International Journal of ZoologyVolume 2011 (2011), Article ID 758573, 17 pagesdoi:10.1155/2011/758573

Research Article

Bird Species Abundance and Their Correlationship with Microclimate and Habitat Variables at Natural Wetland Reserve, Peninsular Malaysia

Muhammad Nawaz Rajpar¹ and Mohamed Zakaria²

¹Forest Education Division, Pakistan Forest Institute, Peshawar 25120, Pakistan²Faculty of Forestry, Universiti Putra Malaysia (UPM), Selangor, 43400 Serdang, Malaysia

Received 6 May 2011; Revised 29 August 2011; Accepted 5 September 2011

Academic Editor: Iain J. McGaw

Copyright © 2011 Muhammad Nawaz Rajpar and Mohamed Zakaria. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

Birds are the most conspicuous and significant component of freshwater wetland ecosystem. Presence or absence of birds may indicate the ecological conditions of the wetland area. The objectives of this study were to determine bird species abundance and their relationship with microclimate and habitat variables. Distance sampling point count method was applied for determining species abundance and multiple regressions was used for finding relationship between bird species abundance, microclimate and habitat variables. Bird species were monitored during November, 2007 to January, 2009. A total of 8728 individual birds comprising 89 species and 38 families were detected. Marsh Swamp was swarmed by 84 species (69.8%) followed open water body by 55 species (17.7%) and lotus swamp by 57 species (12.6%). Purple swamphen Porphyrio porphyrio (9.1% of all detections) was the most abundant bird species of marsh swamp, lesser whistling duck—Dendrocygna javanica (2.3%) was dominant species of open water body and pink-necked green pigeon—Treron vernans (1.7%) was most common species of lotus swamp. Results revealed that the habitat characteristics such as vegetation composition (i.e. emergent and submerged vegetations, grasses, shrubs, and trees), vegetation structures (tree diameter and height) and microclimate variables (temperature, relative humidity and light intensity) were the key factors that influenced the distribution, diversity and density of the wetland bird species. This study also revealed that the wetland bird species have adapted a fairly unique set of microhabitat and microclimate conditions.

1. Introduction

Wetlands are characterized by shallow water overlying waterlogged soil, interspersed submerged and emergent vegetation [1–3]. Wetlands are the most productive ecosystems due to their habitat diversity, great productivity, and diverse attributes including a distinctive avifauna. During the past century, wetland areas have been reduced by more than 50% globally, and their destruction will likely continue [4–6]. The gradual loss and degradation of wetlands due to development [7] and pollution [8] have also been adversely affected wetland bird species [9–11].

Birds are an important component of biotic community of wetland ecosystems [12]. They respond quickly to changing in habitat [13, 14]. Thus, birds are good bioindicators of wetland habitat quality, productivity, and stability. Birds often have correlation with their habitats [15] and have also been used as surrogates for assessing the impact of habitat changes [16, 17]. Monitoring the species abundance, habitat preference, and correlationship between species abundance and habitat provides basic information for determining factors causing population fluctuation of bird species [18]. Subsequently, the information helps in conservation and management of threatened and endangered species [19]. Long-term avian monitoring identifies the bird species that decline due to habitat loss or degradation. Similarly, the assessment of vegetation composition and structure is a useful tool to examine and understand the habitat characteristics and impacts of disturbance or alteration of habitats on the avian species. The alteration in wetland habitats may cause changes in avian abundance and diversity [20].

Distance sampling point count method is widely used to examine the avian species abundance in different habitats and the association of bird species with habitats characteristics and microclimates [21–23]. This method involves the visual and auditory detection of birds within fixed- or variable-radius plots [24]. The relative abundance of bird species is often associated with vegetation community and food resources and positively correlated with habitat structural complexity [25, 26].

Malaysia is blessed with extensive wetland areas, that is, 3.5 to 4.0 million ha or 10.0% of the total land area. This total wetland area is divided into marshes, nipa swamps, mangrove, mudflats, freshwater swamps, peat swamp forests, lakes, rivers, sandy beaches, and rocky shore. Information about relative abundance of birds, habitat preference, and association with habitat characteristics and microclimate variables for various wetlands is lacking [27]. Long-term population trends of wetland birds, habitat and microclimate characteristics, as well as correlationship between wetland bird species and habitat characteristics have not been studied. In fact, very little is known on the ecological roles of bird species in relation to habitat and habitat disturbances. Hence, it is important to determine the relative abundance, habitat preference, and correlationship of bird species between habitat characteristics and microclimate variables.

2. Materials and Methods

2.1. Study Site

Paya Indah (a Malay translation of “beautiful swamp”) Wetland Reserve encompasses 3050 ha of lands, out of which 450 ha are under the administrative control of the Department of Wildlife and National Parks, Peninsular Malaysia. Presently study area is located within the quadrant of 101°10′ to 101°50′ longitude and 2°50′ and 3°00′ latitude (Figure 1). A distinctive feature of this natural wetland area is that it comprises of three major habitats, that is, marsh swamp, lotus swamp and open water body that may vary due to heterogeneity of the existing vegetation composition, vegetation structure, hydrology, and productivity and represent specific environmental features that satisfy the biological needs of wetland bird species.

Figure 1: Location map of the Paya Indah Wetland Reserve, Peninsular Malaysia.

2.2. Marsh Swamp

Marsh swamp was shallow water dominated by lush growths of aquatic vegetation such as sedges, reeds, rushes, and grasses. The plants grow with their stems partly in and partly out of the water. About 85% of the total marsh swamp areas are covered with water, while 15% are terrestrial [28]. The marsh swamp was predominantly covered with aquatic plants, namely, Eleocharis dulcis, Lepironia articulata, Stenochlaena palustris, Philydrum lanuginosum, and Scleria purpurascens, and scattered trees such as Acacia auriculiformis, A. mangium, Macaranga tanarius, Peltophorum pterocarpum, Cinnamomum iners, Melicope glabra, and Melastoma malabathricum along the edges. This area was shallow in water depth and rich in prey resources, that is, fish, amphibians, insects, snails, and larvae of invertebrates.

2.3. Lotus Swamp

Lotus swamp was shallow water body dominated by water lilies, sedges, reeds, and grasses. It allows plants to grow and reach the water surface. About 90% of the lotus swamp areas are covered by water, whereas 10% are terrestrial [28]. This area was extensively covered with Nelumbo nucifera, N. nouchali, N. pubescens, E. dulcis, Elodea sp., Phragmites karka reeds, and Typha angustifolia. On the contrary, the dry land is covered with A. auriculiformis, A. mangium, and some parts with M. malabathricum.

2.4. Open Water Body

Open water body was a larger and deep area dominated by submerged vegetation while the edges in shallow water were covered by reeds, sedges, and grasses. About 90% of the total area was covered by water and 10% by dryland [28]. Open Water Bodies was mostly covered with emergent vegetation, such as Nymphaea odorata, Potamogeton spp., E. dulcis, Myriophyllum spicatum, Salvinia molesta, Scirpus sylvaticus, S. californicus, S. mucronatus, and S. maritimus. The edges were dominated by E. dulcis, S. purpurascens, Sagittaria latifolia, and Hydrilla sp. Open water bodies are rich in invertebrates, amphibians, and fish.

2.5. Bird Surveys

Bird species relative abundance was counted using distance sampling from count points from November 2007 to January 2009. One hundred and twenty-one point count stations at 300 m interval were established within three habitats, namely, Marsh Swamp (43 stations), Lotus Swamp (38 stations), and Open Water Body (40 stations), to avoid double counting of the same birds at more than one station. The birds were counted 15 consecutive times at a monthly interval for each station in order to obtain reliable estimates and reduce bias. The survey was conducted early in the morning from 0730 to 1100 hrs. Birds were counted at each station for 10 minutes following Gutzwiller [29], Jimenez [30], Lee and Marsden [31], and Zakaria et al. [28]. During each count, all bird species and individuals seen or heard were recorded. Flushed birds were also recorded, and their known original positions were included in the analysis. However, flying birds were not recorded due to unknown original position. The methodology was used as described by Bibby et al. [32], Buckland et al. [33], Aborn [34] and Nadeau et al. [35].

2.6. Vegetation Assessment

The vegetation variables were sampled in three habitats using the quadrat method (10 m × 10 m) simultaneously at the sites where birds were counted. This method is one of the most commonly used and accepted methods to survey vegetation in a variety of habitats [8, 36, 37]. A total of 120 quadrant plots were sampled for vegetation structure within the consistency of the point count stations. In each sample plot, soil cover percent (i.e., the proportion of soil surface covered with vegetation and bare one %), species richness (i.e., the number of plant species), vegetation type (i.e., trees, shrubs, grasses, emerged and submerged vegetation, sedges, reeds, ferns, and herbs), vegetation height (i.e., meters), vegetation diameter (i.e., centimetres), and microclimate, such as temperature, relative humidity, and light intensity, were recorded. The soil cover, proportion of shrubs, grasses, emerged and submerged vegetation, sedges, reeds, ferns, and herbs were recorded using the visual estimation while the temperature and relative humidity were recorded using psychrometer. In addition, light intensity was recorded using the LUX meter. The methodology was according to Isacch et al. [38].

Plant samples were brought from the field and processed for plant pressure. The pressed plant samples were kept in the oven for drying for one week. Plants were identified using field guides and cross-checked with the samples kept in the Herbarium of the Faculty of Forestry, Universiti Putra Malaysia, Malaysia.

2.7. Analysis

The relative abundance (%) of bird species was estimated using the following expression: [28], where is the number of a particular bird species and is the total observations detected for all species. The correlationship of birds, microclimate variables, and habitat characteristics was determined using multiple regressions of Constrained Redundancy Ordination (RDA) of canonical correspondence analysis (CCA) Software Version 4.5 by Ter Braak and Smilauer [39] in order to understand the variable factors that influenced distribution of bird species in the study area. Canonical correlation analysis (CCA) is a way to determine the linear relationship between two multidimensional variables. It has two bases, in which the correlation matrix between the variables is diagonal and the correlations on the diagonal are maximized. The advantage of canonical correlation is that, it is invariant with respect to affine transformations of the variables.

Let denote observations of an -dimensional random vector, let denote the th observation.

The sample means and sample covariance matrix are defined as The relative abundance data was used for correlation analysis of three habitats instead of the density data. The relative abundance data was used firstly to maximize the correlation of most bird species with microclimate variables and habitat characteristics. Secondly, most of the bird species in each habitat had very low detections (<5 individuals).

3. Results

During the study period, a total of 8728 individual birds, comprising of 89 species and 38 families, were recorded.

3.1. Relative Abundance of Birds in Marsh Swamp

In Marsh Swamp, a total of 6,086 bird observations, that is, 69.7% of all detections, were recorded. The birds belong to 84 species and 37 families. Three species, purple swamphen—Porphyrio porphyrio (9.1% of all detections), yellow-vented bulbul—Pycnonotus goiavier (7.9%), and pink-necked green pigeon—Treron vernans (7.0%) count showed the highest relative abundance. On the contrary, nine bird species, ashy drongo—Dicrurus leucophaeus, black baza—Aviceda leuphotes, blue-breasted quail—Coturnix chinensis, house crow—Corvus splendens, inornate warbler—Phylloscopus inornatus, little spiderhunter—Arachnothera longirostra, pheasant-tailed jacana—Hydrophasianus chirurgus, rusty-rumped warbler—Locustella certhiola, and speckled piculet—Picumnus innominatus showed the least relative abundance, observed only once (0.01% each) in the wetland reserve (Table 1).

Table 1: Relative abundance of bird species recorded at three habitats of Paya Indah Wetland Reserve, Peninsular Malaysia.

Family  name
Scientific  name
Common  name
No. of observations with habitat

Marsh swamp
Lotus swamp
Open water body

Observation
% of all detection
Observation
% of all detection
Observation
% of all detection

Rallidae
Porphyrio porphyrio
Purple swamphen
798
9.14
78
0.89
25
0.29

Pycnonotidae
Pycnonotus goiavier
Yellow-vented bulbul
690
7.91
101
1.16
129
1.48

Columbidae
Treron vernans
Pink-necked green pigeon
614
7.03
150
1.72
90
1.03

Columbidae
Geopelia striata
Peaceful dove
462
5.29
101
1.16
84
0.96

Columbidae
Streptopelia chinensis
Spotted dove
386
4.42
56
0.64
67
0.77

Hirundinidae
Hirundo tahitica
Pacific swallow
208
2.38
39
0.45
85
0.97

Rallidae
Amaurornis phoenicurus
White-breasted waterhen
200
2.29
38
0.44
25
0.29

Ploceidae
Ploceus philippinus
Baya weaver
173
1.98
7
0.08
52
0.60

Sturnidae
Acridotheres tristis
Common myna
166
1.90
17
0.19
51
0.58

Ardeidae
Ardea purpurea
Purple heron
164
1.88
52
0.60
22
0.25

Ardeidae
Ixobrychus sinensis
Yellow bittern
162
1.86
42
0.48
11
0.13

Sturnidae
Acridotheres fuscus
Jungle myna
154
1.76
15
0.17
117
1.34

Alcedinidae
Halcyon smyrnensis
White-throated kingfisher
128
1.47
51
0.58
42
.48

Estrildidae
Lonchura punctulata
Scaly-breasted munia
125
1.43
36
0.41
49
0.56

Estrildidae
Lonchura malacca
Black-headed munia
122
1.40
0
0
3
0.03

Sturnidae
Aplonis panayensis
Philippine glossy starling
116
1.33
0
0
24
0.27

Motacillidae
Anthus richardi
Richard’s pipit
114
1.31
1
0.01
26
0.30

Passeridae
Passer montanus
Eurasian tree sparrow
94
1.08
8
0.09
1
0.01

Charadriidae
Vanellus indicus
Red-wattled lapwing
93
1.07
8
0.09
41
0.47

Aegithinidae
Aegithina viridissima
Green iora
89
1.02
17
0.19
7
0.08

Turdidae
Copsychus saularis
Oriental magpie robin
84
0.96
19
0.22
13
0.15

Meropidae
Merops philippinus
Blue-tailed bee-eater
68
0.80
37
0.42
142
1.63

Rhipiduridae
Rhipidura javanica
Pied fantail
65
0.74
23
0.26
8
0.09

Cisticolidae
Prinia flaviventris
Yellow-bellied prinia
65
0.74
21
0.24
20
0.23

Laniidae
Lanius cristatus
Brown shrike
64
0.73
16
0.18
12
0.14

Rallidae
Gallinula chloropus
Common moorhen
61
0.70
28
0.32
6
0.07

Oriolidae
Oriolus chinensis
Black-napped oriole
59
0.68
11
0.13
14
0.16

Cuculidae
Centropus bengalensis
Lesser coucal
48
0.55
0
0
12
0.14

Sturnidae
Acridotheres grandis
White-vented myna
44
0.50
7
0.08
6
0.07

Anatidae
Dendrocygna javanica
Lesser whistling duck
37
0.42
0
0
199
2.28

Ardeidae
Ixobrychus cinnamomeus
Cinnamon bittern
28
0.32
0
0
6
0.07

Aegithinidae
Aegithina tiphia
Common iora
28
0.32
3
0.03
5
0.06

Picidae
Dinopium javanense
Common flameback
27
0.31
10
0.11
3
0.03

Sylviidae
Acrocephalus orientalis
Oriental reed warbler
24
0.27
1
0
1
0.01

Rallidae
Porzana cinerea
White-browed crake
24
0.27
5
0.07
0
0

Phasianidae
Gallus gallus
Red jungle-fowl
21
0.24
8
0.09
7
0.08

Ardeidae
Butorides striatus
Little heron
20
0.23
3
0.03
0
0

Campephagidae
Lalage nigra
Pied triller
19
0.22
0
0
7
0.08

Columbidae
Treron bicincta
Orange-breasted green pigeon
17
0.19
15
0.17
0
0

Sylviidae
Orthotomus ruficeps
Ashy tailorbird
14
0.16
4
0.05
0
0

Ardeidae
Nycticorax nycticorax
Black-crowned nightheron
13
0.15
0
0
0
0

Nectariniidae
Nectarinia jugularis
Olive-backed sunbird
13
0.15
1
0.01
2
0.02

Cuculidae
Cacomantis merulinus
Plaintive cuckoo
12
0.14
13
0.15
0
0

Anatidae
Nettapus coromandelianus
Cotton pygmy goose
11
0.13
1
0.01
81
0.93

Meropidae
Merops viridis
Blue-throated bee-eater
10
0.10
9
0.10
0
0

Scolopacidae
Gallinago stenura
Pintail snipe
10
0.10
0
0
2
0.02

Nectariniidae
Anthreptes malacensis
Brown-throated sunbird
8
0.09
3
0.03
0
0

Corvidae
Corvus macrorhynchos
Large-billed crow
8
0.09
0
0
12
0

Columbidae
Treron olax
Little green pigeon
8
0.09
1
0.01
0
0

Estrildidae
Lonchura maja
White-headed munia
8
0.09
0
0
0
0

Turnicidae
Turnix suscitator
Barred button quail
7
0.08
1
0.01
0
0

Ardeidae
Ardea cinerea
Grey heron
7
0.08
4
0.05
1
0.01

Sylviidae
Orthotomus sutorius
Common tailorbird
6
0.07
2
0.02
3
0.03

Pycnonotidae
Pycnonotus plumosus
Olive-winged bulbul
6
0.07
0
0
0
0

Sylviidae
Orthotomus sericeus
Rufous-tailed tailorbird
6
0.07
0
0
0
0

Ardeidae
Ixobrychus eurhythmus
Schrenck’s bittern
6
0.07
0
0
1
0.01

Cuculidae
Chrysococcyx minutillus
Little bronze cuckoo
5
0.06
2
0.02
2
0.02

Cisticolidae
Cisticola juncidis
Zitting cisticola
5
0.06
0
0
5
0.06

Accipitridae
Elanus caeruleus
Black-shoulder kite
4
0.05
0
0
0
0

Coraciidae
Eurystomus orientalis
Dollar bird
4
0.05
0
0
0
0

Ardeidae
Egretta alba
Great egret
4
0.05
0
0
0
0

Cuculidae
Centropus sinensis
Greater coucal
4
0.05
0
0
2
0.02

Ardeidae
Egretta garzetta
Little egret
4
0.05
0
0
0
0

Pachycephalidae
Pachycephala grisola
Mangrove whistler
4
0.05
0
0
1
0.01

Nectariniidae
Anthreptes simplex
Plain sunbird
4
0.05
0
0
0
0

Rallidae
Gallicrex cinerea
Water cock
4
0.05
1
0.01
3
0.03

Rallidae
Porzana pusilla
Baillon’s crake
3
0.03
11
0.13
0
0

Nectariniidae
Aethopyga saturata
Black-throated sunbird
3
0.03
0
0
0
0

Caprimulgidae
Caprimulgus affinis
Savanna nightjar
3
0.03
0
0
1
0.01

Muscicapidae
Muscicapa dauurica
Asian brown flycatcher
2
0.02
2
0.02
0
0

Alcedinidae
Alcedo atthis
Common kingfisher
2
0.02
1
0.01
0
0

Sturnidae
Gracula religiosa
Hill myna
2
0.02
0
0
0
0

Caprimulgidae
Caprimulgus macrurus
Large-tailed nightjar
2
0.02
0
0
1
0.01

Podicipedidae
Tachybaptus ruficollis
Little grebe
2
0.02
2
0.02
7
0.08

Laniidae
Lanius schach
Long-tailed shrike
2
0.02
1
0.01
0
0

Dicruridae
Dicrurus leucophaeus
Ashy drongo
1
0.01
0
0
0
0

Accipitridae
Aviceda leuphotes
Black baza
1
0.01
0
0
1
0.01

Phasianidae
Coturnix chinensis
Blue-breasted quail
1
0.01
0
0
2
0.02

Corvidae
Corvus splendens
House crow
1
0.01
0
0
3
0.03

Sylviidae
Phylloscopus inornatus
Inornate warbler
1
0.01
0
0
0
0

Nectariniidae
Arachnothera longirostra
Little spiderhunter
1
0.01
1
0.01
0
0

Jacanidae
Hydrophasianus chirurgus
Pheasant-tailed jacana
1
0.01
6
0.07
0
0

Sylviidae
Locustella certhiola
Rusty-rumped warbler
1
0.01
1
0.01
0
0

Picidae
Picumnus innominatus
Speckled piculet
1
0.01
0
0
0
0

Scolopacidae
Tringa. hypoleucos
Common sandpiper
0
0.01
2
0.02
0
0

Picidae
Celeus brachyurus
Rufous woodpecker
0
0.00
2
0.02
0
0

Columbidae
Treron curvirostra
Thick-billed green Pigeon
0
0.00
1
0.01
0
0

Nectariniidae
Nectarinia calcostetha
Copper-throated sunbird
0
0.00
1
0.01
0
0

Campephagidae
Pericrocotus divaricatus
Ashy minivet
0
0.00
0
0
3
0.03

Total
6086

1097

1545

3.2. Relative Abundance of Birds in Lotus Swamp Habitat

A total of 1,097 bird observations (12.6%) were recorded in Lotus Swamp. The birds belong to 57 species and 30 families. Pink-necked green Pigeon—Treron vernans (1.7%), yellow-vented bulbul—Pycnonotus goiavier and peaceful dove—Geopelia striata (1.2% each) were the three most common birds in the lotus swamp habitat. Whereas, 12 bird species, Richard’s Pipit—Anthus richardi, oriental reed warbler—Acrocephalus orientalis, olive-backed sunbird—Nectarinia jugularis, cotton pygmy goose—Nettapus coromandelianus, little green pigeon—Treron olax, barred button quail—Turnix suscitator, water cock—Gallicerx cinerea, common kingfisher—Alcedo atthis, long-tailed shrike—Lanius schach, little spiderhunter—Arachnothera longirostra, rusty-rumped warbler—Locustella certhiola, copper-throated sunbird—Nectarinia calcostetha and thick-billed green pigeon—Treron curvirostra, were the least common in lotus swamp habitat, recorded only once (0.01% each) (Table 1).

3.3. Relative Abundance of Birds in Open Water Body

In open water body habitat a total of 1,545 bird observations (17.7%) of all detections were recorded that belong to 55 bird species and 33 families. The results indicated that lesser whistling duck—Dendrocygna javanica (2.3%), blue-tailed bee-eater—Merops philippinus (1.6%) and yellow-vented bulbul—Pycnonotus goiavier (1.5%) were the three most dominant bird species. In contrast, eight bird species, Eurasian tree sparrow—Passer montanus, grey heron—Ardea cinerea, oriental reed warbler—Acrocephalus orientalis, Schrenck’s bittern—Ixobrychus eurhythmus, mangrove whistler—Pachycephala grisola, Savanna nightjar—Caprimulgus affinis, large-tailed nightjar—Caprimulgus macrurus, and black baza—Aviceda leuphotes, were the rarest birds, recorded only once (0.01% each) (Table 1).

3.4. Microclimate and Habitat Variables of Marsh Swamp

Microclimate data indicated that the marsh swamp had 28.1°C mean temperature (25–31°C), 95.3% mean relative humidity (89–97%), and mean 233.65 Lux light intensity (16–520 Lux). The habitat variables showed that marsh swamp area was covered by emergent vegetation (59.1%), submerged vegetation (13.6%), grasses (4.8%), and shrubs (3.7%), while 18.7% of the land was barren. In addition, 67 tree species were recorded along the lake edges in the marsh swamp area (Table 2).

Table 2: List of microclimate and microhabitat variables of marsh swamp, lotus swamp, and open water body at the Paya Indah Wetland Reserve, Peninsular Malaysia.

S. no
Variables
Mean value (range)

Marsh swamp
Lotus swamp
Open water body

1
Microclimate variables

(a)  Mean temperature (°C)
28.1°C (25–31°C)
27.50°C (26–30°C)
28.5°C (26.5–30°C)

(b)  Mean relative humidity (%)
95.3% (89–97%)
96.45% (94–97%)
95.5% (94–97%)

(c)  Mean light intensity (LUX)
233.65 (16–520 Lux)
260.60 (150–362 Lux)
438.16 (351–517 Lux)

2
Microhabitat variables

(A)  Vegetation cover percentage
81.3%
77.0%
76.7%

     (a)   Emergent vegetation (EMR)
59.1%
55.4%
30.8%

     (b) Submerged vegetation (SUB)
13.6%
15.4%
61.5%

     (c) Grasses (GRS)
4.8%
5.0%
4.5%

     (d) Shrubs (SHU)
3.7%
1.2%
3.2%

(B) Number of trees
67
17
6

     (i)  Diameter (cm)

     (a)  Diameter (<15 cm) (DA)
51
0
5

     (b) Diameter (16–30 cm) (DB)
12
15
1

     (c) Diameter (31–45 cm) (DC)
4
2
0

    (ii) Height (meter)

      (a) Height (<10 m) (HA)
50
13
3

      (b) Height (11–20 m) (HB)
16
4
1

      (c) Height (21–30 m) (HC)
1
0
2

3.5. Microclimate and Habitat Variables of Lotus Swamp

The lotus swamp had 27.5°C mean temperature (26–30°C), 96.4% mean relative humidity (94–97%), and mean 260.60 Lux light intensity (150–362 Lux). On the other hand, the habitat variables indicated that 77.0% of the lotus swamp habitat was covered with vegetation, that is, emergent vegetation (55.4%), submerged vegetation (15.4%), grasses (5.0%), and shrubs (1.2%). In addition, 23.0% of the area was bare land and walking paths. There were 17 tree species in the lotus swamp habitat (Table 2).

3.6. Microclimate and Microhabitat Variables of Open Water Body

Microclimate data indicated that the open water body habitat had 28.5°C mean temperature (26.5–30°C), 95.5% mean relative humidity (94–97%), and mean 438.16 Lux light intensity (351–517 Lux). Microhabitat variables showed 76.7% of the area was covered with vegetation, while the rest was dry land area including walking paths. Out of 76.7% of the total vegetated area, 61.5% was dominated by submerged vegetation, 30.8% by emergent vegetation, 4.5% by grasses, and 3.2% by shrubs. Besides, there were six tree species in open water body (Table 2).

3.7. Correlation of Birds, Microclimate, and Microhabitat in Marsh Swamp

The RDA ordination biplot diagram of marsh swamp habitat indicated that cotton pygmy geese and lesser whistling ducks had a strong association with the submerged vegetation. In addition, white-browed crakes, yellow bitterns, purple herons also showed a positive correlationship with the submerged vegetation. Schrenck’s bitterns, common moorhens, purple swamphens, black-headed munias and white-headed munias indicated strong positive association with the emergent vegetation, while oriental reed warblers, baya weavers, grey herons, yellow-bellied prinias and cinnamon bitterns showed a close association with the emergent vegetation and trees. Furthermore, rufous-tailed tailorbirds, plaintive cuckoos, blue-throated bee-eaters, lesser coucals, common flamebacks, brown-throated sunbirds and orange-breasted green pigeons showed a close relationship with the humid areas dominated by trees having the diameter of 16–30 cm and the height of <10 m. Oriental magpie robins, white-breasted waterhens, Richard’s pipits, red junglefowl, barred button quails, yellow-vented bulbuls and spotted doves indicated strong association with the grassy areas. Moreover, pink-necked green pigeons, jungle mynas, black-naped orioles, orange-breasted Green Pigeons and White-vented Mynas showed a strong relationship with the shrubs. Pintail Snipes, common ioras, pied trillers, common tailorbirds and pied fantails also showed a close relationship with light intensity, while blue-tailed bee-eaters, white-throated kingfishers, philippine glossy starlings, ashy tailorbirds, and green ioras indicated an association with the densely vegetated areas (Figure 2).

Figure 2: Ordination plot from a redundancy analysis of the distribution of birds of marsh swamp in relation to 14 environmental variables (for details see Table 2). The biplot of axes 1 and 2 is presented; the orientation of each variable in relation to each of these axes is presented by an arrow, the length of which indicates the degree of correlation with those axes.

3.8. Correlation of Birds, Microclimate, and Microhabitat in Lotus Swamp

The ordination biplot diagram of lotus swamp habitat showed that red-wattled lapwings and white-vented mynas had high relationship with temperature. Notably, blue-tailed bee-eaters, orange-breasted green pigeons, pacific swallows, plaintive cuckoos, yellow-bellied prinias and pink-necked green pigeons showed a strong association with the trees (having height 11–20 m), shrubs and also light intensity. In addition, common flamebacks, black-naped orioles, spotted doves and brown shrikes also showed a positive relationship with the shrubs and trees. Blue-throated bee-eaters, oriental magpie robins, eurasian tree sparrows, white-throated kingfishers and peaceful doves indicated a significant correlationship with the trees having the diameter <15 cm and the height <10 m. Pied fantails and yellow-vented bulbuls also had a strong relationship with relative humidity and vegetation cover greater than 75%. Additionally, white-breasted waterhens, white-browed crakes, purple swamphens and pheasant-tailed jacanas were highly correlated with the emergent vegetation. Red junglefowl, baya weavers, scaly-breasted munias, grey herons, and jungle mynas had a close relationship with the area dominated by grasses (Figure 3).

Figure 3: Ordination plot from a redundancy analysis of the distribution of birds of lotus swamp in relation to 14 environmental variables (for details see Table 2). The biplot of axes 1 and 2 is presented; the orientation of each variable in relation to each of these axes is presented by an arrow, the length of which indicates the degree of correlation with those axes.

3.9. Correlationship of Birds, Microclimate, and Microhabitat in Open Water Body

The RDA biplot diagram of the open water body habitat revealed that purple swamphens, purple herons, yellow bitterns, cinnamon bitterns and yellow-bellied prinias had a strong association with the emergent vegetated areas having cover of 25–50%. In addition, common moorhens and yellow-bellied prinias had an association with the emergent vegetation and grasses. Meanwhile, scaly-breasted munias, peaceful doves, oriental magpie robins, spotted doves, Richard’s pipits, lesser coucals, brown shrikes and common mynas were also highly related with the grasses. Cotton pygmy geese, little grebes and lesser whistling ducks indicated a close relationship with the submerged vegetation, light intensity and temperature. On the other hand, pied fantails, pink-necked green pigeons and yellow-vented bulbuls highlighted a strong association with the shrubs. Baya weavers, blue-tailed Bee-eaters, pied trillers, red junglefowl and green ioras showed a close link with the trees (having diameter of 16–30 cm and the height of 11–20 m), and the vegetation cover of 51–75%. Jungle mynas, large-billed crows, white-vented mynas, Philippine glossy starlings, and black-naped orioles indicated a strong association with the humid area dominated by trees having the diameter of <15 cm and the height of <10 m (Figure 4).

Figure 4: Ordination plot from a redundancy analysis of the distribution of birds of open water body in relation to 14 environmental variables (for details see Table 2). The biplot of axes 1 and 2 is presented; the orientation of each variable in relation to each of these axes is presented by an arrow, the length of which indicates the degree of correlation with those axes.

4. Discussions

It is necessary to integrate spatial distribution with species characteristics in the analysis of factors responsible for distribution of bird species in wetlands. About 40% of the lakes at the Paya Indah Wetland Reserve are open water bodies, dominated by submerged and floating vegetation such as pond weeds (Potamogeton sp.), water milfoils (Myriophyllum sp.), bladderworts (Utricularia sp.), rushes (Scirpus sp), coontails (Ceratophyllum sp.), and waterweeds or hydrillas (Hydrilla sp.). Water level changed from time to time mainly depending on the rainfall pattern. The ratio between the emergent vegetation and open water (40 : 60) was also the key factor that influenced the distribution of waterbirds in the wetland area. About 60% of the water bodies were densely covered by emergent vegetation, such as water chestnuts, marsh sedges, water lilies, water-milfoils, bulrushes and phragmites. The emergent vegetation was an important habitat for the swamphens, moorhens, crakes, herons, and bitterns. These waterbird species used the emergent vegetation for different purposes, such as hunting, perching, and escape cover.

Previously, several studies have demonstrated an association between bird species distribution and wetland habitats [40, 41]. Recently, attention has been given on habitat interaction especially to examine the difference in habitat use among the coexisting species [42–44]. In this study, the results obtained using the canonical correspondence analysis highlighted that the plant species (e.g., emergent vegetation, submerged vegetation, grasses, shrubs, and trees composition), vegetation structures (e.g., diameter and height), and climatic variables (e.g., temperature, relative humidity, and light intensity) were the main factors that influenced the distribution of waterbirds and terrestrial birds in the wetland reserve. The results also indicated that each species had adapted a fairly unique set of microhabitat and microclimate conditions. For instance, the lesser whistling ducks used the water body habitat dominated by submerged vegetation for foraging and loafing on dead trees and reed beds of the emergent vegetation along the edges. They preferred to forage in the morning, and, when the temperature rose, their activity turned to loafing. Similarly, the purple swamphens preferred to use the marsh swamp habitat dominated by emergent vegetation. This revealed that the microhabitat and microclimate selection might vary from species to species.

The results further showed that the waterbirds, for instance, the ducks, geese, and grebes, had a strong correlationship with the submerged vegetation, temperature, and light intensity. This might be due to greater abundance and higher diversity of macroinvertebrates and fish. The macro-invertebrates of the Paya Indah Wetland Reserve consisted of snails, arachnids, insect larvae, and crustaceans. The higher abundance and richness of macro-invertebrates and fish occurred in the submerged vegetation [45–47]. Apparently, relative abundance of ducks and geese was strongly related to the domination of submerged vegetation in open water bodies, and they preferred to forage in submerged vegetation for food items [48–51]. The submerged vegetation supported the complex trophic structure in the wetland [52], and it was an important source of food for invertebrates such as insects, isopods, decapods, crustaceans, and molluscs, as well as fish and birds [53–55].

Anatidae avoided the dense emergent vegetation and preferred submerged vegetation instead because this vegetative cover potentially restricted the movement and foraging efficiency of the birds in the study area. Such types of finding also have been reported by Van Rees-Siewert and Dinsmore [56], King and Wrubleski [57] and Benoit and Askins [58]. Dense vegetation might interfere with the movement and foraging efficiency of the waterbirds. The swamphens, bitterns, moorhens, jacanas, herons, crakes, warblers, prinias and munias showed a positive association with the emergent vegetation in the wetland area. This might be due to diverse food resources occuring in emergent vegetation (e.g., amphibians, fish, and aquatic invertebrates, such as snails, insects larvae, crustaceans, and aquatic annelids), refuge from predators and potential nursery sites for their chicks. The vegetation with moderate to low structure offered suitable foraging opportunities particularly for the herons, bitterns, swamphens, and crakes in the study area. This might also be due assigned to the richness and abundance of aquatic invertebrates, amphibians, and fish in the emergent vegetation.

Additionally, the swamphens, moorhens, and crakes were observed using the dense stands of emergent vegetation [59, 60]. This was because the dense emergent vegetation provided a hiding cover from predator’s visual detection [61]. Apparently, the herons, bitterns, and egrets also selected the emergent vegetation with shallow water for their foraging activity [62]. Needless to say, herons and egrets have long bills and stalks that enable them to submerge for prey while wading in shallow water [63] and capturing their prey by doing a direct head movement [64, 65].

The results showed that the terrestrial birds, such as the minivets, tailorbirds, kites, bee-eaters, and crows, were strongly associated with the trees in the study area. This might be due to the trees that attracted diverse insects and provided suitable foraging surfaces, shelters, and nesting sites for the bird species. Moreover, the weavers, munias, cuckoos, coucals, lapwings, snipes, and waterhens showed a positive correlationship with the emergent vegetation, grasses, relative humidity, temperature, and ground vegetation cover. The grasses provided a variety of flowers and seeds that attracted the insects, whereby the seeds and insects were the main sources of energy for these bird species.

The bee-eaters, fantails, dollar birds, mynas, sparrows, kingfishers, orioles, pigeons, starlings, bulbuls, and trillers indicated a strong relationship with the shrubs, trees, relative humidity, light intensity, and ground vegetation cover in the wetland reserve. The reason was that these birds preferred different microhabitats like the marsh swamp, lotus swamp, open water body, dryland and patches of shrubs, and microclimate, such as the temperature, humidity, and light intensity. The shrubs and trees provided a diversity of flowers and fruits that attracted a wide array of insects. The berries and insects were the main food resources for these birds. In addition, the shrubs and trees provided hiding covers from predators and inclement weather and suitable nesting sites for them.

The robins, doves, junglefowl, coucals, pipits, munias, shrikes, quails, and mynas indicated a strong association with the grasses, shrubs, trees, relative humidity, light intensity, and ground vegetation. The variety of vegetation [66], vertical zonation of shrubs and tree vegetation [67], structural characteristics of vegetation such as diameter and height, distribution of trees [68], food, and nutrients [69], and amount of ground cover [70] were identified as important factors that directly and indirectly influenced the occurrence and distribution of the birds in the wetland reserve.

The vegetation structure and floristic composition were the key factors that affected the habitat selection of the birds and indicated where and how the birds used the resources [71, 72]. Microclimatic factors such as the temperature, rainfall, relative humidity, and microhabitat factors, for instance, vegetation cover, had played important roles in the distribution of prey and bird species in the wetland ecosystem [73, 74]. The light intensity and temperature affects on foraging behaviour, species dispersal and habitat selection, reproduction, and timing of breeding season of avian species. Birds may respond directly to microclimate changes or indirectly to changes in food or cover resulting from microclimate changes [75]. Karr and Freemark [76] suggested the importance of microclimate as a factor in determining avian “physiological comfort.” Extremes in microclimate may have adverse effects on birds and their reproductive fitness [77–79]. Feeding in open areas where the incoming solar radiation and air temperature are greater than the adjacent vegetated area [80] energetically reduces foraging costs [81]. In addition, other factors such as the weather (rainfall), social interactions [82, 83], and predators also played important roles in the distribution and habitat use of the wetland birds in the study area [28, 84, 85].

Overall, the results of the constrained redundancy ordination analysis indicated that the relationship between the birds and habitats was shaped by microhabitat factors such as ground cover (i.e., the proportion of soil covered with vegetation), plant species richness (i.e., the number of plant species), vegetation type (i.e., trees, shrubs, grasses, emerged and submerged vegetation, sedges, reeds, ferns, and herbs), vegetation structure (i.e., vegetation height and diameter), and microclimate factors (i.e., temperature, humidity, and light intensity). These factors influenced on the distribution, diversity and density, of avian species in the study area.

Besides, other factors, for instance, water quality, such as the water of the some part of lakes was too blackish colour; no bird was observed to use that area. In contrast, nearby other lake having clear water with bluish colour many birds were observed to utilize that area and food resources such as fruiting trees, that is, Ficus, Syzygium, Fragraea, Glabra, and Cinnamons. During fruiting season, these trees abundantly preferred by fruit-eating birds such as bulbuls, starlings, pigeons, and orioles. In addition, such purple swamphen fly from edge to deep water to pluck sink fruit of water lily and bring it to dry place to eat and shelters from harsh weather conditions and predators for example, due to emergence of western marsh harrier, and also during raining bittern, moorhens, and swamphen hided into reed beds and pigeons and doves fly away from foraging sites to dense shrubs and trees to get shelter. These sightings showed that water quality, food resources, and shelter played major roles in the distribution of birds in the study area.

5. Conclusion

Marsh swamp was heavily used by wetland bird species (69.7%) as compared to open water body and lotus swamp. Results revealed that wetland bird species have adapted a fairly unique set of microhabitat characteristics such as vegetation composition and vegetation structures, and microclimate variables are key factors that influenced the species abundance, distribution, and diversity.

Appendices

A.

See Table 3.

Table 3: List of vegetation recorded at the Paya Indah Wetland Reserve, Peninsular Malaysia.

Family  name
Scientific  name
Local  name

Tree Species

Anacardiaceae
Mangifera indica
Mangga

Annonaceae
Cananga odorata
Kenanga

Apocynaceae
Alstonia scholaris
Pohon

Dyera costulata
Jelutong

Araliaceae
Schefflera heterophylla

Arecaceae
Cocos nucifera
Coconut tree

Elaeis guineensis
Oil Palm

Casuarinaceae
Casuarina equisetifolia
Rhu

Clusiaceae
Cratoxylum maingayi
Geronggang

Mesua elegans
Penaga

Clusia rosea
Pitch apple

Combretaceae
Terminalia muelleri
Jelawai

Dipterocarpaceae
Shorea materialis
Meranti temak

Shorea sumatrana
Balav sengkawang air

Shorea ochrohloia
Seraya Batu

Ebenaceae
Diospyros argentea
Bedil lalat

Elaeocarpaceae
Elaecocarpus floribundus
Mendung

Elaeocarpus nitidus
Mendung

Euphorbiaceae
Macaranga tanarius
Blush

Mallotus paniculatus
Balik angin

Pimelodendron griffithianum
Perahikan

Fabaceae
Delonix regia
Semarak api

Lauraceae
Cinnamomum iners
Medang teja

Lecythidaceae
Barringtonia edulis
Putat

Leguminosae
Acacia auriculiformis
Acacia

Cassia javanica
Pink shower

Cassia fistula
Amaltas

Acacia mangium
Acacia

Albizia julibrissin
Batai

Saraca cauliflora
Gapis

Sindora wallichii
Spetir daun tebal

Cynometra malaccensis
Kekatong

Tamarindus indica
Asam jawa

Flemingia macrophylla
Serengan jantan

Loganiaceae
Fragraea fragrans
Tembusu

Lythraceae
Lagerstroemia speciosa
Bungor

Malvaceae
Sterculia foetida
Kelumpang jari

Meliaceae
Azadirachta excelsa
Sentang

Moraceae
Artocarpus maingayi
Pudu

Ficus benjamina
Ara

Ficus fistulosa
Ara

Streblus elongatus
Tempinis

Artocarpus lanceifolius
Keledang

Ficus maclellandii
Ara

Ficus rubiginosa
Ara

Myrtaceae
Syzygium linocieroides
Kelat

Syzygium campanulatum
Kelat

Syzygium hanfii
Kelat

Syzygium lineatum
Kelat

Melaleuca cajuputi
Kayu putih (gelam)

Syzygium grande
Kelat jambu laut

Syzygium polyanthum
Kelat

Syzygium jambos
Kelat jambu

Syzygium microcalyx
Kelat

Rutaceae
Melicope glabra
Pepauh

Sapindaceae
Filicium decipiens
Japanese fern leaf tree

Mimusops elengi
Bunga tanjung

Payena lucida
Nyatoh

Simaroubaceae
Ailanthus excelsa
Marakuh

Sterculiaceae
Pteroygota alata
Kasah

Streculia lanceolata
Kalumpang

Heritiera javanica
Mengkulang jari

Firmiana malayana
Mata lembu

Sterculia macrophylla
Kelompang

Thymelaeaceae
Gonystylus banacanus
Ramin melawis

Shrub species

Melastomataceae
Melastoma malabathrcium

Dilleniaceae
Dillenia suffruticosa

Emergent vegetation

Cyperaceae
Eleocharis dulcis
Water chestnut

Nymphaeaceae
Nelumbo nucifera
Indian or bean or lotus

Nelumbo pubescens
Water lily

Nymphaea rubra
Rubra water lily

Philydraceae
Philydrum lanuginosum
Wooly water lily

Grass Species

Cyperaceae
Scirpus olneyi
Three square bulrush

Gramineae
Imperata cylindrica
Cogon grass

Distichlis spicata
Spike grass

Poaceae
Cynodon dactylon
Carpet grass

Panicum maximum
Buffalo grass

Sedge Species

Cyperaceae
Scleria purpurascens
Marsh sedge/nut rush

Poaceae
Spartina alterniflora
Rush

Fern and Moss Species

Blechnaceae
Stenochlaena palustris
Climbing fern

Thelypteridaceae
Cyclosorus interruptus
Fern

Lycopodiaceae
Lycopodium cernuum
Creeping club moss

Salviniaceae
Salvinia molesta
Giant or kariba weed

Gleicheniaceae.
Gleichenia linearis
Fern tree

Reed Species

Philydraceae
Phragmites karka
Phragmites

Typhaceae
Typha angustifolia
Cattail

B.

(a) Microclimate VariablesTem: temperature, RH: relative humidity, LUX: light intensity.

(b) Microhabitat VariablesCB: ground vegetation cover 26–50%, CC: ground vegetation cover 51–75%, CD: ground vegetation cover 75–100%, SUB: submerged vegetation, EMR: emergent vegetation, GRA: grasses, SHU: shrubs, DA: tree diameter <15 cm, DB: tree diameter 16–30 cm, DC: tree diameter 31–45 cm, HA: tree height <10 m, HB: tree height 11–20 m, HC: tree height 21–30 m.

(c) Bird SpeciesAsh Tai: ashy tailorbird, Bar But: barred button quail, Bay Wea: baya weaver, Bla Cro: black-crowned nightheron, Bla HeM: black-headed munia, Bla Nap: black-naped oriole, Blu TaB: blue-tailed bee-eater, Blu ThB: blue-throated bee-eater, Brh Kit: brahminy kite, Bro Shr: brown shrike, Bro ThS: brown-throated sunbird, Che WiC: chestnut winged cuckoo, Cin Bit: cinnamon bittern, Com Flm: common flameback, Com Ior: common iora, Com Moo: common moorhen, Com Myn: common myna, Com TaB: common tailorbird, Cot PyG: cotton pygmy goose, Dol Bir: dollar bird, Eur AsT: eurasian tree sparrow, Gre Egr: great egret, Gre Cou: greater coucal, Gre Ior: green iora, Gre Her: grey heron, Jun Myn: jungle myna, Lar BiC: large-billed crow, Les Cou: lesser coucal, Les WhD: lesser whistling duck, Lit BrC: little bronze cuckoo, Lit GrP: little green pigeon, Lit Her: little heron, Oli BaS: olive-backed sunbird, Oli WiB: olive-wined bulbul, Ora BrP: orange-breasted green pigeon, Ori Mag: oriental magpie robin, Ori ReW: oriental reed warbler, Pac Swa: pacific swallow, Pea Dov: peaceful dove, Phi GlS: Philippine glossy starling, Pie Fan: pied fantail, Pie Tri: pied triller, Pin GrP: pink-necked green pigeon, Pin Sni: pintail snipe, Pla Cuc: plaintive cuckoo, Pur Her: purple heron, Pur SwH: purple swamphen, Red JuF: red junglefowl, Red WaL: red-wattled lapwing, Ric Pip: Richard’s pipit, Ruf TaT: rufous-tailed tailorbird, Sav NiJ: savanna nightjar, Sca BrM: scaly-breasted munia, Sch Bit: Schrenck’s bittern, Spo Dov: spotted dove, Wat Coc: water cock, Whi BrW: white-breasted waterhen, Whi BrC: white-browed crake, Whi HeM: white-headed munia, Whi ThK: white-throated kingfisher, Whi VeM: white-vented myna, Yel Bit: yellow bittern, Yel BeP: yellow-bellied prinia, Yel VeB: yellow-vented bulbul, Zit Cis: zitting cisticola.

Authors’ Contribution

M. N. Rajpar developed the experimental design, conducted research, collected and analyzed data, and drafted paper. M. Zakaria Guided, reviewed and edited the paper.

Acknowledgments

Authors would like to thank the Department of Wildlife and National Parks, Peninsular Malaysia, for allowing us to conduct this study. This research was partially funded by the Fundamental Grant Research Scheme  01-10-07-291FR and Forestry Sector Research and Development Project, Pakistan, Forest Institute, Peshawar, Pakistan.

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