Results and Discussion

All 15 PBFT collected in 2011 contained ¹³⁴Cs (4.0 ± 1.4 Bq kg⁻¹ dry wt) and ¹³⁷Cs (6.3 ±1.5 Bq kg⁻¹) in white muscle tissue (Table 1, Table S1, and Fig. 1A). At the time of capture, total ^134+137Cs concentrations were about 10 times higher in 2011 PBFT than in PBFT from previous years (Table 1). In contrast, 2008 PBFT and 2011 YFT had no measurable ¹³⁴Cs and consistent, much lower ¹³⁷Cs concentrations (consistent with background concentrations from fallout) than the 2011 PBFT (Table 1, Table S2, and Fig. 1A). This is unequivocal evidence that Fukushima-derived radionuclides were transported to the CCLME by Pacific bluefin tuna, as no other sources of ¹³⁴Cs were present in the North Pacific preceding the Fukushima disaster (3, 4). Mean concentrations of the naturally occurring γ-emitting ⁴⁰K in the 2011 PBFT were 347 ± 49 Bq kg⁻¹ (Table 1). Other naturally occurring γ-emitting radionuclides (⁷Be, ²¹¹Bi, and ²¹²Pb) were detectable at extremely low concentrations (Table S3), approximately three orders of magnitude below measured radiocesium concentrations.

Because bluefin tuna are harvested annually in the Eastern Pacific Ocean (EPO) at 1.7–9.9 × 10³ metric tonnes (10) (Table S4) for human consumption (2000 to 2010), the possibility of radioactive contamination raises public health concerns. Radiocesium concentrations of post-Fukushima PBFT reported here were more than an order of magnitude below the recently changed Japanese safety limit of 100 Bq kg⁻¹ wet wt (about 400 Bq kg⁻¹ dry wt) (11). Inferences about the safety of consuming radioactivity-contaminated seafood can be complicated due to complexities in translating food concentration to actual dose to humans (12), but it is important to put the anthropogenic radioactivity levels in the context of naturally occurring radioactivity. Total radiocesium concentrations of post-Fukushima PBFT were approximately thirty times less than concentrations of naturally occurring ⁴⁰K in post-Fukushima PBFT and YFT and pre-Fukushima PBFT (Table 1). Furthermore, before the Fukushima release the dose to human consumers of fish from ¹³⁷Cs was estimated to be 0.5% of that from the α-emitting ²¹⁰Po (derived from the decay of ²³⁸U, naturally occurring, ubiquitous and relatively nonvarying in the oceans and its biota (13); not measured here) in those same fish (12). Thus, even though 2011 PBFT showed a 10-fold increase in radiocesium concentrations, ¹³⁴Cs and ¹³⁷Cs would still likely provide low doses of radioactivity relative to naturally occurring radionuclides, particularly ²¹⁰Po and ⁴⁰K.

However, 2011 PBFT ¹³⁴Cs and ¹³⁷Cs concentrations were less than they would have been in Japanese waters because of growth, radioactive decay, and efflux of cesium. To estimate the concentrations of ¹³⁴Cs and ¹³⁷Cs in 2011 PBFT at the time they left Japanese waters, we back-calculated radiocesium concentrations in muscle over a range of potential trans-Pacific migration times (30–120 d) using a loss rate of assimilated Cs from fish tissue of 1.9% day⁻¹ (14), growth dilution attributable to an increase in body mass during the trans-Pacific migration, and radioactive decay (details in SI Methods). We estimated that PBFT in Japan had 1.5–15 times higher radiocesium concentrations (30–120 d before capture, respectively) than concentrations measured at time of capture in California (Fig. 2 and Table S1). Variations in animal size at exposure and growth because exposure may influence Cs concentrations; there was a negative trend between animal size and ¹³⁷Cs and ¹³⁴Cs concentrations, although the correlation was not significant (Spearman’s ρ; Fig. S2 and SI Methods). The Japanese Ministry of Agriculture, Forestry, and Fisheries report post-Fukushima concentrations of ^134+137Cs in PBFT around Japan at 61–168 Bq kg⁻¹ dry weight (11). Our estimates of total radiocesium (i.e., ¹³⁴Cs + ¹³⁷Cs) concentrations in PBFT for 90 and 120 d before capture are 73–147 Bq kg⁻¹, respectively (Table S1). The similarity between back-calculated values and those measured in Japan PBFT suggests that our model performs well in predicting previous concentrations of Cs in tuna captured months after exposure.

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Fig. 2.

Measured (corrected for background levels of ¹³⁷Cs) and back-calculated estimates of radiocesium concentrations in muscle of post-Fukushima Pacific bluefin tuna Thunnus orientalis (n = 15). Estimated values of ¹³⁴Cs and ¹³⁷Cs concentrations in 2011 PBFT for various times before capture in California (30, 60, 90, 120 d) account for background levels of ¹³⁷Cs, decreases in tissue concentrations because of growth dilution and efflux rates of radiocesium out of the fish during their migration across the Pacific (detailed in SI Methods). Mean concentrations of ¹³⁴Cs (red triangles) or ¹³⁷Cs (gray squares) shown on the left y axis. Error bars represent 1 SD. Ratios of ¹³⁴Cs:¹³⁷Cs for each individual fish (empty circles) shown with scale on the right y axis. Dotted line represents 1:1 ratio of ¹³⁴Cs:¹³⁷Cs, the ratio expected in tuna while in waters off Japan contaminated with radiocesium at a ¹³⁴Cs:¹³⁷Cs ratio of 1.0.

Decay-corrected ¹³⁴Cs:¹³⁷Cs ratios measured in post-Fukushima bluefin caught off California averaged 0.62 ± 0.14 and ranged from 0.26 to 0.84 (Table 1 and Table S1). Ratios of ¹³⁴Cs:¹³⁷Cs have been used to discern sedimentation patterns and water movements in the Irish Sea, which received 15 PBq of discharged ¹³⁷Cs between 1978 and 1983 from the nuclear fuel-reprocessing plant at Sellafield (15, 16). However, Cs ratios have not been used previously to track biota movements. Assuming that PBFT tissue would reflect the ¹³⁴Cs:¹³⁷Cs ratio of 1.0 to which they were exposed near Japan, radiocesium ratios can be used to make inferences about migration and the timing of exposure to contaminated waters. Back-calculated ¹³⁴Cs:¹³⁷Cs ratios in PBFT approached 1.0 (0.8 ± 0.2) at 4 mo before capture (Fig. 2), suggesting departure from Japan ∼4 mo before capture off California. This result suggests that the radiocesium levels in California-caught PBFT were the result of <1 mo exposure to contaminated waters near Japan. Because radiocesium release was pulsed, it is possible that back-calculated ratios will always converge on the period of maximum discharge (rather than on the date of PBFT emigration from Japanese waters). The ¹³⁴Cs:¹³⁷Cs ratio of seawater near Japan would have changed little from 1.0 within 4 mo of the pulsed radioactivity discharge (1.0–0.9; Fig. S1). However, additional PBFT radiocesium data across longer time scales (e.g., PBFT from 2012) will indicate whether back-calculated ¹³⁴Cs:¹³⁷Cs ratios in PBFT consistently converge on 1.0 in April 2011 (period of maximum discharge) or converge on 1.0 over a range of dates after the Fukushima discharge (demonstrating the utility of ¹³⁴Cs:¹³⁷Cs ratios as a tool to assess the timing of PBFT migrations).

The total load of radiocesium transported to the CCLME by PBFT can be estimated from catches in the EPO. Catch data varies yearly (10), but assuming PBFT commercial catches in 2011 were within the range of catch from 2000 to 2010, transported and harvested radiocesium in tuna muscle tissue in 2011 could range from ∼3–17 × 10⁶ Bq (Table S4) or <<1% of total radiocesium released into Japanese waters (4). Catch data represent a portion of the PBFT in the EPO, so total transport of radiocesium by PBFT would likely be higher. Still, this is a small quantity of radiocesium to be introduced to a large pelagic ecosystem, but it is also a conservative estimate based on one species. Other highly migratory species (HMS) (e.g., turtles, sharks, and seabirds) that forage near Japan may assimilate radiocesium and transport it to distant regions of the north and south Pacific (Fig. 1B). Tissue concentrations of radiocesium in these species would depend on time spent near Japan, foraging strategies, and timing of migration. The potential for species in Fig. 1B and other HMS (e.g., pinnipeds, whales, and billfish) that forage in Japan to transport Fukushima-derived radiocesium is speculative. However, the presence of Fukushima-derived radiocesium in all 2011 PBFT individuals reported here suggests that study of other HMS is warranted. Our results demonstrate that Fukushima-derived radionuclides in animal tissues can serve as tracers of both migration origin (presence or absence of ¹³⁴Cs) and, potentially, timing (using ¹³⁴Cs:¹³⁷Cs ratios) in mobile marine animals, providing valuable complementary movement data to extensive tagging programs in the Pacific (8). Extensive data regarding spatiotemporal variations in Cs concentrations in the west Pacific, and consequent uptake by biota, are forthcoming, which will sharpen the precision of these tracers. The Fukushima disaster, thus, provides an opportunity to examine both the extent of transport of anthropogenic radionuclides by highly migratory species and an unexpected tool for examining migratory origins of apex predators in the Pacific Ocean.