Foraging Behaviour of Three Shorebird Species on Coastal Mudflats of Southwestern Sarawak
Keywords:
Foraging Behaviour, Intertidal, Migratory, Sarawak, ShorebirdsAbstract
Many shorebirds are long-distance migrants and they congregate on intertidal mudflats for feeding throughout their non-breeding season. Despite being one of the key staging sites for migratory shorebirds, data on shorebirds foraging ecology in Sarawak is insufficient for the understanding of the interaction between shorebirds and their behaviour. This study aimed to determine the foraging behaviour of Whimbrel (Numenius phaeopus), Bar-tailed Godwit (Limosa lapponica) and Terek Sandpiper (Xenus cinereus) at Asajaya and Buntal mudflats. Data collection of this study was conducted at low tide, during two non-breeding seasons with a total of 12 months of sampling. Focal observations were conducted within a 50 m × 50 m quadrat. A total of 8 exclusive foraging techniques were observed for the three shorebird species, including: pecking, probing, picking, stabbing, snapping, submerging, sweeping and ingesting. Terek Sandpiper displayed all the exclusive foraging behaviours, whereas Whimbrel and Bar-tailed Godwit showed 7 and 5 behaviours, respectively. The three shorebirds also displayed non-exclusive foraging behaviours such as walking, preening and defecating. Spearman correlation test indicates a positive correlation between the foraging behaviours performed among three shorebird species. All three shorebird species adopted similar mixed foraging strategies comprising pecking and probing, with an exception on supplementary behaviours observed in Whimbrel and Terek Sandpiper. Principal Component Analysis (PCA) analysis showed a strong correlation between picking and ingesting behaviours, suggesting a high chance of foraging success with the presence of picking behaviour. The outcome of this study is crucial in understanding how shorebirds maximise their behavioural performance when foraging as well as to assist in formulating better conservation strategies for targeted migratory shorebird species and coastal mudflats.
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Baguette, M., Hannier, L., Kirchhoff, F., Le Floch, G., Schtickzelle, N., Stevens, V. & Bels, V. 2023. Repertoire of food acquisition behaviors in shorebirds (Aves, Charadriiforme). Preprints, 2023: 2023101737. DOI: https://doi.org/10.20944/preprints202310.1737.v1
Baker, M.C. & Baker, A.E.M. 1973. Niche relationships among six species of shorebirds on their wintering and breeding ranges. Ecological Monographs, 43(2): 193-212. DOI: https://doi.org/10.2307/1942194
Bakewell, D., Wong, A., Kong, D. & Rose, A. 2017. Waterbird Surveys of the Sarawak Coast (2010-2012). Malaysian Nature Society, Kuala Lumpur. 271 pp.
Bamford, M., Watkins, D., Bancroft, W., Tischler, G. & Wahl, J. 2008. Migratory Shorebirds of The East Asian-Australasian Flyway: Population Estimates and Internationally Important Sites. Wetlands International - Oceania, Canberra. 24 pp.
Barbosa, A. & Moreno, E. 1999. Evolution of foraging strategies in shorebirds: An ecomorphological approach. The Auk, 116(3): 712-725. DOI: https://doi.org/10.2307/4089332
Barbosa, A. 1995. Foraging strategies and their influence on scanning and flocking behaviour of waders. Journal of Avian Biology, 26(3): 182-186. DOI: https://doi.org/10.2307/3677317
Bijlsma, R.G. & de Roder, F.E. 1991. Foraging behaviour of Terek Sandpipers Xenus cinereus in Thailand. Wader Study Group Bulletin, 61: 22-26.
Birdlife International. 2020. Important bird areas factsheet: Bako-Buntal Bay [WWW Document]. BirdLife International. URL http://datazone.birdlife.org/site/factsheet/bako-buntal-bay-iba-malaysia/refs (assessed 11.03.20).
BirdLife International. 2022. IUCN red list for birds [WWW Document]. BirdLife International. URL datazone bird life.org/species/factsheet (assessed 01.12.22).
Boggies, M.A. 2018. Linking Diet, Behaviour, and Bioenergetics of A Migratory Waterbird to Evaluate Response to Wintering Ground Conditions (Ph.D). New Mexico State University.
Brockmann, H.J. 2011. Measuring behavior: Ethograms, kinematic diagrams, and time budgets [WWW Document]. College of the Holy Cross. URL https://college.holycross.edu/faculty/kprestwi/behavior/e&be_notes/E&BE_ethograms.pdf (assessed 01.12.22).
Carneiro, C., Gunnarsson, T.G. & Alves, J.A. 2017. Bloody cockles: A novel and important food item for whimbrels in the Banc d'Arguin. Wader Study, 124(2): 161-162. DOI: https://doi.org/10.18194/ws.00072
Choi, C.Y. 2015. The Northward Migration Stopover Ecology of Bar-Tailed Godwits and Great Knots in The Yalu Jiang Estuary National Nature Reserve, China (Ph.D). Massey University.
Choi, C., Battley, P.F., Potter, M.A., Ma, Z., Melville, D.S. & Sukkaewmanee, P. 2017. How migratory shorebirds selectively exploit prey at a staging site dominated by a single prey species. The Auk, 134(1): 76-91. DOI: https://doi.org/10.1642/AUK-16-58.1
Choi, S., Kang, S., Lee, S., Min, J. & Kim, B. 2017. Foraging behavior and diet of northward migrating Bar-Tailed Godwits (Limosa laponica) and Great Knots (Calidris tenuirostris) at a key stopover site. International Journal of Sciences: Basic and Applied Research (IJSBAR), 36(6): 276-286.
Colwell, M.A. 2010. Shorebird Ecology, Conservation, and Management. University of California Press, California. 344 pp. DOI: https://doi.org/10.1525/9780520947962
Crews, J., Braude, S., Stephenson, C. & Clardy, T. 2002. The Ethogram and Animal Behaviour Research. Washington University, St. Louis. 122 pp.
Cunningham, S.J., Alley, M.R., Castro, I., Potter, M.A., Cunningham, M. & Pyne, M.J. 2010. Bill morphology of ibises suggests a remote-tactile sensory system for prey detection. Auk, 127(2): 308-316. DOI: https://doi.org/10.1525/auk.2009.09117
Dann, P. 1993. Abundance, diet and feeding behaviour of the Whimbrel, Numenius phaeopus variegatus in Rhyll Inlet, Victoria. Corella, 17(2): 52-57.
Davidson, N.C., Townsend, D.J., Pienkowski, M.W. & Speakman, J.R. 1986. Why do curlews Numenius have decurved bills? Bird Study, 33: 61-69. DOI: https://doi.org/10.1080/00063658609476896
Davis, C.A. & Smith, L.M. 2001. Foraging strategies and niche dynamics of coexisting shorebirds at stopover sites in the Southern Great Plains. Auk, 118: 484-495. DOI: https://doi.org/10.1093/auk/118.2.484
Dierschke, V., Kube, J., Probst, S. & Brenning, U. 1999. Feeding ecology of dunlins Calidis alphina staging in the southern Baltic Sea, I. Habitat use and food selection. Journal of Sea Research, 42(1999): 49-64. DOI: https://doi.org/10.1016/S1385-1101(99)00013-1
Duijns, S., Hidayati, N.A. & Piersma, T. 2013. Bar-tailed Godwits Limosa l. lapponica eat polychaete worms whenever they winter in Europe. Bird Study, 60: 509-517. DOI: https://doi.org/10.1080/00063657.2013.836153
Durell, S. 2000. Individual feeding specialisation in shorebirds: Population consequences and conservation implications. Biological Reviews, 75(4): 503-518. DOI: https://doi.org/10.1111/j.1469-185X.2000.tb00053.x
Finn, P. 2009. Habitat Selection, Foraging Ecology and Conservation of Eastern Curlews on Their Non-Breeding Grounds (Ph.D). Griffith University.
Gerritsen, A.F.C. & Heezrik, Y.M. 1985. Substrate preference and substrate related foraging behaviour in three calidris species. Netherlands Journal of Zoology, 35(4): 671-692. DOI: https://doi.org/10.1163/002829685X00235
Gokula, V. 2012. An ethogram of Spot-billed Pelican (Pelecanus philippensis). Chinese Birds, 2(4): 183-192. DOI: https://doi.org/10.5122/cbirds.2011.0030
Goss-Custard, J.D. 1977. The ecology of the wash. I. Density-related behaviour and the possible effects of a loss of feeding grounds on wading birds (Charadrii). The Journal of Applied Ecology, 14(3): 721-739. DOI: https://doi.org/10.2307/2402805
Granadeiro, J.P., Dias, M.P., Martins, R.C. & Palmeirim, J.M. 2006. Variation in numbers and behaviour of waders during the tidal cycle: Implications for the use of estuarine sediment flats. Acta Oecologica, 29(2006): 293-300. DOI: https://doi.org/10.1016/j.actao.2005.11.008
Granadeiro, J.P., Santos, C.D. & Dias, M.P. 2007. Environmental factors drive habitats partitioning in birds feeding in intertidal flats; implication for conservation. Hydrobiologia, 587: 291-302. DOI: https://doi.org/10.1007/s10750-007-0692-8
Greenhalgh, M.E. 1975. Study of the Food and Feeding Ecology of the Wading Birds (Ph.D). Liverpool Polytechnic.
Hamilton, R.B. 1975. Comparative behaviour of the American Avocet and the Black-necked Stilt (Recurvirostridae). Ornithological Monographs, 47(2): 177. DOI: https://doi.org/10.2307/4512224
Higgins, P.J. & Davies, S.J.J.F. 1996. Handbook of Australian, New Zealand and Antartic Birds Snipe to Pigeons, Volume 3. Oxford University Press, Melbourne. 815 pp.
Jing, K., Ma, Z., Li, B., Li, J. & Chen, J. 2007. Foraging strategies involved in habitat use of shorebirds at the intertidal area of Chongming Dongtan, China. Ecological Research, 22(4): 559-570. DOI: https://doi.org/10.1007/s11284-006-0302-7
Karlionova, N., Remisiewicz, M. & Pinchuk, P. 2006. Biometrics and breeding phenology of Terek Sandpipers in the Pripyat' Valley, S. Belarus. Wader Study Group Bulletin, 110: 54-58.
Katrínardóttir, B., Pálsson, S., Gunnarsson, T.G. & Sigurjónsdóttir, H. 2013. Sexing Icelandic Whimbrels Numenius phaeopus islandicus with DNA and biometrics. Ringing and Migration, 28(1): 43-46. DOI: https://doi.org/10.1080/03078698.2013.811160
King, K.A. 2008. Behaviour Patterns and Habitat Use of the Brolga (Grus rubicundus) at Two Flocking Sites in South-West Victoria (BSc). Deakin University.
Kumar, V., Mishra, H. & Kumar, A. 2021. Foraging behaviour in river lapwing, Vanellus duvaucelii (Lesson, 1826) (Charadriiformes: Charadriidae): differences in technique, prey and habitat. Journal of Asia-Pacific Biodiversity, 14(1): 33-39. DOI: https://doi.org/10.1016/j.japb.2020.09.011
Kuwae, T., Miyoshi, E., Sassa, S. & Watabe, Y. 2010. Foraging mode shift in varying environmental conditions by dunlin Calidris alpina. Marine Ecology Progress Series, 406(May 2010): 281-289. DOI: https://doi.org/10.3354/meps08519
Kvitek, R.G. & Bretz, C.K. 2004. Harmful algal bloom toxins protect bivalve populations from sea otter predation. Marine Ecology Progress Series, 271: 233-243. DOI: https://doi.org/10.3354/meps271233
Lai, C. 2019. Preserving the wintering sites of migratory birds. The Borneo Post, October 6, p. 1.
Landys, M.M., Piersma, T., Guglielmo, C.G., Jukema, J., Ramenofsky, M. & Wingfield, J.C. 2005. Metabolic profile of long-distance migratory flight and stopover in a shorebird. In: Proceedings of the Royal Society B: Biological Sciences. The Royal Society, London. pp. 295-302. DOI: https://doi.org/10.1098/rspb.2004.2952
Moreira, F. 1995. The winter-feeding ecology of Avocets Recurvirostra avosetta on intertidal areas. I. Feeding strategies. Ibis, 137: 92-98. DOI: https://doi.org/10.1111/j.1474-919X.1995.tb03224.x
Mouritsen, K.N. & Jensen, K.T. 1992. Choice of microhabitat in tactile foraging dunlins Calidris alphina: The importance of sediment penetrability. Marine Ecology Progress Series, 85(1): 1-8. DOI: https://doi.org/10.3354/meps085001
Myers, J.P., Williams, S.L. & Pitelka, F.A. 1980. An experimental analysis of prey availability for sanderlings (Aves: Scolopacidae) feeding on sandy beach crustaceans. Canadian Journal of Zoology, 25: 1564-1574. DOI: https://doi.org/10.1139/z80-216
Myers, S. 2016. Birds of Borneo. 2nd Ed. Bloomsbury Publishing PLC, London. 272 pp.
Navedo, J.G., Sauma-Castillo, L. & Fernández, G. 2012. Foraging activity and capture rate of large Nearctic shorebirds wintering at a tropical coastal lagoon. Waterbirds, 35(2): 301-311. DOI: https://doi.org/10.1675/063.035.0211
Nebel, S. & Thompson, G.J. 2005. Foraging behaviour of western sandpiper changes with sediment temperature: implications for their hemispheric distribution. Ecological Research, 20(4): 503-507. DOI: https://doi.org/10.1007/s11284-005-0061-x
Nebel, S., Jackson, D.L. & Elner, R.W. 2005. Functional association of bill morphology and foraging behaviour in calidrid sandpipers. Animal Biology, 55(3): 235-243. DOI: https://doi.org/10.1163/1570756054472818
Nol, E., Mac Culloch, K., Pollock, L. & McKinnon, L. 2014. Foraging ecology and time budgets of non-breeding shorebirds in coastal Cuba. Journal of Tropical Ecology, 30(4): 347-357. DOI: https://doi.org/10.1017/S0266467414000182
Norazlimi, N.A. & Ramli, R. 2015. The relationships between morphological characteristics and foraging behavior in four selected species of shorebirds and water birds utilizing tropical mudflats. Scientific World Journal, 2015: 105296. DOI: https://doi.org/10.1155/2015/105296
Ntiamoa-Baidu, Y., Piersma, T., Wiersma, P., Poot, M., Battley, P. & Gordon, C. 1998. Water depth selection, daily feeding routines and diets of waterbirds in coastal lagoons in Ghana. Ibis, 140(1): 89-103. DOI: https://doi.org/10.1111/j.1474-919X.1998.tb04545.x
Owens, N. 1984. Why do curlews have curved beaks? Bird Study, 31(3): 230-231. DOI: https://doi.org/10.1080/00063658409476846
Pienkowski, M.W. 1983. Changes in the foraging pattern of plovers in relation to environmental factors. Animal Behaviour, 31(1): 244-264. DOI: https://doi.org/10.1016/S0003-3472(83)80195-X
Piersma, T. 1986. Foraging behaviour of Terek Sandpipers Xenus cinereus feeding on Sand-Bubbling Crabs Scopimera globosa. Journal of Ornithology, 127(4): 475-486. DOI: https://doi.org/10.1007/BF01640262
Pyke, G.H., Pulliam, H.R. & Charnov, E.L. 1977. Optimal foraging: A selective review of theory and tests. The Quarterly Review of Biology, 52(2): 137-154. DOI: https://doi.org/10.1086/409852
R Core Team. 2022. R: A language and environment for statistical computing [Computer software]. The R Project for Statistical Computing. URL http://www.R-project.org/ (assessed 10.10.21)
Ramli, R. & Norazlimi, N.A. 2016. Effects of tidal states and time of day on the abundance and behavior of shorebirds utilizing tropical intertidal environment. Journal of Animal and Plant Sciences, 26(4): 1164-1171.
Risdiana, R. 2015. Maintaining habitat for birds in Bako Buntal Bay [WWW Document]. EAAFP. URL https://www.eaaflyway.net/maintaining-habitat-for-birds-in-bako-buntal-bay-eaaf112-malaysia/ (assessed 12.12.21).
Sánchez, M.I., Green, A.J. & Castellanos, E.M. 2005. Seasonal variation in the diet of Redshank Tringa totanus in the Odiel Marshes, Southwest Spain: A comparison of faecal and pellet analysis. Bird Study, 52(2): 210-216. DOI: https://doi.org/10.1080/00063650509461393
Schneider, D. C. 2017. The food and feeding of migratory shorebirds. Oceanus, 26(1): 38-43.
See, C.M. & Chan, K.S. 2020. Coastal Mangrove Birds of Bagan Datuk, Perak. Malaysian Nature Society, Kuala Lumpur. 70 pp.
Stroud, D.A.A., Baker, D.E., Blanco, N.C., Davidson, S., Delany, B., Ganter, R., Gill, R., Gonzalez, P., Haanstra, L., Morrison, R.I.G., Piersma, T., Scott, D.A., Thorup, O., West, R., Wilson, J. & Zockler, C. 2008. The conservation and population status of the world's waders at the turn of the millennium. In: Conference of Waterbirds around the world, Edinburgh, pp. 643-648.
Touhami, F., Idrissi, H.R. & Benhoussa, A. 2020. Foraging behaviour of wintering shorebirds at Merja Zerga lagoon (Atlantic coast, Morocco). Ostrich, 91(3): 244-251. DOI: https://doi.org/10.2989/00306525.2020.1774439
Turpie, J.K. & Hockey, P.A.R. 2008. Adaptive variation in the foraging behaviour of Grey Plover Pluvialis squatarola and Whimbrel Numenius phaeopus. Ibis, 139(2): 289-298. DOI: https://doi.org/10.1111/j.1474-919X.1997.tb04627.x
Watts, B.D., Smith, F.M. & Truitt, B.R. 2017. Departure patterns of whimbrels using a terminal spring staging area. Wader Study, 124(2): 141-146. DOI: https://doi.org/10.18194/ws.00075
Willems, T., Rabaut, M., Stienen, E. & Degraer, S. 2010. Feeding ecology of shorebirds: Habitat preference and tidal constraints (MSc.). Ghent University.
Wilson, J.R., Nebel, S. & Minton, C.D.T. 2007. Migration ecology and morphometrics of two Bar-tailed Godwit populations in Australia. Emu, 107(4): 262-274. DOI: https://doi.org/10.1071/MU07026
Wilson, K. 2002. A survey of coastal and marine birds at Bako National Park and Samunsam Wildlife Sanctuary, Sarawak. Wildlife Management Report Number 28. The Sarawak Biodiversity Centre, Kuching.
Woodley, K. 2022. Bar-tailed Godwit [WWW Document]. New Zealand Birds Online. URL www.nzbirdsonline.org.nz (assessed 20.12.23)
Zakirah, M.T., Shabdin, M.L., Khairul-Adha, A.R. & Fatimah-A'tirah, M. 2019. Distribution of intertidal flat macrobenthos in Buntal Bay, Sarawak, Borneo. Songklanakarin Journal of Science and Technology, 41(5): 1048-1058.
Zusi, R. L. 2020. Charadriiform. [WWW Document]. Britannica. URL https://www.britannica.com/animal/charadriiform (accessed 12.10.20).
Zwarts L. & Dirksen, S. 1990. Digestive bottleneck limits the increase in food intake of Whimbrels preparing for spring migration from the Banc d'Arguin, Mauritania. Ardea, 78:257-258.
Zwarts, L. & Wanink, J. H. 1993. How the food supply harvestable by waders in the wadden sea depends on the variation in energy density, body weight, biomass, burying depth and behaviour of tidal-flat invertebrates. Netherlands Journal of Sea Research, 31(4): 441-476. DOI: https://doi.org/10.1016/0077-7579(93)90059-2
Zwarts, L. 1985. The winter exploitation of fiddler crabs Uca tangeri by waders in Guinea- Bissau. Ardea, 73(1985): 3-12.
Zweers, G. & Gerritsen, A.F.C. 1997. Transition from pecking to probing mechanisms in waders. Netherlands Journal of Zoology, 47(2): 161-208. DOI: https://doi.org/10.1163/156854297X00166
Zweers, G.A. 1991. Transformation of avian feeding mechanisms: a deductive method. Acta Biotheoretica, 29: 15-36. DOI: https://doi.org/10.1007/BF00046405
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Universiti Malaysia Sarawak
Grant numbers F07/SpMYRA/1710/2018