First tagging data on large Atlantic bluefin tuna returning to Nordic waters suggest repeated behaviour and skipped spawning
Satellite tracking has yielded key information about the movements and behaviour of marine vertebrates in ways that were previously logistically impossible34. In the current study, we tagged the first 18 angler-caught ABFT in Skagerrak, and tracked their movements for up to one year. Despite the majority of tags detaching prematurely, our data provides new insights regarding the migration behaviour and habitat use of this species, both locally within the Nordic region and more widely throughout the northeast Atlantic and western Mediterranean Sea. Most fish (N = 9) left Skagerrak via the Norwegian Trench, heading north before exiting into the Atlantic. In addition, the two tags which remained deployed for approximately one full year showed a return migration into the Skagerrak from the northern North Sea and southern Norwegian Sea regions, re-entering north of the British Isles and through the Norwegian Trench. No fish exited or re-entered through the English Channel or the southern North Sea. These observations of entry/exit from the Skagerrak are similar to migration behaviour inferred from historical commercial fishery data in the region during the 1950s–1960s16,19. These historical records also demonstrated that some individuals migrated from the southern Norwegian Sea into the Skagerrak, Kattegat and Øresund, before leaving the area several weeks later, potentially indicating exploratory feeding on herring and mackerel, abundant in the area during this time of year. Our new tagging results confirm this behaviour among at least some of the ABFT migrating to these areas.The migration patterns revealed by our tagging study exposes tuna entering and exiting the Skagerrak, Kattegat and Øresund to targeted exploitation by regional commercial fishing vessels. Presently, these vessels catch ABFT under a Norwegian quota (315 tonnes in 2021) but additional countries in the region may acquire a quota in the future. Moreover, the relatively narrow size distribution of tunas caught indicates that this migratory behaviour may only be performed by a limited number of year classes35, meaning that the continued long-term migration of ABFT to these waters is highly dependent on recruitment and survival of younger year classes. These younger year classes, perhaps once they reach a certain size, could then also undertake a migration to Skagerrak–Kattegat–Øresund. However, the combination of local exploitation pressures, and the presently limited number of year classes found in Skagerrak could result in ABFT migrating into Skagerrak–Kattegat–Øresund being a short-lived phenomenon if those year classes are subject to a large yearly fishing mortality (both regionally within the Nordic region, and more generally throughout the population range) and no younger year classes appear. Additionally, currently there is no scientifically-derived estimates of ABFT abundance for this region. We suggest to monitor the size distribution and abundance of ABFT in Scandinavian waters in the coming years to (1) confirm that visiting ABFT consist of only a few year classes, and clarify if younger year classes begin to appear, (2) evaluate how the numbers migrating to the region annually may change over time (e.g., under different levels of exploitation, or in relation to environmental factors).While most of our tagged ABFT went north after exiting the Skagerrak, one individual turned south into the south-central North Sea before eventually leaving through the northern part of the North Sea. The region to which it migrated in the North Sea is congruent with earlier commercial catches and sightings in this region, including the Dogger Bank vicinity15,16. Although the exact routes that tagged individuals followed were not identical, no individuals used the shortest route to reach the Atlantic: from the Skagerrak through the North Sea to the English Channel, and further south to the Bay of Biscay and other southern regions. Migration along a northerly route probably reflects a trade-off between the potential for higher energetic gain from more abundant food and higher energy resources, and the longer migration distance. This could suggest that ABFT either follow the food, or simply follow the same route by which they came through learned behaviour.Three tags remained attached long enough to explore long-term migration patterns and showed widely different behaviours. One fish crossed the Atlantic and utilized areas near the Grand Banks, crossing the ICCAT management boundary between the Western and Eastern stocks of ABFT (the 45° meridian), while the other two fish remained in the eastern Atlantic. The area west of Ireland, the Bay of Biscay and the area west of Portugal appear to be important feeding areas when the fish are not in Skagerrak or the Norwegian Sea. These results reflect interconnected seascapes for foraging through the NE Atlantic. Connecting foraging grounds off Ireland and the Bay of Biscay, which was previously suggested by Ref.24 is further corroborated by one of the fish tagged in this study, which passed over the Irish continental shelf when returning to Skagerrak in 2018.Depth and temperature useWithin ICES Area 3a, ABFT were predominantly roaming the upper water column, with most observations in the upper 100 m. However, some ABFT did dive to much deeper depths, with the maximum depth recorded being 520 m, showing that they can use the majority of the depth range available in the area (max. depth in the Norwegian Trench is app. 725 m, but represents a relatively small area). The behaviour likely reflects foraging, as ABFT were also observed by both the scientific tagging crews and the anglers to actively chase prey fish, like garfish and mackerel, at the surface during the tagging operations. The temperature ranges recorded varied between 7 and 17 °C. Both the depths and temperatures recorded are well within the thermal and depth limits reported in the literature for ABFT36.SpawningABFT have been shown to successfully spawn at temperatures above 20 °C at night30,31, and to display a distinct dive pattern thought to represent courtship and spawning behaviour29. When matching this described behaviour with the data from fish 34859 in the Mediterranean Sea, almost identical behavioural patterns were detected on specific days (Fig. 4). In total, seven days aligned with temperatures above 20 °C and oscillatory movement past the thermocline. All detected spawning events occurred west of Sardinia, where fishing for mature ABFT has been conducted for centuries37.In light of the recently proposed third spawning area in the Slope Sea of northeast United States38 and other proposed areas outside the Mediterranean19, it is relevant to look for similar temperature and behavioural patterns for fish 34840, which did not enter the Mediterranean Sea, and instead stayed in the eastern Atlantic. We found that this fish did not display a similar oscillatory behaviour, and the temperature experienced during the alleged spawning period (June–July) was above 20 °C only once (20.4 °C on 11 July). In this period, the fish was on the continental shelf west of Ireland, likely feeding and not spawning. Due to the size of the fish (247 cm CFL), reflecting a likely age of 14–16 years (matching the strong 2003 cohort), and the assumption that all eastern ABFT above five years and western ABFT above eight years are mature, we find it unlikely that this fish was immature. As such, these observations may suggest that this fish skipped spawning in 2018. Fish 34861 surfaced on 25 April and the tag was not recovered. The transmitted data does not allow for a detailed analysis of potential spawning behaviour for this fish. It did however, display 6 days where maximum temperatures from the transmitted dataset reached 20 °C (observations from 15. March to 20 April, with temperatures ranging from 20 to 20.6 °C). Given the lack of detailed behaviour and the fact that this time is well outside the normal spawning time for Mediterranean ABFT, we propose that this ABFT did not spawn in that period. However, the documentation of spawning depends on the general applicability of the temperature limits and nightly spawning behaviour30,31. More studies documenting spawning behaviour will be needed to corroborate if this pattern is consistent among locations and stocks. We also suggest more studies with longer lasting tags to elucidate if skipped spawning is a common behaviour and if fish skip one or more consecutive spawning seasons. Skipped spawning has been demonstrated in many fish species, including both freshwater and marine fish39, and likely reflects physiological condition40. If a considerable proportion of the adult population skips spawning every season, current population models, which assume annual spawning by all adult fish, should be modified to more accurately reflect population egg production and reproductive output. Current population modelling may be even further challenged if the proportion of adults that skip spawning varies over time, perhaps depending on environmental conditions. However, we acknowledge that only one of two fish followed through the spawning season appeared to skip spawning, and therefore caution against broad general interpretations. More studies are needed to verify that skipped spawning is a common behaviour, and if so, to estimate just how common that behaviour is.
Return migrationIn exploited fish populations, large adults are hypothesized to be important components of the spawning population because they contribute more to recruitment than smaller individuals due to a variety of maternal effects including higher fecundity, better quality of eggs and differences in spawning behaviour (e.g. time, location)41. Although such effects remain to be documented for ABFT, it may be prudent to conserve these large individuals as a precautionary measure, to maximize their potential contributions to reproduction and recruitment.In order to protect these fish, new knowledge about their movements and distribution is required. Data from ABFT deployed with long-term electronic tags suggests that after spawning in the Gulf of Mexico, the fish return to the feeding grounds where they were initially tagged, indicating a return feeding migration7. The same has been observed more recently from ABFT tagged in Ireland24, and other large highly migratory fish species (e.g., swordfish, Xiphias gladius42). In the current study, both ABFT that retained the tag for one year also returned to the same area, suggesting a similar seasonal return feeding migration. We also note that ABFT appeared to perform recurrent visits to the Norwegian Sea, Ireland and the Bay of Biscay on their way from Nordic waters and upon their return to the latter. Hence, we hypothesize that large ABFT in Nordic waters generally return to the same feeding area the following year, given suitable habitat features (e.g., food and temperature conditions), and follow a similar migration route as they do so. More studies are nonetheless needed to confirm this hypothesis, given few long-term deployments in the current study. For a deeper understanding of behavioural repeatability, and if/when shifts in the behaviour occur, it will be necessary to follow the same fish over multiple years. Such studies would also act as a highly valuable indicator of survival, independent of stock assessment-derived mortality estimates, and could be used to estimate the local abundance of larger ABFT43. Thus, a promising avenue for future research would be to deploy long-lasting ( > 5 to 10 years) acoustic tags and use existing infrastructure from networks such as the European Tracking Network to track these large fish over the next decade44. Given that ABFT appear to return to the area annually, we suggest that Skagerrak is a promising area for the future deployment and retrieval of PSATs and other long-lasting tags, because of the relatively easy access to locate and recover detached floating tags, given that the area is reachable from land within a few hours by boat. Retrieving PSATs that have detached from animals enables scientists to access full datasets (in the present case with 5 s resolution, rather than the much coarser and variable resolution typically transmitted). This much higher resolution enables much more detailed analysis, as shown in our analysis of spawning behaviour. Additionally, floating Pop-off Data Storage Tags (PDST) tags may also be a prominent and less costly avenue forward as the geographical region is densely populated and contains many sandy beaches and highly visited coastal areas, giving ample opportunity for tag recovery. Previous studies with floating DSTs in this area have shown remarkably high return rates45.The evidence that ABFT have returned to Nordic waters following many years of rarity or absence, and our findings that at least some individuals return to the same site for feeding in consecutive years, raises new questions about the mechanisms that underlie habitat discovery—or the return to previously used habitats—by highly migratory fish species. How individuals or entire schools have discovered this region again as a suitable feeding area after an absence of more than 50 years is unclear. In light of the positive stock development in the last 1–2 decades22 and modelling studies showing suitable habitat in the area46, density-dependent foraging and exploratory behaviour for new feeding areas may be a prominent hypothesis for their return, potentially accompanied by complex social learning interactions among individuals within the population47,48. New tagging data which documents the use of new or formerly occupied habitats will be essential for understanding these processes and how they might be affected by human pressures (e.g., exploitation, climate change). Such data can help to parameterize and validate advanced conceptual models of group movement behaviour, collective memory and habitat use49,50,51, as well as to inform modern stock assessment models used for management.
Tag deploymentFollowing recommendations from experienced taggers previously operating in the Mediterranean, most fish were tagged in the water alongside the boat. All these tags surfaced prematurely, while two (out of three) tags deployed on tunas brought on board the tagging boat surfaced after approximately one year. Depending on the conditions at sea, tagging along the side of the boat may not be as precise as on-board tagging, and the quality of the tag anchoring cannot be properly assessed. We therefore suggest that tagging on-board a boat is superior to tagging in the water alongside the boat for the deployment of long-lasting tags. This was also suggested in Ref.24. Furthermore, on-board tagging makes biological sampling fast and feasible, as opposed to tagging in the water alongside the boat. However, our advice is limited by a small sample size, making it difficult to draw formal conclusions; more studies are necessary to assess the best method to tag large ABFT. More
