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 Panamas 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