Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 September 2022 | 14(9): 21818–21825
ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.7650.14.9.21818-21825
#7650 | Received 07 September 2021 | Final received 01 August
2022 | Finally accepted 03 September 2022
Foraging
strata and dietary preferences of fifteen species of babblers in Sarawak,
Malaysia
Jayasilan Mohd-Azlan 1 , Attiqqah Fadziliah Sapian 2 ,
Andrew Alek Tuen 3 & Chong Leong Puan
4
1,3
Institute of Biodiversity and Environmental
Conservation, Universiti Malaysia Sarawak, 94300 Kota
Samarahan, Sarawak, Malaysia.
2
Animal Resources Science and Management, Faculty of
Resource Science and Technology, Universiti Malaysia
Sarawak,
94300
Kota Samarahan, Sarawak, Malaysia.
4
Faculty of Forestry and Environment, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor,
Malaysia.
4
Institute of Tropical Forestry and Forest Products
(INTROP), Universiti Putra Malaysia, 43400 UPM
Serdang, Selangor, Malaysia.
1 azlan@unimas.my (corresponding author), 2 attiqqahfadz@gmail.com, 3 aatuen@unimas.my, 4 chongleong@upm.edu.my
Abstract:
Babblers are the primary insectivorous birds of the
tropical forests in southeastern Asia which have
shown to be affected by forest disturbance. Their high diversity, microhabitat
specificity and specialised feeding guilds provide a good opportunity for ecological
research pertaining to niche segregation. We examined the diet and foraging
strata of 15 sympatric babbler species mist-netted in nine forests in Sarawak,
eastern Malaysia. Based on 222 birds captured from December 2014 to March 2016,
a segregation in foraging strata was found, with half of the species captured
frequenting low strata, while only three were found at mid strata and four at
high strata. Both species richness and abundance were found to decrease when
the foraging height increased. From a total of 136 prey items retrieved from
regurgitated and faecal samples of 13 babbler species, we found that Coleoptera
(41.5%), Hymenoptera (36.2%), and Araneae (12.3%) formed the major diet of the
birds. Diet overlaps among the babblers were relatively low. Our study
demonstrated the possible presence of spatial and trophic niche segregation
among babblers, and justified their ecological role as indicators of tropical
forest ecosystem health, especially in the case of specialists, that deserve
further conservation attention.
Keywords: Forest fragmentation, forest health indicator, forest specialist,
insectivorous birds, niche differentiation.
Editor:
Anonymity requested. Date of
publication: 26 September 2022 (online & print)
Citation:
Mohd-Azlan, J., A.F. Sapian,
A.A.Tuen & C.L. Puan (2022).
Foraging strata and dietary preferences of fifteen species of babblers
in Sarawak, Malaysia. Journal of Threatened Taxa 14(9): 21818–21825.
https://doi.org/10.11609/jott.7650.14.9.21818-21825
Copyright:
© Mohd-Azlan et al. 2022.
Creative Commons Attribution 4.0 International License. JoTT allows
unrestricted use, reproduction, and distribution of this article in any medium
by providing adequate credit to the author(s) and the source of publication.
Funding: Ministry of Higher Education
Malaysia, Fundamental Research Grant Scheme (FRGS/1/2020/WAB11/UNIMAS/02/3); Sarawak
Energy Berhad (GL(I01)/SEB/2014/01(02).
Competing interests: The authors
declare no competing interests.
Author details: Jayasilan Mohd-Azlan is with
the Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak. He studies species of
conservation importance and their ecology in Borneo. Attiqqah Fadziliah Sapian completed
her postgraduate study at the Faculty of Resource Science and Technology, Universiti Malaysia Sarawak and had been involved in bird
surveys in Sarawak. Andrew Alek Tuen
is currently an Honorary Research Associate of the Institute of Biodiversity
and Environmental Conservation, Universiti Malaysia
Sarawak and his expertise is in animal nutrition and ecology. Chong
Leong Puan is currently an Associate Professor at the Faculty of
Forestry and Environment, Universiti Putra Malaysia.
His research covers the behaviour, habitat requirements,
ecological interactions and population genetics of Malaysian birds.
Author contributions: AAT
initiated the project and AFS carried out the fieldwork which was co-supervised
by JMA. AFS analysed the data and wrote the masnucript with input from JMA, AAT and CLP.
Acknowledgements: We would
like to thank Ministry of Higher Education Malaysia, Fundamental Research Grant
Scheme (FRGS/1/2020/WAB11/UNIMAS/02/3), Institute of Biodiversity and
Environmental Conservation, Universiti Malaysia
Sarawak, Sarawak Forestry Corporation and Forest Department Sarawak (Permit no
NCCD.907.4.4 (Jld.11) – 52). This study was conducted under the approval of the
UNIMAS Animal Ethics Committee, Universiti Malaysia
Sarawak (UNIMAS/AEC/R/F07/006) with the support from Sarawak Energy Berhad (GL(I01)/SEB/2014/01(02)). We would like to thank
the following people who had helped in the field: Rahah
Mohamad Yakup, Mohd Hasri Al Hafiz Haba, Isa Sait, Trevor Allen Nyaseng, and
Samuel Lihan.
INTRODUCTION
Bird communities in the tropics can be good systems to
investigate complex interactions among sympatric species (Mansor
& Mohd Sah 2012; Styring
et al. 2016; Mansor & Ramli 2017; Sherry et al.
2020). How communities are structured are dependent on how they partition their
resources and differentiate niches. Understanding how sympatric species utilise
their resources can provide evidence about the coexistence of potential
competitors (Morin 1999). Coexisting species in a community separate their
ecological needs by resource partitioning along temporal, spatial, and
behavioural niches (Mohd-Azlan et al. 2014). In
general, when resources are a limiting factor, competitive interactions between
species can result in non-random pattern of resource use (Morin 1999). Some
studies on closely related species have shown that birds partition food
resources by utilising different vertical strata, or by differential use of
microhabitats (Styring & Hussin
2004; Mohd-Azlan et al. 2014).
Insectivorous birds consume a substantial amount of arthropods, hence their ecological importance in
many ecosystems is significant (Nyffeler et al.
2018). Many studies have demonstrated the effects of forest disturbance on
insectivorous birds, which may be linked to the decline of insect communities
particularly certain insect groups (Didham et al.
1996; Didham 1997; Şekercioğlu
et al. 2002; Stratford & Stouffer 2015; Bowler et al. 2019). In the
tropics, understory insectivores are characterized by high habitat specificity
and lower mobility relative to other passerines (Şekercioğlu
et al. 2002; Yong 2009). Thus birds of the understory
strata are sensitive to forest disturbance (Thiollay
1992; Kattan et al. 1994; Stouffer & Bierregaard 1995; Canaday 1996;
Stratford & Stouffer 1999) and they have adapted to occupy specialized
niches when foraging for their insect prey (Sekercloğlu
et al. 2002). For instance, small forest fragments have been shown to
experience a decline in the number of invertebrates dwelling among the leaf
litter and soil while increasing the generalist numbers at the forest edge (Didham et al. 1996; Didham et al.
1997). These changes can affect understorey insectivores that avoid relatively
open or edge habitats and specialise on arthropod prey that hide within leaf
litter and soil (Canaday 1996).
With the increasing reports on the effects of forest
disturbance on arthropods in the tropics (Hamer et al. 1997; Chey et al. 1998;
Holloway 1998; Lawton et al. 1998; Schowalter & Ganio 1999; Floren & Linsenmair 2001, 2003; Hartshorn et al. 2021), concerns
over the associated effects on insectivorous birds are also raised. Equally,
there is a need for more in-depth study on the foraging ecology of the tropical
insectivorous birds in the tropics so as to determine which species are particularly
affected by or resilient to forest disturbance.
In southeastern Asia,
babblers primarily refer to two insectivorous families, namely Timaliidae (54 extant species) and Pellornidae
(64 species), the majority of which rely on forest or wooded habitats. As many
babbler species are sedentary, with poor ability to disperse across non-forest
habitat (Yong 2009), and are associated especially to lower forest strata of
forest interior, they serve as suitable indicators of the level of forest
disturbance (Lambert & Collar 2002; Hamer et al. 2015). Past studies based
on relative abundance have shown that certain babbler species (Hussin & Francis 2001; Lambert & Collar 2002;
Moradi & Mohamed 2010) and even specific feeding guilds (Johns 1986; Yong
et al. 2011) are sensitive to forest fragmentation.
In the tropical forests of Malaysia, babblers form a
major portion of the diverse middle and understorey avian insectivores (38
species; Puan et al. 2020), with high numbers of congeneric and sympatric
species (Lambert & Collar 2002). This makes them suitable candidates for
the research on avian community ecology including trophic diversification,
resource partitioning and functional morphology, all of which are essential in
driving the associated biotic community assembly in the tropical forests. Such
research is feasible by examining their diets, which comprises of indigestible
exoskeletons of arthropods, as demonstrated in studies elsewhere on food
partitioning (Kent & Sherry 2020; Sherry et al. 2020), seasonal dietary
patterns in relation to changes in the environment (Poulin et al. 1992) or
abundance of resources (Yard et al. 2004). In central Peninsular Malaysia, Mansor et al. (2018) found little dietary overlaps among 12
babbler species. Despite most being morphologically similar (Styring et al. 2016; Mansor &
Ramli 2017; Puan et al. 2018), niche differentiation with respect to foraging
tactics have been demonstrated based on opportunistic visual observations on
the Malaysian babbler species (Mansor & Mohd Sah 2012; Mansor et al.
2015; Styring et al. 2016; Mansor
& Ramli 2017). Owing to their diversity and specialised feeding guilds of
being terrestrial, foliage and/or bark gleaning insectivores (Johns 1986; Mitra
& Sheldon 1993; Yong et al. 2011), this study examined niche segregation,
i.e., diet and foraging strata, of 15 sympatric babbler species found in
Sarawak, Borneo.
MATERIALS
AND METHODS
Study
sites
A total of nine sampling sites were chosen in Sarawak,
eastern Malaysia, which can be grouped according to Pelagus
(three sites), Ulu Baleh (three sites), and Baram (three sites) (Figure 1). Pelagus
is located about 33 km from the Kapit town and the
three sampling sites were Nanga Benin (2.165°N, 113.074°E), Nanga Pelagus (2.171°N, 113.055°E) and Nanga Peraran
(2.193°N, 113.118°E) located along Batang Rajang
River. Ulu Baleh is located along the Baleh River which is about 176 km from Kapit
town. The three sampling sites were Nanga Gaat
(1.645°N, 113.133°E), Putai (1.595°N, 113.791°E) and
Long Singut (1.560°N, 114.202°E). Baram is located
about 120 km from the Miri city. The
three sampling sites were Long San (3.293°N, 114.779°E), Selunggo
(3.208°N, 115.185°E) and Lio Mato (3.174°N, 3.174°E).
Except the Pelagus National Park, all sampling sites
comprised logged over secondary forests located
close to human settlements and some agriculture lands.
Bird
sampling
From December 2014 to March 2016, three double-stacked
mist-nets (measuring 9 × 4 m each) were deployed from 0600–1830 h for four
consecutive days at each of the two sampling stations at each site. The
distance of the two stations was 100–1000 m away from human settlement areas,
so as to assess the effects of anthropogenic disturbance on birds in another
study (Mohd-Azlan et al. unpubl.
data). The double-stacked nets were set vertically to create six shelves
representing foraging strata based on the distance from the forest floor, i.e. Shelves 1 and 2 were categorized as low strata (0–1.2 m
from the forest floor), Shelves 3 and 4 as mid strata (1.3–2.4 m) and Shelves 5
and 6 as high strata (2.5–3.6 m). All birds caught were weighed, measured and
had the capture shelve numbers recorded.
Diet
analysis
All babbler species, except juveniles and birds caught
during the first hour of the sampling (Lopes et al. 2005), were administered
with tartar emetic (Poulin & Lefebvre 1995; Zduniak
2005) before being released immediately. Depending on body weight and species,
careful administration of acceptable concentration of tartar emetic solution (Sing-Tyan
et al. 2017) will extract stomach contents via regurgitation. For every 100 g
of the body mass, a dosage of 0.8 ml of 1.2% potassium antimony tartrate was
used (Durães & Marini 2003). The regurgitated
items and faeces were preserved using 70% alcohol in the field before being
examined under a compound microscope in the laboratory. All prey items were
identified up to taxonomic order and each order found in an individual sample
was counted as one prey item.
Data
analysis
Analysis of bipartite ecological webs (Dormann et al. 2017) was performed to visualize and
calculate indices representing the pattern of ecological networks among prey
and predators. Berger-Parker dominance index was also calculated to determine
whether babblers are specialized in food choice or polyphagous. Species
diversity and evenness were assessed using Shannon (H’) and Pielou’s
(J) evenness indices (Oksanen et al. 2013), respectively, whereas overlaps of
prey items among babbler species were assessed using Pianka
index (EcoSimR package; Gotelli
& Ellison 2013). The outputs of prey item overlap analysis are a histogram
of which its skewness represents the degree of overlap, i.e., left-skewed indicating
a low overlap in the diet and right-skewed if otherwise. This is followed by
two graphical plots with circles indicating the observed and simulated diet
segregation pattern, i.e., a circle represents the relative consumption of prey
category and its size is proportional to the level of such consumption. In
other words, if there is no overlap of prey items among the babbler species, no
circle will be present. Analyses were performed using R version 3.3.1 (R Core
Team 2016).
RESULTS
AND DISCUSSION
Species
diversity and foraging strata
Over 4,800 net-hours, a total of 222 individuals
representing 15 babbler species (nine from Pellorneidae
and six from Timaliidae) were caught during this
study (Table 1). This represents more than 50% of the babblers recorded in
Sarawak. The Black-throated Babbler (Stachyris
nigricollis, n = 32) was the most common species
caught for all sites, followed by Short-tailed Babbler (Trichastoma
malaccense, n = 25). The most common abundant
species recorded for each site was White-chested Babbler (Trichastoma
rostratum, n = 11) in Pelagus,
Rufous-crowned Babbler (Malacopteron magnum,
n = 18) in Ulu Baleh and Chestnut-winged Babbler
(Stachyris erythroptera,
n = 12) in Baram. Based on the Shannon diversity
index, Ulu Baleh had the highest species diversity (H’
= 2.314), followed by Baram (H’ = 2.238) and Pelagus (H’ = 2.193). The distribution of
individuals among species was more even in Ulu Baleh
and Baram compared to Pelagus
(Table 1).
The babblers showed a segregation in foraging strata,
with half of the species captured frequenting low strata while only three were
at mid strata and four at high strata. Both, species richness and abundance
were found to decrease when the foraging height increased. All species were
found foraging mostly at a height of less than two meters, while others such as
the Babbler Fluffy-backed Tit-babbler, Ferruginous, Scaly-crowned, Chestnut-rumped, Black-throated, Grey-hooded Babblers only
occasionally go higher (2.5–3.6 m), whereas the Black-capped Babbler is
strictly below one meter. This implies some form of niche segregation among the
sympatric babbler species. It should be noted that the foraging height recorded
in this study was solely based on the vertical capture location of
double-stacked mist-nets, which may not entirely represent the foraging height.
It also covered flying height of the babblers.
Diet
composition
A total of 136 prey items were retrieved from
regurgitated and faecal samples of 13 babbler species which comprised eight
insect orders, plus one arachnid and one gastropod. Of those identifiable prey
items, Coleoptera (41.5%), Hymenoptera (36.2%), and Araneae (12.3%) formed the
major diet of babblers (Table 2). Based on analysis of bipartite ecological
webs (Figure 2), Sooty-capped and Black-capped Babblers are specialists that
feed solely on Coleoptera. Among all the babbler species, Fluffy-backed
Tit-babbler seems to have the most generalized diet, covering seven insect
orders. With respect to diet overlap analysis (Figure 3), the histogram was
skewed to the left indicating that the diet overlap among the 13 babbler
species was low. The prey items that heavily overlapped were from Categories 1
(for Araneae), 2 (Caterpillar), and 3 (Cicaedae). On
the other hand, prey items that did not overlapped were from Categories 6
(Diptera), 9 (Hymenoptera), 10 (Orthoptera), and 11 (Phasmidae).
Being terrestrial, foliage and/or bark gleaning
insectivores, the major prey groups of the babblers comprises of relatively more
terrestrial (i.e., Coleoptera, Hymenopter,a and
Araneae of understory level, similar to Mansor et al.
(2018), except Blattodea) rather than aerial
arthropods (but see Mansor et al. 2021). The
abundance of Hymenoptera such as ants and Araneae (spiders) on the forest floor
(Griffiths et al. 2018; Hartshorn et al. 2021) as well as those in the aerial
leaf litter (Mansor et al. 2019) might be a reason
that they formed a major portion of the babblers’ diet. With respect to
nutritional composition, Coleoptera and Araneae were found to contain higher
portions of crude protein and lipids than Hymenoptera (Razeng
& Watson 2015). Both protein and lipids (e.g., fats) are crucial for bird
growth (Klasing 2000). Diet overlaps among babblers
in this study were relatively low, consistent with reports from central
Peninsular Malaysia (Mansor et al. 2018, 2021). The
differences noted in foraging tactics might be one of the factors influencing
the diet of the babbler species and vice versa. In addition, low diet overlaps
of these birds could also be due to potential shifts in foraging behaviour when
joining heterospecific feeding flocks (Mansor et al.
2020), which awaits further investigation in the case of Bornean babblers.
CONCLUSION
In the tropics where species diversity is high,
resource partitioning and niche differentiation are essential evolutionary
adaptions that lead to character displacement and reduce the competition among
sympatric species (Wiens 1989). The use of different forest strata, either
vertically or horizontally, and food resources by birds are common ecological
strategies to reduce interspecific competition. Our study demonstrated the
possible presence of spatial and trophic niche segregation among 15 babbler
species in eastern Malaysia, some of which are likely to be specialists while
others are generalists. Similar to other more localised studies conducted in
Malaysia, our study supported that different foraging tactics (Mansor & Mohd Sah 2012; Mansor et al. 2015, 2018; Styring
et al. 2016; Mansor & Ramli 2017), foraging area
and prey preference may have contributed to the difference in the diet of
babblers (both Timaliidae and Pellornidae).
Furthermore, prey size and type preference of the babblers in the Malaysian
forests is believed to be influenced by predation and anti-predation strategies
(Sherry et al. 2020) as well as possibly nutritional composition of the prey
which deserve further investigation.
Having a feeding guild that is more terrestrial,
foliage and/or bark gleaning in nature at the understory strata may render
babblers, particularly those with specific spatial and trophic niches,
exceptionally sensitive to habitat disturbance and fragmentation (Zakaria &
Nordin 1998; Yong 2009). This implies that protection
of this bird group, among others, is essential when forest management practices
are being made. Their ecological role as indicators of forest ecosystem health
(Lambert & Collar 2002; Hamer et al. 2015) is supported by our findings. It
is also worth mentioning that two Near Threatened babbler species, i.e.,
White-necked Babbler (Stachyris leucotis, a rare slope specialist) and Grey-breasted
Babbler (Malacopteron albogulare,
an uncommon peat-swamp and heath forest specialist; Yong et al. 2014) are also
found on Borneo, although not recorded in our study. Both species deserve more research and
protective measures pertaining to their ecological requirements, trophic and
spatial niches.
Table 1.
Species and number of individuals of babblers caught in Pelagus,
Ulu Baleh, and Baram.
|
Common
name |
Species
name |
Study
sites |
Foraging
strata |
||||
|
Pelagus |
Ulu
Baleh |
Baram |
Understorey |
Mid-storey |
Sub-canopy |
||
|
Pellorneidae |
|
|
|
|
|
|
|
|
Rufous-crowned
Babbler |
Malacopteron magnum |
3 |
18 |
0 |
11 |
10 |
0 |
|
Salvadori’s
Babbler |
Malacocincla sepiaria |
0 |
16 |
2 |
16 |
2 |
0 |
|
Scaly-crowned
Babbler |
Malacopteron cinereum |
1 |
11 |
3 |
11 |
2 |
2 |
|
Sooty-capped
Babbler |
Malacopteron affine |
1 |
4 |
0 |
2 |
3 |
0 |
|
Moustached
Babbler |
Malacopteron magnirostre |
1 |
0 |
0 |
1 |
0 |
0 |
|
White-chested
Babbler |
Trichastoma rostratum |
11 |
11 |
1 |
17 |
6 |
0 |
|
Short-tailed
Babbler |
Trichastoma malaccense |
10 |
5 |
10 |
18 |
7 |
0 |
|
Ferruginous
Babbler |
Trichastoma bicolor |
7 |
7 |
3 |
13 |
3 |
1 |
|
Black-capped
Babbler |
Pellorneum nigrocapitatum |
1 |
0 |
3 |
4 |
0 |
0 |
|
|
|
|
|
|
|
|
|
|
Timaliidae |
|
|
|
|
|
|
|
|
Black-throated
Babbler |
Stachyris nigricollis |
8 |
13 |
11 |
15 |
15 |
2 |
|
Grey-headed
Babbler |
Stachyris poliocephala |
6 |
3 |
5 |
11 |
3 |
0 |
|
Chestnut-rumped Babbler |
Stachyris maculata |
1 |
2 |
4 |
4 |
2 |
1 |
|
Grey-hooded
Babbler |
Cyanoderma bicolor |
1 |
5 |
12 |
12 |
4 |
2 |
|
Fluffy-backed
Tit-babbler |
Macronous ptilosus |
3 |
8 |
5 |
7 |
8 |
1 |
|
Bold-striped
Tit-babbler |
Mixornis bornensis |
1 |
0 |
6 |
6 |
1 |
0 |
|
Shannon
index (H’) |
|
2.193 |
2.314 |
2.238 |
|
|
|
|
Species
evenness (J) |
|
0.867 |
0.941 |
0.919 |
|
|
|
|
Total
individual |
|
55 |
103 |
65 |
|
|
|
|
Total
species |
|
14 |
12 |
12 |
|
|
|
Table 2. Prey
item composition identified up to order.
|
Taxa |
Pelagus |
Ulu
Baleh |
Baram |
Total
|
|
Coleoptera |
21 |
14 |
19 |
54 |
|
Hymenoptera |
8 |
24 |
15 |
47 |
|
Araneae |
8 |
6 |
2 |
16 |
|
Orthoptera |
0 |
2 |
2 |
4 |
|
Hemiptera |
1 |
1 |
0 |
2 |
|
Phasmida |
1 |
1 |
0 |
2 |
|
Dictyoptera |
0 |
1 |
1 |
2 |
|
Diptera |
1 |
0 |
0 |
1 |
|
Cicaedae |
0 |
1 |
0 |
1 |
|
Gastropods |
1 |
0 |
0 |
1 |
|
Unidentified |
5 |
0 |
1 |
6 |
For images
and graphs—click here for full PDF.
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