CASTANEA
The Journal of the Southern Appalachian Botanical Society
VOLUME 68, : JUNE 2003 (published July
8, 2003)
Tree canopy myxomycetes and new records from ground sites
in the Great Smoky Mountains National Park
by Snell, Kenneth L, Keller, Harold W, Eliasson, Uno H
ABSTRACT
Thirty-five tree species, represented by 240 individuals, were climbed during two three-week periods in June, July, and August of calendar years 2000 and 2001 in the Great Smoky Mountains National Park. The double rope climbing technique was used because the climbers could advance to higher levels in the tree canopy. Maximum-sized mature trees in old growth park areas were sampled up to 40 m. Bark samples were cultured in moist chamber cultures. Ninety-five myxomycete species were obtained from the tree canopy mostly from the following tree species: Fraxinus americana (white ash), Quercus alba (white oak), Liriodendron tulipifera (yellow poplar), Acer rubrum (red maple), and Pinus strobus (white pine). We report here 52 new records from the tree canopy, 7 from ground sites, bringing to 212 the number of myxomycete species known from the Park. Comatricha penicillata is recorded for the first time outside of the type locality in Japan. This is the first upper tree canopy list of myxomycete species from the Park. The Myxomycetes represent the only group of cryptogams with species only known from the tree canopy.
INTRODUCTION
The Great Smoky Mountains National Park (GSMNP) comprises more than 210,566 ha and is a refuge for one of the richest and most diverse biota in the temperate regions of the world. It has the largest remaining tracts of old growth forest in the eastern United States, estimated at 40,000 ha, which has resulted in its designation as a National Park, June 15, 1934, an International Biosphere Reserve, October 26, 1976, and a World Heritage Site, December 6, 1983. The park forms the boundary between eastern Tennessee and western North Carolina.
A new research initiative, the all Taxa Biodiversity Inventory (ATBI), under the rubric of a non-profit organization Discover Life in America (web site at www.dlia.org) represents a research effort to inventory all life forms in the park. The initial sampling plan developed by the ATBI established 20 one-hectare study plots located in major habitats throughout the park. Site selection was based on major forest/vegetation types, elevation, and relative accessibility. No previous study had collected myxomycetes from the tree canopy. The high canopy of the old growth forest allowed collection from many heights, occasionally over 40 m. The GSMNP is home to five forest types; spruce-fir, northern hardwood, cove hardwood, hemlock, and pine-oak forests (Whittaker 1956).
Hagelstein (1940) published an abbreviated list of Myxomycetes collected during the 1939 Mycological Society of America foray. A complete list of 64 species was published by Linder (1941). Weiden (1951) added 21 species to the park records. A preliminary list of 30 new myxomycete records for the park was published in Inoculum by Counts et al. (2000). These myxomycetes were gathered in two separate forays from June 19 to July 6 and July 31 to August 17, 2000, mostly from the tree canopy. Recently Stephenson et al. (2001) added 75 new myxomycete records, but 15 of these species were duplicates published earlier by Counts et al. (2000).
Study area
The GSMNP was selected for this study because of its favorable climatic conditions, variety of habitats, and high plant and fungal diversity. Moderate temperatures, ranging from 4[degrees] to 23[degrees]C at lower elevations, and an average yearly rainfall ranging from 140 to 216 cm (Shanks 1954) make the park an excellent environment for myxomycetes.
METHODS
Field Methods
Individual trees were selected from geographically different areas of the park, but due to access and climbing restraints, random selection was not practical. Acceptable trees exceeded 21 meters in height and allowed sampling from the ground continuously to near the top. Tree selection was often limited by climbing hazards such as poison ivy [Toxicodendron radicans (L.) Kuntze], dead branches, or overall limb structure.
Canopy bark samples were collected using the double-rope climbing technique. In this technique, a thin plastic slick-line tied to a weighted throw bag was thrown or shot, using a large slingshot, over the highest possible substantial branch. Once the bag and line were lowered to the ground, a climbing rope was tied to the slick-line, which was used to pull it over the branch or tree crotch. One end of the climbing rope was tied to the climbing saddle, as well as the end of a short length of rope called the split tail. The other end of the split tail was tied into a friction knot around the standing end of the climbing rope. When the climber pulled down on the standing end, he/she was pulled upward as the rope slid around the branch. The friction knot was advanced with each pull, holding the climber's position and leaving both hands free to sample from the bark. The double-rope technique also allows the climber to advance the rope to higher branches, often reaching to near the top of the tree (Jepson 2000).
Samples were taken at roughly three-meter increments as the climber advanced upward. Bark was scraped or pried from the trunk using a large knife, taking care not to damage the underlying living tissues of the tree. Efforts were made to sample from all sides of the trunk. All samples were collected from living parts of the tree and placed in paper bags (approximately 1000 cm^sup 3^), on which height and tree number were recorded. Trunk diameters at breast height (DBH = 1.5 m) were measured for each tree, and voucher specimens of leaves were gathered for their positive identification. Each climber used an elevation line marked off in 0.3 m increments to determine tree height measurements. Trees were tagged with numbers, and Global Positioning System (GPS) readings were taken for each climbing site location. In addition, a site description including most recent rain and current weather conditions was recorded.
Tree canopy is defined as a vertical transect beginning at 3 m and extending into the crown or tops of living trees. Canopy structure is the organization in space and time of the above ground components of the vegetation (Parker 1995). This more general definition includes bark surfaces of living trees below the first branches in the crown of individual trees. Trees were selected in part because of their size in total height, usually those with a minimal height of 30 m. Trees with large-diameter bases with buttress roots and epiphytes such as mosses and liver-worts support myxomycete plasmodia and fruiting bodies which are more typical ground species, for example, Lycogala flavofuscum (Ehrenb.) Rost. (Keller and Braun 1999). This assemblage of myxomycete ground species at the base of trees occurs below 2 m (Keller, pers. obs.).
Laboratory Methods
Myxomycetes were cultured from tree bark using the moist chamber technique described by Keller and Braun (1999). Moist chambers consisted of large sterile Petri plates (150 X 25 mm) fitted with a sheet of P8-creped filter paper that covered the dish bottom. Bark was placed face up on the paper in a single layer. Sterile distilled water adjusted to pH 7 with KOH was poured into the plate around the bark, and the lid was replaced to maintain a closed moist chamber. After 24 hours any unabsorbed water was decanted, and the pH of each culture was measured using an Orion model 610 flat probe pH meter. Plates were kept moist, without standing water, at room temperature (22-25[degrees]]C) in indirect natural light. Cursory scanning of fresh cultures was conducted for each plate to check for existing myxomycete fruiting bodies. Each plate was examined every 7-10 days, starting 24 to 48 hours after wetting. Moist chamber cultures were kept wet and observed for four weeks.
Collection and Identification Methods
In the annotated list of species, Myxomycetes are arranged alphabetically by orders, then by genus and species, as recognized by Martin et al. (1983). Collection numbers primarily from the tree canopy are reported by Kenneth L. Snell as KLS followed by the tree number. Specimens collected by Harold W. Keller are indicated as HWK and by Uno H. Eliasson as UHE. Moist chamber cultures are represented by MC. The range of heights at which a species was found is given in meters. Tree species abbreviations are represented by F = Fraxinus americana L. (white ash), Q = Qaercas alba L. (white oak), L = Liriodendron tulipifera L. (yellow poplar), A =Acer rubrum L. (red maple), P = Pinus strobus L. (white pine). Mean pH values for the five tree species are F = 6.9; Q = 6.7; L = 5.2; A - 4.8 and P = 3.9. The number of specimens of each myxomycete species collectively found on each tree species follows in (parentheses). The counties in Tennessee are Blount, Cocke, and Sevier; and in North Carolina Haywood and Swain. all of the tree canopy collections were entered into the Discover Life in America GSMNPATBI database that has latitude and longitude (GPS) readings, place locations, county, elevation, collection date, and collector. To conserve space only one representative specimen is cited for each tree species. An asterisk (*) indicates a species previously not published from the park. A plus (+) indicates new records published by Counts et al. (2000). These myxomycete specimens will be deposited in the herbaria of the GSMNP and the National Fungus Collections (BPI) in the United States. Collections gathered by UHE are deposited in GB in Goteborg, Sweden. Author abbreviations for species follow Brummitt and Powell (1992). Additional comments are made for noteworthy collections. ANNOTATED LIST OF SPECIES
*Pocheina rosea (Cienk.) Loeblich & Tappan is a member of the Class Acrasea (acrasid cellular slime molds). This collection is a new record for the park, MC, 3 m, L(1), Sevier, Ramsay Cascades Trail, HWK4664-301. Olive (1975) reported that P. rosea is common in moist chambers on bark from larch, pine, wild cherry, oak, and maple. Keller and Braun (1999) reported this taxon in moist chambers on bark from red oak, gingko, and grapevine in moist chambers. This GSMNP collection is the first report of this species from Liriodendron tulipifera.
ECHINOSTELIALES
Clastoderma debaryanum A. Blytt, MC, 3-24 m, P(10), L(9), A(4), Q(2), Blount, John Cooper Trail, KLS634-334:. This species frequency of occurrence was higher at acid pH levels and absent on F at pH near 7.0.
*Clastoderma microcarpum (Meyl.) Kowalski, MC, 3-9 m, F(2), Blount, Rabbit Creek Trail, KLS1281-247.
Clastoderma pachypus Nann.-Bremek., MC, 6-27 m, A(3), L(2), Cocke, Albright Grove Loop, KLS813-227.
Echinostelium arboreum H.W. Keller & T.E. Brooks, MC, 13 m, Blount, on bark of living Ulmus rubra Muhlenb., horse trail behind Cades Cove picnic area, KLS22-153. This rare species is known from the type locality at Kabah, Yucatan in Mexico, and also from New Mexico and Kentucky (Keller and Brooks 1976, Whitney 1980); Stephenson et al. (2001) reported it for the GSMNP on Acer rubrum at the Elkmont Campground. This appears to be the fifth collection in published records. Numerous golden sporangia with persistent peridia still intact formed on the bark surface and on mosses. Slide preparations show a persistent peridium, stout dichotomously branched capillitial threads arising from the columella apex, a conspicuous columella, and a wide peridial collar at the sporangial base.
+Echinostelium coelocephalum T.E. Brooks & H.W. Keller, MC, 3-27 m, A(5), Q(4), L(1), Sevier, Porter Creek Trail, KLS1348-240. This rare species was reported previously from Arizona, Arkansas, California, Michigan, and Ohio in the United States (Keller and Braun 1999). To our knowledge, this tiny myxomycete is known only from moist chamber cultures of living tree and vine bark such as elms, grapevines, maples, oaks, red bud (Cercis canadensis L.), red cedar, and yellow poplar. It is probably more common than reported, but is overlooked because of its small size.
+Echinostelium colliculosum K.D.Whitney & H.W. Keller, MC, 18 m, L(I), Cocke, Cosby Nature Trail, KLS936-314. This rare species is only known from Arizona, California, and Nevada in the United States (Whitney 1980). Liriodendron tulipifera is a new substratum for this species.
*Echinostelium elachiston Alexop., MC, 23 m, F(I), Haywood, Manway Trail, HWK4665-303. This is a rare species only known from Kansas and Ohio in the United States. It occurs on bark of Taxodium distichum (L.) Rich., Vitis sp., Salix nigra Marshall, Platanus occidentalis L., Juniperus virginiana L. (Keller and Braun 1999), and a new substratum, Fraxinus americana.
*Echinostelium fragile Nann.-Bremek., MC,12-21 m, L(4), Sevier, Ramsay Cascades Trail, KLS1022-307. This species is only known from Arizona, Arkansas, California, Michigan, and Ohio (Keller and Braun 1999). It is easily identified by its darkly pigmented, brownish, fusiform to narrowly ellipsoid columella. This tiny species is probably more common than reported but because the lack of a peridium and capillitium results in the release of spores, all that remains is the columella and stalk, which are difficult to see against the background of the substratum.
Echinostelium minutum de Bary, MC, 3-30 m, P(40), L(SO), A(30), Q(23), F(2), Sevier, Ramsay Cascades Trail, KLS1000-307. This was the most common and abundant corticolous myxomycete in the park. Abundance of this species followed a pH gradient from the lowest to highest pH in the canopy of all five tree species. Thousands of sporangia were also collected on a moss covered decaying conifer log on a ground site at night with the use of a flashlight.
LICEALES
+Cribraria aurantiaca Schrad., well decayed wood, Blount, along Cades Cove Loop Road and Hyatt Lane Road, June 23, 2000, UHE5491.
Cribraria confusa Nann.-Bremek. & Y. Yamam., MC, 3-27 m, A(19), P(12), L(6), Blount, Bote MountainTrail, KLS876-210. All of the Cribraria species reported here from the tree canopy are also known from ground sites.
*Cribraria microcarpa (Schrad.) Pers., MC, 3-24 m, A(3), L(3), P(3), Blount, Gum Swamp, KLS1196-204:.
*Cribraria minutissima Schwein., MC, 3-24 m, P(S), L(6), Blount, Gum Swamp, KLS1183204. Species of Cribraria are more frequently associated with conifers and hardwoods with a lower pH. All three species, C. confusa, C. microcarpa, and C. minutissima, follow this trend.
*"Cribraria oregana H.C. Gilbert, well decayed conifer wood, ground site, Blount, Rich Mountain Road, June 24, 2000, UHE5687. Sporangia globose, 0.1-0.2 mm in diameter, on long stalks 0.3-0.5 mm gradually tapering toward the top; cup distinct, reaching to about onehalf of the sporangium, dark brown, somewhat shiny; peridial net wide-meshed, nodes flattened and expanded, irregular, dark; dictydine granules 0.8-2 [mu]m in diameter, most pale with a dark nucleus; spores 7-7.5 [mu]m in diameter, pale orange-brown in mass, yellowish gray by transmitted light. This specimen is very close to specimens identified by Nannenga-Bremekamp as C. montana Nann-Bremek., matching closely the description as well as illustration of the type material (Nannenga-Bremekamp 1973). Color and size of dictydine granules are variable among individual sporangia, and the variation overlaps that of dictydine granule structure in C. oregana and C. vulgaris Schrad. Lado and Pando (1997) treated C. montana and C. oregana as conspecific. Small forms of C. vulgaris approach C. oregana in appearance. If the ranges of variation in dictydine granule structure overlap, the borderline becomes indistinct. This illustrates just one of the taxonomic difficulties in the genus Cribraria.
+Cribraria violacea Rex, MC, 3-27 m, F(26), Q(27), A(9), L(8), Sevier, Porter Creek Trail, KLS1333-240; 18 m, bark of living Aesculus flaua Solander ex Hope (yellow buckeye), Hardwood Nature Trail Chimney Picnic Area, Sevier, August 16, 2000, HWK4646-170. This species was never found on Pinus strobus at the lowest pH but more frequently occurred at higher pH levels. It is one of the most common species found in moist chamber cultures of juniperus virginiana with a pH of 7.0 to 7.5 (unpublished results). This suggests that individual species may differ significantly in pH preference from other species in the same genus.
Dictydiaethalium plumbeum (Schumach.) Rostaf., 7 m, bark of living juniperus virginiana, Blount, Cades Cove Loop Road, August 17, 2000, HWK4647-174.
*Enteridium splendens (Morgan) Macbride var. juranum (Meylan) Harkonen. on well decayed wood, Blount, Cades Cove, June 22, 2000, UHE5581.
Licea biforis Morgan, MC, 3-24 m, F(10), Q(4), A(1), P(2), Haywood, Manway Trail, KLS1116303. It is one of the most common species on living Malus sp. (apple) trees with large trunks and fissured bark. Older tree bark often peels off in thin layers, and on the underside this species will form hundreds of sporangia. It also is frequently found on Juniperus virginiana trees, suggesting that it prefers a higher pH.
Licea castanea G. Lister, MC, 6-15 m, Q(2), F(1), Haywood, Manway Trail, KLS1228-3Q2.
Licea denudescens H.W. Keller & T.E. Brooks, MC, bark of Juniperus virginiana (1), 7 m, Blount, Cades Cove Loop Road, HWK4663-174.
+Licea inconspicua T.E. Brooks & H.W. Keller, MC, 18.3 m, Blount, on bark of living Ulmus rubra (3), horse trail behind Cades Cove picnic area, HWK4015-153. A rare species usually associated with lichens on the bark surface of living trees as in this collection. It is known from Arkansas, Kansas, Kentucky, and Ohio in the United States (Keller and Braun 1999). It is locally abundant on lichenized trees of Ulmus americana L. and Juniperus virginiana (Keller and Brooks 1977). Lichen surfaces have different myxomycete stages, including brightly colored orange sclerotia, shiny orange sporangia with a membranous peridium with the orange spore mass within, and mature sporangia covered with a firm, thickened, darker outer peridium. This collection is a new record for Tennessee and the GSMNP.
+Licea kleistobolus G.W. Martin, MC, 3-27 m, L(14), Q(6), A(3), P(2), Sevier, Ramsay Cascades Trail, KLS1026-301.
*Licea marginata Nann.-Bremek., MC, 12-18 m, P(1), A(1), Blount, John Cooper Trail, KLS1155-333.
Licea minima Fr., MC, 3-27 m, P(8), A(3), L(1), Blount, Gum Swamp, KLS1181-204.
*Licea nannengae Pando & Lado, MC, 21 m, L(1), Cocke, Cosby Nature Trail, KLS945314.
Licea operculata (Wingate) G.W. Martin, MC, 3-24 m, A(6), P(4), L(3), Q(1), Cocke, Cosby Nature Trail, KLS924-314.
Liceaparasitica (Zukal) G.W. Martin, MC, 3-24 m, A(7), L(4), F(4), Q(1), Cocke, Cosby Nature Trail, KLS926-3U.
Liceapedicellata (H.C. Gilbert) H.C. Gilbert, MC, 3-18 m, A(4), F(6), Q(3), Haywood, Manway Trail, KLS1088-303.
Licea pseudaconica T.E. Brooks & H.W. Keller, MC, 3-24 m, F(II), Haywood, Manway Trail, KLS1076-3Q3.
Licea pusilla Schrad., MC, 3-27 m, L(17), Sevier, Ramsay Cascades Trail, KLS1003-307. Licea scyphoides T.E. Brooks & H.W. Keller, MC, 15-24 m, F(1), A(1), Blount, Rabbit Creek Trail, KLS1321-247.
*Licea testudinacea Nann.-Bremek., MC, 6-12 m, A(2), Sevier, Porter Creek Trail, KLS1355-240.
+Lindbladia tubulina Fr., on well decayed wood, Indian Gap on Appalachian Trail, June 30, 2000, UHE5509.
Lycogala exiguum Morgan, MC, 9-18 m, A(3), Cocke, Gabes Mountain Trail, KLS361-233.
PHYSARALES
*Badhamia affinis Rostaf., MC, 18-24 m, F(3), Haywood, Manway Trail, KLS1109-303.
+Badhamia papaveracea Berk. & Ravenel, bark of dead lignose, 1.5 m, (1), Blount, Twin Creeks ATBI site, June 26, 2000, UHE5501. This rare species is often misidentified. Its black stalk and distinctive clustered spores separate it from other species (Figures 1-2). These sporangia were collected on a dangling dead vine above ground level.
+Badhamia rugulosa T.E. Brooks & H.W. Keller, MC, 3-27 m, L(6), A(4), Q(2), P(2), F(1), Haywood, Manway Trail, KLS1273-302. This species was also collected in the field on a living Fraxinus americana tree at 13 m, August 4, 2000, Parson Branch Road, Blount, HWK4010114 and on living Vitis sp., August 7, 2000, Parson Branch Road, Blount, HWK4626.
*Badhamia cf. versicolor Lister, MC, 24-27 m, P(2), Haywood, Boogerman Trail, KLS784311. +
Badhamiopsis ainoae (Yamash.) T.E. Brooks & H.W. Keller, MC, 9-21 m, A(5), Cocke, Albright Grove Loop, KLS819-227.
+Craterium minutum (Leers) Fr., on twigs among leaf litter, July 2, 2000, Blount, Abrams Falls Trail 0.8 km past falls, HWK3980 and HWK4624 on well decayed wood in leaf litter, August 7, 2000, Blount, 4.8 km along Parson Branch Road.
*Diachea sp. nov., MC, 18-21 m, F(2), Q(1), Blount, Rabbit Creek Trail, KLS1313-247.
+Diderma chondrioderma (de Bary and Rostaf.) G. Lister, MC, 6-27 m, A(10), L(7), P(5), Q(3), F(2), Sevier, Porter Creek Trail, KLS1375-240.
+Diderma corrugatum T.E. Brooks & H.W. Keller, MC, 9-27 m, F(4), Haywood, Manway Trail, KLS1093-303. This species was also collected from a moss covered living Platanus occidentalis at about 1-2 m, June 27, 2000, along the Cades Cove Road.
Diderma effusum (Schwein.) Morgan, MC, 3-27 m, A(3), Q(3), L(2), F(1), Blount, Gregory Ridge Trail, KLS587-217.
Diderma hemisphaericum (Bull.) Hornem., MC, 15-18 m, A(2), Blount, Bote Mountain Trail, KLS885-2IO.
*Diderma ef. simplex (J. Schrot.) G. Lister, MC, 24 m, A(1), Cocke, Albright Grove Loop, KLS857-227.
+Didymium clavus (Alb. & Schwein.) Rabenh., on bark of living Malus sp. (apple) tree, Twin Creek Natural Resources Center, June 27, 2000, HWK3978; on bark of living Carya tomentosa (Poiret) Nutt. (mockernut hickory), next to Cades Cove House behind Ranger Station, August 2, 2000, HWK4004-111.
*Didymium orthonemata H.W. Keller & T.E. Brooks, MC, 18.3 m, Blount, on bark of living Ulmus rubra, horse trail behind Cades Cove picnic area, HWK4014-153. This is a rare species but locally abundant on Juniperus virginiana in Evergreen Cemetery at Gainesville, Florida (Keller and Brooks 1973) and cemeteries in central Arkansas (Eliasson et al. 1988). Keller and Braun (1999) reported this species from southwestern Ohio at Serpent Burial Mound on Juniperus virginiana and Acer platanoides. Our collection is a new record for Tennessee, GSMNP, and Ulmus rubra. Didymium orthonemata is similar to Didymium dubium Rost, in external appearance but the distinctive capillitial threads are coarse, straight and upright, attached above and below to the peridium, usually with bifurcate tips. The globose, free spores are 12-13 [mu]m in diameter, uniformly and conspicuously spiny. This species is known only from the bark of living trees.
*Physarum aeneum (Lister) R.E. Fr., MC, 3 m, F(1), Blount, Anthony Creek Trail, KLS371244.
*Physarum bogoriense Racib., MC, 3-9 m, Q(2), Blount, Rich Mountain Road, KLS685-322.
+Physarum crateriforme Fetch, MC, 3-30 m, F(18), Q(10), A(6), Blount, Rich Mountain Road, KLS678-322.
+Physarum decipiens M.A. Curtis, MC, 3-27 m, Q(10), F(6), A(4), Blount, Bote Mountain Trail, KLS711-209.
*Physarum digitatum G. Lister & Farquharson, on a well decayed decorticated log near Cades Cove Ranger Station, August 8, 2000, Blount, HWK4630. The type locality for this species is southern Nigeria. It ranges south to Maryland and Nebraska in the United States (Martin and Alexopoulos 1969). Both P. virescens and P. confertum are similar in habit, size and color to P. digitatum. This specimen deviates from the species circumscription in Martin and Alexopoulos (1969) so an expanded description is given here; sporangia sessile, subglobose, obovoid to erect cylindrical, pseudoaethalioid, heaped to tightly clustered in groups of 50 to 100, 4 to 8 mm in length, tawny to brown but mostly with a whitish, calcareous peridium, columella lacking, abundant capillitium with fusiform, white, calcareous nodes, spores dark lilac brown in mass, pale violet with transmitted light, smooth, scattered clustered warts not apparent, 6 [mu] in diameter (Figures 3-4).
*Physarum galbeum Wingate, MC, 15 m, P(1), Blount, Gum Swamp along Cades Cove Loop Road, KLS79-U9.
*Physarum javanicum Racib., MC, 15-27 m, P(2), Blount, Gum Swamp, KLS1208-204. Physarum nutans Pers., MC, 3-30 m, P(29), A(Y), F(4), L(3), Q(3), Blount, Gum Swamp, KLS1198-204.
*Physarum oblatum T. Macbr., MC, 18-24 m, P(5), Blount, Gum Swamp, KLS1212-204.
Physarum psittacinum Ditmar, Tremont Institute ATBI site, West Prong Trail, Dorsey Branch, on well decayed log, July 5, 2000, HWK4006. Hundreds of colorful sporangia covered this log.
+Physarum pusillum (Berk. &M.A. Curtis) G. Lister, MC, 18 m, A(1), Blount, Bote Mountain 11 Trail, KLS900-2W.
+Physarum, robustum (Lister) Nann.-Bremek., on well decayed deciduous wood, ground site, Blount, Twin Creeks ATBI site, UHE5541.
*Physarum cf. sessile Bracirc;ndz , MC, F(1), Blount, 4.8 km up Parson Branch Road, KLS124-151.
*Physarum synsporum S.L. Stephenson & Nann.-Bremek., MC, 9 m, Juniperus virginiana, Blount, Cades Cove Loop Road near donation box, KLS145-174. MC, 18.3 m, Blount, on bark of living Ulmus rubra, horse trail behind Cades Cove picnic area, HWK4014-153. This species is clearly a Badhamia because of the clustered spores and the calcareous, badhamioid capillitium. Questions persist as to the identity and status of Badhamia versicolor and P. synsporum. A detailed discussion of these two species is in Keller and Braun (1999). Physarum synsporum was locally abundant in Ohio in the counties of Adams, Greene and Montgomery based on twelve collections with abundant fruiting bodies collected in the field on juniperus virginiana, Thuja occidentalis L., Juglans nigra L., Prunus serotina Ehrh., Fraxinus sp., and Acer negundo L. Stephenson and Nannenga-Bremekamp (1990) described Physarum synsporum as a new species based on two moist chamber fruitings harvested by Stephenson as numbers 2369 and 2395 on living Juniperus virginiana in Nicholas County, West Virginia. The collections reported here are new records for the substratum, Tennessee, and the GSMNP.
Physarum viride (Bull.) Pers., MC, 15-24 m, A(2), Sevier, Laurel Falls Trail, KLS175-in.
+Trabrooksia applanata H.W. Keller, MC, 3-24 m, F(7), Q(1), P(1), Blount, Rabbit Creek Trail, KLS1283-247.
STEMONITALES
*Comatricha acanthodes Alexop., MC, 3-24 m, L(10), A(5), Q(3), P(17), Cocke, Cosby Nature Trail, KLS910-314. A distinctive species easily identified by it spiny spores. Martin and Alexopoulos (1969) recorded this species from the type locality of Thasos, Greece, and one collection from Mountain Lake, Virginia. Whitney (1982) reported it from Butte and Sonoma Counties in California. Stephenson (1989), in a study of the upland forests of southwestern Virginia, recorded 78 collections of this species on 11 different tree species. Apparently, this species is locally abundant in the Appalachian Mountains based on our 19 collections scattered throughout the park. It occurs on a broad spectrum of bark pH from a mean of 3.9 for Pinus strobus and 6.7 for Quercus alba. Stephenson (1989) reported similar results with a bark pH of 3.8 to 6.8. The distinguishing characters of this species are the opaque, black stalks encased in a hyaline sheath above and expanded below into a pale yellowish basal area with a fibrous network of individual strands. Because of this single character, Nannenga-Bremekamp (1991) assigns this species to the genus Paradiacheopsis. The primary, stout capillitial branches arise from the upper part of the columella, dichotomously branching into flexuose threads. Spores are 12-13 [mu]m, in diameter uniformly covered with conspicuous spines as seen with light microscopy.
Comatricha aequalis Peck, MC, 15 m, P(1), Blount, Gum Swamp, KLS1200-204.
*Comatricha elegans (Racib.) G. Lister, MC, 3-18 m, P(5), Q(1), Blount, Gum Swamp, KLS1185-204.
Comatricha ellae Hark., MC, 3-30 m, P(34), L(20), A(15), Q(6), F(1), Blount, Gum Swamp, KLS1184-204.
Comatricha laxa Rostof., MC, 3-27 m, F(9), Q(5), A(1), Haywood, Manway Trail, KLS1265302.
Comatricha nigra (Pers.) J. Schrot., MC, 12-21 m, A(2), Q(1), Sevier, Porter Creek Trail, KLS1356-240.
*Comatricha penicillata Nann.-Bremek. & Y. Yamam., MC, 3-15 m, P(7), Blount, John Cooper Trail, KLS624-334. This species is recorded for the first time outside of the type locality in Japan. Our specimen matches the line drawing illustration and species description in Nannenga-Bremekamp and Yamamoto (1983). It resembles Comatricha fimbriata, but differs in lacking spatulate tips of the capillitial threads and slender threads that point upward arising from the columella.
Comatricha tenerrima (M.A. Curtis) G. Lister, MC, 3-21 m, A(4), L(2), Blount, Bote Mountain Trail, KLS904-2W.
Enerthenema papillatum (Pers.) Rostaf., MC, 3-30 m, P(SO), L(2), A(1), Q(1), Blount, John Cooper Trail, KLS614-334. This species has a preference for trees with a more acid pH. Noteworthy is the failure to collect this species from Fraxinus americana and Juniperus virginiana, trees close to a neutral pH.
*Lamproderma arcyrionema Rostaf., MC, 3-27 m, F(10, Q(3), L(Z), Blount, Rich Mountain Road, KLS701-322.
* Lamproderma biasperosporum Kowalski, MC, 6 m, A(1), Cocke, Albright Grove Loop, KLS809-227. This species has an unusual distribution pattern, occurring in snowline habitats on decaying coniferous wood near melting snowbanks and in lowland areas on species of Vitis. It is only known from the states of California, Kentucky, Ohio and Oregon. This is the first record on Acer rubrum.
+Macbrideola cornea (G. Lister & Cran) Alexop., MC, 3-30 m, F(32), Q(9), L(2), Blount, Rabbit Creek Trail, KLS1280-247.
+Macbrideola decapillata H.C. Gilbert, MC, 3-9 m, Q(3), Blount, Bote Mountain Trail, KLS715-209.
*Macbrideola declinata T.E. Brooks & H.W. Keller, MC, bark of living Juniperus virginiana tree, 7 m, Blount, Cades Cove Loop Road near donation box, HWK4662-174;MC, Cades Cove Road at Sparks Lane, bark of living Magnolia acuminata L., HWK3987-27. This rare species is found only on living trees and most frequently on Juniperus virginiana. It is known from Arkansas, Kentucky, Ohio, and Tennessee (Eliasson et al. 1988). This is the first record from the GSMNP. The capillitium of M. declinata differs from that of all other species of Macbrideola in the capillitial threads arising from the columella apex, and then dichotomously branching and arched downward, finally becoming attached to the peridium in the basal portions of the sporangium. It is probably overlooked because of its small size, solitary sporangia, and widely scattered habit.
*Macbrideola scintillans H.C. Gilbert, MC, 3-24 m, F(11), L(4), Q(2), Blount, Rabbit Creek Trail, KLS1294-247.
*Paradiacheopsis cribrata Nann.-Bremek., MC, 6-15 m, P(3), Cocke, Gabes Mountain Trail, KLS353-233.
*Paradiacheopsis rigida (Brandz ) Nann.-Bremek., MC, 6-24 m, P(7), Cocke, Albright Grove Loop, KLS853-227.
Paradiacheopsis solitaria (Nann.-Bremek.) Nann.-Bremek., MC, 21 m, P(1), Cocke, Albright Grove Loop, KLS847-227.
*Stemonitis cf. curiosa (ined.), published as Stemonitopsis curiosa Nann.-Bremek. & Y. Yamam., MC, 24 m, A(1), Cocke, Albright Grove Loop, KLS854-227.
Stemonitis flavogenita E. Jahn, MC, 6-12 m, L(2), Q(1), Blount, Bote Mountain Trail, KLS722-209.
Stemonitis fusca Roth, MC, 18-27 m, Q(4), Blount, Gregory Ridge Trail, KLS588-217.
Stemonitis smithii T. Macbr., MC, 3 m, L(1), Sevier, Ramsay Cascades Trail, KLS1001-307.
TRICHIALES
Arcyria cinerea (Bull.) Pers., MC, 3-30 m, L(28), A(24), Q(21), P(14), F(4), Cocke, Albright Grove Loop, KLS811-227. This is the second most common corticolous myxomycete in the tree canopy. Stalked sporangia are variable in color and shape. The digitate form, common on ground sites, was never observed in any of the canopy specimens.
Arcyria incarnata (Pers.) Pers., MC, 12 m, Q(1), Haywood, Manway Trail, KLS1243'-302. Arcyria insignis Kalchbr. & Cooke, MC, 3-24 m, Q(7), L(6), Blount, Gregory Ridge Trail, KLS568-217.
* Arcyria pausiaca H.W. Keller & Buben. -Zurey, MC, 6-27 m, L(7), Sevier, Ramsay Cascades Trail, KLS1013-307. This is a rare species previously only known from Iowa, Michigan, and Ohio. It is easily distinguished from all other species of Arcyria by its dark olivaceous color and broad calyculus. Stalked sporangia were abundant at a number of different sites on the tree. Arcyriapomiformis (Leers) Rostaf., MC, 3-27 m, L(13), A(1), Sevier, Ramsay Cascades Trail, KLS1012-307.
+Calomyxa metallica (Berk.) Nieuwl., MC, 3-30 m, F(11), Q(10), L(6), A(3), Cocke, Cosby Nature Trail, KLS1412-315. This species is more common and abundant on the bark of living Juniperus virginiana with a pH near 7.
Dianema sp., MC, 18-27 m, F(4), Haywood, Manway Trail, KLS1103-303. Hemitrichia cf. abietina (Wigand) G. Lister, MC, 9-15 m, A(3), Blount, Bote Mountain Trail, KLS878-2W.
Hemitrichia serpula (Scop.) Rostaf, MC, 18 m, A(1), Cocke, Albright Grove Loop, KLS842-227. Typically this species is found on the underside of decayed branches, logs, or twigs buried in leaf litter. A specimen was collected at 19 m on the inner bark surface of a living Acer rubrum tree 1.9 km up the Laural Falls Trail, August 5, 2000, HWK4016. This is the first field collection that HWK has seen of this species from a living tree.
Metatrichia vesparium (Batsch) Nann.-Bremek., MC, 9 m, A(1), Sevier, Laurel Falls Trail, KLS166-117.
*Minakatella longifila G. Lister, MC, bark of living Vitis, Blount, 6 km up Parson Branch Road, UHE5754. This is a rare species known from the states of Illinois, Iowa, Kansas, Kentucky, Missouri, Ohio, and West Virginia.
Perichaena chrysosperma (Curr.) Lister, MC, 3-30 m, Q(30), F(20), L(60), A(6), Cocke, Albright Grove Loop, KLS852-227.
Perichaena depressa Lib., MC, 3-24 m, Q(4), Blount, Rich Mountain Road, KLS687-322; on living Vitis sp., Blount, 6.3 km along Parson Branch Road, August 7, 2000, HWK4017.
*Perichaena minor (G. Lister) Hagelst. var. minor, MC, 12-27 m, L(5), A(1), Q(1), Cocke, Cosby Nature Trail, KLS938-314.
+Perichaena minor (G. Lister) Hagelst. var. pardina Minakata, MC, 6-24 m, F(4), Q(4), Haywood, Manway Trail, KLS1079-303; 7 m, on bark of living Juniperus virginiana tree, August 7, 2000, HWK4649-174.
Trichia botrytis (J.F. Gmel.) Pers., MC, 3-30 m, L(27), A(17), Q(6), Sevier, Ramsay Cascades Trail, KLS1004-307. A common tree canopy species but also usually found on decayed logs on ground sites. Mature sporangia were found on the tree bark before moist chamber culture. The same tree species in Ohio (Keller and Braun 1999) failed to produce T. botrytis in moist chamber culture.
*Trichia conforta (Ditmar) Rostaf. var. karstenii (Rostaf.) Ing, MC, on bark of Vitis sp., Blount, 6 km along Parson Branch Road, UHE5784.
Trichia decipiens (Pers.) T. Macbr., MC, 3-24 m, A(1), Cocke, Albright Grove Loop, KLS807-227.
Trichia favoginea (Batsch) Pers., MC, 3-18 m, A(1), Q(1), Sevier, Laurel Falls Trail, KLS152-117. Typically a ground site species, mature fruiting bodies were collected in the field from living trees.
RESULTS
This tree canopy biodiversity research project to inventory the myxomycetes, macrofungi, mosses, liverworts, and lichens in the GSMNP is ongoing. Preliminary data suggest that in certain targeted groups, species found in the tree canopy are also known from ground sites. In the case of canopy collections of macrofungi (5 species), mosses (22 species), liverwort species (16), all are commonly found on ground sites. There are many more samples that still need to be identified. Fieldwork during the summer of calendar year 2000 produced 2,750 lichen samples taken from the tree canopy of 141 trees that yielded 195 lichen species. This total included 78 new lichen records for the GSMNP. All lichen species recorded from the tree canopy also were known to occur on ground sites. In contrast, of the 95 myxomycete species recorded from the tree canopy, approximately 30 are known only from the bark of living trees and vines. Apparently, Myxomycetes are the only group of cryptogams sampled in the GSMNP that has species restricted to the bark of living trees and vines.
DISCUSSION
Most myxomycete species found in the tree canopy, over 65, also typically occur on ground sites. Mature fruiting bodies of Hemitrichia serpula, Trichia botrytis, and Trichia favoginea were documented by field collections in the tree canopy. This suggests that these species are not "contaminants" in moist chamber cultures. One of us (HWK) has collected for over 30 years on living trees in southeastern and central United States (Arkansas, Florida, Georgia, Kansas, Ohio, and Texas), and these ground site species were never found on living trees. One possible explanation for these ground species in the tree canopy is the advanced age and size of the trees sampled for this study. Old growth forest trees in combination with climatic conditions of higher rainfall produce microhabitats similar to ground sites. Much of the sampled bark on older trees, especially Acer rubrum, was loosely attached and in various stages of decay, much like the bark on decaying logs on ground sites. This kind of older tree bark was removed easily by hand. An indicator of community succession with a change in species composition on a living tree occurs when a dead branch or a dead vine, clinging to a living tree, produces an assemblage of ground species never seen on healthy, living parts of the same tree.
The 213 myxomycete species listed for the GSMNP represent a significant number when compared to the state of Ohio where collectors have gathered myxomycetes since 1834 (Keller and Braun 1999) with a total count of 215. In contrast, collecting in the GSMNP since about 1940 to the present has yielded about the same number of myxomycete species as in Ohio in a shorter period of time and with fewer collectors. The varied habitats, elevation gradients, and tracts of old growth forests bode well for a total myxomycete species diversity estimated at over 300 species for the park.
ACKNOWLEDGMENTS
James 'Buck' Counts, Laura Henley, Damon Lesmeister, Melissa Skrabal, and Kenneth L. Snell were student tree climbers from Central Missouri State University who collected samples from the tree canopy. Special thanks go to Charly Pottorff, a professional arborist, who provided tree-climbing instruction and certification for climbers. Keith Langdon from the GSMNP and Jeanie Hilten from Discover Life in America provided assistance with equipment, housing, and logistics. James Murray took many of the photographs while in the GSMNP. More images are displayed on our web page at Discover Life in America "Tree Canopy Biodiversity in the Great Smoky Mountains National Park" . Mike Ferro spent many hours preparing our web page. The multidisciplinary research team included: Drs. Alex Ciegler, lichens, Paul Davison, mosses and liverworts, Professor Uno Eliasson, Goteborg University, Sweden, Myxomycetes and vascular plants, Professor Thomas Gaither, Myxomycetes and macrofungi, Professor Harold W. Keller, Myxomycetes, Ken Nelson, volunteer ecologist, Drs. Jay Raveill, expert on the flora of the GSMNP, David Smith, bryologist, and Ted Stampfer, volunteer moist chamber culture specialist. This research project was funded by the National Science Foundation, Division of Environmental Biology, Biotic Surveys and Inventories Program, Award # DEB-0079058 and Discover Life in America Awards #2001-26 and #2002-17.
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Received June 13, 2002; Accepted November 1, 2002.
KENNETH L. SNELL,1 HAROLD W. KELLER,1* and UNO H. ELIASSON2
1Department of Biology, Central Missouri State University, Warrensburg, Missouri 64093;
2Botanical Institute, Goteborg University, Box 461, SE 405 30 Goteborg, Sweden
