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1 Corticolous Myxomycetes and Other Epiphytic Cryptogams on Seven Native Tree Species in Hunan Province, China Author(s): Marja Härkönen, Jouko Rikkinen, Tarja Ukkola, Johannes Enroth, Viivi Virtanen, Kimmo Jääskeläinen, Eija Rinne, Laura Hiltunen, Sinikka Piippo and Xiaolan He Reviewed work(s): Source: Systematics and Geography of Plants, Vol 74, No 1 (2004), pp Published by: National Botanic Garden of Belgium Stable URL: Accessed: 25/01/ :07 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive We use information technology and tools to increase productivity and facilitate new forms of scholarship For more information about JSTOR, please contact support@jstororg National Botanic Garden of Belgium is collaborating with JSTOR to digitize, preserve and extend access to Systematics and Geography of Plants
2 Syst Geogr Pl 74: (2004) Corticolous myxomycetes and other epiphytic cryptogams on seven native tree species in Hunan Province, China Marja Hiirk6nen, *, Jouko Rikkinena, Tarja Ukkolaa, Johannes Enrotha, Viivi Virtanena, Kimmo Jaaskelaiiinena, Eija Rinnea, Laura Hiltunena, Sinikka Piippob & Xiaolan Heb adepartment of Biological and Environmental Sciences, University of Helsinki, POBox 65, FIN Helsinki, Finland bfinnish Museum of Natural History, University of Helsinki, * author for POBox 7, FIN Helsinki, Finland correspondence [marjaharkonen@kolumbusfi] Abstract - This study examines the diversity and ecology of myxomycetes on seven native tree species in Hunan Province, south-central China All the trees are being cultivated within less strictly protected parts of Badagongshan National Nature Reserve and similar forest reserves Community data were collected for epiphytic bryophytes and lichens and corticolous myxomycetes The data on myxomycetes were acquired by cultivating bark samples in moist chambers Over 80 % of the 200 moist chambers yielded identifiable myxomycete specimens, representing 33 different taxa There were clear differences in epiphyte community composition between the studied tree species Non-metric multidimensional scaling (NMS) was used to produce graphical depictions of community relationships and habitat variables The three tree species with neutral or slightly acid bark had similar epiphyte communities, while each of the other four species grouped separately The main trend in myxomycete diversity contrasted with those of epiphytic bryophytes and lichens Species richness of myxomycetes was highest on relatively acidic bark with a high water retention capacity, while the diversities of epiphytic bryophytes and lichens were highest on less acidic and relatively smooth bark Data on epiphyte community composition can be used to develop simple and cost-effective methods for preserving biodiversity in local forestry It can assist in the choice of an optimal tree species composition for forest plantations in buffer zones of nature reserves and in other areas where maintaining biodiversity is a major concern Key words: corticolous myxomycetes, epiphyticryptogams, associations of cryptogams, China, Hunan 1 Introduction Hunan Province is located in south-central China between 24?39"-30?08" N and T ' E It lies within the subtropical and warm temperate vegetation zones and covers an area of J Rammeloo & A Bogaerts (eds) ICSEM 4 Proceedings of the Fourth Internaional Congress on Systematics and Ecology of Myxomycetes Systematics and Geography of Plants is subjecto copyright All rights reserved? 2004 National Botanic Garden of Belgium Permission for use must always be obtained from the National Botanic Garden of Belgium ISSN
3 Syst Geogr Pl 74 (2004) Proceedings ICSEM 4 ca 212,000 km2 Most of the ca 60 million inhabitants live in and cultivate lowlands around the river Yangtze and its tributaries The relatively inaccessible highlands are more sparsely populated and mostly covered by forest The dominant primeval vegetation type in the region is evergreen broad-leaved forest, with an upper limit at m in the north and m in the south About 5000 species of vascular plants have been reported from Hunan Province The area is also rich in non vascular plants and fungi, but these groups have not been surveyed systematically Since 1982 several nature reserves have been established in Hunan Province The most famous one is Zhangjiajie, which is included in the List of World Heritages of UNESCO Forests and woodlands cover about half of the land area in Hunan Province and the Chinese authorities plan to further increase their proportion For the needs of reforestation and environmental protectionew information is required especially about lower plants and fungi Prof Timo Koponen, a well-known expert of Asian bryophytes, has been in co-operation with the Forestry Department of Hunan Province since 1997, and in September 1999 the research station of Badagongshan National Nature Reserve in NW Hunan was established as a field station of the University of Helsinki (Hiirknen 2000) Several projects dealing with the cryptogam flora of Hunan Province are in progress and some results have already been published or are in press (Koponen& al 2000, Potemkin 2000, Rikkinen 2000, Ukkola & al 2001, Enroth & Koponen 2003, Hark6nen & al 2004, Jusl6n 2004, Koponen & al 2004, Ignatov & al 2004, Potemkin & al 2004, Vaifia & al 2004) When we began our work, only 16 species of myxomycetes had been reported from Hunan Province The 872 identified specimens collected by us in have subsequently increased this number to 127 species (Hiirk6nen & al 2004) In September 2000 a group of scientists and advanced students from the University of Helsinki conducted field work in the forests of Badagongshan In addition to systematic collecting for floristic studies, we made a joint sociological study of cryptogamic epiphytes on seven native tree species These tree species, among others, are being cultivated as limited, short-rotation monocultures in the less strictly protected parts of the Nature Reserve and they are of considerableconomic importance in Hunan as a whole Our aim was to collect basic data of epiphyte community composition on the different trees and to find out which of them are the most favourable hosts for different groups of cryptogamic epiphytes Community data was collected for epiphytic bryophytes, lichens, filamentous cyanobacteria and green algae, and myxomycetes The data on corticolous myxomycetes were acquired by cultivating bark samples in moist chambers An overall goal of our project is to develop simple and cost-effective methods for preserving biodiversity and environmental quality in local forestry Such methods are urgently needed within and around conservation areas where maintaining biodiversity is a primary concern 2 Material and methods Community data of corticolous cryptogams were collected from several foreststands at elevations of metres A total of 100 trunks of seven different tree species were studied: Liriodendron chinense (Magnoliaceae), Magnolia officinalis (Magnoliaceae), Metasequoia glyptostroboides (Taxodiaceae), Phellodendron chinense (Rutaceae), Pterostyrax psilophyllus (Styracaceae), Sassafras tzumu (Lauraceae), and Tapiscia sinensis (Staphyleaceae) For each tree species, 15 trunks were surveyed, except for Liriodendron with 10 studied trunks Trunk size varied considerably between tree species with the mean circumference (at height of I m) ranging from 47 cm in Magnolia and 57 cm in Phellodendron to 198 cm in Sassafras and 234 cm in Metasequoia The size differences reflect differences in rotation-times: the two former tree species are cultivated for the bark of young stems, while the latter two are mainly used for timber The composition of the epiphyte community on each trunk was determined from a cylindrical sample plot around the trunk (05-15 m) Voucher specimens were collected and the abundances (in cover classes) of different physiognomic groups of bryophytes and lichens were estimated Two bark samples from the south- and north-facing trunk surface, respectively, were collected for moist chamber cultures During cultivation the ph of each bark sample was determined This was done after 190
4 M Hirkinen & al, Corticolous myxomycetes and other epiphyticryptograms soaking the bark in distilled water (adjusted with KOH to ph 7) for two days Additional bark samples were collected for determining conductivity, water-retaining capacity and the distribution/structure/abundance of lenticels, fissures and ridges in the bark of each tree species These data were included as explanatory variables in subsequent analyses The water-holding capacity of bark was determined as follows The bark specimen was first dried for six weeks at room temperature After weighing the sample was soaked in distilled water for 24 hours The saturated specimen was then placed on filter paper on a hopper and kept there until no more water was released from the hopper After this the bark specimen was reweighed and the water holding capacity was calculated as percentage of dry weight All myxomycetes from the moist chamber cultures were identified to species, except for a few incompletely matured specimens that could only be identified to genus Also all epiphytic bryophytes, lichens and filamentous cyanobacteria will eventually be identified to species However, at present many of these organisms could only be identified to genus or family and some lichen taxa were pooled into physiognomic groups (eg white sorediate crusts) Non-metric multidimensional scaling (NMS) from the statistical package PC-ORD (McCune& Medford 1997) was used to produce graphical depictions of community relationships and habitat variables NMS is a non-parametric ordination technique and well suited to data that are non-normal, are on discontinuous scales, and contain a large proportion of zero values The raw data matrix was 100 sample units (tree trunks) x 119 taxa (cryptogamic epiphytes) Only presence or absence was recorded for each taxon in each sample unit In order to reduce noise from rare taxa, all taxa that occurred on less than five tree trunks were deleted from the data set, resulting in a matrix of 100 sample units x 65 taxa Species data were then transformed with the Beals smoothing function This transformation smoothes the pattern of joint occurrences of species and facilitates the extraction of the major patterns in community data (McCune 1994) Presence/absence data are replaced with quantitative values (range 0-1 inclusive) that represent the probability of a species occurring in a particular sample unit based on the other species that were also present in that sample The smoothing was done because even after exclusion of rare taxa the data set remained heterogeneous with a large number of zeros in the matrix Notable increases in the strengths of correlations between ordination scores and biologically relevant environmental variables provided evidence tha the transformation had improved the analysis The NMS was performed using the quantitative version of Sorenson's distance measure, 100 iterations, and random starting coordinates The program was run many times with different starting configurations to ensure that the obtained minimum stress was not a local minimum A two dimensional ordination of the data matrix was produced after determining that higher dimensional solutions did not substantially reduce stress The stability of the solution was examined by plotting stress vs iterationumber, and the probability that a similar final stress could have been obtained by chance was determined by using a Monte Carlo test Habitat variables were superimposed on the resulting ordination using a joint plot, based on the correlations (r) of explanatory variables with the axes of the community ordination For visual clarity, the ordination was rigidly rotated to load one environmental factor (conductivity) the vertical axis Variancexplained was expressed by the coefficient of determination between distances in the ordination space and distances in the original species space (McCune & Medford 1997) 3 Results A total of 162 myxomycete specimens developed from the 200 moist chambers prepared Thus, 81 % of the cultures yielded identifiable specimens The real productivity was higher, as unidentifiable plasmodia, sclerotia, and poorly matured fruiting-bodies were not recorded Furthermore, if an individual myxomycete species emerged more than once from the same moist chamber, all the material was treated as one specimen Thirty-three taxa of myxomycetes developed from the moist chambers Most of these were species with wide, more or less cosmopolitan distributions (table 1) Several patterns in myxomycete diversity were correlated to variation in substrate quality and/or epiphyte community composition In the NMS ordination the two axes explained 975 % of community variation (fig 1) Afterotation, 66 % of the variation was explained by axis 2, aligned with the conductivity of the bark of the different tree species (r = 81) This axis was also positively correlated with the abundance of lenticelles in the bark of the tree species (r = 70), and with the ph of bark (r = 74) and the diversity of epiphytic bryophytes on the sample plots (r = 56) It was negatively correlated with the water retention capacity (r = -63) and abundance of ridges (r = -75) and fissures (r = -50) in the bark of the tree species The second axis (axis 1), representing 315 % of the community variation, was correlated with the abundance of fissures in the bark of the tree species (r = 60), and with the diversity of epiphytic bryophytes (r = 50) and lichens (r = 50) on the sample plots All these interdependent variables are shown as vector overlays in fig 1 191
5 Syst Geogr Pl 74 (2004) Proceedings ICSEM 4 Table 1 Myxomycete species harvested from the 200 moist chambers cultured during this study The nomenclature is according to Lado (2001) The tree species are arranged in the order of increasing bark ph Sass = Sassafras, Meta = Metasequoia, Phel = Phellodendron, Pter = Pterostyrax, Tapi = Tapiscia, Liri = Liriodendron, Magn = Magnolia Species Sass Meta Phel I Pter Tapi Liri 1Magn Arcyria cinerea x x - x x - - Clastoderma debaryanum x x - x Colloderma oculatum x x C robustum x Craterium sp - - x Cribraria confusa x C microcarpa x Diacheopsis sp x - Diderma chondrioderma x x D deplanatum x x - x D simplex - x Didymium bahiense x D clavus x - - D iridis - - x - x x x D megalosporum - - x D squamulosum - - x - - x x Echinostelium apitectum x E minutum x x Enerthenema berkeleyanum x Licea biforis - x x - L erecta - - x L operculata - x - x L parasitica x x L pusilla x Paradiacheopsis longipes x P solitaria x Perichaena chrysosperma - x x x P depressa x - - Physarum sp - x - x P compressum - - x P xanthinum x - - Symphytocarpus trechisporus x Trichia subfusca - x Number of species I Myxomycete species diversity was negatively correlated (r = -34) with axis 2 (fig 2) The distribution of non-productive trees (cultures producing 0-1 myxomycete species) was rather intermixed, but there was a strong tendency for the most productive trees to ordinate low on axis 2 As already mentioned, this axis was correlated positively with bark ph and conductivity, and negatively correlated with the water retention capacity of the bark Eighty-three myxomycete specimens originated from bark collected from south-facing trunk surfaces, while 79 specimens originated from north-facing surfaces Thus, we did not find notable differences in productivity between different trunk expositions, possibly because this effect was hidden by differences in canopy shading and other site-dependent variables Many myxomycete species had clear distributions in the ordination (fig 3) For example, Cribraria microcarpa (r = 46) and C confusa (r = 35) were positively correlated with axis 1, while Didymium iridis (r = 49) was positively correlated with axis 2 Cribraria microcarpa (r = -48), Clastoderma debaryanum (r = -38), Licea parasitica (r = -36), and Cribraria confusa (r = -34) 192
6 M Harkonen & al, Corticolous myxomycetes and other epiphyticryptograms Magnolia * U m m ph El EOO Conductivity DOiEEl Tapsicia Le[El Lirio i n Lrm Bryophyte diversity mm m E, m m Phello Ptero Lichen diverstity A(N 0? Fi Water 0 0 retention Ri% 0 0 R0 O0 O 0 0 Metasequoia 400 O 4? 0? Sassafras Axis 1 Figure 1 NMS ordination of sample plots on 100 host trees, representing 10 Liriodendron chinense (+) and 15 each of Magnolia officinalis (n), Tapiscia sinensis (0), Pterostyrax psilophyllus (+), Phellodendron chinense (+), Sassafras tzumu (e), and Metasequoia glyptostroboides (0), in epiphyte space (65 taxa of bryophytes, lichens and myxomycetes) The ordination shows how the studied trees group according to similarities in epiphyte community composition Correlation vectors radiating from the ordination centroid show trends of increasing bark ph and diversity of epiphytic bryophytes and lichens on the sample plots Also differences in conductivity, water retention capacity and the abundance of lenticelles (Le), fissures (Fi) and ridges (Ri) in the bark of different tree species are shown Note that myxomycete diversity did not correlate linearly with the two ordination axes (fig 2) 193
7 Syst Geogr P1 74 (2004) Proceedings ICSEM 4 S Tapiscia l Magnolia Lirio * U a * Phello=I U *~ PteO i i m """ a MEm mm Metasequoia Sassafras Axis 1 Figure 2 Myxomycete diversity on the 100 tree trunk sample plots (data from S- and N-facing surfaces pooled) The underlying ordination is the same as in fig 1 (sample plots in epiphyte species space) Square sizes correspond with the number of myxomycete species (0-6) from moist chamber cultures of bark from each sample plot were negatively correlated with axis 2 While most species were concentrated in the higher diversity sample plots, D iridis and C debaryanum spread relatively widely across the ordination (fig 3) These two species were clearly segregated on axis 2, with D iridis favouring sample plots with exceptionally high bark ph Conversely, some myxomycete species, like Didymium squamulosum, were concentrated tree trunks with neutral or slightly acidic bark These taxa grouped in the middle of the ordination and did not show notable correlations with the two ordination axes (fig 3) Fig 4-5 and tables 1-2 give additional information of the distribution of corticolous myxomycetes on the seven tree species studied 194
8 M Hiirk6nen & al, Corticolous myxomycetes and other epiphyticryptograms * Tapiscia Magnolia El I r- Lirio - O 2 a #0 -Ptero S Phello 0 0 MetasequoiaSassafras Sassafras L Didymium iridis 1 Didymium squamulosum * Clastoderma debaryanum Axis 1 Figure 3 Overlayshowing presence of three common myxomycete species on the studied trees The underlying ordination is the same as in fig 1 and 2 4 Discussion The productivity values of moist chamber cultures of this study can be directly compared to those from our earlier studies (Harkonen& Ukkola 2000) The overall productivity of bark specimens from Badagongshan was high, we have previously found similarly high productivities only from Mediterranean regions In our studies in tropical Africa the productivities were somewhat lower and in boreal regions much lower In Badagongshan the number of myxomycete species per culture was 016 This is much higher than the values that we have previously recorded from boreal and 195
9 Syst Geogr Pl 74 (2004) Proceedings ICSEM M Hepatics 40 Mosses M Lichens * Myxomycetes 20 0 lb< " Figure 4 Number of taxa in different epiphyte groups on all tree species studied The trees are arranged in order of increasing myxomycete diversity, which corresponds with decreasing bark ph (table 1) Table 2 Number of taxa in different epiphyte groups on the studied trees Also the ph range and water holding capacity (% of dry weight) of bark is shown for each tree species Tree Myxomycetes Lichens Mosses Hepatics Total ph Retention Liriodendron Magnolia Metasequoia Phellodendron Pterostyrax Sassafras Tapiscia temperate forests in Finland (Europe) and Oregon (USA), but slightly lower than those from Mediterranean Turkey, and tropical Tanzania and the Gambia (Harkonen& Ukkola 2000) The lower trunks of living trees in Badagongshan support a rich flora of epiphytic bryophytes and lichens (fig 1 & 4, table 2) There are also clear differences in epiphyte community composition between local tree species The three tree species with moderately acid bark (Liriodendron, Phellodendron, Pterostyrax) clustered closely together on the basis of epiphyte community composition (fig 1) Conversely, each of the other four tree species grouped separately, indicating that they all have distinctive features in epiphyte community composition Interestingly, a high diversity of epiphytic bryophytes and lichens did not indicate a similarly high diversity of corticolous myxomycetes (fig 4) According to our present results, high myxomycete richness was generally associated with acidic bark with a high water retention capacity (fig 2) Conversely, the diversity 196
10 M Harkonen & al, Corticolous myxomycetes and other epiphyticryptograms Echinosteliales Trichiales M Stemonitales 0 Physarales 0 Licheales ~\o \~ ~ 1+ Figure 5 All myxomycete specimens according to taxonomic position and host tree The host trees are arranged in order of decreasing bark ph of epiphytic bryophytes and lichens was highest on less acidic and relatively smooth bark (fig 1 & 4) The stringy bark of Metasequoia glyptostroboides had an exceptionally high water holding capacity of more than five times of the dry weight of the bark itself (table 1) Also the bark of Sassafras tzumu was able to store large amounts of water High water holding capacities may be directly beneficial for corticolous myxomycetes as their active plasmodia are highly dependent on the availability of liquid water On the other hand, also epiphytic bryophytes and lichens can hold considerable amounts of water, but in our data high epiphyte cover did not act to increase myxomycete diversity Similar observations have also been made in the humid forests of western North America and it is possible that some secondary metabolites of cryptogamic epiphytes, like usnic acid and other lichen compounds, may play a role in this phenomenon (Ukkola& Rikkinen 2000) The thin trunks of young Magnolia officinalis trees represented an unfavourable habitatype for almost all epiphyte species The smooth, basic bark had a low water holding capacity and supported low diversities of myxomycetes, bryophytes and lichens However, trunk circumference, as such, was not found to be a very important determinant of epiphyte community composition in our study This pilot study has dealt with cryptogam diversity on several economically important native trees in south-central China Similar studies are urgently needed for a better understanding of the effects of local forestry practices on epiphyte diversity The results can be used when planning forest use in areas where maintaining high biodiversity is a primary concern, such as in buffer zones around national parks and othe reserves 197
11 Syst Geogr Pl 74 (2004) Proceedings ICSEM 4 Acknowledgements - This research was done in cooperation with the Forestry Department of Hunan Province and its Forest Botanical Garden, and the Division of Systematic Biology, Department of Ecology and Systematics, and the Botanical Museum, University of Helsinki The project was made possible by financing from the Academy of Finland (project no 44475) and the Finnish-Chinese Botanical Foundation We want to thank Prof Emeritus Timo Koponen, who's enthusiastic interest the cryptogamic flora of Hunan Province laid the groundwork for our work in Badagongshan References Enroth J & Koponen T (2003) Bryophyte flora of Hunan Province, China 8 Additions to the checklist Hikobia 14: Hairkonen M (2000) The fabulous forests of Southern China as a cooperative field of exploration Universitas Helsingiensis : HIirkonen M & Ukkola T (2000) Conclusions on myxomycetes compiled over twenty-five years from 4793 moist chamber cultures Stapfia 73: Hiirkonen M, Ukkola T & Zeng Z (2004) Myxomycetes of the Hunan Province, China, 2 Syst Geogr PL 74: Ignatov M S, Huttunen S & Koponen T (2004) Bryophyte flora of Hunan Province, China 5 Brachytheciaceae, with an overview of Eurhynchiopsis and Rhynchostegiella in southeast Asia Acta Bot Fennica (in press) Juslen A (2004) Bryophyte flora of Hunan Province, China 7 Herbertus (Herbertaceae, Hepaticae) Ann Bot Fennici 41 (in press) Koponen T, Enroth J, Fang Y, Huttunen S, Hyvonen J, Ignatov M, JuslIn A, Lai M, Piippo S, Potemkin A & Rao P (2000) Bryophyte flora of Hunan Province, China 1 Bryophytes from Mangshan Nature Reserve and Wulingyuan Global Cultural Heritage Area Ann Bot Fennici 37: Koponen T, Cao T, Huttunen S, Juslen A, Peng C, Piippo S, Rao P, Vaifia J & Virtanen V (2004) Bryophyte flora of Hunan Province, China 3 Bryophytes from Taoyuandong and Yankou Nature Reserves, and Badagonshan and Hupingshan National Nature Reserves, with additions to floras of Mang-shan Nature Reserve and Wulingyuan Global Cultural Heritage Area Acta Bot Fennica (in press) Lado C (2001) Nomenmyx, a Nomenclatural Database of Myxomycetes Cuad Trab Fl Micol Iber 16: McCune B (1994) Improving community analysis with the Beals smoothing function Ecoscience 1: McCune B & Medford MJ (1997) PC-ORD Multivariate Analysis of Ecological Data, Version 30 MjM Software Design Gleneden Beach Potemkin AD (2000) Bryophyte flora of Hunan Province, China 2 Scapania koponenii sp nova (Scapaniaceae, Hepaticae) Ann Bot Fennici 37: Potemkin AD, Piippo S & Koponen T (2004) Bryophyte flora of Hunan Province, China 4 Diplophyllaceae and Scapaniaceae (Hepaticae) Ann Bot Fennici 41 (in press) Rikkinen J (2000) Two new species of Caliciopsis (Coryneliaceae) from Hunan Province, China Karstenia 40: Ukkola T, Hirkonen M & Zeng Z (2001) Myxomycetes of Hunan Province, China I Ann Bot Fennici 38: Ukkola T & Rikkinen J (2000) Myxomycetes in the forests and woodlands of western Oregon Mycotaxon 76: Vnfia J, Piippo S & Koponen T (2004) Bryophyte flora of Hunan Province, China 6 Jungermanniaceae and Gymnomitriaceae (Hepaticae) Ann Bot Fennici 41 (in press) Manuscript received October 2002; accepted in revised version December
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