Survival and physiological responses of corals exposed to elevated turbidity in the Varadero reef, Colombian Caribbean
DOI:
https://doi.org/10.25268/bimc.invemar.2023.52.1.1192Keywords:
Varadero, Dique Channel, symbiotic corals, optical properties, reciprocal transplantAbstract
The degradation of water optical properties, or increased turbidity, due to anthropogenic disturbances is a common phenomenon in coastal waters. The effects on the underwater light climate and the physiology of symbiotic corals, who largely depend on light to survive and maintain high calcification, have been relatively unexplored. This research describes the effects of the turbid plume of
water from the Canal del Dique on the light climate, coral physiology and survival in Varadero reef. A reciprocal transplant experiment was conducted with fragments of Orbicella faveolata between a shallow area in Varadero (3.5 m) and a deeper reef area (12 m) with clear-water
conditions, where total light exposure was comparable. The water column was strongly stratified in Varadero, which favors the isolation of the reef from the influence of the plume. Corals transplanted to Varadero had higher survivorship, potentially as a result of reduced light
stress and increased heterotrophic nutrition. Their physiological traits suggest acclimation to low-light and limited autotrophic potential, which represents a risk for coral survival at greater depths. The results indicate that a further degradation of the water optical properties of the
Cartagena Bay due to human disturbances in the Magdalena River basin and the coastal zone represents a threat to Varadero reef maintenance.
References
Anthony, K.R.N. and K.E. Fabricius. 2000. Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J. Exp. Mar. Biol. Ecol., 252: 221-253.
Anthony, K.R.N., P.V. Ridd, A.R. Orpin, P. Larcombe and J. Lough. 2004. Temporal variation of light availability in coastal benthic habitats: effects of clouds, turbidity, and tides. Limnol. Oceanogr., 49: 2201-2211. https://doi.org/10.4319/lo.2004.49.6.2201
Canto, M.M., K.E. Fabricius, M. Logan, S. Lewis, L.I.W. McKinna and B.J. Robson. 2021. A benthic light index of water quality in the Great Barrier Reef, Australia. Mar. Pollut. Bull., 169: 112539. https://doi.org/10.1016/j.marpolbul.2021.112539
Colombo-Pallotta, M.F., A. Rodríguez-Román and R. Iglesias-Prieto. 2010. Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs, 29: 899-907.
Díaz, J.M., L.M. Barrios, J. Garzón-Ferreira, J. Geister, M. López-Victoria, G.H. Ospina, F. Parra-Velandia, J. Pinzón, B. Vargas-Ángel, F.A. Zapata y S. Zea. 2000. Áreas coralinas de Colombia. Instituto de Investigaciones Marinas y Costeras. Santa Marta. 175 p.
Dubinsky, Z., N. Stambler, M. Benzion, L.R. Mccloskey, L. Muscatine and P.G. Falkowski. 1990. The effect of external nutrient resources on the opticalproperties and photosynthetic efficiency of Stylophora-Pistillata. Proc. R. Soc. Lond. B, 239: 231-246. https://doi.org/10.1098/rspb.1990.0015.
Enríquez, S., E.R. Méndez and R. Iglesias-Prieto. 2005. Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol. Oceanogr., 50: 1025-1032. https://doi.org/10.4319/lo.2005.50.4.1025
Fabricius, K.E. 2011. Factors determining the resilience of coral reefs to eutrophication: a review and conceptual model. 493-505. En: Dubinsky, Z. and N. Stambler (Eds.). Coral Reefs: An ecosystem in transition. Springer Netherlands. Dordrecht. https://doi.org/10.1007/978-94-007-0114-4_28
Falkowski, P.G., Z. Dubinsky, L. Muscatine and J.W. Porter. 1984. Light and the bioenergetics of a symbiotic coral. Bioscience, 34: 705-709. https://doi.org/10.2307/1309663
Fisher, R., P. Bessell-Browne and R. Jones. 2019. Synergistic and antagonistic impacts of suspended sediments and thermal stress on corals. Nat. Comm.,10: 2346.
Gattuso, J.P., B. Gentili, C.M. Duarte, J.A. Kleypas, J.J. Middelburg and D. Antoine. 2006. Light availability in the coastal ocean: impact on the distribution of benthic photosynthetic organisms and their contribution to primary production. Biogeosciences, 3: 489-513. https://doi.org/10.5194/bg-3-489-2006
Henao-Castro, A. 2013. Efectos de los aportes del Canal del Dique sobre el reclutamiento de especies de coral en los arrecifes del archipiélago Nuestra Señora del Rosario, área marina protegida. Tesis Magister Ciencias Marinas, Univ. Jorge Tadeo Lozano, Bogotá D.C. 125 p.
Hereford, J. 2009. A quantitative survey of local adaptation and fitness trade-offs. Am. Nat., 173: 579-588.
Hoegh-Guldberg, O. and R.J. Jones. 1999. Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar. Ecol. Prog. Ser., 183: 73-86. https://doi.org/10.3354/meps183073
Hoegh-Guldberg, O., P.J. Mumby, A.J. Hooten, R.S. Steneck, P. Greenfield, E. Gomez, C.D. Harvell, P.F. Sale, A.J. Edwards, K. Caldeira, N. Knowlton, C.M. Eakin, R. Iglesias-Prieto, N. Muthiga, R.H. Bradbury, A. Dubi and M.E. Hatziolos. 2007. Coral reefs under rapid climate change and ocean acidification. Science, 318: 1737-1742.
Hoogenboom, M., R. Rodolfo-Metalpa and C. Ferrier-Pagès. 2010. Co-variation between autotrophy and heterotrophy in the Mediterranean coral Cladocora caespitosa. J. Exp. Biol., 213: 2399-2409.
Iglesias-Prieto, R. and R.K. Trench. 1994. Acclimation and adaptation to irradiance in symbiotic dinoflagellates .1. Responses of the photosynthetic unit to changes in photon flux-density. Mar. Ecol. Prog. Ser., 113: 163-175. https://doi.org/10.3354/meps113163
Iglesias-Prieto, R., V.H. Beltrán, T.C. LaJeunesse, H. Reyes-Bonilla and P.E. Thomé. 2004. Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc. R. Soc. Lond. B, 271: 1757-1763. https://doi.org/10.1098/rspb.2004.2757
Jackson, J., M. Donovan, K. Cramer and V. Lam. 2014. Status and trends of Caribbean coral reefs: 1970-2012. Global Coral Reef Monitoring Network, IUCN. Switzerland. 304 p.
Jeffrey, S.W. and G.F. Humphrey. 1975. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher-plants, algae and natural phytoplankton. Biochem. Physiol. Pflanz., 167: 191-194.
Junjie, R.K., N.K. Browne, P.L.A. Erftemeijer and P.A. Todd. 2014. Impacts of sediments on coral energetics: partitioning the effects of turbidity and settling particles. PLoS ONE, 9: https://doi.org/10.1371/journal.pone.0107195
Kahng, S.E., D. Akkaynak, T. Shlesinger, E.J. Hochberg, J. Wiedenmann, R. Tamir and D. Tchernov. 2019. Light, temperature, photosynthesis, heterotrophy, and the lower depth limits of mesophotic coral ecosystems: 801-828. In: Loya, Y., K.A. Puglise and T.C.L. Bridge (Eds.) Mesophotic coral ecosystems. Springer. Cham. https://doi.org/10.1007/978-3-319-92735-0_42
Kemp, D.W., D.J. Thornhill, R.D. Rotjan, R. Iglesias-Prieto, W.K. Fitt and G.W. Schmidt. 2015. Spatially distinct and regionally endemic Symbiodinium assemblages in the threatened Caribbean reef-building coral Orbicella faveolata. Coral Reefs, 34: 535-547. https://doi.org/10.1007/s00338-015-1277-z
Kirk, J.T.O. 2011. Light and photosynthesis in aquatic ecosystems. Cambridge University Press. New York. 649 p.
Kleypas, J.A., J.W. McManus and L.A.B. Meñez. 1999. Environmental limits to coral reef development: where do we draw the line? Amer. Zool., 39: 146-159. https://doi.org/10.1093/icb/39.1.146
Koop, K., D. Booth, A. Broadbent, J. Brodie, D. Bucher, D. Capone, J. Coll, W. Dennison, M. Erdmann, P. Harrison, O. Hoegh-Guldberg, P. Hutchings, G.B. Jones, A.W.D. Larkum, J. O’Neil, A. Steven, E. Tentori, S. Ward, J. Williamson and D. Yellowlees. 2001. ENCORE: The effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions. Mar. Pollut. Bull., 42: 91-120.
Lonin, S., C. Parra, C. Andrade e Y. Thomas. 2004. Patrones de la pluma turbia del canal del Dique en la bahía de Cartagena. Bol. Cient. CIOH, 22: 77-89.
López-Londoño, T., C.T. Galindo-Martínez, K. Gómez-Campo, L.A. González-Guerrero, S. Roitman, F.J. Pollock, V. Pizarro, M. López-Victoria, M. Medina and R. Iglesias-Prieto. 2021. Physiological and ecological consequences of the water optical properties degradation on reef corals. Coral Reefs, 40: 1243-1256. https://doi.org/10.1007/s00338-021-02133-7
López-Londoño, T., K. Gómez-Campo, X. Hernández-Pech, S. Enríquez and R. Iglesias-Prieto. 2022. Photosynthetic usable energy explains vertical patterns of biodiversity in zooxanthellate corals. Sci. Rep., 12: 20821. https://doi.org/10.1038/s41598-022-25094-5
Lopez-Victoria, M., M. Rodríguez-Moreno and F.A. Zapata. 2015. A paradoxical reef from Varadero, Cartagena Bay, Colombia. Coral Reefs, 34: 231.
Marsh, J.A. 1970. Primary productivity of reef-building calcareous red algae. Ecology, 51: 255-263. https://doi.org/10.2307/1933661
Molares, R. and M. Mestres. 2012. Effects of fluctuating river discharge on the water exchange mechanism of a semi-enclosed micro-tidal bay: Cartagena Bay, Colombia. Bol. Cient. CIOH, 30: 53-74.
Morgan, K.M., C.T. Perry, J.A. Johnson and S.G. Smithers. 2017. Nearshore turbid-zone corals exhibit high bleaching tolerance on the Great Barrier Reef following the 2016 ocean warming event. Front. Mar. Sci., 4: 224.
Mumby, P.J., A. Hastings and H.J. Edwards. 2007. Thresholds and the resilience of Caribbean coral reefs. Nature, 450: 98-101. https://doi.org/10.1038/ nature06252
Osinga, R., R. Iglesias-Prieto and S. Enríquez. 2012. Measuring photosynthesis in symbiotic invertebrates: a review of methodologies, rates and processes: 229-256. In: Najafpour, M. (Ed.). Applied photosynthesis. InTech.
Pandolfi, J.M. and A.F. Budd. 2008. Morphology and ecological zonation of Caribbean reef corals: the Montastraea ‘annularis’ species complex. Mar. Ecol. Prog. Ser., 369: 89-102.
Pizarro, V., S.C. Rodríguez, M. López-Victoria, F.A. Zapata, S. Zea, C.T. Galíndo-Martínez, R. Iglesias-Prieto, J. Pollock and M. Medina. 2017. Unraveling the structure and composition of Varadero Reef, an improbable and imperiled coral reef in the Colombian Caribbean. Peerj, 5: https://doi.org/10.7717/peerj.4119
Pollock, F.J., J.B. Lamb, S.N. Field, S.F. Heron, B. Schaffelke, G. Shedrawi, D.G. Bourne and B.L. Willis. 2014. Sediment and turbidity associated with offshore dredging increase coral disease prevalence on nearby reefs. PLoS ONE, 9: https://doi.org/10.1371/journal.pone.0102498
R Core Team. 2015. R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Restrepo, J.D. and E.M. Alvarado. 2011. Assessing major environmental issues in the Caribbean and Pacific coasts of Colombia, South America: an overview of fluvial fluxes, coral reef degradation, and mangrove ecosystems impacted by river diversion: 289-314. In: Wolanski, E. and D.S. McLusky (Eds.) Treatise on estuarine and coastal science. Elsevier
Restrepo, J.D., P. Zapata, J.A. Díaz, J. Garzón-Ferreira and C.B. García. 2006. Fluvial fluxes into the Caribbean Sea and their impact on coastal ecosystems: The Magdalena River, Colombia. Glob. Planet. Change, 50: 33-49.
Restrepo, J.D., E. Park, S. Aquino and E.M. Latrubesse. 2016. Coral reefs chronically exposed to river sediment plumes in the southwestern Caribbean: Rosario Islands, Colombia. Sci. Total Environ., 553: 316-329. https://doi.org/10.1016/j.scitotenv.2016.02.140
Restrepo, J.D., R. Escobar and M. Tosic. 2018. Fluvial fluxes from the Magdalena River into Cartagena Bay, Caribbean Colombia: Trends, future scenarios, and connections with upstream human impacts. Geomorphology, 302: 92-105. http://dx.doi.org/10.1016/j.geomorph.2016.11.007
Rogers, C.S. 1990. Responses of coral reefs and reef organisms to sedimentation. Mar. Ecol. Prog. Ser., 62: 185-202.
Roitman, S., T. López-Londoño, F.J. Pollock, K.B. Ritchie, C.T. Galindo-Martínez, K. Gómez-Campo, L.A. González-Guerrero, V. Pizarro, M. López-Victoria, R. Iglesias-Prieto and M. Medina. 2020. Surviving marginalized reefs: assessing the implications of the microbiome on coral physiology and survivorship. Coral Reefs, 39: 795-807. https://doi.org/10.1007/s00338-020-01951-5
Rowan, R., N. Knowlton, A. Baker and J. Jara. 1997. Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature, 388: 265-269. https://doi.org/10.1038/40843
Scheufen, T., R. Iglesias-Prieto and S. Enríquez. 2017a. Changes in the number of symbionts and Symbiodinium cell pigmentation modulate differentially coral light absorption and photosynthetic performance. Front Mar Sci, 4: 309. https://doi.org/10.3389/fmars.2017.00309
Scheufen, T., W.E. Kramer, R. Iglesias-Prieto and S. Enríquez. 2017b. Seasonal variation modulates coral sensibility to heat-stress and explains annual changes in coral productivity. Sci. Rep., 7: 4937. https://doi.org/10.1038/s41598-017-04927-8
Shantz, A.A. and D.E. Burkepile. 2014. Context-dependent effects of nutrient loading on the coral-algal mutualism. Ecology, 95: 1995-2005. https://doi.org/10.1890/13-1407.1
Sheskin, D.J. 2003. Handbook of parametric and nonparametric statistical procedures. Chapman and Hall/CRC.
Spalding, M., L. Burke, S.A. Wood, J. Ashpole, J. Hutchison and P. Ermgassen. 2017. Mapping the global value and distribution of coral reef tourism. Mar. Pol., 82: 104-113. https://doi.org/10.1016/j.marpol.2017.05.014
Sutherland, K.P., J.W. Porter, J.W. Turner, B.J. Thomas, E.E. Looney, T.P. Luna, M.K. Meyers, J.C. Futch and E.K. Lipp. 2010. Human sewage identified as likely source of white pox disease of the threatened Caribbean elkhorn coral, Acropora palmata. Environ. Microbiol., 12: 1122-1131. https://doi.org/10.1111/j.1462-2920.2010.02152.x
Tosic, M., J.D. Restrepo, S. Lonin, A. Izquierdo and F. Martins. 2019. Water and sediment quality in Cartagena Bay, Colombia: seasonal variability and potential impacts of pollution. Estuar. Coast. Shelf Sci., 216: 187-203.
van Woesik, R., P. Houk, A.L. Isechal, J.W. Idechong, S. Victor and Y. Golbuu. 2012. Climate-change refugia in the sheltered bays of Palau: analogs of future reefs. Ecol. Evol., 2: 2474-2484.
Vásquez-Elizondo, R.M., L. Legaria-Moreno, M.A. Pérez-Castro, W.E. Kramer, T. Scheufen, R. Iglesias-Prieto and S. Enríquez. 2017. Absorptance determinations on multicellular tissues. Photosynth. Res., 132: 311-324. https://doi.org/10.1007/s11120-017-0395-6
Vega Thurber, R.L., D.E. Burkepile, C. Fuchs, A.A. Shantz, R. McMinds and J.R. Zaneveld. 2014. Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Glob. Chang. Biol., 20: 544-554.
Vermeij, M.J.A. and R.P.M. Bak. 2002. How are coral populations structured by light? Marine light regimes and the distribution of Madracis. Mar. Ecol. Prog. Ser., 233: 105-116. https://doi.org/10.3354/meps233105
Wagner, D.E., P. Kramer and R. van Woesik. 2010. Species composition, habitat, and water quality influence coral bleaching in southern Florida. Mar. Ecol. Prog. Ser., 408: 65-78.
Warner, M.E., G.C. Chilcoat, F.K. McFarland and W.K. Fitt. 2002. Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral Montastraea. Mar. Biol., 141: 31-38. https://doi.org/10.1007/s00227-002-0807-8
Warner, M.E., T.C. LaJeunesse, J.D. Robison and R.M. Thur. 2006. The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: potential implications for coral bleaching. Limnol. Oceanogr., 51: 1887-1897. https://doi.org/10.4319/lo.2006.51.4.1887
Weber, M., D. de Beer, C. Lott, L. Polerecky, K. Kohls, R.M.M. Abed, T.G. Ferdelman and K.E. Fabricius. 2012. Mechanisms of damage to corals exposed to sedimentation. Proc. Natl. Acad. Sci. USA, 109: https://doi.org/10.1073/pnas.1100715109
Weil, E. and N. Knowlton. 1994. A multi-character analysis of the Caribbean coral Montastraea annularis (Ellis and Solander, 1786) and its two sibling species, M. faveolata (Ellis and Solander, 1786) and M. franksi (Gregory, 1895). Bull. Mar. Sci., 55: 151-175.
Yentsch, C.S., C.M. Yentsch, J.J. Cullen, B. Lapointe, D.A. Phinney and S.W. Yentsch. 2002. Sunlight and water transparency: cornerstones in coral research. J. Exp. Mar. Biol. Ecol., 268: 171-183.
Zaneveld, J.R., D.E. Burkepile, A.A. Shantz, C.E. Pritchard, R. McMinds, J.P. Payet, R. Welsh, A.M.S. Correa, N.P. Lemoine, S. Rosales, C. Fuchs, J.A. Maynard and R.V. Thurber. 2016. Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales. Nat. Commun., 7: 11833. https://doi.org/10.1038/ncomms11833
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Copyright (c) 2023 Tomás López-Londoño, Kelly Gómez-Campo, Claudia T. Galindo-Martínez, Luis A. González-Guerrero, Sofia Roitman, F. Joseph Pollock, Valeria Pizarro, Mateo López-Victoria, Mónica Medina, Roberto Iglesias-Prieto
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