Ecological assemblages of corticulous myxomycetes in forest communities of the North-East Ukraine

  • A. V. Kochergina H. S. Skovoroda Kharkiv National Pedagogical University
  • T. Y. Markina H. S. Skovoroda Kharkiv National Pedagogical University
Keywords: consortive connections; epiphytic community; Eumycetozoa; moist chamber cultures; Myxogastrea; terrestrial protists; bark of living trees.

Abstract

Corticulous myxomycetes remain one of the least surveyed ecological groups of terrestrial protists. These organisms develop on the bark of trees, mostly feeding on bacteria and microalgae. Their microscopic size and fast developmental cycle (3–5 days) complicate the study of these organisms, and therefore data their on ecological relationships and patterns of biodiversity corticulous myxomycetes remain controversial. On the territory of the southwest spurs of the Central Russian Upland (Northeast Ukraine), no special studies on these organisms have been conducted. During 2017–2020, in nine forest sites located in this territory, we collected samples of bark of 16 species of tree plants, on which sporulating myxomycetes were then identified using the moist chamber technique in laboratory conditions. A total of 434 moist chambers was prepared, and 267 (61.5%) of which were found to contain myxomycete fruiting bodies. In total, we made 535 observations, finding 20,211 sporocarps. As a result, in the surveyed territory, we found 38 species of corticulous myxomycetes, belonging to 18 genera, 10 families, 7 orders, and 2 subclasses of Myxomycetes. Among the species of corticulous myxomycetes, the most abundant were Echinostelium minutum, Arcyria pomiformis, Macbrideola cornea, Perichaena chrysosperma, Licea kleistobolus, Paradiacheopsis fimbriata, Cribraria violacea, Enerthenema papillatum, A. cinerea, and L. operculata. The greatest species richness in the examined biota was observed for genera Comatricha, Licea, Paradiacheopsis and Perichaena, families Amaurochaetaceae and Trichiaceae, orders Stemonitidales, Trichiales and Physarales. By species diversity, dark-spored myxomycetes (Collumellomycetidae) somewhat exceeded bright-spored myxomycetes (Lucisporomycetidae). Badhamia versicolor, Didymium dubium, D. sturgisii, Macbrideola decapillata, and Perichaena luteola are new species for the surveyed area. Four species of myxomycetes were collected in Ukraine for the first time: Hemitrichia pardina, Licea floriformis, L. pygmea, and Macbrideola argentea. Quantitative and qualitative structure of myxomycete consortia developing on different species of substrate-forming plants demonstrated significant differences. The highest level of similarity was demonstrated by Fraxinus excelsior and Acer platanoides, and a relatively strong relationship was seen between Pinus sylvestris and Tilia cordata. The central cluster comprised F. excelsior, A. platanoides and P. sylvestris. By the sum of values of Bray-Curtis coefficient, Quercus robur appeared to be most distinctive plant species by quantitative composition of myxomycete consortia. F. excelsior and T. cordata are the most favourable for the development of corticulous myxomycetes. In all the analyzed consortia, the dominant species belonged to the Stemonitidales and Trichiales orders, while the remaining orders were represented by notably fewer species. Relative species richness of Stemonitidales was the highest in consortia of P. sylvestris, the contribution of Liceales was the greatest in A. platanoides and P. sylvestris, the percentage of Echinosteliales and Physarales was the highest on F. excelsior, the share of Cribrariales was especially large on A. platanoides. Trichiales were represented on all the analyzed substrates to almost the same extent. Representatives of Cribrariales and Physarales were completely absent on P. sylvestris, the species of Clastodermatales – on all species of plants, except Q. robur. Prevalence of bright-spored myxomycetes was determined for consortia of Acer platanoides, the dominance of dark-spored myxomycetes – for F. excelsior, P. sylvestris and Q. robur. The obtained data indicate the presence of stable complexes of corticulous myxomycetes, associated with different species of trees in the forest ecosystems of Northeast Ukraine. This encourages further study of the structure of myxomycete consortia with tree species that were not included in this study and determining the influence of physical-chemical properties of the bark of different plant species on the discovered peculiarities of myxomycete communities.

References

Adl, S. M., Bass, D., Lane, C. E., Lukeš, J., Schoch, C. L., Smirnov, A., Agatha, S., Berney, C., Brown, M. W., Burki, F., Cárdenas, P., Čepička, I., Chistyakova, L., Campo, J., Dunthorn, M., Edvardsen, B., Eglit, Y., Guillou, L., Hampl, V., Heiss, A. A., Hoppenrath, M., James, T. Y., Karpov, S., Kim, E., Kolisko, M., Kudryavtsev, A., Lahr, D. J. G., Lara, E., Le Gall, L., Lynn, D. H., Mann, D. G., Massana i Molera, R., Mitchell, E. A. D., Morrow, C., Park, J. S., Pawlowski, J. W., Powell, M. J., Richter, D. J., Rueckert, S., Shadwick, L., Shimano, S., Spiegel, F. W., Torruella i Cortes G., Youssef, N., Zlatogursky, V., & Zhang, Q. (2019). Revisions to the classification, nomenclature, and diversity of Eukaryotes. Journal of Eukaryotic Microbiology, 66(1), 4–119.

Aguilar, M., Fiore-Donno, A. M., Lado, C., & Cavalier-Smith, T. (2014). Using environmental niche models to test the ‘everything is everywhere’ hypothesis for Badhamia. International Society for Microbial Ecology Journal, 8, 737–745.

Barbarych, A. I. (Ed.). (1977). Geobotanichne rajonuvannja Ukrajins’koji RSR [Geobotanical Zonation of the Ukrainian SSR]. Naukova Dumka, Kyiv (in Ukrainian).

Borg Dahl, M., Brejnrod, A. D., Russel, J., Sørensen, S. J., & Schnittler, M. (2019). Different degrees of niche differentiation for bacteria, fungi, and myxomycetes within an elevational transect in the German Alps. Microbial Ecology, 78(3), 764–780.

Clark, J., & Haskins, E. F. (2013). The nuclear reproductive cycle in the myxomycetes: A review. Mycosphere, 4(2), 233–248.

Everhart, S. E., Ely, J. S., & Keller, H. W. (2009). Evaluation of tree canopy epiphytes and bark characteristic associated with the presence of corticolous myxomycetes. Botany, 87, 509–517.

Everhart, S. E., Keller, H. W., & Ely, J. S. (2008). Influence of bark pH on the occurrence and distribution of tree canopy myxomycete species. Mycologia, 100, 191–204.

Fiore-Donno, A. M., Clissmann, F., Meyer, M., Schnittler, M., & Cavalier-Smith, T. (2013). Two-gene phylogeny of bright-spored myxomycetes (slime moulds, superorder Lucisporidia). PLoS One, 8, e62586.

Fiore-Donno, A. M., Kamono, A., Meyer, M., Schnittler, M., Fukui, M., & Cavalier-Smith, T. (2012). 18S rDNA phylogeny of Lamproderma and allied genera (Stemonitales, Myxomycetes, Amoebozoa). PLoS One, 7, e35359.

Fiore-Donno, A. M., Weinert, J., Wubet, T., & Bonkowski, M. (2016). Metacommunity analysis of amoeboid protists in grassland soils. Scientific Reports, 6, e19068.

Goad, A. E., & Stephenson, S. L. (2013). Myxomycetes appearing in moist chamber cultures on four different types of dead leaves. Mycosphere, 4, 707–712.

Godsil, C., & Royle, G. (2001). Algebraic graph theory. Springer-Verlag, New York.

Gotelli, N. J., & Chao, A. (2013). Measuring and estimating species richness, species diversity, and biotic similarity from sampling data. In: Encyclopedia of biodiversity. New York, Amsterdam, Elsevier. Pp. 195–211.

Heluta, V. P. (1989). Flora gribov Ukrainy. Muchnistorosyanye griby [Fungal Flora of Ukraine. Downy Mildew Fungi]. Naukova Dumka, Kyiv (in Ukrainian).

Ing, B. (1994). The phytosociology of myxomycetes. New Phytologist, 126, 175–201.

Kang, S., Tice, A. K., Spiegel, F. W., Silberman, J. D., Pánek, T., Cepicka, I., Kostka, M., Kosakyan, A., Alcântara, D. M. C., Roger, A. J., Shadwick, L. L., Smirnov, A., Kudryavtsev, A., Lahr, D. J. G., & Brown, M. W. (2017). Between a pod and a hard test: The deep evolution of amoebae. Molecular Biology and Evolution, 34(9), 2258–2270.

Leontyev, D. V. (2006a). Vidovoj sostav miksomitsetov (Myxomycota) Natsionalnogo Prirodnogo Parka “Gomolshnaskie Lesa” (Ukraina) [Species composition of Myxomycota in Gomolsha Forests National Nature Park (Ukraine)]. Mikologiya i Fitopatologiya, 40(2), 101–107 (in Russian).

Leontyev, D. V. (2006b). Novye dlya Ukrainy vidy miksomitsetov (Myxomycota) [New records of myxomycetes in Ukraine (Myxomycota)]. Mikologiya i Fitopatologiya, 40(3), 218–230 (in Russian).

Leontyev, D. V., & Fefelov, K. A. (2012). Nomenclatural status and morphological notes on Tubifera applanata sp. nov. Mycotaxon, 120(2), 247–251.

Leontyev, D. V., & Schnittler, M. (2017). Phylogeny of myxomycetes. In: Myxomycetes. Biology, systematics, biogeography and ecology. Rojas Alvarado, C., & Stephenson, S. L. (Ed.). New York, Amsterdam, Elsevier. Pp. 83–106.

Leontyev, D. V., Dudka, I. O., Kochergina, A. V., & Kryvomaz, T. I. (2012). New and rare myxomycetes of Ukraine 3. Forest and forest-steppe zone. Nova Hedwigia, 94, 335–354.

Leontyev, D. V., McHugh, R., Fefelov, K. A., & Kochergina, A. V. (2011). New and rare myxomycetes of Ukraine 2. South-West Crimea. Nova Hedwigia, 92, 245–256.

Leontyev, D. V., Schnittler, M., & Stephenson, S. L. (2014). Pseudocapillitium or true capillitium? A study of capillitial structures in Alwisia bombarda (Myxomycetes). Nova Hedwigia, 99, 441–451.

Leontyev, D. V., Schnittler, M., Stephenson, S., Novozhilov, Y. K., & Shchepin, O. V. (2019). Towards a phylogenetic classification of myxomycetes. Phytotaxa, 399, 209–238.

Leontyev, D. V., Yatsiuk, I. I., & Kochergina, A. V. (2020). Vkliuchennia miksomitsetiv do Chervonoi Knyhy Ukrainy: Dotsilnist, kryterii vidboru ta rekomendovani vydy [Inclusion of myxomycetes in the Red Data Book of Ukraine: Feasibility, selection criteria and recommended species]. Ukrainian Botanical Journal, 77(3), 189–203 (in Ukrainian).

Macabago, S. A. B., Dagamac, N. H. A., dela Cruz, T. E. E., & Stephenson, S. L. (2017). Implications of the role of dispersal on the occurrence of litter-inhabiting myxomycetes in different vegetation types after a disturbance. Nova Hedwigia, 104, 221–236.

Mitchell, D. W. (2004). A key to corticolous Myxomycota. Systematics and Geography of Plants, 74, 261–285.

Novozhilov, Y. K., Rollins, A. W., & Schnittler, M. (2017a). Ecology and distribution of myxomycetes. In: Myxomycetes. Biology, systematics, biogeography and ecology. Rojas Alvarado, C., & Stephenson, S. L. (Ed.). New York, Amsterdam, Elsevier. Pp. 253–297.

Novozhilov, Y. K., Schnittler, M., Erastova, D. A., & Schepin, O. N. (2017b). Myxomycetes of the Sikhote-Alin State Nature Biosphere Reserve (Far East, Russia). Nova Hedwigia, 104, 183–209.

Novozhilov, Y. K., Schnittler, M., Erastova, D. A., Okun, M. V., Schepin, O. N., & Heinrich, E. (2013). Diversity of nivicolous myxomycetes of the Teberda State Biosphere Reserve (Northwestern Caucasus, Russia). Fungal Diversity, 59, 109–130.

Novozhilov, Y. K., Zemlianskaia, I. V., Schnittler, M., & Stephenson, S. L. (2006). Myxomycete diversity and ecology in the arid regions of the Lower Volga River Basin (Russia). Fungal Diversity, 23, 193–241.

Poulain, M., Meyer, M., & Bozonnet, J. (2011). Les myxomycètes. Dauphiné-Savoie, Sarl Editions.

Prylutskyi, O. V., Akulov, O. Y., Leontyev, D. V., Ordynets, O. V., Yatsiuk, I. I., Usichenko, A. S., & Savchenko, A. O. (2017). Fungi and fungus-like organisms of Homilsha Forests National Park, Ukraine. Mycotaxon, 132(3), 1–56.

Ricotta, C., & Podani, J. (2017). On some properties of the Bray-Curtis dissimilarity and their ecological meaning. Ecological Complexity, 31, 201–205.

Rojas, C., & Stephenson, S. L. (Eds.). (2017). Myxomycetes. Biology, systematics, biogeography and ecology. New York, Amsterdam, Elsevier.

Rollins, A. W., & Stephenson, S. L. (2011). Global distribution and ecology of myxomycetes. Current Topics in Plant Biology, 12, 1–14.

Romanenko, K. O. (2002). Miksomitsety osnovnykh roslynnykh uhrupovan Krymskoho pryrodnoho zapovidnyka [Myxomycetes of the main plant communities of the Crimea Nature Reserve]. Ukrainian Botanical Journal, 59(6), 730–736 (in Ukrainian).

Schnittler, M., Dagamac, N. H. A., Sauke, M., Wilmking, M., Buras, A., Ahlgrimm, S., & Eusemann, P. (2016). Ecological factors limiting occurrence of corticolous myxomycetes – a case study from Alaska. Fungal Ecology, 21, 16–23.

Schnittler, M., Novozhilov, Y. K., Shadwick, J. D. L., Spiegel, F. W., García-Carvajal, E., & König, P. (2015). What substrate cultures can reveal: Myxomycetes and myxomycete-like organisms from the Sultanate of Oman. Mycosphere, 6, 356–384.

Schnittler, M., Unterseher, M., & Tesmer, J. (2006). Species richness and ecological characterization of myxomycetes and myxomycete-like organisms in the canopy of a temperate deciduous forest. Mycologia, 98, 223–232.

Shchepin, O. N., Schnittler, M., Erastova, D. A., Prikhodko, I. S., Borg Dahl, M., Azarovd, D. V., Chernyaeva, E. N., & Novozhilov, Y. K. (2019). Community of dark-spored myxomycetes in ground litter and soil of taiga forest (Nizhne-Svirskiy Reserve, Russia) revealed by DNA metabarcoding. Fungal Ecology, 39, 80–93.

Spiegel, F. W., Stephenson, S. L., Keller, H. W., Moore, D. L., & Cavender, J. C. (2004). Mycetozoans. In: Biodiversity of Fungi. Inventory and monitoring methods. Mueller, G. M., Bills, G. F., & Foster, M. S. (Eds.). Amsterdam, Elsevier, Academic Press. Pp. 547–576.

Stephenson, S. L., & Schnittler, M. (2017). Myxomycetes. In: Handbook of the protists. Archibald, J. M., Simpson, A. G. B., Slamovits, C. H., Margulis, L., Melkonian, M., Chapman, D. J., & Corliss, J. O. (Ed.). Springer, New York. Pp. 1405–1432.

Stephenson, S. L., Schnittler, M., & Novozhilov, Y. K. (2008). Myxomycete diversity and distribution from the fossil record to the present. Biodiversity and Conservation, 17, 285–301.

Stephenson, S. L., Schnittler, M., Mitchell, D. W., & Novozhilov, Y. K. (2001). Myxomycetes of the Great Smoky Mountains National Park. Mycotaxon, 78, 1–15.

Takahashi, K. (2004). Distribution of myxomycetes on different decay states of deciduous broadleaf and coniferous wood in a natural temperate forest in the southwest of Japan. Systematics and Geography of Plants, 74, 133–142.

Takahashi, K., & Hada, Y. (2012). Seasonal occurrence and distribution of myxomycetes on different types of leaf litter in a warm temperate forest of Western Japan. Mycoscience, 53, 245–255.

Takahashi, K., & Harakon, Y. (2012). Comparison of wood-inhabiting myxomycetes in subalpine and montane coniferous forests in the Yatsugatake Mountains of Central Japan. Journal of Plant Research, 125, 327–337.

Urich, T., Lanzén, A., Qi, J., Huson, D. H., Schleper, C., & Schuster, S. C. (2008). Simultaneous assessment of soil microbial community structure and function through analysis of the metatranscriptome. PLoS One, 3, e2527.

Vlasenko, A. V., Novozhilov, Y. K., Asbaganov, S. V., & Dejidmaa, T. (2020). Methods and difficulties of identifying species in studies on the ecology and distribution patterns of spore organisms. Contemporary Problems of Ecology, 13(4), 346–359.

Yatsiuk, I. I., Leontyev, D. V., & Shlakhter, M. (2018). Myxomycetes of National Nature Park Slobozhanskiy (Ukraine): Biodiversity and noteworthy species. Nordic Journal of Botany, 1, e01605.

Published
2021-02-11
Section
Articles