Abstract
Reef settings play key ecosystemic functions in the Caribbean realm, but the unrestrained exploitation of their natural resources and other anthropogenic effects threaten their preservation. Here, we explore the use of the foraminiferal assemblages as bioindicators in two Colombian Caribbean localities with different levels of environmental stress. The material studied was collected from the reef zones in Old Providence Island (San Andrés Archipelago) and Varadero (Cartagena Bay), where typical reef lagoon foraminiferal assemblages are found. The main taxa comprised the symbiont-bearing genera Archaias, Asterigerina, Amphistegina, and Heterostegina, the porcelaneous forms Quinqueloculina,Triloculina, and Spiroloculina, and the rotaliids Rotorbinella, Cymbaloporetta, and Eponides. The stress-tolerant taxa Ammonia, Clavulina, and Cribroelphidium were also identified in variable abundances. The detailed analysis of the faunistic composition in Old Providence and Varadero indicated significant differences in the abundances of some taxa, likely related to specific stress conditions in both localities. These stress conditions were particularly evident in Varadero, where the FORAM (Foraminifers in Reef Assessment and Monitoring) index (FI) estimations suggest moderate to highly stressed reef settings, similar to those found in preliminary surveys in this área and probably influenced by the higher anthropogenic impact at the Cartagena Bay. In contrast, the foraminiferal assemblages and the FI estimations of Old Providence suggest low to moderate stress conditions, as previously reported in other insular bodies of the archipelago.
References
Almeida, C.M., Fernandes-Barbosa, C.F., Cordeiro, R.C., Seoane, J.C.S., Fermino, G.M., Silva, P.O., Turcq, B.J. (2013). Palaeoecology of a 3-kyr biosedimentary record of a coral reef-supporting carbonate shelf. Continental Shelf Research, 70, 168-176.
Arellano-Torres, E., Correa-Metrio, A., Rutiaga-Ramírez, J. M., Escobar, J., & Castañeda-Posadas C. (2024). Holocene benthic foraminifera ecological succession in the Panamanian Caribbean. Palaeogeography, Palaeoclimatology, Palaeoecology, 655, 112536.
Barbosa, C., Prazeres, M., Ferreira, B., Sicoli, J.C. (2009). Foraminiferal assemblage and reef check census in coral reef health monitoring of East Brazilian margin. Marine Micropaleontology, 73(1-2), 62-69.
Barragan, C. & Bernal, G. (2024). Benthic foraminifera as bioindicators of gas seep intensity in the offshore zone of the Sinú fold belt. Journal of South American Earth Sciences, 148, 105103.
Bernal, G., Agudelo, A., López, S., Domínguez, J. (2005). Textura, composición y foraminíferos bentónicos de los sedimentos superficiales en los Bancos de Salmedina, Caribe Colombiano. Boletín Científico CCCP, 12, 95-112.
Bernal, G., Ruiz-Ochoa, M., Piedrahita, M.T., Restrepo, E. (2008). Foraminíferos en los sedimentos superficiales del sistema lagunar de Cispatá y la interacción Río Sinú-Mar Caribe Colombiano. Boletín de las Ciencias de la Tierra, 23, 5-20.
Bolli, H.M., Beckmann, J.P., Saunders, J.B. (1994). Benthic Foraminiferal biostratigraphy of the South Caribbean region. Cambridge University Press.
Brasier, M.D. (1975). The ecology and distribution of recent foraminifera from the reefs and shoals around Barbuda, West Indies. Journal of Foraminiferal Research, 5, 193-210.
Carilli, J. & Walsh, S. (2012). Benthic foraminiferal assemblages from Kiritimati (Christmas) Island indicate human-mediated nutrification has occurred over the scale of decades. Marine Ecology Progress Series, 456, 87-99.
Carnahan, E.A., Hoare, A.M., Hallock, P., Lidz, B.H., Reich, C.D. (2009). Foraminiferal assemblages in Biscayne Bay, Florida, USA: Responses to urban and agricultural influence in a subtropical estuary. Marine Pollution Bulletin, 59, 221-233.
Carvajal-Chitty, H.I. & Navarro, S. (2021). Preliminary foraminiferal survey in Chichiriviche de La Costa, Vargas, Venezuela. Revista Brasileira de Paleontologia, 24(2), 90-103.
Comisión Colombiana del Océano-CCO. (2024). Boletín Expedición Científica Seaflower 2021-I Old Providence y Santa Catalina. Puntoaparte Editores.
Cockey, E., Hallock, P., Lidz, B.H. (1996). Decadal-scale changes in benthic foraminiferal assemblages off Key Largo, Florida. Coral Reefs, 15, 237-248.
CORALINA-INVEMAR. (2012). Atlas de la Reserva de Biósfera Seaflower. Archipiélago de San Andrés, Providencia y Santa Catalina. Serie de Publicaciones Especiales de INVEMAR.
Culver, S.J. (1990). Benthic foraminifera of Puerto Rican mangrove-lagoon systems: potential for paleoenvironmental interpretations. Palaios, 5, 34-51.
Culver, S.J. & Buzas, M.A. (1995). The effects of anthropogenic habitat disturbance, habitat destruction, and global warming on shallow marine benthic foraminifera. Journal of Foraminiferal Research, 25(3), 204-211.
Díaz, J.M., Barrios, L.M., Cendales, M.H., Garzón-Ferreira, J., Geister, J., López-Victoria, M., Ospina, G.H., Parra-Velandia, F., Pinzón, J., Vargas-Ángel, B., Zapata, F., Zea, S. (2000). Áreas coralinas de Colombia. Serie de Publicaciones Especiales de INVEMAR.
Dimiza, M.D., Triantaphyllou, M.V., Koukousioura, O., Hallock, P., Simboura, N., Karageorgis, A.P., Papathanasiou, E. (2016). The Foram Stress Index: A new tool for environmental assessment of soft-bottom environments using benthic foraminifera. A case study from the Saronikos Gulf, Greece, Eastern Mediterranean. Ecological Indicators, 60, 611-621.
Doo, S.S., Fujita, K., Byrne, M., Uthicke, S. (2014). Fate of calcifying tropical symbiont-bearing large benthic foraminifera: Living sands in a changing ocean. The Biological Bulletin, 226(3), 169-186.
Duque-Castaño, M., Trejos-Tamayo, R., Osorio-Tabares, L.C., Angulo-Pardo, E., Vallejo, F., Plata, A., Pardo-Trujillo, A. (2023). Lower to Middle Miocene multiproxy biostratigraphy of the P-18 core-stratigraphic well in Sinú-San Jacinto Basin, Caribbean region of Colombia. Journal of South American Earth Sciences, 123, 104228.
Duque-Caro, H. (1975). Los foraminíferos planctónicos y el Terciario de Colombia. Revista Española de Micropaleontología, 7(3), 403-427.
Duque-Caro, H. (1990). The Chocó block in the northwestern corner of South America: Structural, tectonostratigraphic, and paleogeographic implications. Journal of South American Earth Sciences, 3(1), 71-84.
Durán-Gómez, J.E., Patarroyo, G.D., Torres-Parada, J.M. (2023). Miocene Fossils of Old Providence Island (Western Caribbean, Colombia) and geological heritage of the Seaflower Biosphere Reserve. Caribbean Journal of Science, 53(2), 210-221.
Eder, W., Briguglio, A., Hohenegger, J. (2016). Growth of Heterostegina depressa under natural and laboratory conditions. Marine Micropaleontology, 122, 27-43.
Fatela, F. & Taborda, R. (2002). Confidence limits of species proportions in microfossil assemblages. Marine Micropaleontology, 45, 169-174.
Fiorini, F. (2015). Recent benthic foraminifera from the Caribbean continental slope and shelf off west of Colombia. Journal of South American Earth Sciences, 60, 117-128.
Fiorini, F. & Jaramillo, C. (2007). Paleoenvironmental reconstruction of the Oligocene-Miocene deposits of southern Caribbean (Carmen de Bolivar, Colombia) based on benthic foraminifera. Boletín de Geología, 29(2), 47-55.
Forcino, F.L. (2012). Multivariate assessment of the required sample size for community paleoecological research. Palaeogeography, Palaeoclimatology, Palaeoecology, 315-316, 134-141.
Geister, J. (1986). Recent Coral Reefs and geology history of Providencia Island (Western Caribbean Sea, Colombia). Geología Colombiana, 15, 115-134.
Geister, J. (1992). Modern reef development and Cenozoic evolution of an oceanic island/reef complex: Isla de Providencia (Western Caribbean Sea, Colombia). Facies, 27, 1-70.
Geister, J. & Díaz, J.M. (2007). Reef Environments and Geology of an Oceanic Archipelago: San Andres, Old Providence and Santa Catalina (Caribbean Sea, Colombia) with field guide. INGEOMINAS Special Publication.
Gischler, E., Hauser, I., Heinrich, K., Scheitel, U. (2003). Characterization of depositional environments in isolated carbonate platforms based on benthic foraminifera, Belize, Central America. Palaios, 18, 236-255.
Gischler, E. & Möder, A. (2009). Modern benthic foraminifera on Banco Chinchorro, Quintana Roo, Mexico. Facies, 55, 27-35.
Gómez, C., Millán, S., Acosta-Chaparro, A., Abril-Howard, A., Navas-Camacho, R. (2022). Evaluación preliminar del impacto del huracán Iota en arrecifes coralinos de las islas de Providencia y Santa Catalina. Boletín de Investigaciones Marinas y Costeras, 51(1), 193-200.
Gudnitz, M.N., Collins, L.S., O’Dea, A. (2021). Foraminiferal communities of a mid-Holocene reef: Isla Colón, Caribbean Panama. Palaeogeography, Palaeoclimatology, Palaeoecology, 562, 110042.
Gudnitz, M.N. & Collins, L.S. (2024). Using foraminifera to assess changes in marine coastal habitats of Caribbean Panama since the Middle Holocene. Marine Micropaleontology, 192, 102408.
Hallock, P., Cottey, T.L., Forward, L. B., Halas, J. (1986). Population dynamics and sediment production by Archaias angulatus (Foraminiferida) in Largo Sound, FL. Journal of Foraminiferal Research, 16, 1-18.
Hallock, P., Lidz, B.H., Cockey-Burkhard, E.M., Donnelly, K.B. (2003). Foraminifera as bioindicators in coral reef assessment and monitoring: the FORAM index. En Melzian, B.D., Engle, V., McAlister, M., Sandhu, S., Eads, L.K. (Eds.) Coastal Monitoring through Partnerships (221-238). Springer.
Hammer, O., Harper, D.A.T., & Ryan, P.D. (2001). PAST: paleontological statistics software package for education and data analysis: Palaeontologia Electronica, 4(1), 1-9.
Havach, S.M. & Collins, L.S. (1997). The distribution of recent benthic foraminifera across habitats of Bocas Del Toro, Caribbean Panama: Journal for Foraminiferal Research, 27, 232-249.
Humphreys, A.F., Halfar, J., Ingle, J.C., Manzello, D., Reymond, C.E., Westphal, H., Riegl, B. (2018). Effect of seawater temperature, Ph, and nutrients on the distribution and character of low abundance shallow water benthic foraminifera in the Galapagos. PLoS One, 13, e0202746.
Instituto Humboldt. (2021). Expedición Cangrejo Negro. Isla de Providencia 17 al 24 de enero de 2021. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt.
Langer, M.R. (1993). Epiphytic foraminifera. Marine Micropaleontology, 20(3-4), 235-265.
Li, C. & Jones, B. (1997). Comparison of foraminiferal assemblages in sediments on the windward and leeward shelves of Grand Cayman, British West Indies. Palaios, 12, 12-26.
Li, C., Jones, B., Kalbfleisch, W.B. (1998). Carbonate sediment transport pathways based on foraminifera: case study from Frank Sound, Grand Cayman, British West Indies. Sedimentology, 45, 109-120.
Lidz, B.H. & Rose, P.R. (1989). Diagnostic Foraminiferal Assemblages of Florida Bay and Adjacent Shallow Waters: A Comparison. Bulletin of Marine Science, 44(1), 399-418.
Lintner, M., Schagerl, M., Lintner, B., Nagy, M., Heinz, P. (2022). Photosynthetic performance of symbiont-bearing foraminifera Heterostegina depressa affected by sunscreens. Scientific Reports, 12, 2750.
Manrique-Rodríguez, N., Agudelo, C., Sanjuan-Muñoz, A. (2019). Comunidad de octocorales gorgonáceos del arrecife de coral de Varadero en el Caribe colombiano: diversidad y distribución espacial. Boletín de Investigaciones Marinas y Costeras, 48(1), 55-64.
Martin, R.E. (1986). Habitat and distribution of the foraminifer Archaias angulatus (Fichtel and Moll) (Miliolina, Soritidae), northern Florida Keys. Journal of Foraminiferal Research, 16, 201-206.
Molinares, C.E., Martínez, J.I., Fiorini, F., Escobar, J., Jaramillo, C. (2012). Paleoenvironmental reconstruction for the lower Pliocene Arroyo Piedras section (Tubará – Colombia): Implications for the Magdalena River – paleodelta’s dynamic. Journal of South American Earth Sciences, 39, 170-183.
Ortiz-Moreno, M.L. & Acosta, N. (2003). Inferencia de las condiciones ambientales de la playa “Pilón de azúcar” (Guajira, Colombia), a partir del conjunto de foraminíferos en una muestra de sedimento. Acta Biológica Colombiana, 8(2), 13-22.
Murray, J.W. (1991). Ecology and Paleoecology of Benthic Foraminifera. Longman.
Murray, J.W. (2006). Ecology and Applications of Benthic Foraminifera. Cambridge University Press.
Nobes, K., Uthicke, S., Henderson, R. (2008). Is light limiting factor for the distribution of benthic symbiont bearing foraminfera on the Great Barrier Reef? Journal of Experimental Marine Biology and Ecology, 363, 48-57.
Parada-Ruffinatti, C. (1996). Foraminíferos del Pleistoceno – Holoceno del Caribe Colombiano. Editora Guadalupe.
Parada-Ruffinatti, C. & Londoño de Hoyos, C. (1983). Foraminíferos bentónicos recientes del Norte de Cartagena. Editora Guadalupe.
Parada-Ruffinatti, C. & Pinto, J. (1986). Foraminíferos bentónicos recientes de la Isla Barú. FEN Colombia.
Patarroyo, G., Torres, G., Gómez, D. (2024). Foraminiferal assemblages as bioindicators in the Western Caribbean: Albuquerque Cay (Colombia). Journal of Foraminiferal Research, 54(1), 36-48.
Peebles, M.W., Hallock, P., Hine, A. (1997). Benthic foraminiferal assemblages from current-swept carbonate platforms of the Northern Nicaraguan Rise, Caribbean Sea. Journal of Foraminiferal Research, 27(1), 42-50.
Petters, V. & Sarmiento, S. (1956). Oligocene and Lower Miocene bioestratigraphy of the Carmen-Zambrano area, Colombia. Micropaleontology, 2(1), 7-35.
Pisapia, C., El Kateb, A., Hallock, P., Spezzaferri, P. (2017). Assessing coral reef health in the North Ari Atoll (Maldives) using the FoRAM index. Marine Micropaleontology, 133, 50-57.
Pizarro, V., Rodríguez, S.C., López-Victoria, M., Zapata, F.A., Zea, S., Galindo-Martínez, C.T., Iglesias-Prieto, R., Pollock, J., Medina, M. (2017). Unraveling the structure and composition of Varadero Reef, an improbable and imperiled coral reef in the Colombian Caribbean. PeerJ, 5, e411.
Prazeres, M., Martínez-Colon, M., Hallock, P. (2020). Foraminifera as bioindicators of water quality: The FoRAM Index revisited. Environmental Pollution, 257, 113612.
Puyana, M., Acosta, A., Bernal-Sotelo, K., Velásquez-Rodríguez, T., Ramos, F. (2015). Spatial scale of cyanobacterial blooms in Old Providence Island, Colombian Caribbean. Universitas Scientiarum, 20(1), 83-105.
Ramírez, L.F. (2016). Marine protected areas in Colombia: advances in conservation and barriers for effective governance. Ocean Coastal Management, 125, 49-62.
Restrepo, J.D., Zapata, P., Díaz, J.M., Garzón-Ferreira, J., García, C.B. (2006). Fluvial fluxes into the Caribbean Sea and their impact on coastal ecosystems: the Magdalena River, Colombia. Global and Planetary Change, 50, 33-49.
Rincón-Martínez, D.A., Arenas, J.E., Cuartas, C.H., Cárdenas, A.L., Molinares, C.E., Caicedo, C., Jaramillo, C. (2007). Eocene–Pliocene planktonic foraminifera biostratigraphy from the continental margin of the southwest Caribbean. Stratigraphy, 4, 261-311.
Rodríguez, L., Acosta, A., González-Zapata, F.L., Gómez-Corrales, L., Marrugo, M., Alvarado-Ch., E.M., Dueñas, L.F., Andrade, J., Gutiérrez-Cala, L., Sánchez, J.A. (2023). Conservation at the edge: connectivity and opportunities from non-protected coral reefs close to a national park in the Colombian Caribbean. Biodiversity and Conservation, 32, 1493-1522.
Romero-Murillo, P., Gallego, J.L., Leignel, V. (2023). Marine pollution and advances in biomonitoring in Cartagena Bay in the Colombian Caribbean. Toxics, 11, 631.
Rose, P.R. & Lidz, B. (1977). Diagnostic foraminiferal assemblages of shallow-water modern environments: south Florida and the Bahamas. Sedimenta, 6, 1-55.
Salazar-Ortiz, E.A., Rincón-Martínez, D., Páez, L.A., Restrepo, S.M., Barragán, S. (2020). Middle Eocene mixed carbonate-siliciclastic systems in the southern Caribbean (NW Colombian margin). Journal of South American Earth Sciences, 99, 102507.
Sánchez, J., Zea, S., & Díaz, J. (1998). Patterns of octocoral and black coral distribution in the oceanic barrier reef-complex of Old Providence Island, southwestern Caribbean. Caribbean Journal of Science, 34(3-4), 250-264.
Sánchez, J.A., Gómez-Corrales, M., Gutiérrez-Cala, L., Vergara, D.C., Roa, P., González-Zapata, F.L., Gnecco, M., Puerto, N., Neira, L., Sarmiento, A. (2019). Steady Decline of Corals and Other Benthic Organisms in the Seaflower Biosphere Reserve (Southwestern Caribbean). Frontiers in Marine Science, 6, 416927. https://doi.org/10.3389/fmars.2019.00073
Schueth, J.D. & Frank, T.D. (2008). Reef foraminifera as bioindicators of coral reef health: Low Isles Reef, Northern Great Barrier Reef, Australia. Journal of Foraminiferal Research, 38(1), 11-22.
Sen Gupta, B.K. (1999). Modern Foraminifera. Kluwer Academic Publishers.
Stephenson, C.M., Hallock, P., & Kelmo, F. (2015). Foraminiferal assemblage indices: A comparison of sediment and reef rubble samples from Conch Reef, Florida, USA. Ecological Indicators, 48, 1-7.
Taylor, E., Baine, M., Killmer, A., Howard, M. (2013). Seaflower marine protected area: governance for sustainable development. Marine Policy, 41, 57-64.
Torres, G.A., Patarroyo, G.D., Veloza, G., Mora, J.A., Gómez, D.F. (2022). Asociaciones de foraminíferos aglutinados de la Formación San Cayetano en el Cinturón Plegado de San Jacinto (Norte de Colombia). Boletín de Geología, 44(1), 75-92.
Trejos-Tamayo, R., Garzón, D., Salazar-Ríos, A., Pardo-Trujillo, A., Flores, J.A. (2024). Paleoambientes en la parte central del Cinturón Plegado de San Jacinto (Caribe colombiano) entre el Eoceno tardío y el Mioceno Temprano: Inferencias a partir de foraminíferos bentónicos. Boletín de Geología, 46(3), 169-191.
Trejos-Tamayo, R., Garzón-Oyola, D., Rodríguez-Abaunza, A., Frontalini, F., Betancur, J.P., Gallego, F., Pardo-Trujillo, A., Flores, J.A. (2025). Late Eocene-early Miocene paleoenvironmental shifts in the NW South American margin: Tectonic and climatic drivers inferred from benthic foraminifera. Global and Planetary Change, 104744.
Triffleman, N.J., Hallock, P., Hine, A.C. (1992). Morphology, sediments, and depositional environments of a small carbonate platform; Serranilla Bank, Nicaraguan Rise, Southwest Caribbean Sea. Journal of Sedimentary Research, 62, 591-606.
Triffleman, N.J., Hallock, P., Hine, A.C., Peebles, M.W. (1991). Distribution of foraminiferal tests in sediments of Serranilla Bank, Nicaraguan Rise, southwestern Caribbean. Journal of Foraminiferal Research, 21(1), 39-47.
Uthicke, S., Thompson, A., Schaffelke, B. (2010). Effectiveness of benthic foraminiferal and coral assemblages as water quality indicators on inshore reefs of the Great Barrier Reef, Australia. Coral Reefs, 29, 209-225.
Velásquez, J., López-Angarita, J., Sánchez, J.A. (2011). Evaluation of the FORAM index in a case of conservation: Benthic foraminifera as indicators of ecosystem resilience in protected and non-protected coral reefs of the southern Caribbean. Biodiversity and Conservation, 20, 3591-3603.
Wilson, B. (2006). The environmental significance of Archaias angulatus (Miliolida, Foraminifera) in sediments around Nevis, West Indies. Caribbean Journal of Science, 42(1), 20-23.
Wilson, B. & Ramsook, A. (2007). Population densities and diversities of epiphytal foraminifera on nearshore substrates, Nevis, West Indies. Journal of Foraminiferal Research, 37(3), 213-222.
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Copyright (c) 2025 Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales