MARINE MAMMAL SCIENCE, **(*): ***–*** (*** 2017)
©2017 Society for Marine Mammalogy
Isotopic niche width differentiation between common
bottlenose dolphin ecotypes and sperm whales in the Gulf
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,
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.
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
N) to estimate quantitative metrics of isotopic
niche width (Bayesian standard ellipse areas, SEA
) 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
N values and SEA
, suggesting a latitudinal gradient in nitrogen
sources of coastal localities. The SEA
of inshore and offshore bottlenose dol-
phin ecotypes was completely distinct, indicating resource partitioning. Associ-
ated offshore ecotype and sperm whales had overlapping SEA
. 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
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
Corresponding author (e-mail: firstname.lastname@example.org).
MARINE MAMMAL SCIENCE, 34(2): 440–457 (April 2018)
C2017 Society for Marine Mammalogy
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
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
C and d
N values than their diet
(Peterson and Fry 1987, Das et al. 2000). The d
N enrichment between
cetacean skin and the prey consumed is estimated to be from 1.57&to
2.82&, while that for d
C is estimated to be from 1.01&to 1.28&(Bor-
rell et al. 2012, Gimenez et al. 2016). The d
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
IAZ-GAMBOA ET AL.: ISOTOPIC NICHE WIDTH 3
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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
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
Species Habitat nd
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
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
Offshore 1 –19.43 +3.53 14.9 +3.48
Offshore 7 –17.88 0.96 +1.98 16.35 0.39 +2.03
(17–25 cm ML)
Offshore 5 –17.01 0.93 +1.11 16.11 1.58 +2.27
(86–92 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
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
N and C:N ratios in an isotope-ratio
mass spectrometer interfaced in continuous ﬂow to a Carlo Erba Elemental Analyzer.
C is expressed in relation to the Vienna-Pee Dee Belemnite standard and the
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).
Signiﬁcant differences at a 0.05 level were tested by a multivariate analysis of vari-
ance (MANOVA) using the variables d
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
N, while its position is speciﬁed by the means of both vari-
ables. SEA was corrected for sample size (SEA
), because this approach nulliﬁes the
bias of SEA estimations related to small sample size (Jackson et al. 2011), and SEA
were ﬁtted to bivariate data by using maximum likelihood estimators. The isotopic
niche width is expressed as the SEA
contains 40% of the data regard-
less sample size. To compare the SEA
of different cetacean groups a Bayesian frame-
work was used, and SEA
(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
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
IAZ-GAMBOA ET AL.: ISOTOPIC NICHE WIDTH 5
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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
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
Figure 2. Common bottlenose dolphin ecotypes in the Gulf of California: inshore ecotype
(top) and offshore ecotype (bottom).
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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
Stable Isotope Ratios
Bottlenose dolphin ecotypes—There were signiﬁcant differences among ecotypes in
=80.4, P<0.01). Inshore individuals were enriched in
N than those from offshore locations (UN Tukey HSD, P<0.01) (Fig. 3,
Inshore locations—The mean isotopic ratios showed signiﬁcant differences among
inshore bottlenose dolphins from the northern, central and southern areas (F
Figure 3. Corrected standard ellipse areas (SEA
) representing the isotopic niche width of
common bottlenose dolphin ecotypes from different regions in the Gulf of California.
IAZ-GAMBOA ET AL.: ISOTOPIC NICHE WIDTH 7
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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
N (UN Tukey HSD, P<0.01). While
there were no signiﬁcant differences in d
C among the three zones, a strong trend
was observed for d
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
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
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
) representing the isotopic niche width of
associated offshore common bottlenose dolphins and sperm whales in the Gulf of California.
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IAZ-GAMBOA ET AL.: ISOTOPIC NICHE WIDTH 447
(Table 2), with the samples from the south more depleted in
C than those from the
central zone (UN Tukey HSD, P=0.02). There were no signiﬁcant differences
observed in d
Bottlenose dolphin ecotypes and sperm whales—There were no signiﬁcant differences in
isotopic ratios between sloughed skin and biopsy samples from sperm whales (F
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
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
18.2, P<0.01), with the latter being more enriched in
C (UN Tukey HSD, P<
0.01). No signiﬁcant differences were observed for d
N (Fig. 4, 5).
Potential prey—The d
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 (86–92 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
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
(see Fig. S1) of the inshore bottlenose dolphins from the north
, 95% credibility interval of 0.21&
), central (SEA
, 95% credibility interval
) and south (SEA
bility interval of 0.49&
) 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 (<1–4 cm of mantle
length), Dg.M: D. gigas –Medium (17–25 cm of mantle length), Dg.L: D. gigas –Large (86–
92 cm of mantle length).
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IAZ-GAMBOA ET AL.: ISOTOPIC NICHE WIDTH 449
ellipses of inshore bottlenose dolphins was driven by d
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
, 95% credibility interval of 0.31&
) and south
, 95% credibility interval of
) of the Gulf of California (Fig. 3), but in this case the separation of
the ellipses was mainly driven by d
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&
(95% credibility interval of 6.10e
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
, 95% credibility interval of 0.35&
sperm whales (SEA
, 95% credibility interval of
) exhibited an overlap of 0.18&
(95% credibility interval of
) (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.
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
C resulted in the
separation between ecotypes (Fig. 5). The difference in mean d
cates that the inshore ecotype feeds on prey from a
C-enriched environment, match-
ing the expected distribution of d
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
IAZ-GAMBOA ET AL.: ISOTOPIC NICHE WIDTH 11
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trophic network in coastal ecosystems (Walker et al. 1999). The
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,
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
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
N mean values between ecotypes was of 0.82&,withthe
inshore one being more enriched in
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
N derived from atmospheric
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
N values for inshore bottlenose dolphins in the Gulf of California (Fig. 3). The
isotopic composition of trophic webs tends to be enriched in
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
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
N-enriched values (Aguı~niga-Garcıa 1999, Shumilin et al. 2002). Signiﬁcant dif-
ferences in d
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
Beyond the Gulf of California geographic division used in this study (
rego 1983), differences in d
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
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
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
C, which is interpreted as they fed in a
C-enriched environment. With respect to d
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 (40–82 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 200–400 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
1.57&to 2.82&, while for d
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
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
C and 8.19&for 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,
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)
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
The following supporting information is available for this article online at http://
Figure S1. Posterior Bayesian estimates of the standard ellipse area (SEA
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
mode and the open red circles the corrected stan-
dard ellipse (SEA
) values. North (N), Central (C) and South (S).
Figure S2. Posterior Bayesian estimates of the standard ellipse area (SEA
), 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
mode. Central (C) and South (S).
Figure S3. Posterior Bayesian estimates of the standard ellipse area (SEA
) of associ-
ated offshore bottlenose dolphin ecotypes and sperm whales. Shaded density plots
represent 50%, 75%, and 95% credible intervals. Black dots represent SEA
and the open red circles the corrected standard ellipse (SEA
Figure S4. Posterior Bayesian estimates of the standard ellipse area (SEA
), 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
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