1
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
More pieces for the puzzle: novel information on the genetic diversity
and population structure of Steno bredanensis (Artiodactyla: Delphinidae)
in Central America and the Caribbean Sea
Dalia C. Barragán-Barrera*1, 2, 3; https://orcid.org/0000-0003-4023-9908
Camilo A. Correa-Cárdenas3, 4; https://orcid.org/0000-0001-5009-6213
María Alejandra Duarte-Fajardo3, 5; https://orcid.org/0000-0002-6494-6941
Lissette Trejos Lasso6, 7; https://orcid.org/0000-0002-2495-0452
Betzi Pérez-Ortega6, 8, 9; https://orcid.org/0000-0001-5414-6329
Shakira G. Quiñones-Lebrón6; https://orcid.org/0000-0003-1822-4443
Antonio A. Mignucci-Giannoni10, 11; https://orcid.org/0000-0003-1443-4873
José Julio Casas7, 12, 13; https://orcid.org/0000-0001-9951-0542
Roberto Santamaria Valverde12; https://orcid.org/0000-0001-7371-8273
Nohelia Farías-Curtidor14; https://orcid.org/0000-0002-2617-8988
Susana Caballero3; https://orcid.org/0000-0002-9285-3873
1. Instituto Javeriano del Agua, Pontificia Universidad Javeriana, Carrera 7ª No. 40-62, Bogotá, Colombia; daliac.bar-
raganbarrera@gmail.com (*Correspondence)
2. R&E Ocean Community Conservation Foundation, Oakville, Canada; daliac.barraganbarrera@gmail.com
3. Laboratorio de Ecología Molecular de Vertebrados Acuáticos-LEMVA, Departamento de Ciencias Biológicas,
Universidad de los Andes, Carrera 1 No. 18A-10, Bogotá, Colombia; daliac.barraganbarrera@gmail.com, camilocc510@
gmail.com, aduarte108@gmail.com, sj.caballero26@uniandes.edu.co
4. Grupo de Investigación en Enfermedades Tropicales del Ejército (GINETEJ), Laboratorio de Referencia e Investigación,
Dirección de Sanidad, Ejército Nacional de Colombia, Bogotá, Colombia; camilocc510@gmail.com
5. Fundación Malpelo y otros Ecosistemas Marinos, Bogotá, Colombia; aduarte108@gmail.com
6. Fundación Panacetacea Panamá, Ciudad de Panamá, Panamá; ltrejos@miambiente.gob.pa, betziperez@yahoo.com,
shakiguani@gmail.com
7. Ministerio de Ambiente, Avenida Ascanio Villalaz, edificio 500, Ancón, Panamá; ltrejos@miambiente.gob.pa, jcasas@
miambiente.gob.pa
8. Biology Department and Redpath Museum – McGill University, Montreal, Canada; betziperez@yahoo.com
9. Instituto Smithsonian de Investigaciones Tropicales. Ciudad de Panamá, Panamá; betziperez@yahoo.com
10. Centro de Conservación de Manatíes del Caribe, Universidad Interamericana de Puerto Rico, 500 Carr. Dr. John Will
Harris, Bayamón, Puerto Rico 00957; mignucci@manatipr.org
11. Center for Conservation Medicine and Ecosystem Health, Ross University School of Veterinary Medicine, PO Box 334
Basseterre, St. Kitts West Indies; mignucci@manatipr.org
12. Facultad de Ciencias del Mar, Universidad Marítima Internacional de Panamá – UMIP, Ciudad de Panamá, Panamá;
jcasas@miambiente.gob.pa, santamariaroberto43@gmail.com
13. Estación Científica Coiba AIP, Ciudad de Panamá, Panamá; jcasas@miambiente.gob.pa
14. Fundación Macuáticos Colombia, Calle 27 Nº 79-167, Medellín, Colombia; nohefa@gmail.com
Received 09-VII-2022. Corrected 17-X-2022. Accepted 21-VIII-2023.
https://doi.org/10.15517/rev.biol.trop..v71iS4.57285
SUPPLEMENT • SMALL CETACEANS
2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
ABSTRACT
Introduction: The rough-toothed dolphin (Steno bredanensis) inhabits oceanic waters of tropical latitudes and
exhibits philopatry in some oceanic islands. However, the species has been observed in shallow coastal waters in
a few areas. Particularly in Central America, the rough-toothed dolphin has been reported by occasional records
and strandings. For instance, the first confirmed record of this species in the Panama’s Caribbean was on July 17,
2012, in a coastal region of the Chiriquí Lagoon during a bottlenose dolphin monitoring survey. Similarly, the first
rough-toothed dolphin mass stranding reported for the Pacific of Panama was on April 20, 2016, at the Ostional
Beach, where 60 dolphins stranded and ten died. These sightings and events offered a valuable opportunity to
obtain samples to conduct genetic studies, which are scarce in the region.
Objective: In this study, we present the first assessment of genetic diversity for rough-toothed dolphins based on
mitochondrial DNA Control Region (mtDNA-CR) in the Panamanian Pacific and the Wider Caribbean.
Methods: Samples were collected in Colombia (N=5), Panama (N-Caribbean=1, N-Pacific=9), and Puerto Rico
(N=3) from free-ranging and stranded individuals. DNA was extracted from each sample, and a mtDNA segment
of around 534 to 748 bp was amplified through the PCR reaction. The obtained sequences were compared with
rough-toothed dolphin haplotypes previously published in NCBI (N=70), from the Atlantic, Indian, and the
Pacific Oceans.
Results: Our findings showed significant population structure among ocean basins (strong differentiation with
ΦST data), and high genetic diversity within each phylogroup. Only the Atlantic Ocean showed high genetic dif-
ferentiation within the basin, detecting three phylogroups: the Caribbean, northern, and southern Atlantic.
Conclusions: These findings support previous genetic studies that indicate high levels of population structure
among ocean basins, although this species seems to be widely dispersed. However, samples from Panama and the
Caribbean appear to show connectivity between highly differentiated Atlantic and Pacific Oceans. Therefore, our
results highlight the need for more research to assess the rough-toothed dolphin genetic and population status in
Central America, as the piece of the puzzle needed to clarify its taxonomy and genetic differentiation worldwide.
This information is needed due to the rough-toothed dolphin IUCN categorization as “Least Concern” and its
classification into appendix II according to CITES. While individuals are potentially threatened by incidental
fishing, no management units are currently used to conserve this species despite its high genetic differentiation.
Key words: Delphinids; cetaceans; Control Region; mtDNA; Caribbean; Pacific Ocean; conservation.
RESUMEN
Más piezas del rompecabezas: información preliminar sobre la diversidad genética y estructura poblacional
de Steno bredanensis (Artiodactyla: Delphinidae) en Centroamérica y el Mar Caribe
Introducción: El delfín de dientes rugosos (Steno bredanensis) habita aguas oceánicas de latitudes tropicales y
muestra filopatría en algunas islas oceánicas. Sin embargo, la especie ha sido observada en algunas áreas costeras
de aguas poco profundas. Particularmente en Centroamérica, los delfines de dientes rugosos han sido reportados
por registros ocasionales y varamientos. Por ejemplo, el primer registro confirmado de la especie en el Caribe
Panameño ocurrió el 17 de julio de 2012 en una región costera de la Laguna de Chiriquí, durante un monitoreo
de delfín nariz de botella. De manera similar, el primer reporte de un varamiento masivo de delfines de dientes
rugosos en el Pacífico Panameño ocurrió el 20 de abril de 2016, en la Playa Ostional, donde 60 delfines vararon
y diez murieron. Estos avistamientos y eventos ofrecen una valiosa oportunidad para obtener muestras con el fin
de realizar estudios genéticos, los cuales son escasos en la región.
Objetivo: En este estudio, presentamos la primera evaluación de la diversidad genética de los delfines de dientes
rugosos basado en la Región Control de ADN mitocondrial (CR-ADNmt) en el Pacífico Panameño y la región
Caribe.
Métodos: Las muestras fueron colectadas en Colombia (N=5), Panamá (N-Caribe=1, N-Pacífico=9), y Puerto
Rico (N=3) de individuos vivos y varados. El ADN fue extraído para cada muestra, y un segmento de ADNmt
de aproximadamente 534 a 748 pb fue amplificado mediante la reacción en cadena de la polimerasa PCR. Las
secuencias obtenidas fueron comparadas con haplotipos de delfines de dientes rugosos de los Océanos Atlántico,
Índico y Pacífico, publicados previamente en NCBI (N=70).
Resultados: Nuestros resultados mostraron una estructura poblacional significativa entre las cuencas oceánicas
(una alta diferenciación con base en datos de ΦST), y una alta diversidad genética dentro de cada filogrupo. Solo
el Océano Atlántico mostró una alta diferenciación dentro de la cuenca, detectando tres filogrupos: el Caribe,
Atlántico norte y sur.
Conclusiones: Estos resultados soportan los estudios genéticos previos que indican altos niveles de estructura
poblacional entre las cuencas oceánicas, aunque esta especie parece estar ampliamente distribuida. Sin embargo,
las muestras de Panamá y el Caribe parecen mostrar conectividad entre las cuencas altamente diferenciadas del
Océano Atlántico y Pacífico. Por lo tanto, nuestros resultados destacan la necesidad de realizar más investigación
3
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
INTRODUCTION
The rough-toothed dolphin, Steno breda-
nensis, (G. Cuvier in Lesson, 1828) is distrib-
uted worldwide in tropical, sub-tropical, and
warm-temperate latitudes (Jefferson, 2018). In
general, the species has oceanic habits, but
shows some preference for volcanic islands
where deep waters are close to the coast, such
as the Canary Islands, French Polynesia, and
Hawaii (Kerem et al., 2016). Particularly in
these Indo-Pacific and Pacific islands, where
the species has been extensively studied, the
rough toothed-dolphins show some degree of
philopatry (Baird, 2016; Oremus et al., 2012). In
the Eastern Mediterranean, the rough-toothed
dolphin is reported as an oceanic species with a
seasonal migration pattern between neritic and
oceanic habitats (Kerem et al., 2016). Conse-
quently, the species may occupy both habitats,
despite the apparent tendency to be distributed
in oceanic areas. Indeed, in countries along the
Western Atlantic and the Caribbean including
Brazil, Colombia, Honduras, and recently in
Panama, rough toothed dolphins have been
reported mainly in neritic zones (Barragán-
Barrera et al., 2015; Farías-Curtidor & Ayala,
2015; Farías-Curtidor & Barragán-Barrera,
2017, Farías-Curtidor & Barragán-Barrera,
2019; Kuczaj & Yeater, 2017; Ott & Danilewicz,
1996; Santos et al., 2019).
It is clear the need to study the rough-
toothed dolphins worldwide, in order to under-
stand their distributional patterns as a first step
to assess adequately its conservation threats,
since marine mammal coastal populations are
more exposed to threats than the oceanic ones
(Avila et al., 2018). Central America deserves
special attention as a big gap of information
about rough-toothed dolphins, despite that the
entire region may potentially be occupied by
this species (Kiszka et al., 2019). For instance,
only in 2012 (July 17 at 9:50 a.m.), the rough-
toothed dolphin was reported and confirmed
genetically for the first time in the Caribbean of
Panama, when a group of about six adults was
observed jumping and traveling close to shore
within the Chiriquí Lagoon during a common
bottlenose dolphin (Tursiops truncatus) (Mon-
tagu, 1821) survey (Barragán-Barrera et al.,
2015). Similarly, in 2016, a rare mass-stranding
event of 60 rough-toothed dolphins, of which
ten died on the beach despite local efforts to
rescue them, was reported for the first time at
the Ostional Beach, on the Pacific coast of Pan-
ama (May-Collado et al., 2017). In general, the
few sightings in Central American Caribbean
have taken place in coastal areas (May-Collado
et al., 2017), and even some individuals appear
to show residency patterns like off the coast of
Utila in Honduras (Kuczaj & Yeater, 2017).
Definition of neritic and/or oceanic hab-
its of rough-toothed dolphins, as well their
population status, is needed to assess adequate
management plans. The main threat reported
for the species is bycatch in oceanic waters of
Brazil (Donato et al., 2019; Monteiro-Neto et
al., 2000). However, neritic individuals also
may be affected by contamination and fishery
interactions, particularly in the Atlantic coast
of the USA and in Brazil, where mass strand-
ings have been reported (Baptista et al., 2016;
para determinar el estado genético y poblacional de los delfines de dientes rugosos en Centroamérica, como
la pieza del rompecabezas que falta para esclarecer su taxonomía y diferenciación genética a nivel mundial.
Esta información es necesaria debido a que el delfín de dientes rugosos está categorizado ante la UICN como
“Preocupación Menor” y está clasificado en el apéndice II de CITES. Aunque los individuos pueden estar poten-
cialmente amenazados por captura incidental, no existen actualmente unidades de manejo para conservar esta
especie a pesar de su alta diferenciación genética.
Palabras clave: Delfínidos; cetáceos; Región Control; ADNmt; Caribe; Océano Pacífico; conservación.
Nomenclature: SMT1: Supplementary material Table 1; SMF1: Supplementary material Figure 1.
4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
Donato et al., 2019; Ewing et al., 2020; Lailson-
Brito et al., 2012; Lemos et al., 2013; Meirelles
& Barros, 2007; Struntz et al., 2004). In light
of this, genetic studies based on samples col-
lected opportunistically from stranding events
in areas where non-monitoring programs are
established, for example in Central America,
could be useful to provide an initial status of
rough-toothed dolphins’ population structure.
A recent work aimed to assess this was con-
ducted using samples collected worldwide, and
showed clear genetic differentiation among
ocean basins based on both nuclear and mito-
chondrial markers (Albertson et al., 2022).
Particularly, a strong distinction was detected
between Atlantic and Pacific oceans, which
suggested a potential incipient speciation to at
least subspecies level (Albertson et al., 2022; da
Silva et al., 2015). However, the authors rec-
ognized the need for including more samples
that represent a larger area in the Pacific and
especially in the Indian Ocean to confirm this
assumption (Albertson et al., 2022). Addition-
ally, this work only included six samples from
the Caribbean and one from Brazil, which
could imply no divergence detection between
these two areas, despite a strong differentiation
previously described based on mitochondrial
DNA (mtDNA) data (da Silva et al., 2015).
Following the Albertson et al. (2022) rec-
ommendation, herein we provide new insights
into genetic diversity and population structure
of rough-toothed dolphins based on mtDNA
Control Region (mtDNA-CR) using new
samples collected from the Central American
Pacific coast, specifically from Panama, as well
as new samples from the Caribbean. Addition-
ally, this study aimed to corroborate or not the
population differentiation reported by Alb-
ertson et al. (2022), emphasizing on dolphins
from Central America, which potentially may
provide the resolution needed to clarify the
potential subspeciation process among ocean
basins. This study provides relevant baseline
data about the genetic status of the rough-
toothed dolphin in the region, as a first step
to understand its population status, and thus
propose future adequate management plans for
this enigmatic species in Central America.
METHODS
Study area: The study area in Central
America, where rough-toothed dolphin sam-
ples were collected, encompasses the Azuero
Peninsula on the Pacific coast of Panama and
the Chiriquí Lagoon on the Caribbean coast of
Panama (Fig. 1). The Azuero Peninsula, where
the Ostional beach is situated, is located at
the central portion of Panama, whose coast is
dominated by small portions of mangrove and
beach vegetation (Friedman & Grandmont,
2019). In the Ostional beach, a rare event of
a mass stranding was reported on April 19th,
2016 (Fig. 2A). The Chiriquí Lagoon, where
one sample of one individual from a group of
six free-ranging adult dolphins was collected
on July 17th, 2012 (Fig. 2B), is a semi-enclosed
lagoon located in the Bocas del Toro Prov-
ince at Western Caribbean of Panama, an area
highly influenced by precipitation (Guzmán &
Guevara, 1998).
Additionally, samples from the Caribbean
basin, coming from Colombia and Puerto Rico,
were included in this study (Fig. 1). Samples
from Colombia were collected from two loca-
tions: 1) in waters of Dibulla, located in La
Guajira Peninsula on the northern portion of
Colombia, where four samples of free-ranging
adult individuals from a group of around 15
dolphins were collected on May 19th, 2015 (Fig.
2C) (Farías-Curtidor & Ayala, 2015; Farías-
Curtidor & Barragán-Barrera, 2017, Farías-
Curtidor & Barragán-Barrera, 2019), and 2) in
Gaira, located in the Magdalena department,
where one sample from a stranded individual
was collected. These two areas are in the Eastern
Colombian Caribbean and are influenced by
upwelling events (Arévalo-Martínez & Franco-
Herrera, 2008; Fajardo, 1979; Gutiérrez et al.,
2015), so cetaceans have been usually reported
there (e.g., Barragán-Barrera, do Amaral, et
al., 2019, Barragán-Barrera, Luna-Acosta, et
al., 2019; Farías-Curtidor et al., 2017; Fraija et
al., 2009; Pardo & Palacios, 2006). Regarding
5
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
Puerto Rico, it is a Caribbean archipelago that is
part of the Greater Antilles (Fig. 1), and due its
localization between the Caribbean Sea and the
Atlantic Ocean, holds a high marine mammals’
diversity in the Wider Caribbean (Mignucci-
Giannoni, 1989).
Sample collection: Following Barragán-
Barrera et al. (2017), rough-toothed dolphins
tissue samples in the Chiriquí Lagoon (N =
1) and Dibulla-La Guajira Peninsula (N = 4)
were collected from free-ranging animals using
the PAXARMS system (Krützen et al., 2002).
Samples from the Azuero Peninsula (N = 9),
Gaira-Magdalena (N = 1), and Puerto Rico
(N = 3) were collected from stranded animals.
Samples were preserved in 70 % ethanol and at
−20 °C (Amos & Hoelzel, 1991) for subsequent
laboratory analysis.
DNA extraction, PCR, sequencing, and
sexing: DNA was extracted from tissue samples
using the DNeasy kit (QIAGEN) following
the manufacturer’s instructions. A portion of
mtDNA-CR of around 534 to 748 bp was ampli-
fied by the polymerase chain reaction (PCR),
using the primers Dlp5G (5’- GGAGTACTAT-
GTCCTGTAACCA-3’) or Dlp8G (5’-CCATC-
GWAGATGTCTTATTTAAGRARTTCTA-3’)
and Dlp1.5 (5’-TCACCCAAAGCTGRARTTC-
TA-3’), following the protocol described in
Baker et al. (1998). PCR products were puri-
fied following a Polietilenglicol protocol (PEG
20 %), and DNA was sequenced using the
Sanger sequencing method (Sanger & Coulson,
1975). Following Gilson et al. (1998), the sex
of each individual sampled was identified using
the male-specific SRY gene and ZFY/ZFX genes
of males and females.
Data analysis: The software Geneious v.
4.8.5 (Drummond et al., 2009) was used to
edit manually all obtained sequences. These
haplotypes were compared to 70 GenBank
Fig. 1. Location of the samples of Rough-toothed dolphins (Steno bredanensis) in the Caribbean coast of Colombia (Gaira-
Magdalena and Dibulla-La Guajira), Panama (Chiriquí Lagoon), and Puerto Rico (San Juan), as well as the Pacific coast of
Panama (Ostional Beach).
6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
published sequences from Brazil, China, East-
ern Pacific coast of Central and North Amer-
ica, India, Indonesia, Japan, Mediterranean
Sea, New Zealand, Puerto Rico, Samoa Island,
Society Islands, South Africa, South Korea,
Spain, Taiwan, Thailand, and USA (Western
Atlantic coast and Hawaii) (SMT1). The R
script RemoveRedundantTaxa was used to
characterize the haplotypes. All sequences were
aligned obtaining an alignment of 383 bp. In
order to understand the relationships among all
sequences, the CIPRES Science Gateway V. 3.3
software was used (Miller et al., 2010) to build
a maximum likelihood phylogenetic tree using
the evolutionary model of Generalized-Time-
Reversible γ + Invariant (GTR γ + I) substitu-
tion and 1 000 bootstrap replicates.
Because no information about haplotype
frequencies from Indonesia and Thailand was
available, these were not included in the sub-
sequent analyses. To determine the number of
phylogrups for all haplotypes obtained world-
wide, the software Arlequin v. 3.5 (Excoffier &
Lischer, 2010) was used to assess the best FCT
value by running several possible combina-
tions of geographic areas (two to eight groups)
based on ocean basin and/or previous studies
(Albertson et al., 2017, Albertson et al., 2022; da
Silva et al., 2015; Oremus et al., 2012). The same
software was used to assess the fixation indices
(FIS and FIT). Once the number of phylogrups
was identified, the PopART software (Clement
et al., 2000) was used with the TCS method to
build a haplotype network to visualize to what
population the haplotypes used in this study
Fig. 2. Sightings of rough-toothed dolphins (Steno bredanensis) in which tissue samples for this study were collected. A)
A rare mass-stranding occurred in April 2016 at Ostional Beach in the Azuero Peninsula, Pacific coast of Panama; photo
courtesy Lissette Trejos. B) The first confirmed sighting of rough-toothed dolphins in the Caribbean coast of Panama,
at Chiriquí Lagoon, reported in July 2012; photo by Mónica Acosta. C) A group recorded in May 2015 consisting of 14
adults and one calf in La Guajira Peninsula, Caribbean coast of Colombia; photo by Nohelia Farías-Curtidor. D) A species
description illustrated by Emmanuel Laverde © www.arteyconservacion.com
7
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
belonged and their frequency. To assess the
genetic subdivision among phylogrups identi-
fied, the software Arlequin v. 3.5. (Excoffier &
Lischer, 2010) was used to conduct an analy-
sis of molecular variance (AMOVA) (Excof-
fier et al., 1992), so the pairwise comparison
of population differentiation indices FST and
ΦST between all phylogrups were assessed. The
same software was used to assess diversity indi-
ces as nucleotide (π) and haplotype diversity
(h), as well as the neutrality defining Tajima’s D
index for each phylogrup.
RESULTS
A total of 18 samples were collected, and
17 were successfully amplified (94,44 %) except
one from the Ostional Beach. In total, the 17
sequences obtained represent 13 new haplo-
types ranging between 534 and 748 bp. For
Panama, one haplotype was identified in the
Caribbean while five were identified for the
Pacific. Among these five haplotypes, sequenc-
es SbEPP1 (748 bp) and SbEPP1.1 (691 bp),
which were identical, were reported as differ-
ent haplotypes due the first one was longer,
and we do not have any evidence of polymor-
phism present in the non-amplified region.
For Colombia (Caribbean basin), three hap-
lotypes were identified in Dibulla-La Guajira
and one in Gaira-Magdalena. For Puerto Rico,
three haplotypes were identified (SMT1). All
these new haplotypes were deposited and are
available in GenBank (https://www.ncbi.nlm.
nih.gov/genbank/) under accession numbers
OR436925-OR436936.
Comparison among these new haplo-
types with previously 70 GenBank published
sequences from Atlantic, Indian, and Pacific
Oceans, showed strong differentiation among
ocean basins. Despite of this, four Caribbean
haplotypes, including the ones from Colom-
bia (Dibulla-La Guajira), Panama, and Puerto
Rico (SbGCC2, SbGCC3, SbPC1, and SBPRC3)
nested within the Pacific Ocean clade (the max-
imum likelihood phylogenetic tree illustrates
in green color the Caribbean haplotypes; Fig.
3). Consequently, reciprocal monophyly was
not detected between the Atlantic and Pacific
Oceans, and this last one appears to be a para-
phyletic group (boostrap support > 95 %; Fig.
3). The remaining four Caribbean haplotypes
(SbMCC1, SbPRC1, SBPRC2, and SbGCC1)
exhibited connectivity to the entire Atlantic
Ocean. The SbMCC1 haplotype from Gaira-
Magdalena (Colombian Caribbean) nested with
haplotypes from the Atlantic coast of the USA,
as well as with the haplotypes SbPRC1 and
SBPRC2 from Puerto Rico. The Colombian
haplotype SbGCC1 from Dibulla-La Guajira
Table 1
Estimates of mitochondrial differentiation among the five phylogrups identified for rough-toothed dolphins (Steno
bredanensis) in the Atlantic, Indian, and Pacific Oceans. FST value is shown above diagonal and ΦST below diagonal. P-value
is indicated under each value in parentheses (significant values are considered as P < 0.05). Haplotype (h) and nucleotide
diversity (π) are shown on the diagonal for each phylogrup.
FST
ΦST
Brazil-South
Atlantic Ocean Caribbean North
Atlantic Ocean Indian Ocean Pacific Ocean
Brazil- South Atlantic
Ocean
h = 0.628
π = 0.121
0.233
(P = 0.009)
0.268
(P < 0.001)
0.262
(P < 0.001)
0.189
(P < 0.001)
Caribbean 0.644
(P < 0.001)
h = 0.978
π = 0.109
0.100
(P < 0.001)
0.046
(P < 0.001)
0.043
(P < 0.001)
North Atlantic Ocean 0.746
(P < 0.001)
0.904
(P < 0.001)
h = 0.840
π = 0.060
0.124
(P = 0.009)
0.104
(P = 0.009)
Indian Ocean 0.562
(P < 0.001)
0.768
(P < 0.001)
0.340
(P < 0.001)
h = 0.929
π = 0.167
0.057
(P = 0.027)
Pacific Ocean 0.490
(P < 0.001)
0.780
(P < 0.001)
0.570
(P < 0.001)
0.269
(P < 0.001)
h = 0.942
π = 0.083
8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
showed a higher connectivity to the Atlantic
basin since it nested with haplotypes from the
Atlantic coast of the USA and Canary Islands
(Spain) (Fig. 3). Despite this, high population
structure was detected between the Caribbean
and the North Atlantic phylogrups. Regard-
ing the haplotypes from the Ostional Beach in
the Panamanian Pacific (SbEPP1, SbEPP1.1,
SbEPP2, SbEPP3, and SbEPP4), these exhib-
ited connectivity with haplotypes from the
entire Pacific basin, since they nested with
haplotypes from Central Pacific (mainly Hawaii
and Society Island), Indo-Pacific (India), East-
ern Pacific (Pacific coast of America), and
Thailand (Fig. 3).
In the analysis of population structure, we
identified five phylogrups based on the best FCT
value (FCT = 0.47, P = 0.005): 1) Brazil-South
Atlantic Ocean, 2) Caribbean, 3) North Atlantic
Ocean, 4) Indian Ocean, and 5) Pacific Ocean.
The Caribbean phylogrup was formed by hap-
lotypes from the Caribbean coast of Colombia,
Panama, and Puerto Rico. The North Atlantic
Ocean phylogrup consisted of haplotypes from
the Eastern Mediterranean Sea, Canary Islands
(Spain), and the Atlantic coast of the USA. The
Indian Ocean phylogrup was formed by haplo-
types from India and South Africa. The Pacific
Ocean phylogrup included haplotypes from the
Central Pacific, China, Eastern Pacific, Hawaii,
Japan, Pacific waters of Panama, Samoa Islands,
Society Island, South Korea, Taiwan, and West-
ern Pacific. Pairwise comparisons showed
strong population structure among phylogrups,
Fig. 3. Phylogenetic reconstruction by maximum likelihood of rough-toothed dolphins (Steno bredanensis) Control Region
(752 bp) haplotypes in the Atlantic (purple and pink clades), Indian (red), and Pacific (blue) Oceans. Caribbean clades are
colored green. Phylogeny in a circular polar form shows bootstrap support in branches with percentages of 100 % or > 50 %.
Red letters represent the samples used for this study. Outgroup: Common bottlenose dolphin, Tursiops truncatus.
9
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
mainly at nucleotide level (ΦST) (Table 1). The
haplotype network (Fig. 4) showed the relation-
ship among haplotypes and their frequencies
from the five phylogrups.
The genetic diversity indexes showed high
haplotype and nucleotide diversity for each
phylogrup, with the highest haplotype diversity
in the Caribbean, followed by the Pacific Ocean
and the Indian Ocean. Brazil-South Atlantic
Ocean exhibited the lowest haplotype diversity
(Table 1). Regarding Tajima’s D index, it was
significant only for the Brazil-South Atlantic
Ocean phylogrup and showed a negative value
(Tajima’s D = -1.792, P = 0.013). In general, the
fixation indices for all phylogrups showed a
significant value only for the endogamy index
(FIS = 0.501, P < 0.001).
DISCUSSION
This is the first study on the genetic
population structure of rough-toothed dol-
phins using samples from Central America
(specifically from Panama) based on mtDNA-
CR data. Although we included individuals
from new geographic regions that had not been
sampled before (Panama and the Caribbean),
our data supports strong population structure
reported previously for the species among the
Atlantic, Indian, and Pacific Oceans (Albertson
et al., 2022; da Silva et al., 2015), and pro-
vide new insights about genetic differentiation
within the Atlantic basin (da Silva et al., 2015;
Donato et al., 2019). In general, our findings
highlight that individuals in Central America
may contain crucial genetic information to
elucidate population status of rough-toothed
dolphins in both Atlantic and Pacific Oceans,
where a process of incipient subspeciation has
been suggested (Albertson et al., 2022).
Genetic structure of Panamanian and
Caribbean dolphins in the Atlantic Ocean
Our findings suggest the Atlantic Ocean
is represented by three phylogrups: one in
the Caribbean, a second one in the North
Fig. 4. Haplotype network reconstruction for rough-toothed dolphins (Steno bredanensis) in the Caribbean, North Atlantic
Ocean, South Atlantic Ocean (Brazil), Indian Ocean, and Pacific Ocean, under parsimony criteria with the TCS algorithm
(N = 83, 383 bp). The circle’s size indicates the frequency of each haplotype. Black dot indicates the hypothetical ancestral
haplotype, and the perpendicular lines between the haplotypes refer to the number of nucleotide substitutions between them.
New haplotypes reported in this study are indicated with a red asterisk (*).
10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
Atlantic Ocean, and a third one in Brazil-
South Atlantic Ocean. Although two samples
(haplotype SbGCC1) from Dibulla-La Gua-
jira (Colombian Caribbean) nested with hap-
lotypes from the Atlantic coast of the USA and
Canary Islands (Spain), as well the Chiriquí
Lagoon sample (SbPC1, Panamanian Carib-
bean) nested with haplotypes from the Atlantic
coast of the USA (Fig. 3), a high population
structure exists between the Caribbean and
North Atlantic areas (Table 1). These findings
may be explained by the oligotrophic condi-
tion of Caribbean waters (Aguirre, 2014; Cor-
redor, 1979; Müller-Karger & Aparicio, 1994),
which promote high dolphin dispersion toward
productive Caribbean areas located mainly in
coastal areas (Barragán-Barrera, do Amaral, et
al., 2019). Consequently, despite oceanic habits
of species such as pantropical spotted dolphins
(Stenella attenuata) (Gray, 1846) and rough-
toothed dolphins, individuals have been regis-
tered in coastal areas along the Caribbean Sea
(Barragán-Barrera et al., 2015, Barragán-Bar-
rera, do Amaral, et al., 2019; Farías-Curtidor &
Ayala, 2015; Farías-Curtidor & Barragán-Bar-
rera, 2017, Farías-Curtidor & Barragán-Barre-
ra, 2019; Kuczaj & Yeater, 2017). For instance,
rough-toothed dolphins in Dibulla-La Guajira
have been observed in waters between 2 to 6.8
nautical miles from shore (Farías-Curtidor &
Ayala, 2015; Farías-Curtidor & Barragán-Bar-
rera, 2017, Farías-Curtidor & Barragán-Barre-
ra, 2019). Additionally, this species has been
reported as philopatric in coastal Caribbean
waters of Honduras (Kuczaj & Yeater, 2017).
These philopatric habits towards coastal areas
in Central America, likely because of lack of
resources in oceanic waters, may result in the
genetic differentiation observed here. However,
the high haplotype and nucleotide diversity also
suggests a high connectivity among individuals
within the Caribbean phylogrup. Therefore,
more research focused on distribution, habitat
use, local genetic patterns, and satellite tagging
is needed to confirm if rough-toothed dolphins
exhibit philopatric habits along specific Cen-
tral American Caribbean areas, or if dolphins
migrate between coastal and oceanic areas as
has been reported in the Mediterranean Sea
(Kerem et al., 2016).
The genetic differentiation observed
between rough-toothed dolphins from the
Caribbean and North Atlantic Ocean with
Brazil-South Atlantic Ocean had been previ-
ously described (Donato et al., 2019; Silva et
al., 2015), and agrees with other genetic studies
with delphinids such as the Atlantic spotted
dolphin Stenella frontalis (Cuvier, 1829) (do
Amaral et al., 2021), bottlenose dolphin (Fruet
et al., 2014), clymene dolphin Stenella clymene
(Gray, 1850) (Nara et al., 2017), and common
dolphin (Amaral et al., 2012), which reported
a similar isolation pattern. Oceanographical
features like the Amazon River mouth and the
North Brazilian Current appear to act as a bar-
rier that is segregating fauna from the north-
ern and southern Brazil (Costa et al., 2017).
Consequently, and due the isolation pattern
for delphinid species in southern Brazil, some
populations may be at risk (Fruet et al., 2014).
Particularly rough-toothed dolphins from Bra-
zil are threatened due to bycatch (Donato et al.,
2019; Monteiro-Neto et al., 2000), which may
imply a reduction of this population. Indeed,
the significant and negative D’Tajima value
found for this phylogrup suggests it is in expan-
sion after a historical bottleneck (Weber et al.,
2004). The population reduction resulted in
unique haplotypes emerging, so the expansion
observed here. Therefore, although we don’t
have information about the causes of historical
bottleneck, our findings support the da Silva
et al. (2015) recommendation in considering
the Brazil-South Atlantic Ocean phylogrup as a
distinct management unit due to the restricted
gene flow.
Genetic diversity of Panamanian dolphins
in the Pacific Ocean
New samples from the Pacific coast of Pan-
ama exhibited a genetic connectivity across the
Pacific Ocean. These findings are not in agree-
ment with the Albertson et al. (2022) previous
study, in which they reported population struc-
ture between the Central, Eastern, and Western
11
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
Pacific. Particularly in Central Pacific, where
oceanic islands are present including Hawaii,
Samoa, and Society Islands, rough-toothed dol-
phins show genetic structure and high philopa-
try, with restricted movements even between
closer islands (Albertson et al., 2017, Albert-
son et al., 2022; Baird, 2016; Oremus et al.,
2012). However, this kind of residency pattern
has not been reported in the Pacific basin
of Central America. The few rough-toothed
dolphin records in this region have been done
in oceanic waters (May-Collado et al., 2017).
Consequently, it is possible this species reflects
oceanic habits, and conducts long migrations
along the Pacific Ocean (Learmonth et al.,
2007), as is reflected by several shared haplo-
types among individuals, as well as by their
high haplotype diversity.
Long and multiple migrations patterns
across Pacific islands have been reported in
green turtle, Chelonia mydas (Linnaeus, 1758)
(e.g., Dutton et al., 2014; Jensen et al., 2016),
which are able to travel distances larger than 2
000 km influenced mainly by sea currents (Read
et al., 2014). Additionally, oceanographic events
like El Niño Southern Oscillation (ENSO), may
change the ocean current direction in relation
to the warm (North-Equatorial Current) and
cold currents as Humboldt Current (Rich-
mond, 1990). As a result, temporary migration
routes have been reported for many species,
like fishes (Victor et al., 2004), green turtles
(Seminoff et al., 2008), and marine mammals
(Learmonth et al., 2007), which allows genetic
connectivity along the Pacific Ocean.
One rough-toothed dolphin haplotype
from Panama (SbEPP4) was nested with two
haplotypes from India and Thailand. Despite
this, significant population structure was
detected between Indian and Pacific Oceans
although FST and ΦST values were lower (Table
1). Similarly, pairwise comparisons between the
Pacific and Caribbean basins showed lower FST
and ΦST values (Table 1). These findings may
be the result of some shared ancestral haplo-
types between these three oceans basins (Fig.
3; SMT1), which may imply potential highly
conserved haplotypes or genetic connectivity.
Indeed, Albertson et al. (2022) found few shared
haplotypes between the Atlantic and Pacific
Oceans, as well as did not detect population
structure between the Indian and Pacific Ocean
based on nuclear marker data. Likely, individu-
als from Central America may be maintaining
genetic connectivity among the three ocean
basins, but until no more samples will be
obtained, or satellite tagging research is con-
ducted, this assumption can not be tested.
Conservation and research implications
for dolphins in Central America
Although this is the first genetic assess-
ment of rough-toothed dolphins in Central
America, this study highlights the need for
conducting monitoring and sample collection
as well as more genetic assessments along the
region. Particularly individuals from Central
America are very useful to understand wheth-
er genetic connectivity between Atlantic and
Pacific Oceans exist or are ancestral. Further-
more, the role of Panama Isthmus closure in
the divergence of these phylogrups has not been
completely understood (Albertson et al., 2022).
Despite this, a potential subspeciation has been
reported between these two oceans basin (Alb-
ertson et al., 2022), and our findings based on
new Central America and Caribbean samples
support the population structure despite their
grouping with Pacific haplotypes.
The high and significant endogamy index
value detected here was intriguing since it
suggests the species has a low intrinsic genet-
ic diversity due to considerable inbreeding.
(Weber et al., 2004). Likely, variable sites within
the species are not significant in relation to
DNA analyzed here, despite mtDNA-CR having
a high mutational rate because it is not under
natural selection. Consequently, if the rough-
toothed dolphin is an endogamic species, its
status in the IUCN Red List as “Least Concern”
(Kiszka et al., 2019) should be changed to some
threatened level. However, our findings must
be considered with caution, as we only provide
information from a short portion of the mater-
nal lineage. Analyzing bi-parental genes, and
12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
specifically microsatellite data, are needed to
confirm this endogamy hypothesis. However,
previous research with rough-toothed dolphins
from French Polynesia using 14 microsatel-
lite loci did not detect endogamy (Oremus et
al., 2012). Consequently, samples from Centro
America could be useful to assess if endogamy
exists for this species.
Understanding the population or sub-spe-
ciation status of rough-toothed dolphins will be
essential for their conservation, and sample col-
lection in Central America is critical to achiev-
ing this goal. The Brazil-South Atlantic Ocean
phylogrup is an example of effectiveness of
large sampling to assess its conservation status,
since the increasing number of samples collect-
ed has allowed the genetic isolation detection
(da Silva et al., 2015; Donato et al., 2019).
The Central American rough-toothed dol-
phins, which are distributed in both Atlantic
and Pacific Oceans, may be exposed to differ-
ent threats, but no information about risks has
been obtained yet in this region. The closest
risk case for this species has been reported in
the Colombian Caribbean, where few isolated
bycatch cases were registered (Avila et al., 2018;
Avila & Giraldo, 2022). However, both Carib-
bean and Pacific waters along the Central
American region, mainly in Costa Rica, pres-
ent high bycatch risk for oceanic delphinids as
the pantropical spotted dolphin (Pino, 2021).
Considering this, rough-toothed dolphins may
be at risk in Central America, but this informa-
tion is virtually unknown. We hope this study
provides the baseline data needed to assess the
rough-toothed dolphin genetic and population
status in Central America, which will be essen-
tial for its management in the region. Herein,
we invite to Marine Mammalogists working in
Central America from Belize, Costa Rica, El
Salvador, Honduras, Guatemala, and Nicara-
gua, to create transnational conservation efforts
to increase sampling of rough-toothed dolphins
in both the Eastern Pacific and Caribbean Sea
in order to clarify the intraspecific genetic
dynamics of this species. Furthermore, Panama
must promote continuous genetic surveillance
of its populations.
Ethical statement: the authors declare that
they all agree with this publication and made
significant contributions; that there is no con-
flict of interest of any kind; and that we fol-
lowed all pertinent ethical and legal procedures
and requirements. All financial sources are fully
and clearly stated in the acknowledgments sec-
tion. A signed document has been filed in the
journal archives.
See supplementary material
a10v71s4-MS1
ACKNOWLEDGMENTS
This work is dedicated to the memory of
Christian Harris and Arnulfo Record, whose
support in the fieldwork as excellent captains
and human beings will be always acknowl-
edged. We thank Roger Ayala, Tomás Ayala,
and fishermen for their support on the small-
scale surveys out of La Guajira. We also thank
the Smithsonian Tropical Research Institute
(STRI) Marine Biological Station staff in
Bocas del Toro, and Panacetacea team for their
logistical support. Special thanks to Mónica
Acosta for her support during fieldwork in
Bocas del Toro. We specially thank MiAmbi-
ente, the National Aeronaval Service of Panama
(SENAN), and the International Maritime Uni-
versity of Panama (UMIP) for their logistic
support. Special thanks to the community of
the Ostional Beach in Tonosí for their rapid
response and help in the rescue labors. We
want to thank Ester Quintana-Rizzo and Laura
May-Collado for leading this special issue as
scientific editors. We thank the anonymous
reviewers whose comments improved the final
version of this manuscript. Colombian samples
were collected under Resolution 1177 of Octo-
ber 09, 2014 by which it is defined the General
Permit for Specimen Collection of Wildlife Bio-
diversity Non-Commercial Purposes of Scien-
tific Research. This permit was provided by the
National Authority for Environmental Licenses
13
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
(ANLA) to Universidad de Los Andes. Panama-
nian samples were collected under permission
from the Autoridad Nacional del Ambiente–
Panamá (ANAM, now Ministerio de Ambi-
ente; permit SC/A-11-12) and the Ministry of
Environment (MiAmbiente) of the Republic
of Panama, who granted a scientific permit
(SE/AO-1-16) to Fundación Panacetacea Pan-
amá. This study was supported by the Sciences
Faculty of Universidad de Los Andes through
the Research Grant “Proyecto Semilla” in the
2012-1 Call for Funding of Research Category:
Master and Doctoral students, project “Genetic
structure and diversity of bottlenose dolphins
Tursiops truncatus (Montagu, 1821) (Cetacea:
Delphinidae) in Bocas del Toro, Caribbean
Coast of Panama” (D. Barragán, 2012); the Ruf-
ford Foundation that provided a Rufford Small
Grant (D. Barragán, 2012), and the Society for
Marine Mammalogy that provided a Small
Grant in Aid of Research (D. Barragán, 2014).
The Vicerrectoría de Investigaciones from Pon-
tificia Universidad Javeriana is acknowledged
by providing a Postdoctoral Grant (Call 2021-
2) to D. Barragán (2022), who also thank the
Instituto Javeriano del Agua for its support
during this stay. The funders had no role in the
study design, data collection, analysis, decision
to publish, or preparation of the manuscript.
REFERENCES
Aguirre, R. (2014). Spectral reflectance analysis of the
Caribbean Sea. Geofísica Internacional, 53, 385–398.
https://doi.org/10.1016/S0016-7169(14)70073-X
Albertson, G. R., Baird, R. W., Oremus, M., Poole, M. M.,
Martien, K. K., & Baker, C. S. (2017). Staying close
to home? Genetic differentiation of rough-toothed
dolphins near oceanic islands in the central Pacific
Ocean. Conservation Genetics, 18, 33–51. https://doi.
org/10.1007/s10592-016-0880-z
Albertson, G. R., Alexander, A., Archer, F. I., Caballero, S,
Martien, K. K., Hemery, L. G., Baird, R. W., Oremus,
M., Poole, M. M., Duffield, D. A., Brownell Jr., R. L.,
Kerem, D., Mignucci-Giannoni, A. A., & Baker, C. S.
(2022). Worldwide phylogeography of rough-toothed
dolphins (Steno bredanensis) provides evidence for
subspecies delimitation. Marine Mammal Science, 38,
1371–1397. https://doi.org/10.1111/mms.12933
Amaral, A. R., Beheregaray, L. B., Bilgmann, K., Freitas,
L., Robertson, K. M., Sequeira, M., Stockin, K. A.,
Coelho, M. M., & Möller, L. M. (2012). Influences
of past climatic changes on historical population
structure and demography of a cosmopolitan mari-
ne predator, the common dolphin (genus Delphi-
nus). Molecular Ecology, 21, 4854–4871. https://doi.
org/10.1111/j.1365-294X.2012.05728.x
Amos, W., & Hoelzel, A. R. (1991). Long-term preservation
of whale skin for DNA analysis. Report of the Interna-
tional Whaling Commission, Special Issue, 13, 99–104.
Arévalo-Martínez, D. L., & Franco-Herrera, A. (2008).
Características oceanográficas de la surgencia frente
a la Ensenada de Gaira, Departamento de Magdalena,
época seca menor de 2006. Boletín de Investigacio-
nes Marinas y Costeras, 37, 131–162. https://doi.
org/10.25268/bimc.invemar.2008.37.2.195
Avila, I. C., Kaschner, K., & Dormann, C. F. (2018). Current
global risks to marine mammals: Taking stock of the
threats. Biological Conservation, 221, 44–58. https://
doi.org/10.1016/j.biocon.2018.02.021
Avila, I. C., & Giraldo, A. (2022). Áreas en riesgo para los
mamíferos marinos en Colombia. Revista de Biolo-
gía Tropical, 70, 96–113. https://doi.org/10.15517/rev.
biol. trop..v70i1.48553
Baker, C. S., Medrano-González, L., Calambokidis, J.,
Perry, A., PichlerI, F., Rosenbaum, H., Straley, J. M.,
Urbán-Ramírez, J., Yamaguchi, M., & von Ziegesar,
O. (1998). Population structure of nuclear and mito-
chondrial DNA variation among humpback whales
in the North Pacific. Molecular Ecology, 7, 695–707.
https://doi.org/10.1046/j.1365-294x.1998.00384.x
Baird, R. W. (2016). The Lives of Hawai’i’s Dolphins and
Whales. University of Hawai’i Press.
Baptista, G., Kehrig, H. A., Di Beneditto, A. P. M., Hauser-
Davis, R. A., Almeida, M. G., Rezende, C. E., Siciliano,
S., de Moura, J. F., & Moreira, I. (2016). Mercury, sele-
nium and stable isotopes in four small cetaceans from
the Southeastern Brazilian coast: Influence of feeding
strategy. Environmental Pollution, 218, 1298–1307.
https://doi.org/10.1016/j.envpol.2016.08.088
Barragán-Barrera, D. C., do Amaral, K. B., Chávez-Carre-
ño, P. A., Farías-Curtidor, N., Lancheros-Neva, R.,
Botero-Acosta, N., Bueno, P., Moreno, I. B., Bolaños-
Jiménez, J., Bouveret, L., Castelblanco-Martínez, D.
N., Luksenburg, J. A., Mellinger, J., Mesa-Gutiérrez,
R., de Montgolfier, B., Ramos, E. A., Ridoux, V., &
Palacios, D. M. (2019). Ecological niche modeling of
three species of Stenella dolphins in the Caribbean
Basin, with application to the Seaflower Biosphere
Reserve. Frontiers in Marine Science, 6, 1–17. https://
doi.org/10.3389/fmars.2019.00010
Barragán-Barrera, D. C., Luna-Acosta, A., May-Collado, L.
J., Polo-Silva, C. J., Riet-Sapriza, F. G., Bustamante, P.,
Hernández-Ávila, M. P., Vélez, N., Farías-Curtidor,
14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
N., & Caballero, S. (2019). Foraging habits and levels
of mercury in a resident population of bottleno-
se dolphins (Tursiops truncatus) in Bocas del Toro
Archipelago, Caribbean Sea, Panama. Marine Pollu-
tion Bulletin, 145, 343–356. https://doi.org/10.1016/j.
marpolbul.2019.04.076
Barragán-Barrera, D. C., May-Collado, L. J., Tezanos-Pinto,
G., Islas-Villanueva, V., Correa-Cárdenas, C. A., &
Caballero, S. (2017). High genetic structure and low
mitochondrial diversity in bottlenose dolphins of the
Archipelago of Bocas del Toro, Panama: A popula-
tion at risk? PLoS ONE, 12, e0189370. https://doi.
org/10.1371/journal.pone.0189370
Barragán-Barrera, D. C., Quiñones-Lebrón, S., May-Colla-
do, L. & Caballero, S. (2015). First record of the
Rough-toothed dolphins (Steno bredanensis) in coas-
tal Caribbean waters of Panama [Conference session].
Workshop on RIEMMCCA: Network of Aquatic Mam-
mal Specialists of Central America and the Caribbean
[Workshop]. The 21st Biennial Conference on The
Biology of Marine Mammals, San Francisco, Califor-
nia, United States.
Clement, M., Posada, D., & Crandall, K. A. (2000). TCS:
a computer program to estimate gene genealo-
gies. Molecular Ecology, 9, 1657–1659. https://doi.
org/10.1046/j.1365-294x.2000.01020.x
Corredor, J. E. (1979). Phytoplankton response to low
level nutrient enrichment through upwelling in the
Colombian Caribbean Basin. Deep Sea Research
Part A. Oceanographic Research Papers, 26, 731–741.
https://doi.org/10.1016/0198-0149(79)90010-4
Costa, A. F., Siciliano, S., Emin-Lima, R., Martins, B. M. L.,
Sousa, M. E. M., Giarrizzo, T, & de SES, J. J. (2017).
Stranding survey as a framework to investigate rare
cetacean records of the north and north-eastern
Brazilian coasts. ZooKeys, 688, 111–134. https://doi.
org/10.3897/zookeys.688.12636
da Silva, D. M. P., Azevedo, A. F., Secchi, E. R., Barbosa, L.
A., Flores, P. A. C., Carvalho, R. R., Bisi, T. L., Lailson-
Brito, J., & Cunha, H. A. (2015). Molecular taxonomy
and population structure of the rough-toothed dol-
phin Steno bredanensis (Cetartiodactyla: Delphini-
dae). Zoological Journal of the Linnean Society, 175,
949–962. https://doi.org/10.1111/zoj.12301
do Amaral, K. B., Barragán-Barrera, D. C., Mesa-Gutié-
rrez, R., Farías-Curtidor, N., Caballero, S., Méndez-
Fernández, P., Oliveira-Santos, M. C., Siciliano, S.,
Martín, V., Carrillo, M., de Meirelles, A. C., Franco-
Trecu, V., Fagundes, N., Benites-Moreno, I., Knowles,
L., & Amaral, A. R. (2021). Seascape genetics of the
Atlantic spotted dolphin (Stenella frontalis) based
on mtDNA control region. Journal of Heredity, 112,
646–662. https://doi.org/10.1093/jhered/esab050
Donato, A., Siciliano, S., Weksler, M., Silva, D. A., Car-
valho, E. F., Loiola, S., & Amaral, C. R. L. (2019).
Population structure and the conservation status of
the rough-toothed dolphins based on the analysis of
the mitochondrial control region. Forensic Science
International: Genetics Supplement Series, 7, 294–295.
https://doi.org/10.1016/j.fsigss.2019.09.103
Drummond, A. J., Ashton, B., Cheung, M., Heled, J., Kearse,
M., Moir, R., Stones-Havas, S., Thierer, T., & Wilson,
A. (2009). Geneious Pro (V4.8.5)[Computer software].
Genius by Dotmatics. http://www.geneious.com/
Dutton, P. H., Jensen, M. P., Frutchey, K., Frey, A., LaCase-
lla, E., Balazs, G. H., Cruce, J., Tagarino, A., Farman,
R. S., & Tatarata, M. (2014). Genetic stock structure
of Green Turtle (Chelonia mydas) nesting populations
across the Pacific Islands. Pacific Science, 68, 451–464.
https://doi.org/10.2984/68.4.1
Ewing, R. Y., Rotstein, D. S., McLellan, W. A., Costidis, A.
M., Lovewell, G., Schaefer, A. M., Romero, C. H., &
Bossart, G. D. (2020). Macroscopic and histopatholo-
gic findings from a mass stranding of rough-toothed
dolphins (Steno bredanensis) in 2005 on Marathon
Key, Florida, USA. Frontiers in Veterinary Science, 7,
572. https://doi.org/10.3389/fvets.2020.00572
Excoffier, L., & Lischer, H. E. (2010). Arlequin suite ver
3.5: a new series of programs to perform population
genetics analyses under Linux and Windows. Mole-
cular Ecology Resources, 10, 564–567. https://doi.
org/10.1111/j.1755-0998.2010.02847.x
Excoffier, L., Smouse, P. E., & Quattro, J. M. (1992). Analy-
sis of molecular variance inferred from metric distan-
ces among DNA haplotypes: application to human
mitochondrial DNA restriction data. Genetics, 131,
479–491. https://doi.org/10.1093/genetics/131.2.479
Fajardo, G. E. (1979). Surgencia costera en las proximi-
dades de la Península Colombiana de La Guajira.
Boletín Científico del CIOH, 2, 7–19. https://doi.
org/10.26640/01200542.2.7_19
Farías-Curtidor, N., & Ayala, R. (2015, December 13-18).
Occurrence of odontocetes in the Lower Guajira
(Colombian Caribbean) [Conference session]. Work-
shop on RIEMMCCA: Network of Aquatic Mammal
Specialists of Central America and the Caribbean
[Workshop]. The 21st Biennial Conference on The
Biology of Marine Mammals, San Francisco, Califor-
nia, United States.
Farías-Curtidor, N., & Barragán-Barrera, D. C. (2017, Octo-
ber 23-27). Occurrence of odontocetes in La Guajira
(Northern portion of the Colombian Caribbean)
[Conference session]. The 22nd Biennial Conference
on The Biology of Marine Mammals, Halifax, Nova
Scotia, Canada
Farías-Curtidor, N., & Barragán-Barrera, D. C. (2019,
October 22-25). Ocurrencia de pequeños cetáceos en
La Guajira (Caribe colombiano)[Conference session].
XVIII Seminario Nacional de Ciencias y Tecnolo-
gías del Mar SENALMAR, Barranquilla, Colombia..
15
Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
https://cco.gov.co/docs/senalmar/memorias/memo-
rias-2019.pdf
Farías-Curtidor, N., Barragán-Barrera, D. C., Chávez-
Carreño, P. A., Jiménez-Pinedo, C., Palacios, D.,
Caicedo, D., Trujillo, F., & Caballero, S. (2017). Range
extension for the common dolphin (Delphinus sp.) to
the Colombian Caribbean, with taxonomic implica-
tions from genetic barcoding analysis. PLoS ONE, 12,
e0171000. https://doi:10.1371/journal.pone.0171000
Fraija, N., Flórez-González, L., & Jáuregui, A. (2009).
Cetacean occurrence in the Santa Marta region,
Colombian Caribbean. Latin American Journal of
Aquatic Mammals, 7, 69–73. https://doi.org/10.5597/
lajam00137
Friedman, A., & Grandmont, T. (2019). Roads and Man-
grove Deforestation in Eastern Azuero Peninsula,
Panama. Proyecto Ecológico Azuero. Panama Field
Study Semester. https://www.mcgill.ca/pfss/files/pfss/
roads_and_mangrove_deforestation_in_eastern_azue-
ro_peninsula_panama.pdf
Fruet, P. F., Secchi, E. R., Daura-Jorge, F., Vermeulen, E.,
Flores, P. A. C., Simões-Lopes, P. C., Genoves, R. C.,
Laporta, P., di Tullio, J. C., Freitas, T. R. O., Rosa,
L. D., Valiati, V. H., Beheregaray, L. B., & Möller, L.
M. (2014). Remarkably low genetic diversity and
strong population structure in common bottlenose
dolphins (Tursiops truncatus) from coastal waters
of the Southwestern Atlantic Ocean. Conservation
Genetics, 15(4), 879–895. https://doi.org/10.1007/
s10592-014-0586-z
Gilson, A., Syvanen, M., Levine, K., & Banks, J. (1998). Deer
gender determination by polymerase chain reaction:
Validation study and application to tissues, bloods-
tains, and hair forensic samples from California.
California Fish and Game, 84, 159–169.
Gutiérrez Leones, G. A., Correa Ramírez, M. A., & Hor-
mazabal Fritz, S. E. (2015). Análisis de la variabilidad
espacio-temporal del sistema de surgencia de La
Guajira en el dominio espacio-frecuencia, empleando
el MTM-SVD (Multi Taper Method Singular Value
Decomposition). Boletín Científico CIOH, 33, 87–106.
https://doi.org/10.26640/01200542.33.87_106
Guzmán, H. M., & Guevara, C. A. (1998). Arrecifes cora-
linos de Bocas del Toro, Panamá: distribución,
estructura y estado de conservación de los arrecifes
continentales de la Laguna de Chiriquí y la Bahía
Almirante. Revista de Biología Tropical, 46(3), 601–
623. http://www.scielo.sa.cr/scielo.php?script=sci_
arttext&pid=S0034-77441998000300014&lng=en&tl
ng=es
Jensen, M. P., Bell, I., Limpus, C. J., Hamann, M., Ambar, S.,
Whap, T., Charles, D. & FitzSimmons, N. N. (2016).
Spatial and temporal genetic variation among size
classes of green turtles (Chelonia mydas) provides
information on oceanic dispersal and population
dynamics. Marine Ecology Progress Series, 543, 241–
256. http://dx.doi.org/10.3354/meps11521
Jefferson, T. A. (2018). Rough-toothed dolphin Steno breda-
nensis. In B. Würsig, J. G. M. Thewissen & K. Kovacs
(Eds.), Encyclopedia of Marine Mammals, (3rd ed., pp.
838–840). Academic Press. https://doi.org/10.1016/
B978-0-12-804327-1.00223-5
Kerem, D., Goffman, O., Elasar, M., Hadar, N., Scheinin,
A., & Lewis, T. (2016). The rough-toothed dolphin,
Steno bredanensis, in the eastern Mediterranean Sea.
Advances in Marine Biology, 75, 233–258. https://doi.
org/10.1016/bs.amb.2016.07.005
Kiszka, J., Baird, R., & Braulik, G. (2019). Steno bredanensis
(errata version published in 2020). The IUCN Red List
of Threatened Species. https://dx.doi.org/10.2305/
IUCN.UK.2019-2.RLTS.T20738A178929751.en
Kuczaj II, S. A., & Yeater, D. (2007). Observations of rough-
toothed dolphins (Steno bredanensis) off the coast
of Utila, Honduras. Journal of the Marine Biological
Association of the United Kingdom, 87, 141–148.
https://doi.org/10.1017/S0025315407054999
Krützen, M., Barre, L. M., Möller, L. M., Heithaus, M. R.,
Simms, C., & Sherwin, W. B. (2002). A biopsy sys-
tem for small cetaceans: darting success and wound
healing in Tursiops spp. Marine Mammal Science, 18,
863–878. https://doi.org/10.1111/j.1748-7692.2002.
tb01078.x
Lailson-Brito, J., Dorneles, P. R., Azevedo-Silva, C. E.,
Bisi, T. L., Vidal, L. G., Legat, L. N., Azevedo, A. F.,
Torres, J. P. M., & Malm, O. (2012). Organochlorine
compound accumulation in delphinids from Rio de
Janeiro State, southeastern Brazilian coast. Science
of the Total Environment, 433, 123–131. https://doi.
org/10.1016/j.scitotenv.2012.06.030
Learmonth, J., MacLeod, C., Santos, M., Pierce, G., Crick,
H., & Robinson, R. (2007) Potential effects of climate
change on marine mammals.Oceanography and Mari-
ne Biology: An Annual Review, 44, 431–464 https://
doi.org/10.1201/9781420006391.ch8
Lemos, L. S., de Moura, J. F., Hauser-Davis, R. A., de Cam-
pos, R. C., & Siciliano, S. (2013). Small cetaceans
found stranded or accidentally captured in southeas-
tern Brazil: Bioindicators of essential and non-essen-
tial trace elements in the environment. Ecotoxicology
and Environmental Safety, 97, 166–175. https://doi.
org/10.1016/j.ecoenv.2013.07.025
May-Collado, L. J., Amador-Caballero, M., Casas, J. J.,
Gamboa-Poveda, M. P., Garita-Alpízar, F., Gerrodette,
T., González-Barrientos, R., Hernández-Mora, G.,
Palacios, D. M., Palacios-Alfaro, J. D., Pérez, B., Ras-
mussen, K., Trejos-Lasso. L., & Rodríguez-Fonseca,
J. (2017). Ecology and conservation of cetaceans of
Costa Rica and Panama. In M. Rossi-Santos & C.
Finkl (Eds.), Advances in Marine Vertebrate Research
16 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57285, diciembre 2023 (Publicado Nov. 01, 2023)
in Latin America, (Vol. 22, pp. 293–319). Springer.
https://doi.org/10.1007/978-3-319-56985-7_12
Meirelles, A. C. O., & Barros, H. M. D. R. (2007). Plastic
debris ingested by a rough-toothed dolphin, Steno
bredanensis, stranded alive in northeastern Brazil.
Biotemas, 20, 127–131. https://doi.org/10.5007/%X
Mignucci-Giannoni, A. A. (1989). Zoogeography of Mari-
ne Mammals in Puerto Rico and the Virgin Islands
[Unpublished master’s thesis]. University of Rhode
Island.
Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010, Novem-
ber 14). Creating the CIPRES Science Gateway for
Inference of Large Phylogenetic Trees [Paper pre-
sentation]. 2010 Gateway Computing Environments
Workshop, (GCE), New Orleans, Luisiana, United
States. https://doi.org/10.1109/GCE.2010.5676129
Monteiro-Neto, C., Alves-Junior, T. T., Avilla, F. J. C.,
Campos, A. A., Costa, A. F., Silva, C. P. N., & Furtado-
Neto, M. A. A. (2000). Impact of fisheries on the
tucuxi (Sotalia fluviatilis) and rough-toothed dolphin
(Steno bredanensis) populations off Cerara state, nor-
theastern Brazil. Aquatic Mammals, 26, 49–56.
Müller-Karger, F. E., & Aparicio, R. (1994). Mesoscale proces-
ses affecting phytoplankton abundance in the southern
Caribbean Sea. Continental Shelf Research, 14, 199–
221. https://doi.org/10.1016/0278-4343(94)90013-2
Nara, L., de Meirelles, A. C. O., Souto, L. R. A., Silva-Jr.,
J. M., & Farro, A. P. C. (2017). An initial population
structure and genetic diversity analysis for Stenella
clymene (Gray, 1850): evidence of differentiation
between the North and South Atlantic Ocean. Aqua-
tic Mammals, 43, 507–516. https://doi.org/10.1578/
AM.43.5.2017.507
Oremus, M., Poole, M. M, Albertson, G. R., & Baker, C.
S. (2012). Pelagic or insular? Genetic differentiation
of rough-toothed dolphins in the Society Islands,
French Polynesia. Journal of Experimental Marine
Biology and Ecology, 432–433, 37–46. https://doi.
org/10.1016/j.jembe.2012.06.027
Ott, P. H., & Danilewicz, D. (1996). Southward range exten-
sion of Steno bredanensis in the Southwest Atlantic
and new records of Stenella coeruleoalba for Brazilian
waters. Aquatic Mammals, 22,185–189.
Pardo, M., & Palacios, D. (2006). Cetacean occurrence in
the Santa Marta Region, Colombian Caribbean, 2004-
2005. Latin American Journal of Aquatic Mammals, 5,
129–134. https://doi.org/10.5597/lajam00105
Pino, L. V. (2021). Riesgo potencial de captura incidental del
delfín manchado pantropical (Stenella attenuata) por
pesquerías de atún en el Pacífico Oriental Tropical y
el Gran Caribe [Unpublished Bachelor dissertation].
Universidad del Valle.
Read, T. C., Wantiez, L., Werry, J. M., Farman, R., Petro, G.,
& Limpus, C. J. (2014). Migrations of Green Turtles
(Chelonia mydas) between Nesting and Foraging
Grounds across the Coral Sea. PLoS ONE, 9, e100083.
https://doi.org/10.1371/journal.pone.0100083
Richmond, R. H. (1990). The effects of the El Niño/Southern
oscillation on the dispersal of corals and other marine
organisms. Elsevier Oceanography Series, 52, 127–140.
https://doi.org/10.1016/S0422-9894(08)70034-5
Sanger, F., & Coulson, A. R. (1975). A rapid method
for determining sequences in DNA by pri-
med synthesis with DNA polymerase. Journal of
Molecular Biology, 94, 441–446. https://doi.
org/10.1016/0022-2836(75)90213-2
Santos, M. C. O., Laílson-Brito, J., Flach, L., Oshima, J. E.
F., Figueiredo, G. C., Carvalho, R. R., Ventura, E. S.,
Molina, J. M. B., & Azevedo, A. F. (2019). Cetacean
movements in coastal waters of the southwestern
Atlantic Ocean. Biota Neotropica, 19, e20180670.
https://doi.org/10.1590/1676-0611-BN-2018-0670
Seminoff, J. A., Zárate, P. M., Coyne, M. S., Foley, D. G.,
Parker, D. M., Lyon, B. N., & Dutton, P. H. (2008).
Post-nesting migrations of Galápagos green turtles
Chelonia mydas in relation to oceanographic condi-
tions: integrating satellite telemetry with remotely
sensed ocean data. Endangered Species Research, 4,
57–72. https://doi.org/10.3354/esr00066
Struntz, W. D., Kucklick, J. R., Schantz, M. M., Becker, P.
R., McFee, W. E., & Stolen, M. K. (2004). Persistent
organic pollutants in rough toothed dolphins (Steno
bredanensis) sampled during an unusual mass stran-
ding event. Marine Pollution Bulletin, 48(1-2), 164-
192. https://doi.org/10.1016/j.marpolbul.2003.09.002
Victor, B. C., Wellington, G., Robertson, D. R., & Rutten-
berg, B. I. (2004). The effect of The El Niño - Southern
Oscillation event on the distribution of reef-associa-
ted labrid fishes in the eastern Pacific Ocean. Bulletin
of Marine Science, 69, 279–288.
Weber, D. S., Stewart, B. S., & Lehman, N. (2004). Genetic
consequences of a severe population bottleneck in the
Guadalupe fur seal (Arctocephalus townsendi). Journal
of Heredity, 95, 144–153. https://doi.org/10.1093/
jhered/esh018
