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Feeding ecology of three sympatric species of stingrays on a tropical mudflat

Published online by Cambridge University Press:  02 October 2018

Kean Chong Lim ,
Ving Ching Chong ,
Phaik-Eem Lim ,
Tatsuya Yurimoto  and
Kar Hoe Loh
Kean Chong Lim
Affiliation:
Institute of Biological Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia
Ving Ching Chong*
Affiliation:
Institute of Biological Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia
Phaik-Eem Lim
Affiliation:
Institute of Biological Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia Institute of Ocean and Earth Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia
Tatsuya Yurimoto
Affiliation:
Japan International Research Center for Agricultural Sciences, 1-1 Ohwashi, Tsukuba, Ibaraki, 305-8686, Japan
Kar Hoe Loh
Affiliation:
Institute of Ocean and Earth Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia
*
Author for correspondence: V.C. Chong, E-mail: chong@um.edu.my
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Abstract

Periodic fish ingressions into intertidal areas during high tide are known to occur on tropical mudflats. This study aimed to elucidate the feeding ground function of coastal mudflats for three common stingray species in the Klang Strait, Malaysia. Stingrays (disc width range from 5.65–54.50 cm) sampled over 17 months using a large barrier net (~2 ha enclosure) at two sampling sites were examined for their diet composition, prey frequency and prey volume according to predator species and maturity. The index of relative importance and Schoener's index of diet overlap were calculated. The three stingray species fed on relatively similar prey items which varied in size and contribution. Brevitrygon heterura fed on the widest range of prey taxa (28) whereas Hemitrygon bennetti (22) and Telatrygon biasa (17) showed higher prey specialization. The Penaeidae (dominantly Metapenaeus brevicornis and M. affinis) were the most important food item in the stingray diet which also included Actinopterygii, Amphipoda, Brachyura and Calanoida. The stingray diet showed an ontogenetic shift, with young stingrays tending to be generalists whereas the more mature stingrays (except H. bennetti) become more specialized in their feeding habits. This shift in feeding strategy reflects the diversity of prey taxa abundantly available to young stingrays on the mudflats, while the larger stingrays adapt to feed on larger prey once they enter deeper waters.

Keywords

Diet overlapfeeding groundfeeding habitsmudflatMyliobatiformesontogenetic shift
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 4 , June 2019 , pp. 999 - 1007
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

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References

Ajemian, MJ and Powers, SP (2012) Habitat-specific feeding by cownose rays (Rhinoptera bonasus) of the northern Gulf of Mexico. Environmental Biology of Fishes 95, 79–97.Google Scholar
Alongi, DM (2009) The Energetics of Mangrove Forests. New York, NY: Springer.Google Scholar
Amundsen, PA, Gabler, HM and Staldvik, FJ (1996) A new approach to graphical analysis of feeding strategy from stomach contents data-modification of the Costello (1990) method. Journal of Fish Biology 48, 607–614.Google Scholar
Backwell, PRY, O'Hara, PD and Christy, JH (1998) Prey availability and selective foraging in shorebirds. Animal Behaviour 55, 1659–1667.Google Scholar
Bangley, CW and Rulifson, RA (2017) Habitat partitioning and diurnal-nocturnal transition in the elasmobranch community of a North Carolina estuary. Bulletin of Marine Science 93, 319–338.Google Scholar
Beck, MW, Heck, KL, Able, KW, Childers, DL, Eggleston, DB, Gillanders, BM, Halpern, B, Hays, CG, Hoshino, K, Minello, TJ, Orth, RJ, Sheridan, PF and Weinstein, MP (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. BioScience 51, 633–641.Google Scholar
Blaber, SJM, Dichmont, CM, White, W, Buckworth, R, Sadiyah, L, Nurhakim, S, Pillans, R, Andamari, R, Dharmadi, and Fahmi, (2009) Elasmobranchs in southern Indonesian fisheries: the fisheries, the status of the stocks and management options. Reviews in Fish Biology and Fisheries 19, 367–391.Google Scholar
Bornatowski, H, Natascha, W, Carmo, WPD, Corrêa, MFM and Abilhoa, V (2014) Feeding comparisons of four batoids (Elasmobranchii) in coastal waters of southern Brazil. Journal of the Marine Biological Association of the United Kingdom 1, 1–9.Google Scholar
Broom, MJ (1982) Structure and seasonality in a Malaysian mudflat community. Estuarine, Coastal and Shelf Science 15, 135–150.Google Scholar
Burger, J, Niles, L and Clark, KE (1997) Importance of beach, mudflat and marsh habitats to migrant shorebirds on Delaware Bay. Biology Conservation 79, 283–292.Google Scholar
Carlson, JK, Goldman, KJ and Lowe, CG (2004) Metabolism, energetic demand, and endothermy. In Carrier, JC, Musick, JA and Heithaus, MR (eds) Biology of Sharks and Their Relatives. Boca Raton: CRC Press, pp. 203–224.Google Scholar
Cerutti-Pereyra, F, Thums, M, Austin, CM, Bradshaw, CJA, Stevens, JD, Babcock, RC, Pillans, RD and Meekan, MG (2014) Restricted movements of juvenile rays in the lagoon of Ningaloo Reef, Western Australia – evidence for the existence of a nursery. Environmental Biology of Fishes 97, 371–383.Google Scholar
Chong, VC (1977) Studies on the small grey mullet Liza malinoptera (Valenciennes). Journal of Fish Biology 11, 293–308.Google Scholar
Chong, VC, Sasekumar, A, Leh, MUC and Cruz, RD (1990) The fish and prawn communities of a Malaysian coastal mangrove system, with comparisons to adjacent mudflats and inshore waters. Estuarine, Coastal and Shelf Science 31, 703–722.Google Scholar
Chong, VC, Teoh, HW, Ooi, AL, Jamizan, AR and Tanaka, K (2012) Ingression and feeding habits of fish in Matang coastal mudflats, Malaysia. JIRCAS Working Report 75, 15–24.Google Scholar
Clarke, KR and Gorley, RN (2006) PRIMER V6: User Manual/Tutorial. Plymouth: PRIMER-E.Google Scholar
Corcoran, MJ, Wetherbee, BM, Shivji, MS, Potenski, MD, Chapman, DD and Harvey, GM (2013) Supplemental feeding for ecotourism reverses diel activity and alters movement patterns and spatial distribution of the southern stingray, Dasyatis americana. PLoS ONE 8, e59235.Google Scholar
Cortés, E (1997) A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 54, 726–738.Google Scholar
Ebert, DA and Cowley, PD (2003) Diet, feeding behavior and habitat utilization of the blue stingray Dasyatis chrysonata (Smith, 1828) in South African waters. Marine and Freshwater Research 54, 957–965.Google Scholar
Eschmeyer, WN and Fong, JD (2015) Species by Family/Subfamily in Catalog of Fishes. California Academy of Sciences. Available at http://researcharchive.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp.Google Scholar
Forman, JS and Dunn, MR (2012) Diet and scavenging habits of the smooth skate Dipturus innominatus. Journal of Fish Biology 80, 1546–1562.Google Scholar
Hyslop, EJ (1980) Stomach contents analysis – a review of methods and their application. Journal of Fish Biology 17, 411–429.Google Scholar
Ismen, A (2003) Age, growth, reproduction and food of common stingray (Dasyatis pastinaca L., 1758) in Iskenderun Bay, the eastern Mediterranean. Fisheries Research 60, 169–176.Google Scholar
Jacobsen, IP and Bennett, MB (2011) Life history of the blackspotted whipray Himantura astra. Journal of Fish Biology 78, 1249–1268.Google Scholar
Jacobsen, IP and Bennett, MB (2012) Feeding ecology and dietary comparisons among three sympatric Neotrygon (Myliobatoidei: Dasyatidae) species. Journal of Fish Biology 80, 1580–1594.Google Scholar
Jacobsen, IP and Bennett, MB (2013) A comparative analysis of feeding and trophic level ecology in stingrays (Rajiformes; Myliobatoidei) and electric rays (Rajiformes: Torpedinoidei). PLoS ONE 8, e71348.Google Scholar
Kao, TC, Wong, LW and Chin, CT (1998) Land reclamation in South East Asia. Proceedings of 13th Southeast Asian Geotechnical Conference, pp. 137–144.Google Scholar
Kolmann, MA, Crofts, SB, Dean, MN, Summers, AP and Lovejoy, NR (2015) Morphology does not predict performance: jaw curvature and prey crushing in durophagous stingrays. Journal of Experimental Biology 218, 3941–3949.Google Scholar
Łabuz, TA (2015) Environmental impacts—coastal erosion and coastline changes. In The BACC II Author Team (eds), Second Assessment of Climate Change for the Baltic Sea Basin. Berlin: Springer, pp. 381–396.Google Scholar
Laptikhovsky, VV, Arkhipkin, AI and Henderson, AC (2001) Feeding habits and dietary overlap in spiny dogfish Squalus acanthias (Squalidae) and narrowmouth catshark Schroederichthys bivius (Scyliorhinidae). Journal of the Marine Biological Association of the United Kingdom 85, 1015–1018.Google Scholar
Last, PR, White, WT, Caira, JN, Dharmadi, , Fahmi, , Jensen, K, Lim, APK, Manjaji-Matsumoto, BM, Naylor, GJP, Pogonoski, JJ, Stevens, JD and Yearsley, GK (2010) Sharks and Rays of Borneo. Hobart: CSIRO Marine and Atmospheric Research.Google Scholar
Last, PR, White, W, de Carvalho, M, Séret, B, Stehmann, M and Naylor, G (2016) Rays of the World. Ithaca, NY: Cornell University Press.10.1071/9780643109148Google Scholar
Lee, SL, Chong, VC and Yurimoto, T (2016) Ichthyofauna on a tropical mudflat: implications of spatial and temporal variability in assemblage structure and abundance. Estuaries and Coasts 39, 1543–1560.Google Scholar
Leh, MU and Sasekumar, A (1984) Feeding ecology of prawns in shallow waters adjoining mangrove shores. In Soepadmo, E, Raol, AN and Macintosh, DJ (eds), Proceedings of the Asian Symposium on Mangrove Environmental Research and Management. Kuala Lumpur: University of Malaya, pp. 331–353.Google Scholar
Leh, MUC, Sasekumar, A and Chew, LL (2012) Feeding biology of eel catfish Plotosus canius Hamilton in a Malaysian mangrove estuary and mudflat. Raffles Bulletin of Zoology 60, 551–557.Google Scholar
Lim, KC (2016) Taxonomy of dasyatid stingrays (Myliobatiformes) and a study of their nearshore ecology in Selangor (Malaysia). MSc Thesis, Universiti Malaya, Kuala Lumpur, Malaysia.Google Scholar
Lim, KC, Chong, VC, Lim, PE and Yurimoto, T (2014) Length-weight relationship of stingrays in Kuala Selangor, Malaysia. Journal of Applied Ichthyology 30, 1096–1098.Google Scholar
López-García, J, Navia, AF, Mejía-Falla, PA and Rubio, EA (2012) Feeding habits and trophic ecology of Dasyatis longa (Elasmobranchii: Myliobatiformes): sexual, temporal and ontogenetic effects. Journal of Fish Biology 80, 1563–1579.Google Scholar
Marsitah, I and Chong, VC (2002) Population and feeding ecology of Parapenaeopsis sculptilis (Heller, 1862) in Klang Strait, Peninsular Malaysia. Malaysian Journal of Science 21, 61–68.Google Scholar
Navarro-González, JA, Bohórquez-Herrera, J, Navia, AF and Cruz-Escalona, VH (2012) Diet composition of batoids on the continental shelf off Nayarit and Sinaloa, Mexico. Ciencias Marinas 38, 347–362.Google Scholar
Navia, AF, Mejia-Falla, PA and Giraldo, A (2007) Feeding ecology of elasmobranch fishes in coastal waters of the Colombian Eastern Tropical Pacific. BMC Ecology 7, 1–8.Google Scholar
Navia, AF, Torres, A, Mejía-Falla, PA and Giraldo, A (2011) Sexual, ontogenetic, temporal and spatial effects on the diet of Urotrygon rogersi (Elasmobranchii: Myliobatiformes). Journal of Fish Biology 78, 1213–1224.Google Scholar
Ng, PKL (1998). Crabs. In Carpenter, KE and Niem, VH (eds), The Living Marine Resources of the Western Central Pacific. Volume 2: Cephalopods, Crustaceans, Holothurians and Sharks. Rome: FAO, pp. 1046–1155.Google Scholar
Ong, TL and Sasekumar, A (1984) The trophic relationship of the fishes in the shallow waters adjoining a mangrove shore. In Soepadmo, E, Rao, AN and Macintosh, DJ (eds) Proceedings of the Asian Symposium on Mangrove Environment: Research and Development. Kuala Lumpur: University of Malaya & UNESCO; Ardyas Press, pp. 453–469.Google Scholar
O'Shea, OR, Thums, M, van Keulen, M, Kempster, RM and Meekan, MG (2013) Dietary partitioning by five sympatric species of stingray (Dasyatidae) on coral reefs. Journal of Fish Biology 82, 1805–1820.Google Scholar
Pardo, SA, Burgess, KB, Teixeira, D and Bennett, MB (2015) Local-scale resource partitioning by stingrays on an intertidal flat. Marine Ecology Progress Series 533, 205–218.Google Scholar
Pinkas, LM, Oliphant, S and Iverson, ILK (1971) Food habits of albacore, bluefin tuna, and bonito in California waters. California Fish Game 152, 1–105.Google Scholar
Raje, SG (2003) Some aspects of biology of four species of rays off Mumbai water. Indian Journal of Fisheries 50, 89–96.Google Scholar
Ramarn, T, Chong, VC and Hanamura, Y (2015) Versatile mysids exploit multiple basal resources: implication of the bentho-pelagic habit in estuarine food webs. Hydrobiologia 743, 37–51.Google Scholar
Rodelli, MR, Gearing, JN, Gearing, PJ, Marshall, N and Sasekumar, A (1984) Stable isotope ratio as a tracer of mangrove carbon in Malaysian ecosystems. Oecologia 61, 326–333.Google Scholar
Ruocco, NL and Lucifora, LO (2016) Ecological singularity of temperate mesopredatory myliobatid rays (Chondrichthyes: Myliobatiformes). Marine and Freshwater Research 68, 1098–1111.10.1071/MF15469Google Scholar
Sasekumar, A, Chong, VC, Leh, MU and Cruz, RD (1992) Mangroves as a habitat for fish and prawns. Hydrobiologia 247, 195–207.Google Scholar
Schoener, TW (1970) Non-synchronous spatial overlap of lizards in patchy habitats. Ecology 51, 408–418.Google Scholar
Shibuya, A and Zuanon, J (2013) Catfishes as prey items of Potamotrygonid stingrays in the Solimões and Negro rivers, Brazilian Amazon. Biota Neotropica 13, 376–379.Google Scholar
Soberón, J and Llorente, J (1993) The use of species accumulation functions for the prediction of species richness. Conservation Biology 7, 480–488.Google Scholar
Tan, LWH and Ng, PKL (1988) A Guide to Seashore Life. Singapore: The Singapore Science Centre.Google Scholar
Tanaka, K and Choo, PS (2000) Influences of nutrient outwelling from the mangrove swamp on the distribution of phytoplankton in the Matang mangrove estuary, Malaysia. Journal of Oceanography 56, 69–78.Google Scholar
Teoh, HW and Chong, VC (2015) Versatile hermit crabs harness multiple-source energy from coastal mudflats: implications for fish production. Aquatic Ecology 49, 43–55.Google Scholar
Teoh, HW, Lee, SL, Chong, VC and Yurimoto, T (2016) Nutrient (N, P, Si) concentration and primary production on a perturbed tropical coastal mudflat. Environmental Earth Sciences 75, 1147.Google Scholar
Treloar, MA, Laurenson, LJB and Stevens, JD (2007) Dietary comparisons of six skate species (Rajidae) in south-eastern Australian waters. Environmental Biology of Fishes 80, 181–196.Google Scholar
Trott, LA and Alongi, DM (1999) Variability in surface water chemistry and phytoplankton biomass in two tropical, tidally dominated mangrove creeks. Marine and Freshwater Research 50, 451–457.Google Scholar
Varghese, SP, Somvanshi, VS and Dalvi, RS (2014) Diet composition, feeding niche partitioning and trophic organisation of large pelagic predatory fishes in the eastern Arabian Sea. Hydrobiologia 736, 99–114.Google Scholar
White, WT and Kyne, PM (2010) The status of chondrichthyan conservation in the Indo-Australasian region. Journal of Fish Biology 76, 2090–2117.Google Scholar
White, WT, Platell, ME and Potter, IC (2001) Relationship between reproductive biology and age composition and growth in Urolophus lobatus (Batoidea: Urolophidae). Marine Biology Research 138, 135–147.Google Scholar
White, WT, Last, PR, Stevens, JD, Yearsley, GK, Fahmi, and Dharmadi, (2006) Economically Important Sharks & Rays. Perth: Australian Centre for International Agricultural Research.Google Scholar
Woodland, RJ, Secor, DH and Wedge, ME (2011) Trophic resource overlap between small elasmobranchs and sympatric teleosts in Mid-Atlantic bight nearshore habitats. Estuaries and Coasts 34, 391–404.Google Scholar
Yokota, L, Goitein, R, Gianeti, MD and Lessa, RTP (2012) Reproductive biology of the smooth butterfly ray Gymnura micrura. Journal of Fish Biology 81, 1315–1326.Google Scholar
Zar, JH (1999) Biostatistical Analysis. Englewood Cliffs, NJ: Prentice Hall.Google Scholar
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