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Abstract—We have studied the influence of the stage of decomposition and acidity of wood, as well as the illu-
mination of the microhabitat on the species composition, abundance, and occurrence of slime molds (Myx-
omycetes) of the xylobiontic (inhabitants of the wood) substrate complex of forest communities in Siberia
(Altai krai, Altai Republic, and Novosibirsk oblast). This work is based on a study of 1777 samples of fruit
bodies (sporophores) of myxomycetes. In the analysis of data for communities of Myxomycetes of the xylo-
biontic substrate complex, we recognize a successional series which clearly correlates with the stage of wood
decomposition. The study of the distribution of the species composition of the slime mold on wood of various
stages of decomposition shows that the maximum number of species is observed on dead trunks where the
wood is of medium density and the bark can easily be separated (W3). The lowest specificity and diversity of
species composition is observed on the fallen trunks of trees with very dense wood and dense bark (W1).
These dead trees have low water-retaining capacity, tight bark, and almost intact wood containing large
amounts of lignin, preventing the invasion of plasmodia and myxamoebae of Myxomycetes into the trunk.
A study of the location of slime-mold colonies in relation to the illumination level shows that the greatest
number of species is found on the front, side, and bottom parts of dead trunks of woody plants. The least spec-
ificity and the least variety of Myxomycetes species are found on apical parts of dead tree trunks facing the sun.
The exception are species with large fruit bodies such as Fuligo septica and Reticularia splendens, which are most
often observed on the upper parts of the sun facing trunks of woody plants. In the research area, the complex of
species typical for wood of coniferous trees is described. It is noted that acidophilic slime molds of the genera
Comatricha and Cribraria can be traced in xylobiontic and epiphytic–corticuloid substrate complexes.
Keywords: woody vegetation, xylobionts, Myxomycetes, slime molds, environmental factors, ecology
DOI: 10.1134/S1995425518050104
494
PATTERN OF SUBSTRATE PREFERENCES 495
cultivation of myxomycetes on substrates in “moist diversity index by the formula H = −Σpi logpi2, where
chambers.” Slime-mold sporophores were collected pi is relative abundance of each species equal to n/N,
and dead wood was sampled during the survey of forest ni is the number of records of each species in database,
plant communities of mountain and plain territories of and N is the total number of records in the dataset
three constituent entities of the Russian Federation under analysis (Shannon and Weaver 1963; Magurran,
(Republic of Altai, Altai krai, and Novosibirsk oblast) 1988, 2004).
in the period from 2008 to 2017. A total of 1777 colo-
nies of slime molds (samples) were found. We call one In this work we used the Simpson index describing
or more sporophores, presumably developed from one the probability of attribution of any two specimens
plasmodium, a colony. randomly taken from an indefinitely large community,
When collecting sporophore samples and selecting to different species, by the formula D = Σpi2 , where
samples of wood, we took into consideration and pi is the proportion of specimens of ith species.
recorded the following parameters: species of slime
mold, taxon of woody plant, stage of decomposition of For a comparison of species composition in various
the wood, and exposure of a colony of sporophores in groups of slime molds, we used the Sørensen–Cze-
relation to the light (topical distribution). For statisti- kanowski coefficient of similarity. Based on indexes of
cal calculations, all the above data were recorded in Sørensen–Czekanowski, calculated using Statistica 8
the database created by us in Excel software. software, we built dendrograms. For this purpose, we
The stage of decomposition of woody plant trunks used the method of hierarchical agglomerative family
was estimated on a scale from 1 to 5, where W1 is a (Ward method), in which the minimum dispersion is
fallen tree with a tight-fitting and practically invisible optimized within clusters. As a result, clusters of
damage to bark and very dense wood; W2—there is approximately equal sizes are created. As a measure of
damage to the bark, it partially departs, and wood is difference, a quadratic Euclidean distance was used,
very dense; W3—there is significant damage to the which helps us increase the contrast of the clusters.
bark, it is easily separated, wood is of medium density;
W4—bark is practically absent, wood is soft and easily RESULTS
divided into separate fibers; and W5—bark is com-
pletely absent, wood is very soft and easily divided into We have found on rotten wood of different stages of
individual fibers without the use of cutting objects. decomposition (W1–W5) 152 species of slime molds
We have studied fallen trunks of leaved arboreal from 12 families and 39 genera (Vlasenko and
plants from the genera Acer L., Alnus Mill., Betula L., Novozhilov, 2011, 2012; Vlasenko et al., 2013; Novo-
Malus Mill., Padus Mill., Populus L., Salix L., Sorbus L., zhilov et al., 2010). The nucleus of myxomycete biota
and Tilia L., as well as fallen trunks of conifer arboreal in xylobiontic complex on the territory under study
plants from the genera Abies Mill., Larix Mill., Picea includes 21 species whose occurrence was equal or
A. Dietr., and Pinus L. exceeded 1.5% of total number of the number of records
Exposure in relation to light was estimated accord- in database. These are Arcyria cinerea (Bull.) Pers.,
ing to the location of the colony of sporophores on the A. incarnata (Pers. ex J. F. Gmel.) Pers., A. stipata (Sch-
dead trunk: A, trunk bottom in contact with the wein.) Lister, Ceratiomyxa fruticulosa (O. F. Mull.)
ground (least illuminated); B, side barrel; C, apical T. Macbr., Comatricha nigra (Pers. ex J. F. Gmel.)
part; and D, upper part of the trunk (most illumi- J. Schröt., Cribraria cancellata (Batsch) Nann.-
nated). Bremek., C. microcarpa (Schrad.) Pers., Fuligo septica
The collection of myxomycete sporophores in the (L.) F. H. Wigg., Hemitrichia calyculata (Speg.)
field was carried out by the standard technique M. L. Farr, H. clavata (Pers.) Rostaf., Lycogala epi-
(Vlasenko and Novozhilov, 2012). The following dendrum (L.) Fr., Metatrichia vesparia (Batsch)
information was recorded for each sample: substrate, Nann.-Bremek. ex G. W. Martin et Alexop, Physarum
substrate contact with the ground, character of illumi- album (Bull.) Chevall., Ph. notabile T. Macbr., Stemo-
nation, stage of decomposition and size of wood resi- nitis axifera (Bull.) T. Macbr., S. fusca Roth, Stemoni-
dues, and exposure of the sporophore colony on the topsis typhina (F. H. Wigg.) Nann.-Bremek., Trichia
substrate. In addition to the collection of mycomycete decipiens (Pers.) T. Macbr., T. favoginea (Batsch) Pers.,
sporophores in the field, we also used the method of T. scabra Rostaf. and T. varia (Pers. ex J. F. Gmel.) Pers.
moist chambers (Gilbert and Martin, 1933), where The contribution of myxomycete groups inhabiting
samples of rotten wood are taken in the field. In the wood the different stages of decomposition (W1–W5)
laboratory, samples were placed in Petri dishes and to the formation of the nucleus of biota is uneven. For
incubated at room temperature and ambient light for example, for the most frequently occurring species,
2 months. Metatrichia vesparia, we noted the following frequen-
An analysis of alpha diversity included an estima- cies of occurrence: W1, 0 samples; W2, 2; W3, 92; W4,
tion of species richness and evenness (Vasilevich, 26; and W5, 12; samples. For Lycogala epidendrum, we
1992). Evenness was calculated using the Shannon noted an identical tendency, W1, 0 samples; W2,
Parameters compared W1 W2 W3 W4 W5
3 samples; W3, 63; W4, 19; and W5, 12 samples corre- the greatest biodiversity of myxomycetes is found on
spondingly. the wood of coniferous trees, while deciduous trees
An analysis of the distribution of slime-mold spe- contain complexes of myxomycetes poor in number of
cies composition on wood at different decomposition species, but with a large proportion of dominant spe-
stages showed that the maximum number of species cies (Table 3).
(119) was observed on the tree trunks (W3), where the
wood of medium density and bark is already easily
separated (Table 1). While on tree trunks (W1) with DISCUSSION
very dense wood and tight-fitting bark, the smallest It is known that decaying wood is a heterogeneous
number of species (16 species) was found. substrate and an important habitat for many species of
A study of the location of myxomycete colonies in micro- and macro-organisms in forest communities
relation to the level of sunlight showed that maximum (Boddy, 2001; Siitonen, 2001; Harmon et al., 2004;
number of species (110) was found on the bottom parts Brassard et al., 2008; Van der Wal et al., 2013;
of the fallen tree trunks and the smallest number of Yamashita et al., 2015; Cline et al., 2018). Properties of
species (66) was found on the upper, most illuminated decaying wood are different in tree species and change
parts of the trunks. The lowest value of the Shannon
index and the highest value of Simpson index were
noted for myxomycete communities in the lower and Table 2. Myxomicete diversity on different parts of large
upper parts of the trunks. Thus, the optimal place for fallen trunks in dependence of the sporophore position
the development of sporophores of slime molds is the related to the light source
middle and end apical of dead trunks of woody plants, Stage
while, on the upper and the lower parts, complexes poor
of species develop, but with a large proportion of domi- Compared parameters A B C D
nant species (Table 2).
We separately studied the distribution of identified Number of species 79 72 110 66
myxomycete species depending on the substrate Shannon diversity index 3.7 3.8 4.0 3.6
belonging to coniferous or deciduous woody plants.
Out of 1777 colonies of slime molds, the substrate Simpson domination index 0.04 0.03 0.02 0.04
(dead wood) for softwood or hardwoods was identified Number of unique spe-
for 1745. For the study area, it was found that the mean 14/0.2 30/0.4 13/0.1 9/0.1
cies/index of uniqueness
value of hydrogen index (pH) of coniferous wood is 5.6;
for deciduous it is 6.9. (A) Lower part of the trunk contacting ground (least illuminated),
(B) lateral trunk part, (C) apical part, and (D) upper trunk part
On woody debris of deciduous trees, we identified (most illuminated).
96 species of slime molds belonging to 30 genera of
9 families and, on coniferous, 127 species belonging to
37 genera from 12 families (Table 3). We have not Table 3. Biodiversity of Myxomicetes on the fallen trunks of
leaved and coniferous woody plants
found any members of Dianemataceae, Echinostelia-
ceae, or Liceaceae families on the rotten hardwood of Wood of Wood of
Compared parameters
woody plants (Fig. 1). leaved trees coniferous trees
The Shannon diversity index for slime-mold com- Number of species 96 127
munities developing on wood of coniferous trees is 4.2 Shannon diversity index 3.7 4.2
and the Simpson dominance index is 0.02; for the
community of slime molds growing on rotten wood of Simpson domination index 0.04 0.02
deciduous woody plants, the Shannon diversity index Number of unique species/ 25/0.3 51/0.4
is 3.7 and the Simpson dominance index is 0.04. Thus, index of uniqueness
W1
W2
W3
W4
W5
Fig. 2. Dendrogram of similarity of the species composition of Myxomycetes found on fallen trunks of woody plants with different
stages of decomposition. A description of the classification of wood by the stage of decomposition (W1–W5) is given in the Mate-
rials and Methods section.
The maximum diversity at the level of the spectrum mechanochoria. For example, threads of the capitium
of families (14 families) of myxomycetes is on the of Order Trichiales T. Macbr. have adaptations that
fallen trunks of woody plants with a significant dam- allow prolonged contact with sunrays to spin accord-
age to the bark, the bark is easily separated, and the ing to the type of springs and “shoot” spores (Fig. 5).
wood is of medium density (W3). On wood with the Also, anemochory is quite widespread among slime
stage of decomposition of W2 and W5, nine families molds and the location of mature sporophores on cer-
were noted. At the same time, there is a different spe- tain parts of dead trunks of woody plants can facilitate
cies composition of myxomycetes, which indicates or hinder the dissemination of slime-mold propagules
that in each family there are species with the same eco- by entering the air flow.
logical niche and with different niches. For example, It is known that the acidity of substrate (pH) is a very
Cribraria macrostipitata H. Neubert et Nann.– important parameter for most species of Myxomycetes
Bremek. was found on fallen tree trunks with the stage (Novozhilov et al., 2017). The greatest selectivity with
of wood decomposition W2, W 3, and Cribraria mac- respect to this parameter can be observed in the epi-
rocarpa Schrad. only on fallen trunks with the stage of phytic–corticoid group of myxomycetes (Härkönen,
wood decomposition of W4. 1977, 1978, 1981; Härkönen and Ukkola, 2000).
The study of the distribution of slime-mold colo- Our studies have shown that, for the slime molds of
nies on different parts of dead trunks that have differ- the xylobiont complex, the acidity of the medium
ent exposure towards the sunlight showed that the (pH) is also an important parameter. An analysis of
group of species found on the upper most illuminated the distribution of myxomycetes depending on the
surface of the dead trunk (D) composes a separate substrate belonging to coniferous or deciduous woody
cluster (Fig. 4). plants revealed species with a strict adherence to pH
The combination into separate, small subcluster values. Fifty-one species of myxomycetes were found
groups of myxomycetes living on the side (B) and end exclusively on coniferous species of woody plants,
(C) parts of woody plants of fallen trunks can be where the majority of species were distributed between
explained by almost the same level of illumination of the genera of Arcyria Hill ex F. H. Wigg., Comatricha
these parts of the substrate. It is known that the open- Preuss, Cribraria Schrad., Licea Schrad., and Physa-
ing or cracking of peridium occurs when it dries during rum Pers. Twenty-five species of slime molds were
the maturation of sporophores, which is largely facili- identified exclusively on deciduous species of woody
tated by the level of sunlight. Many species of slime plants, where the majority of species were distributed
molds are characterized by the phenomenon of auto- between the genera Badhamia Berk., Fuligo Haller,
W1 W2
Arcyriaceae Arcyriaceae
25 25
Trichiaceae Ceratiomyxaceae Trichiaceae Ceratiomyxaceae
20 20
Stemonitidaceae
15 Clastodermataceae Stemonitidaceae
15 Clastodermataceae
10 10
5 5
Reticulariaceae 0 Cribrariaceae Reticulariaceae 0 Cribrariaceae
Physaraceae Dianemataceae
Liceaceae Didymiaceae
Echinosteliaceae
Fig. 3. Sequence of the change in the spectra of dominant families of myxomycetes depending on the stage of wood decomposition.
A description of the classification of wood by the stage of decomposition (W1–W5) is given in Materials and Methods section.
Physarum Pers., and Reticularia Bull. Thus, acido- ence of species in it sometimes preferring even con-
philic slime molds of the genera Comatricha and trasting habitat conditions.
Cribraria can be traced in xylobiont and epiphytic–
corticoid substrate complexes. The significant pres-
ence of species of the genus Physarum simultaneously CONCLUSIONS
on deciduous and coniferous woody remains is As a result of an analysis of data within the bound-
explained by both the volume of taxon and the pres- aries of the xylobiont substrate complex of myxomy-
Fig. 4. Dendrogram of similarity of the species composition of myxomycetes on different parts of fallen trunks with different
exposures to sunlight. A description of the classification of wood by the stage of decomposition (W1–W5) is given in Materials
and Methods section.
(a) (b)
Fig. 5. Arcyria helvetica (Meyl.) H. Neubert, Nowotny et K. Baumann: (a) sporophores, scale = 1 mm; (b) threads of capillitium
and spores, scale = 15 μm.
cetes, the presence of successional series clearly eral and apical parts of tree trunks belonging to coni-
related to the stage of decomposition of wood was fers at the W3 stage of decomposition (average density
noted. of wood and easily separating bark).
A study of the effect of the stage of decomposition The lowest specificity and the least diversity of spe-
and acidity of wood on the species composition, abun- cies composition of slime mold were observed in the
dance, and occurrence of the myxomycete xylobiont upper parts of the fallen tree trunks facing the sun.
complex, as well as the location of colonies of their Direct exposure to sunlight on these parts of the valley
sporophores on the fallen trunks of trees, showed that leads to a strong drying of the substrate and rapid dry-
the greatest taxonomic diversity was observed on lat- ing of the still immature sporophores of many species
of myxomycetes. The exceptions are species with large Clissmann, F, Fiore-Donno, A.M., Hoppe, B., Krüger, D.,
sporophores, such as Fuligo septica (L.) F. H. Wigg. Kahl, T., Unterseher, M., and Schnittler, M., First
and Reticularia splendens Morgan, which are most insight into dead wood protistan diversity: a molecular
often noted precisely on the upper (facing the sun- sampling of bright-spored Myxomycetes (Amoebozoa,
light) fallen trunks of woody plants. slime-moulds) in decaying beech logs, FEMS Microbiol.
Ecol, 2015, vol. 91, art. ID fiv050.
On deciduous trees, complexes of Myxomycetes Gilbert, H.C. and Martin, G.W., Myxomycetes found on
with a small number of species develop, but with a the bark of living trees, Univ. Iowa Stud. Nat. Hist.,
large proportion of dominant species; on coniferous 1933, vol. 15, no. 3, pp. 3–8.
tree species, on the contrary, there are complexes with
Härkönen, M., Corticolous Myxomycetes in three different
a large number of species and the absolute and relative habitats in southern Finland, Karstenia, 1977, vol. 17,
number of rare small species increases, resulting in pp. 19–32.
increased total richness.
Härkönen, M., On corticolous Myxomycetes in northern
As a result of our research, we can note that the pH Finland and Norway, Ann. Bot. Fen., 1978, vol. 15,
acid tolerance complex of species associated with pp. 32–37.
coniferous wood was found. It should be noted that Härkönen, M., Myxomycetes developed on litter of com-
acidophilic slime molds of the genera Comatricha and mon Finnish trees in moist chamber cultures, Nord. J.
Cribraria can be traced in xylobiont and epiphytic– Bot., 1981, vol. 1, pp. 791–794.
corticoid substrate complexes. It is shown that, in the Härkönen, M. and Ukkola, T., Conclusions on Myxomy-
study area, Myxomycetes from the genera Collaria cetes completed over twenty-five years from 4793 moist
Nann.-Bremek., Colloderma G. Lister, Dianema Rex, chamber cultures, Stapfia, 2000, vol. 155, pp. 105–112.
Dictydiaethalium Rostaf., Echinostelium de Bary, Lep-
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Gregory, S.V., Lattin, J.D., Anderson, N.H., Cline, S.P.,
Hertel develop exclusively on the wood of coniferous Aumen, N.G., Sedell, J.R., Lienkaemper, G.W., Cro-
trees. mack, K., and Cummins, K.W., Ecology of coarse
The accumulation of information about the envi- woody debris in temperate ecosystems, in Advances in
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ACKNOWLEDGMENTS p. 231.
This study was conducted within the project Lima, V.X. and Cavalcanti, L.D., Ecology of lignicolous
no. АААА-А17-117012610055-3, according to the myxomycetes in Brazilian Atlantic rain forest, Mycol.
Progr., 2015, vol. 14, p. 92.
State Task of the Central Siberian Botanical Garden,
Siberian Branch, Russian Academy of Science. The Loganathan, P., Distribution and ecology of Myxomycetes,
laboratory work of Y.K. Novozhilov was supported by Int. J. Adv. Res. Biol. Sci., 2016, vol. 3, no. 12, pp. 188–
the program ААА–18–118031290108–6. 190.
In this paper we used materials from Herbarium of Madelin, M.F., Myxomycete data of ecological signifi-
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Higher Vascular Plants, Lichens and Fungi (NSK),
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process of coarse woody debris and fungal community Translated by S. Kuzmin