Active swimming and transport by currents
observed in Japanese eels (Anguilla japonica)
acoustically tracked in the western North Pacific
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言語: en出版者:
公開日: 2022-09-28
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キーワード (En):作成者: 福田, 野歩人, 山本, 敏博, 横内, 一樹, 黒木, 洋明,
岡崎, 誠, 三宅, 陽一, 渡邊, 朝生, 張, 成年
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所属: 水産研究・教育機構, 水産研究・教育機構,
水産研究・教育機構, 水産研究・教育機構,
水産研究・教育機構, 水産研究・教育機構,
水産研究・教育機構（退職）,
水産研究・教育機構（退職）URL

https://fra.repo.nii.ac.jp/records/92
CC BY 4.0(c)Authors

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OPEN

Active swimming and transport
by currents observed in Japaneseeels (Anguilla japonica) acousticallytracked in the western North
Pacific
Nobuto Fukuda1,3*, Toshihiro Yamamoto1, Kazuki Yokouchi1, Hiroaki Kurogi1,
Makoto Okazaki1, Yoichi Miyake2, Tomowo Watanabe1 & Seinen Chow1,3
The mechanisms of oceanic animal migration remain enigmatic. Adult Japanese eels start their longdistance oceanic migration from coastal areas to breed near the West Mariana Ridge. We tracked
acoustically tagged eels released in the Kuroshio Current (KC) area near Japan (five silver-phase eels,
three of which had impaired swim bladders) and a tropical/subtropical (TS) area near/in the spawningarea (two yellow-phase and three silver-phase eels). We analyzed their active swimming and transport
by water currents. The strong flow of the KC dominated the eels’ movements in the north, and TS area;
their swimming influenced their movements. In the KC area, greater distances were covered at night
than during the day, because eels swam in shallower layers with strong currents at night. Three andone eel in the TS and KC area in the upper 400 m showed counterclockwise and clockwise movements
around the time of solar culmination, respectively. The meta-analysis showed that eels released at
middle latitudes (20°–34° N) generally swam southward through currents, whereas those released
at low latitudes (12°–13° N) generally swam northward through currents. Our study suggests theinfluence of the surrounding current and a potential effect of solar cues on the movements of Japaneseeels.
Temperate catadromous eels of the genus Anguilla are among the most enigmatic animals exhibiting a longdistance-oriented ­migration1, 2. Anguillid eels are born in the open ocean, their larvae grow drifting with oceanic­currents1, 3, 4. Following this, they migrate to freshwater and estuarine growth habitats. They spend years in continental and coastal waters, and then they metamorphose into silver-phase eels and migrate toward their spawning­areas5–7. Temperate anguillid eels migrate thousands of ­kilometers8, swimming primarily in the mesopelagiczone, showing diel vertical migration (DVM) swimming in relatively shallow water (mainly 150–250 m) during
the night and deep water (mainly 500–800 m) during the day to reach their spawning ­sites9–22 without ­feeding23.
Pop-up satellite archival tags (PSATs) have become increasingly popular for collecting data on the watertemperature, depth, and light intensity experienced by catadromous eels during oceanic m­ igration10–15, 17–21. The
migration route of the American eel, Anguilla rostrata, to the northern edge of the Sargasso Sea was partiallydetermined using depth data transmitted from P­ SATs17. However, elucidating the migration routes of the eels
does not resolve the navigation cues that orient their swimming, as it is not possible to distinguish active swimming from passive transport by currents using the PSAT data alone. Furthermore, satellite-based tracking relieson ocean circulation ­models17, 18, but the daily locations reconstructed from the PSAT data have high uncertainty
with more than 100 km on ­average17. This uncertainty must cause difficulty in differentiating passive transport
and active swimming.
Acoustic telemetry is a useful technique for tracking fi­ sh24 that has been used in several tracking studies on
9, 16, 25–29
migrating anguillid ­eels, which have reported swimming behaviors such as DVM, migration speed, andmigration routes. If the water currents are measured at the same time, the fine-scale active swimming by fish
1

Japan Fisheries Research and Education Agency, Yokohama Station2‑12‑4 Fukuura, Kanazawa, Yokohama,
Kanagawa 236‑8648, Japan. 2Japan Fisheries Research and Education Agency, Hatsukaichi Station2‑17‑5 Maruishi,
Hatsukaichi, Hiroshima 739‑0452, Japan. 3These authors contributed equally: Nobuto Fukuda and SeinenChow. *email: bukuchan@affrc.go.jp
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can be determined using an analysis that considers the speed and direction of water currents, but these types ofstudies are limited because active tracking, which generally involves the tracking of only one individual at a time,
is costly and laborious, especially in offshore areas. There were only a few studies in estuarine or coastal area
attempting to investigate the active swimming behaviors of the American eel and European eel, A. anguilla, in
relation to tidal currents using acoustic tags and a current m­ eter25, 26. The fine-scale movement by active swimming and transport by current of anguillid eels have not been assessed in the open ocean.
Among the anguillid species, the Japanese eel is an ideal model for the investigation of mesopelagic navigation
as its life cycle has been well investigated. This species spawns along the western side of the West Mariana Ridge.
Unlike other catadromous eels, their spawning sites have been definitively identified through the collection offertilized eggs, newly hatched larvae, and mature a­ dults30–36. Thus, the departure and destination of their oceanic
migration are well known. One of the general hypotheses for the migration route of the Japanese eel is that theeels departing from Japan are transported eastward in the KC and thereafter turn s­ outhward2, 37. The first PSAT
study of Japanese eels demonstrated that they moved along the K­ C14; however, the drag caused by the external
tag could affect their swimming p­ erformance38–40. It remains in question whether the hypothesized migrationroute has been traced without the effects of drag by the external tag.
Several laboratory experiments of anguillid eels have shown that magnetic cues may be used by juvenile andadult eels to navigate during ­migration41–44, and this appears to be true for temperate anguillid eels that likely
use a magnetic sense for their spawning m­ igrations45. Whereas a recent comprehensive review indicated thatno single cue or mechanism is used by animals to enable successful navigation over thousands of ­kilometers46.
Among terrestrial animals, the use of celestial navigational cues is fairly ­widespread47–51. Generally, aquatic
animals that inhabit deeper layers, such as the mesopelagic zone (200–1000 m), are unlikely to use celestial cues
because the quality of information from the light of celestial bodies, including information on the refracted angle
and intensity of light, declines as water depth increases. However, a polarization pattern, which could be used
to locate the Sun’s azimuth, was observed down to at a depth of 200 m at the minimum in clear water, possibly
extending to over 1000 m in more transparent w­ aters52, 53. Thus, such fainter cues could potentially be used for
migratory navigation.
In 2010 and 2012, we performed acoustic telemetry tracking of Japanese eels in the tropical–subtropical(TS) areas near/in their spawning area and the Kuroshio Current (KC) area off the coast of Japan. The DVM ofwild-caught eels corresponding to sunrise and sunset has previously been reported using these tracking ­data16;
however, the horizontal movements of these eels have not been analyzed. The North Equatorial Current in the
spawning area has a westward flow of ~ 15–30 cm/s near the s­ urface54, while the KC, i.e., the western boundary
current of the North Pacific Ocean, has a strong northeastward flow that can reach speeds > 100 cm/s near the­surface55. When combined with environmental water flow data measured using an Acoustic Doppler Current
Profiler (ADCP) system, fine-scale vectors of movements through currents (called “active swimming” or “swimming” vectors in this study) can be calculated by subtracting the water-current vectors from the fish travel vectors. The tracked eels in this study had various attributes that included two yellow-phase and three silver-phaseeels in the TS area as well as five silver-phase eels in the KC, of which three eels had impaired swim bladders.
Here, we preliminarily analyzed horizontal-swimming characteristics such as active swimming and transport
by currents of these eels in the open ocean, and their mysterious oceanic migration was discussed in relation to
the surrounding current and potential solar cues.

Results

Eel swimming speed in different environments. To analyze the active swimming (excluding current

transport) and transport by current of the eels, we defined several categories of types of analyses. The horizontal
movement of fish (including both swimming and current transport) was defined as a travel, and the length of
the trajectory indicated a travel distance. The swimming and current vectors were obtained at 10-min intervals.
The magnitudes of each were defined as swimming speed and transport speed, respectively, which represents the
speeds of each when viewed in short time. The mean vectors of 10-min-interval swimming vectors during day
and night over the tracking periods were calculated to measure the average velocity by active swimming overeach period, i.e., the net displacement divided by the time traveled, in which the magnitude of the mean vector
was defined as effective swimming speed.
Five (two yellow-phase and three silver-phase) eels were tracked in the TS area from July to August 2010,
and five silver-phase eels were tracked in the KC area from November to December 2012 (Fig. 1). The tracking
period and travel distance for each eel ranged from 42.5 to 163.4 h and 56.1 to 217.8 km, respectively, in the TSarea and 38.2 to 191.0 h and 106.0 to 379.9 km, respectively, in the KC area (Table 1). The travel distances andtrajectories during the night tended to be longer and more linear than during the day (Fig. 1). Moreover, thetravel distance per day was significantly larger in the KC area (mean ± SD: 50.9 ± 16.9 km/day, i.e., 59 ± 20 cm/s,
n = 14) than in the TS area (31.9 ± 4.5 km/day, i.e., 37 ± 5 cm/s, n = 14) (Welch’s t-test, P < 0.05).
In the KC area, the average swimming speeds, i.e., the average distance of 10-min interval swimming vectors
per second in this study, of each eel were 26–40 cm/s during the day (mean depths: 393–608 m) and 34–40 cm/s
during the night (mean depths: 139–281 m) (Table 2). The average transport speeds, i.e., the average distanceof 10-min-interval current vectors of eel swimming depths per second, were much higher in the shallow layer
where the eels swam during the night (65–103 cm/s) than those in the deep layer where they swam during theday (27–58 cm/s). The swimming speeds in body length per second were significantly higher during the night(mean ± SD, 0.48 ± 0.29 BL/s) than during the day (mean ± SD, 0.41 ± 0.27 BL/s) and were not significantly influenced by swim bladder impairment, which was used by Chow et al.16 to investigate the effect of the swim bladderon vertical movement (Table 3).

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Figure 1.  Track maps for ten eels used for analyses in this study. Trajectories of ship tracking ten eels during
daytime (yellow line) and nighttime (black line). Start (○) and end points (×) of tracking. The topographic andbathymetric map (central bottom) were created using Generic Mapping Tools ver.4 (https://​www.​gener​ic-​mappi​
ng-​tools.​org) and the database ETOPO1 grid (https://​www.​ngdc.​noaa.​gov) was used. Other maps were drawn
using QGIS software (https://​qgis.​org) and the database GSHHG ver. 2.2.2 (http://​www.​soest.​hawaii.​edu).
These maps were further modified using Adobe illustrator ver. 24. The Kuroshio Current (orange area) is drawn
based on the data from the Quick Bulletin of Ocean Conditions by the Japan Coast Guard’s Hydrographic andOceanographic Department, collected on 28 November and 16 December 2012 (http://www1.kaiho.mlit.go.jp).
The spawning area is predicted by collecting fertilized eggs, newly hatched larvae and matured adults is shadedin red.

In the TS area, the average swimming speeds of each eel were 29–39 cm/s during the day (mean depths:
353–538 m) and 29–41 cm/s during the night (mean depths: 162–242 m) (Table 2). The average transport speedsin the deeper layer where they swam during the day were lower (9–12 cm/s) than in the shallower layer where
they swam during the night (11–29 cm/s). Moreover, the swimming speeds in body length per second weresignificantly higher during the night (mean ± SD, 0.46 ± 0.23 BL/s) than during the day (mean ± SD, 0.43 ± 0.23BL/s) and were not significantly different between the yellow-phase and silver-phase eels (Table 3).
The effective swimming speed during day and night over the tracking periods were lower than the abovementioned short-term swimming speeds as the swimming vectors at the 10-min intervals exhibited more orless directional variation (Table 2). The effective swimming speed of each eel were 6–16 cm/s during the day
and 7–18 cm/s during the night in the KC area and 3–24 cm/s during the day and 10–30 cm/s during the nightin the TS area (Table 2).

Eel swimming direction. In the KC area, the mean direction of the 10-min interval swimming vectorsof each individual was eastward (mean bearing: 120°) to westward (304°), whereas the mean direction of the
10-min interval transport vectors was northward (339°) to eastward (70°) (Table 2). In the TS area, the mean
direction of the 10-min interval swimming vectors of each individual was southwestward (226°) to northward(348°), whereas the mean direction of the 10-min interval transport vectors was northeastward (67°) to westward (298°) (Table 2). All five eels in the TS area exhibited a directional swimming during the day and night,
whereas in the KC area, four of the five eels exhibited a directional swimming during the day and three of the fiveeels during the night (Rayleigh test, P < 0.05, Table 2).
The swimming and transport trajectories are superimposed with the travel trajectories in Fig. 2. These trajectories were drawn by the progressive vector plots of the eel’s active swimming through the water, transport by
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ID

1

Releaselocation

Released atTime

Lat (N)Long (E)

TravelPeriod distance
(km)
(h)

3-Dec2012

21:30

30º 29′131º 59′

118.0

256.1

Tracking ceased at

Stage

Date

Time

Lat (N)Long (E) Date

5.97

S1

28-Nov2012

21:27

30º 02′130º 36′

OriginTL (cm)BW (g)

EI

72.6

702

2

3

WE6285_KC

KC

AmikakeRiver,
Kagoshima,
November
2012

WE6288_KC4KCNaka River,Tokyo,
November
2012

83.4

996

4.95

S2

4-Dec2012

21:13

30º 58′132º 01′

6-Dec201221:13

31º 45′132º 27′

48.0

106.0

WE6289_KCKCNaka River,Tokyo,
November
2012

79.6

902

5.54

S2

7-Dec2012

22:42

32º 49′138º 03′15-Dec2012

22:42

32º 30′141º 09′

191.0

379.9

WE6287_KC4KCNaka River,Tokyo,
November
2012

81.8

914

4.67

S2

16-Dec2012

05:19

33º 03’140º59’17-Dec2012

20:00

33º54’

141º18’

38.2

108.3

WE6286_KC4KC

Naka River,Tokyo,
November
2012

83.4

990

5.95

S2

17-Dec2012

23:17

33º57’

140º56’19-Dec2012

23:17

34º55’

140º44’

48.0

125.9

WE2999_TS

TS

Tone River,
Chiba,
September
2009

79.6

860

4.17

S1

10-Jul2010

23:30

12º00′

140º 59′

12-Jul2010

18:35

12º 20′140º 54′

43.1

56.9

WE3001_TS

TS

Tone River,
Chiba,
September
2009

77.5

740

5.11

S1

13-Jul2010

00:25

13º 00′140º 59′

14-Jul2010

19:10

13º 08′140º 49′

42.5

56.1

WE3002_TS

TS

Tone River,
Chiba,
September
2009

90.1

1000

3.97

S1

16-Jul2010

21:10

13º 00′138º 00′

20-Jul2010

21:00

13º 16′137º 18′

95.8

132.4

WE4263_TS6TS

Tone River,
Chiba,
September
2009

70.5

660

5.46

Y25

24-Jul2010

01:10

13º 00′137º 59′

26-Jul2010

20:00

13º 11′137º 39′

67.3

88.8

WE4264_TS

TS

Tone River,
Chiba,
September
2009

77.5

580

5.70

Y25

8-Aug201000:35

14º 15′141º 59′

14-Aug2010

20:00

14º 29′140º 49′

163.4

217.8

WE4265_TS

TS

Tone River,
Chiba,
September
2009

72.2

460

4.96

Y25

15-Aug2010

20:18

20º 00′143º 00′

19-Aug2010

22:10

19º 37′142º 46′

97.9

108.6

Table 1.  Summary of tracking experiments for 11 Japanese eels (Anguilla japonica). KC: Kuroshio Current
area, TS: Tropical-subtropical area. 1 It consists of the ID in the study by Chow et al.16 plus the release location.
2
Eye index (= {[(A + B)/4]2 × π/TL(mm)} × 100, A; horizontal orbital diameter (mm), B; vertical orbital
diameter (mm)). 3Stages were determined from the the colorations of pectoral fins and ventral skin according
to Okamura et al.66. 4Swimbladders of these wild eels were surgically malfunctioned. 5They were Y2 stage froma view of body colorations but had eye index ranging in the S1 stage in Okamura et al.66. 6The eel (WE4263_
TS) did not exhibit normal diel vertical migration, so this eel was exclueded from the horizontal swimming
analysis.

currents and resulting eel movement over the ground. In the KC area, the transport trajectories (Fig. 2A) weresimilar to the travel trajectories. This indicates that the flow of the KC largely dominated the movements of theeels and the swimming by eels had a little effect on the travel trajectories. Contrarily, the swimming trajectories
in the TS area (Fig. 2B) were similar to the travel trajectories, indicating that the swimming by eels significantly
contributes to the travel.
Around the time of solar culmination when the Sun reaches its highest point above the horizon each day, circular or bending curves were observed in the swimming trajectories of several eels (Fig. 2, red arrowhead). Counterclockwise and bending curves were observed around the time of solar culmination in three eels (WE2999_TS,
WE3001_TS, and WE3002_TS) released at low latitudes (12–13°N in the TS area), where the Sun passed fromeast to west in the northern sky. Figure 3A presents the time-series changes in the swimming directions of eels,
indicating that they moved in a southerly direction when the Sun culminated in the northern sky. These three eels
first dove deeper around sunrise and came up shallower and then swam at depths of approximately 300–400 m
during the day (Fig. 4). Clockwise movement by eels was observed on 1 of 22 days (the first day of WE6287_KC)
at middle latitudes (north of 20° N), where the Sun passed from east to west in the southern sky. This eel was

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Release area

Time zone

Daytime

Kuroshio Current

Nighttime

DaytimeTropical-subtropicalNighttime

Swimming vector at 10-min intervals

Transport vector at 10-min intervals

Swimmning velocity overtracking periods

Eel IDN

Mean magnitude(cm/s)

Mean bearing (º)

Mean magnitude(cm/s)

Mean bearing (º)

Magnitude (cm/s)

Bearing (º)

WE6285_KC

280

32 (22)155º (1.92)*

27 (14)47º (1.49)

6

159

WE6288_KC

115

26 (16)254º (1.92)

36 (5)

25º (0.17)

7261

WE6289_KC

384

33 (23)199º (1.57)*

28 (20)67º (1.03)

7200

WE6287_KC

107

40 (19)185º (1.64)*

58 (29)13º (0.26)

10

189

WE6286_KC

103

29 (17)221º (1.23)*

44 (20)339º (0.48)

16

217

WE6285_KC

286

40 (20)120º (1.31)*

65 (26)44º (0.56)

18

116

WE6288_KC

85

34 (20)236º (1.83)

83 (11)29º (0.12)

7218

WE6289_KC496

37 (25)205º (1.34)*

72 (48)70º (0.58)

16

212

WE6287_KC

84

38 (19)304º (1.50)*

103 (14)23º (0.14)

15

309

WE6286_KC

94

34 (22)271º (1.98)

89 (39)332º (0.37)

8270

WE4265_TS

291

29 (18)226º (1.49)*9 (5)233º (1.56)

10

220

WE4264_TS504

31 (20)271º (1.94)*

10 (6)

298º (0.85)

3268

WE3001_TS

146

36 (17)265º (1.96)*

12 (5)

67º (0.96)

5265

WE2999_TS

146

38 (15)342º (1.00)*

10 (6)

86º (1.84)

23

344

WE3002_TS292

39 (16)310º (0.97)*

12 (7)

177º (1.22)

24

312

WE4265_TS

188

29 (17)226º (1.53)*

13 (6)

193º (1.06)

10

209

WE4264_TS320

35 (09)290º (1.48)*

29 (9)

263º (0.52)

11

283

WE3001_TS

57

35 (15)308º (0.82)*

12 (6)

290º (0.73)

26

310

WE2999_TS

53

38 (15)348º (0.75)*

11 (5)

290º (1.11)

30

355

WE3002_TS

168

41 (16)292º (0.85)*

13 (9)

249º (0.94)

29

291

Table 2.  Summary of swimming and transport vectors obtained at 10-min intervals in the acoustic trackingof ten Japanese eels. Values in parenthesis indicate standard deviations. Asterisk(*) in the bearing of theswimming vector indicates a significant difference from the uniformity of a circular distribution by theRayleigh test (P < 0.05).

Estimate

Std. error

df

p

t

(Intercept)

0.433

0.040

2.76

10.83

0.002**

Time of day: Night

0.070

0.012

2028.52

5.64< 0.001***− 0.067

0.052

2.80

− 1.30

0.292

0.448

0.028

4.32

15.85

< 0.001***

0.036

0.010

2466.00

3.76< 0.001***− 0.012

0.039

4.06

− 0.300.780

Swimbladder treatment: Intact(Intercept)
Time of day: Night
Developmental stage: Yellow-phase

Table 3.  Summary of linear mixed models fitted for swimming speeds in body length per second. Signif.
codes: 0 ‘***’ 0.001 ‘**’ 0.01 ‘*’ 0.05 ‘.’ 0.1 ‘ ’ 1.

swimming in an irregular manner in very shallow water during the first day (Fig. 4). The swimming directionsof this eel indicate that it moved in a northerly direction when the Sun culminated in the southern sky (Fig. 3B).
A meta-analysis among the ten tracked individuals was performed to examine whether the swimming along
the north–south and east–west axis was associated with the latitudinal and longitudinal positions of the tracking
area. In the meridional axis (north–south), the swimming trajectories of eels released in the KC area showedthat they swam southward from the release points (Fig. 2A), whereas those of eels released in the TS area, except
WE4265_TS (released at 20°N), demonstrate that they swam northward from the release points (Fig. 2B). The
10-min interval swimming vectors of eels released at 12° to 13° N tended to have northward components (0–90°
and 270–360°) with significantly higher frequencies, whereas the swimming vectors of eels released at 20° to 34°
N tended to have southward components (90°–270°) with significantly higher frequencies (Fig. 5A).
In the zonal axis (east–west), swimming vectors with westward components (180°–360°) were more frequently observed in eels released at the TS area than in eels at the KC area (Fig. 5B). Their tendency to swim in an
east–west direction did not depend on the longitudinal position of the release points toward the spawning area. In
addition, no notable difference was observed in these meridional and zonal movements between day and night.

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A Kuroshio Current area
WE6285_KC

WE6288_KCN

WE6287_KC

WE6289_KC

WE6286
_KC

20 km
20 km

20 km

20 km

5 km

20 km

B Tropical-subtropical area
WE4265_TS

10 km

WE4264_TS

20 km

WE3001_TS

WE2999_TS

10 km

10 km

WE3002_TS

20 km

Figure 2.  Trajectories during tracking eels. Travel trajectories are shown by gray lines, swimming trajectories
by red lines and transport trajectories by blue lines. Vertical and horizontal lines indicate north–south axis andeast–west axis with north at the top. The crossing points of two lines indicate release points. The closed circles
indicate end points of tracking. Circular or bending curves around the time of solar culmination are shown by
red triangles.

Swimming bearing (º E of N)

A

B

360
270
180
90
0
6:00

12:00
Time (JST)

18:00 6:00

12:00
Time (JST)

18:00

Figure 3.  Time-series fluctuation of swimming bearing of four eels. (A) The fluctuations of swimming bearingsin three eels (gray triangle WE2999_TS, blue square WE3001_TS, yellow cross WE3002_TS) released at
12°–13°N in the tropical–subtropical area around the time of Sun culmination (inverted black triangles). (B)The fluctuations of swimming bearings in one eel (gray diamond WE6287_KC) released at 33°N in the Kuroshio
Current area changed swimming bearings around the time of solar culmination. Red circles in both figuresindicate the 50 min moving average of swimming bearings.

Discussion

To our knowledge, this study provides the first recorded information on the active swimming of Japanese eelsand on their transport by currents in the open ocean. Specifically, the strong flow of the KC largely dominatedthe 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 experimentusing stamina tunnels with stable temperatures, the optimal swimming speeds of European eels were estimatedto 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 h­ abitats56. However, field studies
using PSAT tagging also reported that in situ migration speeds (including transport by currents) were less than
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30
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400
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20

WE2999_TS
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12:00

WE3001_TS

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12:00

0:00

12:00

0:00

WE3002_TS
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12:00

12:00

0:00

12:00

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10

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200

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15

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WE6285_KC
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12:00

0:00

12:00

WE6287_KC

WE6288_KC

12:00

0:00

0:00 12:00

12:00

0:00 12:00

Figure 4.  Vertical migration behavior of six eels and temperature structures. The swimming depths of three eels
(WE2999_TS, WE3001_TS, WE3002_TS) released in the tropical–subtropical area and three eels (WE6285_KC,
WE6287_KC, WE6288_KC) released in the Kuroshio Current area were written by black lines. The verticalprofiles of temperatures in the eels’ swimming place were drawn using color coded from blue (5 °C) to red(30 °C). No temperature data was available for gray area. Black bars indicate nighttime.
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 e­ els14.
Silver-phase Japanese eels start migrating from their coastal growth habitats in Japan primarily in October to­December57, 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 (fixedcompass from the departure place to the spawning site) indicate that the minimal swimming speed required toarrive at the spawning area within 8 months is 10–12 cm/s37. Our estimated effective swimming speeds of fiveout 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 beable 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 n­ ight9–22. These
DVMs are likely related to the possible avoidance from visual predators under light c­ onditions19 or maturation­control59. Essentially, through the DVMs, the eels encounter low temperatures (< 10 °C) and high temperatures(> 20 °C) during the same day. Generally, the swimming speeds of fishes are restricted by the ambient water­temperature60, 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 tomesopelagic 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 deep­sea64. The eyes of catadromous eels displayed enlargement during their transformation into migrating silver-phase­eels65, 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 absorptionof ~ 500 nm to a deep-sea type with a maximum absorption of ~ 480 n­ m67–69. Their extreme sensitivity to light isevident 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, eelsalter 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 towhether 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 theirrelease (Fig. 4); a similar phenomenon was observed in European e­ els12, American e­ els17, and long fin ­eels13.
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33˚

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WE4265_TS

* *

20˚

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Southward

0

Northward Lat (ºN) Areaat release

Frequency of swimming vectors (%)

B
WE6288_KC

ID of eels*

WE2999_TS
WE3001_TS*

WE4264_TS
WE4265_TS

100

*

*
*

WE6289_KC
WE6287_KC

100

50

WE6285_KC

WE6286_KC

TS

12˚

*

100

13˚

*

* *

WE2999_TS

WE3002_TS14˚15’*

WE4264_TS
WE3002_TS

KC–

WE6285_KC*

ID of eels

34˚*

WE6289_KC–

WE6287_KC* * *WE6286_KC

50

132˚
138˚

KC

*

*
*
*
*

130˚

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**

Westward

050

Eastward

100

141˚

*
*

TS

142˚
143˚
50

Westward

0

50

100

Eastward Long (ºE) Areaat release

Frequency of swimming vectors (%)

Figure 5.  Frequencies of swimming directions of tracked eels in meridional and zonal axis. (A) Frequency ofnorthward and southward swimming vectors during daytime (yellow shading) and nighttime (gray shading).
Vectors with the bearing of 0°–90° and 270°–360° are categorized as northward, while those at 90°–270° are
southward. Eels released at higher latitudes are ordered from the top. The latitude and area of release points
are shown in the right box. B. Frequency of eastward and westward swimming vectors during daytime andnighttime. Vectors with the bearing of 0°–180° and 180°–360° are eastward and westward, respectively. Eels
released at more west positions are ordered from the top. The longitude and area of release points are shown in
the right box. Asterisks (*) indicate a significant difference in comparison with a uniform expected frequency
under the null hypothesis by Chi-square test (P < 0.05).
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 thecold 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 fromsunlight 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 (stayedat depths of 300–600 m) even during the periods shortly after their release. This is possibly due to higher watertemperatures 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 m­ 14, 20. Therefore, it was assumed that the rotational behavior observedin some eels was not a regular behavior during their migration. However, the rotational behavior observed inthis 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 insunlight intensity at deeper d­ epths9–22. Even though the rotational behavior were not observed below 400 m, it

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A

N

W

E

S

B

C

20km

WE6286_KC
WE6287_KC
WE6289_KC
WE6288_KC
WE6285_KC
WE4265_TS

N

ZenithN

S

D
ZenithW

E

S

WE4264_TS
WE3001_TS
WE3002_TS
WE2999_TS

20km

S

N

Figure 6.  Swimming trajectories of eels and solar paths in the celestial sphere viewed from east during eachtracking period. Swimming trajectories of eels released at (A) 20°N in the tropical–subtropical area and theKuroshio 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 theKuroshio Current area, and (D) 12°–14°15′N in the tropical–subtropical area.

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 ofsolar 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 thesouthern 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 northernsky, 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 thezenith was also indicative of the meridional swimming traits. This eel moved in a northerly direction on the firstday, but then it lost its north–south bias in swimming around 14° 30′ N, where the Sun nearly passed throughthe zenith (Figs. 1 and 6D). These observations imply that the eels might move toward the latitude with the Sunpassing through the zenith.
Theoretically, 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 thepolarization 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 toverify whether the Sun culminating to north or south caused the meridional swimming tendencies of eels inthis study. Potentially, these meridional swimming tendencies could be due to other orientation clues, such as
the geomagnetic field, as discussed for temperate anguillid e­ els17, 45. Nevertheless, in future studies, it would be

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A

B

Air
Water

ZenithaeeAsymptotic depth
Nadir

Figure 7.  Optical features of underwater sunlight. (A) Schematic diagram of sunlight penetrating thedeep 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 thetilt of the electric vector (ee bar) from the horizontal a­ xis53. 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.
worthwhile considering solar cues as a possible candidate factor in the orientation of eels, even when under faintunderwater light conditions.
Given 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 subtropical­g yre2, 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 Japanand 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 DVM­behavior16 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 tothat of the tracking ship and the errors between these two positions could not be evaluated; thus, the positioningof 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 andenhance 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.

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Materials and methods
Tracking experiment.

The tracking data of Japanese eels from Chow et al.16 was used to analyze the horizontal-swimming behavior of eels in the open ocean. Wild eels were captured, commencing in the autumn
before the tracking experiments (Table 1). Beginning 1 month before the research vessel departed for tracking
in the TS area, six eels were injected weekly with salmon pituitary extract to induce maturity. Morphologicalmeasurements revealed that 8 of 11 eels were in the silver phase, whereas the remaining three eels were in the lateyellow phase, according to an established classification that uses body ­colorations66 (Table 1). The late yellowphase eels had an ocular index of 4.9–5.7, thus falling within the silver ­phase66; therefore, they appeared to betransitioning to silver eels.
Tracking was performed using depth-sensitive (P) and depth/temperature-sensitive (TP) ultrasonic transmitters (V16P and V16TP, VEMCO, Halifax, Canada) and the SEA TRACK VP170-PC (VEMCO) biotelemetry
system installed on the R/V Shoyo Maru. A hydrophone with an array of 17 receiving elements was installed
under the bottom of a ship, and each of 16 of these elements were directed to the eight points of the compass
with a lean of 0° (horizontally) and 45° (slantwise); one element was directed with a lean of 90° (downward).
The receiver recorded the depth and temperature data transmitted from the tracked fish every few seconds andestimated the vertical/horizontal directions from the vessel to the fish using the difference of the received signals
among the elements. The horizontal distances between the fish and the vessel were estimated using the verticaldirections from vessel and transmitted fish depths. The vertical/horizontal angular resolutions are both 11.25°.
In actual situations, the estimation values of the fish position relative to the vessel fluctuate as the tracking vessel
moves with waves. During tracking, the vessel was carefully operated to place the fish in front of the vessel’s bow
with a constant horizontal distance of 200–400 m while referring to the estimated fish positions. Therefore, thepositions of the tracking vessel were assumed to be identical to those of the fish, and time was expressed using
the Japan Standard Time, i.e., JST, which is 9 h ahead of the Greenwich Mean Time, i.e., GMT.
Chow et al.16 reported that two yellow-phase eels (WE4264_TS and WE4265_TS) shared similar DVM patterns with silver eels and were thus considered behaviorally analogous to silver eels. However, a third yellow eel(WE4263_TS) did not exhibit DVM. The transmitters were surgically inserted into the abdominal cavities oflarge eels. However, as the specimens WE4263_TS (70.5 cm TL) and WE4265_TS (72.2 cm TL) were relatively
small, the transmitters were externally attached to their backs. Chow et al.16 assumed that the weight or external
attachment of transmitters might affect the swimming behavior of the small eel WE4263_TS; however, the effectof transmitter attachment varied by individual as the other eel WE4265_TS exhibited standard DVM patterns.
Accordingly, the data of WE4263_TS that did not exhibit DVM were excluded from the following analysis ofhorizontal movements in this study. Further, during the study conducted by Chow et al.16, a 5 × 2-mm piece of theswim bladder was removed from three wild eels (WE6286_KC, WE6287_KC, and WE6288_KC) to investigate
the effect of the organ on DVM. However, the resultant DVM profiles of these eels were generally comparablewith those of untreated eels, except that one individual (WE6287_KC) exhibited a peculiar movement of swimming in a very shallow water in the first day. Chow et al.16 concluded that migrating eels do not depend on theirswim bladder to maintain neutral buoyancy, specifically at depth.

Data processing. The geographic position of the tracking vessel was recorded every minute using the
Global Positioning System, and was assumed to be identical to the position of the tracked fish in this study.
The travel vectors (including active swimming and transport by currents) of the eels were calculated using thegeographic positions of the vessel at 10-min intervals. The horizontal vectors of the current were measured at a
depth of 16-m layers from 32- to 816-m depths using an ADCP (Ocean Surveyor VM-ADCP, RD Instruments).
The current vector of the water layer closest to the eel swimming depth was defined as the transport vector,
and the transport vectors were averaged every 10 min. Active swimming vectors were obtained by subtracting
the transport vectors from the eel travel vectors. The swimming speed when viewed in short time and effective
swimming speeds over the tracking period of each eel were calculated from the swimming vectors: the former isthe average magnitude of 10-min interval swimming vectors per second, whereas the latter is the magnitude of
the mean vector of 10-min interval swimming vectors during all day and all night in the tracking, respectively.
The initial nights of tracking were excluded from all analyses to avoid possible release-related effects. Day andnight were indicated by sunrise and sunset. The travel distance on each day was defined as the distance traveled in 24 h from sunrise. Eels demonstrated upward swimming from 10 min before to 80 min after sunset anddownward swimming from 60 min before to 30 min after ­sunrise16. The data collected during these periods was
not used in our analysis of horizontal speeds to avoid interference from DVM factors. The altitude and azimuthof the Sun (see astronomic terminologies in Supplementary Figure 1) during the tracking experiments wereobtained from the Naval Oceanography Portal (http://​www.​usno.​navy.​mil).
Statistical analyses. The travel distances per day were compared between the TS and KC areas using
Welch’s t-test. To investigate the possible effects of the time of day (day/night), developmental stage (yellow
phase/silver phase), and swim bladder treatment (malfunctioned/intact) on their swimming speeds in bodylength per second (BL/s), the swimming speeds with Gaussian distributions were fitted to linear mixed models
using the time of day and developmental stage in the TS area or using the time of day and swim bladder treatment in the KC area, respectively, as possible fixed effects and using the specimen ID as a random effect. The
swimming speeds in body length per second were calculated from the swimming speeds at 10-min intervals
divided by body lengths.
The mean and standard deviation of the magnitude and bearing of each vector were calculated to summarize
the travel, transport, and swimming vector 
obtained at 10-min intervals for individual fish. Here, the standard
deviation of bearings, S, was defined as S = −2log(R), where R indicates the mean resultant length of circular
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data. The uniformity of the circular distribution on the swimming vectors of each eel during day and night wastested using the Rayleigh test.
To determine whether eels released at various locations could swim toward their spawning area (12–15° N
in latitude, 140.5–143° E in longitude) in the meridional (north–south) and zonal (east–west) axes, all 10-min
interval swimming vectors were categorized as northward–southward and eastward–westward. In the meridional analysis, the swimming vectors with angles of 0°–90° and 270°–360° were categorized as northward vectors
and 90°–270°° as southward vectors. In the zonal analysis, the swimming vectors with angles of 0°–180° werecategorized as eastward vectors and 180°–360° as westward vectors. The uniformity of the frequency of these
vectors in each eel was tested using the chi-squared test, compared with a uniform expected frequency under thenull hypothesis. In any test, the level of statistical significance was set to 0.05. Statistical analyses were conductedin R version 3.6.071 using the ‘lme4’ (ver. 1.1–21), ‘lmerTest’ (ver. 3.1–0), and ‘circular’ (ver. 0.4-93) packages.

Ethics. At the time of sampling (September 2009 and November 2012), A. japonica was not an endangered

species. Wild eels were purchased from local fishers with fishing licenses issued by fisher cooperative associations of the Tone River (Chiba Prefecture), Amikake River (Kagoshima Prefecture), and Tokyo Metropolitan
Government (the Naka River). Our experiments were conducted in accordance with the institutional guide of
the National Research Institute of Fisheries Science, Japan Fisheries Research and Education Agency.

Received: 19 January 2021; Accepted: 12 January 2022

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Acknowledgements

We thank K. Watanabe, Captains K. Oshima, S. Toishi, N. Nagai, and crew members of the research vessels ShoyoMaru and Kaiyo-Maru from the Fisheries Agency of Japan for their support with the tracking experiments. We
are grateful to K. Ai, M. Kawai, T. Kawai, and S. Yamamoto for providing us with wild eel specimens. We thank
R. Manabe for assistance with surgery to attach transmitters, which were generously supplied by K. Tsukamoto of
Nihon University. We thank S Sawayama for useful comments to improve the paper. We gratefully acknowledge
financial support from the Fisheries Agency of Japan and the Japan Fisheries Research and Education Agency.

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Author contributions

N.F., S.C. and T.Y. conceived the study. S.C., T.Y., M.O. and T.W. performed research on the tracking experiments.
N.F., S.C., T.Y., K.Y., H.K., M.O. and Y.M. analyzed the data on the tracking experiment. N.F. and S.C. wrote thepaper with contributions from all other authors. All data needed to evaluate the conclusions in the paper arepresent in the paper and/or the supplementary materials.

Competing interests

The authors declare no competing interests.

Additional information

Supplementary Information The online version contains supplementary material available at https://​doi.​org/​
10.​1038/​s41598-​022-​05880-x.
Correspondence and requests for materials should be addressed to N.F.
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