Microfungi from Bark of Healthy and Damaged American Beech, Fraser Fir, and Eastern Hemlock Trees During an All Taxa Biodiversity Inventory in Forests of the Great Smoky Mountains National Park
Richard E. Baird, Clarence E. Watson, and Sandra Woolfolk
Southeastern Naturalist, Volume 6, Number 1 (2007): 67–82
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2007 SOUTHEASTERN NATURALIST 6(1):67–82
Microfungi from Bark of Healthy and Damaged American
Beech, Fraser Fir, and Eastern Hemlock Trees During an
All Taxa Biodiversity Inventory in Forests of the
Great Smoky Mountains National Park
Richard E. Baird1,*, Clarence E. Watson2, and Sandra Woolfolk1
Abstract - The assemblage of microfungi associated with bark samples of healthy
and damaged Fagus grandifolia (American beech), Abies fraseri (Fraser fir), and
Tsuga canadensis (eastern hemlock) trees was evaluated during an All Taxa
Biodiversity Inventory of the Great Smoky Mountains National Park in 2003 and
2004. Bark samples were collected from sampling points 0.3, 0.6, 0.9, and 1.2 m
above the ground surface on the bole of each replicate tree. Patterns of species
composition and diversity (species richness) were evaluated from bark samples over
three sampling dates (May, July, and September) each year. A total of 4814 isolates
were obtained, with greater than 95% belonging to the Deuteromycota. Over 94
species of fungi were identified from bark of the three tree species, which were either
healthy or were damaged or under pressure from exotic pests. The most common
genus was Trichoderma, for which a total of 13 species were identified during the
two-year study. Frequencies of microfungi between healthy and damaged trees were
similar across years, but when data was compared by year, frequencies were significantly
greater in 2004 than 2003. Species richness was almost always significantly
greater in September than in May and July. Frequencies of microfungi isolated from
bark samples collected 1.2 m above the ground were significantly greater than in
samples collected at 0.9, 0.6 and 0.3 m. Increased species richness at the higher bole
positions was likely related to changes in microenvironment, as proposed by previous
researchers. All other comparisons of species richness were similar.
Introduction
Microfungi species, which produce microscopic spore-bearing structures,
belong primarily to the Ascomycota and Deuteromycota, but may also include
species of the Basidiomycota and Zygomycota (Cannon and Sutton 2004).
Large numbers of species and genera of microfungi have been reported from
bark and litter of forest trees (Bills et al. 2004, Fernandez and Boyer 1989).
However, studies to determine species richness of microfungi in different
forest ecosystems have been limited due to the small size of microfungi and
lack of occurrence on economically important hosts. To overcome this disparity
in information for fungi and other organisms, the All Taxa Biological
Inventory (ATBI) was developed to inventory all organisms in unique or
diverse habitats around the world (Sharkey 2001). Fungi were selected as one
1Entomology and Plant Pathology Department, Box 9655, Mississippi State University,
Mississippi State, MS 39762. 2MAFES Administration, Box 9740, Mississippi
State University, Mississippi State, MS 39762. *Corresponding author -
rbaird@plantpath.msstate.edu.
68 Southeastern Naturalist Vol. 6, No. 1
of the groups of organisms to be included as a pilot program for an ATBI in the
Area de Conservación Guanacaste, located in the northwestern corner of Costa
Rica (Janzen 1996, Rossman et al. 1998). Following that initiative, an ATBI
was started in the Great Smoky Mountains National Park (GSMNP) in 1997
(Sharkey 2001). What limited data on fungi that existed was included in a list
for the GSMNP that was compiled from various sources over many years
(Petersen 1979) and for myxomycetes and select phyla known from specific
habitats (H.A. Raja and C.A. Shearer, unpubl. data; Stephenson et al. 2001).
Prior to these studies, little data on microfungi had been obtained in the park
due to cost of the work and lack of mycological expertise. Data for microfungi
from forest ecosystems in the GSMNP are needed especially from sites where
loss of habitat or tree species are occurring from exotic pests, since loss of these
host trees may result in the elimination of fungi specific to the hosts.
The surface of bark from living trees contains a wide variety of organisms
including bacteria, bryophytes, and lichens. Fungi also comprise a
large percentage of the microflora (Bier 1963a, b), and research on the occurrence
of bark fungi has been conducted for many different tree species
(Garner 1967, Sivak and Person 1973). While Butin and Kowalski (1986)
found fungi in the Ascomycota and Deuteromycota were the most common
taxa present on five hardwood species, Kliejunas and Kuntz (1974) identified
many fungal genera from healthy bark with the most common genera
being Alternaria, Epicoccum, Fusarium, Penicillium, Phoma, and Trichoderma.
Other researchers have catalogued caulosphere microorganisms to
determine if bark microfungi inhibit or reduce invasion by pathogenic fungi
(Baird 1991, Cox and Hall 1978, Weir et al. 1996). Unfortunately, very few
studies evaluated changes in microflora following invasion of exotic fungal
pathogens or insect pests.
In the Southern Appalachian Mountains, pests cause significant losses to
three major forest tree species. Nectria coccinea var. faginata Lohm. Wats.
& Ay., the causal organism of beech bark disease, currently attacks Fagus
grandifolia Ehrh. (American beech). Adelges tsuga Annand. (hemlock
woolly adelgid) is attacking Tsuga canadensis (L.) Carr. (eastern hemlock),
and Adelges piceae Ratzeburg (balsam woolly adelgid) is killing Abies
fraseri (Pursh) Poir. (Fraser fir).
American beech occurs in eastern North American forests and is an
important component of the GSMNP. This tree species occurs in areas predominantly
composed of beech, termed “beech gaps.” Since many of these
clusters of beech occur at high elevations, the gaps are considered a rare forest
community type (Whittaker 1956). Unfortunately, the exotic fungus N.
coccinea var. faginata, which entered North America near Nova Scotia
around 1890 (Ehrlich 1934), has spread southward and entered the GSMNP in
1993 (Houston 1994). Since the introduction of this pathogen, the population
of American beech in the GSMNP has been drastically reduced. Permanent
plots were established in 1994 to monitor tree health and mortality (Wiggins et
al. 2004). As of 1997, 26% tree mortality occurred within the plots, but in one
2007 R.E. Baird, C.E. Watson, and S. Woolfolk 69
area, all 77 overstory trees died (G. Taylor, USDA/National Park
Service[NPS]-GSMNP, pers. comm.).
Eastern hemlock is a dominant tree species that is widely distributed in
the southern Appalachian Mountains and covers 3820 acres, or 1% of the
GSMNP (Johnson et al. 1999). The exotic insect, hemlock woolly adelgid,
was first reported in the Pacific Northwest in 1924 and spread to the northeast
in the 1950s. The insect moved southward through the mountains of
Virginia and Tennessee around 2001. In the following year, the insect
entered the GSMNP and now infests large areas of the park where Eastern
hemlock occurs (R. Miller 2002, USDA/NPS-GSMNP, unpubl. data).
Fraser fir is the only fir species endemic to the southern Appalachian
Mountains and has a disjunct distribution that restricts it to higher elevations
in southwest Virginia, eastern Tennessee, and western North Carolina. The
GSMNP has approximately 74% of the total spruce-fir forest in the southern
Appalachians. The balsam woolly adelgid, which entered the eastern portion
of the GSMNP at Mount Sterling, has killed over 90% of the mature Fraser
fir over the last 35 years in these areas, but regeneration from remnant trees
appears to hold hope for survival of this species (Dull et al. 1988). However,
many of the surviving larger trees continue to be newly infested with this
pest, which results in their eventual death (M. Kloster, USDA/NPSGSMNP,
pers. comm.).
As the health of American beech, Fraser fir, and eastern hemlock declines,
changes in the caulosphere fungi can be expected. Unfortunately, no
studies to compare bark fungi are available for healthy and damaged trees.
Development of baseline data to establish identities and frequencies of fungi
present on healthy and damaged trees may be useful for evaluation of tree
health and development of biological control strategies for the pests. The
objectives of this study were: 1) to develop baseline data and catalog the
fungal microflora present on bark tissues of healthy and damaged American
beech, Eastern hemlock, and Fraser fir for the ATBI in the GSMNP; and
2) to determine if sampling positions on boles and dates of sampling influence
species richness.
Materials and Methods
Field collections of bark were obtained from American beech, Fraser fir,
and eastern hemlock stands located within the boundaries of the GSMNP.
Although, it was difficult to establish a similar range of tree sizes for sampling
during the investigation, all trees sampled were 20 cm in diameter at 1.3 m
above the ground. Additional criteria for sampling are discussed below.
Table 1 gives exact dates and locations sampled in 2003 and 2004.
On each sampling date, bark samples were obtained from five healthy and
five damaged trees of each species. Healthy trees exhibited no symptoms of
damage as a result of exotic fungal or insect pest. Damaged American beech
trees selected for sampling included those with greater that 50% canopy
defoliation and die-back (Durr et al. 1988) and a high rating of Nectria spp.
70 Southeastern Naturalist Vol. 6, No. 1
Table 1. Sampling dates and locations within GSMNP of bark samples collected from three tree species over a two-year period. Coordinates are listed on UTM
NAD27 CONUS and are within UTM zone 17S.
Healthy Damaged
Sampling date American beech Fraser fir Eastern hemlock American beech Fraser fir Eastern hemlock
2003
(May 6–7, 2003) Fork Ridge Trail Mt. Sterling A Sugarlands Center Fork Ridge Trail Mt. Sterling A Laurel Falls
3939907N 3952818N 3951831N 3939907N 3952586N 3950395N
0278128E 0307907E 0270532E 0278128E 0307796E 0266283E
(July 1–3, 2003) Mt. Sterling C Mt. Sterling A Sugarlands Center Fork Ridge Trail Mt. Sterling A Laurel Falls
3952349N 3952818N 3951831N 3939907N 3952586N 3950395N
0307646E 0307907E 0270532E 0278128E 0307796E 0266283E
(Sept. 9–10, 2003) Beech Gap A Clingman’s Dome A Rainbow Falls A Beech Gap B Clingman’s Dome B Rainbow Falls B
3946910N 3938104N 3950552N 3946822N 3938080N 3950550N
0300490E 0272998E 0274930E 0300636E 0273302E 0274993E
2004
(May 15, 2004) Double Gap Appal. Trail Twin Creeks Double Gap Appal. Trail Twin Creeks
393 8507N 3938128N 3951948N 393 8507N 3938128N 3951948N
026 9497E 0271952E 0273776E 0269497E 0271952E 0273776E
(July 8–9, 2004) Beech Forest on Mt. Buckley Cove Mt. Trail, Beech Forest on Mt. Buckley Cosby Campground
New Found Gap Near Sugarland New Found Gap on Cosby Nature
Trail Hdq. Trail Trail
3943462N 3938089N 3952482N 3943462N 3938089N 3958992N
0278482E 272790E 0270634E 0278482E 0272790E 0300416E
(Aug. 11–12, 2004) Cataloochee, Clingman’s Dome Cataloochee, Cataloochee, Clingman’s Dome Cataloochee,
GSMNP-Horse Area GSMNP on GSMNP-Big GSMNP-Horse Area GSMNP on GSMNP-Rough
Camp area just Appalachian Trail Fork Ridge Trail Camp area just Appalachian Trail Fork Trail
before Little before Little
Cataloochee Trail Cataloochee Trail
3944395N 3938112N 3939633N 3944395N 3938112N 3942239N
0308693E 0273087E 0307911E 0273087E 0273087E 0307212E
2007 R.E. Baird, C.E. Watson, and S. Woolfolk 71
levels (Vance 1995). Ratings for Nectria spp. (presence of perithecia) were
made on the north and south side of each tree using a rating scale within a 33- x
33-cm area, centered 122 cm above the ground surface. Damaged Fraser fir
selected for sampling included those with greater than 50% canopy defoliation
and die-back, and high numbers of A. piceae present on 100 cm2 of each bole as
determined by applying a 2-cm2 template at 25 points around the circumference
of each tree at 1.5 m above the ground surface (G. Taylor and K. Johnson,
GSMNP, unpubl. USDA/FS BWA Survey Protocol and pers. comm.). Damaged
eastern hemlock trees include those that were rated as heavily infested
with A. tsuga. This included trees that had up to 80% of the branches infested by
the insects (J. Pickering, University of Georgia, pers. comm.).
Following tree selection, four bark samples, each 5 x 5 cm and 5 mm
deep, were taken at 0.3, 0.6, 0.9, and 1.2 m above the ground on the north
side of each bole. Each bark piece was placed into an envelope, kept cool
until returned to the laboratory, and stored at 4 C until processed.
For isolation and identification of fungi, each of the bark samples were
subdivided into four 1-cm2 pieces and surface-sterilized in sodium hypoclorite
(0.524% w/v) for 3 min. Two pieces were then plated onto potato-dextrose agar
(PDA) and water agar (WA) as previously described by Baird et al. (2004). The
plates were incubated for 7 days at room temperature to allow for growth of
fungi. All fungi growing in the plates were subcultured onto PDA and stored for
later identification using standard mycological methods. More than one fungus
was often isolated from a single piece of bark. Isolation frequencies based on
numbers of bark samples infected were determined for genera and species
isolated. Single spores of cultures initially identified as Fusarium spp. were
transferred to carnation leaf agar using original ingredients as previously
defined (Nelson et al. 1983). Keys for general identification of fungi were those
developed by Barnett and Hunter (1998), Ellis (1971, 1976), and Sutton (1980).
In addition, an unpublished guide to Trichoderma spp. by G. Samuels, USDA/
Agricultural Research Service-Beltsville, MD, was used.
Statistical analysis
The experimental design was a completely randomized design (CRD)
with five replications (trees) within each tree species, sampling date, and
condition (healthy or diseased). Data were analyzed by analysis of variance
as a series of combined CRDs over years using the GLM procedure of SAS
(SAS Institute, Cary, NC). Mean separation was carried out using Fisher’s
protected least significant difference (LSD).
Results
Ninety-four species of fungi were isolated from the bark of healthy and
damaged American beech, Fraser fir, and eastern hemlock during the study
(Appendix 1). A total of 2195 fungi was isolated in 2003 and 2619 in 2004.
Greater than 95% of total fungi were from the Deuteromycota, 2.3%
Ascomycota, 1.2% Zygomycota, and 1% others or unknowns.
72 Southeastern Naturalist Vol. 6, No. 1
The most common species identified during the study were Curvularia
lunata (Wakk.) Boedijn, Pestalotia clavipora (Atk.) Steyaert, Pestalotia
funerea (Desmaz) Steyaert, Trichoderma aggressivum Samuels and W.
Gams., Trichoderma aureoviride Rifai, Trichoderma hamatum (Bonord.)
Bainier, Trichoderma harzianum Rifai, Trichoderma koningii Oudem., Trichoderma
virens (J. Miller et al.) Arx, and Trichoderma viride Pers.:Fr.
Yeast species were obtained from American beech, but none were found on
the bark of the other two tree species.
When the percentages of isolation were compared between bark samples
from healthy and damaged trees across years, no differences were observed.
However, the percent isolation data pooled across three tree species, two tree
conditions, and four sampling points were significantly greater in 2004 than
2003. When the 20 most common fungi isolated were evaluated across years,
bark positions, and tree conditions, no differences were observed. Furthermore,
when isolation frequencies were analyzed separately by tree condition,
no differences were observed in 2003 or 2004 (data not shown).
Isolation frequencies were compared between the four bark sampling
points for each tree species and year (Table 2). No differences were observed
between frequencies from bark sample locations collected in 2003, but
differences in species richness occurred in 2004. Isolation frequencies from
the samples collected at 1.2 m above the ground were significantly greater
than bark samples collected from 0.3 and 0.6 m. Percent frequencies from
bark samples from 0.9 m were almost always significantly greater than at 0.3
and 0.6 m, with the exception that the frequencies from eastern hemlock
were similar between 0.6 and 0.9 m bark sample points from both healthy
and damaged trees. When individual fungal species were compared by
sampling position, only Cephalosporium spp. species had significantly different
isolation frequencies on American Beech. No other position differences
by fungal species for the three trees occurred during the study.
Table 2. Percent occurrence of mycobiota isolated from bark at four locations on three tree species
over two years. Position means within a year, condition, and tree species not followed by a
common letter (a–c) are significantly (P 0.05) different according to Fisher’s protected LSD.
Bark sample American beech Fraser fir Eastern hemlock
position DA HB D H D H
2003
0.3m 2.05 1.62 1.76 1.80 1.95 1.62
0.6m 1.86 1.95 1.90 1.80 1.71 2.67
0.9m 1.86 1.80 1.33 2.05 2.05 1.76
1.2m 2.19 2.04 1.67 2.05 2.28 1.95
2004
0.3m 1.50c 1.15c 1.41c 1.19c 1.67c 1.59c
0.6m 1.81c 1.72c 2.03c 1.67c 2.34bc 1.81bc
0.9m 2.91b 2.87b 2.69b 2.60b 3.00b 2.47b
1.2m 4.37a 4.55a 4.64a 4.31a 4.55a 3.31a
AD = Trees damaged from exotic pests (fungi or insect).
BH = healthy trees without occurrence of a pest.
2007 R.E. Baird, C.E. Watson, and S. Woolfolk 73
Percent isolation frequencies across all three tree species and their conditions
were compared by sampling date (Table 3). The largest number of
isolates almost always occurred in September and the percentages were either
numerically or significantly greater than from the May or July samplings. Two
exceptions were that the September frequencies were numerically, but not
significantly lower than for May and July for healthy American beech and
damaged Fraser fir in 2004.
Percent isolation frequencies were similar compared across tree species,
tree conditions, and bark positions. When percent isolations were compared
by tree species across both tree conditions and all bark positions, all data
were similar by year.
Discussion
In December 1997, the ATBI was initiated to collect all species of
organisms in GSMNP (Sharkey 2001), but research on microfungi was not
conducted until 2002 (Raja et al. 2003). Because of this initial effort,
microfungi were sampled over two years from bark of select, potentially
endangered trees that occur in GSMNP. Ninety-four species of fungi were
identified from the bark of the three tree species. Isolation frequencies were
almost always higher during the September sampling than in May and July.
The greater percentages might be expected due to the increase of inoculum
and colonization by fungi towards the end of the growing season. All bark
collections were georeferenced, and the species data with sampling information
were added to the database list of organisms identified for GSMNP.
Previously, Bills and Polishook (1994) collected 300 to 400 species of fungi
within each replicate 1-ml leaf-litter sample collected from a Costa Rican
rainforest. Since the current study of bark samples were much lower, isolation
methods (e.g., media) or substrate differences, such as litter compared
to bark, may have limited species richness.
Table 3. Percent occurrence of mycobiota from three tree species by sampling dates over two
years. Sampling date means with a year, condition, and tree species not followed by a common
letter (a–b) are significantly (P 0.05) different according to Fisher’s protected LSD.
American beech Fraser fir Eastern hemlock
Sampling date DA H D H D H
2003
May 1.86ab 1.71b 1.25b 1.46b 1.43b 1.57b
July 1.67b 1.17b 1.75ab 1.93ab 1.43b 1.57b
September 2.43a 2.68a 2.00a 2.39a 3.14a 2.86a
2004
May 2.09b 2.65a 2.95a 2.21a 3.01ab 2.05a
July 2.78ab 2.81a 3.15a 2.478a 2.38b 2.25a
September 3.08a 2.25a 1.98b 2.88a 3.28a 2.58a
AD = Trees damaged from exotic pests (fungi or insect).
BH = healthy trees without occurrence of a pest.
74 Southeastern Naturalist Vol. 6, No. 1
The majority of fungi isolated in the current study were members of the
Deuteromycota, which coincides with results from past investigations (Baird
1991, Cotter and Blanchard 1982, Fernandez and Boyer 1989). More than 13
species of Trichoderma, a common hyphomycete, were identified, and collectively
had the greatest isolation frequencies of any genus during this
study. Other common fungi on these three tree species included C. lunata,
two Pestalotia spp. and five Penicillium spp. Previously, Cotter and
Blanchard (1982) showed that Trichoderma spp. could be isolated from
American beech bark, but Alternaria, Aureobasidium, and Epicoccum spp.
were the most common fungi identified. Since this previous study was
conducted in the northeastern United States, variations in species richness
from the present study could be expected. In Canada, the most common
fungi isolated from bark of American beech were Alternaria, Aposphaeria,
Aureobasidium, and Cladosporium spp. (Fernandez and Boyer 1989). In the
current investigation, isolation frequencies compared between healthy and
damaged trees were similar. These results also differed from the two previous
studies where species richness was greater from American beech trees
damaged by insects and Nectria canker than healthy ones (Cotter and
Blanchard 1982, Fernandez and Boyer 1989). In those studies, however,
similar fungal microflora occurred on damaged trees as was found in the
current investigation.
Trichoderma was the most common genus identified during this study.
Trichoderma spp. are ubiquitous, occurring in soil, on roots or on aboveground
parts of plants (G. Samuels-USDA/ARS, unpubl. guide to Trichoderma).
Species within the genus are commonly found sporulating on moist
wood and other environments in a forest ecosystem and are believed to be
anamorphs of Hypocrea spp. (Chaverri and Samuels 2003). A study with
Theobroma gileri L. (cocao trees) reported that Trichoderma spp. commonly
occur as endophytes in trunks (Evans et al. 2003). In that study, several of
the endophytic Trichoderma spp. evaluated in vitro were found to be antagonistic
to pathogens of cocao. Previous studies reported that Trichoderma
spp. have antifungal or plant-growth-stimulating potential and are being
tested or used as biological control agents (Chaverri and Samuels 2003).
Trichoderma species are also known to be cellulose-degrading fungi, that
rapidly colonize dying and dead plant tissues (bark) until their depletion
(Harman 2000). This depletion would be expected to limit growth of other
microorganisms. Even though Trichoderma frequencies were higher on
damaged American beech trees, control of N. coccinea var. faginata was not
evident. Trichoderma spp. may be operating as opportunists degrading dying
and dead tissue following invasion by the pathogen.
A rarely isolated fungus, Thysanophora canadensis Stolk and Hennebert,
occurred only on Eastern hemlock. Ellis (1971) reported that T. canadensis
was only found on Tsuga in Canada. The potential loss of the eastern
hemlock throughout Canada and the eastern United States, may also result in
the loss or extinction of T. canadensis.
2007 R.E. Baird, C.E. Watson, and S. Woolfolk 75
Microenvironmental variation that occurs within and among different
microhabitats affects species richness and diversity (Stephenson 1989). The
position of bark samples from each tree affected the isolation frequency of
microfungi during this investigation. Bark samples taken at 0.9 and 1.2 m
had significantly greater percentages of fungi than at 0.3 and 0.6 m. A
previous study surveying myxomycetes showed that aerial leafy litter (1.5–
2.5 m above the ground) had greater species diversity and frequencies than
the substratum of the forest floor (Schnittler and Stephensen 2000). It was
suggested that at lower bole positions, increased moisture levels inhibit
spore development, dispersal, and germination. Furthermore, it was believed
that increased moisture may enhance colonization of a substrate by parasitic
fungi, reducing the survival of other species at lower positions on a tree
(Alexopoulus 1970, Stephenson et al. 2004). In this study, the bark from the
lower sampling points may have received less inoculum dispersal due to
higher moisture levels, resulting in lower fungal populations. In addition, if
moisture levels were greater at the lower bark sampling points, Trichoderma
spp. might be actively growing on the bark surface, thus inhibiting growth
and sporulation of other fungi and reducing species richness. It was uncertain
why the isolation frequencies from the four sampling positions on the
trees varied significantly for the three tree species. It is likely related to
microenvironment factors such as moisture and other parameters such as pH,
but further studies evaluating different microenvironments must be conducted
to clarify the results from the present study.
The similarity of the bark mycobiota between damaged and healthy trees
showed that there is a common group present on American beech, Fraser fir,
and eastern hemlock, even in the presence of exotic pests. Presence of many
Trichoderma spp. on American beech bark did not appear to provide natural
biological control of N. coccinea var. faginata. Potentially, when N.
coccinea var. faginata becomes established on American beech, the pathogen
grows into the inner bark and phloem where other fungi do not actively
grow. When this occurs, control of the pathogen by Trichoderma spp. would
be minimal and insufficient to prevent girdling of the trees. Isolation frequencies
of Penicillium spp., which are ubiquitous in soil, decaying vegetation,
seeds or wood (Pitt 2000), varied across tree species, damaged or
healthy, with no apparent trends being observed during the study.
The results of this and previous studies suggest that a common
mycobiota of Deuteromycota occur on bark of temperate trees (Cotter and
Blanchard 1982), and the majority of species identified occurred across the
three tree species. Even though frequencies of fungi differed at four sampling
points on trees, genera and species of fungi were similar. Furthermore,
trees damaged by one of the exotic pests did not contain a different level or
diversity of microfungi than healthy trees during the investigation. It is well
known that cultural methods for isolating fungi limit the accuracy of species
richness due to selectivity. Therefore, molecular methods appear to have the
greatest potential for maximizing species richness determination for future
ATBI investigations.
76 Southeastern Naturalist Vol. 6, No. 1
Acknowledgments
I would like to acknowledge Discover Life in America for providing research
support both years of the study under Project Numbers GSM # 2003-01 and GSM #
2004-01. Also, thanks go to Chelsey Wilson and Becky Reed for laboratory support
during the investigation.
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2007 R.E. Baird, C.E. Watson, and S. Woolfolk 79
Appendix 1. Mean percent occurrence of fungi from bark of American beech, Fraser fir and eastern hemlock from the Great Smoky Mountains
National Park.
2003 2004
A. Beech F. Fir E. Hemlock A. Beech F. Fir E. Hemlock
Taxa DA H DHDHDHDHDH
Fungi imperfectiB
Acremonium crotocinigenum (Schol-Schwartz) W. Gams 0.0C 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.7 0.0
Alternaria tenuissima (Kunze:Fr.) Wiltshire 0.0 0.0 0.0 1.7 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Aspergillus niger Tiegh. 0.0 0.0 0.0 0.0 1.7 0.0 0.0 0.0 0.0 0.0 0.0
Aureobasidium pullulans (deBary) G. Arnaud 0.0 5.0 0.0 0.0 3.3 0.0 1.7 5.0 5.0 0.0 0.0 0.0
Botrytis cinereaB Pers.:Fr. 3.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Botryoderma sp. Papendorf & Upadhyay 1.7 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Botryosphaeria sp. Ces. & De Not. 3.3 3.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Botryodipodia sp. (Sacc.) Sacc. 0.0 1.7 0.0 0.0 1.7 1.7 0.0 3.3 0.0 0.0 0.0 0.0
Calcarisporium arbuscula Preuss 0.0 1.7 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Candida guilliermondii (Castellani) Langeron & Guerra 0.0 0.0 0.0 0.0 0.0 0.0 3.3 1.7 5.0 0.0 0.0 0.0
Coryneum stromatoideum (Dearn.) Sutton 0.0 0.0 0.0 0.0 5.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Cephalosporium sp. Corda. 5.0 1.7 0.0 0.0 0.0 0.0 6.7 8.3 8.3 3.3 3.3 0.0
Chaetomella oblonga Fuckel 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 3.3 3.3 0.0
Cladosporium herbarumB (Pers.:Fr.) Link 1.7 0.0 0.0 1.7 0.0 0.0 3.3 8.3 6.7 1.7 0.0 0.0
Curvularia lunata (Wakk.) Boedijn. 15.0 18.2 9.9 1.7 1.7 0.0 6.7 5.0 15.0 11.7 6.7 3.3
C. oryzae Bugnicourt 3.3 0.0 3.3 0.0 1.7 3.3 3.3 5.0 10.0 6.7 5.0 3.3
C. fallax Boedijn. 0.0 1.7 1.7 0.0 0.0 0.0 3.3 8.9 16.7 6.7 5.0 3.3
Curvularia sp. Boedijn. 0.0 0.0 0.0 0.0 0.0 0.0 1.7 0.0 3.3 1.7 1.7 3.3
Dinemasporium strigosum (Pers.:Fr.) Sacc. 0.0 0.0 3.3 1.0 0.0 1.7 0.0 0.0 0.0 0.0 0.0 0.0
Epicoccum nigrum Link 1.7 0.0 1.7 5.0 0.0 0.0 6.7 26.7 3.3 6.7 0.0 0.0
Fusarium equisiti (Corda) Sacc. 28.3 1.7 0.0 0.0 0.0 0.0 1.7 0.0 0.0 0.0 0.0 0.0
F. graminearum Schwabe 8.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
F. lateritium Nees.:Fr. 0.0 0.0 0.0 0.0 0.0 0.0 16.7 25.0 3.3 6.7 0.0 0.0
F. oxysporum Schlechtend.:Fr. 3.3 3.3 5.0 0.0 0.0 3.3 0.0 3.3 0.0 1.7 0.0 0.0
80 Southeastern Naturalist Vol. 6, No. 1
2003 2004
A. Beech F. Fir E. Hemlock A. Beech F. Fir E. Hemlock
Taxa DA H DHDHDHDHDH
Fusarium nivale (Fr.) Ces. 3.3 0.0 3.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
F. solani (Mart.) Sacc. 10.0 1.7 1.7 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
F. sambusinum Fuckel 6.7 0.0 1.7 3.3 0.0 0.0 0.0 0.0 0.0 1.7 0.0 0.0
F. semitectum Berk. & Ravenel 0.0 5.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.7
Fusarium spp. Link:Fr. 11.7 6.7 3.3 6.7 0.0 0.0 20.0 0.0 1.7 3.0 0.0 0.0
Gloeosporium sp.B Desmaz. & Mont. 1.7 0.0 0.0 0.0 1.7 1.7 0.0 0.0 0.0 0.0 0.0 0.0
Hansfordia ovalispora S. J. Hughes 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.7 0.0 0.0 0.0
Haplographium delicatum Berk. & Br. 0.0 0.0 0.0 0.0 0.0 0.0 1.7 0.0 1.7 0.0 3.3 0.0
Hapalosphaeria sp. Syd. in Died. & Syd. 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.7 0.0 0.0 0.0
Hyalodendron lignicola Diddens. 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.7 0.0 0.0 0.0 0.0
Humicola spp. Tragen. 1.7 0.0 0.0 0.0 0.0 3.0 3.3 0.0 0.0 0.0 0.0 0.0
Libertella faginea Desmaz. 5.0 0.0 0.0 0.0 0.0 0.0 0.0 1.7 0.0 0.0 0.0 0.0
Melanconium atrum Link 1.7 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Memnoniella echinata (Rivolta) G. Sm. 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 3.3 1.7 0.0
Monochaetia concentrica (Berk. & Br.) Sacc. 5.0 5.5 6.0 3.8 2.5 9.5 0.0 0.0 0.0 0.0 0.0 0.0
Nigrospora sphaerica (Sacc.) E. Mason 8.3 10.0 11.7 10.8 3.3 1.7 6.7 15.0 3.3 3.3 0.0 1.7
Nodulisporium spp. G. Preuss 0.0 3.3 1.7 0.0 15.0 6.7 0.0 0.0 0.0 0.0 0.0 0.0
Paecilomyces sp. Bainier 0.0 0.0 0.0 0.0 0.0 5.0 0.0 0.0 0.0 0.0 1.7 0.0
Papulospora sepedonioidesB G. Preuss 3.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Penicillium spp. Link:Fr. 5.0 13.3 23.0 30.0 33.0 30.0 0.0 1.7 8.3 0.0 8.3 0.0
Penicillium oxalicum Currie & Thom 1.7 1.7 5.0 1.7 28.3 16.6 1.7 1.7 0.0 0.0 10 6.7
P. lividum Westling 0.0 3.3 1.7 0.0 15.0 6.7 1.7 3.3 8.3 5.0 5.0 3.3
P. arenicola Chalabuda 0.0 0.0 0.0 0.0 5.0 0.0 0.0 1.7 8.3 0.0 8.3 0.0
P. islandicum Sopp. 0.0 0.0 0.0 0.0 0.0 1.7 0.0 1.7 0.0 0.0 5.0 3.3
Penicillium sp. A 0.0 1.7 0.0 0.0 10.0 0.0 0.0 0.0 5.0 0.0 1.7 3.4
Periconiella verrucosa E. Stewart & M. corden 0.0 0.0 0.0 0.0 0.0 0.0 3.3 3.3 0.0 0.0 0.0 0.0
Pestalotia clavipora (Atk.) Steyaert 15.0 18.0 0.0 0.0 5.0 15.0 15.0 10.0 0.0 0.0 10.0 20.0
2007 R.E. Baird, C.E. Watson, and S. Woolfolk 81
2003 2004
A. Beech F. Fir E. Hemlock A. Beech F. Fir E. Hemlock
Taxa DA H DHDHDHDHDH
Pestalotia funerea (Desmaz.) Steyaert 0.0 0.0 12.3 7.0 0.0 0.0 0.0 0.0 3.3 1.7 0.0 0.0
Phialophora verrucosa Medlar 0.0 0.0 0.0 0.0 0.0 0.0 1.7 5.0 1.7 1.7 6.7 3.3
Phoma dura Sacc. 5.0 1.7 0.0 0.0 3.3 0.0 0.0 6.2 0.0 0.0 0.0
Phomopsis occultra (Sacc.) Traverso 0.0 0.0 0.0 0.0 1.5 0.0 0.0 0.0 0.0 0.0 0.0 0.0
P. diachenii Sacc. 1.7 5.0 0.0 0.0 0.0 0.0 0.0 1.7 0.0 0.0 0.0
Pithomyces atro-olivaceous (Cooke & Harkn.) M. B. Ellis 0.0 0.0 0.0 1.7 0.0 3.3 0.0 0.0 1.7 0.0 0.0 0.0
Pleospora sp. Rabenh. ex Ces. & De Not. 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 13.3 0.0 0.0
Rhinocladiella atrovirens Nannf. in Melin & Nannf. 0.0 0.0 0.0 0.0 0.0 0.0 1.7 0.0 1.7 0.0 0.0 0.0
Rhizoctonia (CAG) D.C. 1.7 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Scolicosporium macrosporium (Berk.) Sutton 0.0 0.0 0.0 0.0 0.0 1.7 0.0 0.0 0.0 0.0 0.0 0.0
Septonema faciculare (Corda) S. J. Hughes 0.0 0.0 6.7 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Sphaeropsis sapineab (Fr.:Fr.) Dyko & Sutton in Sutton 0.0 1.7 0.0 13.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Sporothrix schenckii Hektoen & Perkins 0.0 0.0 0.0 0.0 0.0 0.0 1.7 0.0 0.0 0.0 0.0 0.0
Stigmella sp. Lév. In Demidoff 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.7 0.0 0.0 0.0 0.0
Stillbospora sp. Pers. ex Mérat. 0.0 0.0 0.0 1.7 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Thysanophora canadensis Stolk & Hennebert 0.0 0.0 0.0 0.0 0.0 3.3 0.0 0.0 0.0 0.0 10.0 0.0
Trichoderma spp. Pers.:Fr. 25.0 48.3 38.3 43.3 48.3 66.7 0.0 0.0 0.0 1.7 3.3 8.3
T. aggressivum Samuels & W. Gams 0.0 0.0 0.0 0.0 0.0 0.0 25.0 17.5 13.3 25 26.7 21.7
Trichoderma atroviride P. Karst. 0.0 0.0 0.0 0.0 0.0 0.0 6.7 7.5 8.3 10.0 11.7 13.3
T. aureoviride Rafai 10.0 13.0 0.0 11.7 23.3 16.7 33.3 8.3 31.7 15.0 26.7 35.0
T. cremeum Chaverri & Samuels 0.0 0.0 0.0 0.0 0.0 0.0 8.3 22.5 6.7 16.7 15.0 15.0
T. ghanense Y. Doi, Y. Abe & J. Sugiyama 0.0 0.0 0.0 0.0 0.0 0.0 6.7 15.0 15.0 16.7 20.0 13.3
T. koningii Oudem. 3.3 13.3 1.7 10.0 15.0 18.3 30.0 31.7 30.0 11.7 31.7 21.7
T. hamatum (Bon.) Bain. 6.7 13.3 6.7 20.0 13.3 5.0 10.0 15.0 21.7 21.7 38.3 25.0
T. harzianum Rifai 15.0 20.0 25.0 21.7 15.0 0.0 38.3 20.0 38.3 45.0 48.3 58.3
T. polysporum (Link:Fr.) Rifai 0.0 0.0 0.0 0.0 0.0 0.0 7.5 7.5 7.5 7.5 8.3 5.0
T. strigosum Bissett 0.0 0.0 0.0 0.0 0.0 0.0 15.0 5.0 2.5 5.0 5.0 7.5
82 Southeastern Naturalist Vol. 6, No. 1
2003 2004
A. Beech F. Fir E. Hemlock A. Beech F. Fir E. Hemlock
Taxa DA H DHDHDHDHDH
Trichoderma virens (J. Miller et al.) Arx 0.0 0.0 0.0 0.0 0.0 0.0 18.3 23.3 25.0 11.7 33.3 6.7
T. viride Pers.:Fr. 0.0 1.7 0.0 0.0 0.0 0.0 21.7 18.3 26.7 33.3 48.3 51.7
Trichoderma sp. A 0.0 1.7 0.0 0.0 0.0 0.0 15.0 0.0 0.0 0.0 0.0 0.0
Truncatella sp. Stey. 5.0 6.5 5.0 4.2 4.2 6.5 0.0 0.0 0.0 0.0 0.0 0.0
Verticillium sp. Nees. 0.0 0.0 0.0 1.7 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Virgaria nigra (Link) Nees. 0.0 0.0 0.0 1.7 0.0 0.0 25.0 28.3 13.3 3.3 3.3 1.7
Ascomycetes
Chaetomium spirale Zorf 3.3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.7
Gelasinospora tetrasperma Dowding 1.7 3.3 5.0 1.7 0.0 0.0 3.3 0.0 0.0 10 0.0 0.0
Nectria coccinea var. faginata (Lohman, A.M. Watson & Ayers)0.0 1.7 0.0 0.0 0.0 0.0 3.3 1.7 0.0 0.0 0.0 0.0
Other spp. 0.0 0.0 0.0 1.7 1.7 3.3 0.0 0.0 0.0 0.0 1.7 0.0
Zygomycetes
Cunninghamella sp. Matr. 0.0 0.0 0.0 8.3 0.0 0.0 0.0 0.0 0.0 0.0 1.7 0.0
Mucor microsporus Naumov. 0.0 0.0 0.0 0.0 1.7 0.0 0.0 0.0 1.7 0.0 0.0 0.0
Mortierella sp. Coem. 0.0 0.0 1.7 0.0 0.0 0.0 0.0 1.7 1.7 6.7 0.0 0.0
Rhizopus arrhizus A. Fisher 0.0 0.0 0.0 1.7 0.0 1.7 3.3 3.3 0.0 1.7 0.0 0.0
R. monosporus Tiegh. 0.0 0.0 0.0 1.7 0.0 0.0 0.0 0.0 1.7 0.0 0.0 0.0
R. solonifera (Ehrenb.:Fr.) Vuill. 0.0 0.0 1.7 2.4 3.3 1.7 3.3 6.7 0.0 3.3 0.0 0.0
Rhizopus sp. Ehrenb. 0.0 0.0 0.0 0.0 0.0 0.0 1.7 0.0 0.0 0.0 1.7 0.0
Basidiomycetes 0.0 5.0 1.7 5.0 5.0 3.3 0.0 3.3 3.3 11.7 1.7 0.0
Unknowns 2.0 1.0 0.0 0.0 3.3 0.0 10.0 18.3 10.0 15.0 6.7 0.0
AD = damaged bark from infected/infested trees, H = bark from healthy trees.
BPetersen, R. 1979. Checklist of fungi GSMNP, Management Report # 29.
CPercent occurrence is based on isolation of a fungus from 60.0 bark samples per year covering 3 sampling dates, 5 replicate trees (infested or
damaged), and 4 pieces per replicate tree.