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Variations in the diet and stable isotope ratios during the ovarian development of female yellowfin tuna (Thunnus albacares) in the Western Indian Ocean

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Abstract

The feeding strategy of female yellowfin tuna (Thunnus albacares) during their reproductive cycle was investigated using a combination of different trophic tracers, i.e., stomach contents and dual stable isotope analysis, along with an assessment of ovarian development based on a histological analysis. To complete these analyses, we collected 215 female yellowfin from the Western Indian Ocean in 2009 and 2010. From these fish, we noted the ovarian development and analyzed the contents of 166 non-empty stomachs and 104 liver and muscle tissue samples. Stomach content analysis identified a large variety of prey species (45 prey families), key groups including crustaceans dominated by the swimming crab Charybdis smithii and crustacean larvae; fish dominated by the cigarfish Cubiceps pauciradiatus; and cephalopods dominated by ommastrephids Sthenoteuthis oualaniensis and Ornithoteuthis volatilis. Individuals capable of spawning appeared to feed intensively, particularly on cigarfish, during the reproductive period. From the mean reconstituted weight values of the preys, our results indicated that this intensive feeding led to increased amounts of acquired energy. The results of the stable isotope analyses, carried out on the muscle and liver tissues, indicated a clear decrease in values from north to south. These analyses also showed that liver δ15N values in spawning females were significantly lower than those in immature and developing individuals. This latter observation highlights the differences in metabolic processes that occur between tissues during ovarian development and underlines the importance of the liver in energy acquisition and mobilization in female yellowfin tuna during reproduction.

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References

  • Bard F, Kouamé B, Hervé A (2002) Schools of large yellowfin (Thunnus albacares) concentrated by foraging on a monospecific layer of Cubiceps pauciradiatus, observed in the eastern tropical Atlantic. ICCAT Coll Vol Sci Pap 54:33–41

    Google Scholar 

  • Bodin N, Budzinski H, Le Ménach K, Tapie N (2009) ASE extraction method for simultaneous carbon and nitrogen stable isotope analysis in soft tissues of aquatic organisms. Anal Chim Acta 643:54–60

    Article  CAS  Google Scholar 

  • Clarke MR (1986) A handbook for the identification of cephalopod beaks. Clarendon Press, Oxford

    Google Scholar 

  • Cortés E (1997) A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Can J Fish Aquat Sci 54:726–738

    Article  Google Scholar 

  • Crosnier A, Forest J (1973) Les crevettes profondes de l’Atlantique oriental tropical. Faune Trop 19:1–409

    Google Scholar 

  • Dagorn L, Holland KN, Itano DG (2007) Behavior of yellowfin (Thunnus albacares) and bigeye (T-obesus) tuna in a network of fish aggregating devices (FADs). Mar Biol 151:595–606

    Article  Google Scholar 

  • Davis RE (2005) Intermediate-depth circulation of the Indian and South Pacific Oceans measured by autonomous floats. J Phys Oceanogr 35:683–707

    Article  Google Scholar 

  • Dragovich A, Potthoff T (1972) Comparative study of food of skipjack and yellowfin tunas off the coast of West Africa. Fish Bull 70:1087–1110

    Google Scholar 

  • Drent R, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252

    Google Scholar 

  • Flynn AJ, Paxton JR (2013) Spawning aggregation of the lanternfish Diaphus danae (family Myctophidae) in the north-western Coral Sea and associations with tuna aggregations. Mar Freshw Res 63:1255–1271

    Article  Google Scholar 

  • Fonteneau A, Lucas V, Tewkai E et al (2008) Mesoscale exploitation of a major tuna concentration in the Indian Ocean. Aquat Living Resour 21:109–121

    Article  Google Scholar 

  • Gislason H, Helgason T (1985) Species interaction in assessment of fish stocks with special application to the North Sea. Dana 5:1–44

    Google Scholar 

  • Graham BS, Grubbs D, Holland K, Popp BN (2007) A rapid ontogenetic shift in the diet of juvenile yellowfin tuna from Hawaii. Mar Biol 150:647–658

    Article  Google Scholar 

  • Grande M (2013) The reproductive biology, condition and feeding ecology of the skipjack, Katsuwonus pelamis, in the Western Indian Ocean. Universidad del Pais Vasco, Leioa

    Google Scholar 

  • Gruber N, Sarmiento JL (1997) Global patterns of marine nitrogen fixation and denitrification. Glob Biogeochem Cycles 11:235–266

    Article  CAS  Google Scholar 

  • Hallier JP, Gaertner D (2008) Drifting fish aggregation devices could act as an ecological trap for tropical tuna species. Mar Ecol Prog Ser 353:255–264

    Article  Google Scholar 

  • Hayashi K, Takagi T, Kondo H, Futawatari M (1978) The lipids of marine animals from various habitat depths. VII. Compositions of diacyl glyceryl ethers in the flesh lipids of two deep-sea teleost fish, Seriollela sp. and S. punctata. Jpn Soc Fish Sci 44:917–923

    Article  CAS  Google Scholar 

  • Hyslop EJ et al (1980) Stomach contents analysis-a review of methods and their application. J Fish Biol 17:411–429

    Article  Google Scholar 

  • IOTC (2012) Report of the fourteenth session of the IOTC working party on tropical tunas. Indian Ocean Tuna Comm, Mauritius

    Google Scholar 

  • Itano (2001) The reproductive biology of yellowfin tuna (Thunnus albacares) in Hawaiian waters and the western tropical Pacific Ocean: project summary. University of Hawaii, Joint Institute for Marine and Atmospheric Research, Hawaii, p 69

    Google Scholar 

  • Jaquemet S, Potier M, Ménard F (2011) Do drifting and anchored fish aggregating devices (FADs) similarly influence tuna feeding habits? A case study from the western Indian Ocean. Fish Res 107:283–290

    Article  Google Scholar 

  • Jennings S, van der Molen J (2015) Trophic levels of marine consumers from nitrogen stable isotope analysis: estimation and uncertainty. ICES J Mar Sci 72(8):2289–2300

    Article  Google Scholar 

  • Juan-Jordá MJ, Mosqueira I, Freire J, Dulvy NK (2013) Life in 3-D: life history strategies in tunas, mackerels and bonitos. Rev Fish Biol Fish 23:135–155

    Article  Google Scholar 

  • Kaplan DM, Chassot E, Amandé JM et al (2014) Spatial management of Indian Ocean tropical tuna fisheries: potential and perspectives. ICES J Mar Sci J Cons 71:1728–1749

    Article  Google Scholar 

  • Lobley GE (2003) Protein turnover—what does it mean for animal production? Can J Anim Sci 83:327–340

    Article  CAS  Google Scholar 

  • Lorrain A, Paulet Y-M, Chauvaud L et al (2002) Differential δ13 C and δ15 N signatures among scallop tissues: implications for ecology and physiology. J Exp Mar Biol Ecol 275:47–61. doi:10.1016/S0022-0981(02)00220-4

    Article  CAS  Google Scholar 

  • Madigan DJ, Litvin SY, Popp BN et al (2012) Tissue turnover rates and isotopic trophic discrimination factors in the endothermic teleost, Pacific Bluefin Tuna (Thunnus orientalis). PLoS One 7:e49220

    Article  CAS  Google Scholar 

  • Margulies D (2007) Spawning and early development of captive yellowfin tuna (Thunnus albacares). Fish Bull 105:249–265

    Google Scholar 

  • Martínez del Rio C, Wolf N, Carleton SA, Gannes LZ (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111. doi:10.1111/j.1469-185X.2008.00064.x

    Article  Google Scholar 

  • McBride RS, Somarakis S, Fitzhugh GR et al (2013) Energy acquisition and allocation to egg production in relation to fish reproductive strategies. Fish Fish. doi:10.1111/faf.12043

    Article  Google Scholar 

  • Ménard F, Labrune C, Shin YJ et al (2006) Opportunistic predation in tuna: a size-based approach. Mar Ecol Prog Ser 323:223–231

    Article  Google Scholar 

  • Ménard F, Lorrain A, Potier M, Marsac F (2007) Isotopic evidence of distinct feeding ecologies and movement patterns in two migratory predators (yellowfin tuna and swordfish) of the western Indian Ocean. Mar Biol 15357:141–152

    Article  Google Scholar 

  • Naqvi SWA, Naik H, Pratihary A et al (2006) Coastal versus open-ocean denitrification in the Arabian Sea. Biogeosciences 3:621–633

    Article  CAS  Google Scholar 

  • Nesis KN, Burgess LA, Levitov BS (1987) Cephalopods of the world: squids, cuttlefishes, octopuses, and allies. T.F.H. Publications Inc., Neptune City

    Google Scholar 

  • Olson RJ, Boggs CH (1986) Apex predation by yellowfin tuna (Thunnus albacares)—independent estimates from gastric evacuation and stomach contents, bioenergetics, and cesium concentrations. Can J Fish Aquat Sci 43:1760–1775

    Article  Google Scholar 

  • Olson RJ, Popp BN, Graham BS et al (2010) Food-web inferences of stable isotope spatial patterns in copepods and yellowfin tuna in the pelagic eastern Pacific Ocean. Prog Oceanogr 86:124–138

    Article  Google Scholar 

  • Popp BN, Graham BS, Olson RJ, Hannides CCS et al (2007) Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids. In: Dawson T, Siegwolf R (eds) Stable isotopes as indicators of ecological change. Elsevier Academic Press, Amsterdam, pp 173–190

    Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Article  Google Scholar 

  • Potier M, Marsac F, Lucas R et al (2004) Feeding partitioning among tuna taken in surface and mid-water layers: the case of yellowfin (Thunnus albacares) and bigeye (T. obesus) in the Western Tropical Indian Ocean. West Indian Ocean J Mar Sci 3:51–62

    Google Scholar 

  • Potier M, Marsac F, Cherel Y et al (2007) Forage fauna in the diet of three large pelagic fishes (lancetfish, swordfish and yellowfin tuna) in the western equatorial Indian Ocean. Fish Res 83:60–72

    Article  Google Scholar 

  • Potier M, Romanov E, Cherel Y et al (2008) Spatial distribution of Cubiceps pauciradiatus (Perciformes: Nomeidae) in the tropical Indian Ocean and its importance in the diet of large pelagic fishes. Aquat Living Resour 21:123–134

    Article  Google Scholar 

  • Potts G, Wootton R (1984) Fish Reproduction: Strategies and Tactics. Academic Press, London, p 1984

    Google Scholar 

  • Roger C (1994) Relationships among yellowfin and skipjack tuna, their prey-fish and plankton in the tropical western Indian Ocean. Fish Oceanogr 3:133–141

    Article  Google Scholar 

  • Romanov E, Potier M, Zamorov V, Ménard F (2009) The swimming crab Charybdis smithii: distribution, biology and trophic role in the pelagic ecosystem of the western Indian Ocean. Mar Biol 156:1089–1107

    Article  Google Scholar 

  • Schaefer (1998) Reproductive biology of yellowfin tuna (Thunnus albacares) in the eastern Pacific Ocean. Inter-American Tropical Tuna Commmission 21

  • Schaefer KM, Fuller DW (2010) Vertical movements, behavior, and habitat of bigeye tuna (Thunnus obesus) in the equatorial eastern Pacific Ocean, ascertained from archival tag data. Mar Biol 157:2625–2642

    Article  Google Scholar 

  • Schmidt K, McClelland JW, Mente E et al (2004) Trophic-level interpretation based on δ15N values: implications of tissue-specific fractionation and amino acid composition. Mar Ecol Prog Ser 266:43–58

    Article  CAS  Google Scholar 

  • Schott FA, Dengler M, Schoenefeldt R (2002) The shallow overturning circulation of the Indian Ocean. Prog Oceanogr 53:57–103

    Article  Google Scholar 

  • Schott FA, Xie SP, McCreary JP (2009) Indian ocean circulation and climate variability. Rev Geophys 47:1–31. doi:10.1029/2007RG000245

    Article  Google Scholar 

  • Smale MJ, Watson G, Hecht T (1995) Otolith atlas of southern African marine fishes. Ichthyological monographs. J/L/B/Smith Institute of Ichthyology, Grahamstown

    Book  Google Scholar 

  • Smith MM, Heemstra PC (1986) Smith’s sea fishes. Macmillan, Johannesburg

    Book  Google Scholar 

  • Stearns S (1992) The evolution of life histories. Oxford University Press, New York

    Google Scholar 

  • Tieszen LL, Boutton TW, Tesdahl KG, Slade NA (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57:32–37

    Article  CAS  Google Scholar 

  • Tregouboff G, Rose M (1978) Manuel de Planctonologie Méditerranéenne. CNRS, Paris

    Google Scholar 

  • Vipin PM, Ravi R, Jose Fernandez T et al (2012) Distribution of myctophid resources in the Indian Ocean. Rev Fish Biol Fish 22:423–436. doi:10.1007/s11160-011-9244-4

    Article  Google Scholar 

  • Wieggert JD, Murtugudde RG, Christian JR (2006) Annual ecosytem variability in the tropical Indian Ocean: results of a couples bio-physical ocean general circulation model. Deep Sea Res 53:644–676

    Article  Google Scholar 

  • Wootton R (1998) Ecology of teleost fishes. Springer, New York

    Google Scholar 

  • Zudaire I, Murua H, Grande M et al (2013a) Fecundity regulation strategy of the yellowfin tuna (Thunnus albacares) in the Western Indian Ocean. Fish Res 138:80–88

    Article  Google Scholar 

  • Zudaire I, Murua H, Grande M, Bodin N (2013b) Reproductive potential of Yellowfin Tuna (Thunnus albacares) in the western Indian Ocean. Fish Bull 111:252–264

    Article  Google Scholar 

  • Zudaire I, Murua H, Grande M et al (2014) Accumulation and mobilization of lipids in relation to reproduction of yellowfin tuna (Thunnus albacares) in the Western Indian Ocean. Fish Res 160:50–59

    Article  Google Scholar 

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Acknowledgments

We thank Dr. Y. Cherel for his assistance in identifying cephalopod species using small-sized beaks, X. Salaberria for his help in processing the samples, and J. Murua, G. Ocio, and A. Sanchez for the onboard collection of the samples. We also thank Dr. J.Alpine for her great professional proof reading service. This research benefited from the financial support of the Department of Agriculture, Fisheries and Food of the Basque Government, and the Pesquería Vasco Montañesa S.A. (PEVASA) fishing company. This work was partly funded by a Ph.D. grant of I. Zudaire Balerdi from the Fundación Centros Tecnológicos Iñaki Goenaga and Basque Government Postdoctoral grant. We are also grateful for the contribution received from the EMOTION Project (ANR JSV7 007 01). The experiments complied with the current laws of the countries in which they were performed. The authors declare that they have no conflicts of interest. This paper is contribution nº 734 from AZTI (Marine Research Department).

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Authors and Affiliations

  1. IKERBASQUE, Basque Foundation for Science, Maria Diaz de Haro, 3-6°, 48013, Bilbao, Bizkaia, Spain

    Iker Zudaire

  2. AZTI - Tecnalia, Marine Research Division, Herrera Kaia-Portu aldea z/g, 20110, Pasaia, Gipuzkoa, Spain

    Iker Zudaire, Hilario Murua, Maitane Grande & Nicolas Goñi

  3. IRD - UMR 248 MARBEC CNRS/Ifremer/IRD/UM, Av. Jean Monnet, BP 171, 34200, Sète, France

    Iker Zudaire & Michel Potier

  4. IRD - MIO, Aix-Marseille Université/CNRS/IRD/Université de Toulon, 13288, Marseille, France

    Frédéric Ménard

  5. IRD - UMR 248 MARBEC CNRS/Ifremer/IRD/UM, SFA, Fishing Port, BP 570, Victoria, Mahé, Seychelles

    Emmanuel Chassot & Nathalie Bodin

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  1. Iker Zudaire
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  2. Hilario Murua
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Correspondence to Iker Zudaire.

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Zudaire, I., Murua, H., Grande, M. et al. Variations in the diet and stable isotope ratios during the ovarian development of female yellowfin tuna (Thunnus albacares) in the Western Indian Ocean. Mar Biol 162, 2363–2377 (2015). https://doi.org/10.1007/s00227-015-2763-0

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