ORI GIN AL PA PER

Diversity and abundance of nematode-trapping fungifrom decaying litter in terrestrial, freshwater andmangrove habitats

Aung Swe Æ Rajesh Jeewon Æ Stephen B. Pointing Æ Kevin D. Hyde

Received: 12 August 2008 / Accepted: 25 November 2008 / Published online: 11 December 2008� Springer Science+Business Media B.V. 2008

Abstract Nematode-trapping fungi are ubiquitous in terrestrial habitats in dung, soils,

litter and woody debris and they also occur in freshwater, but only one species has been

found in marine habitats. The purpose of this study was therefore to investigate whether

nematode-trapping fungi occurred in mangrove habitats. To achieve this we assessed the

diversity of nematode-trapping fungi on decaying litter from mangroves, freshwater and

terrestrial habitats (22 sites) in Hong Kong. Composite samples (n = 1,320) of decaying

litter (wood and leaves) were examined and a total of 31 species of nematode-trapping

fungi belonging to four genera, Arthrobotrys, Monacrosporium, and Dactylella were

recorded. Twenty-nine species reported in this study are new records for Hong Kong and

16 species are new records from mangrove habitats worldwide. Nematode trapping fungi

are therefore present in marine environments. Commonly encountered taxa were Arthro-botrys oligospora and Monacrosporium thaumasium which are abundant in all habitats. A.oligospora, M. thaumasium and Arthrobotrys musiformis were frequent (F [ 10%).

Twenty-six species were rare (0.16–9.32%). Species richness and diversity was higher in

terrestrial than in freshwater and mangrove habitats (ANOVA, P \ 0.001). A higher mean

diversity was observed on decaying leaves as compared to decaying wood in all habitats

(P \ 0.001). Based on Shannon diversity index, it was also observed that taxa charac-

terized by adhesive nets were more frequent in all habitats. This can be explained by the

fact that these taxa may have a better competitive saprotrophic ability which would allow

them to compete favourably in nutrient limited environments. Abiotic factors that could be

A. Swe (&) � R. Jeewon � S. B. PointingDivision of Microbiology, School of Biological Sciences, Faculty of Science, The Universityof Hong Kong, Pokfulam Road, Hong Kong SAR, People’s Republic of Chinae-mail: aung.swe@gmail.com

K. D. HydeInternational Fungal Research & Development Centre, The Research Institute of Resource Insects,Chinese Academy of Forestry, 650224 Kunming, People’s Republic of China

K. D. HydeSchool of Science, Mae Fah Luang University, Chiang Rai, Thailand

123

Biodivers Conserv (2009) 18:1695–1714DOI 10.1007/s10531-008-9553-7

linked to differences in species diversity between decaying wood and leaves are also

discussed.

Keywords Biodiversity � Ecology � Nematode-trapping fungi � Mangrove fungi �Marine fungi

Introduction

Nematode-trapping fungi are hyphomycetous predators of nematodes (Kerry 1987) and

have been used in agriculture and animal husbandry as biological control agents (Larsen

et al. 1997; Kerry 2000). Nematode-trapping fungi are ubiquitous in a variety of habitats

such as agricultural, horticultural and forest soils, but have rarely been reported from

aquatic and especially marine environments (Gray 1983; Persmark and Jansson 1997;

Jansson and Lopez-Llorca 2001). Currently 35 species of nematode-trapping fungi have

been recorded from aquatic environments (Ingold 1944; Peach 1950, 1952, 1954; Johnson

and Autery 1961; Anastasiou 1964; Hao et al. 2004), however, Arthrobotrys dactyloides is

the only a species that has been isolated from brackish water (Johnson and Autery 1961).

Nematodes are populous in marine and mangrove habitats (Tietjen and Alongi 1990;

Somerfield et al. 2002; Zhang and Zhou 2003; Chinnadurai and Fernando 2007). We might

therefore expect nematode-trapping fungi to be ubiquitous in saline habitats.

Thorn and Barron (1984) noted that wood-decomposing, nematode-trapping fungi

resemble carnivorous plants. The plants and fungi grow in nitrogen poor environments;

plants capture animals to support photosynthesis; whereas fungi may capture nematodes to

support saprotrophism. Pfister (1994, 1997) Pfister and Liftik (1995) showed that the

telemorphs of Arthrobotrys oligospora var. oligospora and certain other nematode-trap-

ping fungi (Orbilia species) are saprotrophs on dead wood and bark revealing a connection

between wood and nematode-trapping fungi. Similar findings have been reported (Webster

et al. 1998; Liu et al. 2005; Mo et al. 2005; Yu et al. 2007a, b) and it is probably that the

saprotrophic Orbilia species gain extra nutrition, especially nitrogen through trapping

nematodes (via their anamorphic stage). The teleomorph Orbilia, however, has not been

recorded from marine habitats and therefore other fungal genera may have taken over

this role.

Fungi are considered to be the most important agents involved in wood and leaf decay

in terrestrial, freshwater and mangroves habitats (Sin et al. 2002; Seena et al. 2008). They

release nutrients for other organisms to survive on these substrates (Hyde 1989, 1990;

Hyde and Lee 1995; Whitford 1996; Hyde et al. 1998; Wong et al. 1998; Boddy 2001).

Numerous studies have focused on fungal diversity of decomposing leaf and woody litter

(Hyde and Alias 2000; Tsui et al. 2000; Wai et al. 2001; Berg et al. 2002; Cai et al. 2003;

Ananda and Sridhar 2004; Gopal and Chauhan 2006; O’dor et al. 2006; Gulis et al. 2008;

Lonsdale et al. 2008). These studies, however, provided no information on the diversity of

nematode-trapping fungi. This is because detection of nematode-trapping fungi requires

specific techniques, thus they are usually overlooked by mycologists unless they are

nematode-trapping fungi specialists.

The objectives of this study were (1) to assess whether nematode trapping fungi occur in

marine habitats and (2) to investigate the biodiversity of nematode-trapping fungi in ter-

restrial, freshwater and mangrove habitats to establish if there were differences in species

composition in different substrates and habitats.

1696 Biodivers Conserv (2009) 18:1695–1714

123

Materials and methods

Location and study sites

In this study, 22 sites situated in Hong Kong with seasonal tropical climate were selected,

nine from terrestrial five from freshwater (lotic) and eight from mangrove habitats,

respectively (Fig. 1; Table 1). The terrestrial, freshwater and mangrove sites were in close

proximity. The collection time was between October and April in 2005.

Sampling design and process

A composite sampling method (Rohde 1976) was used. Ten sampling areas were randomly

selected at each site and 50 decaying leaves and 20 decaying wood samples were collected.

All the samples were placed individually in Zip-lock plastic bags and maintained at 4�C

before treatment. Each sample (50 leaves or 20 wood samples) were coarsely ground and

homogenously mixed with a blender. The slurry (3 g) as a composite sample was sprinkled

onto corn meal agar media (three replicates), containing 1% streptomycin to inhibit bac-

teria growth. Five hundred (±32, n = 3) healthy Panagrellus redivivus (free living

nematodes from soil) were added to each plate as nematode baits. Plates were sealed and

incubated for 4 weeks at room temperature (26�C). Following incubation plates were

observed under a dissecting microscope and the nematode-trapping fungi present were

Fig. 1 A map of Hong Kong showing the study sites in three habitats: T terrestrial (j), F freshwater ( ), Mmangrove (d). (Draft)

Biodivers Conserv (2009) 18:1695–1714 1697

123

recorded. A total of 1,320 composite samples were examined. A single spore was trans-

ferred to a new CMA plate with a sterilized toothpick. Then a plug (2 9 2 cm) of media

was removed adjacent to the spore to provide a well and plates were incubated on CMA at

26�C until the mycelium grew out into the well. Living nematodes were placed in the well

in order to stimulate fungi to form trapping devices. Types of trapping device were

checked under a dissecting microscope after 24 h. The isolation method is modified in this

study based on the method of Liu and Zhang (2003) and Hao et al. (2004). Taxa were

identified using the keys of Li et al. (2000) for Arthrobotrys and Monacrosporium and

Chen et al. (2007) for Dactylella.

Data analysis

Total numbers of taxa, frequency of occurrence of each species and abundance (total

occurrence of all taxa) were recorded and calculated for each sampling site at each habitat.

In order to quantify nematode-trapping fungi, we followed the method of Mo et al. (2006).

The individual number of a species was counted as one occurrence of a species if it was

isolated from any of the three replicates.

The species diversity of each sampling site was calculated using Shannon’s diversity

index, H0 (Shannon and Weaver 1963) and the Simpson index, D (Simpson 1949).

Table 1 One location and study sites of the study

Habitats SiteNo.

Location

Terrestrial T1 Tai Mo Shan Country Park, New Territories, 22�25 35.210 0 N 114�10 33.560 0 E

T2 Tai Mo Shan Country Park, New Territories, 22�250 24.900 0 N 114�100 25.110 0 E

T3 Tai Mo Shan Country Park, New Territories, 22�250 28.400 0 N 114�100 39.100 0 E

T4 Tai Lam Country Park, New Territories, 22�240 30.270 0 N 114�030 31.180 0 E

T5 Tai Lam Country Park, New Territories, 22�240 15.970 0 N 114�030 29.090 0 E

T6 Tai Po Kau Natural Reserve, New Territories, 22�250 30.720 0 N 114�100 37.460 0 E

T7 Tai Po Kau, New Territories, 22�240 42.320 0 N 114�070 00.730 0 E

T8 Lantau North Country Park, Mui Wo, Lantau, 22�160 39.570 0 N 113�590 45.000 0 E

T9 Lung Fu Shan Country Park, Hong Kong, 22�160 53.740 0 N 114�080 14.090 0 E

Freshwater FW1 Shing Mu Reservoir, New Territories, 22�230 51.890 0 N 114�020 48.780 0

FW2 Forest Stream, Tai Po Kau, New Territories 22�240 59.080 0 N 114�070 01.620 0 E

FW3 Tai Shing Stream, Tai Mo Shan Country Park, New Territories 22�230 34.010 0 N114�080 3.320 0 E

FW4 Lantau North Contry Park, Mui Wo, Lantau, 22�160 24.170 0 N 113�590 45.000 0 E

FW5 Forest Stream, Pat Sin Leng Country Park, 22�290 28.240 0 N 114�100 53.440 0

Mangroves M1 Mai Po Nature Reserve, Mai Po, New Territories, 22�290 11.000 0 N114�020 24.350 0 E

M2 Shuen Wang, Sai Kung, New Territories, 22�270 49.740 0 N 114�120 33.530 0 E

M3 Ting Kok, Sai Kung, New Territories, 22�280 08.160 0 N 114�130 01.970 0 E

M4 Ha Pak Na, Deep Bay, New Territories, 22�280 22.120 0 N 113�590 10.710 0 E

M5 Kei Ling Ha Lo Wai, Sai Kung, 22�240 49.320 0 N 114�160 21.470 0 E

M6 Sham Chung, Sai Kung, New Territories, 22�260 35.190 0 N 114�170 01.360 0 E

M7 Hoi Ha Wan, Sai Kung, New Territories, 22�280 10.580 0 N 114�200 07.340 0 E

M8 Pak Sha Wan, Sai Kung, New Territories, 22�220 02.910 0 N 114�150 38.330 0

Total 22

1698 Biodivers Conserv (2009) 18:1695–1714

123

H0 ¼ �Xn

i¼1

Pi loge Pi where, Pi ¼Ni

Nð1Þ

D ¼ �Xn

i¼1

P2i ð2Þ

where Ni is individual number of i species and N is individual number of all species: Pi is

the proportion of i species and n is the number of species at the site. The occurrence

frequencies of each species (F) were calculated based on total number of all species by

using following formula:

F ¼ Individual number of species

Individual number of all species� 100 ð3Þ

To compare the similarity of the species composition among different habitats,

Sørensen’s index of similarity (S0) was applied (Magurran 1988).

S0 ¼ 2C

Aþ Bð Þ ð4Þ

where A and B are the number of species at site A and B, respectively and C is the number

of species common to both collections.

Evenness indices were estimated to establish the closeness of equability of species

present (Gotelli and Colwell 2001). All statistical analyses were performed using SPSS

[Release 14.0.0 (2005), SPSS Inc., Chicago, IL, USA] and PRIMER [version 6 (2005),

Primer-E Ltd, Plymouth, UK]. Species diversity between habitats and substrates were

compared using two-way ANOVA followed by Tukey multiple comparison tests (HSD).

ANOSIM was also performed to compare the ranks of species similarities between habi-

tats. Statistical significance was defined at a = 0.05.

Results

Biodiversity of nematode-trapping fungi

Mangrove

Seventeen nematode-trapping fungal species were recorded from 480 composite samples at

eight different of mangrove sites (Table 2). The most common species in mangroves were

Monacrosporium thaumasium (F = 24.62%), A. oligospora (F = 23.12%), and Mon-acrosporium eudermatum (F = 10.55%). A higher diversity was found on decaying leaves

at Site M3 (H0DL = 1.99; DDL = 0.853; SDW = 8), follow by M7 (H0DL = 1.932;

DDL = 0.833; SDL = 8) whereas the lowest diversity was observed at Site M2

(H0DL = 1.28; DDL = 0.694; SDL = 4) (Table 2; Fig. 2).

Terrestrial

Twenty-four nematode-trapping fungal species were recorded from 540 composite samples

collected at nine different terrestrial sites (Table 3). The most common species were

A. oligospora (F = 20.38%), Arthrobotrys musiformis (F = 14.11%), and M. thaumasium(F = 12.85%). Species diversity (H0 and D) varied between sample sites and substrates

Biodivers Conserv (2009) 18:1695–1714 1699

123

Ta

ble

2O

ccu

rren

cefr

equen

cyo

fn

emat

od

e-tr

app

ing

fun

gi

on

dif

fere

nt

site

sat

man

gro

ve

hab

itat

s

Tax

aM

G1

MG

2M

G3

MG

4M

G5

MG

6M

G7

MG

8F

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

A.

art

hro

botr

yoid

es–

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1–

––

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A.

bro

cho

pa

ga

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1

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.00

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da

ctyl

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java

nic

a–

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mu

sifo

rmis

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3–

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32

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9.5

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go

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sup

erba

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la2

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27

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sp1

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bei

jin

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sis

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sp1

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21

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4

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sp2

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did

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ans

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elli

pso

spor

um

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0.0

0

1700 Biodivers Conserv (2009) 18:1695–1714

123

Ta

ble

2co

nti

nu

ed

Tax

aM

G1

MG

2M

G3

MG

4M

G5

MG

6M

G7

MG

8F

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

M.

eud

erm

atu

m–

2–

–1

31

42

2–

–3

3–

–1

0.5

5

M.

gep

hyr

opagu

m–

––

––

––

––

––

––

––

–0

.00

M.

ha

pto

tylu

m–

––

––

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–0

.00

M.

hu

isu

nia

na

24

––

–3

––

––

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4.5

2

M.

meg

alo

spor

um

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0

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mic

rosc

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ides

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M.

thau

ma

siu

m2

41

24

4–

4–

33

46

73

22

4.6

2

N(i

ndiv

idual

no

of

all

spec

ies)

819

37

51

97

20

13

13

10

82

32

48

12

S(s

pec

ies

no

.re

cord

ed)

46

24

28

35

67

43

78

25

H0

(Shan

non–W

einer

index

)1.3

86

1.7

49

0.6

37

1.2

77

0.5

00

1.9

86

0.9

56

1.6

09

1.6

72

1.8

45

1.3

66

1.0

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1.8

77

1.9

32

0.6

62

1.4

68

Sim

pso

n_

1-D

0.7

50

0.8

20

0.4

44

0.6

94

0.3

20

0.8

53

0.5

71

0.8

00

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93

0.8

28

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0.6

25

0.8

36

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33

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36

Ev

ennes

s_e^

H/S

1.0

00

0.9

59

0.9

45

0.8

97

0.8

25

0.9

11

0.8

67

1.0

00

0.8

87

0.9

04

0.9

80

0.9

43

0.9

33

0.8

63

0.9

69

0.8

68

A=

Art

hro

botr

ys,

D=

Da

ctyl

ella

,M

=M

on

acr

osp

ori

um

Biodivers Conserv (2009) 18:1695–1714 1701

123

(Fig. 2). The highest diversity was recorded at Site T8 (H0DW, DL = 2.389, 2.327; DDW,

DL = 0.9, 0.897; SDW, DL = 12, 11) and the lowest diversity at Site T7 from decaying

wood (H0DW = 1.256; DDW = 0.702; SDW = 4). A higher diversity was observed from

decaying leaves than from decaying wood at Sites T1, T2, T5, T6 and T7 whereas a lower

diversity was observed from decaying leaves than from decaying wood at Sites T3, T4, and

T8 (Table 3; Fig. 2).

Freshwater

Twenty nematode-trapping fungal species were recorded from 300 composite samples

collected from five different rivers and streams (Table 4). The most common species were

M. eudermatum (F = 14.75%), A. oligospora (F = 16.39%), M. thaumasium(F = 13.93%), and Arthrobotrys musiformis (F = 13.11%). The highest diversity was

found in Site FW1 from decaying leaves decaying leaves at Site FW1 (H0DL = 1.96;

DDL = 0.847; SDL = 8), whereas the lowest diversity was found on decaying wood at the

same site (H0DW = 0.00; DDW = 0.00; SDW = 1). A higher diversity was observed on

decaying leaves than on decaying wood at all freshwater sites (Table 4; Fig. 2).

All habitats

Thirty-one nematode-trapping taxa were recorded in this study (Tables 2, 3, 4), consisting of

13 Arthrobotrys, 15 Monacrosporium, and 3 Dactylella species. Twenty-six species were

rare (F = 0.16–9.32). Twenty-nine of the species reported in the present study are new

records for Hong Kong. Seventeen species isolated from mangrove have not previously been

recorded from marine habitats. Diversity indices means (H0) were used as variable and

habitat type used as factor for ANOVA analysis. The ANOVA analysis found significant

differences in species diversity between the different habitats (two way ANOVA:

F = 0.00988; P \ 0.001) and between substrates (two way ANOVA: F = 0.0099;

P \ 0.001) (Figs. 3, 4). The species diversity in terrestrial habitats was significantly higher

than that in freshwater and mangrove habitats on leaves and wood (HSD: P \ 0.001)

(Fig. 3). A higher mean diversity was observed on decaying leaves as compared to decaying

wood in all habitats (Fig. 4; Two way ANOVA: F = 0.0099; P \ 0.001). Graphical com-

parison of species diversity between sampling sites in different habitats are showed in Fig. 2.

00.2

0.4

0.6

0.8

1

0

0.5

1

1.5

2

2.5

00.2

0.4

0.6

0.8

1

0.0

0.5

1.0

1.5

2.0

2.5

0

0.2

0.4

0.6

0.8

1

0.0

0.5

1.0

1.5

2.0

2.5

1 2 3 4 5 6 7 8 9

1 2 3 4 5

1 2 3 4 5

1 2 3 4 5 6 7 8

1 2 3 4 5 6 7 8

1 2 3 4 5 6 7 8 9Shan

non-

Wie

ner

Inde

x Si

mps

on in

dex

MangroveFreshwaterTerrestrial

Sampling sites

Fig. 2 Species diversity for three different habitats between the same habitat: H0DW, DL—Shannon’s indexfor decaying wood and leaf, DDW, DL—Simpson’s index for decaying wood and leaves

1702 Biodivers Conserv (2009) 18:1695–1714

123

Tab

le3

Occ

urr

ence

freq

uen

cyof

nem

atode-

trap

pin

gfu

ngi

on

dif

fere

nt

site

sat

terr

estr

ial

hab

itat

Tax

aT

1T

2T

3T

4T

5T

6T

7T

8T

9F

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

A.

art

hro

botr

yoid

es–

––

1–

––

2–

––

––

––

––

–0.9

4

A.

bro

chopaga

12

–1

–2

44

–2

22

–2

33

–1

9.0

9

A.

cladodes

––

–1

––

––

––

––

––

––

––

0.3

1

A.

conoid

es–

––

––

––

––

––

1–

1–

––

–0.6

3

A.

dact

yloid

es–

21

–1

–1

12

2–

2–

–2

1–

–4.7

0

A.

java

nic

a–

––

––

––

––

––

––

––

––

–0.0

0

A.

musi

form

is1

3–

12

21

54

–3

34

44

33

214.1

1

A.

oli

gosp

ora

25

46

31

45

44

42

54

23

34

20.3

8

A.

poly

cephala

–2

––

––

––

––

––

––

––

––

0.6

3

A.

pyr

iform

is–

––

––

––

––

––

––

––

––

–0.0

0

A.

super

ba

––

––

––

––

––

–2

––

––

––

0.6

3

A.

verm

icola

–2

1–

–1

1–

22

–1

–1

22

2–

5.3

3

A.

sp1

––

––

––

––

––

––

––

––

––

0.0

0

D.

bei

jingen

sis

––

––

––

–2

––

–3

––

––

––

1.5

7

D.

sp1

2–

––

––

1–

––

––

––

11

––

1.5

7

D.

sp2

––

––

––

1–

––

––

––

1–

––

0.6

3

M.

aphro

bro

chum

––

––

––

––

––

––

––

––

––

0.0

0

M.

bem

bic

odes

––

––

––

––

––

––

––

––

––

0.0

0

M.

candid

um

––

13

––

––

––

––

––

––

––

1.2

5

M.

cionopagum

––

––

2–

––

–1

––

––

22

1–

2.5

1

M.

cyst

osp

ori

um

3–

–1

––

–1

––

––

––

––

––

1.5

7

M.

dre

chsl

eri

––

––

––

––

––

––

––

––

––

0.0

0

M.

eleg

ans

––

––

––

––

––

––

––

––

––

0.0

0

Biodivers Conserv (2009) 18:1695–1714 1703

123

Ta

ble

3co

nti

nu

ed

Tax

aT

1T

2T

3T

4T

5T

6T

7T

8T

9F

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

DW

DL

M.

elli

pso

sporu

m1

–1

––

––

––

–2

2–

–2

2–

–3.1

3

M.

euder

matu

m–

3–

––

–2

––

13

31

1–

–1

–4.7

0

M.

gep

hyr

opagum

–3

–1

––

––

––

––

––

22

–2

3.1

3

M.

hapto

tylu

m–

––

––

––

––

3–

––

––

––

–0.9

4

M.

huis

unia

na

––

–3

–3

33

–4

22

–2

––

1–

7.2

1

M.

meg

alo

sporu

m–

2–

–1

––

––

––

––

––

––

–0.9

4

M.

mic

rosc

aphoid

es–

––

–1

––

––

––

––

–1

1–

11.2

5

M.

thaum

asi

um

34

53

2–

33

12

––

53

12

31

12.8

5

N(i

ndiv

idual

no

of

all

spec

ies)

13

28

13

21

12

921

26

13

21

16

23

15

18

23

22

14

11

S(s

pec

ies

no.

reco

rded

)7

10

610

75

10

95

96

11

48

12

11

76

H0

(Shan

non–W

einer

index

)1.8

45

2.2

46

1.5

19

2.0

62

1.8

64

1.5

23

2.1

37

2.0

66

1.4

99

2.0

95

1.7

54

2.3

44

1.2

65

1.9

37

2.3

89

2.3

27

1.8

34

1.6

42

Sim

pso

n_1-D

0.8

28

0.8

88

0.7

34

0.8

44

0.8

33

0.7

65

0.8

66

0.8

61

0.7

57

0.8

66

0.8

20

0.9

00

0.7

02

0.8

40

0.9

00

0.8

97

0.8

27

0.7

77

Even

nes

s_e^

H/S

0.9

04

0.9

45

0.7

62

0.7

86

0.9

21

0.9

17

0.8

47

0.8

77

0.8

95

0.9

03

0.9

63

0.9

48

0.8

86

0.8

67

0.9

09

0.9

31

0.8

94

0.8

61

A=

Art

hro

botr

ys,

D=

Da

ctyl

ella

,M

=M

on

acro

spo

rium

1704 Biodivers Conserv (2009) 18:1695–1714

123

Table 4 Occurrence frequency of nematode-trapping fungi on different sites at freshwater habitat

Taxa FW1 FW2 FW3 FW4 FW5 F

DW DL DW DL DW DL DW DL DW DL

A. arthrobotryoides – – – – – – – – 2 – 1.64

A. brochopaga – – – – – – 2 – – – 1.64

A. cladodes – – – – – – – 3 – – 2.46

A. conoides – – – 2 – – – – – – 1.64

A. dactyloides – – – – – – – – 3 – 2.46

A. javanica – – – – – – – – – – 0.00

A. musiformis – 1 – 3 – 1 3 3 2 3 13.11

A. oligospora – 5 2 3 1 1 2 – 4 2 16.39

A. polycephala – 4 – – – 3 – – – – 5.74

A. pyriformis – – – – – – – – – – 0.00

A. superba – – – – – – – – – – 0.00

A. vermicola – 4 – – – 5 – 2 – – 9.02

A. sp1 – – – – – – – – – – 0.00

D. beijingensis – – – – – – – – – – 0.00

D. sp1 – 1 – – 1 – – – – – 1.64

D. sp2 – – – – – – – 1 – – 0.82

M. aphrobrochum – – – – – – – – – 1 0.82

M. bembicodes – – – – – – – – – 2 1.64

M. candidum – – – – – – – – – – 0.00

M. cionopagum – – – – – – – – – – 0.00

M. cystosporum – – – – – – – – – – 0.00

M. drechsleri – – – 1 – – – – – – 0.82

M. elegans – – – – – – – – – – 0.00

M. ellipsosporum – – – – – – 1 – – – 0.82

M. eudermatum – 3 1 3 3 5 – 1 – 2 14.75

M. gephyropagum – 2 – – – – – – – – 1.64

M. haptotylum – – 2 – – – – 1 – – 2.46

M. huisuniana – – – – 1 4 – 2 – – 5.74

M. megalosporum – – – – – 1 – – – – 0.82

M. microscaphoides – – – – – – – – – – 0.00

M. thaumasium 2 3 4 2 – 1 – – 2 3 13.93

N (individual no ofall species)

2 23 9 14 6 21 8 13 13 13

S (species no.recorded)

1 8 4 6 4 8 4 7 5 6

H0 (Shannon–Weiner index)

0.000 1.957 1.273 1.735 1.242 1.857 1.321 1.845 1.565 1.738

Simpson_1-D 0.000 0.847 0.691 0.816 0.667 0.821 0.719 0.828 0.781 0.817

Evenness_e^H/S 1.000 0.884 0.893 0.945 0.866 0.801 0.937 0.904 0.957 0.948

A = Arthrobotrys, D = Dactylella, M = Monacrosporium

Biodivers Conserv (2009) 18:1695–1714 1705

123

Species similarities between habitats

ANOSIM statistical analysis showed that there is significant differences in species

diversity between habitats (R = 0.252, P = 0.001); pairwise comparisons between ter-

restrial versus freshwater (P = 0.004) and terrestrial versus mangrove (P = 0.001) also

differed significantly. However, no significant differences were apparent in a pair wise

comparisons between freshwater and mangrove communities.

Species similarity indices of fungal communities between different sites at three habitats

are shown in Tables 2, 3, 4. The 31 species recorded in this study have previously been

recorded from terrestrial habitats, with the exception of one unidentified species each of

Arthrobotrys and Dactylella. There was considerable species overlap between habitats.

Only seven species (of 23) were unique to terrestrial habitats, only four (of 20) were unique

to freshwater habitats and only three (of 17) were unique to mangrove habitats. Thirteen

species overlapped between all habitats, three species between terrestrial and freshwater

habitats, and one species between terrestrial and freshwater habitats (Fig. 5).

Species abundance between habitats based on trapping devices

Based on type of trapping devices, the taxa recorded clustered in six groups. Sixteen taxa

had adhesive networks and accounted for 51.6% of the total nematode-trapping fungi

1.908

1.5131.364

0.828 0.742 0.693

0.0

0.5

1.0

1.5

2.0

2.5

T F M

Habitats

Sp

ecie

s d

iver

sity

H'

D

***

Fig. 3 Comparison of species diversity Shannon–Wiener index (H0) and Simpson index (D) between threehabitats; T terrestrial, F freshwater, M mangrove, *** P \ 0.001

1.790

1.199 1.132

2.0271.826

1.613

0.0

0.5

1.0

1.5

2.0

2.5

Terrestrial Freshwater Mangrove

DW

DL

Fig. 4 Comparison of species diversity (H0) between two substrates and three habitats; DW decaying wood,DL decaying leaf

1706 Biodivers Conserv (2009) 18:1695–1714

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isolated in this study. Taxa forming adhesive networks were the most frequently isolated

fungi from all habitats with 50, 55 and 70.6% in terrestrial, freshwater and mangrove,

respectively (Fig. 6). Taxa with adhesive knobs and branches were not found in mangrove

0%

20%

40%

60%

80%

100%

Terrestrial Freshwater Mangrove

Unkown

AK & NCR

AC

AK

CR

AN

Fig. 6 Type of trapping devices; AN adhesive network, CR constricting ring, AK adhesive knob, AC adhesivecolumn or branch, AK and NCR adhesive knob and non-constricting ring, by isolated species from different habitats

Fig. 5 Number of species share in different habitats: T terrestrial, F freshwater, M mangrove

Biodivers Conserv (2009) 18:1695–1714 1707

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habitats, whilst all types of trapping devices were isolated from terrestrial and freshwater

habitats.

Discussion

Do nematode trapping fungi occur in marine habitats?

Considering the high diversity and large numbers of nematodes that have been shown to

occur in marine and mangrove habitats (Bongers and Ferris 1999; Lambshead and Boucher

2003), it is surprising that only one species of nematode trapping fungi, A. dactyloides, has

been recorded. It is not clear whether this is due to the fact that saline habitats have never

been studied for nematode-trapping fungi or because they do not exist in nature. The main

purpose of this study was therefore to establish whether nematode-trapping fungi occurred

in marine habitats, and if they did, whether they were typical of or identical to the

terrestrial and freshwater species, or comprised a completely different group.

This study revealed 17 nematode-trapping fungal species from the mangrove habitat.

All species could be accommodated in previously described species, however, their

characteristics differed to a lesser or greater extent and none were identical. This variation

in characters will be discussed in next paper. The nematode-trapping fungi were found to

be typical of the freshwater and terrestrial species found in Hong Kong. One species was

new to science and an unusual hyphomycete which we could not place in any genus (not

shown here) appeared to have sticky knob-like nematode trapping spores.

Although no Orbilia species have been recorded in marine habitats we confirm here that

Orbilia anamorphs are the dominant nematode trapping fungi found in marine environ-

ments. It is interesting that the teleomorphs have not been found in mangroves in nature.

Hyde made extensive collections in mangroves systems in Brunei, Indonesia and the

Seychelles and never found any Orbilia species (Hyde 1988, 1990; Hyde and Goh 1998). It

would be interesting to establish the reason for this.

Comparison of nematode trapping fungi with previous studies

Communities of nematode-trapping fungi among terrestrial, freshwater and mangrove

habitats and substrates in Hong Kong have been compared. There is no similar published

study that we are aware of in any other country, thus direct comparisons with other studies

cannot be made. We can, however, compare our results with those from other specific

habitats. Nematode-trapping fungi were abundant in all the habitats examined, with over

65% of the samples containing nematode-trapping fungi. With the exception of two taxa, a

unidentified species and Arthrobotrys conoides (Poon and Hyde 1998), nematode-trapping

fungal species recorded in this study have not been recorded from Hong Kong. In a survey

of nematode-trapping of lead polluted soil in Kunming, China, Mo et al. (2006) recorded

28 taxa, the most common species being M. thaumasium, A. oligospora and Monacros-porium phymatopagum. It is interesting to note that M. phymatopagum was absent in Hong

Kong, although this species was common in Kunming. In similar survey on diversity of

nematode-trapping fungi from freshwater in Kunming, China, Hao et al. (2005) recorded

35 nematode-trapping species all of which have previously been recorded from terrestrial

habitats. Twenty of the nematode-trapping species isolated from freshwater habitats in this

study are the same as those reported from freshwater in Kunming (Hao et al. 2005). The 16

nematode-trapping species recorded from mangroves in Hong Kong are new records for

1708 Biodivers Conserv (2009) 18:1695–1714

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mangrove habitats worldwide. However, these species have previously been reported from

terrestrial and freshwater habitats (Peterson and Katznelson 1964; Gray 1983; Jaffee et al.

1996; Elshafie et al. 2003; Hao et al. 2005; Mo et al. 2006).

Many fungal genera (e.g. Anthostomella, Aniptodera, Didymella, Massarina, Lophios-toma, Phomatospora, Saccardoella and Savoryella have species reported from freshwater,

marine and terrestrial habitats Vijaykrishna et al. 2006). However, the species are mostly

unique to terrestrial, freshwater or marine habitats. Aniptodera chesapeakensis and Sa-voryella lignicola are exception as they are know from freshwater and marine habitats

(Alias and Jones 2000; Cai et al. 2002; Tsui et al. 2003). In this study, 13 species of

nematode-trapping fungi were overlapped in terrestrial, freshwater and mangrove habitats

of Hong Kong. Cai et al. (2006) noted that fungal species identified from bamboo culms

submerged in freshwater overlapped with those on terrestrial bamboo culms samples—

however, the overlap was low (18.3%). Vijaykrishna et al. (2006) proposed that freshwater

and marine lignicolous ascomcyetes had evolved from terrestrial fungi. There are little to

no distinct morphologically differences between the species of genera Massarina and

Lophiostoma that occur in different habitats (Vijaykrishna et al. 2006). Byrne and Jones

(1975) also pointed out that the conidia carried from freshwater regions to brackish water

may also be able to germinate and colonize the leaf detritus in the brackish water.

Additionally, our observation suggests that the ability of a fungal species to survive and

propagate in wider ecological-niches is a considerable advantageous trait. It is, never-

theless, equally probable that different populations of a fungal species are restricted to

different ecological niches and habitats.

Fungal diversity and similarities between habitats

Biotic and abiotic factors (e.g. altitude, habitat, soil moisture, pH, and nematode density)

affect the occurrence and species diversity of terrestrial nematode-trapping fungi (Gray

1987). In this study we observed that species diversity in terrestrial habitats was signifi-

cantly higher than in freshwater and mangrove habitats, whereas no significant differences

in species diversity were observed between freshwater and mangrove habitats. Shearer

et al. (2007) stated that there is lower diversity of fungi in general in freshwater or marine

habitats as compared to terrestrial habitats. This is thought to be because (a) basidiomy-

cetes, zygomycetes and lichens are uncommon in aquatic habitats (b) of low plant species

diversity in aquatic habitats, and (c) of physiological constraints of growth when sub-

merged in water; especially seawater (Shearer et al. 2007). Some studies, however, have

reported contrasting results; a higher species richness was found on submerged decaying

bamboo culms as compared to terrestrial culms (Cai et al. 2006). Similarly higher diversity

was reported from submerged versus terrestrial wood samples (Fryar et al. 2004).

Accounting for differences in species diversity in decaying wood and leaves

The species diversity (H0) values clearly show that decaying leaves support a significantly

higher nematode-trapping fungal species diversity than decaying wood in all habitats

(Fig. 4). Coarse woody debris provides vital macro habitats for a variety of organisms,

such as fungi, bryophytes, lichens, invertebrates, and amphibians (Maser and Trappe 1984;

Harmon et al. 1986; Esseen et al. 1997; O’dor and Standovar 2002). Generally with

decaying microorganisms, there is lower diversity in larger substrates than smaller sub-

strates due to the high C/N ratio and available oxygen. Moreover, the abundance of

nematodes in the litter is significantly affected by litter quality (low quality: high C/N ratio,

Biodivers Conserv (2009) 18:1695–1714 1709

123

high quality: low C/N ratio); nematode density was significantly higher in the high quality

litter than low quality litter (Ilieva-Makulec et al. 2006). A possible explanation could be

that leaves break down faster than wood because of favourable C/N ratios and relatively

rapid release of nutrients. This would enhance bacteria growth which in turn will feed

bacterivorous nematodes, which eventually feed the nematode-trapping fungi.

When considering species to surface area relationships, we might expect that if a

substrate has a larger surface area it is more likely to harbour a greater number of species.

However, a large item of course woody debris may provide more ‘‘space’’ for larger

individuals to grow, rather than providing more space for a wider range of species

(Lonsdale et al. 2008). Heilmann-Clausen and Christensen (2004) also found that although

the number of wood-inhabiting fungal species increases with coarse woody debris size, the

number of fungi per unit decreases. These findings are supported by our results. Moreover,

annual fungal mass production in wood and leaves per basis has been calculated and

compared by Gulis et al. (2008). The annual fungal mass production from wood was 4.3–

5.5 g cm-2 per year, which is considerably lower than that from leaves (15.8–33.1 g cm-2

per year). Fungal mass production and microbial respiration per gram of detrital C were 3–

13 times lower in wood than in leaves. Fungal growth rates were also higher on leaves than

on wood (Gulis et al. 2008). It is, however, unclear whether these factors correlate with

fungal species members. Nevertheless, species diversity data does not support the higher

species to larger surface area assumption. There should also be different nematode-trap-

ping species communities on the two substrates because the composition of fungal

communities largely depends on environmental factors such as nutrients, C/N ratio, lignin

concentration, size and thickness of substrates, available oxygen, residence time in nature

and biotic factors such as nematode density (Gray 1987; Das et al. 2007; Li et al. 2007;

Lonsdale et al. 2008; Wakelin et al. 2008). The fungal communities on leaves and wood

should therefore differ.

Why adhesive trappers are more abundant than others?

Nematode-trapping fungal species forming adhesive networks were isolated more fre-

quently in all habitats than other trapping types and agrees with previous findings (Gray

1987; Persmark and Jansson 1997; Hao et al. 2005; Mo et al. 2006). Although several

environmental factors may affect the occurrence and diversity of fungi, the frequent

occurrence of adhesive networks might be explained by growth rate and competitive

saprotrophic ability of the fungi. Nematode-trapping fungi with adhesive networks grow

most rapidly, while those with other trapping devices grow 2–3 times more slowly (Cooke

1963). Network trapping fungi appeared to be able to compete successfully with the soil

mycota, whereas those with constricting rings are less competitive (Cooke 1963). Adhesive

network trapping fungi are largely independent of soil fertility and can be found in very

low nutrients soil (Gray 1988). It seems likely that adhesive network trapping fungi have a

good saprotrophic ability and a rapid growth rate which will allow them to compete

favourably with other organisms for limited nutrients. However, whether those abilities are

correlated with a predacious ability in nature is unknown.

Is fungal diversity data technique dependent?

In total 20 nematode-trapping fungal taxa were recorded from freshwater habitats in this

study. Tsui et al. (2000) isolated 92 anamorphic hyphomycetes on decaying wood from

freshwater habitats in Hong Kong. Ho et al. (2002) also recorded 51 hyphomycetes from

1710 Biodivers Conserv (2009) 18:1695–1714

123

the Tai Po Kau forest stream. It is interesting to note that, no nematode-trapping fungi were

isolated from decaying wood in these studies considering that our sample sites cover the

Shing Mun Reservoir stream and Tai Po Kau forest stream. Moreover, numerous studies

have focused on fungal diversity of decomposing leaf and woody litter (Tsui et al. 2000;

Wai et al. 2001; Cai et al. 2003; Ananda and Sridhar 2004; Gopal and Chauhan 2006;

O’dor et al. 2006; Gulis et al. 2008; Lonsdale et al. 2008; Kodsueb et al. 2008; Duong et al.

2008). These studies, however, provided no information on the diversity of nematode-

trapping fungi. These results clearly support the observation that the type of fungi collected

from nature is technique dependent (Shearer et al. 2007).

Nematode-trapping fungi are usually difficult to identify even to genus level without

having information on the type of trapping device. It is a serious flaw of the classical

method, especially in quantifying the frequency of occurrence for nematode-trapping

fungi. Future studies should combine classical methods with other methods (especially

environmental molecular sampling) to measure the taxonomic diversity of nematode-

trapping fungi, e.g. denaturing gradient gel electrophoresis (Anderson and Cairney 2004;

Duong et al. 2006; Kataoka et al. 2008) are encouraged. Now that we have established that

nematode-trapping fungi can occur in mangroves the study should be expanded to involve

other marine habitats (sandy beaches, oceans, deep sea). We also need to establish the role

of NTF in marine habitats as we have found that their ability to produce trapping devices

diminishes with increasing salinity in vitro.

Acknowledgments We would like to thank Dr. Lau Chun Pong for his generosity in sharing knowledge instatistics. Helen Leung is thanked for technical assistance. The University of Hong Kong is thanked forproviding fund, a doctoral studentship.

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