Skip to main content

Advertisement

SpringerLink
Log in

Resource use and the impacts of fisheries on two sympatric sea snake species on the west coast of India

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

We investigated differences in resource use between two sympatric sea snake species from the west coast of India, Hydrophis curtus and H. schistosus, and described the impacts of fishing on the interactions of these species. We compared habitat use, diet, and isotopic niche width between species to determine resource overlap. We then compared trophic overlap of each species with the fisheries in the region and tested the effect of fishing intensity on their isotopic niche width. Hydrophis curtus used deeper habitats than H. schistosus, resulting in increased spatial overlap with fisheries. The two species also had distinct trophic niches and H. curtus prey formed a larger proportion of fishery catch on average than H. schistosus. This greater overlap could make H. curtus more vulnerable to the effects of fisheries. Both species exhibited expansion in short-term and long-term isotopic niche width along a gradient of fishing intensity which may indicate behavioural changes associated with the presence of fisheries. Hydrophis curtus is a trophic generalist, competes with syntopic species and is dominant in most assemblages. However, H. schistosus exhibits higher plasticity in resource use and may have an advantage over H. curtus. Sea snakes play an important role as mesopredators and as intermediate links in coastal marine food webs. Thus, fishing could alter the relative abundance of these mesopredators with cascading effects through coastal food webs.

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
Fig. 5
Fig. 6

Similar content being viewed by others

Availability of data and materials

The data used for this manuscript are available at https://github.com/cheesesnakes/sea-snake-resource-use.

Code availability

All analysis in the current study was conducted in the R statistical software. Code is available at https://github.com/cheesesnakes/sea-snake-resource-use.

References

  • Anderson MJ, Walsh DC (2013) PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol Monogr 83:557–574

    Article  Google Scholar 

  • Bearhop S, Adams CE, Waldron S, Fuller RA, MacLeod H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012

    Article  Google Scholar 

  • Bhathal B, Pauly D (2008) “Fishing down marine food webs” and spatial expansion of coastal fisheries in India, 1950–2000. Fish Res 91:26–34

    Article  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  PubMed  CAS  Google Scholar 

  • Briand MJ, Bonnet X, Goiran C, Guillou G, Letourneur Y (2015) Major sources of organic matter in a complex coral reef lagoon: identification from isotopic signatures (Δ13C and Δ15N). PLoS ONE 10(7):e0131555. https://doi.org/10.1371/journal.pone.0131555

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Briand MJ, Bonnet X, Guillou G, Letourneur Y (2016) Complex food webs in highly diversified coral reefs: insights from δ13C and δ15N stable isotopes. Food Webs 8:12–22. https://doi.org/10.1016/j.fooweb.2016.07.002

    Article  Google Scholar 

  • Brischoux F, Lillywhite HB (2013) Trophic consequences of pelagic life-style in yellow-bellied sea snakes. Mar Ecol Prog Ser 478(May):231–238. https://doi.org/10.3354/meps10177

    Article  Google Scholar 

  • Brischoux F, Bonnet X, Cherel Y, Shine R (2011) Isotopic signatures, foraging habitats and trophic relationships between fish and seasnakes on the coral reefs of New Caledonia. Coral Reefs 30(1):155–165. https://doi.org/10.1007/s00338-010-0680-8

    Article  Google Scholar 

  • Cambiè G, Sánchez-Carnero N, Mingozzi T, Muiño R, Freire J (2013) Identifying and mapping local bycatch hotspots of loggerhead sea turtles using a GIS-based method: implications for conservation. Mar Biol 160:653–665

    Article  Google Scholar 

  • Chao A, Ma KH, Hsieh TC, Chiu CH (2016). SpadeR (Species-richness prediction and diversity estimation in R): an R package in CRAN. Program and User’s Guide also published at http://chao.stat.nthu.edu.tw/blog/software-download/. Accesced 13 Nov 2019

  • DeMaster DP, Trites AW, Clapham P, Mizroch M, Wade P, Small RJ, Ver Hoef J (2006) The sequential megafaunal collapse hypothesis: testing with existing data. Prog Oceanogr 68(2–4):329–342https://doi.org/10.1016/j.pocean.2006.02.007

    Article  Google Scholar 

  • Díaz López B (2018) “Hot deals at sea”: responses of a top predator (Bottlenose dolphin, Tursiops truncatus) to human-induced changes in the coastal ecosystem, Behavioral Ecology, Volume 30, Issue 2, March/April 2019, Pages 291–300, https://doi.org/10.1093/beheco/ary162

  • Dineshbabu AP, Thomas S, Radhakrishnan EV (2010) Bycatch from trawl nets with special reference to its impact on commercial fishery, off Mangalore. Coastal fishery resources of india conservation and sustainable utilisation. Society of Fisheries Technologists, pp 327–334

    Google Scholar 

  • Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JBC, Marquis RJ, Oksanen L, Oksanen T, Paine RT, Pikitch EK, Ripple WJ, Sandin SA, Scheffer M, Schoener TW, Shurin JB, Sinclair ARE, Soulé ME, Virtanen R, Wardle DA (2011) Trophic downgrading of planet earth. Science 333:301–306

    Article  PubMed  CAS  Google Scholar 

  • Fischer W, Bianchi G (1984) FAO identification sheets for fishery purposes. Western Indian Ocean. FAO, Rome

    Google Scholar 

  • Fry GC, Milton DA, Wassenberg TJ (2001) The reproductive biology and diet of sea snake bycatch of prawn trawling in Northern Australia: characteristics important for assessing the impacts on populations. Pac Conserv Biol 7:55–73

    Article  Google Scholar 

  • Glodek GS, Voris HK (1982) Marine snake diets: prey composition, diversity and overlap. Copeia 10:661–666

    Article  Google Scholar 

  • Goiran C, Shine R (2013) Decline in sea snake abundance on a protected coral reef system in the New Caledonian Lagoon. Coral Reefs 32:281–284

    Article  Google Scholar 

  • Gopi GV, Pandav B, Choudhury BC (2007) Efficacy of turtle excluder devices on incidental captures of olive ridley sea turtles (Lepidochelys olivacea) in the trawl fisheries of Orissa, India. Testudo 6:67–73

    Google Scholar 

  • Hanamgond PT, Mitra D (2008) Evolution of Malvan Coast, Konkan, West Coast of India—a case study using remote sensing data. J Coastal Res 24:672–678

    Article  Google Scholar 

  • Hawlena D, Schmitz OJ (2010) Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am Nat 176:537–556

    Article  PubMed  Google Scholar 

  • Hennen D (2006) Associations between the alaska steller sea lion decline and commercial fisheries. Ecol Appl 16:704–717

    Article  PubMed  Google Scholar 

  • Hette-Tronquart N (2019) Isotopic niche is not equal to trophic niche. Ecol Lett 22(11):1987–1989

    Article  PubMed  Google Scholar 

  • IUCN SSC (2017) The IUCN red list of threatened species. Version, 2017

  • Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, work(s): RRWR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638

    Article  PubMed  CAS  Google Scholar 

  • Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER—Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602

    Article  PubMed  Google Scholar 

  • Layman CA, Quattrochi JP, Peyer CM, Allgeier JE (2007) Niche width collapse in a resilient top predator following ecosystem fragmentation. Ecol Lett 10:937–944

    Article  PubMed  PubMed Central  Google Scholar 

  • Lemen CA, Voris HK (1981) A comaprison of reproductive strategoes among marine snakes. J Anim Ecol 50:89–101

    Article  Google Scholar 

  • Lemons G, Eguchi T, LyonV B, LeRoux R, Seminoff J (2012) Effects of blood anticoagulants on stable isotope values of sea turtle blood tissue. Aquat Biol 14:201–206

    Article  Google Scholar 

  • Lobo AS (2003) Estimating sea snake diversity using trawler bycatch along the coast of Goa. PhD thesis. Saurashtra University

    Google Scholar 

  • Lobo AS (2007) The bycatch problem. Resonance 12:60–70

    Article  Google Scholar 

  • Lobo A, Pandav B, Vasudevan K (2004) Weight—length relationships in two species of marine snakes along the coast of Goa, Western India. Hamadryad 29:89–93

    Google Scholar 

  • Lobo AS, Vasudevan K, Pandav B (2005) Trophic ecology of Lapemis curtus (Hydrophiinae) along the western coast of India. Copeia 2005:637–641

    Article  Google Scholar 

  • Lukoschek V (2018) Population declines, genetic bottlenecks and potential hybridization in sea snakes on Australia’s Timor Sea reefs. Biol Conserv 225:66–79

    Article  Google Scholar 

  • Lukoschek V, Beger M, Ceccarelli D, Richards Z, Pratchett M (2013) Enigmatic declines of Australia’s sea snakes from a biodiversity hotspot. Biol Conserv 166:191–202

    Article  Google Scholar 

  • Mashjoor S, Jamebozorgi FH, Kamrani E (2018) Fishery-induced Inter-annual Changes in the Mean Trophic Level, the Northern Sea of Oman off the Iranian Coast, 2002–2011. Ocean Sci J 53(4):655–665

    Article  Google Scholar 

  • Milton DA (2001) Assessing the susceptibility to fishing of populations of rare trawl bycatch: Sea snakes caught by australia’s northern prawn fishery. Biol Cons 101:281–290

    Article  Google Scholar 

  • Mini, K G (2017) Sampling methodology employed by CMFRI for monitoring the fishery and estimation of marine fish landings in India. In: Course Manual Summer School on Advanced Methods for Fish Stock Assessment and Fisheries Management. Lecture Note Series No. 2/2017 . CMFRI; Kochi, Kochi, pp. 109-112.

  • Molina JM, Cooke SJ (2012) Trends in shark bycatch research: current status and research needs. Rev Fish Biol Fisheries 22:719–737

    Article  Google Scholar 

  • Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850

    Article  CAS  PubMed  Google Scholar 

  • Newsome SD, de Rio CM, Bearhop S, Phillips DL (2007) A niche for isotope ecology. Front Ecol Environ 5:429–436

    Article  Google Scholar 

  • Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75

    Article  Google Scholar 

  • Petta J C, Shipley O N, Wintner S P, Cliff G, Dicken M L, Hussey N E (2020) “Are You Really What You Eat? Stomach Content Analysis and Stable Isotope Ratios Do Not Uniformly Estimate Dietary Niche Characteristics in Three Marine Predators.” Oecologia 192 (4): 1111–26. https://doi.org/10.1007/s00442-020-04628-6.

  • Pinkas L (1971) Food habits of albacore, bluefin tuna and bonito in California waters. Calif Dept Fish and Game Fish Bull 152:1–105

    Google Scholar 

  • Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189

    Article  PubMed  Google Scholar 

  • R Core Team (2014). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Rao C, Dsouza S, Gupta T, Manoharakrishnan M, Lobo AS (2021) Fisheries induced shift in sea snake community assemblages along the Konkan coast, India. Aquat Conserv Mar Freshwat Ecosyst. https://doi.org/10.1002/aqc.3658

    Article  Google Scholar 

  • Reich KJ, Bjorndal KA, Martínez Del Rio C (2008) Effects of growth and tissue type on the kinetics of 13C and 15N incorporation in a rapidly growing ectotherm. Oecologia 155:651–663

    Article  PubMed  Google Scholar 

  • Rojas-Bracho L, Reeves RR (2013) Vaquitas and gillnets: Mexico’s ultimate cetacean conservation challenge. Endanger Species Res 21:77–87

    Article  Google Scholar 

  • Sanders KL, Lee MSY, Mumpuni BT, Rasmussen AR (2013) Multilocus phylogeny and recent rapid radiation of the viviparous sea snakes (Elapidae: Hydrophiinae). Mol Phylogenet Evol 66:575–591

    Article  PubMed  Google Scholar 

  • Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions: primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163

    Article  Google Scholar 

  • Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39

    Article  PubMed  CAS  Google Scholar 

  • Sherratt E, Rasmussen AR, Sanders KL (2018) Trophic specialization drives morphological evolution in sea snakes. R Soc Open Sci 5(3):172141

    Article  PubMed  PubMed Central  Google Scholar 

  • Shine R (1991) Why do larger snakes eat larger prey items? Funct Ecol 5:493–502

    Article  Google Scholar 

  • Shine R, Bonnet X, Elphick MJ, Barrott EG (2004) A novel foraging mode in snakes: browsing by the sea snake Emydocephalus annulatus (Serpentes, Hydrophiidae). Funct Ecol 18:16–24

    Article  Google Scholar 

  • Soykan CU, Moore JE, Zydelis R, Crowder LB, Safina C, Lewison RL (2008) Why study bycatch? An introduction to the Theme Section on fisheries bycatch. Endanger Species Res 5(2–3):91–102

    Article  Google Scholar 

  • Srinivasan M (2019) Predator/prey decisions and the ecology of fear. In: Würsig B (ed) Ethology and behavioral ecology of odontocetes. Springer International Publishing, Cham, pp 145–163

    Chapter  Google Scholar 

  • Stelzenmüller V, Rogers SI, Mills CM (2008) Spatio-temporal patterns of fishing pressure on UK marine landscapes, and their implications for spatial planning and management. ICES J Mar Sci 65:1081–1091

    Article  Google Scholar 

  • Steneck RS (2012) Apex predators and trophic cascades in large marine ecosystems: learning from serendipity. Proc Natl Acad Sci 109:7953–7954

    Article  PubMed  PubMed Central  Google Scholar 

  • Terborgh JW (2015) Toward a trophic theory of species diversity. Proc Natl Acad Sci USA 112:11415–11422

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Udyawer V, Read M, Hamann M, Heupel MR, Simpfendorfer CA (2016) Importance of shallow tidal habitats as Refugia from trawl fishing for sea snakes. J Herpetol 50:527–533

    Article  Google Scholar 

  • United Nations Development Programme (UNDP) (2013) Mainstreaming coastal and marine biodiversity conservation into production sectors in the Sindhudurg coast, Maharashtra. Prog Rep 2013:1–116

    Google Scholar 

  • Van Cao N, Tao NT, Moore A, Montoya A, Rasmussen AR, Broad K, Voris HK, Takacs Z (2014) Sea snake harvest in the gulf of Thailand. Conserv Biol 28:1677–1687. https://doi.org/10.1111/cobi.12387

    Article  PubMed  Google Scholar 

  • Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85:183–206

    Article  PubMed  Google Scholar 

  • Vidya R, Shyam SS, Shiledar BAA (2016) Market structure analysis of fish markets in Sindhudurg, Maharashtra. Mar Fish Inf Serv Tech Ext Ser 230:26–28

    Google Scholar 

  • Voris HK (1966) Fish eggs as the apparent sole food item for a genus of sea snake, Emydocephalus (Krefft). Ecology 47:152–154

    Article  Google Scholar 

  • Voris HK (1972) The role of sea snakes (Hydrophiidae) in the trophic structure of coastal ocean communities. J Mar Biol Assoc India 14:429–442

    Google Scholar 

  • Voris HK, Voris HH (1983) Feeding strategies in marine snakes: an analysis of evolutionary, morphological, behavioural and ecological relationships. Am Zool 23:411–425

    Article  Google Scholar 

  • Voris HK, Voris HH, Liat LB (1978) The food and feeding behavior of a marine snake, Enhydrina schistosa (Hydrophiidae). Copeia 1978:134–146

    Article  Google Scholar 

  • Wunder MB (2012) Determining geographic patterns of migration and dispersal using stable isotopes in keratins. J Mammal 93:360–367. https://doi.org/10.1644/11-MAM

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by the Rufford Foundation (Grant No. 24116-1) and the Mangrove Foundation of Maharashtra (Grant No. 2018-19/182). We thank Naveen Namboothri for his invaluable inputs during conceptualisation and analysis, and Maria Thaker for her comments on the manuscript. This work would not be possible without the support and cooperation of the fishers and other local stakeholders in Malvan as well as our many volunteers who helped us during our fieldwork. We would also like to thank the Maharashtra Forest department for providing permits and logistical support. Finally, we would like to thank Ewan Hunter and the anonymous reviewers for their constructive comments that helped improve our manuscript.

Author information

Authors and Affiliations

  1. Dakshin Foundation, Bangalore, India

    Shawn Dsouza, Chetan Rao,  Muralidharan Manoharakrishnan  & Kartik Shanker

  2. Center for Ecological Sciences, Indian Institute of Science, Bangalore, India

    Shawn Dsouza & Kartik Shanker

Authors
  1. Shawn Dsouza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chetan Rao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Muralidharan Manoharakrishnan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kartik Shanker
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: SD, CR, MM; analysis: SD; data collection: SD, CR; writing—draft preparation: SD; writing—editing and review: KS, CR, MM; funding: SD, CR; resources: KS; supervision: KS.

Corresponding author

Correspondence to Shawn Dsouza.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics approval

Research permits were provided by the Maharashtra Forest department (Permit No. SPP-30-2018). Ethics approval was granted by the Dakshin Foundation Human and Animal Ethics Committee (Ref. No. DF_Ethics committee_AS_2019_Mar_01).

Informed consent

We acquired informed consent from all individual human participants in this study (namely fishers) and have published the data on condition of anonymity.

Additional information

Responsible Editor: E. Hunter.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Reviewer: C. Goiran and an undisclosed expert

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 773 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dsouza, S., Rao, C., Manoharakrishnan , . et al. Resource use and the impacts of fisheries on two sympatric sea snake species on the west coast of India. Mar Biol 168, 146 (2021). https://doi.org/10.1007/s00227-021-03956-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-021-03956-2

Search

Navigation