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Mycetozoans of the Great Smoky Mountains National Park: An All Taxa Biodiversity Inventory Project
Steven L. Stephenson and John C. Landolt

Southeastern Naturalist, Volume 8, Number 2 (2009): 317–324

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2009 SOUTHEASTERN NATURALIST 8(2):317–324 Mycetozoans of the Great Smoky Mountains National Park: An All Taxa Biodiversity Inventory Project Steven L. Stephenson1,* and John C. Landolt2 Abstract - During the period of 1998 to 2004, surveys for dictyostelids (cellular slime molds) and myxomycetes (plasmodial slime molds or myxogastrids) were carried out at numerous study sites throughout the Great Smoky Mountains National Park as one component of the All Taxa Biodiversity Inventory (ATBI) project. As a result of these surveys, some general patterns have emerged relating to the occurrence and distribution of these two groups of organisms in the Park. Since the surveys began, the number of dictyostelids known from the Park has increased from 12 to at least 30, the highest total known for any comparable region outside of the tropics. Ten of the 30 species were described as new to science from material collected in the Park. Many of these are “small” species (<2 mm total height) that seem to be confined to marginal habitats at high elevations. The number of myxomycetes known from the Park has increased from 88 to approximately 220, but there are likely to be many additional records as the surveys continue. A number of myxomycetes appear to be restricted largely or exclusively to the Picea rubens (Red Spruce)–Abies fraseri (Fraser Fir) forests found at the very highest elevations in the Park. These forests are currently under considerable environmental stress as the result of industrial pollution and possible global climate change. Introduction The myxomycetes (plasmodial slime molds or myxogastrids) and dictyostelids (cellular slime molds) are two phylogenetically distinct groups of eukaryotic, phagotrophic bacterivores usually present and sometimes abundant in terrestrial ecosystems. Myxomycetes and dictyostelids have rather similar naked amoeboid stages in their life cycle, but the two groups differ in a number of important respects. The myxomycete cycle involves two very different trophic stages, one consisting of uninucleate amoebae, with or without fl agella, and the other consisting of a distinctive multinucleate structure, the plasmodium (Martin et al. 1983). When conditions become unfavorable, the plasmodium gives rise to one or more fruiting bodies containing spores. The fruiting bodies of myxomycetes are somewhat suggestive of those produced by higher fungi, although they are considerably smaller (usually no more than 1–2 mm tall). The spores of myxomycetes are for most species apparently wind-dispersed and complete the life cycle by geminating to produce the uninucleate amoebofl agellate cells. There are approximately 875 recognized species of myxomycetes (Lado 2001). The majority of species are probably cosmopolitan, but a few species appear to be confined to the tropics 1Department of Biological Sciences, University of Arkansas, Fayetteville, AR 72701. 2Department of Biology, Shepherd University, Shepherdstown, WV 25443. *Corresponding author - slsteph@uark.edu. 318 Southeastern Naturalist Vol. 8, No. 2 or subtropics and some others have been collected only in temperate regions of the world (Alexopoulos 1963, Farr 1976, Martin et al. 1983). Myxomycetes appear to be particularly abundant in temperate forests, but at least some species apparently occur in any terrestrial ecosystem with plants (and thus plant detritus) present (Stephenson and Stempen 1994). For most of their life cycle, dictyostelids exist as separate, independent, amoeboid cells (myxamoebae) that feed upon bacteria, grow, and multiply by binary fission. When the available food supply within a given microsite becomes depleted, numerous myxamoebae aggregate to form a structure called a pseudoplasmodium, within which each cell maintains its integrity. The pseudoplasmodium then produces one or more fruiting bodies (sorocarps) bearing spores. Dictyostelid fruiting bodies are microscopic and rarely observed except in laboratory culture. Under favorable conditions, the spores germinate to release myxamoebae, and the life cycle begins anew. The spores produced by dictyostelids are embedded in a mucilaginous matrix that dries and hardens. As such, these spores have a rather limited potential for being dispersed by wind (Olive 1975). However, it has been demonstrated that many different animals, ranging from microscopic invertebrates to birds and small mammals (Stephenson and Landolt 1992), can serve as vectors for dictyostelid spores in nature. Approximately 120 species of dictyostelid are known to science. These organisms are most abundant in the surface humus layers of forest soils, but at least some species can be found in most other types of terrestrial habitats. The Study Area The Great Smoky Mountains National Park encompasses an area of 2080 km2 in eastern Tennessee and western North Carolina between 35°28' and 35°47' N latitude. Elevations range from approximately 270 to 2000 m above sea level. Annual precipitation varies from about 140 cm at low elevations to more than 220 cm for the very highest elevations (Whittaker 1966). Five forest types are dominant over most of the Park, with other types of communities (e.g., shrub balds, grassy balds, bogs, old fields, and rock outcrop communities) having a more limited distribution. Picea rubens Sarg. (Red Spruce)–Abies fraseri [Pursh] Poiret (Fraser Fir) forests are found at elevations above 1525 m, and northern hardwood forests occur at middle elevations (1065 to 1525 m). At lower elevations (generally below 1065 m), pine (Pinus spp.)–oak (Quercus spp.) forests occupy drier sites, and Tsuga canadensis [L.] Carr. (Eastern Hemlock) forests often occur along riverbanks. Cove hardwood forests, the most diverse of all the forest types, are found in valleys throughout the Park. Among the more important and widely distributed trees in these forests are Liridodendron tulipifera L. (Tulip Tree), Fagus grandifolia Ehrhart (American Beech), and Acer saccharum Marshall (Sugar Maple). More detailed information on all of these forest types is provided in Whittaker (1956), Stephenson et al. (2001), and Jenkins (2007). 2009 S.L. Stephenson and J.C. Landolt 319 Materials and Methods Some collecting for myxomycetes in the Park was carried out by the senior author during the period of 1982 to 1997, which predates the beginning of the All Taxa Biodiversity Inventory (ATBI) project (Nichols and Langdon 2007). However, intensive surveys began in 1998 and continued until 2003, and the specimens obtained from these efforts form the basis of the myxomycete portion of this paper. The methods used in carrying out the surveys were essentially those described by Stephenson (1988, 1989). Myxomycetes were collected in different localities and/or vegetation types throughout the Park. At each study site, potential substrates were examined carefully for myxomycete fruiting bodies. A “collection” was defined as one or more fruiting bodies sharing the same substrate and considered to have originated from a single plasmodium. In almost every instance, this could be determined without difficulty. The method used in making a collection involved removing all or most of the fruiting bodies along with a portion of the substrate upon which they occurred. These collections were returned to the laboratory, air-dried and glued in small boxes for permanent storage. In an effort to supplement field collections, samples of various types of plant debris were collected at a number of localities in the Park and used to prepare a series of moist chamber cultures in the manner described by Stephenson and Stempen (1994). However, the data obtained from these cultures are not considered in this paper. Identification of collections was made using the descriptions and keys provided by Martin and Alexopoulos (1969) and various other monographs or by comparison with specimens obtained on loan from the National Fungus Collections (BPI). Vouchers of all species mentioned herein are deposited in the mycological herbarium of the University of Arkansas (UARKM). Nomenclature used for myxomycetes essentially follows Lado (2001). During the period of 1993 to 2004, we collected 412 samples (each approximately 10–15 g) of soil/humus for isolation of dictyostelids from 25 study sites throughout the Park. These sites included examples of all major forest types along with a number of other non-forest habitats (e.g., shrub balds [i.e., treeless areas], grassy balds, bogs, old fields, and rock outcrop communities) having a more limited distribution. Samples for dictyostelids were collected in many of the same localities and/or vegetation types surveyed for myxomycetes, but sampling also was carried out in a number of other study sites. Although sampling for dictyostelids began prior to the ATBI, the majority of samples were collected during the period of 1998– 2004, and many of the study sites were chosen for their proximity to ATBI permanent study plots. Five to 35 samples (each 10–30 g) were collected at each of the 25 study sites, some of which were visited on more than one occasion. All samples were placed in sterile plastic bags and kept away from temperature extremes until processed in the laboratory. Isolation procedures used for dictyostelids were those described by Cavender and Raper (1965). Each sample was weighed and enough sterile distilled water added to create a 1:25 dilution of 320 Southeastern Naturalist Vol. 8, No. 2 sample material. Aliquots (each 0.5 mL) of this suspension were added to each of two or three 95- to100- x 15-mm culture plates prepared with hay infusion agar (Raper 1984). This produced a final dilution of 0.02 g of soil per plate. Approximately 0.4 mL of a heavy suspension of E. coli was added to each culture plate, and plates were incubated under diffuse light at 20–25 ºC. Each plate was examined at least once a day for several days following appearance of initial aggregations, and the location of each aggregate clone marked. When necessary, isolates were subcultured to facilitate identification. Nomenclature used herein follows Raper (1984). Results and Discussion Since the onset of the ATBI, approximately 1300 specimens of myxomycetes that had developed in the field under natural conditions were collected from study sites throughout the Park. This total includes representatives of all six taxonomic orders recognized for the myxomycetes (Martin et al. 1983). The Physarales (31% of all specimens) and Trichiales (31%) were the two predominant orders, the Liceales (20%) and Stemonitales (16%) relatively less important, and the Ceratiomyxales (2%) and Echinosteliales (<1%) were represented by much lower numbers of specimens. However, because no effort was made to collect every specimen of Ceratiomyxa fruticulosa (O.F. Müll.) T. Macbr., the only member of the Ceratiomyxales known to occur in the Park, this species is more abundant than these figures might indicate. In fact, during the period of late May to early September, after a period of rainy weather, fruitings of C. fruticulosa commonly occur on logs and stumps throughout any forest in the Park. Prior to the ATBI, only about 88 species of myxomycetes had been reported from the Park. However, survey efforts carried out in the context of the ATBI have yielded many new records. Stephenson et al. (2001) added 75 species, while Snell and Keller (2003) increased this total by another 35 species. Since then, additional specimens obtained in the field or from chamber-culture cultures (S.L. Stephenson, unpubl. data) have brought the total number of species known to occur in the Park to approximately 220. This total is as high as or higher than those recorded for comparable areas of North America. For example, approximately 180 species are known from the state of West Virginia (Stephenson and Mitchell 1990; S.L. Stephenson, unpubl. data), and 215 species have been reported from the state of Ohio (Keller and Braun 1999). Ongoing surveys in the Park continue to yield new records, and since not all habitats (e.g., grass balds) and microhabitats (e.g., soil) have been subjected to a detailed investigation, it seems likely that many additional species have yet to be documented as occurring in the Park. Thus, the Park may represent one of the world’s “hot spots” for myxomycete biodiversity. Some species can be considered as exceedingly common in most areas of the Park. Prominent examples include: Arcyria cinerea (Bull.) Pers., A. denudata (L.) Wettst., Hemitrichia calyculata (Speg.) M.L.Farr, Metatrichia vesparia (Batsch) Nann.-Bremek., Trichia erecta Rex, and 2009 S.L. Stephenson and J.C. Landolt 321 Trichia favoginea (Batsch) Pers. in the Trichiales; Didymium melanospermum (Pers.) T. Macbr., Physarum album (Bull.) Chevall., P. globuliferum (Bull.) Pers., and P. viride (Bull.) Pers. in the Physarales; Cribraria cancellata (Batsch) Nann.-Bremek., C. intricata Schrad, and Lycogala epidendrum (L.) Fr. in the Liceales; and Collaria arcyrionema (Rostaf.) Nann.-Bremek., Comatricha nigra (Pers. ex J.F. Gmel.) J. Schröt., Stemonitis axifera (Bull.) T. Macbr., S. fusca Roth, and Stemonitopsis hyperopta (Meyl.) Nann.- Bremek. in the Stemonitales. Each of these species represented >1% of the 1300 specimens referred to above. A few examples such as Arcyria cinerea, Hemitrichia calyculata, and Physarum viride were particularly abundant. Collectively, these three species made up almost 20% of all specimens collected in the Park. In contrast, some of the species recorded from the Park are rare. For at least five myxomycetes (Comatricha penicillata Nann.-Bremek. et Y. Yamam., Lamproderma granulosum H. Neubert, Nowotny et Schnittler, Licea microscopica D.W. Mitchell, L. rufocuprea Nann.-Bremek. et Y. Yamam, and L. sambucina D.W. Mitchell), the record reported for the Park also represented the first known occurrence of the species in North America (Snell and Keller 2003, Stephenson et al. 2001). One species (Diachea arboricola H.W. Keller et M. Skrabal) has been described as new from material collected in the Park (Keller et al. 2004), and several other specimens may represent species new to science (S.L. Stephenson, unpubl. data). The majority of myxomycetes are considered to be cosmopolitan (Martin and Alexopoulos 1969) and thus might be expected to occur throughout the Park. This is certainly the case for many of the more commonly collected examples, including virtually all of the species mentioned above as being exceedingly common. The most notable exceptions are Trichia erecta and Didymium melanospermum, both of which tend to be associated with the Red Spruce-Fraser Fir forests found at the very highest elevations in the Park, although they are not limited to these forests. However, a number of other myxomycetes appear to be restricted largely or exclusively to Red Spruce- Fraser Fir forests. Among these are Barbeyella minutissima Meyl., Colloderma oculatum (C. Lippert) G. Lister, Elaeomyxa cerifera (G. Lister) Hagelst., Lamproderma columbinum (Pers.) Rostaf., and Lepidoderma tigrinum (Schrad.) Rostaf. (Stephenson 2004). Red Spruce-Fraser Fir forests are currently under considerable environmental stress as the result of industrial pollution and possible global warming (Eagar and Adams 1992), and it seems likely that they could be reduced considerably in extent over the next few decades. Presumably, this would pose a serious threat to the various organisms (including myxomycetes) found in these forests. More than 2300 clones were recovered from the 412 samples collected for isolation of dictyostelids. These clones included representatives of 20 described species together with 10 species that were described as new to science from material collected in the Park (Cavender et al. 2005). This level of diversity is the highest total known for any comparable region outside of the tropics (Landolt et al. 2006). Two of the already described species (one 322 Southeastern Naturalist Vol. 8, No. 2 commonly found in Germany and the other described originally from Japan) were isolated for the first time in North America. A number of clones could be identified only to genus; in most instances these are likely to have been aberrant examples of one or more of the 30 species referred to above, but some may represent other “new” species. The 25 study sites from which samples have been collected in the Park fall within three elevation zones: high elevation (1570–1920 m), intermediate elevation (732–914 m), and low elevation (463–617 m). As a general observation, dictyostelids displayed a pattern of decreasing density (based on mean numbers of clones/gram) with increasing elevation. Samples from the nine study sites at low elevations yielded 178 clones/g, those from the eight sites at intermediate elevations yielded 141 clones/g, and the nine sites at high elevations produced 111 clones/g. However, species richness was similar in the three zones. Twenty-four species were recorded from the high-elevation sites, 19 from the intermediate-elevation sites, and 21 from the low-elevation sites. The fact that the highest level of species richness was recorded for the high-elevation zone may be related to the fact that two types of forest communities occur at higher elevations in the Park. The first type of forest (spruce, spruce/fir or beech) is characterized by a high level of dominance of one or a few tree species, whereas the other type (northern hardwood) is characterized by a higher number of tree species sharing dominance. In addition, the most important trees present in spruce and spruce/fir forests, the most extensive forest type found at high elevations, are conifers, whereas a northern hardwood forest is made up primarily of broadleaf trees. When the nine study sites at high elevations are separated into these two forest types, dictyostelid density was appreciably lower (43 clones/g) in spruce, spruce-fir, and beech forests than in northern hardwood forests (196 clones/g). However, the number of species recorded from each forest type (15) was exactly the same. Based on pooled data for all study sites, Dictyostelium mucoroides Brefeld, D. minutum Raper, Polysphondylium violaceum Brefeld, P. pallidum Olive, and D. discoideum Raper are the most common and widespread species of dictyostelids in the Park as a whole. Each was recorded from at least half of all study sites. One other species (P. tenuissimum H. Hagiw.) displayed high overall abundance, but this can be attributed to its relatively high densities in just eight study sites. Only three other species (D. lacteum van Tieghem, D. aureostipes Cavender, Raper et Norberg, and D. purpureum Olive) were recorded from as many as 10 study sites, and nine species were limited to a single study site. Several of the more common and widespread species displayed differences in abundance for the three elevation zones described above. For example, D. discoideum and P. tenuissimum were relatively more common at high elevations, whereas D. aureostipes, D. lacteum, D. purpureum, and P. violaceum were relatively more common at low elevations. Dictyostelium minutum, D. mucoroides, and P. pallidum were common over a wide range 2009 S.L. Stephenson and J.C. Landolt 323 of elevations. Thirteen species were limited to or achieved their maximum level of abundance in study sites at high elevations, and the same type of situation applied to eight species for both the intermediate- and lowelevation study sites. Not surprisingly, most of the new species, all of which are represented by limited material, were associated with a single elevation zone. Many of these are “small” species (<2 mm total height) that seem to be confined to marginal habitats at high elevations. The relatively large number of new species, in this case seven (Acytostelium longisorophorum Cavender, Vadell, J.C. Landolt et S. L. Stephenson; A. serpentarium Cavender, Vadell, J.C. Landolt et S.L. Stephenson; D. amphisporum Cavender, Vadell, J.C. Landolt et S.L. Stephenson; D. naviculare Cavender, Vadell, J.C. Landolt et S.L. Stephenson; D. oculare Cavender, Vadell, J.C. Landolt et S.L. Stephenson, D. potamoides Cavender, Vadell, J.C. Landolt et S.L. Stephenson, and D. stellatum Cavender, Vadell, J.C. Landolt et S.L. Stephenson), recovered from high-elevation study sites would seem particularly noteworthy. In summary, the Great Smoky Mountains National Park is characterized by high levels of biodiversity for both myxomycetes and dictyostelids. The number of species of dictyostelids recorded thus far is as high as for any temperate region of the world investigated to date, and the number of species of myxomycetes seems likely to reach the same point if present survey efforts continue. Interestingly, this possibility was first suggested by Robert Hagelstein (1940), a leading authority on the myxomycetes during the second quarter of the 20th century, well over 60 years ago. After collecting myxomycetes in the Park in 1939, he indicated that “the region, with its diverse typographical features, timber belts of many kinds, and heavy annual rainfall, is ideal territory for the Mycetozoa, perhaps the best in the eastern United States” (p. 377). The data obtained in the context of the ATBI seem to indicate that Hagelstein was correct. Acknowledgments This study was supported by several grants from the Discover Life in America Foundation, the Shepherd University Foundation and Alumni Association, the West Virginia NASA Space Grant Consortium, and the National Science Foundation (grant DEB-0316284). Ian Stocks, Chuck Parker, Randy Darrah, Paul Davison, Will Reeves, Melinda Landolt, and Jeanie Hilten contributed sampling assistance to this study, and Nancy Critzer assisted in laboratory isolation procedures. Literature Cited Alexopoulos, C.J. 1963. The myxomycetes II. Botanical Review 29:1–78. Cavender, J.C., and K.B. Raper. 1965. The Acrasieae in nature. I. Isolation. American Journal of Botany 52:294–296. Cavender, J.C., E. Vadell, J.C. Landolt, and S.L. Stephenson. 2005. New species of small dictyostelids from the Great Smoky Mountains National Park. Mycologia 97:493–512. Eagar, C., and M.B. Adams. 1992. Ecology and Decline of Red Spruce in the Eastern United States. Ecological Studies 96. Springer-Verlag, New York, NY. 417 pp. 324 Southeastern Naturalist Vol. 8, No. 2 Farr, M.L. 1976. Flora Neotropica Monograph No. 16 (Myxomycetes). New York Botanical Garden, Bronx, NY. 304 pp. Hagelstein, R. 1940. Notes on the Mycetozoa IV. Mycologia 32:376–387. Jenkins, M.A. 2007. 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