Otolith geochemistry reflects life histories of Pacific bluefin tuna.

Understanding biological and environmental factors that influence movement behaviors and population connectivity of highly migratory fishes is essential for cooperative international management and conservation of exploited populations, like bluefin tuna. Pacific bluefin tuna Thunnus orientalis (PBT) spawn in the western Pacific Ocean and then juveniles disperse to foraging grounds across the North Pacific. Several techniques have been used to characterize the distribution and movement of PBT, but few methods can provide complete records across ontogeny from larvae to adult in individual fish. Here, otolith biominerals of large PBT collected from the western, eastern, and south Pacific Ocean, were analyzed for a suite of trace elements across calcified/proteinaceous growth zones to investigate patterns across ontogeny. Three element:Ca ratios, Li:Ca, Mg:Ca, and Mn:Ca displayed enrichment in the otolith core, then decreased to low stable levels after age 1-2 years. Thermal and metabolic physiologies, common diets, or ambient water chemistry likely influenced otolith crystallization, protein content, and elemental incorporation in early life. Although similar patterns were also exhibited for otolith Sr:Ca, Ba:Ca and Zn:Ca in the first year, variability in these elements differed significantly after age-2 and in the otolith edges by capture region, suggesting ocean-specific environmental factors or growth-related physiologies affected otolith mineralization across ontogeny.

Recent and historical data show no evidence of Pacific bluefin tuna reproduction in the southern California Current system.

Despite their broad distribution across the North Pacific Ocean, the only known spawning grounds for Pacific Bluefin Tuna (Thunnus orientalis) are around coastal Japan and the East China Sea. However, an increase in the prevalence of large bluefin tuna up to 10 years old in the California Current System during exceptionally warm ocean conditions has led to speculation that they may be spawning in this region. To investigate this possibility, we collected samples from 36 females (estimated 3-8 years old) between 2015 and 2019. Histological analyses revealed no signs of imminent, active, or recent spawning. Further examination of historical ichthyoplankton collections showed no records of larval bluefin tuna, but confirmed the presence of the larvae of other tuna species in waters > 24°C. Fishery-dependent records showed that bluefin tuna are rarely recorded in purse seine catches where surface temperatures exceed 23°C. Our study, therefore, provided no evidence of bluefin tuna reproduction in the CCS. However, more comprehensive sampling, in particular off southern Baja California, may be required to confirm the absence of spawning.

Natal origin and age-specific egress of Pacific bluefin tuna from coastal nurseries revealed with geochemical markers.

Geochemical chronologies were constructed from otoliths of adult Pacific bluefin tuna (PBT) to investigate the timing of age-specific egress of juveniles from coastal nurseries in the East China Sea or Sea of Japan to offshore waters of the Pacific Ocean. Element:Ca chronologies were developed for otolith Li, Mg, Mn, Zn, Sr, and Ba, and our assessment focused on the section of the otolith corresponding to the age-0 to age-1 + interval. Next, we applied a common time-series approach to geochemical profiles to identify divergences presumably linked to inshore-offshore migrations. Conspicuous geochemical shifts were detected during the juvenile interval for Mg:Ca, Mn:Ca, and Sr:Ca that were indicative of coastal-offshore transitions or egress generally occurring for individuals approximately 4-6 mo. old, with later departures (6 mo. or older) linked to overwintering being more limited. Changepoints in otolith Ba:Ca profiles were most common in the early age-1 period (ca. 12-16 mo.) and appear associated with entry into upwelling areas such as the California Current Large Marine Ecosystem following trans-Pacific migrations. Natal origin of PBT was also predicted using the early life portion of geochemical profile in relation to a baseline sample comprised of age-0 PBT from the two primary spawning areas in the East China Sea and Sea of Japan. Mixed-stock analysis indicated that the majority (66%) of adult PBT in our sample originated from the East China Sea, but individuals of Sea of Japan origin were also detected in the Ryukyu Archipelago.

Nursery origin and population connectivity of swordfish Xiphias gladius in the North Pacific Ocean.

Element:Ca ratios in the otolith cores of young-of-the-year (YOY) swordfish, Xiphias gladius, were used as natural tracers to predict the nursery origin of subadult and adult swordfish from three foraging grounds in the North Pacific Ocean (NPO). First, the chemistry of otolith cores (proxy for nursery origin) was used to develop nursery-specific elemental signatures in YOY swordfish. Sagittal otoliths of YOY swordfish were collected from four regional nurseries in the NPO between 2000 and 2005: (1) Central Equatorial North Pacific Ocean (CENPO), (2) Central North Pacific Ocean (CNPO), (3) Eastern Equatorial North Pacific Ocean (EENPO) and (4) Western North Pacific Ocean (WNPO). Calcium (43 Ca), magnesium (24 Mg), strontium (88 Sr) and barium (138 Ba) were quantified in the otolith cores of YOY swordfish using laser ablation inductively coupled plasma mass spectrometry. Univariate tests indicated that three element:Ca ratios (Mg:Ca, Sr:Ca and Ba:Ca) were significantly different among nurseries. Overall classification success of YOY swordfish to their nursery of collection was 72% based on quadratic discriminant analysis. Next, element:Ca ratios in the otolith cores of subadults and adults collected from three foraging grounds where targeted fisheries exist (Hawaii, California and Mexico) were examined to calculate nursery-specific contribution estimates. Mixed-stock analysis indicated that the CENPO nursery contributed the majority of individuals to all three foraging grounds (Hawaii 45.6 ± 13.2%, California 84.6 ± 10.8% and Mexico 64.5 ± 15.9%). The results from this study highlight the importance of the CENPO nursery and provide researchers and fisheries managers with new information on the connectivity of the swordfish population in the NPO.

Stable isotope turnover rates and fractionation in captive California yellowtail (Seriola dorsalis): insights for application to field studies.

Stable isotope analysis (SIA) measurements from long-term captivity studies provide required parameters for interpretation of consumer SIA data. We raised young-of-the-year (14-19 cm) California yellowtail (Seriola dorsalis) on a low δ15N and δ13C diet (pellet aquaculture feed) for 525 days, then switched to a high δ15N and δ13C diet (mackerel and squid) for 753 days. Yellowtail muscle was sequentially sampled from each individual after the diet switch (0 to 753 days) and analyzed for δ15N and δ13C, allowing for calculation of diet-tissue discrimination factors (DTDFs) from two isotopically different diets (low δ15N and δ13C: pellets; high δ15N and δ13C: fish/squid) and turnover rates of 15N and 13C. DTDFs were diet dependent: Δ15N = 5.1‰, Δ13C = 3.6‰ for pellets and Δ15N = 2.6‰, Δ13C = 1.3‰ for fish/squid. Half-life estimates from 15N and 13C turnover rates for pooled yellowtail were 181 days and 341 days, respectively, but varied considerably by individual (15N: 99-239 d; 13C: 158-899 d). Quantifying DTDFs supports isotopic approaches to field data that assume isotopic steady-state conditions (e.g., mixing models for diet reconstruction). Characterizing and quantifying turnover rates allow for estimates of diet/habitat shifts and "isotopic clock" approaches, and observed inter-individual variability suggests the need for large datasets in field studies. We provide diet-dependent DTDFs and growth effects on turnover rates, and associated error around these parameters, for application to field-collected SIA data from other large teleosts.

Natal origin of Pacific bluefin tuna from the California Current Large Marine Ecosystem.

Natal origin of subadult (age-1) Pacific bluefin tuna (PBT, Thunnus orientalis) from the California Current Large Marine Ecosystem (CCLME) was determined using natural tracers in ear stones (otoliths). Age-0 PBT collected from the two known spawning areas in the western Pacific Ocean (East China Sea, Sea of Japan) were used to establish baseline signatures from otolith cores over 4 years (2014-2017) based on a suite of trace elements (Li, Mg, Mn, Sr, Zn and Ba). Distinct chemical signatures existed in the otolith cores of age-0 PBT collected from the two spawning areas, with overall classification accuracy ranging 73-93% by year. Subadult PBT collected in the CCLME over the following 4 years (2015-2018) were then age-class matched to baselines using mixed-stock analysis. Natal origin of trans-Pacific migrants in the CCLME ranged 43-78% from the East China Sea and 22-57% from the Sea of Japan, highlighting the importance of both spawning areas for PBT in the CCLME. This study provides the first estimates on the natal origin of subadult PBT in this ecosystem using otolith chemistry and expands upon the application of these natural tracers for population connectivity studies for this species.

Mercury Stable Isotopes Reveal Influence of Foraging Depth on Mercury Concentrations and Growth in Pacific Bluefin Tuna.

Pelagic ecosystems are changing due to environmental and anthropogenic forces, with uncertain consequences for the ocean's top predators. Epipelagic and mesopelagic prey resources differ in quality and quantity, but their relative contribution to predator diets has been difficult to track. We measured mercury (Hg) stable isotopes in young (<2 years old) Pacific bluefin tuna (PBFT) and their prey species to explore the influence of foraging depth on growth and methylmercury (MeHg) exposure. PBFT total Hg (THg) in muscle ranged from 0.61 to 1.93 µg g-1 dw (1.31 µg g-1 dw ±0.37 SD; 99% ± 6% MeHg) and prey ranged from 0.01 to 1.76 µg g-1 dw (0.13 µg g-1 dw ±0.19 SD; 85% ± 18% MeHg). A systematic decrease in prey δ202Hg and Δ199Hg with increasing depth of occurrence and discrete isotopic signatures of epipelagic prey (δ202Hg: 0.74 to 1.49‰; Δ199Hg: 1.76-2.96‰) and mesopelagic prey (δ202Hg: 0.09 to 0.90‰; Δ199Hg: 0.62-1.95‰) allowed the use of Hg isotopes to track PBFT foraging depth. An isotopic mixing model was used to estimate the dietary proportion of mesopelagic prey in PBFT, which ranged from 17% to 55%. Increased mesopelagic foraging was significantly correlated with slower growth and higher MeHg concentrations in PBFT. The slower observed growth rates suggest that prey availability and quality could reduce the production of PBFT biomass.

Assessing Fukushima-Derived Radiocesium in Migratory Pacific Predators.

The 2011 release of Fukushima-derived radionuclides into the Pacific Ocean made migratory sharks, teleosts, and marine mammals a source of speculation and anxiety regarding radiocesium (134+137Cs) contamination, despite a lack of actual radiocesium measurements for these taxa. We measured radiocesium in a diverse suite of large predators from the North Pacific Ocean and report no detectable (i.e., ≥ 0.1 Bq kg-1 dry wt) Fukushima-derived 134Cs in all samples, except in one olive ridley sea turtle (Lepidochelys olivacea) with trace levels (0.1 Bq kg-1). Levels of 137Cs varied within and across taxa, but were generally consistent with pre-Fukushima levels and were lower than naturally occurring 40K by one to one to two orders of magnitude. Predator size had a weaker effect on 137Cs and 40K levels than tissue lipid content. Predator stable isotope values (δ13C and δ15N) were used to infer recent migration patterns, and showed that predators in the central, eastern, and western Pacific should not be assumed to accumulate detectable levels of radiocesium a priori. Nondetection of 134Cs and low levels of 137Cs in diverse marine megafauna far from Fukushima confirms negligible increases in radiocesium, with levels comparable to those prior to the release from Fukushima. Reported levels can inform recently developed models of cesium transport and bioaccumulation in marine species.

Animal physiology. Whole-body endothermy in a mesopelagic fish, the opah, Lampris guttatus.

Endothermy (the metabolic production and retention of heat to warm body temperature above ambient) enhances physiological function, and whole-body endothermy generally sets mammals and birds apart from other animals. Here, we describe a whole-body form of endothermy in a fish, the opah (Lampris guttatus), that produces heat through the constant "flapping" of wing-like pectoral fins and minimizes heat loss through a series of counter-current heat exchangers within its gills. Unlike other fish, opah distribute warmed blood throughout the body, including to the heart, enhancing physiological performance and buffering internal organ function while foraging in the cold, nutrient-rich waters below the ocean thermocline.

Reconstructing transoceanic migration patterns of Pacific bluefin tuna using a chemical tracer toolbox.

Large pelagic predators play important roles in oceanic ecosystems, and may migrate vast distances to utilize resources in different marine ecoregions. Understanding movement patterns of migratory marine animals is critical for effective management, but often challenging, due to the cryptic habitat of pelagic migrators and the difficulty of assessing past movements. Chemical tracers can partially circumvent these challenges by reconstructing recent migration patterns. Pacific bluefin tuna (Thunnus orientalis; PBFT) inhabit the western and eastern Pacific Ocean, and are in steep decline due to overfishing. Understanding age-specific eastward transpacific migration patterns can improve management practices, but these migratory dynamics remain largely unquantified. Here, we combine a Fukushima-derived radiotracer (134Cs) with bulk tissue and amino acid stable isotope analyses of PBFT to distinguish recent migrants from residents of the eastern Pacific Ocean. The proportion of recent migrants to residents decreased in older year classes, though the proportion of older PBFT that recently migrated across the Pacific was greater than previous estimates. This novel toolbox of biogeochemical tracers can be applied to any species that crosses the North Pacific Ocean.

Radiocesium in Pacific bluefin tuna Thunnus orientalis in 2012 validates new tracer technique.

The detection of Fukushima-derived radionuclides in Pacific bluefin tuna (PBFT) that crossed the Pacific Ocean to the California Current Large Marine Ecosystem (CCLME) in 2011 presented the potential to use radiocesium as a tracer in highly migratory species. This tracer requires that all western Pacific Ocean emigrants acquire the (134)Cs signal, a radioisotope undetectable in Pacific biota prior to the Fukushima accident in 2011. We tested the efficacy of the radiocesium tracer by measuring (134)Cs and (137)Cs in PBFT (n = 50) caught in the CCLME in 2012, more than a year after the Fukushima accident. All small PBFT (n = 28; recent migrants from Japan) had (134)Cs (0.7 ± 0.2 Bq kg(-1)) and elevated (137)Cs (2.0 ± 0.5 Bq kg(-1)) in their white muscle tissue. Most larger, older fish (n = 22) had no (134)Cs and only background levels of (137)Cs, showing that one year in the CCLME is sufficient for (134)Cs and (137)Cs values in PBFT to reach pre-Fukushima levels. Radiocesium concentrations in 2012 PBFT were less than half those from 2011 and well below safety guidelines for public health. Detection of (134)Cs in all recent migrant PBFT supports the use of radiocesium as a tracer in migratory animals in 2012.

Stable isotope analysis challenges wasp-waist food web assumptions in an upwelling pelagic ecosystem.

Eastern boundary currents are often described as 'wasp-waist' ecosystems in which one or few mid-level forage species support a high diversity of larger predators that are highly susceptible to fluctuations in prey biomass. The assumption of wasp-waist control has not been empirically tested in all such ecosystems. This study used stable isotope analysis to test the hypothesis of wasp-waist control in the southern California Current large marine ecosystem (CCLME). We analyzed prey and predator tissue for δ¹³C and δ¹5N and used Bayesian mixing models to provide estimates of CCLME trophic dynamics from 2007-2010. Our results show high omnivory, planktivory by some predators, and a higher degree of trophic connectivity than that suggested by the wasp-waist model. Based on this study period, wasp-waist models oversimplify trophic dynamics within the CCLME and potentially other upwelling, pelagic ecosystems. Higher trophic connectivity in the CCLME likely increases ecosystem stability and resilience to perturbations.