Environmental Pollution xxx (2016) 1e10

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Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Mercury, selenium and stable isotopes in four small cetaceans from

the Southeastern Brazilian coast: Inuence of feeding strategy*
Gilberto Baptista a, Helena A. Kehrig b, *, Ana Paula M. Di Beneditto b,
Rachel A. Hauser-Davis c, Marcelo G. Almeida b, Carlos E. Rezende b, Salvatore Siciliano d,
Jailson F. de Moura e, Isabel Moreira a

lica do Rio de Janeiro, RJ 22453-900, Rio de Janeiro, Brazil
Departamento de Qumica, Pontifcia Universidade Cato

rio de Ci^
Laborato
encias Ambientais, Universidade Estadual do Norte Fluminense, Campos dos Goytacazes, RJ 28013-602, Brazil
~o em Ci^

s-Graduaa

gicas e Biodiversidade Neotropical, 22290-240, Rio de
Universidade Federal do Estado do Rio de Janeiro, Programa de Po
encias Biolo
Janeiro e RJ, Brazil
d
~o Mourisco e sala 122, Rio de Janeiro, RJ 21040-360, Brazil
Instituto Oswaldo Cruz/FIOCRUZ, Pavilha
e
Leibniz Center for Tropical Marine Ecology e ZMT, Bremen, 28359, Germany
a

b
c

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 11 April 2016
Received in revised form
28 July 2016
Accepted 31 August 2016
Available online xxx

Dolphins are good bioindicators of the contamination status of marine ecosystems, since their dietary
and habitat plasticity in both coastal and offshore ecotypes provide information on the trace elements
levels originated from natural and anthropogenic sources. In this context, this study aimed to investigate
provides mercury (Hg), selenium (Se) levels, trophic ecology and feeding environments of four small
cetaceans (Tursiops truncatus, Steno bredanensis, Sotalia guianensis and Pontoporia blainvillei) inhabiting
the central-northern coast of Rio de Janeiro State, southeastern Brazil. For the latter, d15N and d13C stable
isotopes were used as indicators in this regard. Stable isotope values indicate that the four studied
species have distinctive foraging habitats, coastal and least coastal, and occupy different trophic positions. The signicant relationship found between muscle Hg and d15N suggests that individual foraging
preference remains relatively constant for the studied dolphin species over extended periods. The individual prey size and species are probably responsible for the differences found in Hg and Se concentrations in muscle tissue among all dolphin species. The vulnerable small coastal cetacean, P. blainvillei,
which feeds on small teleost sh and squid, presented the lowest muscular Hg concentrations (less than
3.5 mg g
1 dry wt.). Meanwhile, S. bredanensis is more likely to uptake large amounts of trace elements
among the four dolphin species, due to its feeding habits mainly being large offshore sh that accumulate high amounts of trace elements in organs and tissues. Differences found between Hg concentrations in fetus-mother pairs were much higher in S. guianensis than in P. blainvillei, suggesting that
maternal contribution of Hg via placenta was more signicant for the former.
2016 Elsevier Ltd. All rights reserved.

Keywords:
Marine mammal
Trace elements
Tropical Western South Atlantic Ocean
Foraging habitat
Trophic position
Environmental risk assessment

1. Introduction
Dolphins are very sensitive to environmental changes, since

This paper has been recommended for acceptance by Maria Cristina Fossi.
* Corresponding author.
E-mail addresses: gilbert-souza@hotmail.com (G. Baptista), helena.kehrig@pq.
cnpq.br (H.A. Kehrig), anadibeneditto@gmail.com (A.P.M. Di Beneditto), rachel.
hauser.davis@gmail.com
(R.A.
Hauser-Davis),
marcelogaa@yahoo.com.br
(M.G. Almeida), crezende@uenf.br (C.E. Rezende), gemmlagos@gmail.com
(S. Siciliano), jailson.moura@zmt-bremen.de (J.F. de Moura), isabel@puc-rio.br
(I. Moreira).

they are long-lived apex predators, and especially susceptible to

anthropogenic impacts (Wells et al., 2004). These marine mammals
are the rst to reect the warnings about actual or potential
negative impacts on human health (Bossart, 2006). Thus, dolphins
are good bioindicators of the contamination status of marine ecosystems, since their dietary and habitat plasticity in both coastal
and offshore ecotypes (Monteiro et al., 2016) provide information
on the trace elements levels originated from natural and anthropogenic sources (Bossart, 2006).
Mercury (Hg) is a toxic trace element that occurs in all environmental compartments as a result of atmospheric transport and/
or deposition from the releases of anthropogenic and natural

http://dx.doi.org/10.1016/j.envpol.2016.08.088
0269-7491/ 2016 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Baptista, G., et al., Mercury, selenium and stable isotopes in four small cetaceans from the Southeastern
Brazilian coast: Inuence of feeding strategy, Environmental Pollution (2016), http://dx.doi.org/10.1016/j.envpol.2016.08.088

G. Baptista et al. / Environmental Pollution xxx (2016) 1e10

sources (Fitzgerald et al., 2007). In aquatic environments, Hg in the

form of methylmercury (MeHg), its more toxic organic form, is
biotransferred along marine food webs (Kehrig et al., 2013),
through benthic and pelagic pathways from base to higher trophic
levels, and undergoes a biomagnication process (Seixas et al.,
2014). This process results in high Hg concentrations in the tissues of apex predators in marine ecosystems (Kehrig et al., 2013;
Seixas et al., 2014). Hg is an exogenous and harmful trace
element that can affect the productivity, reproduction and survival
of marine mammals. High Hg concentrations in the tissues of the
dolphin Tursiops truncatus (Montagu, 1821), for example, have been
associated with markers of endocrine, renal, hepatic, hematologic
and immune system dysfunction (Reif et al., 2015).
Selenium (Se), on the other hand, has been identied as an
essential trace element that acts as a protective agent contrary to
the toxicity of non-essential metals such as Hg (U.S. EPA, 1997;
Feroci et al., 2005). Some studies have shown that this micronutrient may decrease Hg bioavailability, in the form of MeHg, since
it blocks Hg in insoluble compounds (Feroci et al., 2005), consequently decreasing MeHg toxicity. Like sulphur (S), Se readily
complexes with Hg, and both elements tend to bind to the sulphur
groupings present in proteins. Thus, it is reasonable to expect that
both Se and Hg bioaccumulate alongside each other in tissues of
marine organisms (Ganther et al., 1972).
Nitrogen (d15N) and carbon (d13C) stable isotopes are useful indicators of feeding ecology and can be related to contaminant
exposure (Aubail et al., 2011; Di Beneditto et al., 2011; Kehrig et al.,
2013). Trophic relationships and habitat use are of key importance
to the understanding, management and conservation of dolphins
and with regard to their position in marine food webs (Botta et al.,
2012). To achieve this, stable isotope ratios have been applied in the
last decades and have provided complementary data to existing
literature on animal trophic ecology. This technique presents timeintegrated information on food assimilation, and is able to evaluate
differences in trophic niche, trophic position and foraging sites (e.g.
Hobson and Welch, 1992; Di Beneditto et al., 2012).
Generally, stable isotope ratios of a consumer are related to
those of their prey, and consumers that occupy the same trophic
position show similar isotopic measurements (Di Beneditto et al.,
2011). In trophic ecology approaches, stable nitrogen isotopes
(d15N) are mainly used to distinguish different trophic levels and
food assimilation over time, while carbon (d13C) indicates different
dietary-based carbon sources, such as inshore vs. offshore, pelagic
vs. benthic or aquatic vs. terrestrial habits (De Niro and Epstein,
1981; Peterson and Fry, 1987). These isotopes are, therefore,
important indicators in feeding ecology and can also be used as
pollutant exposure indicators (Aubail et al., 2011; Di Beneditto et al.,
2011; Kehrig et al., 2013).
In this setting, in order to provide data about Hg and Se and their
distribution and environmental fate along the central-northern
coast of the Rio de Janeiro State, southeastern Brazil, Se and Hg
concentrations were determined in the muscle tissue of four

dolphin species, Steno bredanensis (Lesson, 1828), T. truncatus,

Pontoporia blainvillei (Gervais & dOrbigny, 1844), and Sotalia

ne

den, 1864), considered bioindicators of marine
guianensis (van Be
ecosystem health. Hg and Se were also evaluated in muscle tissue of
fetus-mother pairs of both P. blainvillei and S. guianensis, in order to
apprise maternal placental transfer of these trace elements. Stable
isotope analyses were then applied to evaluate differences or
similarities in the trophic position and foraging habitat among
dolphin species that could explain variations in Hg and Se
concentrations.
2. Materials and methods
2.1. Dolphin sampling
Four dolphin species with a priori different foraging habitats
(S. bredanensis, T. truncatus, S. guianensis and P. blainvillei) were
studied (Table 1). Specimens were found stranded or incidentally
entangled in shing nets along the central-northern coast of Rio de
Janeiro State (21 S-23 S), southeastern Brazil, mainly during the
wet season (MarcheJune), between 2001 and 2013 (Fig. 1). This
region is under inuence of the Paraiba do Sul River plume and also
is characterized by upwelling events that provide a source of food
for species at the top of the food web, such as marine mammals
(Coelho-Souza et al., 2012; Kehrig et al., 2013).
After each dolphin specimen was sexed and measured in the
eld regarding total length, muscle (back dorsal portion) samples
were removed, freeze-dried (losing around 70% of water content)
and stored until the trace elements (Hg and Se) and stable isotopes
(d15N and d13C) could be analyzed. Samples covered two fetus, and
mature individuals of both sexes, with body length varying from
240 to 272 cm (S. bredanensis), 250e300 cm (T. truncatus),
160e200 cm (S. guianensis) and 115e156 cm (P. blainvillei) (Table 1).
The maturity class of each individual was estimated from its body
length, according to the previous studies conducted by Ramos et al.
(2000) for S. guianensis and P. blainvillei, Siciliano et al. (2007) for
S. bredanensis and Wells et al. (1987) and Mead and Potter (1990)
for T. truncatus.
The rough-tooted dolphin, S. bredanensis, inhabits deep tropical
and subtropical offshore and oceanic waters of all three major
oceans, rarely ranging north of 40 N or south of 35 S (West et al.,
2011), although its distribution is not completely understood in
all areas of the world (Jefferson, 2009). However, in some areas
(such as off the coast of Brazil and West Africa), this species may
occur in shallower coastal waters. They prey on large teleost sh
and cephalopods (Di Beneditto et al., 2001a; Pitman and
Stinchcomb, 2002; Melo et al., 2010).
The bottlenose dolphin, T. truncatus, occurs in temperate and
tropical waters worldwide (Wells et al., 2004). The species inhabits
both open oceans and coastal waters including shallow lagoons,
estuaries and rivers, and is frequently found in water systems used
by humans (Durden et al., 2007). Fishes are the most representative

Table 1
Total number of mature specimens (N), number of specimens by gender, preferential habitat, mean body length (cm), mercury (Hg) and selenium (Se) concentrations
(mg g
1 dry wt.), Se:Hg molar ratios and trophic position (TP) in muscle tissue of the dolphin species from the central-northern coast of Rio de Janeiro State, southeastern Brazil.
Total number of sampling points of the primary consumers, i.e. mesoplankton (N), their body length (mm), Hg and Se concentrations (mg g
1 dry wt.) and TP from Kehrig et al.
(2013) collected at the central-northern coast of Rio de Janeiro State. TP for the dolphin species was determined relative to mesoplankton.
Species

Male

Female

Preferential habitat

Length

Steno bredanensis
Tursiops truncatus
Sotalia guianensis
Pontoporia blainvillei

9
10
28
16

5
5
14
9

4
5
14
7

oceanic
coastal-oceanic
coastal
coastal

255
272
182
130

Pooled species

mesoplankton

13
18
11
13

 290 mm

[Hg]

[Se]

10.15 6.23
4.38 2.47
3.91 2.16
1.92 0.96

3.66
2.25
1.59
1.80

Se:Hg

0.011 0.002

0.11 0.034

1.60
0,84
1.09
0.37

1.01
1.47
1.17
2.89

TP
0.27
0.53
0.81
1.27

26.93 4.30

4.61
4.59
3.92
3.76

0.23
0.09
0.25
0.27

2.00 0.09

Please cite this article in press as: Baptista, G., et al., Mercury, selenium and stable isotopes in four small cetaceans from the Southeastern
Brazilian coast: Inuence of feeding strategy, Environmental Pollution (2016), http://dx.doi.org/10.1016/j.envpol.2016.08.088

G. Baptista et al. / Environmental Pollution xxx (2016) 1e10

Fig. 1. Sampling area on the central-northern Rio de Janeiro coast, southeastern Brazil.

items of the total prey ingested (Di Beneditto et al., 2001a; Melo
et al., 2010).
The Guiana dolphin, S. guianensis and the Franciscana dolphin,
P. blainvillei are the most coastal and vulnerable small cetaceans
along the western South Atlantic Ocean, mainly due to interactions
with sheries (Di Beneditto, 2003). Both are sympatric along the
southwestern Atlantic Ocean, and coexist throughout the southeastern Brazilian coast between 19 S and 27 S. In addition, they
show minimal feeding overlap, exploiting mainly shallow waters
(at about 30 m or a little further) (Di Beneditto et al., 2011; Di
Beneditto and Ramos, 2014) to obtain their food sources, preying
upon pelagic and demersal neritic species. Fishes are the most
representative items in the diet of both species, although squid are
also important in the diet of P. blainvillei (Di Beneditto and Siciliano,
2007; Di Beneditto et al., 2009).
2.2. Mercury (Hg) and selenium (Se) analyses
Concerning Hg determinations, approximately 50 mg of the
freeze-dried muscle samples were digested in a sulphuric-nitric
acid mixture (HNO3/H2SO4) using vanadium pentoxide (V2O5) as
a catalyst. Total Hg in the samples was determined by cold vapor
atomic absorption spectrometry on a Flow Injection Mercury System (FIMS) e FIAS 400 using NaBH4 as the reducing agent, as
described previously (Kehrig et al., 1998; Moura et al., 2012).
Total Se determinations were conducted by digesting a 100 mg
portion of the freeze-dried samples in nitric acid and subsequent
analysis by graphite furnace atomic absorption spectrometry on an
Analytic Jena Model ZEEnit 60 spectrometer with Zeeman Effect
background correction and palladium nitrate as a chemical modier (Seixas et al., 2007).
Quality control of the method was performed by the analysis of
blanks, replicates and certied reference materials. Method accuracy was assessed through the analysis of certied material DORM2 (Hg: 4.64 0.26 mg g
1 dry wt. and Se: 1.40 0.09 mg g
1 dry wt.)
from the National Research Council of Canada. Method reproducibility was evaluated using the coefcient of variation of the replicates, which was always less than 10%. The values found for Hg
and Se were 4.60 0.45 mg g
1 dry wt. (ranging from 4.30 to 5.00;
N 12) and 1.36 0.097 mg g
1 dry wt. (ranging from 1.14 to 1.51;
N 9), respectively.
2.3. Stable isotope (d15N and d13C) analyses
Stable isotope measurements were determined in the freeze-

dried muscle samples using a Delta V Advantage isotope ratio

mass spectrometer (Thermo Scientic) interfaced with Cono IV
linked to an Elemental Analyzer Flash 2000 (Thermo Scientic).
Stable isotope ratios were reported in d notation as parts per
thousand () deviations from the international calibration standards. Pee Dee Belemnite carbonate and atmospheric nitrogen
were used as the standard values for the carbon and nitrogen
analysis, respectively. Samples were run with blank cups and
known analytical standards of the IVA Analysentechnik- 330802174
urea isotopic working standard (CH4N2O Mw 60, C 20%,
N 46%) of certied isotopic composition (d13C
39.79 and
d15N
0.73). Data quality control was checked with a reference
standard run (Elemental Microanalysis Protein Standard OAS, with
certied isotopic composition of d13C
26.98 and
d15N 5.94) after each ten sample batch. Reproducibility based
on triplicate analyses of 10% of the samples was of 0.2 for d13C
and d15N.
Regarding lipid-extraction, Kiljunen et al. (2006) and Post et al.
(2007) stated that a C: N ratio less than 3.5 indicates that the tissue
contains zero extractable lipids. In the present study, the mean C: N
ratios of the muscle samples, by weight from elemental composition, were less than 3.5, indicating low lipid content (Di Beneditto
et al., 2013). In this sense, lipid-extraction was not performed,
since this could have inuenced d13C results, and was not considered a restriction on the interpretation of muscle d13C values.
The Trophic Position (TP) of the dolphin species was estimated
relative to mesoplankton samples (primary consumer) as baseline
(TPprimary consumer) in the central-northern coast of the Rio de
Janeiro State. Mesoplankton samples were taken at three sampling
stations, during the wet season of 2008, by horizontal hauls at the
water surface, using planktonic conical 290 mm mesh size nets, as
reported previously (Kehrig et al., 2013). They were collected in the
same area used for dolphin species feeding, in the central-northern
coast of the Rio de Janeiro State. At these stations, mesoplankton
was composed mainly of microcrustaceans, primarily copepods and
cladocerans.
A
modied
Hobson
and
Welch
(1992)
equation
(TPdolphin [2 (d15Ndolphin
d15Nprimary consumer)]/3.4) was
applied to estimate the TP of each dolphin species. In this equation,
mesoplankton, which is the baseline organism, occupies a trophic
position of 2 (TPprimary consumer 2), while TPdolphin and d15Ndolphin
are the TP and d15N of each dolphin species studied, respectively,
d15Nprimary consumer (7.2 e 8.0; mean 7.61 0.36, according
to Kehrig et al., 2013) and 3.4 represents the most frequently

Please cite this article in press as: Baptista, G., et al., Mercury, selenium and stable isotopes in four small cetaceans from the Southeastern
Brazilian coast: Inuence of feeding strategy, Environmental Pollution (2016), http://dx.doi.org/10.1016/j.envpol.2016.08.088

G. Baptista et al. / Environmental Pollution xxx (2016) 1e10

trophic discrimination factor for d15N used for aquatic organisms

(Lavoie et al., 2013).
2.4. Statistical analyses
The statistical analyses were performed using the Statistica 7.0
software package for Windows (StatSoft, Inc, USA). Data were
tested for normal distributions. As data did not follow a normal
distribution, non-parametric tests were applied. The analysis of
data variance was conducted by the KruskaleWallis test-ANOVA
followed by a post test (ManneWhitney U test), in order to dene
signicant differences between Hg and Se concentrations and d15N,
TP and d13C values in dolphin muscle tissue, and between their
different feeding habitats. Spearman's rank correlation test (r) was
performed to determine the relationships between TP and stable
isotopes values, logarithmic trace element concentrations and trace
element molar ratios. A p value less than 0.05 was chosen to indicate statistical signicance.
3. Results and discussion
3.1. Stable isotopes (d15N and d13C) in dolphin species
The d15N and d13C values in muscle ranged from 15.2 to 17.8
and
15.8 to
17.6 for S. bredanensis; 15.9e16.7 and
15.2
to
15.9 for T. truncatus; 14.1e15.6 and
15.1 to
16.2 for
S. guianensis; and 13.6e14.6 and
15.5 to
16.1 for P. blainvillei,
respectively (Fig. 2). Signicant differences were detected in the
d15N and d13C values among dolphins (H 14.1; p < 0.001 for d15N
and H 8.8; p < 0.01 for d13C).
The d15N values found in dolphin species from the centralnorthern coast of Rio de Janeiro State were consistent and in the
same order of magnitude as previous studies along the southeastern and southern Brazilian coast regarding S. bredanensis (Botta
et al., 2012; Bisi et al., 2013), T. truncatus (Botta et al., 2012; Bisi
et al., 2013), S. guianensis (Di Beneditto et al., 2011; Bisi et al.,
2013; Kehrig et al., 2013; Di Beneditto and Monteiro, 2015) and
P. blainvillei (Di Beneditto et al., 2011; Di Beneditto and Monteiro,
2015).
Nitrogen isotopic data in muscle that integrate a long-term diet
(e.g., months) indicate differences related to this parameter among
the analyzed dolphin species, in which S. bredanensis and
T. truncatus displayed higher d15N values compared to S. guianensis
and P. blainvillei, that presented lower values (Fig. 2), suggesting

Fig. 2. Muscle d15N and d13C values of dolphin species from the central-northern coast
of Rio de Janeiro State, southeastern Brazil.

differences between the predators when considering trophic position (TP) in a long-term diet. TP values for the four dolphin species, determined relative to mesoplankton collected at the centralnorthern coast of Rio de Janeiro State, indicated the possibility of
the existence of two different trophic levels (Table 1): a higher one
for S. bredanensis and T. truncatus (TP 4.61 and 4.59, respectively)
and a lower one for S. guianensis and P. blainvillei (TP 3.92 and
3.76, respectively). Signicant differences were found in the TPs
among the dolphin species (H 22.8; p < 0.001 for TP).
d15N values in muscle of S. bredanensis and T. truncatus were
similar (p > 0.05), indicating that both species present the same
trophic position, i.e. displaying similar TP (Table 1). The same
behavior was observed regarding d15N values in muscle between
S. guianensis and P. blainvillei, suggesting that the trophic position of
these species is similar (Table 1).
In general, small sized specimens of a given dolphin species, i.e.
S. guianensis and P. blainvillei (Table 1), are less d15N enriched than
the large ones (S. bredanensis and T. truncatus), which could explain
muscle d15N differences between apex predators (Di Beneditto
et al., 2013).
The highest d15N values found in the muscle tissues of
S. bredanensis and T. truncatus suggests that these dolphin species
occupy the highest TP among the four dolphins considered in this
study (Fig. 2 and Table 1), and also that rough-toothed dolphin and
bottlenose dolphin probably feed on teleost sh signicantly larger
than those preyed upon by S. guiamensis and P. blainvillei in the
central-northern coast of Rio de Janeiro. According to Lodi and
Hetzel (1999), on different occasions, the authors observed that
rough-toothed dolphins were feeding in association with bottlenose dolphins in the coast of this state, both preying upon
schools of large carnivorous sh (Trichiurus lepturus) and mullet
(Mugil sp.).
In a previous study along the Rio de Janeiro coast, bottlenose
dolphins (14.9 1.7) and false killer whales (15.3 0.9) presented similarities in d15N values, and both species occupied the
highest and similar trophic positions (Bisi et al., 2013). However,
these delphinids were followed in TP by S. bredanensis (mean
d15N 14.4 0.3). These species showed the highest d15N values,
suggesting that these animals occupy the highest TP among the
delphinids considered by Bisi et al. (2013), corroborating with data
found in the present study.
The higher TP of S. bredanensis and T. truncatus in comparison
with S. guianensis and P. blainvillei can reect the food demand due
to differences in body size (Table 1), since, in animals of the same
taxonomic group, body mass is, in general, positively related to
trophic level (Jennings et al., 2002). Despite body size difference,
with S. guianensis being larger than P. blainvillei (Table 1), both
species are comparable in terms of d15N values and TP.
In the study area, as well as in nearby areas, S. guianensis feeds
preferentially on sh varying from 10 to 100 cm length, whereas
P. blainvillei preys upon organisms of up to 15 cm length, including a
large variety of juveniles and small-sized prey species (Di Beneditto
and Ramos, 2001, 2004; Di Beneditto and Siciliano, 2007). These
dolphins are apex predators whose main feeding resources are
associated with coastal and shallow waters (Di Beneditto and
Monteiro, 2015). Despite prey size consumed by P. blainvillei being smaller than S. guianensis, the former species ingests greater
amounts of its prey species when compared to the latter (Di
Beneditto and Ramos, 2001, 2004). For some prey species shared
by S. guianensis and P. blainvillei, the total amount (biomass)
ingested in each meal is equivalent (Di Beneditto et al., 2001b). This
condition can lead to similar isotopic values in consumers (Lassalle
et al., 2014).
Carbon isotopic data in muscle that reect differences in
foraging habitat suggest a difference related to this parameter

Please cite this article in press as: Baptista, G., et al., Mercury, selenium and stable isotopes in four small cetaceans from the Southeastern
Brazilian coast: Inuence of feeding strategy, Environmental Pollution (2016), http://dx.doi.org/10.1016/j.envpol.2016.08.088

G. Baptista et al. / Environmental Pollution xxx (2016) 1e10

among the dolphins, where S. bredanensis displayed lower d13C

values over T. truncatus, S. guianensis and P. blainvillei specimens,
that presented higher values (Fig. 2). The d13C values found in the
dolphin species were consistent and in the same order of magnitude as previous studies regarding along the southeastern and
southern Brazilian coast for S. bredanensis (Botta et al., 2012; Bisi
et al., 2013), T. truncatus (Botta et al., 2012; Bisi et al., 2013),
S. guianensis (Di Beneditto et al., 2011; Bisi et al., 2013; Di Beneditto
and Monteiro, 2015) and P. blainvillei (Di Beneditto et al., 2011; Di
Beneditto and Monteiro, 2015). d13C values are directly related to
geographical location, showing the broad-scale foraging location of
animals in the marine environment (Cherel and Hobson, 2007).
Tursiops truncatus, S. guianensis and P. blainvillei presented similar
d13C values (H 0.56; p > 0.50) in muscle, higher than
S. bredanensis (Fig. 2). These differences in d13C values indicate
distinct carbon source diets, i.e. in primary sources of carbon in food
webs, such as primary producers and consumers, with inshore and/
or benthic systems generally presenting higher values than
offshore and/or pelagic systems (Di Beneditto et al., 2011).
Thus, muscle d13C values indicate that S. bredanensis prefers to
feed on offshore and/or least coastal food webs in the marine
environment, while S. guianensis and P. blainvillei prefer inshore
food webs. In the study area, T. truncatus occurs in both coastal and
oceanic waters, from the shoreline beyond the continental slope
(Siciliano et al., 2006). Thus, the d13C values for this dolphin probably reect its high preference for demersal prey species, as indicated in Di Beneditto et al. (2001a). According to Jefferson (2009),
S. bredanensis are typically found in oceanic regions, but in Brazil
this species is commonly observed in shallow and coastal waters. In
a previous study, the d13C analysis in the muscle of S. bredanensis
indicated that this species uses the continental shelf waters in
southeastern Brazil, primarily foraging along the inner part of the
shelf (Bisi et al., 2013).
3.2. Mercury (Hg) and selenium (Se) in dolphin species
Total Hg and Se concentrations in the muscle tissue of mature
specimens of the four dolphin species did not show signicant
difference (p > 0.05) between genders in all species, conrming
previously reported results (O'Shea, 1999; Gerpe et al., 2002.;
Seixas et al., 2007; Moura et al., 2012; Ansmann and Lanyon, 2015;
Kehrig et al., 2016).
In the present study, P. blainvillei presented the lowest Hg concentrations in muscle tissue from all studied species, whereas the
highest concentrations were found in S. bredanensis (Table 1). The
relationships among the dolphin species regarding Hg concentrations were as follow: P. blainvillei < S. guianensis
T. truncatus S. bredanensis. Considering Se values, S. guianensis
presented the lowest muscle concentrations within all studied
species, while T. truncatus and S. bredanensis presented the highest
(Table 1). The relationships among the dolphin species considering
Se concentrations in muscle tissue were as follow:
S. guianensis < P. blainvillei T. truncatus S. bredanensis. In
general, P. blainvillei specimens from different South America regions have shown low muscle Hg and Se concentrations in comparison with other dolphin species (Gerpe et al., 2002; Carvalho
et al., 2008; Di Beneditto et al., 2011; Kehrig et al., 2016). Hg and
Se concentrations found in S. guianensis muscle were in the same
order of magnitude as data found in previous studies conducted
with this species in the northern Rio de Janeiro coast (3.28 1.69
and 1.60 1.32 mg g
1 dry wt., respectively) (Kehrig et al., 2013) and
in three bays of Rio de Janeiro coast, namely Guanabara Bay
(ranges: 0.7e8.3 mgHg g
1 and 0.3e1.3 mgSe g
1 dry wt.) (Kehrig
et al., 2004), (3.0 2.3 mgHg g
1 dry wt.) (Bisi et al., 2012), Sepetiba
Bay and
Ilha
Grande
Bay
(1.0

1.0
and

2.3 0.7 mgHg g
1 dry wt., respectively) (Bisi et al., 2012).
In a previous study conducted by Shoham-Frider et al. (2014),
the muscle tissue of one male calf of S. bredanensis (160 cm) found
stranded along the Israeli Mediterranean coast presented lower
mean Hg concentrations (four times lower) and higher mean Se
concentrations (two times higher) on a dry weight basis than those
found in specimens from the central-northern coast of Rio de
Janeiro State. On the other hand, T. truncatus specimens from the
Indian River Lagoon System, Florida, USA, presented higher muscle
Hg (5.68 mg g
1 wet wt.) and Se (1.92 mg g
1 wet wt.) concentrations (Durden et al., 2007) than those found in specimens from the
study area.
A number of physiological and environmental factors may inuence trace element bioaccumulation in dolphin tissues. Feeding
behavior (based on Hg- and Se-rich sh and cephalopods) and the
complexity of the marine food chains are the major factors
responsible for the bioaccumulation of trace elements in long-lived
marine animals (Seixas et al., 2007; Biland
zi et al., 2012). Differences among the dolphin species muscle Hg and Se concentrations
(Table 1) could be associated to variations in the capture of preferential prey, due to marine mammals accumulating trace elements
in tissues and organs throughout their lifespan (O'Hara and O'Shea,
2005). Hg and Se concentrations in dolphin tissues may reect
individual prey preferences, variation in habitat use, or differences
in the concentrations of maternally acquired Hg (Dietz et al., 1996;
Storelli and Marcotrigiano, 2000).
Comparing the analyzed marine habitats, the least coastal species, S. bredanensis, presented higher Hg concentrations than dolphin species from inshore marine habitat, S. guianensis and
P. blainvillei (Table 1). This area is a transitional faunistic region that
presents a great biodiversity with high ecosystem biomasses, and
also of food sources to the dolphin species (Kehrig et al., 2013),
which may subsequently dilute Hg and reduce its availability to the
biota, promoting a decrease in its trophic transfer efciency
rmberg et al., 1988; Kehrig et al.,
through the coastal food web (Bjo
1998). Thus, it was observed that the environmental conditions of
Rio de Janeiro's central-northern coastal area inuenced Hg
bioavailability in S. guianensis and P. blainvillei specimens.
The prey size consumed by P. blainvillei is smaller than
S. guianensis, as described previously (Di Beneditto and Ramos,
2001, 2004; Di Beneditto and Siciliano, 2007), and both dolphins
have a strong association with coastal and shallow environments
(Di Beneditto and Monteiro, 2015). Steno bredanensis, an oceanic
species, feed on large carnivorous sh, mainly ribbonsh (Trichiurus
lepturus), and also the squid species Loligo plei (Di Beneditto et al.,
2001a; Melo et al., 2010). Tursiops truncatus can occur in both
coastal and oceanic waters, exploring a wide variety of resources
(Culik, 2004; Wells et al., 2004). In the study area, the feeding
habitat of this dolphin includes mainly demersal sh, with seabottom association (Di Beneditto et al., 2001a).
Differences in growth rates of the dolphin species in this study
could be an explanation for variations in Hg and Se concentrations
of muscle, since dolphin growth rates may affect trace element
accumulation by changing the balance between the rate of deposition of new tissue and the gut adsorption efciencies for both
nutrients and trace elements (Kehrig et al., 1998).
Considering all dolphin species grouped together, Hg concentrations in muscle showed a clear linear increase with body length
(L) (Fig. 3) in the mature dolphin specimens, with an increment in
concentrations from P. blainvillei to S. guianensis, T. truncatus and
S. bredanensis, indicating that the accumulation of this trace
element is a function of the size of each species, i.e. function of
growth rates and species diversity. For S. bredanensis
([Hg] 0.19 L
38.96; p < 0.05; r 0.39), for T. truncatus
([Hg] 0.042 Le7.03; p < 0.05; r 0.30), for S. guianensis

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G. Baptista et al. / Environmental Pollution xxx (2016) 1e10

4,4

log [Hg] = 0.0044*L + 2.67; r = 0.74; p < 0.0001

log [Hg] ( g.kg-1 dry wt.)

S. bredanensis
4,0

3,6

S. guianensis

P.blainvillei
T. truncatus

3,2

2,8
100

150

200

250

300

body length - L (cm)

Fig. 3. Relationship between body length (L) and Hg concentrations (log10) on a dry
weight basis for all collected mature specimens.

([Hg] 0.083 L
11.03; p < 0.01; r 0.40) and for P. blainvillei

([Hg] 0.052 Le4.79; p < 0.001; r 0.68). Previous studies have
indicated a signicant relationship between Hg concentrations in
muscular, hepatic and renal tissues and body length, in certain
species, such as: P. blainvillei (Gerpe et al., 2002; Seixas et al., 2007),
Cephalorhynchus c. commersonii (C

aceres-Saez et al., 2013),
S. guianensis (Kehrig et al., 2013) and T. truncatus (Monteiro et al.,
2016).
In general, in long-lived marine mammals, Hg concentrations
increase with length or age due to these animals accumulating this
trace element in tissues throughout their life (Ikemoto et al., 2004),
probably related to the continuous accumulation of Hg through diet
combined with a much slower turnover rate in the body and also,
the rather long biological half-life of this element in these animals
(Neathery and Miller, 1975), since it shows a strong afnity with the
sulfhydryl groups (SH) present in cysteine (Kunito et al., 2004).
However, no signicant correlations (p > 0.05) were found between body length of specimens of all species and their muscle Se
concentrations although growth rates seem to inuence Se accumulation in other species, such as Commerson's dolphin specimens

ceres-Saez et al., 2013) and P. blainvillei (Kunito et al., 2004;
(Ca
Seixas et al., 2007).
It is difcult to compare data for trace elements among dolphin
species with different feeding habits, life spans, and from various
locations worldwide. In this case, it is better to compare the trace
element concentrations between individuals of the same species
that present a similar life span.
Data from the present study (Table 1) show that Se concentrations were in molar excess of Hg in almost all the evaluated dolphin
specimens, indicating that substantial Se was available in enough
amounts to counter Hg toxicity in these individuals. The Se: Hg
ratios showed signicant variation (H 22.7; p < 0.0001) among
dolphin species, and were also higher or equal to 1: 1 in all species
(Table 1). Furthermore, Se molar concentrations showed a clear
linear increase with Hg concentrations (Fig. 4) in S. bredanensis,
T. truncatus and S. guianensis specimens, whereas for P. blainvillei an
inverse relationship was found, where Hg concentrations
decreased with the increasing of Se concentrations. The high correlation between Hg and Se in the tissues of marine mammals is
well known (Dietz et al., 1996; Seixas et al., 2007) and could be a
reection of a direct association between these trace elements. It is
worth noting that the differences in the metabolism of dolphin
species can also inuence the accumulation of Hg and Se, as

reected in the Se: Hg molar ratios (Seixas et al., 2007).

Some studies showed that Se: Hg molar ratios in excess of 1:1
neutralize the adverse effects of Hg, protecting marine organisms
against Hg toxicity (Ganther et al., 1972; Leonzio et al., 1992). The
toxicity of Hg in its organic form, methylmercury (MeHg), is intimately associated with its high afnities with Se. In addition, MeHg
covalently binds to Se present in selenoenzymes, modifying the
enzyme that results in the adverse effects associated with Hg
toxicity. According to Ralston (2008), MeHg, biochemically, is a
specic inhibitor of selenoenzymes since it forms a highly stable
organic compound, methylmercury-selenocysteine (MeHg-SeCys)
in organisms exposed to Hg.
Hg in muscle tissue is usually found as MeHg, as previously
reported in different marine mammal species (Dietz et al., 1990;
Caurant et al., 1996; Kehrig et al., 2004). In addition, in a previous
study conducted with S. guianensis and P. blainvillei from an area
close to this study area, i.e. in the northern Rio de Janeiro coast,
Kehrig et al. (2016) found that Hg in muscle tissue was mostly in the
form of MeHg (94.4% and 95.2%, respectively).
In the present study, the question about the importance of trace
element transfer from mother to offspring in S. guianensis and
P. blainvillei is raised. Fetus S. guianensis (2.31 mgHg g
1 wet wt.) and
P. blainvillei (2.43 mgHg g
1 wet wt.) muscle Hg concentrations were
3.5 and 1.5 times lower than those found in their mothers
(8.01 mgHg g
1 wet wt. and 3.64 mgHg g
1 wet wt.), respectively.
Although only single data was available with regard to mother-calf
transfer, it is noteworthy that the difference between Hg concentrations in the fetus-mother pair was much higher in S. guianensis, which
may imply that the maternal contribution of Hg via placenta was more
signicant for this species than for P. blainvillei. However, Se concentrations in muscle of fetus and mother of both dolphin species
were similar, of 1.42 and 1.48 mgSe g
1 wet wt. for S. guianensis and
1.75 and 1.44 mgSe g
1 wet wt. for P. blainvillei, respectively.
Indeed, trace elements, mainly Hg, could be transferred via
placental or lactational transfer from mother to fetus and suckling
calves, affecting them during their most sensitive periods of
development (Gerpe et al., 2002; Lahaye et al., 2007). It is noteworthy that Hg, as MeHg, passes through the placental barrier and
accumulates in dolphin fetal tissues, whereas the placenta is an
important barrier against inorganic mercury (Neathery and Miller,
1975). However, knowledge about the maternal transfer of trace
elements to offspring is very limited in marine mammals. According to Gerpe et al. (2002), this situation may be related to the difculties of obtaining suitable samples, which usually take place in
an opportunistic way.
In a previous study with some metals in P. blainvillei tissues from
the Argentinean coast, the Hg and Cd concentrations found in one
fetus-mother pair suggested that the maternal contribution of
these metals via placenta was not signicant (Gerpe et al., 2002).
Meanwhile, a study with trace element levels in fetus-mother pairs
of short-beaked common dolphins (Delphinus delphis) from the
French coast indicated a limited maternal transfer of Hg during
pregnancy, since concentrations in the tissues of fetus were below
1 mg g
1 wet wt. (Lahaye et al., 2007). Yang et al. (2004) reported
that Hg, Cd and Ag concentrations in the liver of a fetus were
apparently lower than those of Dall's porpoise (Phocoenoides dalli)
mother. Results of blood dynamics of Hg and Se in northern
elephant seals (Mirounga angustirostris) suggested that maternal Se
transfer was prominent during lactation, whereas Hg transfer was
higher during gestation (Habran et al., 2011).
3.3. Relationships between trace elements and stable isotopes in
dolphin species
Analysis of dolphin muscle, which reveals differences in long-

Please cite this article in press as: Baptista, G., et al., Mercury, selenium and stable isotopes in four small cetaceans from the Southeastern
Brazilian coast: Inuence of feeding strategy, Environmental Pollution (2016), http://dx.doi.org/10.1016/j.envpol.2016.08.088

G. Baptista et al. / Environmental Pollution xxx (2016) 1e10

Fig. 4. Relationship between molar Hg and Se concentrations in the four dolphin species muscle tissue.

term diet (e.g., months), showed that, among all species, Hg concentrations varied as a function of d15N values and were also
inuenced by the type of foraging habitats (d13C) (Figs. 5 and 6).
Steno bredanensis specimens presented the highest muscle Hg
concentrations and were also enriched in d15N and depleted in d13C
in muscle, whereas the lowest Hg concentrations were found in
P. blainvillei, which presented lower d15N and higher d13C values.
Changes in stable nitrogen and carbon isotope ratios aid in
elucidating trophic relationships within marine food webs and
conrming the relationships between contaminant uptake and
trophic position (Cabana and Rasmussen, 1994). For all adult dolphin specimens combined and mesoplankton as the baseline of
d15N and d13C in the study area, positive relationships (p < 0.0001;
r 0.83 for d15N and p < 0.001; r 0.61 for d13C) were found between logarithmic Hg concentrations and stable isotopes (Figs. 5
and 6). The slope of the regression equation (b 0.20) found in
the relationship between Hg concentrations and d15N (Fig. 5) was
interpreted as indication of biomagnication power, i.e. can
represent the overall degree of Hg biomagnication (Lavoie et al.,
2013). This suggests trophic Hg concentration enrichment from
the baseline (mesoplankton) to the lowest TP dolphin species
(S. guianensis and P. blainvillei) and the highest TP dolphin species
(T. truncatus and S. bredanensis) in the marine food web, i.e. an Hg
biomagnication process. Biomagnication is described as an increase in trace element concentration that occurs through at least

two trophic positions in a food web (Barwick and Maher, 2003). The
biomagnication power found in this study for Hg is in agreement
with values reported in the literature, which vary widely from
0.16 0.16 for tropical, to 0.21 0.07 and 0.22 0.11 for polar and

Fig. 5. Relationship between d15N values and Hg concentrations (log10) on a dry

weight basis for all collected mature specimens.

Please cite this article in press as: Baptista, G., et al., Mercury, selenium and stable isotopes in four small cetaceans from the Southeastern
Brazilian coast: Inuence of feeding strategy, Environmental Pollution (2016), http://dx.doi.org/10.1016/j.envpol.2016.08.088

G. Baptista et al. / Environmental Pollution xxx (2016) 1e10

Fig. 6. Relationship between d13C values and Hg concentrations (log10) on a dry weight
basis for all collected mature specimens.

Fig. 7. Relationship between trophic position (TP) and Se to Hg molar ratio (log10) on a
dry weight basis for all collected mature specimens.

temperate ecosystems, respectively in different coastal and oceanic

areas worldwide (Lavoie et al., 2013).
The signicant relationship found between muscle Hg and d15N
suggests that individual foraging preferences remain relatively
constant over extended periods, thus indicating a degree of
adherence to diet and foraging areas, as also suggested for a
number of marine species in previous studies (Anderson et al.,
2009; Di Beneditto et al., 2012; Kehrig et al., 2013). However, according to Lavoie et al. (2013), the biomagnication process is not
only affected by food web process (e.g. growth rate, species diversity and length of food chain), but also by environmental
physico-chemistry variables. Thus, biomagnication of Hg can also
be assessed using TP in place of d15N values.
Herein, Hg concentrations (log10) in muscle of all collected
mature dolphin specimens and mesoplankton as baseline showed a
positive linear increase with TP in the central-northern coast of Rio
de Janeiro State, presenting the following relationship: log
[Hg] 0.67  TP 0.75; r 0.83; p < 0.05. The biomagnication
power or trophic magnication factor (TMF) was calculated using
the equation (TMF 10(b*3.4)) suggested by Lavoie et al. (2013),
where 3.4 is the trophic discrimination factor for d15N and b is the
slope of the regression equation (0.67). TMF found (0.36) represents the increase of Hg concentration per trophic position, as
previously reported by Lavoie et al. (2013).
Se concentrations for all dolphin specimens combined, unlike
Hg, showed a poor and non-signicant correlation with d15N values
(log[Se] 0.032*d15N 2.80; r 0.20; p > 0.50) in muscle tissue,
suggesting that Se did not increase successively with increasing
d15N values. According to Kehrig et al. (2013), the assimilation and
accumulation of Se in dolphin tissues are inuenced by different
processes in addition to feeding, since negative biotransference of
this element was observed from different prey to consumers
(S. guianensis), indicating that no Se biomagnication occurs, which
was the case of the present study.
Due to the insignicant increment of muscle Se concentrations
and the signicant increase of Hg concentrations with d15N values
and TP in all dolphin specimens combined, the Se to Hg molar ratio
(log10) plotted against TP in collected samples presented a highly
signicant linear negative relationship (r
0.86; p < 0.0001)
(Fig. 7). Thus, muscle Se: Hg molar ratios declined with the
increasing of the trophic position of the marine species, potentially
reducing Se-dependent protection in dolphin species that had
higher d15N values, i.e. were in higher TPs, feeding on least coastal

food webs in the marine environment. However, the coastal dolphins S. guianensis and P. blainvillei, which showed the highest
molar ratios and were in the lowest trophic position of the study
area, were less exposed to Hg by food ingestion and probably most
protected against Hg toxicity by Se.
In summary, individual prey size and prey species are probably
responsible for the differences found in Hg and Se concentrations in
muscle tissue between the dolphin species S. bredanensis, T. truncatus, S. guianensis and P. blainvillei. It is noteworthy that
S. bredanensis is more likely to uptake large amounts of trace elements within all studied species due to its feeding habits, since it
preys mainly on large sh that accumulate high amounts of trace
elements in organs and tissues. The stable isotope values of the four
dolphin species from southeastern Brazil revealed valuable information on their trophic ecology and feeding environments in the
tropical western South Atlantic, indicating that the dolphin species
have distinctive foraging habitats and occupy different trophic
positions.
Ethics statement
The data collection approach, which included dead stranded
animals, is under the protocol and regulations established by the
Brazilian Stranding Network of Aquatic Mammals (REMAB), coordinated by the National Centre for Research and Conservation of
Aquatic Mammals (CMA-ICMBio) from the Brazilian Ministry of the
Environment (MMA) (http://www.icmbio.gov.br/cma). This study
was approved by the Chico Mendes Institute for Biodiversity Conservation (ICMBio), and conducted under SISBIO license #32550e2.
Acknowledgments
The authors would like to thank the Brazilian National Research
~o de Amparo a

Council (CNPq; grant no 301.405/13-1), Fundaa
Pesquisa do Estado do Rio de Janeiro (FAPERJ; grant no E-26/
~o de Aperfeioamento de Pessoal de
201.161/2014) and Coordenaa
Nvel Superior (CAPES, project number BEX 0128/14-7) for nancial
support.
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Brazilian coast: Inuence of feeding strategy, Environmental Pollution (2016), http://dx.doi.org/10.1016/j.envpol.2016.08.088

G. Baptista et al. / Environmental Pollution xxx (2016) 1e10

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Brazilian coast: Inuence of feeding strategy, Environmental Pollution (2016), http://dx.doi.org/10.1016/j.envpol.2016.08.088