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To our knowledge, this study provides the first recorded information on the active swimming of Japanese eels and on their transport by currents in the open ocean. Specifically, the strong flow of the KC largely dominated the movements of the eels and transported them northeastward while they swam mainly southward, and active swimming contributed a little to their travel trajectories. In contrast, the swimming of eels made a relatively higher contribution to their travel trajectories in the TS area.Our in situ estimates of the mean swimming speeds of Japanese eels (26–41 cm/s) were similar or slightly lower than those of European eels. In the acoustic tracking experiment of European eels considering environmental current vectors, their swimming speeds were 35–58 cm/s in the coastal midwater26. In a laboratory experiment using stamina tunnels with stable temperatures, the optimal swimming speeds of European eels were estimated to be 61–68 cm/s (0.74–1.02 BL/s)56, which were higher than the in situ estimates. The minimum swimming speed of European eels is considered to be 40 cm/s if they will arrive at their spawning area in the Sargasso Sea (distance of 5500 km) in 6 months, and their optimal swimming speeds were sufficient to migrate over the long distance in time for the near-spawning period after escape from their growth habitats56. However, field studies using PSAT tagging also reported that in situ migration speeds (including transport by currents) were less than the optimal swimming speeds and suggested that some European eels could reach their spawning area within the near-spawning periods and that others only arrive in time for the following spawning season19.Our estimated effective swimming speed of Japanese eels, all day and all night over the tracking periods, ranged from 3 to 30 cm/s with individual variations. These estimates were consistent with the swimming speeds (excluding transport by currents) of 2.2–15.1 km/day (2–18 cm/s) estimated in the PSAT study of Japanese eels14. Silver-phase Japanese eels start migrating from their coastal growth habitats in Japan primarily in October to December57, 58, and spawning near the West Mariana Ridge occurs in April to August33, 35. Numerical models assuming that migrating eels use true navigation (readjusted compass) or a constant compass heading (fixed compass from the departure place to the spawning site) indicate that the minimal swimming speed required to arrive at the spawning area within 8 months is 10–12 cm/s37. Our estimated effective swimming speeds of five out of ten eels during the day and eight out of ten eels during the night were similar or higher than these minimal speeds. The low effective swimming speeds frequently observed during the day might be due to the relatively low values observed in the swimming speed at 10 min intervals and the swimming directions often varying during the day. When eels swim with stable orientation, as observed in three of the eels (WE2999_TS, WE3001_TS, and WE3002_TS) during the night, the effective swimming speeds exceeded 25 cm/s. If such a stable orientation is maintained and compensate the low speeds during the day, the eels that leave during autumn and winter will be able to arrive at the spawning area during the next spring to summer.It should also be noted that the swimming speeds in body length per second were significantly higher in shallow water during the night than in deep water during the day. In the open ocean, anguillid species exhibit DVMs during oceanic migration, swimming at depth during the day and in the shallows during the night9,10,11,12,13,14,15,16,17,18,19,20,21,22. These DVMs are likely related to the possible avoidance from visual predators under light conditions19 or maturation control59. Essentially, through the DVMs, the eels encounter low temperatures ( 20 °C) during the same day. Generally, the swimming speeds of fishes are restricted by the ambient water temperature60, and the water temperature encountered through DVMs might influence the horizontal-swimming speeds of Japanese eels.Other factors besides swimming speed are important for the success of eel migrations, such as adapting to mesopelagic zones that silver eels undergo during their spawning migrations. The most important and obvious morphological adaptation in mesopelagic fish is their well-developed eyes, and migrating eels also seem to use this strategy. These fish often have relatively large pupils61, high photosensitive structures, such as tubular eyes62, a pure rod multibank retina63, and maximum rhodopsin absorption to adapt to the blue-green light in the deep sea64. The eyes of catadromous eels displayed enlargement during their transformation into migrating silver-phase eels65, 66 and potentially increase their retinal surface area, which results in the possibility of increased photon capture. In addition, the rhodopsins in the eyes change from a freshwater type with a maximum absorption of ~ 500 nm to a deep-sea type with a maximum absorption of ~ 480 nm67,68,69. Their extreme sensitivity to light is evident through their DVM in mesopelagic water, where the timing of a large descent and ascent in the DVM demonstrated by migrating catadromous eels is precisely synchronized with sunrise and sunset. Furthermore, eels alter their swimming depth in response to the phase of the Moon9, 15, 20, 21, appearing to be capable of perceiving extremely low-intensity moonlight.This study showed that three eels released in the TS area (mainly 300–400-m depth) and one eel in the KC area (near surface) were found to change their swimming direction around the time of the solar culmination when the Sun’s bearing changed. The clockwise and counterclockwise trajectories of these eels corresponded to whether the Sun moved from the east to west in the southern and northern sky, suggesting that they demonstrated horizontal negative phototaxis swimming to avoid sunlight. They might move to avoid high-intensity sunlight horizontally, not vertically, as they gradually increase the swimming depths possibly due to acclimation to cold deep water after release. The daytime swimming depths of the eels became deeper day-by-day after their release (Fig. 4); a similar phenomenon was observed in European eels12, American eels17, and long fin eels13. Recently, Higuchi et al.20 observed that the daytime swimming depths of Japanese eels released in the TS area gradually became deeper until 13 days after their release. These facts indicate that they gradually acclimate to the cold water at the deep depths after release. Since this tracking study was conducted 2–8 days after their release, the daytime swimming depth of eels would not have reached a steady state yet. The relatively high intensity from sunlight at the shallow depths where eels swam immediately after release in the TS area might cause horizontal avoidance behavior from the light.In other cases, many eels, especially those released in the KC area, did not demonstrate the rotational behavior. The eels in the KC area mostly stayed deeper (500–800 m) during the day than the eels in the TS area (stayed at depths of 300–600 m) even during the periods shortly after their release. This is possibly due to higher water temperatures even at the deeper depths in the KC area (Fig. 4). The eels in the TS area did not demonstrate clear rotational behavior at depths of more than 400 m. The PSAT studies have reported that the steady swimming depths during the day were 500–800 m14, 20. Therefore, it was assumed that the rotational behavior observed in some eels was not a regular behavior during their migration. However, the rotational behavior observed in this study suggests that they surely perceive the horizontal direction of Sun’s bearing at 400 m depths at least. Generally, they exhibit DVM precisely synchronizing with sunrise and sunset and surely perceive the change in sunlight intensity at deeper depths9,10,11,12,13,14,15,16,17,18,19,20,21,22. Even though the rotational behavior were not observed below 400 m, it remains unknown whether the eels could not perceive the Sun’s bearing from the light penetrated at depth; thus, further investigation of response to underwater light is required in future.While possible negative phototaxis behaviors were observed in some eels after release around the time of solar culmination, the trajectories of ten eels during the entire period of tracking experiments implied that each eel tended to swim meridionally toward the bearing of the Sun at culmination. We observed that eels released at middle (20°–34° N) and low (12°–13°N) latitudes tended to swim southward and northward in the meridional direction, respectively (Fig. 6A, B). The tendency to move in a north–south swimming direction corresponded to whether the Sun culminated to the north or south: eels swam southward if the culmination occurred in the southern sky, but they swam northward if it occurred in the northern sky (Fig. 6). In the KC area (33°–35° N), the Sun rose in the southeast, passed celestial meridian in the southern sky, and set in the southwest (Fig. 6C). At 20° N in the summer time when the tracking study was conducted, the Sun also passed a celestial meridian in the southern sky, but rose in the northeast and set in the northwest (Fig. 6C). When Sun culmination occurred in the southern sky, the meridional swimming directions tended to be southward (Fig. 6A). However, at 12° to 13° N in the summer time, the Sun rose in the northeast, passed the celestial meridian in the northern sky, and set in the northwest (Fig. 6D). When the Sun at culmination appeared in the northern sky, the meridional swimming directions tended to be northward (Fig. 6B). Furthermore, the swimming behavior by one eel (WE4264_TS) that was released slightly south (14° 15′ N) from the latitude with the Sun passing through the zenith was also indicative of the meridional swimming traits. This eel moved in a northerly direction on the first day, but then it lost its north–south bias in swimming around 14° 30′ N, where the Sun nearly passed through the zenith (Figs. 1 and 6D). These observations imply that the eels might move toward the latitude with the Sun passing through the zenith.Figure 6Swimming trajectories of eels and solar paths in the celestial sphere viewed from east during each tracking period. Swimming trajectories of eels released at (A) 20°N in the tropical–subtropical area and the Kuroshio Current area, and (B) 12°–14°15′N in the tropical–subtropical area. Solar paths through the north (N)–south (S) axis and the zenith at the time of tracking in (C) 20°N in the tropical–subtropical area and the Kuroshio Current area, and (D) 12°–14°15′N in the tropical–subtropical area.Full size imageTheoretically, it is possible for mesopelagic animals to use solar cues for navigation at depths shallower than the asymptotic depth, below which penetrating light rays are symmetrical around the vertical axis and the polarization plane becomes horizontal. For example, the Sargasso Sea, where the two Atlantic catadromous eels spawn1, 3, has extremely transparent water70, and the major axis of radiance distribution still remains tilted in the mesopelagic zone. The angle of maximum radiance of sunlight at 475 nm was 13° at depths of 400 m when the Sun’s elevation was 60° (Fig. 7)52, 53. In highly transparent water, the asymptotic depth could be as high as 1000–1200 m, and the depths below this cannot be utilized for compass use53. Currently, it is not possible to verify whether the Sun culminating to north or south caused the meridional swimming tendencies of eels in this study. Potentially, these meridional swimming tendencies could be due to other orientation clues, such as the geomagnetic field, as discussed for temperate anguillid eels17, 45. Nevertheless, in future studies, it would be worthwhile considering solar cues as a possible candidate factor in the orientation of eels, even when under faint underwater light conditions.Figure 7Optical features of underwater sunlight. (A) Schematic diagram of sunlight penetrating the deep ocean at 90° to the solar bearing. The line of arrows indicates the major axis of the incident beam in a vertical plane perpendicular to the Sun’s bearing. Blue light (around 475 nm) reaches the lowest depths. With increasing depth, the light field alters its character into a less directed distribution and a lower energetic level through scattering and absorption processes. Penetrating light rays are symmetrical around the region below the asymptotic depth. (B) An example of spectral radiance distribution (e. g. 475 nm) at a certain depth. The radiance distribution is shown by an ellipsoid and the major axis is drawn by a line with arrow. The refracted angular deviation (a) of the major axis of underwater radiance distribution from the vertical axis equals the tilt of the electric vector (ee bar) from the horizontal axis53. When the Sun’ s elevation was 60° in the Sargasso Sea, the radiance distributions were measured at three different depths and the tilt of the electric vector were estimated to be 24° at depths of 100 m and 200 m and 13° at depth of 400 m52, 53.Full size imageGiven that eels might be able to use the Sun’s bearing at culmination to orient their meridional swimming direction, this orientation scheme could support a clockwise eel migration route following a partial subtropical gyre2, 37. Japanese eels that departed from the nursery area first transported northeastward via the strong KC. Maintaining southward swimming in the current, they eventually crossed the current and shifted to the southward migration course. When they enter the KC, movement to the left of the bearing of the Sun at culmination (i.e., south) is the typical pattern for the early migration of eels from Japan. The movements of eels observed in the KC were consistent with the expected route; however, eels released at low latitudes of the TS area often swam northward but also westward, which resulted in their traveling an unreasonable distance from the spawning area. This might be due to their behavior during early migration. In this study, eels were transported from Japan and released into the open ocean at low latitudes. They might have swum toward the expected bearing of the Sun at culmination as if they were in the north and moved to the left of the Sun’s bearing along with the North Equatorial Current, which would mimic the early migration of eels leaving Japan and moving along the KC.Among the eels tracked in this study were individuals with impaired swim bladders, yellow-phase eels in the process of hormone-treatment maturation, and silver-phase eels collected from different rivers in different years. Despite these variations, the swimming characteristics of the eels did not differ in terms of their DVM behavior16 and swimming speed. Nevertheless, confirmation of our results using samples with a uniform status in future research would be highly desirable. In this study, the tracked eel position was assumed to be identical to that of the tracking ship and the errors between these two positions could not be evaluated; thus, the positioning of tracked fish also may need to be improved in future studies. Experimental studies, such as tracking of blind, magnetically disturbed, or olfactory-blocked eels, could help obtain or eliminate alternative candidate clues and enhance our understanding of the navigational system of anguillid eels. Controlled laboratory experiments are required to directly quantify the ability of eels to perceive radiance distribution or polarization, along with any associated behaviors. In addition, the internal clock of eels required to perform celestial navigation should be investigated. Meanwhile, the results obtained from this study can enhance our knowledge of the mechanisms underlying the migratory behaviors of eels in the open ocean. More

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