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

OAI: https://revistas.ucr.ac.cr/index.php/rbt/oai
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
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Keywords

Delphinids; cetaceans; Control Region; mtDNA; Caribbean; Pacific Ocean; conservation.
Delfínidos; cetáceos; Región Control; ADNmt; Caribe; Océano Pacífico; conservación.

How to Cite

Barragán-Barrera, D. C., Correa-Cárdenas, C. A., Duarte-Fajardo, M. A., Trejos Lasso, L., Pérez-Ortega, B., Quiñones-Lebrón, S. G., Mignucci-Giannoni, A. A., Casas, J. J., Santamaria Valverde, R., Farías-Curtidor, N., & Caballero, S. (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. Revista De Biología Tropical, 71(S4), e57285. https://doi.org/10.15517/rev.biol.trop.v71iS4.57285

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 differentiation 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.

https://doi.org/10.15517/rev.biol.trop..v71iS4.57285
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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 marine predator, the common dolphin (genus Delphinus). 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 International 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 Investigaciones 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 Biología 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 mitochondrial 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, selenium 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-Carreño, 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, 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. 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 population at risk? PLoS ONE, 12, e0189370. https://doi.org/10.1371/journal.pone.0189370

Barragán-Barrera, D. C., Quiñones-Lebrón, S., May-Collado, L. & Caballero, S. (2015). First record of the Rough-toothed dolphins (Steno bredanensis) in coastal Caribbean waters of Panama [Conference session]. Workshop 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, California, United States.

Clement, M., Posada, D., & Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. 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 dolphin Steno bredanensis (Cetartiodactyla: Delphinidae). 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-Gutiérrez, 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., Carvalho, 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., LaCasella, 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 histopathologic 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. Molecular 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). Analysis of molecular variance inferred from metric distances 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 proximidades 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]. Workshop 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, California, United States.

Farías-Curtidor, N., & Barragán-Barrera, D. C. (2017, October 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 Tecnologías del Mar SENALMAR, Barranquilla, Colombia.. https://cco.gov.co/docs/senalmar/memorias/memorias-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 implications 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 Mangrove 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_azuero_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, bloodstains, and hair forensic samples from California. California Fish and Game, 84, 159–169.

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. https://doi.org/10.26640/01200542.33.87_106

Guzmán, H. M., & Guevara, C. A. (1998). Arrecifes coralinos 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&tlng=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 bredanensis. 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 system 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 Marine 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 Campos, R. C., & Siciliano, S. (2013). Small cetaceans found stranded or accidentally captured in southeastern Brazil: Bioindicators of essential and non-essential 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., 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). 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 Marine Mammals in Puerto Rico and the Virgin Islands [Unpublished master’s thesis]. University of Rhode Island.

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, 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, northeastern Brazil. Aquatic Mammals, 26, 49–56.

Müller-Karger, F. E., & Aparicio, R. (1994). Mesoscale processes 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. Aquatic 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 extension 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 primed 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 conditions: 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 stranding 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., & Ruttenberg, B. I. (2004). The effect of The El Niño - Southern Oscillation event on the distribution of reef-associated 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

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