Skip to main content

Advertisement

SpringerLink
Log in

Pre-spawning habitat use of Atlantic bluefin tuna (Thunnus thynnus) inferred from stable isotope analysis

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

Abstract

Atlantic bluefin tuna (ABFT; Thunnus thynnus) spawn primarily in the Gulf of Mexico and Mediterranean Sea, but migrate to foraging habitats throughout the North Atlantic where they are the target of commercial and recreational fisheries. Their natal origin has been characterized through otolith oxygen isotope analysis to link fish on both spawning grounds and foraging habitats to their spawning ground origins, but connectivity on a shorter, seasonal timescale is still not completely understood. Nitrogen isoscapes in the North Atlantic include a distinct separation of productive, nearshore and more oligotrophic open ocean foraging habitats. We used linear discriminant analysis of bulk nitrogen isotope data to estimate the percent of ABFT that occupied shelf or open ocean foraging habitats prior to capture on eastern and western Atlantic spawning grounds. ABFT in the Gulf of Mexico were mainly classified as previous shelf foragers (91%), while ABFT associated with eastern Atlantic spawning grounds primarily had an open ocean/Mediterranean Sea classification (96% Morocco, 79% Strait of Gibraltar, 91% Balearic Sea, 100% Adriatic Sea). Amino acid nitrogen isotope data of ABFT from the Gulf of Mexico confirmed that observed bulk nitrogen isotope differences were due to baseline rather than trophic variability and source amino acid values generally aligned most closely with literature values from shelf and slope waters rather than open ocean habitats. These data provide insight into the foraging habitats that support eastern and western Atlantic spawning assemblages.

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

Data availability

The datasets used in this manuscript are available from the corresponding author on request.

References

  • Aarestrup K, Baktoft H, Birnie-Gauvin K, Sundelöf A, Cardinale M, Quilez-Badia G, Onandia I, Casini M, Nielsen EE, Koed A, Alemany F, MacKenzie BR (2022) First tagging data on large Atlantic bluefin tuna returning to Nordic waters suggest repeated behaviour and skipped spawning. Sci Rep 12:11772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abascal FJ, Medina A, de la Serna JM, Godoy D, Aranda G (2016) Tracking bluefin tuna reproductive migration into the Mediterranean Sea with electronic pop-up satellite archival tags using two tagging procedures. Fish Oceanogr 25:54–66

    Article  Google Scholar 

  • Abrantes KG, Barnett A (2011) Intrapopulation variations in diet and habitat use in a marine apex predator, the broadnose sevengill shark Notorynchus cepedianus. Mar Ecol Prog Ser 442:133–148

    Article  Google Scholar 

  • Ackman RG, Hooper SN, Epstein S, Kelleher M (1972) Wax esters of barracudina lipid: a potential replacement for sperm whale oil. J Am Oil Chem Soc 49:378–382

    Article  CAS  Google Scholar 

  • Anonymous (2017) Report of the 2017 ICCAT bluefin stock assessment meeting. ICCAT Col Vol Sci Pap 76:2372–2535

    Google Scholar 

  • Aranda G, Abascal FJ, Varela JL, Medina A (2013) Spawning behaviour and post-spawning migration patterns of Atlantic bluefin tuna (Thunnus thynnus) ascertained from satellite archival tags. PLoS ONE 8:e76445. https://doi.org/10.1371/journal.pone.0076445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Austin RS (2022) Age, growth, foraging, and trophic ecology of bigeye (Thunnus obesus) and yellowfin (Thunnus albacares) tuna in continental shelf and slope regions of the northeast U.S. Electronic Theses and Dissertations. 3556. https://digitalcommons.library.umaine.edu/etd/3556

  • Baglin RE (1982) Reproductive biology of western Atlantic bluefin tuna. Fish Bull 80:121–134

    Google Scholar 

  • Barría C, Coll M, Navarro J (2015) Unravelling the ecological role and trophic relationships of uncommon and threatened elasmobranchs in the western Mediterranean Sea. Mar Ecol Prog Ser 539:225–240

    Article  Google Scholar 

  • Battaglia P, Andaloro F, Consoli P, Esposito V, Malara D, Musolino S, Pedà C, Romeo T (2013) Feeding habits of the Atlantic bluefin tuna, Thunnus thynnus (L. 1758), in the central Mediterranean Sea (Strait of Messina). Helgol Mar Res 67:97–107

    Article  Google Scholar 

  • Block BA, Dewar H, Blackwell SB, Williams TD, Prince ED, Farwell CJ, Boustany A, Teo SLH, Seitz A, Walli A, Fudge D (2001) Migratory movements, depth preferences, and thermal biology of Atlantic bluefin tuna. Science 293:1310–1314

    Article  CAS  PubMed  Google Scholar 

  • Block BA, Teo SLH, Walli A, Boustany A, Stokesbury MJW, Farwell CJ, Weng KC, Dewar H, Williams TD (2005) Electronic tagging and population structure of Atlantic bluefin tuna. Nature 434:1121–1127

    Article  CAS  PubMed  Google Scholar 

  • Bode A, Alvarez-Ossorio M, Cunha M, Garrido S, Peleteiro J, Porteiro C, Valdes L, Varela M (2007) Stable nitrogen isotope studies of the pelagic food web on the Atlantic shelf of the Iberian Peninsula. Prog Oceanogr 74:115–131

    Article  Google Scholar 

  • Bradley CJ, Wallsgrove NJ, Choy CA, Drazen JC, Hetherington ED, Hoen DK, Popp BN (2015) Trophic position estimates of marine teleosts using amino acid compound specific isotopic analysis. Limnol Oceanogr Methods 13:476–493

    Article  Google Scholar 

  • Brand WA (2011) New reporting guidelines for stable isotopes—an announcement to isotope users. Isotopes Environ Health Stud 47:535–536

    Article  CAS  PubMed  Google Scholar 

  • Brill RW (1996) Selective advantages conferred by the high performance physiology of tunas, billfishes, and dolphin fish. Comp Biochem Physiol 113:3–15

    Article  Google Scholar 

  • Butler MJA, Mason JA (1978) Behavioural studies on impounded bluefin tuna. Col Vol Sci Pap ICCAT 7:379–382

    Google Scholar 

  • Butler CM, Rudershausen PJ, Buckel JA (2010) Feeding ecology of Atlantic bluefin tuna (Thunnus thynnus) in North Carolina: diet, daily ration, and consumption of Atlantic menhaden (Brevoortia tyrannus). Fish Bull 108:56–69

    Google Scholar 

  • Butler CM, Logan JM, Provaznik JM, Hoffmayer ER, Staudinger MD, Quattro JM, Roberts MA, Ingram GW Jr, Pollack AG, Lutcavage ME (2015) Atlantic bluefin tuna Thunnus thynnus feeding ecology in the northern Gulf of Mexico: a preliminary description of diet from the western Atlantic spawning grounds. J Fish Biol 86:365–374

    Article  CAS  PubMed  Google Scholar 

  • Cardona L, Álvarez de Quevedo I, Borrell A, Aguilar A (2012) Massive consumption of gelatinous plankton by Mediterranean apex predators. PLoS ONE 7:e31329. https://doi.org/10.1371/journal.pone.0031329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carey FG, Teal JM (1966) Heat conservation in tuna fish muscle. Proc Natl Acad Sci USA 56:1464–1469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carlsson J, McDowell JR, Carlsson JEL, Graves JE (2007) Genetic identity of YOY bluefin tuna from the eastern and Western Atlantic spawning areas. J Hered 98:23–28

    Article  CAS  PubMed  Google Scholar 

  • Cermeño P, Quílez-Badia G, Ospina-Alvarez A, Sainz-Trápaga S, Boustany AM, Seitz AC, Tudela S, Block BA (2015) Electronic tagging of Atlantic bluefin tuna (Thunnus thynnus, L.) reveals habitat use and behaviors in the Mediterranean Sea. PLoS ONE 10:e0116638. https://doi.org/10.1371/journal.pone.0116638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapman EW, Jørgensen C, Lutcavage ME (2011) Atlantic bluefin tuna (Thunnus thynnus): a state dependent energy allocation model for growth, maturation, and reproductive investment. Can J Fish Aquat Sci 68:1934–1951

    Article  Google Scholar 

  • Chase B (2002) Differences in diet of Atlantic bluefin tuna (Thunnus thynnus) at five seasonal feeding grounds on the New England continental shelf. Fish Bull 100:168–180

    Google Scholar 

  • Chouvelon T, Spitz J, Caurant F, Mèndez-Fernandez P, Chappuis A, Laugier F, Le Goff E, Bustamante P (2012) Revisiting the use of δ15N in meso-scale studies of marine food webs by considering spatio-temporal variations in stable isotopic signatures. The case of an open ecosystem: the Bay of Biscay (north-east Atlantic). Prog Oceanogr 101:95–102

    Article  Google Scholar 

  • Chouvelon T, Chappuis A, Bustamente P, Lefebvre S, Mornet F, Guillou G, Violamer L, Dupuy C (2014) Trophic ecology of European sardine Sardina pilchardus and European anchovy Engraulis encrasicolus in the Bay of Biscay (north-east Atlantic) inferred from δ13C and δ15N values of fish and identified mesozooplanktonic organisms. J Sea Res 85:277–291

    Article  Google Scholar 

  • Choy CA, Davison PC, Drazen JC, Flynn A, Gier EJ, Hoffmann JC, McClain-Counts JP, Miller TW, Popp BN, Ross SW, Sutton TT (2012) Global trophic position comparison of two dominant mesopelagic fish families (Myctophidae, Stomiidae) using amino acid nitrogen isotopic analyses. PLoS ONE 7:e50133. https://doi.org/10.1371/journal.pone.0050133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choy CA, Popp BN, Hannides CCS, Drazen JC (2015) Trophic structure and food resources of epipelagic and mesopelagic fishes in the North Pacific Subtropical Gyre ecosystem inferred from nitrogen isotopic compositions. Limnol Oceanogr 60:1156–1171

    Article  Google Scholar 

  • Collins MA, Xavier JC, Johnston NM, North AW, Enderlein P, Tarling GA, Waluda CM, Hawker EJ, Cunningham NJ (2008) Patterns in the distribution of myctophid fish in the northern Scotia Sea ecosystem. Polar Biol 31:837–851

    Article  Google Scholar 

  • Conley KR, Lombard F, Sutherland KR (2018) Mammoth grazers on the ocean’s minuteness: a review of selective feeding using mucous meshes. Proc R Soc B-Biol Sci 285:20180056

    Article  Google Scholar 

  • Corriero A, Karakulak S, Santamaria N, Deflorio M, Spedicato D, Addis P, Desantis S, Cirillo F, Fenech-Farrugia A, Vassallo-Agius R, de la Serna J, Oray Y, Cau A, Megalofonou P, De Metrio G (2005) Size and age at sexual maturity of female bluefin tuna (Thunnus thynnus L. 1758) from the Mediterranean Sea. J Appl Ichthyol 21:483–486

    Article  Google Scholar 

  • Corriero A, Heinisch G, Rosenfeld H, Katavic I, Passantino L, Zupa R, Grubišić L, Lutcavage ME (2020) Review of sexual maturity in Atlantic bluefin tuna, Thunnus thynnus (Linnaeus, 1758). Rev Fish Sci Aquac 28:182–192

    Article  Google Scholar 

  • Costalago D, Navarro J, Álvarez-Calleja I, Palomera I (2012) Ontogenetic and seasonal changes in the feeding habits and trophic levels of two small pelagic fish species. Mar Ecol Prog Ser 460:169–181

    Article  Google Scholar 

  • de la Serna JM, Godoy MD, Olaso I, Zabala J, Majuelos E, Báez JC (2012) Preliminary study on the feeding of bluefin tuna (Thunnus thynnus) in the Mediterranean and the Strait of Gibraltar area. ICCAT Collect Vol Sci Pap 68:115–132

    Google Scholar 

  • Décima M, Stukel MR, López-López L, Landry MR (2019) The unique ecological role of pyrosomes in the Eastern Tropical Pacific. Limnol Oceanogr 64:728–743

    Article  Google Scholar 

  • Dickhut RM, Deshpande AD, Cincinelli A, Cochran MA, Corsolini S, Brill RW, Secor DH, Graves JE (2009) Atlantic bluefin tuna (Thunnus thynnus) population dynamics delineated by organochlorine tracers. Environ Sci Technol 43:8522–8527

    Article  CAS  PubMed  Google Scholar 

  • Domingues R, Goni G, Bringas F, Muhling B, Lindo-Atichati D, Walter J (2016) Variability of preferred environmental conditions for Atlantic bluefin tuna (Thunnus thynnus) larvae in the Gulf of Mexico during 1993–2011. Fish Oceanogr 25:320–336

    Article  Google Scholar 

  • Fitzgibbon Q, Seymour R, Ellis D, Buchanan J (2007) The energetic consequence of specific dynamic action in southern bluefin tuna Thunnus maccoyii. J Exp Biol 210:290–298

    Article  CAS  PubMed  Google Scholar 

  • Fromentin JM, Lopuszanski D (2014) Migration, residency, and homing of bluefin tuna in the western Mediterranean Sea. ICES J Mar Sci 71:510–518

    Article  Google Scholar 

  • Fromentin JM, Powers JE (2005) Atlantic bluefin tuna: population dynamics, ecology, fisheries and management. Fish Fish 6:281–306

    Article  Google Scholar 

  • Fry B (1988) Food web structure on Georges Bank from stable C, N, and S isotopic compositions. Limnol Oceanogr 33:1182–1190

    Article  CAS  Google Scholar 

  • Fry B (2006) Stable isotope ecology. Springer, New York

    Book  Google Scholar 

  • Galuardi B, Royer F, Golet W, Logan J, Neilson J, Lutcavage M (2010) Complex migration routes of Atlantic bluefin tuna question current population structure paradigm. Can J Fish Aquat Sci 67:966–976

    Article  Google Scholar 

  • Gartner J, Sulak K, Ross S, Necaise A (2008) Persistent near-bottom aggregations of mesopelagic animals along the North Carolina and Virginia continental slopes. Mar Biol 153:825–841

    Article  Google Scholar 

  • Glaser SM (2010) Interdecadal variability in predator–prey interactions of juvenile North Pacific albacore in the California Current System. Mar Ecol Prog Ser 414:209–221

    Article  Google Scholar 

  • Goetsch C, Conners MG, Budge SM, Mitani Y, Walker WA, Bromaghin JF, Simmons SE, Reichmuth C, Costa DP (2018) Energy-rich mesopelagic fishes revealed as a critical prey resource for a deep-diving predator using quantitative fatty acid signature analysis. Front Mar Sci. https://doi.org/10.3389/fmars.2018.00430

    Article  Google Scholar 

  • Graham BS (2008) Trophic dynamics and movements of tuna in the tropical Pacific Ocean inferred from stable isotope analyses. Ph.D. Thesis, University of Hawaii, Manoa, Hawaii, USA

  • Graham BS, Koch P, Newsome S, McMahon KW, Aurioles D (2010) Using isoscapes to trace the movements and foraging behavior of top predators in oceanic ecosystems. In: West JB, Bowen GJ, Dawson TE, Tu KP (eds) Isoscapes: understanding movement, pattern and processes on Earth through isotope mapping. Springer, New York

    Google Scholar 

  • Haas H, Freeman C, Logan J, Deegan L, Gaines E (2009) Examining mummichog growth and movement: are some individuals making intra-season migrations to optimize growth? J Exp Mar Biol Ecol 369:8–16

    Article  Google Scholar 

  • Heady WN, Moore JW (2013) Tissue turnover and stable isotope clocks to quantify resource shifts in anadromous rainbow trout. Oecologia 172:21–34

    Article  PubMed  Google Scholar 

  • Hernández CM, Richardson DE, Rypina II, Chen K, Marancik KE, Shulzitski K, Llopiz JK (2022) Support for the Slope Sea as a major spawning ground for Atlantic bluefin tuna: evidence from larval abundance, growth rates, and particle-tracking simulations. Can J Fish Aquat Sci 79:814–824

    Article  Google Scholar 

  • Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326

    Article  PubMed  Google Scholar 

  • Hobson KA (2007a) An isotopic exploration of the potential of avian tissues to track changes in terrestrial and marine ecosystems. In: Dawson TE, Siegwolf RTW (eds) Stable isotopes as indicators of ecological change. Elsevier, Amsterdam

    Google Scholar 

  • Hobson KA (2007b) Isotopic tracking of migrant wildlife. In: Michener R, Lajtha K (eds) Stable isotopes in ecology and environmental science. Blackwell Publishing Ltd, Malden

    Google Scholar 

  • Karakulak FS, Salman A, Oray IK (2009) Diet composition of bluefin tuna (Thunnus thynnus L. 1758) in the Eastern Mediterranean Sea. Turkey J Appliced Ichthyol 25:757–761

    Article  Google Scholar 

  • Keller HR, Hirons AC, Kerstetter DW (2016) Combined stomach content and δ13C/δ15N analyses of oilfish, escolar, snake mackerel and lancetfish in the western North Atlantic. Mar Ecol 37:727–736

    Article  CAS  Google Scholar 

  • Kerr LA, Whitener ZT, Cadrin SX, Morse MR, Secor DH, Golet W (2020) Mixed stock origin of Atlantic bluefin tuna in the U.S. rod and reel fishery (Gulf of Maine) and implications for fisheries management. Fish Res 224:105461

    Article  Google Scholar 

  • Knapp JM, Aranda G, Medina A, Lutcavage M (2014) Comparative assessment of the reproductive status of female Atlantic bluefin tuna from the Gulf of Mexico and the Mediterranean Sea. PLoS ONE 9:e98233. https://doi.org/10.1371/journal.pone.0098233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Korsmeyer KE, Dewar H (2001) Tuna metabolism and energetics. In: Block BA, Stevens ED (eds) Tuna: physiology, ecology, and evolution. Academic Press, San Diego, pp 35–78

    Chapter  Google Scholar 

  • Korsmeyer K, Dewar H, Lai N, Graham J (1996) The aerobic capacity of tunas: adaptation for multiple metabolic demands. Comp Biochem Physiol 113:17–24

    Article  Google Scholar 

  • Laiz-Carrión R, Gerard T, Suca JJ, Malca E, Uriarte A, Quintanilla JM, Privoznik S, Llopiz JK, Lamkin J, García A (2019) Stable isotope analysis indicates resource partitioning and trophic niche overlap in larvae of four tuna species in the Gulf of Mexico. Mar Ecol Prog Ser 619:53–68

    Article  Google Scholar 

  • Lavoie RA, Hebert CE, Rail JF, Braune BM, Yumvihoze E, Hill LG, Lean DRS (2010) Trophic structure and mercury distribution in a Gulf of St. Lawrence (Canada) food web using stable isotope analysis. Sci Total Environ 408:5529–5539

    Article  CAS  PubMed  Google Scholar 

  • Le-Alvarado M, Romo-Curiel AE, Sosa-Nishizaki O, Hernández-Sánchez O, Barbero L, Herzka SZ (2021) Yellowfin tuna (Thunnus albacares) foraging habitat and trophic position in the Gulf of Mexico based on intrinsic isotope tracers. PLoS ONE 16:e0246082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leanza U (1993) The delimitation of the continental shelf of the Mediterranean Sea. Int J Mar Coast Law 8:373–396

    Article  Google Scholar 

  • Logan J (2009) Tracking diet and movement of Atlantic bluefin tuna (Thunnus thynnus) using carbon and nitrogen stable isotopes. University of New Hampshire, Ph.D. Thesis, University of New Hampshire, Durham, New Hampshire, USA

  • Logan JM, Lutcavage ME (2013) Assessment of trophic dynamics of cephalopods and large pelagic fishes in the central North Atlantic Ocean using stable isotope analysis. Deep-Sea Res Part II 95:63–73

    Article  CAS  Google Scholar 

  • Logan JM, Rodriguez-Marín E, Goñi N, Barreiro S, Arrizabalaga H, Golet W, Lutcavage ME (2011) Diet of young Atlantic bluefin tuna (Thunnus thynnus) in eastern and western Atlantic foraging grounds. Mar Biol 158:73–85

    Article  Google Scholar 

  • Logan JM, Toppin R, Smith S, Galuardi B, Porter J, Lutcavage ME (2013) Contribution of cephalopod prey to the diet of large pelagic fish predators in the central North Atlantic Ocean. Deep-Sea Res II 95:74–82

    Article  Google Scholar 

  • Logan JM, Golet W, Lutcavage ME (2015) Diet and condition of Atlantic bluefin tuna (Thunnus thynnus) in the Gulf of Maine, 2004–2008. Environ Biol Fishes 98:1411–1430

    Article  Google Scholar 

  • Logan JM, Pethybridge H, Lorrain A, Somes CJ, Allain V, Bodin N, Choy CA, Duffy L, Goñi N, Graham B, Langlais C, Ménard F, Olson R, Young J (2020) Global patterns and inferences of tuna movements and trophodynamics from stable isotope analysis. Deep Sea Res Part II Top Stud Oceanogr 175:104775

    Article  CAS  Google Scholar 

  • Logan JM, Golet W, Smith SC, Neilson J, Van Guelpen L (2021) Broadbill swordfish (Xiphias gladius) foraging and vertical movements in the north-west Atlantic. J Fish Biol 99:557–568

    Article  PubMed  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 

  • Madigan DJ, Litvin SY, Popp BN, Carlisle AB, Farwell CJ, Block BA (2012) Tissue turnover rates and isotopic trophic discrimination factors in the endothermic teleost, Pacific bluefin tuna (Thunnus orientalis). PLoS ONE 7:e49220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Madigan DJ, Baumann Z, Carlisle AB, Hoen DK, Popp BN, Dewar H, Snodgrass OE, Block BA, Fisher NS (2014) Reconstructing transoceanic migration patterns of Pacific bluefin tuna using a chemical tracer toolbox. Ecology 95:1674–1683

    Article  PubMed  Google Scholar 

  • Malek AJ, Collie JS, Taylor DL (2016) Trophic structure of a coastal fish community determined with diet and stable isotope analyses. J Fish Biol 89:1513–1536

    Article  CAS  PubMed  Google Scholar 

  • Malpica-Cruz L, Herzka SZ, Sosa-Nichizaki O, Escobedo-Olvera MA (2013) Tissue-specific stable isotope ratios of shortfin mako (Isurus oxyrinchus) and white (Carcharodon carcharias) sharks as indicators of size-based differences in foraging habitat and trophic level. Fish Oceanogr 22:429–445

    Article  Google Scholar 

  • Martínez-Baena F, Navarro J, Albo-Puigserver M, Palomera I, Rosas-Luis R (2016) Feeding habits of the short-finned squid Illex coindetii in the western Mediterranean Sea using combined stomach content and isotopic analysis. J Mar Biol Assoc UK 96:1235–1242

    Article  Google Scholar 

  • Mather FJ, Mason Jr. JM, Jones AC (1995) Historical document: life history and fisheries of Atlantic bluefin tuna. NOAA Technical Memorandum NMFS-SEFSC-370. Miami, Fla, pp 165

  • Matley JK, Fisk AT, Tobin AJ, Heupel MR, Simpfendorfer CA (2016) Diet–tissue discrimination factors and turnover of carbon and nitrogen stable isotopes in tissues of an adult predatory coral reef fish, Plectropomus leopardus. Rapid Commun Mass Spectrom 30:29–44

    Article  CAS  PubMed  Google Scholar 

  • Matthews FD, Damkaer DM, Knapp LW, Collette BB (1977) Food of western North Atlantic tunas (Thunnus) and lancetfishes (Alepisaurus). U.S. Department of Commerce NOAA Technical Report NMFS SSRF-706, pp 1–19

  • McClelland JW, Holl CM, Montoya JP (2003) Relating low δ15N values of zooplankton to N2-fixation in the tropical North Atlantic: insights provided by stable isotope ratios of amino acids. Deep-Sea Res Part Oceanogr Res Pap 50:849–861

    Article  CAS  Google Scholar 

  • McMahon KW, McCarthy MD (2016) Embracing variability in amino acid δ15N fractionation: mechanisms, implications, and applications for trophic ecology. Ecosphere 7:e01511

    Article  Google Scholar 

  • McMahon KW, Newsome SD (2019) Amino acid isotope analysis: a new frontier in studies of animal migration and foraging ecology. In: Hobson KA, Wassenaar LI (eds) Tracking animal migrations with stable isotopes, 2nd edn. Academic Press, San Diego, pp 173–190

    Chapter  Google Scholar 

  • McMahon K, Johnson B, Ambrose W (2005) Diet and movement of the killifish, Fundulus heteroclitus, in a Maine salt marsh assessed using gut contents and stable isotope analyses. Estuaries 28:966–973

    Article  Google Scholar 

  • McMahon KW, Hamady LL, Thorrold SR (2013) A review of ecogeochemistry approaches to estimating movements of marine animals. Limnol Oceanogr 58:697–714

    Article  CAS  Google Scholar 

  • Mellon-Duval C, Harmelin-Vivien M, Métral L, Loizeau V, Mortreux S, Roos D, Fromentin JM (2017) Trophic ecology of the European hake in the Gulf of Lions, northwestern Mediterranean Sea. Sci Mar 81:7–18

    Article  Google Scholar 

  • Mills KE, Pershing AJ, Brown CJ, Chen Y, Chiang FS, Holland DS, Lehuta S, Nye JA, Sun JC, Thomas AC, Wahle RA (2013) Fisheries management in a changing climate: lessons from the 2012 ocean heat wave in the Northwest Atlantic. Oceanography 26:191–195

    Article  Google Scholar 

  • Mompeán C, Bode A, Gier E, McCarthy MD (2016) Bulk vs. amino acid stable N isotope estimations of metabolic status and contributions of nitrogen fixation to size-fractionated zooplankton biomass in the subtropical N Atlantic. Deep Sea Res I 114:137–148

    Article  Google Scholar 

  • Mourente G, Quintero O, Cañavate JP (2015) Trophic links of Atlantic bluefin tuna (Thunnus thynnus L.) inferred by fatty acid signatures. J Exp Mar Biol Ecol 463:49–56

    Article  CAS  Google Scholar 

  • Munroe SE, Heupel MR, Fisk AT, Logan M, Simpfendorfer CA (2015) Regional movement patterns of a small-bodied shark revealed by stable-isotope analysis. J Fish Biol 86:1567–1586

    Article  CAS  PubMed  Google Scholar 

  • Nakamura Y, Horinouchi M, Shibuno T, Tanaka Y, Miyajima T, Koike I, Kurokura H, Sano M (2008) Evidence of ontogenetic migration from mangroves to coral reefs by black-tail snapper Lutjanus fulvus: stable isotope approach. Mar Ecol Prog Ser 355:257–266

    Article  Google Scholar 

  • Navarro J, Albo-Puigserver M, Serra PE, Sáez-Liante R, Coll M (2020) Trophic strategies of three predatory pelagic fish coexisting in the north-western Mediterranean Sea over different time spans. Estuar Coast Shelf Sci 246:107040

    Article  Google Scholar 

  • Nielsen JM, Popp BN, Winder M (2015) Meta-analysis of amino acid stable nitrogen isotope ratios for estimating trophic position in marine organisms. Oecologia 178:631–642

    Article  PubMed  Google Scholar 

  • Olafsdottir D, MacKenzie B, Chosson-P V, Ingimundardottir T (2016) Dietary evidence of mesopelagic and pelagic foraging by Atlantic bluefin tuna (Thunnus thynnus L) during autumn migrations to the Iceland Basin. Front Mar Sci. https://doi.org/10.3389/fmars.2016.00108

    Article  Google Scholar 

  • Phillips ND, Smith EAE, Newsome SD, Houghton JDR, Carson CD, Alfaro-Shigueto J, Mangel JC, Eagling LE, Kubicek L, Harrod C (2020) Bulk tissue and amino acid stable isotope analyses reveal global ontogenetic patterns in ocean sunfish trophic ecology and habitat use. Mar Ecol Prog Ser 633:127–140

    Article  CAS  Google Scholar 

  • Pleizier NK, Campana SE, Schallert RJ, Wilson SG, Block BA (2012) Atlantic bluefin tuna (Thunnus thynnus) diet in the Gulf of St. Lawrence and on the Eastern Scotian Shelf. J Northwest Atl Fish Sci 44:67–76

    Article  Google Scholar 

  • Popp B, Graham B, Olson R, Hannides C, Lott M, López-Ibarra G, Galván-Magaña F, Fry B (2007) Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids. In: Dawson T, Seigwolf R (eds) Isotopes as tracers of ecological change. Elsevier Academic Press, San Diego, pp 173–190

    Google Scholar 

  • R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Richardson DE, Marancik KE, Guyon JR, Lutcavage ME, Galuardi B, Lam CH, Walsh HJ, Wildes S, Yates DA, Hare JA (2016) Discovery of a spawning ground reveals diverse migration strategies in Atlantic bluefin tuna (Thunnus thynnus). Proc Natl Acad Sci 113:3299–3304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivas LR (1955) A comparison between giant bluefin tuna (Thunnus thynnus) from the Straits of Florida and the Gulf of Maine with reference to migration and population identity. Proc Gulf Caribb Fish Inst Seventh Annu Sess 7:133–149

    Google Scholar 

  • Rodgers K, Wing S (2008) Spatial structure and movement of blue cod Parapercis colias in Doubtful Sound, New Zealand, inferred from δ13C and δ15N. Mar Ecol Prog Ser 359:239–248

    Article  Google Scholar 

  • Rooker J, Bremer J, Block B, Dewar H, De Metrio G, Corriero A, Kraus R, Prince E, Rodríguez-Marín E, Secor D (2007) Life history and stock structure of Atlantic bluefin tuna (Thunnus thynnus). Rev Fish Sci 15:265–310

    Article  Google Scholar 

  • Rooker JR, Arrizabalaga H, Fraile I, Secor DH, Dettman DL, Abid N, Addis P, Deguara S, Karakulak FS, Kimoto A, Sakai O, Macías D, Santos MN (2014) Crossing the line: migratory and homing behaviors of Atlantic bluefin tuna. Mar Ecol Prog Ser 504:265–276

    Article  CAS  Google Scholar 

  • Rubenstein DR, Hobson KA (2004) From birds to butterflies: animal movement patterns and stable isotopes. Trends Ecol Evol 19:256–263

    Article  PubMed  Google Scholar 

  • Rumolo P, Bonanno A, Barra M, Fanelli E, Calabrò M, Genovese S, Ferreri R, Mazzola S, Basilone G (2016) Spatial variations in feeding habits and trophic levels of two small pelagic fish species in the central Mediterranean Sea. Mar Environ Res 115:65–77. https://doi.org/10.1016/j.marenvres.2016.02.004

    Article  CAS  PubMed  Google Scholar 

  • Rumolo P, Fanelli E, Barra M, Basilone G, Genovese S, Gherardi S, Ferreri R, Gargano A, Mazzola S, Bonanno A (2018) Trophic relationships between anchovy (Engraulis encrasicolus) and zooplankton in the Strait of Sicily (Central Mediterranean sea): a stable isotope approach. Hydrobiologia 821:41–56

    Article  CAS  Google Scholar 

  • Ryan C, Berrow SD, McHugh B, O’Donnell C, Trueman C, O’Connor I (2014) Prey preferences of sympatric fin (Balaenoptera physalus) and humpback (Megaptera novaeangliae) whales revealed by stable isotope mixing models. Mar Mammal Sci 40:242–258

    Article  Google Scholar 

  • Safina C (2016) Data do not support new claims about bluefin tuna spawning or abundance. Proc Natl Acad Sci USA 113:E4261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saito H, Murata M (1998) Origin of the monoene fats in the lipid of midwater fishes: relationship between the lipids of myctophids and those of their prey. Mar Ecol Prog Ser 168:21–33

    Article  CAS  Google Scholar 

  • Sara G, Sara R (2007) Feeding habits and trophic levels of bluefin tuna Thunnus thynnus of different size classes in the Mediterranean Sea. J Appl Ichthyol 23:122–127

    Article  Google Scholar 

  • Schmittner A, Somes CJ (2016) Complementary constraints from carbon (13C) and nitrogen (15N) isotopes on the glacial ocean’s soft-tissue biological pump. Paleoceanogr Paleoclimatol 31:669–693

    Article  Google Scholar 

  • Schram JB, Sorensen HL, Brodeur RD, Galloway AWE, Sutherland KR (2020) Abundance, distribution, and feeding ecology of Pyrosoma atlanticum in the Northern California Current. Mar Ecol Prog Ser 651:97–110

    Article  CAS  Google Scholar 

  • Seminoff JA, Benson SR, Arthur KE, Eguchi T, Dutton PH, Tapilatu RF, Popp BN (2012) Stable isotope tracking of endangered sea turtles: validation with satellite telemetry and δ15N analysis of amino acids. PLoS ONE 7(5):e37403. https://doi.org/10.1371/journal.pone.0037403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sherwood OA, Heikoop JM, Scott DB, Risk MJ, Guilderson TP, McKinney RA (2005) Stable isotopic composition of deep-sea gorgonian corals Primnoa spp.: a new archive of surface processes. Mar Ecol Prog Ser 301:135–148

    Article  CAS  Google Scholar 

  • Somes CJ, Schmittner A, Galbraith ED, Lehmann MF, Altabet MA, Montoya JP, Letelier RM, Mix AC, Bourbonnais A, Eby M (2010) Simulating the global distribution of nitrogen isotopes in the ocean. Glob Biogeochem Cycles 24:GB4019

    Article  Google Scholar 

  • Spiess AN (2014) Propagate: propagation of uncertainty. R package version 1.0–4. https://CRAN.R-project.org/package=propagate. Accessed May 2022

  • Stokesbury MJW, Teo SLH, Seitz A, O’Dor RK, Block BA (2004) Movement of Atlantic bluefin tuna (Thunnus thynnus) as determined by satellite tagging experiments initiated off New England. Can J Fish Aquat Sci 61:1976–1987

    Article  Google Scholar 

  • Suzuki K, Kasai A, Nakayama K, Tanaka M (2005) Differential isotopic enrichment and half-life among tissues in Japanese temperate bass (Lateolabrax japonicus) juveniles: implications for analyzing migration. Can J Fish Aquat Sci 62:671–678

    Article  Google Scholar 

  • Teo SLH, Boustany A, Dewar H, Stokesbury MJW, Weng KC, Beemer S, Seitz AC, Farwell CJ, Prince ED, Block BA (2007a) Annual migrations, diving behavior, and thermal biology of Atlantic bluefin tuna, Thunnus thynnus, on their Gulf of Mexico breeding grounds. Mar Biol 151:1–18

    Article  Google Scholar 

  • Teo SLH, Boustany AM, Block BA (2007b) Oceanographic preferences of Atlantic bluefin tuna, Thunnus thynnus, on their Gulf of Mexico breeding grounds. Mar Biol 152:1105–1119

    Article  Google Scholar 

  • Thomas SM, Crowther TW (2015) Predicting rates of isotopic turnover across the animal kingdom: a synthesis of existing data. J Anim Ecol 84:861–870

    Article  PubMed  Google Scholar 

  • Uriarte A, Prouzet P, Villamor B (1996) Bay of Biscay and Ibero Atlantic anchovy populations and their fisheries. Sci Mar 60:237–255

    Google Scholar 

  • Uriarte A, Laiz-Carrión R, Llopiz J, Quintanilla JM, Alemany F, García A (2016) Trophic position of Mediterranean bluefin tuna larvae estimated by different stable isotope analyses. In: XIX Iberian Symposium on Marine Biology Studies, Porto (Portugal). pp 5–9.

  • Varela JL, Larrañaga A, Medina A (2011) Prey-muscle carbon and nitrogen stable isotope discrimination factors in Atlantic bluefin tuna (Thunnus thynnus). J Exp Mar Biol Ecol 406:21–28

    Article  CAS  Google Scholar 

  • Varela JL, Rodríguez-Marín E, Medina A (2013) Estimating diets of pre-spawning Atlantic bluefin tuna from stomach content and stable isotope analyses. J Sea Res 76:187–192

    Article  Google Scholar 

  • Varela JL, Sorell JM, Macías D, Goñi N, Arrizabalaga H, Medina A (2018a) New insight into the trophic biology of age-0 Atlantic bluefin tuna in the western Mediterranean using stomach content and stable isotope analyses. Fish Res 208:274–285

    Article  Google Scholar 

  • Varela JL, Rojo-Nieto E, Sorell JM, Medina A (2018b) Using stable isotope analysis to assess trophic relationships between Atlantic bluefin tuna (Thunnus thynnus) and striped dolphin (Stenella coeruleoalba) in the Strait of Gibraltar. Mar Environ Res 139:57–63

    Article  CAS  PubMed  Google Scholar 

  • Varela JL, Sorell JM, Laiz-Carrión R, Baro I, Uriarte A, Macías D, Medina A (2019) Stomach content and stable isotope analyses reveal resource partitioning between juvenile bluefin tuna and Atlantic bonito in Alboran (SW Mediterranean). Fish Res 215:97–105

    Article  Google Scholar 

  • Varela JL, Spares AD, Stokesbury MJW (2020) Feeding ecology of Atlantic bluefin tuna (Thunnus thynnus) in the Gulf of Saint Lawrence. Canada Mar Environ Res 161:105087

    Article  CAS  PubMed  Google Scholar 

  • Varela JL, Medina A, Déniz S, Abascal FJ (2022) Feeding of Atlantic bluefin tuna Thunnus thynnus around the Canary Islands assessed from stomach content and stable isotope analyses. Mar Ecol Prog Ser 686:177–186

    Article  CAS  Google Scholar 

  • Walli A, Teo SLH, Boustany A, Farwell CJ, Williams T, Dewar H, Prince E, Block BA (2009) Seasonal movements, aggregations and diving behavior of Atlantic bluefin tuna (Thunnus thynnus) revealed with archival tags. PLoS ONE 4(7):e6151. https://doi.org/10.1371/journal.pone.0006151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walsh RG, He S, Yarnes CT (2014) Compound-specific δ13C and δ15N analysis of amino acids: a rapid, chloroformate-based method for ecological studies. Rapid Commun Mass Spectrom 28:96–108

    Article  CAS  PubMed  Google Scholar 

  • Walter JF III, Porch CE, Lauretta MV, Cass-Calay SL, Brown CA (2016) Implications of alternative spawning for bluefin tuna remain unclear. Proc Natl Acad Sci USA 113:E4259–E4260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • West JB, Bowen GJ, Dawson TE, Tu KP (2010) Isoscapes: Understanding movement, pattern, and processing on Earth through isotope mapping. Springer, New York

    Book  Google Scholar 

  • Wilson S, Jonsen I, Schallert R, Ganong J, Castleton M, Spares A, Boustany A, Stokesbury M, Block B (2015) Tracking the fidelity of Atlantic bluefin tuna released in Canadian waters to the Gulf of Mexico spawning grounds. Can J Fish Aquat Sci 72:1700–1717

    Article  Google Scholar 

  • Xue Y, Hu Z, Kumar A, Banzon V, Smith TM, Rayner NA (2013) [Global Oceans] Sea surface temperatures [in “State of the Climate in 2012”]. Bull Am Meterological Soc BAMS 94(8):S47–S50

  • Yarnes CT, Herszage J (2017) The relative influence of derivatization and normalization procedures on the compound-specific stable isotope analysis of nitrogen in amino acids. Rapid Commun Mass Spectrom 31:693–704

    Article  CAS  PubMed  Google Scholar 

  • Zorica B, Ezgeta-Balić D, Vidjak O, Vuletin V, Šestanović M, Isajlović I, Čikeš Keč V, Vrgoč N, Harrod C (2021) Diet composition and isotopic analysis of nine important fisheries resources in the Eastern Adriatic Sea (Mediterranean). Front Mar Sci 8:609432. https://doi.org/10.3389/fmars.2021.609432

Download references

Acknowledgements

Gulf of Mexico data: Robert Allman (NOAA) oversaw sample archiving, organization, and distribution of muscle tissue samples. Jessica Gwinn and Corinne Sweeney (University of South Alabama and the Dauphin Island Sea Lab, respectively) provided assistance in sample lyophilization, pulverization, and subsampling for bulk and compound-specific stable isotope analyses. Andrew Ouimette and Chris Yarnes and their respective staffs at the UNH and UC-Davis Stable Isotope Laboratories performed bulk and compound-specific stable isotope analyses, respectively. Funding for these analyses was provided through support from the U.S. NOAA Bluefin Tuna Research Program (NOAA Award NA16NMF4720098). Eastern Atlantic data: This research was supported by the Andalusian Government (P12-RNM733, FEDER-UCA18-107069). Joan Navarro provided bulk stable isotope data for our training dataset. We also thank the following authors that contributed raw data for our amino acid stable isotope comparisons: Riley Austin, Sharon Herzka, Joel Llopiz, and Owen Sherwood. Sharon Herzka and two anonymous reviewers also provided helpful edits to earlier drafts of this manuscript.

Funding

Research funding was provided from NOAA through Award NA16NMF4720098. This research was also supported by the Andalusian Government (P12-RNM733, FEDER-UCA18-107069).

Author information

Authors and Affiliations

  1. Massachusetts Division of Marine Fisheries, New Bedford, MA, 02744, USA

    John M. Logan

  2. School of Marine Science and Policy, University of Delaware, Lewes, DE, 19958, USA

    Andrew S. Wozniak

  3. Departamento de Biología, Facultad de Ciencias del Mar y Ambientales, Universidad de Cádiz, República Saharui s/n, 11510, Puerto Real, Spain

    José Luis Varela

  4. School of Marine and Environmental Sciences, University of South Alabama, Mobile, AL, 36688, USA

    Alison Robertson

  5. Dauphin Island Sea Lab, Dauphin Island, AL, 36528, USA

    Alison Robertson

Authors
  1. John M. Logan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrew S. Wozniak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. José Luis Varela
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alison Robertson
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conception and design were performed by JL, AW, and AR. Material preparation was performed by AR and JLV. Sample collection was performed by JLV. Data analysis was performed by JL. The manuscript was drafted by JL and edited by AW, JLV, and AR. All authors read and approved the final manuscript.

Corresponding author

Correspondence to John M. Logan.

Ethics declarations

Conflict of interest

The authors have not disclosed any competing interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Responsible Editor: S. Hamilton.

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

227_2023_4210_MOESM1_ESM.pdf

Supplementary file1 ∆δ15N (‰) offset of source amino acids for individual marine fauna from representative shelf and open ocean Atlantic bluefin tuna (ABFT; Thunnus thynnus) foraging habitats in the Gulf of Mexico, Mediterranean Sea, and North Atlantic Ocean. All values were normalized to our Gulf of Mexico shelf migrant dataset based on estimates of trophic position for this ABFT group (TP=4.4) and each comparative faunal group with estimated trophic discrimination factors of 0.1‰ (Phe), 0.4‰ (Met), and 0.8‰ (Lys). Individual datasets corresponding to each region are detailed in Supplementary Table 2 (PDF 120 KB)

Supplementary file2 (PDF 15 KB)

Supplementary file3 (PDF 129 KB)

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

Logan, J.M., Wozniak, A.S., Varela, J.L. et al. Pre-spawning habitat use of Atlantic bluefin tuna (Thunnus thynnus) inferred from stable isotope analysis. Mar Biol 170, 67 (2023). https://doi.org/10.1007/s00227-023-04210-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-023-04210-7

Keywords

Search

Navigation