Mar Biol (2015) 162:1251–1263
DOI 10.1007/s00227-015-2666-0

ORIGINAL PAPER

Summer migration to temperate foraging habitats and active
winter diving of juvenile loggerhead turtles Caretta caretta in thewestern North Pacific
Tomoko Narazaki1 · Katsufumi Sato2 · Nobuyuki Miyazaki3

Received: 19 November 2014 / Accepted: 12 April 2015 / Published online: 30 April 2015
© Springer-Verlag Berlin Heidelberg 2015

Abstract Endangered loggerhead turtles (Caretta
caretta) are highly migratory marine reptiles that spend
extended maturation periods at sea. Although an understanding of the biology and ecology of juveniles is essential for effective conservation of this species, such information is still limited, especially for the North Pacificpopulation. The first quantitative bycatch survey in northern Japan revealed that the Sanriku coastal area served as
an important summer foraging habitat for large juvenile
loggerhead turtles in the western North Pacific. To examine their year-round distribution and diving behaviour, we
deployed satellite-relayed data loggers on six turtles (mean
SCLn–t ± SD = 69.2 ± 9.2 cm, range = 58.3–82.5 cm).
While turtles predominantly utilize the Sanriku coastal
area and surrounding oceanic waters during summer, allturtles spent most of their time travelling in oceanic waters(>200 m) several kilometres east of Japan and sometimes
in association with the Kuroshio Extension Current during
winter. Although water temperature experienced by turtles

Communicated by J. Houghton.
Electronic supplementary material The online version of thisarticle (doi:10.1007/s00227-015-2666-0) contains supplementarymaterial, which is available to authorized users.
* Tomoko Narazaki
naratomoz@gmail.com
1

Sea Mammal Research Unit, School of Biology, Universityof St Andrews, Fife KY16 9TS, UK

2

Atmosphere and Ocean Research Institute, The Universityof Tokyo, 5‑1‑5 Kashiwanoha, Kashiwa, Chiba 277‑8564,
Japan

3

Japan Marine Science Foundation, 1‑1‑1 Ikenohata, Taito‑ku,
Tokyo 110‑0008, Japansignificantly decreased during winter, they predominantly
stayed in water >15 °C. There was no strong seasonal pattern in diving behaviour, and daily average dive duration
was 20.9 ± 11.6 min regardless of summer or winter. In
addition, turtles sporadically performed deep dives, including the deepest dive (>340 m) ever recorded for this species, during winter. These results suggest that juveniles
remained active and possibly foraging in oceanic habitats
throughout the winter rather than adopting the quiescentoverwintering strategy (i.e. undertaking prolonged diveslasting >300 min) previously reported in adult females.

Introduction
While knowledge of distribution, habitat range and behaviour is essential for designing effective conservation management for threatened species (Parrish 2005; Hamann
et al. 2010), such information is often deficient for animals
inhabiting the marine realm (Norse and Crowder 2005).
Endangered loggerhead turtles, Caretta caretta (Linnaeus
1758), are highly migratory animals that travel between
breeding and foraging habitats (Musick and Limpus 1997).
Although modern telemetry studies have identified important foraging habitats (Polovina et al. 2006; Casale et al.
2012) and seasonal migration patterns (e.g. Mansfield
et al. 2009) for some populations, our knowledge beyond
the breeding habitats is still limited. As sea turtles are slow
growing and late maturing, understanding their biology
during extended maturation periods at sea is particularly
important for their conservation.
In the North Pacific, the south-west coast of the JapaneseArchipelago hosts the largest loggerhead turtle nesting habitats with >90 % of the North Pacific population (Bowenet al. 1995). Immediately after hatching, turtles disperse

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Mar Biol (2015) 162:1251–1263

(a)

(b)

Fig. 1  Maps of the study site. a Japanese archipelago showing thelocation of the study site. Coastal area encircled by a dashed line
indicates the geographic range of nesting sites of North Pacific loggerhead turtles based on information by Kamezaki et al. (2003).
The black star indicates Yakushima Island, the largest nesting site

in North Pacific. b Map of the study site indicating set net locations
where turtles were collected since 2005 (open dot), 2006 (closeddots) and 2008 (closed squares). The open star indicates the locationof the International Coastal Research Center. The dashed line represents 200-m-depth contour

into the ocean undertaking a mostly passive migrationtransported by oceanic gyre systems, such as the Kuroshio
and North Pacific Currents, and some turtles reach Baja
California in the eastern Pacific (Bowen et al. 1995). Afterseveral years, large juveniles return and recruit to foraging
habitats around Japan. Upon maturity, adult females undertake seasonal breeding migration between foraging habitats and specific nesting beaches every few years (Plotkin2003). Flipper tag recovery and satellite tracking studies
suggest that adult females nested in Japan migrate to either
the East China Sea or the Pacific Ocean along the Kuroshio
Current (Kamezaki et al. 1997; Hatase et al. 2002b, 2007).
In addition, bycatch surveys reported aggregations of large
juveniles and adults in the Japanese coastal areas in thevicinity of their nesting beaches (Ishihara and Kamezaki
2011; Ishihara et al. 2011). However, there is a paucity ofdata regarding how large juveniles returning from the eastern Pacific utilize potential foraging habitats around Japan
until they reach sexual maturity.
Foraging habitats for large juvenile loggerhead turtles
have been better documented for North Atlantic populations. For example, large juvenile loggerhead turtles arewidely found in the lagoons, estuaries and coastal waters
in the eastern USA from Florida to Long Island in New
York (Mendoca and Ehrhart 1982; Dodd 1988). The major
developmental foraging habitats for North Atlantic populations are located in temperate coastal waters of Virginia andChesapeake Bay where a number of large juveniles show

strong seasonal philopatry during summer (Lutcavage andMusick 1985; Musick and Limpus 1997; Mansfield et al.
2009). In the western North Pacific, Sanriku coastal area islocated at similar latitudes as Chesapeake Bay (39°N). The
Sanriku coastal area is located at ‘Kuroshio–Oyashio confluence zone’ where dynamic physical processes derived
by coexistence of warm Kuroshio-derived water and nutrient-rich cold Oyashio water result in high productivity(Lohrenz and Castro 2006). Although it is located >500 km
north from the major Japanese nesting beaches (Fig. 1),
there are anecdotal records of sea turtle bycatch in the commercial set nets fishery in this area. Thus, it is highly possible that this area hosts summer foraging habitats for North
Pacific loggerhead turtles.
As a strategy, seasonal migration enables animals to
exploit seasonal peaks of food resources and/or to avoid thephysiological stresses of unfavourable climates (Alerstam
et al. 2003; Ultsch 2006). While migration to higher latitudes allows turtles to exploit profitable foraging habitats
in temperate water, distribution of turtles is also restrictedby thermal conditions of the environment (e.g. Coles andMusick 2000; Mansfield et al. 2009; Hawkes et al. 2011)
because their body temperatures are only a few degrees
above the ambient temperature and their physiology andbehaviour are profoundly influenced by decreasing temperature (Lutz et al. 1989; Sato et al. 1994; Hochscheid
et al. 2004; Sato 2014). Due to large seasonal variations,
thermal conditions at temperate foraging habitats may not

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1253

be favourable for turtles during the winter (Morreale et al.
1992; Mansfield et al. 2009). Some turtles avoid cold winter temperatures by migrating into lower latitudes and/or warmer waters (Hawkes et al. 2007; Mansfield et al.
2009; Hawkes et al. 2011). Yet, not all sea turtles seem toadopt this strategy; at least some turtles may enter a stateof hibernation, potentially having reduced metabolic rates
in response to decreased ambient temperature. Carr et al.
(1980–1981) documented that an aggregation of loggerhead turtles captured by shrimp trawlers during winter in
Florida was lethargic and often covered in mud, suggesting that they were hibernating in the mud at the sea bottom.
More recently, Hochscheid et al. (2005) showed using satellite-relayed data loggers (SRDLs) that a loggerhead turtle
made long resting dives lasting up to 6.8 h during winterwhen water temperature fell <15 °C. Such prolonged winter dives (>5 h) have been reported in the Mediterranean(Hochscheid et al. 2005; Broderick et al. 2007; Hochscheid
et al. 2007), North Atlantic (Hawkes et al. 2007) and North
Pacific populations (Hatase et al. 2007), albeit with small
sample sizes.
Like many other populations, the North Pacific population of loggerhead turtles is of profound conservation concern. The number of nesting female decreased >80 % overthe past three decades (Kamezaki et al. 2003) most likely asa result of anthropogenic threats including fisheries bycatch(Hatase et al. 2002a; Lewison et al. 2004). Understanding
year-round distribution and behaviour of this species atthe population level is essential for the application of efficient mitigation measures. However, such information is
critically deficient in the North Pacific population compared with the North Atlantic and Mediterranean. Thus,
we first set out to quantitatively describe seasonal occurrence and size distribution of turtles at temperate habitats
in the western North Pacific by conducting bycatch survey
at the potential foraging habitats in northern Japan (Sanriku
coastal area). Due to large seasonal temperature variations,
it is expected that turtles in Sanriku coastal area migrate towarmer water and/or reduce activity during winter. Usingsatellite tracking, the aims of this study were to examine year-round movements of large juveniles in the North
Pacific and to discuss their overwintering strategy by comparing seasonal distributions and diving behaviours.

Materials and methods
Bycatch survey
We collected loggerhead turtles (Caretta caretta) between
2005 and 2010, which were incidentally captured by commercial set nets at the Sanriku coastal area (Iwate Prefecture, Japan, Fig. 1). All turtles were promptly transferredto the outdoor flow-through saltwater tanks of the International Coastal Research Center, Atmosphere and Ocean
Research Institute, the University of Tokyo (39°21′05N,
141°56′04E), where they were retained for 1 day to up to
3 months. The turtles were fed on soft tissues of Japanesecommon squid (Todarodes pacificus) to keep them healthy.
Following the definition by Bolten (1999), we measured
straight carapace length notch to tip (SCLn–t), total taillength (TTL) and body mass (BM). Sex was not determined unless an obvious extension of tail (TTL > 30 cm)
was observed in a large turtle (SCLn–t > 70 cm), which is asecondary sexual characteristic of males. As this study was
conducted as part of a tag and release program, all turtles
were released from the study area after applying plastic andmetal ID tags issued by the Sea Turtle Association of Japan(Non-Profit Organization; http://www.umigame.org/).
Satellite tracking
In 2009 and 2010, satellite-relayed data loggers (SRDL;
Sea Mammal Research Unit, St. Andrews, UK) were
deployed on nine turtles that were collected during the
bycatch survey (Table 1). After the SRDLs were glued on

Table 1  Summary of satellite tagged loggerhead turtles
Turtle ID

SCLn–t (cm)Sex

Release date (year/month/day)Tracking duration (days)

Experienced temperature range* (°C)

L0941
L0905
L0707
L0910
L0912
L0956
L1002
L1004

78.5
88.4
65.0
58.3
63.3
68.4
63.8
77.8

Male
Male
Unknown
Unknown
Unknown
Unknown
UnknownMale

2009/08/17
2009/08/20
2009/08/17
2009/08/20
2009/08/20
2009/09/25
2010/07/21
2010/07/23

17
22
133
239
403
111
94
311

19.4–24.9
16.9–21.1
17.2–24.1
10.3–25.4
13.1–28.6
13.2–26.3
16.3–26.3
17.7–26.1

L1005

82.5

Male

2010/07/23

255

15.5–26.8* Temperature ranges experienced by tracked turtles were recorded by SRDL at 2 m depth

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the turtles’ carapaces using epoxy resin (Loctite E-60 NC,
Henkel, Düsseldorf, Germany), all turtles were released in
Otsuchi Bay, Iwate, Japan (39°20′30N, 141°56′00E). The
locations of SRDLs were determined using the ARGOS
system, which assigns a quality index for each location.
Accuracy of the location classes 3, 2 and 1 is <150 m,
350 m and 1 km, respectively, and there are no limits ofaccuracy for the remaining location classes 0, A, B and Z.
But, maximum error of class 0 was estimated <19 km at
coastal water of Japan (Baba et al., 2000). To reconstruct
the migration track of each turtle, we used locations ofclasses 3, 2, 1 and 0. In addition, implausible locations having unnaturally high swim speeds (>9 km h−1) were filteredout from the track (Hochscheid et al. 2007). We calculated
daily median locations for each turtle based on the filtered
track. Then, daily median locations of all turtles were tailed
into hexagonal area bins using QGIS Geographic Information System (Open Source Geospatial Foundation Project,
http://qgis.osgeo.org).
The SRDL was fitted with an internal clock, a depth sensor and a temperature sensor. The SRDL measured depth
every 4 s and recorded individual dives when the turtle
submerged to the depth below 3 m for more than 30 s. The
configuration of SRDLs differed between the deployment
years: the maximum depth ranges were 220 and 340 m in2009 and 2010, respectively (see supplemental tables forthe resolutions of dive parameters). Once a dive was completed, the raw dive data were processed on-board to determine the time and depth of the five most significant points
of inflection, and the resulting dive profile data were stored
in a buffer within the SRDL. Then, the data in the buffer
were randomly transmitted via ARGOS system for the next
5 days, insuring that the transmitted dives were representative and not biased by the transmission schedule (Fedaket al. 2002). In addition, all dive data were summarized
for 24-h periods and transmitted as daily summary that
includes total number of dives, mean and maximum values
for both dive depth and duration.
The SRDL also measured ambient temperatures every
4 s at a resolution of 0.1 °C, providing temperature profiles
over the depth range used by the turtles. Of all temperatures measured, 12 depth–temperature points were selectedbased on the conventional broken-stick algorithm used for
expendable bathythermographs. Then, the resulting data
were stored in a buffer where it was made available fortransmission for up to 5 days. Hereafter, we refer to watertemperature as the temperature recorded at 2 m depth, theshallowest temperature obtained by SRDLs, as an approximate measure of sea surface temperature. In this study,
we obtained water temperature data from SRDLs at intervals of 0.6 ± 0.8 days on average. However, temperature
data were not available for up to 17 days because SRDLs
were programmed to prioritize transmitting dive data over13

Mar Biol (2015) 162:1251–1263

temperature data. Therefore, daily median water temperature was calculated by linear interpolation.
The seasonal effect on water temperature experienced
by turtles and diving behaviours were examined using
generalized linear mixed models (GLMM) with a Gaussian distribution (identity link). Summer and winter seasons
were defined as the periods between May 1 and October
31, and November 1 and April 30, respectively. As the
SRDL deployed on three turtles (L0941, L0905 and L1002)
ceased transmission before entering winter periods, thesedata were excluded from the statistical analysis. Turtle ID
was included as random effects to account for pseudoreplication because data obtained from the same turtle were notindependent. Dependent variables were daily water temperature and daily summary of diving behaviour (log-transformed maximum and average dive depth and duration).
Explanatory variable was ‘season’ (summer or winter) for
the water temperature model. For the diving behaviourmodels, explanatory variables were ‘season’ and ‘dailywater temperature’. For each dependent variable, the mostparsimonious model was selected on the basis of AIC. The
significance of the fixed effect of the selected model wastested using Wald’s F test. All statistical analysis was performed using R (The R project for Statistical Computing,
http://www.r-project.org).

Results
Bycatch survey
Between 2005 and 2010, a total of 152 loggerhead turtles
were captured as bycatch in set nets. The number of turtles
collected each year ranged from 6 to 55. However, interannual variation will not be discussed since the number of
set nets increased over the study periods: one net in 2005,
15 nets in 2006–2007 and 22 nets in 2008–2010 (Fig. 1b).
Only three out of 152 turtles were found dead during thestudy resulting in 2 % mortality rate. Bycatch incidents werereported from mid-June to late October (Fig. 2). Mean temperature, at which turtles were captured, was 18.5 ± 2.4 °C(±SD, range = 12.0–23.8 °C). Size of turtles ranged from49.5 to 88.4 cm SCLn–t (mean ± SD = 70.8 ± 6.4 cm;
Fig. 3a). However, the smallest turtle showed an apparent
deformity having a concaved carapace. Excluding this malformed turtle, the SCLn–t of the smallest turtle in this study
was 52.5 cm. Body mass ranged from 21.5 to 104.5 kg(55.5 ± 13.5 kg: Fig. 3b) and was positively correlatedwith SCLn–t (BM = 0.00109 × SCLn–t2.54, R2 = 0.90,
F1, 147 = 1264.0, P < 0.01: Fig. 3c). Distinctive elongationin the tail (TTL > 30 cm) was found in 17 turtles (mean
SCLn–t ± SD = 79.3 ± 3.7 cm, range = 72.8–88.4 cm).
None of the turtles were marked by the old ID tags at their

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1255
25

20

30

15
20
10

SST(°C)

Number of turtles

50

Number of turtles

40

40
30
20
10
0

40

50

60

70

80

90

SCLn-t (cm)

10

5

JUN

JUL

E M L

E M L

SEP

OCT

AUG

0

SeasonsFig. 2  Number of loggerhead turtles captured in the set nets. E, M
and L represent the early, mid and late periods of each month. Average sea and standard deviation of surface temperature measured at
the fixed observation point in the study site (at Kamaishi Bay; http://
www.suigi.pref.iwate.jp/teichi) is showed on the right axis

initial capture at our study site. Thus, new ID tags wereapplied to all turtles before releasing from our study site.
During the 6-year study period, four out of 149 tagged
turtles were recaptured at the study site 1–3 years after
the release. Annual growth rate of the three smaller turtles (SCLn–t range = 62.6–70.1 cm at the initial capture)was 1.2–1.6 cm year−1, whereas that of the largest turtle(SCLn–t = 80.7 cm) was only 0.1 cm year−1.
Satellite tracking and general movements
Nine turtles were tracked for an average of 176 ± 133 days
(mean ± SD, range = 17–403 days; Table 1). The SRDLs
deployed on three turtles (L0941, L0905 and L1002)
worked for relatively short periods (17–94 days) andstopped transmitting data before the winter. During these
periods, the three turtles showed similar patterns utilizing
neritic water (<200 m): two males (L0941 and L0905) travelled southward along the coast of Honshu, while L1002
travelled northward up to 42°14′N in September 2010.
After spending a few days in the coastal area of Hokkaido, it headed back southward along the coast until early
October 2010. Then, L1002 travelled eastward staying inoceanic water (>200 m) until the transmission ceased inlate October 2010. The remaining six turtles were tracked>100 days covering both summer and winter periods. Afterrelease from the Sanriku coastal area, all of these turtles concentrated their movements in waters off the eastern coast of Honshu (35–45°N, 140–145°E) during the

(b)

40
30
20
10
0

20

40

60

80

100

80

90

BM (kg)
120
100

(c)

80

BM (kg)E M L E M L E M L

Number of turtles

50
0

(a)

60
40
20
0
40

50

60

70

100

SCLn-t (m)Fig. 3  Size distribution of loggerhead turtles captured at Sanriku
coastal area: a frequency histogram of straight carapace length, b frequency histogram of body mass and c a relationship between bodymass and straight carapace length. Equation for the regression curve
is BM = 0.00109 × SCLn–t2.54

summer, but some turtles continued eastward travelling as
far as 170°E (Figs. 4a, 5a, b). During winter, the turtles predominantly stayed in oceanic waters (>200 m), travellinghundreds kilometres offshore east of Japan and within the
Kuroshio Extension Current region (Figs. 4b, 5c, d).
Ambient temperature
Mean water temperature experienced by the nine turtles(i.e. recorded at 2 m depth) throughout the entire tracking

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Mar Biol (2015) 162:1251–1263

Fig. 4  Spatial use and movements of loggerhead turtles
equipped with SRDLs during
a summer (817 track daysby nine turtles) and b winter(810 track days by six turtles).
Colour denotes the numberof days turtles were recordedin each hexagon. The area of
each hexagon is 2282 km2 onaverage. The star represents therelease site. The dashed line
represents 200-m-depth contour.
Open circles indicate locations
where deep dives (>200 m)
were recorded

periods ranged from 19.4 to 22.7 °C. Six turtles (L0707,
L0910, L0912, L0956, L1004 and L1005) were successfully tracked during both summer and winter periods.
For the six turtles, water temperature significantly varied
between summer and winter (F1, 1349.2 = 568.6, P < 0.01;
Fig. 6): the turtles experienced warmer water during summer (mean ± SD = 22.2 ± 2.6 °C, N = 621 days) thanwinter periods (19.3 ± 2.5 °C, N = 733 days). Three turtles (L0910, L0912 and L0956) experienced sea surface
temperatures <15 °C during winter (Fig. 7). L0956 briefly
stayed in cold water (i.e. <15 °C at 2 m depth) for 2 days in
the end of November, whereas L0910 and L0912 moved tocold water several times spending up to 10 and 18 days in
the water <15 °C, respectively. The lowest temperature of
10.3 °C was recorded by L0910 in 2 April 2010. Although
this lowest temperature was recorded 9 days before the
SRDL ceased transmitting temperature data, it is less likelythat the turtle was dead or cold-stunned because the SRDL
continued transmitting dive data until 25 May 2010.

13

Diving behaviour
Daily dive summary data showed that turtles generally
undertook shallow dives (range of medians of daily average dive depth = 6–24 m, N = 6 turtles), but occasionallyperformed deep dives (range of medians of daily maximum
dive depth = 20–65 m). Five turtles in this study performed
dives beyond the maximum depth range of SRDLs (i.e.
>220 m for L0910 and L0912; >340 m for L1004, L1005
and L1002). The GLMM analysis showed that daily average dive depth was influenced by both season and watertemperature: daily average depth increased during summer (mean ± SD = 17.5 ± 9.2 m, range = 3.0–50.0 m,
N = 621 days for summer, 14.8 ± 10.4 m, 3.0–72.5 m,
N = 733 days for winter; F1, 1347.5 = 30.61, P < 0.01)
and with increasing water temperature (F1, 1349.1 = 73.86,
P < 0.01). Daily maximum dive depth was also positively
related to water temperature (F1, 1350.2 = 329.84, P < 0.01).
However, there was no significant seasonal effect on

Mar Biol (2015) 162:1251–1263

1257

(a)

(b)

(c)

(d)

Fig. 5  Satellite tracks of loggerhead turtles and sea surface temperature (SST) in the western North Pacific. a Tracks of L0707, L0905,
L0910, L0912, L0956 and L0941 during August and October 2009
(black lines). Coloured background shading shows mean SST for
September 2009. b Tracks of L0912, L1002, L1004 and L1005 during May and October 2010 overlaid onto mean SST for September

100

50

0

200

Frequency (day)30(a)
Water temperature (ºC)

Frequency (day)

150

10

15

20

25

30

L0707
L0910
L0912
L0956
L1004
L1005

25

20

15

10
Nov 1

(b)

Dec 1

Jan 1

Feb 1

Mar 1

Apr 1

May 1

Month of tracking

150

Fig. 7  Temporal variations in water temperature at 2 m depth measured by SRDLs during winter months. Note that three turtles experienced low temperatures below 15 °C (dashed line) for more than afew days100
50
02010. c Tracks of L0707, L0910, L0912 and L0956 during November 2009 and April 2010 overlaid onto mean SST for December 2009.
d Tracks of L1004 and L105 during November 2010 and April 2011
overlaid onto mean SST for January 2011. For the monthly mean
SST, NOAA’s AVHRR Oceans Pathfinder SST (http://podaac.jp.asa.
gov) was used

10

15

20

25

30

Temperature (ºC)
Fig. 6  Frequency histogram of daily water temperature at 2 m depth
recorded by SRDLs of six turtles during a summer and b winterdaily maximum dive depth (57.6 ± 47.6 m, 4.0–340.0 m,
N = 1354 days), and all six turtles undertook deep dives(>100 m) during winter, including the deepest dives(>340 m) by L1004 and L1005 (Table 2). The GLMM

analysis for daily dive duration showed that both maximum
and average duration were not significantly affected bytemperature. Moreover, there was no significant seasonal
difference in daily average dive duration (20.9 ± 11.6 min,
0.7–80.0 min, N = 1354 days). Daily maximum dive
duration was significantly longer during the winter(67.9 ± 32.0 min, 0.7–200.0 min, N = 733 days) than thesummer (51.5 ± 22.5 min, 12.0–140.0 min, N = 621 days;
F1, 1348.5 = 94.16, P < 0.01). The longest dive recorded inthis study was 200 min, which was performed by L1005

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Mar Biol (2015) 162:1251–1263

Table 2  Descriptive dive statistics during summer and winterID

Summer

WinterNo. of Duration (min)dives [Q1 − Q3]

Depth (m)[Q1 − Q3]

1124
1159
3086
673
2304

7.0 [1.3–24.0]
7.0 [1.3–18.0]
16.0 [1.7–35.0]*
9.0 [1.3–22.0]*
18.0 [5.0–28.0]

8.0 [4.0–16.0]90
8.0 [5.0–22.0]75
8.0 [4.0–24.0]* 115
8.0 [5.0–20.0]*
80
19.0 [7.0–37.5]* 75

L1005 1665

10.0 [1.3–30.0]

7.0 [4.0–16.0]

L0707
L0910
L0912
L0956
L1004

No. ofdives

Duration (min)[Q1 − Q3]

Depth (m)[Q1 − Q3]

Max dura- Max depthtion (min) (m)

180
>220
>220
120
>340

762
1302
2069
801
2681

10.0 [1.3–24.0]
4.0 [2.0–30.0]
2.0 [0.8–30.0]
2.0 [0.8–10.0]
20.0 [2.3–35.0]*

8.0 [4.0–16.0]
8.0 [5.0–20.0]
3.0 [3.0–6.0]
6.0 [4.0–14.0]
12.0 [5.0–32.5]

100
140
130
115
150

120
200
160
140
>340

160

1962

16.0 [4.0–30.0]* 10.0 [5.0–17.0]* 200>340

Max dura- Maxtion (min) depth
(m)

140

Median dive duration and depth are provided with 25 % (Q1) and 75 % (Q3) quintiles
Seasonal differences in dive duration and depth were examined for each turtle, and significantly larger value was marked with an asterisk(* P < 0.05, Wilcoxon’s rank test)

in January 2011 (daily water temperature = 21.1 °C). We
obtained a total of 19,588 dive profiles (10,011 and 9577
dives during summer and winter, respectively) from six turtles. Descriptive statistics of these dives are summarized inTable 2.

Discussion
Highly migratory loggerhead turtles are the most temperate
species of hard-shelled marine turtles. Combining bycatchsurvey and satellite tracking, our study highlighted that loggerhead turtles in the western North Pacific utilized temperate habitats on a seasonal basis, as previously reported in the
North Atlantic and Mediterranean populations (e.g. Hawkes
et al. 2007; Zbinden et al. 2008; Mansfield et al. 2009). Our
study provided the first quantitative report of the seasonaloccurrence of loggerhead turtles in the Sanriku coastal area.
The Sanriku coastal area is known for highly productive fishery grounds in Japan due to complex oceanographic structures caused by mixing of nutrient-rich Oyashio and warm
Kuroshio-derived waters. Tens of turtles were incidentally
captured by coastal set nets annually during June and October, which coincided with the period when the effect of theKuroshio-derived water increases (Hanawa and Mitsudera,
1987). Satellite tracking also showed that turtles frequently
used the Sanriku coastal area and adjacent oceanic areas
during the summer (Fig. 4a). Recent population genetic
analysis revealed that individuals in feeding aggregations
from Sanriku mainly originated from southern rookeries inJapan, especially from Yakushima Island (Nishizawa et al.
2014). Some turtles seasonally migrate with warm Kuroshioderived water to capitalize on the highly productive Sanriku
coastal area although it is located > 1400 km from theirmajor natal sites (i.e. Yakushima Island, see Fig. 1a).

13

In the North Pacific, juvenile loggerhead turtles undertake transoceanic migration from their juvenile nursery
habitats in the eastern Pacific (Bowen et al. 1995). Ishihara et al. (2011) estimated the size of loggerhead turtles
re-entering Japanese water at 56.0–74.9 cm by examining
the size distribution of turtles captured off Cape Muroto in
Japan (33°15′N, 134°11′E) which is approximately 950 km
south-west from our study site. The size distribution ofSanriku and Muroto aggregations largely overlaps. However, it is interesting to note that turtles captured in Sanriku (mean ± SD = 70.8 ± 6.4 cm, range = 52.5–88.4 cm)
were slightly smaller than that in Muroto (75.7 ± 6.7 cm,
56.3–105.0 cm). It might be possible that the Sanriku
coastal area provides seasonal foraging habitat for younger
juveniles, including the ones that just completed their transpacific migration from their nursery habitats in the eastern
Pacific (Nishizawa et al. 2014).
It is generally challenging to determine the degree ofmaturity of living sea turtles without using an endoscope.
However, we speculate that turtles migrating to the Sanriku coastal area were predominantly juveniles because of
the small body sizes. Based on the anatomical examination of >100 bycatch individuals in Japan, the size at maturity (where 50 % of turtles had fully developed gonads or
genital duct) for North Pacific loggerhead turtles was estimated at 82.1 cm in SCLn–t for both sexes (Ishihara andKamezaki 2011). The smallest mature turtle reported intheir study was 73.8 and 77.8 cm for females and males,
respectively, which coincided with the smallest nestingfemales recorded in their major nesting ground (i.e. 73.5 cm
in Yakushima Island; Kamezaki 2003). Only 33 % of turtles captured in Sanriku were larger than 73.5 cm and 3 %were larger than 82.1 cm, inferring that most of them had
not reached sexual maturity. Furthermore, no old tags wereattached on any of the turtles when they were first captured

Mar Biol (2015) 162:1251–1263

at the study site although standardized tags have been
affixed to nesting females in Japan since 1990 (Suganuma
and Kamezaki 1991). For example, a total of 2219 adultfemales were tagged at 16 major nesting beaches in Japan
during 1991 and 1995 (Kamezaki et al. 1997). Given thatsimilar efforts have been made until recently, the absenceof old tags infers that most of turtles captured at Sanriku
have not reached reproductive maturity. It is possible some
adult males migrated to Sanriku coastal water as 11 % of
turtles showed the secondary characteristics of males, having a distinctively long tail (SCLn–t = 72.8–88.4 cm). Yet,whether these males reached maturity remains uncertain
because tail elongation appears to begin before reachingsexual maturity (Ishihara and Kamezaki 2011).
Although the Sanriku coastal area provides favourable
foraging habitat for juvenile loggerhead turtles during summer, it is subject to large seasonal variation in water temperature. In the later autumn through the spring, sea surface temperature progressively decreases as low as 4 °C
(Takasugi 1992; Sato et al. 2007). The lethal temperatureof loggerhead turtles would be just below 10 °C at which
turtles become lethargic and float due to physiological
failure (Milton and Lutz 2003), and cold-stunning eventswere widely reported at <8 °C (e.g. Witherington andEhrhart 1989). Therefore, turtles in Sanriku should migrate
to warmer water to avoid lethally cold temperature. Thishypothesis was supported by the fact that bycatch incidents
were limited during June and October while sea surface
temperatures were ≥12 °C (Fig. 2). Satellite tracking of six
overwintering turtles showed that they predominantly travelled in the north-west Pacific off east Japan (Fig. 4b). Oneof the key features characterizing oceanographic conditionin this region is Kuroshio Extension Current, a strong warm
eastward-flowing inertial jet accompanied by large-amplitude meanders (Qiu 2002). During the winters in 2009–2011, the mean axis of the Kuroshio Extension Current
was located around 35°N latitude in the region between
142° and 155°E longitude (Seo et al. 2014). Movementsof the overwintering turtles seemed to be associated with
the northern and southern edges of the Kuroshio Extension Current, which is recognized for its high eddy kinetic
energy and high phytoplankton and zooplankton productivity (Kimura et al. 2000; Qiu 2002). Movements associated with meso-scale eddies are not uncommon in loggerhead turtles, potentially taking advantage of eddy-induced
aggregation of prey (Polovina et al. 2004, 2006; Mansfield
et al. 2009). A large satellite tracking dataset of juvenile
loggerhead turtles in the central and eastern North Pacificidentified some important oceanic foraging habitats, suchas the Kuroshio Extension Bifurcation Region (30°–40°N,
155°–180°E; Polovina et al. 2006) and the Transition Zone
Chlorophyll Front in the central North Pacific (Polovina
et al. 2000). The size of turtles tracked in the central North

1259

Pacific was smaller (41.0–81.0 cm in SCL; Polovina et al.
2000, 2006) but partly overlapped with that of turtles inSanriku coastal area (52.5–88.4 cm). In this study, one turtle (L0912) migrated eastward as far as 170°E. It is possible that some turtles in Sanriku coastal area might migrate
further east to use oceanic foraging habitats in the central
North Pacific.
There are only a few reports about the diving behaviourof overwintering loggerhead turtles, all of which showedsignificant increases in dive duration during the winter associated with decreasing water temperatures (Hochscheid et al.
2005; Broderick et al. 2007; Hatase et al. 2007; Hawkes
et al. 2007; Hochscheid et al. 2007). For example, dive duration of an adult female recorded in the coldest months in
the Mediterranean Sea (i.e. mean ± SD = 307 ± 127 min,max = 614 min) was more than tenfold longer than summer dives (Broderick et al. 2007). In our study, however,there was no significant seasonal effect on dive duration.
Furthermore, maximum dive duration recorded in this study
was much shorter than previous studies (Fig. 8), inferringthat turtles in this study retained more active throughout the
winter although minimum water temperature was as low as
10.3 °C. Prolonged winter dives (>5 h) previously reported
were typically characterized by repeated U-shaped dives tosimilar depth, suggesting that turtles remained quiescent, or
potentially hibernating, on the sea bottom (Hochscheid et al.
2005, 2007; Broderick et al. 2007) or mid-water (Hatase
et al. 2007; Hawkes et al. 2007). In contrast, our turtles performed various types of dives during winter, including someV-shaped dives to deep depths (>200 m) during the winter(Fig. 9). Some dives were deeper than 340 m although theexact dive depths were not recorded because it was outside of the range of the tags’ depth sensors. Nevertheless,this is a new record for loggerhead turtles as previously the
maximum dive depth recorded was 233 m (Sakamoto et al.
1990). It is estimated that adult loggerhead turtles become
neutrally buoyant at depths near 14 m (Minamikawa et al.
2000). Thus, these deep dives can be considered as active
dives because turtles need to stroke hard to compensate fornegative buoyancy while ascending from the deep depth(Watanabe et al. 2006). In this study, overwintering turtles
generally undertook relatively shallow dives (i.e. daily average depth = 14.8 ± 10.4 m), perhaps foraging on gelatinous
prey while travelling at relatively shallow depths where they
can attain near neutral buoyancy (Narazaki et al. 2013).
In the open ocean, dense aggregations of gelatinous zooplankton can be formed around physical discontinuities
such as fronts (Graham et al. 2001). Despite its low caloric
value (Doyle et al. 2007), dense aggregation of gelatinous
prey may offer substantial food resource for loggerhead
turtles in the open ocean. It has been reported that loggerhead turtles consume various types of gelatinous prey,such as scyphozoan, urochordates (e.g. salps, pyrosomes)

13Mar Biol (2015) 162:1251–1263

600
L0707
L0910
L0912
L0956
L1004
L1005
Adult female (NW Pacific)
Adult females (NW Atlantic)
Adullt female (Mediterranean)
Subadults (Mediterranean)

0
20

400

(b)

60
12:00

15:00

18:00

21:00

00:00

03:00

06:00

09:00

12:00

15:00

18:00

21:00

0
50

300

100

200

100

150
200
250
300
350
03:00

0
10

15

20

25

30

Minimum temperature (°C)

Fig. 8  Relationship between monthly maximum dive duration andmonthly minimum water temperature. Maximum dive durationand the lowest temperature previously reported in an adult in North
Pacific (Hatase et al. 2007), adults in North Atlantic (Hawkes et al.
2007), an adult and subadults in Mediterranean (Hochscheid et al.
2005, 2007) are added for comparative purposes. The dashed line
indicates the longest dive duration ever recorded for this species (i.e.
614 min, no temperature information) reported in an adult in Mediterranean (Broderick et al. 2007)

and siphonophores (e.g. Dodd 1988; Narazaki et al. 2013).
While some coastal scyphozoan jellyfish disappear during winter, many siphonophores and urochordates can befound in the open ocean throughout the year (Doyle et al.
2013). Although these species generally distribute in the
deep-water column beyond the regular reach of turtles,
overwintering turtles may still be able to feed on these mesopelagic prey because many siphonophores and urochordates conduct diel vertical migration into the upper 100 m
during night (Angel and Pugh 2000). In fact, some mesopelagic species (e.g. Phyrosoma atlanticum) were found in
the stomach of loggerhead turtles captured in central North
Pacific (Parker et al. 2005). It is also possible that somedeep dives (>200 m) were associated with deep-water foraging. However, such deep dives (>200 m) were recorded
sporadically in oceanic habitats (Fig. 4) and are more likely
to be exploratory dives as seen in deep-diving leatherback
turtles (Houghton et al. 2008).
Both the wide spatial distribution associated with the
Kuroshio Extension Current and active dives presented inthis study are suggestive of active pelagic foraging during
winter, which highly contrasts to the ‘hibernation’ strategy

13

40

80
09:00

Depth (m)Maximum dive duration (min)

500

(a)
Depth (m)1260Time (hh:mm)

Fig. 9  Examples of dive profiles for 18-h periods: a summer divesrecorded on 15–16 October 2010 by L1005 while experiencing watertemperature of 25.8 °C (i.e. daily median temperature at 2 m depth);b winter dives recorded on 12 December 2011 by L1005 while experiencing water temperature of 22.8 °C

mostly reported for post-nesting females (Broderick et al.
2007; Hawkes et al. 2007; Hatase et al. 2007). Our results
showed that juveniles in the western North Pacific predominantly stayed in water >15 °C although water temperaturesignificantly decreased during winter (Fig. 6). Some juveniles in the north-west Atlantic seemed to adopt similar
active overwintering strategies where they migrate large
geographic distances in association with the warm Gulf
Stream (Mansfield et al. 2009). It might be more beneficial for juveniles to continue foraging in relatively warm
water during winter because the higher food intake rates
and temperature result in faster growth rates (Balazs andChaloupka 2004). Foraging ecology of loggerhead turtles
appears to be more plastic than previously believed, andfacultative oceanic-to-neritic shifts have been reported forlarge juveniles (McClellan and Read 2007; Casale et al.
2008; Mansfield et al. 2009) and adult females (e.g. Hatase
et al. 2002b; Hawkes et al. 2006). In this study, two turtles migrated southward along the coast by the end of summer although their overwintering habitats were unknown
due to short tracking durations. In addition, according to amark-and-recapture survey conducted concurrent with ourstudy, a few turtles were recaptured at Kochi and Mie prefecture in the south-western part of Japan during the winter(Narazaki 2009; Narazaki et al. unpublished data). It is possible that juveniles in western North Pacific have dichotomous seasonal migration strategies (oceanic vs neritic) as

Mar Biol (2015) 162:1251–1263

demonstrated in North Atlantic population (McClellan andRead 2007; Mansfield et al. 2009). Additional tracking of
turtles linking with long-term diet study (e.g. stable isotope
analysis) will help elucidate polymorphism in foraging andoverwintering strategies in this population.
North Pacific loggerhead turtles are a genetically distinct population (Hatase et al. 2002c) that experienced
drastic population declines over the past three decades(Kamezaki et al. 2003). By combining bycatch surveys andsatellite tracking, we demonstrated that the Sanriku coastal
area (summer) and Kuroshio Extension region (winter) are
important foraging habitats for large juvenile loggerhead
turtles in the western North Pacific. The use of temperate
foraging habitats and seasonal migrations to oceanic habitats by large juveniles have been reported for the North
Atlantic population (McClellan and Read 2007; Mansfield
et al. 2009), but never for the North Pacific population.
Fortunately, bycatch mortality rate in the Sanriku coastal
area was only 2 % during this study. There was low riskof drowning primarily because the set nets adopted in the
study site consist of large nets stretched vertically from thesea surface to the bottom without covering the top of thenets. However, the use of large geographic areas of western
North Pacific by large juveniles implies that they are at considerable risk of fishery-induced mortality because pelagic
longline fishery effort is generally high throughout the year
in the western and central North Pacific (Lewison et al.
2004; Roe et al. 2014). A stage-based population model
based on demographic data for loggerhead turtles suggested
that conservation efforts should be focused on large juveniles for effective population recovery (Crouse et al. 1987;
Crowder et al. 1994). Our study provided a new insightabout year-round behaviour of North Pacific large juveniles, suggesting that special mitigation measures should
be considered in their oceanic habitats in the western North
Pacific. It is clear that subsequent studies integrating turtles’
movements and regional fishing effort data will help identifying the priority areas for conservation management.
Acknowledgments This study was conducted with permission fromthe Ethics Committee of the University of Tokyo. This study could
not be achieved without great volunteers from Fisheries Cooperative
Association of Funakoshi Bay, Hirota Bay, Kamaishi Bay, KamaishiTobu, Miyako, Ofunato, Okirai, Omoe, Otsuchi, Ryori, Sanriku-Yamada, Sasaki, Toni and Yoshihama for providing us with wild-caught
sea turtles. We are grateful to Y. Fujiwara, H. Murasaki, K. Onizuka
and S. Takuma for their assistance in collecting, measuring and handling the turtles. We gratefully acknowledge M. Kurosawa, K. Morita,
J. Takada, M. Hirano, A. Koshida, R. Koshida, Y. Watanabe, N. Katsumata, E. Sawai and I. Nakamura for their assistance in the field.
We also acknowledge NPO Everlasting Nature of Asia for recovering
satellite-relayed data logger from a stranded turtle. Special thanks go
to K. Aoki, H. Shimadzu, S. Isojunno and Y. Papastamatiou for lots ofuseful advices. This work was supported by the program ‘Bio-logging
Science’, The University of Tokyo (UTBLS), a JSPS research grant(24241001 to KS), a JSPS Research Fellowship for Young Scientists

1261
to TN (21-7432) and a Sasakawa Scientific Research Grant from The
Japan Science Society to TN (19-526). We also acknowledge the useof the Maptool (http://www.seaturtle.org/) program for the maps ofstudy site. The AVHRR Oceans Pathfinder SST data were obtained
from Physical Oceanography Distributed Active Archive Center(http://podaac.jpl.asa.gov). We thank two anonymous reviewers forthe constructive comments. Finally, we would like to dedicate ourwork to all the people in our study site who were severely suffered bytsunami in 11 March 2011.

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