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     

Seasonal Movements,Aggregations and Diving Behavior of Atlantic Bluefin Tuna (Thunnus thynnus) Revealed with Archival Tags

Electronic tags were used to examine the seasonal movements, aggregations and diving behaviors of Atlantic bluefin tuna (Thunnus thynnus) to better understand their migration ecology and oceanic habitat utilization. Implantable archival tags (n = 561) were deployed in bluefin tuna from 1996 to 2005 and 106 tags were recovered. Movement paths of the fish were reconstructed using light level and sea-surface-temperature-based geolocation estimates. To quantify habitat utilization we employed a weighted kernel estimation technique that removed the biases of deployment location and track length. Throughout the North Atlantic, high residence times (167±33 days) were identified in four spatially confined regions on a seasonal scale. Within each region, bluefin tuna experienced distinct temperature regimes and displayed different diving behaviors. The mean diving depths within the high-use areas were significantly shallower and the dive frequency and the variance in internal temperature significantly higher than during transit movements between the high-use areas. Residence time in the more northern latitude high-use areas was significantly correlated with levels of primary productivity. The regions of aggregation are associated with areas of abundant prey and potentially represent critical foraging habitats that have seasonally abundant prey. Throughout the North Atlantic mean diving depth was significantly correlated with the depth of the thermocline, and dive behavior changed in relation to the stratification of the water column. In this study, with numerous multi-year tracks, there appear to be repeatable patterns of clear aggregation areas that potentially are changing with environmental conditions. The high concentrations of bluefin tuna in predictable locations indicate that Atlantic bluefin tuna are vulnerable to concentrated fishing efforts in the regions of foraging aggregations.     

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.     

Size and age at sexual maturity of female bluefin tuna (Thunnus thynnus L. 1758) from the Mediterranean Sea

The ovaries of 501 female eastern Atlantic bluefin tuna (Thunnus thynnus Linnaeus, 1758) captured in the Mediterranean Sea from May to September between 1998 and 2004 were analysed histologically. Body size at median sexual maturity (L₅₀) was 103.6 cm fork length (FL), while 100% maturity was reached above 135 cm FL. The age analysis, based on the count of the translucent zones of the first spiniform ray of the first dorsal fin, showed that most of the specimens with FL = L₅₀ were 3 years old while 100% maturity was reached between 4 to 5 years. The reported evidence indicates that for the eastern Atlantic bluefin tuna stock, the size and age of first sexual maturity of females was lower than in the western Atlantic stock.     

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.     

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).     

Electronic Tagging of Atlantic Bluefin Tuna (Thunnus thynnus,L.) Reveals Habitat Use and Behaviors in the Mediterranean Sea

We analyzed the movements of Atlantic tuna (Thunnus thynnus L.) in the Mediterranean Sea using data from 2 archival tags and 37 pop-up satellite archival tags (PAT). Bluefin tuna ranging in size from 12 to 248 kg were tagged on board recreational boats in the western Mediterranean and the Adriatic Sea between May and September during two different periods (2000 to 2001 and 2008 to 2012). Although tuna migrations between the Mediterranean Sea and the Atlantic Ocean have been well reported, our results indicate that part of the bluefin tuna population remains in the Mediterranean basin for much of the year, revealing a more complex population structure. In this study we demonstrate links between the western Mediterranean, the Adriatic and the Gulf of Sidra (Libya) using over 4336 recorded days of location and behavior data from tagged bluefin tuna with a maximum track length of 394 days. We described the oceanographic preferences and horizontal behaviors during the spawning season for 4 adult bluefin tuna. We also analyzed the time series data that reveals the vertical behavior of one pop-up satellite tag recovered, which was attached to a 43.9 kg tuna. This fish displayed a unique diving pattern within 16 days of the spawning season, suggesting a use of the thermocline as a thermoregulatory mechanism compatible with spawning. The results obtained hereby confirm that the Mediterranean is clearly an important habitat for this species, not only as spawning ground, but also as an overwintering foraging ground.     

A new blood fluke of the genus Cardicola (Trematoda: Sanguinicolidae) from Pacific bluefin tuna Thunnus orientalis (Temminck & Schlegel, 1844) cultured in Japan

A new sanguinicolid blood fluke, Cardicola orientalis n. sp., is described from the afferent branchial artery and heart of Pacific bluefin tuna Thunnus orientalis (Temminck & Schlegel) cultured in Mie and Nagasaki Prefectures, Japan. The new species is most similar to C. ambrosioi Braicovich, Etchegoin, Timi et Sardella, 2006 from the Brazilian flathead, Percophis brasiliensis Quoy & Gaimard, but can be differentiated by the position of the female genital pore (in midline or slightly sinistral in C. orientalis vs. sinistral in C. ambrosioi) and much longer distance between male and female genital pore (101 μm vs. 27 μm). In wet mount preparations of infected fish, eggs were accumulated in great numbers in the gill lamellae and afferent filament arteries. Importance of this blood fluke infection of cultured Pacific bluefin tuna in Japan is discussed.     

Further evidence of spawning of bluefin tuna (Thunnus thynnus L., 1758) and the tuna species (Auxis rochei Ris., 1810, Euthynnus alletteratus Raf., 1810) in the eastern Mediterranean Sea: preliminary results of TUNALEV larval survey in 2004

A tuna larval survey (TUNALEV) in the Northern Levantine Basin (Cilician Basin) was conducted onboard a trawler from 5 to 18 June 2004. To determine the spatial distribution and abundance of tuna larvae, Bongo 60 and Bongo 90 nets were used. Ichtyoplankton samples from 104 stations were taken. In total, 121 bluefin tuna (Thunnus thynnus), 94 bullet tuna (Auxis rochei) and 22 Atlantic black skipjack (Euthynnus alletteratus) larvae were collected. In comparison with the other tuna larvae, the concentration of bluefin tuna larvae was highest in the Bay of Mersin. The collected larvae in this area were composed mainly of 5–9 mm size specimens.     

Spawning Behaviour and Post-Spawning Migration Patterns of Atlantic Bluefin Tuna (Thunnus thynnus) Ascertained from Satellite Archival Tags

Spawning behaviour of Atlantic bluefin tuna (Thunnus thynnus) was investigated using electronic satellite tags deployed in the western Mediterranean spawning ground, around the Balearic Islands (years 2009-2011). All the fish were tagged underwater and released within schools. In general, the fish tagged in the same year/school displayed common migratory trends. Following extended residency around the Balearic Islands, most tagged tuna crossed the Strait of Gibraltar heading for the North Atlantic. Discrepancies between the migratory tracks reconstructed from this and previous electronic tagging studies suggest that the bluefin tuna Mediterranean population may comprise distinct units exhibiting differing migratory behaviours. The diving behaviour varied between oceanic regions throughout the migratory pathways, the shallowest distribution taking place in the spawning ground and the deepest at the Strait of Gibraltar. A unique diving pattern was found on the majority of nights while the fish stayed at the spawning ground; it consisted of frequent and brief oscillatory movements up and down through the mixed layer, resulting in thermal profiles characterized by oscillations about the thermocline. Such a pattern is believed to reflect recent courtship and spawning activity. Reproductive parameters inferred from the analysis of vertical profiles are consistent with those estimated in previous studies based on biological samples.     

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.     

Feeding habits of the Atlantic bluefin tuna, Thunnus thynnus (L. 1758), in the central Mediterranean Sea (Strait of Messina)

The study of feeding habits of the Atlantic bluefin tuna was carried out in 123 specimens, ranging from 115 to 222 cm fork length (FL) and collected during spring seasons of 2010 and 2011 in the central Mediterranean Sea (Strait of Messina). The analysis of stomach contents allowed us to identify 91 taxa of prey items, mainly belonging to Teleostea (54), Cephalopoda (20) and Crustacea (13). The percentage of index of relative abundance (IRI) shows the highest values for the myctophid Hygophum benoiti (%IRI = 22.854) and the stomiid Chauliodus sloani (%IRI = 15.124), followed by the oegopsid squid Illex coindetii (%IRI = 14.316). The broad spectrum of prey items could suggest a generalist behavior of this predator, with several species that occasionally occurs in its diet. However, if prey are grouped into food categories, the importance of mesopelagic and benthopelagic fishes can be appreciated (54.41 % of %IRI). The assessment of the hypothetical foraging rhythm of the Atlantic bluefin tuna highlighted that its feeding activity is concentrated on diel migrating fauna during night and on larger preys upon daylight. The predation on the high-energetic food as mesopelagic and bathypelagic fishes during the pre-spawning and the spawning period may bring an energetic advantage in tuna metabolism and gonadal maturation     

Atlantic Bluefin Tuna (Thunnus thynnus) Biometrics and Condition

The compiled data for this study represents the first Atlantic and Mediterranean-wide effort to pool all available biometric data for Atlantic bluefin tuna (Thunnus thynnus) with the collaboration of many countries and scientific groups. Biometric relationships were based on an extensive sampling (over 140,000 fish sampled), covering most of the fishing areas for this species in the North Atlantic Ocean and Mediterranean Sea. Sensitivity analyses were carried out to evaluate the representativeness of sampling and explore the most adequate procedure to fit the weight-length relationship (WLR). The selected model for the WLRs by stock included standardized data series (common measurement types) weighted by the inverse variability. There was little difference between annual stock-specific round weight-straight fork length relationships, with an overall difference of 6% in weight. The predicted weight by month was estimated as an additional component in the exponent of the weight-length function. The analyses of monthly variations of fish condition by stock, maturity state and geographic area reflect annual cycles of spawning and feeding behavior. We update and improve upon the biometric relationships for bluefin currently used by the International Commission for the Conservation of Atlantic Tunas, by incorporating substantially larger datasets than ever previously compiled, providing complete documentation of sources and employing robust statistical fitting. WLRs and other conversion factors estimated in this study differ from the ones used in previous bluefin stock assessments.     

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.     

Dispersal routes and habitat utilization of juvenile Atlantic bluefin tuna, Thunnus thynnus, tracked with mini PSAT and archival tags

Between 2005 and 2009, we deployed 58 miniature pop-up satellite archival tags (PSAT) and 132 implanted archival tags on juvenile Atlantic bluefin tuna (age 2-5) in the northwest Atlantic Ocean. Data returned from these efforts (n?=?26 PSATs, 1 archival tag) revealed their dispersal routes, horizontal and vertical movements and habitat utilization. All of the tagged bluefin tuna remained in the northwest Atlantic for the duration observed, and in summer months exhibited core-use of coastal seas extending from Maryland to Cape Cod, MA, (USA) out to the shelf break. Their winter distributions were more spatially disaggregated, ranging south to the South Atlantic Bight, northern Bahamas and Gulf Stream. Vertical habitat patterns showed that juvenile bluefin tuna mainly occupied shallow depths (mean=?5-12 m, sd?=?15-23.7 m) and relatively warm water masses in summer (mean=?17.9-20.9°C, sd=?4.2-2.6°C) and had deeper and more variable depth patterns in winter (mean=?41-58 m, sd=?48.9-62.2 m). Our tagging results reveal annual dispersal patterns, behavior and oceanographic associations of juvenile Atlantic bluefin tuna that were only surmised in earlier studies. Fishery independent profiling from electronic tagging also provide spatially and temporally explicit information for evaluating dispersals rates, population structure and fisheries catch patterns.     

Euryphorus brachypterus (Copepoda: Caligidae) on wild pacific bluefin tuna from the Tsugaru Strait,northern Japan

Parasitic copepods infecting large scombrid fishes have been known for a long time because their hosts are economically important. Most studies, however, have focused on their morphology or their infection status in aquaculture from pathological viewpoints, and very few quantitative surveys have been conducted under conditions in the wild. This study therefore investigated the prevalence of Euryphorus brachypterus (Caligidae) in wild Pacific bluefin tuna (PBF). Results of sampling from August to September 2014 at the western area of the Tsugaru Strait, Japan showed that 13.2% of the PBF individuals (n = 1978) were infected with this copepod. The prevalence of infections was highest in larger fish but varied among landing dates, which were classified into three clusters and in all smaller fish, the prevalence of infections was zero. This suggests that E. brachypterus mainly uses the larger PBF, which becomes sources of further infections in other seas, and that at least two host populations with different infection statuses at the strait.     

Discovery of intermediate hosts for two species of blood flukes Cardicola orientalis and Cardicola forsteri (Trematoda: Aporocotylidae) infecting Pacific bluefin tuna in Japan

Fish blood flukes (Aporocotylidae) are important pathogens of farmed finfish around the world. Among them, Cardicola spp. infecting farmed tuna are considered to be serious threats to tuna farming and have received tremendous attention. We conducted periodical samplings at a tuna farming site in Japan between January and May, 2015 to determine the life cycle of Cardicola spp. We collected over 4700 terebellid polychaetes from ropes, floats and frames of tuna culture cages and found nearly 400 infected worms. Sporocysts and cercariae found in Nicolea gracilibranchis were genetically identified as Cardicola orientalis by 28S and ITS2 ribosomal DNA sequences. This was the first discovery of the intermediate host for this parasite species. Infection prevalence and the abundance of N. gracilibranchis significantly varied between sampling points and the highest number of infected terebellids were collected from ropes. We also demonstrated morphologically and molecularly that asexual stages found in a single Amphitrite sp. (Terebellidae) and adult worms isolated from farmed juvenile tuna were Cardicola forsteri. This is the first report of C. forsteri in Pacific bluefin tuna (PBT) Thunnus orientalis in Japan. Our results demonstrated that all three species of Cardicola orientalis, C. forsteri and Cardicola opisthorchis exist in Japanese farmed PBTs and that they all use terebellid polychaetes as the intermediate hosts.     

Isolation and characterization of seven tetranucleotide microsatellite loci from Atlantic northern bluefin tuna Thunnus thynnus thynnus

Microsatellite‐enriched genomic libraries were obtained from the Atlantic northern bluefin tuna, Thunnus thynnus thynnus and seven tetranucleotide markers were successfully isolated and characterized from this library. These markers were found to have between 1 and 17 alleles in Atlantic northern bluefin tuna and heterozygosity ranged from 0 to 0.85. No deviations from the expectation of Hardy‐Weinburg equilibrium were found for any marker. Several of these markers amplify reliably in other tuna species.     

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.