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Vertical distribution and assemblages of corticolous myxomycetes on five tree species in the Great Smoky Mountains National Park

     Department of Biology, Central Missouri State University, Warrensburg, Missouri 64093

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

Corticolous myxomycetes of the Great Smoky Mountains National Park were studied in relation to their association with certain tree species and height of occurrence in the forest canopy. Using the double-rope climbing method, bark was collected at 3 m increments to the tops of trees of five different species. Bark samples from 25 trees were used to prepare 418 moist chamber cultures maintained and observed 4 wk. Eighty-four myxomycete species were identified, including 30 species not known to occur in the park. Tree species, pH, height in tree and water-holding capacity of the bark samples were analyzed to determine the relationships of myxomycete assemblages cultured on the bark. Results suggested that myxomycete community composition among selected tree species were similar, but occurrence and abundance of certain species were related to differences in bark pH. Community similarity values among trees of different species show that trees with the most similar myxomycete communities also have the most similar bark pH. Most myxomycete species in this study have a pH optimum. No variation in species richness was detected at different heights in the trees, and most species were obtained at all heights up to at least 24 m. The water-holding capacity of the bark could not be correlated with species richness or abundance of myxomycetes that inhabit the bark of living trees. This is the first study to characterize myxomycete communities of tree canopies.

Key words: bark, ecology, Great Smoky Mountains National Park, Mycetozoa, Myxomycetes, tree canopy, tree climbing

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Myxomycetes, or the true slime molds, are phagotrophic eukaryotes typically found on moist decaying plant matter and in the soils of most terrestrial ecosystems. These organisms are not classified with the decomposers of these habitats, such as the true fungi, because they feed primarily on bacteria, spores and other living microscopic organisms (Olive 1975). Most myxomycete studies have centered on systematics; although brief notes on ecological factors such as substratum preference were included in many of these studies, basic ecological research on myxomycetes has only begun in the past few decades (Eliasson 1981, Stephenson 1988).

Myxomycetes have a life cycle in which both the haploid and diploid phases are mobile, actively feeding stages (Gray and Alexopoulos 1968). Haploid spores germinate under moist conditions, releasing tiny amoeboid cells called myxamoebae. Compatible myxamoebae or swarm cells serve as sexual gametes that eventually fuse to form a diploid zygote. The zygote undergoes repeated and synchronous mitotic nuclear divisions without cytokinesis. The resulting multinucleate stage, called the plasmodium, develops into one or more fruiting bodies in which meiosis will produce the haploid spores (Gray and Alexopolous 1968).

Various resting stages of the life cycle are capable of surviving long periods in a dormant state. Sclerotia are resting structures produced from the plasmodial stage of the life cycle in response to adverse environmental conditions. Sclerotia may revive and complete their cycle after several years of dormancy (de Bary 1887). Dry spores are protected by a cell wall and may remain from months to 75 years in a dormant resting state, depending on the species (Erbisch 1964). Even the myxamoebae can form thin-walled, resting structures called microcysts when subjected to periods of desiccation. Although more sensitive to desiccation, these microcysts can revive and complete the life cycle, sometimes after a year of dormancy (Gray and Alexopolous 1968). Each of these three structures represents a possible resting stage for each particular phase of the life cycle, increasing the chances for successful cultures after the removal of bark samples from the field. Sclerotia in particular are the source of the rapid appearance of fruiting bodies in moist chamber culture, some maturing in 24 to 48 h.

Relatively little fieldwork has been conducted on the myxomycetes of the Great Smoky Mountains National Park. The four papers that specifically refer to myxomycetes in the park consist only of collection lists of park records. 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). Welden (1951) added 21 species to the park records, and a recent list by Stephenson et al (2001) added 75 more. Previous studies of myxomycetes in the park concentrated on the taxonomy and identification of collections from ground sites and from trees up to 2 m high on the trunk.

Myxomycete ecology and distribution in the past emphasized records of collections and species lists. More recently, distribution patterns based on a number of variables, including forest types (e.g., Stephenson 1988, Schnittler and Stephenson 2000, Novozhilov et al 2001), geography (Schnittler et al 2000) and substrata (Stephenson 1989, Schnittler and Stephenson 2002) were described. Stephenson (1989) compared species richness and diversity of corticolous myxomycetes on 15 species of trees in southwestern Virginia. He also compared species assemblages of myxomycetes occurring on five tree species in spruce fir forests in the southern Appalachians (Stephenson 1983).

The bark of living trees long has been known to be a suitable substratum for many species of myxomycetes. The first documented collections of myxomycetes from living trees were those of the Rev. William Cran, a Scottish teacher and amateur slime mold enthusiast. Between 1883 and 1918, Cran collected myxomycetes from bark and other substrata (Lister 1938). Gilbert and Martin (1933) collected bark from living trees to demonstrate to their classes the growth of algae in moist chamber cultures and discovered the development of mature, identifiable myxomycete sporangia. This accidental discovery resulted in the description of several new myxomycete species, and since that time nearly all researchers in the field have employed moist chamber cultures. Keller and Brooks (1973) used the term "corticolous myxomycetes" to describe those species that grow and fruit on the bark surface of living trees and vines.

Keller and others (e.g., Keller and Brooks 1976, 1977, Keller 1980, Keller et al 1988) have noted that certain myxomycete species nearly always are associated with living trees and rarely occur on decaying wood or leaves on the ground. Specificity to living trees was noted by Ing (1997), who went so far as to categorize corticolous myxomycetes as either "obligate corticoles," "facultative corticoles" or "casual corticoles." Obligate corticoles are those species rarely found on any other substratum, and casual corticoles are thought to be accidental species on living trees that normally occur on other substrata. It is not clear how this microhabitat on living trees differs from typical ground sites of decayed wood and leaf litter, but corticolous species tend to complete their life cycle in a shorter span of 24 to 72 h (Keller and Brooks 1976).

Few myxomycologists have compared the assemblages of corticolous species found at different heights and on different tree species. Peterson (1952) conducted a limited analysis of myxomycete diversity at three different heights. Peterson collected bark from near the base, at 1.2 and 2.4 m high on a number of trees, partly to determine the difference in abundance of myxomycetes at those heights. Härkönen (1977) sampled bark from living trees below 1.5 m and compared tree species, forest type and pH of substratum, with the frequency of occurrence and species of myxomycetes in Finland. Some researchers have studied the myxomycetes that grow on a single tree species (McHugh 1998, Wrigley de Basanta 1998) from ground level to 1.5 m in height. Chopra (1984) compared the myxomycetes at three different heights (3, 6 and 9 m) on three tree species.

This study is concerned with answering three questions regarding the distribution of myxomycetes that inhabit bark. First, are there consistent assemblages of tree species-specific myxomycetes or are most species opportunistic as to the particular substratum? Second, is there a difference in the number of species found at different heights on the same tree species? Third, do bark pH and water-holding capacity affect the myxomycete assemblages that are associated with the bark of living trees (Snell 2002).

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Study area – Great Smoky Mountains National Park was selected for this study because of its favorable climatic conditions and diverse habitats, characterized by high plant and fungal diversity. The park stradles the boundary between eastern Tennessee and western North Carolina between 35° 28' and 35° 47' N latitude. It includes 210 566 ha, 40 000 of which are old-growth forest. These are the largest tracts of old-growth forest remaining in the eastern United States. Elevations range from 263 m to 1994 m. Moderate temperatures, ranging from 4 to 23 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. The Smokies are home to a variety of forest types, including spruce fir, northern hardwood, pine, oak, hemlock and cove hardwood (Whittaker 1956). In addition, these forests harbor more than 130 species of trees, more than 1800 plant species and more than 2200 fungi. The high canopy of the old-growth forests allowed for collection from a great range of heights, occasionally to more than 40 m above the forest floor. A total of 240 trees representing 35 different tree species were climbed during June 19 to July 6 and July 31 to August 17, 2000, and June 9 to June 28 and July 22 to August 9, 2001. Our tree climbing was concentrated along the northern boundary of the park.

Tree canopy definition – 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 liverworts, support myxomycete plasmodia and fruiting bodies that are more typical ground-site species, such as Lycogala flavofuscum. This assemblage of myxomycete ground-site species at the base of trees occurs below 2 m (Keller and Braun 1999).

Field methods – Five tree species were selected for their upper canopy heights and bark texture (typically absorbent and ridged), as well as the fact that each represented a different family: Acer rubrum (red maple, Aceraceae); Fraxinus americana (white ash, Oleaceae); Liriodendron tulipifera (tulip poplar, Magnoliaceae); Pinus strobus (eastern white pine, Pinaceae); and Quercus alba (white oak, Fagaceae). Other studies have shown that Quercus and Acer harbor a wide diversity of myxomycetes (Stephenson 1989, McHugh 1998) and our preliminary culture work and the experience of Keller and Braun (1999) suggested that the myxomycetes found on trees of the other three genera would be rich in species. 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 27 m in height and allowed sampling from 3 m continuously to near the top. Tree selection was limited by climbing hazards, such as poison ivy, dead branches or limb structure.

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 to 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 or 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 the bark. The double-rope technique also lets the climber advance the rope to higher branches, often reaching to near the top of the tree (Jepson 2000, Counts et al 2000).

Bark was sampled at ca 3 m increments as the climber advanced. Bark was scraped or pried from the trunk with a large knife, taking care not to damage the underlying tissues. Efforts were made to sample from all sides of the trunk and some upper branches, although no distinction was made as to the specific area or aspect sampled. All samples were collected from living parts of the tree, placed in paper bags (approximately 1000 cm³) until half-filled and labeled with the height and tree number in each instance. Wet samples were air-dried for storage and packed together by tree. 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. Elevation lines, marked off in feet from the ground, were carried by each climber for accurate collection and tree measurements. Trees were tagged with numbers, and Global Positioning System (GPS) readings were taken for each climbing site. In addition, a site description, including most recent rain and current weather conditions, was recorded.

Laboratory methods – A second phase of tree selection took place before bark culturing. Five trees were chosen for each of the five species to be used in the study. Trees selected were all more than 23 m in height, with bark samples taken at every 3 m increment. Attempts were made to select trees of the same species from different areas to better represent the entire park and to avoid the problem of opportunist species dispersing to nearby trees.

Myxomycetes were cultured from bark using the moist chamber technique described by Keller and Braun (1999). Moist chambers consisted of large sterile Petri plates (150 x 25 mm), each fitted with a single sheet of P8-creped filter paper that covered the bottom. Bark was placed face up on the paper in a single layer, covering the bottom of the Petri dish. 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 h, any unabsorbed water was decanted and the pH of each culture was measured with an Orion model 610 flat probe pH meter. Plates were kept moist without any standing water, at room temperature (22–25 C) in indirect natural light. Cursory scanning of fresh cultures was conducted for each plate to check for existing fruiting bodies.

Bark samples from a particular tree were prepared at the same time. Two plates from each height were prepared, resulting in approximately equal treatments for each height. Some samples from the tops of trees were sparse and would fill only one plate. Tree number, sample height and initial wet date were recorded for each culture.

Each plate was examined every 7–10 days, starting 24–48 h after wetting. All cultures were examined an equal number of times using a dissecting stereomicroscope with a low heat, fiber-optic light source. Mature fruiting bodies were removed from the bark as small pieces to reduce disturbance of the sample. Fruiting bodies were glued to small cards labeled with the tree number, height, wet date and harvest date. Cards from the same height were glued into small boxes for later identification. Each plate remained moist 4 wk and then was allowed to dry. A final scanning was performed after plates dried to search for any remaining fruiting bodies on the surface and underside of the bark. Although some researchers (e.g., Stephenson 1989, McHugh 1998) have let plates remain wet for much longer periods, we limited the culture to 4 wk to reduce the problem of noncorticolous species that would not grow naturally on the bark. According to Ing (1998), "casual corticoles" often develop much later than species adapted to living on bark. During preliminary culture work for this study, plates kept longer than a month produced several myxomycete species known only from ground sites but not known to fruit on living trees. In this study, we were interested only in corticolous myxomycetes (sensu Keller and Brooks 1973), those species that grow and fruit naturally on living trees.

Species identification and nomenclature follows that of Martin and Alexopolous (1969) and Keller and Braun (1999). Lists of identified species collected from each height of each tree were compiled and compared.

Water-holding capacity of the bark was determined by drying a remaining, uncultured portion of the bark from each tree at 90 C in an oven until it had reached a constant weight over time. Samples included a mixture of bark from each collected height. Samples typically took 8 h to reach a constant weight. Each sample was weighed and placed in a separate resealable plastic bag and wetted with approximately 1 L of distilled water, ensuring that all bark was directly exposed to the water. After 18 h, the water was drained off and the bark was placed on paper towels to remove excess moisture. Wet samples were weighed, and the percentage of water to the weight of dry bark was calculated.

Data analysis – Myxomycete assemblages identified from the cultured bark of each tree were compared using the Sørensen coefficient of community index (CC), which is a widely employed similarity index that might be more mathematically sound than its original form as proposed by Jaccard (Mueller-Dombois and Ellenberg 1974). This is because Sørenson's index expresses the actually measured coinciding species occurrences against the theoretically possible ones. The equation is based on the presence or absence of species in two communities: CC = 2c/(a + b), where a = total number of species in the first community, b = total number of species in the second community, and c = number of species both communities have in common. Other researchers have used this index to compare myxomycete community similarity among different study regions (Stephenson 1988, 1989, Novozhilov et al 1999). Individual trees of the same species were compared first in pairwise fashion, resulting in 50 combinations. This was followed by the 250 community comparisons among trees of different species.

Analysis of height variations was limited to same-tree species comparisons. Myxomycete species richness for each height on each tree was compared to species richness at different heights for all five trees of the same species. Comparisons of all data (species richness, CC, height distribution, pH, and water-holding capacity) were tested for normality using the chi-square analysis and for homogeneity using Bartlett's analysis, both at the = 0.01 level. A parametric analysis of variance (ANOVA) was used only if data passed both normality and homogeneity tests. Tukey's method of multiple comparisons was used at the = 0.05 level. If data did not pass normality and homogeneity tests, they were analyzed with the Kruskal-Wallis non-parametric ANOVA at the = 0.05 level. Means of datasets in the text are reported with standard deviation values (±SD). Mean pH was derived by the conversion of pH values to their appropriate hydrogen ion concentrations. These concentrations were used to calculate the mean and converted back to pH units.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
For the purpose of this study, the term "site" will indicate a particular height on a specific tree, with each represented by two moist chambers. A total of 418 moist chamber cultures, representing 209 sites, yielded 84 species of myxomycetes representing 24 genera, with an additional 10 taxa identified only to genus. Every site produced at least one identifiable species, with an average of 6.0 ± 2.6 species per site. In total, 1231 collections were gathered. Thirty-six percent (30) of the identified species were found only on one of the 25 trees, and 17% (14) were found only at a single site. The two species most commonly collected were Echinostelium minutum and Arcyria cinerea. Echinostelium minutum occurred on 21 trees and at 125 sites, making it considerably more common than any other species. Echinostelium minutum was also one of the first to produce sporangia in moist chamber cultures. Arcyria cinerea was collected on 22 different trees at 91 sites. Arcyria cinerea, Badhamia rugulosa, Comatricha ellae, Diderma chondrioderma, Echinostelium minutum, Licea kleistobolus and Physarum nutans were collected on all five species of tree. Common species are summarized in Table I.

Pinus strobus showed the highest mean CC (0.62 ± 0.12) values. Only P. strobus CC values were significantly different from those of other species. The considerably higher values for P. strobus communities to one another compared to those of the other trees are partly the result of a lower incidence of uncommon species and partly due to the presence of a group of species that consistently occurred on P. strobus. Seven species—Arcyria cinerea, Comatricha ellae, Cribraria confusa, Cribraria minutissima, Echinostelium minutum, Enerthenema papillatum and Physarum nutans—all occurred on at least four of the five P. strobus trees. Only eight of the 24 (33%) identified species on P. strobus were found on one tree.

Acer rubrum, which produced 20 more total species than F. americana, had very similar CC values to those trees. Eight of the species on A. rubrum–Arcyria cinerea, Comatricha ellae, Cribraria confusa, Cribraria violacea, Diderma chondrioderma, Echinostelium minutum, Physarum nutans and Trichia botrytis—occurred on at least four of the five trees. This considerable number of repeats was offset by 30 species found only on one A. rubrum tree, which represented 61% of the total species collected on those trees. Liriodendron tulipifera and Q. alba had similar mean CC values, 0.49 ± 0.07 and 0.50 ± 0.07, respectively, as well as having nearly the same total number of species and species per-tree. Community relationships among trees of the same species are illustrated in Figs. 1–5.

View larger version (36K): [in this window] [in a new window]   FIGS. 1–5. Mean community coefficient (CC) values comparing communities of myxomycetes on different species of trees. Black bars = comparisons of myxomycete communities on the same species of tree. White bars = significant difference (p < 0.05) between CC values of same tree comparisons vs. communities on different tree species. Gray bars = no significant difference

Vertical distribution – To determine if any trends exist in the data for the numbers of species occurring at different heights in the trees, species per height data were compared among individual trees of the same species. If upper-height data were available only for three or fewer trees in the groups of five, they were excluded from the analysis (for example, if only one of the five P. strobus trees had bark from 30 m, those cultures were omitted from analysis). This sampling disparity comes from the fact that it was possible to sample some trees to a greater height than others.

There was no significant difference (p < 0.05) among the number of species cultured at different heights on any of the tree species. It is interesting to note though that Diderma chondrioderma was never found lower than 6 m, although it was cultured at 27 different sites.

pH – pH values were analyzed to test for differences among trees of the same species, and pooled values of pH for each species were compared to test for differences in pH among species. The range of pH values for bark from the same tree and among trees of the same species showed some variation, but in general, the mean pH values for trees of the same species in this study were consistent overall. The bark from one tree each of Q. alba and P. strobus was significantly different (p < 0.05) from three other trees of the same species. Individual trees of the other species were consistent in the pH of their bark. Bark of P. strobus was significantly more acidic, with an overall mean of 3.8 ± 0.36, than that of any other species. Fraxinus americana had the highest overall pH of 6.7 ± 0.35, but this species was not significantly different (p < 0.05) from Q. alba (5.7 ± 1.03). Mean pH values per tree are summarized in Table III.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
A surprising number of species were cultured from the bark in this study, adding credence to Hagelstein's (1940) statement that the park might be the best region for mycetozoans in the eastern United States. Several species rarely if ever before known to inhabit the bark of living trees appeared regularly in culture. Some may be opportunist species that grew in moist chamber and do not normally mature on trees in nature, but a few unanticipated species were found on the trees during collection in the field and others appeared in culture so frequently that it would seem they naturally occur on those trees.

Mature fruitings of Hemitrichia serpula and Trichia favoginea were obtained 18 m above the ground during the collection phase of this study, and both were cultured later in moist chamber. These species are typically found on well-decayed logs and fallen branches (Martin and Alexopolous 1969). Trichia botrytis usually is reported on dead logs, but this species was common on the cultured bark of A. rubrum and L. tulipifera trees at all heights. This species also was found on the bark before it was cultured. Collaria arcyrionema was collected from culture at 15 different sites, mostly on the bark of F. americana. Other less frequently occurring species, not typically associated with living trees, included, Arcyria incarnata, A. insignis, Diderma hemisphaericum, Lycogala exiguum, Metatrichia vesparium, Stemonitis fusca and S. smithii.

One hypothesis for this unexpected group of species is the advanced age and size of most of the trees sampled for this study. Because bark is dead tissue, subject to slow decay even while attached to the trees, it might begin to resemble the microhabitats inhabited by ground species. Much of the sampled bark on the older trees was attached very loosely and in various stages of decay, similar to the bark inhabited by ground species on decaying logs.

The preponderance of a few common species was consistent with several other studies of corticolous myxomycetes. Echinostelium minutum often is reported in the United States as the most abundant species on bark (e.g., Peterson 1952, Stephenson 1983, 1989), and Arcyria cinerea also is common in these types of studies (Härkönen 1977, Stephenson 1989, McHugh 1998). Of note are the 30 species never before recorded from the park. Most of these rarely were encountered in this study, but 13 were identified on at least two separate trees. One is an undescribed species of Diachea, cultured on two trees from this study and from several other trees in the park. Stephenson et al (2001) compiled all known records for the park before this study, with a combined total of 168 taxa. To this list we add 30 species.

Species richness of A. rubrum, Q. alba and L. tulipifera were nearly identical when viewed as average species per tree. This was consistent with Stephenson's study (1989) in southwestern Virginia, where high numbers of species were obtained for Q. alba and A. rubrum. The genus Quercus repeatedly has been shown to support some of the most diverse assemblages of myxomycetes (Stephenson 1989, McHugh 1998, Wrigley de Basanta 1998, Keller and Braun 1999). Individual trees of the same species varied considerably as a substratum for myxomycetes. Each same-species group of five trees contained one tree whose cultures produced about half the number of species as the most productive tree. This degree of variability, coupled with the similarity of communities among tree species, seems to indicate that bark factors are outweighed by other extrinsic factors in the overall quality of microhabitat for myxomycetes.

Myxomycete communities occurring on the bark of the same tree species in general were similar to those occurring on trees of different species. Communities on certain trees of the same species had few similarities with one another, while some of the greatest individual similarities between communities were found to occur for trees of different species. The notable exception to this pattern was Pinus strobus. These trees consistently shared close to half of the same species with one another and considerably fewer with trees of other species. Pinus strobus was the only species that had mean community coefficient values that were significantly different (p < 0.05) from those of the other tree species when compared to the similarity that P. strobus communities had with one another. Pinus strobus in this study supported a more consistent and somewhat different assemblage of myxomycetes when compared to other trees. Considering that most myxomycete communities showed similar CC values in comparisons among the same-tree species and cross-tree species, it seems that little can be said about the specificity of communities to a particular type of tree. It appears that the myxomycetes common to these trees typically are generalists with little specificity to substratum.

Pinus strobus trees typically have not been studied in work on corticolous myxomycetes. Härkönen (1977) and Peterson (1952) compared overall productivity of coniferous bark to deciduous bark in general. Härkönen found no difference in myxomycete abundance between the two groups of trees, while Peterson showed slightly lower numbers on coniferous trees. Stephenson (1989) reported similar numbers between conifers and deciduous trees, although he did not include Pinus species. Though none of these studies involves community comparisons among trees, there is some agreement with the data in this study that conifers tend to have lower species richness but similar abundance of myxomycetes.

A second examination of community similarity based on the mean CC values (Figs. 1–5) among tree species suggests a possible connection among trees with more similar myxomycete assemblages. Grouping the pairs of most similar myxomycete communities in order—F. americana, Q. alba, L. tulipifera, A. rubrum, P. strobus—places them in order of mean bark pH values. Without exception, trees with the most similar communities also had the most similar bark pH.

The effect of pH differences on the occurrence of certain myxomycetes in the field was discussed by several authors, and some laboratory experiments were carried out to determine approximate pH optima for species grown on artificial media. Emoto (1938), as reported by Gray and Alexopolous (1968), found that, from collections of 106 different species in the field, fruitings occurred most frequently on substrata with a pH between 4.2 and 5.8. It is interesting to note that A. rubrum, the tree species in this study with the highest species richness, also had the mean pH (4.8) that best fits this pH optimum. Smart (1937) also found that an acid medium is more favorable. He conducted experiments on spore germination and found that, of 70 species, a pH between 4.5 and 7.0 was the optimum. Gray (1939) demonstrated that the combination of temperature and pH was important to the fruiting of Physarum polycephalum. He found that at a higher temperature, a lower pH was needed to ensure sporangial formation.

Most field studies that have considered pH as a factor have found that most myxomycetes have a wide pH tolerance, while a few species have more narrow pH optima at which they occur in greater abundance. Härkönen (1977), in her study of corticolous myxomycetes in Finland, stated that Comatricha nigra seems to prefer an acidic substratum while Arcyria cinerea prefers a more basic one. Stephenson (1989) placed even more importance on pH in myxomycete distribution patterns. His data, using the bark of living trees, indicated that members of the order Stemonitales developed under more acidic conditions than did members of the orders Physarales and Trichiales. His data also showed a preponderance of the Stemonitales on conifer bark, which was the most acidic in the comparison of the 15 tree species. Stephenson went on to compare the occurrence of certain species found on bark to that on leaf litter. The pH of both substrata was similar where certain species were abundant. He concluded that pH is an important factor in myxomycete distribution patterns. In a recent study, Schnittler and Stephenson (2002) discovered several species of myxomycetes that clearly exhibit a preference for the high pH of decaying floral parts of certain tropical herbs.

In this study, the two tree species with the least community similarity, P. strobus and F. americana, are at either end of the pH gradient (Table III). In addition, these two species displayed the most interesting variations from the other tree species in community composition. As mentioned before, Cribraria minutissima was found on the bark of four of the five P. strobus trees and on only one of the other 20 trees. Enerthenema papillatum occurred on all five P. strobus trees and on only four of the other 20 trees. Equally interesting are several common species that appeared on all other tree species except pine. These were Calomyxa metallica, Cribraria violacea, Diderma effusum and Perichaena chrysosperma. The genera Macbrideola and Perichaena, in general, were absent from pine, and only one species, Arcyria cinerea, from the order Trichiales, was present.

Fraxinus americana, which had the least-acidic bark, had similar trends of abundance or relative scarcity of other species. Most notable is Echinostelium minutum, which appeared on all 20 of the other trees but only on one white ash. Macbrideola cornea was much more abundant on F. americana than on other tree species. Most of the common species in this study are not evenly distributed in abundance, and their distributions tend to follow the pH gradient among bark types. Table IV compares the abundance of some selected species with the mean pH of trees.

Considering the age and size of most of the trees sampled in this study, the barks of A. rubrum, F. americana, L. tulipifera and Q. alba were similar. These species were chosen largely because they have deeply furrowed, corky-textured bark known to support diverse communities of myxomycetes. The bark of P. strobus typically consists of dense flat plates with less depth between the scales, but the bark of these older trees, in at least the lower third of their height, had rather thick-ridged plates that appear to offer nearly as much surface area as other species. Barkman (1958) referred to lichen and bryophyte cryptogams that are restricted to smooth or rough bark but, considering the typical size of myxomycete fructifications, most individual trees offer a great variety of textures from this perspective of scale. Stephenson (1989) did find some connection between myxomycete abundance and tree genera, attributing some of this to the similar textures of congeneric trees. In this study, it is difficult to evaluate species based on their bark texture aside from P. strobus, but the overall myxomycete occurrence on this bark was slightly higher than that of F. americana, which had a bark similar in texture to the other deciduous trees.

Water-holding capacity of the bark of different trees could not be associated with any other variable in this study. Owing to the fact that myxomycete species richness and abundance among tree species did not vary significantly, it is difficult to place any weight on the minor degree of variability found in this factor. Although P. strobus was shown to harbor a more consistent assemblage of myxomycetes, as well as having a lower water-holding capacity, mean overall abundance of myxomycetes on this species was very similar to that of the other trees. In addition, F. americana, which had a relatively high water-holding capacity, had the lowest number of species per site. Billings and Drew (1938) suggested that the combination of pH and water-holding capacity accounted for most of the variation in the corticolous bryophyte communities in their study.

All common species in this study, along with most other species numerous enough to be considered here, occurred in nearly equal numbers from heights of 3 m up to at least 24 m. This is consistent with Peterson's (1952) rather limited study of vertical distribution, where he concluded that there was no change in abundance higher in the tree.

Conclusions – Myxomycete communities and species distribution among the five species of trees in this study show correlative trends with differences in bark pH. Communities on various trees were composed largely of a common set of species, but a higher degree of similarity in the frequency of those species very often occurred in trees of comparable pH. This trend was reflected in the community coefficient data as well as in the frequency data of individual myxomycete species. A stronger connection possibly could have been made had data been collected for the specific bark from which a species was taken. Although trees of the same species showed a general consistency in pH values, the bark at some heights on individual trees varied considerably. No trends related to the water-holding capacity of the bark or height of the tree were observed in the abundance or assemblages of myxomycetes.

The vertical distribution patterns noted here suggest that the general practice of collecting bark from living trees at a diameter at breast height or at head height represents a sampling technique that will recover the vast majority of myxomycete species cultured in moist chambers. Although many species of corticolous myxomycetes are restricted to living trees and vines, vertical distribution patterns indicate individual and groups of species are not confined to the canopy. Future studies will evaluate pH patterns of distribution for myxomycetes on living tree species known to exhibit high species richness, such as Juniperus virginiana and Taxodium distichum (conifers), Ulmus americana (a broadleaf deciduous tree) and Vitis species (grapevines).

	ACKNOWLEDGMENTS

 
This research project was conducted originally as a master's thesis. We would like to thank Central Missouri State University Graduate School for two awards: first place for the Graduate Student Thesis Award and the Reid Hemphill Outstanding Graduate Scholar Award to Kenneth L. Snell. We also would like to thank James "Buck" Counts, Damon Lesmeister and Melissa Skrabal for their help in making tree-canopy collections and to Charly Pottorff for teaching us how to climb trees. Dr. Jay Raveill identified the trees and Professor Uno Eliasson helped to identify myxomycetes. We are grateful to Drs. Stefan Cairns, Steven L. Stephenson and Steve Wilson for their assistance with the statistics and editorial corrections. Park employee Keith Langdon and Jeanie Hilten of Discover Life in America were important to the climbing and ground crews in the park, helping with access, directions, equipment and lodging. This project was financed by grants from the National Science Foundation (DEB#0079058) and Discover Life in America (#2001-26).

	FOOTNOTES

 
¹ Corresponding author. E-Mail: keller{at}cmsu1.cmsu.edu

Accepted for publication January 17, 2003.

	LITERATURE CITED

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
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