Journal of Experimental Marine Biology and Ecology 501 (2018) 36–45

Contents lists available at ScienceDirect

Journal of Experimental Marine Biology and Ecology

journal homepage: www.elsevier.com/locate/jembe

Pre and post-settlement movements of juvenile green turtles in the T

Southwestern Atlantic Ocean
⁎
Vélez-Rubio G.M.a,b,c, , Cardona L.d, López-Mendilaharsu M.a,e, Martinez Souza G.f,
Carranza A.c,g, Campos P.d, González-Paredes D.a,h, Tomás J.b
a
Karumbé NGO, Av. Rivera 3245, C.P.11600 Montevideo, Uruguay
b
Marine Zoology Unit, Cavanilles Institute of Biodiversity and Evolutionary Biology (ICBIBE), University of Valencia, Aptdo. 22085, E-46071, Valencia, Spain
c
Centro Universitario Regional del Este (CURE), Universidad de la República, Campus de Maldonado, 20100 Punta del Este, Uruguay
d
Biodiversity Research Institute (IRBio) and Department of Evolutionary Biology, Ecology and Environmental Science, Faculty of Biology, Universitat de Barcelona, Av.
Diagonal 643, 08028 Barcelona, Spain
e
Fundação Pró Tamar, Rua Rubens Guelli, 134, sala 307, Salvador, Bahia, Brazil
f
Instituto Ciencias Biologicas, Universidade Federal do Rio Grande – FURG, CP 474 Rio Grande, RS, Brazil
g
Área Biodiversidad y Conservación, Museo Nacional de Historia Natural, C.C. 399, C.P. 11000 Montevideo, Uruguay
h
Hombre y Territorio Asociación, C/ Betania, 13, 41007 Seville, Spain

A R T I C L E I N F O A B S T R A C T

Keywords: Detailed knowledge on migratory routes connecting distant breeding, developmental and foraging areas is a key
juvenile turtles prerequisite for the successful management of marine vertebrates. The present study combines stable isotopes
Chelonia mydas analysis of carapace scutes and satellite tracking of juvenile green turtles as an experimental approach to un-
displacement derstand the pre and post settlement (recruit to neritic habitats) movements in the Southwestern Atlantic Ocean.
development feeding grounds
To this end, carapace scute biopsies were collected from 20 turtles foraging on coastal rocky outcrops in East
stable isotopes
telemetry
Uruguay and sliced in successive 30-μm layers using a cryostat. The δ15N and δ13C values of the newest layer
Uruguayan coastal waters increased significantly with turtle size and they also increased from the oldest to the newest layer in most of the
individuals. According to the regional isoscape, such a pattern was consisted with the shift from tropical, oceanic
habitats to neritic habitats in northern Brazil and the subsequent southward movement along the coast. Using
the δ15N values of the scute layers, seven turtles were considered new-settlers and 13 residents, as only the latter
had δ15N and δ13C values consistent with those of local potential prey. According to satellite tracking, some
resident turtles perform short seasonal migrations to northern Brazilian waters during the austral winter. This
behaviour is also recorded in scute layers as a small drop of δ15N values. The present study thus provides
empirical evidence supporting the hypothesis that turtles reaching 40–45 cm of curved carapace length arrive to
Uruguayan waters following a coastal migratory route along the Brazilian coast and confirms the existence of
seasonal movements between Uruguayan and South-Brazilian waters and a high fidelity for feeding grounds in
the Southwestern Atlantic Ocean.

1. Introduction impossibility of instrumenting too small juvenile individuals and the

Many marine vertebrates perform long migrations connecting dis-
tant breeding, developmental and adult foraging areas (Webster et al.,
2002). Hence, the detailed knowledge of these regular movements is
required for the successful management of those species (e.g. González-
Solís et al., 2007; Scott et al., 2012; Graham et al., 2012; López-Castro
et al., 2014). Recently, advances in biologging have increased greatly
our knowledge about those processes (Rutz and Hays, 2009; Bograd
et al., 2010; Payne et al., 2014), but the migratory routes of some
species still remain largely unknown, in part because of the
incapacity of retrieving archival tags from juveniles engaged in multi-
year dispersal.
Stable isotope ratios in tissues such as feathers, whiskers, carapace
scutes, dentine and bones provide an alternative approach to re-
construct ontogenetic changes in diet and habitat, although resolution
is often coarse (e.g. Hobson and Sease, 1998; Hobson and Schell, 1998;
Reich et al., 2007; Newland et al., 2011; Borrell et al., 2013;
Tomaszewicz et al., 2017). The basic assumptions of this method are (1)
that stable isotope ratios in animal tissues integrate those in diet, plus a
trophic discrimination factor that is tissue, diet and taxa specific (Caut

⁎
Corresponding author at: Karumbé NGO, Av. Rivera 3245, C.P.11600 Montevideo, Uruguay.
E-mail address: gabriela.velez@uv.es (G.M. Vélez-Rubio).

https://doi.org/10.1016/j.jembe.2018.01.001
Received 1 August 2017; Received in revised form 27 November 2017; Accepted 8 January 2018
0022-0981/ © 2018 Elsevier B.V. All rights reserved.
G.M. Vélez-Rubio et al.
et al., 2008); (2) that metabolically inert tissues represent a consumer's
diet at the time of deposition and hence these tissues can be used as a
timeline of the consumer's isotopic history; and (3) that variations of
stable isotope ratios across habitats (isoscapes) are known (Bowen,
2010; Graham et al., 2010; Somes et al., 2010; Maggozi et al., 2017).
The applications of stable isotope analysis (SIA) in marine ecosystems
have increased substantially in recent decades as analytical cost has
decreased, the capabilities of laboratories and the statistical meth-
odologies for interpretation of isotopic data have improved and become
more accessible for non-specialized researchers (Jackson et al., 2011;
Layman et al., 2012; Navarro et al., 2013).
Most cheloniid turtles have complex life cycles encompassing huge
areas across entire oceans and involving both neritic and oceanic ha-
bitats (Bolten, 2003; Meylan et al., 2011). Early juveniles are typically
oceanic and usually recruit to neritic habitats after a few years, which
results into the spatial separation between juveniles and adults, some-
thing rather unusual in animals with direct development (Congdon
et al., 1992; Meylan et al., 2011). Available evidence indicates that
juvenile cheloniid turtles have some control of their movements
(Lohmann et al., 2001; Mansfield et al., 2014; Putman and Mansfield,
2015; Briscoe et al., 2016), but their tracks largely agree with those of
major currents, which in turn determine the migratory routes they will
latter follow as adults (Scott et al., 2014a; Cardona and Hays, 2018).
The green turtle, Chelonia mydas, is a circumglobal species occurring
throughout tropical and to subtropical waters throughout the world's
oceans (Seminoff et al., 2003). The migratory movements of adult fe-
males are relatively well known worldwide thanks to satellite telemetry
and passive tagging (Luschi et al., 1998; Broderick et al., 2007; Troëng
et al., 2005; Seminoff et al., 2008; Stokes et al., 2015; Christiansen
et al., 2017). Conversely, most of our knowledge about the early years
of life of green turtles has been inferred through oceanographic mod-
eling (Monzón-Argüello et al., 2010; Putman and Naro-Maciel, 2013;
Scott et al., 2014a) and changes in the stable isotope ratios of C, N and S
across the layers of carapace scute (Reich et al., 2007; Cardona et al.,
2009, 2010; Vander Zanden et al., 2013) although juveniles have also
been satellite-tracked (Gonzalez Carman et al., 2012; Putman and
Mansfield, 2015; Williard et al., 2017). The keratinous tissue of car-
apace scutes is inert, grows continuously and scute layers offer a record
of several intrinsic biomarkers such as metal levels and stable isotope
ratios of C and N (Alibardi, 2005; Reich et al., 2007, 2008; Hobson,
2008; López-Castro et al., 2013, 2014). Moreover, scutes can be sam-
pled from live turtles more easily than other tissues.
The relative abundance of light and heavy isotopes of carbon (C),
reported as δ13C, is widely used as a habitat marker (e.g. Cardona et al.,
2009, 2010) and provides information on foraging strategies and
feeding locations (Newsome et al., 2010; De Niro and Epstein, 1978;
Drago et al., 2016); for example, to identify oceanic or neritic feeding
habits (e.g. Reich et al., 2007; Eder et al., 2012). On the other hand, the
relative abundance of light and heavy isotopes of nitrogen (N), reported
as δ15N, is widely used to asses trophic level (e.g. Cardona et al., 2009)
but can also be used as a habitat marker at a basin scale (e.g. Cardona
et al., 2014).
Ascension Island (UK overseas territory, Fig. 1) is the main nesting
rookery for the green turtle in the South Atlantic Ocean (Weber et al.,
2014 and references therein) and the source of most green turtles in
foraging aggregations in the Southwestern Atlantic (SWA hereafter)
(Caraccio, 2008; Monzón-Argüello et al., 2010; Naro-Maciel et al.,
2012; Proietti et al., 2012; Prosdocimi et al., 2012). Virtual particle
drifting experiments and studies based on Lagrangian drifters suggest
that hatchlings from Ascension would drift westward directly to the
coast of Brazil (close to latitude 10°S) in less than one year and then will
move southward, reaching Uruguay (latitude 33°S) in < 4 years
(Putman and Naro-Maciel, 2013; Scott et al., 2014a). The second largest
rookery in the South Atlantic Ocean is Trindade Island (Fig. 1), closer to
the Brazilian coast, with clearly favorable ocean currents for turtles to
arrive to the feeding grounds of South Brazil, Uruguay and Argentina
37
Journal of Experimental Marine Biology and Ecology 501 (2018) 36–45
(Proietti et al., 2012), although actual tracking data are lacking.
The values of δ15Nplankton in the SWAO are known to decrease as
much as 5‰ eastward from Ascension Island (7°56′S 14°22′W) to
Paraiba (Brazil, 7°09′S 36°49′W) and then increase as much as 4‰
southward from Paraiba to Uruguay (33°44′S 53°21′W) (Somes et al.,
2010; Navarro et al., 2013). Hence, the δ15N values of the carapace
scutes of green turtles would offer a good method to validate the above-
proposed migratory route for early juvenile green turtles in the SWAO
(Fig. 2), as far as they are not confounded by changes in δ15N associated
to the ontogenetic dietary shift (Vélez-Rubio et al., 2016). The same
approach, combined with satellite telemetry, should allow detecting
seasonal movements and provide insights into the overwintering
strategy of juvenile green turtles feeding in Uruguayan waters. This is
critical, because green turtles inhabiting temperate regions may suffer
hypothermic stunning in winter unless they migrate to warmer waters
(Broderick et al., 2007), move to oceanic waters or perform a bruma-
tion strategy (Vélez-Rubio et al., 2016; Vélez-Rubio et al., 2017).
In this context, the objectives of the present study are 1) to test the
hypothesis that most juvenile turtles disperse from Ascension Island to
Uruguay moving along the coastal waters of Brazil, 2) to assess the size
when juvenile greens settle in the coastal waters of Uruguay and 3) to
describe the seasonal migrations between Uruguay and Brazil.
2. Material and methods
2.1. Study site
The Uruguayan coast (710 km length) is part of a complex hydro-
logical system comprising the frontal zone of the Rio de la Plata estuary
and the Atlantic Ocean (Fig. 1), with a prevalence of the Malvinas/
Falkland current during the austral winter and the Brazilian current
during the austral summer (Garcia, 1998; Ortega and Martínez, 2007).
This causes variations of > 15 °C in sea surface temperature (range
10–27 °C) throughout the year (Acha et al., 2004). The coastline is a
succession of sandy beaches separated by rocky outcrops rich in mussels
and macroalgae (see e.g. Borthagaray and Carranza, 2007; Gónzalez-
Etchebehere et al., 2017). Juvenile green turtles are found within the
whole area, but the major foraging grounds are located in the rocky
outcrops at Canelones, Maldonado and Rocha Departments (López-
Mendilaharsu et al., 2006; Vélez-Rubio et al., 2013).
2.2. Turtle capture, sample collection and sample processing
Green turtles were captured by the local NGO Karumbé as part of a
long-term study on the abundance and habitat use of green turtles in the
east coast of Uruguay, mainly in two coastal-marine protected areas
(CMPA), Cerro Verde e Islas de La Coronilla and Cabo Polonio (Fig. 1).
Turtles were captured alive while feeding over rocky and sandy bot-
toms < 5 m deep. Set nets (nylon monofilament, 50 m length × 3 m
depth, 30 cm stretched mesh size) were deployed perpendicular to wave
direction and were monitored constantly to avoid turtle drowning (see
Martinez Souza, 2014 for more details of the capture methodology).
Curved Carapace Length (CCL notch to tip) was measured for each
turtle using a flexible tape (error = 0.1 cm) and all turtles were tagged
with Inconel flipper tags before release. All turtles captured were in
good condition after sampling and tagging and were released at the site
of capture.
Carapace samples were collected from 20 juvenile green turtles in
CMPAs of Cerro Verde and Cabo Polonio and adjacent areas of Rocha
Department, from January to April in 2012 and 2013. We selected this
period because these are the months with higher number of green
turtles in the study area (Vélez-Rubio et al., 2013; López-Mendilaharsu
et al., 2016). Biopsies were collected from the posterior medial region
of the third left lateral scute of each individual, close to the posterior
margin using a 6-mm diameter Miltex biopsy punch (Fig. 2), following
Reich et al. (2007). Only the biopsy samples going all the way through
G.M. Vélez-Rubio et al. Journal of Experimental Marine Biology and Ecology 501 (2018) 36–45

Fig. 1. The Southwestern Atlantic Ocean (SWAO) and the study area. A: Major currents in SWAO: Ecuatorial Current (SEC), Brazilian Current (BrC), and Malvinas Current (MC). Nesting
areas of green turtles in the region are shown by stars. B: Map of the Uruguayan coast with the three sections (inner estuarine influence zone, outer estuarine influence zone, oceanic
influence zone). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

the scute and reaching the innermost layer were used.
According to dietary studies, green turtles off Uruguay rely pri-
marily on several species of Ulva complex and Chondracanthus teedei
(Vélez-Rubio et al., 2016). To assess the existence of the latitudinal
gradient in δ15N suggested by Somes et al. (2010) and Navarro et al.
(2013), five samples of Ulva spp. and C. teedei were collected at four
sites along the potential coastal migratory route from Ascension Island
to Uruguay: Praia do Forte (northern Brazil), Ubatuba (Central Brazil),
Florianopolis (Southern Brazil) and Punta del Diablo (Northeast Ur-
uguay).
All samples were stored and preserved in NaCl until processing
(Barrow et al., 2008).

38
G.M. Vélez-Rubio et al.
Fig. 2. A: Schematic representation of carapace scute sampling and, B: expected shifts in δ15N values as green turtles migrate from northern Brazil to Uruguay. (For interpretation of the
references to color in this figure legend, the reader is referred to the web version of this article.)
2.3. Stable isotope analysis
All scute samples were rinsed with deionized water in the laboratory
prior to analysis. Each sample was embedded in O.C.T. (Optimal
Cutting Temperature compound, Tissue-Teck®) with the dorsal side
(oldest tissue) down, frozen at −21 °C and subsampled in successive
30-μm layers using a cryostat (Leica Cryostat CM 3050S). Each layer
was rinsed during 24 h with deionized water and kept separately.
Previous tests confirmed that this procedure left no O.C.T. traces and
did not modify the stable isotope ratios of C or N. Samples were dried at
60 °C for three days and lipids extracted with a chloroform/methanol
(2:1) solution (Bligh and Dyer 1959). Lipids are depleted in 13C in
comparison with other molecules, which could bias δ13C values if lipid
proportions were not constant (De Niro and Epstein, 1978). After lipid
removal, the C:N ratio of scute layers ranged 3.1–3.5 (see Supplemen-
tary material), thus confirming that lipids had been removed efficiently.
The number of layers obtained was proportional to the scute
thickness, which varied individually. As scute grows outward, the
oldest tissue is sloughed off and replaced by the youngest layers mi-
grating from the innermost section of the scute (Alibardi, 2005). Ac-
cording to previous studies (Reich et al., 2007; Cardona et al., 2010;
Vander Zanden et al., 2013) we estimated that each 30-μm-thick layer
integrated 54 days, although this should be considered a coarse esti-
mate because the growth rate might decline with age (Bjorndal et al.,
2017). Each layer was analyzed independently for the stable isotope
ratios of carbon and nitrogen. Samples were weighed into tin cups with
a microbalance (approximately 0.3 mg of sample), combusted at
1000 °C, and analyzed in continuous flow isotope ratio mass spectro-
meter (Flash 1112 IRMS Delta C Series EA; Thermo Finnigan) at the
Centres Científics i Tecnològics de la Universitat de Barcelona (Spain).
Stable isotope abundances were expressed in δ notation according
to the following expression:
δX = [(Rsample / Rstandard ) − 1] × 103
where X is 13C or 15N, Rsample is the heavy to light isotope ratio of
the sample (13C/12C or 15N/14N) respectively, and Rstandard is the heavy
to light isotope ratio of the reference standards, which were VPDB
(Vienna Pee Dee Belemnite) calcium carbonate for 13C and atmospheric
nitrogen (air) for 15N. International secondary standards of known
13
C/12C ratios, as given by the IAEA (International Atomic Energy
Agency IAEA), namely polyethylene (IAEA CH7, δ13C = −31.8‰),
graphite (IAEA USGS24, δ13C = −16.1‰) and sucrose (IAEA CH6,
δ13C = −10.4‰), were used for calibration at a precision of 0.2‰. For
nitrogen, international secondary standards of known 15N/14N ratios,
namely (NH4)2SO4 (IAEA N1, δ15N = +0.4‰ and IAEA N2,
δ15N = +20.3‰) and KNO3 (IAEA NO3, δ15N = +4.7‰), were used
to a precision of 0.3‰.
39
Journal of Experimental Marine Biology and Ecology 501 (2018) 36–45
The prey-to-consumer trophic discrimination factor (TDF) for the
scutes of green turtles has been assessed empirically by Shimada et al.
(2014) as −1.4‰ for δ13C and 2.5‰ for δ15N. Thus, any green turtle
with a δ15N value around or higher than 13.1‰ in the innermost car-
apace layer likely have foraged for at least several months in Uruguayan
coastal waters (resident), whereas any green turtle with a δ15N value
lower than 13.1‰ in the innermost scute layer was likely a recent
settler. A similar approach has been used by Madigan et al. (2014) to
reconstruct transoceanic migrations of tuna. If the δ15N values of the
scute layers decreased with distance to the scute base (Fig. 2), the turtle
was considered to have migrated southward along the coast of Brazil
(Somes et al., 2010; Navarro et al., 2013). We estimated the time of
residency in Uruguay accordingly to the number of scute layers with
δ15N values higher of 13.1‰ and a carapace growth rate of 30 μm in
54 days.
We also used the δ15N values of the innermost layer from each in-
dividual, which integrated approximately the last 54 days of its life
(Reich et al., 2007; Cardona et al., 2010; Vander Zanden et al., 2013),
to assess the approximated size when turtles would settled in Ur-
uguayan coastal waters. To do so, we used a general liner model (GLM)
with a binomial error distribution and logit link. We categorized the
turtles with 1 if they crossed the 13.1‰ threshold across the 5 inner-
most carapace layers layers and 0 to turtles not crossing that threshold.
Prior to statistical analysis, data sets were checked for normality
(Lilliefors test) and homogeneity of variances (Levene test). Non-para-
metric tests were used if those assumptions were not meet.
2.4. Satellite telemetry analysis
Three turtles were captured and satellite tagged in the CMPA of
Cerro Verde e Islas de La Coronilla in January 2007 and instrumented
with Platform Terminal Transmitters (PTT) Kiwisat 101 model
(Sirtrack). Before attaching the transmitter, each turtle was measured
and tagged with small metal Inconel tags on each to the front flippers.
Each turtle was prepared for satellite tag attachment by scrubbing the
carapace to remove epibionts, light sanding, and cleaning with acetone
The PTT was latter attached with two components epoxy resin and
covered with antifouling blue paint (Marcovaldi et al., 2010). Data
were downloaded from the ARGOS satellite system and subsequently
analyzed with the satellite tracking and analysis tool (STAT, Coyne and
Godley, 2005) to archive and filter location data. Argos locations are
assigned to different accuracy classes, called location classes [LC]. Lo-
cation classes 3, 2, 1, 0 are categorized to lie within 150 m, 150–350 m
or 350–1000 m, > 1000 m respectively of the tag's true position, while
locations classes A and B have no location error estimate. Routes were
reconstructed using high quality positions (LC 1, 2 and 3) and filtered
low quality positions (LC 0, A and B) based on maximum rate of travel
G.M. Vélez-Rubio et al. Journal of Experimental Marine Biology and Ecology 501 (2018) 36–45

of 5 km/h. To reduce the effects of spatial autocorrelation of con-
secutive positions on short time intervals, we selected for each turtle
one position every 12 h. A geographic information systems software
(ArcGis 9.3, ESRI) was used to map turtle movements and calculate
high-use areas through fixed kernel home ranges using Hawth's analysis
tools for ArcGis (Beyer, 2004). Individual core-use areas were deli-
neated using 50% kernel density utilization distributions.
3. Results
3.1. Stable isotope analysis
The δ15N mean values of macroalgae increased southward along the
coast of South America: 6.0 ± 1.9‰ in Praia do Forte (northern
Brazil), 5.8 ± 0.4‰ in Ubatuba (Central Brazil), 7.7 ± 0.2‰ in
Florianopolis (Southern Brazil) and 10.6 ± 0.9‰ in Punta del Diablo
(Northeastern Uruguay). Accordingly, the δ15N value of the innermost
layer of green turtles resident in Uruguay should be ≥13.1‰ and in-
dividuals with lower δ15N values in the innermost carapace layers
should be considered recent settlers coming from somewhere else
(Fig. 2).
The δ15N and δ13C values of the 30-μm scute layers ranged from
5.8‰ to 15.8‰, and from −19.8‰ to −14.8‰ respectively. The δ15N
and δ13C values of the innermost layer departed from normality
(Lilliefors test, δ15N p = .019, δ13C p = .023) and both increased sig-
nificantly with CCL (δ15N: Spearman Rho = 0.680, p = .001; δ13C,
Spearman Rho = 0.515, p = .020) (Table 1), as expected if turtles had
traveled southward along the coast of Brazil as their carapace layers
grew.
According to the above reported δ15N threshold value (≥13.1‰)
reported above we considered seven turtles (range: 27.8–39.4 cm CCL)
recent settlers and 13 turtles (range: 30.1–66.8 cm CCL) as residents
(Fig. 3). This hypothesis was supported by the negative correlation
between the δ15N values of the scutes layers and the distance to the
scute base in 11 turtles (Table 1). When only the five more recent scute
layers were considered, individuals with Δ15Nscute values ≥3‰ were
significantly smaller than those with lower Δ15Nscute values
(39.1 ± 9.7 vs 50.4 ± 11.8 cm CCL, t = 2.343, df = 18, p = .031).
Furthermore, the logistic analysis revealed that 45 cm CCL was the
turtle size where the probability of Δ15Nscute values ≥3‰ was 50%,
which suggests that this is the average turtle size at settlement in
Uruguay. Assuming a carapace growth rate of 30 μm in 54 days, the
resident turtles would have spent at least 162 days in Uruguayan waters
before capture, with an estimated maximum residency time of 540 days
(Table 1). However, at least five animals showed a drop in δ15N larger
than 1‰ in intermediate layers, possibly indicating seasonal move-
ments to Brazil.
The δ13C values of newly settled turtles (δ13C < −18‰) were
lower than those of resident turtles (δ13C range: −14.5‰/−18.5‰).
Furthermore, resident turtles showed a decrease in δ13C values as the
distance to the inner parte of the scute increased (Table 1).
When comparing the values of stable isotopes in the inner layer of
turtles with those of potential prey from Uruguay, two groups of turtles
emerged: new settlers and residents (Figs. 3 and 4). After correcting for
TDF, the bivariate stable isotope ratios of new settlers laid outside the
limits of the Uruguayan isospace, while those of resident turtles laid
close to that of macroalgae, thus suggesting a macroalgae-based diet.
3.2. Satellite telemetry analysis
The three satellite tagged turtles were of juvenile size (Table 2).
After release, two of them spent 5 months in CMPA of Cerro Verde (East
Uruguay) and then migrated to feeding grounds in waters of Santa
Catarina (Brazil) during the coldest months (June to August) (Fig. 5).
With the onset of austral spring, they returned to CMPA of Cerro Verde,
after 3 to 4 months out of Uruguayan waters, including the round-trip
migration (Table 2, Fig. 5). During their stay at Cerro Verde, turtle
spend most of the time around the islands and thus roughly within the
limits of the CMPA (Fig. 6). The core areas of the two turtles overlapped
largely (Fig. 6). The smallest turtle spend only 13 days at the Cerro
Verde and then moved southward to the Rio de La Plata estuary. This
turtle was found dead stranded in Mar del Plata port (Argentina)
70 days after release. One of these two turtles had been flipper tagged
previously in 2004 in CMPA of Cerro Verde, being recaptured several
times in 2004, 2007 and the last time in 2008, still with the satellite
attached although without transmitting, in an area not bigger than 50 m
distant from the place of the first capture.
We detected a slight decrease from June to November in the δ15N
values of 9 of the 14 turtles classified as resident individuals (Fig. 2),
consistent with a northward migration during the winter months, as
recorded for the former two turtles satellite tagged.

Table 1
Summary of stable isotope descriptors of the 20 green turtles (Chelonia mydas) sampled. Values correlation of the signal with de distance to the base of the scute, * indicates when
statistical significance is present.

Turtle Month CCL (cm) Layers Thickness (μ) Correlation signal with distance to the base of the Differences of extreme Days in New settler/
scute values Uruguay resident

δ13C (p-value) δ15N (p-value) δ13C (%) δ15N (%o)

A2 January 27.8 4 120 0.54 (0.45) −0.97 (0.03)* 0.3 2.0 < 54 NS
A5 April 30.4 7 210 −0.89 (0.007)* −0.97 (< 0.001)* 2.3 7.2 162–216 R
A8 March 30.1 5 150 −0.24 (0.69) −0.39 (0.51) 0.8 1.0 > 270 R
A7 March 31.0 6 180 0.74 (0.09) −0.95 (0.003)* 0.6 3.4 < 54 NS
A6 April 31.1 4 120 −0.95 (0.04)* −0.95 (0.04)* 0.9 3.1 54–108 NS
B5 April 36.2 7 210 −0.20 (0.66) 0.68 (0.09) 0.8 0.5 < 54 NS
B2 March 38.6 15 450 −0.04 (0.87) −0.31 (0.25) 1.1 1.4 < 54 NS
B4 March 39.2 6 180 0.87 (0.02)* −0.45 (0.37) 0.3 1.0 < 54 NS
B3 March 39.3 8 240 −0.98 (< 0.001)* −0.84 (0.009)* 2.5 2.2 > 432 R
B6 April 39.4 9 270 −0.76 (0.02)* −0.75 (0.02)* 0.8 3.0 < 54 NS
C3 April 45.6 16 480 −0.83 (< 0.001)* −0.69 (0.002)* 1.5 6.3 270–324 R
C4 April 45.9 8 240 −0.70 (0.05)* −0.83 (0.01)* 2.6 3.9 > 432 R
C8 January 45.9 7 210 −0.82 (0.02)* 0.15 (0.74) 0.9 0.9 > 378 R
C5 January 49.8 5 150 0.39 (0.52) 0.06 (0.92) 0.7 0.2 > 270 R
C9 January 49.3 9 270 0.34 (0.37) −0.65 (0.06) 0.5 1.3 > 486 R
D3 February 55.6 10 300 −0.07 (0.85) 0.30 (0.40) 0.4 0.6 > 540 R
D2 February 58.4 8 240 −0.50 (0.20) 0.82 (0.01)* 0.7 1.4 > 432 R
D5 January 61.5 7 210 −0.47 (0.28) 0.51 (0.24) 0.6 0.5 > 378 R
D1 January 62.0 5 150 −0.07 (0.91) 0.92 (0.02)* 2.2 1.4 > 270 R
D4 March 66.8 5 150 −0.38 (0.52) 0.39 (0.51) 0.7 0.6 > 270 R

40
G.M. Vélez-Rubio et al. Journal of Experimental Marine Biology and Ecology 501 (2018) 36–45

Fig. 3. The life history of green turtles in Uruguay recorded as variations of δ13C (A and B) and δ15N (C and D) across 30-μm carapace scute layers. New settlers: left panels (A and C),
black dots. Residents: right panels (B and D), open dots. T0: indicate the inner part of the carapace scute and integrates turtle diet 54 days before sampling. The green area shows the
region of the isoscape compatible with benthic foraging along the Brazilian coastline, the blue area that compatible with benthic foraging in Uruguay and the white area other, unknown
foraging grounds. The dotted black line corresponds to the δ15N threshold value, 13.1‰. (For interpretation of the references to color in this figure legend, the reader is referred to the
web version of this article.)

Fig. 4. δ15N-δ13C biplot showing the position of new set-

tlers (black circles) and resident green turtles (open cir-
cles) within the regional isospace of Urugay after cor-
recting for trophic discrimination factors. Potential dietary
items include macroalgae (black squares: Chondracanthus
teedei, Cryptopleura ramosa, Grateloupia cuneifolia,
Polysiphonia spp., Pterocladiella capillacea and Ulva spp.),
the jellyfish Chrysaora lactea (black triangle) and the squid
Loligo sanpaulensis (black diamond). Note that new settlers
lay outside the Uruguayan potential prey mixing polygon
(red dotted polygon). (For interpretation of the references
to color in this figure legend, the reader is referred to the
web version of this article.)

4. Discussion in turtle size at settlement on neritic habitats in the region and a high
fidelity to feeding grounds after settlement, although at least some in-
The results presented here are consistent with the hypothesis that dividuals overwintered in southern Brazil.
green turtles occurring in Uruguay have dispersed previously along the
coast of Brazil and not recruited directly from oceanic foraging grounds
at latitude 34°S. They also revealed a high level of individual variability

41
G.M. Vélez-Rubio et al. Journal of Experimental Marine Biology and Ecology 501 (2018) 36–45

Table 2
Satellite telemetry information of the three juvenile green turtles tagged in Cerro Verde, Uruguay, in 2007; a: recaptured dead in Argentina, b: Round-trip migration (see Fig. 6). n/a: no
applicable.

Turtle ID CCL Weight Release date Release site (permanency Migration Destination (permanency Stop transmitting N° days Distance
days) (days) in days) date tracked traveled

“Candombe”a 41.3 8.0 16/1/07 Cerro Verde, Uy (13 d) n/a Mar del Plata (Arg.) 27/3/07 70 670
“Ska”b⁎ 53.7 18.3 16/1/07 Cerro Verde, Uy (156 d) 39/35 Imbituba (Br.) (32 d) 30/11/07 318 1900
“Caibate”b 56.0 18.0 16/1/07 Cerro Verde, Uy (162 d) 40/45 Laguna (Br.) (25 d) 1/1/08 350 2307

* Turtle flipper tagged in 2004 before at the Cerro Verde area, and recaptured and satellite tagged exactly at the same location in 2007.

Fig. 5. Displacement from released site plot of the three tracked green turtle. The left panels (A and B) show the tracks of those turtles that performed a round-trip migration between
summer and winter foraging areas in Uruguay and Brazil respectively. The three right panels (C, D and E) show distance to the release point through time. Phases of migration are
represented by rapid changes in displacement distance; summer and winter foraging areas are revealed by plateaus. Each turtle is represented by a different color. (For interpretation of
the references to color in this figure legend, the reader is referred to the web version of this article.)

42
G.M. Vélez-Rubio et al. Journal of Experimental Marine Biology and Ecology 501 (2018) 36–45

coast of the SWAO (Brazil: Ubatuba, Silva et al., 2017; Paraná, Gama
et al., 2016; Santa Catarina, Martinez Souza, 2014; Rio Grande do Sul,
Monteiro et al., 2016. Uruguay: Vélez-Rubio et al., 2013; Martinez
Souza, 2014; López-Mendilaharsu et al., 2016. Argentina: Gonzalez
Carman et al., 2011). Similar settlement sizes were recorded for juve-
nile green turtles in the Northwestern Pacific Ocean and Australia
(straight carapace length (SCL) > 35 cm, Arthur et al., 2008; Ishihara,
2012; Shimada et al., 2014; Fukuoka et al., 2015). However, smaller
settlement sizes have been reported for the wider Caribbean and North
Atlantic populations (Bjorndal, 1997; Meylan et al., 2011 and refer-
ences therein).
In conclusion, juvenile green turtles would reach Uruguayan feeding
grounds using a coastal route along the Brazilian coast and settle when
40–45 cm CCL.

4.2. Post-settlement movements

Satellite tracking has confirmed the migration of the large juvenile

turtles (CCL > 50 cm) occurring off Uruguay during the austral
summer to southern Brazil when water temperature decreases during
the austral winter. For these turtles, the time spent in Brazilian waters is
short, returning after three to five months to the same place of release,
and hence spending most of the year in Uruguayan coastal waters.
Fig. 6. Turtle's positions and core-use areas (50% KDE contours) for the two green turtles Juvenile green turtles tagged in Argentina also migrate northward to
that remained for several months at the CMPA of Cerro Verde and Coronilla islands. The Brazil in winter and came back to Rio de La Plata estuary during
limits of the CMPA are represented by a hatched contour. (For interpretation of the re-
summer, when they remain close to Uruguayan coast (Gonzalez Carman
ferences to color in this figure legend, the reader is referred to the web version of this
article.) et al., 2012). Furthermore, some turtles over-winter in Uruguay
(Martinez Souza, 2014; Vélez-Rubio et al., 2013, 2016). Overwintering
in southern Brazil was expected to cause a drop in δ15N values of car-
4.1. Pre-settlement movements
apace layers, because prey species from southern Brazil are depleted in
15
N as compared to those in Uruguay and northern Argentina (Vélez-
According to genetics studies, > 85% of the green turtles in
Rubio et al., 2016). Such a drop has been observed in five of the re-
Uruguay came from the rookery in Ascension Island (Caraccio, 2008),
sident turtles and is consistent with their movement to Brazil several
which is also the major source for green turtle foraging aggregations in
months prior to sampling. In any case, the two satellite tracked turtles
Argentina (Prosdocimi et al., 2012) and southern Brazil (Proietti et al.,
that moved to Brazil in winter, returned to the capture area the next
2012). Virtual particle dispersal studies suggest that 70–90% of the
spring. This suggests high site fidelity of these turtles to their foraging
hatchlings from Ascension Island are expected to drift westward to the
grounds. Stable isotope data also support the existence of high levels of
foraging grounds along the Atlantic coast of South America (Putman
site fidelity in immature green turtles larger than 55 cm CCL off Ur-
and Naro-Maciel, 2013; Scott et al., 2014b). According to the isoscapes
uguay, even if some of them overwinter in Brazil. Alternatively, smaller
of the South Atlantic we would expect an initial decrease in the
turtles may overwinter in oceanic areas (Gonzalez Carman et al., 2012;
δ15Nscute values, as early juveniles disperse westward, and a latter in-
Southwood Williard et al., 2017).
crease in the δ15Nscute values, as juveniles move southward along the
Fidelity to foraging grounds and wintering sites had previously been
coast of Brazil (Somes et al., 2010; Navarro et al., 2013). This was
reported for adult green turtles in the Mediterranean (Broderick et al.,
precisely the pattern observed in the turtle with the thickest carapace
2007) and for juvenile loggerhead turtles in the Pacific (Watanabe
scute sample in the present data set (turtle C3, Table 1, Fig. 3B), but in
et al., 2011), but is less common for juvenile green turtles (Godley et al.,
many turtles we observed only the most recent increase in the δ15Nscute
2003; Gonzalez Carman et al., 2012) that should exhibit broad dispersal
values. This is caused by the slough of the outermost, older carapace
(Godley et al., 2003). In our studied area, this high site fidelity was also
layers as they grow; however, steady enrichment of carapace scutes in
15
detected during the mark-recapture program conducted in the Cerro
N through time is sufficient to suggests that they moved southwards
Verde area since 2001 by Karumbé, when 76% of turtles were re-
along the coast of Brazil.
captured exactly at the same location as the original site of capture
This enrichment most likely corresponds to the time when turtles
(López-Mendilaharsu et al., 2016). In addition, the two satellite tagged
were < 45 cm CCL and was not paralleled by a simultaneous enrich-
turtles that remained in Cerro Verde for several months, showed that
ment in 13C. Indeed, δ13C values were low and constant across carapace
core foraging areas of activity were very similar in size and were par-
layers in new settlers, thus suggesting a pelagic diet, although we lack
tially overlapped, indicating that this area is rich in food resources for
information about the stable isotope ratios in potential pelagic prey off
the green turtles.
Brazil. Only after settlement, variability in δ13C values increased, which
We show a rapidly increase in N and C in the group of smallest
likely represented the high variability in the δ13C values Uruguayan
turtles sampled, comparing with the biggest ones that show no great
macroalgae (Vélez-Rubio et al., 2016 and references therein).
variations in their signals. This remarks the importance of the combi-
The results presented here are consistent with the hypothesis posed
nation of different techniques, helping us to detect and understand the
by Barata et al. (2011), suggesting that juvenile green turtles recruit to
turtle's behavior. Also the use of different techniques improves the
neritic foraging grounds in northeast Brazil when they are < 30 cm
knowledge of the movement of small juveniles in the South Atlantic (i.e.
CCL, but some move southward to Uruguay and northern Argentina,
Vander Zanden et al., 2015; Sepúlveda et al., 2015).
where they settle in neritic habitats when at 40–45 cm CCL. Only three
The high degree of fidelity to feeding grounds in Uruguay enforces
of the turtles classified as resident actually settled at a smaller size, but
to keep protecting the coastal areas but also contributes to the creation
the average length at settlement calculated here was consistent with the
of a protected coastal corridor in all the SWAO, encouraging interna-
sizes of other studies based on mark-recapture or strandings along the
tional cooperation for sea turtle conservation in the region. This

43
G.M. Vélez-Rubio et al.
corridor will help to protect other species of sea turtles and other
marine fauna that also use the coastal water.
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.jembe.2018.01.001.
Acknowledgement
We would like to thank the volunteers and Karumbé members,
especially Andrés Estrades, Alejandro Fallabrino, Natalia Teryda,
Virginia Ferrando, Carlos Romero, Alfredo Hargain, Coco Meirana,
Vannessa Massimo, Marina Reyes, Manuela Calvo, Martin Makarewicz,
Tatiana Curbelo, and Lucía Dominguez, for their collaboration in the
present study. Also an special thank to Luciana Alonso. We also thank
the support of the Marine Zoology Unit of the Cavanilles Institute of
Biodiversity and Evolutionary Biology (University of Valencia), espe-
cially to Ohiana Revuelta, Natalia Fraija and Francesc Domenech, and
also thank to the Department of Evolutionary Biology, Ecology and
Environmental Science of the University of Barcelona in special to
Fabiana Sapotitti, Lisette Zenteno, Irene Álvarez de Quevedo and
Marcel Clusa; for all their help with the stable isotopes analysis.
Authors are really grateful to all the persons and institutions that col-
laborated with Karumbé in Uruguay marine turtle stranding network:
volunteers, local fishermen, government institutions (DINARA and
DINAMA), specially to Sistema Nacional de Áreas Protegidas (SNAP),
Prefectura Nacional Naval, lifeguard service, rangers, civil organiza-
tions (particularly SOCOBIOMA), citizens, tourist and Faculty of
Science and Centro Universitario Regional del Este (CURE) of the
Universidad de la República (UdelaR, Uruguay). Also thanks to Alvaro
Soutullo and to the Estación Biológica Terra Natura (Fundación Terra
Natura-CBIO, University of Alicante) with their help with the telemetry
devices and ARGOS systems. A special mention for the workers of the
CMPA of Cerro Verde and Islas de La Coronilla: Jorge Pereira, Paula
Laporta, Dante Ruibal, Manuel Barreneche e Ivan Muraña. We also
acknowledge the financial support Rufford Small Grants Foundation to
Karumbé members (ML-M and GV-R; 17651-1 and 17651-2) and
Agencia Nacional de Investigación e Innovación (ANII) to AC and GV-R.
JT is supported by project Prometeo of the Generalitat Valenciana (UV-
CI-12-151). This research was conducted under license (No. 200/04,
073/08 and 323/11) from the Fauna Department-Ministry of Cattle,
Agriculture and Fishing of Uruguay. CITES permits for export and im-
port of the samples were obtained.
Funding
This work was supported by BP Conservation to NGO Karumbe and
Rufford Small Grants, UK [grant number 17651-1, 17651-2].
References
Acha, E.M., Mianzan, H.W., Guerrero, R.A., Favero, M., Bava, J., 2004. Marine fronts at
the continental shelves of austral South America. Physical and ecological processes. J.
Mar. Sys. 44, 83–105.
Alibardi, L., 2005. Proliferation in the epidermis of chelonians and growth of the horny
scutes. J. Morphol. 265, 52.
Arthur, K.E., Boyle, M.C., Limpus, C.J., 2008. Ontogenetic changes in diet and habitat use
in green sea turtle (Chelonia mydas) life history. Mar. Ecol. Prog. Ser. 362, 303–311.
Barata, P., Gonzalez Carman, V., dos Santos, A.S., ... Naro-Maciel, E., 2011. Variação
latitudinal na distribuição do tamanho de tartarugas-verdes (Chelonia mydas) ao
longo de parte da costa leste da américa do sul. In: Proceedings of the V Jornada
sobre Tartarugas Marinhas do Atlântico Sul Ocidental 27 e 28 de Novembro de 2011 -
Florianópolis, Brasil.
Barrow, L.M., Bjorndal, K.A., Reich, K.J., 2008. Effects of mreservation method on stable
carbon and nitrogen isotope values. Physiol. Biochem. Zool. 81 (5), 688–693.
Beyer, H.L., 2004. Hawth's Analysis Tools for ArcGIS. Available at: www.spatialecology.
com/htools.
Bjorndal, K.A., 1997. Foraging ecology and nutrition of sea turtles. In: Lutz, P.L., Musick,
J.A. (Eds.), The Biology of Sea Turtles. CRC Press, Boca Ratón, pp. 199–231.
Bjorndal, K.A., Bolten, A.B., Chaloupka, M., et al., 2017. Ecological regime shift drives
declining growth rates of sea turtles throughout the West Atlantic. Glob. Chang. Biol.
23, 4556–4568.
Blight, E.G., Dyer, W.J., 1959. A rapid method of total lipid extraction and purification.
44
Journal of Experimental Marine Biology and Ecology 501 (2018) 36–45
Can. J. Biochem. Phys. 37, 911–917.
Bograd, S.J., Block, B.A., Costa, D.P., Godley, B.J., 2010. Biologging technologies: new
tools for conservation. Introduction. Endanger. Species Res. 10, 1–7.
Bolten, A.B., 2003. Variation in sea turtle life history patterns: neritic vs. oceanic de-
velopmental stages. In: Lutz, P.L., Musick, J.A., Wyneken, J. (Eds.), The Biology of
Sea Turtles. Vol III. CRC Press, Boca Ratón, pp. 243–257.
Borrell, A., Velásquez Vacca, A., Pinela, A.M., Kinze, C., Lockyer, C.H., et al., 2013. Stable
isotopes provide insight into population structure and segregation in Eastern North
Atlantic Sperm Whales. PLoS One 8 (12), e82398.
Borthagaray, A.I., Carranza, A., 2007. Mussels as ecosystem engineers: their contribution
to species richness in a rocky littoral community. Acta Oecol. 31, 243–250.
Bowen, G.J., 2010. Isoscapes: spatial pattern in isotopic biogeochemistry. Annu. Rev.
Earth Planet. Sci. 38, 161–187.
Briscoe, D.K., Parker, D.M., Balazs, G.H., Kurita, M., Saito, T., Okamoto, H., ... Crowder,
L.B., 2016. Active dispersal in loggerhead sea turtles (Caretta caretta) during the ‘lost
years’. Proc. R. Soc. B 283 (1832), 20160690.
Broderick, A.C., Coyne, M.S., Fuller, W.J., Glen, F., Godley, B.J., 2007. Fidelity and over-
wintering of sea turtles. Proc. Biol. Sci. 274, 1533–1538.
Caraccio, M.N., 2008. Análisis de la composición genética de Chelonia mydas (tortuga
verde) en el área de alimentación y desarrollo de Uruguay. Universidad de la
Republica, Montevideo, Uruguay.
Cardona, L., Hays, G.C., 2018. Ocean currents, individual movements and genetic
structuring of populations. Mar. Biol. 165 (10).
Cardona, L., Aguilar, A., Pazos, L., 2009. Delayed ontogenic dietary shift and high levels
of omnivory in green turtles (Chelonia mydas) from the NW coast of Africa. Mar. Biol.
156, 1487–1495.
Cardona, L., Campos, P., Levy, Y., Demetropoulos, A., Margaritoulis, D., 2010.
Asynchrony between dietary and nutritional shifts during the ontogeny of green
turtles (Chelonia mydas) in the Mediterranean. J. Exp. Mar. Biol. Ecol. 393, 83–89.
Cardona, L., Clusa, M., Eder, E., Demetropoulos, A., Margaritoulis, D., Rees, A.F., Hamza,
A.A., Khalil, M., Levy, Y., Türkozan, O., Marín, I., 2014. Distribution patterns and
foraging ground productivity determine clutch size in Mediterranean loggerhead
turtles. Mar. Ecol. Prog. Ser. 497, 229–241.
Caut, S., Guirlet, E., Angulo, E., Das, K., Girondot, M., 2008. Isotope analysis reveals
foraging area dichotomy for Atlantic leatherback turtles. PLoS One 3 (3), e1845.
Christiansen, F., Esteban, N., Mortimer, J.A., Dujon, A.M., Hays, G.C., 2017. Diel and
seasonal patterns in activity and home range size of green turtles on their foraging
grounds revealed by extended Fastloc®GPS tracking. Mar. Biol. 164 (10).
Congdon, J.D., Gotte, S.W., McDiarmid, R.W., 1992. Ontogenetic changes in habitat use
by immature turtles, Chelydra serpentina and Chrysemys picta. Can. field-nat. 106,
241–248.
Coyne, M.S., Godley, B.J., 2005. Satellite Tracking and Analysis Tool (STAT): an in-
tegrated system for archiving, analyzing and mapping animal tracking data. Mar.
Ecol. Prog. Ser. 301, 1–7.
De Niro, M.J., Epstein, S., 1978. Influence of diet on the distribution of carbon isotopes in
animals. Geochim. Cosmochim. Acta 42, 495–506.
Drago, M., Franco-Trecu, V., Cardona, L., Inchausti, P., Tapia, W., Páez-Rosas, D., 2016.
Stable isotopes reveal long-term fidelity to foraging grounds in the Galapagos sea lion
(Zalophus wollebaeki). PLoS One 11 (1), e0147857.
Eder, E., Ceballos, A., Martins, S., Pérez-García, H., Marín, I., Marco, A., Cardona, L.,
2012. Foraging dichotomy in loggerhead sea turtles Caretta caretta off northwestern
Africa. Mar. Ecol. Prog. Ser. 470, 113–122.
Fukuoka, T., Narazaki, T., Sato, K., 2015. Summer-restricted migration of green turtles
Chelonia mydas to a temperate habitat of the northwest Pacific Ocean. Endanger.
Species Res. 28 (1), 1–10.
Gama, L.R., Domit, C., Broadhurst, M.K., Fuentes, M.M., Millar, R.B., 2016. Green turtle
Chelonia mydas foraging ecology at 25 S in the western Atlantic: evidence to support a
feeding model driven by intrinsic and extrinsic variability. Mar. Ecol. Prog. Ser. 542,
209–219.
Garcia, C.A.E., 1998. Oceanografia física. In: Seeliger, U., Ode-Brecht, C., Castello, J.P.
(Eds.), Os Ecossistemas Costeiro e Marinho do Extremo Sul do Brasil. Rio Grande,
Brasil. Ecoscientia, pp. 104–106.
Godley, B.J., Lima, E.H.S.M., Åkesson, S., Broderick, A.C., Glen, F., Godfrey, M.H., ...
Hays, G.C., 2003. Movement patterns of green turtles in Brazilian coastal waters
described by satellite tracking and flipper tagging. Mar. Ecol. Prog. Ser. 253,
279–288.
Gonzalez Carman, V., Álvarez, K., Prosdocimi, L., Inchaurraga, M.C., Dellacasa, R.,
Faiella, A., Echenique, C., González, R., Andrejuk, J., Mianzan, H., Campagna, C.,
Albareda, D., 2011. Argentinian coastal waters: a temperate habitat for three species
of threatened sea turtles. Mar. Biol. Res. 7, 500–508.
Gonzalez Carman, V., Falabella, V., Maxwell, S., Albareda, D., Campagna, C., Mianzan,
H., 2012. Revisiting the ontogenetic shift paradigm: the case of juvenile green turtles
in the SW Atlantic. J. Exp. Mar. Biol. Ecol. 429, 64–72.
Gónzalez-Etchebehere, L., Kruk, C., Scarabino, F., Laporta, F., Zabaleta, M., González, L.,
Vélez-Rubio, G.M., 2017. Comunidades de macroalgas en puntas rocosas de la costa
de Rocha, Uruguay. Innotec 14, 9–18.
González-Solís, J., Croxall, J.P., Oro, D., Ruiz, X., 2007. Trans-equatorial migration and
mixing in the wintering areas of a pelagic seabird. Front. Ecol. Environ. 5 (6),
297–301.
Graham, B.S., Koch, P.L., Newsome, S.D., McMahon, K.W., Aurioles, D., West, J.B.,
Bowen, G.J., Dawson, T.E., Tu, K.P., 2010. Using isoscapes to trace the movements
and foraging behavior of top predators in oceanic ecosystems. In: Isoscapes:
Understanding Movement, Pattern, and Process on Earth through Isotope Mapping.
Springer, Netherlands, pp. 299–318.
Graham, R.T., Witt, M.J., Castellanos, D.W., Remolina, F., Maxwell, S., et al., 2012.
Satellite tracking of manta rays highlights challenges to their conservation. PLoS One
G.M. Vélez-Rubio et al.
7 (5), e36834.
Hobson, K.A., 2008. Applying isotopic methods to tracking animal movements. Terr. Ecol.
2, 45–78.
Hobson, K.A., Schell, D.M., 1998. Stable carbon and nitrogen isotope patterns in baleen
from eastern Arctic bowhead whales (Balaena mysticetus). Can. J. Fish. Aquat. Sci. 55
(12), 2601–2607.
Hobson, K.A., Sease, J.L., 1998. Stable isotope analyses of tooth annuli reveal temporal
dietary records: an example using Steller sea lions. Mar. Mamm. Sci. 14 (1), 116–129.
Ishihara, T., 2012. Life history. In: Kamezaki, N. (Ed.), Natural History of Sea Turtles in
Japan. University of Tokyo Press, Tokyo, pp. 57–83 (in Japanese).
Jackson, A.L., Inger, R., Parnell, A.C., Bearhop, S., 2011. Comparing isotopic niche widths
among and within communities: SIBER–Stable Isotope Bayesian Ellipses in R. J.
Anim. Ecol. 80 (3), 595–602.
Layman, C.A., Araujo, M.S., Boucek, R., Hammerschlag-Peyer, C.M., Harrison, E., Jud,
Z.R., ... Post, D.M., 2012. Applying stable isotopes to examine food-web structure: an
overview of analytical tools. Biol. Rev. 87 (3), 545–562.
Lohmann, K.J., Cain, S.D., Dodge, S.A., Lohmann, C.M., 2001. Regional magnetic fields as
navigational markers for sea turtles. Science 294, 364–366.
López-Castro, M.C., Bjorndal, K.A., Kamenov, G.D., Zenil-Ferguson, R., Bolten, A.B., 2013.
Sea turtle population structure and connections between oceanic and neritic foraging
areas in the Atlantic revealed through trace elements. Mar. Ecol. Prog. Ser. 490,
233–246.
López-Castro, M., Bjorndal, K., Bolten, A., 2014. Evaluation of scute thickness to infer life
history records in the carapace of green and loggerhead turtles. Endanger. Species
Res. 24, 191–196.
López-Mendilaharsu, M., Estrades, A., Caraccio, M.N., Calvo, V., Hernández, M., Quirci,
V., 2006. Biología, ecología y etología de las tortugas marinas en la zona costera
uruguaya. In: Menafra, R., Rodriguez-Gallego, L., Scarabino, F., Conde, D. (Eds.),
Bases para la Conservación y el manejo de la costa uruguaya. Vida Silvestre
Uruguay, (pp).
López-Mendilaharsu, M., Vélez-Rubio, G.M., Lezama, C., Aisenberg, A., Bauzá, A.,
Berrondo, L., Calvo, V., Caraccio, N., Estrades, A., Hernández, M., Laporta, M., et al.,
2016. Demographic and tumour prevalence data for juvenile green turtles at the
Coastal-Marine Protected Area of Cerro Verde, Uruguay. Mar. Biol. Res. 12 (5),
541–550.
Luschi, P., Hays, G.C., Del Seppia, C., Marsh, R., Papi, F., 1998. The navigational feats of
green sea turtles migrating from Ascension Island investigated by satellite telemetry.
Proc. R. Soc. Lond. B 265, 2279–2284.
Madigan, D.J., Baumann, Z., Carlisle, A.B., Hoen, D.K., Popp, B.N., Dewar, H., Snodgrass,
O.E., Block, B.A., Fisher, N.S., 2014. Reconstructing transoceanic migration patterns
of Pacific bluefin tuna using a chemical tracer toolbox. Ecology 95 (6), 1674–1683.
Maggozi, S., Yool, A., Vander Zanden, H.B., Wunder, M.B., Trueman, C.N., 2017. Using
ocean models to predict spatial and temporal variation in marine Carbone isotopes.
Ecospheres 8, e01763.
Mansfield, K.L., Wyneken, J., Porter, W.P., Luo, J., 2014. First satellite tracks of neonate
sea turtles redefine the ‘lost years’ oceanic niche. Proc. R. Soc. Lond. Ser. B Biol. Sci.
281 (1781), 20133039.
Marcovaldi, M.Â., Lopez, G.G., Soares, L.S., Lima, E.H., Thomé, J.C., Almeida, A.P., 2010.
Satellite-tracking of female loggerhead turtles highlights fidelity behavior in north-
eastern Brazil. Endanger. Species Res. 12 (3), 263–272.
Martinez Souza, G., 2014. Caracterização populacional de juvenis de tartaruga-verde
(Chelonia mydas) em duas áreas do Atlântico Sul Ocidental (PhD Dissertation).
Universidade Federal do Rio Grande, Rio grande do Sul, Brazil.
Meylan, P.A., Meylan, A.B., Gray, J.A., 2011. The ecology and migrations of sea turtles.
Tests of the developmental habitat hypothesis. Bull. Am. Mus. Nat. Hist. 357, 1–70.
Monteiro, D.S., Estima, S.C., Gandra, T.B., Silva, A.P., Bugoni, L., Swimmer, Y., Seminoff,
J.A., Secchi, E.R., 2016. Long-term spatial and temporal patterns of sea turtle
strandings in southern Brazil. Mar. Biol. 163 (12), 247.
Monzón-Argüello, C., López-Jurado, L.F., Rico, C., Marco, A., López, P., Hays, G.C., Lee,
P.L.M., 2010. Evidence from genetic and Lagrangian drifter data for transatlantic
transport of small juvenile green turtles. J. Biogeogr. 37 (9), 1752–1766.
Naro-Maciel, E., Bondioli, A.C.V., Martin, M., de Pádua Almeida, A., Baptistotte, C.,
Bellini, C., Marcovaldi, M.Â., Santos, A.J.B., Amato, G., 2012. The interplay of
homing and dispersal in green turtles: a focus on the Southwestern Atlantic. J. Hered.
103, 792–805.
Navarro, J., Coll, M., Somes, C.J., Olson, R.J., 2013. Trophic niche of squids: insights from
isotopic data in marine systems worldwide. Deep-Sea Res. II Top. Stud. Oceanogr. 95,
93–102.
Newland, C., Field, I.C., Cherel, Y., Guinet, C., Bradshaw, C.J.A., McMahon, C.R., Hindell,
M.A., 2011. Diet of juvenile southern elephant seals reappraised by stable isotopes in
whiskers. Mar. Ecol. Prog. Ser. 424, 247–258.
Newsome, S.D., Clementz, M.T., Koch, P.L., 2010. Using stable isotope biogeochemistry to
study marine mammal ecology. Mar. Mamm. Sci. 26, 509–572.
Ortega, L., Martínez, A., 2007. Multiannual and seasonal variability of water masses and
fronts over the Uruguayan shelf. J. Coast. Res. 233, 618–629.
Payne, N.L., Taylor, M.D., Watanabe, Y.Y., Semmens, J.M., 2014. From physiology to
physics: are we recognizing the flexibility of biologging tools? J. Exp. Biol. 217,
317–322.
Proietti, M.C., Reisser, J.W., Kinas, P.G., Kerr, R., Monteiro, D.D.S., Marins, L.F., Secchi,
E.R., 2012. Green turtle Chelonia mydas mixed stocks in the western South Atlantic, as
revealed by mtDNA haplotypes and drifter trajectories. Mar. Ecol. Prog. Ser. 447,
195–209.
Prosdocimi, L., González Carman, V., Albareda, D.A., Remis, M.I., 2012. Genetic com-
position of green turtle feeding grounds in coastal waters of Argentina based on
mitochondrial DNA. J. Exp. Mar. Biol. Ecol. 412, 37–45.
45
Journal of Experimental Marine Biology and Ecology 501 (2018) 36–45
Putman, N.F., Mansfield, K.L., 2015. Direct evidence of swimming demonstrates active
dispersal in the sea turtles “lost years”. Curr. Biol. 25, 1–7.
Putman, N.F., Naro-Maciel, E., 2013. Finding the ‘lost years’ in green turtles: insights from
ocean circulation models and genetic analysis. Proc. R. Soc. Lond. Biol. 280 (1768),
20131468.
Reich, K.J., Bjorndal, K.A., Bolten, A.B., 2007. The ‘lost years’ of green turtles: using
stable isotopes to study cryptic life stages. Biol. Lett. 3, 712–714.
Reich, K.J., Bjorndal, K.A., Del Rio, C.M., 2008. Effects of growth and tissue type on the
kinetics of 13C and 15N incorporation in a rapidly growing ectotherm. Oecologia 155
(4), 651–663.
Rutz, C., Hays, G.C., 2009. New frontiers in biologging science. Biol. Lett. 5, 289–292.
Scott, R., Hodgson, D.J., Witt, M.J., Coyne, M.S., Adnyana, W., Blumenthal, J.M.,
Broderick, A.C., ... Richardson, P.B., Rees, A.F., Godley, B.J., 2012. Global analysis of
satellite tracking data shows that adult green turtles are significantly aggregated in
marine protected areas. Glob. Ecol. Biogeogr. 21, 1053–1061.
Scott, R., Mash, R., Hays, G.C., 2014a. Ontogeny of long distance migration. Ecology 95
(10), 2840–2850.
Scott, R., Biastoch, A., Roder, C., Stiebens, V.A., Eizaguirre, C., 2014b. Nano-tags for
neonates and ocean-mediated swimming behaviours linked to rapid dispersal of
hatchling sea turtles. Proc. R. Soc. Lond. B 281, 20141209.
Seminoff, J.A., Jones, T.T., Resendiz, A., Nichols, W.J., Chaloupka, M.Y., 2003.
Monitoring green turtles (Chelonia mydas) at a coastal foraging area in Baja
California, Mexico: multiple indices to describe population status. J. Mar. Biol. Assoc.
UK 83 (06), 1355–1362.
Seminoff, J.A., Zárate, P., Coyne, M., Foley, D.G., Parker, D., Lyon, B.N., Dutton, P.H.,
2008. Post-nesting migrations of Galápagos green turtles Chelonia mydas in relation to
oceanographic conditions: integrating satellite telemetry with remotely sensed ocean
data. Endanger. Species Res. 4 (1–2), 57–72.
Sepúlveda, M., Pelican, K., Cross, P., Eguren, A., Singer, R., 2015. Fine-scale movements
of rural free-ranging dogs in conservation areas in the temperate rainforest of the
coastal range of southern Chile. Mamm. Biol. 80 (4), 290–297.
Shimada, T., Aoki, S., Kameda, K., Hazel, J., Reich, K., Kamezaki, N., 2014. Site fidelity,
ontogenetic shift and diet composition of green turtles Chelonia mydas in Japan in-
ferred from stable isotope analysis. Endanger. Species Res. 25, 151–164.
Silva, B.M., Bugoni, L., Almeida, B.A., Giffoni, B.B., Alvarenga, F.S., Brondizio, L.S.,
Becker, J.H., 2017. Long-term trends in abundance of green sea turtles (Chelonia
mydas) assessed by non-lethal capture rates in a coastal fishery. Ecol. Indic. 79,
254–264.
Somes, J., Schmittner, A., Galbraith, E.D., Lehmann, M.F., Altabet, M.A., Montoya, J.P.,
Letelier, R.M., ... Eby, M., 2010. Simulating the global distribution of nitrogen iso-
topes in the ocean. Global Biogeochem. 24, GB4019.
Southwood Williard, A., Goodman Hall, A., Fujisaki, I., Braun McNeill, J., 2017. Oceanic
overwintering in juvenile green turtles Chelonia mydas from a temperate latitude
foraging ground. Mar. Ecol. Prog. Ser. 564, 235–240.
Stokes, K.L., Broderick, A.C., Canbolat, A.F., Candan, O., Fuller, W.F., Glen, F., Levy, Y.,
Rees, A.F., Rilov, G., Snape, R.T., Stott, I., Tchernov, D., Godley, B.J., 2015. Migratory
corridors and foraging hotspots: critical habitats identified for Mediterranean green
turtles. Divers. Distrib. 21, 665–674.
Tomaszewicz, T., Calandra, N., Seminoff, J.A., Peckham, S.H., Avens, L., Kurle, C.M.,
2017. Intrapopulation variability in the timing of ontogenetic habitat shifts in sea
turtles revealed using δ15N values from bone growth rings. J. Anim. Ecol. 86 (3),
694–704.
Troëng, S., Evans, D.R., Harrison, E., Lagueux, C.J., 2005. Migration of green turtles
Chelonia mydas from Tortuguero, Costa Rica. Mar. Biol. 148, 435–447.
Vander Zanden, H.B., Bjorndal, K.A., Bolten, A.B., 2013. Temporal consistency and in-
dividual specialization in resource use by green turtles in successive life stages.
Oecologia 173, 767–777.
Vander Zanden, H.B., Tucker, A.D., Hart, K.M., Lamont, M.M., Fujisaki, I., Addison, D.S.,
Mansfield, K.L., Phillips, K.F., Wunder, M.B., Bowen, G.J., Pajuelo, M., 2015.
Determining origin in a migratory marine vertebrate: a novel method to integrate
stable isotopes and satellite tracking. Ecol. Appl. 25 (2), 320–335.
Vélez-Rubio, G.M., Estrades, A., Fallabrino, A., Tomás, J., 2013. Marine turtle threats in
Uruguayan waters: insights from 12 years of stranding data. Mar. Biol. 160,
2797–2811.
Vélez-Rubio, G.M., Cardona, L., López-Mendilaharsu, M., Martinez Souza, G., Carranza,
A., González-Paredes, D., Tomás, J., 2016. Ontogenetic dietary changes of green
turtles (Chelonia mydas) in the temperate southwestern Atlantic. Mar. Biol. 163 (3),
1–16.
Vélez-Rubio, G.M., Trinchin, R., Estrades, A., Ferrando, V., Tomás, J., 2017. Hypothermic
stunning in juvenile green turtles (Chelonia mydas) in Uruguayan coastal waters:
learning for future events. Chelonian Conserv. Biol. 16 (2), 151–158.
Watanabe, K., Hatase, H., Kinoshita, M., Omuta, K., Bando, T., Kamezaki, N., Sato, K.,
Matsuzawa, Y., Goto, K., Nakashima, Y., Takeshita, H., Aoyama, J., Tsukamoto, K.,
2011. Population structure of the loggerhead turtle Caretta caretta, a large marine
carnivore that exhibits alternative foraging behaviors. Mar. Ecol. Prog. Ser. 424,
273–283.
Weber, S.B., Weber, N., Ellick, J., Avery, A., Frauenstein, R., Godley, B.J., ... Broderick,
A.C., 2014. Recovery of the South Atlantic's largest green turtle nesting population.
Biodivers. Conserv. 23 (12), 3005–3018.
Webster, M., Marra, P., Haig, S., Bensch, S., Holmes, R., 2002. Links between worlds:
unraveling migratory connectivity. Trends Ecol. Evol. 17, 76–83.
Williard, A.S., Hall, A.G., Fujisaki, I., McNeill, J.B., 2017. Oceanic overwintering in ju-
venile green turtles Chelonia mydas from a temperate latitude foraging ground. Mar.
Ecol. Prog. Ser. 564, 235–240.