(1)

(2)
(3)
(4)
Marine Biology
International Journal on Life in Oceans and Coastal Waters
Springer-Verlag Berlin Heidelberg 2014
10.1007/s00227-014-2467-x
Feature Article
Biological and environmental influences on the
trophic ecology of leatherback turtles in the
northwest Atlantic Ocean
Bryan P. Wallace
1, 2
, Joel Schumacher
3
, Jeffrey A. Seminoff
3
and Michael C. James
4
Stratus Consulting, 1881 Ninth St., Suite 201, Boulder, CO 80302, USA
Nicholas School of the Environment, Duke University, Beaufort, NC, USA
Southwest Fisheries Science Center, NMFS-NOAA, La Jolla, CA, USA
Population Ecology Division, Fisheries and Oceans Canada, Dartmouth, NS, B2Y 4A2, Canada
Bryan P. Wallace
Email: bwallace@stratusconsulting.com
Received: 20 December 2013
Accepted: 20 May 2014
Published online: 6 June 2014
Communicated by R. Lewison.
Abstract
Understanding the causes and consequences of variability in trophic status is important for
interpreting population dynamics and for identifying important habitats for protected species like
marine turtles. In the northwest Atlantic Ocean, many leatherback turtles (Dermochelys coriacea)
from distinct breeding stocks throughout the Wider Caribbean region migrate to Canadian waters
seasonally to feed, but their trophic status during the migratory and breeding cycle and its
implications have not yet been described. In this study, we used stable carbon and nitrogen isotope
analyses of bulk skin to characterize the trophic status of leatherbacks in Atlantic Canadian waters
by identifying trophic patterns among turtles and the factors inuencing those patterns. !
15
N values
of adult males and females were signicantly higher than those of turtles of unknown gender (i.e.,
presumed to be subadults), and !
15
N increased signicantly with body size. We found no signicant
differences among average stable isotope values of turtles according to breeding stock origin.
Signicant inter-annual variation in !
15
N among cohorts probably reects broad-scale
oceanographic variability that drives uctuations in stable isotope values of nutrient sources
transferred through several trophic positions to leatherbacks, variation in baseline isotope values
among different overwintering habitats used by leatherbacks, or a combination of both. Our results
demonstrate that understanding effects of demographic and physiological factors, as well as
oceanographic conditions, on trophic status is key to explaining observed patterns in population
dynamics and for identifying important habitats for widely distributed, long-lived species like
leatherbacks.
Introduction
Intraspecic or intrapopulation variability in trophic status can affect variation in demographic rates
and thus population dynamics (Broderick et al. 2001; Suryan et al. 2009). In marine ecosystems,
drivers of variability in trophic status among individuals belonging to the same species or population
can be biological [i.e., different life history and/or ontogenetic demands (Forero et al. 2002; Bearhop
et al. 2006; Cherel et al. 2007)] and/or environmental [i.e., heterogeneous resource availability [Saba
et al. 2008], variable oceanographic conditions (Wallace et al. 2006a; Pajuelo et al. 2010)].
Understanding the causes and consequences of trophic status variability in protected species with
broad distributions is important for designing effective conservation actions to promote population
resilience and for identifying critical habitats (Hobson 2008; Ceriani et al. 2012; Pajuelo et al.
2012).
Leatherback turtles (Dermochelys coriacea) in the northwest Atlantic Ocean are highly migratory,
capital breeders (Plot et al. 2014) that range from breeding areas throughout the Wider Caribbean
region to distant feeding areas in boreal, temperate, and tropical regions (James et al. 2005a, 2007;
Fossette et al. 2010a, b; Dodge et al. 2011, 2014) (Fig. 1). In particular, Canadian waters off Nova
Scotia, including the southern Gulf of St. Lawrence, have been identied as critical feeding areas
during specic times of year for adult males and females, as well as subadults (James et al. 2005a, b,
2006, 2007; Stewart et al. 2013). Despite the long distances and time required to migrate to and
from these temperate feeding areas, prey availability is sufciently reliable and abundant to attract a
high density of leatherbacks each year (James et al. 2007). Leatherbacks feed almost exclusively on
large scyphozoan jellysh (Cyanea capillata, Chrysaora quinquecirrha) while in temperate
northwest Atlantic shelf waters (James and Herman 2001; Dodge et al. 2011, 2014; Heaslip et al.
2012) and apparently time their arrival and departure to and from these areas to coincide with
conditions that favor high abundance of these prey items (Sherril-Mix et al. 2007).
Fig. 1
Leatherback turtle (Dermochelys coriacea) foraging and nesting sites in the northwest Atlantic Ocean.
Leatherback tissue samples analyzed in this study were collected at two foraging area field sites off Nova
Scotia, Canada (triangles; all sampling locations are encompassed by the symbols on the map). Leatherbacks
captured in Canadian waters have been linked to nesting sites (circles) throughout the Wider Caribbean by
satellite telemetry and tag returns. Leatherback stable isotope values are available from other northern foraging
field sites off Massachusetts and Florida, USA, (Dodge et al. 2011) and are referenced in the text. Generalized
overwintering area based on turtles tracked by satellite telemetry from Canadian waters (James et al. 2005a, b,
c) also shown for reference
The composition of these annual feeding cohorts of foraging leatherbacks varies in gender,
reproductive status (i.e., breeding or non-breeding adults and subadults), breeding stock origin, and
other factors (James et al. 2005a; Stewart et al. 2013). Furthermore, despite leatherbacks highly
specialized diet, they have shown wide inter-population (Wallace et al. 2006a) and intrapopulation
(Caut et al. 2008) variations in trophic status, as well as body sizes and reproductive output, which
have been linked to oceanographic variability (Wallace et al. 2006b; Saba et al. 2008). However,
these studies generally focused on adult female turtles on nesting beaches, rather than in-water
aggregations of feeding animals that include other life stages. Dodge et al. (2011) used carbon and
nitrogen stable isotope analyses to describe the trophic status of leatherbacks foraging off
Massachusetts (northeastern USA) between 2005 and 2010 and off Georgia and Florida
(southeastern USA) in 2007 (sites shown in Fig. 1 for comparison with present study) and reported
relationships between leatherback stable isotope values and biological factors such as body size and
gender. Characterizing trophic status of leatherbacks that forage in Canadian watersencompassing
the northern limits of this species regular distribution in the western Atlanticwould improve our
understanding of leatherback trophic ecology overall.
Stable isotope analysis is an informative and cost-effective tool that facilitates understanding of
trophic ecology, migration patterns, and food web dynamics (Hobson 2008; Bowen 2010; Boecklen
et al. 2011). Using very small tissue samples, it is possible to derive the naturally occurring ratios of
stable isotopes of carbon, nitrogen, and other elements to augment life history and distribution
information gained by other means, such as satellite telemetry, shipboard surveys, and capture
markrecapture studies for various animal species (Hobson and Norris 2008), including marine
turtles (Hatase et al. 2002; Zbinden et al. 2011; Seminoff et al. 2012; Ceriani et al. 2012; Pajuelo et
al. 2012). Feeding areas can be distinguished using isoscapesi.e., modeled spatiotemporal
distributions of stable isotopes in the environment based on information about biogeochemical
processes of elemental cycling (Bowen 2010)if sufcient differences among areas exist in isotope
values of nutrients at the base of trophic webs, or in the number and/or types of trophic levels
present in a food web, thereby reinforcing habitat use analyses using more conventional tools
(Pajuelo et al. 2012; McMahon et al. 2013). Recently, combined analyses of stable isotopes, satellite
tracking, and demographic data from capturemarkrecapture studies have been used to illustrate
intrapopulation variation in the use of multiple feeding areas by loggerhead turtles (Caretta caretta)
and green turtles (Chelonia mydas) and how these variation patterns might manifest in variation in
reproductive output among turtles belonging to the same population (Ceriani et al. 2012; Pajuelo et
al. 2012; Vander Zanden et al. 2013).
Population characteristics, movements, and nesting origins of leatherbacks using Canadian foraging
habitat have been well established through long-term monitoring (James et al. 2005a, b, 2007;
Stewart et al. 2013). Our primary objective was to use stable isotope analyses to characterize the
trophic status of leatherbacks in Atlantic Canadian waters by identifying trophic patterns among
turtles and the factors inuencing those patterns, such as intra- and inter-annual variation in
proportion of turtles from different breeding stocks, different migratory behaviors and reproductive
status, other morphometric (e.g., body sizes) and demographic (e.g., gender) parameters, and
oceanographic processes. The northwest Atlantic leatherback population is currently stable (Wallace
et al. 2011), but remains a federally listed endangered species in the USA and Canada, as well as
many other countries in the region, because several serious threats to their survival persist (James et
al. 2005b; TEWG 2007). In the last decade, much has been learned about broad-scale migration
patterns, connectivity between breeding and feeding areas, and other aspects of leatherback biology
in the northwest Atlantic that are relevant to their management in this region (James et al. 2005a, b,
2006, 2007; TEWG 2007; Stewart et al. 2013; Dodge et al. 2014). In this study, we analyzed stable
isotope values of leatherback bulk skin in relation to a detailed dataset compiled as part of a long-
term monitoring program (James et al. 2005a, b, 2006, 2007) that encompassed migratory behavior,
morphometrics, gender, and breeding stock origin of over 100 leatherbacks foraging in Canadian
Atlantic waters. Our results provide a detailed description of the trophic ecology of northwest
Atlantic leatherbacks sampled in Atlantic Canada, as well as biological and environmental drivers of
variability in trophic status that could aid management efforts in this important foraging area and
beyond.
Materials and methods
Data collection and tissue sampling of leatherbacks
The eld portion of this study was conducted in the temperate shelf waters off Nova Scotia, Canada
(Fig. 1), during the late summerearly fall months (JulyOctober) from 2001 to 2012. Previous
studies have described this eld site and have documented a relatively large, seasonal foraging
aggregation of subadult and adult leatherbacks in this area every year (James et al. 2005a, b, 2006).
At-sea eld research methods are described in detail elsewhere (James et al. 2005a; 2007); we
describe them briey here. Leatherbacks were captured at or near the sea surface using a breakaway
hoop net, and curved carapace length (CCL) and width (CCW) were collected from most turtles
(i.e., when sea state permitted). Sexual dimorphism in tail length was used to assign sex to
leatherbacks; total tail length of mature male turtles is typically twice that of mature females of the
same carapace length (Eckert et al. 2012). Previous studies have shown that although some female
Atlantic leatherbacks reach sexual maturity at CCL <145 cm, this reects the minimum size at
maturity for most turtles (Stewart et al. 2007). To reduce the potential of erroneous assignment of
sex to turtles of smaller size classes, we conservatively assigned sex to turtles of "145 cm CCL only,
following James et al. (2007) and Stewart et al. (2013). We recognize that this threshold likely omits
some mature females, but it also increases our condence in visual assignments of sex to turtles
encountered away from nesting beaches by using tail length.
Bulk skin samples (hereafter referred to simply as skin, unless otherwise noted) were obtained
from 173 leatherbacks that had been captured alive as described above (n = 161), encountered while
entangled in shing gear (n = 9), or stranded on land (n = 3). These turtles were a subset of the >300
individual turtles captured in Atlantic Canada (Stewart et al. 2013) and were selected primarily
because their breeding stock origins were known (see below). We collected skin tissue (stratum
corneum) from the margin of the front ipper of each captured turtle using a biopsy punch
(Acuderm, 5 mm diameter). Skin samples were promptly preserved in saturated salt (NaCl) and
transported to the National Marine Fisheries Service-NOAA Southwest Fisheries Science Center
laboratory (La Jolla, California, US) where they were stored at #20 C until preparation and
analysis.
Prior to stable isotope analysis, skin samples were thawed, rinsed with distilled water, and then
refrozen. We then freeze-dried the skin samples (VirTis Benchtop K-Manifold Liophilizer) at #55C
for 8 h and ground to small size (0.05 mm particle diameter). We removed the lipids from samples
using an accelerated solvent extractor (Dionex ASE 200) with petroleum ether as the solvent for one
30-min ASE cycle. We completed sample preparation by freeze-drying for an additional 2 h to
remove any residual solvent before sending samples for isotopic analysis.
Stable isotope analysis
Approximately 1.0 mg of leatherback skin was loaded into sterilized tin capsules and analyzed by a
continuous-ow isotope-ratio mass spectrometer in the Stable Isotope Laboratory at the University
of Florida, Gainesville, Florida, USA. We used a Costech ECS 4010 elemental combustion system
interfaced via a ConFlo III device (Finnigan MAT, Bremen, Germany) to a Deltaplus gas isotope-
ratio mass spectrometer (Finnigan MAT, Bremen, Germany). Sample stable isotope ratios relative to
the isotope standard are expressed in the following conventional delta (!) notation in parts per
thousand ()
where R
sample
and R
standard
are the corresponding ratios of heavy to light isotopes (
13
C/
12
C:!
13
C and
15
N/
14
N:!
15
N) in the sample and standard, respectively. R
standard
for
13
C was Baker acetanilide
(C
8
H
9
N
O
; !
13
C = #10.4) calibrated monthly against the Peedee Belemnite (PDB) limestone
=
([
/
]
1
)
(1000) R
sample
R
standard
formation international standard; R
standard
for
15
N was IAEA N1 ammonium sulfate ((NH
4
)2SO
4
;
!
15
N = + 0.4) calibrated against atmospheric N
2
and USGS nitrogen standards. All analytical runs
included samples of standard materials inserted every 67 samples to calibrate the system and
compensate for any drift over time. Replicate assays of standard materials indicated measurement
errors of 0.05 and 0.095 for carbon and nitrogen, respectively. In addition to stable isotope ratios,
we measured %C and %N for each leatherback bulk skin sample. Samples were combusted in pure
oxygen in the elemental analyzer. Resultant CO
2
and N
2
gasses were passed through a series of
thermal conductivity detectors and element traps to determine percent compositions. Acetanilide
standards (10.36% N, 71.09% C) were used for calibration.
Some studies have detected small changes in !
15
N of tissues as a result of lipid extraction (e.g.,
Sotiropoulos et al. 2004; Sweeting et al. 2006; Kojadinovic et al. 2008), as well as long-term storage
in freezers (Barrow et al. 2008; Flemming et al. 2011), but the changes were extremely small
(<1); both slight enrichment and depletion were seen in !
15
N, with virtually unchanged sample
variances as a result. To examine potential effects of prolonged preservation by freezing, we
analyzed our !
15
N values (and standard deviations) in relation to time in storage and found no
signicant relationships (data not shown). Furthermore, because we consider changes for !
15
N to be
signicant when sample groups vary upward by 34, we concluded that the effects of lipid
extraction or long-term storage in our study do not signicantly impact the biological interpretations
of our ndings.
No empirical measurements of isotopic turnover rates for any tissues exist for leatherbacks that we
could use to estimate the dietary history reected in skin stable isotope ratios in this study. In
juvenile loggerhead sea turtles (Caretta caretta), skin samples reected the turtles dietary histories
over relatively long periods of time (i.e., up to 4 months) (Reich et al. 2008). Pajuelo et al. (2012)
assumed that skin samples would probably reect even longer periods for adult turtles because rates
of isotope incorporation slow with reduced growth rates (Reich et al. 2008) and increased body mass
(Carleton and Martnez del Rio 2005). Likewise, Seminoff et al. (2012) assumed that adult
leatherback skin stable isotope ratios reected longer periods on the order of 6 months. In the
absence of better empirical data, we assumed that leatherback skin stable isotope values reected
dietary histories of approximately 46 months prior to sample collection occurred in Nova Scotia,
which presumably corresponds to oceanic areas where leatherbacks forage during winter months
before moving onto the continental shelf during the following summer (Fig. 1).
Assignment of breeding stock origin
We assigned turtles to breeding stocks based on recent genetic determination of Atlantic leatherback
population structure (Dutton et al. 2013; Stewart et al. 2013) and grouped different stocks together
into regional breeding stocks to include turtles from specic nesting sites that had not been explicitly
sampled for genetic analyses. Regional breeding stocks were northern Caribbean (i.e., Florida, St.
Croix, Puerto Rico), mainland Central America (i.e., Costa Rica, Panama) and Colombia, and the
Guiana Shield/Trinidad (i.e., Suriname, Guyana, French Guiana, Trinidad, Venezuela, Grenada). We
determined breeding stock origins for 142 turtles using at least one of the following methods:
1) Tag returns: To determine whether turtles had been tagged prior to capture in Nova Scotia, we
inspected the rear ippers for metal tags, and the right and left shoulders and neck were scanned for
the presence of passive integrated transponders (PIT) using handheld scanners. Untagged turtles
were equipped with ipper tags (Monel No. 49, National Band and Tag) and a PIT in the right
shoulder muscle (AVID encrypted or unencrypted and/or Trovan ID100) to enable identication of
previously tagged turtles on nesting beaches.
2) Satellite telemetry: We inferred residency behavior in waters directly adjacent to nesting areas by
turtles that had been equipped and tracked with satellite transmitters (20012012; updated from
James et al. 2005b, c). Turtles were assigned to a particular nesting stock if they migrated to and
remained in the area of a nesting beach or area for an extended period during a breeding season,
rather than continuing to move.
3) Genetic assignments: If a turtle had not been assigned to a breeding stock by either tag returns or
telemetry, we used genetic assignments based on microsatellite allele frequencies of turtles captured
in Nova Scotia relative to genotyped baseline nesting populations in the North Atlantic following
Stewart et al. (2013). Specically, we accepted assignments to a regional breeding stock that
exceeded 90 % probability.
Hypotheses and data analyses
In general, our objective was to describe the trophic status of leatherbacks based on skin samples
from turtles foraging in Atlantic Canadian waters and to use associated biological data available
obtained by the long-term monitoring program (e.g., body sizes, sex, breeding stock origin, and
reproductive status), as well as relevant oceanographic indices (e.g., North Atlantic Oscillation,
NAO), to explain patterns detected by our analyses. Because leatherbacks are considered dietary
specialists (Bjorndal 1997; Eckert et al. 2012), but arrive to shelf waters off Nova Scotia from
several breeding areas and migratory pathways (James et al. 2005a; 2007; TEWG 2007), we
expected low variation in !
15
N values and high variation in !
13
C values among turtles, respectively,
following the concept of trophic niche width (sensu Bearhop et al. 2004). Therefore, we expected
any observed variation in stable isotope values to be due to within- and among-cohort variation in
biological and/or environmental factors, rather than to differences in prey selection or trophic
position.
Mature female leatherbacks tend to arrive off Nova Scotia during the second year of their
remigration interval (i.e., number of years between consecutive nesting events), with very few
turtles reaching Nova Scotia in the same calendar year (i.e., JulyOctober) as nesting (i.e., April
August) (James et al. 2007; Fossette et al. 2010a). However, some turtles do reach Nova Scotia late
in the foraging season after nishing nesting in the spring/early summer (Eckert et al. 2006; James et
al. 2007; Fossette et al. 2010a). Furthermore, mature males can make annual migrations between
Canada and breeding areas (James et al. 2005c). To explore whether trophic status varied according
to breeding status and gender, we constructed capturerecapture histories of adult female turtles by
compiling available records of turtles captured in Nova Scotia that had been tagged on beaches in
the Wider Caribbean prior to capture in Nova Scotia and/or resighted on beaches after capture in
Nova Scotia (updated from James et al. 2007). Because remigration intervals are typically 23 years
for female leatherbacks in the North Atlantic (TEWG 2007), we limited our analyses to those turtles
that were sighted on nesting beaches within 3 years before or after being captured in Canada to
ensure that we were including only the remigration interval that included the visit to Canadian
waters. We also compared stable isotope values of these internesting females to those of males,
considering the observed gender-based differences in migratory cycles (James et al. 2005a, c). We
hypothesized that stable isotope values might vary according the amount of time turtles had been
foraging (i.e., time since or until the next breeding season), with a particularly strong difference
between turtles that nested within one or two nesting seasons prior to being captured in Canada, and
turtles captured in Canada within a year of being sighted on nesting beaches, and between these
groups and males. These groups of turtles would have had nearly opposite breeding statuses, which
might have manifested in distinct isotope signatures related to differences in reproductive
physiology, dietary histories, and migratory cycles (Hobson et al. 1993; James et al. 2005a, c;
Hobson 2008; Dodge et al. 2011, 2014).
We used discriminant analyses to determine whether stable isotope ratios varied by breeding stock
origins. We examined inter-annual variation in stable isotope ratios among cohorts, with body sizes,
sexes, breeding stock origins, and the NAO indexa key oceanographic index that governs broad-
scale climate conditions and processes in the North Atlantic Ocean (Townsend et al. 2006)as
explanatory variables in analysis of variance models coupled with TukeyKramer HSD post hoc
tests. All statistical analyses were performed in JMP Pro 10 (SAS Institute, Inc.), and signicance
was accepted at ! $ 0.05.
Results
Leatherback !
13
C and !
15
N ranged over 5 (!
13
C: #18.8 to #13.0; !
15
N: 8.313.3 ) (Table 1),
but the distribution of !
13
C values was narrower than the distribution of !
15
N values, with >90 % of
values falling within 2 for !
13
C and 4 for !
15
N (Fig. 2).
Table 1
Summary of stable isotope values and elemental composition for carbon and nitrogen in skin from leatherback
turtles (Dermochelys coriacea) sampled off Nova Scotia, Canada
Category !
13
C () !
15
N () %C %N
Nova Scotia, Canada
"16.9 0.7
(173)
10.7 1.1
(173)
36.3 6.4
(105)
12.5 2.3
(105)
Known breeding stock
"17.0 0.7
(142)
10.7 1.1
(142)
36.0 6.3
(91)
12.4 2.3
(91)
Adults
"16.9 0.7
(160)
10.7 1.0
a
(160)
35.9 6.5
c
(96)
12.3 2.3
(96)
Subadults
"17.1 0.7
(14)
9.6 1.0
b
(14)
40.9 2.0
d
(9)
14.4 0.7 (9)
Massachusetts, U.S.A. (Dodge et al.
2011)
"17.8 0.7
(27)
11.1 1.3
(26)

Florida, Georgia, U.S.A. (Dodge et al.
2011)
"17.9 0.5 (4) 11.7 0.6 (4)
Categories include all turtles sampled, turtles for which breeding stock origin is known (i.e., turtles sighted before
or after capture in Canada, or identified based on genetic analyses, as belonging to a particular breeding stock),
adults (both males and females), and subadults (i.e., turtles < 145 cm curved carapace length; see Methods for
details of sex assignments to turtles). Different superscripts represent statistically significant differences
(p ! 0.05)
Fig. 2
Scatterplot of stable carbon ("
13
C) and nitrogen ("
15
N) isotopes in skin of leatherback turtles (Dermochelys
coriacea) sampled off Nova Scotia, Canada, shown according to distinct regional breeding stocks (see Methods
for details): triangles: Northern Caribbean, including Florida, and St. Croix, USVI, Puerto Rico, U.S.A.;
diamonds: Guiana Shield, Trinidad, Venezuela; squares: mainland Central America (Costa Rica, Panama) and
Colombia. There were no significant differences among breeding stocks. Black symbols are mean values 1
SD; gray symbols are raw data points. Circle represents all turtles together
We found no signicant differences in either !
15
N (p = 0.2) or !
13
C (p = 0.5) among breeding stocks
(Fig. 2). However, turtles of unknown gender (i.e., CCL < 145 cm), which we assumed to be
subadults (e.g., James et al. 2005a), had signicantly lower !
15
N values (F
172
= 7.55, p < 0.001)
than those of adult females or males (Fig. 3; Table 1). Similarly, !
15
N values increased with body
size among turtles (F
172
= 27.39, r
2
= 0.145, p < 0.0001) (Fig. 4). Furthermore, body sizes of adult
turtles (males: 152.3 7.7 cm, n = 37; females: 152.4 7.8 cm, n = 115) were signicantly larger (F
164
= 24.32, p < 0.0001) than those of turtles of unknown gender (136.8 6.5 cm, n = 14). We found
no signicant relationships between !
13
C and sex or body sizes (all p > 0.05).
Fig. 3
Nitrogen stable isotope values of skin samples from mature female (F) and male (M) leatherback turtles
(Dermochelys coriacea) captured off Nova Scotia, Canada, are significantly higher than those from turtles of
unknown gender (U), which are presumed to be subadults (significant differences denoted by stars). Dark, open
circles are mean values, vertical bars are standard deviations, numbers in parentheses are sample sizes, and
gray open circles are raw data points. There was no significant difference in stable carbon isotope values among
these groups (data not shown)
Fig. 4
Stable nitrogen isotope values of leatherback turtle (Dermochelys coriacea) skin samples increased significantly
with body size (cm, curved carapace length) in turtles captured off Nova Scotia, Canada. Circles: adult females;
squares: adult males; and diamonds: turtles of unknown gender, presumed to be subadult turtles (see Methods
for details). Trendline and r
2
value shown for all data combined. There was no significant difference in stable
carbon isotope values among these groups (data not shown)
We identied 66 turtles that had been sighted on nesting beaches within 3 years prior to or after
being captured in Canada. There was no signicant relationship between !
13
C (p = 0.5) and !
15
N
(p = 0.1) values and remigration year, i.e., the time between capture in Nova Scotia and conrmed
nesting (Fig. 5). Male stable isotope values were not signicantly different (!
13
C: p = 0.08; !
15
N:
p = 0.2) from those of females in any remigration year.
Fig. 5
Stable carbon and nitrogen isotope values in skin of leatherback turtles (Dermochelys coriacea) did not vary
significantly with remigration year, which was calculated as the time between capture in a temperate feeding
area off Nova Scotia, Canada (dashed line) and observations on nesting beaches in the Wider Caribbean
region. x-axis represents time prior to (year; below zero) or time after (year; above zero) capture in Canada
(zero). Assuming minimum nesting remigration interval of 2 years for Atlantic leatherbacks, turtles observed
nesting during periods indicated by dark gray bars would be precluded from nesting in season immediately prior
to their capture in Canada (light gray bar)
Percent carbon (F
104
= 19.3, p < 0.0001), percent nitrogen (F
104
= 19.7, p < 0.0001), and the ratio
of carbon to nitrogen (C:N) (F
104
= 6.5, p < 0.0001) in leatherback tissues varied signicantly
across years, with 2007 being a particularly unusual year of signicantly depleted %C and %N and
elevated C:N. !
13
C increased signicantly with %C (F
104
= 8.1, p = 0.005) and decreased
signicantly with C:N (F
104
= 57.3, p < 0.0001), but !
15
N values were not signicantly related to
either %N (p = 0.9) or C:N (p = 0.7). Small sample sizes of elemental composition in 2005 (n = 1),
2006 (n = 2), and 2008 (n = 0) likely contributed to these results, and complicated interpretation (see
Discussion).
Both !
13
C (F
172
= 2.16, p < 0.0189) and !
15
N (F
172
= 5.61, p < 0.001) exhibited signicant inter-
annual variation (Fig. 6). However, no similar inter-annual variations existed in body sizes, gender
proportions, or breeding stock proportions across annual cohorts (all p > 0.05).
Fig. 6
Stable carbon (a) and nitrogen (b) stable isotope values of leatherback turtle (Dermochelys coriacea) skin
samples collected off Nova Scotia, Canada, from 20012012. Black circles are annual mean values 1 SD,
sample sizes are in parentheses at the top of each panel, and gray symbols are raw data points. Significant
differences between years by different letters; that is, years with different letters are statistically different from
each other
Average !
13
C and !
15
N values were not correlated with either the average or standard deviation of
the NAO index during either the rst quarters (JanMar), rst and second quarters (JanJune) of
each year, or with the fourth and rst quarters (OctMar), which all approximately corresponded to
the assumed periods of isotopic incorporation (i.e., winter before arrival in Nova Scotia ca. 4
6 months later). Approximately 26 % of the variation in !
15
N was explained by the standard
deviation of the NAO index in the rst quarter of each year (r
2
= 0.26), but this relationship failed
to reach statistical signicance (p = 0.09).
Discussion
Trophic status of widely distributed, long-lived species like leatherback turtles can be inuenced by
biological and environmental factors. Understanding the drivers of trophic status variation is
fundamental to identifying important habitats and population dynamics (Hobson 2008; Ceriani et al.
2012; Pajuelo et al. 2012). Adult leatherback !
15
N values sampled in continental shelf waters off
Nova Scotia, Canada, were signicantly higher than putative subadults (Fig. 3), and !
15
N increased
with body size (Fig. 4), but we found no signicant differences in stable isotope ratios in bulk skin
samples of turtles based on breeding stock origin (Fig. 2). Biological factors did not explain inter-
annual variation in nitrogen stable isotope values among cohorts (Fig. 6). These ndings point to
broad-scale oceanographic inuences on source !
15
N values transferred through several trophic
positions to leatherbacks, while they occupied overwintering areas in mid- to low latitudes in the
North Atlantic, and possible spatial variation in habitat use by leatherbacks prior to converging in
Canadian foraging areas. Below, we discuss these potential scenarios and highlight priorities for
future research to clarify the nature of habitat connectivity between temperate feeding areas and
tropical breeding areas for leatherbacks in the northwest Atlantic Ocean.
Nova Scotia leatherback !
15
N compared to other northwest Atlantic
feeding areas
Stable isotope values of leatherback bulk skin sampled in Nova Scotia waters were slightly different
from those reported for leatherback skin samples from Massachusetts, USA, another seasonal
feeding area south of our study site, and from northern Florida, USA, further south along the
continental shelf (Dodge et al. 2011) (Table 1). When we considered only isotope data from the
same years (20052010) as reported by Dodge et al. (2011), our !
13
C values were 0.9 higher and
our !
15
N values 0.6 lower. These discrepancies could be attributed to differences in
overwintering areas used by turtles feeding in these different areas prior to summer/fall foraging in
northwest Atlantic shelf waters (see below), but Dodge et al. (2014) showed that leatherbacks off
Massachusetts use similar overwintering areas to those occupied by leatherbacks found off Nova
Scotia (James et al. 2005a) (Fig. 1).
Alternatively, the differences between skin isotope values from Nova Scotia leatherbacks compared
to those from leatherbacks sampled in the southeast (Florida, Georgia) or northeast (Massachusetts)
USA could reect differences in the isotopic window represented by samples from each site relative
to the arrival of turtles to those sites. For example, leatherbacks feed in Southeast US waters in the
springsamples from Florida and Georgia reported by Dodge et al. (2011) were collected in March
2007and arrive in higher latitudes later in the year. Therefore, the dietary histories captured by
skin samples from these different latitudes would not reect similar time periods, but rather might
provide a more sequential view of leatherback isotope values as the foraging seasons progress
through time and space (Reich et al. 2008; Dodge et al. 2011). Likewise, leatherbacks might arrive
off the Northeast USA earlier in the summer than those off Nova Scotia, and skin isotope values
between these sites might be temporally offset in a similarly sequential way. However, Dodge et al.
(2011) reported that leatherback tissue samples were collected in JulyOctober of each year, which
is the same period that we collected samples off Nova Scotia for this study. A focused, combined
analysis of leatherback feeding areas throughout the northwest Atlanticparticularly off
Massachusetts, USA, and off Nova Scotia, Canadashould be performed to characterize
leatherback trophic ecology and migratory cycles, and to discern relationships among feeding areas
used by leatherbacks in the region.
Variation in leatherback !
15
N based on sex, maturity, and body sizes
Although we found no signicant differences in carbon and nitrogen stable isotope values in skin
from adult male and female leatherbacks sampled in Atlantic Canada, skin !
15
N was higher in adult
leatherbacks (males and females together) than in subadults (Fig. 3) and increased with body size
(Fig. 4). In contrast, Dodge et al. (2011) found no such relationships for skin stable isotope values,
but did report differences in !
13
C in whole blood, red blood cells, and blood plasma among males,
females, and turtles of unknown sex. Furthermore, the authors reported a signicant relationship
between !
15
N and body size for red blood cells and a nearly signicant relationship (p = 0.07)
between skin !
15
N and body size. Although there was some agreement between our results and
those of Dodge et al. (2011), lack of congruence was likely due to variation in incorporation rates
among tissue types, but could also suggest differences in trophic status between aggregations of
foraging leatherbacks at the two sites.
Higher !
15
N values are often interpreted as indicating higher trophic levels of consumers (DeNiro
and Epstein 1981), and positive correlations between !
15
N and body sizes can represent increased
access to higher-trophic-level prey for larger individuals, even within the same species (Barnes et al.
2008). However, leatherbacks are dietary specialists for gelatinous zooplankton throughout their
lives (Bjorndal 1997), and body sizes of turtles in this study encompassed the largest size classes for
this population (Eckert et al. 2012), so available prey sizes were probably similar for all turtles.
Isotopic differences according to sex (i.e., due to sexual size dimorphisms) and age (i.e., between
parents and offspring) have been documented in seabirds and marine mammals (e.g., Forero et al.
2002; Cherel et al. 2007), but leatherbacks do not exhibit size dimorphisms or parental care like
those species (Eckert et al. 2012). Therefore, possible, non-mutually exclusive explanations for the
signicant variations in !
15
N according to sexual maturity (i.e., adult vs. subadult) and body size
that we report here are (1) differences in isotopic incorporation rates and/or discrimination factors
related to size-dependent growth rates (Carleton and Martnez del Rio 2005; Reich et al. 2008;
Seminoff et al. 2009), and (2) effects of behavioral and physiological differences between mature
and immature individuals on stable isotope values (Hobson et al. 1993).
Considering the rst explanation, Reich et al. (2008) conrmed signicant effects of somatic growth
rates on stable isotope discrimination factors and incorporation rates in multiple tissues of young
loggerhead sea turtles, a notion also postulated for leatherbacks by Seminoff et al. (2009).
Leatherbacks, like most reptiles, exhibit indeterminate growth, with growth rates decreasing with
body size, even among large animals (Price et al. 2004), and reaching nearly asymptotic limits at
approximately 140 cm CCL (Jones et al. 2011). Carleton and Martnez del Rio (2005) reported an
allometric relationship between isotopic incorporation rate and body size in birds, and Reich et al.
(2008) suggested that isotopic incorporation rates might be size dependent for animals with
indeterminate growth. For these reasons, we suggest that different size-dependent growth rates
among turtles in our study might have inuenced isotopic incorporation rates and resulting stable
isotope values in leatherback skin according to differences in body sizes.
In addition to effects of size-dependent growth rates, differences in !
15
N between subadults and
larger adults might also indicate differences in behavior and physiology based on reproductive
status. James et al. (2005a) and Dodge et al. (2014) described different migratory routes exhibited
by subadults, non-breeding females, breeding females, and males, wherein adultsparticularly
those in a breeding yearmigrate all the way to breeding areas in the Wider Caribbean, whereas
putative subadults make a similar southward migration to lower latitudes, but do not make the full
journey to breeding areas. Furthermore, physiological demands of reproductione.g., migration,
egg production and deposition (for females), and fasting during the breeding seasoncould cause
enrichments in !
15
N in breeding adults, particularly females, as shown in birds (Hobson et al. 1993).
Therefore, differences in migratory routes and habitat use, especially if accompanied by
physiological differences according to reproductive maturity and status, might underlie the isotopic
differences between adult and subadult leatherbacks in our study (Barnes et al. 2008; Hobson 2008;
Bowen 2010; Flaherty and Ben-David 2010). Analyses of multiple tissue types and samples from
multiple sites during different points in leatherback migration and reproduction cycles might clarify
possible relationships between breeding status, maturity stages, and trophic status.
Inter-annual variation in leatherback stable isotope values
We found signicant inter-annual variation in !
13
C and !
15
N (Fig. 6) that was not explained by
inter-annual variation in body sizes, proportions of adults to putative subadults, or proportions of
breeding stocks present in yearly leatherback cohorts. However, inter-annual variation in !
13
C was
signicant for only three years (20072009; Fig. 6) and appeared to be due at least in part to the
signicant effect of %C on !
13
C in leatherback skin samples and, in particular, the signicantly low
%C in 2007. We have no biological explanation for these values, and there were no technical issues
with the mass spectrometry analyses with these particular samples (J. Curtis, University of Florida,
pers. comm.). Without %C values from 2008, and very small sample sizes from 2005 and 2006, we
were unable to evaluate whether inter-annual variation in !
13
C that we report here was due to
variation in %C or some other factor.
Overall, the low variation in !
13
C compared with variation in !
15
N in our samples likely reects the
relatively constrained latitudinal distribution of oceanic overwintering areas used by leatherbacks
sampled in Nova Scotian waters (James et al. 2005a, b) (Fig. 1). !
13
C gradients have been
documented from nearshore to offshore areas and across latitudes in marine ecosystems (Reich et al.
2007; Bowen 2010). Similar to our present ndings, Wallace et al. (2006a) reported low variation in
!
13
C values of leatherback tissues from two separate nesting stocks and concluded that these results
were due to the oceanic nature of leatherback migration and foraging. Analyses of tissues reecting
different temporal windows, and/or of turtles at different stages of migration, might capture habitat-
based variation in !
13
C values that reect incorporation of carbon across a wider breadth of the !
13
C
range in marine ecosystems.
In the case of !
15
N, inter-annual variation can indicate either broad-scale oceanographic changes
that affect all turtles in a given cohort (Saba et al. 2007), variation in habitat-derived isotope values
related to variation in habitat use (Flaherty and Ben-David 2010), or a combination of the two.
Wallace et al. (2006a) surmised that signicant differences in !
15
N values between East Pacic and
northwest Atlantic leatherbacks were not due to differences in trophic position because leatherbacks
are considered dietary specialists globally (Bjorndal 1997; Eckert et al. 2012), but rather to
differences in baseline, or source !
15
N values in foraging areas used by each population. The authors
suggested that source !
15
N differences in the two trophic systems were driven by distinct nitrogen
cycling regimes that result in elevated !
15
N values in the East Pacic due to high levels of
denitrication and depressed !
15
N values in the North Atlantic due to high levels of N
2
xation
(Gruber and Sarmiento 1997). Pajuelo et al. (2010) implicated the same dynamic as the driver for
!
15
N differences between loggerhead populations from the same two regions. Similarly, Seminoff et
al. (2012) combined bulk (i.e., total tissue) and compound-specic stable isotope analyses of amino
acids (AA-CSIA) with satellite telemetry to determine that cohorts of western Pacic leatherbacks
from the same breeding stock exhibited a dichotomy in foraging behavior that was due to
differences in source !
15
N in distinct foraging areas.
Extending these ideas to the present study, it is possible that inter-annual variation in leatherback
!
15
N values reects uctuations in N
2
xation rates, i.e., source !
15
N values in overwintering areas
occupied by leatherbacks before they move into continental shelf waters off Nova Scotia in the
following summer. Previous studies using satellite telemetry to track the long-term and long-
distance movements of leatherbacks in the North Atlantic have shown that non-breeding
leatherbacks appear to overwinter in open-ocean, tropical/subtropical areas (e.g., James et al. 2005a;
Dodge et al. 2014) (Fig. 1). In a recent synthesis of available stable isotope data used to create
isoscapes for the Atlantic Ocean, this region was generally characterized by depleted !
15
N values
(McMahon et al. 2013), probably due to high N
2
xation (Gruber and Sarmiento 1997; Hood et al.
2001; Montoya et al. 2002). Thus, inter-annual variations in leatherback !
15
N values among cohorts
might mirror patterns of broad-scale oceanographic variability that drive uctuations in the degree
of N
2
xation relative to other processes that make nitrogen available to oceanic marine food webs
in the North Atlanticand thus baseline !
15
Nin the overwintering areas occupied by
leatherbacks. The narrow range of !
13
C values among leatherbacks in this study also suggests
common geographic foraging areas across years (Figs. 2, 6), which would enable environmental
variability to affect all turtles in a similar way.
Iron availability governs uctuations in N
2
xation, which means that iron from airborne dust or
riverine inputs is a strong determinant of the level of N
2
xation (Berman-Frank et al. 2001). In the
North Atlantic, in particular, consistent delivery of airborne dust from the Sahara desert provides
iron that is used by diazotrophic organisms (e.g., Trichodesmium) to x atmospheric nitrogen
(Berman-Frank et al. 2001; Hood et al. 2001). However, this process varies seasonally as well as
inter-annually, possibly in relation to the North Atlantic Oscillation (Hood et al. 2001), which likely
means that N
2
xation also tracks the variation in iron input via airborne dust to the North Atlantic
Ocean. However, we found no relationship between the NAO index and inter-annual variation in
leatherback !
15
N. It is likely that this comparison was too crude to detect a signicant pattern, given
the several intermediate and complex processes between the NAO and leatherback stable isotope
values. Other oceanographic indices and processes that govern broad-scale climate patterns in the
region (e.g., Atlantic Multi-decadal Oscillation, positions of the Gulf Stream and Labrador Current;
Townsend et al. 2006) could also play a role in inuencing food web dynamics that manifest in
variation in leatherback stable isotope values and deserve further attention.
In addition to oceanographic factors, there are other potential explanations for the inter-annual
variations in leatherback !
15
N we report here. For example, variation in leatherback habitat use, and
associated variation in !
15
N among habitats, could explain this pattern. Inter- and intraspecic
variation in stable isotope values have been linked to differential habitat use and trophic status in
seabirds and marine mammals (Forero et al. 2002; Cherel et al. 2007; Jaeger et al. 2013), as well as
marine turtles (Hatase et al. 2002; Ceriani et al. 2012; Pajuelo et al. 2012; Seminoff et al. 2012). If
different overwintering areas used by leatherbacks within as well as across years had different
baseline !
15
N values, nitrogen stable isotope values among annual foraging cohorts sampled in
Nova Scotia could have differed accordingly. In fact, although most leatherbacks tracked to date
overwintered in the generalized oceanic area depicted in Fig. 1, some leatherbacks have been
observed to overwinter in North American shelf habitats (James et al. 2005a; K. Dodge, pers
comm), which could cause both !
15
N and !
13
C values to vary signicantly between oceanic and
shelf areas (Reich et al. 2007; McMahon et al. 2013). A more thorough analysis of habitat use
among leatherbacks prior to their migration to the North American continental shelf for summer/fall
foraging in the context of higher spatiotemporal resolution in isoscape values from those areas
would elucidate this possibility.
Another possible explanation for inter-annual variation in leatherback !
15
N values is variation in
food web dynamics, e.g., trophic status of leatherback prey. Gelatinous zooplankton as a group
exhibits diverse feeding strategies ranging from herbivorous planktivory (e.g., Aurelia aurita) to at
least partial piscivory (e.g., Stomolophus spp., Chrysaora spp.), and their rapid ontogeny and growth
and exible life history demands allow them to thrive in ephemeral and challenging oceanographic
and trophic conditions (Richardson et al. 2009; Lilley et al. 2011). Therefore, variation in trophic
positions of jellies due to availability, abundance, or distribution of their own prey items and/or
variation in leatherback diet composition might have inuenced the inter-annual variation in
leatherback !
15
N values. There is a general lack of understanding at present about trophic ecology
and position among jellysh species, particularly in the North Atlantic, despite growing interest in
ecological impacts of these species on marine ecosystems (Richardson et al. 2009; Lilley et al.
2011). To clarify whether variation in trophic status of leatherback prey might have inuenced
patterns we report here, we recommend analysis of samples from multiple jellysh species from
areas with potentially different isotopic baselines (e.g., shelf vs. offshore habitats; Dodge et al.
2011).
To distinguish among these possibilities, compound-specic stable isotope analyses of amino acids
(AA-CSIA) could be performed to accompany and interpret results from bulk (total tissue) isotope
analyses. This technique is used to determine whether variation in bulk isotope values is due to
differences in baseline isotope values or differences in trophic position and has been used in several
studies of trophic status of marine consumers (see McMahon et al. 2013 for review), including sea
turtles (Seminoff et al. 2012; Vander Zanden et al. 2013). We recommend future research that
integrates analysis of relevant oceanographic processes with results of AA-CSIA and bulk isotope
analyses to distinguish between source and trophic inuences on leatherback stable isotope
signatures and provide a more detailed picture of leatherback trophic ecology.
Connectivity between temperate feeding areas and tropical breeding
areas
In general, improved characterizations of connectivity among breeding and feeding areasand the
migratory routes that link themused by leatherbacks in the northwest Atlantic are critical to
understanding leatherback trophic ecology, life history, and population dynamics in this region.
Stable isotope analysis of animal tissues interpreted in the context of marine isoscapes can be a
powerful combination for inferring linkages between distinct habitats utilized by migratory species
(McMahon et al. 2013). The ability to distinguish among habitats using stable isotope analyses of
marine turtles, in particular, provides valuable information about life history variability, differential
habitat quality, and consequences for otherwise cryptic population dynamics detected on nesting
beaches (NRC 2010; Zbinden et al. 2011; Ceriani et al. 2012; Pajuelo et al. 2012).
We found no signicant variation in stable isotope values of leatherback skin sampled in Canadian
waters according to breeding stock origin, which could reect the homogenization of distinct
isotopic signatures following extended periods on common foraging areas away from distinct
breeding areas. This possibility is supported by the stable isotope values of two turtles that were
captured in Nova Scotia during the same calendar year that they had been conrmed to be nesting in
the Wider Caribbean (one in St. Croix, USVI, and the other in Trinidad), as they had relatively
higher !
15
N (12.7 and 11.8 ) and lower !
13
C (#17.2 and #17.7 ) values than turtles in other
remigration year groups (!
15
N means: 10.611.2 ; !
13
C: #17.2 to #16.9 ) (Fig. 5). While noting
the small sample size, this observation might illustrate different isotopic histories based on
reproductive status, which could allow assignment of nesting turtles to distinct foraging areas,
assuming that isotopic signatures of slow-turnover tissues (e.g., skin and red blood cells) from
nesting turtles reect resources incorporated while feeding; this idea has considerable support
already (Caut et al. 2008; Pajuelo et al. 2012; Ceriani et al. 2012; Vander Zanden et al. 2013).
Stable isotope analyses of multiple tissue types with varying isotopic turnover rates reecting
different time periods could be used together as an isotopic clock to infer transitions by individual
turtles among different habitats over time (Reich et al. 2008). Dodge et al. (2011) used stable isotope
values of blood plasma, which has a fast turnover rate (Reich et al. 2008), to infer trophic status of
leatherbacks in a temperate foraging area off the northeastern USA and compared these isotope
values to those of other tissue types with slower turnover rates to piece together longer dietary
histories among sexes, body sizes, and maturity stages. As a next step, we recommend stable isotope
analyses of multiple leatherback tissues collected from several nesting sites (and breeding stocks)
and foraging areas across several years in the temperate and tropical North Atlantic (TEWG 2007;
Fossette et al. 2010b) to capture trophic variability within nesting and foraging cohorts in relation to
reproduction and remigration cycles. Such an approachsimilar to a mixed-stock genetic analysis
(e.g., Bolker et al. 2007)would provide a more holistic view of leatherback trophic ecology and
connectivity among habitats and would enhance ongoing management efforts in the northwest
Atlantic. Overall, our results demonstrate the importance of interpreting site-scale studies in broad-
scale contexts to adequately assess population status and dynamics of widely distributed, highly
migratory species like leatherbacks.
Acknowledgments
The work was supported by Canadian Wildlife Federation, Environment Canada, Fisheries and Oceans Canada,
Habitat Stewardship Program for Species at Risk, National Fish and Wildlife Foundation (USA), and the Natural
Sciences and Engineering Research Council of Canada. Fieldwork in Canada was conducted in association with
the Canadian Sea Turtle Network, and in accordance with guidelines of the Canadian Council on Animal Care,
with review and approval by the Dalhousie University Animal Care Committee (permit numbers 00008, 02053,
04055, 06069, 07077, 08077, 09069 and 11073) and Fisheries and Oceans Canada (license and permit
numbers 2001425, 2002550, 2003534, 2004519, MAR-SA-2004004, 2005557, MAR-SA-2006006,
2006526, MARSA-2006006, 2007024, MAR-SA-2007006, 2008454, MAR-SA-2008006, 323395, 323398,
326240 and 332697). Samples were imported into the USA over a span of 10 years under CITES permit 844694/9
and were archived in the NOAA Southwest Fisheries Science Center Marine Mammal and Turtle Molecular
Research Sample Collection. We thank employees and volunteers of the Canadian Sea Turtle Network and
members of its eld research team, including D. Archibald, L. Bennett, B. Fricker, H. Fricker, K. Fricker, K.
Hamelin, P. MacDonald, K. Martin, B. Mitchell, and M. Nicholson for collection and organization of samples and
other data used in this study. We are grateful to Erin LaCasella (NOAA SWFSC) and D. Archibald (CSTN) for
assistance with sample preparation and shipping. We thank P. Dutton, S. Roden, and K. Stewart (NOAA SWFSC)
for providing critical insights on stock assignments of Canadian turtles based on distinct northwest Atlantic
leatherback breeding stocks. We also thank J. Curtis at the University of Florida for conducting the mass
spectrometry analyses, V. Saba and K. McMahon for helpful discussions, and K. Dodge and an anonymous
reviewer for helpful comments that improved the manuscript.
References
Barnes C, Jennings S, Polunin NVC, Lancaster JE (2008) The importance of quantifying inherent
variability when interpreting stable isotope eld data. Oecologia 155:227235
CrossRef
Barrow LM, Bjorndal KA, Reich KJ (2008) Effects of preservation method on stable carbon and
nitrogen isotope values. Physiol Biochem Zool 81:688693
CrossRef
Bearhop S, Adams CE, Waldron S, Fuller RA, MacLeod H (2004) Determining trophic niche width:
a novel approach using stable isotope analysis. J Anim Ecol 73:10071012
CrossRef
Bearhop S, Phillips RA, McGill R, Cherel Y, Dawson DA, Croxall JP (2006) Stable isotopes
indicate sex-specic and long-term individual foraging specialisation in diving seabirds. Mar Ecol
Prog Ser 311:157164
CrossRef
Berman-Frank I, Cullen JT, Shaked Y, Sherrell RM, Falkowski PG (2001) Iron availability, cellular
iron quotas, and nitrogen xation in Trichodesmium. Limnol Oceanogr 46:12491260
CrossRef
Bjorndal KA (1997) Foraging ecology and nutrition of sea turtles. In: Lutz PL, Musick JA (eds) The
biology of sea turtles. CRC Press, Boca Raton, pp 199232
Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic
ecology. Ann Rev Ecol Evol Syst 42:411440
CrossRef
Bolker BM, Okuyama T, Bjorndal KA, Bolten AB (2007) Incorporating multiple mixed stocks in
mixed stock analysis: many-to-many analyses. Mol Ecol 16:685695
CrossRef
Bowen GJ (2010) Isoscapes: spatial pattern in isotopic biogeochemistry. Ann Rev Ecol Evol Syst
38:161187
Broderick AC, Godley BJ, Hays GC (2001) Trophic status drives interannual variability in nesting
numbers of marine turtles. Proc R Soc Lond B 268:14811487
CrossRef
Carleton SA, Martnez del Rio C (2005) The effect of cold-induced increased metabolic rate on the
rate of 13C and 15 N incorporation in house sparrows (Passer domesticus). Oecologia 114:226232
CrossRef
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. doi:10. 1371/journal. pone.
0001845
CrossRef
Ceriani SA, Roth JD, Evans DR, Weishampel JF, Ehrhart LM (2012) Inferring foraging areas of
nesting loggerhead turtles using satellite telemetry and stable isotopes. PLoS ONE 7(9):e45335.
doi:10.1371/journal. pone. 0045335
CrossRef
Cherel Y, Hobson KA, Guinet C, Vanpe C (2007) Stable isotopes document seasonal changes in
trophic niches and winter foraging individual specialization in diving predators from the Southern
Ocean. J Anim Ecol 76:826836
CrossRef
DeNiro MJ, Epstein S (1981) Inuence of diet on the distribution of nitrogen isotopes in animals.
Geochim Cosmochim Acta 45:341351
CrossRef
Dodge KL, Logan JM, Lutcavage ME (2011) Foraging ecology of leatherback sea turtles in the
Western North Atlantic determined through multi-tissue stable isotope analyses. Mar Biol
158:28132824
CrossRef
Dodge KL, Galuardi B, Miller TJ, Lutcavage ME (2014) Leatherback turtle movements, dive
behavior, and habitat characteristics in ecoregions of the Northwest Atlantic Ocean. PLoS ONE
9(3):e91726. doi:10.1371/journal. pone. 0091726
CrossRef
Dutton PH, Roden SE, Stewart KR, LaCasella E, Tiwari M, Formia A, Thom JA, Livingstone SR,
Eckert S, Chacn-Chaverri D, Rivalan P, Allman P (2013) Population stock structure of leatherback
turtles (Dermochelys coriacea) in the Atlantic revealed using mtDNA and microsatellite markers.
Conserv Genet. doi:10. 1007/s10592-013-0456-0
Eckert SA, Bagley D, Kubis S, Ehrhart L, Johnson C, Stewart K, DeFreese D (2006) Internesting
and postnesting movements and foraging habitats of leatherback sea turtles (Dermochelys coriacea)
nesting in Florida. Chel Cons Biol 5:239248
CrossRef
Eckert KL, Wallace BP, Frazier JG, Eckert SA, Pritchard PCH (2012) Synopsis of the biological
data on the leatherback sea turtle, Dermochelys coriacea (Vandelli, 1761). US Fish and Wildlife
Service PO no. 20181-0-0169, Jacksonville, FL, pp 214
Flaherty EA, Ben-David M (2010) Overlap and partitioning of the ecological and isotopic niches.
Oikos 119:14091416
CrossRef
Flemming NEC, Houghton JDR, Magill CL, Harrod C (2011) Preservation methods alter stable
isotope values in gelatinous zooplankton: implications for interpreting trophic ecology. Mar Biol
158:21412146
CrossRef
Forero MG, Bortolotti GR, Hobson KA, Donazar JA, Bertelloti M, Blanco G (2002) High trophic
overlap within the seabird community of Argentinian Patagonia: a multiscale approach. J Anim Ecol
73:789801
CrossRef
Fossette S, Hobson VJ, Girard C, Calmettes B, Gaspar P, Georges J-Y, Hays GC (2010a) Spatio-
temporal foraging patterns of a giant zooplanktivore, the leatherback turtle. J Mar Syst 81:225234
CrossRef
Fossette S, Girard C, Lpez-Mendilaharsu M, Miller P, Domingo A, Evans D, Kelle L, Plot V,
Prosdocimi L, Verhage S, Gaspar P, Georges J-Y (2010b) Atlantic leatherback migratory paths and
temporary residence areas. PLoS ONE 5(11):e13908. doi:10. 1371/journal. pone. 0013908
CrossRef
Gruber N, Sarmiento JL (1997) Global patterns of marine nitrogen xation and denitrication.
Global Biogeochem Cycles 11:235266
CrossRef
Hatase H, Takai N, Matsuzawa Y, Sakamoto W, Omuta K, Goto K, Arai N, Fujiwara T (2002) Size-
related differences in feeding habitat use of adult female loggerhead turtles Caretta caretta around
Japan determined by stable isotope analysis and satellite telemetry. Mar Ecol Prog Ser 233:273281
CrossRef
Heaslip SG, Iverson SJ, Bowen WD, James MJ (2012) Jellysh support high energy intake of
leatherback sea turtles (Dermochelys coriacea): video evidence from animal-borne cameras. PLoS
ONE 7(3):e33259. doi:10.1371/journal. pone. 0033259
CrossRef
Hobson KA (2008) Applying isotopic methods to tracking animal movements. In: Hobson KA,
Wassenaar LI (eds) Tracking animal migration with stable isotopes. Academic Press, Elsevier,
London, pp 4578
CrossRef
Hobson KA, Norris DR (2008) Animal migration: a context for using new techniques and
approaches. In: Hobson KA, Wassenaar LI (eds) Tracking animal migration with stable isotopes.
Academic Press, Elsevier, London, pp 120
CrossRef
Hobson KA, Alisauskas RT, Clark RG (1993) Stable nitrogen isotope enrichment in avian tissues
due to fasting and nutritional stress: implications for isotopic analyses of diet. Condor 95:388394
CrossRef
Hood RR, Bates NR, Capone DG, Olson DB (2001) Modeling the effect of nitrogen xation on
carbon and nitrogen uxes at BATS. Deep-Sea Res II 48:16091648
CrossRef
Jaeger A, Jaquemet S, Phillips RA, Wanless RM, Richard P, Cherel Y (2013) Stable isotopes
document inter-and intra-specic variation in feeding ecology of nine large southern
Procellariiformes. Mar Ecol Prog Ser 490:255266
CrossRef
James MC, Herman TB (2001) Feeding of Dermochelys coriacea on medusae in the northwest
Atlantic. Chelonian Conserv Biol 4:202205
James MC, Myers RA, Ottensmeyer CA (2005a) Behaviour of leatherback sea turtles, Dermochelys
coriacea, during the migratory cycle. Proc R Soc B 272:15471555
CrossRef
James MC, Ottensmeyer CA, Myers RA (2005b) Identication of high-use habitat and threats to
leatherback sea turtles in northern waters: new directions for conservation. Ecol Lett 8:195201
CrossRef
James MC, Eckert SA, Myers RA (2005c) Migratory and reproductive movements of male
leatherback turtles (Dermochelys coriacea). Mar Biol 147:845853
CrossRef
James MC, Sherrill-Mix SA, Martin K, Myers RA (2006) Canadian waters provide critical foraging
habitat for leatherback sea turtles. Biol Conserv 133:347357
CrossRef
James MC, Sherrill-Mix SA, Myers RA (2007) Population characteristics and seasonal migrations of
leatherback sea turtles at high latitudes. Mar Ecol Prog Ser 337:245254
CrossRef
Jones TT, Hastings MD, Bostrom BL, Pauly D, Jones DR (2011) Growth of captive leatherback
turtles, Dermochelys coriacea, with inferences on growth in the wild: implications for population
decline and recovery. J Exp Mar Biol Ecol 399:8492
CrossRef
Kojadinovic J, Richard R, Le Corre M, Cosson RP, Bustamante P (2008) Effects of lipid extraction
on !
13
C and !
15
N values in seabird muscle, liver and feathers. Waterbirds 31:169178
CrossRef
Lilley MKS, Beggs SE, Doyle TK, Hobson VJ, Stromberg KHP, Hays GC (2011) Global patterns of
epipelagic gelatinous zooplankton biomass. Mar Biol. doi:10. 1007/s00227-011-1744-1
McMahon KW, Hamady LL, Thorrold SR (2013) A review of ecogeochemistry approaches to
estimating movements of marine animals. Limnol Oceanogr 58:697714
CrossRef
Montoya JP, Carpenter EJ, Capone DG (2002) Nitrogen xation and nitrogen isotope abundances in
zooplankton of the oligotrophic North Atlantic. Limnol Oceanogr 47:16171628
CrossRef
National Research Council (NRC) (2010) Assessment of sea turtle status and trends: integrating
demography and abundance. National Academies Press, Washington DC
Pajuelo M, Bjorndal KA, Alfaro-Shigueto J, Seminoff JA, Mangel JC, Bolten AB (2010) Stable
isotope variation in loggerhead turtles reveals Pacic-Atlantic oceanographic differences. Mar Ecol
Progr Ser 417:277285
CrossRef
Pajuelo M, Bjorndal KA, Reich KJ, Vander Zanden HB, Hawkes LA, Bolten AB (2012) Assignment
of nesting loggerhead turtles to their foraging areas in the Northwest Atlantic using stable isotopes.
Ecosphere 3(10):89. doi:10. 1890/ES12-00220. 1
CrossRef
Plot V, Jenkins T, Robin JP, Fossette S, Georges JY (2014) Leatherback turtles are capital breeders:
morphometric and physiological evidence from longitudinal monitoring. Physiol Biochem Zool
86:385397
CrossRef
Price ER, Wallace BP, Reina RD, Spotila JR, Paladino RV, Piedra R, Vlez E (2004) Size, growth,
and reproductive output of adult female leatherbacks Dermochelys coriacea. Endang Species Res
5:18
Reich KJ, Bjorndal KA, Bolten AB (2007) The lost years of green turtles: using stable isotopes to
study cryptic lifestages. Biol Lett 3:714721
Reich KJ, Bjorndal KA, Martnez del Rio C (2008) Effects of growth and tissue type on the kinetics
of
13
C and
15
N incorporation in a rapidly growing ectotherm. Oecologia 155:651663
CrossRef
Richardson AJ, Bakun A, Hays GC, Gibbons MJ (2009) The jellysh joyride: causes, consequences,
and management responses to a more a gelatinous future. TREE. doi:10. 1016/j. tree. 2009. 01. 010
Saba VS, Santidrin-Tomillo P, Reina RD, Spotila JR, Musick JA, Evans DA, Paladino FV (2007)
The effect of the El Nio Southern Oscillation on the reproductive frequency of eastern Pacic
leatherback turtles. J Appl Ecol 44:395404
CrossRef
Saba VS, Shillinger GL, Spotila JR, Chavez FP, Musick JA (2008) Bottom-up and climatic forcing
on the worldwide population of leatherback turtles. Ecology 89:14141427
CrossRef
Seminoff JA, Jones TT, Eguchi T, Hastings M, Jones DR (2009) Stable carbon and nitrogen isotope
discrimination in soft tissues of the leatherback turtle (Dermochelys coriacea): insights for trophic
studies of marine turtles. J Exp Mar Biol Ecol 381:3341
CrossRef
Seminoff JA, Benson SR, Arthur KE, Eguchi T, Dutton PH, Tapilatu RF, Popp BN (2012) Stable
isotope tracking of endangered sea turtles: validation with satellite telemetry and !
15
N analysis of
amino acids. PLoS ONE 7:e37403. doi:10. 1371/journal. pone. 0037403
CrossRef
Sherril-Mix SA, James MC, Myers RA (2007) Migration cues and timing in leatherback turtles.
Behav Ecol 19:231236
CrossRef
Sotiropoulos MA, Tonn WM, Wassenaar LI (2004) Effects of lipid extraction on stable carbon and
nitrogen isotope analyses of sh tissues: potential consequences for food web studies. Ecol Freshw
Fish 13:155160
CrossRef
Stewart K, Johnson C, Godfrey MH (2007) The minimum size of leatherbacks at reproductive
maturity, with a review of sizes for nesting females from the Indian, Atlantic, and Pacic Ocean
basins. Herp J 17:123128
Stewart KR, James MC, Roden S, Dutton PH (2013) Assignment tests, telemetry and tag-recapture
data converge to identify natal origins of leatherback turtles foraging in Atlantic Canadian waters. J
Anim Ecol. doi:10.1111/1365-2656. 12056
Suryan RM, Saba VS, Wallace BP, Hatch SA, Frederiksen M, Wanless S (2009) Environmental
forcing on life history strategies: evidence for multi-trophic level responses at ocean basin scales.
Progr Oceanogr 81:214222. doi:10. 1016/J. Pocean. 04. 012
CrossRef
Sweeting CJ, Polunin NVC, Jennings S (2006) Effects of chemical lipid extraction and arithmetic
lipid correction on stable isotope ratios of sh tissues. Rapid Commun Mass Spectrom 20:595601
CrossRef
Townsend DW, Thomas AC, Mayer LM, Thomas MA, Quinlan JA (2006) Oceanography of the
Northwest Atlantic continental shelf (1 W). In: Robinson AR, Brink KH (eds) The Sea: The Global
Coastal Ocean: Interdisciplinary Regional Studies and Syntheses. Harvard University Press,
Cambridge, pp 119168
Turtle Expert Working Group (TEWG) (2007) An assessment of the leatherback turtle population in
the Atlantic Ocean. NOAA Technical Memorandum NMFS-SEFSC-555, pp 116
Vander Zanden HB, Arthur KA, Bolten AB, Popp BN, Lagueux CJ, Harrison E, Campbell CL,
Bjorndal KA (2013) Trophic ecology of a green turtle breeding population. Mar Ecol Prog Ser
476:237249
CrossRef
Wallace BP, Seminoff JA, Kilham SS, Spotila JR, Dutton PH (2006a) Leatherback turtles as
oceanographic indicators: stable isotope analyses reveal a trophic dichotomy between ocean basins.
Mar Biol 149:953960
CrossRef
Wallace BP, Kilham SS, Paladino FV, Spotila JR (2006b) Energy budget calculations indicate
resource limitation in Eastern Pacic leatherback turtles. Mar Ecol Prog Ser 318:263270
CrossRef
Wallace BP, DiMatteo AD, Bolten AB, Chaloupka MY, Hutchinson BJ et al (2011) Global
conservation priorities for marine turtles. PLoS ONE 6(9):e24510. doi:10. 371/journalpone. 0024510
CrossRef
Zbinden JA, Bearhop S, Bradshaw P, Gill B, Margaritoulis D, Newton J, Godley BJ (2011)
Migratory dichotomy and associated phenotypic variation in marine turtles revealed by satellite
tracking and stable isotope analysis. Mar Ecol Progr Ser 421:291302
CrossRef
Over 8.5 million scientic documents at your ngertips
Springer, Part of Springer Science+Business Media