Unidirectional trans-Atlantic gene flow and a mixed spawning area shape the genetic connectivity of Atlantic bluefin tuna.

The commercially important Atlantic bluefin tuna (Thunnus thynnus), a large migratory fish, has experienced notable recovery aided by accurate resource assessment and effective fisheries management efforts. Traditionally, this species has been perceived as consisting of eastern and western populations, spawning respectively in the Mediterranean Sea and the Gulf of Mexico, with mixing occurring throughout the Atlantic. However, recent studies have challenged this assumption by revealing weak genetic differentiation and identifying a previously unknown spawning ground in the Slope Sea used by Atlantic bluefin tuna of uncertain origin. To further understand the current and past population structure and connectivity of Atlantic bluefin tuna, we have assembled a unique dataset including thousands of genome-wide single-nucleotide polymorphisms (SNPs) from 500 larvae, young of the year and spawning adult samples covering the three spawning grounds and including individuals of other Thunnus species. Our analyses support two weakly differentiated but demographically connected ancestral populations that interbreed in the Slope Sea. Moreover, we also identified signatures of introgression from albacore (Thunnus alalunga) into the Atlantic bluefin tuna genome, exhibiting varied frequencies across spawning areas, indicating strong gene flow from the Mediterranean Sea towards the Slope Sea. We hypothesize that the observed genetic differentiation may be attributed to increased gene flow caused by a recent intensification of westward migration by the eastern population, which could have implications for the genetic diversity and conservation of western populations. Future conservation efforts should consider these findings to address potential genetic homogenization in the species.

Prevalence, intensity and pathology of the nasal parasite Nasicola hogansi in Atlantic bluefin tuna (Thunnus thynnus).

Ectoparasitic flatworms of Nasicola (Monogenoidea: Capsalidae), which infect nasal epithelium of true tunas (Thunnus spp.), are not well studied, nor have their impacts on the host's olfactory organ been evaluated. Infections of Nasicola hogansi on Atlantic bluefin tuna, Thunnus thynnus, were investigated with emphasis on the relationship between infection prevalence, abundance and mean intensity with bluefin tuna size, sex, body condition and capture month, as well as histopathological effects. Commercially caught Atlantic bluefin tuna (n = 161, 185-305 cm curved fork length) from the Gulf of Maine were sampled during June through August 2009 for infections by N. hogansi. A total of 247 specimens of N. hogansi were collected, with a prevalence of 45.3%, mean abundance of 1.57 (CI: 1.21-2.03) and mean intensity of 3.45 (CI: 2.91-4.22). Neither fish sex nor landing month had a significant effect on parasite parameters. Larger and better-conditioned Atlantic bluefin tuna had a higher mean intensity of infection. Pathology associated with infection by N. hogansi included extensive necrosis, sloughing of the nasal epithelium and associated inflammation of underlying connective tissues. Further epidemiological and pathological study of this host-parasite system is warranted since impaired olfaction, if present, could adversely affect spawning and migration of this top ocean predator.

Discovery of a spawning ground reveals diverse migration strategies in Atlantic bluefin tuna (Thunnus thynnus).

Atlantic bluefin tuna are a symbol of both the conflict between preservationist and utilitarian views of top ocean predators, and the struggle to reach international consensus on the management of migratory species. Currently, Atlantic bluefin tuna are managed as an early-maturing eastern stock, which spawns in the Mediterranean Sea, and a late-maturing western stock, which spawns in the Gulf of Mexico. However, electronic tagging studies show that many bluefin tuna, assumed to be of a mature size, do not visit either spawning ground during the spawning season. Whether these fish are spawning in an alternate location, skip-spawning, or not spawning until an older age affects how vulnerable this species is to anthropogenic stressors including exploitation. We use larval collections to demonstrate a bluefin tuna spawning ground in the Slope Sea, between the Gulf Stream and northeast United States continental shelf. We contend that western Atlantic bluefin tuna have a differential spawning migration, with larger individuals spawning in the Gulf of Mexico, and smaller individuals spawning in the Slope Sea. The current life history model, which assumes only Gulf of Mexico spawning, overestimates age at maturity for the western stock. Furthermore, individual tuna occupy both the Slope Sea and Mediterranean Sea in separate years, contrary to the prevailing view that individuals exhibit complete spawning-site fidelity. Overall, this complexity of spawning migrations questions whether there is complete independence in the dynamics of eastern and western Atlantic bluefin tuna and leads to lower estimates of the vulnerability of this species to exploitation and other anthropogenic stressors.

Declining Mercury Concentrations in Bluefin Tuna Reflect Reduced Emissions to the North Atlantic Ocean.

Tunas are apex predators in marine food webs that can accumulate mercury (Hg) to high concentrations and provide more Hg (∼40%) to the U.S population than any other source. We measured Hg concentrations in 1292 Atlantic bluefin tuna (ABFT, Thunnus thynnus) captured in the Northwest Atlantic from 2004 to 2012. ABFT Hg concentrations and variability increased nonlinearly with length, weight, and age, ranging from 0.25 to 3.15 mg kg-1, and declined significantly at a rate of 0.018 ± 0.003 mg kg-1 per year or 19% over an 8-year period from the 1990s to the early 2000s. Notably, this decrease parallels comparably reduced anthropogenic Hg emission rates in North America and North Atlantic atmospheric Hg0 concentrations during this period, suggesting that recent efforts to decrease atmospheric Hg loading have rapidly propagated up marine food webs to a commercially important species. This is the first evidence to suggest that emission reduction efforts have resulted in lower Hg concentrations in large, long-lived fish.

Orientation behaviour of leatherback sea turtles within the North Atlantic subtropical gyre.

Leatherback sea turtles (Dermochelys coriacea) travel thousands of kilometres between temperate feeding and tropical breeding/over-wintering grounds, with adult turtles able to pinpoint specific nesting beaches after multi-year absences. Their extensive migrations often occur in oceanic habitat where limited known sensory information is available to aid in orientation. Here, we examined the migratory orientation of adult male, adult female and subadult leatherbacks during their open-ocean movements within the North Atlantic subtropical gyre by analysing satellite-derived tracks from fifteen individuals over a 2-year period. To determine the turtles' true headings, we corrected the reconstructed tracks for current drift and found negligible differences between current-corrected and observed tracks within the gyre. Individual leatherback headings were remarkably consistent throughout the subtropical gyre, with turtles significantly oriented to the south-southeast. Adult leatherbacks of both sexes maintained similar mean headings and showed greater orientation precision overall. The consistent headings maintained by adult and subadult leatherbacks within the gyre suggest use of a common compass sense.

Near resonance acoustic scattering from organized schools of juvenile Atlantic bluefin tuna (Thunnus thynnus).

Schools of Atlantic bluefin tuna (Thunnus thynnus) can exhibit highly organized spatial structure within the school. This structure was quantified for dome shaped schools using both aerial imagery collected from a commercial spotter plane and 400 kHz multibeam echo sounder data collected on a fishing vessel in 2009 in Cape Cod Bay, MA. Observations from one school, containing an estimated 263 fish within an approximately ellipsoidal volume of 1900 m(3), were used to seed an acoustic model that estimated the school target strength at frequencies between 10 and 2000 Hz. The fish's swimbladder resonance was estimated to occur at approximately 50 Hz. The acoustic model examined single and multiple scattering solutions and also a completely incoherent summation of scattering responses from the fish. Three levels of structure within the school were examined, starting with fish locations that were constrained by the school boundaries but placed according to a Poisson process, then incorporating a constraint on the distance to the nearest neighbor, and finally adding a constraint on the bearing to the nearest neighbor. Results suggest that both multiple scattering and spatial organization within the school should be considered when estimating the target strength of schools similar to the ones considered here.

Behaviour and buoyancy regulation in the deepest-diving reptile: the leatherback turtle.

In the face of the physical and physiological challenges of performing breath-hold deep dives, marine vertebrates have evolved different strategies. Although behavioural strategies in marine mammals and seabirds have been investigated in detail, little is known about the deepest-diving reptile - the leatherback turtle (Dermochelys coriacea). Here, we deployed tri-axial accelerometers on female leatherbacks nesting on St Croix, US Virgin Islands, to explore their diving strategy. Our results show a consistent behavioural pattern within dives among individuals, with an initial period of active swimming at relatively steep descent angles (∼-40 deg), with a stroke frequency of 0.32 Hz, followed by a gliding phase. The depth at which the gliding phase began increased with the maximum depth of the dives. In addition, descent body angles and vertical velocities were higher during deeper dives. Leatherbacks might thus regulate their inspired air-volume according to the intended dive depth, similar to hard-shelled turtles and penguins. During the ascent, turtles actively swam with a stroke frequency of 0.30 Hz but with a low vertical velocity (∼0.40 ms(-1)) and a low pitch angle (∼+26 deg). Turtles might avoid succumbing to decompression sickness ('the bends') by ascending slowly to the surface. In addition, we suggest that the low body temperature of this marine ectotherm compared with that of endotherms might help reduce the risk of bubble formation by increasing the solubility of nitrogen in the blood. This physiological advantage, coupled with several behavioural and physical adaptations, might explain the particular ecological niche the leatherback turtle occupies among marine reptiles.

Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods.

1. Lipids have more negative delta(13)C values relative to other major biochemical compounds in plant and animal tissues. Although variable lipid content in biological tissues alters results and conclusions of delta(13)C analyses in aquatic food web and migration studies, no standard correction protocol exists. 2. We compared chemical extraction and mathematical correction methods for freshwater and marine fishes and aquatic invertebrates to better understand impacts of correction approaches on carbon (delta(13)C) and nitrogen (delta(15)N) stable isotope data. 3. Fish and aquatic invertebrate tissue delta(13)C values increased significantly following extraction for almost all species and tissue types relative to nonextracted samples. In contrast, delta(15)N was affected for muscle and whole body samples from only a few freshwater and marine species and had a limited effect for the entire data set. 4. Lipid normalization models, using C : N as a proxy for lipid content, predicted lipid-corrected delta(13)C for paired data sets more closely with parameters specific to the tissue type and species to which they were applied. 5. We present species- and tissue-specific models based on bulk C : N as a reliable alternative to chemical extraction corrections. By analysing a subset of samples before and after lipid extraction, models can be applied to the species and tissues of interest that will improve estimates of dietary sources using stable isotopes.

Spatial dynamics and mixing of bluefin tuna in the Atlantic Ocean and Mediterranean Sea revealed using next-generation sequencing.

The Atlantic bluefin tuna is a highly migratory species emblematic of the challenges associated with shared fisheries management. In an effort to resolve the species' stock dynamics, a genomewide search for spatially informative single nucleotide polymorphisms (SNPs) was undertaken, by way of sequencing reduced representation libraries. An allele frequency approach to SNP discovery was used, combining the data of 555 larvae and young-of-the-year (LYOY) into pools representing major geographical areas and mapping against a newly assembled genomic reference. From a set of 184,895 candidate loci, 384 were selected for validation using 167 LYOY. A highly discriminatory genotyping panel of 95 SNPs was ultimately developed by selecting loci with the most pronounced differences between western Atlantic and Mediterranean Sea LYOY. The panel was evaluated by genotyping a different set of LYOY (n = 326), and from these, 77.8% and 82.1% were correctly assigned to western Atlantic and Mediterranean Sea origins, respectively. The panel revealed temporally persistent differentiation among LYOY from the western Atlantic and Mediterranean Sea (FST  = 0.008, p = .034). The composition of six mixed feeding aggregations in the Atlantic Ocean and Mediterranean Sea was characterized using genotypes from medium (n = 184) and large (n = 48) adults, applying population assignment and mixture analyses. The results provide evidence of persistent population structuring across broad geographic areas and extensive mixing in the Atlantic Ocean, particularly in the mid-Atlantic Bight and Gulf of St. Lawrence. The genomic reference and genotyping tools presented here constitute novel resources useful for future research and conservation efforts.

Sailfish migrations connect productive coastal areas in the West Atlantic Ocean.

Isla Mujeres, Mexico is home to one of the most well-known aggregations of sailfish. Despite its fisheries prominence, little is known about this sailfish assemblage, or its relationship to other aggregation sites in the western Atlantic. In January 2012, April 2013 and 2014, we deployed 34 popup satellite archival tags on sailfish in order to study their behavior, population connectivity and biophysical interactions. Sailfish were monitored for up to one year, and displayed (1) predominantly shelf associated activity (2) occupancy of the Yucatán Current near Isla Mujeres for up to five months and (3) subsequent dispersals from the Yucatán to productive coastal areas in the Gulf of Mexico, the Caribbean Sea and along the South American coast. Tagged sailfish occupied a median temperature of 26.4°C (interquartile range, IQR = 2.5 °C; range = 12.3-33.3 °C) and median depth of 4.4 m (IQR = 19 m; range = 0-452 m). Diel activity was present and individuals made distinctive descents before sunrise and sunset. Tracking missions of sufficient duration (~1 year) revealed previously undetected connectivity between western Atlantic sailfish fisheries and pelagic longline catches, and highlighted how fishery independent tagging can improve understanding of sailfish migrations and behavior for assessment and management.

Leatherback turtle movements, dive behavior, and habitat characteristics in ecoregions of the Northwest Atlantic Ocean.

Leatherback sea turtles, Dermochelys coriacea, are highly migratory predators that feed exclusively on gelatinous zooplankton, thus playing a unique role in coastal and pelagic food webs. From 2007 to 2010, we used satellite telemetry to monitor the movements and dive behavior of nine adult and eleven subadult leatherbacks captured on the Northeast USA shelf and tracked throughout the Northwest Atlantic. Leatherback movements and environmental associations varied by oceanographic region, with slow, sinuous, area-restricted search behavior and shorter, shallower dives occurring in cool (median sea surface temperature: 18.4°C), productive (median chlorophyll a: 0.80 mg m(-3)), shallow (median bathymetry: 57 m) shelf habitat with strong sea surface temperature gradients (median SST gradient: 0.23°C km(-1)) at temperate latitudes. Leatherbacks were highly aggregated in temperate shelf and slope waters during summer, early fall, and late spring and more widely dispersed in subtropical and tropical oceanic and neritic habitat during late fall, winter and early spring. We investigated the relationship of ecoregion, satellite-derived surface chlorophyll, satellite-derived sea surface temperature, SST gradient, chlorophyll gradient and bathymetry with leatherback search behavior using generalized linear mixed-effects models. The most well supported model showed that differences in leatherback search behavior were best explained by ecoregion and regional differences in bathymetry and SST. Within the Northwest Atlantic Shelves region, leatherbacks increased path sinuosity (i.e., looping movements) with increasing SST, but this relationship reversed within the Gulf Stream region. Leatherbacks increased path sinuosity with decreasing water depth in temperate and tropical shelf habitats. This relationship is consistent with increasing epipelagic gelatinous zooplankton biomass with decreasing water depth, and bathymetry may be a key feature in identifying leatherback foraging habitat in neritic regions. High-use habitat for leatherbacks in our study occurred in coastal waters of the North American eastern seaboard and eastern Caribbean, putting turtles at heightened risk from land- and ocean-based human activity.

Comparative assessment of the reproductive status of female Atlantic bluefin tuna from the Gulf of Mexico and the Mediterranean Sea.

Despite attention focused on the population status and rebuilding trajectory of Atlantic bluefin tuna (Thunnus thynnus), the reproduction and spawning biology remains poorly understood, especially in the NW Atlantic. At present, the eastern and western spawning populations are believed to exhibit different reproductive characteristics and, consequently, stock productivity. However, our study suggests that the two spawning populations, the Gulf of Mexico and the Mediterranean Sea, could show similar reproductive features and spawning strategies. Between 2007 and 2009, gonad samples from female Atlantic bluefin tuna were collected in the northern Gulf of Mexico (n = 147) and in the western Mediterranean Sea (n = 40). The histological and stereological analysis confirmed that sampled eastern and western bluefin tuna exhibit the same spawning duration (three months) but the spawning in the Gulf of Mexico begins one month earlier than in the Mediterranean Sea. Western bluefin tuna caught in the peak of the spawning season (May) showed a similar spawning frequency (60%) to the spawning peak observed in the Mediterranean Sea (June). Fecundity for the Gulf of Mexico fish (28.14 eggs · g(-1)) was lower but not significantly different than for fish sampled in the Mediterranean Sea (45.56 eggs · g(-1)). Our study represents the first comparative histological analysis of the eastern and western spawning stocks whose findings, combined with new determinations of size/age at maturity and possible alternative spawning areas, might suggest basic life history attributes warrant further scientific and management attention.

Sexual maturity in western Atlantic bluefin tuna.

We introduce a novel endocrine approach for assessing the unresolved matter of the timing of sexual maturation in western Atlantic bluefin tuna (ABFT), a highly migratory population whose status remains uncertain. Ratios of follicle stimulating hormone to luteinizing hormone, a sexual maturity indicator, in all ABFT ≥ 134 cm curved fork length (CFL) were <0.4, similar to Mediterranean spawners, indicating that western ABFT mature at considerably smaller sizes and at a much younger age than currently assumed (≥ 185 cm CFL).

Serial assessment of the physiological status of leatherback turtles (Dermochelys coriacea) during direct capture events in the northwestern Atlantic Ocean: comparison of post-capture and pre-release data.

The physiological status of seven leatherback turtles (Dermochelys coriacea) was assessed at two time points during ecological research capture events in the northwestern Atlantic Ocean. Data were collected as soon as possible after securing each turtle onboard the capture vessel and again immediately prior to release. Measured parameters included sea surface temperature, body temperature, morphometric data, sex, heart rate, respiratory rate and various haematological and blood biochemical variables. Results indicated generally stable physiological status in comparison to previously published studies of this species. However, blood pH and blood potassium concentrations increased significantly between the two time points (P = 0.0018 and P = 0.0452, respectively). Turtles were affected by a mild initial acidosis (mean [SD] temperature-corrected pH = 7.29 [0.07]), and blood pH increased prior to release (mean [SD] = 7.39 [0.07]). Initial blood potassium concentrations were considered normal (mean [SD] = 4.2 [0.9] mmol/l), but turtles experienced a mild to moderate increase in blood potassium concentrations during the event (mean [SD] pre-release potassium = 5.9 [1.7] mmol/l, maximum = 8.5 mmol/l). While these data support the general safety of direct capture for study of this species, the observed changes in blood potassium concentrations are of potential concern due to possible adverse effects of hyperkalaemia on cardiac function. The results of this study highlight the importance of physiological monitoring during scientific capture events. The results are also likely to be relevant to unintentional leatherback capture events (e.g. fisheries interactions), when interactions may be more prolonged or extreme.

Changes in the distribution of atlantic bluefin tuna (Thunnus thynnus) in the Gulf of Maine 1979-2005.

The Gulf of Maine, NW Atlantic Ocean, is a productive, seasonal foraging ground for Atlantic bluefin tuna (Thunnus thynnus), but commercial landings of adult size classes were up to 40% below the allocated total allowable catch between 2004 to 2008 for the rod and reel, harpoon, and purse seine categories in the Gulf of Maine. Reduction in Atlantic bluefin tuna catches in the Gulf of Maine could represent a decline in spawning stock biomass, but given wide-ranging, complex migration patterns, and high energetic requirements, an alternative hypothesis is that their dispersal patterns shifted to regions with higher prey abundance or profitability, reducing availability to U.S. fishing fleets. This study fit generalized linear models to Atlantic bluefin tuna landings data collected from fishermen's logbooks (1979-2005) as well as the distances between bluefin tuna schools and Atlantic herring (Clupeaharengus), a primary prey species, to test alternative hypotheses for observed shifts in Atlantic bluefin tuna availability in the Gulf of Maine. For the bluefin model, landings varied by day of year, latitude and longitude. The effect of latitude differed by day of year and the effect of longitude differed by year. The distances between Atlantic bluefin tuna schools and Atlantic herring schools were significantly smaller (p<0.05) than would be expected from a randomly distributed population. A time series of average bluefin tuna school positions was positively correlated with the average number of herring captured per tow on Georges Bank in spring and autumn surveys respectively (p<0.01, r(2)=0.24, p<0.01, r(2)=0.42). Fishermen's logbooks contributed novel spatial and temporal information towards testing these hypotheses for the bluefin tuna fishery.

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.

A comparison of carbon and nitrogen stable isotope ratios of fish tissues following lipid extractions with non-polar and traditional chloroform/methanol solvent systems.

Stable isotope ratios act as chemical tracers of animal diet, and are used to study food web dynamics. Because carbon stable isotope values are influenced by tissue lipid content, a number of extraction methods have been used to remove lipid bias, but, in some species and tissues, extractions also alter nitrogen isotope values. We have analyzed delta(13)C and delta(15)N in Atlantic bluefin tuna liver and white muscle, and whole Atlantic herring, fish tissues covering a wide range of lipid content (bulk C:N 3.1-12.5). In order to compare delta(13)C and delta(15)N values from traditional chloroform/methanol extractions with non-polar solvent alternatives, we analyzed samples following (1) no treatment, (2) lipid removal using chloroform/methanol (2:1), and (3) Soxhlet extractions using chloroform, diethyl ether or hexane. Chloroform/methanol and chloroform extractions produced the lowest C:N values and highest delta(13)C values. In bluefin tuna, chloroform and hexane extractions significantly altered liver delta(15)N, and all methods significantly altered delta(15)N values in white muscle. Whole Atlantic herring delta(15)N was not altered by any extraction method, while the 2:1 chloroform/methanol extraction most completely removed fish tissue lipid components. Our results indicate that delta(15)N effects are not limited to common chloroform/methanol extractions and suggest that chloroform/methanol is the most effective extraction for delta(13)C correction. Given evidence for delta(15)N alteration among all tested methods, mathematical correction approaches should be further explored as an alternative to lipid correction.

Inferring resource distributions from Atlantic bluefin tuna movements: an analysis based on net displacement and length of track.

We use observed movement tracks of Atlantic bluefin tuna in the Gulf of Maine and mathematical modeling of this movement to identify possible resource patches. We infer bounds on the overall sizes and distribution of such patches, even though they are difficult to quantify by direct observation in situ. To do so, we segment individual fish tracks into intervals of distinct motion types based on the ratio of net displacement to length of track (DeltaD/DeltaL) over a time window Deltat. To find the best segmentation, we optimize the fit of a random-walk movement model to each motion type. We compare results from two distinct movement models: biased turning and biased speed, to check the model-dependence of our inferences, and find that uncertainty in choice of movement model dominates the uncertainties of our conclusions. We find that our data are best described using two motion types: "localized" (DeltaD/DeltaL small) and "long-ranged" (DeltaD/DeltaL large). The biased turning model leads to significantly better resolution of localized movement intervals than the biased speed model. We hypothesize that localized movement corresponds to exploitation of resource patches. Comparison with visual behavior observations made during tracking suggests that many inferred intervals of localized motion do indeed correspond to feeding activity. From our analysis, we estimate that, on average, bluefin tuna in the Gulf of Maine encounter a resource patch every 2h, that those patches have an average radius of 0.7-1.2 km, and that, overall, there are at most 5-9 such patches per 100 km(2) in the region studied.