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Octopodotus stupendus gen. & sp. nov. and Phyllachora paludicola sp. nov., two marine fungi from Spartina alterniflora

     Institute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, North Carolina, USA 28557

	ABSTRACT

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The coelomycete Octopodotus stupendus and the ascomycete Phyllachora paludicola are described as obligate marine fungi from the decomposing salt-marsh plant, Spartina alterniflora. Both species fruit only on the leaf blades, not on the leaf sheaths. Whereas O. stupendus is known so far only from North Carolina, P. paludicola has been collected from Florida to Delaware. The total number of marine fungi reported from Spartina spp. is 41.

Key words: ascomycetes, coelomycetes, salt marsh, systematics

	INTRODUCTION

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The smooth cord-grass Spartina alterniflora Loisel. is the dominant species in salt marshes along the Atlantic coast of North America. Ellis and Everhart (1885) described the first marine fungi from this plant, i.e., Lulworthia medusa (Ellis et Everh.) Cribb et J.W. Cribb (as Ophiobolus medusa) and Phaeosphaeria spartinae (Ellis et Everh.) Shoemaker et C. E. Babc. (as Leptosphaeria spartinae). A recent compilation lists 39 marine ascomycetes and mitosporic fungi occurring on Spartina spp. (Kohlmeyer and Volkmann-Kohlmeyer 2002). Results from our earlier pilot studies and present investigations indicate that S. alterniflora still hosts a large number of undescribed fungal decomposers, but probably not as many as found on Juncus roemerianus Scheele, a close associate of Spartina. Over 100 fungal species have been recorded so far on J. roemerianus (Kohlmeyer and Volkmann-Kohlmeyer 2001). Two new species from S. alterniflora are described.

	MATERIALS AND METHODS

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Decaying leaves from the lower half of standing culms of Spartina alterniflora were cut off and examined under a dissecting microscope for the presence of fungal stromata or single fruiting bodies. Small pieces of the leaf containing single stromata or pycnidia were sectioned at 4 to 16 µm with a cryostat microtome (Minotome of the International Equipment Company). Photos were taken in Nomarski interference contrast or brightfield on a Zeiss photomicroscope. Permanent microscope slides were prepared with the double-coverglass method (Volkmann-Kohlmeyer and Kohlmeyer 1996). Dried material and slides are maintained in the herbarium of the Institute of Marine Sciences (IMS).

	TAXONOMY

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Octopodotus Kohlm. et Volkm.-Kohlm., gen. nov.

Conidiomata pycnidialia, subglobosa, partim immersa, papillata, ostiolata, coriacea, brunnea. Peridium tenue, cellulis texturam angularem formans. Conidiophora ad cellulas conidiogenas reducta. Cellulae macroconidiogenae discretae, multangulares, e cellulis interioribus parietis oriundae. Macroconidia unicellularia, ellipsoidea, brunnea, pachydermatica, verruculosa, tunica gelatinosa cum appendicibus tentaculiformibus tecta. Cellulae microconidiogenae polygonales, ad tectum conidiomatis prope ostiolum restrictae. Microconidia unicellularia, hyalina, guttas olei continentia.

Conidiomata pycnidial, subglobose, partly immersed, papillate, ostiolate, coriaceous, brown. Peridium thin, composed of cells forming a textura angularis. Conidiophores reduced to conidiogenous cells. Macroconidiogenous cells discrete, polygonal, originating on the inner cells of the peridium. Macroconidia one-celled, ellipsoidal, brown, thick-walled, verruculose, surrounded by a gelatinous sheath with tentaculiform appendages. Microconidiogenous cells polygonal, arising from the inner cells of the peridium at the base of the ostiolar canal. Microconidia one-celled, hyaline, containing an oil globule.

Type species. Octopodotus stupendus Kohlm. et Volkm. Kohlm.

Etymology. From octopus and the Greek suffix–otus, indicating resemblance, because of the tentaculiform conidial appendages.

Octopodotus stupendus Kohlm. et Volkm.-Kohlm., sp. nov. Figs. 1–10

View larger version (133K): [in this window] [in a new window]    FIGS. 1, 2. Octopodotus stupendus, longitudinal sections through pycnidia. 1. 14 µm section, showing macroconidiogenous cells at the bottom, origin of microconidia at the base of the ostiolar canal. 2. 6 µm section, showing structure of peridium. From Herb. J.K. 5711. Scale bars: 25 µm. Both figures in Nomarski interference contrast

Substratum. Folia mortua Spartinae alterniflorae.

Distribution. Littus Oceani Atlantici, America Septentrionalis (USA: North Carolina).

HOLOTYPUS. UNITED STATES. NORTH CAROLINA: Carteret County, Broad Creek, 34° 43' N, 76° 55' 07'' W, in S. alterniflora, 26 Mar 2001, J. Kohlmeyer & B. Volkmann-Kohlmeyer, J.K. 5711 (IMS); ISOTYPUS J.K. 5711 (NY).

Etymology. From the Latin, meaning astonishing or wonderful, in reference to the ornate conidia.

Conidiomata 115–225 µm high, 125–275 µm diam, pycnidial, subglobose, unilocular, partly embedded in the mesophyll between vascular bundles, partly free between the ridges of the adaxial surface of the leaf, papillate, ostiolate, coriaceous, light brown, single or lined up in small groups (Figs. 1, 2). Papilla 35–50 µm high, 35–55 µm diam, dark brown, piercing the abaxial surface of the leaf. Peridium 6–12 µm thick, composed of 2 to 5 layers of polygonal, flattened cells, forming a textura angularis in longitudinal section (Figs. 2, 4). Conidiophores reduced to conidiogenous cells. Macroconidiogenous cells 3.5–7 µm high, 5–8.5 µm diam, discrete, conoidal or irregularly polygonal, hyaline, originating on the inner cells of the peridium, all around the locule (Figs. 1, 2, 4, 5). Macroconidia 16.5–22.5 x 11–13.5 µm ( = 18.8 x 11.9 µm; n = 38), one-celled, ellipsoidal, dark brown, thick-walled, verruculose (Fig. 10), surrounded by a gelatinous sheath with tentaculiform appendages (Figs. 3, 6, 7, 9); the sheath extended at base and apex, basally rounded and apically flattened, drawn out at the apex into 5 to 9 terete ‘tentacles’, 18–50 µm long, 2–3.5 µm diam (Figs. 6, 7, 9); the ‘tentacles' attached to the conidial wall by an inconspicuous thin core (Fig. 7); conidia germinating from one or both ends. Microconidiogenous cells 2.5–3.5 µm high, 3.5–5.5 µm diam, irregularly polygonal, hyaline, arising from the inner cells of the peridium at the base of the ostiolar canal (Fig. 1). Microconidia 3.5–5.5 x 3–4 µm, one celled, subglobose to ellipsoidal, hyaline, each containing a large oil globule (Fig. 8).

View larger version (140K): [in this window] [in a new window]    FIGS. 3–10. Octopodotus stupendus. 3. Mature (dark) and immature (light) conidia, showing presence of appendages already in early stages. 4. Section (6 µm) through peridium with two macroconidiogenous cells giving rise to conidial initials. 5. Section (14 µm) through peridium, showing early stage of conidial development; the young hyaline conidial cell is surrounded by the gelatinous sheath, bearing apical appendages. 6. Mature conidia. 7. Immature and mature conidium; the latter shows the thin connection of appendages with the brown conidial cell. 8. Microconidia. 9. Mature conidium. 10. Conidia, showing verruculose surface. Figs. 3, 6, 7, 10 from Herb. J.K. 3817, the others from Herb. J.K. 5711. Scale bars: 3 = 25 µm; 4–9 = 20 µm; 10 = 10 µm. All figures in Nomarski interference contrast

Distribution. Atlantic Coast (USA: North Carolina).

Additional specimens examined. UNITED STATES. NORTH CAROLINA: Carteret County, Broad Creek, in dead leaves on standing culms of S. alterniflora, 3 Nov 1976, J. Kohlmeyer, J.K. 3817, (IMS); 26 Mar 2001, J. Kohlmeyer & B. Volkmann-Kohlmeyer, J.K. 5691, 5692 (IMS).

Perusal of Nag Raj's (1993) monograph of coelomycetes with appendage-bearing conidia did not yield any taxon resembling Octopodotus stupendus. In addition to the unusual macroconidia, this species produces also microconidia that originate at the base of the ostiolar canal (Fig. 1). Such microconidia occur in 15 genera included in Nag Raj (1993). Their function in O. stupendus is unknown.

Pycnidia of O. stupendus are mostly found in the lower, regularly submersed leaves of S. alterniflora; therefore, the species is classified as an obligate marine fungus. Our pilot studies, making monthly collections at the type location, indicate that the species fruits throughout the year.

Phyllachora paludicola Kohlm. et Volkm.-Kohlm., sp. nov. Figs. 11–20

View larger version (164K): [in this window] [in a new window]    FIGS. 11–14. Phyllachora paludicola. 11, 12. Longitudinal sections (16 µm) through ascomata, in Fig. 12 parasitized by Septoriella sp. 13. Tangential section (6 µm) through stroma, showing immersed ascomata arranged in rows. 14. Ascus and paraphyses. From Herb. J. K. 5692. Scale bars: 11–13 = 50 µm; 14 = 20 µm. All figures in Nomarski interference contrast

Substratum. Folia mortua Spartinae alterniflorae.

Distribution. Littus Oceani Atlantici, America Septentrionalis (USA: Florida, Georgia, North Carolina, Maryland, Delaware).

HOLOTYPUS. UNITED STATES. NORTH CAROLINA: Carteret County, Broad Creek, in S. alterniflora, 26 Mar 2001, J. Kohlmeyer & B. Volkmann-Kohlmeyer, J.K. 5692 (IMS); ISOTYPUS J.K. 5692 (NY).

Etymology. From the Latin paludicola, a dweller in marshes.

Stromata linear, 1.3–3 cm long, about 0.5 cm wide, 350–700 µm high, immersed, forming a pseudoparenchyma of textura angularis to epidermoidea (Figs. 16, 20), black on the outside, light brown on the inside (Fig. 20), containing crystals (Fig. 17) and copious amounts of small lipid droplets, enclosing 5–20 ascomata (Fig. 13) and cells of the host, raising the surface of the leaf. Ascomata 260–355 µm high, 170–310 µm wide, ampulliform to subglobose, ostiolate (Figs. 11, 12), coriaceous, light brown to orange colored, mostly arranged in two to four parallel rows (Fig. 13). Neck absent, ostiolar canal densely periphysate. Peridium dark brown, 13–20 µm thick at the sides and composed of compressed cells, 30–40 µm thick at the base and composed of more or less rounded cells, forming a textura angularis in longitudinal section, merging on the outside with the stromatic tissue (Figs. 16, 17). Hamathecium consisting of apically free, septate paraphyses, 3–4 µm thick at the base, tapering to 1.5–2 µm at the tip, between and above the asci (Figs. 11, 14). Asci 125–140 x 15–21 µm, 8-spored, cylindrical, tip conical, short pedunculate, thick-walled, unitunicate, without apical apparatus, not blueing in IKI, maturing successively at the bottom of the locule (Figs. 14, 18). Ascospores 13.5–18.5 x 9–12 µm ( = 16 x 11.5 µm; n = 42), uniseriate, subglobose to somewhat ellipsoidal, one-celled, hyaline, orange-yellowish in masses, smooth, containing 1 or 2 large oil drops and many small ones, without sheaths or appendages (Figs. 18, 19).

View larger version (174K): [in this window] [in a new window]    FIGS. 15–20. Phyllachora paludicola. 15. Longitudinal section (4 µm) through ostiole with periphyses. 16, 17. Longitudinal sections through base of ascomata (Fig. 16 = 4 µm; Fig. 17 = 8 µm), showing dark peridium merging with stromatic tissue; bases of immature asci at the top, followed by the ascogenous tissue, brown peridium and light crystals at the bottom, visible in Fig. 17. 18. Tip of mature ascus. 19. Ascospore. 20. Longitudinal section (6 µm) through edge of stroma with remains of host tissue on upper side. Figs. 18, 19 from Herb. J.K. 5686, the others from Herb. J. K. 5692. Scale bars: 15, 20 = 25 µm; 16, 17 = 20 µm; 18, 19 = 10 µm. Fig. 16 in brightfield, the others in Nomarski interference contrast

Distribution. Atlantic Coast (U.S.A.: Florida, Georgia, North Carolina, Maryland, Delaware).

Additional specimens examined. UNITED STATES. NORTH CAROLINA: Carteret County, Broad Creek, in dead leaves of standing culms of S. alterniflora, 1 Aug 1977, J. Kohlmeyer, J. K. 5712; 3 Apr 1978, J. Kohlmeyer, J. K. 3903; 6 May 2001, J. Kohlmeyer & B. Volkmann-Kohlmeyer, J. K. 5699; 27 July 2001, J. Kohlmeyer & B. Volkmann-Kohlmeyer, J. K. 5706. GEORGIA: Sapelo Island, Southend Creek, same substrate, 1 Mar 2001, S. Y. Newell, J. K. 5686 (all previous collections IMS). The following specimens on S. alterniflora from BPI (filed under Phyllachora spartinae Orton): DELAWARE: Smyrna, 24 Aug 1946, H. L. Dozier, 639692; Misspillion Marshes near Milford, 2 Oct 1946, H. L. Dozier, 639693. MARYLAND: Anne Arundel County, Herold Harbor, 11 Oct 1931, J. A. Stevenson, 639691; 13 Oct 1935, J. A. Stevenson, 639691. GEORGIA: Savannah, 20 Jan 1921, S. B. Dayton, 639694.

Phyllachora paludicola was described before by Orton (1944) as P. spartinae Orton, however, according to article 36 of the International Code of Botanical Nomenclature, this name is invalid because it was published without a Latin diagnosis. Moreover, Orton's description is brief and not accompanied by any illustration. It therefore appeared necessary to redescribe the species in detail. It is well placed in the genus, as circumscribed by von Arx and Müller (1954). The description and illustration of the type species of Phyllachora, P. graminis (Pers. : Fr.) Nitschke in von Arx and Müller (1954, Fig. 64) and the illustration in Hanlin (1990, p. 43) agree in most features with the new species from Spartina. In P. graminis ascomata develop between epidermal and subepidermal black clypei, whereas the host mesophyll around ascomata contains a pseudostroma of mainly sinuous, vertical hyphae or irregular masses of small cells; the ascospores are distinctly ellipsoidal (von Arx and Müller 1954). In contrast, ascomata of P. paludicola are always enclosed in distinct stromata, and the ascospores are subglobose to somewhat ellipsoidal. Winka and Eriksson (2000) list P. graminis in the Phyllachorales, Phyllachoraceae.

Mature ascomata of P. paludicola have been collected between January and March in Georgia, between March and August in North Carolina, but four collections from Maryland and Delaware (BPI) made in August and October were still immature. Orton (1944) notes the occurrence of P. paludicola (sub P. spartinae) in Florida, but did not cite any particular collection. It can be assumed that the species will fruit in Florida in early winter. The characteristic ellipsoidal stromata, visible on both sides of the leaf blade, can be seen long before asci develop. An interesting observation was the parasitic growth of a Septoriella sp. inside of ascomata of P. paludicola (Fig. 12).

	ACKNOWLEDGMENTS

 
We are grateful to Stephen Y. Newell for supplying material of Phyllachora paludicola from Georgia and to Amy Y. Rossman for loans from BPI. We also appreciate helpful comments by an anonymous reviewer. We wish to thank Teri Lynn Herbert for assistance during pilot studies on fungi from marsh plants in North Carolina. Laura White and Howard Barnes assisted with the preparation of the manuscript.

	FOOTNOTES

 
¹ Corresponding author, bjkohlm{at}email.unc.edu

Accepted for publication June 8, 2002.

	LITERATURE CITED

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS TAXONOMY LITERATURE CITED

 
Arx JA von, Müller E., 1954 Die Gattungen der amerosporen Pyrenomyceten. Beitr Kryptogamenflora Schweiz 11:1-434

Ellis JB, Everhart B M., 1885 New fungi. J Mycol 1:42-154

Hanlin RT., 1990 Illustrated genera of ascomycetes. St. Paul, Minnesota: APS Press. 263 p

Kohlmeyer J, Volkmann-Kohlmeyer B., 2001 The biodiversity of fungi on Juncus roemerianus. Mycol Res 105:1027-1028

———, ———. 2002 Fungi on Juncus and Spartina: new marine species of Anthostomella, with a list of marine fungi known on Spartina. Mycol Res 106 (In press)

Nag Raj TR., 1993 Coelomycetous anamorphs with appendage-bearing conidia. Waterloo, Canada: Mycologue Publications. 1101 p

Orton CR., 1944 Graminicolous species of Phyllachora in North America. Mycologia 36:18-53

Volkmann-Kohlmeyer B, Kohlmeyer J., 1996 How to prepare truly permanent microscope slides. Mycologist 10:107-108

Winka K, Eriksson OE., 2000 Papulosa amerospora accommodated in a new family (Papulosaceae, Sordariomycetes, Ascomycota) inferred from morphological and molecular data. Mycoscience 41:97-103

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