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Isotopic niche width differentiation between common bottlenose dolphin ecotypes and sperm whales in the Gulf of California

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World populations or stock distinction of Tursiops truncatus has been difficult to assess, because of large variations in morphology, habitat, feeding habits, and social structure among areas, which may reflect phylogenetic segregation or ecological plasticity. In the Gulf of California, Mexico, two common bottlenose dolphin ecotypes (inshore and offshore) have been reported. The offshore ecotype is frequently observed in association with sperm whales (Physeter macrocephalus) but the reason for this is still unknown. To explore the degree of resource partitioning/overlap between these species and stocks, we used skin stable isotope values (δ13C, δ15N) to estimate quantitative metrics of isotopic niche width (Bayesian standard ellipse areas, SEAB) and estimated their diet composition using Bayesian isotopic mixing models. The inshore ecotype in different regions (north, central, and south) of the Gulf of California exhibited distinct δ15N values and SEAB, suggesting a latitudinal gradient in nitrogen sources of coastal localities. The SEAB of inshore and offshore bottlenose dolphin ecotypes was completely distinct, indicating resource partitioning. Associated offshore ecotype and sperm whales had overlapping SEAB. The isotopic mixing model indicates that a considerable proportion of both species’ diet is large Humbolt squid. Our results suggest that resource partitioning and species association are two strategies that bottlenose dolphin ecotypes use in this zone.
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MARINE MAMMAL SCIENCE, **(*): ***–*** (*** 2017)
©2017 Society for Marine Mammalogy
DOI: 10.1111/mms.12465
Isotopic niche width differentiation between common
bottlenose dolphin ecotypes and sperm whales in the Gulf
of California
RA
UL E. D
IAZ-GAMBOA,Instituto Politecnico Nacional, Centro Interdisciplinario de Cien-
cias Marinas, Avenida IPN s/n Colonia Playa Palo de Santa Rita, CP 23096, La Paz, Baja Cali-
fornia Sur, Mexico and Campus de Ciencias Biologicas y Agropecuarias-UADY, Km. 15.5
Merida-Xmatkuil AP. 4-116 Itzimna, Merida, Yucatan, Mexico; DIANE GENDRON,
1
and
GERALDINE BUSQUETS-VASS,Instituto Politecnico Nacional, Centro Interdisciplinario de
Ciencias Marinas, Avenida IPN s/n Colonia Playa Palo de Santa Rita, CP 23096, La Paz, Baja
California Sur, Mexico.
Abstract
World populations or stock distinction of Tursiops truncatus has been diffi-
cult to assess, because of large variations in morphology, habitat, feeding
habits, and social structure among areas, which may reflect phylogenetic segre-
gation or ecological plasticity. In the Gulf of California, Mexico, two common
bottlenose dolphin ecotypes (inshore and offshore) have been reported. The off-
shore ecotype is frequently observed in association with sperm whales (Physeter
macrocephalus) but the reason for this is still unknown. To explore the degree
of resource partitioning/overlap between these species and stocks, we used skin
stable isotope values (d
13
C, d
15
N) to estimate quantitative metrics of isotopic
niche width (Bayesian standard ellipse areas, SEA
B
) and estimated their diet
composition using Bayesian isotopic mixing models. The inshore ecotype in
different regions (north, central, and south) of the Gulf of California exhibited
distinct d
15
N values and SEA
B
, suggesting a latitudinal gradient in nitrogen
sources of coastal localities. The SEA
B
of inshore and offshore bottlenose dol-
phin ecotypes was completely distinct, indicating resource partitioning. Associ-
ated offshore ecotype and sperm whales had overlapping SEA
B
. The isotopic
mixing model indicates that a considerable proportion of both species’ diet is
large Humbolt squid. Our results suggest that resource partitioning and spe-
cies association are two strategies that bottlenose dolphin ecotypes use in this
zone.
Key words: trophic relationships, isotopic niche width, bottlenose dolphin, Tursiops
truncatus, sperm whale, Physeter macrocephalus, Humbolt squid, Dosidicus gigas.
The bottlenose dolphin, Tursiops truncatus (Montagu 1821), exhibits a world-
wide distribution, with the exception of polar regions, and can be found from
inshore waters to the open ocean. Two ecotypes, inshore and offshore, have
1
Corresponding author (e-mail: dianegendroncicimar@gmail.com).
1
440
MARINE MAMMAL SCIENCE, 34(2): 440–457 (April 2018)
V
C2017 Society for Marine Mammalogy
DOI: 10.1111/mms.12465
been reported in various oceans. The ecotypes differ in coloration pattern, body
size, pectoral and dorsal fin size, parasites, cranial characteristics, as well as
physiological and genetic traits (Walker 1981, Hersh and Duffield 1990, Mead
and Potter 1990, Waerebeek et al. 1990, Torres et al. 2003). These differences
reflect adaptations to different habitats and feeding habits. The occurrence of
these ecotypes has been proposed for the Gulf of California based on genetic
studies (Segura et al. 2006) that show a low mutation rate, suggesting a recent
divergence between them.
The bottlenose dolphin has been described as an opportunistic top predator (Norris
and Prescott 1961, Shane et al. 1986, Barros and Odell 1990). In general, the off-
shore ecotype includes a larger percentage of cephalopods in its diet than the inshore
ecotype (Clarke 1986, Cockcroft and Ross 1990, Gonzalez et al. 1994, Barros et al.
2000), similar to other teuthophagous cetaceans, such as the long-finned pilot whale,
Globicephala melas, Risso’s dolphin, Grampus griseus, and the pigmy sperm whale,
Kogia breviceps (Walker et al. 1999). This similarity in their diet could lead bottlenose
dolphins to associate with larger cetaceans (Norris and Prescott 1961), possibly to
increase feeding success (Querouil et al. 2008), although the behavioral basis of these
associations is not well understood. In the Gulf of California, bottlenose dolphins are
commonly associated with Risso’s dolphins, short-finned pilot whales, G. macro-
rhynchus, and sperm whales, P. macrocephalus, (Mangels and Gerrodette 1994, Jaquet
and Gendron 2002). Dietary comparisons between bottlenose dolphins and associated
teuthophagous cetaceans are necessary to determine if these species are feeding on the
same prey.
Most of the trophic information on these ecotypes has been inferred from
field observations and stomach and feces content analysis (Cockcroft and Ross
1990, Waerebeek et al. 1990, Barros et al. 2000). These analyses have the
advantage of providing information about the most recent prey consumed,
but may generate biases in the overall diet information due to sickness or
fasting, especially in stranded animals (Barros and Odell 1990, Dunshea et al.
2013). Stable isotope abundances are useful for the understanding of feeding
relationships and trophic positions in aquatic ecosystems (Peterson and Fry
1987, Hobson and Welch 1992, Rau et al. 1992). The consumer’s body com-
position signal reflects the food ingested, assimilated and integrated over
time, but varies depending on the tissue used and its respective metabolic
and turnover rate (Tieszen et al. 1983, Hobson et al. 1994). Due to the fact
that there is a selective retention of heavier isotopes and an excretion of the
lighter ones, animals have higher d
13
C and d
15
N values than their diet
(Peterson and Fry 1987, Das et al. 2000). The d
15
N enrichment between
cetacean skin and the prey consumed is estimated to be from 1.57&to
2.82&, while that for d
13
C is estimated to be from 1.01&to 1.28&(Bor-
rell et al. 2012, Gimenez et al. 2016). The d
13
C is also used to better under-
stand the relative dietary contributions from various primary carbon sources
exploited by consumers, allowing us to distinguish between terrestrial vs.
aquatic, inshore vs. offshore or pelagic vs. benthic prey (Rau et al. 1992, Das
et al. 2000, Fernandez et al. 2011).
In this study, we used stable carbon and nitrogen isotope ratios from bottlenose
dolphins sampled in different areas of the Gulf of California to: (1) corroborate the
existence of ecotypes, (2) investigate isotopic differences among regions, (3) compare
isotopic ratios between dolphin ecotypes and among their potential prey, and (4)
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IAZ-GAMBOA ET AL.: ISOTOPIC NICHE WIDTH 441
examine the contribution of potential prey to the diet in the offshore bottlenose dol-
phin-sperm whale association.
Materials and Methods
Ecotype differentiation. The differentiation between inshore and offshore bot-
tlenose dolphin ecotypes was based upon field observations, focusing mainly on color
pattern, morphology, group size, water depth, and distance to shore. Significant dif-
ferences at a 0.05 level were tested by a multivariate analysis of variance (MANOVA)
using the variables depth, distance to shore and group size for ecotypes, followed by
Tukey HSD post hoc multiple comparison tests to find differences among them using
Statistica software v.7 (http://statistica.io/).
Figure 1. Gulf of California, Mexico, showing sampling locations of inshore (triangles) and
offshore (circles) bottlenose dolphins. Crossed circles represent locations of bottlenose dolphins
and sperm whales in association. Dashed lines indicate geographic divisions of the Gulf of Cali-
fornia (northern, central, and southern areas based on
Alvarez-Borrego 1983).
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Tissue collection. Skin samples (n=87) from free-ranging adult bottlenose dol-
phins, as well as sloughed and biopsy skin from sperm whales (n=13), were collected
in the spring of 2002 throughout the northern, central, and southern areas of the
Gulf of California (Fig. 1), following a geographic division based on phytoplankton
distribution (
Alvarez-Borrego 1983). Inshore samples from coastal bottlenose dol-
phins (n=11) were collected in all three zones, while offshore ecotype samples (n=
76) were collected only in the central and southern zones.
Skin and blubber biopsies from bottlenose dolphins were collected using a 2 m car-
bon fiber pole with a 5 mm diameter, 25 mm long stainless steel core sampler
equipped with three inward-facing barbs. This method was successful for bow-riding
dolphins, the biopsies were collected when animals approached the surface to breathe
and were close enough to make contact. A second collection method, as suggested for
small cetaceans (Patenaude and White 1995), involved a biopsy dart with the same
core sampler, shot from a 25 kg crossbow. Photo-identification images of these ani-
mals were used to avoid using duplicate samples. Skin samples from female and
immature sperm whales associated with offshore bottlenose dolphins were also col-
lected using two different methods (Fig. 1). The first one used a similar biopsy dart,
but 6 mm in diameter and 50 mm long, which was shot from a 45 kg crossbow. The
biopsies were collected from the fluke at the same time as identification photographs
were taken. The second method collected sloughed skin, using a dip net with a 1 mm
mesh size (Ruiz-Cooley et al. 2004).
Skin samples were extracted from the sampler using sterilized tweezers and then
stored in a 20% dimethyl-sulfoxide (DMSO)/saturated NaCl solution (Amos and
Hoelzel 1991). In order to eliminate any remaining organic matter, prevent sample
contamination and possible infection to the animals, the core sampler was sterilized
before each biopsy attempt by immersion in a 50% chlorine solution, then transferred
to a 70% ethanol solution and finally exposed for 10 s to a blowtorch flame.
Table 1. Stable isotope ratios of inshore and offshore potential prey in the Gulf of California
(mean SD in &) and the corresponding mean isotope enrichment of bottlenose dolphin
ecotypes.
Species Habitat nd
13
C
Mean d
13
C
enrichment d
15
N
Mean d
15
N
enrichment
Mugil cephalus Inshore 2 11.51 1.06 2.59 11.11 0.15 +8.19
Opistonema libertate Offshore 3 16.49 0.38 +0.59 17.76 0.08 +0.62
Hemiramphus
saltator
Offshore 3 16.56 1.30 +0.66 17.08 1.52 +1.3
Cheilopogon papilio Offshore 1 17.77 +1.87 16.1 +2.28
Tylosurus pacificus Offshore 1 17.25 +1.35 15.03 +3.35
Benthosema
panamense
Offshore 1 19.43 +3.53 14.9 +3.48
Dosidicus gigas
(<14cmML)
Offshore 7 17.88 0.96 +1.98 16.35 0.39 +2.03
Dosidicus gigas
(1725 cm ML)
Offshore 5 17.01 0.93 +1.11 16.11 1.58 +2.27
Dosidicus gigas
(8692 cm ML)
Offshore 3 16.27 0.93 +0.37 17.75 0.84 +0.63
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In order to analyze the relationships between these predators and their potential
prey, opportunistic muscle samples from five fish species and Humbolt squids
(Dosidicus gigas) were collected in the same areas and time where bottlenose dolphins
and sperm whales were sampled (Table 1). One fish species was collected in the
southern inshore area. All samples were stored frozen at 20°C.
Stable Isotope Analysis
Average diet and relative trophic position were determined by carbon and nitrogen
stable isotope analysis. Each sample was rinsed in distilled water, cut, and separated
from blubber when present. Samples were freeze-dried at 50°C and 50 910
3
mbar
of vacuum pressure to remove water. Lipids were removed applying Microwave
Assisted Extraction (MAE), using a chloroform-methanol (1:1) solution with a 1000
MARS 5 CEM microwave oven (Pareet al. 1994, Renoe 1995). This was also useful
to eliminate the effect of DMSO on the isotope values of cetacean skin samples, as
described in Burrows et al. (2010) and Busquets-Vass et al. (2017). The samples were
then dried and homogenized to a fine powder. Subsamples of 1.5 0.01 mg in
pressed tin capsules were analyzed for d
13
C, d
15
N and C:N ratios in an isotope-ratio
mass spectrometer interfaced in continuous flow to a Carlo Erba Elemental Analyzer.
The d
13
C is expressed in relation to the Vienna-Pee Dee Belemnite standard and the
d
15
N to atmospheric nitrogen. Analytical errors for samples were 0.07&for carbon
and 0.18&for nitrogen. The C:N ratio of each sample was analyzed to ensure that
the lipid extraction was successful, with a value of 3 representing pure protein
(McConnaughey and McRoy 1979).
Statistical Analyses
Significant differences at a 0.05 level were tested by a multivariate analysis of vari-
ance (MANOVA) using the variables d
13
Candd
15
N for groups, followed by unequal
N Tukey HSD (UN Tukey HSD) post hoc multiple comparison tests to find differ-
ences among them using Statistica software v.7. Isotopic niche width was estimated
by using stable isotope ellipses, implemented with the R package SIBER 2.1.0 (Jack-
son et al. 2011). The standard ellipse area (SEA) is the equivalent of standard devia-
tion for bivariate data. The shape and size of the ellipses are defined by the covariance
matrix of d
13
Candd
15
N, while its position is specified by the means of both vari-
ables. SEA was corrected for sample size (SEA
C
), because this approach nullifies the
bias of SEA estimations related to small sample size (Jackson et al. 2011), and SEA
C
were fitted to bivariate data by using maximum likelihood estimators. The isotopic
niche width is expressed as the SEA
C
in &
2
.SEA
C
contains 40% of the data regard-
less sample size. To compare the SEA
C
of different cetacean groups a Bayesian frame-
work was used, and SEA
B
(Bayesian SEA) was estimated by using Markov chain
Monte Carlo (MCMC) simulations for 200,000 iterations. To estimate parameters,
this method uses vague normal priors for the means describing the likely range of
d
13
Candd
15
N, and a vague Inverse-Wishart prior for the covariance matrix
(McCarthy 2007, Jackson et al. 2011). MCMC are used to construct the posterior
estimates of the parameters. Parameters were finally constructed by using the priors
and the likelihoods. This approach allows the incorporation of uncertainties associ-
ated with parameter construction and small sample size into niche metrics. The
degree of overlap between isotopic niches (or between ellipses of different groups) was
also estimated using a Bayesian framework. Isotopic niche width was estimated
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separately for each bottlenose dolphin ecotypes sampled within specific regions of the
Gulf of California (inshore north, inshore central, inshore south, offshore central, and
offshore south) and for combined associations of species (offshore bottlenose dolphin
ecotypes and sperm whales). To further explore the potential dietary preferences of
the combined associations of offshore bottlenose dolphin ecotypes and sperm whales,
we used a Bayesian isotopic mixing model. The model was developed with the R
package “SIAR” (Parnell et al. 2010). These models are used to calculate the likely
proportional contribution of different prey to a consumer’s diet based on their respec-
tive isotope values and the trophic discrimination factor (Parnell et al. 2010, Yeakel
et al. 2016). We used vague priors for the Bayesian model, because of the lack of
information on the proportional contribution of different prey to the diet of offshore
bottlenose dolphins and sperm whales in the Gulf of California. The variables intro-
duced to the model were the isotope values of the consumers (offshore bottlenose dol-
phins and sperm whales), potential prey (Table 1) and we used the trophic
discrimination factor derived from the longest controlled feeding experiment with
captive bottlenose dolphins (d
15
N=1.6&0.5&;d
13
C=1&0.4&)(Gimenez
et al. 2016). A dietary model was used for each species separately. This model allows
the incorporation of multiple prey into the analysis and incorporates the associated
uncertainty in the final estimations of the relative contribution of prey sources to the
consumer’s diet.
Figure 2. Common bottlenose dolphin ecotypes in the Gulf of California: inshore ecotype
(top) and offshore ecotype (bottom).
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Results
Ecotype Differentiation
Based on the sightings and comparison of both ecotypes observed in the Gulf of
California, the following general pattern was observed: (1) the individuals of the
inshore bottlenose ecotype were longer and bigger, lighter-colored dorsal view, with
dorsal layer evidently darker than lateral and ventral layers and a white belly (Fig. 2).
It was mostly found in small groups (mean =11 individuals, SD =6.3) in shallow
(mean =13.2 m, SD =9.1) and nearshore waters (mean =11.2 km from shore, SD =
0.7); (2) individuals from the offshore ecotype were smaller, darker-colored in dorsal
view without evident differences in color pattern between dorsal and lateral layers, an
evident lighter colored peduncle (multiple scars) and a light gray belly (Fig. 2). It
was mostly found in large groups (mean =400 individuals, SD =369.1) close to the
islands and deep-offshore waters (depth mean =922.7 m, SD =393.7; mean =44.9
km from shore, SD =35.1). There were significant differences among ecotypes in all
variables (F
3,6
=11.7, P<0.01).
Stable Isotope Ratios
Bottlenose dolphin ecotypes—There were significant differences among ecotypes in
d
13
Candd
15
Nvalues(F
2,84
=80.4, P<0.01). Inshore individuals were enriched in
13
Cand
15
N than those from offshore locations (UN Tukey HSD, P<0.01) (Fig. 3,
Table 2).
Inshore locations—The mean isotopic ratios showed significant differences among
inshore bottlenose dolphins from the northern, central and southern areas (F
4,14
=
Figure 3. Corrected standard ellipse areas (SEA
C
) representing the isotopic niche width of
common bottlenose dolphin ecotypes from different regions in the Gulf of California.
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7.5, P<0.01) (Table 2). Samples from the northern zone were significantly different
from the central and southern zones for d
15
N (UN Tukey HSD, P<0.01). While
there were no significant differences in d
13
C among the three zones, a strong trend
was observed for d
15
N, with the mean value decreasing from 20.4&in the north, to
19.2&in the central zone and 18&in the southern Gulf (Fig. 3).
Offshore locations—Although the range of values was more restricted compared to
the inshore locations (Fig. 3), the average isotopic composition for the two sampled
offshore zones (central and south) differed significantly (F
2,73
=7.9, P<0.01)
Table 2. Stable isotope ratios of inshore and offshore common bottlenose dolphin ecotypes
and female and immature sperm whales in the Gulf of California (mean SD in &).
Species Areas/tissue nd
13
Cd
15
N
Inshore T. truncatus Northern 4 13.96 0.36 20.42 0.62
Central 3 14.61 0.17 19.17 0.07
South 4 13.84 1.13 18.00 0.53
Mean 11 14.10 0.49 19.20 0.78
Offshore T. truncatus Central 32 15.76 0.33 18.31 0.55
South 44 15.98 0.38 18.43 0.56
Mean 76 15.89 0.37 18.39 0.56
P. macrocephalus Sloughed skin 7 15.04 0.76 19.47 0.65
Biopsy 6 15.56 0.54 19.16 0.65
Mean 13 15.28 0.69 19.33 0.65
Figure 4. Corrected standard ellipse areas (SEA
C
) representing the isotopic niche width of
associated offshore common bottlenose dolphins and sperm whales in the Gulf of California.
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(Table 2), with the samples from the south more depleted in
13
C than those from the
central zone (UN Tukey HSD, P=0.02). There were no significant differences
observed in d
15
N.
Bottlenose dolphin ecotypes and sperm whales—There were no significant differences in
isotopic ratios between sloughed skin and biopsy samples from sperm whales (F
2,10
=
0.9, P=0.4) (Table 2). Thus, the mean isotopic ratio for female and immature sperm
whales (n=13) found associated with offshore bottlenose dolphins was 15.3&for
d
13
Cand19.3&for d
15
N (Fig. 4, 5, Table 2).
The mean isotopic ratios in bottlenose dolphins and sperm whales sampled in asso-
ciation were significantly different to those of the inshore dolphin ecotype (F
4,76
=
18.2, P<0.01), with the latter being more enriched in
13
C (UN Tukey HSD, P<
0.01). No significant differences were observed for d
15
N (Fig. 4, 5).
Potential prey—The d
13
Candd
15
N values of potential prey samples from offshore
and inshore fish species (n=11) and one squid species (n=15) are shown in Table 1.
Regarding fish species, five of them were from the offshore area and one collected
inshore (Fig. 3). In the case of the Humbolt squid, all samples were from the offshore
area. The results of the Bayesian mixing model showed that a considerable proportion
of the diet of offshore bottlenose dolphins and sperm whales were large Humboldt
squid (8692 cm of mantle length) and Opisthonema libertate (Fig. 6). Offshore bot-
tlenose dolphins also fed on Hemiramphus saltator and medium Humboldt squid (17
25 cm of mantle length) but in a lesser proportion. The rest of prey sources con-
tributed to less than 6% of the diet of these species (Fig. 6).
Figure 5. Mean d
13
Candd
15
Nvalues(&) of inshore and offshore common bottlenose dol-
phin ecotypes, female and immature sperm whales and potential prey from the Gulf of Califor-
nia. Error bars indicate 1 SD.
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Isotopic Niche Width
The SEA
C
and SEA
B
(see Fig. S1) of the inshore bottlenose dolphins from the north
(SEA
C
=1.03&
2
;SEA
B
mean =0.94&
2
, 95% credibility interval of 0.21&
2
2.04&
2
), central (SEA
C
=0.02&
2
;SEA
B
mean =0.05&
2
, 95% credibility interval
of 0.01&
2
0.12&
2
) and south (SEA
C
=1.96&
2
;SEA
B
mean =2.14&
2
,95%credi-
bility interval of 0.49&
2
4.71&
2
) of the Gulf of California, were completely dis-
tinct, as the ellipses of these groups did not overlap (Fig. 3). The separation of the
Figure 6. Bayesian isotopic mixing model results: probability densities of the proportional
contributions of different sources (prey) to consumer’s diet (cetacean). Graphs show the 25%,
75%, and 95% credibility intervals. Ol:Opisthonema libertate,Hs:Hemiramphus saltator,Cp:
Cheilopogon papilio,Tp:Tylosurus pacificus,Dg.S:Dosidicus gigas Small (<14 cm of mantle
length), Dg.M: D. gigas Medium (1725 cm of mantle length), Dg.L: D. gigas Large (86
92 cm of mantle length).
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ellipses of inshore bottlenose dolphins was driven by d
15
N. The same results were
obtained when comparing the ellipses of all the inshore bottlenose dolphin ecotype
groups to the offshore ecotype groups from the central region (SEA
C
=0.44&
2
;
SEA
B
mean =0.45&
2
, 95% credibility interval of 0.31&
2
0.62&
2
) and south
region (SEA
C
=0.61&
2
;SEA
B
mean =0.61&
2
, 95% credibility interval of
0.44&
2
0.80&
2
) of the Gulf of California (Fig. 3), but in this case the separation of
the ellipses was mainly driven by d
13
C. In contrast, the ellipses of the offshore bot-
tlenose dolphins in the central and south regions of the Gulf of California exhibited
an overlap of 0.20&
2
(95% credibility interval of 6.10e
19
&
2
0.40&
2
)(see
Fig. S2), which represented 43% of the ellipse surface of the former and 32% of the
latter, indicating that these ecotypes share a considerable proportion of their isotopic
niche. For associated species, the ellipses of offshore bottlenose dolphins (SEA
C
=
0.57&
2
;SEA
B
mean =0.62&
2
, 95% credibility interval of 0.35&
2
0.91&
2
)and
sperm whales (SEA
C
=0.83&
2
;SEA
B
mean =0.97&
2
, 95% credibility interval of
0.49&
2
1.55&
2
) exhibited an overlap of 0.18&
2
(95% credibility interval of
8.67e
19
&
2
0.50&
2
) (Fig. 4) (see Fig. S3, S4). The overlapping area represented
30% of the ellipse surface of the offshore bottlenose dolphins and 19% of the ellipse
surface of sperm whales.
Discussion
Ecotype Differentiation
In this study, the differentiation of bottlenose dolphin ecotypes based on field
observation was corroborated using carbon and nitrogen stable isotope analysis.
The ecotype descriptions for the dolphins in the Gulf of California agree with
those reported for dolphins found in the Northeast and Southeast Pacific Ocean
(Walker 1981), with the offshore form being described as having a darker col-
oration in the dorsal layer and a sharper, narrower rostrum compared to the
inshore form. The inshore ecotype of the Southeast Pacific has lighter coloration,
with three different layers (dorsal, lateral and ventral layers) compared to the off-
shore ecotype (Waerebeeck et al. 1990). In contrast, these ecotype differences do
not match those from the Northeast Atlantic Ocean, in which the offshore ecotype
is described as larger in size with a shorter rostrum than the inshore one (Hersh
and Duffield 1990). The relative body size of inshore and offshore ecotypes appears
to be opposite in the Pacific and Atlantic Oceans. In general, the body size in bot-
tlenose dolphins varies inversely with water temperature, except for the Eastern
Pacific form (Wells and Scott 2002).
Stable Isotope Ratios
Bottlenose dolphin ecotypes—The inshore ecotype had statistically higher carbon iso-
topic ratios than the offshore ecotype, and this difference in d
13
C resulted in the
SEA
C
separation between ecotypes (Fig. 5). The difference in mean d
13
Cratiosindi-
cates that the inshore ecotype feeds on prey from a
13
C-enriched environment, match-
ing the expected distribution of d
13
C in the ocean (Fig. 5). The latter agrees with the
pattern observed in stranded bottlenose dolphins from the northern Gulf of Mexico
(Barros et al. 2010), South Carolina, (Olin et al. 2012), and Galicia, Spain (Fernandez
et al. 2011). Inland contributions can cause isotopic ratio variations at the base of the
D
IAZ-GAMBOA ET AL.: ISOTOPIC NICHE WIDTH 11
MARINE MAMMAL SCIENCE, VOL. 34, NO. 2, 2018450
trophic network in coastal ecosystems (Walker et al. 1999). The
13
Cenrichmentof
inshore phytoplankton can also be associated with blooms stimulated by the mixing
in the shallower water column, which brings nutrient-enriched waters into the photic
zone (Schell et al. 1998). During these blooms,
13
C increases by 2&3&in the phy-
toplankton during photosynthesis (Burton and Koch 1999). In the offshore ecosys-
tems, where the nutrients are limited, phytoplankton growth rates are lower and, as a
result, the
13
C values of fixed carbon at the trophic network base are lower than in
coastal ecosystems (Schell et al. 1998, Burton and Koch 1999).
The difference in the d
15
N mean values between ecotypes was of 0.82&,withthe
inshore one being more enriched in
15
N, which indicates that this is associated with
distinct environments rather than a difference in trophic levels. Sampling more
inshore potential prey would help to determine if they are feeding in different trophic
levels. The nitrogen supply in the coastal environment comes from the atmosphere,
land, anthropogenic activity and sediments outputs; and an increase of 2.8&can be
observed in particulate organic matter (Kumar et al. 2004, Voss et al. 2005). In con-
trast, the oceanic environment has low values of d
15
N derived from atmospheric
cyanobacterial N
2
fixation, low nutrients and limited exchange of surface waters with
deeper waters, which are often low in oxygen in the NE Pacific (Carpenter et al.
1997, Galloway et al. 2004).
Bottlenose dolphin locations—The differences among zones suggest a latitudinal trend
in d
15
N values for inshore bottlenose dolphins in the Gulf of California (Fig. 3). The
isotopic composition of trophic webs tends to be enriched in
15
N in lower latitudes
compared to higher latitudes (Rau et al. 1992, Burton and Koch 1999). For the
inshore locations in this study, the differences observed in d
15
N can be explained by
the oceanographic features of the northern Gulf of California, rather than the latitudi-
nal effect. The upper Gulf is a semienclosed marginal sea limited by land to the
north, west, and east and by the Midriff Islands to the south, characterized by strong
tidal mixing, high turbidity, detritus accumulation, and shallow waters, leading to
15
N-enriched values (Aguı~niga-Garcıa 1999, Shumilin et al. 2002). Significant dif-
ferences in d
15
N were found only between the northern and the southern zones, while
the central Gulf appears to be a transitional zone. These differences also reflect the
southern zone of the Gulf of California exposure to the Pacific Ocean, leading to val-
ues depleted in
15
N(Fig. 1).
Beyond the Gulf of California geographic division used in this study (
Alvarez-Bor-
rego 1983), differences in d
15
N values were observed in bottlenose dolphins from dif-
ferent inshore areas (Fig. 3), possibly as a result of different nitrogen sources.
Anthropogenic activities and agricultural practices contribute to eutrophication of
nearshore marine systems by adding nutrients, leading to
15
N enrichment compared
to those not affected by human settlements (Voss et al. 2005). In the Gulf of Califor-
nia, offshore bottlenose dolphins apparently occupy a wider habitat, because they
occasionally are observed in deep nearshore waters. On the other hand, in areas such
as the east coast of North America, where the continental shelf is much wider than
the very narrow band of continental shelf in the western Gulf of California, the
inshore ecotype can be found far from the coast (Kenney 1990, Torres et al. 2003),
suggesting that water depth is a controlling factor.
Sperm whales—We found no difference in the isotope ratios from biopsies and
sloughed skin samples from female and immature sperm whales, thus we inferred the
sperm whales did not change their diet during the period of skin formation. The
complete skin turnover rate of bottlenose dolphin is estimated at 104 d for carbon
and 205 d for nitrogen (Gimenez et al. 2016). If the skin turnover time of sperm
12 MARINE MAMMAL SCIENCE, VOL. **, NO. **, 2017
D
IAZ-GAMBOA ET AL.: ISOTOPIC NICHE WIDTH 451
whales is similar to that of the bottlenose dolphin, the sperm whales sampled in this
study had been feeding in the Gulf of California for around 205 d.
Bottlenose dolphin ecotypes and sperm whales—Sperm whale carbon stable isotopes val-
ues did not differ significantly from offshore dolphins, but were different to those
from inshore (Fig. 4, 5). This result was to be expected because of the known associa-
tion of sperm whales and offshore bottlenose dolphins, and it may be that the relative
contributions of the primary sources to the diet were the same. The inshore ecotype
skin samples had higher values of d
13
C, which is interpreted as they fed in a
13
C-enriched environment. With respect to d
15
N, no differences were found among
inshore and offshore ecotypes and sperm whales, indicating that all three apparently
fed at the same relative trophic level. Combining the information from both isotopes,
we propose that the inshore and offshore ecotypes of bottlenose dolphin inhabit dif-
ferent environments, and that the offshore ecotype and the sperm whales share some
prey in common.
Potential prey—The diet of female and immature sperm whales has been widely
described as being based on meso- and bathypelagic cephalopods (Okutani et al.
1976, Clarke 1986, Gonzalez et al. 1994), with a preference for Humbolt squid in
the Eastern Tropical Pacific and Gulf of California (Clarke et al. 1988, Jaquet and
Gendron 2002). Using stable isotope analysis, large Humbolt squid (4082 cm of
mantle length) proved an important prey for sperm whales feeding in the Gulf of Cal-
ifornia (Ruiz-Cooley et al. 2004). The stable-isotope-based findings of niche width
overlap analysis agrees with the previously observed close relationship between bot-
tlenose dolphins and females and immature sperm whales in the Gulf of California
(Jaquet and Gendron 2002) (Fig. 4). The offshore bottlenose dolphins have adapted
to the pelagic environment by diving longer and deeper than the inshore ecotype
(Hersh and Duffield 1990); however, they do not have the same ability to dive as
sperm whales. The association between cetacean species is believed to be linked to
protection against predators, energy efficiency and better prey search and detection.
Such a relationship has been referred to as “social parasitism” (Norris and Prescott
1961, Norris and Dohl 1980). In the Gulf of California, the Humbolt squid spent
about 75% of the time in the 200400 m depth range during daytime hours, and
excursions into warm surface waters at night are often terminated by deep dives to
typical daytime depths, after which the squid appeared to be relatively quiescent
(Gilly et al. 2006). Sperm whales, showed a similar dive-depth preference during
daytime, but continue to dive deep during the night, when squid are recovering at
depth from stress after recent surface activity and are probably more susceptible to
predation (Davis et al. 2007). We suggest that the offshore bottlenose dolphins asso-
ciate with female and immature sperm whales to benefit from their ability to follow
the Humbolt squid during the day, while the dolphins themselves can close on the
prey at lower depth during the night.
Striped mullet, Mugil cephalus, was the only prey sampled in the inshore environ-
ment during this study. There is a well-documented feeding preference for mullet by
inshore bottlenose dolphins in the Atlantic (e.g., Barros and Odell 1990, Shane
1990). The prey-predator relationship has been estimated as the d
15
Nincreasefrom
1.57&to 2.82&, while for d
13
C is estimated from 1.01&to 1.28&(Borrell et al.
2012, Gimenez et al. 2016). Although the muscle tissue from the mullet collected in
the southern area had the highest d
13
C value, as expected for the inshore environ-
ment, both isotope values obtained in this study suggest that mullet is not the main
prey of inshore bottlenose dolphins. The estimated enrichment from mullet to
inshore bottlenose dolphins based on the 2.59&for d
13
C and 8.19&for d
15
Ndoes
D
IAZ-GAMBOA ET AL.: ISOTOPIC NICHE WIDTH 13
MARINE MAMMAL SCIENCE, VOL. 34, NO. 2, 2018452
not fit the expected prey-consumer relationship (Fig. 5). Regarding the potential
prey caught in offshore waters, large Humbolt squid and O. libertate contributed a
considerable proportion to the diet of the offshore ecotype, with H. saltator and med-
ium Humboldt squid in a lesser proportion (Fig. 6). This agrees with the stomach
content analyses of the Eastern Pacific offshore ecotype, which had previously revealed
their preference for epipelagic fish and cephalopods, with 70% of the cephalopods
ingested being D. gigas (Walker 1981, Waerebeek et al. 1990).
Different characteristics of marine habitats lead to adaptive divergence and genetic
differentiation being maintained by philopatry as a result of foraging specialization
and social organization (Hersh and Duffield 1990, Torres et al. 2003, Louis et al.
2014). It is unknown whether variations in morphology, habitat, feeding habits, and
social structure reflect phylogenetic segregation or ecological plasticity. In the Gulf
of California, reproductive isolation between bottlenose dolphin ecotypes with no evi-
dence of lineage sorting was observed, possibly as a result of recent isolation or gene
flow (Segura et al. 2006). The present study corroborates the usefulness of the stable
isotopes technique for differentiating between inshore and offshore ecotypes of bot-
tlenose dolphin, for distinguishing distinct inshore populations and for better under-
standing the dietary similarities of the offshore dolphins with the female and
immature sperm whales with which they associate. Our results indicate that resource
partitioning and species association are two strategies that bottlenose dolphin eco-
types use in this zone. By providing both population and environmental information,
d
13
Candd
15
N analysis could be an effective tool to better distinguish bottlenose dol-
phin management units in the Gulf of California as well as other cetaceans in differ-
ent areas (Borrell et al. 2006, Barros et al. 2010, Esteban et al. 2016)
Acknowledgments
Funding was provided by CONACTY-SEMARNAT-2002-C01-0628, Instituto Politec-
nico Nacional and CONACYT scholarship to RD-G. We thank C. Arista de la Rosa and A.
M. Zamarron for their valuable contributions to the sampling collection. We are grateful to
N. Jaquet, L. Rojo, and I. Segura for providing tissue samples. We also thank anonymous
reviewers for their comments and English improvement. Data and tissue collection were
obtained under scientific permits SGPA/DGVS/7000-00624 from the Secretarıa de Medio
Ambiente y Recursos Naturales.
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Received: 8 August 2016
Accepted: 11 October 2017
Supporting Information
The following supporting information is available for this article online at http://
onlinelibrary.wiley.com/doi/10.1111/mms.12465/suppinfo.
Figure S1. Posterior Bayesian estimates of the standard ellipse area (SEA
B
)of
inshore and offshore bottlenose dolphin ecotypes sampled in different regions of the
Gulf of California. Shaded density plots represent 50%, 75%, and 95% credible
intervals. Black dots represent SEA
B
mode and the open red circles the corrected stan-
dard ellipse (SEA
C
) values. North (N), Central (C) and South (S).
Figure S2. Posterior Bayesian estimates of the standard ellipse area (SEA
B
), and of
the overlapping area of offshore bottlenose dolphin ecotypes of different regions of
the Gulf of California. Shaded density plots represent 50%, 75%, and 95% credible
intervals. Black dots represent SEA
B
mode. Central (C) and South (S).
Figure S3. Posterior Bayesian estimates of the standard ellipse area (SEA
B
) of associ-
ated offshore bottlenose dolphin ecotypes and sperm whales. Shaded density plots
represent 50%, 75%, and 95% credible intervals. Black dots represent SEA
B
mode
and the open red circles the corrected standard ellipse (SEA
C
)values.
Figure S4. Posterior Bayesian estimates of the standard ellipse area (SEA
B
), and of
the overlapping area of associated offshore bottlenose dolphins and sperm whales.
Shaded density plots represent 50%, 75%, and 95% credible intervals. Black dots
represent SEA
B
mode.
18 MARINE MAMMAL SCIENCE, VOL. **, NO. **, 2017
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IAZ-GAMBOA ET AL.: ISOTOPIC NICHE WIDTH 457
... Pilot whales and sperm whales had similar carbon and nitrogen stable isotope ratios, indicating that both fed in the same isotopic region and at a similar trophic level; therefore, it is possible they focused on the same prey (Table 1). The jumbo squid (Dosidicus gigas) has been reported as the main prey of female and immature sperm whales in the Gulf of California (Ruiz-Cooley et al., 2004;Díaz-Gamboa et al., 2018). Both our results and those of Díaz-Gamboa et al. (2018) agree that the potential primary prey of sperm whales and pilot whales was the jumbo squid (Table 1). ...
... Both our results and those of Díaz-Gamboa et al. (2018) agree that the potential primary prey of sperm whales and pilot whales was the jumbo squid (Table 1). Although the number of sperm whale samples is low, the isotopic values agree with those reported by Díaz-Gamboa et al. (2018). Pilot whales have been observed behaving aggressively towards other cetaceans such as humpback whales (Megaptera novaeangliae), common dolphins (Delphinus delphis), and Stenella sp. ...
... Female and immature sperm whale (Physeter macrocephalus) group in the Gulf of California before the interaction with short-finned pilot whales (Globicephala macrorhynchus) (Photo credit: Raúl E. Díaz-Gamboa, CICIMAR) Pilot whales (PW) chasing the sperm whales (SW) (Photo credit: Raúl E. Díaz-Gamboa, CICIMAR)the average diet of both species in the area(Díaz- Gamboa et al., 2018). Trophic level was estimated using the following(Hobson & Welch, 1992): TL = 1 + (Dm -Dn) / 2.82‰ ...
... We organized the data to allow us to infer cranial differences between the inshore and offshore ecotypes. Because our sample did not come from captured specimens, we were unable to identify ecotypes following criteria previously employed with data obtained in situ (Díaz-Gamboa et al., 2017;Lowther-Thieleking et al., 2015;Perrin et al., 2011). ...
... Studies on trophic ecology have indicated that the δ 13 C isotopic signal in dolphins is related to their geographic distribution (Aurioles-Gamboa et al., 2013, Díaz-Gamboa et al., 2017 and therefore can be employed to recognize ecotypes. Enrichment of 13 C values is found in the inshore ecotype, while low 13 C values are found in the offshore ecotype. ...
... The size of the skulls, represented by the distance of the total length from the rostral tip to the occipital condyles, was 554-443 cm for the inshore ecotype, with a mean of 491 cm, and 515-464 cm for the offshore ecotype, with a mean of 482 cm. Of the 47 skulls reviewed, we classified 43, 24 of which were inshore and 19 offshore, using the δ 13 C values and the cutoff considered for the inshore and offshore areas (Figure 3) based on previous studies (Aurioles-Gamboa et al., 2013;Díaz-Gamboa, 2009;Díaz-Gamboa et al., 2017;Segura-García et al., 2018). From all inshore and 18 offshore skulls, morphometric information was obtained from all three views (dorsal, ventral, and lateral). ...
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The distribution of common bottlenose dolphins Tursiops truncatus is associated with environmental factors, which influence morphological adaptations. In the present study, we examined the cranial characteristics of this species from the Pacific Northwest of Mexico to detect the main variations using geometric morphometric analysis. From stable isotope concentrations (δ13C), we identified 24 specimens of the inshore coastal ecotype and 18 of the offshore ecotype. Maturity was determined using the degree of fusion of the maxillae and premaxillae. Allometry was detected in the skull lateral region, indicating that the relationship between shape and size is maintained in adults. After eliminating the allometric effect by discarding the smallest individuals, morphometric comparisons indicated differences between the ecotypes that were associated mainly with the intersection between the frontal bone and zygomatic process, the anteriormost point in the curvature of the zygomatic process, and the meeting of the suture between squamosal and exoccipital bones, with the supramastoid crest to anteriormost in the curvature of the temporal crest of the intersection between the parietal and interparietal. No significant differences were found in the ventral view. The cranial differences between both Tursiops truncatus ecotypes could be mainly associated with the different types of feeding.
... Previous work has also shown that zooplankton d 15 N values in the CCE are consistent over decadal scales (Rau et al., 2003). In the GC, there are marked latitudinal baseline gradients in d 15 N north and south of Midriff Islands (Dıáz-Gamboa et al., 2018), which produces a large range in krill d 15 N values (Busquets-Vass et al., 2017;Busquets-Vass et al., 2021). In addition, the opportunistic consumption of lanternfish also results in higher values in blue whale tissues in this region compared to the CCE and CRD. ...
... Our results also show that significant latitudinal variation in baseline d 15 N values across the GC may allow for the identification of foraging in the northern versus southern areas of this region. The northern region of the GC located at~28 latitude has a d 15 N baseline~2‰ higher than the southern region (Dıáz-Gamboa et al., 2018). Blue whales typically use the southern region of the GC (Gendron, 2002), however, whales H (adult male) and M (recently weaned whale) stranded in the northern region and the last few subsamples of baleen in both individuals deposited prior to death had anomalously high d 15 N values ( Figure 2). ...
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Migration is a complex behavior that has evolved in multiple taxonomic groups as a means of accessing productive foraging grounds and environmentally stable areas suitable for reproduction. For migratory whales that forage throughout the year because of their high energetic demands, changes in the abundance of prey in different areas along their migratory route(s) can have serious implications for individual fitness and population viability. Thus, identifying the regions these species use to forage and breed while evaluating their migratory plasticity at the individual level can provide key information for their management and conservation. Serial stable isotope analysis of whale baleen, a continuously growing but metabolically inert tissue, has proven useful in generating individual migratory and foraging records over several years prior to death. We measured carbon ( δ ¹³ C) and nitrogen ( δ ¹⁵ N) isotope values along the length of baleen plates collected from thirteen blue whales of different sex and age classes, representing the largest collection analyzed to date in the northeast Pacific Ocean. Adult females exhibited relatively stable seasonal movements between temperate latitude foraging grounds and subtropical breeding grounds, although two skipped migration one year and subsequently moved to the same subtropical breeding ground near the Costa Rica Dome, potentially to give birth. Adult males exhibited two movement strategies with most remaining at temperate latitudes for 3-4 years before death, while two migrated to subtropical breeding grounds. In contrast, movement patterns in juveniles were erratic. These results are potentially driven by the energetic requirements during pregnancy and nursing in adult females, intra-specific competition among adult males, and inexperience in locating prey in juveniles. We also describe baleen δ ¹⁵ N patterns in recently weaned whales (<16.5m) that reflect switching from the consumption of milk to solid food (krill). In addition, baleen δ ¹³ C data suggest that weaned whales continue to use stored nutrients (blubber) acquired during the nursing period long after they are weaned. These results broaden our understanding of habitat selection in this species, highlight the importance of nursing for the critical period after weaning, and indicate that the Costa Rica Dome is an important calving region for this endangered population.
... In pinnipeds, for instance, skull bone contains information about the assimilated diet for a period of months in juveniles and up to five years in matures individuals (Sealy et al. 1995, Riofrío-Lazo & Aurioles-Gamboa 2013. Variability in δ 13 C values can be associated with changes in diet, however, it mainly reflects variation in C sources and primary production (Peterson & Fry 1987, Fry & Wainright 1991, Díaz-Gamboa et al. 2018). The δ 15 N baseline values vary between coastal and pelagic habitats across large ecosystems, and consumers reflect similar variation (DeNiro & Epstein 1981). ...
... Other odontocete species such as Tursiops truncatus (Díaz-Gamboa et al. 2018), Pontoporia blainvillei (Troina et al. 2016), and Monodon monoceros (Louis et al. 2021) also exhibited similar isotope values between males and females. Although different prey types can have a similar isotopic composition (Bearhop et al. 2004), this pattern might suggest an interspecific competition between sexes, which could not be favorable for the feeding success (Bolnick et al. 2003). ...
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The worldwide smallest cetacean, the vaquita (Phocoena sinus), is on the verge of extinction with fewer than 20 individuals left as of summer 2018. The main cause of mortality is bycatch by entanglement in illegal gillnets and environmental changes. Habitat disturbances have negatively impacted prey diversity, and therefore, the vaquita’s feeding success. We investigated the trophic niche of the vaquita and its variability from 1985 to 1993 by quantifying δ¹³C and δ¹⁵N values from bone samples (n = 33). We reconstructed part of vaquita’s refuge food web and identified some prey items. Between 1985 to 1993 the vaquita’s isotopic ellipses shifted moderately, δ¹³C and δ¹⁵N without significant differences, suggesting variations in habitat baseline values and probably prey composition. We observed a high overlap in the ellipses between males and females, suggesting that both sexes were feeding in the same geographic area over several years and with similar prey composition. Together, our results indicate that the vaquita is a generalist high-TL consumer, feeding on benthic and small pelagic prey it maintained similar mean δ¹⁵N values for years. Given these results, conservation efforts should intensify to protect the biodiversity of the Upper Gulf of California and the surviving vaquita.
... Stable isotope analyses are widely used to investigate foraging ecology of mammals (Herman et al. 2005, Mendes et al. 2007 , with carbon isotopic values (δ 13 C) providing information on likely carbon sources relating to feeding habitat (Rubenstein & Hobson 2004), and nitrogen isotopic values (δ 15 N) indicating trophic level of the organism (Minagawa & Wada 1984, Post 2002. Due to the spatial variation in baseline isotope ratios of autotrophic sources, both δ 13 C and δ 15 N values of marine predators are also influenced by latitude and oceanographic processes within the foraging region , Díaz-Gamboa et al. 2018. The similarity in mean δ 13 C values of the individuals stranded in Taranaki compared to those of sperm whales off Kaikōura (Guerra et al. 2020b) suggests a similar source of organic carbon supporting their food webs (e.g. ...
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Cetacean strandings provide important opportunities to extend current knowledge on species or populations, particularly for species that are notoriously difficult to study such as sperm whales (Physeter macrocephalus; parāoa). Between 25 May and 9 June 2018, 13 male sperm whales stranded in Taranaki, Aotearoa New Zealand, with an additional male stranding one month later in Clifford Bay, Marlborough. We profiled these 14 males for mitochondrial DNA (mtDNA) and carbon and nitrogen stable isotopes to examine their similarity to sperm whales from other geographic areas. Analyses of mtDNA revealed seven haplotypes, including one not previously described (‘New’), and an additional haplotype (‘M’) new-to-New Zealand that had been previously reported in sperm whales of the Pacific region. Analysis of rare haplotypes found in New Zealand males suggested genetic links within New Zealand and the Southwest Pacific. Differences in stable isotope ratios indicated that, despite the close temporal proximity of these stranding events, individuals originated from at least two separate groups, with the whale stranded in Clifford Bay identified as being a regular visitor to Kaikōura. The analysis of stranding records in New Zealand dating back to 1873 indicated an increase in recorded single strandings since 1970, and a peak in single strandings in the austral summer months, but no seasonality for mass strandings. Sex predicted latitudinal location for single strandings, with 95.1% of female strandings occurring north of 42°S latitude, fitting the general global distribution of female sperm whales limited to lower latitudes. This study provides the first temporal and spatial assessment of sperm whale strandings in New Zealand and highlights the need for future research on movements and genetic exchange between New Zealand sperm whales and sperm whales in the wider Pacific region.
... Bottlenose dolphins and melon-headed whales use both nearshore and pelagic regions for resting and foraging (Baumann-Pickering et al., 2015;Tobeña et al., 2014). Bottlenose dolphins are represented by two ecotypes, coastal and oceanic, that may occur in adjacent areas, but fulfill specific niches in distinct habitats (Díaz-Gamboa et al., 2018;Zaeschmar et al., 2020). At Palmyra, melon-headed whales rest nearshore during the day and forage offshore at night (Baumann-Pickering et al., 2015). ...
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Marine protected area (MPA) designs, including large-scale MPAs (LSMPAs; >150,000 km2), mobile MPAs (fluid spatiotemporal boundaries), and MPA networks, may offer different benefits to species and could enhance protection by encompassing spatiotemporal scales of animal movement. We sought to understand how well LSMPAs could benefit nine highly-mobile marine species in the tropics now and into the future by: 1) evaluating current range overlap within a LSMPA; 2) evaluating range overlap under climate change projections; and 3) evaluating how well theoretical MPA designs benefit these nine species. We focused on Palmyra Atoll and Kingman Reef, a 2000 km2 area within the 1.2 million km2 U.S. Pacific Remote Islands Marine National Monument (PRIMNM) that contains marine megafauna (reef and pelagic fishes; sea turtles; seabirds; cetaceans) reflecting different behaviors and habitat use. Our approach is useful for evaluating the effectiveness of the Palmyra-Kingman MPA and PRIMNM in protecting these species, and tropical LSMPAs in general, and for informing future MPA design. Stationary MPAs provided protection at varying scales. Reef manta rays (Mobula alfredi), grey reef sharks (Carcharhinus amblyrhynchos), green sea turtles (Chelonia mydas), and bottlenose dolphins (Tursiops truncatus) had overall small ranges (
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The sperm whale ( Physeter macrocephalus ) is a deep-diving cetacean with a global distribution and a multi-leveled, culturally segregated, social structure. While sperm whales have previously been described as ‘ocean nomads’, this might not be universal. We conducted surveys of sperm whales along the Lesser Antilles to document the acoustic repertoires, movements and distributions of Eastern Caribbean (EC) sperm whale cultural groups (called vocal clans). In addition to documenting a potential third vocal clan in the EC, we found strong evidence of fine-scale habitat partitioning between vocal clans with scales of horizontal movements an order of magnitude smaller than from comparable studies on Eastern Tropical Pacific sperm whales. These results suggest that sperm whales can display cultural ecological specialization and habitat partitioning on flexible spatial scales according to local conditions and broadens our perception of the ecological flexibility of the species. This study highlights the importance of incorporating multiple temporal and spatial scales to understand the impact of culture on ecological adaptability, as well as the dangers of extrapolating results across geographical areas and cultural groups.
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Trophic ecology information about cetaceans is essential to understand their role in ecosystem dynamics. Stable isotope analysis is a valuable complementary approach to conventional methods usually applied to the study of the foraging behavior of cetaceans because it provides dietary information over different time scales and can potentially use tissues archived in scientific collections. However, the considerable increase in stable isotope analysis by a growing number of cetacean research groups demands the use of proper protocols to ensure that accurate isotopic data are obtained. We provide a theoretical background of stable isotope analysis and its application to assess cetaceans‘ trophic ecology. We review the factors that can influence isotopic measurements and propose a practical guideline with suitable techniques for sample preparation of biological tissues to be employed by researchers to yield reliability in the interpretation of isotopic data. We summarized the main assumptions and inherent limitations that can lead to confounding interpretations of isotopic data, such as species‐ and tissue‐specific discrimination factors, temporal or spatial variation in prey, and baseline isotopic values in the context of cetacean ecology. Our detailed review offers important guidance for researchers who want to use stable isotope analysis to address different ecological questions with cetacean species. A practical guide on stable isotope analysis for cetacean research.
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Background. Since the formation of the research group in marine biology at the CCBA, different aspects of this discipline have been developed. One of them is the identification of populations and possible stocks of fish of commercial importance, using different techniques. The stock delineation (or population structure) are central considerations for fishery assessment and strategic management of marine natural resources and have to be addressed from a meta-population perspective where complementary technical approaches meet to enable the best picture to delineate complex stock structures. Objective. To review the current knowledge on the stock concept and the use of a multidisciplinary approach to properly assess commercially important marine stocks in the coastal waters of the Yucatan peninsula. Methodology. We present the research explored so far by the marine biology laboratory (LABIOMA by its acronym in Spanish) of the Autonomous University of Yucatán regarding the marine resources off the coast of the Yucatan peninsula, and the future lines of investigation pursued by our personnel, from fishing gear selectivity, abundances and catchability estimates, traditional morphometrics, parasitological and life history traits as biological tags, to more precise analyses such as fish otolith shape or even stable isotope analysis, genotypic markers, and marine natural products chemistry. Main findings. Single technical approaches are insufficient to delineate complex stock structures, especially in wide marine open access ecosystems, and there is a need to harness the full power of complementary and synergistic multidisciplinary approaches to improve fishery assessment and management efficiency in marine natural resources from the coastal areas of the Yucatan peninsula. Implications. Most stock assessment models are based on a single unit stock assumption, however the full impact of management actions, including identifying the complexity of the stock of any marine species subject to fishing, could affect the perpetuity of its abundances if the population subunits are not properly located. Conclusion. Identification of stocks is necessary for several reasons including allocation of catches, recognition and protection of nursery and spawning areas, and for development of optimal harvest and monitoring strategies. To this end, the LABIOMA are strengthening the assessments of commercially important marine stocks by using multidisciplinary approaches, whose lines of research represent basic aspects to be known and would be of great help to decision makers at the time of establishing more precisely, catch quotas, fishing areas, closed seasons, and therefore make more efficient the management strategies.
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Coexistence among sympatric species requires a certain degree of resource partitioning. In this regard, there is a lack of knowledge regarding S. attenuata (SA) and S. longirostris (SL) in Mexico; hence, the stable isotope analysis was used to assess the differences between their feeding habits, particularly in trophic poisition/amplitude and habitat use (δ 15 N and δ 13 C, respectively; Bayesian comparisons and estimations of isotopic niches and trophic levels), to identify trophic relationships with other species from the region (Bayesian mixing model). Additionally, the possible intra-specific feeding diversification was explored by linking the isotopic values of both species with their matrilineages (mtDNA, Random Forest Classifier). Surveys were performed in the Central Coast of Oaxaca, from 2016 to 2019 (dry seasons). A trend towards feeding segregation was found between both delphinids, especially in carbon sources (δ 13 C, p(SA>SL)=100 %); furthermore, SA (n=22) presented a higher isotopic niche than SL (n=25; SIBER, SEAc=0.9 h 2 vs 0.7 h 2 ) and more positive δ 13 C, with an 33 % overlap, which suggests more coastal habits of SA. An interannual variation for both isotopes of both species was found, mainly in 2018, possibly due to signals coming from different isoscapes, alhtough changes in the trophic spectrum are not discarded. In SL, these isotopic differences were related with the presence of different haplotypic groups with distinct isotopic values and isotopic niche amplitude each year. The most relevant prey species were Benthosema panamense and Hyporhamphus naos (∼50 %), although B. panamense was more dominant for SL (p( %SL> %SA)=89 %). Calculated trophic levels were 4.1 and 3.8 for SA and SL, respectively. This work provides evidence of a resource partitioning between and within both dolphin species that inhabit the Central Coast of Oaxaca.
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Stable isotope analysis in mysticete skin and baleen plates has been repeatedly used to assess diet and movement patterns. Accurate interpretation of isotope data depends on understanding isotopic incorporation rates for metabolically active tissues and growth rates for metabolically inert tissues. The aim of this research was to estimate isotopic incorporation rates in blue whale skin and baleen growth rates by using natural gradients in baseline isotope values between oceanic regions. Nitrogen (δ 15 N) and carbon (δ 13 C) isotope values of blue whale skin and potential prey were analyzed from three foraging zones (Gulf of Cali-fornia, California Current System, and Costa Rica Dome) in the northeast Pacific from 1996–2015. We also measured δ 15 N and δ 13 C values along the lengths of baleen plates collected from six blue whales stranded in the 1980s and 2000s. Skin was separated into three strata: basale, externum, and sloughed skin. A mean (±SD) skin isotopic incorporation rate of 163±91 days was estimated by fitting a generalized additive model of the seasonal trend in δ 15 N values of skin strata collected in the Gulf of California and the California Current System. A mean (±SD) baleen growth rate of 15.5±2.2 cm y-1 was estimated by using seasonal oscillations in δ 15 N values from three whales. These oscillations also showed that individual whales have a high fidelity to distinct foraging zones in the northeast Pacific across years. The absence of oscillations in δ 15 N values of baleen sub-samples from three male whales suggests these individuals remained within a specific zone for several years prior to death. δ 13 C values of both whale tissues (skin and baleen) and potential prey were not distinct among foraging zones. Our results highlight the importance of considering tissue isotopic incorporation and growth rates when studying migratory mysticetes and provide new insights into the individual movement strategies of blue whales.