Taylor, Thomas N.

White, James F., Jr.

English

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BRIEF ARTICLES 6 4 3 Mycologia, 81(4), 1989, pp. 643-646. © 1989, by The New York Botanical Garden, Bronx, NY 10458-5126 A T R I C H O M Y C E T E - L I K E F O S S I L F R O M T H E T R I A S S I C O F A N T A R C T I C A JAMES F. WHITE, JR. Department of Biology, Auburn University at Montgomery, Montgomery, Alabama 36193 AND THOMAS N. TAYLOR Department of Botany and Byrd Polar Research Center, The Ohio State University, Columbus, Ohio 43210 Fungi, particularly the lower fungi, are usually considered to be primit ive organisms, despite the fact that almost nothing is known about their evolutionary histories. This dearth of knowledge may be rectified, in part, by acquiring informa-tion on the diversity of fungi in the fossil record. This task has proven to be a slow process; how-ever, data on fossil fungi are slowly accummu-lating (e.g., Kidston and Lang, 1921; Davis and Leisman, 1962; Dilcher, 1965; Stubblefield and Taylor, 1983; Whi te and Taylor, 1988; Osborn et al, 1989). Although a nucleus of information on fossil fungi is available, evolutionary biolo-gists rarely incorporate such data into meaning-ful evolutionary scenarios. As our knowledge of fossil fungi increases, studies which rely on fossil data, like that by Pirozynski (1976) where evo-lutionary schemes are proposed to explain pat-terns of geographic distribution and host ranges of various fungal groups, may represent a valu-able contribution to development of an under-standing of the history of fungi. However, at the present t ime some groups of fungi are completely unknown in the fossil record. Among these un-known groups are fungi placed in the class Trichomycetes of the Zygomycotina. In a recent study of silicified peat deposits col-lected f rom the Fremouw formation of the Bea-con Supergroup in Antarctica, specimens which resemble extant members of the Trichomycetes were found. This formation is considered to con-tain fossils of Early-Middle Triassic age (White and Taylor, 1989). Light microscope slides were prepared f rom cellulose acetate peels of rock sur-faces which had been etched with hydrofluoric acid (Smoot et al., 1985). Slides and peels are deposited in The Ohio State Paleobotanical Col-lection under acquisi t ion numbers 18 ,054-18,058. Individual thalli are cylindrical and measure 9-12 x 50-55 Aim (FIGS. 1-6). At one end of each thallus is an isodiametric cell, measuring 8-13 fjLm diam (FIGS. 3, 4). This cell, which morpho-logically resembles a holdfast, attaches the thal-lus to a substrate (FIG. 4). The opposite end of each thallus is somewhat truncate, with a cen-trally located diffuse septal plug (FIG. 5) and a frill of wall material on the periphery of the tip (FIG. 6). Near the tips of several thalli are spher-ical to ellipsoidal spores, each averaging 9-10 x 12-14 jam (FIG. 6). Thalli are completely en-closed by, and attach to, the inner surface of a poorly preserved irregularly-shaped structure (FIG. 2), which we interpret as the remains of an arthropod cuticle. Trichomycetes are predominantly endosym-biotic associates of arthropods. They often in-habit the hindgut region of organisms in several different orders, e.g., Coleoptera, Diplopoda, Diptera, Ephemeroptera, and Plecoptera. These fungi have branched or unbranched thalli that attach to the cuticles of their hosts by cellular or acellular holdfasts. Four orders of Trichomyce-tes are currently recognized: Harpellales, Asella-riales, Eccrinales, and Amoebidiales. Species of Eccrinales, commonly referred to as eccrinids, are often found associated with ter-restrial arthropods, such as millipedes (Diplo-poda) and some beetles (Coleoptera). These hosts are detritivores and are often found in environ-ments with abundant organic debris. The typical eccrinid possesses a coenocytic thallus with septa 6 4 4 MYCOLOGIA B R I E F ARTICLES 6 4 5 delimiting one or more sporangia in a series, each containing a single sporangiospore. Sporangio-spores may be released into the alimentary tract of the ar thropod by lysis of the sporangial wall and expelled into the environment where they may be ingested by other arthropods. A feature that eccrinids share with other Trichomycetes and a few other fungal groups is the possession of large septal plugs. The fossil fungus bears several points of sim-ilarity with extant eccrinids. These include the possession of holdfasts (FIGS. 3,4), aseptate thalli (FIG. 1), spores (FIG. 6), and septal plugs (FIG. 5), all of which are comparable both in size and shape to species of the eccrinid genus Entero-bryus Leidy (Lichtwardt, 1986). In addition, some thalli of the fossil bear a frill of wall remnants (FIG. 5) which may represent the remains of the lysed sporangial walls. In a previous paper clus-ters of cylindrical structures (FIG. 7) resembling eccrinid thalli without holdfasts and sporangia were observed and described from silicifications of the same age and collection locality (White and Taylor, 1988). These structures were inter-preted as arthroconidia, but they may also rep-resent disarticulated thalli or large secondary sporangiospores which are commonly produced by eccrinids (Lichtwardt, 1986). Morphologically, this fossil appears to corre-spond closely to the Eccrinales; however, the di-agnostic feature of the arthropod is lacking. A well-preserved ar thropod body or cuticle would give further evidence for Trichomycete affinities of this fossil. However, host cuticles and body parts were not encountered in the silicifications bearing these fungi. Nevertheless, it is evident that ar thropods or other small detritivores were abundant in the peat due to numerous fecal de-posits present in the fossil matrix. The structure in which thalli are borne (FIG. 2) could be the remains of a cuticle of an arthropod hindgut. The fungus may have somehow facilitated preser-vation of the cuticle in areas colonized by thalli while uncolonized areas were not preserved or disarticulated during the fossilization process. The presence of Trichomycetes in possible ar-thropod remains of Triassic age suggests that the symbiotic relationship between both groups is ancient and may explain the geographically widespread nature of the association between those organisms (Lichtwardt, 1986). Several of the insect hosts of Trichomycetes have been doc-umented to occur in earlier Paleozoic sediments (Minkoff, 1983). It is probable that the present symbiotic relationship between arthropods and Trichomycetes is the result of several hundred million years of coevolution between the groups. However, whether the symbiotic relationship be-tween arthropods or their ancestors and Tricho-mycetes or their ancestors was initially com-mensalistic, or alternately was pathogenic, is unknown. It is possible that studies of sediments where arthropods are better preserved may pro-vide an answer to this question. ACKNOWLEDGMENTS The authors are grateful to Dr. Robert Lichtwardt for his advice concerning this fossil. This research was supported by National Science Foundation grant BSR-8516323. Key Words: Eccrinales, fossil fungus, Triassic, tricho-mycete. LITERATURE CITED Davis, B., and G. A. Leisman. 1962. Further obser-vations on Sporocarpon and allied genera. Bull. TorreyBot. Club 89: 97-109. Dilcher, D. L. 1965. Epiphyllous fungi from Eocene deposits in western Tennessee, U.S.A. Palaeon-togr. B116: 1-54. Kidston, R., and W. H. Lang. 1921. On old red sand-stone plants showing structure, from the Rhynie Chert Bed, Aberdeenshire. Trans. Roy. Soc. Edinb. 52: 855-902. Lichtwardt, R. W. 1986. The Trichomycetes: fungal associates of arthropods. Springer-Verlag, New York. Minkoff, E. C. 1983. Evolutionary biology. Addison-Wesley Publ. Co., Inc., Reading, Massachusetts. Osborn, J. M., T. N. Taylor, and J. F. White, Jr. 1989. A clamp-bearing fungus from the Triassic of Ant-arctica. Mycologia. (In press) FIGS. 1-7. Fossil trichomycete. 1. Palisade of thalli on inner surface of possible arthropod cuticle remains. C.B. 10,145D(bot-3), x300. 2. Elongate extension of possible cuticle remains (above) and thalli (below). C.B. 10,145D(bot-3), x200. 3, 4. Thalli with holdfasts (arrows). C.B. 10,145D(bot-3), x700. 5. Aseptate thalli with truncate tips and septal plugs (arrows). C.B. 10,145D(bot-3), xl300. 6. Several thalli showing sporangial wall remains (arrow) at the tip and an adjacent ellipsoidal sporangiospore (arrowhead). C.B. 10,145D(bot-14), x700. 7. Cluster of secondary sporangiospores or disarticulated thalli. C.B. 562B(bot-2), x224. 6 4 6 MYCOLOGIA Pirozynski, K. A. 1976. Fossil fungi. Annu. Rev. Phy-topath. 14: 237-246. Smoot, E. L., T. N. Taylor, and T. Delevoryas. 1985. Structurally preserved fossil plants from Antarc-tica. I. Antarcticycas, gen. nov., a Triassic cycad stem from the Beardmore Glacier Area. Amer. J. Bot. 72: 1410-1423. Stubblefield, S. P., and T. N. Taylor. 1983. Studies of Paleozoic fungi. I. The structure and organi-zation of Traquairia (Ascomycota). Amer. J. Bot. 70: 387-399. White, J. F., Jr., and T. N. Taylor. 1988. A Triassic fungus from Antarctica with possible ascomyce-tous affinities. Amer. J. Bot. 75: 1495-1500. , and . 1989. Triassic fungi with sug-gested affinities to the Endogonales (Zygomyco-tina). Rev. Paleobot. Palynol. (In press) Mycologia, 81(4), 1989, pp. 646-650. © 1989, by The New York Botanical Garden, Bronx, NY 10458-5126 T O X I C I T Y A N D I N T E R A C T I O N S O F S O M E FUSARIUM GRAMINEARUM M E T A B O L I T E S T O C A T E R P I L L A R S PATRICK F. DOWD Northern Regional Research Center, USDA-ARS, Peoria, Illinois 61604 J. DAVID MILLER,1 AND R. GREENHALGH Plant Research Centre, Agriculture Canada, Ottawa, Ontario K1A 0C6, Canada Fusarium graminearum Schwabe is a patho-gen of wheat, corn and other cereals in north temperate climates. Its presence causes a reduc-tion in quality of grains, primarily because this fungus produces mycotoxins such as the trich-othecene deoxynivalenol (DON) and analogs, and zearalenone (ZEA), an estrogenic compound (Marasas et al, 1984). These metabolites can af-fect both the growth and reproduction of live-stock, especially swine, when fed contaminated grain (Trenholm et al, 1984). Toxic secondary metabolites of fungi are thought to be produced as a means of conserving food resources (interference competition) and/or avoiding predation (Janzen, 1977; Wicklow, 1984). Approximately 40 secondary metabolites of F. graminearum have been described for which no obvious ecological role has been determined (Greenhalgh et al, 1984, 1986). Concentrations of individual metabolites in naturally occurring moldy grain are normally at trace levels. As in-dividual toxic contaminants, their toxicity should be quite low, but additive or synergistic effects of fungal metabolites may be involved in toxicity of contaminated feedstuffs (Foster et al, 1986). 1 Corresponding author. Insects are also affected by fungal secondary me-tabolites (Wright et al, 1982), and may be se-lectively affected by compounds that are of rel-atively low toxicity to mammals (Wicklow et al, 1988). Some relatively non-toxic fungal second-ary metabolites affect insects by synergistic tox-icity of co-occurring toxins (Dowd, 1989). This report concerns evaluation of some F. graminearum metabolites for their toxicity to fall armyworm [Spodoptera frugiperda (J. E. Smith)] and the corn earworm [Heliothis zea (Boddie)]. Both relative toxicity and toxicity of selected combinations were determined. The metabolites DON, sambucinol (SAM), dihydroxycalonectrin (DHCAL), culmorin (CUL) and 8-hydroxycalonectrin (HCAL) (FIG. 1) were isolated and characterized according to pub-lished procedures (Greenhalgh et al, 1984, 1986).Dihydrodeoxynivalenol (DHD) was pre-pared by the hydrogenation of DON using a pal-ladium/charcoal catalyst. All of these com-pounds, except DHD, have been found in F. graminearum-infected maize ears (Miller et al, 1983; Miller, unpubl.). The metabolites were incorporated into pinto bean-based diets used to rear caterpillars (Dowd, 1987) by blending appropriate concentrations dissolved in acetone or water (125 /xl) with un-

A Trichomycete-like Fossil from the Triassic of Antarctica

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A Trichomycete-like Fossil from the Triassic of Antarctica

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