyphae and asci enlarges, becomes membranaceous, and constitutes t he ascomata, that is cysts sensu stricto. After evanescenee of the asci t he sp ores may or may not be united in spore balls. On the basis of the above the taxonomic position of Ascosphaerales is given by t he foliowing key: Subclass : Euascomycetidae sensu ALEXOPOULOS Series : Plectomycet es ALEXOPOULOS Ordo : Ascosphaerales GAUMANN 1964 emend. Familia: Ascosphaeracea e OLIVE et SPILTOIR 1955 emend. Basionym: Synascomycetaceae V ARITCHAK Illegitimate according to article 18 of t he International Code of Botanical Nomenelature (LANJOUW et al. 1966). Synonym: Pericystaceae BESSEY 195 0, nom. nud.

7 - 5- Genera: I. Bettsia gen. nov. segregated from Ascosphaera, see below. II. Ascosphaera OLIVE et SPILTOIR 1955 emend. Basionym: Pericystis BETTS 1912, non. J. AGARDH X ) GENERA AND SPECIES The order of A scosphaerales comprises only few known members, and hitherto all investigations have included only one or two species. In the present studies all the members were compared, which uncovered new characters of systematic value and made a more detailed separation possible. The first known species of the order, already deseribed by BETTS (1912) as Pericystis aloei, and later only stated to be different from P. apis (MAASSEN 1916, CLAUSSEN 1921) (cf. below), was found to differ so decisively from the other members that it appeared necessary to separate it into an independent genus. Further three species of Ascosphaera were recognized. I. 8ettsia gen. nov. Synonym: Pericystis BETTS (1912) nom. illeg., non Pericystis J. A GARDH (1848). Etymolog y : The name is given in honour of A NNIE D. BETTS who first deseribed the fungus (BETTS 1912). D e s c r i p t i o e m e n d a t a: Fungi secundum sexum dimorphi, myceliis septatis, masculo papillas receptivas gerente, femineo ascogonia, quorum cuique trichogynum unum vel plura et cellula nutritoria una. Cellula nutritoria ascog onialis in ascomata transformata cystas veras efficientia, forma varias, ovoides vel subglobulares, saepe etiam obcampanulatas vel pyriformes, hyphis suffultoriis valde manifestis ut trichogynis cum cystis unitis, interdum per partes infundibuli ad instar dilatatas in eas transientibus. Membrana cystae ut partium cum ea conjunctarum denique fusca. Asci evanescentes, sporas sphaericas non in globulos congregatas ita liberantes. Hyphae repentes vel suberectae, intertextae, mu ltis cellulis in chlamydosporas inter- * ) P ericystis AGARDH 1848 with the species P. aeruginosa AGARDH is a red a lga deseribed from a herbarium collected by Prof. F. M. LIEBMANN ( ), Copenhagen, on a journey to Mexico 1840/43 and obviously also to Cuba as the alga was collected at Havana.

8 - 6 - calares mutatis, denique dissilientibus. Status conidialis aleuriosporus sporas in ramulis brevibus terminales gerens saepe sub angulo recto emissis, ex ipso mycelio ortis vel ex hyphis suberectis conidiophoris similibus, ramulo nu nc septo a hypha limitato, nunc nullo septo separat o. Species typifi ca: Bettsia alvei (BETTS) comb. nov., Pericystis alvei BETTS D e s c r i p t i o n: Bettsia gen. nov., Le. Pericystis BETTS (1912) emend. Sexually dimorphic fungi with septate mycelia, the male producing receptive papillae, the female producing ascogonia with one or more trichogynes a nd a nutriocyte. The ascogonial nutriocyte grows and constit ut es the ascomata which are cysts sensu siricio, form variable, ovoi d to subglobose, often obcampanulate or pyriform, with very pronounced support ing hyphae and trichogynes as integral parts, now and then forming funnel-shaped connections to the cyst itself (Fig. 4). Fig. 4. Bettsia alvei. Spore cysts. In the young cysts only the centre is filled with aggregated more or less g tobese protoplasmi c bodies. Later the free ascospores are visible. Note the globose, pyriform and obcampa.nulate form, and further the trichogynes and pronounced supporting hyphae. Bottom left, a broken spore cyst with ascospor es inside and outside. - X 400. Young cysts contain aggregated globose protoplasmic bodies in the centre, possibly the evanescent asci which in time leave the spherical spores free without forming sp ore balls. The membranaceous cyst wall with its connections ultimately turns dark-coloured. Hyphae creeping or suberect, interwoven, with many cells con-

9 verted into intercalary chlamydospores, ultimately breaking up. Aleuriosporic conidial state (sensu BARRON 1968) with the spores on short branches, often at right angles, direct on the mycelium or on conidiophore -like suber ect hyphae from which the branches may or may not be separat ed by a septum. Bettsia alvei (BETTS ) comb. nov. Ge nus t ype. B asiony m : Pericystis alvei B ETTS Synonym: Ascosphaera alvei ( B ETTS) OLIVE et SPILTOIR between septa, 4-8, av. 5.4,Li for hyphae with intercalary chlamydospores but outside these, and 2-6, av. 3.4 p for other hyphae (BETTS 1912: 2-6, av. 5.0 l i ). The structureless, smooth spore cyst membrane D e s c r i p t i o n: The following in addition to t he charact ers of t he genus. Mycelium pu re white, hyphae variable in diam. and distance in size a nd shape; often they are only weakly modified from the hyphal cells giving r ise to them, or they may have a ene-sided swelling, but other forms are not uncommon. This makes it pointless to give any figure for their size (Fig. 5). On media with poor growth, e.g. low osmotic pressure, most of the hyphae may be converted into chlamydospores. appear sticky and are not very easily pressed out of the cysts, diam. 3-5, av. 3.7 p ( B ETTS 1912: , av. 4.3 p) (Figs. 4 and 10). turns dark olivaceous to brown (Fig. 7), cysts form vari able, the extremes bein g almost globose 15.5 and 42 p, av X 30.6 p, the 1912: X Il ). No difference in size was observed between largest difference in two dimensions in a cyst of 19 X 34 p (BETTS cysts from honeycombs and those from culture (Figs. 4 and 8). 'pollen mould'. 1968) are mainly pyriform with truncate base, but oval to subglobose measure 4-10 X 5-11, av. 6.0 X 7.9 P (BETTS 1912: X p, forms occur. The spor es often have a hyphal rest at the base. They but this also ineludes the chlamydospores) (Fig. 5); cf. GIAUFFRET & TALIERCIO (1967). mellifera L.) in the cells of the honeycomb, hence the common name The free, hyaline, spherical, unicellular and smooth ascospores The chlamydospores are hyaline and thick-walled, greatly vari able The hyaline, thich-walled and smooth aleuriospores (sensu BARRON H a b i t a t : Sapr ophytic on pollen stored by honey bees (Apis - 7 -

10 - 8- Fig. 5. Bettsia aloei. Aleuriospores and chlamydospores. Top right, air mycelium or aleuriophores with aleuriospores on very short branches. X To the left, aleuriospores. X Bottom right, mycelium with intercalary chlamydospores. X 400. G r o w t h c o n d i t i o n s: B. alvei grows poorly or not at all on ordinary media ; on a medium containing 250 g honey (cf. BETTS 1912), 2 g yeast extract and 1.5 g mycological peptone pro litre growth is fairly good with produetion of sp ore cysts, but the growth is best and with plenty of sp ore cysts when the peptone is replaced by 5 g pollen (after melting the agar, the medium is boiled with the other ingredients f or 15 min; - do not autoclave - aureomycin may be added to prevent bacterial growth). On a medium with 250 g glucose + fructose (1: 1) the mycelial growth appears normal, but no spore cysts were produced. On comparable amounts of suerose growth is po or. B. alvei does not start growth at room temperature (20-23 o C). but placed at 18 0 the growth rate is fairly good but even at those obviously favourable conditions the fungus may suddenly stop sp orulating. These specialized requirements restriet the growth in nature to one particular habitat, the honeycomb. The experience of bee keepers is that the pollen mould, B. alvei) is rather common from autumn to spring when it grows on pollen in the cells of the honeycomb, mainly in those removed from the beehive.

11 - 9- For storage, the bees fill the cells with pollen, though normally finished with a layer of honey on top before they are closed with wax. In such cells B. aivei does not grow, but in cells not filled up with honey or where the honey on the top is removed, it grows excellently (Fig. 6). This agr ees with my results and those of BETTS (1912) and GIAUFFRET & TALIERCIO (1967). F ig. 6. Bettsia alvei. Cross section of a honeycomb with stored pollen infe ste d with the pollen mould, The white mycelium on the pollen in the three cells to the left is clearly visible with a sharp black rim between the mycelium and the pollen. This r im consist s of huge amounts of spore cysts. To the right, the bottom of t hree empty cells may be seen. - X 3. Materia l exa mi n e d: (a) CBS , leg. A. MAASSEN as Pericystis alvei. (b) CBS , leg. Dr. A. MAURIZIO as a + st rain of Pericystis alvei. (c) CBS , leg. Dr. A. MAURIZIO as a - strain of Pericystis alvei. These strains show increased gr owt h on the honey-pollen medium compared with common media, but for the rest their growth and habitus were ab normal ; and do not mate. (d) Isolates from a honeycomb with pollen heavily infested with the pollen mould, B. alvei'y) ) supplied by the experienced bee keeper, P. RØNNE, Skee, Ringsted, Zealand, March * ) B. alvei grew to gether with Erem ascu.s, probably E. [ertiiis STOPPEL, a lso an osmophilic fungus, that has earlier been found on such a habitat by M AURIZIO a ccor ding to HARROLD (1950 ) ; compare the taxonomy of t he fungi above.

12 10 - A search for the type of B. alvei was unsuccessful, so after all it do es not exist, and therefore culture No. 858 of (d) is designated as neotype for B. alvei and deposited at CBS, Baarn, The Netherlands, as accession No. CBS and a subc ult ur e is deposited at CMI, Kew, Surrey, E ngla nd, as IMI No II. Aseosphaera OLIVE et SPILTOIR Basionym: Pericusiis B ETTS This genus has been well deseribed by SPILTOIR & OLIVE (1955), though the present author does not think any of its species has mor e than one t r ichogyne pro ascogonium after separating Bettsia. F urther it should be stated that the fungi have a septate mycelium, a nd t herefore t hey are not coenocytic (s ensu nonseptate) a s c1aim ed by GAU MANN (196 4). 1. Aseosphaera apis (MAASSEN ex CLAUSSEN) OLIVE et SPILTOIR Genus type emend. Basionym: Pericystis apis M AASSEN ex CLAUSSEN Synonyms: Peri cystis api s M AASSEN ex CLAUSSE var. minor P ROKSCHL et ZOBL Illegitimate according to the rules. A scosphaera apis ( MAASSEN ex CLAUSSEN) OLIVE et SPIL TOIR var. tipis OLIVE et SPILTOIR MAASSEN (1916 ) recognized the fungus causing chalk brood in honey bees (A pis me lli ier«l.), and found it different from Pericystis alv ei BETTS (see above). He proposed the name P. apis which was retained by CLAUSSEN (1921) who made a not very detailed description of the fungus. The morphology and physiology of A. apis were further studied by MAURIZIO (1934, 1935) who compared it with isolates with larger spore cysts (see below) and supposed that they might be two separate species. MAURIZIO (1935) and later PROKSCHL (1953) both tried, without success, t o cross A. apis with isolates of that with larger spore cysts. On this basis the latter erected varieties. SPILTOIR & OLIVE (1955) introduced Ascosphaera and validated the varieties, but their results were based on A. apis and literature only. The main part of the studies on ontogeny and cytology of this group of fungi was made on A. apis (cf. e.g, VARITCHAK 193 2, 1933, PROKSCHL 1953, SPILTOIR 1955).

13 - I l - D e s c r i p t i o n e m e n d.: The mycelium is loosely arachnoid caused by long distances between the dicotomous branching, uniform with few small vacuoles, white to greyish white , av. 4.5 Il (SPILTOIR 1955: 4-8 Il) in diam. No conidial state or chlamydospores are observed which is in agreement with all authors but PROKSCHL (1953), who c1aimed the existence of chlamydospores, The olivaceous or brown globose spor e cyst s occur in s pots or spread all over t he agar. The rather fragile cyst membrane is very finely verrucous (Fig. 7). This may be obscured wit h age by crystalliferous precipi tations in or on the mebrane. Left, t he structure-iess m embrane of B ettsi a alvei; middle left, the fin ely verr ucous membrane of Ascosphaera apis; middle ri ght, the indistinctly also be substrate-dep endent as a bacterial contamination lowered the size of the spore cysts (CBS , see material examined), but did spotted membrane of A. m ajor; r ight, the membrane of A. proliperda ver - MAURIZIO (1935) found an average of 65.8 Il with 17.4 % at 40 Il or below and 0.1 % above 120 Il, while PROKSCHL noted J1 and structures, but with a viscous surface, ellipsoidal to reniform or s ubcylindr ic with very few having clearly parallel sides. Their size Besides being temperature-dependent (MAURIZIO 1935) the size may SPILTOIR & OLIVE (1955) Il. The present author found sizes in the range from 45 to 119, av p for CBS (Fig. 8 ). not change the size of spore balls and spores. significant differences between CBS and CBS (Fig. 9). No other authors have presented figures for this character. The diameter of the spore cysts va ri es to some extent ; thus The spherical spore balls measured , av Il wit h out The one-celled hyaline ascospores are without visible internal rucous with confluent small and larger warts. - X Fig. 7. Surfaee structure of the spore cyst membranes.

14 12 Fig. 8. Gen er al view of the spore cysts. Left, B ettsi a azvei; middle left, A scosp haer a apis; middle r ight, A. major; right, A. prozi perda. Note t he extreme variation in the size of t he spor e cysts of A. maj or, - X Fig. 9. Spore balls of the Ascosphaera sp ecies. Left, A. apis; middle left, A. m ajor, spore balls from an isolate wit h a rather persistent joint membrane around the ascospores; middle right, A. major,' right A. proziperda. Note the differen ce in internal structure of A. proziperda and the others which gives a hint about the larger a sc ospores of the for m er. - X 400. was found to be X li by PROKSCHL (195 3 ), 1.9 X 3.2 p by SPILTOIR (1955), and X p by SPILTOIR & OLIVE (1955), while the present author got X , av. 1.4 X 2.7 p, ratio lengthjbreadth 1.9, without significant differences between cul tures studied (Fig. 10). H a b i t a t: Cause of chalk brood in honey bee s (Apis mellif era L.), and a few obscure cases in leaf-cutting bees, M egachize sp. (MELVILLE & DADE 1944) and M. i nermis PROW. (BARER & TORCHIO 1968) ; see further the discussion. G r o w t h c o n d i t i o n s : A. api s grows fairly well on malt extract agar, more slowly on potato dextrose agar or oat meal agar. Mycelial growth and sporulation at C without pronounced effect on the size of the spore cysts (cf. MAURIZIO 1935).

15 Material examined: 13 - (a) CBS , leg. Dr. A. MAURIZIO as Pericystis apis. (b) CBS , leg. CBS as Ascosphaera apis. (c) Larvae of honey bees mummified 'by the chalk-brood-causing fungus, leg. Dr. L. BAILEY, Rothamsted, England, 1965 as Pericystis apis. (d) Two sets of similar material from Denmark, leg. Dr. O. HAM MER, Danish Gover nment Bee Research Service, June 1971 as chalk br ood. pared it with A. apis which made her suggest that it might be a separate species. Unfortunately she did not give figures for spore balls MAURIZIO (1935) first discovered this fungus and carefully com and spores and no material of hers exists any more*). it with A. apis (see this). On this basis he erected the variety Pericy.stis apis var. major) mentioning only en passant that the ascospores were 10 % larger than those of the type. No latin diagnosis was given, and apparently his material do es not exist any more>"). the variety under Ascosphaera without seeing any material. rediscovered several times during the last two years (cf. NØRGAARD HOLM & SKOU, in the press). **) Personal communication from Professor Dr. M. MOSER, Universit Y af 2. Ascosphaera major (PROKSCHL et ZOBL) comb. nov. emend. SPILTOIR & OLIVE (1955) did not add anything new, but validated Basionym: P er icystis apis MAASSEN ex CLAUSSEN var. major PR6KSCHL et ZOBL Synonym: Ascosphaera apis (MAASSEN ex CLAUSSEN) OLIVE et SPIL Etymology: 'major ' refers to the spore cysts which, greatly variable in size, may range up to 280 Il in diam. according to PROKSCHL (1953) rediscovered thefungus and was unable to cross In the studies of diseases in pollinating bees A. major has been D e s c r i p t i o n e m e n d.: Sex characters and morphology as Innsbruck, Austria. * ) Personal communication from Dr. ANNA MAURIZIO, Liebefeld, Switzerland, and Dr. J. A. VON ARX, Baarn, The Netherlands. TOIR var. m ajor (PROKSCHL et ZOBL) OLIVE et SPILTOIR MAURIZIO (1935) who referred to them as the 'grossfrtichtigen Form'.

16 Fig. 10. The ascospores. Left, Bettsia azvei; middle lef't, A scosphaer a apis; middle ri ght, A. major) and right, A. proliperdo, N ote the sl ender spores of A. major. - X 700. t hose of t he type. 'I'he mycel ium is caespitous ca used by short dist ances between the dicotomous branching, dense mycelium with small vacuoles, loose wit h greater va cuoles, white to gr eyi sh white, , av. 5.8 li in diam. No conidial state or chlamydospores were observed, but numerous t hin-walled protoplasma-rich swellings may occu r on the mycelium, especially at poor growth conditions. The dark-brown globose sp ore cysts normally occur in huge amounts spr ea d over t he agar. They are extremely variable in size which is in clos e a greement with MAURIZIO (1935) who found an average of li with 4.4 % at 60 I l or below and 3.7 % above 200 li (4 out of 2500 measured 280 p ), while PROKSCHL (1953) only noted adiam. of li. The present author found sizes from 59 to 213, av li (Fig. 8). The rather fragile cyst membrane is indistinctly spotted (Fig. 7), hardly verrucous, with crystalliferous precipitations occurring with age. The spherical sp ore balls measure 9-24, av li (Fig. 9). Their membranes are more persistent and their spores more viscous than those of the other species, but there are differences between isolat es. The one-celled hyaline ascospores are normally without internal structure, but infrequently a subterminal, hardly visible refractive spot occurs. They are mainly plano-convex to suballantoid or cylindric (Fig. 10), measuring X , av. 1.3 X 3.4 li, ratio lengthj breadth 2.6. This gives a clear difference in shape between A. api s and A. maj or) and t he difference in size agrees with the findings of PROKSCHL (1953). H a b i t a t: Cause of chalk brood in honey bees (Apis mellif er a L.) (MAURIZIO 1935, PROKSCHL 1953), and in the leaf-cutting bee (Megachile centuncularis L.) (author) ; cf. further the discussion.

17 G r o w t h c o n d i t i o n s: A. maj or grows well on ordinary me dia, but somewhat more vigor ously than A. api s. Mycelial growth at C a nd sporulation at C with a clear temperature effect on t he size of the spore cysts accor ding to MAVRIZIO (19 35). M a t e r i a l e x a m i n e d: Ten isolates from cases of chalk brood in cells of M egachile centuncularis L. All but one from a garden a t Glostrup (suburb of Cop enhagen ) in 1969 a n d 1970 (NØRGAARD H OLM & SKOV, in t he pr ess ). Culture No. 848 from 1969 is designated as ne otype for A. maior and deposited at CBS, Baarn, The Net herla nds, as accession No. CBS , and a subculture is deposited at CMI, Kew, Surrey, E ngland, as 1M! No Ascosphaera proliperda sp. no v. E tymology: 'proli' of proles = brood, progen y, and 'pe r da' of perdo = dest ro y. A. pr oiiperiia was discovered from one to several times in each of t he years , causing a ehalk-brood-iike disease in M egachile centuncularis L. reared in greenhouses at the Department of Crop Husbandry and Plant Breeding of the Royal Veterinary and Agricultural University of Copenhagen (cf. the introduction). The f ungus must have been introduced to the g r eenhouses from outside and only propagates where the bees live close together (NØRGAARD HOLM & SKOV, in the press). D e s c r i p t i o : Characteres morphologici et sexuales ut in specie typifica. Mycelium rude, granulosum, vacuolis multis, sparse vel crebre dichotomum, caespites formans e fasciculis laxis compositos, album vel cinereoalbum, J.l crassum. Nullus status conidialis nec chlamydosporae observata. Sporocystae sphaericae, fuseae, verrucis parvis et majoribus confluentibus ornatae, fragiles, J.l diam. Ascospor ae in globulos sphaericos J.l diam. congregatae, un icellulares, hyalinae, maculis refringentibus singulis vel pluribus, impri mis cuiq ue una subterminali, notatae, muco sub microscopio manifesto viscosae, s ubcylin dr ica e vel suballantoides, lateribus pl erumque parallelis, Il crassa e, 2.2 diametros vel li longae. Habitat in M ega chile centuncu lari L. parasitica. D e s c r i p t i o n: Sex characters and morphology as those of the type. The mycelium is caespitous caused by growth in loose fascicles and va rying degrees of dicotomous branching, coarse, granu-

18 Fig. 11. Ascosphaera proliperda. As cospores showing the refra ct ive spots and the m ucous secreti on on t heir surface. - X lal', and rich in vacuoles, white to greyish white, , av. 6.2 u. No conidial state Ol' chlamydospores are observed. The spherical dark-brown spore cysts spread over the agar. The rather fragile cyst membrane is verrucous with small and larger warts which are to a varying degree confluent (Fig. 7). Crystalliferous precipitations in Ol' on the membrane occur with age. Cyst diam , av ,li with 0.4 % below 80 and above 200,il (Fig. 8). The spherical spore balls with the outer spores lying parallel with the surface are 11-25, av /l in diam. (Fig. 9). In the one-celled hyaline ascospores one Ol' more clearly visible refractive spots, primarily one subterminal, are often seen. Their surfaee is viscous, a nd the mucous secretion is easily seen in phase contrast (Fig. 11). The spores are subcylindric to suballantoid, nearly always with parallel sides, measuring X , av. 2.5 X 5.5 Il, ratio length/breadth 2.2 (Fig. 10). H a b i t a t: The cause of a chalk-brood-like disease in the leafcutting bee M egaehile centuncular is L. : G r o w t h c o n d i t i o n s : As the other Ascosphaera species A. proliperda grows well on ordinary media, but addition of 0.2 % yeast extract enhances the gr owth and sporulat ion. One out of nine isolates differed by a more voluminous air mycelium and only few ascomata on malt extract agar and none on potato dextrose agar and oatmeal agar. A. proliperda grows slowly Ol' not at all at 10 C ; at 15 C the growth is slow, and no ascomata are forme d, but at

19 room temperature (20-23 C) the growth is excellent and the amount was only recognized by similarity in growth and symptoms on cell present. An attacked cell collected in June 1967 in the greenhouses (cf. the introduction) is designated as the holotype, and culture No. 787 Netherlands, as accession No. CBS , and further culture No. 810 as CBS A subculture is deposited at CMI, Kew, Surrey, England, as IMI No isolated from this cell is designated as the typeculture for Ascosphaera proliperda sp. nov. Both are deposited at CBS, Baarn, The of ascomata abundant. M a t e r i a l e x a In i n e d: Ten isolates from attacked larvae of M. centuncularis collected as mentioned above. One isolate differed in growth requirements and by slightly larger spores, another gr ew as sterile mycelium at the conditions tried and to be sure of the real differences between the species and to estimate their value for erecting species. The following comparisons should In spite of the fact that differences were observed in most characters examined, it may be difficult, from the figures given above, clarify this. a nd larva. Such cases were also observed in A. apis and A. major by MAURIZIO (1935 ). Obviously only one of the two sexes has been gr oss morphology, hyphal morphology, hyphal diameter, surface structure of the ascomata and so on, but however important they might and their contents, the figures of which are compared below. The be, they will always be ranged lower than those of the ascomata agar at room temperature. comparisons were made after growth on malt extract-yeast extract separating the species as the peaks for A. apis and A. proliperda are variation in the size of the cysts. The curves for A. apis and A. major distinct, whereas that of A. major falls in between with an extreme are in close agreement with those of MAURIZIO (1935). the others. as it is only possible to distinguish the smaller ones of A. apis from COMPARISON OF THE ASCOSPHAERA SPECIES It is worth noting the substantial differences in characters as The size distribution of the spore cysts (Fig. 12) is of value for F R IES IA X The size distribution of the spore balls (Fig. 13) is of less value

20 oa. apis la. major ~A. proliperda spore cysts (diam.) 200 fj Fig. 12. A scosphaera. Size distribution of the spore cysts of the three species 40 0J0 DA. apis 30 IA.major ~A. protiperda fj spore batts (diam.) Fig. 13. Ascosphaera. Size distribution of the spore balls of the three species. The shape and size of the ascospores are almost invariable characters at varying conditions for which reason they are unique for separating the species. The distribution curves for their length (Fig. 14) show three distinct peaks for the three species and a greater variation in the spore size of A. proliperda. The difference between A. apis and A. major is in agreement with that noticed by PROKSCHL (1953). The distribution curves for the breadth of the ascospores (Fig. 15) show no significant difference between A. apis and A. major)

21 DA. apis la.major ~A.proliperda 2 3 l. 5 6 length of spores 7 }l Fig. 14. Ascosphaera. Length distribution of the ascospores of the three species. though A. apis in contrast to A. major has about 10 % spores above 1.6 p. In faet, the spores af A. major appear more slender than those af A. cpi«, which may be expressed by the lengthjbreadth ratio which is 2.6 and 1.9 respectively. The spores af A. proliperda are very different from the others. In Figs the columns give the amount of units ranging from one figure to the next at the abscissa, i. e. for the spore cysts p, p, - - -, 200 p and above. All the measurements were made with a Carl Zeiss Ocular Screw Micrometer, making it possible to differentiate between the figures on the abscissa in Fig. 15 assuming the error being constant at each measurement. an the basis of the above it may be concluded that the fungi differ so decisively in most respects that it is natural to separate them into species, and further that all four species may be effectively identified by means of the foliowing key.

22 DA. apis la.major ~A. proliperda breadth of spores }J Fig. 15. Ascosphaera. Breadth distribution of the ascospores of the three species. KEY TO THE SPECIES OF ASCOSPHAERA AND BETTSIA Spore cyst membrane structureless, cysts small, form variable, extreme 19 X 34 u, av. approx. 30;il, pronounced supporting hyphae ; ascospores one-celled, spherical, 3-5 u, not in spore balls; mycelium pure white with numerous 1 aleuriospores and chlamydospores; saprophytic on pollen in beehives Bettsia alvei Spore cysts larger, globose, supporting hyphae not pronounced; ascospores one-celled, not spherical, in sp ore balls; no conidia or chlamydospores 2 Spore cyst membra ne very fi nely verrucous; cysts, spore balls, and t he ellipsoidal to r eniform spores small, , 2 av. 80 p, 7-18, av. 12.5;il and 1-2 X 2-3.5;il respectively; parasitic on honey bees Ascosphaera apis Spore cysts, spore balls and spores larger 3

23 Spore cyst membrane indistinctly spotted, cysts extremely variable in size, Il, av. 128 Il; spore balls 9-24, av. 16 Il; spores plano-convex to suballantoid, X 3-4 Il ; parasitic on honey bees and some solitary bees. Ascosphaera major less variable Il, av. 134 Il; spore balls Il, av. 17 Il; spores subcylindric to suballantoid, typically with parallel sides X Il, with internal refractive spots and mucous surface ; parasitic on some solitary bees Ascosphaera proliperda saprophytic on pollen in beehives, though some confusion may be found in the literature ; likewise that A. apis and A. major are the cause of chalk brood in honey bees, and further that A. major and A. proliperda are responsible for a chalk-brood-like disease in the leaf-cutting bee M. centuncularis (cf. NØRGAARD HOLM & SKOU, in the press), though A. major is obviously also able to thrive on the excrements of those bees and is, may be, primarily a facultative parasite. 3 Spore cyst membrane verrucous with confluent warts, cysts the drone brood, and that this should be decisive for its importance. but the statements in the literature are very uncertain as the authors seen something between contaminants. According to MELVILLE & have not measured or cultured the organisms, or they have just DADE (1944) and to BAKER & TORCHIO (1968) A. apis should also be pathogenic on Megachile sp. and M. inermis PROW. Further BAKER & honey bees. This is in agreement with the experience in Denmark, TORCHIO (1968) c1aime to have found A. major on Anthophora paciiica CRESS., but if it was an Ascosphaera species at all, it might have been A. proliperda as well. More obscure is the finding of Ascosphaera sp. on the mason bee (CLOUT 1956). is not mentioned in any previous study. It may be of significance for the transfer of the fungi (cf. NØRGAARD HOLM & SKOU, in the press). It seems well established that B. alvei is apathogenic, solely It is possible that the Ascosphaera species also attack other bees, STElNHAUS (1949) incorrectly states that A. apis only attacks The viscous to slimy surface of the ascospores of all the species GIAUFFRET & TALIERCTO (1967) state that A. apis is endemic in DI S CU S SIO N

24 and our findings with A. major and A. proliperda point in the same direction for these species in M. centuncularis, but this does not prevent serious attacks when the conditions are for it (cf. NØRGAARD HOLM & SKOD, in the press). The signifieanes of the crystalliferous precipitations in the cyst membrane is unknown, but might be connected with the disintegration of the mycelium also occurring with age. At the same time the cultures, at least that of A. proliperda, get a characteristic smell. When many cultures of A. proliperda are growing old t oget her, nothing special happens to them, but if new cultures are propagated close to old cultures, they seem to ha ve an inhibitory effect on the chitinizing and ripening of t he spo re cyst s. A. proliperda sporulat es best when growing on slants with screw cap o A connection between t hese observations is questionable. ACKNOWLEDGEMENTS The author is gr ea tly indebted to sv, N ØRGAARD HOLM, t h e Royal Veterinary and Agricultural University of Copenhagen, without whose careful and inspirative studies on the pollinating bees, the diseases, which gave the start to the present work, would hardly have come into the author's fie Id of interest. Further the a uthor wishes to thank Dr. J. A. VON ARX, director, CBS, Baarn, The Netherlands, for his kind answer s to all my questions, Dr. L. BAILEY, Rothamsted and Dr. O. H AMMER, the Danish Government Bee Research Se rvice, for the mummified honey bee larvae supplied, and the bee keeper, P. RØNNE, Skee, Ringsted, Zealand, for the honeycomb infested with the pollen mould. Finally, special thanks are du e to Dr. T YGE CHRISTENSEN, Institut for Sporeplanter, University of Copenhagen, for preparing the Latin diagnoses. REFERENCES Agardh, J.: Nya alger f'r ån Mexico. - ofversikt Kung!. Vetensk. Akad. Forhandl. 1847, 4 : 5-17, Ainsworth, G. C., P. W. James & D. L. Hawksworth: AI NSWORTH & BISBY'S dictionary of the fungi. 663 pp. - CMI, Kew, Surrey Alexopoulos, C. J.: Introductory mycology, 2nd ed., 613 pp. - John Wiley & Sons, N.Y von Arx, J. A.: The genera of fungi sporulating in pure culture, 288 pp. Verlag J. Cramer, Lehre Baker, G. M. & P. F. Torchio: New records of Ascosphaera apis from North America. - Mycologia 60 : , 1968.

25 Ba rron, G. L. : The ge nera of Hyphomycetes from soil, 364 pp. - Williams & Wilkins Co., Baltimore Bessey, E. A.: Morphology and taxonomy of fungi. (Family Pericustaceae, p ). - The Blakiston Co., Philadelphia Betts, Annie D.: A bee-hive fungus, P ericystis aloei, gen. et sp. nov. Ann. Bot. 26: , Booth, C.: Fruit bodies in Ascom.ucetes. - In: G. C. AI NSWORTH & A. S. SUSSMAK (eds.): The fungi. An advanced treatise II, p , Buchanan, R. E.: Morui sou e pur pureus in silage. - Mycologia 2: , von Biiren, G.: Die schweizerischen P rotomycetaceen mit besonderer Be rlicksichtigung ihrer Entwicklungsgeschichte und Biologre. Beitr. zur Kryptogamenfl. der Schweiz 5(1) : 1-95, Claussen, P.: Entwlcklungsgeschichtliche Untersuchungen uber den Erreger der als "Kalk br ut" bezeichnet en Krankheit der Bienen. - Arb. Biol. Rei chsanst. Land.-Forstw. 10 : , Clout, G. A.: Chalk brood and hunchback flies. - Bee Craft 38: 135, Cole, G. T. & W. B. I\:endrick: Conidium ontogeny in Hyphomycetes. The imperfect state of M onascus ruber and its meristem arthrospores. -- Canad. J. Bot. 46: , Fitzpatrick, H. M.: The low er fu ngi. Ph.ucomu cetes, 331 pp. - N. Y McGraw-Hill, Gaumann, E.: Vergl eichende Morphologi e der Pilze, 626 pp. - Verlag Gustav F'ischer, J ena : Die Pilze. Gr undztige ihrer E ntwicklungsgeschichte und Morphologie, 2. Aufl. 541 pp. - Birkhåuser, Basel Giauffret, A. & Y. P. Taliercio: Les mycoses de l'abeille ( A pis m ellijica L.), et ude de quelques a nti mycosiques. - BuH. Apicole Doc. Scl. Tech. Inform., F r. 10 : , HarroId, C. E.: Studies in t he gen us Eremascu s. I. The rediscovery of E r e: m ascus al bus EWAM a nd som e new observations concerning its lif e-history and cytology. - Ann. Bot., N.S. 14: , Holm, S. Nørgaard & J. P. Skou : Studies on trapping, nesting and rearing of some M eg achile species (Humenoptera, M egachilidae) in Denmark. - In the press. Lanjouw, J. et al. (e ds.) : International code of botanical nomenclature. Re gnum Veg etabile 46: 1-402, Maass en, A. : trber Bi en enkrankheiten..- Mitt. kaiserl. Bio l. Anst. Land. Forstw. 16: 51-58, Maurizio, Anna : trber di e Kalkbrut ( Pericystis Mykose) der Bienen. Arch. Bienenkunde 15: , : Bertra ge zur Kenntnis der Pilzflora im Bienenstock. r. Die P er i cy stis-infektionen der Bienenlarven. - Ber icht e Schw. Bot. Ges. 44: , 1935.

26 Melvill e, R. & H. A. Dade : Chalk brood attacking a wild bee. - Nature 153: 112, Prokschl, H.: Bettråge zur Kenntnis der Entwicklungsgeschichte von Pericystis apis MAASSEN. - Arch. Microbiol. 18: Spiltoir, C. F.: Life cy cle of Ascosphaera apis (P ericystis apis). - Arner. J. Bot. 42 : & L. S. Olive: A reclassification of the genus Pericystis BETTS. - Mycologia 47: , Steinhaus, E. A.: Principles of insect pathology. 757 pp. - McGraw-Hill, Lond on Varitchak, B.: L'evolution nucleaire chez le Pericy stis api s MAASSEN. C. r. hebd. SeanCe Acad. ScL, Fr. 194: , Deuxieme contribution 11 l'etude du developpement des Ascornycetes. L'evolution nucleaire dans le sac sporirere de Pericystis apis MAASSEN et sa signification pour la phylogenie des Ascomycetes. -- Le Botaniste 25 : , Young, E. M.: The rnorphology and cytology of Monascus rub er, - Arner. J. Bot. 18: , Roskilde, October 1971.

27 FRIESIA. Bind X. Hefte LEAF SPOT DISEASES ON GRAMINICOLOUS SPECIE S AT A LOCALITY IN GREENLAND By V. SMEDEGÅRD-PETERSEN and J. E. HERMANSEN Department of Plant Pathology. The Royal Veterinary a nd Agricultural University, Copenhagen. SUMMARY In the period cereal and grass samples from Greenland were examined for leaf spot diseases. N o leaf spot diseases were identified from cereal samples, whereas each of the following pathogens were isolated from one or more grass species: Drechslera poa e, E rysiphe graminis) H et erosporium phlei, Mastigosporium rubricosum, Rhynchosporium orthosporwm, Selenophoma donacis var. stomaticola and Spermospora subulaia. With the exception of a few localities at which rye is grown for grazing, cereal growing in Greenland is confined to the Agricultural Station Uperniviarssuk at Julianehåb. In addition to the local grass flora, cultivated grass species are present at Uperniviarssuk. Little information is available concerning the appearance of grass and cereal diseases in Greenland. HERMANSEN (1968) demonstrated that examination of cereal samples consisting of about 50 shoots may reveal low degrees of severity of cereal rust and mildew diseases. Similar results were obtained by HERMANSEN & WIBERG (1972) in studies of barley samples from the Faerdes. In order to obtain preliminary information on the situation in Greenland concerning the occurrence of leaf spot diseases on cereals and grasses, the Royal Greenland Trade Department was asked to

28 provide samples of cereals and grasses. It was arranged for the colleetion of such samples at Uperniviarssuk and shipment by ai r to Copenhagen bimonthly in the period from ultimo July t o primo October during the years The samples, which usually consisted of ab out 50 tillers, generally arrived in very good condition and the plants were immediately examined for leaf spot diseases. Each collection of samples consisted of one or more varieties of rye, wheat, barley and oats, together with a varying number of grass species. The foliowing cereal vari eties were used. Spring rye : P et kus (diploid), Petkus (tetraploid) and Rheidol grazing rye ; Spring wheat : Pompe and land-wheat; Spring barley: Bomi, Nordland, Nordlys, and Jotum; Spring oats: Rex, Sun II (Stål), Astor, Sørbo, Walisian, Mustang, Silva, Bento and two numbered oat lines. The foliowing grass species were examined. Without leaf spot diseases : Agropyron repens (L.) BEAUV., Deschampsia caespitosa (L.) BEAUV., Elymus arenarius L., Festuco rubra L., Festuca vivipara (L.) SM., Lolium multijlorum LAM., and Poa annua L. With leaf spot diseases : Agrostis stolonijera L., Agrostis tenuis SIBTH., Agrostis sp., Alopecurus pratensis L., Calamagrostis langsdorjii (LINK) TRIN., Phleum prat ense L., and Poa prat ens is L. The following pathogens were identified and isolated from the lea f spots: Drechslera poae (BAUDYS) SHOEM. Erysiphe graminis DC. ex MERAT. Heterosporium phlei GREGORY. Mastigosporium rub ricosum (DEARN. & BARTH.) NANNF. Rhynchosporium orthosporum CALDWELL. Selenophoma donacis var. stomaticola (BAUEML.) SPRAGUE & A. G. JOHNs. Spermospora subulata (SPRAGUE) SPRAGUE-BLAST. The host pathogen combinations are listed in Table 1. Except for a preliminary note by SMEDEGÅRD-PETERSEN (1970), the present paper constitutes the first report on grass diseases in Greenland. All of the pathogens listed in Table 1, with the exception of Spermospora subulaia, are known to occur in Denmark. Rhynchosporium orthosporum, however, has not previously been noted as a pathogen on Calamagrostis langsdorjii (this species does not occur in Denmark) or Alopecurus pratensis. Similarly, Mastigosporium ru-

29 D r echeler a poae Erysiphe graminis H et er ospo r i u m phlei TABLE 1 P athogen Host plant M asti g osp orium rubricosum Poa pratensis P oa pratensis P h l eu m pratense Agrosti s stoloniiera Number of samples with total symptoms bricosum has not previously been reported as a pathogen on Agrostis stolonijera or A grostis tenuis in Denmark. Spermospora subulata eauses olive grey spots with dark red borders. These spots are often diffuse as a scald and increase to large portions of the leaf blade. On A grostis stolonijera the fungus was often found together with Mast igosporium ru bricosum. The symptoms caused by the two pathogens were somewhat similar, but the lesions formed by Spermospora subulata were larger and more diffuse than lesions caused by MasNgospori'um ru bricosum: Spermo spora su bulaia produces spores in large numbers which appear as a compact mass on the affected tissue. Conidia are hyaline with 1-3 septa, broadly rounded at the base and often constricted at the septa. The distal cells are elongated with an appendage or cilium which is sometimes straight, but very often curved or flexuous (see Fig. 1). Conidia from Agrostis stolonijer a measure 44 by 4.1,u (a verage of 33 conidia). In a few cases the samples arrived in poor condition and the identification of grass species a nd pathogens in such samples was not always possible. Leaf spot diseases appeared on more than half of the grass species regularly received but were not found on any of the cereal species. R hy n cho spor-ium orthosp or u m Selenophoma donecis var. stomaticola Bpermosp ora subulata Agrostis t enuis Agr ostis sp. Phleu m pratense Alop ecurus pr at ensi s Ca lamagrostis langsdo rfii Phleum prat ense Agrostis stolonifer a Poa pratens i s Leaf spot pathogens and their host species based on 65 samples of grasses.

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