Keywords
Delfín Nariz de Botella; enfermedad similar a Lobomicosis; Golfo Dulce; Golfo de Nicoya; Costa Pacífica; ecotipo costero.
How to Cite
Abstract
Introduction: Lobomycosis, is a chronic mycotic disease of the skin and sub-dermal tissue caused by Paracoccidioides ceti, which affects dolphins worldwide. In Costa Rica, the incidence of lobomycosis Like Disease (LLD) has been documented in inshore common bottlenose dolphins (Tursiops truncatus) from the waters of Golfo Dulce, South Pacific.
Objective: Examine the prevalence pattern of LLD in inshore T. truncatus from Costa Rica Pacific waters, specifically in Golfo Dulce and Golfo de Nicoya.
Methods: We examined over 20 000 photographs of T. truncatus, collected during long-term research on cetaceans in 2005-2020 (n = 476 surveys), in Golfo Dulce, as well of nine sightings T. truncatus from the Golfo de Nicoya , obtained during 17 samplings events in 2014-2022, these records for the presence of LLD allowed to calculate the prevalence rate with a confidence interval.
Results: The prevalence rate of LLD in adult photo-identified individuals was 13.1 % (CI: 12 -14.2) in Golfo Dulce, and 100 % in Golfo de Nicoya, considering the size of the population for the period of 2022.
Conclusion: The persistence and high prevalence levels of LLD in small, localized, communities of T. truncatus are a cause for serious concern.
References
Acevedo, A., & Burkhart, S. (1998). Seasonal distribution of bottlenose (Tursiops truncatus) and pan-tropical spotted (Stenella attenuata) dolphins (Cetacea: Delphinidae) in Golfo Dulce, Costa Rica. Revista de Biología Tropical, 46, 91–101.
Acuña-González, J. A., Vargas-Zamora, J. A., Gómez-Ramírez, E., & García-Céspedes, J. (2004). Hidrocarburos de petróleo, disueltos y dispersos en cuatro ambientes costeros de Costa Rica. Revista Biología Tropical, 52, 43–50.
Bermudez, L., Van Bressem, M., Reyes, O., Sayegh, A., & Paniz, A. (2009). Lobomycosis in man and lobomycosis like disease in bottlenose dolphin, Venezuela. Emerging Infectious Diseases, 15, 1301–1303. https://doi.org/10.3201/eid1508.090347
Bessesen, B., Oviedo, L., Acevedo-Gutiérrez, A., Burdett Hart, L., Herra-Miranda, D., Pacheco-Polanco, J. D., Baker, L., Saborío-R, G., & Bermúdez-Villapol, L. (2014). Lacaziosis-like disease in Costa Rica from photographic records of bottlenose dolphins Tursiops truncatus in Golfo Dulce. Emerging Infectious Diseases, 107, 173–180.https://doi.org/10.3354/dao02692
Burdett Hart, L., Rotstein, D. S, Wells, R. S, Bassos-Hull, K., & Schwacke, L. H. (2011). Lacaziosis and lacaziosis-like pre - valence among wild, common bottlenose dolphins Tursiops truncatus from the west coast of Florida, USA. Diseases of Aquatic Organisms, 95, 49–56.https://doi.org/10.3354/dao02345
Burdett Hart, L., Rotstein, D. S., Wells, R. S., Allen, J., Barleycorn, A., Balmer, B. C., Lane, S. M., Speakman, T., Zolman, E. S., Stolen, M., McFee, W., Goldstein, T., Rowles, T. K., & Schwacke, L. H. (2012). Skin Lesions on Common Bottlenose Dolphins (Tursiops truncatus) from Three Sites in the Northwest Atlantic, USA. Plos One, 7, e33081. https://doi.org/10.1371/journal.pone.0033081
Brenes, C. L., León, S., & Chaves, J. (2001). Variación de las propiedades termohalinas en el Golfo de Nicoya, Costa Rica. Revista de Biología Tropical, 49, 145–152.
Cubero-Pardo, P. (1998). Distribución y patrones de actividad del bufeo (Tursiops truncatus) y el delfín manchado (Stenella attenuata) en el Golfo Dulce [Unpublished Master’s thesis]. Universidad de Costa Rica.
Daura-Jorge, F., & Simōes-Lopes, A. (2011). Lobomycosis like disease in wild bottlenose dolphins Tursiops truncatus of Laguna, southern Brazil: monitoring a progressive case. Diseases of Aquatic Organisms, 93, 163–170. https://doi.org/10.3354/dao02291
Dalsgaard, T., Canfield, D. E., Petersen, J., Thamdrup, B., & Acuña-González, J. (2003). N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature, 422(6932), 606–608.https://doi.org/10.1038/nature01526
Dalsgaard, T., Thamdrup, B., & Canfield, D. E. (2005). Anaerobic ammonium oxidation (anammox) in the marine environment. Research in Microbiology, 156, 457–464. https://doi.org/10.1016/j.resmic.2005.01.011
Di Giacomo, A. B., & Ott, P. H. (2016). Long-term site fidelity and residency patterns of bottlenose dolphins (Tursiops truncatus) in the Tramandaí Estuary, southern Brazil. Latin American Journal of Aquatic Mammals, 11, 155–161. https://doi.org/10.5597/00224
Ferdelman, T. G., Thamdrup, B., Canfield, D. E., Nøhr Glud, R., Kuever, J., Lillebæk, R., & Wawer, C. (2006). Biogeochemical controls on the oxygen, nitrogen and sulfur distributions in the water column of Golfo Dulce: an anoxic basin on the Pacific coast of Costa Rica revisited. Revista de Biología Tropical, 54, 171–191.
Félix, F., Van Bressem, M. F., & Van Waerebeek, K. (2019). Role of social behaviour in the epidemiology of lobomycosis-like disease (LLD) in estuarine common bottlenose dolphins from Ecuador. Diseases of Aquatic Organisms, 134, 75–87. https://doi.org/10.3354/dao03356
Félix, F., Zavala, M., & Centeno, R. (2019). Distribución espacial, estructura social y amenazas de conservación de una pequeña comunidad de delfines nariz de botella, Tursiops truncatus (Odontoceti: Delphinidae) en Ecuador. Revista de Biología Tropical, 67, 1059–1076.
Gómez-Salazar, C., Coll, M., & Whitehead, H. (2012). River dolphins as indicators of ecosystem degradation in large tropical rivers. Ecological Indicators, 23, 19–26. https://doi.org/10.1016/j.ecolind.2012.02.034
Gowans, S., Würsig, B., & Karczmarski, L. (2008). The social structure and strategies of delphinids: predictions based on an ecological framework. Advances in Marine Biology, 53, 195–294. https://doi.org/10.1016/S0065-2881(07)53003-8
Harzen, S., & Brunnick, B. J. (1997). Skin disorders in bottlenose dolphins (Tursiops truncatus), resident in the Sado estuary, Portugal. Aquatic Mammals, 23, 59–68.
Jepson, P. D., Bennett, P. M., Deaville, R., Allchin, C. R., Baker, J. R., & Law, R. J. (2005) Relationships between polychlorinated biphenyls and health status in harbor porpoises (Phocoena phocoena) stranded in the United Kingdom. Environmental Toxicology and Chemistry, 24, 238–248.https://doi.org/10.1897/03-663.1
Karcmarski, L., Wursig, B., Gailey G., Larson, K. L., & Vanderlip, C. (2005). Spinner dolphins in a remote Hawaiian atoll: social grouping and population structure. Behavioral Ecology, 16, 675–685. https://doi.org/10.1093/beheco/ari028
Kiszka, J., Van Bressem, M., & Pusineri, C. (2009). Lobomycosis like disease and other skin conditions in Indo-Pacific bottlenose dolphins Tursiops aduncus from the Indian Ocean. Diseases of Aquatic Organisms, 84, 151–157.https://doi.org/10.3354/dao02037
León Coto, S., Kress, N., Brenes Rodriguez, C., & Brenner, S. (1998). Una Contribución a la Ecología del Golfo de Nicoya. Uniciencia, 15, 35–37.
Lizano, O. G. (1998). Dinámica de las aguas en la parte interna de Golfo de Nicoya ante altas descargas del Río Tempisque. Revista de Biología Tropical, 46(S6), 11–20.
Marín Alpizar, B. (2000). Diagnóstico de los Recursos Costeros en Golfo de Nicoya, Costa Rica [Unpublished thesis ofLicenciatura].Universidad Nacional de Costa Rica.
Maurer, D., & Vargas, J. A. (1984). Diversity of soft bottom benthos in a tropical estuary: Gulf of Nicoya. Costa Rica. Marine Biology, 81, 97–106. https://doi.org/10.1007/BF00397631
Moreno I. B, Ott, P. H, Tavares, M., Oliveira, L. R., Borda, M. R., Driemeier, D., Nakashima, S. N., Heinzelman, L. S., Siciliano, S., & Van Bressem, M. F. (2008, June 23-27). Mycotic dermatitis in common bottlenose dolphins (Tursiops truncatus) from southern Brazil, with a confirmed record of lobomycosis disease [Paper presentation, SC/60/DW1] International Whaling Commission Scientific Committee Annual Meeting, Santiago, Chile.
Morera-González, M., Saravia-Arguedas, A.Y., García-Céspedes, J., & Mena-Rivera L. (2019, June 4-7). Utilización de índices de contaminación por hidrocarburos en pianguas (Anadara Tuberculosa) obtenidas en el Golfo de Nicoya, Costa Rica para la categorización del grado de contaminación. In Y. Morales-López (Ed.), Memorias del I Congreso Internacional de Ciencias Exactas y Naturales [Congress]. Universidad Nacional, Costa Rica, Heredia, Costa Rica. https://repositorio.una.ac.cr/bitstream/handle/11056/24755/2019%20Ponencia%20Utilizaci%C3%B3n%20de%20%C3%ADndices%20de%20contaminaci%C3%B3n.pdf?sequence=1&isAllowed=y
Moore, S. (2008). Marine Mammals as Ecosystem Sentinels. Journal of Mammalogy, 89, 534–540. https://doi.org/10.1644/07-MAMM-S-312R1.1
Murdoch, M. E., Reif, J. S., Mazzoil, M., McCulloch, S. D., Fair, P. A., & Bossart, G. D. (2008). Lobomycosis in bottlenose dolphins (Tursiops truncatus) from the Indian River Lagoon, Florida: estimation of prevalence, temporal trends, and spatial distribution. EcoHealth, 5, 289–297. https://doi.org/10.1007/s10393-008-0187-8
Oviedo, L. (2018). Patrones y procesos de selección de hábitat en delfines simpátricos en Golfo Dulce, Costa Rica [Unpublished doctoral dissertation]. Instituto Politécnico Nacional.
Oviedo, L. E., Pacheco-Polanco, J. D., & Herra-Miranda, D. (2009). Evaluación de los riesgos de afectación por el establecimiento de granjas atuneras en relación con la distribución espacial de cetáceos en el Golfo Dulce, Costa Rica. Revista Ciencias Marinas y Costeras, 1, 159–174. https://doi.org/10.15359/revmar.1.9
Oviedo, L., Herra-Miranda, D., Pacheco-Polanco, J. D., Figgener, C., Márquez-Artavia, A., Quiros-Pereira, W., & Iñiguez, M. (2015). Diversidad de cetáceos en el paisaje marino costeros de Golfo Dulce, Península de Osa, Costa Rica. Revista de Biología Tropical, 63, 395–406.
Oviedo, L., Fernández, M., Pacheco- Polanco, J. D., & Herra-Miranda, D. (2019). Spatial analysis on the occurence of inshore and offshore bottlenose dolphins (Tursiops truncatus) in Osa Peninsula Waters. Journal of Cetacean Research Management, 20, 1–11. https://doi.org/10.47536/jcrm.v20i1.233
Paniz-Mondolfi, A., Talhari, C., Sander-Hoffmann L., Connor D. L., Talhari, S., Bermúdez-Villapol, L., Hernández-Pérez, M., & Van Bressem, M. F. (2012). Lobomycosis: an emerging disease in humans and delphinidae. Mycoses, 55, 298–309. https://doi.org/10.1111/j.1439-0507.2012.02184.x
Ramos, E. A., Castelblanco-Martínez, D. N, García, J., Rojas Arias, J., Foley, J. R., Audley, K., Van Waerebeek, K., & Van Bressem, M. F. (2018). Lobomycosis-like disease in common bottlenose dolphins Tursiops truncatus from Belize and Mexico: bridging the gap between the Americas. Disease of Aquatic Organisms, 128, 01–12. https://doi.org/10.3354/dao03206
Reif, J. S., Peden-Adams, M. M., Romano, T. A., Rice, C. D., Fair, P. A., & Bossart, G. D. (2009). Immune dysfunction in Atlantic bottlenose dolphins (Tursiops truncatus) with lobomycosis. Medical Mycology, 47, 125–135. https://doi.org/10.1080/13693780802178493
Rincón-Alejos, F., & Ballestero-Sakson, D. (2015). Hidrografía y Plumas Estuarinas en Golfo Dulce, Pacífico Sur de Costa Rica. Revista Biología Tropical, 63, 161–181.
Rodriguez-Chaves, D., Saravia Arguedas, A., Pacheco Urpí, O., & Piedra Marín, G. (2014). Evaluación de los Niveles de Hidrocarburos en Sedimentos Marinos, su Posible Origen y Efectos sobre la Actividad de Acuicultura en el Golfo de Nicoya. Revista Geográfica de América Central, 53, 113–134.
Ross, P. S. R. (2002) The role of immunotoxic environmental contaminants in facilitating the emergence of infectious diseases in marine mammals. Human and Ecological Risk Assessment, 8, 277–292. https://doi.org/10.1080/20028091056917
Rotstein, D. S, Burdett Hart, L. G., McLellan, W., Schwacke, L., Rowles, T., Terio, K. A., Schultz, S., & Pabst, A. (2009). Lobomycosis in offshore bottlenose dolphins (Tursiops truncatus), North Carolina. Emerging Infectious Diseases, 15, 588–590. https://doi.org/10.3201/eid1504.081358
Sánchez-Robledo, E., Oviedo, L., Herra-Miranda, D., Pacheco-Polanco J. D., Goodman, S., & Guzmán, H. (2020). The Abundance of False Killer Whaler, Pseudorca crassidens (Artiodactyla: Delphinidae) in coastal waters of Golfo Dulce and Osa Peninsula, Costa Rica. Revista de Biología Ambiental, 68, 1–10.
Spongberg, A., & Davis, P. (1998). Organochlorinated pesticide contaminants in Golfo Dulce, Costa Rica. Revista Biología Tropical, 46, 111–124.
Spongberg, A. (2004a). PCB contamination in marine sediments from Golfo Dulce, Pacific coast of Costa Rica. Revista Biología Tropical, 52, 23–32.
Spongberg, A. (2004b). PCB contamination in surface sediments in the coastal waters of Costa Rica. Revista Biología Tropical, 52, 1–10.
Svendsen, H., Rosland R., Myking, S., Vargas, J. A., Lizano, O. G., & Alfaro, E. J. (2006). A physical oceanographic study of Golfo Dulce, Costa Rica. Revista Biología Tropical, 54, 147–170.
Taborda, P. R., Taborda, V. A., & McGinnis, M. R. (1999) Lacazia loboi gen. nov., comb. nov., the etiologic agent of lobo mycosis. Journal of Clinical Microbiology, 37, 2031–2033. https://doi.org/10.1128/jcm.37.6.2031-2033.1999
Thamdrup, B., Canfield, D. E., Ferdelman, T. G., Glud, R. N., & Gundersen, J. K. (1996). A biogeochemical survey of the anoxic basin Golfo Dulce, Costa Rica. Revista de Biología Tropical, 44, 19–34.
Umaña, G. (1998). Characterization of some Golfo Dulce drainage basin rivers (Costa Rica). Revista de Biología Tropical, 46, 125–135.
Van Bressem, M. F., Van Waerebeak, K., Reyes, J. C., & Félix, F. (2007). A preliminary overview of skin and skeletal diseases and traumata in small cetaceans from South American waters. Latin America Journal Aquatic Mammals, 6, 7–42. https://doi.org/10.5597/lajam00108
Van Bressem, M. F., Raga, J. A., Di Guardo, G., Jepson, P. D., Duignan, P. J., Siebert, U., Barrett, T., De Oliveira Santos, M. C., Moreno, I. B., Siciliano, S., Aguilar, A., & Van Waerebeek, K. (2009). Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors. Diseases of Aquatic Organisms, 83, 143–157. https://doi.org/10.3354/dao02101
Van Bressem, M. F., Simōes-Lopes, P. C., Felix, F., Kriszka, J. J., Daura-Jorge, F. G., Avila, I. C., Secchi, E. R., Flach, L., Fruet, P. F., Du Toit, K., Ott, P. H., Elwen, S., Di Giacomo, A. B., Wagner, J., Banks, A., & Van Waerebeek, K. (2015). Epidemiology of lobomycosis-like disease in bottlenose dolphin Tursiops spp. from South America and Southern Africa. Disease of Aquatic Organisms, 117(1), 59–75. https://doi.org/10.3354/dao02932
Vilela R, Bossart, G. D., St. Leger, J. A., & Dalton, L. M. (2016). Cutaneous granulomas in dolphins caused by novel uncultivated Paracoccidioides brasiliensis. Emerging Infectious Disease, 22, 2063−2069. https://doi.org/10.3201/eid2212.160860
Vilela, R., Huebner, M., Vilela, C., Vilela, G., Pettersen, B., Oliveira, C., & Mendoza, L. (2021). The taxonomy of two uncultivated fungal mammalian pathogens is revealed through phylogeny and population genetic analyses. Scientific Reports, 11, 1–13. https://doi.org/10.1038/s41598-021-97429-7
Wilson, B., Arnold, H., Bearzi, B., Fortuna, M., Gaspar, R., Ingram, S., Liret, C., Pribanic, S., Read, A., Ridoux, V., Schneider, K., Urian, K., Wells, R., Wood, C., Thompson, M., & Hammond, P. S. (1999). Epidermal diseases in bottlenose dolphins: impacts of natural and anthropogenic factors. Proceedings of the Royal Society Biological Science, 199,1077–1083. https://doi.org/10.1098/rspb.1999.0746
Wolf, M., Koch, V., Bautista Chavarría, J., & Vargas, J. A. (1998). A trophic flow model of the Golfo de Nicoya, Costa Rica. Revista de Biología Tropical, 46, 63–79.
Comments
This work is licensed under a Creative Commons Attribution 4.0 International License.