Skip to main content
SpringerLink
Log in

Ontogenetic Dietary Shift in Megabenthic Predatory Elasmobranchs of a Tropical Estuarine Bay

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Elasmobranchs play a significant role in structuring the marine food webs in many marine habitats. Estuaries provide an essential habitat primarily as nurseries for elasmobranchs. The present study investigates the feeding preferences of megabenthic predatory elasmobranchs from Caranzalem Bay, Goa. The elasmobranchs in this habitat were represented by guitarfishes, Glaucostegus granulatus and Glaucostegus obtusus; rays, Brevitrygon walga, Pastinachus sephen, Neotrygon kuhlii, and Maculabatis gerrardi; and bamboo sharks, Chiloscyllium griseum and Chiloscyllium spp. Crustaceans were the major prey of these predators followed by teleosts and cephalopods. The bamboo shark was an opportunistic predator while rays and guitarfish were specialised feeders on penaeid shrimps. Indices suggest that bamboo sharks occupy the highest trophic level in this benthic food chain while guitarfishes and rays function as mesopredators. Ontogenetic dietary changes were observed in all predators, indicating the feeding niche segregation among size classes. Low resource overlap was observed between and within species probably due to high prey availability in the bay. These elasmobranch species frequently occur in bycatch, which can negatively affect their populations and thereby impact the lower trophic strata resulting in large-scale ecological repercussions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ajemian, M.J., and S.P. Powers. 2012. Habitat-specific feeding by cownose rays (Rhinoptera bonasus) of the northern Gulf of Mexico. Environmental Biology of Fishes 95 (1): 79–97.

    Article  Google Scholar 

  • Annon. 2017. https://www.prokerala.com/news/photos//fishermen-gather-fish-at-caranzalem-beach-283740.html. Accessed 07 Dec 2021.

  • Annon. 2018. https://www.indiacontent.in/caranzalem--fishermen-gather-fish-from-the-bumper-catch-found-through-their-traditional-method-of-fishing-called-raampon-at-caranzalem-beach--in-goa-on-july-30--2018--photo--ians-/pr-701079/. Accessed 07 Dec 2021.

  • Annon. 2019. https://www.goa365.tv/general/N/ramponkars-get-bumper-catch-of-variety-fish/07758.html. Accessed 07 Dec 2021.

  • Annon. 2020a. https://www.goaprism.com/local-ramponkars-delighted-with-bumper-catch-over-the-long-weekend/. Accessed 07 Dec 2021.

  • Annon. 2020b. https://www.heraldgoa.in/Videos/First-bumper-fish-catch-at-Caranzalem-beach-people-flock-to-buy-fresh-fish/164859. Accessed 07 Dec 2021.

  • Annon. 2021a. https://www.youtube.com/watch?v=LaaHAU0acvM. Accessed 07 Dec 2021.

  • Annon. 2021b. https://www.youtube.com/watch?v=T6YY64C2YHo. Accessed 07 Dec 2021.

  • Ansari, Z.A., A. Chatterji, B.S. Ingole, R.A. Sreepada, C.U. Rivonkar, and A.H. Parulekar. 1995. Community structure and seasonal variation of an inshore demersal fish community at Goa, west coast of India. Estuarine, Coastal and Shelf Science 41 (5): 593–610.

    Article  Google Scholar 

  • Barbini, S.A., and L.O. Lucifora. 2012. Ontogenetic diet shifts and food partitioning between two small sympatric skates (Chondrichthyes, Rajidae) in the Southwestern Atlantic. Marine and Freshwater Research 63 (10): 905–913.

    Article  Google Scholar 

  • Barbini, S.A., L.B. Scenna, D.E. Figueroa, M.B. Cousseau, and J.M. Díaz de Astarloa. 2010. Feeding habits of the Magellan skate: Effects of sex, maturity stage, and body size on diet. Hydrobiologia 641 (1): 275–286.

    Article  Google Scholar 

  • Barbini, S.A., D.E. Sabadin, and L.O. Lucifora. 2018. Comparative analysis of feeding habits and dietary niche breadth in skates: The importance of body size, snout length, and depth. Reviews in Fish Biology and Fisheries 28 (3): 625–636.

    Article  Google Scholar 

  • Baum, J.K., and B. Worm. 2009. Cascading top-down effects of changing oceanic predator abundances. Journal of Animal Ecology 78 (4): 699–714.

    Article  Google Scholar 

  • Belleggia, M., C. Battagliotti, F. Cortés, and J.H. Colonello. 2019. Feeding together: A global diet analysis of twenty-three species of Chondrichthyes on a feeding ground area. Hydrobiologia 842 (1): 77–99.

    Article  CAS  Google Scholar 

  • Bengil, F., E.G. Bengil, S. Mavruk, O. Heral, O.D. Karaman, and Ozaydin, O. 2019. Feeding ecology of four demersal shark species (Etmopterus spinax, Galeus melastomus, Scyliorhinus canicula and Squalus blainville) from the eastern Aegean Sea.

  • Bonfil, R. (1994). Overview of world elasmobranch fisheries (No. 341). Food and Agriculture Org.

  • Bornatowski, H., A.F. Navia, R.R. Braga, V. Abilhoa, and M.F.M. Corrêa. 2014. Ecological importance of sharks and rays in a structural food web analysis in southern Brazil. ICES Journal of Marine Science 71 (7): 1586–1592.

    Article  Google Scholar 

  • Borrell, A., L. Cardona, R.P. Kumarran, and A. Aguilar. 2011. Trophic ecology of elasmobranchs caught off Gujarat, India, as inferred from stable isotopes. ICES Journal of Marine Science 68 (3): 547–554.

    Article  Google Scholar 

  • Camhi, M. 1998. Sharks and their relatives: ecology and conservation (No. 20). IUCN.

  • Clarke, K.R., and R.N. Gorley. 2001. Primer v5: user manual/tutorial, primer e: Plymouth. Plymouth Marine Laboratory, Plymouth, UK.

  • CMFRI, F. 2020. Marine Fish Landings in India-2019.

  • Cortés, E. 1999. Standardized diet compositions and trophic levels of sharks. ICES Journal of Marine Science 56 (5): 707–717.

    Article  Google Scholar 

  • Dale, J.J., N.J. Wallsgrove, B.N. Popp, and K.N. Holland. 2011. Nursery habitat use and foraging ecology of the brown stingray Dasyatis lata determined from stomach contents, bulk, and amino acid stable isotopes. Marine Ecology Progress Series 433: 221–236.

    Article  Google Scholar 

  • Dean, M.N., C.D. Wilga, and A.P. Summers. 2005. Eating without hands or tongue: Specialization, elaboration and the evolution of prey processing mechanisms in cartilaginous fishes. Biology Letters 1 (3): 357–361.

    Article  Google Scholar 

  • Dean, M.N., J.J. Bizzarro, B. Clark, C.J. Underwood, and Z. Johanson. 2017. Large batoid fishes frequently consume stingrays despite skeletal damage. Royal Society Open Science 4 (9): 170674.

    Article  Google Scholar 

  • Ebert, D. 2003. Sharks, rays, and chimeras of California (No. 71). Univ of California Press.

  • Ebert, D.A., and J.J. Bizzarro. 2007. Standardized diet compositions and trophic levels of skates (Chondrichthyes: Rajiformes: Rajoidei). In Biology of Skates (pp. 115–131). Springer, Dordrecht.

  • Ebert, D.A., and P.D. Cowley. 2003. Diet, feeding behavior and habitat utilisation of the blue stingray Dasyatis chrysonota (Smith, 1828) in South African waters. Marine and Freshwater Research 54 (8): 957–965.

    Article  Google Scholar 

  • Egeberg, C.A., R.M. Kempster, S.M. Theiss, N.S. Hart, and S.P. Collin. 2014. The distribution and abundance of electrosensory pores in two benthic sharks: A comparison of the wobbegong shark, Orectolobus maculatus, and the angel shark. Squatina Australis. Marine and Freshwater Research 65 (11): 1003–1008.

    Article  Google Scholar 

  • Elston, C., P.D. Cowley, R.G. von Brandis, and J. Lea. 2021. Residency and habitat use patterns by sympatric stingrays at a remote atoll in the Western Indian Ocean. Marine Ecology Progress Series 662: 97–114.

    Article  CAS  Google Scholar 

  • Every, S.L., C.J. Fulton, H.R. Pethybridge, P.M. Kyne, and D.A. Crook. 2019. A seasonally dynamic estuarine ecosystem provides a diverse prey base for Elasmobranchs. Estuaries and Coasts 42 (2): 580–595.

    Article  CAS  Google Scholar 

  • Flowers, K.I., M.R. Heithaus, and Y.P. Papastamatiou. 2021. Buried in the sand: Uncovering the ecological roles and importance of rays. Fish and Fisheries 22 (1): 105–127.

    Article  Google Scholar 

  • Frisch, A.J., M. Ireland, J.R. Rizzari, O.M. Lönnstedt, K.A. Magnenat, C.E. Mirbach, and J.P.A. Hobbs. 2016. Reassessing the trophic role of reef sharks as apex predators on coral reefs. Coral Reefs 35 (2): 459–472.

    Article  Google Scholar 

  • Froese, R., and D. Pauly. 2021. Editors. FishBase. World Wide Web electronic publication. www.fishbase.org, version (08/2021).

  • George, R., K.R. Muraleedharan, G.D. Martin, P. Sabu, V.J. Gerson, P.K. Dineshkumar, and K.K.C. Nair. 2013. Nutrient biogeochemistry of the eastern Arabian Sea during the southwest monsoon retreat. Environmental Earth Sciences 68 (3): 703–718.

    Article  CAS  Google Scholar 

  • Guillory, V. 1993. Ghost fishing by blue crab traps. North American Journal of Fisheries Management 13 (3): 459–466.

    Article  Google Scholar 

  • Gupta, T., H. Booth, W. Arlidge, C. Rao, M. Manoharakrishnan, N. Namboothri, and E.J. Milner-Gulland. 2020. Mitigation of elasmobranch bycatch in trawlers: A case study in Indian fisheries. Frontiers in Marine Science 7: 571.

    Article  Google Scholar 

  • Hajisamae, S., L.M. Chou, and S. Ibrahim. 2004. Feeding habits and trophic relationships of fishes utilizing an impacted coastal habitat. Singapore. Hydrobiologia 520 (1): 61–71.

    Article  Google Scholar 

  • Haque, A.B., R.D. Cavanagh, and N. Seddon. 2021. Evaluating artisanal fishing of globally threatened sharks and rays in the Bay of Bengal. Bangladesh. Plos One 16 (9): e0256146.

    Article  CAS  Google Scholar 

  • Hegde, M.R., V.P. Padate, and C.U. Rivonker. 2014. Biological aspects and catch trends of elasmobranchs in the inshore waters of Goa, West Coast of India.

  • Heithaus, M.R., T. Alcoverro, R. Arthur, D.A. Burkholder, K.A. Coates, M.J. Christianen, and J.W. Fourqurean. 2014. Seagrasses in the age of sea turtle conservation and shark overfishing. Frontiers in Marine Science 1: 28.

  • Heupel, M.R., D.M. Knip, C.A. Simpfendorfer, and N.K. Dulvy. 2014. Sizing up the ecological role of sharks as predators. Marine Ecology Progress Series 495: 291–298.

    Article  Google Scholar 

  • Horn, P.L. 2016. Biology of the New Zealand carpet shark Cephaloscyllium isabellum (Scyliorhinidae). Journal of Ichthyology 56 (3): 336–347.

    Article  Google Scholar 

  • Kimber, J.A., D.W. Sims, P.H. Bellamy, and A.B. Gill. 2014. Elasmobranch cognitive ability: Using electroreceptive foraging behaviour to demonstrate learning, habituation and memory in a benthic shark. Animal Cognition 17 (1): 55–65.

    Article  Google Scholar 

  • Krebs, C.J. 1999. Ecological methodology (No. 574.5072 K7).

  • Liao, H., C.L. Pierce, and J.G. Larscheid. 2001. Empirical assessment of indices of prey importance in the diets of predacious fish. Transactions of the American Fisheries Society 130 (4): 583–591.

    Article  Google Scholar 

  • Liu, K.M., Y.H. Lin, S.K. Chang, S.J. Joung, and K.Y. Su. 2020. Examining an ontogenetic shift in the diet of the whitespotted bamboo shark Chiloscyllium plagiosum in northern Taiwanese waters. Regional Studies in Marine Science 35: 101234.

    Article  Google Scholar 

  • McCurdy, D.G., M.R. Forbes, S.P. Logan, D. Lancaster, and S.I. Mautner. 2005. Foraging and impacts by benthic fish on the intertidal amphipod Corophium volutator. Journal of Crustacean Biology 25 (4): 558–564.

    Article  Google Scholar 

  • Menon, M., G. Maheswarudu, K.S. Ramulu, and S.J. Kizhakudan. 2020. Reproductive biology and diet of the longtail butterfly ray Gymnura poecilura (Shaw, 1804) along western Bay of Bengal. Journal of the Marine Biological Association of the United Kingdom 100 (3): 461–470.

    Article  Google Scholar 

  • Moss, S. 1977. Feeding mechanisms in sharks. American Zoologist 17 (2): 355–364.

    Article  Google Scholar 

  • Mulas, A., A. Bellodi, R. Cannas, P. Carbonara, A. Cau, M.F. Marongiu, and M.C. Follesa. 2019. Resource partitioning among sympatric elasmobranchs in the central-western Mediterranean continental shelf. Marine Biology 166 (12): 1–16.

    Article  Google Scholar 

  • Navia, A.F., P.A. Mejía-Falla, and A. Giraldo. 2007. Feeding ecology of elasmobranch fishes in coastal waters of the Colombian Eastern Tropical Pacific. BMC Ecology 7 (1): 1–10.

    Article  Google Scholar 

  • Navia, A.F., P.A. Mejía-Falla, J. López-García, A. Giraldo, and V.H. Cruz-Escalona. 2017. How many trophic roles can elasmobranchs play in a marine tropical network? Marine and Freshwater Research 68 (7): 1342–1353.

    Article  Google Scholar 

  • Nur Farhana, A., A. Samat. C.C. Zaidi, and A.G. Mazlan. 2013. Stomach content and trophic level position of two bamboo shark species Chiloscyllium indicum and C. hasseltii (Hemiscylliidae) from south eastern waters of Peninsular Malaysia. Journal of Sustainability Science and Management (Malaysia) 8 (1): 113–120.

  • O’Shea, O.R., M. Thums, M. Van Keulen, R.M. Kempster, and M.G. Meekan. 2013. Dietary partitioning by five sympatric species of stingray (Dasyatidae) on coral reefs. Journal of Fish Biology 82 (6): 1805–1820.

    Article  Google Scholar 

  • Platell, M.E., I.C. Potter, and K.R. Clarke. 1998. Resource partitioning by four species of elasmobranchs (Batoidea: Urolophidae) in coastal waters of temperate Australia. Marine Biology 131 (4): 719–734.

    Article  Google Scholar 

  • Plumlee, J.D., K.M. Dance, P. Matich, J.A. Mohan, T.M. Richards, T.C. TinHan, and R.D. Wells. 2018. Community structure of elasmobranchs in estuaries along the northwest Gulf of Mexico. Estuarine, Coastal and Shelf Science 204: 103–113.

    Article  Google Scholar 

  • Raje, S.G., G. Mathew, K.K. Joshi, R.J. Nair, G. Mohanraj, M. Srinath, and N. Rudramurthy. 2002. Elasmobranch fisheries of India-an appraisal. CMFRI Special Publication 71: 1–76.

    Google Scholar 

  • Rastgoo, A.R., and J. Navarro. 2017. Trophic levels of teleost and elasmobranch species in the Persian Gulf and Oman Sea. Journal of Applied Ichthyology 33 (3): 403–408.

    Article  Google Scholar 

  • Rastgoo, A.R., S.M.R. Fatemi, T. Valinassab, and M.S. Mortazavi. 2018. Feeding habits and trophic level of Himantura gerrardi (Elasmobranchii; Dasyatidae) in northern Oman Sea: Effects of sex and size class. Iranian Journal of Fisheries Sciences. 17 (1): 137–150.

    Google Scholar 

  • Roff, G., C. Doropoulos, A. Rogers, Y.M. Bozec, N.C. Krueck, E. Aurellado, and P.J. Mumby. 2016. The ecological role of sharks on coral reefs. Trends in Ecology and Evolution 31 (5): 395–407.

    Article  Google Scholar 

  • Shaw, A.L., B.S. Frazier, J.R. Kucklick, and G. Sancho. 2016. Trophic ecology of a predatory community in a shallow-water, high-salinity estuary assessed by stable isotope analysis. Marine and Coastal Fisheries 8 (1): 46–61.

    Article  Google Scholar 

  • Sherman, C.S., M.R. Heupel, S.K. Moore, A. Chin, and C.A. Simpfendorfer. 2020. When sharks are away, rays will play: Effects of top predator removal in coral reef ecosystems. Marine Ecology Progress Series 641: 145–157.

    Article  Google Scholar 

  • Sreekanth, G.B., A.K. Jaiswar, H.B. Shivkumar, B. Manikandan, and E.B. Chakurkar. 2020. Fish composition and assemblage structure in tropical monsoonal estuaries: Estuarine use and feeding guild approach. Estuarine, Coastal and Shelf Science 244: 106911.

    Article  Google Scholar 

  • Sreekanth, G.B., A.K. Jaiswar, and K.V. Akhliesh. 2021a. Feeding ecology of giant guitarfish, Glaucostegus cf. granulatus (Glaucostegidae: Rhinopristiformes) from Eastern Arabian Sea. National Academy Science Letters 1–6 (a).

  • Sreekanth, G.B., T.S. Mayekar, A. Giriyan, F. D’souza, S. Dourado, B. Ingole, and E.B. Chakurkar. 2021b. Inventory of fishery resources using participatory research approach in Mandovi Estuary in Central western coast of India. Journal of Environmental Biology 42 (5): 1257–1263(b).

  • Stevens, J.D., R. Bonfil, N.K. Dulvy, and P.A. Walker. 2000. The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57 (3): 476–494.

    Article  Google Scholar 

  • Sukhsangchana, C., S. Phuynoia, Y. Monthuma, N. Whanpetcha, and N. Kulanujareeb. 2020. Catch composition and estimated economic impacts of ghost-fishing squid traps near Suan Son Beach, Rayong province. Thailand. SCIENCEASIA 46 (1): 87–92.

    Article  Google Scholar 

  • Swift, D.G., and D.S. Portnoy. 2021. Identification and delineation of essential habitat for elasmobranchs in estuaries on the Texas coast. Estuaries and Coasts 44 (3): 788–800.

    Article  CAS  Google Scholar 

  • Tamaki, A., K. Harada, Y. Sogawa, and S. Takeuchi. 2020. Effect of stingray (Hemitrygon akajei) foraging on a ghost shrimp population (Nihonotrypaea harmandi) on an intertidal sandflat, western Kyushu. Japan. Marine and Freshwater Research 71 (9): 1128–1148.

    Article  Google Scholar 

  • Tambre, G., S. Mote, K. De, D. Yogi, M. Jadhav, B. Ingole, and M. Nanajkar. 2020. By-catch mortality of beaked sea snake Hydrophis schistosus (Daudin, 1803) by entanglement in shore-seine operation in Goa-India. Acta Biologica 27: 67–76.

    Article  Google Scholar 

  • Tobin, A.J., A. Mapleston, A.V. Harry, and M. Espinoza. 2014. Big fish in shallow water; use of an intertidal surf-zone habitat by large-bodied teleosts and elasmobranchs in tropical northern Australia. Environmental Biology of Fishes 97 (7): 821–838.

    Article  Google Scholar 

  • Uhlmann, S.S., and M.K. Broadhurst. 2015. Mitigating unaccounted fishing mortality from gillnets and traps. Fish and Fisheries 16 (2): 183–229.

    Article  Google Scholar 

  • Valenzuela-Quiñonez, F., F. Galván-Magaña, D.A. Ebert, and E.A. Aragón-Noriega. 2018. Feeding habits and trophic level of the shovelnose guitarfish (Pseudobatos productus) in the upper Gulf of California. Journal of the Marine Biological Association of the United Kingdom 98 (7): 1783–1792.

    Article  Google Scholar 

  • Vaudo, J.J., and M.R. Heithaus. 2009. Spatiotemporal variability in a sandflat elasmobranch fauna in Shark Bay. Australia. Marine Biology 156 (12): 2579–2590.

    Article  Google Scholar 

  • Vaudo, J.J., and M.R. Heithaus. 2011. Dietary niche overlap in a nearshore elasmobranch mesopredator community. Marine Ecology Progress Series 425: 247–260.

    Article  Google Scholar 

  • Velip, D.T., and C.U. Rivonker. 2018. Trophic dynamics of few selected nearshore coastal finfishes with emphasis on prawns as prey item. Journal of Sea Research 136: 28–36.

    Article  Google Scholar 

  • Wheeler, C.R., C.R. Gervais, M.S. Johnson, S. Vance, R. Rosa, J.W. Mandelman, and J.L. Rummer. 2020. Anthropogenic stressors influence reproduction and development in elasmobranch fishes. Reviews in Fish Biology and Fisheries 30 (2): 373–386.

    Article  Google Scholar 

  • Wilga, C.D., P.J. Motta, and C.P. Sanford. 2007. Evolution and ecology of feeding in elasmobranchs. Integrative and Comparative Biology 47 (1): 55–69.

    Article  Google Scholar 

  • WoRMS Editorial Board. 2021. World Register of Marine Species. Available from https://www.marinespecies.org at VLIZ. Accessed 08 Dec 2021. https://doi.org/10.14284/170.

Download references

Acknowledgements

This study is part of doctoral work of the first author. The first author acknowledges the CSIR fellowship (Award Letter No. 1061730943) for doctoral research programme (CSIR-NIO contribution no.: 6978).

Author information

Authors and Affiliations

  1. CSIR-National Institute of Oceanography, Dona Paula, Panaji, Goa, 403004, India

    Deepa Shashikant Yogi, Akshay Naik, Prema Piyusha Panda, Ranjana Yadav, Aniket Desai & Mandar Nanajkar

  2. Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, 201002, India

    Deepa Shashikant Yogi, Ranjana Yadav, Aniket Desai & Mandar Nanajkar

Authors
  1. Deepa Shashikant Yogi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Akshay Naik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Prema Piyusha Panda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ranjana Yadav
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aniket Desai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mandar Nanajkar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

DY: sampling, analysis, conceptualization and writing; AN, PP, RY, AD: sampling and analysis; MN: conceptualization and writing.

Corresponding author

Correspondence to Mandar Nanajkar.

Ethics declarations

Competing Interests

The authors declare no competing interests.

Additional information

Communicated by Jill A. Olin.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yogi, D., Naik, A., Panda, P.P. et al. Ontogenetic Dietary Shift in Megabenthic Predatory Elasmobranchs of a Tropical Estuarine Bay. Estuaries and Coasts 46, 279–291 (2023). https://doi.org/10.1007/s12237-022-01130-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-022-01130-5

Keywords

Search

Navigation