Fungal diversity on submerged wood in a tropical stream and an artificial lake

Abstract

Two collections of submerged wood were made from the Mushroom Research Centre in northern Thailand. One collection comprising
100 samples was made from an artificial lake, which had been made by damming a stream running through a secondary forest.
The other collection comprising 90 samples was made from an adjacent non dammed shallow stream running through a similar forest.
A total of 68 fungal taxa were recorded during the study and the Shannon–Weiner index (H′) was applied to evaluate the diversities
of freshwater fungi. Sørensen’s index (S′) was calculated to evaluate the similarity of different fungal communities. The
variation of freshwater fungi on submerged wood between lentic and lotic habitat is discussed and compared with previous studies.
A dramatic decrease in species richness and diversity, with significantly changed species composition were observed in the
artificial lake as compared to the non dammed stream.

KeywordsBiodiversity-Damming-Ecology-Freshwater-Fungi-Taxonomy

Full text

1 23
Biodiversity and
Conservation
ISSN 0960-3115
Volume 19
Number 13
Biodivers Conserv (2010)
19:3799-3808
DOI 10.1007/
s10531-010-9927-5
Fungal diversity on submerged wood in a
tropical stream and an artificial lake

1 23
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ORIGINAL PAPER
Fungal diversity on submerged wood in a tropical stream
and an artificial lake
DianMing Hu
•
Lei Cai
•
Hang Chen
•
Ali Hassan Bahkali
•
Kevin D. Hyde
Received: 17 April 2010 / Accepted: 22 September 2010 / Published online: 6 October 2010
Ó Springer Science+Business Media B.V. 2010
Abstract Two collections of submerged wood were made from the Mushroom Research
Centre in northern Thailand. One collection comprising 100 samples was made from an
artificial lake, which had been made by damming a stream running through a secondary
forest. The other collection comprising 90 samples was made from an adjacent non
dammed shallow stream running through a similar forest. A total of 68 fungal taxa were
recorded during the study and the Shannon–Weiner index (H
0
) was applied to evaluate the
diversities of freshwater fungi. Sørensen’s index (S
0
) was calculated to evaluate the sim-
ilarity of different fungal communities. The variation of freshwater fungi on submerged
wood between lentic and lotic habitat is discussed and compared with previous studies. A
dramatic decrease in species richness and diversity, with significantly changed species
composition were observed in the artificial lake as compared to the non dammed stream.
Electronic supplementary material The online version of this article (doi:10.1007/s10531-010-9927-5)
contains supplementary material, which is available to authorized users.
D. Hu  H. Chen  K. D. Hyde
International Fungal Research & Development Centre, The Research Institute of Resource Insects,
Chinese Academy of Forestry, Bailongsi, Kunming 650224, People’s Republic of China
D. Hu
School of Chemistry and Life Science, Gannan Normal University,
Ganzhou 341000, People’s Republic of China
L. Cai (&)
Key Laboratory of Systematic Mycology and Lichenology, Institute of Microbiology, Chinese
Academy of Sciences, No.10, North 4th Ring Road West, Beijing 100190, People’s Republic of China
e-mail: mrcailei@gmail.com
A. H. Bahkali  K. D. Hyde
Botany and Microbiology Department, College of Science, King Saud University,
Riyadh, Saudi Arabia
K. D. Hyde (&)
School of Science, Mae Fah Luang University, Chiang Rai, Thailand
e-mail: kdhyde3@gmail.com
123
Biodivers Conserv (2010) 19:3799–3808
DOI 10.1007/s10531-010-9927-5
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Keywords Biodiversity  Damming  Ecology  Freshwater  Fungi  Taxonomy
Introduction
Freshwater fungi play an important role in freshwater ecosystems mainly due to their role
in decomposing woody debris and leaves and with the mycelium and fruiting bodies being
available to the animal food web (Cai et al. 2006; Ho et al. 2001; Bergbauer et al. 1992).
There are many reports on freshwater fungi from both lentic and lotic habitats in different
areas (Raja et al. 2009; Cai et al. 2002, 2006; Nikolcheva et al. 2005; Pascoal and Ca
´
ssio
2004; Rajashekhar and Kaveriappa 2003; Tsui et al. 2001a, b, 2003; Sivichai et al. 2002,
2000 ; Ho et al. 2001; El-Hissy et al. 2000; Hyde and Goh 1999; Raviraja et al. 1998) and
much has been written on the subject (Tsui and Hyde 2003).
There have, however, been few studies that have investigated the effects of human
disturbance on such habitats (Tsui et al. 1998). Disturbances to streams and rivers may
results from road building, destruction of riparian vegetation, organic runoff, pollution (Tsui
et al. 2001a, b) and damming. There are numerous reports of rivers being dammed for
electricity projects which result in losses of huge areas of forest and associated diversity
(Poff et al. 2007; Wu et al. 2004; Xie 2003; March et al. 2003; Park et al. 2003); however
freshwater fungi have never been considered in these investigations. For example there has
been much written on the damming of the Yangtze River, concerning human displacement
and flora and fauna loss (Morley 2007; Wu et al. 2004; Park et al. 2003), but no data has
been available on the changes likely to occur in fungal communities. Documentation of
changes in fungal community in a large river system presents a challenging research project
and has not been attempted; no such study has also been carried out on small forest streams.
In northern Thailand a small stream running through a relatively undisturbed forest was
dammed while an adjacent stream 200 m away was left undisturbed. We therefore saw the
opportunity to compare these habitats and provide data on the effects of such disturbance.
Freshwater habitats that support lignicolous fungi are generally divided into: (1) lentic
(lakes, ponds, swamps, pools); (2) lotic (rivers, streams, creeks, brooks) and (3) artificial
habitats (water-cooling tower, etc.) (Wong et al. 1998). Some previous studies suggested
that the fungal communities of lentic and lotic habitats are not significantly different (Raja
et al. 2009; Ho et al. 2001). There have been few studies on freshwater fungi in lotic and
lentic habitat types in close proximity (Raja et al. 2009), as most studies have been
conducted separately.
In this project we select two small streams running through a rain forest and examine
the effect of damming one of the streams. This will provide much needed microdata which
could be used to estimate the effect of damming larger areas. Both collecting sites are in
very close proximity with the similar vegetation. This study also expands our present
knowledge of fungal distribution in lentic and lotic freshwater habitats.
Materials and methods
Study sites
Both collection sites are located in the grounds of the Mushroom Research Centre
(N 19°07
0
13.7
00
,E98°43
0
52.9
00
, 850–905 m), in Pha Deng Village, Pa Pae sub-district,
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Mae Taeng District, Chiang Mai Province, Thailand. The collection area is an abandoned
Miang tea plantation where the Mushroom Research Centre is located. The grounds are
covered by regenerating forest comprising Adenanthera microsperma, Alangium kurzii,
Bacaurea ramiflora, Canthium glabrum, Castanopsis tribuloides, Chionanthus ramiflorus,
Cinnamomum iners, Clausena excavata, Cratoxylum formosum, Diospyros glandulosa,
Ficus benjamina, Ficus tonanatoria, Gnetum leptostachyum, Gluta obolata, Heynea tijuga,
Lagerstroemia tomentosa, Litrocarpus thomsonii, Lithocarpus elongan, Melia toonsendan,
Microcos paniculata, Michelia baillonii, Prunus arborea, Rhus rhetsoides, Schima wall-
chii, Sapidus rarak, Suregata multiflora and Toona ciliate (Sysouphanthong et al. 2010).
Initially the site had comprised two streams about 200 m from each other within adjacent
valleys. The sources of both streams started very close to the Mushroom Research Centre
(MRC) and the system could be considered as natural as there is no disturbance from other
means. In 2001 the stream nearer to the road had been dammed by a road made to enter
MRC, and to provide a fishing lake as well as water for the fire brigade during the dry
season. The area above the lake was dug out to produce five fish ponds while the source of
the stream occurs 50 m above the first fish pond in secondary forest. The area below the
lake was relatively disturbed as it ran through a sparsely built up area along the roadside.
The second site, a stream at the back of MRC was relatively undisturbed being regener-
ating forest with many uncut large trees and the occasional grazing by unwanted cows.
Sample collection and incubation
A visit was made to MRC Lake and MRC Stream on 24 August 2008. Samples were
randomly collected and caution was taken to ensure that the wood samples were in a
similar submerged state of decay. During the visit, 100 samples were collected from the
lake and 90 samples were collected from the stream. The dimensions of these samples
ranged from ca. 2–6 cm diameter and ca. 30 cm long. The samples were incubated fol-
lowing the method described by Cai et al. (2006). The specimens are deposited in Mae Fah
Luang University herbarium.
Ecological analysis
The species–area curves were plotted for the two collections to examine the sample size
(Begon et al. 1992). The number of species, the occurrence and the frequency were
recorded and calculated. To compare the fungal communities between the two sites,
species richness and species abundance were calculated. Shannon–Weiner index (H
0
) was
applied to evaluate the diversities of freshwater fungi, including species richness. A t-test
was performed to compare the Shannon–Weiner indices between different fungal com-
munities (Hutcheson 1970). Sørensen’s index of similarity (S
0
) was calculated to evaluate
different fungal communities and expressed with values between 0 (no similarity) and 1
(absolute similarity). The above data are calculated using the following formulas:
H
0
¼
X
s
i¼1
P
i
log
e
P
i
; where P
i
¼ N
i
=N
S
0
¼
2c
a þb
N
i
is the individual number of ith species, N is the individual number of all species, P
i
is
the proportion of ith species, Log
e
P
i
is the natural logarithm of P
i
, a is total number of
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species from site 1, b is total number of species from site 2, c is number of common
species to both sites.
Results
Sample size
Species–area curves are presented in Fig. 1. The species–area curve for the lake and stream
reached asymptotes at 60 and 80 samples, respectively and therefore 90 samples provided a
reasonable estimate of freshwater fungal communities at both collection sites.
Fungal communities
A total of 68 fungal taxa were recorded during the study, comprising 17 ascomycetes
(representing 25% of all taxa) and 51 anamorphic taxa (representing 75% of all taxa). The
list of taxa for both collecting sites and their occurrence and frequency are presented in
Table S1(presented as online-only supplementary material). Seven common genera were
identified in this study as Aquaphila, Aquaticola, Dactylaria, Dictyocheata, Monodictys,
Spirosphaera and Sporoschisma, with each genus represented by more than three different
species. Annulatascus velatisporus was the most common species identified in this study
(21%).
Twenty-three fungal taxa were recorded from the artificial lake, comprising seven
ascomycetes (representing about 30% of the taxa from the MRC Lake) and 16 anamorphic
taxa (representing about 70% of the taxa from the MRC Lake). The three most common
species in the artificial lake are Annulatascus velatisporus (29%), Sporoschisma unisept-
atum (6%), Spirosphaera sp. (5%) (Table 1).
Fifty-four taxa were recorded from the stream, comprising 12 ascomycetes (repre-
senting about 22% of the taxa from the MRC Stream) and 42 anamorphic taxa (repre-
senting about 78% of the taxa from the MRC Stream). The three most common species in
the stream are Annulatascus velatisporus (12.22%), Xylomyces giganteus (8.89%) and
Curvularia robusa (6.67%) (Table 1).
Both of the two study sites share the most common species Annulatascus velatisporus.
Nine species were shared by both sites, i.e. Annulatascus velatisporus, Ascominuta lig-
nicola, Phaeoisaria clematidis, Pleurothecium recurvatum, Savoryella lignicola, Spiro-
sphaera sp., Sporoschisma saccardoi, Sporoschisma uniseptatum and Mariannaea
0
10
20
30
40
50
60
1 8 15 22 29 36 43 50 57 64 71 78 85 92 99
Number of samples
Number of taxa
MRC lake
MRC stream
Fig. 1 Species–area curves
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aquaticola. The Sørensen’s index of the fungal communities between MRC Lake and
MRC Stream is 0.12 (Table 1), indicating a low similarity between two communities.
Similar studies in tropical areas are compared to this study in Table 2. The common
species in lentic habitats are Helicosporium guianense, Phaeoisaria clematidis, Sporos-
chisma saccardoi and Sporoschisma uniseptatum in the compared studies, while that in
lotic habitats are Annulatascus velatisporus, Candelabrum brocchiatum, Helicomyces ro-
seus, Savoryella lignicola, Sporoschisma saccardoi, Sporoschisma uniseptatum. The
overlapping species between the lentic and lotic habitats are Sporoschisma saccardoi and
Sporoschisma uniseptatum. By evaluating Sørensen’s indices between different fungal
communities, it was found that the highest similarity (S
0
) was that between Malaysia
stream and Brunei stream (S
0
= 0.38), and the lowest was that between MRC Lake and the
Hong Kong reservoir (S
0
= 0.1).
Fungal diversity
The Shannon–Weiner indices (H
0
) of both study sites are presented in Table 1. The
Shannon–Weiner indices indicate that the fungal diversity of MRC Stream is higher than
that of MRC Lake (3.68 vs. 2.34). The Shannon–Weiner indices (H
0
) of similar studies in
tropical areas are presented in Table 2 to compare the fungal diversity among different
study sites. The Hong Kong stream had the highest fungal diversity (4.2), followed by
Brunei stream (3.87), MRC Stream (3.68), Malaysia stream (3.68), Hong Kong reservoir
(3.21), Lake Barrine (2.85), and MRC Lake the lowest (2.34). The fungal diversity from
lotic habitats (3.21, 2.85, 2.34) was significantly higher than that of lentic habitats (4.2,
3.87, 3.68, 3.68) (0.01 \ P \ 0.05).
Discussion
Fungal species from freshwater
Ascominuta ovalispora is a new ascomycete found in MRC stream (Hu et al. 2010). So far,
there are 579 ascomycetes and 537 anamorphic fungi recorded from freshwater (see
http://fungi.life.uiuc.edu/). Shearer et al. (2007) predicted that many species remain to be
Table 1 Species richness, species richness per sample and bio-diversity index
Sampling sites MRC lake MRC stream
Sample size 100 90
Average number of taxa per sample 0.69 1.1
Unique species 14 45
Overlapping species in two sites 9
Three most common species Annulatascus velatisporus Annulatascus velatisporus
Sporoschisma uniseptatum Xylomyces giganteus
Spirosphaera sp. Curvularia robusa
Species richness 23 54
H
0
2.34 3.68
S
0
0.12
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Table 2 Comparison of similar studies in tropic area
Lentic habitat Lotic habitat
MRC lake
(this study)
Hong Kong reservoir
(Goh and Hyde 1999)
Barrine lake
(Hyde and Goh 1998)
MRC stream
(this study)
Brunei stream
(Ho et al. 2001)
Hong Kong stream
(Ho et al. 2001)
Malaysia stream
(Ho et al. 2001)
S
0
MRC lake 1
Hong Kong reservoir 0.1 1
Barrine lake 0.19 0.23 1
MRC stream 0.12 0.14 0.19 1
Brunei stream 0.15 0.17 0.22 0.13 1
Hong Kong stream 0.12 0.14 0.17 0.11 0.27 1
Malaysia stream 0.12 0.14 0.2 0.11 0.38 0.19 1
Sample size 100 100 100 90 50 50 50
Overlapping species Helicosporium guianense, Phaeoisaria clematidis,
Sporoschisma saccardoi, Sporoschisma uniseptatum
Annulatascus velatisporus, Candelabrum brocchiatum, Helicomyces roseus,
Savoryella lignicola, Sporoschisma saccardoi, Sporoschisma uniseptatum
Species richness 23 57 39 54 81 91 60
H
0
2.34 3.21 2.85 3.68 3.87 4.2 3.68
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discovered and concluded that the least sampled geographic areas include Africa, Aus-
tralia, China, South America and boreal and tropical regions worldwide. During our study
of Asian freshwater fungi (Hu et al. 2007; Luo et al. 2004; Cai et al. 2003), numerous new
or newly recorded species from freshwater were reported. Further studies on freshwater
fungi in tropical areas should be performed to improve our understanding on freshwater
fungi.
Comparison of fungal communities and diversity
MRC lake and MRC stream shared the most common species Annulatascus velatisporus
and other eight species (Table S1) (presented as online-only supplementary material). Of
the species found to be common in this study (e.g. Annulatascus velatisporus, Savoryella
lignicola, Sporoschisma uniseptatum), most have found to be common elsewhere (Cai
et al. 2002, 2006; Fryar et al. 2004; Ho et al. 2001; Hyde and Goh 1998); however
Ascominuta lignicola has previously been shown to be rare in freshwater habitats. The
Sørensen’s index of 0.12 for the communities of MRC Lake and MRC Stream is low and
indicates that the communities differ greatly. The species richness and Shannon–Weiner
index (H
0
) in MRC Lake are 23 and 2.34, and are lower than those in MRC stream (species
richness = 54, H
0
= 3.68). The fungal diversity of MRC Lake is therefore lower than that
of the stream. In comparison to similar tropical areas, the diversity in MRC Lake is lowest
(Table 2). This may be because the lake was recently constructed and thus few lentic fungi
have been able to colonize the lake during its short life span.
Damming effect on freshwater fungal communities
The fungal communities in MRC Lake and stream differ significantly with the lake having a
lower diversity. Various factors can affect fungal communities and diversity in freshwater
habitats. Ba
¨
rlocher and Graca (2002) investigated eight streams in Portugal, and found that
exotic riparian vegetation results in lower diversity. Tsui et al. (2000) also suggested that
different riparian vegetation composition is important factor in regulating fungal commu-
nities. Goh and Hyde (1999) investigated the fungi in Plover Cove Reservoir in Hong Kong
and compared this with previous studies. They concluded that species diversity of fungi is
lower and the species composition is different in temperate streams than that in subtropical/
tropical streams, a result compared in many studies (Ho et al. 2001; Hyde and Goh 1999;
Hyde et al. 1998; Goh 1997). Luo et al. (2004) compared the fungal communities and
diversity between Lake Fuxian (an unpolluted lake) and Lake Dianchi (a heavily polluted
lake), and concluded that pollution causes change in the fungal communities, but had little
effect on fungal diversity. Tsui et al. (2001a, b) investigated the longitudinal and temporal
distribution of freshwater ascomycetes and hyphomycetes on submerged wood in the Lam
Tsuen River in Hong Kong, and found that the fungal species composition changed cor-
related with concentrations of NO
3
-N, NH
3
-N, and PO
4
-P resulting from human distur-
bance. Sivichai et al. (2000) investigated fungal species colonized on the test blocks of
Dipterocarpus alatus and Xylia dolabriformis exposed in a freshwater stream and found that
the fungal communities and diversity were different between the two substrata.
Previous studies have shown that riparian vegetation, eco-climatic zone, pollution and
substrata are important factors that affect the fungal communities and diversity in fresh-
water habitats. In this study, the two sites are in the same eco-climatic zone, sharing the
similar riparian vegetation. We randomly collected the woody samples from both sites. The
sources of both streams started very close to the Mushroom Research Centre (MRC) and
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the system could be considered as relatively natural as there is little disturbance from other
means beside damming. The study suggests that damming causes significant changes in
fungal communities with decreased diversity. The reasons for the changes are unknown but
changes in water aeration, pH, turbidity and silt content may be causal factors.
Freshwater ecosystems are at the forefront of the global biodiversity crisis, with more
declining and extinct species than in terrestrial or marine environments (Johnson et al.
2008). As essential nature resource, freshwater is widely used by human beings. Numerous
dams have been and are being constructed for irrigation and electricity generation. The
effect of damming on freshwater fungi is rarely studied, as compared to the flora and fauna.
Fungi play a dominant role in microbial decomposition of plant litter in freshwater (Pas-
coal and Ca
´
ssio 2008), and mycelium and fruiting bodies could serve as the animal food
(Bergbauer et al. 1992). It is therefore important to consider the effect on freshwater fungi
and ecosystem functioning when evaluating the effects of damming waterways.
To understand the impact of damming on freshwater fungi, further studies should be
conducted. Comparison of the fungal communities and diversity in streams and rivers
upstream and downstream of dams and within the dams may provide useful data to
understand the effect of damming on fungal communities. Comparing the fungal com-
munities and diversity from a river before and after damming would be even more useful.
It was not possible to do this in the present study as the stream had already been dammed
and the stream above the dam was rather short and that below relatively disturbed.
Comparison of fungal communities and diversity between lentic and lotic habitats
The fungal community in MRC Lake (lotic habitat) differed from that in the MRC Stream
(lentic habitat) (Table 1). Of the listed fungal taxa in this study, only Mukhakesa lignicola
appears to be restricted to lentic habitats, and Bactrodesmium longisporum, Cercophora
terricola, Exserticlava globosa, E. yunnanensis, Monodictys melanocephaloide, Ophioc-
eras lepatosporum, Pseudofuscophialis lignicola, Spirosphaera floriformis, Sporidesmium
tropicale and Xylomyces giganteus are unique to lotic habitats. Fungal diversity in lotic
habitats is significantly higher than that of lentic habitat (0.01 \ P \ 0.05). So far, there
have been 259 ascomycetes recorded in lentic habitats and 340 ascomycetes recorded in
lotic habitats (http://fungi.life.uiuc.edu/). All these results and conclusions show that lotic
habitats have a higher fungal diversity than lentic habitats. The still waters may result in
low oxygen and reduce the number of fungi present (Ba
¨
rlocher 1992).
Acknowledgments Funds for research were provided by the Grant for Essential Scientific Research of
Chinese National Non-profit Institute (no. CAFYBB2007002) and the Knowledge Innovation Program of
the Chinese Academy of Sciences, No. KSCX2-YW-1026.
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