DIVERSITY AND VERTICAL DISTRIBUTION OF VASCULAR EPIPHYTES ON A MALAYSIAN MANGROVE ISLAND

Full text

(1)

1 ACCEPTED MANUSCRIPT

1 2

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

9

To appear in : BIOTROPIA Issue 10

11

Received date : 01 January 2019 12

Accepted date : 07 February 2019 13

14

This manuscript has been accepted for publication in BIOTROPIA journal. It is unedited, thus, 15

it will undergo the final copyediting and proofreading process before being published in its final 16

form.

17

brought to you by CORE View metadata, citation and similar papers at core.ac.uk

provided by BIOTROPIA - The Southeast Asian Journal of Tropical Biology

(2)

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)

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)

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)

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)

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)

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)

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)

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)

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)

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)

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

REFERENCES 267

Awasthi OP, Sharma E, Palni LMS. 1995. Stemflow: A Source of Nutrients in some Naturally 268

Growing Epiphytic Orchids of the Sikkim Himalaya Annals of Botany 75: 5-11 269

Barrera-Zambrano V, Lawson T, Olmos E, Fernández-Garcia N, Borland A. 2014. Leaf anatomical 270

traits which accomodate the facultative engagement of crassulacean acid metabolism in 271

tropical trees of the genus Clusia. Journal of Experimental Botany 65: 3513–3523 272

Benzing DH. 1990. Vascular epiphytes: general biology and related biota. Cambridge, UK:

273

Cambridge University Press 274

Cardelús CL, Mack MC 2010. The nutrient status of epiphytes and their host trees along an 275

elevational gradient in Costa Rica. Plant Ecology 207:25–37 276

Cascante-Marín A, von Meijenfeld N, de Leeuw HMH, Wolf JHD, Oostermeijer JGB, den Nijs JCM.

277

2009. Dispersal limitation in epiphytic bromeliad communities in a Costa Rican fragmented 278

montane landscape. Journal of Tropical Ecology 25: 63-73.

279

Chomicki G, Renner SS. 2016. Obligate plant farming by a specialized ant. Nature Plants [Internet].

280

[cited 2018 October 5]; 2:16181.Available from: http://rspb.royalsocietypublishing.org/ doi:

281

10.1038/nplants.2016.181 282

Chuyong GB, Newbery DM, Songwe NC. 2004. Rainfall input, throughfall and stemflow of nutrients 283

in a central African rain forest dominated by ectomycorrhizal trees. Biogeochemistry 67:73–

284 285 91

Coxson DS, Nadkrni NM. 1995. Ecological roles of epiphytes in nutrient cycles of forest ecosystems.

286

In Lowman NM, Nadkarni MD, editors. Forest Canopies (1st ed.). New York: Academic 287

Press. p. 495–543 288

Dejean A, Durou S, Olmstedt I, Snellingt RR, Orivel J. 2003. Nest site selection by ants in a flooded 289

Mexican mangrove, with special reference to the epiphytic orchid Myrmecophila christinae.

290

Journal of Tropical Ecology 19(3):325–331 291

FürnkranzM, Wanek W, Richter A, Abell G, Rasche F, Sessitsch A. 2008. Nitrogen fixation by 292

phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical 293

lowland rainforest of Costa Rica. The ISME Journal 2:561–570 294

Getaneh ZA, Gamo FW. 2016. Vascular epiphytes in Doshke and Kurpaye: a comparative study, 295

Gamo Gofa, Ethiopia. International Journal of Biodiversity [Internet]. [cited 2018 September 296

28]; 2016:1–10. Available from: http://dx.doi.org/10.1155/2016/9482057 297

Giesen W, Wulffraat S, Zieren M, Scholten L. 2007. Mangrove guidebook for Southeast Asia.

298

Bangkok: FAO and Wetlands International 299

Gradstein SR, Hietz P, Lücking R, Lücking A, Sipman HJM, Vester HFM, Wolf JHD, Gardette E 300

1996. How to sample the epiphytic diversity of tropical rain forests. Ecotropica 2:59–72 301

Hammer Ø, Harper DAT, Ryan PD. 2001. PAST-Palaeontological statistics software package for 302

education and data analysis. Palaeontologia Electronica [Internet]. [cited 2018 September 28];

303

4(1):1-9. Available from: https://palaeo-electronica.org/2001_1/past/issue1_01.htm 304

(13)

13 Hayasaka D, Kimura N, Fujiwara K, Thawatchai W, Nakamura T. 2012. Relationship between 305

microenvironment of mangrove forests and epiphytic fern species richness along the Pan Yi 306

River, Thailand. Journal of Tropical Forest Science 24(2):265–274 307

Hew CS, Yong JWH. 2004. The physiology of tropical orchids in relation to the industry.

308

New Jersey, London, Singapore, World Scientific Press 309

Hietz P, Wanek W, Popp M (1999) Stable isotopic composition of carbon and nitrogen and nitrogen 310

content in vascular epiphytes along an altitudinal transect. Plant, Cell & Environment 311

22:1435–1443 312

Hietz P, Wanek W, Wania R, Nadkarni NM (2002) Nitrogen- 15 natural abundance in a montane 313

cloud forest canopy as an indicator of nitrogen cycling and epiphyte nutrition. Oecologia 314

131:350–355 315

Holtum JAM, Winter K, Weeks MA, Sexton TR (2007) Crassulacean acid metabolism of the ZZ 316

plant, Zamioculcas zamiifolia (Araceae). American Journal of Botany 94:1670–1676 317

Jamilah MS, Faridah M, Rohani S. 2015. Setiu: more than a wetland. In: Jamilah MS, Faridah M, 318

Rohani S. editors. Setiu Wetlands: Species, Ecosystem and Livelihoods. Kuala Terengganu:

319

Penerbit Universiti Malaysia Terengganu. p. 87–100 320

Japar Sidik B, Arshad A, Muta Harah Z, Normazilla M. 2001. Epiphytes of mangrove vegetation of 321

Pulau Redang, Terengganu, Malaysia. In Husain ML, Shahrom F, Law AT, Yunus K, Yaman 322

ARG, editors. Proceeding of National Symposium on Marine Park and Terengganu Islands.

323

2001 Feb 12-13; Kuala Terengganu, Malaysia. P. 68-80 324

Kaufmann E, Weissflog A, Hashim R, Maschwitz U. 2001. Ant-gardens on the giant bamboo, 325

Gigantochloa scortechinii (Poaceae) in West-Malaysia. Insectes Sociaux 48(2):125–133 326

Kersten RA, Borgo M, Silva SM. 2009. Diversity and distribution of vascular epiphytes in an insular 327

Brazilian coastal forest. Biotropica 32(3):385–396 328

Kiew R, Anthonysamy S. 1987. A comparative study of vascular epiphytes in three epiphyte rich 329

habitats at Ulu Endau Johore Malaysia. Malayan Nature Journal 41:303–315 330

Madison M. 1979. Distribution of epiphytes in a rubber plantation in Sarawak. Selbyana 5(2):207–

331 332 213

Magurran AE, McGill BJ. (Eds.). 2011. Biological diversity: frontiers in measurement and 333

assessment. Oxford University Press 334

Mohamed E, Kebebew M, Awas T. 2017. Diversity of vascular epiphytes in Wondo Genet natural 335

forest, Southern, Ethiopia. International Research Journal of Biological Sciences 6(2):5–15 336

Mojiol AR, Merlyn A, Jitinu A, Adella A. 2009. Vascular epiphytes diversity at Pusat Sejadi, Kawang 337

Forest Reserve, Sabah, Malaysia. Journal of Sustainable Development 2(1):121–127 338

Nadkarni NM, Matelson TJ. 1989. Bird use of epiphyte resources in Neotropical trees. The Condor 339

91(4):891–907 340

Nadkarni NM, Schaefes D, Matelson MJ, Solano R. 2004. Biomass and nutrient pools of canopy and 341

terrestrial components in a primary and a secondary montane cloud forest, Costa Rica. Forest 342

Ecology and Management 198:223–236 343

Nieder J, Engwald S, Klawun M, Barthlott W. 2000. Spatial distribution of vascular epiphytes 344

(including hemiepiphytes) in a lowland Amazonian rain forest (Surumoni crane plot) of 345

Southern Venezuela. Biotropica 32(3):385–396 346

Nurfadilah S. 2015. Diversity of epiphytic orchids and host trees (phorophytes) in secondary forest 347

of Coban Trisula, Malang Regency, East Java. Biotropia 22(2): 120–128 348

(14)

14 Quaresma A, Jardin M. 2014. Floristic composition and spatial distribution of vascular epiphytes in 349

the restingas of Maracanã, Brazil. Acta Botanica Brasilica 28(1):68–75 350

Reyes F, Silvana Z, Espinosa A, Marysol A. 2010. Biochemical properties in vascular epiphytes 351

substrate from a temperate forest of Chile. Revista de La Ciencia Del Suelo Y Nutrición Vegetal 352

10(2): 126–138 353

Rohani S, Shukor AY, Kamaruzzaman MF, Salam MR. 2017. Distribution and Host Identification of 354

Epiphytic Plant, Hydnophytum formicarum Jack., in Pulau Telaga Tujuh, Setiu, Terengganu.

355

Journal of Sustainability Science and Management 12(2):128-134 356

Sáyago R, Lopezaraiza-Mikel M, Quesada M, Álvarez-Añorve MY, Cascante-Marín A, Bastida J 357

M. 2013. Evaluating factors that predict the structure of a commensalistic epiphyte- 358

phorophyte network. Proceedings of The Royal Society of Biological Sciences 280: 1-9 359

Silvera K, Neubig KM, Whitten WM, Williams NH, Winter K, Cushman JC (2010) Evolution along 360

the crassulacean acid metabolism continuum. Functional Plant Biology 37:995–1010 361

Sousa MM, Colpo KD. 2017. Diversity and distribution of epiphytic bromeliads in a Brazilian 362

subtropical mangrove. Anais da Academia Brasileira de Ciências, 89(2): 1085-1093 363

Teeri JA, Tonsor SJ, Turner M. 1981. Leaf thickness and carbon isotope composition in the 364

Crassulaceae. Oecologia 50(3): 367-369 365

Ting IP. 1985. Crassulacean acid metabolism. Annual Review of Plant Physiology 36:595–622 366

Turner IM. 1995. A catalogue of the vascular plants of Malaya. Gardens' Bulletin Singapore 47(2):

367

347-655 368

Wagner K, Mendieta-Leiva G, Zotz G. 2015. Host specificity in vascular epiphytes: a review of 369

methodology, empirical evidence and potential mechanisms. AoB Plants [Internet]. [cited 370

2019 February 18]; 7: plu092. Available from:

371

https://academic.oup.com/aobpla/article/doi/10.1093/aobpla/plu092/198714 372

Wang X, Long W, Schamp BS, Yang X, Kang Y, Xie Z, Xiong M. 2016. Vascular epiphyte diversity 373

differs with host crown zone and diameter, but not orientation in a tropical cloud forest. PLoS 374

ONE 11(7):1–13 375

Winter K, Wallace BJ, Stocker GC & Roksandic Z. 1983. Crassulacean acid metabolism in Australian 376

vascular epiphytes and some related species. Oecologia 57:129–141 377

Woods CL, Cardelús CL, Dewalt SJ. 2015. Microhabitat associations of vascular epiphytes in a wet 378

tropical forest canopy. Journal of Ecology 103(2):421–430 379

Woods CL. 2013. Factors influencing the distribution and structure of tropical vascular epiphyte 380

communities at multiple scales [Dissertation]. Retrieved from Clemson University, South 381

Carolina 382

Wyse SV, Burns B R. 2011. Do host bark traits influence trunk epiphyte communities? New Zealand 383

Journal of Ecology 35(3): 296–301 384

Zotz G, Reuter N. 2009. The effect of exposure to sea water on germination and vegetative growth 385

of an epiphytic bromeliad. Journal of Tropical Ecology 25(3):311-319 386

Zotz G, Schultz S. 2008. The vascular epiphytes of a lowland forest in Panama-species composition 387

and spatial structure. Plant Ecology 195(1): 131-141 388

Zotz G, Ziegler H. 1997. The occurrence of crassulacean acid metabolism among vascular 389

epiphytes from Central Panama. New Phytology 137:223–229 390

(15)

15 Zotz G. 2004. How prevalent is crassulacean acid metabolism among vascular epiphytes?

391

Oecologia 138:184–192 392

Zotz G. 2013. The systematic distribution of vascular epiphytes–a critical update. Botanical Journal 393

of the Linnean Society 171(3):453-481 394

Zotz G. 2013. Plants on Plants - The Biology of Vascular Epiphytes. Switzerland: Springer Nature 395

Zytynska SE, Fay MF, Penney D, Preziosi RF. 2011. Genetic variation in a tropical tree species 396

influences the associated epiphytic plant and invertebrate communities in a complex forest 397

ecosystem. Philosophical Transactions of the Royal Society B: Biological Sciences 366: 1329–

398

1336 399

Figure

Updating...

Related subjects :