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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.
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 - firstname.lastname@example.org.
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
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.
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.
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