Oecologia (2006) 149: 52–64
DOI 10.1007/s00442-006-0431-2

POPULATION ECOLOGY

Hideo Hatase Æ Katsufumi Sato Æ Manami Yamaguchi
Kotaro Takahashi Æ Katsumi Tsukamoto

Individual variation in feeding habitat use by adult female green
sea turtles (Chelonia mydas): are they obligately neritic herbivores?

Received: 15 September 2005 / Accepted: 29 March 2006 / Published online: 9 May 2006
 Springer-Verlag 2006

Abstract Satellite telemetry and stable isotope analysis
were used to conﬁrm that oceanic areas (where water
depths are >200 m) are alternative feeding habitats for
adult female green sea turtles (Chelonia mydas), whichhave been thought to be obligate herbivores in neritic
areas (where depths are <200 m). Four females were
tagged with satellite transmitters and tracked during
post-nesting periods from Ogasawara Islands, Japan.
Three females migrated to neritic habitats, while transmissions from another female ceased in an oceanic
habitat. The overall mean nighttime dive depths during
oceanic swimming periods in two females were <20 m,
implying that the main function of their nighttime diveswere resting with neutral buoyancy, whereas the meansin two other females were >20 m, implying that they
not only rested, but also foraged on macroplankton thatexhibit diel vertical migration. Comparisons of stablecarbon and nitrogen isotope ratios between 89 females
and the prey items in a three-source mixing model estimated that 69% of the females nesting on Ogasawara
Islands mainly used neritic habitats and 31% mainly
used oceanic habitats. Out of four females tracked bysatellite, two females were inferred from isotope ratios toElectronic Supplementary Material Supplementary material isavailable for this article at http://dx.doi.org/10.1007/s00442-0060431-2 and is accessible for authorized users.
Communicated by Wolf Mooij
H. Hatase (&) Æ K. Tsukamoto
Ocean Research Institute, University of Tokyo,
Nakano, Tokyo 164-8639, Japan
E-mail: hatase@ori.u-tokyo.ac.jp
Tel.: +81-3-53516879
Fax: +81-3-53516514
K. SatoInternational Coastal Research Center,
Ocean Research Institute, University of Tokyo, Otsuchi,
Iwate 028-1102, JapanM. Yamaguchi Æ K. Takahashi
Sea Turtle Association of Japan and Ogasawara Marine Center,
Chichijima, Ogasawara, Tokyo 100-2101, Japanbe neritic herbivores and the two others oceanic planktivores. Although post-nesting movements for four females were not completely consistent with the inferencesfrom isotope ratios, possibly due to short tracking
periods (28–42 days), their diving behaviors were consistent with the inferences. There were no relationships
between body size and the two isotope ratios, indicatinga lack of size-related diﬀerences in feeding habitat use by
adult female green turtles, which was in contrast withloggerhead sea turtles (Caretta caretta). These results
and previous ﬁndings suggest that ontogenetic habitat
shifts by sea turtles are facultative, and consequently,
their life histories are polymorphic.
Keywords Life history Æ Ontogenetic habitat shifts Æ
Reptile Æ Satellite telemetry Æ Stable isotope analysis

Introduction
Animals often shift habitats to meet their changing
needs during ontogeny, e.g., to maximize growth rates,
to minimize mortality risk, or to minimize the ratio of
mortality risk to growth rate (e.g., Werner and Gilliam
1984; Dahlgren and Eggleston 2000). These shifts are
not obligate but facultative, because if the needs of anindividual are met in a habitat, it may continue to use
the habitat throughout its life. Individual variation inhabitat use can result in intrapopulational polymorphism in life history. This has often been reported inrelatively small, abundant, easily handled/observed, orcommercially important animals such as insects (Harrison 1980), ﬁshes (Tsukamoto et al. 1998; Maekawa andNakano 2002), amphibians (Wilbur and Collins 1973),
and birds (Lundberg 1988), and various mechanismsthat evolve and maintain the life-history polymorphism
within populations have been proposed in studies ofthese animals (e.g., Gross 1996; Brockmann 2001).
Because sea turtles do not have any of these attributes, studies on their behavior and ecology are challenging and typically qualitative except during nesting

53

periods (and subsequent hatchling stages) when theyland on sandy beaches. For example, although recent
technological advances in satellite telemetry have enabled the foraging behavior of sea turtles to be observedin remote locations far from land during non-nesting
periods (e.g., Hays et al. 2004a), the sample sizes of theseobservations are still small due to their high cost. This
makes it diﬃcult to generalize their behavior and ecology quantitatively (i.e. as a population). However, a
recent study has overcome this diﬃculty by simultaneously using direct (telemetry) and indirect (biogeochemical analysis) methods (Hatase et al. 2002).
Stable isotope analysis has increasingly been used toinfer animal movement patterns from invertebrates tohigher vertebrates (Rubenstein and Hobson 2004). This
technique is generally based on the fact that isotope
ratios of animals reﬂect those of their diets with someenrichment. Thus, if isotope ratios in diets from diﬀerent
geographical origins are highly separated, comparison
between isotope ratios in animals and diets can tell us
where the animals came from. Although fractionation
factors (enrichment values) between isotope ratios inanimals and diets, and the turnover rates of isotope ratios in animals, are diﬀerent both among tissues within
an individual and among species, those for sea turtles are
not yet available (but see Seminoﬀ et al. 2006). Fractionation factors and turnover rates determined forother species have been applied to sea turtle studies(Godley et al. 1998; Hatase et al. 2002). In the present
study, egg-yolks were used for analysis. Since vitellogenesis of sea turtles is presumed to begin 4–6 months
prior to the mating season and to be completed prior tomating (Rostal et al. 1998), the isotope signatures of
their egg-yolks should reﬂect the prey consumed inforaging areas before migration to nesting beaches.
Green sea turtles (Chelonia mydas) spend their earlylife history stages in open ocean pelagic habitats (wherewater depths are >200 m), feeding mainly on planktonic animals (Musick and Limpus 1997; Bjorndal
1997). After several years of the early developmental
stage, they leave oceanic/pelagic habitats and recruit toneritic/benthic habitats (where depths are <200 m) inwhich they shift to herbivorous diets consisting ofmacroalgae and seagrasses (Kurata et al. 1978; Miyawaki 1994; Musick and Limpus 1997; Bjorndal 1997).
After reaching sexual maturity, they start seasonal
migrations between the neritic feeding habitats anddistant nesting beaches (e.g., Tachikawa and Sasaki
1990; Baba et al. 1992, 1993; Luschi et al. 1998; Cheng
2000; Godley et al. 2002), which are undertaken every
few years (Hirth 1997).
In contrast to this general understanding of the green
turtle life history, recent satellite telemetry revealed that,during post-nesting seasons, adult females not only migrated into neritic habitats, but also wandered in oceanic
habitats for several months (Japan Fisheries Resource
Conservation Association 1999). They feed presumably
on planktonic animals in the oceanic habitat as thejuveniles do. This suggests that not all green turtles shift

habitats ontogenetically, but that their habitat shifts arefacultative. The same phenomenon has recently been
documented in loggerhead sea turtles (Caretta caretta)
nesting in Japan, because both oceanic and neritic areas
were quantitatively conﬁrmed to be used as feeding
habitats (Hatase et al. 2002). These behavioral diﬀerences inﬂuence several life history traits of female loggerheads, and this was considered as a life-history
polymorphism within populations (Hatase et al. 2004).
In this study, we tested whether oceanic areas arealternative feeding habitats for adult female green turtles, which have been believed to be obligate herbivores
in neritic areas. First, post-nesting movements and diving behavior of tagged individuals were directly measured using satellite telemetry. Green turtles have beenthought not to feed either during the migration to andfrom a nesting ground or during their stay at a nesting
ground (Mortimer and Carr 1987). From dive information during the migration, they were considered tosimply alternate between travelling just beneath thesurface and resting within the depths where they could
attain neutral buoyancy (Hays et al. 2001). Thus, if
green turtles forage during migration, it is predicted thatthey would show diﬀerent diving behaviors from thoseabove. For example, they may frequently dive deeper
beyond the maximum depth of neutral buoyancy to
exploit planktonic prey. Therefore, we focused on divedata during oceanic swimming periods and analyzed
them in light of the use of neutral buoyancy associatedwith resting. Second, stable isotope analysis was used toinfer the feeding habits of adult female green turtles.
Synthesizing these ﬁndings, we determined their feeding
habitat use and evaluated their apparent life history in
relation to those of other sea turtle species.

Materials and methods
Satellite telemetry
On 10 August 2003 and 17 August 2004 (the end of thenesting season), satellite transmitters (Satellite Relayed
Data Loggers, Series 7000, Sea Mammal Research Unit,
University of St Andrews, St Andrews, UK) were attached to four adult female green turtles (the smallest
and largest turtles in each year: turtles 1 and 2 in 2003,
turtles 3 and 4 in 2004; Table 1), which were kept in abreeding pool of the Ogasawara Marine Center(2705¢N, 14212¢E) on Chichijima Island, Ogasawara
Islands, Japan. Every year, some adult female green
turtles are legally captured by ﬁshermen early in thebreeding season and kept in the pool to collect eggs forheadstarting projects (Sato et al. 1998). The data loggers
were attached to the carapaces of the turtles with epoxy
resin and glass-ﬁber cloth. Their eggs were also collected
for stable isotope measurements. Turtle 1 was brought
oﬀshore, 8.5 km west of Chichijima Island, by a boatand released there, while Turtles 2, 3, and 4 were released at a beach adjacent to the breeding pool.

54
Table 1 Summary of information on adult female green turtles (Chelonia mydas) tracked by satellite from Ogasawara Islands, Japan
TurtleStraight
carapace
length
(mm)

Body
mass
(kg)

Releasedata

Lasttransmission

Tracking
duration(days)

Distance
covered(km)

d13C (&)

d15N (&)

1
2
3
4

905
1,068
927
1,092

115.2a200.0
125.2a211.0

10 Aug 2003
10 Aug 2003
17 Aug 2004
17 Aug 2004

21 Sep 2003
13 Sep 2003
19 Sep 2004
14 Sep 2004

42 (14)34 (18)33 (19)28 (15)

1,962
1,546
1,627
966

17.7
18.4
17.3
18.2

8.3
11.4
11.4
9.3

Numbers in parentheses next to the tracking durations are the days during which turtles swam in oceanic areas and the dive data wereanalyzeda
Estimated from straight carapace length

The data loggers were located with the Argos system,
which classiﬁed locations into seven classes of decreasing
accuracy (<150 m, 350 m, 1 km for the ﬁrst threeclasses: 3, 2, 1; and with no limits of accuracy for theremaining four classes: 0, A, B, Z). Because there
were insuﬃcient locations of high-accuracy classes toreconstruct migratory routes, all locations, except for
the locations that required a high speed of travel(>7.2 km/h), were used for the route reconstruction.
The total distance covered was calculated as the sum of
the shortest distances between successive locations.
The data loggers recorded depth every 4 s with aresolution of 0.33 m (range: surface to 10 m) or 1 m(range: 10–486 m). The start of dives was deﬁned by thetime that the saltwater switch on the data logger perceived that the transmitter was submerged and the depth
became below 2 m for 30 s, and the end of the dives wasdeﬁned when either the depth became less than 2 m, or
the saltwater switch recorded the transmitter breaking
the surface. When dives were completed between 2 and10 m, the data logger transmitted only the maximum
depth, the time of the end of the dive, and dive duration.
When dives exceeded 10 m, the data logger transmitted
the time and depth of the ﬁve most signiﬁcant points ofinﬂection during the dive, the time of the end of the dive,and dive duration. Because of the limited bandwidth of
the Argos system, not all dive data were obtained. In
addition to relaying individual dives, the data logger also
summarized the dive information, such as the percentageof time spent deeper than 2 m into 6-h summaries.
Individual dives were used as a proxy for the proportionof time spent diving over the 24-h cycle, and these proxyvalues were converted into absolute units using the mean
percentage of time spent diving supplied in the 6-hsummaries (Hays et al. 2004a).
Sea turtles often show midwater resting dives withneutral buoyancy (e.g., Minamikawa et al. 2000; Hayset al. 2001). During these dives they spend most of theirtime in the gradual ascent phase following the occasional
steep deep drop so mean dive depth should be a better
indicator of the dive (Hays et al. 2001). Thus, bothmaximum and mean dive depths were used for analysis
in this study. For a dive exceeding 10 m, the mean divedepth was calculated by reconstructing the dive proﬁlefrom the ﬁve inﬂection points and the start and end

points. Depths of the start and end points were deﬁned
as 2 m, and depths at every 10% of dive duration were
calculated using equations between the seven points.
Mean dive depth was then calculated averaging these 11
depths (including start and end depths).
The data loggers also recorded water temperatures on
selected dives. In each of these dives, 12 coordinate pairsof pressure and temperature were obtained. The temperature sensor in the data logger has long-term stability(McMahon et al. 2005).
Samples for stable isotope analysis
Eggs of captive green turtles were collected during
nightly watches at enclosed sandy beaches adjacent tobreeding pools, which are managed by the Ogasawara
Marine Center on Chichijima Island, and the Hahajima
Fisheries Cooperative (2638¢N, 14209¢E) on Hahajima
Island, Ogasawara Islands, from late May to late July in2003 and 2004. Their body mass was measured by ﬁshermen with a hanging scale when the turtles were captured, and they were not fed while being held captive
during the nesting season. Eggs were also collectedduring nightly patrols at the natural Hatsune (300 m
length) and Kitahatsune (100 m) Beaches (2705¢N,
14214¢E) on Chichijima Island during the latter half ofJune 2004. Turtles were identiﬁed by placing tags on one
front and both rear ﬂippers, or from existing tags. Theirstraight carapace lengths were measured with calipers. A
total of 89 females (42 from breeding pools and 47 fromnatural beaches) were sampled. Green turtles lay several
clutches of eggs (about 100 eggs per clutch) during anesting season. In 2003 and 2004, they laid 800–900
clutches annually at Ogasawara Islands (Ogasawara
Marine Center, unpublished data). Since their mean
clutch frequency at the Ogasawara Islands is 4.1(Suganuma et al. 1996), the annual number of nestingfemales was estimated to be 200–220. Thus, the 89
sampled females represented 40–45% of the annual
nesting females.
One egg was collected per individual female except
for one female, which was kept in a breeding pool of the
Ogasawara Marine Center in 2003. Five eggs were collected per clutch from ﬁve serial clutches laid by this55

female in order to examine inter- and intra-clutch variation in stable isotope ratios of egg-yolks. Eggs werefrozen at 20C until analytical preparation.

Stable isotope measurements
Egg-yolks of green turtles were used for isotopic analysis. Subsamples of well-mixed yolks were dried at 60C.
Lipids were removed with a chloroform–methanol (2:1)
solution, and lipid-removed yolks were ground to a ﬁne
powder. Lipids were again removed with a chloroform–
methanol solution from the powder. Isotope ratios were
determined using a mass spectrometer (Finnigan DELTAplusXP, Thermo Electron, Mass., USA) interfacedwith an elemental analyzer (FlashEA1112, Thermo
Electron). Approximately 0.8–1.3 mg of powderedsample was used for d13C and d15N measurements. Ratios, d13C and d15N, were expressed as per mil deviations
from the standard as deﬁned by the following equation:
d13 C or d15 N ¼ ðRsample =Rstandard  1Þ  1000ð‰Þ;ð1Þ

where R is 13C/12C or 15N/14N.
Belemnite (PDB) and atmospheric nitrogen were usedas the carbon and nitrogen isotope standards, respectively. L-alanine and sodium L(+)-glutamate monohydrate standards with known isotope ratios were used forevery six or eight samples in sequence to assess theanalytical precision and correct the drift in isotope ratiosof the samples. The analytical precision was £ 0.17&
for d13C and £ 0.07& for d15N. The complete data of
isotope ratios in the samples are available as an appendix in the Electronic Supplementary Material.
During non-nesting seasons, green turtles that nest
on Ogasawara Islands inhabit two areas: coastal watersof Japan and the oceanic Paciﬁc (e.g., Tachikawa andSasaki 1990; Japan Fisheries Resource Conservation
Association 1999). In coastal waters of Japan, they feed
mainly on macroalgae (Kurata et al. 1978). Although
their diet in the oceanic Paciﬁc is unknown, they arethought to feed mainly on macroplankton, such as jellyﬁsh and salps as in other regions (Bjorndal 1997). In
general, stable isotope signatures of nearshore food webs
are highly diﬀerent from those of oﬀshore food webs
(Wu et al. 1997; Pinnegar and Polunin 2000; Brodeur
et al. 2002; Smit et al. 2005). Thus, d13C and d15N of
prey items (macroalgae, macroplankton, and also benthic animals) from or near these two areas (i.e., coastal
waters of Japan and the oceanic Paciﬁc) were cited fromliterature and compared with those of green turtle eggs
using a three-source mixing model (Phillips and Gregg
2001) in order to identify feeding habitats for the individual turtles. There are no published values for fractionation factors between isotope ratios of prey andthose of sea turtle eggs. In several avian species, fractionation factors between isotope ratios of diet andthose of lipid-free yolks were 0.1 to 0.2& for d13C and3.1 to 3.6& for d15N (Hobson 1995). These values weresimilar to generally reported values for diet-tissue fractionation in many animal species: ca. 1& for d13C
(DeNiro and Epstein 1978) and 3–4& for d15N (Minagawa and Wada 1984). Thus, 0& for d13C and 3.4&
for d15N were applied to the fractionation between isotope ratios of prey and those of sea turtle egg-yolks. In
the mixing model, proportions (with 95% conﬁdence
intervals) of food sources in a turtle’s diet were estimated. A turtle was considered to have mainly used thearea with the highest contributing prey, i.e., if thehighest contributing prey for a turtle was either macroalgae or benthic animals, the turtle would have foraged
mainly in neritic areas, and if the highest contributing
prey for a turtle was macroplankton, the turtle would
have foraged mainly in oceanic areas. Alternatively, if
the diﬀerence between proportions of prey was <10%,
the prey with smaller conﬁdence intervals was adopted
to determine the main foraging area for a turtle.

Results
Post-nesting movements
There was a highly signiﬁcant positive correlation between straight carapace length and body mass for green
turtles (r2=0.74, n=35, P<0.0001). Using the regression equation (body mass = 0.452 · straight carapace
length 293.818), the estimated body mass for turtle 1
with a carapace length of 905 mm was 115.2 kg and thatfor turtle 3 with a carapace length of 927 mm was
125.2 kg (Table 1). The carapace length and actually
measured body mass for turtle 2 were 1,068 mm and200.0 kg, and those for turtle 4 were 1,092 mm and211.0 kg (Table 1).
Four turtles were tracked for 28–42 days and thetotal distances covered were from 966 to 1,962 km(Table 1). After release, turtle 1 was located around the
Ogasawara Islands for 3 days (Fig. 1). She crossed
oceanic areas northwards for 14 days, and then wandered around neritic areas of the Izu Islands for 25 days.
Turtle 4 showed a similar migratory route (Fig. 1). She
was located around the Ogasawara Islands for 1 day
after release. She crossed oceanic areas northwards for
15 days, and then stayed at a ﬁxed neritic area of the Izu
Islands for 12 days. Turtle 2 stayed around the Ogasawara Islands for 16 days after release (Fig. 1). Since
there were long haulout records near Chichijima Island
at night on 13 and 20 August 2003 (3 and 8 h, respectively), she might have landed to nest on either day. She
then moved northwestwards, and her transmission
stopped in an oceanic area 18 days after departing fromthe Ogasawara Islands. Turtle 3 was located around the
Ogasawara Islands for 2 days after release (Fig. 1). She
crossed oceanic areas northwestwards for 19 days, andthen wandered in neritic areas south of Shikoku andKyushu for 12 days. Percentages of the days during
which turtles 1–4 swam in oceanic areas were 33.3, 52.9,
57.6, and 53.6%, respectively.

56
Fig. 1 Post-nesting migratoryroutes of four green turtles(Chelonia mydas) tracked bysatellite from the Ogasawara
Islands, Japan. Contour line
200 m depth. Inset a schematic
map of post-nesting migratoryroutes of seven green turtles
tracked by satellite from theOgasawara Islands during
1994–1998 (Japan Fisheries
Resource Conservation
Association 1999). Broken lines
indicate the periods during
which transmissions were notreceived

Post-nesting diving behavior
Dive data during oceanic swimming periods for the four
turtles were analyzed (14–19 days; Table 1). Totals of
152, 140, 70, and 28 dives were obtained from turtles 1
to 4, respectively, and within those dives, totals of 142,
122, 51, and 24 dive proﬁles were obtained (Fig. 2).
Most of their maximum dive depths were <80 m andtheir dive durations were <50 min (Fig. 3). The maximum dive depths for turtles 2 and 3 were greater thanthose for turtles 1 and 4 (Fig. 3). Diﬀerences in divedepth distributions among turtles were clearer in mean
depth. Turtles 1 and 4 seldom showed mean dive depths
greater than 25 m, whereas turtles 2 and 3 frequently
showed mean dive depths greater than 25 m (Fig. 3).
The percentages of dives with a mean depth greater than
25 m were 4.2, 10.7, 49.0, and 4.2% for turtles 1–4,
respectively.
The time spent diving deeper than 2 m increased atnight and decreased in the day for turtles 1, 2, and 3(Fig. 4), while the pattern was not clear for turtle 4 due
to a small sample size. All four turtles showed deeper
dives at night than in the day (Fig. 4). At night, most of
the mean dive depths of turtle 1 were <20 m, while
those of turtles 2 and 3 were >20 m (Fig. 4). The trend
in mean nighttime dive depths for turtle 4 was unclear
because of the small sample size. The means (±SD) of
the mean dive depths at night (the dives starting during 1900–0459 hours Japan Standard Time) for turtles
1 and 4 were 18.5±2.7 (n=81) and 19.6±1.8 m (n=14),
respectively, while the means for turtles 2 and 3 were21.3±3.0 (n=69) and 24.8±2.7 m (n=41), respectively.
The body sizes of turtles were not related to their diving
behaviors.
Water temperatures during oceanic swimming periods were obtained only from turtles 1 and 2 (in 14 and

16 dives, respectively). The mean (±SD) water temperature experienced by turtle 1 was 26.9±3.8 C (n=168),
while that for turtle 2 was 28.4±1.2C (n=192).
Stable isotope ratios in green turtle egg-yolks
The d13C in egg-yolks were not signiﬁcantly diﬀerent
among the ﬁve serial clutches (ﬁve eggs per clutch) from
one turtle (one-way repeated measures ANOVA;
P=0.16), although the d15N were signiﬁcantly diﬀerent
and increased with the clutch order (one-way repeatedmeasures ANOVA; P<0.001) (Table 2). The diﬀerence
in mean d15N between the ﬁrst and last clutches was
0.9&. We have no explanation for the signiﬁcantenrichment in d15N among clutches from the green turtle. In a loggerhead turtle, there was no similar trend in
d15N among clutches (Hatase et al. 2002). Signiﬁcantenrichment in d15N has been reported in several tissues(such as liver and muscle) of non-fed animals (Hobson
et al. 1993; Doucett et al. 1999). However, because
vitellogenesis of sea turtles is thought to be completed
prior to the mating period when turtles presumably start
to fast (Rostal et al. 1998), the observed enrichment in
d15N among clutches from a green turtle would not be
attributable to nutritional stress from fasting. A larger
sample size is needed to verify whether signiﬁcantenrichment in d15N among clutches is a general tendency
in sea turtles.
The standard deviations of the isotopic values for theﬁve eggs within each clutch were small (d13C, 0.0–0.1&;
d15N, 0.1–0.2&; Table 2). In addition, the standard
deviations of the isotopic values for a total of 25 eggs
were also small (d13C, 0.1&; d15N, 0.3&, Table 2).
Thus, a single egg-yolk from any clutch in a nestingseason could be used to represent the d13C and d15N of a

57

(a)

(b)

Fig. 2 Examples of dive proﬁles from two green turtles. Symbols
are the start and end points (2 m depths) and the ﬁve mostsigniﬁcant inﬂection points. a Data from turtle 1 collected on 26
August 2003. The maximum and mean depths were 35 and 16.4 m,
respectively. This proﬁle has a gradual ascent phase between 2112
and 2128 hours Japan Standard Time. b Data from turtle 2
collected on 3 September 2003. The maximum and mean depths
were 41 and 28.4 m, respectively

nesting green turtle. For the turtle used to compare
clutches, the mean d13C and d15N of its 25 eggs wereused in the following analysis.
The straight carapace lengths of 89 female turtles
whose eggs were sampled for d13C and d15N ranged from
871 to 1,092 mm (Fig. 5). For statistical analysis,
they were divided into 4 size groups: <900 mm (n=6),
900–950 mm (n=35), 950–1,000 mm (n=39), and‡1,000 mm (n=9) straight carapace length. The d13C of
the 89 green turtles varied from 23.1 to 11.4&, while
their d15N varied from 6.6 to 14.2& (Fig. 6a). The mean(±SD) d13C values in the four size groups from small tolarge were 16.7±3.3, 17.5±1.0, 17.7±1.0, and18.5±1.9, respectively, whereas the mean d15N values
in these groups were 10.2±2.1, 9.3±1.7, 9.4±1.3, and
9.9±1.7&, respectively. There were no signiﬁcant differences in both isotopic values among groups (Kruskal–
Wallis test; d13C, P=0.18: d15N, P=0.48; Fig. 6a). No
signiﬁcant correlation was found between d13C and d15Nof all females (Spearman’s rank correlation=0.14,
n=89, P=0.19; Fig. 6a).
Comparison between isotope ratios of prey items
and green turtle eggs
The mean (±SD) d13C of many macroalgae species incoastal waters of Taiwan was 16.8±4.3& (n=33:

Wang and Yeh 2003), and the mean d13C of somemacroplankton and many benthic animal species around
Japan was 18.5±1.6& (n=11) and 15.0±1.3&(n=120), respectively (Hatase et al. 2002). The d13C ofthe three prey groups overlapped somewhat with eachother (Fig. 6b). The mean (±SD) d15N of two macroalgae species-groups in coastal waters of Japan was
3.9±1.6& (n=155: Umezawa et al. 2002), and the mean
d15N of some macroplankton and many benthic animal
species around Japan was 9.4±2.2& (n=11) and10.9±1.4& (n=120), respectively (Hatase et al. 2002).
The d15N of the three prey groups were distinct(Fig. 6b). There were signiﬁcant correlations between
d13C and d15N in both macroplankton and benthic
animals (macroplankton: r=0.91, n=11, P <0.0001;
benthic animals: r=0.23, n=120, P<0.05), and these
correlations were incorporated into a three-source mixing model (Phillips and Gregg 2001).
Using the mixing model, it was estimated that, among
the 89 adult female green turtles, 56 turtles foraged
mainly on macroalgae in neritic areas, 28 on macroplankton in oceanic areas, and 5 on benthic animals in
neritic areas (Fig. 6b). Mean (±SE) proportions (with
95% conﬁdence intervals) of the three prey items(macroalgae, macroplankton, and benthic animals) for
the 56 turtles (neritic herbivores) were 73.4±6.3%(60.9–85.9%), 30.8±19.1% (0–69.3%), and 4.2±
15.1% (0–26.2%), respectively. Those for the 28 turtles(oceanic planktivores) were 36.2±13.2% (9.6–62.9%),84.2±21.9% (40.5–100%), and 20.5±17.9% (0–15.3%), respectively. Those for the ﬁve turtles (neritic
carnivores) were 42.7±15.4% (5.1–80.2%), 19.1±
34.1% (0–68.6%), and 76.4±27.1% (6.9–100%),
respectively. There were no signiﬁcant diﬀerences instraight carapace length among the three groups(Kruskal–Wallis test: P=0.58). These data suggested
that 69% of the green turtles nesting on the Ogasawara
Islands mainly used neritic habitats and 31% mainly
used oceanic habitats.
The d13C and d15N for satellite-tracked females wereas follows: 17.7 and 8.3& for turtle 1, 18.4 and
11.4& for turtle 2, 17.3 and 11.4& for turtle 3, and18.2 and 9.3& for turtle 4 (Table 1). In the mixing
model, turtles 1 and 4 that showed shallow dives inoceanic areas and migrated into neritic areas were inferred to be neritic herbivores, while turtles 2 and 3 thatshowed deeper dives in oceanic areas were inferred to beoceanic planktivores, although turtle 3 migrated into
neritic areas.

Discussion
This study provided some evidence that adult female
green turtles, which have been thought to be obligate
herbivores in neritic areas, also used oceanic areas as
their feeding habitats. Intrapopulational variation inhabitat use is widely reported in many animal species
from invertebrates to higher vertebrates. In some

58
Fig. 3 Relationships between
maximum dive depth and dive
duration (left) and between
mean dive depth and dive
duration (right) for four green
turtles during oceanicswimming periods. Mean divedepth is the mean of 11 depth
values in a dive proﬁle whose
maximum depth was deeper
than 10 m

marine birds and mammals that exhibit long-distancemigration, habitats are diﬀerent by age and sex (e.g.,
Minami and Ogi 1997; Burton and Koch 1999;

Le Boeuf et al. 2000). In sea turtles, most studies are
conducted on adult females that land to nest, and thegeneralization of their behavior and ecology at sea has

59
Fig. 4 Left the time spent
diving deeper than 2 m in eachhour throughout the day (opencircle) and night (ﬁlled circle)
for four green turtles during
oceanic swimming periods.
Right the mean of mean divedepths in each hour of the day
for the turtles. Error bars show
standard deviations. Numbers
below symbols are sample sizes.
Some hours lack data

long been challenging due to the diﬃculty in obtaining
information about them. However, recent technologicaladvances in telemetry and simultaneous use of several
methods have made it possible to elucidate their feeding habitat use.

Post-nesting movements and feeding habits
Satellite telemetry recently conducted in Japan has
suggested that green turtles may not be obligate herbivores in neritic areas. The Japan Fisheries Resource

60
Table 2 The sample sizes (n)and intra- and inter-clutch
variation in stable isotope ratios of egg-yolks laid by a green
turtleValues are means±SD.
Ranges are also shown inparentheses

Clutch ordernd13C (&)

d15N (&)

1st
2nd
3rd
4th
5th
Total

5
5
5
5
5
25

18.3±0.1 (18.5 to 18.1)
18.4±0.0 (18.4 to 18.3)
18.4±0.1 (18.5 to 18.3)
18.4±0.1 (18.7 to 18.3)
18.3±0.0 (18.4 to 18.3)
18.4±0.1 (18.7 to 18.1)

10.9±0.2 (10.8 to 11.1)
11.2±0.1 (11.1 to 11.3)
11.3±0.1 (11.2 to 11.4)
11.5±0.1 (11.4 to 11.6)
11.8±0.1 (11.7 to 11.9)
11.4±0.3 (10.8 to 11.9)

Fig. 5 Size distribution of 89 adult female green turtles whose eggs
were collected at the Ogasawara Islands, Japan

Conservation Association (1999) tracked seven adultfemale green turtles by satellite from Ogasawara Islands during post-nesting seasons and reported thatfour turtles moved into neritic areas south of Honshu,
Shikoku, and Kyushu, whereas one turtle wandered inoceanic areas, temporarily approaching neritic areas(transmissions from two other turtles stopped in oceanic areas) (Fig. 1). Dive data were not available inthese ﬁndings, but the oceanic wandering turtle wastracked for 8 months. After release, the turtle stayedaround the Ogasawara Islands for 1 month, and thenwandered in oceanic areas for 2 months. After that,the turtle was located around the Izu Islands for
2 months, and then she wandered again in oceanic
waters for 3 months. In addition, it has been revealed
that oceanic areas are alternative feeding habitats for
adult female loggerhead turtles, which had been considered to be obligate carnivores in neritic areas (Hatase et al. 2002). The life history pattern for bothgreen and loggerhead turtles has been considered to be
the same, with immature turtles developing in oceanic
areas during their early life history stages and thenlater recruiting to neritic areas (Type 2: Bolten 2003).
These ﬁndings suggest that adult female green turtles
also use oceanic areas as their alternative feeding
habitats.

Simultaneous use of indirect and direct methods enables the feeding habitats of green turtles to be identiﬁed
quantitatively. Stable isotope analysis provides information on pre-nesting foraging areas of turtles and satellite telemetry provides information on their postnesting foraging areas. In this study, there was large
variation in both d13C and d15N in the egg-yolks ofgreen turtles, which can be compared to the d13C
and d15N values in various potential prey items. Using athree-source mixing model, it was estimated that 69% of
green turtles nesting on Ogasawara Islands mainly usedneritic habitats and 31% mainly used oceanic habitats.
It was particularly unexpected that a few turtles were
estimated to have foraged mainly on benthic animals in
neritic areas, although a similar possibility of selective
feeding on animal matter by green turtles was reported
in the Mediterranean (Godley et al. 1998). The postnesting movements of green turtles tracked by satellite
were not completely consistent with these inferences.
Although turtles 1 and 4 that were inferred from isotope
ratios to be neritic herbivores did indeed migrate into
neritic habitats, out of the two turtles inferred to beoceanic planktivores, turtle 3 also migrated into neritic
areas. This inconsistency may be attributed to the short
tracking durations, i.e., turtle 3 may have come back tooceanic areas after temporarily approaching neritic
areas like a turtle in a previous study (Japan Fisheries
Resource Conservation Association 1999; Fig. 1).
Otherwise, this might imply that there are some turtles
that change their main foraging areas between seasons.
To improve the conﬁdence of estimates from stable
isotope analysis, feeding habits of wild turtles should be
examined more thoroughly using conventional gut
content analysis, and the diet-tissue fractionation factors
for turtles should be determined by captive feeding
experiments in future studies. In addition, isotope ratios
of long-term satellite-tracked turtles that would remigrate to nest after several years should be measured andcompared with their pre-nesting movements and diving
behavior.
Diving behaviors and feeding habits
The diving behaviors of green turtles during oceanicswimming periods were consistent with the inferencesfrom stable isotope analysis in the present study. The
two turtles that were inferred to be neritic herbivores
from their isotope ratios showed shallow dives, whileother two that were inferred to be oceanic planktivores

61

(a)

(b)

Fig. 6 The d13C-d15N maps for green turtle egg-yolks and prey
items. a Sizes (straight carapace lengths) of individual females thatlaid the eggs: open triangle <900 mm, open circle 900–950 mm,
ﬁlled diamond 950–1,000 mm, and ﬁlled square ‡1000 mm.
b Groups that were divided by main prey in a three-source mixing
model: open square neritic herbivore, ﬁlled triangle oceanicplanktivore, and inverted triangle neritic carnivore. Values for prey
items (large symbols) are means±SD. The values are cited fromliterature (macroplankton and benthic animals: Hatase et al. 2002;
macroalgae: Umezawa et al. 2002 and Wang and Yeh 2003)

showed deep dives. Adult female green turtles around
Ascension Island in the mid-Atlantic had a range ofmean dive depths (excluding shallow dives) that were
between 13.1 and 20.6 m during their oceanic migration(Hays et al. 2001). Because Ascension Island green turtles can attain neutral buoyancy within this range(maximum 17–20 m; Hays et al. 2000, 2004b), themain function of these dives was considered to be resting (Hays et al. 2001; although there might be otherfunctions in these dives: Hays et al. 2004c). These diveswere conducted mainly at night (Hays et al. 2001), andin the present study, a longer time was spent making
nighttime dives. Although the maximum depth of neutral buoyancy might change with body size in sea turtles(Hays et al. 2004b), the body sizes of satellite-tracked
green turtles in this study (115–211 kg) were similar to
those of green turtles at Ascension Island (130–225 kg:
Hays et al. 2000), suggesting that green turtles at Ogasawara Islands could attain neutral buoyancy within thesame range. In fact, the depths of resting dives (U-dives)for green turtles (n=6; estimated body mass 105.8–
161.3 kg) at the Ogasawara Islands during internesting
periods almost never exceeded 20 m, and most of thosewere <15 m (Sato et al. 1998; Japan Fisheries Resource
Conservation Association 1999). Furthermore, althoughwater temperature aﬀects buoyancy (i.e., cooler temperature induces larger buoyancy, possibly leading togreater depth of neutral buoyancy, and vice versa), differences in water temperatures experienced by turtles
between Ogasawara Islands and Ascension Island were
not very large (Hays et al. 2002), supporting the above
suggestion. There was also no observation of a turtle
that had experienced lower temperatures showing deeper
dives than a turtle that had experienced higher temperatures in the present study. The mean of nighttime mean
dive depths (18.5 and 19.6 m) for turtles 1 and 4, whichwere inferred to be neritic herbivores from their isotope
ratios, was similar to that of Ascension Island green
turtles. These turtles are thus considered to have mainly
rested at night. However, the mean of nighttime mean
dive depths (21.3 and 24.8 m) for turtles 2 and 3, whichwere inferred to be oceanic planktivores, was beyond
that of Ascension Island green turtles, implying that thefunction of nighttime dives for these turtles was not justresting. They may have foraged on zooplankton thatexhibit diel vertical migrations, which occur near thesurface at night and much deeper than turtles’ range ofdives during the day (Nishikawa et al. 2001), as doleatherback turtles (Dermochelys coriacea) that are specialized predators of gelatinous zooplankton in oceanic
areas (Hays et al. 2004a). Similar foraging and diving
behaviors in response to the vertical distribution of prey
have often been reported in other marine animals suchas penguins and seals (e.g., Wilson et al. 1993; Horning
and Trillmich 1999). In addition, recent satellite telemetry of post-nesting movements and diving behavior bysome adult female green turtles around Costa Rica
similarly showed evidence of potential oceanic foraging(Troëng et al. 2005).
There is some indication that variation in prey quality
might cause body size variation within populations ofadult female sea turtles. Adult female loggerhead turtles
used diﬀerent feeding habitats as a function of body sizearound Japan (Hatase et al. 2002), with small females
mainly using oceanic habitats and large females mainly
using neritic habitats. It was suggested that nutritional
diﬀerences in their main prey (macroplankton vs benthic
animals) between the habitats were related to this62

phenomenon (Hatase et al. 2002). Satellite telemetry andstable isotope analysis in the present study did not show
similar trends in the use of feeding habitats (neritic vsoceanic) by green turtles, implying that nutritional differences in their main prey (macroalgae vs macroplankton) between the habitats might not be large
enough to inﬂuence the body size of adult female green
turtles.
Possible mechanisms behind individual variationin feeding habitat use
Why do some adult female green turtles mainly use
oceanic habitats and others mainly use neritic habitats?
We speculate that variation in ontogenetic habitat shifts
by turtles may be related to this phenomenon. Alljuvenile Atlantic loggerhead turtles are considered toleave oceanic habitats and move to neritic habitats when
their growth rates begin to slow (Bolten 2003). Given therelatively large size of juvenile sea turtles, diﬀerences inmortality (predation) risk between the habitats may be
negligible. If the main function of habitat shifts by
juvenile sea turtles is to maximize growth rates, turtles
that do not shift habitats should be the turtles that haveundergone better growth in previous (i.e., oceanic)
habitats. However, Atlantic loggerheads are considered
to compensate for early bad growth, lessening the individual variation in growth rates during oceanic stages(Bjorndal et al. 2003). Individuals that have undergone
compensatory growth may incur a variety of costs(Metcalfe and Monaghan 2001). Although, at present, it
is not known whether there are some turtles that do notshift habitats in the Atlantic, turtles that have undergone
compensatory growth in the Atlantic might not be able
to grow and prepare for reproduction unless they recruit
to neritic habitats and shift diets, while those that havenot undergone compensatory growth might be able togrow and still reach sexual maturity in oceanic habitats.
It is also not known whether Paciﬁc turtles undergo
compensatory growth during oceanic stages. In the Paciﬁc, however, food availability early in life might have adisproportionate eﬀect on an individual’s later growthtrajectory (silver spoon eﬀect: Grafen 1988; Madsen andShine 2000), as has been speculated in Japanese loggerheads (Hatase et al. 2004). In this case, turtles that haveundergone better growth in oceanic habitats continue to
use the habitats throughout their lives, while turtles withbad growth in oceanic habitats leave them and move toneritic habitats in order to maximize growth rates andprepare for reproduction (at a size of 300–400 mm
straight carapace length in Japanese green turtles: Miyawaki 1994). Habitats where turtles have grown might
be imprinted and this might aﬀect habitat selection
throughout their lives (Limpus and Limpus 2001).
Similar individual variation in feeding habitat use
was reported by satellite telemetry in adult female
hawksbill turtles (Eretmochelys imbricata) (Japan Fisheries Resource Conservation Association 1999), whichhave been considered to possess the same life history
pattern as loggerhead and green turtles (Type 2: Bolten2003). Out of eight female hawksbills released fromwaters oﬀ Okinawajima (2636¢N, 12748¢E), Japan, six
females moved into neritic waters, while two females
wandered in oceanic waters during almost the whole
tracking periods (3 and 9 months, respectively) (Japan
Fisheries Resource Conservation Association 1999). It istherefore suggested that ontogenetic habitat shifts by sea
turtles (at least Type 2 species) are facultative, andconsequently, their life histories are polymorphic. Future research must address how alternative life histories
are maintained in a population, i.e. (1) whether alternative life histories have a genetic basis, and (2) whether
there are diﬀerences in ﬁtness between alternative life
histories. Solving these questions will help in understanding how sea turtles have survived and adapted tothe marine environment during their evolutionary history of >110 million years (Hirayama 1998).
Acknowledgements We thank H. Suganuma and K. Narushima ofEverlasting Nature of Asia (ELNA), the staﬀ (Y. Iwata, Y. Horita,
and M. Ogasawara) and volunteers of the Ogasawara Marine
Center, M. Kaneko and the staﬀ of the Club Noah Hahajima, andthe ﬁshermen of Chichijima and Hahajima Islands, for ﬁeld assistance and logistical support. We also thank the Sea Turtle Association of Japan for supplying tags and equipment, and
Y. Matsuzawa for discussion. T. Miyajima and Y. Umezawa of the
Biogeochemistry Laboratory, Ocean Research Institute, Universityof Tokyo, assisted with the stable isotope analysis and allowed us
to use their mass spectrometer. G.C. Hays provided useful advice
on attachment of the transmitter and data analysis. M.J. Miller
helped to improve the manuscript. Figure 1 was created by the
Maptool at http://www.seaturtle.org. Two anonymous referees
provided constructive comments on the manuscript. This work waspartly supported by a Grant-in-Aid from the Japanese Society for
the Promotion of Science (No. 15255003) to K.S. and a Grant-inAid for Creative Scientiﬁc Research (No. 12NP0201) from the
Ministry of Education, Culture, Sports, Science and Technology ofJapan to K.T. The experiments were conducted under licenses
issued by the Ministry of the Environment and complied withthe current Japanese laws.

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