Marine Flora and Fauna of the Northeastern United States Higher Fungi: Ascomycetes, Deuteromycetes, and Basidiomycetes

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NOAA Technical Report NMFS Circular 398 Marine Flora and Fauna of the Northeastern United States Higher Fungi: Ascomycetes, Deuteromycetes, and Basidiomycetes A. R. Cavaliere March 1977 U.S. DEPARTMENT
NOAA Technical Report NMFS Circular 398 Marine Flora and Fauna of the Northeastern United States Higher Fungi: Ascomycetes, Deuteromycetes, and Basidiomycetes A. R. Cavaliere March 1977 U.S. DEPARTMENT OF COMMERCE Juanita M. Kreps, Secretary National Oceanic and Atmospheric Administration Robert M. White, Administrator National Marine Fisheries Service Robert W. Schoning. Director For Sale by the Superintendent of Documents, U.S. Government Printing Office Washinglon, D.C Stock 1\ I rd-- CONTENTS Introduction Methods of harvesting and studying Glossary. Figures of reproductive structures and spore shapes Key to major groups of fungi occurring in the marine environment Key to spore groups of Ascomycetes.... Key to genera and species of Scolecosporae Key to species of Lindra Key to genera and species of Amerosporae Key to species of Haloguignardia... Key to genera and species of Dictyosporae (Pleospora) Key to genera and species of Didymosporae Key to species of Ceriosporopsis Key to species of Corollospora Key to species of Didymosphaeria Key to species of Halosphaeria.. Key to genera and species of Phragmosporae Key to species of Haligena Key to species of Leptosphaeria..... Key to species of Sphaerulina Key to genera and species of Deuteromycetes Key to species of Dendryphiella Key to species of Zalerion Annotated list of species Ascomycetes Deuteromycetes Basidiomycetes Selected bibliography Index to genera and species of marine fungi Acknowledgments Coordinating Editor's comments iii FOREWORD This issue of the Circulars is part of a subseries entitled Marine Flora and Fauna of the Northeastern United States. This subseries will consist of original, illustrated, modern manuals on the identification, classification, and general biology of the estuarine and coastal marine plants and animals of the Northeastern United States. Manuals will be published at irregular intervals on as many taxa of the region as there are specialists available to collaborate in their preparation. The manuals are an outgrowthofthe widely used Keysto MarineInvertebratesofthe Woods Hole Region, edited by R. I. Smith, published in 1964, and produced under the auspices of the Systematics-Ecology Program, Marine Biological Laboratory, Woods Hole, Mass. Instead of revising the Woods Hole Keys, the staff of the Systematics~EcologyProgram decided to expand the geographic coverage and bathymetric range and produce the keys in an entirely new set of expanded publications. The Marine Flora and Fauna of the Northeastern United States is being prepared in collaboration with systematic specialists in the United States and abroad. Each manual will be based primarilyon recent and ongoing revisionary systematic research and a fresh examination of the plants and animals, Each major taxon, treated in a separate manual, will include an introduction, illustrated glossary, uniform originally illustrated keys, annotated check list with information when available on distribution, habitat, life history, and related biology, references to the major literature of the group, and a systematic index. These manuals are intended for use by biology students, biologists, biological oceanographers, informed laymen, and others wishing to identify coastal organisms for this region. In many instances the manuals will serve as a guide to additional information about the species or the group. Geographic coverage of the Marine Flora and Fauna of the Northeastern United States is planned to include organisms from the headwaters of estuaries seaward to approximately the 200 m depth on the continental shelf from Maine to Virginia, but may vary somewhat with each major taxon and the interests of collaborators. Whenever possible representative specimens dealt with in the manuals will be deposited in the reference collections of major museums. After a sufficient number of manuals of related taxonomic groups have been published, the manuals will be revised, grouped, and issued as special volumes. These volumes will thus consist of compilations of individual manuals within phyla such as the Coelenterata, Arthropoda, and Mollusca, or of groups of phyla. ii Marine Flora and Fauna ofthe Northeastern United States. Higher Fungi: Ascomycetes, Deuteromycetes, and Basidiomycetes A. R. CAVALIERE' ABSTRACT This manual provides an illustrated key and alphabetical listing, with brief descriptions. of common genera of higher marine fungi in the classes Ascomycetes, Deuteromycetes (Fungi Imperfecti), and a single member ofthe Basidiomycetes. A glossary and selected bibliography complement the key. Information on methods of harvesting, incubation, and studying these fungi is also included. INTRODUCTION This manual is a guide to the genera of higher marine fungi that inhabit the intertidal zone of the Atlantic waters extending from North Carolina to Nova Scotia. Keys, descriptions, and illustrations are included for genera of Ascomycetes, Deuteromycetes (Fungi Imperfecti), and a single member of the Basidiomycetes. Less conspicuous saline forms of zoosporic fungi, the socalled marine Phycomycetes, as well as parasitic fungi, amoeboid forms, and those inhabiting the intestinal tract of arthropods, are not included in this account. In addition, species of higher fungi are excluded which have been reported only once or are rare or inconspicuous in the mycological flora. Fungi inhabiting the saline environment appear to be cosmopolitan in distribution with only a few species having been shown to be endemic to one particular region. Some members of the marine mycoflora which are tropical, however, tend to be associated only with mangrove communities or other phanerogams which are restricted to warmer waters. METHODS OF HARVESTING AND STUDYING Marine Ascomycetes, Basidiomycetes, and Fungi Imperfecti occur as saprophytes on driftwood, cordage, and other cellulosic material, or as weak parasites infesting dying species of marine phanerogams or algae. Various plant parts, grass culms, driftwood, and algae are best collected along the shore at low tide and kept submerged in a container of seawater until studied. Fungi may also be induced to grow on substrates introduced into the seawater. A li4-inch hole is drilled through the center of small, 4 X 6 inch panels of various 'Department of Biology, Gettysburg College, Gettysburg, PA kinds of wood. These are then attached, in linear fashion, to a knotted, polyethylene or nylon line and submerged at or below the low tide limit for a 2-4 mo period. When panels are harvested, they are scraped of all macroscopic fouling organisms and rinsed in seawater. They are then examined for fungal growth and/or incubated individually for an additional period of one to several months in sterile, dry, air-tight aquaria or other glass containers. Several methods of harvesting and incubating-lignicolous fungi are described in the literature. Ascocarps, dense mycelial growth as well as conidial clusters, are located with a dissecting scope utilizing a high intensity light source. Conidial heads may also be located by placing thin strips of substrate in a drop of seawater on a slide and observing the preparation direct ly under a compound microscope. Semipermanent mounts are made by placing fruiting structures into a drop of lactophenol (20 g phenol crystals; 20 g lactic acid; 40 g glycerol; 20 g distilled water; 0.01 g cotton blue or acid fuchsin) or Hoyer's medium (made by soaking 30 g of flake -gum arabic in 50 ml of distilled water for 24 h, dissolving 200 g of chloral hydrate into the mixture, and then stirring in 20 ml of glycerol. Allow the mixture to settle before using.) When examining ascocarps or pycnidial structures, it is best to crush the fruiting bodies to expose the centrum. This is best accomplished by lightly tapping the cover slip with the handle endof a dissecting needle or the eraser en'd of a pencil. Spores of several of the marine species have gelatinous appendages which are best observed in a seawater mount under reduced light intensity or by phase contrast microscopy. Gelatinous appendages are deliquescent in most cases, short-lived, and, unfortunately, not retained satisfactorily in any known mounting medium. Pure cultures of marine Ascomycetes and Fungi Imperfecti are initiated by introducing spores or centrum cells from several ascocarps onto low nutrient level, seawater agar media and incubating at room temperature. Kirk (1969) offers the most useful account of the isolation and culture of lignicolous marine fungi (0.1% glucose; 0.01% yeast extract; 1.8% agar in aged seawater adjusted to approximately 20 0 /00 ; 0.03% U.S.P. streptomycin sulfate). White birch applicator sticks, balsa strips, filter paper, or toweling paper added to the culture tubes serve as an additional cellulosic substrate. Methods of preparing specimens for embedding, serial sectioning, and differential staining are outlined elsewhere (Cavaliere 1966, 1973). Several additional works covering various aspects of the biology and taxonomy of marine Ascomycetes may be useful to the student (Barghoorn and Linder 1944; Johnson and Sparrow 1961; Cavaliere and Johnson 1966; Kohlmeyer and Kohlmeyer 1971). GLOSSARY The use of mycological terminology has been reduced to a minimum. Several terms are defined as well as illustrated. More complete definitions are found in Snell and Dick (1957) and Ainsworth and Bishy (1971). Acuminate Gradually narrowing to a point. Amerospore One-celled spore; spore without partitions. Amorphous Without definite shape or structure. Anastomose To form a network of interconnecting hyphae. Antepenultimate Refers to the third to the last cell in any row of cells. Apiculate Having one to many sharp points or denticles. Appendage A process of any kind; a structure which adheres. Ascocarp A fructification in Ascomycetes bearing asci and ascospores (see Figs. 1-3). Ascospore A spore, typical of the sexual stage or cycle in Ascomycetes, borne in an ascus. Ascus A reproductive cell in Ascomycetes; a structure, within which are produced, by meiosis, normally 4-8 haploid spores (see Figs. 6, 7). Atte'nuate' Gradually narrowing or thinning. Awl-shaped Gradually tapering from the hase to a sharp, flexible or semirigid point. Bacilliform Refers to spores which are rod-shaped (see Fig. 24). Basidiocarp A fructification in Basidiomycetes producing basidia and basidiospores. Basidiospore A sexual spore; produced by meiosis and borne on a basidium. Basidium A cell within which nuclei first undergo reduction division then pass onto extensions externally forming basidiospores. Bitunicate Refers to asci having two walls; doublelayered (see Fig. 7). Biturbinate Refers to 2-celled spores having both ends conical and slightly curved. Catenulate Attached in chains. Clavate Cluh-shaped or thickened at the apex (see Fig. 13). Cleistothecium A more or less spherical covering en- closing asci; a fruiting structure in' the Ascomycetes (Plectomycetes) produced as a result of sexual reproduction and opening at maturity by a rupture (see Fig. 1). Concolorous Refers to the pigmentation being the same color throughout. Conidiophore A specialized hypha or cell hearing conidia. Conidium Spores produced by the Deuteromycetes; a spore borne on or in a specialized hypha termed a conidiophore; asexually produced spores. Deciduous Short-lived; falling away; not persistent. Deliquescent Dissolving or liquifying. Denticulate Having small teeth. Dictyospore A spore with many transverse and longitudinal septations; a muriform spore (see Fig. 23). Didymospore Two-celled spores; spores with a single partition. Echinulate With minute spines. Ellipsoidal Refers to spores having the shape of an ellipse; generally rounded at both ends and having curved sides (see Fig. 19). Elongate Longer than hroad, having parallel sides (see Fig. 18). Endogenous Borne or developing within. Epispore The outer layer of the spore wall. Erumpent Breaking through the surface of the substrate; refers to the position of the fruiting body with relationship to the substrate. Eucarpic Refers to a condition in which only part of the somatic thallus is converted in the formation offructifications. Filiform Refers to spores which are slender and threadlike (see Fig. 22). Fuscous Drab, gray or smokey in color. Fusiform Spindle-shaped or tapering at hoth ends (see Fig. 12). Fusoid Somewhat fusiform. Globose Refers to spores which are spherical (see Fig. 8). Guttule Oily, spherical glohule. Helicospore A spiral or helicoid spore (see Fig. 20). Holocarpic Refers to a condition in which the entire somatic thallus is converted into a fructification. Hyaline Transparent or translucent, colorless. Inequilateral Having unequal sides. Innate Occurring below the surface of the substrate. Refers to the position of the fruiting hody with relationship to the substrate. Intercalary Borne or developed hetween the hase and apex of hyphae. Involuted Rolled or enrolled. Lenticular Refers to spores shaped like a double convex lens (see Fig. 11). Muriform Refers to spores having both transverse and longitudinal septations (see Fig. 23). Oblong Longer than broad with approximately parallel sides (see Fig. 15). Obpyriform Reverse pear-shaped (see Fig. 17). Obtuse Blunt or rounded, not pointed. 2 Ovoid Egg-shaped (see Fig. 10). Pedicellate Borne on a pedicel or stalk. Penultimate Refers to the next to the last cell in any row of cells. Perithecium A more or less flask-shaped, papillate or beaked covering enclosing asci; a fruiting structure in the Ascomycetes (Pyrenomycetes) produced as a result of sexual reproduction (see Fig. 2). Peritrichous Having flagellumlike hairs surrounding the structure. Phialide Specialized conidiophore or cell within which conidia are produced and released (see Fig. 5). Phragmospore A spore having two or more transverse septations. Pleomorphic Having more than one form; polymorphic. Polymorphic Occurring in several forms. Pseudothecium A unilocular stroma. A cavity or lacule formed by the dissolution of stromatic tissue (see Fig. 3). Pycnidium In Deuteromycetes, a more or less flaskshaped structure bearing conidia on conidiophores internally (see Fig. 4). Pyriform Pear-shaped (see Fig. 16). Rhomboidal Refers to spores having oblique angles and equal or unequal adjacent sides; more or less diamond shaped. Scolecospore A long, thread-shaped, filiform or vermicular spore (see Fig. 22). Septate Having crosswalls or partitions. Sessile Without a pedicel or stalk. Seta Slender, bristle-shaped structure. Sheath A covering or envelope. Staurospore A spore which is more or less star-shaped (see Fig. 21). Stroma A more or less tightly interwoven mass of hyphae within or on which reproductive structures are formed. Subglobose Refers to spores or ascocarps which are nearly spherical; sides slightly flattened or compressed from the top (see Fig. 9). Truncate Ending abruptly, squared off at the apex. Undulant Wavy sheath or covering. Unitunicate Refers to asci having a single wall (see Fig. 6). Verrucose Covered with warts or marks. Verruculose Covered with minute warts. 3 FIGURES OF REPRODUCTIVE STRUCTURES AND SPORE SHAPES 1. cleistothecium 2. perithecium 3. pseudothecium Figures 1-3.-Reproductive structures in Ascomycetes. 4 4. pycnidium 5. phialide 6. unitunicate asci 7. bitunicate asci Figures 4-7.-Reproductive structures in Ascomycetes and Deuteromycetes... 5 8. globose 9. subglobose 10. ovoid '.., ,. 11. lenticular 12. fusiform 13. clavate 14. cylindrical 15. oblong 16. pyriform 17. obpyriform Figures Spore shapes in fungi. 6 18. elongate 19. ellipsoidal 20. helicoid 21. staurospore 22. filiform 23. muriform 24. bacilliform Figures 18 24,-Spore shapes in fungi. 7 KEY TO MAJOR GROUPS OF FUNGI OCCURRING IN THE MARINE ENVIRONMENT The preliminary key separates the nine major groups of fungi occurring in the marine environment: Labyrinthulae, Chytridiomycetes, Hyphochytridiomy cetes, Plasmodiophoromycetes, Oomycetes, Trichomycetes, Deuteromycetes, Ascomycetes, and Basidiomycetes (Nia vibrissa, the only representative of the Basidiomycetes included in this treatment, is keyed out directly). Both the classes Ascomycetes and Deuteromycetes are separated into genera utilizing the Saccardo sporological system. Morphology and color of the spores and conidia are the essential features employed in the Saccardo system. While the Deuteromycetes are keyed directly to genera or species, the Ascomycetes are divided into spore groups (Amerosporae, Dictyosporae, Didymosporae, Phragmosporae, Scolecosporae). Each spore group is then separated into the various genera. Genera of Ascomycetes are finally delimited into species based primarily on spore size and on the nature of spore appendages in those species possessing them. 1 Vegetative phase or stage entirely amoeboid Labyrinthulae 1 Vegetative phase or stage one- to many-celled, holocarpic or eucarpic 2 2 (1) Flagellated cells present &~ g~~=~~~ 2 (1) Flagellated cells lacking 6 3 (2) Motile cells uniflagellate 4 8 3 (2) Motile cells biflagellate (3) Flagellum of the whiplash type, posteriorly inserted Chytridiomycetes ~ ,~ ~ ~ 4 (3) Flagellum of the tinsel type, anteriorly inserted... Hyphochytridiomycetes 5 (3) Flagella heterokont, both ofthe whiplash type...plasmodiophoromycetes 5 (3) Flagella nearly isokont, one of the whiplash type, the other tinsel Oomycetes 9 6 (2) Hyphae attached to the digestive tract or cuticle of arthropods Trichomycetes 6 (2) Hyphae saprobic or parasitic on algae, phanerogams or other cellulosic materials (6) Sexually formed spores lacking; conidia usually formed in pycnidia (Fig. 4) or directly on vegetative hyphae. Deuteromycetes (p. 32) 7 (6) Sexually formed spores present 8 8 (7) Sexual spores, usually 8 in number, produced endogenously within asci Ascomycetes (p. 11) 10 8 (7) Sexual spores, usually 2-4 in number, exogenously produced on basidia Basidiomycetes (Nia vibrissa p. 46) KEY TO SPORE GROUPS OF ASCOMYCETES 1 Ascospores filiform or slender; more than 10 times as long as broad SCOLECOSPORAE (p. 12) 1 Ascospores not filiform or slender; never more than 10 times as long as broad 2 2 (1) Ascospores single celled (nonseptate) AMEROSPORAE (p. 14) 2 (1) Ascospores two- or more-celled (septate) 3 II 3 (2) Ascospores with transverse septa only (2) Ascospores with transverse and longitudinal septations; muriform. o 0 DICTYOSPORAE (po 15) 4 (3) Ascospores 2-celled (one septation only) DIDYMOSPORAE (po 16) 4 (3) Ascospores three~ or more~celled (multiseptations) PHRAGMOSPORAE (po 27) KEY TO GENERA AND SPECIES OF SCOLECOSPORAE 1 Ascospores single-celled (nonseptate) Ascospores three- to many-celled (multiseptate) (1) Ascospores 50~750/-l; provided with a conoid cell or appendage at each end..... LUlworth~i~a~m:e:d:u:s:a~;::;:#~::::~ 12... 2 (1) Ascospores usually shorter than 30.u; without appendages... (see also Amerosporae) Halonectria milfordensis 3 (1) Ascospores with a caplike, bulhous or threadlike appendage ateach end (1) Ascospores without appendages (3) Appendages bulbous, subspherical Lindra (po 14) 0 0 (see 4 (3) Appendages caplike or threadlike 0 also Pbragmosporae) Haligena (po 29) (3) Ascospares to long, 3- to 4-celled, tapering at one end Trailia ascophylli 5 (3) Ascospores to 400,u long, filiform, cylindrical or tapering at both ends 13 o Lindra (po 14) Key to Species oflindra 1 Ascospores 15- to 19 celled, tips slightly inflated L. thalassiae 1 Ascospores 28- to 52-celled, tips provided with a globose appendage..l. inflata KEY TO GENERA AND SPECIES OF AMEROSPORAE 1 Ascospores with several rigid, awl-shaped appendages arising from several positions along the spore wall Amylocarpus encephaloides 1 Ascospores not provided with appendages (1) Ascospores many times longer than broad, fusiform or cylindrical, straight or curved (see also Scolecosporae Halonectria milfordensis 14... 2 (1) Ascospores more or less ellipsoidal, not many times longer than broad Haloguign
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