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Using Fatty-Acid Profile Analysis as an Ecologic Indicator in the Management of Tourist Impacts on Marine Wildlife: A Case of Stingray-Feeding in the Caribbean

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Abstract

Feeding marine wildlife as a tourism experience has become a popular means by which to attract both people and wildlife, although management efforts are still in their infancy. “Stingray City Sandbar” in the Cayman Islands, where visitors can hand feed free-ranging Southern Stingrays (Dasyatis americana), is a world-famous attraction currently undergoing visitor and wildlife management. One plan is to decrease the amount of nonnatural food provided by tourists with the intention of decreasing stingray habituation to the artificial food source and promoting stingray health. However, the effectiveness of this action is uncertain given that neither the extent of squid composition in the stingray diet nor the degree of nutrient similarity between the fed and natural diets is unknown. We used fatty acid (FA) profile analysis to address these questions by assessing the serum nonesterified FA composition of fed and unfed stingrays around the island and compared them with FA profiles of (1) the provisioned food source (squid) and (2) other warm- and cold-water elasmobranchs (sharks and rays). Our results indicated that fed stingrays were distinct. The FA profiles of the fed stingray population were expressly different from those of the unfed populations and showed a remarkable similarity to the FA composition of squid, suggesting that squid is the main food source. The tropical fed stingrays also exhibited essential FA ratios, specific to both species and habitat, comparable with those of elasmobranchs and squid from cold-water environs, implying that the provisioned food does not provide a similar nutritional lipid composition to that eaten in the wild. Our results suggest that FA profiles are a valuable indicator for the management and monitoring of fed Southern Stingrays because they can be used to assess differences in diet composition and provide an index of nutritional similarity. Our findings are currently being used by Caymanian stakeholders in designing practical management actions for their wildlife attraction.

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References

  • Ackman RG, Eaton CA (1966) Lipids in the fin whale (Balaenoptera physalus) from North Atlantic waters. III. Occurrence of eicosenoic and docosenoic fatty acids in the zooplankton Meganyctiphanes norvegica (M. Sars) and their effect on whale oil composition. Canadian Journal of Biochemistry 44:1561–1566

    Article  CAS  Google Scholar 

  • Anderson MJ (2004a) DISTLIM v.5: a FORTRAN computer program to calculate a distance-based multivariate analysis for a linear model. Department of Statistics, University of Auckland, New Zealand

  • Anderson MJ (2004b) PERMDISP: a FORTRAN computer program for permutatinoal analysis of multivariate dispersions (for any two-factor ANOVA design) using permutation tests. Department of Statistics, University of Auckland, New Zealand

  • Ballantyne JS (1997) Jaws, the inside story. The metabolism of elasmobranch fishes. Comparative Biochemistry and Physiology B, Comparative Biochemistry 118:703–742

    Article  Google Scholar 

  • Ballantyne JS, Mercure F, Gerrits MF Van Der Kraak G McKinley S Martens DW, et al. (1996) Plasma nonesterified fatty acid profiles in male and female sockeye salmon, Oncorhynchus nerka, during the spawning migration. Canadian Journal of Fisheries and Aquatic Sciences 53:1418–1426

    Article  CAS  Google Scholar 

  • Basiron MN (1997) Marine tourism industry–trends and prospects. Paper presented at the National Seminar on the Development of Marine Tourism Industry in South East Asia at Langkawi. September 25 to 28

  • Bell JG, Sargent JR (2003) Arachidonic acid in aquaculture feeds: current status and future opportunities. Aquaculture 218:491–499

    Article  CAS  Google Scholar 

  • Bradshaw CJA, Hindell MA, Best NJ, Phillips KL, Wilson G, Nichols PD (2003) You are what you eat: describing the foraging ecology of southern elephant seals (Mirounga leonina) using blubber fatty acids. Proceedings of the Royal Society of London B 270:1283–1292

    Article  Google Scholar 

  • Budge SM, Iverson SJ, Bowen WD, Ackman RG (2002) Among- and within-species variability in fatty acid signatures of marine fish and invertebrates on the Scotian Shelf, Georges Bank, and southern Gulf of St. Lawrence. Canadian Journal of Fisheries and Aquatic Sciences 59:886–898

    Article  CAS  Google Scholar 

  • Cartland-Shaw LK, Cree A, Skeaff CM, Grimmond NM (1998) Differences in dietary and plasma fatty acids between wild and captive populations of a rare reptile, the tuatara (Sphenodon punctatus). Journal of Comparative Physiology B, Biochemical, Systemic, and Environmental Physiology 168:569–580

    Article  CAS  Google Scholar 

  • Castell JD, Bell JG, Tocher DR, Sargent JR (1994) Effects of purified diets containing different combinations of arachidonic and docosahexaenoic acid on survival, growth and fatty acid composition of juvenile turbot (Scophthalmus maximus). Aquaculture 128:315–333

    Article  CAS  Google Scholar 

  • Cayman Islands Ministry of Tourism (2002) Focus for the future–a tourism policy framework for the Cayman Islands. The Tourism Company, London, UK

    Google Scholar 

  • Corcoran M (2006) The effects of supplemental feeding on the activity space and movement patterns of the Southern stingray, Dasyatis americana, at Grand Cayman, Cayman Islands. Master’s thesis, Nova Southeastern University, Fort Lauderdale, FL

  • Dunkley L, Cattet MRL (2003) A comprehensive review of the ecological and human social effects of artificial feeding and baiting of wildlife. Canadian Cooperative Wildlife Health Center, Saskatoon, Saskatchewan, Canada

    Google Scholar 

  • Fillion FL, Foley JP, Jaquemot AJ (1992) The economics of global tourism. Paper presented at the fourth World Congress on National Parks and Protected Areas, Caracas, Venezuela, February 10 to 21

  • Garrod B, Wilson JC (2004) Nature on the edge? Marine ecotourism in peripheral coastal areas. Journal of Sustainable Tourism 12:95–120

    Google Scholar 

  • Gibson RA, Kneebone R, Kneebone GM (1984) Comparative levels of arachidonic acid and eicosapentaenoic acid in Malaysian fish. Comparative Biochemistry and Physiology C, Comparative Pharmacology 78:325–328

    Article  CAS  Google Scholar 

  • Gilliam D, Sullivan KM (1993) Diet and feeding habits of the Southern stingray Dasyatis americana in the Central Bahamas. Bulletin of Marine Science 52:1007–1013

    Google Scholar 

  • Green RJ, Higgenbottom K (2000) The effects of non-consumptive wildlife tourism on free-ranging wildlife: a review. Pacific Conservation Biology 6:183–197

    Google Scholar 

  • Greene D, Selivonchick D (1987) Lipids metabolism in fish. Progress in Lipid Research 26:53–85

    Article  CAS  Google Scholar 

  • Guitart R, Silvestre AM, Guerrero X, Mateo R (1999) Comparative study on the fatty acid composition of two marine vertebrates: striped dolphins and loggerhead turtles. Comparative Biochemistry and Physiology B, Comparative Biochemistry 124:439–443

    Article  CAS  Google Scholar 

  • Hansel M, Rao KS, Matsuoka T, Rali T, Burrows I, Huber ME (1993) The distribution of fatty acids in flesh and liver of Papua New Guinean fish. Comparative Biochemistry and Physiology B, Comparative Biochemistry 106:655–658

    Article  Google Scholar 

  • Harel M, Koven W, Lein I, Bar Y, Behrens P, Stubblefield J, et al. (2002) Advanced DHA, EPA and ArA enrichment materials for marine aquaculture using single cell heterotrophs. Aquaculture 213:347–362

    Article  CAS  Google Scholar 

  • Henderson RJ, Tocher DR (1987) The lipid composition and biochemistry of freshwater fish. Progress in Lipid Research 28:281–347

    Article  Google Scholar 

  • Ishigame G, Baxter GS, Lisle AT (2006) Effects of artificial foods on the blood chemistry of the Australian magpie. Austral Ecology 31:199–207

    Article  Google Scholar 

  • Iverson SJ, Field C, Bowen WD, Blanchard W (2004) Quantitative fatty acid signature analysis: a new method of estimating predator diets. Ecological Monographs 74:211–235

    Article  Google Scholar 

  • Iverson SJ, Oftedal OT (1992) Fatty acid composition of black bear (Ursus americanus) milk during and after the period of winter dormancy. Lipid 27:940–943

    Article  CAS  Google Scholar 

  • Jangaard PM, Ackman RG (1965) Lipids and component fatty acids of the Newfoundland squid, Illex illecebrosus (Le Sueur). Journal of the Fisheries Resource Board of Canada 22:131–137

    CAS  Google Scholar 

  • Joseph JD, Ackman RG, Seaborn GT (1985) Effect of diet on depot fatty acid composition in the green turtle, Chelonia mydas. Comparative Biochemistry and Physiology B, Comparative Biochemistry 80:15–22

    Article  Google Scholar 

  • Kirsch PE, Iverson SJ, Bowen WD, Kerr SR, Ackman RG (1998) Dietary effects on fatty acid signature of whole Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 55:1378–(1386)

    Article  CAS  Google Scholar 

  • Lall SP (2000) Nutrition and health of fish. Paper presented in Avances en Nutrición Acuicola Memorial V del V Simposium Internacional de Nutrición Acuicola. Cruz-Suarez, LE, Ricque-Marie D, Tapia-Salazar M, Olvera-Novoa MA, Civera-Cerecedo R (eds.) Mérida, Yucatán, Mexico, November19–22 to (2000). Available at: http://www.w3.dsi.uanl.mx/publicaciones/maricultura/acuiculturaV/lall.pdf. Accessed: August 2006

  • McGarigal K, Cushman S, Stafford S (2000) Multivariate statistics for wildlife and ecology research. Springer-Verlag, New York, NY

    Google Scholar 

  • McKinley RS, Singer TD, Ballantyne JS, Power G (1993) Seasonal variation in plasma nonesterified fatty acids of Lake sturgeon (Acipenser fulvescens) in the vicinity of hydroelectric facilities. Canadian Journal of Fisheries and Aquatic Sciences 50:2440–2447

    Article  CAS  Google Scholar 

  • Miller ML (1993) The rise of coastal and marine tourism. Ocean and Coastal Management 20:181–199

    Article  Google Scholar 

  • Newcombe RG (2006) Confidence intervals for an effect size measure based on the Mann-Whitney statistic. Part 2. Asymptotic methods and evaluation. Statistics in Medicine 25:559–573

    Article  Google Scholar 

  • Newsome D, Dowling R, Moore S (2005) Wildlife tourism. Channel View Publications, Clevedon, USA

    Google Scholar 

  • Orams M (1999) Marine tourism―development, impacts and management. Routledge, New York, NY

    Google Scholar 

  • Orams MB (2002) Feeding wildlife as a tourism attraction: a review of issues and impacts. Tourism Management 23:281–293

    Article  Google Scholar 

  • Phillips KL, Jackson GD, Nichols PD (2001) Predation on myctophids by the squid Moroteuthis ingens around Macquarie and Heard islands: stomach contents and fatty acid analyses. Marine Ecology Progress Series 215:179–189

    Article  CAS  Google Scholar 

  • Reynolds PC, Braithwaite D (2001) Towards a conceptual framework for wildlife tourism. Tourism Management 22:31–42

    Article  Google Scholar 

  • Rice CD, Arkoosh MR (2002) Immunological indicators of environmental stress and disease susceptibility in fishes. In Adams SM (ed.), Biological indicators of aquatic ecosystem stress. American Fisheries Society, Symposium 8, Bethesda, MD. pp 187–220

    Google Scholar 

  • Rodriguez C, Acosta C, Badia P, Cejas JR, Santamaria FJ, Lorenzo A (2004) Assessment of lipid and essential fatty acids requirements of black seabream (Spondyliosoma cantharus) by comparison of lipid composition in muscle and liver of wild and captive adult fish. Comparative Biochemistry and Physiology B, Comparative Biochemistry 139:619–629

    Article  CAS  Google Scholar 

  • RuleQuest Research. (1997) RuleQuest research data mining tools. RuleQuest Research, St. Ives, New South Wales, Australia

    Google Scholar 

  • Sargent JR, Bell JG, Bell MV, Henderson RJ, Tocher DR (1995) Requirement criteria for essential fatty acids. Symposium of European Inland Fisheries Advisory Commission. Journal of Applied Ichthyology 11:183–198

    Article  CAS  Google Scholar 

  • Sargent JR, Bell G, McEvoy LA, Tocher DR, Estevez A (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191–199

    Article  CAS  Google Scholar 

  • Schaufler L, Heintz R, Sigler M, Hulbert L (2005) Fatty acid composition of sleeper shark (Somniosus pacificus) liver and muscle reveals nutritional dependence on planktivores. International Council for the Exploration of the Sea, Conference Meeting, Session N:05, Elasmobranch Fisheries Science

  • Seaborn GT, Jahncke ML, Smith TIJ (2000) Differentiation between cultured hybrid striped bass and wild striped bass and hybrid bass using fatty acid profiles. North American Journal of Fisheries Management 20:618–626

    Article  Google Scholar 

  • Seaborn GT, Moore MK, Balazs GH (2005) Depot fatty acid composition in immature green turtles (Chelonia mydas) residing at two near-shore foraging areas in the Hawaiian Islands. Comparative Biochemistry and Physiology B, Comparative Biochemistry 140:183–195

    Article  CAS  Google Scholar 

  • Semeniuk CAD, Dill LM (2005) Cost/benefit analysis of group and solitary resting in the cowtail stingray (Pastinachus sephen). Behavioral Ecology 16:417–426

    Article  Google Scholar 

  • Shackley M (1998) “Stingray City”―Managing the impact of underwater tourism in the Cayman Islands. Journal of Sustainable Tourism 6:328–338

    Google Scholar 

  • Sinclair AJ, O’Dea K, Naughton JM, Sutherland T, Wankowski J (1984) Polyunsaturated fatty acid types in some Australian and Antarctic fish. Proceedings of the Nutrition Society of Australia 9:188

    Google Scholar 

  • Singer TD, Mahadevappa VG, Ballantyne JS (1990) Aspects of the energy metabolism of lake sturgeon, Acipenser fulvescens, with special emphasis on lipid and ketone body metabolism. Canadian Journal of Fisheries and Aquatic Sciences 47:873–881

    Article  CAS  Google Scholar 

  • Smith SJ, Iverson SJ, Bowen WD (1997) Fatty acid signatures and classification trees: new tools for investigating the foraging ecology of seals. Canadian Journal of Fisheries and Aquatic Sciences 54:1377–1386

    Article  CAS  Google Scholar 

  • Speers-Roesch B (2005) Metabolic organization of the chondrichthyan fishes: evolutionary implications. M.Sc. thesis, University of Guelph, Ontario, Canada

    Google Scholar 

  • Thiemann GW, Budge SM, Bowen WD, Iverson SJ (2004) Comment on Grahl-Nielsen and others (2003) Fatty acid composition of the adipose tissue of polar bears and of their prey: ringed seals, bearded seals and harp seals. Marine Ecology Progress Series 281:297–301

    Article  Google Scholar 

  • Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Reviews in Fisheries Science 11:107–184

    Article  CAS  Google Scholar 

  • Virtue P, Mayzaud P, Albessard E, Nichols P (2000) Use of fatty acids as dietary indicators in northern krill, Meganyctiphanes norvegica, from northeastern Atlantic, Kattegat, and Mediterranean waters. Canadian Journal of Fisheries and Aquatic Sciences 57(Suppl. 3):104–114

    Article  CAS  Google Scholar 

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Acknowledgments

C. A. D. S and K. D. R. acknowledge financial support from Fonds Québécois de la Recherche sur la Nature et les Technologies and the National Sciences and Engineering Research Council of Canada (NSERC), respectively. B. S.-R. was supported by a NSERC postgraduate scholarship. This work was partially supported by a PADI AWARE research grant. We thank the following individuals for their assistance in the field: J. Verspoor, R. Wrangham, M. Potenski, A. Briggs, and C. Sherrit. We thank M. Murray of the Monterey Bay Aquarium, CA, for advice on stingray blood-sampling techniques, and the Cayman Island Department of Environment and the Guy Harvey Research Institute for the use of marine and laboratory equipment. We also thank J. S. Ballantyne for use of the gas chromatograph for FA analysis. Last, we thank M. Orams and two anonymous reviewers for their helpful comments on the manuscript.

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Correspondence to Christina A. D. Semeniuk.

Appendix

Appendix

Appendix 1 FA composition of Southern Stingrays in the Cayman Islands

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Semeniuk, C.A.D., Speers-Roesch, B. & Rothley, K.D. Using Fatty-Acid Profile Analysis as an Ecologic Indicator in the Management of Tourist Impacts on Marine Wildlife: A Case of Stingray-Feeding in the Caribbean. Environmental Management 40, 665–677 (2007). https://doi.org/10.1007/s00267-006-0321-8

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