Bird Communities in the Karst Forests of Teluk Sumbang, East Kalimantan, Indonesia

Mukhlisi Mukhlisi1,*, Tri Sayektiningsih2 and Ishak Yassir1

1Research and Development Institute for Natural Resources Conservation Technology, Indonesia

2Environmental and Forestry Research Institute of Makassar, Indonesia

ABSTRACT

Birds are important components of karst forests. Their presence can be an indicator for habitat occupied. We identified bird communities in the karst forests of Teluk Sumbang, East Kalimantan. Bird sampling was done in hill karst forests and coastal karst forests. We employed a point count method by following transects. Observers walked constantly along transect and stopped every distance of ±200 m to record all sighted birds for 10-15 min. We found 89 bird species: 67 bird species were identified in hill karst forest and 33 bird species were recorded in coastal karst forests. Eleven bird species were found in both study sites. The score of diversity, species richness, and evenness indices of hill karst forests was higher than that in coastal karst. A t-test revealed that there was a significant difference in diversity index between coastal and hill karst (T = 2.016, p = 0.039). Birds characterized by a wide range of distribution and were able to adapt to various types of environments, particularly secondary forests, were most dominant. Nevertheless, the karst forests of Teluk Sumbang were also essential habitat for threatened and protected bird species.

Article Information

Received 14 January 2021

Revised 10 February 2021

Accepted 16 February 2021

Available online 10 June 2021

(early access)

Published 22 February 2022

Authors’ Contribution

MM planned and developed study design, collected data, and wrote the manuscript. TS participated in writing the manuscript. IY supervised the study and proofread the manuscript.

Key words

Birds communities, Karst forests, Secondary forests, Sangkulirang-Mangkalihat.

DOI: https://dx.doi.org/10.17582/journal.pjz/20210114070106

* Corresponding author: mukhlisi.arkan@gmail.com

0030-9923/2022/0003-1239 $ 9.00/0

Copyright 2022 Zoological Society of Pakistan

Introduction

A tropical karst rainforest is an essential habitat of Bornean bird communities. The niche complexity and various microclimates due to the long geological processes in the past contribute to bird species richness, rarity, and endemicity (Clements et al., 2006; Battistia et al., 2017; Tolentino et al., 2020). Karst forests are typically characterized by dolines, ponors, and caves, creating microhabitat diversity for birds. These kinds of environment also serve as refugia for birds and invertebrates sensitive to climate change (Clements et al., 2006; Bátori et al., 2014). Frugivorous bird communities in karst forests are particularly important in accelerating native plant regeneration in degraded areas (Caves et al., 2013). In term of economic importance, birds have a high economic value for people. For example, nests of swiftlets (Collocalia spp.) found in karst forests are highly prized for their usage in traditional medicine (Thorburn, 2014; Haryono et al., 2017).

Numerous studies have dealt with bird richness in karst forests, particularly in Borneo (Rahman and Abdullah, 2002; Salas et al., 2005; Mansor et al., 2011). Nevertheless, information on birds in Teluk Sumbang’s karst forests is limited. It is crucial since birds in Teluk Sumbang is under threat because of illegal poaching (Salas et al., 2005), habitat loss due to illegal logging, forest fires, and mining expansion. In addition, karst forests which are sensitive and fragile ecosystem are challenging in terms of restoration (Zhou et al., 2020). Thus, there are likely many a bird species got extinct before we could recognize their occurence (Satyanti and Kusuma, 2010; Liu et al., 2018). Therefore, research on bird communities in Teluk Sumbang is urgently required to support bird conservation.

Teluk Sumbang is a small part of Sangkulirang-Mangkalihat landscape located on the east coast of Indonesian Borneo. Totally, karst of Sangkulirang-Mangkalihat landscape covers an area of 1 million Ha, which is influenced by different tectonic processes and structural settings (Haryono et al., 2017). The karst is ecologically important as habitat of diverse flora and fauna. It also provides and regulates water beneficial for community and preserves history of people through archaeological site protection (Haryono et al., 2017; Suwasono et al., 2018). Teluk Sumbang’s karst is a unique ecosystem. It is comprised of ancient limestone formation strecthing from narrow coast to hilly forests. Karst of Teluk Sumbang is also situated between marine tourism roads famous in East Kalimantan. The karst is currently developed as an ecotourism area due to their beautiful landscape and biodiversity.

This study was aimed to determine the diversity and abundance of birds in the Teluk Sumbang’s karst forests. Specifically, we compared bird communities between karst forests located in the coastal karst forests and hill karst forests. We hope our research can be a reference to manage biodiversity in the karst forests of Teluk Sumbang.

Materials and methods

Study site

Study was conducted in the karst forests of Teluk Sumbang, Berau Regency, East Kalimantan (Fig. 1). The area is a small part of the Sangkulirang-Mangkalihat landscape protected by Governor Regulation of East Kalimantan No. 67/2012 with total area of 1.867.676 ha. Data collection was carried out in two distinct habitats: coastal and hill karst forests (200-300 above sea level). Coastal karst forests are typified by less abundant trees in comparison to hill karst. Vegetation is dominated by Cocos nucifera, Ficus spp., Sonneratia alba, and shrubs. Meanwhile, hill karst forests are mainly consisting of mix dipterocarp forests with dominant trees such as Shorea spp., Dryobalanops spp., Dipterocarpus spp., Ficus spp., and various pioneer trees like Macaranga spp., Acalypha caturus, and Trema tomentosa. Data were collected during August 2020.

 

Sampling

We used a point count method by following transect lines installed in each sampling location to record birds (Bibby et al., 2000). According to this method, observers walked constantly along transect and stopped every distance of ± 200 m to record all sighted birds for 10-15 min. Each transect was 2 km in length. Transects situated in coastal karst forests were installed parallel to the shoreline. Meanwhile, for uphill karst forests, transects were placed vertically so that they cut contour lines. Birds were counted twice: morning (06.30-09.00) and evening (15.30-18.00). All time were in Central Indonesian Time setting (UTC + 08.00). We used MacKinnon et al. (2010), and Phillips and Phillips (2011) for bird identification.

Data analysis

Data were grouped into scientific name, family, and conservation status. The abundance of birds was counted according to formula from Bibby et al. (2000). We also calculated the Shannon Wienner diversity index (H’), the species richness index (R), and the evenness index (E). Similarity of birds between coastal and hill karst was analyzed using Sorensen formula. All analyses were run by using software PAST. 3.1 (Hammer et al., 2001). A t-test was used to compare diversity, species richness, and dominance indices of birds between coastal and hill karst forests.

Results

Species composition

As many as 89 species of birds belonging to 41 families were identified (Table I). We found 33 species of birds in coastal karst forests and 67 species in hill karst forests. There was 11 species of birds found in the two habitats, which were Dicaeum trigonostigma, Chalcophaps indica, Chloropsis cyanopogon, Corvus enca, Haliastur indus, Lonchura fuscans, Orthotomus ruficeps, Pycnonotus goiavier, Eurylaimus ochromalus, Aerodramus fuciphagus, and Spilopelia chinensis.

Family Muscicapidae was dominant in hill karst forest which accounted for 8.96% bird species. Megalaimidae (7.46%) and Pycononotidae (7.46%) were the second and third most dominant bird species. Furthermore, Columbidae (9.38%) was the most abundant family of birds found in coastal karst forests. Other families with the same proportion (6.25%) were Alcedinicae, Anhingidae, Cuculidae, and Nectariniidae.

Community structure

The relative abundance of bird species in the karst forests of Teluk Sumbang varied considerably (Fig. 2). We noted that Aplonis panayensis had the highest value of relative abundance (13.24%) in coastal karst forests, followed by Aerodramus fuciphagus (11.76%). Todiramphus chloris, Chloropsis cyanopogon, and Antrheptes malacensis had the same value of relative abundance, which was 6.62%. On the other hand, Pycnonotus simplex was the most abundant bird in the hill karst forests (8.59%). It was followed by Cypsiurus balasiensis (4.29%), Aerodramus fuciphagus (4.29%), Chloropsis cyanopogon (4.29%), and Eurylaimus ochromalus (4.29%).

 

Table I.- A list of birds in the karst forests of Teluk Sumbang.

No	Family/ Scientific name	Common name	Site		Conservation status
			Hill karst	Coastal karst	IUCN	P.LHK	CITES
	Acanthizidae
1	Gerygone sulphurea	Golden-bellied gerygone		√	LC
	Acciptridae
2	Nisaetus cirrhatus	Changeable hawk-eagle	√		LC	√	App II
3	Haliastur indus	Brahminy kite	√	√	LC	√	App II
4	Accipiter trivirgatus	Crested goshawk	√		LC	√	App II
5	Aviceda jerdoni	Jerdon's baza	√		LC	√	App II
	Aegithinidae
6	Aegithina tiphia	Common Iora	√		LC
	Alcedinidae
7	Ceyx erithaca	Black-backed dwarf-kingfisher	√		LC
8	Todiramphus chloris	Collared kingfisher		√	LC
9	Pelargopsis capensis	Stork-billed kingfisher		√	LC
	Anhingidae
10	Anhinga melanogaster	Oriental darter		√	NT	√
	Apodidae
11	Cypsiurus balasiensis	Asian palm-swift	√		LC
12	Apus nipalensis	House swift	√		LC
13	Apus pacificus	Pacific swift		√	LC
14	Aerodramus fuciphagus	White-nest swiftlet	√	√	LC
	Ardeidae
15	Ardea cinerea	Grey heron		√	LC

No	Family/ Scientific name	Common name	Site		Conservation status
			Hill karst	Coastal karst	IUCN	P.LHK	CITES
	Artamidae
16	Artamus leucoryn	White-breasted woodswallow		√	LC
	Bucerotidae
17	Anthracoceros albirostris	Oriental pied-hornbill	√		LC	√	App II
18	Anthracoceros malayanus	Black hornbill	√		VU	√	App II
19	Buceros rhinoceros	Rhinoceros hornbill	√		VU	√	App II
20	Rhyticeros undulatus	Wreathed hornbill	√		VU	√	App II
	Calyptomenidae
21	Calyptomena viridis	Green broadbill		√	NT
	Chloropseidae
22	Chloropsis cyanopogon	Lesser green leafbird	√	√	NT	√
23	Chloropsis sonnerati	Greater green leafbird	√		EN	√
	Ciconiidae
24	Leptoptilos javanicus	Lesser adjutant		√	VU	√
	Cisticolidae
25	Orthotomus atrogularis	Dark-necked tailorbird	√		LC
26	Orthotomus ruficeps	Ashy tailorbird	√	√	LC
27	Prinia flaviventris	Yellow-bellied prinia	√		LC
	Columbidae
28	Chalcophaps indica	Asian emerald dove	√	√	LC
29	Ducula aenea	Green imperial-pigeon	√		LC
30	Treron vernans	Pink-necked green-pigeon		√	LC
31	Spilopelia chinensis	Spotted dove	√	√	LC
	Corvidae
32	Corvus enca	Slender-billed crow	√	√	LC
	Cuculidae
33	Cacomantis sonneratii	Banded bay cuckoo	√		LC
34	Centropus bengalensis	Lesser coucal	√	√	LC
35	Centropus sinensis	Greater coucal			LC
36	Phaenicophaeus diardi	Black-bellied malkoha		√	NT
37	Zanclostomus javanicus	Red-billed malkoha	√		LC
38	Rhinortha chlorophaea	Raffles's malkoha	√		LC
	Dicaeidae
39	Dicaeum trigonostigma	Orange-bellied flowerpecker	√	√	LC
	Dicruridae
40	Dicrurus paradiseus	Greater racket-tailed drongo	√		LC
	Eurylaimidae
41	Cymbirhynchus macrorhynchos	Black-and-red broadbill	√		LC
42	Eurylaimus ochromalus	Black-and-yellow broadbill	√	√	NT

No	Family/ Scientific name	Common name	Site		Conservation status
			Hill karst	Coastal karst	IUCN	P.LHK	CITES
	Estrildidae
43	Lonchura fuscans	Dusky munia	√	√	LC
44	Lonchura malacca	Tricolored munia	√		LC
	Hirundinidae
45	Hirundo tahitica	Pacific swallow		√	LC
	Laridae
46	Thalasseus bergii	Great crested tern		√	LC
	Leiotrichidae
47	Alcippe brunneicauda	Brown fulvetta	√		NT
	Megalaimidae
48	Psilopogon duvaucelii	Blue-eared barbet	√		LC
49	Psilopogon henricii	Yellow-crowned barbet	√		NT	√
50	Psilopogon mystacophanos	Red-throated barbet	√		NT	√
51	Psilopogon rafflesii	Red-crowned barbet	√		NT	√
52	Psilopogon chrysopogon	Gold-whiskered barbet	√		LC	√
	Meropidae
53	Nyctyornis amictus	Red-bearded bee-eater	√		LC
54	Merops philippinus	Blue-tailed bee-eater		√	LC
	Monarchidae
55	Terpsiphone paradisi	Indian paradise-flycatcher	√		LC
	Muscicapidae
56	Kittacincla malabarica	White-rumped shama	√		LC
57	Copsychus saularis	Oriental magpie-robin	√		LC
58	Cyornis umbratilis	Gray-chested jungle-flycatcher	√		NT
59	Ficedula dumetoria	Rufous-chested flycatcher	√		LC
60	Cyanoptila cyanomelana	Blue-and-white flycatcher	√		LC
61	Enicurus ruficapillus	Chestnut-naped forktail	√		NT
	Nectariniidae
62	Aethopyga siparaja	Crimson sunbird		√	LC	√
63	Anthreptes malacensis	Brown-throated sunbird		√	LC
64	Arachnothera longirostra	Little spiderhunter	√		LC
	Passeridae
65	Passer montanus	Eurasian tree sparrow		√	LC
	Pellorneidae
66	Malacopteron affine	Sooty-capped babbler	√		NT
67	Malacocincla sepiaria	Horsfield's babbler	√		LC
	Phasianidae
68	Argusianus argus	Great argus	√		VU	√	App II
69	Rollulus rouloul	Crested partridge	√		NT
70	Lophura ignita	Crested fireback	√		VU
71	Synoicus chinensis	Blue-breasted quail	√		LC

No	Family/ Scientific name	Common name	Site		Conservation status
			Hill karst	Coastal karst	IUCN	P.LHK	CITES
	Picidae
72	Dryocopus javensis	White-bellied woodpecker	√		LC		App I
73	Meiglyptes tukki	Buff-necked woodpecker		√	NT
	Pittidae
74	Erythropitta granatina	Garnett pitta	√		NT	√
75	Pitta sordida	Hooded pitta	√		LC	√
	Psittaculidae
76	Loriculus galgulus	Blue-crowned hanging-parrot	√		LC	√	App II
	Pycnonotidae
77	Alophoixus finschii	Finsch's bulbul	√		NT
78	Brachypodius atriceps	Black-headed bulbul	√		LC
79	Pycnonotus goiavier	Yellow-vented bulbul	√	√	LC
80	Pycnonotus simplex	Cream-vented bulbul	√		LC
81	Pycnonotus plumosus	Olive-winged bulbul	√		LC
	Rallidae
82	Rallina fasciata	Red-legged crake		√	LC
	Rhipiduridae
83	Rhipidura javanica	Malaysian pied-fantail	√		LC	√
	Sturnidae
84	Aplonis panayensis	Asian glossy starling		√	LC
85	Gracula religiosa	Common hill myna	√		LC	√	App II
86	Acridotheres javanicus	Javan myna		√	VU
	Timaliidae
87	Pomatorhinus montanus	Chestnut-backed scimitar-babbler	√		LC
	Trogonidae
88	Harpactes diardii	Diard's trogon	√		NT	√
	Turdidae
89	Geokichla interpres	Chestnut-capped thrush	√		EN

 

P.LHK is a regulation which consists of lists of protected plants and animals based on P.LHK No.P.106/2018.

 

Table II.- Diversity, species richness, and evenness indices of birds on the study site.

Index	Study site		t test
	Coastal karst	Hill karst
Shannon-Wiener diversity (H)	2.47 ± 024	2.80 ± 0.39	Significant
Species richness (R)	3.91 ± 0.57	5.53 ± 1.51	Not significant
Evenness (E)	0.75 ± 0.14	0.79 ± 0.18	Not significant

 

The score of diversity, species richness, and evenness indices of hill karst forests was higher than that in coastal karst (Table II). A t-test revealed that there was a significant difference in diversity index between coastal and hill karst (T = 2.016, p = 0.039). Bird species between two types of habitats significantly differed, showed by the low similarity index value of 22.00%.

DISCUSSION

Birds observed in this study contribute to 13.30% of the total number of birds in Borneo (669 species) (Phillips and Phillips, 2011). This study complements Salas et al. (2005) who recorded 120 avian species in the southern Sangkulirang Peninsula. Nevertheless, some studies in karst forests of Borneo found lower bird species, such as in Padawan-Malaysia (80 species) (Mansor et al., 2011), and Banggi-Malaysia (28 species) (Rahman and Abdullah, 2002). The discrepancies are due to a wide variation of habitats, disturbance levels, size of sampling areas, and duration of observation. Teluk Sumbang is a small part of the Sangkulirang-Mangkalihat landscape covering an area of over 1 million ha. The number of bird species grows significantly if we broaden our coverage area of research.

Muscicapidae is the most dominant family of bird in hill karst. This is consistent with Mansor et al. (2011). Muscicapidae distributes in a wide range of habitats (Sangster et al., 2010). In the Southeast Asia region, they occupy areas with low disturbances. Muscicapidae is an insectivorous bird. Their occurrence corresponds to thick litters, high humidity, and dense vegetation (Moradi et al., 2009; Wielstra et al., 2011). Moreover, the family of Columbidae is the most abundant in coastal karst. Some of Columbidae occur in hill karst as well such as Chalcophaps indica and Spilopelia chinensis. As a frugivorous bird, they are benefitted by Ficus spp. growing from the coast to hill. Ficus spp. is key species yielding abundant fruits all year round, thereby attracting all frugivorous birds.

The bird family associated with wetlands can be seen in coastal karst, such as Alcedinidae, Anhingidae, Ardeidae, Ciconiidae, and Lariidae. Their presence follows tides in which they are foraging when the sea level falls. Shallow waters help water bird find food like fishes, crustaceans, aquatic insectivores, etc. (Burton et al., 2004; Zakaria and Rajpar, 2013). Teluk Sumbang is rich in fishes since it is situated within Indo-Pacific Coral Triangle (Kusumoto et al., 2019). Coral reefs, which are a habitat for marine animals, are a high quality food source for birds. Its growth is enhanced by CaCo3 derived from karst. The fish abundance, aquatic ecosystems and birds are interwined, forming a complex food web (Vilchis et al., 2014).

The abundance of Pycnonotus simplex was the highest in hill karst. This species is widely distributed in Southeast Asia, particularly in Malaysia Peninsula, Sumatera, Java, and Borneo (MacKinnon et al., 2010; Phillips and Phillips, 2011). Pycnonotus simplex is a generalist bird tolerant to various habitat types like primary forests, secondary forests, and garden up to 1,300 above sea level (MacKinnon et al., 2010). Furthermore, Aerodramus fuciphagus and Cypsiurus balasiensis are two typical birds of karst with the high abundance as well. Aerodramus fuciphagus is widespread over coast in comparison to the Asian palm swift which is only found in hill forests. Dolines, ponors, and caves in karst are ideal for swifts for breeding and nesting. Our findings are in line with Haryono et al. (2017) who reported that as of 61 caves located in the Sangkulirang-Mangkalihat landscape are nesting sites for swifts. Due to its economic value, swift’s nests are periodically harvested and sold by local community.

Aplonis panayensis is the most abundance bird species in coastal karst. The bird builds nest and forages on coconut trees and Ficus spp. grown along the coast. Naturally, Aplonis panayensis is an insect hunter bird visiting various fruit trees, but the abundance of Ficus spp. is sufficient enough to support the bird’s reproduction success. It is consistent with Shazali et al. (2016) who confirmed that 86% of Aplonis panayensis’s droppings in Kuching-Malaysia contained seeds of Ficus spp. Aplonis panayensis lives in group. Sometimes, each group is assembled, forming a flock. The bird has a wide distribution because of its ability to adapt in various habitat conditions: disturbed environments, cities, open areas, and secondary forests (Sountag and Louette, 2007; Shazali et al., 2016; Shieh et al., 2016). Aplonis panayensis is native to Teluk Sumbang and other eastern parts of Borneo. However, in other locations, such as in Taiwan, the bird is considered as an exotic and invasive bird species (Shieh et al., 2016).

The high abundance of Chloropsis cyanopogon both in hill karst and coastal karst forests is a good indicator. Besides, we also found Chloropsis sonnerati in hill karst, even though the bird’s abundance is lower than that of Chloropsis cyanopogon. We frequently noticed the two birds along edge forests containing fruiting trees, such as Acalypha caturus, Macaranga spp., and Trema tomentosa. Although Chloropsis spp. is protected, the bird is popular as pet in Indonesia. Its population declines dramatically due to illegal hunting. Chng et al. (2017) stated that Chloropsis spp. has been locally extinct in some parts of Borneo because of massive hunting. It is estimated that over 2000 individuals of birds are traded each year. Our observation indicated that Chloropsis spp. was also illegally poached in Teluk Sumbang. It was supported by a report concluding that Berau Regency is one of illegal hunting spots for Chloropsis spp. and other wildlife in East Kalimantan Province (Salas et al., 2005; Mukhlisi et al., 2020).

Diversity, richness, and evenness of bird species in hill karst forests are higher than that in coastal karst forests. However, only the diversity index is significantly different. It can be caused by a wide variation in physical conditions of hill karst forests, creating different microhabitats for birds. Dolines, ponors, and caves are predominantly found in hill karst. They are a suitable habitat for birds, especieally those which are sensitive to temperature change (Clements et al., 2006; Battistia et al., 2017; Bátori et al., 2014). In terms of vegetation, hill karst forests are diverse in vegetation composition and structure. For example Sitepu et al. (2020) recorded 89 species of plants in young and old secondary hill karst forests. The complexity of vegetation structure as well as species diversity is beneficial for birds in providing food and shelter. Costantini et al. (2016) mentioned that birds’ diversity and abundance in tropical forest of Borneo were associated with vegetation cover.

Furthermore, anthropogenic disturbances in hill karst forests are lower compared to the coastal karst forests. Some parts of hill karst experienced disturbances in the past such as illegal logging, but the impacts on vegetation are low. We found that the disturbed vegetation has regenerated, transforming into secondary forests which are characterized by Macaranga spp. and Duabanga moluccana. On the other hand, infrastructure development supporting tourism and settlements is concentrated around the coastal zone. Lack of vegetation on the coastal zone reduces habitat carrying capacity, affecting bird diversity. It is consistent with Putri et al. (2017) who concluded birds in Sulawesi’s karst showed negative responses towards habitat change in the form of number of individuals and species. In addition, birds with large body size are reduced.

Although there is a difference in habitat pressures between hill karst and coastal karst, both are connected and become an important habitat for avifauna. Acevedo and Aide (2008) argued that karst and wetland in spite of being patchy and surrounding by settlements and shrubs can still support resident and migrant birds. Doline, ponors, and caves have high conservation values for birds and other vertebrates (Battistia et al., 2017). It is confirmed by a finding which recorded 24 threatened and protected bird species based on regulation in Indonesia. Some are sensitive birds so that they can be used as an indicator for habitat change in tropical forest, such as hornbill (Bucerotidae) and garnett (Pittidae). As of 4 out of 9 hornbills in Borneo are found in Teluk Sumbang. Pittidae, furthermore, which is the guild of terrestrial insectivorous birds, shows a considerably decline in its abundance once its habitat is disturbed (Lambert and Collar, 2002; Wielstra et al., 2011; Hamer et al., 2015).

Conclusion

There was a significant difference in bird communities between hill karst and coastal karst forests of Teluk Sumbang. The abundance and species richness of birs in hill karst forests were higher than that in coastal karst. Generally, dominant birds were those which had wide distribution and were adapted to various habitats, particularly secondary forests. Teluk Sumbang was essential home to threatened and protected birds. Therefore, Teluk Sumbang is crucial for conservation in the landscape scale. It is required efforts to conserve karst securing connectivity among habitat types from the coast to the hill.

Acknowledgements

We would like to thank and appreciate Warsidi, Jumri, Tutui, Bina Sitepu, Priyono, and Iman Suharja for their help during data collection. The authors also thank to Bpk. Ronald Lolang (Lamin Guntur) who has supported fieldwork in Teluk Sumbang. This research was funded by DIPA Balitek KSDA year of 2020.

Statement of conflict of interest

The authors declare no conflict of interest.

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