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Trophic Relationships and Habitat Preferences of
Delphinids from the Southeastern Brazilian Coast
Determined by Carbon and Nitrogen Stable Isotope
Composition
T atiana Lemos Bisi1'2'3*, Paulo R enato D óm eles3, Jo sé Lailson-Brito1, Gilles L epoint4, A lexandre d e
Freitas A zevedo1, L eonardo Flach5, Olaf M alm3, Krishna Das4
1 Laboratório d e M am íferos A quáticos e ßio in d icad o res "Profa. Izabel G urgel" (MAQUA), F acu ld ad e d e O cean o g rafía, U niversidade d o E stado d o Rio d e Jan eiro (UERJ), Rio
d e Janeiro, RJ, Brazil, 2 P rogram a d e P ôs-G raduaçâo em Ecología, U n iv ersid ad e F ederal d o Rio d e Jan eiro (UFRJ), Rio d e Jan eiro , RJ, Brazil, 3 Laboratorio d e R ad io isó to p o s
Eduardo P en n a F ranca, In stitu to d e Biofísica Carlos C hagas Filho, U niversidade F ederal d o Rio d e J an eiro (UFRJ), Rio d e Jan eiro , RJ, Brazil, 4 L ab o rato ire d 'O c ean o lo g ie MARE, U niversité d e Liège, Liège, Belgique, 5 Instituto B oto-cinza, M an g aratib a, RJ, Brazil
A bstract
To investigate the foraging habitats o f delphinids in southeastern Brazil, we analyzed stable carbon (S13C) and nitrogen
(S15N) isotopes in muscle samples o f the fo llo w in g 10 delphlnld species: Sotalia guianensis, Stenella frontalis, Tursiops
truncatus, Steno bredanensis, Pseudorca crassidens, Delphinus sp., Lagenodelphis hosei, Stenella attenuata, Stenella longirostris
and Grampus griseus. We also com pared the S13C and S15N values am ong fou r populations o f 5. guianensis. Variation In
carbon Isotope results from coast to ocean indicated th a t there was a significant decrease In S13C values from estuarlne
dolphins to oceanic species. 5. guianensis from Guanabara Bay had the highest mean S13C value, w hile oceanic species
showed significantly lower S13C values. The highest S15N values were observed fo r P. crassidens and T. truncatus, suggesting
th a t these species occupy the highest troph ic position am ong the delphinids studied here. The oceanic species 5. attenuata,
G. griseus and L. hosei had the lowest S15N values. Stable isotope analysis showed tha t the three populations o f S. guianensis
in coastal bays had different S13C values, but sim ilar S15N results. Guiana dolphins from Sepetiba and llha Grande bays had
different foraging habitat, w ith specimens from llha Grande show ing more negative S13C values. This study provides further
Inform ation on the feeding ecology o f delphinids occurring In southeastern Brazil, w ith evidence o f distinctive foraging
habitats and the occupation o f different ecological niches by these species In the study area.
C itation : Bisi TL, D orneles PR, Lailson-Brito J, L epoint G, A zev ed o AdF, e t al. (2013) T rophic R elationships a n d H ab itat P references o f D elphinids fro m th e
S o u th e a ste rn Brazilian C oast D ete rm in ed by C arbon a n d N itrogen S tab le Iso to p e C o m p o sitio n . PLoS ONE 8(12): e82205. doi:10.137 1 /jo u rn al.p o n e.0 0 8 2 2 0 5
Editor: Hans G. D am , U niversity o f C o n n ec tic u t, U nited S tates o f A m erica
Received May 15, 2013; A ccepted O cto b e r 22, 2013; Published D ecem b er 16, 2013
C opyrigh t: © 2013 Bisi e t al. This is an o p en -ac cess article d istrib u ted u n d e r th e te rm s o f th e C reative C o m m o n s A ttrib u tio n License, w hich p erm its u n restricted
use, distrib u tio n , an d rep ro d u c tio n in an y m e d iu m , p rovided th e original a u th o r a n d so u rc e a re cred ited .
Funding: This stu d y w as s u p p o rte d by Rio d e Jan eiro S ta te G o v ern m en t R esearch A gency - FAPERJ ("Pensa Rio" P ro g ram - Proc. E-26/110.371/2007 a n d APQ12009/1 - Proc. E26-110.858-2009), M inistry o f E ducation o f Brazil - CAPES ("Ciências d o Mar" - Proc. 23038.051661/2009-18), Brazilian R esearch Council - CNPq
(Proc. 482938/2007-2 an d Proc. 480701/2009-1) a n d C etacean S ociety In tern atio n al g ran t. This s tu d y w as also s u p p o rte d by a scientific c o o p e ra tio n e sta b lish ed
b e tw e e n CNPq a n d F.R.S.-FNRS (Proc. 490471/2010-2 CNPq). TLB h ad a sch o larsh ip fro m th e M inistry o f E ducation o f Brazil - CAPES, JL-B h as a research g r a n t from
FAPERJ/UERJ ("Prociência" P rogram ) a n d CNPq (g ran t # 3 0 5 3 0 3 /2 0 1 0 -4 ), AFA h as a research g r a n t fro m CNPq (g ran t # 3 0 4 8 2 6 /2 0 0 8 -1 ) a n d FAPERJ (JCNE
# 1 0 1 .4 4 9 /2 0 1 0 ), OM has a research g ra n t from CNPq a n d FAPERJ (CNE). GL a n d KD a re F.R.S.-FNRS R esearch A ssociates. T h e fu n d ers h ad n o role in s tu d y d esig n ,
d a ta collection a n d analysis, decision to publish, o r p re p a ra tio n o f th e m an u scrip t.
C om peting Interests: T he au th o rs h av e d ec lared th a t n o c o m p e tin g in terests exist.
* E-mail: tbisi@ yahoo.com .br
Introduction
occupy off-shore areas. Investigating the hab itat preferences a n d the
trophic relationships am o n g the delphinid species is o f great
im p ortance for u n d erstan d in g the roles a n d ecological niches
occupied by these anim als in m arine food webs. T his inform ation
will m ake it possible to b e tte r u n d e rstan d the degree o f overlap a n d
segregation o f delphinids in the foraging a rea in southeastern Brazil.
R io de Ja n e iro State is located along the southeastern Brazilian
coast. T his region is u n d e r high a nthropogenic pressure because it
is a n im p o rta n t u rb a n a n d industrial cen ter for Brazil [5,6,7,8],
H a rb o r activities, oil refineries, oil a n d n a tu ra l gas exploration,
seismic prospecting, e xpanding industrial parks, intense vessel
traffic a n d intense com m ercial fishing are also im p o rta n t sources o f
im pact along the R io d e ja n e ir o coast [5,9,10], In the face o f this
a nthropogenic pressure, ecological research o n delphinids, includ­
ing o n such topics as trophic relationships a n d h a b ita t preferences,
D elphinidae constitutes the richest taxonóm ica! fam ily o f all
cetaceans, w ith 36 currently recognized species. T h e presence o f
delphinids along the R io de Ja n e iro coast has b e e n re p o rte d from
direct observation o r from stranding records [1,2,3,4], T hese
species are distributed w ithin bays a n d estuaries (e.g., G u ia n a
dolphin, Sotalia guianensis), as well as along the continental shelf a n d
in oceanic environm ents off the coast o f R io de Ja n e iro State.
H ow ever, there is little inform ation regarding the h a b ita t prefer­
ences a n d feeding ecology o f delphinids from the study area. M ost of
the species, including false killer w hale (Pseudorca crassidens), R isso’s
dolphin (Grampus griseus), spinner dolphin (Stenella longirostris), F raser’s
dolphin (Lagenodelphis hosei) a n d pantropica! spotted dolphin (Stenella
attenuata), have b e en observed opportunistically because they usually
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Habitat Preferences of Delphinids
60°0'0"W
Brazil
30°0'0"S-
SG1
SG2
SG3
SG4
SF
TT
SB
•
PC
DC
■ LH
A SA
0
21W S
GC
-22°0'0"S
Rio de Janeiro State
G uanabara Bay
Sepetiba Bay
□O
V+
Atlantic Ocean
llha G rande Bay
44°0'0"W
23°0'0"S
43°0'0"W
42°0,0"W
41°0'0"W
Figure 1. M ap o f th e study area in Rio de Janeiro State, southeastern Brazil. S tranding sites of delphinids are show n. SG1 - Sotalia
guianensis from G uanabara Bay, SG2 - S. guianensis from S epetiba Bay, SG3 - S. guianensis from llha G rande Bay, SG4 - S. guianensis from "Regiáo dos
Lagos", SB - Steno bredanensis, TT - Tursiops truncatus, SF - Stenella frontalis, PC - Pseudorca crassidens, DC - Delphinus sp., LH - Lagenodelphis hosei, SA Stenella attenuata, SL - Stenella longirostris and GG - Grampus griseus.
doi:10.1371/journal.pone.0082205.g001
is re q u ire d to assess a n d m o n ito r the poten tial th reats to these
anim als in m arin e environm ents [11]. F or m ost o f the delphinid
species in southeastern Brazil, basic ecological know ledge is still
scarce.
T h e m ore trad itio n al m ethods used for studying the feeding
ecology o f cetaceans relies on stom ach co ntent analyses from
stran d ed o r accidentally caught anim als [12,13,14]. T his a p p ro ac h
m akes it possible to identify the species consum ed; how ever, the
technique used fragm ents o f preys in different stages o f digestion,
w hich can lead to over- o r und erestim atio n o f the im p o rtan ce o f
certain p re y species an d consequently h in d e r the in te rp reta tio n o f
dolphin feeding habits [15,16]. In addition, the use o f stran d ed
anim als can be biased, reflecting the diet o f sick o r injured anim als
th a t w ere not feeding norm ally before dying [17,18].
T h e analysis o f carb o n an d nitrogen stable isotopes has been
show n to be a useful com p lem en tary tool for investigating foraging
a n d feeding beh av io r o f cetaceans [19,20,21]. T h e usefulness o f
the technique is a consequence o f the fact th a t the stable-isotope
com position o f p re d ato rs reflects p rey signatures assim ilated over
tim e [22,23]. C a rb o n isotope (613C) values have b een used to trace
the p rim a ry source o f carb o n in the food w eb because this isotope
is indicative o f low trophic en rich m en t (1—2%o) [24,25]. T h u s, it is
possible to differentiate food sources originating from the following
systems: terrestrial versus m arine, coastal versus oceanic, or
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benthic versus pelagic [24,26,27]. In addition, ö 13C values o f
particu late organic m a tte r (PO M ) an d p h y toplankton can vary
along a gradient o f coastal to oceanic regions, w ith h igher ö 13C
values in w aters closer to the coast [28]. T h u s, it is possible to
investigate the foraging a rea a n d geographical v ariation in the use
o f the region by cetaceans, as well as to differentiate coastal species
o r populations from oceanic ones [19,21,29]. N itrogen isotopes
(615N) have b een used to study trophic relationships in m arine
food webs an d to assess trophic levels [20,30]. T his is possible due
to the relationship betw een 6 15N values an d the trophic position
th a t an organism occupies [31,32].
Stable carb o n a n d nitrogen isotope analyses w ere perform ed
using delphinid m uscle to 1) investigate the foraging a rea an d
trophic relationships o f 10 delphinid species from southeastern
Brazil, 2) com pare the stable isotope values a m ong four G u ian a
dolphin populations from the coast o f R io de Ja n e iro State, an d 3)
identify possible trophic differences betw een sexes an d am o n g age
classes o f G u ian a dolphins.
M aterials an d M ethods
Ethics S ta tem e n t
M uscle sam ples o f delphinids w ere collected w ith a p p ro p ria te
perm issions from B razilian E nv iro n m en tal Agencies - IB A M A /
2
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Habitat Preferences o f Delphinids
M M A (perm ission n u m b e r 11495-1) a n d IC M B io /M M A (perm ission n u m b e r 11579-1).
deviation o n replicated m easurem ents from a single delphinid
sam ple was ±0.3%o.
Because lipids have b e en show n to b e depleted in 13C a n d lipid
tissue c ontent can b e variable [24], we m easu red the elem ental
content a n d calculated the sam ple C :N ratio to verify the lipid
content o f each sam ple [33]. A total o f 24 sam ples presen ted
C :N > 3 .5 ; therefore, w e n orm alization the S13C values according
to the follow ing e q u atio n [33]:
Sam pling
M uscle sam ples o f 10 delphinids species (131 individuals) w ere
o b tain e d from specim ens either incidentally caught in gillnet
fisheries o r stran d ed o n the beaches o f R io de Ja n e iro State in
southeastern Brazil from 1994 to 2009 (Fig. 1). T h e following
species w ere targeted: A tlantic spotted dolphin, Stenella frontalis
(n = 1 3 ), bottlenose dolphin, Tursiops truncatus (n = 7), ro u g h ­
to o th e d dolphin, Steno bredanensis (n = 3), false killer w hale, Pseudorca
crassidens (n = 2), c om m on dolphin, Delphinus sp. (n = 2), F raser’s
dolphin, Lagenodelphis hosei (n = 1 0 ), p a n tro p ica l spotted dolphin,
Stenella attenuata (n = 2), spinner dolphin, Stenella longirostris (n = 1),
a n d R isso’s dolphin, Grampus griseus (n = 1), a n d 4 populations o f
G u ia n a dolphin, Sotalia guianensis, from G u a n a b a ra B ay (n = 26),
S epetiba Bay (n = 49), lilia G ra n d e Bay (n = 10) a n d “ R egiâo dos
L agos” (n = 5).
513Cnormalized = (513Cimtreated —3.32 + 0.99 * C : N
Statistical analysis
T h e K olm ogorov-S m irnov test was used to test for norm ality o f
the d a ta (K-S d = 0.083 a n d d = 0.081, p > 0 .2 0 ). Analyses o f
v ariance (ANOVA), follow ed b y a n L hiequal N F1SD post-hoc test,
w ere used to co m p a re carb o n a n d n itrogen isotope values am o n g
species; d o lphin calves w ere excluded from these analyses. In
addition, w e p erfo rm ed a cluster analysis aim ing to detect isotopic
p attern s am o n g delphinids species. F or this analysis, we used
W a rd ’s m eth o d (m inim um variance) a n d E u clidean distances [34].
A N O V A s w ere also used to verify differences in S 13C a n d S 15N
values a m o n g adult m ales, a d u lt females a n d calves o f G u ia n a
dolphins from G u a n a b a ra a n d Sepetiba bays. T h e S tu d e n t’s t-test
was p erfo rm ed to co m p are m ale a n d fem ale dolphins from lilia
G ra n d e Bay.
A nalysis o f 8 13C an d 8 1SN
M uscle sam ples w ere dried a t 60"C for 72 h a n d th en gro u n d
into a hom ogeneous pow der. D ried sam ples ( ~ 1.5 mg) w ere
w eighed a n d p laced in tin capsules (3 x 5 nini), a n d carb o n a n d
n itrogen stable isotope m easurem ents w ere p erfo rm ed on a V .G .
O p tim a (Isoprim e LTK) isotope ratio m ass spectrom eter coupled to
a n N -C -S elem ental analyzer (Carlo E rba). Stable isotope ratios
w ere expressed in delta n o tatio n as p a rts p e r th o u san d according
to the follow ing equation:
Results
<5X= [(Rsam ple/Rstandard) — 1] x 1000
F o r the analyses, the four populations o f G u ia n a dolphins
occurring along the R io de Ja n e iro State coast w ere trea te d as
distinct groups. T h re e o f these populations use in n er areas o f
coastal bays (i.e., G u a n a b a ra Bay, lilia G ra n d e Bay a n d S epetiba
Bay) a n d the fourth occurs along the coast in a n a re a know n as
“ R egiâo dos L agos” . M e a n S 13C a n d S 15N values from the 10
delphinids species from the R io de Ja n e iro State coast ra n g ed from
w here X is 13C o r 15N a n d R is the corresponding ratio o f 13C/*~C
o r 15N / 14N . C a rb o n a n d n itrogen ratios w ere expressed in
relationship to the V -P D B (V ienna P eedee Belem nite) sta n d ard
a n d to atm ospheric nitrogen, respectively. R eference m aterials
(IAEA C H -6 a n d IAEA-N 1) w ere also analyzed. T h e sta n d ard
T a b le 1 . Mean (±SD ) 013C and 015N values in delphinids muscle tissues from the coast o f Rio de Janeiro State, southeastern Brazil.
C om m on nam e
G uiana dolphin
Species
n
513C (%»)
8 15N (%»)
mean ± S D
m in /m a x
m ean ± S D
m in /m a x
S o talia guianensis
G u an ab ara Bay
20
—1 3 .8 ± 0 .7
-1 5 .3 /- 1 2 .5
14.2 ± 0 .9
12.2/16.2
S ep etib a Bay
44
—1 4 .6 ± 0 .9
- 1 6 .9 /- 1 2 .8
14.1 ± 0 .6
12.9/15.5
llha G ran d e Bay
10
- 1 6 .6 ± 0 .4
- 1 7 .3 /- 1 6 .0
14.2 ± 0 .2
13.5/15.3
G uiana dolphin
S o talia guianensis
"R egiâo d o s Lagos"
5
—1 4 .9 ± 0 .6
- 1 5 .7 /- 1 3 .9
1 3 .7 ± 0 .7
12.6/14.5
A tlantic s p o tte d d olphin
Stenella fron talis
13
- 1 6 .0 ± 0 .4
- 1 6 .6 /- 1 5 .4
13.5 ± 1.0
12.2/15.4
B ottlenose d o lp h in
Tursiops trun catus
7
- 1 5 .5 ± 0 .5
- 1 6 .1 /- 1 4 .6
14.9 ± 1.7
11.6/16.7
R o u g h -to o th ed d o lp h in
Steno bredanensis
3
—1 4 .9 ± 0 .5
-1 5 .4 /- 1 4 .3
14.4 ± 0 .3
14.1/14.8
False killer w h ale
Pseudorca crassidens
2
- 1 4 .5 ± 0 .3
-1 4 .8 /- 1 4 .3
15.3 ± 0 .9
14.7/15.9
C om m on d o lp h in
D elphinus sp.
2
—1 5 .6 ± 0 .6
—1 6 .1 /—15.2
12.3 ± 0 .4
12.0/12.6
Fraser's d o lp h in
Lagenodelphis hosei
10
- 1 6 .5 ± 0 .3
- 1 7 .2 /- 1 6 .0
12.6 ± 1.0
10.0/13.8
P antropical s p o tte d d o lp h in
Stenella a tte n u a ta
2
—1 5 .8 ± 0 .2
- 1 6 .1 - 1 5 .7
11.4 ± 0 .2
11.1/11.4
S pinner d o lp h in
Stenella lo ngirostris
1
-1 7 .1
Risso's dolphin
G ram pus griseus
1
- 1 5 .7
12.1
-
11.3
-
doi:10.1371 /journal.pone.0082205.t001
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December 2013 | Volume 8 | Issue 12 | e82205
Habitat Preferences o f Delphinids
killer w hales a n d bottlenose dolphins h a d higher S 15N m ea n values
c o m p a red to com m on, F raser’s a n d p a n tro p ical spotted dolphins
(Lhiequal N H S D test, p < 0 .0 5 ; T ab le 2). T h e lowest S 13C a n d
S 15N values w ere observed for oceanic delphinids (i.e., spinner,
R isso’s, F raser’s a n d p a n tro p ical spotted dolphins). W e found
significant differences betw een the oceanic species (i.e., F raser’s
a n d p a n tro p ical spotted dolphins) a n d G u ia n a dolphins for b o th
S 13C a n d S 15N values (LTnequal N H S D test, p < 0 .0 5 ; T ab le 2).
LTsing S 13C a n d S 15N values, cluster analysis (W ard’s m ethod)
identified five groups am o n g the delphinid species (Fig. 4). T h e
analysis show ed a carb o n isotopic contin u u m , w ith the highest
values in estilarm e dolphins (G uiana dolphin), a n d the lowest
values in oceanic delphinids (spinner a n d F raser’s dolphins). T h e
five groups found w ere classified as follows: 1) estuarine dolphins
a n d species th a t use the in n er continental shelf (G uiana dolphins
from G u a n a b a ra Bay, Sepetiba B ay a n d “ R egiâo dos Lagos” a n d
ro u g h -to o th ed dolphin); 2) co n tinental shelf species (bottlenose
do lphin a n d false killer whale); 3) species influenced b y the S outh
A tlantic C en tral W ater (SACW) (G uiana dolphins from lilia
G ra n d e Bay a n d A tlantic spotted dolphin); 4) shelf-slope species
(com m on, R isso’s a n d p a n tro p ical spotted dolphin); a n d 5) oceanic
species (Fraser’s a n d spinner dolphin).
W e c o m p a red adult m ales, adult fem ales a n d calves from
G u a n a b a ra a n d Sepetiba bays. T h e re was no significant difference
in 8 C values in individuals from G u a n a b a ra Bay (A N O V A
F(2 .2 2 ) = 0.26; p = 0.77), a lthough there was a difference in S 15N
values (A N O V A F,2.22) = 6.44; p = 0.006). Calves show ed higher
S 15N values in relation to a d u lt m ales a n d females; the adult m ales
a n d females them selves did n o t show differences (LTnequal N H S D
test; p < 0 .0 2 a n d p > 0 .9 8 , respectively) (T able 3). T h e re was
difference b etw een adult m ales, adult fem ales a n d calves from
Sepetiba Bay b o th for S13C (A N O V A F,2 44) = 4.93; p = 0.011) a n d
S 15N values (A N O V A F,2.44) 34.99; pC O .00001) (T able 3). T h e
post-hoc test show ed th a t there was no significant difference
betw een m ales a n d females for S 13C a n d S 15N values (LTnequal
N H S D test; p < 0 .9 9 a n d p = 0.08, respectively). Calves h a d higher
S 15N values th a n adults (LTnequal N H S D test; pCO.OOOl). F or
specim ens from lilia G ra n d e Bay, the only possible com parison
p erfo rm ed was betw een adult m ales a n d females due to the
absence o f calf sam ples. V alues o f S 13C a n d S15N w ere sim ilar for
b o th sexes (T able 3; /-test; t = 1.16, p = 0.28 a n d t = 0.40, p = 0.69,
respectively).
16 PC
TT
SG1
SG3
SG2
LH
DC
SL
12
-
.GG
-18
-17
-16
15
-14
-13
S 1 3 C (% o )
Figure 2. M ean (±S E ) ô13C and ô15N values fo r d elphinid
muscle tissues from specimens collected from Rio d e Janeiro
State. • Sotalia guianensis from G uanabara Bay (SG1), O 5. guianensis
from S epetiba Bay (SG2), ▼ S. guianensis from llha G rande Bay (SG3), A
S. guianensis from "Regiâo d o s Lagos" (SG4), ♦ Steno bredanensis (SB),
□ Tursiops truncatus (TT), ■ Stenella frontalis (SF), O Pseudorca
crassidens (PC), ▲ Delphinus sp. (DC), V Lagenodelphis hosei (LH), ♦
Stenella attenuata (SA), 0 Stenella longirostris (SL) and 9 Grampus
griseus (GG).
doi:10.1371/jo u rn al.pone.0082205.g002
—17.1 to —13.8%o a n d from 11.3 to 15.3%o, respectively (T able 1,
Fig. 2). T hese values varied significantly am o n g species (A N O V A ,
S 13C: F(10,io 7 ) = 18.64, pCO.OOOl a n d S 15N: F (10, io?) = 7.04,
pCO.OOOl) (T able 2). Statistical tests could not be p erform ed
using d a ta from spinner a n d R isso’s dolphins (n = 1).
O f the four populations o f G u ia n a dolphins, the specim ens from
G u a n a b a ra Bay exhibited the highest S 13C values, while dolphins
from Sepetiba Bay a n d “ R egiâo dos L agos” h a d interm ediate
values a n d individuals from the lilia G ra n d e B ay h a d the lowest
S 13C values (Lhiequal N F1SD test; p < 0 .0 3 ) (T able 2). H ow ever,
th ere was no difference in S15N values am o n g these populations
(U nequal N H S D test; p > 0 .9 9 ) (Fig. 3).
G u ia n a dolphins from G u a n a b a ra Bay also displayed signifi­
cantly higher S 13C values th a n A tlantic spotted, bottlenose a n d
F raser’s dolphins (LTnequal N H S D test, p < 0 .0 5 ; T ab le 2). False
Table 2. Results o f the Unequal N HSD post-hoc test fo r m ultiple comparisons o f S13C (upper-right) and S15N (lower-left) values
from samples o f delphinid muscle tissues collected from the coast o f Rio de Janeiro State, southeastern Brazil.
SG1
SG1
SG2
SG3
SG4
SF
TT
SB
PC
DC
LH
SA
0 .0 3
0 .0 0
0.35
0 .0 0
0 .0 0
0.75
0.99
0.30
0 .0 0
0.15
0 .0 0
0.99
0 .0 0
0.45
0.99
1.00
0.93
0 .0 0
0.80
0 .0 2
0.86
0.22
0.19
0.19
0.97
1.00
0.99
0.42
0.97
1.00
0.99
0.99
0 .0 3
0.96
0.96
0.74
0.64
0.99
0.89
1.00
0.99
0.96
1.00
0.25
0.99
0.99
0.99
0.21
0.95
0.91
0.21
0.75
SG2
0.99
SG3
1.00
0.99
SG4
0.99
0.99
0.99
SF
0.57
0.82
0.69
0.99
TT
0.91
0.77
0.93
0.52
0.09
SB
1.00
0.99
1.00
0.99
0.96
0.99
PC
0.97
0.94
0.97
0.76
0.59
0.99
0.99
DC
0.54
0.65
0.52
0.88
0.96
0.11
0.39
0 .0 3
LH
0 .0 0
0.0 1
0 .0 0
0.66
0.50
0 .0 0
0.31
0.09
1.00
SA
0 .0 4
0.06
0 .0 3
0.17
0.29
0 .0 0
0 .0 2
0 .0 0
0.97
0.98
1.00
0.99
0.09
doi:10.1371 /jo u rn al.pone.0082205.t002
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Habitat Preferences of Delphinids
-13.5
14.6
-14.0
14 4
-14.5
14.2
-15.0
14.0
é
&
•o
-15.5
-16.0
13.6
-16.5
13.4
-17.0
13.2
SG1
SG2
SG3
SG4
Figure 3. M ean (±S E) ô13C and ô15N values fo r Guiana d olph in muscle tissues. S pecim ens are from G uanabara Bay (SGI), S epetiba Bay
(SG2), llha G rande Bay (SG3) and "Regiâo dos Lagos" (SG4), Rio d e Janeiro State, so u th e astern Brazil. (A) 813C values; (B) 81SN values.
doi:10.1371/journal.pone.0082205.g003
D iscussion
systems having h igher values th a n oceanic a n d /o r pelagic systems
[24,26,27],
G u ia n a dolphin is a species th a t inhabits estuarine a n d coastal
regions th ro u g h o u t its distribution [37] a n d is found in th e three
coastal bays o f R io de Ja n e iro State [3,38,39], A m ong th e species
studied, G u ian a dolphins from G u a n a b a ra Bay h a d th e highest
average 8 loC values, even w hen co m p ared w ith th e sam e species
from S epetiba a n d llh a G ra n d e bays. F o r dolphins from
G u a n a b a ra Bay, high site fidelity [3] a n d p re d atio n prim arily on
dem ersal, estuarine fish [40] result in the populatio n being u n d e r
th e constant influence o f the in terio r w aters o f th a t bay, w hich m ay
explain th e high 8 'C values.
Analysis o f c arb o n isotopes has pro v en to be a very useful tool
for identifying differences in b o th inter-[19,30] a n d intra-specific
[29,35] h a b ita t preference. D elphinid 8 loC values revealed
differences betw een species a n d allow ed us to define groups
according to th eir foraging h ab itat. T h e re was a significant
decrease in 8 loC values from estuarine dolphins to oceanic species,
indicating coast-ocean variatio n in isotopic ratios. Sim ilar results
w ere observed in o th er studies involving cetaceans [19,29,30,36],
T hese differences are due to distinct 8 loC values in p rim a ry
sources o f c arb o n in food w ebs, w ith coastal a n d /o r benthic
SG1
Estuarine and inner continental sh e lf use
SG2
SB :
SG4
TT
Continental she lf
PC
SG3
SF
Influenced by the SACW*
DC
SA
slope break
GG
LH
SL
Oceanic environm ent
0
2
4
6
8
10
12
Distance m etric (Euclidean)
Figure 4. Results o f the cluster analysis (W ard's m ethods) based on ö13C and ö1sN in delphinids muscle tissues. SGI - Sotalia guianensis
from G uanabara Bay, SG2 - S. guianensis from S epetiba Bay, SG3 - S. guianensis from llha G rande Bay, SG4 - S. guianensis from "Regiâo d os Lagos", SB Steno bredanensis, TT - Tursiops truncatus, SF - Stenella frontalis, PC - Pseudorca crassidens, DC - Delphinus sp., LH - Lagenodelphis hosei, SA - Stenella
attenuata, SL - Stenella longirostris and GG - Grampus griseus. *SACW - S outh Atlantic Central Water.
doi:10.1371/joum al.pone.0082205.g004
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Habitat Preferences o f Delphinids
in the trophic position o f these populations due to v a riation in the
nitrogen isotopic com position a t the base o f the food webs am o n g
different systems. Bisi et al. [46] suggested th a t S 15N values w ere
red u ced at the base o f the G u a n a b a ra Bay food w eb. T h e sam e
au th o rs verified th a t G u ia n a dolphins from G u a n a b a ra Bay
occupy the top trophic level o f the food w eb in this estuary,
exhibiting the highest S 15N values am o n g the different organism s
studied. In contrast, the specim ens from S epetiba Bay are feeding
o n organism s th a t occupy relatively low er trophic levels [46],
T h u s, although G u ia n a dolphins from G u a n a b a ra Bay show ed
sim ilar S 15N values to those o f o th er populations o f the species,
they m ay occupy a h igher trophic position in the food web.
Previous studies on m arin e m am m als have show n th a t feeding
ecology m ay or m ay n o t vary betw een m ales a n d females
[20,21,49,50], T his study found no influence o f sex o n feeding
o f G u ia n a dolphins in G u a n a b a ra , Sepetiba o r lilia G ra n d e bays.
F u rth e rm o re , calves h a d h igher S15N values th a n adults in
G u a n a b a ra a n d Sepetiba bays. T hese findings are p ro b ab ly due
to isotopic fractionation d u rin g the assim ilation o f b reast milk, as
calves occupy a h igher “ trophic level” th a n th eir m others du rin g
nursing periods [49], O u r results are in accordance w ith sim ilar
studies cond u cted o n o th er m arin e m am m al species [20,49,50],
G u ia n a dolphins from lilia G ra n d e Bay a n d the A tlantic spotted
do lphin w ere gro u p ed by cluster analysis. E xcept for two
specim ens, the A tlantic spotted dolphins sam pled w ere obtain ed
from beaches o f “ R egiâo dos L agos” , a n a rea influenced b y the
South A tlantic C entral W ater (SACW) upw elling d u rin g the
sum m er [51,52]. S A C W also enters lilia G ra n d e Bay in the
sum m er season, influencing the richness, diversity a n d a b u n d an c e
o f organism s [53]. M o re negative S13C values o f organic carb o n
dissolved in w aters u n d e r the influence o f S A C W have b een
observed [54], a n d the sim ilarity o f S13C values b etw een G u ia n a
dolphins from lilia G ra n d e Bay a n d A tlantic spotted dolphins
suggest th a t SA C W influences the foraging areas o f these two
species along the coast o f R io de Ja n e iro State.
R o u g h -to o th e d dolphins are typically found in oceanic regions
[55], b u t in Brazil they are com m only observed in shallow a n d
coastal w aters [55,56,57]. T h e results o f the S13C analysis suggest
th a t the species uses continental shelf w aters in southeastern Brazil,
prim arily foraging along the in n er p a rt o f the shelf. T his
hypothesis is reinforced b y the results o f the cluster analysis, in
w hich G u ia n a a n d ro u g h -to o th ed dolphins shared the sam e group.
Bottlenose dolphins a n d false killer w hales occupied sim ilar
trophic niches, w ith sim ilarities in S 13C a n d S 15N values. T hese
species h a d the highest S15N values, suggesting th a t these anim als
occupy the highest trophic level a m o n g the delphinids considered
in this study. S tom ach c ontent analyses show ed th a t bottlenose
dolphins feed m ainly o n teleost fish a n d cephalopods along the
south-central coast o f R io de Ja n e iro State [14], M oreover, fish
p rey ed u p o n b y this species w ere significantly larg er th a n those
p rey ed u p o n by o th er delphinids in this region. False killer whales
also feed o n fish a n d cephalopods, b u t the intake o f small cetaceans
has also b e en re p o rte d [56,58], In addition, som e studies have
show n distinct foraging p attern s for false killer w hales in the S outh
A tlantic O c e a n based o n S 15N values [19,36], T h e false killer
w hale w ith low S15N values are p ro b ab ly feeding specifically on
cephalopods, w hereas individuals th a t are 15N -en rich ed w ould be
feeding a t h igher trophic levels (e.g., fish) [19,36], D u e to the high
S 15N values found in this study, it is likely th a t false killer whales
p rey m ainly o n high-trophic-level fish o r even o n m arin e
m am m als. T hese results are in acco rd an ce w ith the high
concentrations o f o rg anohalogen com pounds found in tissues o f
false killer whales from the study region, w hich suggest regular
feeding on m arin e m am m als [59,60], B ottlenose dolphins a n d false
Table 3. Mean (±SD) S13C and S15N values o f muscle tissues
from adult males, adult females and calves1 o f Guiana
dolphins.
513c (%»)
m ale
815n (%»)
fe m a le
calf
m ale
G uanabara Bay - 1 3 .6 ± 0 .6 - 1 3 .8 ± 0 .6 -1 3 .5 ± 1 .1 14.2±1.1
(n = 11)
Sepetiba Bay
(n = 8)
(n = 6)
(n = 13)
(n = 6)
14.4±0.4 16.2±0.7
(n = 5)
llha G rande Bay —16.4±0.3 —16.8±0.6
(n = 6)
calf
14.4±0.7 16.0±1.3
(n = 8)
1 4 .6 ± 0 .9 -1 4 .6 ± 1 .0 —13.2±0.6 13.9±0.6
(n = 29)
fe m a le
(n = 3)
14.4 ± 0.6 14.02 ± 0.8
(n = 6)
(n = 3)
S p e c im e n s m easu rin g up to 117.5 cm [72].
dol:10.1371 /jo u rn al.pone.0082205.t003
Site fidelity o f G u ia n a d o lphin has also b e en observed in
S epetiba B ay [38], H ow ever, som e au th o rs suggest th a t lilia
G ra n d e Bay is also used by individuals from Sepetiba Bay [41],
because these bays are adjacen t a n d con n ected by a central
channel. O u r results show ed th a t G u ia n a dolphins from Sepetiba
a n d lilia G ra n d e bays have different foraging h a b ita t, w ith
specim ens from lilia G ra n d e h aving 13C -depleted values. S13C
values p o in t to tw o distinct ecological populations in Sepetiba a n d
lilia G ra n d e bay. T hese findings c o rro b o rate results from previous
studies show ing differences in the accum ulation o f organochlorine
com pounds [42], in sound em ission characteristics [43], a n d in
genetic structure [44] betw een the two populations. T hese results
from previous studies, in conjunction w ith the stable isotope data,
suggest th a t m ovem ent o f G u ia n a dolphins b etw een the two bays is
not frequent, fu rth er suggesting th a t the species shows high site
fidelity [3].
T h e S13C values o f G u ia n a dolphins from S epetiba Bay varied
widely, ra nging from —16.9%o to —12.8%o. T his finding m ay
indicate the existence o f distinct food sources for this population,
suggesting th a t som e individuals forage outside the b a y ra th e r th an
feeding exclusively w ithin Sepetiba Bay. D ias et al. [45] found
different distributio n p a tte rn s b etw een G u ia n a d o lphin “groups”
(one to 90 individuals) a n d “ aggregations” (m ore th a n 100
individuals) in Sepetiba Bay; m ost “ groups” w ere observed at
the entrance, w hile m ost “ aggregations” w ere reco rd ed in the
interior o f the b a y [45]. F u rth e r investigations focusing o n these
gro u p s/ag g reg atio n s will help to elucidate the existence o f distinct
fo rag in g /feed in g beh av io r in the G u ia n a d o lphin p o p u latio n from
Sepetiba Bay.
G u ia n a dolphins from lilia G ra n d e B ay h a d low er S 13C values
c o m p a red to specim ens from the o th er bays investigated, w ith
values close to those o f oceanic delphinids. It is im p o rta n t to
highlight th a t the species is typically a coastal species and, to date,
no sighting has b e en described in the oceanic env iro n m en t [37].
Bisi et al. [46] also verified th a t cephalopods a n d fish w ith different
feeding habits in lilia G ra n d e Bay w ere 13C -depleted. F u rth e r­
m ore, lilia G ra n d e Bay is a sem i-open system th a t is m ore heavily
influenced by the colder, m o re saline w ater from the m arine
c u rre n t flowing from the continental shelf th a n are G u a n a b a ra
a n d Sepetiba bays [47,48], O u r findings suggest th a t the low S13C
values in G u ia n a dolphins from lilia G ra n d e Bay w ere due to the
influence o f external w ater in this estuarine environm ent.
T h e four populations o f G u ia n a dolphins h a d sim ilar 8 ' N
values, indicating th a t they are feeding o n p re y from the sam e
trophic level. H ow ever, it is believed th a t th ere m ay b e differences
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Habitat Preferences o f Delphinids
C onclusions
killer w hales h a d sim ilar S 13C values to o th er nearsh o re species
(rough-toothed a n d G u ia n a dolphins), suggesting th a t these species
also forage in the region along the continental shelf, w ith sim ilar
h a b ita t preferences. T his is a relevant finding because studies have
re p o rte d the use o f oceanic habitats, in w aters o f greater th an
1,000 m , for false killer w hales [56,58] a n d have revealed a distinct
foraging p a tte rn th ro u g h o u t the species distribution [19,36,56].
H ow ever, the results o f this study highlight the lim ited know ledge
a b o u t th a t h a b ita t preferences o f this species.
T h e S13C values indicated th a t R isso’s a n d p an tro p ical spotted
dolphins in h ab it w aters along the continental shelf break. A sim ilar
result was observed for R isso’s dolphins in T ie rra del Fuego,
A rgentina [19], as well as those found along the northw est coast o f
A frica [30]. S pinner a n d F raser’s dolphins h a d the low est S13C
values, lending furth er support to the described use o f oceanic
h a b it [56]. T hese oceanic species also h a d the low est S15N values
a n d w ere found in groups four (Risso’s d o lphin a n d pan tro p ical
spotted dolphin) a n d five (spinner d o lphin a n d F raser’s dolphin),
identified from the cluster analysis. Studies have show n a positive
correlation betw een tro p h ic level a n d S15N values [31,32,61].
N evertheless, S 15N values o f the isotopic baseline can vary
considerably am o n g ecosystem s a n d regions [24,30,62]. T hereby,
o u r S 15N results m ay reflect oceanic species feeding o n low trophic
level p rey o r could b e due to the low S 15N values a t the base o f the
ocean food w eb. A n im p o rta n t source o f nitro g en in the o cea n ’s
photic zone is in the form o f n itrate, w hich typically features
h igher S 15N values o f approxim ately 6 %o [63,64], O n the o th er
han d , several studies have associated low S15N values in the b io ta
to the influence o f atm ospheric N 2 fixation by c yanobacteria in
oceanic w aters [65,66,67], w hich seems to be a m u ch greater
source o f nitro g en th a n assum ed in the p ast [65]. T h e low S 15N
values in oceanic d o lphin species p o in t to a substantial in p u t o f N 2
fixed by cyanobacteria ra th e r th a n n itrate as a p rim a ry source o f
n itrogen in foraging areas.
A m o n g the oceanic species, p a n tro p ical spotted a n d R isso’s
dolphins h a d the lowest S 15N values. S tom ach c o n te n t analyses
have show n th a t p a n tro p ical spotted dolphins feed m ainly on
m esopelagic fish o f the M y ctophidae family, as well as on
cephalopods from the families E n o ploteuthidae a n d O m m astre ­
ph id ae [13,68]. R isso’s dolphins feed alm ost exclusively on
cephalopods, prim arily from the families O ctopodidae, Loliginidae
a n d O m m astre p h id ae [69,70,71]. T hese studies show ed th a t these
two species h a d som e sim ilar p re y types, such as om m astrep h id
squids. In the p re sen t study, S13C a n d S15N values w ere very
sim ilar a m o n g p a n tro p ical spotted a n d R isso’s dolphins, suggesting
a large overlap in foraging a rea o r p rey consum ed.
T his study provides new inform ation on the tro p h ic ecology o f
10 delphinid species, including four populations o f G u ia n a
dolphins, in southeastern Brazil. E vidence from S 13C a n d S 15N
values indicated th a t th ere was segregation am o n g the delphinids
occurring along the coast o f R io de Ja n e iro State, w ith species
having distinctive foraging habitats a n d occupying different
ecological niches. F o r exam ple, ro u g h -to o th ed dolphins ap p ea r
to forage along the in n er shelf, w hereas bottlenose dolphins a n d
false killer whales use the co n tinental shelf. V alues o f 8 C suggest
th a t R isso’s a n d p a n tro p ical spotted dolphins forage along the
p latform break, while spinner a n d F raser’s dolphins used sim ilar
oceanic h a b ita t. B ottlenose dolphins a n d false killer whales
occupied the highest trophic position, while spinner a n d F raser’s
dolphins fed o n low er tro p h ic level prey. H ow ever, investigations
reg ard in g the S 15N values a t the base o f food w ebs in different
environm ents are necessary for a b e tte r u n d erstan d in g o f the
tro p h ic levels occupied b y delphinid species. Lastly, S13C values
show ed a clear separation b etw een the G u ia n a d o lphin p o p u la ­
tions from ad jacen t areas. It is im p o rta n t to em phasize th a t the
delphinid species studied occur in a region u n d e r high a n th ro p o ­
genic pressure, subject to pollution, intense vessel traffic, off
exploration, seismic prospecting, a n d intense com m ercial fishing,
a m o n g o th er factors. K now ledge a n d u n d erstan d in g o f the h a b ita t
preferences o f d elphinids in southeastern B razil is o f fundam ental
im p o rtan ce for identifying p oten tial threats to w hich these anim als
are subjected, as well as for supporting a p p ro p ria te conservation
actions.
A cknow ledgm ents
Muscle samples were collected under perm its 11495-1 and 11579-1, issued
by the Brazilian Ministry o f the E nvironm ent (IB A M A /M M A and
IC M B io/M M A , respectively). W e thank to A quatic M am m al and
Bioindicator L aboratory (M A Q U A /U ER J) team for invaluable assistance
in sampling, as well as in sample preparation for stable isotopes analysis.
W e also thank R R Carvalho for helping with m ap production.
A uthor C ontributions
Conceived and designed the experiments: TLB P R D JL B AFA O M KD.
Perform ed the experiments: TLB P R D G L LF. Analyzed the data: TLB
PR D JL B ALA O M . C ontributed reagents/m aterials/analysis tools: JLB
GL AFA O M K D . W rote the paper: TLB JLB OM .
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