Atlantic Bluefin Tuna ( Thunnus thynnus) Population Dynamics Delineated by Organochlorine Tracers REBECCA M. DICKHUT,* ,† ASHOK D. DESHPANDE, ALESSANDRA CINCINELLI, § MICHELE A. COCHRAN, SIMONETTA CORSOLINI, | RICHARD W. BRILL, DAVID H. SECOR, AND JOHN E. GRAVES Virginia Institute of Marine Science, Gloucester Point, Virginia 23062, National Marine Fisheries Service, Highlands, New Jersey 07732, Department of Chemistry, University of Florence, 50019 Sesto Fiorentino, Florence, Italy, Department of Environmental Science, University of Siena, I-53100 Siena, Italy, and Chesapeake Biological Laboratory, University of Maryland Center for Environmental Science, Solomons, Maryland 20688 Received June 19, 2009. Revised manuscript received September 11, 2009. Accepted September 15, 2009. Atlantic bluefin tuna (ABFT) are highly valued and heavily exploited, and critical uncertainties regarding their population structure hinder effective management. Evidence supports the existence of two breeding populations of ABFT; a western population in the Gulf of Mexico and an eastern population in the Mediterranean Sea; both of which migrate and mix in the North Atlantic. Conventional tagging studies suggest low rates of trans-Atlantic migrations; however, electronic tagging and stable isotopes in otoliths indicate stock mixing up to 57% between management zones delineated by 45° W longitude. Here we show that organochlorine pesticides and polychlorinated biphenyls (PCBs) can be used as tracers of bluefin tuna foraging grounds in the North Atlantic and confirm that stock mixing of juvenile tuna within the U.S. Mid Atlantic Bight is indeed high (33-83% eastern origin), and is likely spatially and temporally variable. We further demonstrate that >10% of the Mediterranean population is migratory, that young bluefin tuna migrate from the Mediterranean to western Atlantic foraging grounds as early as age 1, and then return to the Mediterranean Sea as young as age 5, presumably to breed. The tracer method described here provides a novel means for distinguishing bluefin tuna populations and ontogenetic shifts in migration in the North Atlantic. Introduction Atlantic bluefin tuna (ABFT), high-valued recreational and commercial fish, are distributed from subtropical to subarctic regions throughout the North Atlantic (1). The member nations of the International Commission for the Conservation of Atlantic Tunas (ICCAT) currently manage ABFT fisheries assuming two units (a western stock spawning in the Gulf of Mexico, and an eastern stock which spawns in the Mediterranean Sea) ostensibly separated by the 45° W meridian with little intermixing between stocks. However, tagging studies indicate that bluefin tuna undergo extensive and complex migrations, including trans-Atlantic migrations, and that stock mixing could be as high as 30% (2-4). Extensive mixing of eastern and western stocks (35-57% bluefin tuna of eastern origin) within the U.S. Mid Atlantic Bight was also reported recently based on otolith δ 18 O values (5). The uncertainty of stock structures due to mixing makes it difficult for fisheries managers to assess the effectiveness of rebuilding efforts for the dwindling western Atlantic spawning stock of bluefin tuna. Understanding ABFT spatial distributions and dynamics are vital for robust population assessments and the design of effective management strategies, and there is a critical need for improved methods to resolve key attributes of this highly migratory species (1). Reports of low levels of chlordane compounds (cis- chlordane, trans-chlordane, cis-nonachlor, trans-nonachlor, oxychlordane) relative to polychlorinated biphenyls (PCBs) in marine species from the Mediterranean Sea (MS, 6, 7) compared to the western North Atlantic (WNA, 8-11) led us to propose chlordane/PCB ratios as chemical tags for fish feeding in these geographically distinct ecosystems. PCBs and chlordanes are synthetic chemicals that were released into the environment by human activity, bioaccumulate in organism lipids, and biomagnify, increasing in concentration with trophic level such that top predators attain the highest concentrations (12-15). Nonmetabolizable PCB congeners persist in fish and the environment; likewise, chlordanes, a group of organochlorine pesticides are slowly metabolized, if at all, by fish (16, 17). PCB and chlordane concentrations increase with fork length in Pacific bluefin tuna (Thunnus orientalis) from juveniles through adult sized fish (18), indicating that uptake exceeds elimination and that persistent organochlorine compounds are retained in these fish such that they could be useful tracers of bluefin tuna foraging regions over time scales of years. The objective of our research was to establish the utility of PCBs and organochlorine pesticides as tracers of ABFT natal origin and stock mixing. A tracer technique based on the ratios of chemical markers was proposed as it is advantageous compared to measurement of absolute con- centrations of specific markers for various reasons. First, concentrations of persistent organochlorine compounds increase with fish lipid content (10) and size (18), and are also higher in fish that reside in more contaminated habitats (19, 20). These confounding variables can be eliminated by using compound ratios to assign origin to an individual within a mixed population of fish provided that the compound ratios differ significantly between foraging habitats and remain constant in fish residing within a single habitat. Large differences in the relative amounts of chlordanes and PCBs are found in marine organisms from the MS and WNA, as noted above, and data from the Sea of Japan demonstrate linear increases in PCBs and chlordanes with size such that the ratio of these compounds remains constant over the life span of bluefin tuna residing within a specific ecosystem (18). Therefore, chlordane/PCB ratios are likely to be useful for distinguishing ABFT origin and stock mixing. Second, there is often interlaboratory variability in measurement of absolute concentrations of PCBs and pesticides based on extraction techniques, sample recoveries, and instrument * Corresponding author e-mail: rdickhut@vims.edu. Virginia Institute of Marine Science. National Marine Fisheries Service. § University of Florence. | University of Siena. University of Maryland Center for Environmental Science. Environ. Sci. Technol. 2009, 43, 8522–8527 8522 9 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 43, NO. 22, 2009 10.1021/es901810e CCC: $40.75 2009 American Chemical Society Published on Web 09/28/2009