Association between corticolous myxomycetes and tree vitality in Cryptomeria japonica

Abstract

The bark of live trees provides an important microhabitat for corticolous myxomycetes. However, the association between the presence of myxomycetes and health of host trees has not been studied in detail. In this study, we aimed to investigate the relationship between tree vitality and myxomycetes on the bark of Cryptomeria japonica trees in a montane forest in western Japan. The vitality of trees was categorized into four grades based on the visual assessment of tree shape and leaf density in the upper branches. Myxomycetes on the bark surface were examined using the moist chamber culture method. A decline in tree vitality increased bark pH and decreased electrical conductivity of the bark exudates. Seventeen myxomycete species were recorded in 74 C. japonica trees. The structure of myxomycete communities varied between healthy and unhealthy trees, and species diversity increased as the vitality declined. The relative abundance of Cribraria confusa decreased as the vitality declined, while that of Paradiacheopsis solitaria increased. The results showed that acidophilic myxomycetes grew on healthy C. japonica bark, but changes in bark pH associated with vitality decline led to the weakening of acidity and shifted the community structure; thus, corticolous myxomycete diversity was enhanced as tree vitality decline.

1. Introduction

Myxomycetes (kingdom Protista) are common microbes that are primarily found on decaying wood, plant debris, and the bark surface of living trees. They play a role as predators of bacteria and fungi in the detritus food web and have an important function in carbon and nutrient cycling (Stephenson & Rojas, 2017). Myxomycetes found on the bark (corticolous myxomycetes) are a distinct ecological group (Gilbert & Martin, 1933; Keller & Brooks, 1973) and are closely associated with tree species and particular bark traits (Everhart, Keller, & Ely, 2008; Rollins & Stephenson, 2011; Takahashi, 2014; Vaz et al., 2017).

Forests generally consist of different tree species, and they vary in tree size, growth stage, and health conditions, thus providing heterogeneous micro-habitats for corticolous myxomycetes. However, studies on the association between the presence of corticolous myxomycetes and condition of host trees are limited. The bark of Cryptomeria japonica (L. f.) D. Don. trees effects as a habitat for several myxomycete species in the forests of the Japanese archipelago (Takahashi, Harakon, & Fukasawa, 2018). The endemic species, C. japonica, is distributed throughout Japan, and C. japonica plantations account for approximately 45% of the total area of artificial forests in Japan, because it is the main source of timber for construction work (The Forest Agency; https://www.rinya.maff.go.jp/j/sin_riyou/kafun/data.html). Therefore, the health of trees is an important parameter in forestry management. The states of tree growth can be easily observed from the shape of the tree (Yambe, 1978) and visual classifications of tree vitality have been developed, based on the shape of trees and density of leaves and branches (Katoh, Kasuya, Kagamimori, Kozuka, & Kawano, 1991; Kaneko, Hijii, & Futai, 1994; Matsumoto et al., 2002). The relationship between tree vitality and myxomycetes inhabiting the bark surface has not been fully assessed. This is because bark traits that determine preferred microhabitats for corticolous myxomycetes are not known; furthermore, it is not clear whether myxomycetes can affect the bark condition.

Cryptomeria japonica normally maintains strongly acidic conditions on the bark of live trees (Minami & Takahashi, 1994) and releases acidic exudates from its roots (Yambe, 1978). Furthermore, the bark secretes antimicrobial products to protect the tree from pathogens and decomposers (Shibutani, Samejima, & Saburi, 1998; Li, Chang, Chang, & Chang, 2008). A decline in tree vitality could degrade the physicochemical properties of C. japonica trees, which may influence corticolous myxomycetes on the tree bark. For example, myxomycete communities on unhealthy trees in an urban area were different from those on healthy bark in a rural area (Takahashi, 2016). However, it was not possible to determine whether the differences in the myxomycete communities were related to tree vitality or environmental differences in the survey area of that study. Therefore, the present study was conducted in a single forest in a mountain national park with low levels of human activity to eliminate the effects of environmental difference on corticolous myxomycetes. The aim of the study was to investigate the relationships among tree vitality, bark traits, and myxomycete communities on the bark of C. japonica trees.

2. Materials and methods

2.1. Study site

The present survey was conducted in a forest zone in Kagamiganaru, Mt. Daisen (34.5283°N, 133.4915°E, 900 m elevation), Tottori Prefecture, in Daisen-Oki national park in western Japan. The forest consists of Fagus crenata Blume and Quercus crispula Blume trees, with a scattered distribution of C. japonica trees. The survey area was far from industrial, agricultural, or residential areas and therefore had low levels of human activity. Over one hundred and ten C. japonica trees were sampled from an area of 9 ha surrounding the Kagamiganaru resort park, and several trees were sampled from a plantation of C. japonica, which was located beside the natural forest. The diameter at breast height (DBH) of the sampled trees ranged from 24 to 135 cm (Table 1). Healthy C. japonica trees are triangular with a pointed crown; however, there were several trees at the forest edges with degenerated crown and branches. There was an occasional decline in tree vitality in the mature stage of C. japonica. Although the direct cause for the dieback of C. japonica branches has not been identified, damages of trees were able to visually observe and evaluate.

Table 1. Properties of sampled trees and the bark traits corresponding to the tree vitality grades.

	V1	V2	V3	V4	Range*
Tree bark traits
Number of sample trees	19	21	18	16	-
Diameter (DBH, cm)	49ab	53b	41a	43ab	24-135
Bark pH	3.7a	4.0b	4.0b	4.2c	3.3-4.6
EC (μS/cm)	173b	123ab	96ab	71a	38-456

Vitality grades follow Fig. 1. Different superscript letters indicate significant differences (Tukey's HSD test, p < 0.05). ^*Range shows the value from minimum to maximum of sampled 74 trees and bark pH was negatively correlated with EC among them (r = −0.781, p < 0.01).

Observatories at the closest meteorological station in Yonago City and Daisenji indicated that the mean annual temperature and annual precipitation in this area were 10.6 °C and 3111 mm, respectively (http://www.data.jma.go.jp/obd/stats/etrn/index.php; accessed Aug 1, 2018). Snow cover was observed from Dec 2017 to Mar 2018. The present survey area receives a high precipitation and is a climatically conducive environment for the growth of C. japonica trees (Tsukada, 1982).

2.2. Bark sampling for determining tree vitality grades

The dieback of branches of C. japonica trees was observed and estimated. The vitality of trees was categorized based on the tree canopy shape and leaf density of branches, as described in a previous study (Urushibara, Hijikata, & Shinkawa, 2004). The vitality grades were determined as follows (Fig. 1): V1, healthy tree with steeple-shaped crowns and high leaf density; V2, round and declining tree canopy crown with fairly healthy branches ; V3, considerably degenerated crown with blasted upper branches ; and V4, severely damaged crowns and degenerated upper and side branches.

Fig. 1. Categorization of Cryptomeria japonica tree vitality in the study area based on tree shape and leaf density. V1: healthy trees with steeple-shaped crowns; V2: moderately healthy trees with rounded crowns; V3: trees showing a slight decline with damaged crown and upper branches; V4: trees showing a severe decline with severely damaged crown, side branches, and upper branches.

Bark sampling was performed twice, on Aug 28, 2017 and May 6, 2018. Seven to twelve trees were sampled for each vitality grade (V1-V4), with a total of 34 trees in Aug and 40 trees in May (Table 1). Most trees were sampled twice, and a few additional trees were sampled in 2018. A previous study indicated that the species richness of corticolous myxomycetes at a site was saturated within a 10-tree sampling effort (Takahashi & Harakon, 2018). The bark fragments of each sampled tree were completely stripped manually at approximately 800 cm² (approximately 50 g of dry weight) around the trunk surface at 0.5-2.0 m above the ground level, excluding the epiphytes. The bark samples of each tree were preserved in a paper bag (23 × 35 cm) and labeled. They were then stored in a dry environment at room temperature (approximately 19 °C-24 °C) for a few weeks before myxomycete culturing.

2.3. Myxomycete culture

The myxomycete communities were examined using the moist chamber culture method (Stephenson, 1989), which was conducted within a few weeks of sampling. Each bark sample was cut into small pieces (approximately 2-7 cm in length), and approximately 50 cm² (4 g) of the bark was randomly selected and placed with the outer surface facing up in a Petri dish (diameter: 9 cm) layered with filter paper (diameter: 7 cm). Ten such Petri dish moist chambers were prepared for bark samples per tree at a single time point. The bark pieces in the Petri dishes were soaked in 25 mL of distilled water (pH 6.9) and then incubated at 23 °C with a 12 h light/dark photoperiod. After 3 d, the excess water was drained from the Petri dishes, and the lid was placed on the Petri dish for 3 wk. The culture dishes were then opened halfway to allow the chambers to dry slowly. After 4 wk, the myxomycete fruiting bodies were examined under a dissecting stereomicroscope.

We examined the bark pH of individual trees and the electrical conductivity (EC) using the drained excess water after 3 d of soaking. EC was determined as the ionic strength of the bark exudates. The bark pH was measured using a compact pH meter (Horiba, Kyoto, Japan), and the median pH was calculated for each tree based on five cultures. The EC was measured using a compact ion meter (Horiba, Kyoto, Japan), and the average EC was calculated for each tree based on five cultures. The average values of bark pH and EC were further calculated for each vitality grade. The pH preference of a species was evaluated as an average value of bark pH with standard deviation, which indicated that a given species occurred on ten or more trees.

Myxomycete species were examined in 740 culture dishes and identified based on the microscopic observations of their fruiting bodies as described by Yamamoto (1998). Their binomial nomenclature was recorded according to the most recent classification (http://eumycetozoa.com/data/genera.php). The incidence of a given species was recorded as the number of positive cultures, and the number of cultures in which myxomycete fruiting bodies occurred was denoted as the abundance of a given species. Bark pieces containing fruiting bodies of each species were glued to the bottom of a paper collection box and maintained and stored in the laboratory.

2.4. Data analyses

The values of bark pH and species richness per tree were compared among the four vitality grade groups using multiple comparison tests of Tukey's honest significant difference test (Tukey's HSD test, p < 0.05), performed with ESUMI Excel Statistics 5.0 (ESUMI Co. Ltd., Tokyo, Japan). The correlation between the measured characteristics was analyzed with Pearson product-moment correlation coefficient (r), using Excel Statistics 2012 (SSRI Co., Ltd., Tokyo, Japan). Statistical significance was set at p < 0.01. Kendall rank correlation coefficient (τ) was applied between the vitality grades and other measured characteristics.

The observed number of species (S_obs) in each vitality grade was recorded as the number of species occurring in the culture. The presumed number of species was estimated as species richness (S_est) using the Chao1 method (Chao, 1984) based on the S_obs and the abundance of a given species in each community of the vitality grade. The survey efforts were evaluated by comparing S_obs and S_est. The species diversity of myxomycete communities was obtained using the Shannon-Wiener index (Hʹ) (Shannon & Weaver, 1963) and the equitability (Jʹ) index (Pielou, 1966), as in previous studies (Stephenson, 1989). These indices were also estimated for each community within each vitality grade using PAST software (Hammer, Harper, & Ryan, 2001; http://folk.uio.no/ohammer/past/).

Similarities between the healthy community (V1) and communities whose vitality declined (V2−V4) were indicated by the percentage similarity (PS) index: PS = Σ_min (a, b, c, …, x), where min is the lower value of the percentage compositions of species a, b, ..., x in the two communities. PS indicates the relative abundance of common species found in both communities (Table 2).

Table 2. Species richness and diversity of myxomycete communities corresponding to the tree vitality grades.

	V1	V2	V3	V4
Positive culture (%)	99	99	99	95
Average species per tree*	5.8 ± 2.3a	5.9 ± 1.8a	6.8 ± 2.1a	7.1 ± 2.4a
Species richness (Sobs)	13	15	15	15
Chao-1 (Sest)	13	15	15	15
Species diversity (H')	2.12	2.12	2.23	2.39
Equitability (J')	0.83	0.78	0.82	0.88
Percentage similarity**	1.00	0.73	0.69	0.65

Vitality grades follow Fig. 1. ^*The values show average with standard deviation. Superscript letters indicate no significant differences (Tukey's HSD test, p < 0.05). ^**The indices are calculated to V1 community.

Myxomycete species and their abundances, shown as the number of positive cultures, were cross tabulated per tree, and the data were arranged into eight communities in two survey occasions according to the vitality grades. The cumulative community was aggregated for each vitality grade (Table 3; Fig. 2). Species were arranged according to the ordination of species abundance and occurrence across the tree vitality grades. The relative abundance (%) of a species was calculated as follows: abundance of a given species/total abundance in each community unit of vitality grade × 100.

Table 3. Corticolous myxomycete species and their abundance in different decline grades of tree vitality. Species are arranged in order to abundance in healthy tree (V1) and occurrence in vitality grades (V2-V4). Italic indicates score of relative abundance (%). Total abundance and species richness were shown in the bottom.

	Decline in tree vitality				Total abundance	Relative abundance (%)
Species	V1	V2	V3	V4
Paradiacheopsis rigida (Brândzǎ) Nann.-Bremek.	138	154	127	75	494	22
Enerthenema berkeleyanum Rostaf.	118	71	64	53	306	14
Arcyria cinerea (Bull.) Pers.	70	72	69	56	267	12
Cribraria confusa Nann.-Bremek. & Y. Yamam.	65	24	16	5	110	5
Hemitrichia velutina Nann.-Bremek. & Y. Yamam.	55	7	4	12	78	4
Cribraria minutissima Schwein.	48	95	58	68	269	12
Physarum nutans Pers.	38	55	60	43	196	9
Macbrideola argentea Nann.-Bremek. & Y. Yamam.	24	8	7	12	51	2
Licea variabilis Schrad.	19	70	89	55	233	11
Cribraria microcarpa (Schrad.) Pers.	9	4	4	24	41	2
Comatricha laxa Rostaf.	3	―	―	―	3	0.1
Lycogala exiguum Morgan	2	―	―	2	4	0.2
Comatricha elegans (Racib.) G. Lister	1	11	11	4	27	1
Paradiacheopsis solitaria (Nann.-Bremek.) Nann.-Bremek.	―	6	33	34	73	3
Clastoderma debaryanum A. Blytt	―	2	20	12	34	2
Echinostelium minutum de Bary	―	5	4	16	25	1
Macbrideola dubia Nann.-Bremek. & Y. Yamam.	―	3	1	―	4	0.2
Total abundance	590	587	567	471	2215	100
Species richness	13	15	15	15	17

Fig. 2. Species ranking in the order of relative abundances in the V1 community and that in the communities with declined vitality grades (V2−V4). Species arrangement is in the same order as in Table 3. Relative abundances of several species changed and the community structure changed as vitality declined.

Ordination of eight myxomycete communities in two survey occasions was estimated using nonmetric multidimensional scaling (NMDS) based on Bray-Curtis similarity in PAST, which is a useful method for comparing community structures (Takahashi et al., 2018). The NMDS scores show the similarity among myxomycete communities, which were plotted according to the NMDS scores of the first two axes as shown in Figure 3. The relationship between the NMDS scores and tree bark traits was analyzed using Pearson product-moment correlation coefficient.

Fig. 3. Plots of myxomycete communities with different vitality grades (V1-V4) in two surveys (August and May) according to the first two axis scores of nonmetric multidimensional scaling (NMDS). Stress value was 0.101. Coefficient of determination for first axis was r² = 0.579 and that for second axis was r² = 0.290. August (●): with V1a, V2a, V3a, and V4a. May (▲): with V1m, V2m, V3m, and V4m. Vitality grades are the same as those shown in Figure 1. The communities in the two sampling occasions were separated by the first axis scores. The second axis scores were positively correlated with bark pH (r = 0.902, p < 0.01) and negatively correlated with EC (r = −0.885, p < 0.01).

3. Results

3.1. Bark traits

The bark traits were examined for the different vitality grades as shown in Table 1. The bark pH of individual trees ranged from 3.3 to 4.6, and the average bark pH among the vitality grades increased from 3.7 to 4.2 (Table 1, significant difference by Tukey's HSD test). The EC of individual trees ranged from 38 to 456 μS/cm, and the average value decreased from 173 to 71 μS/cm with a decline in tree vitality. The variance in pH negatively correlated with the EC (r = −0.781, p < 0.01). The healthy V1 grade trees maintained a more acidic pH with higher EC, but a decline in tree vitality reduced bark acidity. The variance in DBH of the sampled trees did not significantly correlate with the bark pH and EC.

3.2. Myxomycete communities

Myxomycete fruiting bodies appeared in over 95% of culture chambers across the vitality grades (Table 2). The average number of species per tree showed an increasing trend from 5.8 to 7.1 but was not significantly different across the vitality grades. S_obs was consistent with S_est in each vitality grade. Grade V1 trees hosted 13 myxomycete species on the bark, and each of the V2, V3, and V4 trees hosted 15 species. Species diversity (H′) in each vitality grade showed a tendency to increase as vitality declined, i.e., the H′ values changed from 2.12 to 2.39, and the equitability value (J′) was the highest in the V4 trees. The indices of PS based on the V1 community gradually decreased from V2 to V4 communities and was 0.65 for the V4 community (Table 2).

The cumulative number of species and abundances in each vitality grade are presented in Table 3. Seventeen species were identified and ordered by relative abundance. Figure 2 shows the comparison of the structure of myxomycete communities between V1 and the other vitality grades. When the species of V1 community were arranged in the order of their relative abundances, species composition in the V2−V4 communities shifted from that of the V1 community. Four species showed a decreased abundance (Enerthenema berkeleyanum Rostaf., Cribraria confusa Nann.-Bremek. & Y. Yamam., Hemitrichia velutina Nann.-Bremek. & Y. Yamam., and Macbrideola argentea Nann.-Bremek. & Y. Yamam.) and several species showed an increased abundance (Cribraria minutissima Schwein., Physarum nutans Pers., Licea variabilis Schrad., and Paradiacheopsis solitaria (Nann.-Bremek.) Nann.-Bremek). The V1 community appeared to retain a distinctive community structure of myxomycetes.

Eleven species were commonly found across all the tree vitality grades. Three species (P. solitaria, Clastoderma debaryanum A. Blytt, and Echinostelium minutum de Bary) did not appear in the V1 grade but appeared in the V2−V4 grades. The remaining three species occurred rarely. Paradiacheopsis rigida (Brândzǎ) Nann.-Bremek. was the most abundant species (22% relative abundance), the second abundant species was E. berkeleyanum (14% relative abundance), and the third abundant species was C. minutissima (12% relative abundance). The relative abundances of both Arcyria cinerea (Bull.) Pers. and L. variabilis were ≥ 10% each. The relative abundances of both P. nutans and C. confusa were ≥ 5%, while those of common species such as H. velutina, M. argentea, Cribraria microcarpa (Schrad.) Pers., and Comatricha elegans (Racib.) G. Lister were ≥ 1%.

3.3. Ordination of myxomycete communities

The eight myxomycete communities in two surveys were visually indicated by ordination along the first two axis scores of NMDS as shown in Figure 3. The arrangement of communities was separated by the first axis, i.e., the communities sampled in May were arranged on the positive side of the first axis, while communities sampled in August were arranged on the negative side. The vitality grades were arranged in order along the second axis, and the ordination indicated similar trends as tree vitality declined in the two sampling occasions.

The first axis scores of communities had no significant correlation with tree traits, but the second axis scores had a significantly positive correlation with vitality grades (r = 0.955, p < 0.01) and bark pH (r = 0.902, p < 0.01) and a negative correlation with EC (r = −0.885, p < 0.01). In the case of myxomycete communities, the first NMDS scores were significantly correlated with the average number of species per tree (r = 0.881, p < 0.01) and equitability of communities (r = 0.797, p < 0.05). The second NMDS scores were significantly correlated with the total species richness (r = 0.746, p < 0.05).

3.4. Species response to declining tree vitality and bark pH

The response of relative abundance of a species to tree vitality grades was examined using Kendall rank correlation. The relative abundance of three species changed according to a decline in tree vitality (Fig. 4), that is, the relative abundance of E. berkeleyanum and C. confusa decreased as the vitality declined, whereas that of P. solitaria increased (respectively, τ = −1.00, p < 0.01).

Fig. 4. Relative abundances of three species that responded to tree vitality grades. The abundance of Enerthenema berkeleyanum and Cribraria confusa decreased as vitality declined. The abundance of Paradiacheopsis solitaria increased as vitality declined.

Response to bark pH was estimated by the pH preference of a given species. Fourteen species were arranged from 3.7 to 4.1 (Fig. 5). Hemitrichia velutina and C. confusa preferred strongly acidic bark (pH = 3.7), followed by M. argentea and E. berkeleyanum (pH = 3.8). In contrast, L. variabilis, P. solitaria, E. minutum and C. debaryanum preferred a higher pH of 4.1. The other six species showed preferences for around pH of 3.9-4.0.

Fig. 5. Preference for bark pH of 14 species that were ordered according to the average pH preference with standard deviation. Values indicate the average pH preference of the species.

4. Discussion

A previous nationwide study found 30 species (including varieties) of myxomycetes on the bark of C. japonica trees (n = 188, Takahashi et al., 2018) and another study found 28 species (n = 176, Takahashi & Harakon, 2018). The most abundant species were P. rigida > C. confusa > E. berkeleyanum. The bark of C. japonica trees generally retains strong acidic condition, such as average pH with standard deviation of 3.7 ± 0.3 (Takahashi et al., 2018) and 3.7 ± 0.2 (Takahashi & Harakon, 2018). In the present study, slightly less acidity was observed on the bark, that is, the average pH was 3.9 ± 0.3 (n = 74) and ranged from 3.3 to 4.6. A comparison of community structures revealed that the two most abundant species were in the same order as the above mentioned studies, whereas C. minutissima 12%, A. cinerea 12%, L. variabilis 11%, and P. nutans 9% were more abundant than in the previous studies. In addition, C. confusa was less abundant at only 5%. The healthy tree bark nourished specific myxomycete species, but the abundance of several species changed in association with a decline in tree vitality and weakening of bark acidity. The relative abundance of two myxomycete species, that is, E. berkeleyanum and C. confusa, particularly decreased in response to a decline in vitality, whereas that of P. solitaria increased as vitality declined.

The decline in vitality correlated with increased bark pH, and the change is considered an important factor affecting myxomycete growth and inhabitation (Stephenson, 1989; Takahashi, 2014). For example, in cases of acidification of leaf-litter by fertilization, the species richness of myxomycetes was suppressed (Takahashi, 2017). Some myxomycete species are sensitive to the changes in substrate pH. Previous studies have shown the peak pH and ranges for various species (Härkönen, 1977; Stephenson, 1989; Everhart et al., 2008), that is, the relative abundance of C. minutissima peaked at around pH 3.7-3.8, whereas that of C. confusa and Enerthenema papillatum (Pers.) Rostaf. peaked at around pH of 4.1-4.5 and A. cinerea and E. minutum peaked at around pH of ≥ 4.5.

In the present study, myxomycete species preference for bark pH of C. japonica differed from that of previous studies (Fig. 4). For instance, C. confusa preferred the more acidic bark of V1 (pH = 3.7), whereas C. minutissima was the most abundant on the V2 tree bark (pH = 4.0), which these values were slightly different from the above-mentioned pH values. Furthermore, A. cinerea was abundant in V1-V4 with a preference for bark pH (pH = 3.9). The abundance of E. minutum increased as tree vitality declined, and it preferred weakening of bark acidity (pH = 4.1). Less acidification of bark caused a change in myxomycete microhabitat and diversified the species composition of the community.

It is well known that myxomycetes feed on bacteria as a nourishment resource in nature (Stephenson & Rojas, 2017), and bacterial diversity is similarly influenced by soil pH, that is, its diversity is lower in acidic soils than in neutral soils (Fierer & Jackson, 2006; Wu, Zeng, Zhu, Zhang, & Lin, 2017). It is suggested that bacterial diversity may have a strong relationship with myxomycetes activity under acidic bark conditions. Tree vitality could be influenced by pathogens (Kubono & Ichihara, 2010) and decomposers (Kofujita et al., 2001), and it occasionally happens in the juvenile or mature stage. Therefore, corticolous myxomycetes, which are scavengers of bacteria and fungi, may have an ecological function on healthy live tree bark.

To summarize, the present study shows that myxomycete communities on the barks of living C. japonica trees were closely associated with tree vitality levels, which is reflected in the bark pH levels. Habitat pH is a primary determinant for the survival of many organisms (Partel, Helm, Ingerpuu, Reier, & Tuvi, 2004). Substrate pH is known to influence zygote formation (Shinnick, Pallotta, Jones-Brown, Youngman, & Holt, 1978), plasmodium formation (Collins & Tang, 1973), and sporulation of certain species of myxomycetes (Gray & Alexopoulos, 1968). Some myxomycete species are sensitive to changes in substrate pH as well as changes in bark pH associated with vitality decline, as seen in the present study. Several field studies have also shown that species of the genus Cribraria occur preferentially in acidic environments (Schnittler, Unterseher, & Tesmer, 2006; Rojas & Stephenson, 2007, Everhart et al., 2008; Fukasawa, Takahashi, Arikawa, Hattori, & Maekawa, 2015). Bark pH gradients were an important limitation for the shift of myxomycete species and communities.

Although the ecological functions of myxomycetes on the tree barks is not fully understood, tree growth and health may be associated with the inhabitation of corticolous myxomycetes. The relationship among corticolous myxomycetes, tree vitality, and bark chemical traits may provide useful information on tree health, aiding in forestry management. Further studies are required to improve our understanding of the ecology of corticolous myxomycetes and their functions in the microecosystems on tree barks.

Declarations of interest

none.