Skip to main content
SpringerLink
Log in

Stable isotope profiles in whale shark (Rhincodon typus) suggest segregation and dissimilarities in the diet depending on sex and size

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

We investigated the sex- and size-related differences in the diet of whale sharks from the Arabian Sea (north-western Indian Ocean) using carbon and nitrogen stable-isotope analyses in white muscle. The samples were collected during the commercial fishing season between April and May of 2001 in Veraval (Gujarat, India). The overall isotope signature was similar to that of the pelagic-neritic zooplanktivore Ilisha melastoma, which suggests that both species are feeding on similar prey. In whale sharks, a positive relationship was found between δ15N and δ13C. This, together with a significant enrichment of both heavy stable isotopes with total length indicates that the contribution to the diet of small fish and/or larger zooplankton of higher trophic level increases with the movement from offshore areas to coastal areas as they grow. Gender differences in the isotopic ratios were not statistically significant, but small sample size cannot rule out completely the existence of some degree of spatial or dietary segregation between sexes.

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

Similar content being viewed by others

References

  • Arrington DA, Winemiller KO (2002) Preservation effects on stable isotope analysis of fish muscle. Trans Am Fish Soc 131:337–342

    Article  CAS  Google Scholar 

  • Beckley LE, Cliff G, Smale MJ, Compagno LJV (1997) Recent strandings and sightings of whale sharks in South Africa. Environ Biol Fish 50:343–348

    Article  Google Scholar 

  • Boustany AM, Davis SF, Pyle P, Anderson SD, Le Boeuf BJ, Block BA (2002) Expanded niche for white sharks. Nature 415:35–36

    Article  PubMed  CAS  Google Scholar 

  • Bres M (1993) The behaviour of sharks. Rev Fish Biol Fish 3:133–159

    Article  Google Scholar 

  • Burton RK, Koch PL (1999) Isotopic tracking of foraging and long distance migration in northeastern Pacific pinnipeds. Oecologia 119:578–585

    Article  Google Scholar 

  • Cabana G, Rasmussen JB (1996) Comparison of aquatic food chains using nitrogen isotopes. Proc Natl Acad Sci USA 93:10844–10847

    Article  PubMed  CAS  Google Scholar 

  • Carpenter K, Krupp F, Jones DA, Zajonz W (1997) Living marine resources of Kuwait, eastern Saudi Arabia, Bahrain, Qatar, and the United Arab Emirates. FAO, Rome

    Google Scholar 

  • Chang WB, Leu M, Fang LS (1997) Embryos of the whale shark, Rhincodon typus: early growth and size distribution. Copeia 97:444–446

    Article  Google Scholar 

  • Chen CT, Liu KM, Joung SJ (2002) Preliminary report on Taiwan’s whale shark fishery. In: Fowler SL, Reed TM, Dipper FA (eds) Elasmobranch biodiversity, conservation and management: proceedings of the international seminar and workshop, Sabah, Malaysia, July 1997 IUCN SSC. Shark Specialist Group, IUCN, Gland, Switzerland, pp 162–167

    Google Scholar 

  • Clark E, Nelson DR (1997) Young whale sharks, Rhincodon typus, feeding on a copepod bloom near La Paz, Mexico. Environ Biol Fish 50:63–73

    Article  Google Scholar 

  • Colman JG (1997) A review of the biology and ecology of the Whale Shark. J Fish Biol 51:1219–1234

    Article  Google Scholar 

  • Compagno LJV (1984) Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Carcharhiniformes. FAO species catalogue for fishery purposes 1, vol. 4, 269 FAO, Rome pp 251–655

  • Compagno LJV (2001) Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Bullhead, mackerel and carpet sharks (Heterodontiformes, Lamniformes and Orectolobiformes). FAO species catalogue for fishery purposes 1, vol. 2, 269 pp FAO, Rome

  • Cortés E (1999) Standardized diet compositions and trophic levels of sharks. ICES J Mar Sci 56:707–717

    Article  Google Scholar 

  • DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    Article  CAS  Google Scholar 

  • DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351

    Article  CAS  Google Scholar 

  • Dolenec T, Vokal B, Dolenec M (2005) Nitrogen—15 signals of anthropogenic nutrient loading in Anemonia sulcata as a possible indicator of human sewage impacts on marine coastal ecosystems: a case study of Pirovac Bay and the Murter Sea (Central Adriatic). Croat Chem Acta 78(4):593–600

    CAS  Google Scholar 

  • Domi N, Bouquegneau J, Das K (2005) Feeding ecology of five commercial shark species of the Celtic Sea through stable isotope and trace metal analysis. Mar Environ Res 60:551–569

    Article  PubMed  CAS  Google Scholar 

  • Duffy CAJ (2002) Distribution, seasonality, lengths, and feeding behaviour of whale sharks (Rhincodon typus) observed in New Zealand waters. NZ J Mar Fresh Res 36:565–570

    Article  Google Scholar 

  • Dutta R (2001) Whale Sharks. The gentle giants of the Sea. Traffic Dispatches 17:10

  • Eckert SA, Stewart BS (2001) Telemetry and satellite tracking of whale sharks, Rhincodon typus, in the Sea of Cortez, Mexico, and the north Pacific Ocean. Environ Biol Fish 60:299–308

    Article  Google Scholar 

  • Eckert SA, Dolar LL, Kooyman GL, Perrin W, Ridzwan RA (2002) Movements of whale sharks (Rhincodon typus) in Southeast Asia waters as determined by satellite telemetry. J Zool (Lond) 257:111–115

    Article  Google Scholar 

  • Estrada JA, Rice AN, Lutcavage ME, Skomal GB (2003) Predicting trophic position in sharks of the north-west Atlantic Ocean using stable isotope analysis. J Mar Biol Ass UK 83:1347–1350

    Article  CAS  Google Scholar 

  • Estrada JA, Rice AN, Natanson LJ, Skomale GB (2006) Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87:829–834

    Article  PubMed  Google Scholar 

  • Fisk AT, Tittlemier ShA, Pranschke JL, Norstrom RJ (2002) Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of Greenland sharks (Somniosus microcephalus). Ecology 83:2162–2172

    Article  Google Scholar 

  • Focken U (2001) Stable isotopes in animal ecology: the effect of ration size on the trophic shift of C and N isotopes between feed and carcass. Isot Environ Health Stud 37:199–211

    Article  CAS  Google Scholar 

  • Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509

    PubMed  CAS  Google Scholar 

  • Fry B, Wainright SC (1991) Diatom sources of 13C-rich carbon in marine food webs. Mar Ecol Progr Ser 76:149–158

    Article  Google Scholar 

  • Garrick JAF (1964) Additional information on the morphology of an embryo whale shark. Proc US Nat Mus 115:10

    Google Scholar 

  • Gaye-Siessegger J, Focken U, Abel HJ, Becker K (2003) Feeding level and diet quality influence trophic shift of C and N isotopes in Nile tilapia (Oreochromis niloticus L.). Isot Environ Health Stud 39:125–134

    Article  CAS  Google Scholar 

  • Graham RT, Roberts CM (2007) Assessing the size, growth rate and structure of a seasonal population of whale sharks (Rhincodon typus Smith 1828) using conventional tagging and photo identification. Fish Res 84:71–80

    Article  Google Scholar 

  • Gunn JS, Stevens JD, Davis TLO, Norman BM (1999) Observations on the short-term movements and behaviour of whale sharks (Rhincodon typus) at Ningaloo Reef, Western Australia. Mar Biol 135:553–559

    Article  Google Scholar 

  • Hanfee F (2001) Trade in Whale shark and its products in the coastal state of Gujarat, India. Report to the Rufford Foundation from TRAFFIC India

  • Hemminga MA, Mateo MA (1996) Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Mar Ecol Prog Ser 140:285–298

    Article  Google Scholar 

  • Heyman WD, Graham RT, Kjerfve B, Johannes RE (2001) Whale sharks Rhincodon typus aggregate to feed on fish spawn in Belice. Mar Ecol Prog Ser 215:275–282

    Article  Google Scholar 

  • Hobbs JPA, Frisch AJ, Hamanaka T, McDonald CA, Gilligan JJ, Neilson J (2009) Seasonal aggregation of juvenile whale sharks (Rhincodon typus) at Christmas Island, Indian Ocean. Coral Reefs 28:577–577

    Article  Google Scholar 

  • Hoem J (2008) The reporting of statistical significance in scientific journals. Demographic Res 18:437–442

    Article  Google Scholar 

  • Hsu CK, Chang TY, Zu HC, Huang KF, Tsai WS (2000) Preliminary attempt on Whale Shark ranching (in Chinese). TFRI Newsletter 143:6–11

    Google Scholar 

  • Hueter RE, Heupel MR, Heist EJ, Keeney DB (2005) Evidence of philopatry in sharks and implications for the management of shark fisheries. J Northw Atl Fish Sci 35:239–247

    Google Scholar 

  • Hussey NE, Brush J, McCarthy ID, Fisk AT (2010) δ15N and δ13C diet–tissue discrimination factors for large sharks under semi-controlled conditions. Comp Biochem Physiol 155:445–453

    Article  Google Scholar 

  • IUCN (2003) Inclusion of whale shark Rhincodon typus in Appendix II. Proponent: India and Philippines. The IUCN/TRAFFIC Analyses of Proposals to Amend the CITES Appendices Prepared for the 12th meeting of the Conference of the Parties (CoP12) Santiago, Chile, 3–15

  • Joung SJ, Chen CT, Clark E, Uchida S, Huang WYP (1996) The whale shark, Rhincodon typus, is a livebearer: 300 embryos found in one ‘megamamma' supreme. Environ Biol Fish 46:219–223

    Article  Google Scholar 

  • Klimley AP (1987) The determinants of sexual segregation in the scalloped hammerhead shark, Sphyrna lewini. Environ Biol Fish 18:27–40

    Article  Google Scholar 

  • Kukuyev EI (1995) The new finds in recently born individuals of the whale shark Rhiniodon typus (Rhiniodontidae) in the Atlantic Ocean. J Ichthyol 36:203–205

    Google Scholar 

  • Last PR, Stevens JD (1994) Sharks and Rays of Australia. CSIRO, Australia

    Google Scholar 

  • Logan JM, Lutcavage ME (2010) Stable isotope dynamics in elasmobranch fishes. Hydrobiol 644:231–244

    Article  CAS  Google Scholar 

  • MacNeil MA, Skomal GB, Fisk AT (2005) Stable isotopes from multiple tissues reveal diet switching in sharks. Mar Ecol Prog Ser 302:199–206

    Article  Google Scholar 

  • Meekan MG, Bradshaw CJA, Press M, McLean C, Richards A, Quasnichka S, Taylor JA (2006) Population size and structure of whale sharks (Rhincodon typus) at Ningaloo Reef, Western Australia. Mar Ecol Prog Ser 319:275–285

    Article  Google Scholar 

  • Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochimic Acta 48:1135–1140

    Article  CAS  Google Scholar 

  • Nelson J, Eckert S (2007) Foraging ecology by whale sharks (Rhincodon typus) within Bahia de los Angeles, Baja California Norte, Mexico. Fish Res 84:47–64

    Article  Google Scholar 

  • Nishida K (2001) Whale shark—the world's largest fish. In: Kakabo T, Machida Y, Yamaoka K, Nishida K (eds) Fishes of the Kuroshio Current, Japan. Osaka Aquarium KAIYUKAN, Minato-ku, Osaka, pp 20–26

  • Norman BM (1999) Aspects of the biology and ecotourism industry of the Whale Shark Rhincodon typus in North-western Australia. MPhil. Thesis. Murdoch University, Western Australia

    Google Scholar 

  • Norman BM, Stevens JD (2007) Size and maturity status of the whale shark (Rhincodon typus) at Ningaloo Reef in Western Australia. Fish Res 84:81–86

    Article  Google Scholar 

  • Overman NC, Parrish DL (2001) Stable isotope composition of walleye: 15N accumulation with age and area-specific differences in 13C. Can J Fish Aquatic Sci 58:1253–1260

    Article  Google Scholar 

  • Pardini AT, Jones CS, Noble LR, Kreiser B, Malcolm H, Bruce BD, Stevens JD, Cliff G, Scholl MC, Francis M, Duffy CAJ, Martin AP (2001) Sex-biased dispersal of great white sharks. Nature 412:139–140

    Article  PubMed  CAS  Google Scholar 

  • Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320

    Article  Google Scholar 

  • Pravin P (2000) Whale shark in the Indian coast—Need for conservation. Curr Sci 79:310–315

    Google Scholar 

  • Rau GH, Mearns AJ, Young DR, Olson RJ, Schafer HA, Kaplan IR (1983) Animal 13C/12C correlates with trophic level in pelagic food webs. Ecology 64:1314–1318

    Article  Google Scholar 

  • Rau GH, Chavez FP, Andfriederich GE (2001) Plankton 13C/12C variations in Monterey Bay, CA: evidence of non-diffusive inorganic carbon uptake by phytoplankton in an upwelling environment. Deep Sea Res 48:79–94

    Article  CAS  Google Scholar 

  • Riley MJ, Harman A, Rees RG (2009) Evidence of continued hunting of whale sharks Rhincodon typus in the Maldives. Environ Biol Fish 86:371–374

    Article  Google Scholar 

  • Rowat D (2007) Occurrence of whale shark (Rhincodon typus) in the Indian Ocean: a case for regional conservation. Fish Res 84:96–101

    Article  Google Scholar 

  • Rowat D, Meekan MG, Engelhardt U, Pardigon B, Vely M (2007) Aggregation of juvenile whale shark (Rhincodon typus) in the Gulf of Tadjoura, off Djibouti. Environ Biol Fish 80:465–472

    Article  Google Scholar 

  • Rowat D, Gore MA, Baloch BB, Islam Z, Ahmed E, Ali QM, Culloch R, Hameed S, Hasnain SA, Hussain B, Kiani S, Siddiqui J, Ormond RF (2008) New records of neonatal whale shark (Rhincodon typus) from the Northern Indian Ocean. Environ Biol Fish 82:215–219

    Article  Google Scholar 

  • Schmidt JV, Schmidt CL, Ozer F, Ernst RE, Feldheim KA, Ashley MV, Levine M (2009) Low genetic differentiation across three major ocean populations of the Whale Shark, Rhincodon typus. PLoS ONE; 4(4):e4988. doi:10.1371/journal.pone.0004988

    Article  PubMed  Google Scholar 

  • Sims DW (2005) Differences in habitat selection and reproductive strategies of male and female sharks. In: Ruckstuhl KE, Neuhaus P (eds) Sexual segregation in vertebrates: ecology of the two sexes. Cambridge University Press, Cambridge, pp 127–14

    Google Scholar 

  • Sleeman JC, Meekan MG, Wilson SG, Polovina JJ, Stevens JD, Boggs GS, Bradshaw CJA (2010) To go or not to go with the flow: environmental influences on whale shark movement patterns. J Exp Mar Ecol Biol 390:84–98

    Article  Google Scholar 

  • Sommer CW, Schneider J, Poutiers M (1996) FAO species identification field guide for fishery purposes. The living marine resources of Somalia. FAO, Rome, 376

    Google Scholar 

  • Stevens JD (2007) Whale shark (Rhincodon typus) biology and ecology: a review of the primary literature. Fish Res 84:4–9

    Article  Google Scholar 

  • Stewart B, Wilson S (2005) Threatened Fishes of the World: Rhincodon typus (Smith 1828) (Rhincodontidae). Environ Biol Fish 74:184–185

    Article  Google Scholar 

  • Taylor G (1994) Whale Sharks. Angus & Robertson Publishers, Sydney, Australia

    Google Scholar 

  • Taylor JG (1996) Seasonal occurrence, distribution and movements of the whale shark, Rhincodon typus, at Ningaloo reef, Western Australia. Mar Freshwater Res 47:637–642

    Article  Google Scholar 

  • Trueman CN, McGill R, Guyard PH (2005) The effect of growth rate on tissue-diet isotopic spacing in rapidly growing animals. An experimental study with Atlantic salmon (Salmo salar). Rapid Comm Mass Spec 19:3239–3247

    Article  CAS  Google Scholar 

  • Uchida S, Toda M, Kamei Y, Teruya H (2000) The husbandry of 16 whale sharks Rhincodon typus, from 1980 to 1998 at the Okinawa expo aquarium. American Elasmobranch Society 16th Annual Meeting June 14–20, 2000 La Paz, B.C.S., México, U.S.A. Okinawa Expo Aquarium, Okinawa, Japan

  • Whitehead PJP (1985) FAO species catalogue. Vol. 7. Clupeoid fishes of the world (suborder Clupeioidei). An annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, shads, anchovies and wolf-herrings.. Part 1—Chirocentridae, Clupeidae and Pristigasteridae. FAO Fish. Synop. 125(7/1):1–303

    Google Scholar 

  • Wilson SG, Newbound DR (2001) Two whale shark faecal. samples from Ningaloo Reef, Western Australia. Bull Mar Sci 68:361–362

    Google Scholar 

  • Wilson SG, Taylor JG, Pearce AF (2001) The seasonal aggregation of whale sharks at Ningaloo Reef, Western Australia: currents, migrations and the El Niño/Southern Oscillation. Environ Biol Fish 61:1–11

    Article  Google Scholar 

  • Wilson SG, Polovina JJ, Stewart BS, Meekan MG (2006) Movements of Whale Sharks (Rhincodon typus) tagged at Ningaloo Reef, Western Australia. Mar Biol 148:1157–1166

    Article  Google Scholar 

  • Wintner SP (2000) Preliminary study of vertebral growth rings in the whale shark, Rhincodon typus, from the east coast of South Africa. Environ Biol Fish 59:441–451

    Article  Google Scholar 

  • Wolfson FH (1983) Records of seven juveniles of the whale shark Rhiniodon typus. J Fish Biol 22:647–655

    Article  Google Scholar 

  • Zingde MD (2005) Inputs into the oceans from land/rivers and pollution. In: Gupta HK (ed) Oceanology. Universities Press, India, pp 92–117

    Google Scholar 

Download references

Acknowledgments

We acknowledge the Fundació pel Desenvolupament Sostenible (FDS) for providing funds for the sampling fieldwork, to the Serveis Cientifico Tècnics (SCT) of the University of Barcelona for analytical assistance, and to the Vicerectorate of International Relations of the University of Barcelona for travel funding during the elaboration and correction of the manuscript.

Author information

Authors and Affiliations

  1. IrBio; Institut de Recerca de la Biodiversitat and Department of Animal Biology, Faculty of Biology, University of Barcelona, Avinguda Diagonal 645, 08028, Barcelona, Spain

    Asunción Borrell, Alex Aguilar, Manel Gazo & Luis Cardona

  2. Mullai Nagar, Anna Nagar, Chennai, 600040, India

    R. P. Kumarran

Authors
  1. Asunción Borrell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alex Aguilar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Manel Gazo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. P. Kumarran
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Luis Cardona
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Asunción Borrell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Borrell, A., Aguilar, A., Gazo, M. et al. Stable isotope profiles in whale shark (Rhincodon typus) suggest segregation and dissimilarities in the diet depending on sex and size. Environ Biol Fish 92, 559–567 (2011). https://doi.org/10.1007/s10641-011-9879-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-011-9879-y

Keywords

Search

Navigation