Fisheries Science

, Volume 79, Issue 3, pp 417–424

Vertical behavior of juvenile yellowfin tuna Thunnus albacares in the southwestern part of Japan based on archival tagging

Authors

    • National Research Institute of Far Seas FisheriesFisheries Research Agency
  • Takashi Kitagawa
    • Atmosphere and Ocean Research InstituteUniversity of Tokyo
  • Shingo Kimura
    • Atmosphere and Ocean Research InstituteUniversity of Tokyo
    • Graduate School of Frontier SciencesUniversity of Tokyo
Original Article Biology

DOI: 10.1007/s12562-013-0614-9

Cite this article as:
Matsumoto, T., Kitagawa, T. & Kimura, S. Fish Sci (2013) 79: 417. doi:10.1007/s12562-013-0614-9

Abstract

The behavior of juvenile yellowfin tuna Thunnus albacares in southwestern Japan was investigated using archival tag data from five fish (fork length 52.5–92 cm, days at liberty 26–280 days) released near the Nansei Islands (24–29°N, 122–130°E). Vertical behavior was classified into three patterns: “shallow” (≥50 % of daytime hours at depth of <50 m), “deep” (≥50 % of daytime hours at ≥100 m), and “intermediate” (other than “shallow” or “deep”). The pooled proportion of the number of days of each behavior was 29, 25 and 46 %, respectively. The proportion of “shallow” behavior increased with fish size. The proportion of time spent near the surface at nighttime increased in the colder season, when the thermal gradient was relatively small. Surface-oriented behavior (fish remained at a depth of <10 m for more than 10 min) occurred mainly during nighttime and between November and January. Dives exceeding 500 m were occasionally observed (0.02 day−1), and one fish dived to 1230 m. The results of our study show that yellowfin tuna were typically distributed in the mixed layer or upper thermocline where the water temperature was close to the sea surface temperature and that the vertical behavior was variable.

Keywords

Archival tagsVertical behaviorYellowfin tunaNorthwestern Pacific Ocean

Introduction

Numerous ultrasonic telemetry and some archival and pop-up tag studies have been conducted to date to clarify the vertical behavior of yellowfin tuna Thunnus albacares. The authors of several of these studies reported that the fish stayed in a shallower layer based on data collected using fish aggregating devices (FADs) or tracking vessels [13]. Behavioral patterns in this species have been observed to vary between studies and/or individuals. For example, in some studies yellowfin tuna were found to spend relatively more time in deep water during the daytime than at nighttime [1, 410], while such patterns were not observed in other studies [11, 12]. It is thus likely that vertical behavior in this species is affected by a number of factors, including oceanographic conditions. It has been reported that vertical distribution of this species is usually limited to the layer where water temperature is close to sea surface temperature [1, 7, 11, 12]. However, individual fish have also been shown to vary in vertical behavior [6]. Relatively few studies have been conducted on the behavior of yellowfin tuna in the northwestern Pacific Ocean, including the sea near Japan, which is the fishing ground of this species. Such information on the behavior of yellowfin tuna in this area would be useful for comparison with results obtained in studies conducted in other areas. Elucidating the vertical behavior of this species is important for evaluating catchability by different types of fishing gear, especially by surface fisheries. The information will also be useful for standardizing the CPUE (catch per unit effort) and for developing stock assessment models which use information on fish behavior, such as habitat-based model. Although tracking fish by boat using ultrasonic telemetry can provide detailed behavioral information, including horizontal movements, most such observations are short term. In comparison, the use of archival tags makes it possible to monitor long-term behavior and is therefore considered to be the better approach when the aim is to investigate changes in behavior associated with seasons or oceanographic conditions.

In the study reported here, we used archival tagging to characterize the vertical behavior of juvenile yellowfin tuna in southwestern Japan, especially with respect to the relationship with water temperature and change in behavior by season and body size. The results, which form part of a national tropical tuna resources research project by the Fisheries Agency of Japan, are analyzed and discussed.

Materials and methods

Tag and release methods

Yellowfin tuna were captured by pole-and-line, trolling and handline around anchored FADs in southwestern Japan (Nansei Islands, 24–29°N, 122–130°E; Fig. 1), and the fish thus captured which showed with no bleeding or serious injury were selected for tag deployment. Archival tags (NMT ver.1.0 and ver.1.1, Northwest Marine Technologies, Shaw Island, WA, and LTD-2310, Lotek Wireless, Newmarket, ON, Canada; Table 1) were used. NMT and LTD-2310 tags were set to record time-series data (external and internal temperatures, water depth and light intensity) at intervals of 256 and 60 s, respectively. Tags were surgically implanted in the peritoneal cavity of the fish. Two conventional tags (PDA tag: length 15 cm, diameter 1.7 mm; Hallprint Pty Ltd, Hindmarsh Valley, Australia) were also deployed on the dorsal region of the fish for increasing the possibility of tag discovery and recovery rate. A total of 90 individuals [fork length (FL) 38–120 cm] were released with archival tags between 2000 and 2009.
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Fig. 1

Release positions of yellowfin tuna fitted with archival tags

Table 1

Specifications of archival tags used for in study

Tag properties

NMT Ver.1.0

NMT Ver.1.1

LTD-2310 (8 MB)

LTD-2310 (16 MB)

Memory size

256 kB

256 kB

8 MB

16 MB

Length (cm)

10

10

7

7

Diameter (cm)

1.6

1.6

1.6

1.6

Resolution of the sensors

 Depth (m)

1 (≤126 m depth), 3 (≥127 m depth)

1 (≤126 m depth), 3 (≥127 m depth)

1

1

 Temperature (°C)

0.2

0.2

0.05

0.05

Accuracy of the sensors

 Depth (m)

N/A

N/A

±20

±20

 Temperature (°C)

≈±0.2

≈±0.2

±0.1

±0.1

Weight in air (g)

52

52

40

40

Sampling interval (s)

256

256

60

60

Days of data recordeda

 Fixed part

40

40

500

500

 B part

122

122

480

1460

Archival tags NMT ver.1.0 and ver.1.1 (Northwest Marine Technologies, Shaw Island, WA) and LTD-2310 (Lotek Wireless, Newmarket, ON, Canada) were used

aNumber of days for sampling interval used in the study. “Fixed part” is the area in which time-series data are first recorded and not overwritten; “B part” is the area in which time-series data are overwritten when the memory gets full

Data analyses

All of the day log and time-series data were downloaded from the recovered archival tags and used for analysis. Time-series depth and temperature records were separated into daytime and nighttime periods based on sunrise and sunset times estimated from light intensity using proprietary software Readable provided by NMT or Viewer provided by Lotek Wireless. In cases where the estimated sunrise or sunset times appeared to be abnormal, the time of the preceding or subsequent day was used, or an average of both was taken. Only nighttime swimming depth was used for the analysis of the relationship between the proportion of distribution near the surface and oceanographic conditions because nighttime swimming depth was comparatively constant between behavior types [6]; nighttime is considered to reduce the effects of other factors. Length of the fish at liberty was primarily estimated based on the length at release and at recapture and on the assumption that the growth rate was constant. If length at recapture was not available and weight at recapture was available, length was estimated using a length–weight relationship (W = 1.94 × 10−5 × L3.00, where W is body weight in kilograms, and L is fork length in centimeters) derived from purse seine catches in the western and central Pacific Ocean (National Research Institute of Far Seas Fisheries, unpublished data, 1999). If neither data on length nor weight were available at the time of recapture, then length at release and growth rate of another fish captured in the study were used to estimate length.

Classification of vertical behavior

Vertical movement was classified into three categories according to the daytime swimming depths of the fish over a 24-h period using a modification of the classifications of Leroy et al. [13] for yellowfin and bigeye tuna Thunnus obesus, Wilson and Block [14] for Atlantic bluefin tuna T. thynnus and Howell et al. [15] for bigeye tuna. “Shallow” behavior was defined as fish spending ≥50 % of daytime hours above a depth of 50 m; “deep” behavior, as fish spending ≥50 % of daytime hours below a depth of 100 m; “intermediate” behavior, if the swimming behavior was neither “shallow” nor “deep.” “Surface-oriented behavior” was defined as when fish remained at depths of <10 m for more than 10 min [3, 13], which is considered to be related with catchability for surface fisheries. This behavior was only detected in data recorded by the LTD-2310 tags, which were set to record time-series data every 1 min. “Deep diving” were defined as dives to depths of >500 m [3].

Results

A total of seven (7.8 %) fish were recaptured, and archival tags from six fish were recovered. Time-series data for one of the recovered tags (Northwest Marine Technologies ver.1.0) were completely lost due to overwriting after recapture. Consequently, data from five individuals were available for analysis (days at liberty 26–280; total no. of days 539 days; Table 2). Free swimming fish ranged in size from 52.5 to 92 cm FL, which corresponds to age 1–2 years based on a growth curve by Wankowski [16].
Table 2

Yellowfin tuna individuals monitored using archival tags

Release

Recapture

Days at liberty

Tag no.

Tag type

Date

Latitude

Longitude

Fork length (cm)

Date

Latitude

Longitude

Fork length (cm)

1483

NMT ver.1.0

10/10/2001

26°40′N

126°57′E

85.2

11/5/2001

26°40′N

126°56′E

92a

26

1718

NMT ver.1.0

4/24/2002

24°22′N

122°53′E

54.5

8/1/2002

34°16′N

136°38′E

63b

99

748

LTD-2310

10/17/2003

27°54′N

129°36′E

68.0

12/10/2004

27°53′N

129°31′E

76a

95

B3295

LTD-2310

11/1/2004

24°22′N

122°58′E

62.0

12/10/2004

24°59′N

125°00′E

64a

39

D2073

LTD-2310

5/13/2008

24°22′N

122°58′E

52.5

2/17/2009

28°45′N

130°45′E

77c

280

aReported

bEstimated by length at time of release and growth rate

cInferred from reported body weight

Examples of vertical behavior are shown in Fig. 2, and frequency distribution of the swimming depths for each individual by month with the average water temperature is shown in Fig. 3. The fish usually performed frequent up and down movements, and sometimes followed a “U-shaped” trajectory during the day with a clear diurnal pattern, especially with “deep” behavior. The range of distribution was usually between the near surface and around a depth of 150 m, which corresponds to the mixed layer or above the thermocline. Swimming depth during nighttime was usually shallower than that during daytime. The proportion of time spent in the surface layer (<10 m) during nighttime was often high, especially between October and January, but it was low between May and August—except for fish No. 1718 in June and July, which was recaptured in the Honshu area where the water temperature near the surface was lower than that in the Nansei Islands area. Fish no. 1483, which was larger than the other individuals monitored, spent a higher proportion of time in the surface layer than the other individuals. Two to three individuals of similar body size were monitored during October–December, but the vertical distribution among these individuals varied. The swimming depths for each behavioral pattern and for all of the patterns combined were significantly deeper during the daytime than at nighttime (P < 0.0001 for all comparisons, Wilcoxon rank sum test). The proportion of days spent exhibiting “shallow,” “intermediate” and “deep” behaviors was 29, 46 and 25 %, respectively, and the average duration of each behavior was 7.8, 5.6 and 3.6 days, respectively. In the case of the “deep” behavior, the lowest temperatures typically encountered during the daytime ranged between 12 and 21 °C, and the difference between the highest and lowest daytime temperatures ranged between 6 and 15 °C. Fish spent 56 % of their time in waters that were within 1 °C of the surface temperature.
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Fig. 2

Example of the vertical swimming profile of yellowfin tuna [fish D2073, with an estimated fork length (FL) of 75 cm at this time]. Shaded zones Nighttime

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Fig. 3

Frequency distribution of swimming depth (bars) and water temperature profile (dots) for each individual by month. Figures in the graph Average estimated length (cm FL) of the fish

Figure 4 shows monthly changes in the proportion of days for behavior types for fish of <80 cm FL and recaptured in the Nansei Islands area, and changes in the proportion of days for behavior types by body size for the data collected in October and November (containing data on many individuals with different body size). Although seasonality of the behavior was not clear, the “shallow” behavioral pattern dominated in January and was not—or only rarely—observed between May and July (Fig. 4a). As a function of body size, the proportion of the “shallow” behavioral pattern generally increased with increasing body size (Fig. 4b), being 8 % in the FL size classes 60–69 cm and >50 % in the FL size classes 80–89 and 90–99 cm. “Deep” behavior was only observed in the FL size classes 60–69 and 70–79 cm. “Intermediate” behavior was observed in all size classes comparatively equally.
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Fig. 4

Relative proportion of days for different swimming behaviors as a function of season (only for the fish <80 cm FL and recaptured in the Nansei Islands area) (a) and body size (based only on data for October and November) (b). N, n Number of individuals and of days, respectively

The proportion of fish distributed near the surface differed according to the season. In January and February, the near-surface temperature (20–30 m) reached lows of approximately 22 °C (Fig. 3), and the thermal gradient (temperature difference between the sea surface and the average temperature at 20–30 m) was <0.2 °C (Fig. 5). Under these conditions, the proportion of time spent swimming at the surface was high at night (approx. 60–70 %). During June to August, the near-surface temperature was as high as about 29 °C and the thermal gradient was large (>0.3 °C). At that time, the frequency of nighttime swimming at the surface was low (<40 %) except for fish No. 1718, whose ambient temperature near the surface was about 27 °C. These results imply that the near-surface temperature as well as the thermal gradient may both have affected the distribution of yellowfin tuna near the sea surface. Using the methods of Kitagawa et al. [17] to analyze the partial correlations among these three factors, we found that the relationship between thermal gradient and time spent near the surface was significant (partial correlation coefficient −0.6796, P = 0.031; Fig. 5). Conversely, the correlation between average temperature at a depth of 20–30 m and time spent near the surface was not significant (partial correlation coefficient −0.5354, P = 0.111).
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Fig. 5

The relationship between thermal gradient [delta-T: difference between sea surface temperature (SST) and average temperature at a depth of 20–30 m] and nighttime swimming frequency at the surface (0–30 m). R, rp Coefficient of determination and partial correlation coefficient, respectively

A total of 1967 surface-oriented behavior events (mean 4.7 day−1) were observed, with most occurring at nighttime (Fig. 6a). The number of events decreased sharply with increasing duration, with the duration being mostly within 30 min (mean 27.7 min; Fig. 6b). This behavior occurred more frequently between November and January and again in February, September and October, but rarely in the other months, although no data are available for March and April (Fig. 6c).
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Fig. 6

Distribution of diving events by time of day (a), frequency distribution of duration (b) and daily dive frequency in each month by fish size (c) for surface-oriented behavior

Deep diving was observed in four of five individuals. A total of 12 dives were recorded; the estimated body length at the time of the event was 58–76 cm FL and the frequency ranged from 0.00 to 0.05 dives/fish/day (average 0.02 dives/fish/day). The duration of each dive was 8–85 min (average 24 min). Four dives occurred within 2 days of the previous dive. One dive was extremely deep, reaching a depth of 1230 m (water temperature was 4.6 °C) (Fig. 7), while the rest of the dives were shallower than 633 m (mean 557 m). All of the dives except for one occurred during the daytime.
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Fig. 7

Time series for swimming depth, ambient and body temperature during a deep dive by a yellowfin tuna (Fish No. B3295; date 11/25/2004; estimated body length 63 cm FL at this time; maximum depth 1230 m)

Discussion

In this study, several characteristics of the vertical behavior of yellowfin tuna were elucidated, including variations in the behavior, seasonality, changes in behavior by body size and the relationship with oceanographic conditions.

Although daily variations in the daytime swimming depth of yellowfin tuna were observed, the difference between day and night was not as apparent as has been found for bigeye tuna in the equatorial eastern (54–159 cm FL) [18, 19] or northwestern Pacific Ocean (49–72 cm FL at release) [20].

Josse et al. [21] reported that the swimming depth of yellowfin tuna appeared to be related to the sound scattering layer during both daytime and nighttime. Around the Nansei Islands, the deep scattering layer was observed at depths of <160 m during nighttime and partly during the daytime [2224]. This agrees with the swimming behavior of the yellowfin tuna observed in our study. Regarding prey species of yellowfin tuna, Kondo [22] reported that small yellow tuna individuals (mean 42.3 cm FL) caught near Okinawa Island (25°54′N, 127°41′E) fed primarily on mesopelagic Vinciguerria spp. (Phosichthyidae). Ménard et al. [25, 26] also reported that yellowfin tuna (<90 cm FL) caught in the equatorial Atlantic Ocean fed on V. nimbaria, cephalopods, and other pelagic species. These findings indicate that yellowfin tuna appear to make dives to feed on mesopelagic species.

Limited daily differences in ambient water temperatures (generally <16 °C) and the high incidence of the yellowfin tuna in this study in waters where ambient temperatures were close to surface temperatures (<1 °C difference) imply that the vertical distribution of yellowfin tuna depends more on temperature differences than on temperature itself. While the daily differences in the ambient temperatures observed in our study were similar to those observed in the equatorial eastern Pacific Ocean [6], these differences were smaller than those observed in the western Indian Ocean (mostly 13–20 °C [27]). Since the authors of these studies monitored large fish (134 cm FL at release), it is possible that the tolerance of fish to thermal gradients differs according to fish size. However, no studies have been conducted to date clarifying the effect of body size on the capacity for thermoregulation in yellowfin tuna. The distribution of the differences between ambient and surface temperatures was also similar to the results of a previous study (near the main Hawaii Islands and in the eastern Pacific Ocean [12]). Holland et al. [1], who investigated the distribution of ambient temperature relative to mixed layer temperatures near Hawaii, reported a similar result that ambient temperature was usually close to the temperature of the mixed layer. Block et al. [11] reported that >90 % of the temperatures the fish (75–90 cm FL) experienced were limited to a narrow thermal range that was close to that of the surface water temperatures (17.5–20.0 °C). Mitsunaga et al. [10] reported that a juvenile yellowfin tuna (25 cm FL) that was associated with an anchored FAD in the Philippines mainly stayed in the surface mixed layer, and Weng et al. [7] reported that adult yellowfin tuna (estimated 136–155 cm FL) in the Gulf of Mexico appeared to prefer layers where the water temperature was <6 °C cooler than that of the surface water. The results of these studies suggest that, regardless of body size, the vertical distribution of yellowfin tuna is mainly limited to layers where the water temperature is close to that of the sea surface. Thus, based on the results of our study, we suggest that seasonal differences in the distribution of tuna near the surface depend on the thermal gradient near the surface, indicating that the vertical distribution of yellowfin tuna is affected by differences in water temperature. Seasonal changes in the proportion of behavioral types, for example, that the proportion of “shallow” behavior increased in the colder season, were also observed. These seasonal changes are also considered to be induced by changes in oceanographic conditions. It is interesting to note that two individuals of similar body size in our study (fish No. 1718 and D2073) differed with respect to the proportion of distribution near the surface in June and July. The water temperature near the surface where fish No. 1718 was recaptured, in the Honshu area, was lower than that for fish No. D2073 (about 29 °C). This result also suggests that the vertical distribution of yellowfin tuna is affected by water temperature.

The incidence of surface-oriented behaviors in our study (mean 4.7 day−1) was markedly higher than that of bigeye tuna (49–72 cm FL at release) in the same area (mean 1.0 day−1) [20], and the duration of this behavior for yellowfin tuna (mean 27.7 min) was longer than that of bigeye tuna (mean 21.8 min) [20], indicating that yellowfin tuna have a higher affinity for surface waters than bigeye tuna. The incidence of surface-oriented behaviors in yellowfin tuna in the equatorial eastern Pacific Ocean (mean 14.3 day−1 [6]) is markedly higher than that of the yellowfin tuna in our study, probably because of the colder temperatures and higher thermal gradient in the equatorial eastern Pacific Ocean, which seems to increase the proportion of stays near the surface based on the findings of our study. The occurrence of surface-oriented behavior in the colder season (November to February) during nighttime in our study agrees with the observation of higher surface distribution during nighttime in the colder season. Interestingly, distinct changes in surface distribution in response to ocean conditions between August and September coincided with changes in the frequency of surface-oriented behavior. Similar changes may have occurred between April and May, but data on the surface-oriented behaviors during that period are not available.

Although the reasons for performing deep diving are not clear, several hypotheses have been put forward, including foraging, predator avoidance, exploration of bathymetry and parasite removal [6, 29]. In our study, the low frequency (mean 0.02 day−1), short duration (mean 24 min) and occurrence of successive deep diving within a short period (<2 days) suggests that predator avoidance is the most likely explanation. Extremely deep dives such as those observed in our study (maximum 1230 m) have also been reported by Dagorn et al. [29] (maximum 1160 m), Leroy et al. [13] (maximum 1315 m) and Schaefer et al. [9] (maximum 1423 m). Taking into account the prolonged duration of the deep diving {1 h 57 min (1160 m) reported by Dagorn et al. [29]; 1 h 30 min (1160 m) reported by Schaefer et al. [6]} it is possible that deep dives are also used for foraging.

Holland et al. [1] and Marsac and Cayré [28] reported that, of FAD-associated yellowfin tuna, the daytime swimming depths of some fish decreased and others did not change. Cayré and Marsac [29] modeled the vertical distribution of yellowfin tuna and their association with FADs relative to water temperature and dissolved oxygen profile and found that the depths of FAD-associated and unassociated fish were similar. In our study, all of the fish were released around a FAD and most were also recaptured around a FAD; therefore, the behavior is considered to be at least partly affected by FADs. It would appear that one of the reasons for the changes in vertical movements of the yellowfin tuna in our study is the effect of FADs. Individual differences in vertical distribution for the fish of similar body size in the same season also suggests the possibility of effects of FADs.

This is the first detailed investigation of the vertical behavior of yellowfin tuna in the sea near Japan. We found that juvenile yellowfin tuna of all size classes investigated in our study generally stayed in the shallow water layers (mixed layer or the upper region of the thermocline) in all seasons. We also found that the vertical distribution of this species changed in accordance with differences in water temperature relative to sea surface temperatures. A diurnal pattern was observed in the vertical movements of this species. Changes in vertical behavior through associations with floating objects remain unclear, and further investigations, such as analyses of horizontal distribution and movement based on archival tag data, or direct observation based on ultrasonic telemetries, need to be conducted.

Acknowledgments

We are thankful to the staff of the Fisheries Agency of Japan, who organized the tagging project, and to I. Ohta, S. Kondo, K. Maeda, M. Okuhara, J. Sakaki, M. Mizoguchi and A. Nitta, for their assistance with the tagging project. We also thank the staff and crew of the Yonaguni-cho, Itoman, Okinawa-shi, Minatogawa, Yaeyama and Setouchi fisheries cooperatives. We extend our thanks to H. Okamoto, H. Shono and Y. Semba, for their support with the tagging project.

Copyright information

© The Japanese Society of Fisheries Science 2013