Spawning of bluefin tuna in the black sea: historical evidence, environmental constraints and population plasticity

The lucrative and highly migratory Atlantic bluefin tuna, Thunnus thynnus (Linnaeus 1758; Scombridae), used to be distributed widely throughout the north Atlantic Ocean, Mediterranean Sea and Black Sea. Its migrations have supported sustainable fisheries and impacted local cultures since antiquity, but its biogeographic range has contracted since the 1950s. Most recently, the species disappeared from the Black Sea in the late 1980s and has not yet recovered. Reasons for the Black Sea disappearance, and the species-wide range contraction, are unclear. However bluefin tuna formerly foraged and possibly spawned in the Black Sea. Loss of a locally-reproducing population would represent a decline in population richness, and an increase in species vulnerability to perturbations such as exploitation and environmental change. Here we identify the main genetic and phenotypic adaptations that the population must have (had) in order to reproduce successfully in the specific hydrographic (estuarine) conditions of the Black Sea. By comparing hydrographic conditions in spawning areas of the three species of bluefin tunas, and applying a mechanistic model of egg buoyancy and sinking rate, we show that reproduction in the Black Sea must have required specific adaptations of egg buoyancy, fertilisation and development for reproductive success. Such adaptations by local populations of marine fish species spawning in estuarine areas are common as is evident from a meta-analysis of egg buoyancy data from 16 species of fish. We conclude that these adaptations would have been necessary for successful local reproduction by bluefin tuna in the Black Sea, and that a locally-adapted reproducing population may have disappeared. Recovery of bluefin tuna in the Black Sea, either for spawning or foraging, will occur fastest if any remaining locally adapted individuals are allowed to survive, and by conservation and recovery of depleted Mediterranean populations which could through time re-establish local Black Sea spawning and foraging.     

Establishment and characterization of two cell lines from bluefin trevally Caranx melampygus

Bluefin trevally Caranx melampygus Cuvier is a popular game fish and highly valued sea food with potential importance for aquaculture. To help establish this marine animal as an important aquacultural species in Hawaii and the Pacific and develop in vitro cell culture systems for long-term management and control of potential viral diseases 2 cell lines were established from body muscle (bluefin trevally muscles, BTMS) and fins (bluefin trevally fins, BTF). Primary culture of these cells was conducted at 25 degrees C using L-15 medium supplemented with 20% fetal bovine serum and various antibiotics. These cells have been serially subcultured 37 to 41 times since their initiation in June 2002. Growth of the bluefin trevally cells was serum-dependent at the time of the experiments and their plating efficiencies ranged from 11 to 28.2%. Comparative analysis showed that these bluefin trevally cells grew equally well in the media L-15 (Leibovitz medium), RPMI 1640, M199 and MEM (minimum essential medium), which are commonly used for cell cultures derived from aquatic animals and mammalian species. Examination of the early passage cells stored at -196 degrees C revealed a large percent (nearly 98%) of cell viability following a 6 mo storage in liquid nitrogen. Karyotyping analysis indicated that these bluefin trevally derived cell lines remained diploid with a chromosome count of 48 at passage 7 and 12. These 2 cell lines shared a same pattern of viral susceptibility and they were sensitive to infectious hematopoietic necrosis virus (IHNV), infectious pancreatic necrosis (IPN), spring viremia carp virus (SVCV), viral hemorrhagic septicemia virus (VHSV), and snakehead rhabdovirus (SHRV) but refractory to channel catfish virus (CCV) infection. These newly established cell lines are currently being used to facilitate the diagnosis of viral disease affecting marine fish aquaculture in Hawaii, and will be available for future isolation and study of bluefin trevally fish viruses.     

A finite-state continuous-time approach for inferring regional migration and mortality rates from archival tagging and conventional tag-recovery experiments

Spatially structured population dynamics models are important management tools for harvested, highly mobile species and although conventional tag recovery experiments remain useful for estimation of various demographic parameters of these models, archival tagging experiments are becoming an important data source for analyzing migratory behavior of mobile marine species. We provide a likelihood-based approach for estimating the regional migration and mortality rate parameters intrinsic to these models that may use information obtained from conventional tag recovery and archival tagging experiments. Specifically, we assume that the regional location and survival of animals through time is a finite-state continuous-time stochastic process. The stochastic process is the basis of probability models for observations provided by the different types of tags. Results from application to simulated tagging experiments for western Atlantic bluefin tuna show that maximum likelihood estimators based on archival tagging observations and corresponding confidence intervals perform similar to conventional tagging observations for a given number of tag releases and releasing tags in each region can improve the behavior of maximum likelihood estimators regardless of tag type. We provide an example application with Atlantic bluefin tuna released with conventional tags in 1990-1992.     

Fast versus slow growing tuna species: age,growth, and implications for population dynamics and fisheries management

Growth models describe the change in length or weight as a function of age. Growth curves in tunas can take different forms from relatively simple von Bertalanffy growth curves (Atlantic bluefin, albacore tunas) to more complex two- or three-stanza growth curves (yellowfin, bigeye, skipjack, southern bluefin tunas). We reviewed the growth of the principal market tunas (albacore, bigeye, skipjack, yellowfin and the three bluefin tuna species) in all oceans to ascertain the different growth rates among tuna species and their implications for population productivity and resilience. Tunas are among the fastest-growing of all fishes. Compared to other species, tunas exhibit rapid growth (i.e., relatively high K) and achieve large body sizes (i.e., high L _∞ ). A comparison of their growth functions reveals that tunas have evolved different growth strategies. Tunas attain asymptotic sizes (L _∞ ), ranging from 75 cm FL (skipjack tuna) to 400 cm FL (Atlantic bluefin tuna), and reach L _∞ at different rates (K), varying from 0.95 year^?1 (skipjack tuna) to 0.05 year^?1 (Atlantic bluefin tuna). Skipjack tuna (followed by yellowfin tuna) is considered the “fastest growing” species of all tunas. Growth characteristics have important implications for population dynamics and fisheries management outcomes since tunas, and other fish species, with faster growth rates generally support higher estimates of Maximum Sustainable Yield (MSY) than species with slower growth rates.     

Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes

Comparative phylogeography has revealed remarkable patterns of concordance in the maternal phylogenies of many species. The phylogeography and historical demography of the mitochondrial control region I for 607 Atlantic bluefin tuna (Thunnus thynnus) and 275 swordfish (Xiphias gladius) were analyzed to clarify the complex phylogenetic signals in the North Atlantic-Mediterranean region where they are sympatric. Atlantic bluefin tuna mtDNA is polyphyletic, and includes rare sequences sister to Pacific bluefin tuna (Thunnus orientalis) and introgressed albacore (Thunnus alalunga) sequences. There is no geographic partitioning between Atlantic and Mediterranean samples of Atlantic bluefin tuna (Phi(ST)=0.002). In contrast, Atlantic and Mediterranean swordfish are differentiated (Phi(ST)=0.091) due to the combined effects of vicariance, secondary contact, and dissimilar regional demographic histories. Mediterranean swordfish has substantially less variation, and a more recent history (tau=2.42) than that of Atlantic swordfish (tau=7.02). In spite of the discordant phylogenetic and phylogeographic signals, the demographic history of Atlantic swordfish and Atlantic bluefin tuna (tau=7.51) suggests concordance in the timeline of population expansion. Possible scenarios of cladogenesis, expansion, and contraction, influenced by glacial cycles during the Pleistocene, are formulated.     

Phylogenetic relationships between tuna species of the genus Thunnus (Scombridae: Teleostei): Inconsistent implications from morphology,nuclear and mitochondrial genomes

In order to infer phylogenetic relationships between tuna species of the genus Thunnus, partial sequences of the mitochondrial cytochrome b and ATPase genes were determined in all eight species. Supplemental restriction analysis on the nuclear rRNA gene was also carried out. Pacific northern bluefin tuna (Thunnus thynnus orientalis) was found to have mtDNA distinct from that of the Atlantic subspecies (T. t. thynnus) but very similar to that from the species albacore (T. alaluga). In contrast, no differentiation in nuclear genome was observed between the Atlantic and Pacific northern bluefin tunas. The Atlantic northern bluefin and southern bluefin tunas possessed mtDNA sequences very similar to species of yellowfin tuna group and not so similar to albacore and bigeye tunas which were morphologically assigned to the bluefin tuna group. The molecular data indicate that (1) mtDNA from albacore has been incorporated into the Pacific population of northern bluefin tuna and has extensively displaced the original mtDNA, and (2) albacore is the earliest offshoot, followed by bigeye tuna in this genus, which is inconsistent with the phylogenetic relationships between these tuna species inferred from morphology. Correspondence to: S. Chow     

The role of discounting and dynamics in determining the economic efficiency of time-area closures for managing fishery bycatch

Time-area closures are commonly used to manage fisheries bycatch and involve temporarily closing an area of the ocean to particular fishing gears. We examine conditions in which implementing a time-area closure would increase the economic value of fisheries, focusing on a case study application in the Gulf of Mexico. Pelagic longline fishermen catch the highly valued Atlantic bluefin tuna (Thunnus thynnus, Scombridae) on their Gulf of Mexico spawning grounds while fishing for Atlantic yellowfin tuna (Thunnus albacares). We analyze a multispecies, multifishery bioeconomic model that includes information on migratory patterns from electronic tagged bluefin tuna. We use dynamic optimization to identify management strategies that would maximize the net present value of tuna fisheries, allowing for discounting of future benefits and costs relative to the present. If past fishing mortality rates continue in Atlantic bluefin tuna fisheries, implementing a time-area closure in the Gulf of Mexico incurs economic costs. However, the net present value of the fisheries is increased by implementing a time-area closure as part of a broader commitment to rebuild the heavily depleted bluefin population, provided the discount rate and the costs of such a closure in forgone fishing opportunities are not too large. The increase in economic value offered by a time-area closure is small relative to the overall economic value of rebuilding itself and it may be economically optimal only to implement a closure once sufficient rebuilding has already taken place.     

Atlantic Bluefin Tuna in the Gulf of Maine, I: Estimation of Seasonal Abundance Accounting for Movement, School and School-Aggregation Behaviour

Direct assessment of the abundance of highly migratory pelagic species, such as tuna, is rarely available and most indices are based on catch information. We estimate the seasonal abundance of North Atlantic bluefin tuna, Thunnus thynnus, in the Gulf of Maine (GOM) from a 3-year aerial survey conducted with commercial spotter pilots, while also utilizing findings from analyses of tracking and tagging data. We apply statistical correction and calibration to seasonal abundance estimates accounting for measured changes in horizontal and vertical movement behaviour, size, shape and aggregation of bluefin tuna schools. Our approach relies on ecological knowledge of bluefin tuna to extrapolate survey observations across areas not sampled by correcting survey abundance estimates based on range of movement search pattern and depth preference. We demonstrate how separate findings obtained through the analysis of data collected across different spatial and temporal scales can be integrated to correct and calibrate estimates of population abundance. We obtain fitted estimates of seasonal abundance of bluefin tuna in the GOM during 1994–1996 in the range of 45,000–51,000 individuals. If tuna behaviour is not accounted for, we estimate that the base or residual survey precision would be 4–7% determined from analysis of recent spotter survey data in the study region. We estimate the precision in estimating seasonal abundance accounting for tuna behaviour to lie within a range of 1,301–3,302%. Under hypothetical future improvements in survey design that achieve a precision of 20% in transect length and placement, we calculate net-precision to lie within a range of 82–93%. This calculation assumes reducible uncertainty in school size estimation and irreducible uncertainty in movement and school-aggregation behaviour. We infer that survey precision could be further reduced by 43–32% to attain 10–50% in which a 3–8 years adaptive survey design may reliably detect a seasonal abundance trend.     

Genetic identity of YOY bluefin tuna from the eastern and western Atlantic spawning areas

We used 320 young-of-the-year (YOY) specimens of the highly migratory and overfished Atlantic bluefin tuna, Thunnus thynnus, Linnaeus 1758, to evaluate the hypothesis that Atlantic bluefin tuna comprises 2 stocks with spawning grounds in the Gulf of Mexico and in the Mediterranean Sea. Significant genetic differentiation at 8 nuclear microsatellite loci (F(ST) = 0.0059, P = 0.0005) and at the mitochondrial control region (Phi(ST) = 0.0129, P = 0.0139) was detected among YOY Atlantic bluefin tuna captured on spawning grounds in the Gulf of Mexico (n = 40) versus the western (n = 255) and eastern (n = 25) basins of the Mediterranean Sea. The genetic divergence among spawning populations, combined with the extensive trans-Atlantic movements reported for juvenile and adult Atlantic bluefin tuna, indicates a high degree of spawning site fidelity. Recognition of genetically distinct populations necessitates independent management of Atlantic bluefin tuna on spawning grounds and warrants evaluation of the level of mixing of populations on feeding grounds. The genetic pattern might not have been detected unless juvenile specimens or actively spawning adults had been sampled.     

Reproduction and larval biology in tunas,and the importance of restricted area spawning grounds

Tunas show a wide variety of life history strategies, spatial distributions and migratory behaviors, yet they share a common trait of spawning only in tropical and sub-tropical regions. The warm-water tuna species generally show significant overlap between spawning and feeding grounds, and longer spawning seasons of several months to near year-round. In contrast, the cool-water bluefin tunas migrate long distances between feeding and spawning grounds, and may spawn over periods as short as 2 months. Here, we examine the spatial distributions of tuna larvae in the world’s oceans, and examine interspecific differences in the light of adult behaviors and larval ecology. We discuss the links between larval tuna and their oceanographic environments and relate these to current knowledge of larval growth, feeding and trophodynamics, with a focus on the better-studied bluefin tunas. We show that larval tunas have moderate to fast growth rates and selective feeding habits, and thus appear to be adapted for survival in warm, oligotrophic seas. We also examine the challenges of sustainably managing species which migrate across multiple management boundaries to reach spatio-temporally restricted spawning grounds and discuss the previous and future anthropogenic impacts on tuna spawning areas.     

Orthodox and unorthodox phylogenetic relationships among tunas revealed by the nucleotide sequence analysis of the mitochondrial DNA control region

A phylogeny of all eight recognized taxa of the genus Thunnus was constructed from approximately 400 base pairs of sequence of the mitochondrial DNA (mtDNA) control region. The PCR-amplified control region I segment studied contained a total of 186 variable sites and 159 phylogenetically informative sites. Diagnostic sequences for every taxon were identified. Neighbour-joining phylogenies supported monophyletic origins of the temperate subgenus Thunnus and of the tropical subgenus Neothunnus . Similar results were obtained by maximum parsimony analyses except that there was no support for a monophyletic origin of the subgenus Thunnus . Bigeye tuna, which have been difficult to place in either subgenus using conventional morphological data, was identified as the sister species of Neothunnus . Within the subgenus Thunnus , the Atlantic bluefin and Southern bluefin tunas were shown to be sister taxa of the highly divergent monophyletic clade formed by the Pacific northern bluefin and the Albacore tunas. The conspecific Atlantic ( T. thynnus thynnus ) and Pacific ( T. t. orientalis ) northern bluefin tunas were more divergent (Tamura-Nei distance 0·145 ± 0·019) from each other than the average distance separating most species-pairs within the genus. Thus, a re-examination of their status as subspecies of T. thunnus is warranted.     

Morphometric differentiation between two juvenile tuna species [Thunnus thynnus (Linnaeus, 1758) and Euthynnus alletteratus (Rafinesque, 1810)] from the Eastern Mediterranean Sea

The main objective of this study was to analyse the differences in morphometric characteristics among specimens of Atlantic juvenile bluefin tuna Thunnus thynnus [12.2–46.5 cm fork length (FL)] and juvenile little tuna Euthynnus alletteratus (14.1–26.4 cm FL). A total of 353 bluefin tuna (young of the year) and 288 little tuna (young of the year) were collected from the commercial hand line fisheries in the eastern Mediterranean Sea between July and October of 2011–2013 with three round‐bent hook sizes (numbers 10, 12 and 14; Mustad 2315S). By using univariate and multivariate analysis, 11 morphometric characters were investigated. anova revealed highly significant differences (P < 0.001) for all morphometric parameters among the two species. The principal component analysis showed that the difference between the species resulted mainly from preanal length (LA), caudal fin hight (CC), snout length (SnL), eye diameter (ED) and postorbital length (PO). The stepwise discriminant analysis revealed that juveniles of the two tuna species were correctly classified, with a percentage of 99.2%. Length of pectoral fin (LP) was the strongest predictor in the discriminant functions.     

A cascade of warming impacts brings bluefin tuna to Greenland waters

Rising ocean temperatures are causing marine fish species to shift spatial distributions and ranges, and are altering predator‐prey dynamics in food webs. Most documented cases of species shifts so far involve relatively small species at lower trophic levels, and consider individual species in ecological isolation from others. Here, we show that a large highly migratory top predator fish species has entered a high latitude subpolar area beyond its usual range. Bluefin tuna, Thunnus thynnus Linnaeus 1758, were captured in waters east of Greenland (65°N) in August 2012 during exploratory fishing for Atlantic mackerel, Scomber scombrus Linnaeus 1758. The bluefin tuna were captured in a single net‐haul in 9–11 °C water together with 6 tonnes of mackerel, which is a preferred prey species and itself a new immigrant to the area. Regional temperatures in August 2012 were historically high and contributed to a warming trend since 1985, when temperatures began to rise. The presence of bluefin tuna in this region is likely due to a combination of warm temperatures that are physiologically more tolerable and immigration of an important prey species to the region. We conclude that a cascade of climate change impacts is restructuring the food web in east Greenland waters.     

Diet composition of bluefin tuna (Thunnus thynnus L. 1758) in the Eastern Mediterranean Sea,Turkey

This study gives relevant information on the diet composition of the bluefin tuna (Thunnus thynnus) during the spawning period in the eastern Mediterranean Sea. The stomach contents of 218 bluefin tuna were sampled from 2003 to 2006 during the fishing season (May–June) aboard purse seiners operating in the northern Levantine Sea off the coast of Turkey. Stomachs were removed from the fish soon after landing and kept frozen at ?18°C until analysis. Prey items were classified into large taxonomic categories and preserved in 70% ethanol. A total of 745 different prey specimens belonging to 47 taxa were identified, including 34 species of fish, 11 of squid, and two of crustaceans. The most important fish and cephalopod prey belonged to the families Myctophidae, Carangidae, Chauliodontidae, Paralepididae, and Octopoda. This study marks the observation of myctophid fish in the stomach contents of bluefin tuna from the Mediterranean Sea. The paper offers some new information of regional importance and compares the feeding habits of the species to other regions, bringing confirmation on the opportunistic feeding ecology of the species in the enclosed Mediterranean Sea, where bluefin tuna seasonally occur as a strong cohort. New information on the diet composition of T. thynnus in the eastern Mediterranean Sea is revealed; the findings indicate that, depending on the abundance of the different prey species in the habitat, the dominant prey species can be distinctive.     

Spatial Scale,Means and Gradients of Hydrographic Variables Define Pelagic Seascapes of Bluefin and Bullet Tuna Spawning Distribution

Seascape ecology is an emerging discipline focused on understanding how features of the marine habitat influence the spatial distribution of marine species. However, there is still a gap in the development of concepts and techniques for its application in the marine pelagic realm, where there are no clear boundaries delimitating habitats. Here we demonstrate that pelagic seascape metrics defined as a combination of hydrographic variables and their spatial gradients calculated at an appropriate spatial scale, improve our ability to model pelagic fish distribution. We apply the analysis to study the spawning locations of two tuna species: Atlantic bluefin and bullet tuna. These two species represent a gradient in life history strategies. Bluefin tuna has a large body size and is a long-distant migrant, while bullet tuna has a small body size and lives year-round in coastal waters within the Mediterranean Sea. The results show that the models performance incorporating the proposed seascape metrics increases significantly when compared with models that do not consider these metrics. This improvement is more important for Atlantic bluefin, whose spawning ecology is dependent on the local oceanographic scenario, than it is for bullet tuna, which is less influenced by the hydrographic conditions. Our study advances our understanding of how species perceive their habitat and confirms that the spatial scale at which the seascape metrics provide information is related to the spawning ecology and life history strategy of each species.     

Microsatellite DNA markers for population‐genetic studies of Atlantic bluefin tuna (Thunnus thynnus thynnus) and other species of genus Thunnus

Twenty‐five microsatellites from Atlantic bluefin tuna (Thunnus thynnus thynnus) were characterized. All 25 microsatellites were polymorphic; the number of alleles among up to 56 individuals surveyed ranged from two to 23. Atlantic bluefin tuna are highly exploited and major questions remain as to stock structure and abundance in the eastern and western North Atlantic. The microsatellites will be useful in testing stock‐structure hypotheses and in generating estimates of effective population size. The polymerase chain reaction primer sets developed also amplified identifiable alleles in three other species of genus Thunnus: T. albacares (yellowfin tuna), T. alalunga (albacore tuna) and T. obesus (bigeye tuna).     

Mitochondrial DNA sequence variation within and between tuna Thunnus species and its application to species identification

Restriction analysis detected two types of bigeye tuna (α and β); the α type was in the majority in the Atlantic but nearly absent in the Indo-Pacific. The β type shared a larger number of restriction sites with other species than the conspecific β type, but bigeye-specific nucleotide substitutions with a novel diagnostic restriction profile were found. Although the nucleotide sequence difference between Atlantic and Pacific sub-species of the northern bluefin tuna was nearly the largest among species, individuals possessing the Atlantic type of mtDNA were found at very low frequency in the Pacific and vice versa. Previous RFLP markers were found to be diagnostic for the other five species (albacore, blackfin, longtail, southern bluefin and yellowfin tunas). Genetic information is provided to discriminate all Thunnus species regardless of their origin and to identify the ocean of capture in the northern bluefin and bigeye tunas.     

The Capercaillie (<Emphasis Type="Italic">Tetrao urogallus</Emphasis>): an iconic focal species for knowledge-based integrative management and conservation of Baltic forests

Biodiversity loss was a central argument for redefining sustainable forest management in the 1990s, but threatened species remain poorly addressed in forestry governance. Management history of the Capercaillie (Tetrao urogallus) population in the Baltic States reveals a high potential of socially valued threatened species for developing the missing forestry–conservation interfaces. We review the history of the Baltic Capercaillie population since the 19th century, showing how its status transformed, both ecologically and socially, from a famous hunting target to the most widely protected forest species in the region. Compilation of recent national survey data confirms that at least 3450 lekking males currently survive in 961 leks; they are distributed between six large and about twenty small populations. During the 20th century, lek sizes decreased and local extirpations spread from South-Baltic mosaic lands to northern forests. As a social response, innovative management initiatives have repeatedly enabled periods of population stability and local recoveries. The most recent developments in Capercaillie conservation combine elements from the historically separated nature conservation, forestry and game-management approaches. The consistency of such social responses despite political upheavals suggests that iconic species can culturally stabilize long-term sustainable development.     

Population genetics of tunas

Population genetic studies on tunas are reviewed. These studies have focused on phylogenetic reconstructions, species identifications and stock delineation, and have used tools ranging from blood group and allozyme analysis to PCR-aided examination of mitochondrial DNA variation. Both allozyme and mtDNA approaches show tunas in the genus Thunnus to be very closely related to one another, but also indicate that the two presently recognized subspecies of northern bluefin tuna, Thunnus thynnus thynnus and T. t. orientalis , in fact may be worthy of species status. These techniques also permit the unequivocal recognition of specimens, which is not always possible on morphological grounds. However, it is arguable that, until recently, tunas have not received their due attention from geneticists given their commercial significance and the need for information on stock structure to ensure sustainable management. This may be because tunas are known to be highly vagile and therefore levels of population differentiation are expected to be low. None the less, population subdivision has been recorded in several species (skipjack, yellowfin, albacore), although this tends to be on a broad (intra- or inter-oceanic) rather than on a more local scale. New molecular tools, including the PCR-based analyses of nuclear genes and microsatellite loci, are yielding new, highly polymorphic markers, and will enable more powerful analyses of stock structure than have hitherto been possible.     

Evidence of Atlantic bluefin tuna spawning in the Bay of Biscay,north-eastern Atlantic

The spawning grounds of the Atlantic bluefin tuna (Thunnus thynnus) are traditionally considered to be the Gulf of Mexico (Gulf of Mexico) and the Mediterranean Sea (Mediterranean Sea). However, for the western Atlantic, unequivocal evidence of bluefin spawning outside the Gulf of Mexico has been shown. In this study we present the first records of genetically confirmed bluefin larvae in the southern Bay of Biscay (eastern Atlantic). These findings provide evidence of bluefin spawning activity outside the Mediterranean Sea, in the north-eastern Atlantic. However, our results suggest that the bluefin spawning in the Bay of Biscay is a sporadic phenomenon.