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.     

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.     

Evidence of separate subgroups of juvenile southern bluefin tuna

Archival tagging studies of southern bluefin tuna (SBT, Thunnus maccoyii) have revealed that juveniles residing in the Great Australian Bight (GAB) over the austral summer undertake seasonal cyclic migrations to the southeast Indian Ocean and the Tasman Sea during winter. However, there remains disagreement about the extent of mixing between juvenile SBT regularly caught by longline fleets south of Africa and those observed in the GAB. Some researchers have argued that archival tag recoveries indicate most juveniles reside in the GAB over the austral summer. Others have suggested that recoveries of conventional and archival tags are better explained by a juvenile population consisting of separate groups on the eastern and western sides of the Indian Ocean with limited intermixing. We present analyses of catch and tag recovery data and re‐examine archival tagging studies. The evidence provided strongly favors the hypothesis of separate juvenile subgroups, or contingents, with limited intermixing. We draw some tentative conclusions about the nature of the putative contingents and discuss some implications of these findings for the interpretation of existing datasets and future research priorities. We also provide the first evidence that the migration choices of juveniles that summer in the GAB are influenced by fidelity to winter feeding grounds and suggest this helps explain the collapse of the surface fishery off New South Wales in the 1980s.     

Results of satellite tagging of Atlantic bluefin tuna, <Emphasis Type="Italic">Thunnus thynnus</Emphasis>, off the coast of Ireland

Pop-up satellite archival tags were attached to six Atlantic bluefin tuna (Thunnus thynnus) off the west coast of Ireland in autumn 2003 and 2004. The satellite tags measured pressure, ambient temperature and light for the term of deployment. Radio pop-up satellite endpoint positions, light and sea surface temperature estimations of geolocation indicate that two fish tagged minutes apart off the coast of County Donegal, migrated to the eastern and western Atlantic Ocean over the following 8 months. The two fish were 5218 km apart at the termination of the experiment. After tagging in September and popping up the following March and April, one fish had traveled to the western Atlantic while the other was located in the waters off the southwest coast of Portugal. A third fish tagged off the coast of County Donegal in October 2004 moved into the Mediterranean Sea and was caught by a fishing vessel southeast of Malta on 11 June 2005. The results link bluefin tuna feeding on European foraging grounds with known eastern breeding regions and western Atlantic waters.     

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.     

Immature Pacific bluefin tuna, <Emphasis Type="Italic">Thunnus orientalis</Emphasis>, utilizes cold waters in the Subarctic Frontal Zone for trans-Pacific migration

The habitat and movements of a Pacific bluefin tuna were investigated by reanalyzing archival tag data with sea surface temperature data. During its trans-Pacific migration to the eastern Pacific, the fish took a direct path and primarily utilized waters, in the Subarctic Frontal Zone (SFZ). Mean ambient temperature during the trans-Pacific migration was 14.5 ± 2.9 (°C ± SD), which is significantly colder than the waters typically inhabited by bluefin tuna in their primary feeding grounds in the western and eastern Pacific (17.6 ± 2.1). The fish moved rapidly through the colder water, and the heat produced during swimming and the thermoconservation ability of bluefin tuna likely enabled it to migrate through the cold waters of the SFZ.     

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.     

Shark Tagging: A Review Of Conventional Methods and Studies

The tagging of sharks using conventional tags has long been recognized as a valuable means for studying various aspects of their life history, migrations and movements, and population structure. Conventional tags are defined as those that can be identified visually without the use of special detection equipment. Tagging studies specifically targeting sharks began in the late 1920's, and today numerous cooperative shark tagging programs exist worldwide. Cooperative programs depend on the joint participation of scientists and public volunteers to accomplish research objectives. Benefits and problems of these programs are discussed using the tagging methodologies, protocols, and results of the National Marine Fisheries Service Cooperative Shark Tagging Program. An additional 63 shark tagging studies and programs of all types are reviewed. Information useful for behavioral, biological, and fishery management studies can be derived from data resulting from these studies, including species and size composition, sex ratios, spatial and temporal distribution, migrations, movement patterns, rates of travel, delineation of pupping grounds, distribution of maturity intervals, indices of relative abundance, and recognition of individuals. Specific tagging experiments can be designed to provide additional data on age and growth, homing and site fidelity, dispersal rate, residence time, movement rates, tag shedding, and population parameters (e.g. size, mortality, recruitment, exploitation, interaction rates, and stock identity). Sources of bias inherent in tagging and recapture data include mortality, variation in tagging effort and fishing pressure, non-recovery and non-reporting of tags, and tag shedding. Recent advances in tagging methodologies that complement and extend conventional tagging studies will further our knowledge on shark movements and migrations, particularly in the areas of resource utilization and management, space utilization, and population dynamics.     

Estimating animal behavior and residency from movement data

We present a process‐based approach to estimate residency and behavior from uncertain and temporally correlated movement data collected with electronic tags. The estimation problem is formulated as a hidden Markov model (HMM) on a spatial grid in continuous time, which allows straightforward implementation of barriers to movement. Using the grid to explicitly resolve space, location estimation can be supplemented by or based entirely on environmental data (e.g. temperature, daylight). The HMM method can therefore analyze any type of electronic tag data. The HMM computes the joint posterior probability distribution of location and behavior at each point in time. With this, the behavioral state of the animal can be associated to regions in space, thus revealing migration corridors and residence areas. We demonstrate the inferential potential of the method by analyzing satellite‐linked archival tag data from a southern bluefin tuna Thunnus maccoyii where longitudinal coordinates inferred from daylight are supplemented by latitudinal information in recorded sea surface temperatures.     

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.     

Vulnerability of the Oceanic Whitetip Shark to Pelagic Longline Fisheries

A combination of fisheries dependent and independent data was used to assess the vulnerability of the oceanic whitetip shark to pelagic longline fisheries. The Brazilian tuna longline fleet, operating in the equatorial and southwestern Atlantic, is used as a case study. Fisheries dependent data include information from logbooks (from 1999 to 2011) and on-board observers (2004 to 2010), totaling 65,277 pelagic longline sets. Fisheries independent data were obtained from 8 oceanic whitetip sharks tagged with pop-up satellite archival tags in the area where longline fleet operated. Deployment periods varied from 60 to 178 days between 2010 and 2012. Tagging and pop-up sites were relatively close to each other, although individuals tended to travel long distances before returning to the tagging area. Some degree of site fidelity was observed. High utilization hotspots of tagged sharks fell inside the area under strongest fishing pressure. Despite the small sample size, a positive correlation between tag recorded information and catch data was detected. All sharks exhibited a strong preference for the warm and shallow waters of the mixed layer, spending on average more than 70% of the time above the thermocline and 95% above 120 m. Results indicate that the removal of shallow hooks on longline gear might be an efficient mitigation measure to reduce the bycatch of this pelagic shark species. The work also highlights the potential of tagging experiments to provide essential information for the development of spatio-temporal management measures.     

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     

Classifying movement behaviour in relation to environmental conditions using hidden Markov models

1.  Linking the movement and behaviour of animals to their environment is a central problem in ecology. Through the use of electronic tagging and tracking (ETT), collection of in situ data from free-roaming animals is now commonplace, yet statistical approaches enabling direct relation of movement observations to environmental conditions are still in development.
2.  In this study, we examine the hidden Markov model (HMM) for behavioural analysis of tracking data. HMMs allow for prediction of latent behavioural states while directly accounting for the serial dependence prevalent in ETT data. Updating the probability of behavioural switches with tag or remote-sensing data provides a statistical method that links environmental data to behaviour in a direct and integrated manner.
3.  It is important to assess the reliability of state categorization over the range of time-series lengths typically collected from field instruments and when movement behaviours are similar between movement states. Simulation with varying lengths of times series data and contrast between average movements within each state was used to test the HMMs ability to estimate movement parameters.
4.  To demonstrate the methods in a realistic setting, the HMMs were used to categorize resident and migratory phases and the relationship between movement behaviour and ocean temperature using electronic tagging data from southern bluefin tuna ( Thunnus maccoyii ). Diagnostic tools to evaluate the suitability of different models and inferential methods for investigating differences in behaviour between individuals are also demonstrated.     

Development of an automated method of detecting stereotyped feeding events in multisensor data from tagged rorqual whales

The introduction of animal‐borne, multisensor tags has opened up many opportunities for ecological research, making previously inaccessible species and behaviors observable. The advancement of tag technology and the increasingly widespread use of bio‐logging tags are leading to large volumes of sometimes extremely detailed data. With the increasing quantity and duration of tag deployments, a set of tools needs to be developed to aid in facilitating and standardizing the analysis of movement sensor data. Here, we developed an observation‐based decision tree method to detect feeding events in data from multisensor movement tags attached to fin whales (Balaenoptera physalus). Fin whales exhibit an energetically costly and kinematically complex foraging behavior called lunge feeding, an intermittent ram filtration mechanism. Using this automated system, we identified feeding lunges in 19 fin whales tagged with multisensor tags, during a total of over 100 h of continuously sampled data. Using movement sensor and hydrophone data, the automated lunge detector correctly identified an average of 92.8% of all lunges, with a false‐positive rate of 9.5%. The strong performance of our automated feeding detector demonstrates an effective, straightforward method of activity identification in animal‐borne movement tag data. Our method employs a detection algorithm that utilizes a hierarchy of simple thresholds based on knowledge of observed features of feeding behavior, a technique that is readily modifiable to fit a variety of species and behaviors. Using automated methods to detect behavioral events in tag records will significantly decrease data analysis time and aid in standardizing analysis methods, crucial objectives with the rapidly increasing quantity and variety of on‐animal tag data. Furthermore, our results have implications for next‐generation tag design, especially long‐term tags that can be outfitted with on‐board processing algorithms that automatically detect kinematic events and transmit ethograms via acoustic or satellite telemetry.     

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.     

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.     

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.     

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.     

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.     

Peptides from the SARS-associated coronavirus as tags for protein expression and purification

Protein tagging with a peptide is a commonly used technique to facilitate protein detection and to carry out protein purification. Flexibility with respect to the peptide tag is essential since no single tag suites all purposes. This report describes the usage of two short peptides from the SARS-associated coronavirus nucleocapsid (SARS-N) protein as protein tags. Plasmids for the generation of tagged proteins were generated by ligating synthetic oligonucleotides for the peptide-coding regions downstream of the protein coding sequence. The data show recognition of prokaryotically expressed HIV-1 Gag/p24 fusion protein by Western blot and efficient affinity purification using monoclonal antibodies against the tags. The SARS peptide antibody system described presents an alternative tagging opportunity in the growing field of protein science.