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DIVERSITY AND VERTICAL DISTRIBUTION OF VASCULAR EPIPHYTES 3
ON A MALAYSIAN MANGROVE ISLAND 4
5
Rohani S, Lee FL, Jusoh AS 6
7
DOI: - 8
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To appear in : BIOTROPIA Issue 10
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Received date : 01 January 2019 12
Accepted date : 07 February 2019 13
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This manuscript has been accepted for publication in BIOTROPIA journal. It is unedited, thus, 15
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2 DIVERSITY AND VERTICAL DISTRIBUTION OF VASCULAR EPIPHYTES
18
ON A MALAYSIAN MANGROVE ISLAND**
19 20
Shahrudin Rohani*, Fei Lin Lee and Abdul Shukor Jusoh 21
School of Marine and Environmental Sciences, Universiti Malaysia Terengganu, 21030 Kuala 22
Nerus, Malaysia 23
*Corresponding author, e-mail: rohanishahrudin@umt.edu.my 24
**This paper was presented at the 3rd International Conference on Tropical Biology (ICTB) 2018, 25
20-21 September 2018, Bogor, West Java, Indonesia 26
27
Running title: Diversity and vertical distribution of vascular epiphytes in mangrove ecosystem 28
29
ABSTRACT 30
Many studies have attempted to explain the diversity and abundance of epiphytic plants in 31
major ecosystems worldwide. However, investigations of the abundance of epiphytic plants in 32
mangroves have remained rare. The aim of this research was to study the diversity and distribution 33
of vascular epiphytes in a mangrove forest in peninsular Malaysia. The sampling took place over 0.1 34
hectares of Pulau Telaga Tujuh, a mangrove island in Terengganu, Malaysia. Trees with vascular 35
epiphytes were divided into three strata: basal, trunk and canopy. Vascular epiphytes were identified, 36
and the number of individuals in each stratum was recorded. In total, 8 species of vascular epiphytes 37
from 6 genera and 4 families were recorded. Pulau Telaga Tujuh mangrove forest exhibited a 38
relatively low diversity of vascular epiphytes (H’=1.43). The dominance of Hydnopytum formicarum 39
contributes significantly to the diversity of vascular epiphytes in this forest. Meanwhile, the highest 40
abundance of epiphytes was recorded on the trunks of the host trees. The vertical distribution pattern 41
observed in this study can be associated with the adaptation of the epiphytic plants to stresses in 42
mangrove ecosystem, which is drought and salt spray. In conclusion, Pulau Telaga Tujuh had a high 43
density of vascular epiphytes but lower diversity compared with some ecosystems.
44 45
Keywords: Epiphyte ecology, mangroves, Setiu Wetlands, spatial distribution 46
47
INTRODUCTION 48
Epiphytes are plants that germinate and live on trees without taking nutrients from the soil or 49
the host tree. Vascular epiphytes such as orchids and ferns are able to adapt to an aerial environment, 50
an ability that has led to variations in their morphology. The diversity of vascular epiphytes is 51
important because it contributes to the diversity of vascular plants, which constitute roughly 9% of 52
all vascular plants (Zotz 2013). Since the 18th century, studies of vascular epiphytes have been 53
conducted around the world, particularly in tropical regions known for their biodiversity (Zotz 2016).
54
Vascular epiphyte diversity plays an important role in forest ecosystems. Vascular epiphytes, 55
especially those that live in the canopy zone, help to regulate the cycling of nutrients (Coxson &
56
Nadkarni, 1995). Dead vascular epiphytes decompose and create organic matter on the ground or 57
form humus on tree branches or trunks (Coxson & Nadkarni, 1995). This organic matter provides 58
nutrients and increases the biomass of the ground, especially in primary forest (Nadkarni et al. 2004).
59
3 Vascular epiphytes also provide a variety of food resources for many organisms such as birds and 60
insects. For example, 59% of 33 species of birds in a tropical rain forest in Costa Rica were observed 61
foraging epiphytes resources (Nadkarni & Matelson, 1989). Some epiphytes exhibit a positive 62
association with ants. Ants help to disperse seeds for epiphytes, and the plants provide a nest for the 63
ants (Kaufmann et al. 2001; Dejean et al. 2003).
64
The distribution of vascular epiphytes tends to be affected by the availability of substrate and 65
the distance of dispersal of seeds rather than the mode of dispersal (Nieder et al. 2000). The 66
microhabitat (e.g. light intensity, proximity to soil or exposure to wind and precipitation) has been 67
suggested to be associated with the availability of substrate and therefore influence species richness 68
and the abundance of vascular epiphytes in each stratum and host trees (Quaresma & Jardin, 2014;
69
Woods et al. 2015; Getaneh & Gamo, 2016; Wang et al. 2016). Woods (2013) also found that vascular 70
epiphytes tended to colonize zones with similar microhabitats, which indicated that vascular 71
epiphytes may be specific to particular strata. Strata specificity was also been used to explain the 72
pattern of vertical distribution of vascular epiphytes (Kersten, 2009).
73
The tendency of epiphytes in occupying a similar microhabitat can also stem out from their 74
mechanisms in utilizing the resources. Since major portion of epiphytes does not attach to the soil, 75
epiphytes show several strategies to obtain nutrients and water supply from their microenvironment 76
(Benzing 1990). Epiphytes get nutrients from internal and external inputs (Zotz 2016). Internal inputs 77
can be from leaves leachate from host-tree (Hietz et al. 2002) and nitrogen fixing bacteria (Fürnkranz 78
et al. 2008) while they gain nutrients externally through dry deposition and precipitation (Zotz 2016).
79
Throughfalls and stemflow also contribute to the nutrients input for epiphytes (Awasthi et al. 1995;
80
Chuyong et al. 2005). Cardelús and Mack (2010) showed that different epiphytes use different 81
nutrient uptake mechanisms, hence explain the co-occurrence the different assemblage of epiphytes.
82
To adapt in drought environment on the canopy, epiphytes developed morphological 83
adaptations such as succulent leaves and water absorbing structures (Benzing 1990; Hietz et al. 1999).
84
Meanwhile, physiological adaptation such as Crassulacean Acid Metabolism (CAM) photosynthetic 85
has been found in many epiphytes (Holtum et al. 2007; Silvera et al. 2010). CAM refers to plants 86
which open their stomata during night time to capture CO2 and close the stomata during daylight.
87
Many epiphytic studies have focused on documenting the richness of mangrove flora.
88
However, little attention has been paid to epiphytic plants in this type of forest. Epiphytes are perhaps 89
most susceptible to mangrove destruction because they depend on having large trees as their hosts. A 90
recent study found a remarkable abundance of an epiphytic species, Hydnophytum formicarum, in 91
Pulau Telaga Tujuh, Malaysia (Rohani et al. 2017). This finding motivated us to investigate the 92
occurrence of other vascular epiphytes on this particular island. This study aimed to determine the 93
4 species diversity and vertical distribution of vascular epiphytes in a mangrove ecosystem in the Setiu 94
Wetlands in the east coast of peninsular Malaysia.
95 96
MATERIALS AND METHODS 97
Study Site 98
We conducted our research in Pulau Telaga Tujuh, which is part of the Setiu Wetlands, 99
Terengganu, Malaysia (N 05° 41.800’ E 102 ° 41.770’). The Setiu Wetlands is a wetland ecosystem 100
with nine interconnected habitats consisting of beach, sea, mudflat, fresh and brackish water, river, 101
islands, coastal and mangrove forests (Jamilah et al. 2015). This unique ecosystem has been gazetted 102
as state park in May 2018. These natural ecosystems support a myriad of biodiversity and are 103
accordingly important to local people’s livelihoods. The study site was one of the small islets (5.42 104
ha) in the lagoon of Setiu. Besides this island, there are about 13 other islands in the lagoon.
105 106
Data Collection 107
We randomly established 10 plots with the size of 10 m2 each (1,000 m2 in total) along the 108
island. Every tree in each subplots was inspected for the occurrence of vascular epiphytes. The 109
abundance of all vascular epiphytes, the strata and the host characteristics (e.g., stem diameter and 110
height) were recorded. The strata of the hosts were classified into three strata: 1) canopy - first branch 111
to the tip of the tree, 2) trunk - 1.3 m above the ground to the first branch, and 3) basal - ground up to 112
1.3 m high in the host tree (for trees with an enlarged stem the base was 1.3 m above the ground) 113
(Mojiol et al. 2009; Getaneh & Gamo, 2016).
114
All of the vascular epiphytes were included in the census except for the seedlings that we 115
found it difficult to identify up to the species level. The epiphytes that grew in clusters that were 116
difficult to count individuallywere counted as an independent individual (Getaneh & Gamo, 2016).
117
Binoculars were used to observe the epiphytes that were located high in the trees. The names of the 118
epiphyte species and host plants were checked in A Catalogue of the Vascular Plants of Malaya 119
(Turner, 1995). Voucher specimens were deposited in the Universiti Malaysia Terengganu Herbarium 120
(UMTP).
121 122
Data Analysis 123
Vascular epiphyte diversity was analysed using two diversity indices; Shannon diversity index 124
(H’) and Simpson’s index (D) (Magurran & McGill, 2011). Cluster analysis was carried out using the 125
Jaccard similarity index based on the number of individuals of each vascular epiphyte species on each 126
5 host tree species to check the similarity between the epiphytes communities of each host tree. The 127
data were analysed using PAST version 3.15 software (Hammer et al. 2001).
128 129
RESULTS AND DISCUSSION 130
Species Diversity 131
A total of 929 individuals spanning 8 species, 6 genera and 4 families were recorded in this 132
study (Table 1) (Figure 1). The density of vascular epiphytes in the plots was, on average, 0.93 133
individuals/m2. The alpha diversity of this plant was low, as shown by Shannon diversity index 134
(H’=1.43). Meanwhile, the Simpson’s index (D) was 0.31, which indicated the dominance of one 135
species in the species richness. According to Giesen et al. (2007), mangrove forests in Southeast Asia 136
exhibit at least 28 species of epiphytic plants. In other words, only 2% of epiphytic species can be 137
found in Pulau Telaga Tujuh. As a comparison, an earlier epiphytic study in a mangrove forest in 138
Malaysia found 16 species from 8 families (Japar Sidik et al. 2001). Gradstein et al. (1996) recorded 139
a larger number of species with a larger sampling area. This situation may explain the low H’ value 140
found in this study.
141
Apocynaceae was the well-represented family in term of numbers of species (3 species).
142
Hydnophytum formicarum was found the species with largest individual numbers in the study site. In 143
many previous epiphytic studies, species with dust-like seeds have been found to be dominant. For 144
example, Orchidaceae was recorded as the dominant family in natural forests as well as in rubber 145
plantations in Malaysia (Madison, 1979; Kiew & Anthonysamy, 1987). Most species from 146
Orchidaceae have small seeds, which increases their ability to be dispersed by wind.
147 148
Table 1 List of vascular epiphytes in Pulau Telaga Tujuh, Terengganu, Malaysia 149
150
Species Family Number of individuals
Dendrobium crumenatum Orchidaceae 8
Dischidia nummularia Apocynaceae 150
Hoya coronaria Apocynaceae 51
Hoya verticillata Apocynaceae 5
Hydnophytum formicarum Rubiaceae 462
Pyrrosia piloselloides Polypodiaceae 127
Taeniophyllum glandulosum Orchidaceae 125
Dendrobium sp. Orchidaceae 1
6 151
152
153 154 155 156 157 158 159 Figure 2 Photos of vascular epiphytes found in 160
Pulau Telaga Tujuh, Terangganu:
161
A – Dendrobium cruminatum; B – Hydnophytum 162
formicarum; C - Dischidia nummularia; D - 163
Hoya verticillata; E - Pyrrosia piloselloides; F - 164
Taeniophyllum glandulosum; G - Dendrobium sp.
165
166
167
A B
C
E
G
D
F
7 The rank-abundance curve (Figure 3) reveals an unequal proportion of common species and 168
rare species. The steep line in the graph derives from the dominance of Hydnophytum formicarum.
169
This plant, which has a close association with ants (hence sometimes called the “ant plant”), was also 170
reported to be a common species and more abundant than other non-ant-associated species in Ulu 171
Endau, Johor, Malaysia (Kiew & Anthonysamy, 1987). Similarly, Nieder et al. (2000) also found that 172
there was high abundance of ant-associated epiphytic species in the Amazonian lowland rainforest.
173
The high abundance of the ant plant in one ecosystem may be explained by ants helping to cultivate 174
the seeds. This phenomenon, which is called ant farming, was proposed by Chomicki and Renner 175
(2016) after their observation of the evolutionary history between ants and epiphytic plants. The ants 176
collected the seeds and planted the seeds in the bark fissures, where they germinated. This situation 177
might also have occurred in Hydnophytum formicarum in Pulau Telaga Tujuh because the individuals 178
of the species were found to be distributed in a clumped pattern (Rohani et al. 2017).
179 180
181
Figure 3 Rank-abundance plot based on the number of individuals of each vascular epiphyte species 182
in Pulau Telaga Tujuh, Terengganu 183
184
We found a total of 152 trees were occupied with vascular epiphytes (Table 2). These host 185
trees were comprised of nine families, 11 genera and 13 species. Host trees that were occupied by the 186
large number of epiphytes included Heritiera littoralis, Xylocarpus granatum and Ceriops zippeliana;
187
meanwhile Hibiscus tiliaceus was the least occupied (Table 3). According to the composition of 188
epiphytic species on the host trees, cluster analysis grouped the host species into three major groups 189
(Figure 4). Thirty percent of the vascular epiphytes of Planchonella obovata were similar to those of 190
other hosts; other host trees shared at least 50% similar vascular epiphytes.
191 192
Table 2 List of host tree species for vascular epiphytes in Pulau Telaga Tujuh, Terengganu 193
Host tree Family Number of individuals
Avicennia marina Avicenniaceae 3
8 194
Epiphyte species richness has been shown to exhibit a positive correlation with stem diameter 195
in many studies (e.g. Kersten et al. 2009; Hayasaka et al. 2012; Woods, 2013; Wang et al. 2016;
196
Sousa et al. 2017). However, it is interesting to note that hosts with a high degree of epiphyte species 197
richness were inland trees. This finding was demonstrated in our clustering analysis; the third group 198
was comprised of trees that grow at mid-intertidal to landward zones. Hayasaka et al. (2012) 199
highlighted the important role of inland trees as hosts to many epiphytic ferns in mangroves in 200
Thailand. The trees in the inland zone tend to be mature and larger. This situation might be also true 201
in our study because the largest tree in our study plot was Xylocarpus granatum, with a DBH size of 202
60 cm.
203
Phorophytes characteristics such as bark structure also could influence the distribution of the 204
epiphytes (Wyse & Burns, 2011; Sáyago et al., 2013; Wagner et al., 2015). Three phorophytes with 205
highest number of epiphytes were observed sharing a common trait, which having generally rough 206
bark surface. We observed Xylocarpus granatum possess flaky and dippled bark, meanwhile Hiritiera 207
littoralis and Ceriops decandra had fissured barks. Rough bark structures were able to trap much 208
humus and deposited as substrates for epiphytes (Nurfadilah, 2015). Rough and fissured barks 209
structure have high ability to accumulate litter and debris and also retain moisture from water trapped 210
in between their crevices (Reyes et al., 2010; Zytynska et al., 2011). These will serve as microsites 211
for epiphytes attachments besides acting as water catchment and accumulating nutrients (Cascante- 212
Marín et al. 2009, Wagner et al. 2015). Rough surfaces also provided better mechanical supports for 213
epiphytes attachments with better gripped surfaces for frictions, hence logically explaining why plants 214
species with smooth surface structure such as Nypa fruticans was not chosen as phorophytes even 215
though they are quite numbered on Pulau Telaga Tujuh.
216
Bruguiera cylindrica Rhizophoraceae 7
Bruguiera gymnorrhiza Rhizophoraceae 4
Casuarina equisetifolia Casuarinaceae 5
Ceriops tagal Rhizophoraceae 9
Ceriops zippeliana Rhizophoraceae 30
Excoecaria agallocha Euphorbiaceae 4
Heritiera littoralis Sterculiaceae 34
Hibiscus tiliaceus Malvaceae 3
Pandanus fascicularis Pandanaceae 2
Planchonella obovata Sapotaceae 3
Rhizophora apiculata Rhizophoraceae 13
Xylocarpus granatum Meliaceae 35
9 Table 3 Abundance of the vascular epiphytes on each host tree species in Pulau Telaga Tujuh, Terengganu
217
(DC= Dendrobium crumenatum, DN= Dischidia nummularia, HC= Hoya coronaria, HV= Hoya verticillata, HF= Hydnophytum 218
formicarum, PP= Pyrrosia piloselloides, TG= Taeniophyllum glandulosum, DS= Dendrobium sp.) 219
220
Host tree species
Number of epiphytic individuals in each epiphytic species
Total
DC DN HC HV HF PP TG DS
Avicennia marina 5 2 0 0 9 0 0 0 16
Brugueira cylindrica 0 1 0 0 6 15 2 0 24
Brugueira gymnorrhiza 0 7 0 0 4 14 0 0 25
Casuarina equisetifolia 0 0 0 0 10 6 0 0 16
Ceriops tagal 0 3 1 3 3 2 7 0 19
Ceriops zippeliana 1 22 7 0 52 14 53 0 149
Exoecaria agallocha 0 26 0 0 10 11 0 0 47
Heritiera littoralis 0 38 11 2 158 28 42 1 280
Hibiscus tiliaceus 0 1 0 0 3 0 0 0 4
Pandanus fascicularis 1 11 0 0 4 2 0 0 18
Pallaquim obovata 0 0 2 0 7 0 0 0 9
Rhizophora apiculata 1 9 2 0 23 25 20 0 80
Xylocarpus. granatum 0 30 28 0 173 10 1 0 242
10 221
222
Figure 4 Cluster analysis according to the number of individuals of each vascular epiphyte species 223
on each host tree species using the Jaccard similarity index 224
225
Vertical Distribution 226
The strata “trunk” was most frequently found to harbour epiphytes, followed by “canopy” and 227
“basal” (Table 4). This type of vertical distribution was more or less consistent with many epiphytic 228
studies (Zotz & Schultz 2008; Quaresma & Jardin 2014; Getaneh & Gamo 2016; Mohamed et al.
229
2017). The preference of epiphytes in certain strata is influenced by their ability to adapt with various 230
levels of photon flux density (PFD) and humidity (Benzing 1990). This acclimation process might 231
prominent in stressing environment such as in mangrove. Epiphytes in mangrove forest are highly 232
exposed to stresses such as drought and salt spray. To adapt to the drought, epiphytes in Pulau Telaga 233
Tujuh probably utilize the CAM photosynthesis as physiological adaptation to survive in the stress 234
environment (Table 5). The relation between CAM strategy and the preference of the epiphytes in 235
certain strata in our study is consistent with other observations that CAM species tend to clump in 236
areas of higher light intensity and exposed site (Ting 1985; Zotz & Ziegler 1997; Zotz 2004).
237 238
Table 4 The occurrence of epiphytic plants on each stratum in Pulau Telaga Tujuh 239
Vascular Epiphyte species Number of Epiphytic Individuals per Stratum
Basal Trunk Canopy
Dendrobium crumenatum 6 2 0
Dischidia nummularia 22 82 46
Hoya coronaria 4 41 6
Hoya verticillata 0 4 1
11 240
Most CAM species is characterized by thick leaves, trait that assist the plants in reducing 241
water lost (Teeri et al. 1981; Barrera-Zambrano et al. 2014), which also was observed in all species 242
found in Pulau Telaga Tujuh. Having schlerophyllous leaves also helps the epiphytes in counter the 243
high salinity environment. Zotz and Reuter (2009) found that most epiphytes do not become 244
halophyte to adapt the saline environment. This factor could explain the lower preference of epiphytes 245
at basal area. Furthermore, long-term inundation of the basal region in water is not favourable for 246
plant growth because a stable substrate is an important factor for epiphyte establishment (Nieder et 247
al. 2000; Woods 2013). This factor has also been suggested by Hayasaka et al. (2012) as one of the 248
contributing factors for the distribution of ferns in mangrove forests in Thailand. Hence, we observed 249
a low concentration of epiphytes at the lower strata of individual host trees in our study.
250 251
Table 5 Mode of photosynthesis for each vascular epiphytes in Pulau Telaga Tujuh that was 252
extrapolated from published works (Winter et al. 1983; Hew & Yong 2004) 253
Epiphyte species Mode photosynthesis
Dendrobium crumenatum CAM
Dischidia nummularia CAM
Hoya coronaria CAM
Hoya verticillata CAM
Hydnophytum formicarum Likely to be variable between C3-CAM
Pyrrosia piloselloides CAM
Taeniophyllum glandulosum CAM
Dendrobium sp. More likely to be CAM than C3 254
CONCLUSION 255
The diversity of vascular epiphytes in mangrove forest on Pulau Telaga Tujuh was relatively 256
low, with Shannon index (H’) 1.43. Hydnophytum formicarum was the most abundant species in the 257
study area. The vertical distribution of epiphytes in the study area was depicting the adaptations of 258
these plants to the stresses in mangrove ecosystem. The findings from this study can be used to 259
support the conservation effort of this unappreciated plant group.
260 261
Hydnophytum formicarum 22 289 151
Pyrrosia piloselloides 31 74 22
Taeniophyllum glandulosum 45 59 21
Dendrobium sp. 0 0 1
Total 130 551 248
12 ACKNOWLEDGEMENTS
262
The authors thank the Ministry of Education of Malaysia for funding this project under Niche 263
Research Grant Scheme (Vot No. 53131/12). We also thank Mohamad Razali Salam for helping us 264
identify the epiphytes and host species.
265 266
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