Seasonal Patterns of Myxomycete Occurrences on …—383— Seasonal Patterns of Myxomycete...
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Seasonal Patterns of Myxomycete Occurrences on Varied Leaf-Litters in a Mixed Forest of Warm Temperate Western Japan
Kazunari Takahashia,* and Yumi iuchib
aOkayama University of Science High School, 1-1 Ridai-cho, Kita-ku, Okayama, 700-0005 JAPAN;bThe Himeji-City Nature Sanctuary, 915-6, Oichinaka, Himeji, 671-2233 JAPAN
*Corresponding author: [email protected]
(Accepted on October 19, 2014)
Seasonal myxomycete occurrence was examined for two years in a mixed forest of warm temperate western Japan. The deciduous tree leaves defoliate in late autumn and evergreen tree leaves defoliate in late April. Those newly defoliated leaf-litters were incubated in containers on the forest floor. Thirty-three myxomycete species were recorded from 1348 collected samples of both litter types; deciduous leaf-litter yielded 23 species and evergreen leaf-litter yielded 24 species, with 14 species common for both litter types. Eight species showed preference for deciduous leaf litter and 7 species for evergreen leaf litter. The fruiting bodies of myxomycetes appeared from late April to early November and 22 species occurred in a peak at late June. The fruiting season was divided into three seasonal phases by correspondence analysis based on species occurrence. The middle phase contained 28 species which accounted for 85% of the total number of species throughout the seasons. Characteristic seasonality of species was found in four species in the early phase, nine in the middle phase, and three in the late phase. Species with no overlap phase were seven species. Physarum roseum especially had remarkable seasonality from summer to early autumn of the late phase. Thus, different tree types of defoliation in a mixed forest influence species reproduction in seasons and yield greater species diversity of myxomycetes in warm temperate Japan.
Key words: Deciduous tree, evergreen tree, seasonal three phases, species diversity.
J. Jpn. Bot. 89: 383–393 (2014)
Myxomycetes are eukaryotic microorganisms, whose life cycle consists of a vegetative stage and a reproductive stage that produces the fruiting bodies that are used to identify myxomycetes in studies. The main biotopes for myxomycetes in terrestrial ecosystems are forests, and the organisms occur in association with decaying plant materials, i.e., leaf-litter and woody debris (Ing 1994). Newly fallen leaf litter on the forest floor is a particular habitat for myxomycetes (Takahashi 2011). However, few ecological studies have examined their occurrence and distribution on new leaf
litter on the forest floor. Most species of leaf-litter inhabiting myxomycetes (foliicolous myxomycetes) have fragile sporocarps, which are found only occasionally and tend to last only a short time on the forest floor. Thus, foliicolous species have rarely been closely examined.
In warm temperate regions of Japan, deciduous litter falls in autumn and evergreen litter falls in late spring. As the annual cycle of new leaf litter and its decomposition progresses, the varied leaf litter types should provide highly variable microhabitat for myxomycetes. We expect that both the defoliation season and tree
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accurate ecological understandings of foliicolous myxomycetes, by using the in-situ incubation method (Takahashi 2013), for accurate assessment of foliicolous myxomycetes present on the deciduous trees and evergreen trees in a mixed forest floor.
Materials and MethodsStudy site and leaf-litter incubation
The study site was situated in the 59-ha Himeji-City Nature Sanctuary, which is mostly covered with woods forming a typical secondary forest of the Seto Inland Sea region in western Japan. The Sanctuary is in Oichinaka, Himeji City, Hyogo Prefecture (34°51.33′N, 134°37.18′E, 80 m above sea level). The forest mainly consists of deciduous trees (Quercus
type would affect the microhabitat of foliicolous myxomycetes with respect to the seasonal occurrence and their substrate preference. The objectives of the present study are to verify the seasonal occurrence patterns of foliicolous myxomycetes in a warm temperate region of Japan. Although Takahashi and Hada (2012) have studied the seasonal occurrence of foliicolous myxomycetes, expanding investigation needs to get additional information including several forest types within the heterogeneous leaf-litter microhabitat in the same region. It is surprising that very little quantitative data of foliicolous myxomycetes exist, considering myxomycetes likely have a substantial role in nutrient cycling and the detritus food chain (Stephenson et al. 2011). The purpose of this study is to contribute
Fig. 1. Containers of leaf-litter masses on the forest floor and fruiting bodies of myxomycetes. A. Containers accumulating leaf litter of Quercus serrata trees. B. Fruiting bodies of Comatricha pulchella in the early seasonal phase on deciduous leaf-litter. C. Fruiting bodies of Didymium squamulosum in the middle seasonal phase on evergreen leaf litter. D. Fruiting bodies of Physarum roseum in the late seasonal phase. Bars = 1 mm.
December 2014 TheJournal of Japanese Botany Vol. 89 No. 6 385
serrata in the crown mixed with Prunus jamasakura) and evergreen trees (Quercus glauca and Ilex pedunculosa). The forest canopy reaches over 18 m in height. The understory and shrub layer is dominated by Q. serrata and Clethra barbinervis interspersed with Eurya japonica and young Q. glauca. The fallen leaves make a new, rich litter layer derived from two tree types, deciduous trees (Q. serrata and Prunus jamasakura) in late autumn and evergreen trees (Q. glauca and Ilex pedunculosa) in late spring.
Newly defoliated leaf litters were collected at sites under the dominant trees, i.e., for deciduous trees, Quercus serrata and Prunus jamasakura, and for evergreen trees, Ilex pedunculosa and Quercus glauca, on a southwest slope at altitudes from 65 m to 110 m. Two hundred liters of deciduous tree leaves were collected in early February, and evergreen tree leaves in late April, during their respective defoliation seasons. Then, their litter masses were incubated in the three containers (respectively 60 L in volume, 96 × 69 × 20 cm) by the in-situ incubation method (Takahashi 2013) on the same forest floor where they were collected. Three containers for
each tree species were incubated in the forest floor (Fig. 1A). All twigs over about 5 mm in diameter were removed from the litter masses. Each container had four small holes bored into the bottom to allow for adequate humidity from rainfall and to drain excess water. A plastic sheet was placed under each container to separate it from soil or humus on the forest floor.
At a neighboring study site, annual precipitation was 1465.5 mm, and the mean annual temperature was 15.5°C (2013, at a Japan Meteorological Agency observation point, 34°50.3′N, 134°40.2′E, 38.2 m above sea level). Hourly temperature and humidity measurements 30 cm above the forest floor in the study site were recorded from April to November 2013 using data loggers. Mean values of temperature and humidity data were averaged for 2-week periods over a year to illustrate seasonal changes in weather conditions (Fig. 2). The minimum air temperature of the forest floor peaked at 24.5°C in early August, and humidity peaked at 80.9% in late July during the rainy season (June to July). The maximum, minimum, and mean for temperature and humidity as climatic factors were examined in correlation with myxomycete
Fig. 2. Variation in 2-week averages in humidity and minimum temperature on the forest floor of the study site (2012). X-axis indicates survey codes—Ap2 represents the last two weeks of April and M1 represents the first two weeks of May; all subsequent months follow similar naming system.
386 植物研究雑誌 第 89巻 第 6号 2014年 12月Ta
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December 2014 TheJournal of Japanese Botany Vol. 89 No. 6 387
occurrence.
Sampling and identifying of myxomycetesThe occurrence of myxomycete fruiting
bodies in the leaf litter was observed with both the naked eye and loupes at approximately 2-week intervals from April to November for two years (2012–2013). The fruiting that occurred was removed from the containers, allowed to dry, and then glued inside a small paper box, for long-term storage. The number of myxomycete occurrences was defined as the number of leaves and twigs to which three or more sporocarps adhered (considered a sample). If myxomycete sporocarps occurred on a leaf fragment that was ≤1 cm2 in area or on a twig that was ≤1 cm in length, the samples were excluded from analyses. One leaf usually contained 1 species of myxomycete; there were only a few leaves with multiple species. The collected specimens were identified under the microscope, and the nomenclature followed that of Yamamoto (1998, 2006), referring to Lado (2001).
Species richness and characteristic species of myxomycetes were compared between the deciduous tree leaves and the evergreen tree leaves and across surveyed months and seasons. The relative abundance of myxomycetes was calculated by the proportion of samples in every 2-week period to the total number of samples on the deciduous or evergreen leaves throughout the field season.
Data analysis of myxomycete assemblagesThe study period was divided into 14
periods of 2 weeks each from late April to early November, as described in the survey codes in Table 1. The study data from the two years contained assemblages by two-week steps on deciduous and evergreen leaves throughout the fruiting season, and they were periodically combined into 12 total assemblages in a seasonal change series. To examine patterns in the species composition of the assemblages in
relation to periodical change, the data matrix of values of the myxomycete assemblages was analysed using correspondence analysis (CA; Hill 1974), which is used for ordination analysis of the myxomycete assemblages (Schnittler and Stephenson 2002) and reveal for species with unimodal responses to the underlying parameters. Then, cluster analysis (Ward’s Method) was carried out depending on the scores of the first 2 axes in the correspondence analysis. According to the blade with bootstrap proportions of ≥70% (Hillis and Bull 1993), the 12 assemblages were classified into 3 groups. For the ordination method used to reveal the relationship among the myxomycete assemblages, the numbers of samples of species in assemblages were computed using the computer application PAST (Hammer et al. 2001; http://folk.uio.no/ohammer/past/).
Test for species characteristicsThe numbers of samples of myxomycete
species between the two leaf types, deciduous or evergreen, and those among 3 seasonal phases were analysed using Fisher’s exact probability test of independence (e.g., Sokal and Rohlf 1973). When the frequency of a species on any tree type was significantly higher (p < 0.01) than 0 according to Fisher’s exact probability test, the species was considered to occur frequently in association with a particular tree type or seasonal phase, with the exception of those species with <5 total samples. Analysis of variance was performed using the Excel statistics version 5.0 software package (Esumi Co. Ltd. 2001).
ResultsMyxomycete species on litters
The leaf-litter containers created nurseries for myxomycete growth on the forest floor and assisted in quantifying myxomycete occurrence (Fig. 1A). Throughout the study, 1348 samples yielded 33 myxomycete species (with varieties treated as species), with 23 species on deciduous leaf litter and 24 species on evergreen leaf litter
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(Table 1). The species richness of myxomycetes did not appear to be different between the types. However, only 14 species were common to both tree types. Twenty species occurred in five or more samples. The most abundant and dominant species, which occurred in 100 samples (7.4% of all samples) or more were Physarum melleum, followed by Physarum cinereum, Craterium minutum, Didymium squamulosum, and Didymium nigripes. Species of Physarales, including from the genera Physarum, Didymium, Craterium, Diderma, Fuligo, and Diachea, represented 29 species, which equaled to 88% of all species and reached 96% of all litter samples.
The species composition of assemblages was rather different between the litter types (Table 1). Several species clearly showed a preference between the types based on Fisher’s exact probability test. The characteristic species on evergreen leaves included Physarum cinereum, Didymium squamulosum, Didymium nigripes,
Diderma effusum, Diderma simplex, and Didymium iridis, and the species characteristic of deciduous tree leaves included Physarum melleum, Craterium leucocephalum var. cylindricum, Diderma saundersii, Physarum bivalve, Comatricha pulchella, Didymium serpula, Didymium minus, and Physarum serpula. Species of Physarum and Comatricha significantly preferred deciduous tree litter, while species of Didymium and Fuligo significantly preferred evergreen tree litter (Fig. 3).
Seasonal patterns of myxomycete occurrenceSpore production began in late April,
when only 2 myxomycete species occurred on deciduous tree leaves (Fig. 4). The fruiting season lasted from late April to early November; the relative abundance of myxomycete samples showed a remarkable peak in early July on both types of tree leaves, and in late June, species richness peaked on both types of tree
Fig. 3. Comparison of relative abundance on deciduous and evergreen leaf litter by 10 genera that appeared on the forest floor. Significant differences in frequencies between leaf-litter types by exact probability test of independence **p < 0.01.
December 2014 TheJournal of Japanese Botany Vol. 89 No. 6 389
leaves, with 22 species. The appearance of myxomycetes returned subsequently in late August to September and then fruiting decreased in early November. Although myxomycete occurrence exhibited similar seasonal patterns between both types of tree leaves, the starting and ending of myxomycete occurrences were different, i.e., being later on the evergreen than deciduous tree leaves, and ending sooner on evergreen leaves. The changes in total species richness on both types of leaves were significantly correlated with the minimum and average temperatures and with humidity, with a higher correlation with minimum than average values (Table 2). However, the abundance of
samples had no remarkable correlations.Twelve myxomycete assemblages from
both leaf-litter types from monthly field studies (Table 1) were ordered by calculation of the correspondence analysis. The scores of the first 2 axes showed in biplots the similarity of the assemblages (Fig. 5). Assemblages were divided into 3 groups by cluster analysis, which indicated 3 fruiting seasons: late April to early June (early phase), late June to early August (middle phase), and late August to early November (late phase).
Seasonality of myxomycete speciesOccurrence patterns of twenty species with
five or more samples were indicated for three
Fig. 4. Occurrence patterns of myxomycetes on deciduous and evergreen leaf-litter masses during the entire fruiting season. A. Seasonal change in the relative abundance of samples. B. Seasonal change in species richness.
390 植物研究雑誌 第 89巻 第 6号 2014年 12月
seasonal phases (Table 3). Thus, 16 species clearly showed a preference for a distinctive seasonal phase according to Fisher’s exact probability test. The species composition of the myxomycete assemblage clearly shifted from late April to early June to late June to early August and again from late August to early November. The characteristic species in the early phase were four species: Didymium serpula, Comatricha pulchella (Fig. 1B), Didymium melanospermum, and Collaria rubens. The middle phase had nine
characteristic species: Physarum melleum, P. cinereum, Craterium minutum, D. squamulosum (Fig. 1C), D. nigripes, Craterium leucocephalum var. cylindricum, Physarum bivalve, P. serpula, and Diderma simplex. The late phase had three characteristic species: Physarum roseum (Fig. 1D), D. saundersii, and Diderma effusum. Thus, 48% of species had clear seasonal changes across the fruiting season. Occurrence pattern of three species, Physarum melleum, P. cinereum, and Diderma saundersii, appeared in all
Table 2. Correlations between myxomycete occurrence and climatic factors. Significance differences **p < 0.01, *p < 0.05
Species richness Abundance of samplesTemperature (ºC) Maximum 0.506 0.351 Minimum 0.643* 0.434 Average 0.584* 0.394Humidity (%) Maximum 0.524 0.415 Minimum 0.733** 0.480 Average 0.678** 0.460
Fig. 5. Arrangement of myxomycete assemblages from a monthly field survey using correspondence analysis based on the first 2 scores. Twelve seasonal assemblages were statistically divided into three groups. Early phase. Late April to early June. Middle phase. Late June to early August. Late phase. Late August to early November. According to the blade of cluster analysis (Ward’s method) with bootstrap proportions of ≥70%. Abbreviations indicate the survey codes as given in Table 1.
December 2014 TheJournal of Japanese Botany Vol. 89 No. 6 391
phases, whereas they had significantly greater abundance in a particular season to indicate seasonality. And also species with overlap in two phases were six species, whereas they preferred a particular season. Species with no overlap were seven species. Physarum roseum especially had remarkable seasonality from summer to early autumn of the late phase.
DiscussionLeaf-litter-mass containers (Takahashi 2013)
can be used to measure ecological characteristics excluding the soil on foliicolous myxomycetes inhabiting natural forest floors, allowing for statistical analysis of temporal changes associated with leaf-litter types. The leaf-litter masses provided adequate microhabitat for myxomycetes to grow and complete their life cycles. Newly defoliated leaf litters seasonally
supplied adequate microhabitats and foods for myxomycetes under natural conditions on the forest floor. Consequently, seasonality of foliicolous myxomycetes was classified into 3 seasonal phases associated with the microhabitats represented by newly defoliated leaf litters of deciduous or evergreen trees in a mixed forest.
The values for species richness obtained in the current study was 33 species, to be rather high when compared to other studies. Stephenson (1989) found 34 species of foliicolous myxomycetes using the moist chamber culture technique in five forest areas in the Mountain Lake area of southwestern Virginia. A study carried out in an oak-hickory forest of Arkansas, USA represented 21 species (Rollins and Stephenson 2012). However, the species richness in the present study was less
Table 3. Relative abundance of 20 species that appeared in five or more samples in distinctive seasonal phases and their preference to leaf-litter types. Significant differences in frequencies among the three seasonal phases by exact probability test of independence **p < 0.01, *p < 0.05
Seasonal phasePreferenceEarly Middle Late
Didymium serpula 21.1** 1.5Comatricha pulchella 19.7** 2.8 DDidymium melanospermum 18.3** 0.1Collaria rubens 7.0**Physarum melleum 11.3 18.1* 11.4 DPhysarum cinereum 7.0 17.2** 8.9 ECraterium minutum 13.9**Didymium squamulosum 10.6** EDidymium nigripes 9.7** ECraterium leucocephalum var. cylindricum 7.0** 0.6 DPhysarum bivalve 1.4 6.0** DPhysarum serpula 2.1* DDiderma simplex 1.7* EPhysarum roseum 35.4**Diderma saundersii 4.2 1.5 33.5**Diderma effusum 1.0 8.9** EDidymium minus 4.2 2.2 DDidymium iridis 1.3 EPhysarum oblatum 1.4 0.6Fuligo gyrosa 0.5
Abbreviations. Early. Late April to early June. Middle. Late June to early August. Late. Late August to early November. D. Deciduous leaf litter. E. Evergreen leaf litter.
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than the 45 species found in a previous study in the same region, which were recorded for three years on the leaf litter of four tree species, including Cinnamomum camphora (Takahashi and Hada 2012). The results of this investigation not only depend on the assessment technique but also may be influenced by tree species, since several foliicolous myxomycetes have preference for particular tree leaves and microhabitat on the forest floor (Takahashi 2013).
Stephenson (1989) indicated that several species showed distributional trends for deciduous or coniferous litter and that Arcyria cinerea was an exceedingly common species. In the warm temperate region of Japan, Physarum melleum and Physarum cinereum were abundant and common species on leaf litter as shown in this as well as a previous study (Takahashi and Hada 2012). Several dominant species of myxomycete assemblages have preferences for tree species, either the deciduous or the evergreen leaves of broadleaf trees (Takahashi 2013). Cavender and Raper (1968) demonstrated that the dominant cellular slime mold species in the soil were related to the dominant trees in the forest canopy. Thus, it is presumed as an aspect of myxomycete ecology that different types of leaf litter defoliated during different seasons yield different myxomycete assemblages in a temperate mixed forest, thereby increasing the myxomycete species diversity.
Foliicolous myxomycetes occurred on different types of leaf litters under the influence of seasonal changes in minimum temperature and humidity, affirming the results of previous studies in the same climate region (Takahashi and Hada 2012). Most of the myxomycetes (28 species, 85% of species) fructified sporangia during late June to late July under warm temperatures and >70% humidity. The temporal pattern of species distribution consisted of three seasonal phases in the warm seasons with increasing or decreasing temperature and humidity. The present study confirmed the general view that, as long as temperature
and moisture conditions are appropriate, myxomycetes are productive and fruiting with prominent diversity (e.g., Elliot and Brazier 1933, Stephenson 1988, Tran et al. 2006, Ko Ko et al. 2011, Takahashi and Hada 2012).
On the seasonality of species, at the beginning of the fruiting season, Didymium melanospermum was the chief myxomycete on deciduous leaves, replaced in the middle phase by Physarum melleum, P. cinereum, Didymium nigripes, D. squamulosum, Craterium leucocephalum var. cylindricum, and C. minutum. In September in the late phase another species, Physarum roseum, specifically occurred. The deciduous leaves defoliate in late autumn and decompose. On the other hand, evergreen leaves defoliate in late April and immediately decompose. Certain species strongly appear to occur in association with the decomposition state of leaf litter (Takahashi 2011), and foliicolous myxomycete occurrence may be adaptive to the annual leaf defoliation time and the progression of decomposition.
Myxomycetes may play a role in nutrient cycling in woodlands (Rayner and Boddy 1988). In a subtropical monsoon area in India, seasonal changes in temperature and humidity were shown to be related to patterns of fungal and bacterial communities on newly fallen leaves of the alder Alnus nepalensis D. Don. (Kayang 2001). Food supply, i.e., nourishment from seasonal decomposition of leaves and bacteria, may be a potential factor regulating changes in myxomycete species composition. Thus, seasonality was shown as an interesting parameter for further complete understanding of the distribution and ecology of myxomycetes in terrestrial forest ecosystems.
We thank the Himeji-City Nature Sanctuary of Himeji City, Hyogo Prefecture, for allowing us to use the facilities. Furthermore we thank Ms. Takako Nomura who conducted collecting leaf-litters and sampling of the myxomycete fruiting bodies in the study site.
December 2014 TheJournal of Japanese Botany Vol. 89 No. 6 393
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高橋和成 a,井内由美 b:西日本の暖温帯の混交林における落葉生変形菌の季節的発生パターン 西日本の暖温帯の混交林で,季節的に発生する落葉生変形菌を 2年間にわたって調査した.晩秋に落葉する落葉広葉樹と 4月下旬に落葉する常緑樹で,それぞれの新規落葉をコンテナに蓄積し林床で自然培養したところ,全体で 1348の採集標本から 33種の変形菌が出現した.落葉広葉樹には 23種,常緑樹には 24種が出現し,14種が共通して出現した.樹種タイプに選好性を示した種は,落葉広葉樹に 8種,常緑樹に 7種であった.変形菌の子実体は 4月下旬から 11月上旬に観察され,6月下旬に最多の 22種が出現した.各種の出現頻度に基づいた対応分析から結実季節は 3つの時期に
分けられ,中期(6月下旬~ 8月上旬)に出現種の 85%(28種)が出現した.出現種の季節性は,初期(4月下旬~ 6月上旬)に 4種,中期に 9種,後期(8月下旬~ 11月上旬)に 3種が特徴的に認められた.特に,アカモジホコリ Physarum roseumは,晩夏から初秋に出現した.暖温帯の混交林を構成する異なる樹種や落葉時期は,変形菌の季節的な発生に影響を与え,変形菌の種多様性を高めている.
(a岡山理科大学附属高校,b姫路市自然観察の森)