Temperature dependent pre- and postprandial activity in Pacific bluefin tuna (Thunnus orientalis).

Bluefin tunas are highly specialized fish with unique hydrodynamic designs and physiological traits. In this study, we present results in a captive population that demonstrate strong effects of ambient temperature on the tail beat frequency and swimming speed of a pelagic fish in both pre- and post-prandial states. We measured the responses of a ram ventilator, the Pacific bluefin tuna (Thunnus orientalis), after digestion of a meal to explore the impacts of the metabolic costs of digestion on behavior and respiration. A combination of respirometry, physiological biologging of visceral temperatures, and activity monitoring with accelerometry were used to explore the metabolic costs of digestion and the impacts on ventilation and swimming speed. Experiments were conducted at temperatures that are within the metabolic optimum for Pacific bluefin tuna (17 °C), and at a second temperature corresponding to the upper distributional limit of the species in the California Current (24 °C). Warmer temperatures resulted in higher tail-beat frequency and greater elevation of body temperature in pre-prandial Pacific bluefin tuna. Specific dynamic action (SDA) events resulted in a significant postprandial increase in tail-beat frequency of ~0.2 Hz, compared to pre-prandial levels of 1.5 Hz (17 °C) and 1.75 Hz (24 °C), possibly resulting from ventilatory requirements. Data of fish exercised in a swim-tunnel respirometer suggest that the observed increase in tail-beat frequency comprise 5.5 and 6.8% of the oxygen demand during peak SDA at 24 °C and 17 °C respectively. The facultative increase in swimming speed might increase oxygen uptake at the gills to meet the increasing demand by visceral organs involved in the digestive process, potentially decreasing the available energy of each meal for other metabolic processes, such as growth, maturation, and reproduction. We hypothesize that these post-prandial behaviors allow tuna to evacuate their guts more quickly, ultimately permitting fish to feed more frequently when prey is available.

The effect of temperature on postprandial metabolism of yellowfin tuna (Thunnus albacares).

Specific dynamic action (SDA), the increase in metabolic expenditure associated with consumption of a meal, represents a substantial portion of fish energy budgets and is highly influenced by ambient temperature. The effect of temperature on SDA has not been studied in yellowfin tuna (Thunnus albacares, Bonnaterre 1788), an active pelagic predator that occupies temperate and subtropical waters. The energetic cost and duration of SDA were calculated by comparing routine and post-prandial oxygen consumption rates. Mean routine metabolic rates in yellowfin tuna increased with temperature, from 136 mg O2 kg(-1)h(-1) at 20 °C to 211 mg O2 kg(-1)h at 24 °C. The mean duration of SDA decreased from 40.2h at 20 °C to 33.1h at 24 °C, while mean SDA coefficient, the percentage of energy in a meal that is consumed during digestion, increased from 5.9% at 20 °C to 12.7% at 24 °C. Digestion in yellowfin tuna is faster at a higher temperature but requires additional oxidative energy. Enhanced characterization of the role of temperature in SDA of yellowfin tuna deepens our understanding of tuna physiology and can help improve management of aquaculture and fisheries.

Electronic tagging and population structure of Atlantic bluefin tuna.

Electronic tags that archive or transmit stored data to satellites have advanced the mapping of habitats used by highly migratory fish in pelagic ecosystems. Here we report on the electronic tagging of 772 Atlantic bluefin tuna in the western Atlantic Ocean in an effort to identify population structure. Reporting electronic tags provided accurate location data that show the extensive migrations of individual fish (n = 330). Geoposition data delineate two populations, one using spawning grounds in the Gulf of Mexico and another from the Mediterranean Sea. Transatlantic movements of western-tagged bluefin tuna reveal site fidelity to known spawning areas in the Mediterranean Sea. Bluefin tuna that occupy western spawning grounds move to central and eastern Atlantic foraging grounds. Our results are consistent with two populations of bluefin tuna with distinct spawning areas that overlap on North Atlantic foraging grounds. Electronic tagging locations, when combined with US pelagic longline observer and logbook catch data, identify hot spots for spawning bluefin tuna in the northern slope waters of the Gulf of Mexico. Restrictions on the time and area where longlining occurs would reduce incidental catch mortalities on western spawning grounds.

Influence of swimming speed on metabolic rates of juvenile pacific bluefin tuna and yellowfin tuna.

Bluefin tuna are endothermic and have higher temperatures, heart rates, and cardiac outputs than tropical tuna. We hypothesized that the increased cardiovascular capacity to deliver oxygen in bluefin may be associated with the evolution of higher metabolic rates. This study measured the oxygen consumption of juvenile Pacific bluefin Thunnus orientalis and yellowfin tuna Thunnus albacares swimming in a swim-tunnel respirometer at 20 degrees C. Oxygen consumption (Mo2) of bluefin (7.1-9.4 kg) ranged from 235+/-38 mg kg(-1) h(-1) at 0.85 body length (BL) s(-1) to 498+/-55 mg kg(-1) h(-1) at 1.80 BL s(-1). Minimal metabolic rates of swimming bluefin were 222+/-24 mg O(2) kg(-1) h(-1) at speeds of 0.75 to 1.0 BL s(-1). Mo2 of T. albacares (3.7-7.4 kg) ranged from 164+/-18 mg kg(-1) h(-1) at 0.65 BL s(-1) to 405+/-105 mg kg(-1) h(-1) at 1.8 BL s(-1). Bluefin tuna had higher metabolic rates than yellowfin tuna at all swimming speeds tested. At a given speed, bluefin had higher metabolic rates and swam with higher tailbeat frequencies and shorter stride lengths than yellowfin. The higher M dot o2 recorded in Pacific bluefin tuna is consistent with the elevated cardiac performance and enhanced capacity for excitation-contraction coupling in cardiac myocytes of these fish. These physiological traits may underlie thermal-niche expansion of bluefin tuna relative to tropical tuna species.

Direct quantification of energy intake in an apex marine predator suggests physiology is a key driver of migrations.

Pacific bluefin tuna (Thunnus orientalis) are highly migratory apex marine predators that inhabit a broad thermal niche. The energy needed for migration must be garnered by foraging, but measuring energy intake in the marine environment is challenging. We quantified the energy intake of Pacific bluefin tuna in the California Current using a laboratory-validated model, the first such measurement in a wild marine predator. Mean daily energy intake was highest off the coast of Baja California, Mexico in summer (mean ± SD, 1034 ± 669 kcal), followed by autumn when Pacific bluefin achieve their northernmost range in waters off northern California (944 ± 579 kcal). Movements were not always consistent with maximizing energy intake: the Pacific bluefin move out of energy rich waters both in late summer and winter, coincident with rising and falling water temperatures, respectively. We hypothesize that temperature-related physiological constraints drive migration and that Pacific bluefin tuna optimize energy intake within a range of optimal aerobic performance.

Exposure to Deepwater Horizon weathered crude oil increases routine metabolic demand in chub mackerel, Scomber japonicus.

During the 2010 Deepwater Horizon incident, the continuous release of crude oil from the damaged Macondo 252 wellhead on the ocean floor contaminated surface water habitats for pelagic fish for more than 12weeks. The spill occurred across pelagic, neritic and benthic waters, impacting a variety of ecosystems. Chemical components of crude oil are known to disrupt cardiac function in juvenile fish, and here we investigate the effects of oil on the routine metabolic rate of chub mackerel, Scomber japonicus. Mackerel were exposed to artificially weathered Macondo 252 crude oil, prepared as a Water Accommodated Fraction (WAF), for 72 or 96h. Routine metabolic rates were determined pre- and post-exposure using an intermittent-flow, swim tunnel respirometer. Routine energetic demand increased in all mackerels in response to crude oil and reached statistical significance relative to unexposed controls at 96h. Chemical analyses of bile from exposed fish revealed elevated levels of fluorescent metabolites, confirming the bioavailability of polycyclic aromatic hydrocarbons (PAHs) in the exposure WAF. The observed increase in metabolic demand is likely attributable to the bioenergetic costs of contaminant detoxification. These results indicate that short-term exposure (i.e. days) to oil has sub-lethal toxicity to mackerel and results in physiological stress during the active spill phase of the incident.

Tissue turnover rates and isotopic trophic discrimination factors in the endothermic teleost, pacific bluefin tuna (Thunnus orientalis).

Stable isotope analysis (SIA) of highly migratory marine pelagic animals can improve understanding of their migratory patterns and trophic ecology. However, accurate interpretation of isotopic analyses relies on knowledge of isotope turnover rates and tissue-diet isotope discrimination factors. Laboratory-derived turnover rates and discrimination factors have been difficult to obtain due to the challenges of maintaining these species in captivity. We conducted a study to determine tissue- (white muscle and liver) and isotope- (nitrogen and carbon) specific turnover rates and trophic discrimination factors (TDFs) using archived tissues from captive Pacific bluefin tuna (PBFT), Thunnus orientalis, 1-2914 days after a diet shift in captivity. Half-life values for (15)N turnover in white muscle and liver were 167 and 86 days, and for (13)C were 255 and 162 days, respectively. TDFs for white muscle and liver were 1.9 and 1.1‰ for δ(15)N and 1.8 and 1.2‰ for δ(13)C, respectively. Our results demonstrate that turnover of (15)N and (13)C in bluefin tuna tissues is well described by a single compartment first-order kinetics model. We report variability in turnover rates between tissue types and their isotope dynamics, and hypothesize that metabolic processes play a large role in turnover of nitrogen and carbon in PBFT white muscle and liver tissues. (15)N in white muscle tissue showed the most predictable change with diet over time, suggesting that white muscle δ(15)N data may provide the most reliable inferences for diet and migration studies using stable isotopes in wild fish. These results allow more accurate interpretation of field data and dramatically improve our ability to use stable isotope data from wild tunas to better understand their migration patterns and trophic ecology.

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.

Temperature effects on metabolic rate of juvenile Pacific bluefin tuna Thunnus orientalis.

Pacific bluefin tuna inhabit a wide range of thermal environments across the Pacific ocean. To examine how metabolism varies across this thermal range, we studied the effect of ambient water temperature on metabolic rate of juvenile Pacific bluefin tuna, Thunnus thynnus, swimming in a swim tunnel. Rate of oxygen consumption (MO2) was measured at ambient temperatures of 8-25 degrees C and swimming speeds of 0.75-1.75 body lengths (BL) s(-1). Pacific bluefin swimming at 1 BL s(-1) per second exhibited a U-shaped curve of metabolic rate vs ambient temperature, with a thermal minimum zone between 15 degrees C to 20 degrees C. Minimum MO2 of 175+/-29 mg kg(-1) h(-1) was recorded at 15 degrees C, while both cold and warm temperatures resulted in increased metabolic rates of 331+/-62 mg kg(-1) h(-1) at 8 degrees C and 256+/-19 mg kg(-1) h(-1) at 25 degrees C. Tailbeat frequencies were negatively correlated with ambient temperature. Additional experiments indicated that the increase in MO2 at low temperature occurred only at low swimming speeds. Ambient water temperature data from electronic tags implanted in wild fish indicate that Pacific bluefin of similar size to the experimental fish used in the swim tunnel spend most of their time in ambient temperatures in the metabolic thermal minimum zone.