Revista de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

Mitochondrial DNA supports the low genetic diversity of Tursiops truncatus (Artiodactyla: Delphinidae) in Bocas del Toro, Panama and exhibits new Caribbean haplotypes

Supplementary Files



bottlenose dolphin; cetaceans; mtDNA; genetic diversity; La Guajira, Colombia, Central America.
delfín nariz de botella; cetáceos; ADNmt; diversidad genética; La Guajira, Colombia, Centroamérica.

How to Cite

Duarte-Fajardo, M. A., Barragán-Barrera, D. C., Correa-Cárdenas, C. A., Pérez-Ortega, B., Farías-Curtidor, N., & Caballero, S. (2023). Mitochondrial DNA supports the low genetic diversity of Tursiops truncatus (Artiodactyla: Delphinidae) in Bocas del Toro, Panama and exhibits new Caribbean haplotypes. Revista De Biología Tropical, 71(S4), e57291.


Introduction: The common bottlenose dolphin (Tursiops truncatus) is one of the most studied cetaceans worldwide; however, information about the genetic structure of wild populations is scarce in some regions like Central America and the Caribbean. There are two known genetic forms identified in the Caribbean based on mitochondrial DNA Control Region (mtDNA-CR) data: the ‘inshore (or coastal) form’ and the ‘Worldwide distributed form’. In general, the inshore form refers to coastal and highly philopatric populations that show low genetic diversity. Worldwide distributed form refers to highly mobile populations with coastal and oceanic individuals that do not show philopatry and usually display high genetic diversity.

Objective: To determine the preliminary genetic status of common bottlenose dolphins in La Guajira, Colombian Caribbean, using a hypervariable portion of mtDNA-CR. The obtained haplotypes were compared with samples collected in Panama (likely ‘inshore form’) and with haplotypes previously found in other areas of the Caribbean.

Methods: In 2016, a total of 26 skin samples were obtained by remote biopsy system (PAXARMS) in two locations, La Guajira (Colombia, N=7) and Bocas del Toro (Panama, N=19). DNA was extracted, samples sexed, and a segment of mtDNA-CR (~550-750 bp) was amplified by PCR. The successfully amplified DNA sequences were manually reviewed and cleaned, and subsequently compared with 44 haplotypes previously reported for the Caribbean.

Results: The mtDNA-CR sequences from Bocas del Toro shared the same unique inshore haplotype previously reported for this population, while the samples from La Guajira represented six novel haplotypes, five belonging to the Worldwide distributed form and one to the ‘inshore form.’ Population structure analysis revealed two phylogroups for the Caribbean (FST=0.1353, ΦST=0.3330) with high haplotype diversity: Panama(Bocas del Toro)-Bahamas-Cuba-Mexico (h=0.8489, π=4.2536 %) and Colombia-Costa Rica-Honduras-Puerto Rico (h=0.8837, π=4.2423 %).

Conclusions: These findings support the results previously reported for common bottlenose dolphins in Bocas del Toro-Panama and reinforce the need to protect this vulnerable ‘inshore’ population by treating it as a unique population management unit. Mitochondrial DNA analysis of samples collected from La Guajira dolphins provide the first insight into the genetic diversity of common bottlenose dolphins in this region, indicating the presence of both inshore and Worldwide distributed genetic forms. The potential connectivity of this last form among La Guajira-Colombia, Costa Rica, and Honduras in Central America highlights the need for more genetic and ecological studies to determine the appropriate management units for this species in Central America and the Caribbean.


Amos, W., & Hoelzel, A.R., (1991). Long-term preservation of whale skin for DNA analysis. Report of the International Whaling Commission, Special Issue, 13, 99–104.

Amos, W., Schloetterer, C., & Tautz, D. (1993). Social structure of pilot whales revealed by analytical DNA profiling. Science, 260, 670 – 672.

Andrade, C. A., & Barton, E. D. (2005). The Guajira upwelling system. Continental Shelf Research, 25, 1003–1022.

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

Avila, I. C., & Giraldo, A. (2022). Áreas en riesgo para los mamíferos marinos en Colombia. Revista de Biología Tropical, 70, 96–113. trop..v70i1.48553

Baker, C. S., Medrano-González, L., Calambokidis, J., Perry, A., PichlerI, F., Rosenbaum, H., Straley, J. M., Urban-Ramirez, J., Yamaguchi, M., & von Ziegesar, O. (1998). Population structure of nuclear and mitochondrial DNA variation among humpback whales in the North Pacific. Molecular Ecology, 7, 695–707.

Baker, C. S., Perry, A., Bannister, J. L., Weinrich, M. T., Abernethy, R. B., Calambokidis, J., Lien, J., Lambertsen, R. H., Ramírez, J. U., &; Vasquez, O. (1993). Abundant mitochondrial DNA variation and world-wide population structure in humpback whales. Proceedings of the National Academy of Sciences, 90, 8239–8243.

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, N., & Caballero, S. (2019). Foraging habits and levels of mercury in a resident population of bottlenose dolphins (Tursiops truncatus) in Bocas del Toro Archipelago, Caribbean Sea, Panama. Marine Pollution Bulletin, 145, 343–356.

Barragán-Barrera, D. C., Farías-Curtidor, N., Luna-Acosta, A.,Bustamante, P., Ayala, R. & Caballero, S. (2019, September 15 – 18). Evidence of mercury bioaccumulation in skin samples of wild delphinids in La Guajira, Colombian Caribbean [Poster presentation]. SETAC Latin America 13th Biennial Meeting, Cartagena, Colombia.

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 population at risk? PLOS ONE, 12, e0189370.

Bigg, M. A., Ellis, G. M., Ford, J. K. B., & Balcomb, K. C. (1987). Killer whales: A study of their identification, genealogy, and natural history in British Columbia and Washington State. Phantom Press.

Caballero, S., Islas-Villanueva, V., Tezanos-Pinto, G., Duchene, S., Delgado-Estrella, A., Sanchez-Okrucky, R., & Mignucci-Giannoni, A. A. (2012). Phylogeography, genetic diversity and population structure of common bottlenose dolphins in the Wider Caribbean inferred from analyses of mitochondrial DNA control region sequences and microsatellite loci: conservation and management implications. Animal Conservation, 15, 95–112. https ://

Clement, M., Posada, D., & Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659.

Coates, A. G., McNeill, D. F., Aubry, M. P., Berggren, W. A., & Collins, L. S. (2005). An introduction to the geology of the Bocas del Toro Archipelago, Panama. Caribbean Journal of Science, 41, 374–391.

Combatt, J. A., & González, E. A. (2007). Ocurrencia y distribución del delfín nariz de botella Tursiops truncatus en las costas de Dibulla, Baja Gaujira, durante el periodo de agosto a diciembre de 2005 [Bachelor’s thesis, Universidad de Bogotá Jorge Tadeo Lozano]. Expeditio.

Costa, A. P. B., Mcfee, W., Wilcox, L. A., Archer, F. I., & Rosel, P. E. (2022). The common bottlenose dolphin (Tursiops truncatus) ecotypes of the western North Atlantic revisited: an integrative taxonomic investigation supports the presence of distinct species. Zoological Journal of the Linnean Society, 196, 1608–1636.

Corporación autónoma Regional de La Guajira, & Instituto de Investigaciones Marinas y Costeras (2012). Atlas marino costero de La Guajira. Serie de Publicaciones Especiales de Invemar No. 27. Instituto de Investigaciones Marinas y Costeras.

Drummond, A.J., Ashton, B., Cheung. M., Heled, J., Kearse, M., Moir, R., et al. (2009). Geneious Pro (V4.8.5) [Computer software]. Geneious by Dotmatics.,503,

Duffield, D. a., Ridgway, S. H., & Cornell, L. H. (1983). Hematology distinguishes coastal and offshore forms of dolphins (Tursiops). Canadian Journal of Zoology, 61, 930–933.

Escorza-Treviño, S., & Dizon, A. E. (2000). Phylogeography, intraspecific structure and sex-biased dispersal of dall’s porpoise, Phocoenoides dalli, revealed by mitochondrial and microsatellite DNA analyses. Molecular Ecology, 9, 1049–1060.

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. Molecular Ecology Resources, 10(3), 564–567.

Farías-Curtidor, N., Barragán-Barrera, D. C., Chávez-Carreno, P. A., Jiménez-Pinedo, C., Palacios, D. M., Caicedo, D., Trujillo, F., & Caballero, S. (2017). Range extension for the common dolphin (Delphinus sp.) to the Colombian Caribbean, with taxonomic implications from genetic barcoding and phylogenetic analyses. PloS ONE, 12, e0171000.

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, 879–895.

Gilson, A., Syvanen, M., Levine, K., & Banks, J. (1998). Deer gender determination by polymerase chain reaction: Validation study and application to tissues, bloodstains, and hair forensic samples from California. California Fish and Game, 84, 159–169.

González-Velásquez, M. (2020). Insights on mercury biomagnification in the Pantropical Spotted Dolphin (Stenella attenuata) food chain from Belize [Bachelor’s thesis, Universidad de Los Andes]. Séneca.

Gutiérrez Leones, G. A., Correa Ramírez, M. A., & Hormazabal 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.

Guzmán, H. M., Barnes, P. A. G., Lovelock, C. E., & Feller, I. C. (2005). A site description of the CARICOMP mangrove, seagrass and coral reef sites in Bocas del Toro, Panama. Caribbean Journal of Science, 41, 430–440.

Hersh, S.L. & Duffield, D.A. (1990). Distinction between northwest Atlantic offshore and coastal bottlenose dolphins based on hemoglobin profile and morphometry. In S. Leatherwood. & R. R. Reeves (Eds), The bottlenose dolphin (pp. 129–139). Academy Press.

Hoelzel, A. R., Potter, C. W., & Best, P. B. (1998). Genetic differentiation between parapatric “nearshore” and “offshore” populations of the bottlenose dolphin. Proceedings of the Royal Society B: Biological Sciences, 265, 1177–1183.

Kassamali-Fox, A., Christiansen, F., May-Collado, L. J., Ramos, E. A., & Kaplin, B. A. (2020). Tour boats affect the activity patterns of bottlenose dolphins (Tursiops truncatus) in Bocas del Toro, Panama. PeerJ, 8, e8804.

Krützen, M., Barre, L. M., Moller, L. M., Heithaus, M. R., Simms, C., & Sherwin, W. B. (2002). A biopsy system for small cetaceans: darting success and wound healing in Tursiops spp. Marine Mammal Science, 18, 863–878.

May-Collado, L. J., Barragán-Barrera, D. C., Quiñones-Lebrón, S. G., & Aquino-Reynoso, W. (2012, July 2-6). Dolphin watching boats impact on habitat use and communication of bottlenose dolphins of Bocas del Toro, Panama during [Paper presentation, SC/64/WW2]. International Whaling Commission 2012 Panama City, Panama.

May-Collado, L. J., & Quiñones-Lebrón, S. G. (2014). Dolphin changes in whistle structure with watercraft activity depends on their behavioral state. The Journal of the Acoustical Society of America, 135, EL193–EL198.

May-Collado, L. J., Quinones-Lebron, S., Barragán-Barrera, D. C., Jose D. Palacios, Monica Gamboa Poveda, & Ayshah Kassamali-Fox. (2015, May 22 - June 3). The Bocas del Toro’s dolphin watching industry relies on a small community of bottlenose dolphins: implications for management [Paper presentation SC/66a/WW10]. International Whaling Commission 2015, San Diego, California, United States.

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., Rasmussen, 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 in Latin America (Vol. 22, pp. 293–319).

May-Collado, L. J., Pérez, B., Barragán-Barrera, D. C., Gonzalez, K., Swack, N., Gamboa-Poveda, M. & J. D. Palacios-Alfaro, J. D. (2019, May 10-23). An update of the conservation status of the bottlenose dolphins of Bocas del Toro Panama: Female calving intervals and calf survivorship [Paper presentation, SC/68A/WW/WP/03/rev1]. International Whaling Commission 2019, Nairobi, Kenya.

Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010, November 14). Creating the CIPRES science gateway for inference of large phylogenetic trees [Paper presentation]. 2010 Gateway Computing Environments Workshop (GCE), New Orleans, LA, United States.

Möller, L. M., & Beheregaray, L. B. (2004). Genetic evidence for sex-biased dispersal in resident bottlenose dolphins (Tursiops aduncus). Molecular Ecology, 13(6), 1607–1612.

Natoli, A., Peddemors, V. M., & Rus Hoelzel, A. (2004). Population structure and speciation in the genus Tursiops based on microsatellite and mitochondrial DNA analyses. Journal of Evolutionary Biology, 17, 363–375.

Palacios, D. M., Gärtner, A., Caicedo, D., Farías, N., Jiménez-Pinedo, C., Curcio-Valencia, J., Aldana-Domínguez, J., Trujillo, F., & Moná-Sanabria, Y. (2013). Mamíferos acuáticos de la región Caribe colombiana. In F. Trujillo, A. Gärtner, D. Caicedo & M. C. Diazgranados (Eds.), Diagnóstico del estado de conocimiento y conservación de los mamíferos acuáticos en Colombia (pp. 95–126). Ministerio de Ambiente y Desarrollo Sostenible, Fundación Omacha, Conservación Internacional y WWF.

Paramo, J., Correa, M., & Núñez, S. (2011). Evidencias de desacople físico-biológico en el sistema de surgencia en la Guajira, caribe Colombiano. Revista de Biologia Marina y Oceanografia, 46, 421–430.

Parsons, K. M., Durban, J. W., Claridge, D. E., Herzing, D. L., Balcomb, K. C., & Noble, L. R. (2006). Population genetic structure of coastal bottlenose dolphins (Tursiops truncatus) in the northern Bahamas. Marine Mammal Science, 22, 276–298.

Pérez-Ortega, B., Daw, R., Paradee, B., Gimbrere, E., & May-Collado, L. J. (2021). Dolphin-Watching Boats Affect Whistle Frequency Modulation in Bottlenose Dolphins. Frontiers in Marine Science, 8, 618420.

Reynolds, J. E., Wells, R. S., & Eide, S. D. (2000). The bottlenose dolphin: Biology and conservation. University Press of Florida.

Rosel, P. E., France, S. C., Wang, J. Y., &; Kocher, T. D. (1999). Genetic structure of Harbour Porpoise Phocoena phocoena populations in the northwest Atlantic based on mitochondrial and nuclear markers. Molecular Ecology, 8, S41-54.

Sanger, F, & Coulson, A. R. (1975). A rapid method for determining sequences in DNA by primed synthesis with DNA polymerase. Journal of Molecular Biology, 94, 441–446.

Sellas, A. B., Wells, R. S., & Rosel, P. E. (2005). Mitochondrial and nuclear DNA analyses reveal fine scale geographic structure in bottlenose dolphins (Tursiops truncatus) in the Gulf of Mexico. Conservation Genetics, 6, 715–728.

Tezanos-Pinto, G., & Baker, C. S. (2012). Short-term reactions and long-term responses of bottlenose dolphins (Tursiops truncatus) to remote biopsy sampling. New Zealand Journal of Marine and Freshwater Research, 46, 13–29.

Tezanos-Pinto, G., Baker, C. S., Russell, K., Martien, K., Baird, R. W., Hutt, A., Stone, G., Mignucci-Giannoni, A. A., Caballero, S., Endo, T., Lavery, S., Oremus, M., Olavarría, C., & Garrigue, C. (2009). A Worldwide Perspective on the Population Structure and Genetic Diversity of Bottlenose Dolphins (Tursiops truncatus) in New Zealand. Journal of Heredity, 100, 11–24.

Wang, J. Y., Chou, L.-S., & White, B. N. (1999). Mitochondrial DNA analysis of sympatric morphotypes of bottlenose dolphins (genus: Tursiops) in Chinese waters. Molecular Ecology, 8, 1603–1612.

Wells, R.S., Natoli, A. & Braulik, G. (2019). Tursiops truncatus (errata version published in 2019). e.T22563A156932432. The IUCN Red List of Threatened Species

Wiszniewski, J., Beheregaray, L. B., Allen, S. J., & Möller, L. M. (2010). Environmental and social influences on the genetic structure of bottlenose dolphins (Tursiops aduncus) in southeastern australia. Conservation Genetics, 11, 1405–1419.


Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.


Download data is not yet available.