Foraging strata and dietary preferences of fifteen species of babblers in Sarawak, Malaysia
Article Sidebar
Main Article Content
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.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors own the copyright to the articles published in JoTT. This is indicated explicitly in each publication. The authors grant permission to the publisher Wildlife Information Liaison Development (WILD) Society to publish the article in the Journal of Threatened Taxa. The authors recognize WILD as the original publisher, and to sell hard copies of the Journal and article to any buyer. JoTT is registered under the Creative Commons Attribution 4.0 International License (CC BY), which allows authors to retain copyright ownership. Under this license the authors allow anyone to download, cite, use the data, modify, reprint, copy and distribute provided the authors and source of publication are credited through appropriate citations (e.g., Son et al. (2016). Bats (Mammalia: Chiroptera) of the southeastern Truong Son Mountains, Quang Ngai Province, Vietnam. Journal of Threatened Taxa 8(7): 8953–8969. https://doi.org/10.11609/jott.2785.8.7.8953-8969). Users of the data do not require specific permission from the authors or the publisher.
References
Bowler, D.E., H. Heldbjerg, A.D. Fox, M. de Jong & K. Böhning-Gaese (2019). Long-term declines of European insectivorous bird populations and potential causes. Conservation Biology 33(5): 1120–1130. https://doi.org/10.1111/cobi.13307
Canaday, C. (1996). Loss of insectivorous birds along a gradient of human impact in Amazonia. Biological Conservation 77(1): 63–77. https://doi.org/10.1016/0006-3207(95)00115-8
Chey, V.K., J.D. Holloway, C. Hambler & M.R. Speight (1998). Canopy knockdown of arthropods in exotic plantation and natural forest in Sabah, north-east Borneo, using insecticidal mist-blowing. Bulletin of Entomological Research 88: 15–24. https://doi.org/10.1017/S0007485300041511
Didham, R.K., J. Ghazoul, N.E. Stork & A.J. Davis (1996). Insects in fragmented forests: a functional approach. Trends in Ecology & Evolution 11(6): 255–260. https://doi.org/10.1016/0169-5347(96)20047-3
Didham, R.K. (1997). The influence of edge effects and forest fragmentation on leaf-litter invertebrates in central Amazonia. In: Laurence, W.F. & R.O. Jr. Bierregaard (eds). Tropical Forest Remnants: Ecology, Management, and Conservation of Fragmented Communities. University of Chicago Press, Chicago, I.L., USA.
Dormann, C.F., J. Fründ & H.M. Schaefer (2017). Identifying causes of patterns in ecological networks: opportunities and limitations. Annual Review of Ecology, Evolution, and Systematics 48: 559–584. https://doi.org/10.1146/annurev-ecolsys-110316-022928
Durães, R. & M.Â. Marini (2003). An evaluation of the use of tartar emetic in the study of bird diets in the Atlantic forest of southeastern Brazil. Journal of Field Ornithology 74(3): 270–280. https://doi.org/10.1648/0273-8570-74.3.270
Floren, A. & K.E. Linsenmair (2001). The influence of anthropogenic disturbances on the structure of arboreal arthropod communities. Plant Ecology 153: 153–167. https://doi.org/10.1023/A:1017510312462
Floren, A. & K.E. Linsenmair (2003). How do beetle assemblages respond to anthropogenic disturbance? In: Basset, Y., V. Novotny, S.E. Miller & R.L. Kitching (eds). Arthropods of Tropical Forests. Cambridge University Press, Cambridge, I.L., USA.
Gotelli, N.J. & A.M. Ellison (2013). EcoSimR, Version 1.00. Burlington, VT. http://www.uvm.edu/~ngotelli/EcoSim/EcoSim.html
Griffiths, H.M., L.A. Ashton, A.E. Walker, F. Hasan, T.A. Evans, P. Eggleton & C.L. Parr (2018). Ants are the major agents of resource removal from tropical rainforests. Journal of Animal Ecology 87: 293–300. https://doi.org/10.1111/1365-2656.12728
Hamer, K.C., J.K. Hill, L.A. Lace & A.M. Langhan (1997). Ecological and biogeographic effects of forest disturbance on tropical butterflies of Sumba, Indonesia. Journal of Biogeography 24: 67–75. https://doi.org/10.1111/j.1365-2699.1997.tb00051.x
Hamer, K.C., R.J. Newton, F.A. Edwards, S. Benedick, S.H. Bottrell & D.P. Edwards (2015). Impacts of selective logging on insectivorous birds in Borneo: the importance of trophic position, body size and foraging height. Biological Conservation 188: 82–88. https://doi.org/10.1016/j.biocon.2014.09.026
Hartshorn, J. (2021). A review of forest management effects on terrestrial leaf litter inhabiting arthropods. Forests 12(1): 23. https://doi.org/10.3390/f12010023
Holloway, J.D. (1998). The impact of traditional and modern cultivation practices, including forestry, on Lepidoptera diversity in Malaysia and Indonesia. In: Newbery, D.M., H.H.T. Prins & N. Brown (eds). Dynamics of Tropical Communities. Blackwell Science, Oxford.
Johns, A.D. (1986). Effects of selective logging on the ecological organization of a peninsular Malaysian Rainforest avifauna. Forktail 1: 65–79.
Kattan, G.H., H. Alvarez-Lópes & M. Giraldo (1994). Forest fragmentation and bird extinctions: San Antonio eight years later. Conservation Biology 8(1): 138–146. https://doi.org/10.1046/j.1523-1739.1994.08010138.x
Kent, C.M. & T.W. Sherry (2020). Behavioural niche partitioning reexamined: do behavioural differences predict dietary differences in warbles? Ecology 101(8): e03077. https://doi.org/10.1002/ecy.3077
Klasing, K.C. (2000). Comparative Avian Nutrition. CAB International, Wallingford.
Lawton, J.H., D.E. Bingnell, B. Bolton, G.F. Bloemers, P. Eggleton, P.M. Hammond, M. Hodda, R.D. Holt, T.B. Larsen, N.A. Mawdsley, N.E. Stork, D.S. Srivastava & A.D. Watt (1998). Biodiversity inventories, indicator taxa and effects of habitat modification in tropical forest. Nature 391: 72–76.
Lopes, L.E., A.M. Fernandes & M.Â. Marini (2005). Diet of some Atlantic forest birds. Ararajuba 13(1): 95–103.
Mansor, M.S., N.A. Abdullah, M.R.A. Halim, S.M. Nor & R. Ramli (2018). Diet of tropical insectivorous birds in lowland Malaysian rainforest. Journal of Natural History 52: 2301–2316. https://doi.org/10.1080/00222933.2018.1534015
Mansor, M.S. & S.A.M. Sah (2012). Foraging patterns reveal niche separation in tropical insectivorous birds. Acta Ornithologica 47(1): 27–36. https://doi.org/10.3161/000164512X653890
Mansor, M.S. & R. Ramli (2017). Foraging niche segregation in Malaysian babblers (Family: Timaliidae). PLoS ONE 12(3): e0172836.
https://doi.org/10.1371/journal.pone.0172836
Mansor, M.S., F.Z. Rozali, N.A. Abdullah, S.M. Nor & R. Ramli (2019). How important is aerial leaf litter for insectivorous birds foraging in a Malaysian tropical forest? Global Ecology and Conservation 20: e00722. https://doi.org/10.1016/j.gecco.2019.e00722
Mansor, M.S., F.Z. Rozali, S. Davies, S.M. Nor & R. Ramli (2021). High-throuput sequencing reveals dietary segregation in Malaysian babblers. Current Zoology 68(4): 381–389. https://doi.org/10.1093/cz/zoab074
Mansor, M.S., R. Ramli & S.A.M. Sah (2015). The foraging tactics of Chestnut-winged Babbler (Stachyris erythroptera) and Abbott’s Babbler (Malacocincla abbotti) in a lowland rainforest, Malaysia. Sains Malaysiana 44(5): 687–692.
Mansor, M.S., S.M. Nor & R. Ramli (2020). Shifts in foraging behaviour of heterospecific flocking birds in a lowland Malaysian rainforest. Behavioural Processes 180: 104229. https://doi.org/10.1016/j.beproc.2020.104229
Mitra, S.S. & F.H. Sheldon (1993). Use of an exotic tree plantation by Bornean lowland forest birds. Auk 110(3): 529–540. https://doi.org/10.2307/4088417
Mohd-Azlan, J., R. Noske & M.J. Lawes (2012). Avian species-assemblage structure and indicator bird species of mangroves in the Australian monsoon tropics. Emu 112: 287-297. https://doi.org/10.1071/MU12018
Mohd-Azlan, J., R.A. Noske & M.J. Lawes (2014). Resource partitioning by mangrove bird communities in north Australia. Biotropica 46(3): 331–340. https://doi.org/10.1111/btp.12108
Moradi, H.V. & Z. Mohamed (2010). Responses of babblers (Timaliidae) to the forest edge-interior gradient in an isolated tropical rainforest in Peninsular Malaysia. Journal of Tropical Forest Science 22(1): 36–48.
Morin, P. (1999). Community Ecology. Blackwell Science Inc., Malden, M.A., USA.
Nyffeler, M., Ç.H. Şekercioğlu & C J. Whelan (2018). Insectivorous birds consume an estimated 400-500 million tons of prey annually. The Science of Nature 105(7): 47. https://doi.org/10.1007/s00114-018-1571-z
Oksanen, F.G. Blanchet, R. Kindt, P. Legendre, P.R. Minchin, R.B. O’Hara, G.L. Simpson, P. Solymos, M.H. H. Stevens & H. Wagner (2013). Vegan: Community Ecology Package. R package version 2.0‐9. http://CRAN.R-project.org/package=vegan.
Poulin, B. & G. Lefebvre (1995). Additional information on the use of tartar emetic in determining the diet of tropical birds. Condor 97(4): 897–902. https://doi.org/10.2307/1369529
Poulin, B., G. Lefebvre & R. McNeil (1992). Tropical avian phenology in relation to abundance and exploitation of food resources. Ecology 73(6): 2295–2309. https://doi.org/10.2307/1941476
Puan, C.L., G. Davison & K.C. Lim (2020). Birds of Malaysia: Covering Peninsular Malaysia, Malaysian Borneo and Singapore. Lynx and BirdLife International Field Guilds. Lynx Edicions, Barcelona.
Puan, C.L., A.J. Norehan, W.L. Ng & C.S.Y. Yong (2018). Intersexual and interspecific morphometric variations among three sympatric babbler species from Peninsular Malaysia. Malayan Nature Journal 70(1): 27–32.
Razeng, E. & D.M. Watson (2015). Nutritional composition of the preferred prey of insectivorous birds: popularity reflects quality. Journal of Avian Biology 46(1): 89–96. https://doi.org/10.1111/jav.00475
R Core Team (2016). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available at: http://www.r-project.org.
Schowalter, T.D. & L.M. Ganio (1999). Invertebrate communities in a tropical rain forest canopy in Puerto Rico following Hurricane Hugo. Ecological Entomology 24: 191–201.
Şekercioğlu, Ç.H., P.R. Ehrlich, G.C. Daily, D. Aygen, D. Goehring & R.F. Sandí (2002). Disapperarance of insectivorous birds from tropical forest fragments. Proceedings of the National Academy of Sciences of the United States of Amerca 99(1): 263–267. https://doi.org/10.1073/pnas.012616199
Sherry, T.W., C.M. Kent, N.V. Sánchez & Ç.H. Şekercioğlu (2020). Insectivorous birds in the Neotropics: ecological radiations, specialization, and coexistence in species-rich communities. Auk 137(4): 1–27. https://doi.org/10.1093/auk/ukaa049
Sing-Tyan, P., F.S. Attiqqah, I. Khatijah, M.Y. Rahah, A.H.H. Mohd-Hasri, S. Isa & A.A. Tuen (2017). The use of tartar emetic to study the diet of insectivorous birds in Borneo. Malaysian Applied Biology 46(2): 153–156.
Stouffer, P.C. & R.O. Bierregaard (1995). Use of Amazonian forest fragments by understory insectivorous birds. Ecology 76: 2429–2445. https://doi.org/10.2307/2265818
Stratford, J.A. & P.C. Stouffer (2015). Forest fragmentation alters microhabitat availability for Neotropical terrestrial insectivorous birds. Biological Conservation 188: 109–115. https://doi.org/10.1016/j.biocon.2015.01.017
Styring, A.R., R. Ragai, M. Zakaria & F.H. Sheldon (2016). Foraging ecology and occurrence of seven sympatric babbler species (Timaliidae) in the lowland rainforest of Borneo and peninsular Malaysia. Current Zoology 62(4): 345–355. https://doi.org/10.1093/cz/zow022
Thiollay, J.M. (1992). Influence of selective logging on bird species diversity in a Guianan rain forest. Conservation Biology 6(1): 47–63.
Wiens, J.A. (1989). The Ecology of Bird Communities, Vol. 1. Cambridge University Press, Cambridge, IL, USA.
Yard, H.K., C. van Riper III, B. T. Brown & M. J. Kearsley (2004). Diets of insectivorous birds along the Colorado River in the Grand Canyon, Arizona. Condor 106: 106–115. https://doi.org/10.1093/condor/106.1.106
Yong, D.L., K.C. Lim, J.A. Eaton, K.H. Tan, W.T. Lau & C. Foley (2014). The Grey-breasted Babbler Malacopteron albogulare, a poorly known Sundaic species. BirdingASIA 21: 71–75.
Yong, D.L., L. Qie, N.S. Sodhi, L.P. Koh, K.S.H. Peh, T.M. Lee, H.C. Lim & S.L.H. Lim (2011). Do insectivorous bird communities decline on land-bridge forest islands in Peninsular Malaysia? Journal of Tropical Ecology 27: 1–14. https://doi.org/10.1017/S0266467410000520
Yong, D.L. (2009). Persistence of babbler (Timaliidae) communities in Singapore forests. Nature in Singapore 2: 365–371.
Zakaria, M. & M. Nordin (1998). Comparison of visitation rates of frugivorous birds in primary and logged forest in Sabah lowland dipterocarp forest. Tropical Biodiversity 5(1): 1–9.
Zduniak, P. (2005). Forced regurgitation with tartar emetic as an effective and safe method to study diet composition in Hooded Crow nestlings. European Journal of Wildlife Research 51(2): 122–125. https://doi.org/10.1007/s10344-005-0090-3